Abstract

The research of mitochondrial dysfunction is of great importance and implicated in a range of neurodegenerative diseases. Traditionally, to investigate mitochondrial dynamics and functions, mitochondria are usually stimulated indirectly by treating cells with exogenous chemicals like oxidative agents. Such treatment lacks precision and controllability, and will simultaneously activate unknown complex cell processes. In this study, we report that two-photon 100-μs line scan by a femtosecond laser can induce restorable fragmentation or swelling of any targeted mitochondria instead of ablation or disruption. It can be defined by a customized two-photon line scan and inserted into any microscopy sequence as a single frame. The mitochondrial response is dependent on the peak power of laser pulses, cellular oxidative environment, and membrane permeability transition pores of mitochondria. The translocation of cytochrome C and Bax can be regulated by the photostimulation. Moreover, significant upregulation of Bcl-2 can be observed if the whole cell is stimulated. Those results suggest the mitochondrial and molecular response to photostimulation is quite complex. This femtosecond-laser stimulation method can thus provide a very noninvasive, precise, and controllable method to stimulate single target mitochondria for related biological research.

© 2017 Optical Society of America

Full Article  |  PDF Article
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References

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2017 (1)

Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
[PubMed]

2015 (1)

2014 (2)

W. Yan, H. He, Y. Wang, Y. Wang, M. Hu, and C. Wang, “Controllable generation of reactive oxygen species by femtosecond-laser irradiation,” Appl. Phys. Lett. 104, 083703 (2014).

R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
[PubMed]

2013 (1)

M. H. Yan, X. Wang, and X. Zhu, “Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease,” Free Radic. Biol. Med. 62, 90–101 (2013).
[PubMed]

2012 (2)

E. Sahin and R. A. DePinho, “Axis of ageing: telomeres, p53 and mitochondria,” Nat. Rev. Mol. Cell Biol. 13(6), 397–404 (2012).
[PubMed]

J. Brugués, V. Nuzzo, E. Mazur, and D. J. Needleman, “Nucleation and transport organize microtubules in metaphase spindles,” Cell 149(3), 554–564 (2012).
[PubMed]

2011 (1)

Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
[PubMed]

2010 (1)

R. McFarland, R. W. Taylor, and D. M. Turnbull, “A neurological perspective on mitochondrial disease,” Lancet Neurol. 9(8), 829–840 (2010).
[PubMed]

2009 (3)

S. H. Chung and E. Mazur, “Surgical applications of femtosecond lasers,” J. Biophotonics 2(10), 557–572 (2009).
[PubMed]

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
[PubMed]

J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14(5), 054040 (2009).
[PubMed]

2008 (2)

S. X. Guo, F. Bourgeois, T. Chokshi, N. J. Durr, M. A. Hilliard, N. Chronis, and A. Ben-Yakar, “Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies,” Nat. Methods 5(6), 531–533 (2008).
[PubMed]

C. Henchcliffe and M. F. Beal, “Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis,” Nat. Clin. Pract. Neurol. 4(11), 600–609 (2008).
[PubMed]

2007 (1)

A. Heisterkamp, J. Baumgart, I. Z. Maxwell, A. Ngezahayo, E. Mazur, and H. Lubatschowski, “Fs-laser scissors for photobleaching, ablation in fixed samples and living cells, and studies of cell mechanics,” Methods Cell Biol. 82, 293–307 (2007).
[PubMed]

2006 (4)

S. Kumar, I. Z. Maxwell, A. Heisterkamp, T. R. Polte, T. P. Lele, M. Salanga, E. Mazur, and D. E. Ingber, “Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics,” Biophys. J. 90(10), 3762–3773 (2006).
[PubMed]

N. Nishimura, C. B. Schaffer, B. Friedman, P. S. Tsai, P. D. Lyden, and D. Kleinfeld, “Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke,” Nat. Methods 3(2), 99–108 (2006).
[PubMed]

M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature 443(7113), 787–795 (2006).
[PubMed]

P. M. Abou-Sleiman, M. M. Muqit, and N. W. Wood, “Expanding insights of mitochondrial dysfunction in Parkinson’s disease,” Nat. Rev. Neurosci. 7(3), 207–219 (2006).
[PubMed]

2005 (3)

I. Maxwell, S. Chung, and E. Mazur, “Nanoprocessing of subcellular targets using femtosecond laser pulses,” Med. Laser Appl. 20, 193–200 (2005).

M. F. Beal, “Mitochondria take center stage in aging and neurodegeneration,” Ann. Neurol. 58(4), 495–505 (2005).
[PubMed]

T. Shimada, W. Watanabe, S. Matsunaga, T. Higashi, H. Ishii, K. Fukui, K. Isobe, and K. Itoh, “Intracellular disruption of mitochondria in a living HeLa cell with a 76-MHz femtosecond laser oscillator,” Opt. Express 13(24), 9869–9880 (2005).
[PubMed]

2004 (4)

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Neurosurgery: functional regeneration after laser axotomy,” Nature 432(7019), 822 (2004).
[PubMed]

W. Watanabe, N. Arakawa, S. Matsunaga, T. Higashi, K. Fukui, K. Isobe, and K. Itoh, “Femtosecond laser disruption of subcellular organelles in a living cell,” Opt. Express 12(18), 4203–4213 (2004).
[PubMed]

D. R. Green and G. Kroemer, “The pathophysiology of mitochondrial cell death,” Science 305(5684), 626–629 (2004).
[PubMed]

R. A. Butow and N. G. Avadhani, “Mitochondrial signaling: the retrograde response,” Mol. Cell 14(1), 1–15 (2004).
[PubMed]

2003 (1)

D. D. Newmeyer and S. Ferguson-Miller, “Mitochondria: releasing power for life and unleashing the machineries of death,” Cell 112(4), 481–490 (2003).
[PubMed]

2002 (1)

U. K. Tirlapur and K. König, “Targeted transfection by femtosecond laser,” Nature 418(6895), 290–291 (2002).
[PubMed]

2001 (2)

K. F. Ferri and G. Kroemer, “Organelle-specific initiation of cell death pathways,” Nat. Cell Biol. 3(11), E255–E263 (2001).
[PubMed]

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K. J. Halbhuber, “Femtosecond Near-Infrared Laser Pulses Elicit Generation of Reactive Oxygen Species in Mammalian Cells Leading to Apoptosis-like Death,” Exp. Cell Res. 263(1), 88–97 (2001).
[PubMed]

Abou-Sleiman, P. M.

P. M. Abou-Sleiman, M. M. Muqit, and N. W. Wood, “Expanding insights of mitochondrial dysfunction in Parkinson’s disease,” Nat. Rev. Neurosci. 7(3), 207–219 (2006).
[PubMed]

Abramov, A. Y.

R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
[PubMed]

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
[PubMed]

Angelova, P. R.

R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
[PubMed]

Arakawa, N.

Avadhani, N. G.

R. A. Butow and N. G. Avadhani, “Mitochondrial signaling: the retrograde response,” Mol. Cell 14(1), 1–15 (2004).
[PubMed]

Baumgart, J.

J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14(5), 054040 (2009).
[PubMed]

A. Heisterkamp, J. Baumgart, I. Z. Maxwell, A. Ngezahayo, E. Mazur, and H. Lubatschowski, “Fs-laser scissors for photobleaching, ablation in fixed samples and living cells, and studies of cell mechanics,” Methods Cell Biol. 82, 293–307 (2007).
[PubMed]

Beal, M. F.

C. Henchcliffe and M. F. Beal, “Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis,” Nat. Clin. Pract. Neurol. 4(11), 600–609 (2008).
[PubMed]

M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature 443(7113), 787–795 (2006).
[PubMed]

M. F. Beal, “Mitochondria take center stage in aging and neurodegeneration,” Ann. Neurol. 58(4), 495–505 (2005).
[PubMed]

Ben-Yakar, A.

S. X. Guo, F. Bourgeois, T. Chokshi, N. J. Durr, M. A. Hilliard, N. Chronis, and A. Ben-Yakar, “Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies,” Nat. Methods 5(6), 531–533 (2008).
[PubMed]

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Neurosurgery: functional regeneration after laser axotomy,” Nature 432(7019), 822 (2004).
[PubMed]

Bintig, W.

J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14(5), 054040 (2009).
[PubMed]

Bourgeois, F.

S. X. Guo, F. Bourgeois, T. Chokshi, N. J. Durr, M. A. Hilliard, N. Chronis, and A. Ben-Yakar, “Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies,” Nat. Methods 5(6), 531–533 (2008).
[PubMed]

Brugués, J.

J. Brugués, V. Nuzzo, E. Mazur, and D. J. Needleman, “Nucleation and transport organize microtubules in metaphase spindles,” Cell 149(3), 554–564 (2012).
[PubMed]

Butow, R. A.

R. A. Butow and N. G. Avadhani, “Mitochondrial signaling: the retrograde response,” Mol. Cell 14(1), 1–15 (2004).
[PubMed]

Cao, Y.

Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
[PubMed]

Chen, Q.

Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
[PubMed]

Cheng, H.

Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
[PubMed]

Chisholm, A. D.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Neurosurgery: functional regeneration after laser axotomy,” Nature 432(7019), 822 (2004).
[PubMed]

Chokshi, T.

S. X. Guo, F. Bourgeois, T. Chokshi, N. J. Durr, M. A. Hilliard, N. Chronis, and A. Ben-Yakar, “Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies,” Nat. Methods 5(6), 531–533 (2008).
[PubMed]

Chronis, N.

S. X. Guo, F. Bourgeois, T. Chokshi, N. J. Durr, M. A. Hilliard, N. Chronis, and A. Ben-Yakar, “Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies,” Nat. Methods 5(6), 531–533 (2008).
[PubMed]

Chung, S.

I. Maxwell, S. Chung, and E. Mazur, “Nanoprocessing of subcellular targets using femtosecond laser pulses,” Med. Laser Appl. 20, 193–200 (2005).

Chung, S. H.

S. H. Chung and E. Mazur, “Surgical applications of femtosecond lasers,” J. Biophotonics 2(10), 557–572 (2009).
[PubMed]

Cinar, H.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Neurosurgery: functional regeneration after laser axotomy,” Nature 432(7019), 822 (2004).
[PubMed]

Cinar, H. N.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Neurosurgery: functional regeneration after laser axotomy,” Nature 432(7019), 822 (2004).
[PubMed]

de Castro, I. P.

R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
[PubMed]

Deas, E.

R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
[PubMed]

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
[PubMed]

DePinho, R. A.

E. Sahin and R. A. DePinho, “Axis of ageing: telomeres, p53 and mitochondria,” Nat. Rev. Mol. Cell Biol. 13(6), 397–404 (2012).
[PubMed]

Dinsdale, D.

R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
[PubMed]

Downward, J.

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
[PubMed]

Duchen, M. R.

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
[PubMed]

Durr, N. J.

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J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14(5), 054040 (2009).
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Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
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S. Kumar, I. Z. Maxwell, A. Heisterkamp, T. R. Polte, T. P. Lele, M. Salanga, E. Mazur, and D. E. Ingber, “Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics,” Biophys. J. 90(10), 3762–3773 (2006).
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S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
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Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
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U. K. Tirlapur and K. König, “Targeted transfection by femtosecond laser,” Nature 418(6895), 290–291 (2002).
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U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K. J. Halbhuber, “Femtosecond Near-Infrared Laser Pulses Elicit Generation of Reactive Oxygen Species in Mammalian Cells Leading to Apoptosis-like Death,” Exp. Cell Res. 263(1), 88–97 (2001).
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J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14(5), 054040 (2009).
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S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
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R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
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A. Heisterkamp, J. Baumgart, I. Z. Maxwell, A. Ngezahayo, E. Mazur, and H. Lubatschowski, “Fs-laser scissors for photobleaching, ablation in fixed samples and living cells, and studies of cell mechanics,” Methods Cell Biol. 82, 293–307 (2007).
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J. Brugués, V. Nuzzo, E. Mazur, and D. J. Needleman, “Nucleation and transport organize microtubules in metaphase spindles,” Cell 149(3), 554–564 (2012).
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R. McFarland, R. W. Taylor, and D. M. Turnbull, “A neurological perspective on mitochondrial disease,” Lancet Neurol. 9(8), 829–840 (2010).
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J. Brugués, V. Nuzzo, E. Mazur, and D. J. Needleman, “Nucleation and transport organize microtubules in metaphase spindles,” Cell 149(3), 554–564 (2012).
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D. D. Newmeyer and S. Ferguson-Miller, “Mitochondria: releasing power for life and unleashing the machineries of death,” Cell 112(4), 481–490 (2003).
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J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14(5), 054040 (2009).
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R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
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N. Nishimura, C. B. Schaffer, B. Friedman, P. S. Tsai, P. D. Lyden, and D. Kleinfeld, “Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke,” Nat. Methods 3(2), 99–108 (2006).
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S. Kumar, I. Z. Maxwell, A. Heisterkamp, T. R. Polte, T. P. Lele, M. Salanga, E. Mazur, and D. E. Ingber, “Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics,” Biophys. J. 90(10), 3762–3773 (2006).
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N. Nishimura, C. B. Schaffer, B. Friedman, P. S. Tsai, P. D. Lyden, and D. Kleinfeld, “Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke,” Nat. Methods 3(2), 99–108 (2006).
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Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
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R. McFarland, R. W. Taylor, and D. M. Turnbull, “A neurological perspective on mitochondrial disease,” Lancet Neurol. 9(8), 829–840 (2010).
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U. K. Tirlapur and K. König, “Targeted transfection by femtosecond laser,” Nature 418(6895), 290–291 (2002).
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U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K. J. Halbhuber, “Femtosecond Near-Infrared Laser Pulses Elicit Generation of Reactive Oxygen Species in Mammalian Cells Leading to Apoptosis-like Death,” Exp. Cell Res. 263(1), 88–97 (2001).
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N. Nishimura, C. B. Schaffer, B. Friedman, P. S. Tsai, P. D. Lyden, and D. Kleinfeld, “Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke,” Nat. Methods 3(2), 99–108 (2006).
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Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
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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).
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Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
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Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
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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).
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W. Yan, H. He, Y. Wang, Y. Wang, M. Hu, and C. Wang, “Controllable generation of reactive oxygen species by femtosecond-laser irradiation,” Appl. Phys. Lett. 104, 083703 (2014).

W. Yan, H. He, Y. Wang, Y. Wang, M. Hu, and C. Wang, “Controllable generation of reactive oxygen species by femtosecond-laser irradiation,” Appl. Phys. Lett. 104, 083703 (2014).

Watanabe, W.

Wei, X.

Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
[PubMed]

Willis, A. E.

R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
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Wood, N. W.

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
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P. M. Abou-Sleiman, M. M. Muqit, and N. W. Wood, “Expanding insights of mitochondrial dysfunction in Parkinson’s disease,” Nat. Rev. Neurosci. 7(3), 207–219 (2006).
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S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
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Xu, Z.

Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
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M. H. Yan, X. Wang, and X. Zhu, “Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease,” Free Radic. Biol. Med. 62, 90–101 (2013).
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Yan, W.

W. Yan, H. He, Y. Wang, Y. Wang, M. Hu, and C. Wang, “Controllable generation of reactive oxygen species by femtosecond-laser irradiation,” Appl. Phys. Lett. 104, 083703 (2014).

Yanik, M. F.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Neurosurgery: functional regeneration after laser axotomy,” Nature 432(7019), 822 (2004).
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Yao, Z.

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
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Ye, T.

Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
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Zheng, M.

Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
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Zhu, X.

M. H. Yan, X. Wang, and X. Zhu, “Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease,” Free Radic. Biol. Med. 62, 90–101 (2013).
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M. F. Beal, “Mitochondria take center stage in aging and neurodegeneration,” Ann. Neurol. 58(4), 495–505 (2005).
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Appl. Phys. Lett. (1)

W. Yan, H. He, Y. Wang, Y. Wang, M. Hu, and C. Wang, “Controllable generation of reactive oxygen species by femtosecond-laser irradiation,” Appl. Phys. Lett. 104, 083703 (2014).

Biomed. Opt. Express (1)

Biophys. J. (1)

S. Kumar, I. Z. Maxwell, A. Heisterkamp, T. R. Polte, T. P. Lele, M. Salanga, E. Mazur, and D. E. Ingber, “Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics,” Biophys. J. 90(10), 3762–3773 (2006).
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Cell (2)

J. Brugués, V. Nuzzo, E. Mazur, and D. J. Needleman, “Nucleation and transport organize microtubules in metaphase spindles,” Cell 149(3), 554–564 (2012).
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D. D. Newmeyer and S. Ferguson-Miller, “Mitochondria: releasing power for life and unleashing the machineries of death,” Cell 112(4), 481–490 (2003).
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U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K. J. Halbhuber, “Femtosecond Near-Infrared Laser Pulses Elicit Generation of Reactive Oxygen Species in Mammalian Cells Leading to Apoptosis-like Death,” Exp. Cell Res. 263(1), 88–97 (2001).
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M. H. Yan, X. Wang, and X. Zhu, “Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease,” Free Radic. Biol. Med. 62, 90–101 (2013).
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J. Biol. Chem. (1)

Q. Ma, H. Fang, W. Shang, L. Liu, Z. Xu, T. Ye, X. Wang, M. Zheng, Q. Chen, and H. Cheng, “Superoxide Flashes: Early Mitochondrial Signals For Oxidative Stress-Induced Apoptosis,” J. Biol. Chem. 286(31), 27573–27581 (2011).
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J. Biomed. Opt. (1)

J. Baumgart, K. Kuetemeyer, W. Bintig, A. Ngezahayo, W. Ertmer, H. Lubatschowski, and A. Heisterkamp, “Repetition rate dependency of reactive oxygen species formation during femtosecond laser-based cell surgery,” J. Biomed. Opt. 14(5), 054040 (2009).
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J. Biophotonics (2)

Y. Wang, H. He, S. Wang, Y. Liu, M. Hu, Y. Cao, S. Kong, X. Wei, and C. Wang, “Photostimulation by femtosecond laser triggers restorable fragmentation in single mitochondrion,” J. Biophotonics 10(2), 286–293 (2017).
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R. McFarland, R. W. Taylor, and D. M. Turnbull, “A neurological perspective on mitochondrial disease,” Lancet Neurol. 9(8), 829–840 (2010).
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I. Maxwell, S. Chung, and E. Mazur, “Nanoprocessing of subcellular targets using femtosecond laser pulses,” Med. Laser Appl. 20, 193–200 (2005).

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A. Heisterkamp, J. Baumgart, I. Z. Maxwell, A. Ngezahayo, E. Mazur, and H. Lubatschowski, “Fs-laser scissors for photobleaching, ablation in fixed samples and living cells, and studies of cell mechanics,” Methods Cell Biol. 82, 293–307 (2007).
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Mol. Cell (2)

S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D. S. Latchman, S. J. Tabrizi, N. W. Wood, M. R. Duchen, and A. Y. Abramov, “PINK1-associated Parkinson’s disease is caused by neuronal vulnerability to calcium-induced cell death,” Mol. Cell 33(5), 627–638 (2009).
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R. Tufi, S. Gandhi, I. P. de Castro, S. Lehmann, P. R. Angelova, D. Dinsdale, E. Deas, H. Plun-Favreau, P. Nicotera, A. Y. Abramov, A. E. Willis, G. R. Mallucci, S. H. Loh, and L. M. Martins, “Enhancing nucleotide metabolism protects against mitochondrial dysfunction and neurodegeneration in a PINK1 model of Parkinson’s disease,” Nat. Cell Biol. 16(2), 157–166 (2014).
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C. Henchcliffe and M. F. Beal, “Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis,” Nat. Clin. Pract. Neurol. 4(11), 600–609 (2008).
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N. Nishimura, C. B. Schaffer, B. Friedman, P. S. Tsai, P. D. Lyden, and D. Kleinfeld, “Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke,” Nat. Methods 3(2), 99–108 (2006).
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S. X. Guo, F. Bourgeois, T. Chokshi, N. J. Durr, M. A. Hilliard, N. Chronis, and A. Ben-Yakar, “Femtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies,” Nat. Methods 5(6), 531–533 (2008).
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E. Sahin and R. A. DePinho, “Axis of ageing: telomeres, p53 and mitochondria,” Nat. Rev. Mol. Cell Biol. 13(6), 397–404 (2012).
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Nat. Rev. Neurosci. (1)

P. M. Abou-Sleiman, M. M. Muqit, and N. W. Wood, “Expanding insights of mitochondrial dysfunction in Parkinson’s disease,” Nat. Rev. Neurosci. 7(3), 207–219 (2006).
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Nature (3)

M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature 443(7113), 787–795 (2006).
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M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Ben-Yakar, “Neurosurgery: functional regeneration after laser axotomy,” Nature 432(7019), 822 (2004).
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Science (1)

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Figures (4)

Fig. 1
Fig. 1 Fragmentation and swelling were found in photostimulated mitochondria. (a) The two-photon line scan scheme to a single mitochondrion. Red line: the scanning line across the mitochondrial tubule. Blue line: the microscopy sequence. The stimulation (red) can be inserted into the confocal microscopy sequence to provide a continuous observation. (b) Fragmentation of the mitochondrial tubule structure was found immediately after the phototimulation at the 9th s. At the 36th s, recovery of the fragmented mitochondrion was observed. (c) Swollen mitochondria were induced by chance and could not recover. (d) The MMP of the stimulated mitochondrion during fragmentation and recovery. (e) No significant photobleaching of GFP was found by continuous two-photon scanning on cells. (f) Femtosecond-laser stimulation in a 1.5-μm spot at 30 mW disrupted the mitochondria inside. (g) Two-photon scanning in a microregion (3 × 3 μm2) induced complex changes of several mitochondria nearby. Arrow: photostimulation events. (h) Mitochondrial responses to different photostimulations with different scanning types in (b,c), (f), and (g) respectively. White box: 2D scanning. Orange box: the area magnified in the right. Bar: 10 μm.
Fig. 2
Fig. 2 Mitochondrial response to photostimulation was dependent on the peak power and wavelength of laser pulses (a), the cellular oxidative environment (b), and mPTP (c).The inhibition of mPTP by CsA greatly prolonged the recovery duration of fragmented mitochondria as in (c). Arrow: the position of femtosecond-laser stimulation. Bar: 10 μm. *** P<0.0005.
Fig. 3
Fig. 3 Translocation of Bax and Cyto C by different photostimulations. (a) Bax did not translocate at 16-mW stimulation (n = 30). No release of Cyto C from the stimulated mitochondrion was found (n = 30). (b) Bax concentrated to the stimulated mitochondria (n = 30) and Cyto C release (n = 30) was found at 20-mW stimulation. IF: immunofluorescence microscopy, performed 20 minutes after photostimulation. Arrow: the position of femtosecond-laser stimulation. Bar: 10 μm. (c) The Co-Localization rate of Bax and Cyto C calculated by the number of overlapping pixels in the crossing line in the zoom-in views (n = 30). *** P<0.0005.
Fig. 4
Fig. 4 Cellular response to the whole-cell photostimulation. (a) Un-recoverable fragmentation of mtiochondria was induced if the intense stimulation was performed to the whole cell. (b) The PI fluorescence in HeLa cells with 100 μM H2O2 treated for 1 hour (left) and control (right). (c) Upregulation of Bcl-2 was found in the stimulated cells. Bar: 20 μm.

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