Abstract

We have extensively characterized the sarcomeric SHG signal as a function of animal species (rat versus xenopus), age (adult versus larval) and tissue preparation (fixed or fresh) and we found that the main feature of this signal is a single peak per mature sarcomere (about 85% of all sarcomeres). The remaining (15%) was found to be either double peak per mature sarcomere or mini sarcomeres (half of a sarcomere) using α-actinin immuno detection of the Z-band. The mini sarcomeres are often found in region of pitchfork-like SHG pattern. We suggest that double peak SHG pattern could indicate regions of sarcomeric proteolysis whereas pitchfork-like SHG pattern could reveal sarcomeric assembly.

© 2009 Optical Society of America

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2009

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

J. C. Sparrow, and F. Schock, "The initial steps of myofibril assembly: integrins pave the way," Nat. Rev. Mol. Cell Biol. 10, 293-298 (2009).
[CrossRef] [PubMed]

2008

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, "Collagen and myosin characterization by orientation field second harmonic microscopy," Opt. Express 16, 16151-16165 (2008), http://www.opticsinfobase.org/oe/abstract.cfm?URI=oe-16-20-16151.
[CrossRef] [PubMed]

2007

2006

R. Craig and J. L. Woodhead, "Structure and function of myosin filaments," Curr. Opin. Struct. Biol. 16, 204-212 (2006).
[CrossRef] [PubMed]

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

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

A. M. Solomon and P. M. G. Bouloux, "Modifying muscle mass - the endocrine perspective," J. Endocrinol. 191, 349-360 (2006).
[CrossRef] [PubMed]

2005

S. K. Powers, A. N. Kavazis, and K. C. DeRuisseau, "Mechanisms of disuse muscle atrophy: role of oxidative stress," Am J Physiol Regul Integr Comp Physiol 228, R337-R344 (2005).

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

G. Cox, N. Moreno, J. Feijó, "Second-harmonic imaging of plant polysaccharides," J. Biomed. Opt. 10, 024013 (2005).
[CrossRef] [PubMed]

2004

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

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (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]

2003

I. Agarkova, E. Ehler, S. Lange, R. Schoenauer, and J. C. Perriard, "M-band: a safeguard for sarcomere stability?," J. Muscle Res. Cell Motil. 24, 191-203 (2003).
[CrossRef] [PubMed]

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

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

2002

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]

2001

D. E. Rudy, T. A. Yatskievych, P. B. Antin and C. C. Gregorio, "Assembly of thick, thin, and titin filaments in chick precardiac explants," Dev. Dyn. 221, 61-71 (2001).
[CrossRef] [PubMed]

1999

J. L. Thompson, E. M. Balog, R. H. Fitts, and D. A. Riley, "Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle - A test model," Anat. Record 254, 39-52 (1999).
[CrossRef]

1994

D. Rhee, J. M. Sanger, and J. W. Sanger, "The premyofibril: evidence for its role in myofibrillogenesis," Cell Motil. Cytoskeleton 28, 1-24 (1994).
[CrossRef] [PubMed]

1989

L. D. Taylor and E. Bandman, "Distribution of fast myosin heavy chain isoforms in thick filaments of developing chicken pectoral muscle," J. Cell Biol. 108, 533 - 542 (1989).
[CrossRef] [PubMed]

1988

R. W. Ogilvie, R. B. Armstrong, K. E. Baird, and C. L. Bottoms, "Lesions in the rat soleus muscle following eccentrically biased exercise," Am. J. Anat. 182, 335-346 (1988).
[CrossRef] [PubMed]

1986

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]

1985

T. Shimizu, J. E. Dennis, T. Masaki, and D. A. Fischman, "Axial Arrangement of the Myosin Rod in Vertebrate Thick Filaments: Immunoelectron Microscopy with a Monoclonal Antibody to Light Meromyosin," J. Cell Biol. 101, 1115-1123 (1985).
[CrossRef] [PubMed]

1963

S. G. Page, and H. E. Huxley, "Filament Lengths in Striated Muscle," J. Cell Biol. 19, 369-390 (1963).
[CrossRef] [PubMed]

Adams, D. J.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Agarkova, I.

I. Agarkova, E. Ehler, S. Lange, R. Schoenauer, and J. C. Perriard, "M-band: a safeguard for sarcomere stability?," J. Muscle Res. Cell Motil. 24, 191-203 (2003).
[CrossRef] [PubMed]

Alkilani, A.

Amat-Roldan, I.

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

Antin, P. B.

D. E. Rudy, T. A. Yatskievych, P. B. Antin and C. C. Gregorio, "Assembly of thick, thin, and titin filaments in chick precardiac explants," Dev. Dyn. 221, 61-71 (2001).
[CrossRef] [PubMed]

Antolini, R.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Armstrong, R. B.

R. W. Ogilvie, R. B. Armstrong, K. E. Baird, and C. L. Bottoms, "Lesions in the rat soleus muscle following eccentrically biased exercise," Am. J. Anat. 182, 335-346 (1988).
[CrossRef] [PubMed]

Artigas, D.

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

Baird, K. E.

R. W. Ogilvie, R. B. Armstrong, K. E. Baird, and C. L. Bottoms, "Lesions in the rat soleus muscle following eccentrically biased exercise," Am. J. Anat. 182, 335-346 (1988).
[CrossRef] [PubMed]

Balog, E. M.

J. L. Thompson, E. M. Balog, R. H. Fitts, and D. A. Riley, "Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle - A test model," Anat. Record 254, 39-52 (1999).
[CrossRef]

Bandman, E.

L. D. Taylor and E. Bandman, "Distribution of fast myosin heavy chain isoforms in thick filaments of developing chicken pectoral muscle," J. Cell Biol. 108, 533 - 542 (1989).
[CrossRef] [PubMed]

Barzda, V.

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

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]

Beaurepaire, E.

Bembi, B.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Boryskina, O. P.

Both, M.

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

Bottinelli, R.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Bottoms, C. L.

R. W. Ogilvie, R. B. Armstrong, K. E. Baird, and C. L. Bottoms, "Lesions in the rat soleus muscle following eccentrically biased exercise," Am. J. Anat. 182, 335-346 (1988).
[CrossRef] [PubMed]

Boulesteix, T.

Bouloux, P. M. G.

A. M. Solomon and P. M. G. Bouloux, "Modifying muscle mass - the endocrine perspective," J. Endocrinol. 191, 349-360 (2006).
[CrossRef] [PubMed]

Campagnola, P. J.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

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

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

W. 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]

Canepari, M.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Capitanio, M.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

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 x(2)/x(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 x(2)/x(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86, 3914- 3922 (2004).
[CrossRef] [PubMed]

Cheng, J. X.

Y. Fu, H. Wang, R. Shi, and J. X. Cheng, "Second harmonic and sum frequency generation imaging of fibrous astroglial filaments in ex vivo spinal tissues," Biophys J. 92, 3251-3259 (2007).
[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 x(2)/x(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86, 3914- 3922 (2004).
[CrossRef] [PubMed]

Chien, Y. H.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[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 x(2)/x(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86, 3914- 3922 (2004).
[CrossRef] [PubMed]

Cicchi, R.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Cisek, R.

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

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]

Cox, G.

G. Cox, N. Moreno, J. Feijó, "Second-harmonic imaging of plant polysaccharides," J. Biomed. Opt. 10, 024013 (2005).
[CrossRef] [PubMed]

Craig, R.

R. Craig and J. L. Woodhead, "Structure and function of myosin filaments," Curr. Opin. Struct. Biol. 16, 204-212 (2006).
[CrossRef] [PubMed]

Czapiga, M.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Dauser, D.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Dennis, J. E.

T. Shimizu, J. E. Dennis, T. Masaki, and D. A. Fischman, "Axial Arrangement of the Myosin Rod in Vertebrate Thick Filaments: Immunoelectron Microscopy with a Monoclonal Antibody to Light Meromyosin," J. Cell Biol. 101, 1115-1123 (1985).
[CrossRef] [PubMed]

DeRuisseau, K. C.

S. K. Powers, A. N. Kavazis, and K. C. DeRuisseau, "Mechanisms of disuse muscle atrophy: role of oxidative stress," Am J Physiol Regul Integr Comp Physiol 228, R337-R344 (2005).

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]

Dougherty, R. P.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Du, A. P.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

Ehler, E.

I. Agarkova, E. Ehler, S. Lange, R. Schoenauer, and J. C. Perriard, "M-band: a safeguard for sarcomere stability?," J. Muscle Res. Cell Motil. 24, 191-203 (2003).
[CrossRef] [PubMed]

Fink, R. H.

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

Fischman, D. A.

T. Shimizu, J. E. Dennis, T. Masaki, and D. A. Fischman, "Axial Arrangement of the Myosin Rod in Vertebrate Thick Filaments: Immunoelectron Microscopy with a Monoclonal Antibody to Light Meromyosin," J. Cell Biol. 101, 1115-1123 (1985).
[CrossRef] [PubMed]

Fitts, R. H.

J. L. Thompson, E. M. Balog, R. H. Fitts, and D. A. Riley, "Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle - A test model," Anat. Record 254, 39-52 (1999).
[CrossRef]

Fleury, V.

Freeman, N.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[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, 693-712 (1986).
[CrossRef] [PubMed]

Friedrich, O.

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

Fu, Y.

Y. Fu, H. Wang, R. Shi, and J. X. Cheng, "Second harmonic and sum frequency generation imaging of fibrous astroglial filaments in ex vivo spinal tissues," Biophys J. 92, 3251-3259 (2007).
[CrossRef] [PubMed]

Green, C.

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

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]

Greenhalgh, C.

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

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]

Gregorio, C. C.

D. E. Rudy, T. A. Yatskievych, P. B. Antin and C. C. Gregorio, "Assembly of thick, thin, and titin filaments in chick precardiac explants," Dev. Dyn. 221, 61-71 (2001).
[CrossRef] [PubMed]

Guilbert, T.

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]

Huxley, H. E.

S. G. Page, and H. E. Huxley, "Filament Lengths in Striated Muscle," J. Cell Biol. 19, 369-390 (1963).
[CrossRef] [PubMed]

Hwu, W. L.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Joseph, C.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Kang, S. M.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

Kavazis, A. N.

S. K. Powers, A. N. Kavazis, and K. C. DeRuisseau, "Mechanisms of disuse muscle atrophy: role of oxidative stress," Am J Physiol Regul Integr Comp Physiol 228, R337-R344 (2005).

Kenny, A. M.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Kuchel, G. A.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Kunsting, T.

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

Lange, S.

I. Agarkova, E. Ehler, S. Lange, R. Schoenauer, and J. C. Perriard, "M-band: a safeguard for sarcomere stability?," J. Muscle Res. Cell Motil. 24, 191-203 (2003).
[CrossRef] [PubMed]

Le Grand, Y.

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 x(2)/x(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86, 3914- 3922 (2004).
[CrossRef] [PubMed]

Linari, M.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[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," Nature Biotechnology 21, 1356-1360 (2003).
[CrossRef] [PubMed]

Lombardi, V.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Loza-Alvarez, P.

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

Maffei, M.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Major, A.

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

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]

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]

Masaki, T.

T. Shimizu, J. E. Dennis, T. Masaki, and D. A. Fischman, "Axial Arrangement of the Myosin Rod in Vertebrate Thick Filaments: Immunoelectron Microscopy with a Monoclonal Antibody to Light Meromyosin," J. Cell Biol. 101, 1115-1123 (1985).
[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, 693-703 (2006).
[CrossRef]

W. 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.

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

Mohler, W. A.

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]

Moreno, N.

G. Cox, N. Moreno, J. Feijó, "Second-harmonic imaging of plant polysaccharides," J. Biomed. Opt. 10, 024013 (2005).
[CrossRef] [PubMed]

Nucciotti, V.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Odin, C.

Ogilvie, R. W.

R. W. Ogilvie, R. B. Armstrong, K. E. Baird, and C. L. Bottoms, "Lesions in the rat soleus muscle following eccentrically biased exercise," Am. J. Anat. 182, 335-346 (1988).
[CrossRef] [PubMed]

Page, S. G.

S. G. Page, and H. E. Huxley, "Filament Lengths in Striated Muscle," J. Cell Biol. 19, 369-390 (1963).
[CrossRef] [PubMed]

Pavone, F. S.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Perriard, J. C.

I. Agarkova, E. Ehler, S. Lange, R. Schoenauer, and J. C. Perriard, "M-band: a safeguard for sarcomere stability?," J. Muscle Res. Cell Motil. 24, 191-203 (2003).
[CrossRef] [PubMed]

Piazzesi, G.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Pilbeam, C. C.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Piroddi, N.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Pittis, M. G.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Plotnikov, S. V.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

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

Plotz, P.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Poggesi, C.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Powers, S. K.

S. K. Powers, A. N. Kavazis, and K. C. DeRuisseau, "Mechanisms of disuse muscle atrophy: role of oxidative stress," Am J Physiol Regul Integr Comp Physiol 228, R337-R344 (2005).

Prent, N.

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

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]

Psilodimitrakopoulos, S.

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

Raben, N.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Ralston, E.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Recher, G.

Rhee, D.

D. Rhee, J. M. Sanger, and J. W. Sanger, "The premyofibril: evidence for its role in myofibrillogenesis," Cell Motil. Cytoskeleton 28, 1-24 (1994).
[CrossRef] [PubMed]

Riley, D. A.

J. L. Thompson, E. M. Balog, R. H. Fitts, and D. A. Riley, "Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle - A test model," Anat. Record 254, 39-52 (1999).
[CrossRef]

Rouède, D.

Rudy, D. E.

D. E. Rudy, T. A. Yatskievych, P. B. Antin and C. C. Gregorio, "Assembly of thick, thin, and titin filaments in chick precardiac explants," Dev. Dyn. 221, 61-71 (2001).
[CrossRef] [PubMed]

Sacconi, L.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Sanger, J. M.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

D. Rhee, J. M. Sanger, and J. W. Sanger, "The premyofibril: evidence for its role in myofibrillogenesis," Cell Motil. Cytoskeleton 28, 1-24 (1994).
[CrossRef] [PubMed]

Sanger, J. W.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

D. Rhee, J. M. Sanger, and J. W. Sanger, "The premyofibril: evidence for its role in myofibrillogenesis," Cell Motil. Cytoskeleton 28, 1-24 (1994).
[CrossRef] [PubMed]

Santos, S.

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

Sauviat, M. P.

Schanne-Klein, M. C.

Schock, F.

J. C. Sparrow, and F. Schock, "The initial steps of myofibril assembly: integrins pave the way," Nat. Rev. Mol. Cell Biol. 10, 293-298 (2009).
[CrossRef] [PubMed]

Schoenauer, R.

I. Agarkova, E. Ehler, S. Lange, R. Schoenauer, and J. C. Perriard, "M-band: a safeguard for sarcomere stability?," J. Muscle Res. Cell Motil. 24, 191-203 (2003).
[CrossRef] [PubMed]

Schwartz, O.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Scranton, V. L.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Shi, R.

Y. Fu, H. Wang, R. Shi, and J. X. Cheng, "Second harmonic and sum frequency generation imaging of fibrous astroglial filaments in ex vivo spinal tissues," Biophys J. 92, 3251-3259 (2007).
[CrossRef] [PubMed]

Shimizu, T.

T. Shimizu, J. E. Dennis, T. Masaki, and D. A. Fischman, "Axial Arrangement of the Myosin Rod in Vertebrate Thick Filaments: Immunoelectron Microscopy with a Monoclonal Antibody to Light Meromyosin," J. Cell Biol. 101, 1115-1123 (1985).
[CrossRef] [PubMed]

Siebrands, C. C.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

Solomon, A. M.

A. M. Solomon and P. M. G. Bouloux, "Modifying muscle mass - the endocrine perspective," J. Endocrinol. 191, 349-360 (2006).
[CrossRef] [PubMed]

Sparrow, J. C.

J. C. Sparrow, and F. Schock, "The initial steps of myofibril assembly: integrins pave the way," Nat. Rev. Mol. Cell Biol. 10, 293-298 (2009).
[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.

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

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]

Stout, A. L.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

Stringari, C.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

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 x(2)/x(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy," Biophys. J. 86, 3914- 3922 (2004).
[CrossRef] [PubMed]

Swaim, B.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Taylor, L. D.

L. D. Taylor and E. Bandman, "Distribution of fast myosin heavy chain isoforms in thick filaments of developing chicken pectoral muscle," J. Cell Biol. 108, 533 - 542 (1989).
[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]

Tesi, C.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Thayil, A. K. N.

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

Thompson, J. L.

J. L. Thompson, E. M. Balog, R. H. Fitts, and D. A. Riley, "Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle - A test model," Anat. Record 254, 39-52 (1999).
[CrossRef]

Tiaho, F.

Tsai, T. H.

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

Uttenweiler, D.

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

Vanzi, F.

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

Vogel, M.

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

vonWegner, F.

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

Walsh, S. J.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Wang, H.

Y. Fu, H. Wang, R. Shi, and J. X. Cheng, "Second harmonic and sum frequency generation imaging of fibrous astroglial filaments in ex vivo spinal tissues," Biophys J. 92, 3251-3259 (2007).
[CrossRef] [PubMed]

Wang, J. S.

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

Woodhead, J. L.

R. Craig and J. L. Woodhead, "Structure and function of myosin filaments," Curr. Opin. Struct. Biol. 16, 204-212 (2006).
[CrossRef] [PubMed]

Xu, M.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Yatskievych, T. A.

D. E. Rudy, T. A. Yatskievych, P. B. Antin and C. C. Gregorio, "Assembly of thick, thin, and titin filaments in chick precardiac explants," Dev. Dyn. 221, 61-71 (2001).
[CrossRef] [PubMed]

Zubrowski, B.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

Am J Physiol Regul Integr Comp Physiol

S. K. Powers, A. N. Kavazis, and K. C. DeRuisseau, "Mechanisms of disuse muscle atrophy: role of oxidative stress," Am J Physiol Regul Integr Comp Physiol 228, R337-R344 (2005).

Am. J. Anat.

R. W. Ogilvie, R. B. Armstrong, K. E. Baird, and C. L. Bottoms, "Lesions in the rat soleus muscle following eccentrically biased exercise," Am. J. Anat. 182, 335-346 (1988).
[CrossRef] [PubMed]

Anat. Record

J. L. Thompson, E. M. Balog, R. H. Fitts, and D. A. Riley, "Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle - A test model," Anat. Record 254, 39-52 (1999).
[CrossRef]

Appl. Opt.

Biophys J.

Y. Fu, H. Wang, R. Shi, and J. X. Cheng, "Second harmonic and sum frequency generation imaging of fibrous astroglial filaments in ex vivo spinal tissues," Biophys J. 92, 3251-3259 (2007).
[CrossRef] [PubMed]

Biophys. 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]

Biophys. J.

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

F. Légaré, C. Pfeffer, and B. R. Olsen, "The role of backscattering in SHG tissue imaging," Biophys. J. 93, 1312-1320 (2007).
[CrossRef] [PubMed]

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. 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, 693-703 (2006).
[CrossRef]

Cell Motil. Cytoskeleton

D. Rhee, J. M. Sanger, and J. W. Sanger, "The premyofibril: evidence for its role in myofibrillogenesis," Cell Motil. Cytoskeleton 28, 1-24 (1994).
[CrossRef] [PubMed]

Curr. Opin. Struct. Biol.

R. Craig and J. L. Woodhead, "Structure and function of myosin filaments," Curr. Opin. Struct. Biol. 16, 204-212 (2006).
[CrossRef] [PubMed]

Dev. Dyn.

D. E. Rudy, T. A. Yatskievych, P. B. Antin and C. C. Gregorio, "Assembly of thick, thin, and titin filaments in chick precardiac explants," Dev. Dyn. 221, 61-71 (2001).
[CrossRef] [PubMed]

J Biomed. Opt.

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, andW. A. Mohler, "Measurement of muscle disease by quantitative second-harmonic generation imaging," J Biomed. Opt. 13, 044018 (2008).
[CrossRef] [PubMed]

J. Biomed. Opt.

S. Psilodimitrakopoulos, S. Santos, I. Amat-Roldan, A. K. N. Thayil, D. Artigas, and P. Loza-Alvarez, "In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy," J. Biomed. Opt. 14, 014001 (2009).
[CrossRef] [PubMed]

G. Cox, N. Moreno, J. Feijó, "Second-harmonic imaging of plant polysaccharides," J. Biomed. Opt. 10, 024013 (2005).
[CrossRef] [PubMed]

M. Both, M. Vogel, O. Friedrich, F. vonWegner, T. Kunsting, R. H. Fink, and D. Uttenweiler, "Second harmonic imaging of intrinsic signals in muscle fibers in situ," J. Biomed. Opt. 9, 882-892 (2004).
[CrossRef] [PubMed]

N. Prent, C. Green, C. Greenhalgh, R. Cisek, A. Major, B. Stewart, and V. Barzda, "Intermyofilament dynamics of myocytes revealed by second harmonic generation microscopy," J. Biomed. Opt. 13, 041318 (2008).
[CrossRef] [PubMed]

J. Cell Biol.

T. Shimizu, J. E. Dennis, T. Masaki, and D. A. Fischman, "Axial Arrangement of the Myosin Rod in Vertebrate Thick Filaments: Immunoelectron Microscopy with a Monoclonal Antibody to Light Meromyosin," J. Cell Biol. 101, 1115-1123 (1985).
[CrossRef] [PubMed]

L. D. Taylor and E. Bandman, "Distribution of fast myosin heavy chain isoforms in thick filaments of developing chicken pectoral muscle," J. Cell Biol. 108, 533 - 542 (1989).
[CrossRef] [PubMed]

S. G. Page, and H. E. Huxley, "Filament Lengths in Striated Muscle," J. Cell Biol. 19, 369-390 (1963).
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J. Endocrinol.

A. M. Solomon and P. M. G. Bouloux, "Modifying muscle mass - the endocrine perspective," J. Endocrinol. 191, 349-360 (2006).
[CrossRef] [PubMed]

J. Muscle Res. Cell Motil.

I. Agarkova, E. Ehler, S. Lange, R. Schoenauer, and J. C. Perriard, "M-band: a safeguard for sarcomere stability?," J. Muscle Res. Cell Motil. 24, 191-203 (2003).
[CrossRef] [PubMed]

J. W. Sanger, S. M. Kang, C. C. Siebrands, N. Freeman, A. P. Du, J. S. Wang, A. L. Stout, and J. M. Sanger, "How to build a myofibril," J. Muscle Res. Cell Motil. 26, 343-354 (2005).
[CrossRef]

F. Vanzi, M. Capitanio, L. Sacconi, C. Stringari, R. Cicchi, M. Canepari, M. Maffei, N. Piroddi, C. Poggesi, V. Nucciotti, M. Linari, G. Piazzesi, C. Tesi, R. Antolini, V. Lombardi, R. Bottinelli, and F. S. Pavone, "New techniques in linear and non-linear laser optics in muscle research," J. Muscle Res. Cell Motil. 27, 469-479 (2006).
[CrossRef] [PubMed]

J. Struct. Biol.

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, "Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence," J. Struct. Biol. 162, 500-508 (2008).
[CrossRef] [PubMed]

Methods

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

Nat. Rev. Mol. Cell Biol.

J. C. Sparrow, and F. Schock, "The initial steps of myofibril assembly: integrins pave the way," Nat. Rev. Mol. Cell Biol. 10, 293-298 (2009).
[CrossRef] [PubMed]

Nature Biotechnology

P. J. Campagnola and L. M. Loew, "Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms," Nature Biotechnology 21, 1356-1360 (2003).
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Opt. Express

Opt. Lett.

Other

J. W. Sanger, J. Wang, B. Holloway, A. Du, and J. M. Sanger, "Myofibrillogenesis in skeletal muscle cells in zebrafish," Cell Motil Cytoskeleton, Epub ahead of print (2009).
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Figures (9)

Fig. 1
Fig. 1

Schematic diagram illustrating the major sarcomeric components of striated muscles. (a) Global view of two myofibrils (thickness ≈ 1 μm) formed by contractile sarcomeres (width ≈ 2.2 μm) which assemble laterally and display a pattern of alternating light (I) and dark (A) bands. (b) View of the sarcomere showing overlapping arrays of bipolar myosin thick filaments and actin thin filaments. Thick and thin filaments are transversally interconnected at the M- and Z- band respectively. Myomesin or M-protein (M-band) involved in these connections are not represented. Thick filaments are longitudinally connected at the Z- and M- band by titin and for simplicity only the connection at the Z-band is represented. (c) The myosin molecule is an hexamere of two heavy chains and two pairs of light chains (not presented) and has a length of about 160 nm. The heavy chain α-helix tails of each myosin molecule form a coiled-coil super helix dimer. (d) Schematic representation of the antiparallel assembly of myosin molecules at the M-band free of heads (width ≈ 120–200 nm). Myosin heads point away from the filament center and myosin tails have antiparallel overlapping (width 85 –130 nm).

Fig. 2
Fig. 2

Typical SHG images and intensity profiles from adult gastrocnemius muscles. (a) Optical sections illustrating SHG images from xenopus (a) and rat (b) muscles. The scale bar is 2 μm and the full image is 40×40 μm. A Gaussian Blur filter (radius=2) was applied for each image. Arrowheads and arrows indicate respectively bright double-band sarcomeric SHG signal and bright pitchfork SHG pattern. (c, d) SHG intensity profiles along the indicated segments in respectively (a) and (b). The left and right profiles of images (c) and (d) correspond respectively to the horizontal black and white lines drawn in (a) and (b). Note that the optical resolution was not sufficient to discriminate indiviual myofibrils that are horizontally aligned.

Fig. 3
Fig. 3

Typical sarcomeric TPEF and SHG signal of gastrocnemius muscles. Single-band (a,b) and double-band (c,d) sarcomeres from xenopus (a,c) and rat (b,d). The upper and lower panels of (a–d) correspond respectively to α-actinin TPEF and myosin SHG signals. Scale bar (2 μm).

Fig. 4
Fig. 4

SHG images illustrating the effect of 1 day proteolysis on sarcomeric SHG patterns of xenopus tail muscles. (a) Control without proteolysis (J0). (b) After 24H proteolysis (J1). Each image is 13×13 μm.

Fig. 5
Fig. 5

TPEF α-actinin analysis of regions with pitchfork-like SHG pattern of gastrocnemius muscles and diagram of myofibrils with mature and mini sarcomeres. Upper (TPEF) and lower (SHG) panels are respectively from xenopus (a) and rat (b). Note the progressive alignment of the Z-band from left to right in (a) suggesting maturation of the myofibril. Scale bar (2μm).

Fig. 6
Fig. 6

Polarization dependence study of the SHG signal in regions with pitchfork-like structures. (a) Typical SHG pitchfork-like pattern. (b) SHG optical sections illustrating the effect of five different incident polarization angles α (0°, 50°, 90°, 130°, 180°) on the emitted signal from the same field of view. The arrows indicate the polarization of the incident electric field for each panel (the upperward vertical arrow represents 0°). (c) Normalized SHG signal as a function of the incident polarization angle α for ROIs ▪, ▴ and • indicated in (a). Note the correspondance between the ROIs in (a) and legend symbols in (c). The long axis of myosin filaments was oriented along the X axis of the laboratory coordinates (X, Y, Z) as shown in the inset.

Fig. 7
Fig. 7

Single-band and double-band frequency estimation by FFT analysis. (a) Before processing FFT’s the SHG image (512×512), corresponding to that of Fig. 2(a) after a Gaussian Blur filter (radius=1), is manually rotated in order to orientate horizontally the main direction of myofibrils. The full image is 40×40 μm. (b) SHG intensity profile Ii(x) for lines i=208 and i=248. (c) The modulus of the FFT, |Ii(x)^| is given for lines i=208 and i=248. Line i = 208 contains single- and double- band sarcomeres while line i = 448 contains only single-band sarcomeres. (d) In order to highlight main frequencies components, |Ii(x)^| are then averaged on all lines i providing |I(x)^|¯. Estimation of the single band frequency f1 is done by the selection on |I(x)^|¯ of the peak corresponding to the fundamental frequency (bold circle on (d)).

Fig. 8
Fig. 8

Gabor filter analysis. Impulse responses of Gabor filters associated to (a) single band frequency gf1 (x) = gr(x, f1) + igi(x, f1) and (b) double band frequency gf2 (x) = gr(x, f2) + igi(x, f2). A high value of σ provides a precise spectral analysis but a poor spatial resolution. A good compromise is a value of σ of 1f124pixels. Response of the two Gabor filters gf1 (x) and gf2 (x) for intensity profiles Ii(x) of lines i=208 (c) and i=448 (d) of Fig. 7(b). Operator * represents the convolution of the intensity profile with the impulse response of the Gabor filter. Single- and double- band frequency filtering f1 and f2 are respectively in full and dash line. Line i=208 contains single- and double- band sarcomeres while line i = 448 contains only single band sarcomeres. (e) and (f) represent the result of the smoothing after Gabor filtering at frequencies f1 and f2 applied to the SHG image of Fig. 7(a). (g) and (h) represent the result of the decision step for respectively single-band and double-band sarcomeres. Lines i=208 and i=448 considered in (c,d) are drawn in white in (g,h). In order to limit side effects caused by Gabor filtering, two vertical bands of width 24 pixels ( 1f124pixels) are not considered for decision in (g) and (h).

Fig. 9
Fig. 9

Description of the method of intensity profile analysis. 3D schematic view of an entire stack where the first image of the stack corresponds to that of Fig. 2(a). Each image is oriented wih the myofibril main axis oriented along the X axis of the laboratory. The number of peaks Ni,k of the pixel intensity profile is determined for line i of slice k. The minimum value mink Ni,k is determined for line i from all slices k and the average minkNi,k¯ is deduced from all lines i.

Tables (2)

Tables Icon

Table 1 Quantification of sarcomeric SHG patterns in xenopus and rat muscles. The first two lines represent the mean percentage and standard deviation (± SD) of single-band (SB) sarcomeres from xenopus gastrocnemius (X Gastroc), xenopus tail (X tail) and rat gastrocnemius (R Gastroc) muscles. The tissues were fixed with PFA 4% (incubated or perfused) or either fresh. Note that the mean percentage has been determined using the Gabor filtering method (Gabor) or the intensity profile analysis (IPA) presented in Appendix 1 and Appendix 2 respectively. The values were obtained from 5 to 24 thick slices (40×40×10 μm3) from at least five animals for each experimental condition. The mean sarcomere size (± SD) and the average (± SD) full width at half maximum (FWHM) of the sarcomeric SHG signal were determined for both single-band (SB) and double-band (DB) sarcomeres for each experimental condition.

Tables Icon

Table 2 Quantification of the effect of proteolysis on sarcomeric SHG patterns in xenopus tail muscles. The values represent the mean percentage and standard deviation (± SD) of single-band (SB) sarcomeres from xenopus tail (X tail) muscles. J0 is the control without proteolysis, J1 and J2 correspond respectively to 24 H and 48H proteolysis. The values were obtained from 5 to 12 thick slices from two or three animals for each experimental condition.

Equations (2)

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I2ω[sin22α+(sin2α+χ33χ15cos2α)2].
card({(i,k):Ni,k(1,t)×minkNi,k¯})card({(i,k)})×100,

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