Abstract

We provide evidence that the chirality of collagen can give rise to strong second-harmonic generation circular dichroism (SHG-CD) responses in nonlinear microscopy. Although chirality is an intrinsic structural property of collagen, most of the previous studies ignore that property. We demonstrate chiral imaging of individual collagen fibers by using a laser scanning microscope and type-I collagen from pig ligaments. 100% contrast level of SHG-CD is achieved with sub-micrometer spatial resolution. As a new contrast mechanism for imaging chiral structures in bio-tissues, this technique provides information about collagen morphology and three-dimensional orientation of collagen molecules.

© 2013 OSA

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2012 (4)

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[CrossRef] [PubMed]

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
[CrossRef] [PubMed]

T. Y. Lau, R. Ambekar, and K. C. Toussaint, “Quantification of collagen fiber organization using three-dimensional Fourier transform-second-harmonic generation imaging,” Opt. Express20(19), 21821–21832 (2012).
[CrossRef] [PubMed]

X. Y. Chen, C. Raggio, and P. J. Campagnola, “Second-harmonic generation circular dichroism studies of osteogenesis imperfecta,” Opt. Lett.37(18), 3837–3839 (2012).
[CrossRef] [PubMed]

2011 (7)

M. J. Huttunen, G. Bautista, M. Decker, S. Linden, M. Wegener, and M. Kauranen, “Nonlinear chiral imaging of subwavelength-sized twisted-cross gold nanodimers Invited,” Opt. Mater. Express1(1), 46–56 (2011).
[CrossRef]

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
[CrossRef] [PubMed]

D. J. Kissick, D. Wanapun, and G. J. Simpson, “Second-order nonlinear optical imaging of chiral crystals,” Annu. Rev. Anal. Chem.4(1), 419–437 (2011).
[CrossRef] [PubMed]

S. Tripathi, B. J. Davis, K. C. Toussaint, and P. S. Carney, “Determination of the second-order nonlinear susceptibility elements of a single nanoparticle using coherent optical microscopy,” J. Phys. B44(1), 015401 (2011).
[CrossRef]

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
[CrossRef] [PubMed]

P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J.100(8), 2053–2062 (2011).
[CrossRef] [PubMed]

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
[CrossRef] [PubMed]

2010 (7)

E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol.86(2), 302–310 (2010).
[CrossRef] [PubMed]

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
[CrossRef] [PubMed]

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer10(1), 94 (2010).
[CrossRef] [PubMed]

C. Loison and D. Simon, “Additive model for the second harmonic generation hyperpolarizability applied to a collagen-mimicking peptide (Pro-Pro-Gly)10,” J. Phys. Chem. A114(29), 7769–7779 (2010).
[CrossRef] [PubMed]

F. Hache, “Quantum calculation of the second-order hyperpolarizability of chiral molecules in the “one-electron” model,” J. Phys. Chem. A114(37), 10277–10286 (2010).
[CrossRef] [PubMed]

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

S. Brasselet, D. Aït-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express18(14), 14859–14870 (2010).
[CrossRef] [PubMed]

2009 (3)

M. J. Huttunen, M. Erkintalo, and M. Kauranen, “Absolute nonlinear optical probes of surface chirality,” J. Opt. A, Pure Appl. Opt.11(3), 034006 (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]

L. M. Haupert and G. J. Simpson, “Chirality in nonlinear optics,” Annu. Rev. Phys. Chem.60(1), 345–365 (2009).
[CrossRef] [PubMed]

2008 (1)

E. J. Gualtieri, L. M. Haupert, and G. J. Simpson, “Interpreting nonlinear optics of biopolymer assemblies: Finding a hook,” Chem. Phys. Lett.465(4-6), 167–174 (2008).
[CrossRef]

2007 (4)

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt.12(4), 044002 (2007).
[CrossRef] [PubMed]

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech.70(2), 162–170 (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]

F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express15(19), 12286–12295 (2007).
[CrossRef] [PubMed]

2006 (1)

2005 (3)

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

M. A. Kriech and J. C. Conboy, “Imaging chirality with surface second harmonic generation microscopy,” J. Am. Chem. Soc.127(9), 2834–2835 (2005).
[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]

2003 (2)

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
[CrossRef] [PubMed]

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol.21(11), 1356–1360 (2003).
[CrossRef] [PubMed]

2002 (1)

1999 (1)

J. Baum and B. Brodsky, “Folding of peptide models of collagen and misfolding in disease,” Curr. Opin. Struct. Biol.9(1), 122–128 (1999).
[CrossRef] [PubMed]

1997 (2)

Y. B. Feng, G. Melacini, and M. Goodman, “Collagen-based structures containing the peptoid residue N-isobutylglycine (Nleu): synthesis and biophysical studies of Gly-Nleu-Pro sequences by circular dichroism and optical rotation,” Biochemistry36(29), 8716–8724 (1997).
[CrossRef] [PubMed]

J. F. de Boer, T. E. Milner, M. J. C. van Gemert, and J. S. Nelson, “Two-dimensional birefringence imaging in biological tissue by polarization-sensitive optical coherence tomography,” Opt. Lett.22(12), 934–936 (1997).
[CrossRef] [PubMed]

1995 (1)

J. J. Maki, M. Kauranen, and A. Persoons, “Surface second-harmonic generation from chiral materials,” Phys. Rev. B51(3), 1425–1434 (1995).
[CrossRef]

1994 (2)

M. Kauranen, T. Verbiest, J. J. Maki, and A. Persoons, “Second-harmonic generation from chiral surfaces,” J. Chem. Phys.101(9), 8193–8199 (1994).
[CrossRef]

J. D. Byers, H. I. Yee, and J. M. Hicks, “A second harmonic generation analog of optical rotatory dispersion for the study of chiral monolayers,” J. Chem. Phys.101(7), 6233–6241 (1994).
[CrossRef]

1993 (1)

T. Petralli-Mallow, T. M. Wong, J. D. Byers, H. I. Yee, and J. M. Hicks, “Circular dichroism spectroscopy at interfaces: a surface second harmonic generation study,” J. Phys. Chem.97(7), 1383–1388 (1993).
[CrossRef]

1979 (1)

S. Roth and I. Freund, “Second harmonic-generation in collagen,” J. Chem. Phys.70(4), 1637–1643 (1979).
[CrossRef]

1971 (1)

L. D. Barron and A. D. Buckingham, “Rayleigh and Raman scattering from optically active molecules,” Mol. Phys.20(6), 1111–1119 (1971).
[CrossRef]

Aït-Belkacem, D.

Ambekar, R.

Barron, L. D.

L. D. Barron and A. D. Buckingham, “Rayleigh and Raman scattering from optically active molecules,” Mol. Phys.20(6), 1111–1119 (1971).
[CrossRef]

Baum, J.

J. Baum and B. Brodsky, “Folding of peptide models of collagen and misfolding in disease,” Curr. Opin. Struct. Biol.9(1), 122–128 (1999).
[CrossRef] [PubMed]

Bautista, G.

Beaurepaire, E.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech.70(2), 162–170 (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]

Behar-Cohen, F.

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[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]

Biagioni, P.

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
[CrossRef] [PubMed]

Boucher, Y.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
[CrossRef] [PubMed]

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]

Bourges, J. L.

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[CrossRef] [PubMed]

Brasselet, S.

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]

Brewer, M. A.

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer10(1), 94 (2010).
[CrossRef] [PubMed]

Brodsky, B.

J. Baum and B. Brodsky, “Folding of peptide models of collagen and misfolding in disease,” Curr. Opin. Struct. Biol.9(1), 122–128 (1999).
[CrossRef] [PubMed]

Brown, D. J.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
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J. D. Byers, H. I. Yee, and J. M. Hicks, “A second harmonic generation analog of optical rotatory dispersion for the study of chiral monolayers,” J. Chem. Phys.101(7), 6233–6241 (1994).
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X. Y. Chen, C. Raggio, and P. J. Campagnola, “Second-harmonic generation circular dichroism studies of osteogenesis imperfecta,” Opt. Lett.37(18), 3837–3839 (2012).
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S. Tripathi, B. J. Davis, K. C. Toussaint, and P. S. Carney, “Determination of the second-order nonlinear susceptibility elements of a single nanoparticle using coherent optical microscopy,” J. Phys. B44(1), 015401 (2011).
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M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
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Chen, J. X.

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
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Chen, W. L.

P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J.100(8), 2053–2062 (2011).
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Chen, X. Y.

Chen, Y. F.

P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J.100(8), 2053–2062 (2011).
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Cheng, J.-X.

Chu, S. W.

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Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
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R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
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M. A. Kriech and J. C. Conboy, “Imaging chirality with surface second harmonic generation microscopy,” J. Am. Chem. Soc.127(9), 2834–2835 (2005).
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de Boer, J. F.

De Giorgi, V.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
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E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol.86(2), 302–310 (2010).
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E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
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P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J.100(8), 2053–2062 (2011).
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Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
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E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol.86(2), 302–310 (2010).
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M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
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A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt.12(4), 044002 (2007).
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Gasecka, A.

Goodman, M.

Y. B. Feng, G. Melacini, and M. Goodman, “Collagen-based structures containing the peptoid residue N-isobutylglycine (Nleu): synthesis and biophysical studies of Gly-Nleu-Pro sequences by circular dichroism and optical rotation,” Biochemistry36(29), 8716–8724 (1997).
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Gualtieri, E. J.

E. J. Gualtieri, L. M. Haupert, and G. J. Simpson, “Interpreting nonlinear optics of biopolymer assemblies: Finding a hook,” Chem. Phys. Lett.465(4-6), 167–174 (2008).
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Guller, A. E.

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
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Hache, F.

F. Hache, “Quantum calculation of the second-order hyperpolarizability of chiral molecules in the “one-electron” model,” J. Phys. Chem. A114(37), 10277–10286 (2010).
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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).
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L. M. Haupert and G. J. Simpson, “Chirality in nonlinear optics,” Annu. Rev. Phys. Chem.60(1), 345–365 (2009).
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E. J. Gualtieri, L. M. Haupert, and G. J. Simpson, “Interpreting nonlinear optics of biopolymer assemblies: Finding a hook,” Chem. Phys. Lett.465(4-6), 167–174 (2008).
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Hecht, B.

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
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Hernest, M.

Hicks, J. M.

J. D. Byers, H. I. Yee, and J. M. Hicks, “A second harmonic generation analog of optical rotatory dispersion for the study of chiral monolayers,” J. Chem. Phys.101(7), 6233–6241 (1994).
[CrossRef]

T. Petralli-Mallow, T. M. Wong, J. D. Byers, H. I. Yee, and J. M. Hicks, “Circular dichroism spectroscopy at interfaces: a surface second harmonic generation study,” J. Phys. Chem.97(7), 1383–1388 (1993).
[CrossRef]

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A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt.12(4), 044002 (2007).
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Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
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Huang, Y. C.

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
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Huttunen, M. J.

M. J. Huttunen, G. Bautista, M. Decker, S. Linden, M. Wegener, and M. Kauranen, “Nonlinear chiral imaging of subwavelength-sized twisted-cross gold nanodimers Invited,” Opt. Mater. Express1(1), 46–56 (2011).
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M. J. Huttunen, M. Erkintalo, and M. Kauranen, “Absolute nonlinear optical probes of surface chirality,” J. Opt. A, Pure Appl. Opt.11(3), 034006 (2009).
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Ignatieva, N. Y.

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
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Jain, R. K.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
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Jester, B.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
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Jester, J. V.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
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Jiang, X. S.

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
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Jin, L.

Juhasz, T.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
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Kamensky, V. A.

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
[CrossRef] [PubMed]

Kapsokalyvas, D.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
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Kauranen, M.

M. J. Huttunen, G. Bautista, M. Decker, S. Linden, M. Wegener, and M. Kauranen, “Nonlinear chiral imaging of subwavelength-sized twisted-cross gold nanodimers Invited,” Opt. Mater. Express1(1), 46–56 (2011).
[CrossRef]

M. J. Huttunen, M. Erkintalo, and M. Kauranen, “Absolute nonlinear optical probes of surface chirality,” J. Opt. A, Pure Appl. Opt.11(3), 034006 (2009).
[CrossRef]

J. J. Maki, M. Kauranen, and A. Persoons, “Surface second-harmonic generation from chiral materials,” Phys. Rev. B51(3), 1425–1434 (1995).
[CrossRef]

M. Kauranen, T. Verbiest, J. J. Maki, and A. Persoons, “Second-harmonic generation from chiral surfaces,” J. Chem. Phys.101(9), 8193–8199 (1994).
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D. J. Kissick, D. Wanapun, and G. J. Simpson, “Second-order nonlinear optical imaging of chiral crystals,” Annu. Rev. Anal. Chem.4(1), 419–437 (2011).
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Kowalczuk, L.

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
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Kriech, M. A.

M. A. Kriech and J. C. Conboy, “Imaging chirality with surface second harmonic generation microscopy,” J. Am. Chem. Soc.127(9), 2834–2835 (2005).
[CrossRef] [PubMed]

Kriling, S.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
[CrossRef] [PubMed]

LaComb, R. B.

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer10(1), 94 (2010).
[CrossRef] [PubMed]

Lai, H. M.

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

Latour, G.

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[CrossRef] [PubMed]

Lau, T. Y.

Liao, C. S.

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

Linden, S.

Lindgren, M.

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt.12(4), 044002 (2007).
[CrossRef] [PubMed]

Liu, Y. C.

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
[CrossRef] [PubMed]

Lo, W.

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

Loew, L. M.

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol.21(11), 1356–1360 (2003).
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Loison, C.

C. Loison and D. Simon, “Additive model for the second harmonic generation hyperpolarizability applied to a collagen-mimicking peptide (Pro-Pro-Gly)10,” J. Phys. Chem. A114(29), 7769–7779 (2010).
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Lotti, T.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
[CrossRef] [PubMed]

Ma, H.

Maio, V.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
[CrossRef] [PubMed]

Maki, J. J.

J. J. Maki, M. Kauranen, and A. Persoons, “Surface second-harmonic generation from chiral materials,” Phys. Rev. B51(3), 1425–1434 (1995).
[CrossRef]

M. Kauranen, T. Verbiest, J. J. Maki, and A. Persoons, “Second-harmonic generation from chiral surfaces,” J. Chem. Phys.101(9), 8193–8199 (1994).
[CrossRef]

Marchal-Somme, J.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech.70(2), 162–170 (2007).
[CrossRef] [PubMed]

Martin, J. L.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech.70(2), 162–170 (2007).
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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).
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Massi, D.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
[CrossRef] [PubMed]

McKee, T.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
[CrossRef] [PubMed]

Melacini, G.

Y. B. Feng, G. Melacini, and M. Goodman, “Collagen-based structures containing the peptoid residue N-isobutylglycine (Nleu): synthesis and biophysical studies of Gly-Nleu-Pro sequences by circular dichroism and optical rotation,” Biochemistry36(29), 8716–8724 (1997).
[CrossRef] [PubMed]

Meskers, S. C. J.

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
[CrossRef] [PubMed]

Milner, T. E.

Munhoz, F.

Nadiarnykh, O.

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer10(1), 94 (2010).
[CrossRef] [PubMed]

Nelson, J. S.

Netter, P.

E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol.86(2), 302–310 (2010).
[CrossRef] [PubMed]

Nien, C. J.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
[CrossRef] [PubMed]

Ortegren, J.

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt.12(4), 044002 (2007).
[CrossRef] [PubMed]

Pavone, F. S.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
[CrossRef] [PubMed]

Pena, A. M.

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech.70(2), 162–170 (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]

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]

Persoons, A.

J. J. Maki, M. Kauranen, and A. Persoons, “Surface second-harmonic generation from chiral materials,” Phys. Rev. B51(3), 1425–1434 (1995).
[CrossRef]

M. Kauranen, T. Verbiest, J. J. Maki, and A. Persoons, “Second-harmonic generation from chiral surfaces,” J. Chem. Phys.101(9), 8193–8199 (1994).
[CrossRef]

Petralli-Mallow, T.

T. Petralli-Mallow, T. M. Wong, J. D. Byers, H. I. Yee, and J. M. Hicks, “Circular dichroism spectroscopy at interfaces: a surface second harmonic generation study,” J. Phys. Chem.97(7), 1383–1388 (1993).
[CrossRef]

Plamann, K.

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[CrossRef] [PubMed]

Pluen, A.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
[CrossRef] [PubMed]

Raggio, C.

Recher, G.

Roth, S.

S. Roth and I. Freund, “Second harmonic-generation in collagen,” J. Chem. Phys.70(4), 1637–1643 (1979).
[CrossRef]

Rouède, D.

Sandnes, B.

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
[CrossRef] [PubMed]

Savoini, M.

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
[CrossRef] [PubMed]

Savoldelli, M.

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[CrossRef] [PubMed]

Schanne-Klein, M. C.

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[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]

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech.70(2), 162–170 (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]

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]

Seed, B.

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
[CrossRef] [PubMed]

Shekhter, A. B.

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
[CrossRef] [PubMed]

Simon, D.

C. Loison and D. Simon, “Additive model for the second harmonic generation hyperpolarizability applied to a collagen-mimicking peptide (Pro-Pro-Gly)10,” J. Phys. Chem. A114(29), 7769–7779 (2010).
[CrossRef] [PubMed]

Simpson, G. J.

D. J. Kissick, D. Wanapun, and G. J. Simpson, “Second-order nonlinear optical imaging of chiral crystals,” Annu. Rev. Anal. Chem.4(1), 419–437 (2011).
[CrossRef] [PubMed]

L. M. Haupert and G. J. Simpson, “Chirality in nonlinear optics,” Annu. Rev. Phys. Chem.60(1), 345–365 (2009).
[CrossRef] [PubMed]

E. J. Gualtieri, L. M. Haupert, and G. J. Simpson, “Interpreting nonlinear optics of biopolymer assemblies: Finding a hook,” Chem. Phys. Lett.465(4-6), 167–174 (2008).
[CrossRef]

Stoltz, J. F.

E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol.86(2), 302–310 (2010).
[CrossRef] [PubMed]

Strupler, M.

Su, P. J.

P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J.100(8), 2053–2062 (2011).
[CrossRef] [PubMed]

Tharaux, P. L.

Tiaho, F.

Toussaint, K. C.

T. Y. Lau, R. Ambekar, and K. C. Toussaint, “Quantification of collagen fiber organization using three-dimensional Fourier transform-second-harmonic generation imaging,” Opt. Express20(19), 21821–21832 (2012).
[CrossRef] [PubMed]

S. Tripathi, B. J. Davis, K. C. Toussaint, and P. S. Carney, “Determination of the second-order nonlinear susceptibility elements of a single nanoparticle using coherent optical microscopy,” J. Phys. B44(1), 015401 (2011).
[CrossRef]

Tripathi, S.

S. Tripathi, B. J. Davis, K. C. Toussaint, and P. S. Carney, “Determination of the second-order nonlinear susceptibility elements of a single nanoparticle using coherent optical microscopy,” J. Phys. B44(1), 015401 (2011).
[CrossRef]

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Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

van Gemert, M. J. C.

Van Wiechen, A.

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
[CrossRef] [PubMed]

Verbiest, T.

M. Kauranen, T. Verbiest, J. J. Maki, and A. Persoons, “Second-harmonic generation from chiral surfaces,” J. Chem. Phys.101(9), 8193–8199 (1994).
[CrossRef]

Wanapun, D.

D. J. Kissick, D. Wanapun, and G. J. Simpson, “Second-order nonlinear optical imaging of chiral crystals,” Annu. Rev. Anal. Chem.4(1), 419–437 (2011).
[CrossRef] [PubMed]

Wang, Y.

Webb, W. W.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

Wegener, M.

Werkmeister, E.

E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol.86(2), 302–310 (2010).
[CrossRef] [PubMed]

Williams, R. M.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

Winkler, M.

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
[CrossRef] [PubMed]

Wong, T. M.

T. Petralli-Mallow, T. M. Wong, J. D. Byers, H. I. Yee, and J. M. Hicks, “Circular dichroism spectroscopy at interfaces: a surface second harmonic generation study,” J. Phys. Chem.97(7), 1383–1388 (1993).
[CrossRef]

Wu, X. F.

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
[CrossRef] [PubMed]

Xie, X. S.

Xu, J.

Xue, P.

Yee, H. I.

J. D. Byers, H. I. Yee, and J. M. Hicks, “A second harmonic generation analog of optical rotatory dispersion for the study of chiral monolayers,” J. Chem. Phys.101(7), 6233–6241 (1994).
[CrossRef]

T. Petralli-Mallow, T. M. Wong, J. D. Byers, H. I. Yee, and J. M. Hicks, “Circular dichroism spectroscopy at interfaces: a surface second harmonic generation study,” J. Phys. Chem.97(7), 1383–1388 (1993).
[CrossRef]

Yu, H. B.

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
[CrossRef] [PubMed]

Yu, J. Y.

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

Zakharkina, O. L.

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
[CrossRef] [PubMed]

Zhong, J. Z.

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
[CrossRef] [PubMed]

Zhuo, S. M.

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
[CrossRef] [PubMed]

Zhuo, Z. Y.

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

Ziegler, J.

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
[CrossRef] [PubMed]

Zipfel, W. R.

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

Zvyagin, A. V.

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
[CrossRef] [PubMed]

Annu. Rev. Anal. Chem. (1)

D. J. Kissick, D. Wanapun, and G. J. Simpson, “Second-order nonlinear optical imaging of chiral crystals,” Annu. Rev. Anal. Chem.4(1), 419–437 (2011).
[CrossRef] [PubMed]

Annu. Rev. Phys. Chem. (1)

L. M. Haupert and G. J. Simpson, “Chirality in nonlinear optics,” Annu. Rev. Phys. Chem.60(1), 345–365 (2009).
[CrossRef] [PubMed]

Biochemistry (1)

Y. B. Feng, G. Melacini, and M. Goodman, “Collagen-based structures containing the peptoid residue N-isobutylglycine (Nleu): synthesis and biophysical studies of Gly-Nleu-Pro sequences by circular dichroism and optical rotation,” Biochemistry36(29), 8716–8724 (1997).
[CrossRef] [PubMed]

Biophys. J. (2)

R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophys. J.88(2), 1377–1386 (2005).
[CrossRef] [PubMed]

P. J. Su, W. L. Chen, Y. F. Chen, and C. Y. Dong, “Determination of collagen nanostructure from second-order susceptibility tensor analysis,” Biophys. J.100(8), 2053–2062 (2011).
[CrossRef] [PubMed]

BMC Cancer (1)

O. Nadiarnykh, R. B. LaComb, M. A. Brewer, and P. J. Campagnola, “Alterations of the extracellular matrix in ovarian cancer studied by Second Harmonic Generation imaging microscopy,” BMC Cancer10(1), 94 (2010).
[CrossRef] [PubMed]

Chem. Phys. Lett. (1)

E. J. Gualtieri, L. M. Haupert, and G. J. Simpson, “Interpreting nonlinear optics of biopolymer assemblies: Finding a hook,” Chem. Phys. Lett.465(4-6), 167–174 (2008).
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Curr. Opin. Struct. Biol. (1)

J. Baum and B. Brodsky, “Folding of peptide models of collagen and misfolding in disease,” Curr. Opin. Struct. Biol.9(1), 122–128 (1999).
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Invest. Ophthalmol. Vis. Sci. (1)

M. Winkler, D. Chai, S. Kriling, C. J. Nien, D. J. Brown, B. Jester, T. Juhasz, and J. V. Jester, “Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics,” Invest. Ophthalmol. Vis. Sci.52(12), 8818–8827 (2011).
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J. Am. Chem. Soc. (3)

M. A. Kriech and J. C. Conboy, “Imaging chirality with surface second harmonic generation microscopy,” J. Am. Chem. Soc.127(9), 2834–2835 (2005).
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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]

M. Savoini, X. F. Wu, M. Celebrano, J. Ziegler, P. Biagioni, S. C. J. Meskers, L. Duò, B. Hecht, and M. Finazzi, “Circular dichroism probed by two-photon fluorescence microscopy in enantiopure chiral polyfluorene thin films,” J. Am. Chem. Soc.134(13), 5832–5835 (2012).
[CrossRef] [PubMed]

J. Biomed. Opt. (1)

A. Erikson, J. Ortegren, T. Hompland, C. de Lange Davies, and M. Lindgren, “Quantification of the second-order nonlinear susceptibility of collagen I using a laser scanning microscope,” J. Biomed. Opt.12(4), 044002 (2007).
[CrossRef] [PubMed]

J. Biophotonics (1)

R. Cicchi, D. Kapsokalyvas, V. De Giorgi, V. Maio, A. Van Wiechen, D. Massi, T. Lotti, and F. S. Pavone, “Scoring of collagen organization in healthy and diseased human dermis by multiphoton microscopy,” J. Biophotonics3(1-2), 34–43 (2010).
[CrossRef] [PubMed]

J. Chem. Phys. (3)

S. Roth and I. Freund, “Second harmonic-generation in collagen,” J. Chem. Phys.70(4), 1637–1643 (1979).
[CrossRef]

M. Kauranen, T. Verbiest, J. J. Maki, and A. Persoons, “Second-harmonic generation from chiral surfaces,” J. Chem. Phys.101(9), 8193–8199 (1994).
[CrossRef]

J. D. Byers, H. I. Yee, and J. M. Hicks, “A second harmonic generation analog of optical rotatory dispersion for the study of chiral monolayers,” J. Chem. Phys.101(7), 6233–6241 (1994).
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J. Opt. A, Pure Appl. Opt. (1)

M. J. Huttunen, M. Erkintalo, and M. Kauranen, “Absolute nonlinear optical probes of surface chirality,” J. Opt. A, Pure Appl. Opt.11(3), 034006 (2009).
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J. Opt. Soc. Am. B (1)

J. Phys. B (1)

S. Tripathi, B. J. Davis, K. C. Toussaint, and P. S. Carney, “Determination of the second-order nonlinear susceptibility elements of a single nanoparticle using coherent optical microscopy,” J. Phys. B44(1), 015401 (2011).
[CrossRef]

J. Phys. Chem. (1)

T. Petralli-Mallow, T. M. Wong, J. D. Byers, H. I. Yee, and J. M. Hicks, “Circular dichroism spectroscopy at interfaces: a surface second harmonic generation study,” J. Phys. Chem.97(7), 1383–1388 (1993).
[CrossRef]

J. Phys. Chem. A (2)

C. Loison and D. Simon, “Additive model for the second harmonic generation hyperpolarizability applied to a collagen-mimicking peptide (Pro-Pro-Gly)10,” J. Phys. Chem. A114(29), 7769–7779 (2010).
[CrossRef] [PubMed]

F. Hache, “Quantum calculation of the second-order hyperpolarizability of chiral molecules in the “one-electron” model,” J. Phys. Chem. A114(37), 10277–10286 (2010).
[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. (1)

Z. Y. Zhuo, C. S. Liao, C. H. Huang, J. Y. Yu, Y. Y. Tzeng, W. Lo, C. Y. Dong, H. C. Chui, Y. C. Huang, H. M. Lai, and S. W. Chu, “Second harmonic generation imaging — a new method for unraveling molecular information of starch,” J. Struct. Biol.171(1), 88–94 (2010).
[CrossRef] [PubMed]

Lasers Med. Sci. (1)

N. Y. Ignatieva, A. E. Guller, O. L. Zakharkina, B. Sandnes, A. B. Shekhter, V. A. Kamensky, and A. V. Zvyagin, “Laser-induced modification of the patellar ligament tissue: comparative study of structural and optical changes,” Lasers Med. Sci.26(3), 401–413 (2011).
[CrossRef] [PubMed]

Microsc. Res. Tech. (1)

A. M. Pena, A. Fabre, D. Débarre, J. Marchal-Somme, B. Crestani, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, “Three-dimensional investigation and scoring of extracellular matrix remodeling during lung fibrosis using multiphoton microscopy,” Microsc. Res. Tech.70(2), 162–170 (2007).
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L. D. Barron and A. D. Buckingham, “Rayleigh and Raman scattering from optically active molecules,” Mol. Phys.20(6), 1111–1119 (1971).
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Nat. Biotechnol. (1)

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol.21(11), 1356–1360 (2003).
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Nat. Med. (1)

E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med.9(6), 796–801 (2003).
[CrossRef] [PubMed]

Opt. Express (5)

Opt. Lett. (2)

Opt. Mater. Express (1)

Photochem. Photobiol. (1)

E. Werkmeister, N. de Isla, P. Netter, J. F. Stoltz, and D. Dumas, “Collagenous extracellular matrix of cartilage submitted to mechanical forces studied by second harmonic generation microscopy,” Photochem. Photobiol.86(2), 302–310 (2010).
[CrossRef] [PubMed]

Phys. Rev. B (1)

J. J. Maki, M. Kauranen, and A. Persoons, “Surface second-harmonic generation from chiral materials,” Phys. Rev. B51(3), 1425–1434 (1995).
[CrossRef]

PLoS ONE (1)

G. Latour, L. Kowalczuk, M. Savoldelli, J. L. Bourges, K. Plamann, F. Behar-Cohen, and M. C. Schanne-Klein, “Hyperglycemia-induced abnormalities in rat and human corneas: the potential of second harmonic generation microscopy,” PLoS ONE7(11), e48388 (2012).
[CrossRef] [PubMed]

Scanning (1)

X. S. Jiang, J. Z. Zhong, Y. C. Liu, H. B. Yu, S. M. Zhuo, and J. X. Chen, “Two-photon fluorescence and second-harmonic generation imaging of collagen in human tissue based on multiphoton microscopy,” Scanning33(1), 53–56 (2011).
[CrossRef] [PubMed]

Other (3)

A. Yariv and P. Yeh, Photonics - Optical Electronics in Modern Communications (Oxford University Express, 2007), Chap. 9.

A. B. H. Lodish, S. L. Zipursky, P. Matsudaira, D. Baltimore, and J. Darnell, “Collagen: the fibrous proteins of the matrix,” in Molecular Cell Biology (W. H. Freeman & Co, 2000).

L. D. Barron, Molecular Light Scattering and Optical Activity (Cambridge University Press, 1982), Chap. 5.

Supplementary Material (1)

» Media 1: MOV (462 KB)     

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Figures (3)

Fig. 1
Fig. 1

(a) Schematic representation of the collagen triple helix, consisting of a heterotrimer of alpha peptides. The red and blue colors correspond to α1 and α2 chains, respectively. Scale bar corresponds to 10 nm. Model susceptibilities of the collagen were formed by summing up (b) homotrimers or (c) heterotrimers of harmonophores with C symmetry. Also (d) homotrimers with C2v symmetry were considered.

Fig. 2
Fig. 2

(a) and (b) are the lateral (x-y) SHG images of the ligament illuminated by excitations in LCP and RCP, respectively. The gray bars describe the SHG intensity counted by PMT. (c) is the SHG-CD image calculated pixel-wise from (a) and (b) with ImageJ software. The green and red colors indicate the SHG-CD value with positive sign and negative sign, respectively. (d) to (f) show results from different ligaments, demonstrating the reproducibility of SHG-CD responses. All scale bars are 5 μm. (g) θ is defined as the angle between the collagen molecular orientation z and the transverse XY-plane. Z denotes the direction of excitation. (h) Calculated SHG-CD responses as a function of the θ angle.

Fig. 3
Fig. 3

Optical sections of SHG-CD in a collagen fiber (Media 1).

Tables (1)

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Table 1 The Symmetry Groups and Corresponding Non-Zero Molecular Hyperpolarizabilities of the Harmonophores Together with the Symmetry Groups of the Calculated Susceptibilitiesa

Equations (2)

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χ IJK (2) = m=1 N ijk [ c Ii c Jj c Kk β ijk ] m ,
I SHGCD = [ I LCP (2ω) I RCP (2ω)] [ I LCP (2ω)+ I RCP (2ω)]/2 .

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