Abstract

We performed Second Harmonic Generation (SHG) imaging microscopy of endogeneous myosin-rich and collagen-rich tissues in amphibian and mammals. We determined the relative components of the macroscopic susceptibility tensor χ(2) from polarization dependence of SHG intensity. The effective orientation angle θe of the harmonophores has been determined for each protein. For myosin we found θe≈62° and this value was unchanged during myofibrillogenesis. It was also independent of the animal species (xenopus, dog and human). For collagen we found θe≈49° for both type I- and type III- rich tissues. From these results we localized the source of SHG along the single helix of both myosin and collagen.

© 2007 Optical Society of America

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  1. P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82, 493–508 (2002).
    [CrossRef]
  2. P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21, 1356–1360 (2003).
    [CrossRef] [PubMed]
  3. W. A. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods,  29, 97–109 (2003).
    [CrossRef] [PubMed]
  4. I. Freund and L. Kopf, “Long-Range Order in NH4Cl,” Phys. Rev. Lett. 24, 1017–1021 (1970).
    [CrossRef]
  5. D. A. Kleinman, “Nonlinear dielectric polarization in optical media,” Phys. Rev. 126, 1977–1979 (1962).
    [CrossRef]
  6. T. Boulesteix, E. Beaurepaire, M. P. Sauviat, and M. C. Schanne-Klein, “Second-harmonic microscopy of unstained living cardiac myocytes: measurements of sarcomere length with 20-nm accuracy,” Opt. Lett. 29, 2031–2033 (2004).
    [CrossRef] [PubMed]
  7. S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90, 328–339 (2006).
    [CrossRef]
  8. C. Greenhalgh, N. Prent, C. Green, R. Cisek, A. Major, B. Stewart, and V. Barzda, “Influence of semicrystalline order on the second-harmonic generation efficiency in the anisotropic bands of myocytes,” Appl. Opt. 46, 1852–1859 (2007).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef]
  11. K. Beck and B. Brodsky, “Supercoiled protein motifs: the collagen triple-helix and the α-helical coiled coil,” J. Struct. Biol. 122, 17–29 (1998).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  14. Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
    [CrossRef] [PubMed]
  15. C. Alexakis, T. Partridge, and G. Bou-Gharios, “Implication of the satellite cell in dystrophic muscle fibrosis: a self perpetuating mechanism of collagen over-production,” Am. J. Physiol. Cell. Physiol. (2007) (to be published).
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    [CrossRef] [PubMed]
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    [CrossRef]
  20. J. F. Nye, Physical Properties of Crystals, (Oxford University Press, Oxford, 1985).
  21. W. H. Press, B. P. Flannery, S. A. Teukolsky, and W. T. Veterlin, Numerical Recipe (Section 14.4), (Cambridge, 1986).
  22. T. F. Heinz, H. W. K. Tom, and Y. R. Shen, “Determination of molecular orientation of monolayer adsorbates by optical second-harmonic generation,” Phys. Rev. A 28, 1883–1885 (1983).
    [CrossRef]
  23. P. F. Brevet, Surface Second Harmonic Generation, (first edition, Presses Polytechniques et Universitaires Romandes, Lausanne, 1996).
  24. A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
    [CrossRef] [PubMed]
  25. G. J. Simpson and K. L. Rowlen, “An SHG magic angle: dependence of second harmonic generation orientation measurements on the width of the orientation distribution,” J. Am. Chem. Soc. 121, 2635–2636 (1999).
    [CrossRef]
  26. P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
    [CrossRef] [PubMed]
  27. J. Bella, M. Eaton, B. Brodsky, and H. M. Berman, “Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution,” Science 266, 75–81 (1994).
    [CrossRef] [PubMed]

2007 (2)

2006 (1)

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90, 328–339 (2006).
[CrossRef]

2005 (1)

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

2004 (4)

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

T. Boulesteix, E. Beaurepaire, M. P. Sauviat, and M. C. Schanne-Klein, “Second-harmonic microscopy of unstained living cardiac myocytes: measurements of sarcomere length with 20-nm accuracy,” Opt. Lett. 29, 2031–2033 (2004).
[CrossRef] [PubMed]

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[CrossRef] [PubMed]

2003 (2)

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

W. A. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods,  29, 97–109 (2003).
[CrossRef] [PubMed]

2002 (2)

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

P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
[CrossRef] [PubMed]

1999 (2)

G. J. Simpson and K. L. Rowlen, “An SHG magic angle: dependence of second harmonic generation orientation measurements on the width of the orientation distribution,” J. Am. Chem. Soc. 121, 2635–2636 (1999).
[CrossRef]

M. B. Ferrari and N. C. Spitzer, “Calcium signaling in the developing xenopus myotome,” Dev. Biol. 213, 269–289 (1999).
[CrossRef] [PubMed]

1998 (1)

K. Beck and B. Brodsky, “Supercoiled protein motifs: the collagen triple-helix and the α-helical coiled coil,” J. Struct. Biol. 122, 17–29 (1998).
[CrossRef] [PubMed]

1994 (1)

J. Bella, M. Eaton, B. Brodsky, and H. M. Berman, “Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution,” Science 266, 75–81 (1994).
[CrossRef] [PubMed]

1989 (1)

Y. R. Shen, “Surface properties probed by second-harmonic and sum-frequency generation,” Nature 337, 519–525 (1989).
[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, 693–712 (1986).
[CrossRef] [PubMed]

1983 (1)

T. F. Heinz, H. W. K. Tom, and Y. R. Shen, “Determination of molecular orientation of monolayer adsorbates by optical second-harmonic generation,” Phys. Rev. A 28, 1883–1885 (1983).
[CrossRef]

1979 (1)

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

1970 (1)

I. Freund and L. Kopf, “Long-Range Order in NH4Cl,” Phys. Rev. Lett. 24, 1017–1021 (1970).
[CrossRef]

1962 (1)

D. A. Kleinman, “Nonlinear dielectric polarization in optical media,” Phys. Rev. 126, 1977–1979 (1962).
[CrossRef]

Akagi, A.

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Alexakis, C.

C. Alexakis, T. Partridge, and G. Bou-Gharios, “Implication of the satellite cell in dystrophic muscle fibrosis: a self perpetuating mechanism of collagen over-production,” Am. J. Physiol. Cell. Physiol. (2007) (to be published).
[CrossRef] [PubMed]

Barzda, V.

Beaurepaire, E.

Beck, K.

K. Beck and B. Brodsky, “Supercoiled protein motifs: the collagen triple-helix and the α-helical coiled coil,” J. Struct. Biol. 122, 17–29 (1998).
[CrossRef] [PubMed]

Bella, J.

J. Bella, M. Eaton, B. Brodsky, and H. M. Berman, “Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution,” Science 266, 75–81 (1994).
[CrossRef] [PubMed]

Berman, H. M.

J. Bella, M. Eaton, B. Brodsky, and H. M. Berman, “Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution,” Science 266, 75–81 (1994).
[CrossRef] [PubMed]

Blanchard-Desce, M.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Bou-Gharios, G.

C. Alexakis, T. Partridge, and G. Bou-Gharios, “Implication of the satellite cell in dystrophic muscle fibrosis: a self perpetuating mechanism of collagen over-production,” Am. J. Physiol. Cell. Physiol. (2007) (to be published).
[CrossRef] [PubMed]

Boulesteix, T.

Brevet, P. F.

P. F. Brevet, Surface Second Harmonic Generation, (first edition, Presses Polytechniques et Universitaires Romandes, Lausanne, 1996).

Brodsky, B.

K. Beck and B. Brodsky, “Supercoiled protein motifs: the collagen triple-helix and the α-helical coiled coil,” J. Struct. Biol. 122, 17–29 (1998).
[CrossRef] [PubMed]

J. Bella, M. Eaton, B. Brodsky, and H. M. Berman, “Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution,” Science 266, 75–81 (1994).
[CrossRef] [PubMed]

Campagnola, P. J.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90, 328–339 (2006).
[CrossRef]

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

W. A. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods,  29, 97–109 (2003).
[CrossRef] [PubMed]

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

Chen, S. Y.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[CrossRef] [PubMed]

Chen, Y. C.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[CrossRef] [PubMed]

Chern, G. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[CrossRef] [PubMed]

Chu, S. W.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[CrossRef] [PubMed]

Cisek, R.

Da Silva, L. B.

P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
[CrossRef] [PubMed]

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, 693–712 (1986).
[CrossRef] [PubMed]

Eaton, M.

J. Bella, M. Eaton, B. Brodsky, and H. M. Berman, “Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution,” Science 266, 75–81 (1994).
[CrossRef] [PubMed]

Faber, J.

P. D. Nieuwkoop and J. Faber, Table of Xenopus laevis (Daudin), (Garland Publishing Inc, New York, 1967).

Ferrari, M. B.

M. B. Ferrari and N. C. Spitzer, “Calcium signaling in the developing xenopus myotome,” Dev. Biol. 213, 269–289 (1999).
[CrossRef] [PubMed]

Flannery, B. P.

W. H. Press, B. P. Flannery, S. A. Teukolsky, and W. T. Veterlin, Numerical Recipe (Section 14.4), (Cambridge, 1986).

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, 693–712 (1986).
[CrossRef] [PubMed]

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

I. Freund and L. Kopf, “Long-Range Order in NH4Cl,” Phys. Rev. Lett. 24, 1017–1021 (1970).
[CrossRef]

Green, C.

Greenhalgh, C.

Heinz, T. F.

T. F. Heinz, H. W. K. Tom, and Y. R. Shen, “Determination of molecular orientation of monolayer adsorbates by optical second-harmonic generation,” Phys. Rev. A 28, 1883–1885 (1983).
[CrossRef]

Hernest, M.

Hoppe, P. E.

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

Kashiyama, T.

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Kim, B. M.

P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
[CrossRef] [PubMed]

Kleinman, D. A.

D. A. Kleinman, “Nonlinear dielectric polarization in optical media,” Phys. Rev. 126, 1977–1979 (1962).
[CrossRef]

Kopf, L.

I. Freund and L. Kopf, “Long-Range Order in NH4Cl,” Phys. Rev. Lett. 24, 1017–1021 (1970).
[CrossRef]

Le Grand, Y.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Leray, A.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Leroy, L.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Lin, B. L.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[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, 1356–1360 (2003).
[CrossRef] [PubMed]

Major, A.

Mallegol, T.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Malone, C. J.

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

Matsuzaki, T.

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Millard, A. C.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90, 328–339 (2006).
[CrossRef]

W. A. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods,  29, 97–109 (2003).
[CrossRef] [PubMed]

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

Mohler, W. A.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90, 328–339 (2006).
[CrossRef]

W. A. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods,  29, 97–109 (2003).
[CrossRef] [PubMed]

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

Mongin, O.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Nakae, Y.

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Nieuwkoop, P. D.

P. D. Nieuwkoop and J. Faber, Table of Xenopus laevis (Daudin), (Garland Publishing Inc, New York, 1967).

Nonaka, I.

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Nye, J. F.

J. F. Nye, Physical Properties of Crystals, (Oxford University Press, Oxford, 1985).

Odin, C.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Partridge, T.

C. Alexakis, T. Partridge, and G. Bou-Gharios, “Implication of the satellite cell in dystrophic muscle fibrosis: a self perpetuating mechanism of collagen over-production,” Am. J. Physiol. Cell. Physiol. (2007) (to be published).
[CrossRef] [PubMed]

Pena, A. M.

Plotnikov, S. V.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90, 328–339 (2006).
[CrossRef]

Prent, N.

Press, W. H.

W. H. Press, B. P. Flannery, S. A. Teukolsky, and W. T. Veterlin, Numerical Recipe (Section 14.4), (Cambridge, 1986).

Reiser, K. M.

P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
[CrossRef] [PubMed]

Renault, A.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Roth, S.

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

Rouède, D.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Rowlen, K. L.

G. J. Simpson and K. L. Rowlen, “An SHG magic angle: dependence of second harmonic generation orientation measurements on the width of the orientation distribution,” J. Am. Chem. Soc. 121, 2635–2636 (1999).
[CrossRef]

Rubenchik, A. M.

P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
[CrossRef] [PubMed]

Sauviat, M. P.

Schanne-Klein, M. C.

Shen, Y. R.

Y. R. Shen, “Surface properties probed by second-harmonic and sum-frequency generation,” Nature 337, 519–525 (1989).
[CrossRef]

T. F. Heinz, H. W. K. Tom, and Y. R. Shen, “Determination of molecular orientation of monolayer adsorbates by optical second-harmonic generation,” Phys. Rev. A 28, 1883–1885 (1983).
[CrossRef]

Shono, M.

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Simpson, G. J.

G. J. Simpson and K. L. Rowlen, “An SHG magic angle: dependence of second harmonic generation orientation measurements on the width of the orientation distribution,” J. Am. Chem. Soc. 121, 2635–2636 (1999).
[CrossRef]

Spitzer, N. C.

M. B. Ferrari and N. C. Spitzer, “Calcium signaling in the developing xenopus myotome,” Dev. Biol. 213, 269–289 (1999).
[CrossRef] [PubMed]

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, 693–712 (1986).
[CrossRef] [PubMed]

Stewart, B.

Stoller, P.

P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
[CrossRef] [PubMed]

Stoward, P. J.

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Strupler, M.

Sun, C. K.

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[CrossRef] [PubMed]

Terasaki, M.

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

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W. H. Press, B. P. Flannery, S. A. Teukolsky, and W. T. Veterlin, Numerical Recipe (Section 14.4), (Cambridge, 1986).

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T. F. Heinz, H. W. K. Tom, and Y. R. Shen, “Determination of molecular orientation of monolayer adsorbates by optical second-harmonic generation,” Phys. Rev. A 28, 1883–1885 (1983).
[CrossRef]

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S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
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W. H. Press, B. P. Flannery, S. A. Teukolsky, and W. T. Veterlin, Numerical Recipe (Section 14.4), (Cambridge, 1986).

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A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

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, 1377–1386 (2005).
[CrossRef]

Werts, M. H. V.

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[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, 1377–1386 (2005).
[CrossRef]

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, 1377–1386 (2005).
[CrossRef]

Appl. Opt. (1)

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, 693–712 (1986).
[CrossRef] [PubMed]

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

S. W. Chu, S. Y. Chen, G. W. Chern, T. H. Tsai, Y. C. Chen, B. L. Lin, and C. K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J. 86, 3914–3922 (2004).
[CrossRef] [PubMed]

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

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90, 328–339 (2006).
[CrossRef]

Dev. Biol. (1)

M. B. Ferrari and N. C. Spitzer, “Calcium signaling in the developing xenopus myotome,” Dev. Biol. 213, 269–289 (1999).
[CrossRef] [PubMed]

J. Am. Chem. Soc. (1)

G. J. Simpson and K. L. Rowlen, “An SHG magic angle: dependence of second harmonic generation orientation measurements on the width of the orientation distribution,” J. Am. Chem. Soc. 121, 2635–2636 (1999).
[CrossRef]

J. Biomed. Opt. (1)

P. Stoller, B. M. Kim, A. M. Rubenchik, K. M. Reiser, and L. B. Da Silva, “Polarization-dependent optical second-harmonic imaging of a rat-tail tendon,” J. Biomed. Opt. 7, 205–214 (2002).
[CrossRef] [PubMed]

J. Chem. Phys. (1)

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

J. Struct. Biol. (1)

K. Beck and B. Brodsky, “Supercoiled protein motifs: the collagen triple-helix and the α-helical coiled coil,” J. Struct. Biol. 122, 17–29 (1998).
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J.Mol. Histol. (1)

Y. Nakae, P. J. Stoward, T. Kashiyama, M. Shono, A. Akagi, T. Matsuzaki, and I. Nonaka, “Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice,” J.Mol. Histol. 35, 489–499, (2004).
[CrossRef] [PubMed]

Langmuir (1)

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second-harmonic generation and atomic force microscopy,” Langmuir 20, 8165–8171 (2004), http://www.perso.univ-rennes1.fr/denis.rouede/research/la0491706.pdf.
[CrossRef] [PubMed]

Methods (1)

W. A. Mohler, A. C. Millard, and P. J. Campagnola, “Second harmonic generation imaging of endogenous structural proteins,” Methods,  29, 97–109 (2003).
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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, 1356–1360 (2003).
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Nature (1)

Y. R. Shen, “Surface properties probed by second-harmonic and sum-frequency generation,” Nature 337, 519–525 (1989).
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Opt. Express (1)

Opt. Lett. (1)

Phys. Rev. (1)

D. A. Kleinman, “Nonlinear dielectric polarization in optical media,” Phys. Rev. 126, 1977–1979 (1962).
[CrossRef]

Phys. Rev. A (1)

T. F. Heinz, H. W. K. Tom, and Y. R. Shen, “Determination of molecular orientation of monolayer adsorbates by optical second-harmonic generation,” Phys. Rev. A 28, 1883–1885 (1983).
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Phys. Rev. Lett. (1)

I. Freund and L. Kopf, “Long-Range Order in NH4Cl,” Phys. Rev. Lett. 24, 1017–1021 (1970).
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P. F. Brevet, Surface Second Harmonic Generation, (first edition, Presses Polytechniques et Universitaires Romandes, Lausanne, 1996).

P. D. Nieuwkoop and J. Faber, Table of Xenopus laevis (Daudin), (Garland Publishing Inc, New York, 1967).

C. Alexakis, T. Partridge, and G. Bou-Gharios, “Implication of the satellite cell in dystrophic muscle fibrosis: a self perpetuating mechanism of collagen over-production,” Am. J. Physiol. Cell. Physiol. (2007) (to be published).
[CrossRef] [PubMed]

J. F. Nye, Physical Properties of Crystals, (Oxford University Press, Oxford, 1985).

W. H. Press, B. P. Flannery, S. A. Teukolsky, and W. T. Veterlin, Numerical Recipe (Section 14.4), (Cambridge, 1986).

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Figures (4)

Fig. 1.
Fig. 1.

Optical sections illustrating SHG images from different muscles and collagen-rich tissues. (a–c): swimming body muscles of developing xenopus tadpoles of respectively 1 day (stage 32), 2 days (stage 37) and 4 days (stage 46) post fertilization. (d): gastrocnemius muscle of adult xenopus. (e): gastrocnemius muscle of a 71 years old human female. (f,g): gastrocnemius muscle and collagen of 4 months old Golden retriever dog with DMD. (h–j): collagen from respectively adult xenopus tendon and aorta and adult healthy Beagle dog muscle. Images (a–e, g) are optical section images of 50×50mm2 while image (f) is a 90×90µm2 XY crossed-section. Note the presence of ectopic collagen in the endomysium (star). Arrowhead indicated a transsected muscle fiber. (g): Arrowhead and star indicated respectively muscle and ectopic collagen fibers. (h): Projection of 100mm thick stack of a 500×500µm2 image. (i,j): Projection of 17mm thick stack of a 500×500µm2 image. Note that image (c) was obtained from in vivo 46 stage xenopus larva and image (j) was obtained from fresh slice of Beagle dog muscle whereas all other images were from PFA-fixed tissues.

Fig. 2.
Fig. 2.

Polarization dependence of the SHG signal of different muscles. (a): SHG optical sections of adult xenopus gastrocnemius muscle illustrating the effect of four different incident polarization angles α(0°, 45°, 90°, 135°) on the emitted signal from the same field of view. Scale bar: 20 µm. Arrows represent the polarization of the incident electric field (0 degree is vertical). (b): normalized SHG signal as a function of the incident polarization angle α for different muscles of different species. Experimental data are represented with different symbols. ♦, ◦ and ▾ from xenopus tadpole body wall muscles of respectively 1 day (stage 32), 2 days (stage 37) and 4 days (stage 46). ▪, ▴ and ● from adult gastrocnemius muscles of respectively xenopus, 71 years old human female and DMD Golden retriever dog. The full lines are drawn using the best fit obtained from Eq. 2. On the inset, a schematic top view is shown. The long axis of myosin filaments for each specimen was oriented along the Z axis of the laboratory coordinates (X, Y, Z).

Fig. 3.
Fig. 3.

Polarization dependence of the SHG signal of different collagen-rich tissues. (a): SHG optical sections of adult xenopus tendon illustrating the effect of four different incident polarization angles α(0°, 45°, 90°, 135°) on the emitted signal from the same field of view. Scale bar: 10 µm. Arrows represent the incident polarization angles α. (b): normalized SHG signal as a function of the incident polarization anglea for different collagen-rich tissues of xenopus and dog. Experimental data are represented with different symbols. ●, ◦ respectively for xenopus tendon and aorta. ▾ and ▪ respectively for epimysium of healthy dog and muscles of DMD dog. Note that data from healthy dog muscle epimysium was from fresh slice whereas all other data were from PFA-fixed tissues. The lines are drawn from the best fit obtained from Eq. 2. On the inset, a schematic top view is shown. The long axis of collagen filaments for each specimen was oriented along the Z axis of the laboratory coordinates (X, Y, Z).

Fig. 4.
Fig. 4.

Schematic view of single helix of myosin (left) and collagen (right). Mean harmonophore orientation angle θo and disorder width δ are shown. According to the model, θo is ranging from 62° to 69° for myosin and 49° to 57° for collagen with maximum disorder width δ=41° (D=0.22, θo =69°) for myosin and δ=67° (D=0.42, θo =57°) for collagen. P and R are helix pitch and radius. For myosin P=5.5 Å, R=2.2 Å and for collagen P=9.5 Å, R=1.5 Å [11, 27].

Tables (1)

Tables Icon

Table 1. Ratio of coefficients χ31/χ15 and χ33/χ15 for myosin-rich and collagen-rich tissues obtained from fit of Eq. 2 with the experimental data of Fig. 2(b) and Fig. 3(b). The orientation parameter D and the effective orientation angle θe are defined by Eq. 4.

Equations (8)

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P X 2 ω = 0
P Y 2 ω = 2 χ 15 E Y ω E Z ω
P Z 2 ω = χ 31 ( E Y ω ) 2 + χ 33 ( E Z ω ) 2 .
I 2 ω [ sin 2 2 α + ( χ 31 χ 15 sin 2 α + χ 33 χ 15 cos 2 α ) 2 ] .
χ 33 = N s β < cos 3 θ >
χ 15 = χ 31 = 1 2 N s β < cos θ sin 2 θ > .
D = < cos 3 θ > < cos θ > = χ 33 χ 15 2 + χ 33 χ 15 = cos 2 θ e .
D ( δ , θ o ) = 1 2 ( 1 + cos δ cos 2 θ o ) .

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