Inhibition of Drp1-dependent mitochondrial division impairs myogenic differentiation

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 8, 2013, Pages

  Kim, Boa ^a   Kim, Ji Seok ^a   Yoon, Yisang ^b   Santiago, Mayra C ^a   Brown, Michael D ^a,c   Park, Joon Young ^a  

^a TEMPLE UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Dynamin related protein 1; Mdivi 1; Mitochondrial dynamics; Myogenesis

Indexed keywords

CASPASE 3; DYNAMIN; DYNAMIN RELATED PROTEIN 1; GUANOSINE TRIPHOSPHATASE; MITOCHONDRIAL DNA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; MEMBRANE POTENTIAL; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

DYNAMIN-RELATED PROTEIN 1; MDIVI-1; MITOCHONDRIAL DYNAMICS; MYOGENESIS;

ANIMALS; APOPTOSIS; CASPASE 3; CELL LINE; DEATH-ASSOCIATED PROTEIN KINASES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MUSCLE DEVELOPMENT; MYOBLASTS; PHOSPHORYLATION; QUINAZOLINONES;

EID: 84885675007     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00502.2012     Document Type: Article

References (62)

1. Bakkar N, Guttridge DC. NF-kappaB signaling: a tale of two pathways in skeletal myogenesis. Physiol Rev 90: 495-511, 2010.
2. Barbieri E, Battistelli M, Casadei L, Vallorani L, Piccoli G, Guescini M, Gioacchini AM, Polidori E, Zeppa S, Ceccaroli P, Stocchi L, Stocchi V, Falcieri E. Morphofunctional and biochemical approaches for studying mitochondrial changes during myoblasts differentiation. J Aging Res 2011: 845379, 2011.
3. Bossy-Wetzel E, Barsoum MJ, Godzik A, Schwarzenbacher R, Lipton SA. Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr Opin Cell Biol 15: 706-716, 2003.
4. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T, Kurth MJ, Shaw JT, Hinshaw JE, Green DR, Nunnari J. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 14: 193-204, 2008.
5. Cereghetti GM, Stangherlin A, Martins de Brito O, Chang CR, Blackstone C, Bernardi P, Scorrano L. Dephosphorylation by calcineu-rin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci USA 105: 15803-15808, 2008.
6. Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev 84: 209-238, 2004.
7. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200, 2003.
8. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141: 280-289, 2010.
9. Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122: 289-301, 2005.
10. Cribbs JT, Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 8: 939-944, 2007.
11. Cui M, Tang X, Christian WV, Yoon Y, Tieu K. Perturbations in mitochondrial dynamics induced by human mutant PINK1 can be rescued by the mitochondrial division inhibitor mdivi-1. J Biol Chem 285: 11740-11752, 2010.
12. Day K, Shefer G, Shearer A, Yablonka-Reuveni Z. The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol 340: 330-343, 2010.
13. De Palma C, Falcone S, Pisoni S, Cipolat S, Panzeri C, Pambianco S, Pisconti A, Allevi R, Bassi MT, Cossu G, Pozzan T, Moncada S, Scorrano L, Brunelli S, Clementi E. Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation. Cell Death Differ 17: 1684-1696, 2010.
14. De Vos KJ, Allan VJ, Grierson AJ, Sheetz MP. Mitochondrial function and actin regulate dynamin-related protein 1-dependent mitochondrial fission. Curr Biol 15: 678-683, 2005.
15. Detmer SA, Chan DC. Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol 8: 870-879, 2007.
16. Durrani S, Konoplyannikov M, Ashraf M, Haider KH. Skeletal myo-blasts for cardiac repair. Regen Med 5: 919-932, 2010.
17. Elgass K, Pakay J, Ryan MT, Palmer CS. Recent advances into the understanding of mitochondrial fission. Biochim Biophys Acta, 2012.
18. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F, Smith CL, Youle RJ. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 1: 515-525, 2001.
19. Frezza C, Cipolat S, Scorrano L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc 2: 287-295, 2007.
20. Fujio Y, Guo K, Mano T, Mitsuuchi Y, Testa JR, Walsh K. Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol Cell Biol 19: 5073-5082, 1999.
21. Givvimani S, Munjal C, Tyagi N, Sen U, Metreveli N, Tyagi SC. Mitochondrial division/mitophagy inhibitor (Mdivi) ameliorates pressure overload induced heart failure. PLos One 7: e32388, 2012.
22. Gussoni E, Blau HM, Kunkel LM. The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med 3: 970-977, 1997.
23. Herzberg NH, Zwart R, Wolterman RA, Ruiter JP, Wanders RJ, Bolhuis PA, van den Bogert C. Differentiation and proliferation of respiration-deficient human myoblasts. Biochim Biophys Acta 1181: 63-67, 1993.
24. Hom JR, Gewandter JS, Michael L, Sheu SS, Yoon Y. Thapsigargin induces biphasic fragmentation of mitochondria through calcium-mediated mitochondrial fission and apoptosis. J Cell Physiol 212: 498-508, 2007.
25. Hong F, Lee J, Song JW, Lee SJ, Ahn H, Cho JJ, Ha J, Kim SS. Cyclosporin A blocks muscle differentiation by inducing oxidative stress and inhibiting the peptidyl-prolyl-cis-trans isomerase activity of cyclophi-lin A: cyclophilin A protects myoblasts from cyclosporin A-induced cytotoxicity. FASEB J 16: 1633-1635, 2002.
26. Horn SR, Thomenius MJ, Johnson ES, Freel CD, Wu JQ, Coloff JL, Yang CS, Tang W, An J, Ilkayeva OR, Rathmell JC, Newgard CB, Kornbluth S. Regulation of mitochondrial morphology by APC/CCdh1-mediated control of Drp1 stability. Mol Biol Cell 22: 1207-1216, 2011.
27. Inoue-Yamauchi A, Oda H. Depletion of mitochondrial fission factor DRP1 causes increased apoptosis in human colon cancer cells. Biochem Biophys Res Commun 421: 81-85, 2012.
28. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K, Otera H, Nakanishi Y, Nonaka I, Goto Y, Taguchi N, Morinaga H, Maeda M, Takayanagi R, Yokota S, Mihara K. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11: 958-966, 2009.
29. Jash S, Adhya S. Induction of muscle regeneration by RNA-mediated mitochondrial restoration. FASEB J 26: 4187-4197, 2012.
30. Jheng HF, Tsai PJ, Guo SM, Kuo LH, Chang CS, Su IJ, Chang CR, Tsai YS. Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol Cell Biol 32: 309-319, 2012.
31. Kaliman P, Canicio J, Testar X, Palacin M, Zorzano A. Insulin-like growth factor-II, phosphatidylinositol 3-kinase, nuclear factor-kappaB and inducible nitric-oxide synthase define a common myogenic signaling pathway. J Biol Chem 274: 17437-17444, 1999.
32. Koopman WJ, Verkaart S, Visch HJ, van der Westhuizen FH, Murphy MP, van den Heuvel LW, Smeitink JA, Willems PH. Inhibition of complex I of the electron transport chain causes O2-mediated mitochon-drial outgrowth. Am J Physiol Cell Physiol 288: C1440-C1450, 2005.
33. Kraft CS, LeMoine CM, Lyons CN, Michaud D, Mueller CR, Moyes CD. Control of mitochondrial biogenesis during myogenesis. Am J Physiol Cell Physiol 290: C1119-C1127, 2006.
34. Lackner LL, Nunnari J. Small molecule inhibitors of mitochondrial division: tools that translate basic biological research into medicine. Chem Biol 17: 578-583, 2010.
35. Lee Y, Lee HY, Hanna RA, Gustafsson AB. Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes. Am J Physiol Heart Circ Physiol 301: H1924-H1931, 2011.
36. Malinska D, Kudin AP, Bejtka M, Kunz WS. Changes in mitochondrial reactive oxygen species synthesis during differentiation of skeletal muscle cells. Mitochondrion 12: 144-148, 2012.
37. Marsboom G, Toth PT, Ryan JJ, Hong Z, Wu X, Fang YH, Thenap-pan T, Piao L, Zhang HJ, Pogoriler J, Chen Y, Morrow E, Weir EK, Rehman J, Archer SL. Dynamin-related protein 1-mediated mitochon-drial mitotic fission permits hyperproliferation of vascular smooth muscle cells and offers a novel therapeutic target in pulmonary hypertension. Circ Res 110: 1484-1497, 2012.
38. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495, 1961.
39. Mitra K, Rikhy R, Lilly M, Lippincott-Schwartz J. RP1-dependent mitochondrial fission initiates follicle cell differentiation during Drosoph-ila oogenesis. J Cell Biol 197: 487-497, 2012.
40. Mitra K, Wunder C, Roysam B, Lin G, Lippincott-Schwartz J. A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase. Proc Natl Acad Sci USA 106: 11960-11965, 2009.
41. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M. Direct isolation of satellite cells for skeletal muscle regeneration. Science 309: 2064-2067, 2005.
42. Mortensen OH, Frandsen L, Schjerling P, Nishimura E, Grunnet N. PGC-1alpha and PGC-1beta have both similar and distinct effects on myofiber switching toward an oxidative phenotype. Am J Physiol Endo-crinol Metab 291: E807-E816, 2006.
43. Moyes CD, Mathieu-Costello OA, Tsuchiya N, Filburn C, Hansford RG. Mitochondrial biogenesis during cellular differentiation. Am J Physiol Cell Physiol 272: C1345-C1351, 1997.
44. Nakanishi K, Sudo T, Morishima N. Endoplasmic reticulum stress signaling transmitted by ATF6 mediates apoptosis during muscle development. J Cell Biol 169: 555-560, 2005.
45. O'Flaherty J, Mei Y, Freer M, Weyman CM. Signaling through the TRAIL receptor DR5/FADD pathway plays a role in the apoptosis associated with skeletal myoblast differentiation. Apoptosis 11: 2103-2113, 2006.
46. Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ. Inhibiting mitochondrial fission protects the heart against ischemia/ reperfusion injury. Circulation 121: 2012-2022, 2010.
47. Park JY, Wang PY, Matsumoto T, Sung HJ, Ma W, Choi JW, Anderson SA, Leary SC, Balaban RS, Kang JG, Hwang PM. P53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ Res 105: 705-712, 2009.
48. Parone PA, James DI, Da Cruz S, Mattenberger Y, Donze O, Barja F, Martinou JC. Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol Cell Biol 26: 7397-7408, 2006.
49. Partridge T, Lu QL, Morris G, Hoffman E. Is myoblast transplantation effective? Nat Med 4: 1208-1209, 1998.
50. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, Gussoni E, Kunkel LM, Huard J. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15: 867-877, 2007.
51. Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques 50: 98-115, 2011.
52. Philp A, Belew MY, Evans A, Pham D, Sivia I, Chen A, Schenk S, Baar K. The PGC-1a-related coactivator promotes mitochondrial and myogenic adaptations in C2C12 myotubes. Am J Physiol Regul Integr Comp Physiol 301: R864-R872, 2011.
53. Piao YJ, Seo YH, Hong F, Kim JH, Kim YJ, Kang MH, Kim BS, Jo SA, Jo I, Jue DM, Kang I, Ha J, Kim SS. Nox 2 stimulates muscle differentiation via NF-kappaB/iNOS pathway. Free Radic Biol Med 38: 989-1001, 2005.
54. Shaltouki A, Freer M, Mei Y, Weyman CM. Increased expression of the pro-apoptotic Bcl2 family member PUMA is required for mitochondrial release of cytochrome C and the apoptosis associated with skeletal myoblast differentiation. Apoptosis 12: 2143-2154, 2007.
55. Shao D, Liu Y, Liu X, Zhu L, Cui Y, Cui A, Qiao A, Kong X, Chen Q, Gupta N, Fang F, Chang Y. PGC-1 beta-regulated mitochondrial biogenesis and function in myotubes is mediated by NRF-1 and ERR alpha. Mitochondrion 10: 516-527, 2010.
56. Sheppard RL, Spangenburg EE, Chin ER, Roth SM. Androgen receptor polyglutamine repeat length affects receptor activity and C2C12 cell development. Physiol Genomics 43: 1135-1143, 2011.
57. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K. Mitotic phos-phorylation of dynamin-related GTPase Drp1 participates in mitochon-drial fission. J Biol Chem 282: 11521-11529, 2007.
58. Twig G, Shirihai OS. The interplay between mitochondrial dynamics and mitophagy. Antioxid Redox Signal 14: 1939-1951, 2011.
59. Wang J, Walsh K. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273: 359-361, 1996.
60. Youle RJ, Karbowski M. Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 6: 657-663, 2005.
61. Yu T, Robotham JL, Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mito-chondrial morphology. Proc Natl Acad Sci USA 103: 2653-2658, 2006.
62. Yu T, Sheu SS, Robotham JL, Yoon Y. Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc Res 79: 341-351, 2008.