Abstract

The morphology and topology of mitochondria provide useful information about the physiological function of skeletal muscle. Previous studies of skeletal muscle mitochondria are based on observation with transmission, scanning electron microscopy or fluorescence microscopy. In contrast, photothermal (PT) microscopy has advantages over the above commonly used microscopic techniques because of no requirement for complex sample preparation by fixation or fluorescent-dye staining. Here, we employed the PT technique using a simple diode laser to visualize skeletal muscle mitochondria in unstained and stained tissues. The fine mitochondrial network structures in muscle fibers could be imaged with the PT imaging system, even in unstained tissues. PT imaging of tissues stained with toluidine blue revealed the structures of subsarcolemmal (SS) and intermyofibrillar (IMF) mitochondria and the swelling behavior of mitochondria in damaged muscle fibers with sufficient image quality. PT image analyses based on fast Fourier transform (FFT) and Grey-level co-occurrence matrix (GLCM) were performed to derive the characteristic size of mitochondria and to discriminate the image patterns of normal and damaged fibers.

© 2017 Optical Society of America

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  1. L. E. Bakeeva, Chentsov YuS, and V. P. Skulachev, “Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle,” Biochim. Biophys. Acta 501(3), 349–369 (1978).
    [Crossref] [PubMed]
  2. M. Picard, K. White, and D. M. Turnbull, “Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study,” J. Appl. Physiol. 114(2), 161–171 (2013).
    [Crossref] [PubMed]
  3. M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
    [Crossref] [PubMed]
  4. B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
    [Crossref] [PubMed]
  5. J. B. Gale, “Mitochondrial swelling associated with exercise and method of fixation,” Med. Sci. Sports 6(3), 182–187 (1974).
    [PubMed]
  6. P. D. Gollnick and D. W. King, “The immediate and chronic effect of exercise on the number and structure of skeletal muscle mitochondria,” Biochem. Exerc. Med. Sport 3, 239–244 (1969).
  7. D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes 51(10), 2944–2950 (2002).
    [Crossref] [PubMed]
  8. M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
    [Crossref] [PubMed]
  9. C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
    [PubMed]
  10. T. Shimada, K. Horita, M. Murakami, and R. Ogura, “Morphological studies of different mitochondrial populations in monkey myocardial cells,” Cell Tissue Res. 238(3), 577–582 (1984).
    [Crossref] [PubMed]
  11. T. Ogata and Y. Yamasaki, “Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers,” Anat. Rec. 248(2), 214–223 (1997).
    [Crossref] [PubMed]
  12. A. V. Kuznetsov, Y. Usson, X. Leverve, and R. Margreiter, “Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging,” Mol. Cell. Biochem. 256(1-2), 359–365 (2004).
    [Crossref] [PubMed]
  13. F. Shi, H. He, Y. Wang, D. Liu, M. Hu, and C. Wang, “Mitochondrial swelling and restorable fragmentation stimulated by femtosecond laser,” Biomed. Opt. Express 6(11), 4539–4545 (2015).
    [Crossref] [PubMed]
  14. I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
    [Crossref] [PubMed]
  15. P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
    [Crossref] [PubMed]
  16. A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
    [Crossref] [PubMed]
  17. D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
    [Crossref] [PubMed]
  18. J. Miyazaki, H. Tsurui, K. Kawasumi, and T. Kobayashi, “Optimal detection angle in sub-diffraction resolution photothermal microscopy: application for high sensitivity imaging of biological tissues,” Opt. Express 22(16), 18833–18842 (2014).
    [Crossref] [PubMed]
  19. J. Miyazaki, H. Tsurui, and T. Kobayashi, “Reduction of distortion in photothermal microscopy and its application to the high-resolution three-dimensional imaging of nonfluorescent tissues,” Biomed. Opt. Express 6(9), 3217–3224 (2015).
    [Crossref] [PubMed]
  20. J. Miyazaki, H. Tsurui, K. Kawasumi, and T. Kobayashi, “Simultaneous dual-wavelength imaging of nonfluorescent tissues with 3D subdiffraction photothermal microscopy,” Opt. Express 23(3), 3647–3656 (2015).
    [Crossref] [PubMed]
  21. D. Lasne, G. A. Blab, F. De Giorgi, F. Ichas, B. Lounis, and L. Cognet, “Label-free optical imaging of mitochondria in live cells,” Opt. Express 15(21), 14184–14193 (2007).
    [Crossref] [PubMed]
  22. J. He, J. Miyazaki, N. Wang, H. Tsurui, and T. Kobayashi, “Biological imaging with nonlinear photothermal microscopy using a compact supercontinuum fiber laser source,” Opt. Express 23(8), 9762–9771 (2015).
    [Crossref] [PubMed]
  23. Y. Kano, K. Sampei, and H. Matsudo, “Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise,” Acta Physiol. Scand. 180(3), 291–299 (2004).
    [Crossref] [PubMed]
  24. J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
    [Crossref] [PubMed]
  25. A. Materka, “Texture analysis methodologies for magnetic resonance imaging,” Dialogues Clin. Neurosci. 6(2), 243–250 (2004).
    [PubMed]

2015 (5)

2014 (1)

2013 (3)

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

M. Picard, K. White, and D. M. Turnbull, “Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study,” J. Appl. Physiol. 114(2), 161–171 (2013).
[Crossref] [PubMed]

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

2012 (1)

D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
[Crossref] [PubMed]

2010 (1)

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

2008 (1)

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

2007 (1)

2005 (1)

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

2004 (3)

A. V. Kuznetsov, Y. Usson, X. Leverve, and R. Margreiter, “Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging,” Mol. Cell. Biochem. 256(1-2), 359–365 (2004).
[Crossref] [PubMed]

A. Materka, “Texture analysis methodologies for magnetic resonance imaging,” Dialogues Clin. Neurosci. 6(2), 243–250 (2004).
[PubMed]

Y. Kano, K. Sampei, and H. Matsudo, “Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise,” Acta Physiol. Scand. 180(3), 291–299 (2004).
[Crossref] [PubMed]

2003 (1)

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

2002 (1)

D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes 51(10), 2944–2950 (2002).
[Crossref] [PubMed]

1997 (1)

T. Ogata and Y. Yamasaki, “Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers,” Anat. Rec. 248(2), 214–223 (1997).
[Crossref] [PubMed]

1992 (1)

C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
[PubMed]

1984 (1)

T. Shimada, K. Horita, M. Murakami, and R. Ogura, “Morphological studies of different mitochondrial populations in monkey myocardial cells,” Cell Tissue Res. 238(3), 577–582 (1984).
[Crossref] [PubMed]

1978 (1)

L. E. Bakeeva, Chentsov YuS, and V. P. Skulachev, “Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle,” Biochim. Biophys. Acta 501(3), 349–369 (1978).
[Crossref] [PubMed]

1974 (1)

J. B. Gale, “Mitochondrial swelling associated with exercise and method of fixation,” Med. Sci. Sports 6(3), 182–187 (1974).
[PubMed]

1969 (1)

P. D. Gollnick and D. W. King, “The immediate and chronic effect of exercise on the number and structure of skeletal muscle mitochondria,” Biochem. Exerc. Med. Sport 3, 239–244 (1969).

Adur, J.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Ayyadevara, S.

D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
[Crossref] [PubMed]

Bakeeva, L. E.

L. E. Bakeeva, Chentsov YuS, and V. P. Skulachev, “Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle,” Biochim. Biophys. Acta 501(3), 349–369 (1978).
[Crossref] [PubMed]

Balaban, R. S.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Barrett, K. E.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

Baxter, B. T.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Berggren, J. R.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Blab, G. A.

Bonilla, E.

C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
[PubMed]

Brusnichkin, A. V.

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Carvalho, H. F.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Casale, G. P.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Cesar, C. L.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Chentsov YuS,

L. E. Bakeeva, Chentsov YuS, and V. P. Skulachev, “Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle,” Biochim. Biophys. Acta 501(3), 349–369 (1978).
[Crossref] [PubMed]

Cline, G. W.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Cognet, L.

Combs, C. A.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Connelly, P. S.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Copeland, R. G.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

Cortright, R. N.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

De Giorgi, F.

DiMauro, S.

C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
[PubMed]

Dohm, G. L.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Dudek, R. W.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Galanzha, E. I.

D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
[Crossref] [PubMed]

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Gale, J. B.

J. B. Gale, “Mitochondrial swelling associated with exercise and method of fixation,” Med. Sci. Sports 6(3), 182–187 (1974).
[PubMed]

Gartside, S. E.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

Gentil, B. J.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

Glancy, B.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Gollnick, P. D.

P. D. Gollnick and D. W. King, “The immediate and chronic effect of exercise on the number and structure of skeletal muscle mitochondria,” Biochem. Exerc. Med. Sport 3, 239–244 (1969).

Gourley, C. R.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

Gourley, P. L.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

Gutti, T. L.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Hartnell, L. M.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

He, H.

He, J.

J. He, J. Miyazaki, N. Wang, H. Tsurui, and T. Kobayashi, “Biological imaging with nonlinear photothermal microscopy using a compact supercontinuum fiber laser source,” Opt. Express 23(8), 9762–9771 (2015).
[Crossref] [PubMed]

D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes 51(10), 2944–2950 (2002).
[Crossref] [PubMed]

Hendricks, J. K.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

Horita, K.

T. Shimada, K. Horita, M. Murakami, and R. Ogura, “Morphological studies of different mitochondrial populations in monkey myocardial cells,” Cell Tissue Res. 238(3), 577–582 (1984).
[Crossref] [PubMed]

Houmard, J. A.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Hu, M.

Hulver, M. W.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Ichas, F.

Kano, Y.

Y. Kano, K. Sampei, and H. Matsudo, “Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise,” Acta Physiol. Scand. 180(3), 291–299 (2004).
[Crossref] [PubMed]

Kawasumi, K.

Kelley, D. E.

D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes 51(10), 2944–2950 (2002).
[Crossref] [PubMed]

King, D. W.

P. D. Gollnick and D. W. King, “The immediate and chronic effect of exercise on the number and structure of skeletal muscle mitochondria,” Biochem. Exerc. Med. Sport 3, 239–244 (1969).

Kobayashi, T.

Kuznetsov, A. V.

A. V. Kuznetsov, Y. Usson, X. Leverve, and R. Margreiter, “Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging,” Mol. Cell. Biochem. 256(1-2), 359–365 (2004).
[Crossref] [PubMed]

Lasne, D.

Leverve, X.

A. V. Kuznetsov, Y. Usson, X. Leverve, and R. Margreiter, “Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging,” Mol. Cell. Biochem. 256(1-2), 359–365 (2004).
[Crossref] [PubMed]

Liu, D.

Lounis, B.

Lynch, T. G.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

MacDonald, K. G.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Malide, D.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Margreiter, R.

A. V. Kuznetsov, Y. Usson, X. Leverve, and R. Margreiter, “Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging,” Mol. Cell. Biochem. 256(1-2), 359–365 (2004).
[Crossref] [PubMed]

Materka, A.

A. Materka, “Texture analysis methodologies for magnetic resonance imaging,” Dialogues Clin. Neurosci. 6(2), 243–250 (2004).
[PubMed]

Matsudo, H.

Y. Kano, K. Sampei, and H. Matsudo, “Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise,” Acta Physiol. Scand. 180(3), 291–299 (2004).
[Crossref] [PubMed]

McComb, R. D.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

McDonald, A. E.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

McManus, M. J.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

Menshikova, E. V.

D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes 51(10), 2944–2950 (2002).
[Crossref] [PubMed]

Miyazaki, J.

Moraes, C. T.

C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
[PubMed]

Murakami, M.

T. Shimada, K. Horita, M. Murakami, and R. Ogura, “Morphological studies of different mitochondrial populations in monkey myocardial cells,” Cell Tissue Res. 238(3), 577–582 (1984).
[Crossref] [PubMed]

Naviaux, R. K.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

Nedosekin, D. A.

D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
[Crossref] [PubMed]

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Nella, A. A.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Ogata, T.

T. Ogata and Y. Yamasaki, “Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers,” Anat. Rec. 248(2), 214–223 (1997).
[Crossref] [PubMed]

Ogura, R.

T. Shimada, K. Horita, M. Murakami, and R. Ogura, “Morphological studies of different mitochondrial populations in monkey myocardial cells,” Cell Tissue Res. 238(3), 577–582 (1984).
[Crossref] [PubMed]

Pedroni, M. V.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Pelegati, V. B.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Picard, M.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

M. Picard, K. White, and D. M. Turnbull, “Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study,” J. Appl. Physiol. 114(2), 161–171 (2013).
[Crossref] [PubMed]

Pipinos, I. I.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Pories, W. J.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Proskurnin, M. A.

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Ricci, E.

C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
[PubMed]

Ritov, V. B.

D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes 51(10), 2944–2950 (2002).
[Crossref] [PubMed]

Sampei, K.

Y. Kano, K. Sampei, and H. Matsudo, “Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise,” Acta Physiol. Scand. 180(3), 291–299 (2004).
[Crossref] [PubMed]

Schon, E. A.

C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
[PubMed]

Shevtsova, E. F.

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Shi, F.

Shimada, T.

T. Shimada, K. Horita, M. Murakami, and R. Ogura, “Morphological studies of different mitochondrial populations in monkey myocardial cells,” Cell Tissue Res. 238(3), 577–582 (1984).
[Crossref] [PubMed]

Shmookler Reis, R. J.

D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
[Crossref] [PubMed]

Shulman, G. I.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Singh, K. K.

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

Skulachev, V. P.

L. E. Bakeeva, Chentsov YuS, and V. P. Skulachev, “Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle,” Biochim. Biophys. Acta 501(3), 349–369 (1978).
[Crossref] [PubMed]

Souza-Li, L. D.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

St Louis, K.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

Steiner, C. E.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Subramaniam, S.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Swanson, S. A.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Thomaz, A. A. D.

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Thompson, R. P.

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Tsurui, H.

Turnbull, D. M.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

M. Picard, K. White, and D. M. Turnbull, “Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study,” J. Appl. Physiol. 114(2), 161–171 (2013).
[Crossref] [PubMed]

Usson, Y.

A. V. Kuznetsov, Y. Usson, X. Leverve, and R. Margreiter, “Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging,” Mol. Cell. Biochem. 256(1-2), 359–365 (2004).
[Crossref] [PubMed]

Vladimirov, Y. A.

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Wallace, D. C.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

Wang, C.

Wang, N.

Wang, Y.

Weiss, D. J.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

White, K.

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

M. Picard, K. White, and D. M. Turnbull, “Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study,” J. Appl. Physiol. 114(2), 161–171 (2013).
[Crossref] [PubMed]

Yamasaki, Y.

T. Ogata and Y. Yamasaki, “Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers,” Anat. Rec. 248(2), 214–223 (1997).
[Crossref] [PubMed]

Yu, Z. X.

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Zharov, V. P.

D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
[Crossref] [PubMed]

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Zhu, Z.

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Acta Physiol. Scand. (1)

Y. Kano, K. Sampei, and H. Matsudo, “Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise,” Acta Physiol. Scand. 180(3), 291–299 (2004).
[Crossref] [PubMed]

Am. J. Hum. Genet. (1)

C. T. Moraes, E. Ricci, E. Bonilla, S. DiMauro, and E. A. Schon, “The mitochondrial tRNA(Leu(UUR)) mutation in mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes (MELAS): genetic, biochemical, and morphological correlations in skeletal muscle,” Am. J. Hum. Genet. 50(5), 934–949 (1992).
[PubMed]

Am. J. Physiol. Endocrinol. Metab. (1)

M. W. Hulver, J. R. Berggren, R. N. Cortright, R. W. Dudek, R. P. Thompson, W. J. Pories, K. G. MacDonald, G. W. Cline, G. I. Shulman, G. L. Dohm, and J. A. Houmard, “Skeletal muscle lipid metabolism with obesity,” Am. J. Physiol. Endocrinol. Metab. 284(4), E741–E747 (2003).
[Crossref] [PubMed]

Am. J. Physiol. Regul. Integr. Comp. Physiol. (1)

I. I. Pipinos, S. A. Swanson, Z. Zhu, A. A. Nella, D. J. Weiss, T. L. Gutti, R. D. McComb, B. T. Baxter, T. G. Lynch, and G. P. Casale, “Chronically ischemic mouse skeletal muscle exhibits myopathy in association with mitochondrial dysfunction and oxidative damage,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R290–R296 (2008).
[Crossref] [PubMed]

Anat. Rec. (1)

T. Ogata and Y. Yamasaki, “Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers,” Anat. Rec. 248(2), 214–223 (1997).
[Crossref] [PubMed]

Biochem. Exerc. Med. Sport (1)

P. D. Gollnick and D. W. King, “The immediate and chronic effect of exercise on the number and structure of skeletal muscle mitochondria,” Biochem. Exerc. Med. Sport 3, 239–244 (1969).

Biochim. Biophys. Acta (1)

L. E. Bakeeva, Chentsov YuS, and V. P. Skulachev, “Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle,” Biochim. Biophys. Acta 501(3), 349–369 (1978).
[Crossref] [PubMed]

Biomed. Opt. Express (2)

Biophys. J. (1)

D. A. Nedosekin, E. I. Galanzha, S. Ayyadevara, R. J. Shmookler Reis, and V. P. Zharov, “Photothermal confocal spectromicroscopy of multiple cellular chromophores and fluorophores,” Biophys. J. 102(3), 672–681 (2012).
[Crossref] [PubMed]

Cell Tissue Res. (1)

T. Shimada, K. Horita, M. Murakami, and R. Ogura, “Morphological studies of different mitochondrial populations in monkey myocardial cells,” Cell Tissue Res. 238(3), 577–582 (1984).
[Crossref] [PubMed]

Diabetes (1)

D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes,” Diabetes 51(10), 2944–2950 (2002).
[Crossref] [PubMed]

Dialogues Clin. Neurosci. (1)

A. Materka, “Texture analysis methodologies for magnetic resonance imaging,” Dialogues Clin. Neurosci. 6(2), 243–250 (2004).
[PubMed]

J. Appl. Physiol. (2)

M. Picard, K. White, and D. M. Turnbull, “Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study,” J. Appl. Physiol. 114(2), 161–171 (2013).
[Crossref] [PubMed]

M. Picard, B. J. Gentil, M. J. McManus, K. White, K. St Louis, S. E. Gartside, D. C. Wallace, and D. M. Turnbull, “Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle,” J. Appl. Physiol. 115(10), 1562–1571 (2013).
[Crossref] [PubMed]

J. Biophotonics (1)

A. V. Brusnichkin, D. A. Nedosekin, E. I. Galanzha, Y. A. Vladimirov, E. F. Shevtsova, M. A. Proskurnin, and V. P. Zharov, “Ultrasensitive label-free photothermal imaging, spectral identification, and quantification of cytochrome c in mitochondria, live cells, and solutions,” J. Biophotonics 3(12), 791–806 (2010).
[Crossref] [PubMed]

Med. Sci. Sports (1)

J. B. Gale, “Mitochondrial swelling associated with exercise and method of fixation,” Med. Sci. Sports 6(3), 182–187 (1974).
[PubMed]

Mol. Cell. Biochem. (1)

A. V. Kuznetsov, Y. Usson, X. Leverve, and R. Margreiter, “Subcellular heterogeneity of mitochondrial function and dysfunction: evidence obtained by confocal imaging,” Mol. Cell. Biochem. 256(1-2), 359–365 (2004).
[Crossref] [PubMed]

Nature (1)

B. Glancy, L. M. Hartnell, D. Malide, Z. X. Yu, C. A. Combs, P. S. Connelly, S. Subramaniam, and R. S. Balaban, “Mitochondrial reticulum for cellular energy distribution in muscle,” Nature 523(7562), 617–620 (2015).
[Crossref] [PubMed]

Opt. Express (4)

PLoS One (1)

J. Adur, L. D. Souza-Li, M. V. Pedroni, C. E. Steiner, V. B. Pelegati, A. A. D. Thomaz, H. F. Carvalho, and C. L. Cesar, “The severity of osteogenesis imperfecta and type I collagen pattern in human sukin as determined by nonlinear microscopy: Proof of principle of a diagnostic method,” PLoS One 8(7), e69186 (2013).
[Crossref] [PubMed]

Technol. Cancer Res. Treat. (1)

P. L. Gourley, J. K. Hendricks, A. E. McDonald, R. G. Copeland, K. E. Barrett, C. R. Gourley, K. K. Singh, and R. K. Naviaux, “Mitochondrial correlation microscopy and nanolaser spectroscopy - new tools for biophotonic detection of cancer in single cells,” Technol. Cancer Res. Treat. 4(6), 585–592 (2005).
[Crossref] [PubMed]

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Figures (6)

Fig. 1
Fig. 1

Schematics of PT microscopy. BS: beam splitter, DM: dichroic mirror, OB: objective lens, CL: condenser lens, SA: sample, BPF: band pass filter, SMF: single mode fiber, MMF: multimode fiber, BD: auto-balanced detector, LIA: lock-in amplifier.

Fig. 2
Fig. 2

(a, b) Bright field images in identical structure area for skeletal muscle tissues without and with toluidine blue staining. (c, d) PT images on the area outlined by black rectangles on (a, b). (e, f) PT images at white square area on (c, d), where the lateral line noise arising from the instability of stage motion is reduced by the line filter of FFT. (g) Normalized intensity profiles on line A-B in (e) and (f). Pump laser powers are 1.0 mW and 0.1 mW for measurement of unstained and stained tissue, respectively. Probe laser powers are 1 mW for both tissues.

Fig. 3
Fig. 3

Images of stained tissues of muscle fibers for 1 day after excising. (a-c) Bright field images of three different areas. (d-f) PT images taken on the square area on (a-c), corresponding to the area at the center of the normal fiber (d), near the capillary (e), and at the center of the swollen fiber (f). Pump and probe laser powers are 50 μW and 1 mW, respectively.

Fig. 4
Fig. 4

1D-FFT power spectra of PT image profiles for the normal fiber and the swollen fiber for images of Fig. 3(d) and 3(f), respectively. Line profile at 0, 15, and 90 degree from x axis defined in Fig. 3 are plotted. Power spectra are calculated by averaging spectra for 36 signal profiles for each angles with a sampling length of 7.5 μm. (c) Largest mean wave number of power spectra over all profile angles, μ max , and corresponding standard deviation, σ max . μ max ¯ and σ max ¯ in the Table are calculated by averaging μ max and σ max over four normal and four swollen fibers, respectively. Average size, width of the spectral peak, and deviation of size in the Table are derived from inverse of μ max ¯ , σ max ¯ and the deviation of μ max ¯ among fibers, respectively.

Fig. 5
Fig. 5

(a, b) The profiles of correlation, C, for the PT images for the normal fiber (shown in Fig. 3 (d)) and the swollen fiber (shown in Fig. 3(f)), respectively. C are calculated for two pixels separated with a distance, d, by GLCM analysis on the image size for 7 × 7 μm2. The orientation angle of two pixels, θ, is θ = 45 deg from the x axis depicted in Fig. 3, indicated in arrows in (c) and (d). Inset: Enlarged curve of C profile for the normal fiber. (c, d) The peak positions of the C profiles, dpeak, for different angle, θ, for the normal and the swollen fiber, respectively. The blue curves in (c) are the fitted profiles by equally spaced arch-shape curves, corresponding to equally spaced straight lines in x-y real space.

Fig. 6
Fig. 6

Maximum dpeak spacing, Δdmax, versus minimum dpeak spacing (swelling index), Δdmin, of PT image patterns for normal and swollen fibers.

Equations (4)

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μ= k 1 k 2 Akdk k 1 k 2 Adk ,
σ= [ k 1 k 2 A (kμ) 2 dk k 1 k 2 Adk ] 0.5 ,
C= i j (i m i )(j m j ) s i s j P(i,j) ,
d peak =Δ d f /cos(θ θ f ),

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