Abstract

Wide-field second harmonic generation (SHG) microscopy was developed using a high-power (> 4 W) and high-repetition-rate (MHz range) laser oscillator to achieve fast SHG imaging over a large area (400 µm × 400 µm). The microscope was used for high spatial resolution imaging of contracting muscles in live Drosophila melanogaster larvae. Anisotropic and isotropic bands of striated muscle were distinguished, allowing accurate determination of sarcomere length and SHG intensity from individual sarcomeres. Therefore, wide-field SHG microscopy has applications in basic contractility research and studying arrhythmias, muscular dystrophies and pharmaceutical effects on the muscle contraction dynamics of sarcomeres.

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

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References

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    [Crossref]

2016 (2)

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

C. Macias-Romero, V. Zubkovs, S. Wang, and S. Roke, “Wide-field medium-repetition-rate multiphoton microscopy reduces photodamage of living cells,” Biomed. Opt. Express 7(4), 1458–1467 (2016).
[Crossref]

2015 (1)

2014 (2)

2013 (1)

2012 (1)

2008 (2)

M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[Crossref]

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(4), 041318 (2008).
[Crossref]

2007 (2)

R. Le Harzic, I. Riemann, K. König, C. Wüllner, and C. Donitzky, “Influence of femtosecond laser pulse irradiation on the viability of cells at 1035, 517, and 345 nm,” J. Appl. Phys. 102(11), 114701 (2007).
[Crossref]

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(10), 1852–1859 (2007).
[Crossref]

2006 (2)

A. Major, V. Barzda, P. A. E. Piunno, S. Musikhin, and U. J. Krull, “An extended cavity diode-pumped femtosecond Yb:KGW laser for applications in optical DNA sensor technology based on fluorescence lifetime measurements,” Opt. Express 14(12), 5285–5294 (2006).
[Crossref]

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref]

2005 (3)

2004 (1)

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
[Crossref]

2003 (1)

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

2002 (1)

1999 (1)

D. E. Rassier, B. R. MacIntosh, and W. Herzog, “Length dependence of active force production in skeletal muscle,” J. Appl. Physiol. 86(5), 1445–1457 (1999).
[Crossref]

1997 (1)

1995 (1)

H. L. Granzier and T. C. Irving, “Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments,” Biophys. J. 68(3), 1027–1044 (1995).
[Crossref]

1991 (1)

D. L. Morgan, D. R. Claflin, and F. J. Julian, “Tension as a function of sarcomere length and velocity of shortening in single skeletal muscle fibres of the frog,” J. Physiol. 441(1), 719–732 (1991).
[Crossref]

1985 (1)

A. Magid and D. J. Law, “Myofibrils bear most of the resting tension in frog skeletal muscle,” Science 230(4731), 1280–1282 (1985).
[Crossref]

Barretto, R. P. J.

M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[Crossref]

Barzda, V.

Boucher, Y.

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

Bredeloux, P.

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

Brown, E.

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

Campagnola, P. J.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref]

Chang, C.-Y.

Chang, N.-S.

Chen, S.-J.

Cheng, L.-C.

Chiang, A.-S.

Cho, K.-C.

Cisek, R.

Claflin, D. R.

D. L. Morgan, D. R. Claflin, and F. J. Julian, “Tension as a function of sarcomere length and velocity of shortening in single skeletal muscle fibres of the frog,” J. Physiol. 441(1), 719–732 (1991).
[Crossref]

Delp, S. L.

M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[Crossref]

Didier, M. E. P.

DiTomaso, E.

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

Dong, C. Y.

Donitzky, C.

R. Le Harzic, I. Riemann, K. König, C. Wüllner, and C. Donitzky, “Influence of femtosecond laser pulse irradiation on the viability of cells at 1035, 517, and 345 nm,” J. Appl. Phys. 102(11), 114701 (2007).
[Crossref]

Durst, M.

Enejder, A. M. K.

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
[Crossref]

Fujita, K.

Gannier, F.

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

Golaraei, A.

Granzier, H. L.

H. L. Granzier and T. C. Irving, “Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments,” Biophys. J. 68(3), 1027–1044 (1995).
[Crossref]

Gratton, E.

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(4), 041318 (2008).
[Crossref]

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(10), 1852–1859 (2007).
[Crossref]

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(4), 041318 (2008).
[Crossref]

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(10), 1852–1859 (2007).
[Crossref]

Hellerer, T.

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
[Crossref]

Herzog, W.

D. E. Rassier, B. R. MacIntosh, and W. Herzog, “Length dependence of active force production in skeletal muscle,” J. Appl. Physiol. 86(5), 1445–1457 (1999).
[Crossref]

Irving, T. C.

H. L. Granzier and T. C. Irving, “Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments,” Biophys. J. 68(3), 1027–1044 (1995).
[Crossref]

Jain, R. K.

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

Jourdain, P.

Julian, F. J.

D. L. Morgan, D. R. Claflin, and F. J. Julian, “Tension as a function of sarcomere length and velocity of shortening in single skeletal muscle fibres of the frog,” J. Physiol. 441(1), 719–732 (1991).
[Crossref]

Kaneko, T.

Kawata, S.

Kobayashi, M.

König, K.

R. Le Harzic, I. Riemann, K. König, C. Wüllner, and C. Donitzky, “Influence of femtosecond laser pulse irradiation on the viability of cells at 1035, 517, and 345 nm,” J. Appl. Phys. 102(11), 114701 (2007).
[Crossref]

K. König, P. T. C. So, W. W. Mantulin, and E. Gratton, “Cellular response to near-infrared femtosecond laser pulses in two-photon microscopes,” Opt. Lett. 22(2), 135–136 (1997).
[Crossref]

Krouglov, S.

Krull, U. J.

Law, D. J.

A. Magid and D. J. Law, “Myofibrils bear most of the resting tension in frog skeletal muscle,” Science 230(4731), 1280–1282 (1985).
[Crossref]

Le Harzic, R.

R. Le Harzic, I. Riemann, K. König, C. Wüllner, and C. Donitzky, “Influence of femtosecond laser pulse irradiation on the viability of cells at 1035, 517, and 345 nm,” J. Appl. Phys. 102(11), 114701 (2007).
[Crossref]

Li, P.-K.

Li, Y.-C.

Lin, C.-Y.

Llewellyn, M. E.

M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[Crossref]

Macias-Romero, C.

MacIntosh, B. R.

D. E. Rassier, B. R. MacIntosh, and W. Herzog, “Length dependence of active force production in skeletal muscle,” J. Appl. Physiol. 86(5), 1445–1457 (1999).
[Crossref]

Magid, A.

A. Magid and D. J. Law, “Myofibrils bear most of the resting tension in frog skeletal muscle,” Science 230(4731), 1280–1282 (1985).
[Crossref]

Magistretti, P.

Major, A.

Malécot, C. O.

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

Mantulin, W. W.

Marquet, P.

Maupoil, V.

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

McKee, T.

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

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(2), 693–703 (2006).
[Crossref]

Mohler, W. A.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref]

Morgan, D. L.

D. L. Morgan, D. R. Claflin, and F. J. Julian, “Tension as a function of sarcomere length and velocity of shortening in single skeletal muscle fibres of the frog,” J. Physiol. 441(1), 719–732 (1991).
[Crossref]

Musikhin, S.

Nakamura, O.

Navab, R.

Niu, C.

Oron, D.

Pasqualin, C.

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

Piunno, P. A. E.

Plotnikov, S. V.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref]

Pluen, A.

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

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(4), 041318 (2008).
[Crossref]

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(10), 1852–1859 (2007).
[Crossref]

Radenovic, A.

Rassier, D. E.

D. E. Rassier, B. R. MacIntosh, and W. Herzog, “Length dependence of active force production in skeletal muscle,” J. Appl. Physiol. 86(5), 1445–1457 (1999).
[Crossref]

Riemann, I.

R. Le Harzic, I. Riemann, K. König, C. Wüllner, and C. Donitzky, “Influence of femtosecond laser pulse irradiation on the viability of cells at 1035, 517, and 345 nm,” J. Appl. Phys. 102(11), 114701 (2007).
[Crossref]

Roke, S.

Sakashita, S.

Schnitzer, M. J.

M. E. Llewellyn, R. P. J. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[Crossref]

Seed, B.

E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nat. Med. 9(6), 796–800 (2003).
[Crossref]

Silberberg, Y.

So, P. T. C.

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(4), 041318 (2008).
[Crossref]

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(10), 1852–1859 (2007).
[Crossref]

Takamatsu, T.

Tal, E.

Tarun, O. B.

Tsao, M.-S.

Van Howe, J.

Wang, S.

Wilson, B. C.

Wüllner, C.

R. Le Harzic, I. Riemann, K. König, C. Wüllner, and C. Donitzky, “Influence of femtosecond laser pulse irradiation on the viability of cells at 1035, 517, and 345 nm,” J. Appl. Phys. 102(11), 114701 (2007).
[Crossref]

Xu, C.

Yasufuku, K.

Yen, W.-C.

Yu, A.

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

Zhao, H.

Zhu, G.

Zipfel, W.

Zubkovs, V.

Zumbusch, A.

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
[Crossref]

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

C. Pasqualin, F. Gannier, A. Yu, C. O. Malécot, P. Bredeloux, and V. Maupoil, “SarcOptiM for ImageJ: high-frequency online sarcomere length computing on stimulated cardiomyocytes,” Am. J. Physiol. Cell Physiol. 311(2), C277–C283 (2016).
[Crossref]

Appl. Opt. (1)

Appl. Phys. Lett. (1)

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
[Crossref]

Biomed. Opt. Express (3)

Biophys. J. (2)

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(2), 693–703 (2006).
[Crossref]

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Supplementary Material (1)

NameDescription
» Visualization 1       Dynamics of live larva muscle contraction. Size: 425 µm × 425.

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Figures (3)

Fig. 1.
Fig. 1. Wide-field microscope with the high power oscillator (dashed rectangle). HR - highly reflective mirrors, LD - fiber-coupled diode laser, F1 (f1 = 35 mm) and F2 (f2 = 125 mm) - plano-convex lenses, and DM - dichroic mirror. R1, R2 and R3 - concave mirrors with radii of curvature of 350 mm, 400 mm and 600 mm, respectively, coated for high reflection at 1020-1080 nm with -1000 fs2 group delay dispersion. OC - 7.5% output coupler. F3 (f3 = 200 mm) and F4 (f4 = 50 mm) - plano-convex lenses. HWP - half wave plate, PBS - polarizing beamsplitter, AD - achromatic doublet, TL - tube lens, and F – optical filters.
Fig. 2.
Fig. 2. Fixed larval muscle wide-field SHG images. (a) 425 µm × 425 µm image area (20× 0.5 NA objective), and (c) 213 µm × 213 µm area (40× 1.3 NA oil objective). The laser power at the sample is ~3.0 W and the frame integration time is 100 ms. SHG intensity profiles (b, d) along the myofibrils from the yellow rectangles in (a, c), respectively.
Fig. 3.
Fig. 3. Dynamics of live larva muscle contraction. (a) The first frame from the wide-field microscope video (425 µm × 425 µm area, 20× 0.5 NA objective, see Visualization 1). (b) Wide-field SHG images of a myofibril over time during a contraction. The horizontal bar shows 0.1 s and the vertical bar is 30 µm. (c) The variation of average sarcomere length (blue triangles) and the normalized SHG intensity per sarcomere (red circles). A few data points are omitted in (c), due to blurring of sarcomeres during fast movement. The A and B labels correspond to shortening and elongation events, respectively.

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