Abstract

Cardiac tissue engineering is a promising strategy for regenerative therapies to overcome the shortage of donor organs for transplantation. Besides contractile function, the stiffness of tissue engineered constructs is crucial to generate transplantable tissue surrogates with sufficient mechanical stability to withstand the high pressure present in the heart. Although several collagen cross-linking techniques have proven to be efficient in stabilizing biomaterials, they cannot be applied to cardiac tissue engineering, as cell death occurs in the treated area. Here, we present a novel method using femtosecond (fs) laser pulses to increase the stiffness of collagen-based tissue constructs without impairing cell viability. Raster scanning of the fs laser beam over riboflavin-treated tissue induced collagen cross-linking by two-photon photosensitized singlet oxygen production. One day post-irradiation, stress-strain measurements revealed increased tissue stiffness by around 40% being dependent on the fibroblast content in the tissue. At the same time, cells remained viable and fully functional as demonstrated by fluorescence imaging of cardiomyocyte mitochondrial activity and preservation of active contraction force. Our results indicate that two-photon induced collagen cross-linking has great potential for studying and improving artificially engineered tissue for regenerative therapies.

© 2011 OSA

Full Article  |  PDF Article

References

  • View by:
  • |
  • |
  • |

  1. WHO (World Health Organization), “Cardiovascular Diseases,” Fact Sheet Number 317, Geneva, Switzerland, January2011.
  2. W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
    [CrossRef] [PubMed]
  3. W. H. Zimmermann, M. Tiburcy, and T. Eschenhagen, “Cardiac tissue engineering: a clinical perspective,” Future Cardiol. 3, 435–445 (2007).
    [CrossRef] [PubMed]
  4. K. L. Kreutziger and C. E. Murry, “Engineered human cardiac tissue,” Pediatr. Cardiol. 32, 334–341 (2011).
    [CrossRef] [PubMed]
  5. B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).
  6. L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
    [CrossRef]
  7. A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
    [CrossRef] [PubMed]
  8. C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
    [PubMed]
  9. G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
    [CrossRef]
  10. W. M. Elbjeirami, E. O. Yonter, B. C. Starcher, and J. L. West, “Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity,” J. Biomed. Mater. Res. 66, 513–521 (2003).
    [CrossRef]
  11. T. S. Girton, T. R. Oegema, and R. T. Tranquillo, “Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering,” J. Biomed. Mater. Res. 46, 87–92 (1999).
    [CrossRef] [PubMed]
  12. C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
    [PubMed]
  13. H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
    [CrossRef]
  14. G. Wollensak, E. Spoerl, and T. Seiler, “Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus,” Am. J. Ophthalmol. 135, 620–627 (2003).
    [CrossRef] [PubMed]
  15. A. Jayakrishnan and S. R. Jameela, “Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices,” Biomaterials 17, 471–484 (1996).
    [CrossRef] [PubMed]
  16. M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coordin. Chem. Rev. 233–234, 351–371 (2002).
    [CrossRef]
  17. A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
    [CrossRef]
  18. G. Wollensak, E. Spoerl, M. Wilsch, and T. Seiler, “Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment,” Cornea 23, 43–49 (2004).
    [CrossRef] [PubMed]
  19. T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
    [CrossRef] [PubMed]
  20. K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. (Paris) 45, 195–201 (1999).
  21. W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
    [CrossRef] [PubMed]
  22. D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
    [CrossRef]
  23. K. Kuetemeyer, R. Rezgui, H. Lubatschowski, and A. Heisterkamp, “Influence of laser parameters and staining on femtosecond laser-based intracellular nanosurgery,” Biomed. Opt. Express 1, 587–597 (2010).
    [CrossRef]
  24. P. K. Frederiksen, M. Jorgensen, and P. R. Ogilby, “Two-photon photosensitized production of singlet oxygen,” J. Am. Chem. Soc. 123, 1215–1221 (2001).
    [CrossRef] [PubMed]
  25. K. Koenig, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
    [CrossRef]
  26. A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80, 2029–2036 (2001).
    [CrossRef] [PubMed]
  27. S. Kalies, K. Kuetemeyer, and A. Heisterkamp, “Mechanisms of high-order photobleaching and its relationship to intracellular ablation,” Biomed. Opt. Express 2, 805–816 (2011).
    [CrossRef] [PubMed]
  28. A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).
    [CrossRef]
  29. G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
    [CrossRef]
  30. W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
    [CrossRef] [PubMed]
  31. R. A. Lorbeer, M. Heidrich, C. Lorbeer, D. F. Ramirez-Ojeda, G. Bicker, H. Meyer, and A. Heisterkamp, “Highly efficient 3D fluorescence microscopy with a scanning laser optical tomograph,” Opt. Express 19, 5419–5430 (2011).
    [CrossRef] [PubMed]
  32. M. H. Niemz, Laser-Tissue Interactions: Fundamentals and Applications (Springer, 2007).
  33. B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
    [CrossRef] [PubMed]
  34. G. Wollensak, E. Spoerl, and T. Seiler, “Stress-strain measurements of human and porcine corneas after riboflavinultraviolet-A-induced cross-linking,” J. Cataract Refractive Surg. 29, 1780–1785 (2003).
    [CrossRef]
  35. M. Eghbali and K. T. Weber, “Collagen and the myocardium: fibrillar structure, biosynthesis and degradation in relation to hypertrophy and its regression,” Mol. Cell. Biochem. 96, 1–14 (1990).
    [CrossRef] [PubMed]
  36. C. Xu and W. W. Webb “Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm,” J. Opt. Soc. Am. B 13, 481–491 (1996).
    [CrossRef]
  37. B. P. Yu, “Cellular defenses against damage from reactive oxygen species,” Physiol. Rev. 74, 139–162 (1994).
    [PubMed]
  38. Z. H. Syedain, J. Bjork, L. Sando, and R. T. Tranquillo, “Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue,” Biomaterials 30, 6695–6701 (2009).
    [CrossRef] [PubMed]
  39. A. Vogel and V. Venugopalan, “Mechanisms of pulsed laser ablation of biological tissues,” Chem. Rev. 103, 577–644 (2003).
    [CrossRef] [PubMed]
  40. G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, and J. W. Holmes, “Model-based design of mechanical therapies for myocardial infarction,” J. Cardiovasc. Transl. Res. 4, 82–91 (2011).
    [CrossRef]

2011 (6)

K. L. Kreutziger and C. E. Murry, “Engineered human cardiac tissue,” Pediatr. Cardiol. 32, 334–341 (2011).
[CrossRef] [PubMed]

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, and J. W. Holmes, “Model-based design of mechanical therapies for myocardial infarction,” J. Cardiovasc. Transl. Res. 4, 82–91 (2011).
[CrossRef]

S. Kalies, K. Kuetemeyer, and A. Heisterkamp, “Mechanisms of high-order photobleaching and its relationship to intracellular ablation,” Biomed. Opt. Express 2, 805–816 (2011).
[CrossRef] [PubMed]

R. A. Lorbeer, M. Heidrich, C. Lorbeer, D. F. Ramirez-Ojeda, G. Bicker, H. Meyer, and A. Heisterkamp, “Highly efficient 3D fluorescence microscopy with a scanning laser optical tomograph,” Opt. Express 19, 5419–5430 (2011).
[CrossRef] [PubMed]

2010 (5)

K. Kuetemeyer, R. Rezgui, H. Lubatschowski, and A. Heisterkamp, “Influence of laser parameters and staining on femtosecond laser-based intracellular nanosurgery,” Biomed. Opt. Express 1, 587–597 (2010).
[CrossRef]

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

2009 (1)

Z. H. Syedain, J. Bjork, L. Sando, and R. T. Tranquillo, “Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue,” Biomaterials 30, 6695–6701 (2009).
[CrossRef] [PubMed]

2007 (1)

W. H. Zimmermann, M. Tiburcy, and T. Eschenhagen, “Cardiac tissue engineering: a clinical perspective,” Future Cardiol. 3, 435–445 (2007).
[CrossRef] [PubMed]

2005 (2)

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).
[CrossRef]

2004 (1)

G. Wollensak, E. Spoerl, M. Wilsch, and T. Seiler, “Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment,” Cornea 23, 43–49 (2004).
[CrossRef] [PubMed]

2003 (5)

G. Wollensak, E. Spoerl, and T. Seiler, “Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus,” Am. J. Ophthalmol. 135, 620–627 (2003).
[CrossRef] [PubMed]

W. M. Elbjeirami, E. O. Yonter, B. C. Starcher, and J. L. West, “Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity,” J. Biomed. Mater. Res. 66, 513–521 (2003).
[CrossRef]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

A. Vogel and V. Venugopalan, “Mechanisms of pulsed laser ablation of biological tissues,” Chem. Rev. 103, 577–644 (2003).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, “Stress-strain measurements of human and porcine corneas after riboflavinultraviolet-A-induced cross-linking,” J. Cataract Refractive Surg. 29, 1780–1785 (2003).
[CrossRef]

2002 (2)

B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
[CrossRef] [PubMed]

M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coordin. Chem. Rev. 233–234, 351–371 (2002).
[CrossRef]

2001 (3)

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
[CrossRef]

P. K. Frederiksen, M. Jorgensen, and P. R. Ogilby, “Two-photon photosensitized production of singlet oxygen,” J. Am. Chem. Soc. 123, 1215–1221 (2001).
[CrossRef] [PubMed]

A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80, 2029–2036 (2001).
[CrossRef] [PubMed]

2000 (3)

K. Koenig, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
[CrossRef]

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

1999 (2)

T. S. Girton, T. R. Oegema, and R. T. Tranquillo, “Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering,” J. Biomed. Mater. Res. 46, 87–92 (1999).
[CrossRef] [PubMed]

K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. (Paris) 45, 195–201 (1999).

1996 (2)

C. Xu and W. W. Webb “Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm,” J. Opt. Soc. Am. B 13, 481–491 (1996).
[CrossRef]

A. Jayakrishnan and S. R. Jameela, “Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices,” Biomaterials 17, 471–484 (1996).
[CrossRef] [PubMed]

1994 (1)

B. P. Yu, “Cellular defenses against damage from reactive oxygen species,” Physiol. Rev. 74, 139–162 (1994).
[PubMed]

1990 (2)

M. Eghbali and K. T. Weber, “Collagen and the myocardium: fibrillar structure, biosynthesis and degradation in relation to hypertrophy and its regression,” Mol. Cell. Biochem. 96, 1–14 (1990).
[CrossRef] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
[CrossRef] [PubMed]

1976 (1)

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

1975 (1)

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Ailawadi, G.

G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, and J. W. Holmes, “Model-based design of mechanical therapies for myocardial infarction,” J. Cardiovasc. Transl. Res. 4, 82–91 (2011).
[CrossRef]

Akhyari, P.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Baer, A.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Baier, R.

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

Bhana, B.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Bicker, G.

Bjork, J.

Z. H. Syedain, J. Bjork, L. Sando, and R. T. Tranquillo, “Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue,” Biomaterials 30, 6695–6701 (2009).
[CrossRef] [PubMed]

Blab, G. A.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
[CrossRef]

Bolze, F.

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Bradshaw, H. E.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Chen, W. L.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Christie, R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

Clement, E. M.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Cognet, L.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
[CrossRef]

Conrad, G. W

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Crutchley, R. J.

M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coordin. Chem. Rev. 233–234, 351–371 (2002).
[CrossRef]

Dahlmann, J.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

Dai, P.

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

Dardik, H.

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

Dardik, I. I.

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

Dedeic, Z.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Denk, W.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
[CrossRef] [PubMed]

DeRosa, M. C.

M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coordin. Chem. Rev. 233–234, 351–371 (2002).
[CrossRef]

Dionne, M. J. C.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Draeger, G.

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

Edelhauser, H. F.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Eghbali, M.

M. Eghbali and K. T. Weber, “Collagen and the myocardium: fibrillar structure, biosynthesis and degradation in relation to hypertrophy and its regression,” Mol. Cell. Biochem. 96, 1–14 (1990).
[CrossRef] [PubMed]

Elbjeirami, W. M.

W. M. Elbjeirami, E. O. Yonter, B. C. Starcher, and J. L. West, “Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity,” J. Biomed. Mater. Res. 66, 513–521 (2003).
[CrossRef]

Epstein, S. E.

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Ergun, S.

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

Eschenhagen, T.

W. H. Zimmermann, M. Tiburcy, and T. Eschenhagen, “Cardiac tissue engineering: a clinical perspective,” Future Cardiol. 3, 435–445 (2007).
[CrossRef] [PubMed]

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

Fink, C.

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

Fischer, P.

K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. (Paris) 45, 195–201 (1999).

Fomovsky, G. M.

G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, and J. W. Holmes, “Model-based design of mechanical therapies for myocardial infarction,” J. Cardiovasc. Transl. Res. 4, 82–91 (2011).
[CrossRef]

Frederiksen, P. K.

P. K. Frederiksen, M. Jorgensen, and P. R. Ogilby, “Two-photon photosensitized production of singlet oxygen,” J. Am. Chem. Soc. 123, 1215–1221 (2001).
[CrossRef] [PubMed]

Fujita, K.

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

Gao, J.

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Girton, T. S.

T. S. Girton, T. R. Oegema, and R. T. Tranquillo, “Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering,” J. Biomed. Mater. Res. 46, 87–92 (1999).
[CrossRef] [PubMed]

Goeldner, M.

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Gruh, I.

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Gug, S.

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Halbhuber, K. H.

K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. (Paris) 45, 195–201 (1999).

Harms, G. S.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
[CrossRef]

Haverich, A.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Heidrich, M.

Heisterkamp, A.

Holmes, J. W.

G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, and J. W. Holmes, “Model-based design of mechanical therapies for myocardial infarction,” J. Cardiovasc. Transl. Res. 4, 82–91 (2011).
[CrossRef]

Hopt, A.

A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80, 2029–2036 (2001).
[CrossRef] [PubMed]

Huettman, G.

A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).
[CrossRef]

Hyman, B. T.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

Ibrahim, I. M.

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

Itscoitz, S. B.

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Iyer, R. K.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Jameela, S. R.

A. Jayakrishnan and S. R. Jameela, “Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices,” Biomaterials 17, 471–484 (1996).
[CrossRef] [PubMed]

Jayakrishnan, A.

A. Jayakrishnan and S. R. Jameela, “Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices,” Biomaterials 17, 471–484 (1996).
[CrossRef] [PubMed]

Jorgensen, M.

P. K. Frederiksen, M. Jorgensen, and P. R. Ogilby, “Two-photon photosensitized production of singlet oxygen,” J. Am. Chem. Soc. 123, 1215–1221 (2001).
[CrossRef] [PubMed]

Kalies, S.

Kensah, G.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Kidder, G. W.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Kirschning, A.

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

Koenig, K.

K. Koenig, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
[CrossRef]

K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. (Paris) 45, 195–201 (1999).

Kokini, K.

B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
[CrossRef] [PubMed]

Kraft, S.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Kralisch, D.

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

Krause, A.

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

Kreutziger, K. L.

K. L. Kreutziger and C. E. Murry, “Engineered human cardiac tissue,” Pediatr. Cardiol. 32, 334–341 (2011).
[CrossRef] [PubMed]

Kuetemeyer, K.

Levy, M.

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

Likhitpanichkul, M.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Lommerse, P. H. M.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
[CrossRef]

Lorbeer, C.

Lorbeer, R. A.

Lubatschowski, H.

Lundquist, R. R.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

Macadangdang, J. R.

G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, and J. W. Holmes, “Model-based design of mechanical therapies for myocardial infarction,” J. Cardiovasc. Transl. Res. 4, 82–91 (2011).
[CrossRef]

Maidhof, R.

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Marsano, A.

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Martin, U.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

McCall, A. S.

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

McIntosh, C. L.

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Meyer, H.

R. A. Lorbeer, M. Heidrich, C. Lorbeer, D. F. Ramirez-Ojeda, G. Bicker, H. Meyer, and A. Heisterkamp, “Highly efficient 3D fluorescence microscopy with a scanning laser optical tomograph,” Opt. Express 19, 5419–5430 (2011).
[CrossRef] [PubMed]

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Michaelis, L. L.

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Moeller, L.

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

Morrow, A. G.

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Mourot, A.

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Murry, C. E.

K. L. Kreutziger and C. E. Murry, “Engineered human cardiac tissue,” Pediatr. Cardiol. 32, 334–341 (2011).
[CrossRef] [PubMed]

Neher, E.

A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80, 2029–2036 (2001).
[CrossRef] [PubMed]

Nicoud, J. F.

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Niemz, M. H.

M. H. Niemz, Laser-Tissue Interactions: Fundamentals and Applications (Springer, 2007).

Nikitin, A. Y.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

Noack, J.

A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).
[CrossRef]

Oegema, T. R.

T. S. Girton, T. R. Oegema, and R. T. Tranquillo, “Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering,” J. Biomed. Mater. Res. 46, 87–92 (1999).
[CrossRef] [PubMed]

Ogilby, P. R.

P. K. Frederiksen, M. Jorgensen, and P. R. Ogilby, “Two-photon photosensitized production of singlet oxygen,” J. Am. Chem. Soc. 123, 1215–1221 (2001).
[CrossRef] [PubMed]

Oyamada, M.

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

Paltauf, G.

A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).
[CrossRef]

Radisic, M.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Ramirez-Ojeda, D. F.

Redwood, D. R.

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Remmers, U.

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

Rezgui, R.

Riemann, I.

K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. (Paris) 45, 195–201 (1999).

Robinson, J. P.

B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
[CrossRef] [PubMed]

Roeder, B. A.

B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
[CrossRef] [PubMed]

Sando, L.

Z. H. Syedain, J. Bjork, L. Sando, and R. T. Tranquillo, “Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue,” Biomaterials 30, 6695–6701 (2009).
[CrossRef] [PubMed]

Schmidt, T.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
[CrossRef]

Schumann, H.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Seiler, T.

G. Wollensak, E. Spoerl, M. Wilsch, and T. Seiler, “Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment,” Cornea 23, 43–49 (2004).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, “Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus,” Am. J. Ophthalmol. 135, 620–627 (2003).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, “Stress-strain measurements of human and porcine corneas after riboflavinultraviolet-A-induced cross-linking,” J. Cataract Refractive Surg. 29, 1780–1785 (2003).
[CrossRef]

Sider, K. L.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Simmons, C. A.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Skvorc, D.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Specht, A.

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Spoerl, E.

G. Wollensak, E. Spoerl, M. Wilsch, and T. Seiler, “Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment,” Cornea 23, 43–49 (2004).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, “Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus,” Am. J. Ophthalmol. 135, 620–627 (2003).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, “Stress-strain measurements of human and porcine corneas after riboflavinultraviolet-A-induced cross-linking,” J. Cataract Refractive Surg. 29, 1780–1785 (2003).
[CrossRef]

Sprayregen, S.

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

Starcher, B. C.

W. M. Elbjeirami, E. O. Yonter, B. C. Starcher, and J. L. West, “Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity,” J. Biomed. Mater. Res. 66, 513–521 (2003).
[CrossRef]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
[CrossRef] [PubMed]

Sturgis, J. E.

B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
[CrossRef] [PubMed]

Syedain, Z. H.

Z. H. Syedain, J. Bjork, L. Sando, and R. T. Tranquillo, “Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue,” Biomaterials 30, 6695–6701 (2009).
[CrossRef] [PubMed]

Takamatsu, T.

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

Tanabe, T.

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

Tanaka, H.

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

Tandon, N.

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Tiburcy, M.

W. H. Zimmermann, M. Tiburcy, and T. Eschenhagen, “Cardiac tissue engineering: a clinical perspective,” Future Cardiol. 3, 435–445 (2007).
[CrossRef] [PubMed]

Tranquillo, R. T.

Z. H. Syedain, J. Bjork, L. Sando, and R. T. Tranquillo, “Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue,” Biomaterials 30, 6695–6701 (2009).
[CrossRef] [PubMed]

T. S. Girton, T. R. Oegema, and R. T. Tranquillo, “Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering,” J. Biomed. Mater. Res. 46, 87–92 (1999).
[CrossRef] [PubMed]

Venugopalan, V.

A. Vogel and V. Venugopalan, “Mechanisms of pulsed laser ablation of biological tissues,” Chem. Rev. 103, 577–644 (2003).
[CrossRef] [PubMed]

Viering, J.

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Vogel, A.

A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).
[CrossRef]

A. Vogel and V. Venugopalan, “Mechanisms of pulsed laser ablation of biological tissues,” Chem. Rev. 103, 577–644 (2003).
[CrossRef] [PubMed]

Voytik-Harbin, S. L.

B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
[CrossRef] [PubMed]

Vunjak-Novakovic, G.

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Wan, L. Q.

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Wang, Y.

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Warther, D.

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Webb, W. W.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

C. Xu and W. W. Webb “Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm,” J. Opt. Soc. Am. B 13, 481–491 (1996).
[CrossRef]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
[CrossRef] [PubMed]

Weber, K. T.

M. Eghbali and K. T. Weber, “Collagen and the myocardium: fibrillar structure, biosynthesis and degradation in relation to hypertrophy and its regression,” Mol. Cell. Biochem. 96, 1–14 (1990).
[CrossRef] [PubMed]

Weil, J.

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

West, J. L.

W. M. Elbjeirami, E. O. Yonter, B. C. Starcher, and J. L. West, “Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity,” J. Biomed. Mater. Res. 66, 513–521 (2003).
[CrossRef]

Williams, R. M.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

Wilsch, M.

G. Wollensak, E. Spoerl, M. Wilsch, and T. Seiler, “Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment,” Cornea 23, 43–49 (2004).
[CrossRef] [PubMed]

Wollensak, G.

G. Wollensak, E. Spoerl, M. Wilsch, and T. Seiler, “Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment,” Cornea 23, 43–49 (2004).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, “Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus,” Am. J. Ophthalmol. 135, 620–627 (2003).
[CrossRef] [PubMed]

G. Wollensak, E. Spoerl, and T. Seiler, “Stress-strain measurements of human and porcine corneas after riboflavinultraviolet-A-induced cross-linking,” J. Cataract Refractive Surg. 29, 1780–1785 (2003).
[CrossRef]

Xu, C.

Yonter, E. O.

W. M. Elbjeirami, E. O. Yonter, B. C. Starcher, and J. L. West, “Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity,” J. Biomed. Mater. Res. 66, 513–521 (2003).
[CrossRef]

Yu, B. P.

B. P. Yu, “Cellular defenses against damage from reactive oxygen species,” Physiol. Rev. 74, 139–162 (1994).
[PubMed]

Zhao, R.

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Zimmermann, W. H.

W. H. Zimmermann, M. Tiburcy, and T. Eschenhagen, “Cardiac tissue engineering: a clinical perspective,” Future Cardiol. 3, 435–445 (2007).
[CrossRef] [PubMed]

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

Am. J. Ophthalmol. (1)

G. Wollensak, E. Spoerl, and T. Seiler, “Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus,” Am. J. Ophthalmol. 135, 620–627 (2003).
[CrossRef] [PubMed]

Appl. Phys. B (1)

A. Vogel, J. Noack, G. Huettman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81, 1015–1047 (2005).
[CrossRef]

Biomaterials (2)

Z. H. Syedain, J. Bjork, L. Sando, and R. T. Tranquillo, “Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue,” Biomaterials 30, 6695–6701 (2009).
[CrossRef] [PubMed]

A. Jayakrishnan and S. R. Jameela, “Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices,” Biomaterials 17, 471–484 (1996).
[CrossRef] [PubMed]

Biomed. Opt. Express (2)

Bioorgan. Med. Chem. (1)

D. Warther, S. Gug, A. Specht, F. Bolze, J. F. Nicoud, A. Mourot, and M. Goeldner, “Two-photon uncaging: new prospects in neuroscience and cellular biology,” Bioorgan. Med. Chem. 18, 7753–7758 (2010).
[CrossRef]

Biophys. J. (1)

A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80, 2029–2036 (2001).
[CrossRef] [PubMed]

Biotechnol. Bioeng. (2)

W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnol. Bioeng. 68, 106–114 (2000).
[CrossRef] [PubMed]

B. Bhana, R. K. Iyer, W. L. Chen, R. Zhao, K. L. Sider, M. Likhitpanichkul, C. A. Simmons, and M. Radisic, “Influence of substrate stiffness on the phenotype of heart cells,” Biotechnol. Bioeng. 105, 1148–1160 (2010).

Biotechnol. Prog. (1)

A. Marsano, R. Maidhof, L. Q. Wan, Y. Wang, J. Gao, N. Tandon, and G. Vunjak-Novakovic, “Scaffold stiffness affects the contractile function of three-dimensional engineered cardiac constructs,” Biotechnol. Prog. 26, 1382–1390 (2010).
[CrossRef] [PubMed]

Cell Mol. Biol. (Paris) (1)

K. Koenig, I. Riemann, P. Fischer, and K. H. Halbhuber, “Intracellular nanosurgery with near infrared femtosecond laser pulses,” Cell Mol. Biol. (Paris) 45, 195–201 (1999).

Chem. Phys. Lett. (1)

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, “Two-photon exciation action cross-sections of the autofluorescent proteins,” Chem. Phys. Lett. 350, 71–77 (2001).
[CrossRef]

Chem. Rev. (1)

A. Vogel and V. Venugopalan, “Mechanisms of pulsed laser ablation of biological tissues,” Chem. Rev. 103, 577–644 (2003).
[CrossRef] [PubMed]

Coordin. Chem. Rev. (1)

M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coordin. Chem. Rev. 233–234, 351–371 (2002).
[CrossRef]

Cornea (1)

G. Wollensak, E. Spoerl, M. Wilsch, and T. Seiler, “Keratocyte apoptosis after corneal collagen cross-linking using riboflavin/UVA treatment,” Cornea 23, 43–49 (2004).
[CrossRef] [PubMed]

FASEB J. (1)

C. Fink, S. Ergun, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” FASEB J. 14, 669–679 (2000).
[PubMed]

Future Cardiol. (1)

W. H. Zimmermann, M. Tiburcy, and T. Eschenhagen, “Cardiac tissue engineering: a clinical perspective,” Future Cardiol. 3, 435–445 (2007).
[CrossRef] [PubMed]

Int. J. Artif. Organs (1)

L. Moeller, A. Krause, J. Dahlmann, I. Gruh, A. Kirschning, and G. Draeger, “Preparation and evaluation of hydrogel-composites from methacrylated hyaluronic acid, alginate, and gelatin for tissue engineering,” Int. J. Artif. Organs 34, 93–102 (2011).
[CrossRef]

Invest. Ophthalmol. Visual Sci. (1)

A. S. McCall, S. Kraft, H. F. Edelhauser, G. W. Kidder, R. R. Lundquist, H. E. Bradshaw, Z. Dedeic, M. J. C. Dionne, E. M. Clement, and G. W Conrad, “Mechanisms of corneal tissue cross-linking in response to treatment with topical riboflavin and long-wavelength ultraviolet radiation (UVA),” Invest. Ophthalmol. Visual Sci. 51, 129–138 (2010).
[CrossRef]

J. Am. Chem. Soc. (1)

P. K. Frederiksen, M. Jorgensen, and P. R. Ogilby, “Two-photon photosensitized production of singlet oxygen,” J. Am. Chem. Soc. 123, 1215–1221 (2001).
[CrossRef] [PubMed]

J. Biomech. Eng. (1)

B. A. Roeder, K. Kokini, J. E. Sturgis, J. P. Robinson, and S. L. Voytik-Harbin, “Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure,” J. Biomech. Eng. 124, 214–222 (2002).
[CrossRef] [PubMed]

J. Biomed. Mater. Res. (2)

W. M. Elbjeirami, E. O. Yonter, B. C. Starcher, and J. L. West, “Enhancing mechanical properties of tissue-engineered constructs via lysyl oxidase crosslinking activity,” J. Biomed. Mater. Res. 66, 513–521 (2003).
[CrossRef]

T. S. Girton, T. R. Oegema, and R. T. Tranquillo, “Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering,” J. Biomed. Mater. Res. 46, 87–92 (1999).
[CrossRef] [PubMed]

J. Cardiovasc. Transl. Res. (1)

G. M. Fomovsky, J. R. Macadangdang, G. Ailawadi, and J. W. Holmes, “Model-based design of mechanical therapies for myocardial infarction,” J. Cardiovasc. Transl. Res. 4, 82–91 (2011).
[CrossRef]

J. Cataract Refractive Surg. (1)

G. Wollensak, E. Spoerl, and T. Seiler, “Stress-strain measurements of human and porcine corneas after riboflavinultraviolet-A-induced cross-linking,” J. Cataract Refractive Surg. 29, 1780–1785 (2003).
[CrossRef]

J. Microsc. (1)

K. Koenig, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
[CrossRef]

J. Opt. Soc. Am. B (1)

JAMA J. Am. Med. Assoc. (1)

H. Dardik, I. M. Ibrahim, R. Baier, S. Sprayregen, M. Levy, and I. I. Dardik, “Human umbilical cord. A new source for vascular prosthesis,” JAMA J. Am. Med. Assoc. 236, 2859–2862 (1976).
[CrossRef]

Mol. Cell. Biochem. (1)

M. Eghbali and K. T. Weber, “Collagen and the myocardium: fibrillar structure, biosynthesis and degradation in relation to hypertrophy and its regression,” Mol. Cell. Biochem. 96, 1–14 (1990).
[CrossRef] [PubMed]

Nat. Methods (1)

T. Tanabe, M. Oyamada, K. Fujita, P. Dai, H. Tanaka, and T. Takamatsu, “Multiphoton excitationevoked chromophore assisted laser inactivation using green fluorescent protein,” Nat. Methods 2, 503–505 (2005).
[CrossRef] [PubMed]

Opt. Express (1)

Pediatr. Cardiol. (1)

K. L. Kreutziger and C. E. Murry, “Engineered human cardiac tissue,” Pediatr. Cardiol. 32, 334–341 (2011).
[CrossRef] [PubMed]

Physiol. Rev. (1)

B. P. Yu, “Cellular defenses against damage from reactive oxygen species,” Physiol. Rev. 74, 139–162 (1994).
[PubMed]

Proc. Natl. Acad. Sci. U.S.A. (1)

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100, 7075–7080 (2003).
[CrossRef] [PubMed]

Science (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
[CrossRef] [PubMed]

Surgery (1)

C. L. McIntosh, L. L. Michaelis, A. G. Morrow, S. B. Itscoitz, D. R. Redwood, and S. E. Epstein, “Atrioventricular valve replacement with the Hancock porcine xenograft: a five-year clinical experience,” Surgery 78, 768–775 (1975).
[PubMed]

Tissue Eng. Pt. C Methods (1)

G. Kensah, I. Gruh, J. Viering, H. Schumann, J. Dahlmann, H. Meyer, D. Skvorc, A. Baer, P. Akhyari, A. Heisterkamp, A. Haverich, and U. Martin, “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Eng. Pt. C Methods 17, 463–473 (2011).
[CrossRef]

Other (2)

WHO (World Health Organization), “Cardiovascular Diseases,” Fact Sheet Number 317, Geneva, Switzerland, January2011.

M. H. Niemz, Laser-Tissue Interactions: Fundamentals and Applications (Springer, 2007).

Cited By

OSA participates in CrossRef's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (6)

Fig. 1
Fig. 1

(a) Phase contrast microscopy image of a MEF-based tissue suspended between titanium rods on day 7 prior to laser irradiation. Scale bar: 1 mm. (b) Schematic setup for two-photon induced collagen cross-linking. L1 / L2: f1=250 and f2=−50 mm planoconvex and plano-concave lenses; L3: focusing lens with f=140 mm or f=400 mm. (c) Tissue constructs were raster-scanned with a constant scanning speed and line separation Δy being equal to the focal spot radius.

Fig. 2
Fig. 2

(a) Stress-strain relation of MEF-based tissues after RF treatment and fs laser irradiation. RF or laser treatment alone did not have an effect on tissue stiffness. Increased stiffening occurred after RF treatment and irradiation at 160 J/cm2. At the higher fluence of 320 J/cm2, this positive effect was no longer observed. (b) Irradiation of RF treated tissues at 160 J/cm2 resulted in an increase of engineering stress at 20% strain and Young’s modulus by 35% compared to untreated controls. Each data point represents the mean ± SEM of two experiments.

Fig. 4
Fig. 4

(a) Average TMRM fluorescence intensity in untreated control and RF treated + laser irradiated MEF-based tissues and BCTs. Each bar represents the mean ± SEM of two (MEF) and five (BCT) measurements. (b) Phase contrast and TMRM fluorescence images over the cross-sectional area of a BCT treated with RF and irradiated from below at 300 J/cm2. The maximum depth of laser treatment was measured at an incident angle of 0° to about 520 μm. Scale bar: 200 μm.

Fig. 3
Fig. 3

Representative (a,b) TMRM and (c,d) DAPI fluorescence microscopy images of RF treated and laser irradiated BCTs: (a,c) 160 J/cm2 laser fluence + RF; (b,d) 320 J/cm2 laser fluence + RF. The white dotted lines separate the irradiated (bottom) and non-irradiated areas (top). A high magnification image of the boxed area in (e) is provided in (b). At the higher laser fluence, irradiation resulted in a marked decrease of TMRM fluorescence intensity, while DAPI fluorescence was still intense. Scale bar: 500 μm.

Fig. 5
Fig. 5

Representative SLOT fluorescence images of cross-linked BCT after fixation and DAPI staining. The section plane of the right image is indicated by the red dashed line in the left image. No difference in the volumetric cell density was observed between irradiated and non-irradiated areas. Scale bar: 200 μm.

Fig. 6
Fig. 6

(a) Stress-strain relation of bioartificial cardiac tissue (BCT) after optimization of the cross-linking procedure. Significant stiffening was observed in a small process window around 50 J/cm2. (b) Laser irradiation of RF treated BCTs at 50 J/cm2 resulted in a significantly increased stiffness by 40% at 20 % strain, while the active contraction force was comparable to untreated controls. Each data point represents the mean ± SEM of at least four experiments. * P<0.05 versus untreated control group.

Metrics