Abstract

We present a study of the optical second-order nonlinearity of type I collagen fibers grown in vitro via second harmonic generation (SHG) experiments and analyze the observed polarization-resolved SHG signal using previously reported SHG analytical expressions obtained for anisotropic tissue. Our results indicate that the effective second-order nonlinearity measured in the grown fibers is one order of magnitude lower than that of native collagen fibers. This is attributed to the formation of loose and dispersive fibrillar networks of thinner collagen fibrils that constitute the reassembled collagen fibers. This is confirmed by scanning electronic microscopy (SEM) imaging and the polarization dependence of the SHG signal. The measured values of the anisotropy parameter ρ of the reassembled collagen fibers are found to be similar to that obtained for native fibers on the relevant sub-µm scale.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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    [Crossref]

2015 (1)

Y. Han, J. Hsu, N.-H. Ge, and E. O. Potma, “Polarization-sensitive sum-frequency generation microscopy of collagen fibers,” J. Phys. Chem. B 119(8), 3356–3365 (2015).
[Crossref]

2013 (1)

2012 (1)

2011 (3)

M. Rivard, M. Laliberté, A. Bertrand-Grenier, C. Harnagea, C. P. Pfeffer, M. Vallières, Y. St-Pierre, A. Pignolet, M. A. El Khakani, and F. Légaré, “The structural origin of second harmonic generation in fascia,” Biomed. Opt. Express 2(1), 26–36 (2011).
[Crossref]

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]

P. J. Campagnola and C.-Y. Dong, “Second harmonic generation microscopy: principles and applications to disease diagnosis,” Laser Photonics Rev. 5(1), 13–26 (2011).
[Crossref]

2010 (4)

I. Gusachenko, G. Latour, and M.-C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[Crossref]

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, and F. Leroy, “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]

A. Emoto, M. Nishi, M. Okada, S. Manabe, S. Matsui, N. Kawatsuki, and H. Ono, “Form birefringence in intrinsic birefringent media possessing a subwavelength structure,” Appl. Opt. 49(23), 4355–4361 (2010).
[Crossref]

L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
[Crossref]

2009 (4)

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. B 113(40), 13437–13445 (2009).
[Crossref]

T. Yasui, Y. Takahashi, M. Ito, S. Fukushima, and T. Arak, “Ex vivo and in vivo second-harmonic-generation imaging of dermal collagen fiber in skin: comparison of imaging characteristics between mode-locked Cr:forsterite and Ti:sapphire lasers,” Appl. Opt. 48(10), D88–D95 (2009).
[Crossref]

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

M. D. Shoulders and R. T. Raines, “Collagen Structure and Stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

2008 (1)

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[Crossref]

2007 (5)

A. Erikson, J. Örtegren, 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]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

R. J. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: Fibril polymorphism and colloidal gold labelling,” Micron 38(5), 513–521 (2007).
[Crossref]

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[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]

2006 (2)

M. J. Buehler, “Nature designs tough collagen: explaining the nanostructure of collagen fibrils,” Proc. Natl. Acad. Sci. U. S. A. 103(33), 12285–12290 (2006).
[Crossref]

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

2005 (3)

2004 (1)

F. 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]

2003 (1)

2002 (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. 99(17), 11014–11019 (2002).
[Crossref]

A. T. Yeh, N. Nassif, A. Zoumi, and B. J. Tromberg, “Selective corneal imaging using combined second-harmonic generation and two-photon excited fluorescence,” Opt. Lett. 27(23), 2082–2084 (2002).
[Crossref]

2000 (1)

D. L. Christiansen, E. K. Huang, and F. H. Silver, “Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties,” Matrix Biol. 19(5), 409–420 (2000).
[Crossref]

1996 (1)

K. E. Kadler, D. F. Holmes, J. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(1), 1–11 (1996).
[Crossref]

1986 (1)

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50(4), 693–712 (1986).
[Crossref]

Aimé, C.

Alexander, S.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

and Milner, T. E.

Arak, T.

Bancelin, S.

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. B 113(40), 13437–13445 (2009).
[Crossref]

Bertrand-Grenier, A.

Bille, J. F.

Bratton, C.

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

Bratton, C. G.

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

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. B 113(40), 13437–13445 (2009).
[Crossref]

Buehler, M. J.

M. J. Buehler, “Nature designs tough collagen: explaining the nanostructure of collagen fibrils,” Proc. Natl. Acad. Sci. U. S. A. 103(33), 12285–12290 (2006).
[Crossref]

Campagnola, P. J.

P. J. Campagnola and C.-Y. Dong, “Second harmonic generation microscopy: principles and applications to disease diagnosis,” Laser Photonics Rev. 5(1), 13–26 (2011).
[Crossref]

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[Crossref]

Celliers, P. M.

Chapman, J. A.

K. E. Kadler, D. F. Holmes, J. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(1), 1–11 (1996).
[Crossref]

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).
[Crossref]

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).
[Crossref]

Chen-Yuan, D.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Ching-Chuan, J.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Christiansen, D. L.

D. L. Christiansen, E. K. Huang, and F. H. Silver, “Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties,” Matrix Biol. 19(5), 409–420 (2000).
[Crossref]

Chu, S. W.

Coradin, T.

Coussens, L.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

de Lange Davies, C.

A. Erikson, J. Örtegren, 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]

Deng, X.

L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
[Crossref]

Deniset-Besseau, A.

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. B 113(40), 13437–13445 (2009).
[Crossref]

Deryugina, E.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

Deutsch, M.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50(4), 693–712 (1986).
[Crossref]

Dong, C.-Y.

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]

P. J. Campagnola and C.-Y. Dong, “Second harmonic generation microscopy: principles and applications to disease diagnosis,” Laser Photonics Rev. 5(1), 13–26 (2011).
[Crossref]

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. B 113(40), 13437–13445 (2009).
[Crossref]

El Khakani, M. A.

Emoto, A.

Erikson, A.

A. Erikson, J. Örtegren, 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]

Fagot, D.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, and F. Leroy, “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]

Frank, C. W.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[Crossref]

Freund, I.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50(4), 693–712 (1986).
[Crossref]

Friedl, P.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

Fukushima, S.

Galey, J.-B.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, and F. Leroy, “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]

Ge, N.-H.

Y. Han, J. Hsu, N.-H. Ge, and E. O. Potma, “Polarization-sensitive sum-frequency generation microscopy of collagen fibers,” J. Phys. Chem. B 119(8), 3356–3365 (2015).
[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]

Giese, G.

Guo, Z.

L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
[Crossref]

Gusachenko, I.

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. B 113(40), 13437–13445 (2009).
[Crossref]

Han, M.

Han, Y.

Y. Han, J. Hsu, N.-H. Ge, and E. O. Potma, “Polarization-sensitive sum-frequency generation microscopy of collagen fibers,” J. Phys. Chem. B 119(8), 3356–3365 (2015).
[Crossref]

Harnagea, C.

Harris, R. J.

R. J. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: Fibril polymorphism and colloidal gold labelling,” Micron 38(5), 513–521 (2007).
[Crossref]

Holmes, D. F.

K. E. Kadler, D. F. Holmes, J. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(1), 1–11 (1996).
[Crossref]

Hompland, T.

A. Erikson, J. Örtegren, 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]

Hörber, H.

F. 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]

Howard, J.

F. 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]

Hsiao-Ching, C.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Hsu, J.

Y. Han, J. Hsu, N.-H. Ge, and E. O. Potma, “Polarization-sensitive sum-frequency generation microscopy of collagen fibers,” J. Phys. Chem. B 119(8), 3356–3365 (2015).
[Crossref]

Hsu, K. J.

Hsuan-Shu, L.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Huang, E. K.

D. L. Christiansen, E. K. Huang, and F. H. Silver, “Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties,” Matrix Biol. 19(5), 409–420 (2000).
[Crossref]

Huttunen, M. J.

Ito, M.

Jiang, F.

F. 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]

Jin, Y.

L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
[Crossref]

Kadler, K. E.

K. E. Kadler, D. F. Holmes, J. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(1), 1–11 (1996).
[Crossref]

Kauranen, M.

Kawatsuki, N.

Kemp, N. J.

Knoesen, A.

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[Crossref]

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]

LaComb, R.

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[Crossref]

Laliberté, M.

Latour, G.

Lee, H.

Légaré, F.

Leroy, F.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, and F. Leroy, “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]

Lindgren, M.

A. Erikson, J. Örtegren, 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]

Ling-Ling, C.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Lotz, J.

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

Lotz, J. C.

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[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]

Manabe, S.

Matsui, S.

Meng, Y.

L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
[Crossref]

Michelet, J.-F.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, and F. Leroy, “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]

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]

Müller, D. J.

F. 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]

Nadiarnykh, O.

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[Crossref]

Nassif, N.

Nishi, M.

Okada, M.

Olive, C.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, and F. Leroy, “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]

Ono, H.

Örtegren, J.

A. Erikson, J. Örtegren, 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]

Park, J.

Partanen, M.

Pena, A.-M.

A.-M. Pena, D. Fagot, C. Olive, J.-F. Michelet, J.-B. Galey, and F. Leroy, “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]

Pfeffer, C. P.

Pignolet, A.

Potma, E. O.

Y. Han, J. Hsu, N.-H. Ge, and E. O. Potma, “Polarization-sensitive sum-frequency generation microscopy of collagen fibers,” J. Phys. Chem. B 119(8), 3356–3365 (2015).
[Crossref]

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]

Qu, J.

L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
[Crossref]

Raines, R. T.

M. D. Shoulders and R. T. Raines, “Collagen Structure and Stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

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]

Reiber, A.

R. J. Harris and A. Reiber, “Influence of saline and pH on collagen type I fibrillogenesis in vitro: Fibril polymorphism and colloidal gold labelling,” Micron 38(5), 513–521 (2007).
[Crossref]

Reiser, K. M.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[Crossref]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

P. Stoller, P. M. Celliers, K. M. Reiser, and A. M. Rubenchik, “Quantitative second-harmonic generation microscopy in collagen,” Appl. Opt. 42(25), 5209–5219 (2003).
[Crossref]

Rivard, M.

Rocha-Mendoza, I.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[Crossref]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

Rubenchik, A. M.

Rylander, G. H.

Schacht, V.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

Schanne-Klein, M. C.

Schanne-Klein, M.-C.

I. Gusachenko, G. Latour, and M.-C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[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. B 113(40), 13437–13445 (2009).
[Crossref]

Shoulders, M. D.

M. D. Shoulders and R. T. Raines, “Collagen Structure and Stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

Shu-Wen, T.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Silver, F. H.

D. L. Christiansen, E. K. Huang, and F. H. Silver, “Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties,” Matrix Biol. 19(5), 409–420 (2000).
[Crossref]

Sprecher, A.

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50(4), 693–712 (1986).
[Crossref]

Stoller, P.

St-Pierre, Y.

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]

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]

Takahashi, Y.

Tian, L.

L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
[Crossref]

Townsend, S. S.

R. LaComb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, “Phase matching considerations in second harmonic generation from tissues: effects on emission directionality, conversion efficiency and observed morphology,” Opt. Commun. 281(7), 1823–1832 (2008).
[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]

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. 99(17), 11014–11019 (2002).
[Crossref]

A. T. Yeh, N. Nassif, A. Zoumi, and B. J. Tromberg, “Selective corneal imaging using combined second-harmonic generation and two-photon excited fluorescence,” Opt. Lett. 27(23), 2082–2084 (2002).
[Crossref]

Trotter, J.

K. E. Kadler, D. F. Holmes, J. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(1), 1–11 (1996).
[Crossref]

Tze-Yu, L.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Vallières, M.

Van Rheenen, J.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

Von Adrian, U. H.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

Wang, M.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[Crossref]

Webb, W. W.

R. M. Williams, W. M. Zipfel, and W. W. Webb, “Interpreting Second-Harmonic Generation Images of Collagen I Fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref]

Wen, L.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Williams, R. M.

R. M. Williams, W. M. Zipfel, and W. W. Webb, “Interpreting Second-Harmonic Generation Images of Collagen I Fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref]

Wolf, K.

K. Wolf, S. Alexander, V. Schacht, L. Coussens, U. H. Von Adrian, 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]

Yankelevich, D. R.

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[Crossref]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

K. M. Reiser, C. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, J. Lotz, K. M. Reiser, C. G. Bratton, D. R. Yankelevich, A. Knoesen, I. Rocha-Mendoza, and J. C. Lotz, “Quantitative analysis of structural disorder in intervertebral disks using second harmonic generation imaging: comparison with morphometric analysis,” J. Biomed. Opt. 12(6), 064019 (2007).
[Crossref]

Yasui, T.

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. 99(17), 11014–11019 (2002).
[Crossref]

Yeh, A. T.

Yen, S.

L. Hsuan-Shu, T. Shu-Wen, C. Hsiao-Ching, L. Wen, S. Yen, L. Tze-Yu, C. Ling-Ling, J. Ching-Chuan, and D. Chen-Yuan, “Imaging Human Bone Marrow Stem Cell Morphogenesis in Polyglycolic Acid Scaffold by Multiphoton Microscopy,” Tissue Eng. 12(10), 2835–2841 (2006).
[Crossref]

Zaatari, H. N.

Zhuo, G. Y.

Zipfel, W. M.

R. M. Williams, W. M. Zipfel, and W. W. Webb, “Interpreting Second-Harmonic Generation Images of Collagen I Fibrils,” Biophys. J. 88(2), 1377–1386 (2005).
[Crossref]

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. 99(17), 11014–11019 (2002).
[Crossref]

A. T. Yeh, N. Nassif, A. Zoumi, and B. J. Tromberg, “Selective corneal imaging using combined second-harmonic generation and two-photon excited fluorescence,” Opt. Lett. 27(23), 2082–2084 (2002).
[Crossref]

Annu. Rev. Biochem. (1)

M. D. Shoulders and R. T. Raines, “Collagen Structure and Stability,” Annu. Rev. Biochem. 78(1), 929–958 (2009).
[Crossref]

Appl. Opt. (3)

Biochem. J. (1)

K. E. Kadler, D. F. Holmes, J. Trotter, and J. A. Chapman, “Collagen fibril formation,” Biochem. J. 316(1), 1–11 (1996).
[Crossref]

Biomed. Opt. Express (3)

Biophys. J. (5)

I. Freund, M. Deutsch, and A. Sprecher, “Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon,” Biophys. J. 50(4), 693–712 (1986).
[Crossref]

I. Rocha-Mendoza, D. R. Yankelevich, M. Wang, K. M. Reiser, C. W. Frank, and A. Knoesen, “Sum Frequency Vibrational Spectroscopy: The Molecular Origins of the Optical Second-Order Nonlinearity of Collagen,” Biophys. J. 93(12), 4433–4444 (2007).
[Crossref]

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]

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).
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L. Tian, J. Qu, Z. Guo, Y. Jin, Y. Meng, and X. Deng, “Microscopic second-harmonic generation emission direction in fibrillous collagen type I by quasi-phase-matching theory,” J. Appl. Phys. 108(5), 054701 (2010).
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A. Erikson, J. Örtegren, 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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J. Phys. Chem. B (2)

Y. Han, J. Hsu, N.-H. Ge, and E. O. Potma, “Polarization-sensitive sum-frequency generation microscopy of collagen fibers,” J. Phys. Chem. B 119(8), 3356–3365 (2015).
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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. B 113(40), 13437–13445 (2009).
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Proc. Natl. Acad. Sci. (1)

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[Crossref]

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Figures (7)

Fig. 1.
Fig. 1. Simulated SHG polar intensity ($I_x^{2\omega } + I_y^{2\omega }$) dependence from (a) collagen fibrils thickness (as labeled), and (b) collagen fibers and tendon thickness (as labeled). The birefringence, cross-talks and diattenuation parameters values used were $\; \Delta n = 6.6 \times {10^{ - 3}}$; ${\eta _{xy}} = 0.065;$ ${\eta _{yx}} = 0.1$; $l_a^o = 190\; \mu m$, and $l_a^e = 91\; \mu m$. (c) Influence of these physical effects on the ratio ${I_{SHG,\parallel }}/{I_{SHG, \bot }}$. A value of $\rho = $2 was used in (a-c).
Fig. 2.
Fig. 2. SHG experimental setup. In figure HWP: half-wave plate; SL: scan lens; TL: tube lens; and PMT: Photomultiplier tube.
Fig. 3.
Fig. 3. a) SHG imaging of a type I collagen tendon. The intensity profile indicated with the dashed line is shown on the bottom of this figure, the collagen fibers have a thickness of about 2-4 µm. b) polar dependence of SHG signal corresponding to two fibers labeled as F1 and F2 in Fig. 2a. These polar graphs show the typical anisotropic behavior of the SHG signal obtained from type I collagen fibers.
Fig. 4.
Fig. 4. a) Transmission bright field image (BF) of the zone where the collagen fibers were grown in vitro. b) SHG image. c) SHG polar dependence from the fibers f1, f2 and the region R1 outside of the fibrous zone indicated in Fig. 4b. The curves obtained from the fibers shown and anisotropic behavior and their shape corresponds to the obtained for thin fibers. For the region R1 the polar curve has completely an isotropic behavior indicating the absence of collagen fiber formation. d) Zoomed merged image of BF (gray color) and SHG (red-hot color). The imaged area is 40×40 µm2
Fig. 5.
Fig. 5. Fibril diameter estimation for native collagen fibrils (a) and collagen fibrils grown in vitro (b). Experimental data IF (filled squares) and If (filled triangles) are computed using Eq. 8. Solid lines are fitted curves computed with Eqs. (6) and (7) using of z = 170 nm and ${\rho _F} = 1.85$ in (a) and of z = 40 nm and ${\rho _f} = 1.87$ in (b). In both figures $\; \Delta n = 6.6 \times {10^{ - 3}}$; ${\eta _{xy}} = 0.065;$ ${\eta _{yx}} = 0.1$; $l_a^o = 190\; \mu m$, and $l_a^e = 91\; \mu m$.
Fig. 6.
Fig. 6. SEM imaging on a) native collagen fibers and collagen fibers grown in vitro at b) pH = 7.5 and c) pH = 7. d), e) and f) are zoomed images of a), b) and c), respectively, where thinner fibrils can be observed in collagen grown in vitro (see arrows). Histograms showing the distribution of the diameters measured on 50 native collagen fibrils (g) and 50 collagen fibrils grown in vitro at pH = 7.5 and pH = 7 (h,i).
Fig. 7.
Fig. 7. Comparison of the second-order nonlinearity obtained from collagen fibers grown in vitro and native collagen fibers considering as reference a lithium niobate (LiNbO3) crystal.

Equations (8)

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P I = χ I J K ( 2 ) E J E K ,
P 2 ω , x ( χ x x x ( 2 ) c o s 2 α + χ x y y ( 2 ) s i n 2 α ) E 0 2 ,
P 2 ω , y ( χ x y y ( 2 ) s i n 2 α ) E 0 2 .
I x 2 ω = K | ρ c o s 2 α + s i n 2 α | 2
I y 2 ω = K | 2 s i n α c o s α | 2 ,
I x 2 ω ( z ) = K e 2 z l a o ( | ρ e z Δ l a c o s 2 α e i Δ φ + s i n 2 α | 2 + η X Y e z Δ l a | s i n 2 α | 2 ) ,
I y 2 ω ( z ) = K e 2 z l a o ( e z Δ l a | s i n 2 α | 2 + η Y X | ρ e z Δ l a c o s 2 α e i Δ φ + s i n 2 α | 2 ) ,
I F = i N I F i / m a x ( I F i ) N and I f = i N I f i / m a x ( I f i ) N ,

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