Abstract

We implemented in situ time-lapse Second Harmonic Generation (SHG) microscopy to monitor the three-dimensional (3D) self-assembly of collagen in solution. As a proof of concept, we tuned the kinetics of fibril formation by varying the pH and measured the subsequent exponential increase of fibril volume density in SHG images. We obtained significantly different time constants at pH = 6.5 ± 0.3 and at pH = 7.5 ± 0.3. Moreover, we showed that we could focus on the growth of a single isolated collagen fibril because SHG microscopy is sensitive to well-organized fibrils with diameter below the optical resolution. This work illustrates the potential of SHG microscopy for the rational design and characterization of collagen-based biomaterials.

© 2012 OSA

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  1. D. E. Birk and P. Bruckner, “Collagen suprastructures,” Top. Curr. Chem.247, 185–205 (2005).
  2. M.-M. Giraud-Guille, L. Besseau, and R. Martin, “Liquid crystalline assemblies of collagen in bone and in vitro systems,” J. Biomech.36(10), 1571–1579 (2003).
    [CrossRef] [PubMed]
  3. S. Köster, H. M. Evans, J. Y. Wong, and T. Pfohl, “An in situ study of collagen self-assembly processes,” Biomacromolecules9(1), 199–207 (2008).
    [CrossRef] [PubMed]
  4. C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
    [CrossRef] [PubMed]
  5. J. R. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: fibril polymorphism and colloidal gold labelling,” Micron38(5), 513–521 (2007).
    [CrossRef] [PubMed]
  6. F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
    [CrossRef] [PubMed]
  7. F. Z. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” J. Struct. Biol.148(3), 268–278 (2004).
    [CrossRef] [PubMed]
  8. T. Starborg, Y. Lu, K. E. Kadler, and D. F. Holmes, “Electron microscopy of collagen fibril—structure in vitro and in vivo including three-dimensional reconstruction,” in Methods in Cell Biology (Elsevier, 2008), Vol. 88, 319–345.
  9. V. K. Yadavalli, D. V. Svintradze, and R. M. Pidaparti, “Nanoscale measurements of the assembly of collagen to fibrils,” Int. J. Biol. Macromol.46(4), 458–464 (2010).
    [CrossRef] [PubMed]
  10. D. A. Cisneros, C. Hung, C. M. Franz, and D. J. Muller, “Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy,” J. Struct. Biol.154(3), 232–245 (2006).
    [CrossRef] [PubMed]
  11. A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
    [CrossRef] [PubMed]
  12. Y. L. Yang and L. J. Kaufman, “Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly,” Biophys. J.96(4), 1566–1585 (2009).
    [CrossRef] [PubMed]
  13. K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
    [CrossRef] [PubMed]
  14. I. Freund and M. Deutsch, “Second-harmonic microscopy of biological tissue,” Opt. Lett.11(2), 94–96 (1986).
    [CrossRef] [PubMed]
  15. P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
    [CrossRef] [PubMed]
  16. A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
    [CrossRef] [PubMed]
  17. 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(12), 7075–7080 (2003).
    [CrossRef] [PubMed]
  18. M. Strupler, A.-M. Pena, M. Hernest, P.-L. Tharaux, J.-L. Martin, E. Beaurepaire, and M.-C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express15(7), 4054–4065 (2007).
    [CrossRef] [PubMed]
  19. R. W. Boyd, Nonlinear Optics (Academic, 2003).
  20. S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
    [CrossRef] [PubMed]
  21. A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
    [CrossRef] [PubMed]
  22. A. Deniset-Besseau, P. De Sa Peixoto, G. Mosser, and M.-C. Schanne-Klein, “Nonlinear optical imaging of lyotropic cholesteric liquid crystals,” Opt. Express18(2), 1113–1121 (2010).
    [CrossRef] [PubMed]
  23. A.-M. Pena, T. Boulesteix, T. Dartigalongue, and M.-C. Schanne-Klein, “Chiroptical effects in the second harmonic signal of collagens I and IV,” J. Am. Chem. Soc.127(29), 10314–10322 (2005).
    [CrossRef] [PubMed]
  24. C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
    [CrossRef]
  25. A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
    [CrossRef] [PubMed]
  26. M.-M. Giraud-Guille, L. Besseau, D. Herbage, and P. Gounon, “Optimization of Collagen Liquid-Crystalline Assemblies - Influence of Sonic Fragmentation,” J. Struct. Biol.113(2), 99–106 (1994).
    [CrossRef]
  27. I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
    [CrossRef]
  28. G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express3(1), 1–15 (2012).
    [CrossRef] [PubMed]
  29. M.-M. Giraud Guille, C. Helary, S. Vigier, and N. Nassif, “Dense fibrillar collagen matrices for tissue repair,” Soft Matter6(20), 4963–4967 (2010).
    [CrossRef]

2012 (2)

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef]

G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express3(1), 1–15 (2012).
[CrossRef] [PubMed]

2010 (4)

M.-M. Giraud Guille, C. Helary, S. Vigier, and N. Nassif, “Dense fibrillar collagen matrices for tissue repair,” Soft Matter6(20), 4963–4967 (2010).
[CrossRef]

A. Deniset-Besseau, P. De Sa Peixoto, G. Mosser, and M.-C. Schanne-Klein, “Nonlinear optical imaging of lyotropic cholesteric liquid crystals,” Opt. Express18(2), 1113–1121 (2010).
[CrossRef] [PubMed]

V. K. Yadavalli, D. V. Svintradze, and R. M. Pidaparti, “Nanoscale measurements of the assembly of collagen to fibrils,” Int. J. Biol. Macromol.46(4), 458–464 (2010).
[CrossRef] [PubMed]

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

2009 (4)

Y. L. Yang and L. J. Kaufman, “Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly,” Biophys. J.96(4), 1566–1585 (2009).
[CrossRef] [PubMed]

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
[CrossRef]

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

2008 (2)

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

S. Köster, H. M. Evans, J. Y. Wong, and T. Pfohl, “An in situ study of collagen self-assembly processes,” Biomacromolecules9(1), 199–207 (2008).
[CrossRef] [PubMed]

2007 (3)

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

J. R. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: fibril polymorphism and colloidal gold labelling,” Micron38(5), 513–521 (2007).
[CrossRef] [PubMed]

M. Strupler, A.-M. Pena, M. Hernest, P.-L. Tharaux, J.-L. Martin, E. Beaurepaire, and M.-C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express15(7), 4054–4065 (2007).
[CrossRef] [PubMed]

2006 (2)

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

D. A. Cisneros, C. Hung, C. M. Franz, and D. J. Muller, “Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy,” J. Struct. Biol.154(3), 232–245 (2006).
[CrossRef] [PubMed]

2005 (2)

D. E. Birk and P. Bruckner, “Collagen suprastructures,” Top. Curr. Chem.247, 185–205 (2005).

A.-M. Pena, T. Boulesteix, T. Dartigalongue, and M.-C. Schanne-Klein, “Chiroptical effects in the second harmonic signal of collagens I and IV,” J. Am. Chem. Soc.127(29), 10314–10322 (2005).
[CrossRef] [PubMed]

2004 (1)

F. Z. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” J. Struct. Biol.148(3), 268–278 (2004).
[CrossRef] [PubMed]

2003 (2)

M.-M. Giraud-Guille, L. Besseau, and R. Martin, “Liquid crystalline assemblies of collagen in bone and in vitro systems,” J. Biomech.36(10), 1571–1579 (2003).
[CrossRef] [PubMed]

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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

2002 (2)

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

2000 (1)

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

1994 (1)

M.-M. Giraud-Guille, L. Besseau, D. Herbage, and P. Gounon, “Optimization of Collagen Liquid-Crystalline Assemblies - Influence of Sonic Fragmentation,” J. Struct. Biol.113(2), 99–106 (1994).
[CrossRef]

1986 (1)

Alexander, S.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Allain, J.-M.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef]

Anglo, A.

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

Bayan, C.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
[CrossRef]

Beaurepaire, E.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

M. Strupler, A.-M. Pena, M. Hernest, P.-L. Tharaux, J.-L. Martin, E. Beaurepaire, and M.-C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express15(7), 4054–4065 (2007).
[CrossRef] [PubMed]

Belamie, E.

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

Benichou, E.

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

Besseau, L.

M.-M. Giraud-Guille, L. Besseau, and R. Martin, “Liquid crystalline assemblies of collagen in bone and in vitro systems,” J. Biomech.36(10), 1571–1579 (2003).
[CrossRef] [PubMed]

M.-M. Giraud-Guille, L. Besseau, D. Herbage, and P. Gounon, “Optimization of Collagen Liquid-Crystalline Assemblies - Influence of Sonic Fragmentation,” J. Struct. Biol.113(2), 99–106 (1994).
[CrossRef]

Birk, D. E.

D. E. Birk and P. Bruckner, “Collagen suprastructures,” Top. Curr. Chem.247, 185–205 (2005).

Boulesteix, T.

A.-M. Pena, T. Boulesteix, T. Dartigalongue, and M.-C. Schanne-Klein, “Chiroptical effects in the second harmonic signal of collagens I and IV,” J. Am. Chem. Soc.127(29), 10314–10322 (2005).
[CrossRef] [PubMed]

Brevet, P.-F.

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

Brightman, A. O.

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

Bruckner, P.

D. E. Birk and P. Bruckner, “Collagen suprastructures,” Top. Curr. Chem.247, 185–205 (2005).

Campagnola, P. J.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Cisneros, D. A.

D. A. Cisneros, C. Hung, C. M. Franz, and D. J. Muller, “Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy,” J. Struct. Biol.154(3), 232–245 (2006).
[CrossRef] [PubMed]

Colonna, A.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

Coussens, L. M.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Dartigalongue, T.

A.-M. Pena, T. Boulesteix, T. Dartigalongue, and M.-C. Schanne-Klein, “Chiroptical effects in the second harmonic signal of collagens I and IV,” J. Am. Chem. Soc.127(29), 10314–10322 (2005).
[CrossRef] [PubMed]

Davidson, P.

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

De Sa Peixoto, P.

Deniset-Besseau, A.

A. Deniset-Besseau, P. De Sa Peixoto, G. Mosser, and M.-C. Schanne-Klein, “Nonlinear optical imaging of lyotropic cholesteric liquid crystals,” Opt. Express18(2), 1113–1121 (2010).
[CrossRef] [PubMed]

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

Deryugina, E.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Deutsch, M.

Duboisset, J.

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

Evans, H. M.

S. Köster, H. M. Evans, J. Y. Wong, and T. Pfohl, “An in situ study of collagen self-assembly processes,” Biomacromolecules9(1), 199–207 (2008).
[CrossRef] [PubMed]

Fagot, D.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

Franz, C. M.

D. A. Cisneros, C. Hung, C. M. Franz, and D. J. Muller, “Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy,” J. Struct. Biol.154(3), 232–245 (2006).
[CrossRef] [PubMed]

Freund, I.

Friedl, P.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Galey, J.-B.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

Georgakoudi, I.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
[CrossRef]

George, S. C.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

Giraud Guille, M.-M.

M.-M. Giraud Guille, C. Helary, S. Vigier, and N. Nassif, “Dense fibrillar collagen matrices for tissue repair,” Soft Matter6(20), 4963–4967 (2010).
[CrossRef]

Giraud-Guille, M.-M.

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

M.-M. Giraud-Guille, L. Besseau, and R. Martin, “Liquid crystalline assemblies of collagen in bone and in vitro systems,” J. Biomech.36(10), 1571–1579 (2003).
[CrossRef] [PubMed]

M.-M. Giraud-Guille, L. Besseau, D. Herbage, and P. Gounon, “Optimization of Collagen Liquid-Crystalline Assemblies - Influence of Sonic Fragmentation,” J. Struct. Biol.113(2), 99–106 (1994).
[CrossRef]

Gobeaux, F.

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

Gounon, P.

M.-M. Giraud-Guille, L. Besseau, D. Herbage, and P. Gounon, “Optimization of Collagen Liquid-Crystalline Assemblies - Influence of Sonic Fragmentation,” J. Struct. Biol.113(2), 99–106 (1994).
[CrossRef]

Gusachenko, I.

G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express3(1), 1–15 (2012).
[CrossRef] [PubMed]

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef]

Hache, F.

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

Harris, J. R.

J. R. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: fibril polymorphism and colloidal gold labelling,” Micron38(5), 513–521 (2007).
[CrossRef] [PubMed]

Helary, C.

M.-M. Giraud Guille, C. Helary, S. Vigier, and N. Nassif, “Dense fibrillar collagen matrices for tissue repair,” Soft Matter6(20), 4963–4967 (2010).
[CrossRef]

Herbage, D.

M.-M. Giraud-Guille, L. Besseau, D. Herbage, and P. Gounon, “Optimization of Collagen Liquid-Crystalline Assemblies - Influence of Sonic Fragmentation,” J. Struct. Biol.113(2), 99–106 (1994).
[CrossRef]

Hernest, M.

Hoppe, P. E.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Hörber, H.

F. Z. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” J. Struct. Biol.148(3), 268–278 (2004).
[CrossRef] [PubMed]

Houssen, Y. G.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef]

Howard, J.

F. Z. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” J. Struct. Biol.148(3), 268–278 (2004).
[CrossRef] [PubMed]

Hung, C.

D. A. Cisneros, C. Hung, C. M. Franz, and D. J. Muller, “Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy,” J. Struct. Biol.154(3), 232–245 (2006).
[CrossRef] [PubMed]

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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Jiang, F. Z.

F. Z. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” J. Struct. Biol.148(3), 268–278 (2004).
[CrossRef] [PubMed]

Kaplan, D.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
[CrossRef]

Kaufman, L. J.

Y. L. Yang and L. J. Kaufman, “Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly,” Biophys. J.96(4), 1566–1585 (2009).
[CrossRef] [PubMed]

Köster, S.

S. Köster, H. M. Evans, J. Y. Wong, and T. Pfohl, “An in situ study of collagen self-assembly processes,” Biomacromolecules9(1), 199–207 (2008).
[CrossRef] [PubMed]

Kowalczuk, L.

Krasieva, T.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

Lamarre, I.

Latour, G.

Leroy, F.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

Levitt, J. M.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
[CrossRef]

Lyubovitsky, J.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

Malone, C. J.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Martin, J.-L.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

M. Strupler, A.-M. Pena, M. Hernest, P.-L. Tharaux, J.-L. Martin, E. Beaurepaire, and M.-C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express15(7), 4054–4065 (2007).
[CrossRef] [PubMed]

Martin, R.

M.-M. Giraud-Guille, L. Besseau, and R. Martin, “Liquid crystalline assemblies of collagen in bone and in vitro systems,” J. Biomech.36(10), 1571–1579 (2003).
[CrossRef] [PubMed]

McCallister, M. E.

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

Michelet, J.-F.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

Mih, J. D.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

Millard, A. C.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Miller, E.

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
[CrossRef]

Mohler, W. A.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Mosser, G.

A. Deniset-Besseau, P. De Sa Peixoto, G. Mosser, and M.-C. Schanne-Klein, “Nonlinear optical imaging of lyotropic cholesteric liquid crystals,” Opt. Express18(2), 1113–1121 (2010).
[CrossRef] [PubMed]

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

Muller, D. J.

D. A. Cisneros, C. Hung, C. M. Franz, and D. J. Muller, “Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy,” J. Struct. Biol.154(3), 232–245 (2006).
[CrossRef] [PubMed]

Müller, D. J.

F. Z. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” J. Struct. Biol.148(3), 268–278 (2004).
[CrossRef] [PubMed]

Nassif, N.

M.-M. Giraud Guille, C. Helary, S. Vigier, and N. Nassif, “Dense fibrillar collagen matrices for tissue repair,” Soft Matter6(20), 4963–4967 (2010).
[CrossRef]

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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Olive, C.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

Panine, P.

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

Pena, A.-M.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

M. Strupler, A.-M. Pena, M. Hernest, P.-L. Tharaux, J.-L. Martin, E. Beaurepaire, and M.-C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express15(7), 4054–4065 (2007).
[CrossRef] [PubMed]

A.-M. Pena, T. Boulesteix, T. Dartigalongue, and M.-C. Schanne-Klein, “Chiroptical effects in the second harmonic signal of collagens I and IV,” J. Am. Chem. Soc.127(29), 10314–10322 (2005).
[CrossRef] [PubMed]

Pfohl, T.

S. Köster, H. M. Evans, J. Y. Wong, and T. Pfohl, “An in situ study of collagen self-assembly processes,” Biomacromolecules9(1), 199–207 (2008).
[CrossRef] [PubMed]

Pidaparti, R. M.

V. K. Yadavalli, D. V. Svintradze, and R. M. Pidaparti, “Nanoscale measurements of the assembly of collagen to fibrils,” Int. J. Biol. Macromol.46(4), 458–464 (2010).
[CrossRef] [PubMed]

Plotnikov, S. V.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

Putnam, A. J.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

Rajwa, B. P.

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

Raub, C. B.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

Reiber, A.

J. R. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: fibril polymorphism and colloidal gold labelling,” Micron38(5), 513–521 (2007).
[CrossRef] [PubMed]

Robinson, J. P.

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

Schacht, V.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Schanne-Klein, M.-C.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef]

G. Latour, I. Gusachenko, L. Kowalczuk, I. Lamarre, and M.-C. Schanne-Klein, “In vivo structural imaging of the cornea by polarization-resolved second harmonic microscopy,” Biomed. Opt. Express3(1), 1–15 (2012).
[CrossRef] [PubMed]

A. Deniset-Besseau, P. De Sa Peixoto, G. Mosser, and M.-C. Schanne-Klein, “Nonlinear optical imaging of lyotropic cholesteric liquid crystals,” Opt. Express18(2), 1113–1121 (2010).
[CrossRef] [PubMed]

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

M. Strupler, A.-M. Pena, M. Hernest, P.-L. Tharaux, J.-L. Martin, E. Beaurepaire, and M.-C. Schanne-Klein, “Second harmonic imaging and scoring of collagen in fibrotic tissues,” Opt. Express15(7), 4054–4065 (2007).
[CrossRef] [PubMed]

A.-M. Pena, T. Boulesteix, T. Dartigalongue, and M.-C. Schanne-Klein, “Chiroptical effects in the second harmonic signal of collagens I and IV,” J. Am. Chem. Soc.127(29), 10314–10322 (2005).
[CrossRef] [PubMed]

Strupler, M.

Sturgis, J. E.

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

Suresh, V.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

Svintradze, D. V.

V. K. Yadavalli, D. V. Svintradze, and R. M. Pidaparti, “Nanoscale measurements of the assembly of collagen to fibrils,” Int. J. Biol. Macromol.46(4), 458–464 (2010).
[CrossRef] [PubMed]

Terasaki, M.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Tharaux, P.-L.

Tran, V.

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef]

Tromberg, B. J.

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

van Rheenen, J.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Vigier, S.

M.-M. Giraud Guille, C. Helary, S. Vigier, and N. Nassif, “Dense fibrillar collagen matrices for tissue repair,” Soft Matter6(20), 4963–4967 (2010).
[CrossRef]

von Andrian, U. H.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Voytik-Harbin, S. L.

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Wolf, K.

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Wong, J. Y.

S. Köster, H. M. Evans, J. Y. Wong, and T. Pfohl, “An in situ study of collagen self-assembly processes,” Biomacromolecules9(1), 199–207 (2008).
[CrossRef] [PubMed]

Yadavalli, V. K.

V. K. Yadavalli, D. V. Svintradze, and R. M. Pidaparti, “Nanoscale measurements of the assembly of collagen to fibrils,” Int. J. Biol. Macromol.46(4), 458–464 (2010).
[CrossRef] [PubMed]

Yang, Y. L.

Y. L. Yang and L. J. Kaufman, “Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly,” Biophys. J.96(4), 1566–1585 (2009).
[CrossRef] [PubMed]

Yeh, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Zoumi, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

Biomacromolecules (1)

S. Köster, H. M. Evans, J. Y. Wong, and T. Pfohl, “An in situ study of collagen self-assembly processes,” Biomacromolecules9(1), 199–207 (2008).
[CrossRef] [PubMed]

Biomed. Opt. Express (1)

Biophys. J. (5)

I. Gusachenko, V. Tran, Y. G. Houssen, J.-M. Allain, and M.-C. Schanne-Klein, “Polarization-resolved second-harmonic microscopy in tendon upon mechanical stretching,” Biophys. J.102(9), 2220–2229 (2012).
[CrossRef]

C. B. Raub, V. Suresh, T. Krasieva, J. Lyubovitsky, J. D. Mih, A. J. Putnam, B. J. Tromberg, and S. C. George, “Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy,” Biophys. J.92(6), 2212–2222 (2007).
[CrossRef] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Y. L. Yang and L. J. Kaufman, “Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly,” Biophys. J.96(4), 1566–1585 (2009).
[CrossRef] [PubMed]

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

Biopolymers (1)

A. O. Brightman, B. P. Rajwa, J. E. Sturgis, M. E. McCallister, J. P. Robinson, and S. L. Voytik-Harbin, “Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro,” Biopolymers54(3), 222–234 (2000).
[CrossRef] [PubMed]

Int. J. Biol. Macromol. (1)

V. K. Yadavalli, D. V. Svintradze, and R. M. Pidaparti, “Nanoscale measurements of the assembly of collagen to fibrils,” Int. J. Biol. Macromol.46(4), 458–464 (2010).
[CrossRef] [PubMed]

J. Am. Chem. Soc. (1)

A.-M. Pena, T. Boulesteix, T. Dartigalongue, and M.-C. Schanne-Klein, “Chiroptical effects in the second harmonic signal of collagens I and IV,” J. Am. Chem. Soc.127(29), 10314–10322 (2005).
[CrossRef] [PubMed]

J. Appl. Phys. (1)

C. Bayan, J. M. Levitt, E. Miller, D. Kaplan, and I. Georgakoudi, “Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels,” J. Appl. Phys.105(10), 102042 (2009).
[CrossRef]

J. Biomech. (1)

M.-M. Giraud-Guille, L. Besseau, and R. Martin, “Liquid crystalline assemblies of collagen in bone and in vitro systems,” J. Biomech.36(10), 1571–1579 (2003).
[CrossRef] [PubMed]

J. Biomed. Opt. (1)

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, F. Leroy, E. Beaurepaire, J.-L. Martin, A. Colonna, and M.-C. Schanne-Klein, “Multiphoton microscopy of engineered dermal substitutes: assessment of 3-D collagen matrix remodeling induced by fibroblast contraction,” J. Biomed. Opt.15(5), 056018 (2010).
[CrossRef] [PubMed]

J. Mol. Biol. (1)

F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, M.-M. Giraud-Guille, and E. Belamie, “Fibrillogenesis in dense collagen solutions: a physicochemical study,” J. Mol. Biol.376(5), 1509–1522 (2008).
[CrossRef] [PubMed]

J. Phys. Chem. B (1)

A. Deniset-Besseau, J. Duboisset, E. Benichou, F. Hache, P.-F. Brevet, and M.-C. Schanne-Klein, “Measurement of the second-order hyperpolarizability of the collagen triple helix and determination of its physical origin,” J. Phys. Chem. B113(40), 13437–13445 (2009).
[CrossRef] [PubMed]

J. Struct. Biol. (3)

F. Z. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” J. Struct. Biol.148(3), 268–278 (2004).
[CrossRef] [PubMed]

D. A. Cisneros, C. Hung, C. M. Franz, and D. J. Muller, “Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy,” J. Struct. Biol.154(3), 232–245 (2006).
[CrossRef] [PubMed]

M.-M. Giraud-Guille, L. Besseau, D. Herbage, and P. Gounon, “Optimization of Collagen Liquid-Crystalline Assemblies - Influence of Sonic Fragmentation,” J. Struct. Biol.113(2), 99–106 (1994).
[CrossRef]

Micron (1)

J. R. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: fibril polymorphism and colloidal gold labelling,” Micron38(5), 513–521 (2007).
[CrossRef] [PubMed]

Opt. Express (2)

Opt. Lett. (1)

Proc. Natl. Acad. Sci. U.S.A. (2)

A. Zoumi, A. Yeh, and B. J. Tromberg, “Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence,” Proc. Natl. Acad. Sci. U.S.A.99(17), 11014–11019 (2002).
[CrossRef] [PubMed]

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(12), 7075–7080 (2003).
[CrossRef] [PubMed]

Semin. Cell Dev. Biol. (1)

K. Wolf, S. Alexander, V. Schacht, L. M. Coussens, U. H. von Andrian, J. van Rheenen, E. Deryugina, and P. Friedl, “Collagen-based cell migration models in vitro and in vivo,” Semin. Cell Dev. Biol.20(8), 931–941 (2009).
[CrossRef] [PubMed]

Soft Matter (1)

M.-M. Giraud Guille, C. Helary, S. Vigier, and N. Nassif, “Dense fibrillar collagen matrices for tissue repair,” Soft Matter6(20), 4963–4967 (2010).
[CrossRef]

Top. Curr. Chem. (1)

D. E. Birk and P. Bruckner, “Collagen suprastructures,” Top. Curr. Chem.247, 185–205 (2005).

Other (2)

T. Starborg, Y. Lu, K. E. Kadler, and D. F. Holmes, “Electron microscopy of collagen fibril—structure in vitro and in vivo including three-dimensional reconstruction,” in Methods in Cell Biology (Elsevier, 2008), Vol. 88, 319–345.

R. W. Boyd, Nonlinear Optics (Academic, 2003).

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Figures (4)

Fig. 1
Fig. 1

3D reconstruction of SHG images of collagen fibrillogenesis in a slow kinetic sample (pH = 6.5 ± 0.3). Acquisition times are indicated in top of every image. Image size: 163 × 159 × 30 µm3.

Fig. 2
Fig. 2

TEM micrographs of collagen fibrils observed in a slow kinetic sample (pH = 6.5 ± 0.3), at different magnifications. Red arrows underline the characteristic D-banded periodicity.

Fig. 3
Fig. 3

Quantization of collagen fibrillogenesis using a statistical approach. Fibril volume density (pixel fraction, %) over time (min) for (a) a slow kinetics sample (pH = 6.5 ± 0.3): τ = 352 ± 59 min and (b) a fast kinetics sample (pH = 7.5 ± 0.3): τ = 33 ± 7 min. Black squares and red lines correspond to experimental data and exponential fitting respectively. Green line figures the asymptote of the exponential fit. (c) Statistics over all samples (see Table 1) in every condition. Red and green columns represent respectively the mean time constants and the mean rise time at origin for slow (sparse hatching) and fast (dense hatching) kinetics; error bars represent the standard error of the mean.

Fig. 4
Fig. 4

Kinetics of single fibril growth. (a) SHG images of the same fibril at increasing times after the onset of fibrillogenesis (scale bar: 5µm). (b) Kinetic diagram of the fibril length evolution. (c) Time profile of the area fraction of pixels with significant SHG signal during single fibril formation. The red line corresponds to exponential fitting and provides a time constant of the fibril lengthening of 103 ± 18 min.

Tables (1)

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Table 1 Time constants obtained for all samples with slow and fast kineticsa

Equations (1)

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y(t)= τ B ( 1 e t τ ),

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