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).
  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]
  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]
  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]
  7. S. V. Plotnikov, A. C. Millard, P. J. Campagnola andW. A.Mohler, "Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres," Biophys. J. 90,328-339 (2006).
  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).
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  10. S. Roth and I. Freund, "Second harmonic generation in collagen," J. Chem. Phys. 70,1637-1643 (1979).
    [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]
  12. P. D. Nieuwkoop and J. Faber, Table of Xenopus laevis (Daudin), (Garland Publishing Inc, New York, 1967).
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    [CrossRef]
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  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).
    [CrossRef]
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    [CrossRef]
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    [CrossRef]
  18. 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]
  19. 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).
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  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. Vi’e, D. Rou`ede, 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]
  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]
  27. J. Bella, M. Eaton, B. Brodsky and H. M. Berman, " Crystal and molecular structure of a collagen-like peptide at 1.9 °A resolution," Science 266,75-81 (1994).
    [CrossRef]

2007 (3)

2006 (1)

S. V. Plotnikov, A. C. Millard, P. J. Campagnola andW. A.Mohler, "Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres," Biophys. J. 90,328-339 (2006).

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).

2004 (4)

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vi’e, D. Rou`ede, 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]

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).

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]

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]

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]

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

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).

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]

1999 (2)

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

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]

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]

1994 (1)

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

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).

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]

Am. J. Physiol. Cell. Physiol. (1)

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]

Appl. Opt. (1)

Biophys. J. (5)

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).

S. V. Plotnikov, A. C. Millard, P. J. Campagnola andW. A.Mohler, "Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres," Biophys. J. 90,328-339 (2006).

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).

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]

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).

Dev. Biol. (1)

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

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]

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).
[CrossRef]

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).

Langmuir (1)

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vi’e, D. Rou`ede, 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]

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).
[CrossRef]

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).
[CrossRef]

Nature (1)

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

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).
[CrossRef]

Phys. Rev. Lett. (1)

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

Science (1)

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

Other (4)

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

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).

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

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