Mitochondrial fission-fusion as an emerging key regulator of cell proliferation and differentiation

BioEssays

Volumn 35, Issue 11, 2013, Pages 955-964

  Mitra, Kasturi ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Cell cycle; Cell differentiation; Cell proliferation; Mitochondrial fission; Mitochondrial fusion

Indexed keywords

CYCLIN B; CYCLIN D1; CYCLIN E; DYNAMIN I; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

ARTICLE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FUSION; CELL PROLIFERATION; CELL STRUCTURE; CYTOLOGY; DOWN REGULATION; ENDOSYMBIOSIS; ENERGY TRANSFER; FIBROBLAST; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MITOSIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EUKARYOTA; PROKARYOTA;

CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; MITOCHONDRIAL FISSION; MITOCHONDRIAL FUSION;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYCLIN E; EVOLUTION, MOLECULAR; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MODELS, MOLECULAR; SIGNAL TRANSDUCTION; STEM CELLS; YEASTS;

EID: 84885381258     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201300011     Document Type: Article

References (109)

1. Lewis MR, Lewis WH. 1914. Mitochondria in tissue culture. Science 39: 330-3.
2. Hoppins S, Nunnari J. 2012. Cell biology. Mitochondrial dynamics and apoptosis - the ER connection. Science 337: 1052-4.
3. Youle RJ, van der Bliek AM. 2012. Mitochondrial fission, fusion, and stress. Science 337: 1062-5.
4. Lodish H, Berk A, Zipursky SL, Matsudaira P, et al. Molecular Cell Biology. 4th edition. New York: W. H. Freeman. 2000. Section 13.1, Overview of the Cell Cycle and Its Control. Available from: http://www.ncbi.nlm.nih.gov/books/NBK21466/
5. Reed SI. 2003. Ratchets and clocks: the cell cycle, ubiquitylation and protein turnover. Nat Rev Mol Cell Biol 4: 855-64.
6. Kageyama Y, Zhang Z, Sesaki H. 2011. Mitochondrial division: molecular machinery and physiological functions. Curr Opin Cell Biol 23: 427-34.
7. Palmer CS, Osellame LD, Stojanovski D, Ryan MT. 2011. The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Cellular Signal 23: 1534-45.
8. Kim H, Scimia MC, Wilkinson D, Trelles RD, et al. 2011. Fine-tuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol Cell 44: 532-44.
9. Otera H, Wang C, Cleland MM, Setoguchi K, et al. 2010. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 191: 1141-58.
10. Zhao J, Liu T, Jin S, Wang X, et al. 2011. Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J 30: 2762-78.
11. Palmer CS, Osellame LD, Laine D, Koutsopoulos OS, et al. 2011. MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep 12: 565-73.
12. Pedrola L, Espert A, Wu X, Claramunt R, et al. 2005. GDAP1, the protein causing Charcot-Marie-Tooth disease type 4A, is expressed in neurons and is associated with mitochondria. Hum Mol Genet 14: 1087-94.
13. Niemann A, Ruegg M, La Padula V, Schenone A, et al. 2005. Ganglioside-induced differentiation associated protein 1 is a regulator of the mitochondrial network: new implications for Charcot-Marie-Tooth disease. J Cell Biol 170: 1067-78.
14. Chen H, Chan DC. 2010. Physiological functions of mitochondrial fusion. Ann N Y Acad Sci 1201: 21-5.
15. Song Z, Chen H, Fiket M, Alexander C, et al. 2007. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 178: 749-55.
16. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, et al. 2006. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126: 177-89.
17. von der Malsburg K, Muller JM, Bohnert M, Oeljeklaus S, et al. 2011. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell 21: 694-707.
18. Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, et al. 2011. A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J Cell Biol 195: 323-40.
19. Merkwirth C, Dargazanli S, Tatsuta T, Geimer S, et al. 2008. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 22: 476-88.
20. Wakabayashi J, Zhang Z, Wakabayashi N, Tamura Y, et al. 2009. The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J Cell Biol 186: 805-16.
21. Goyal G, Fell B, Sarin A, Youle RJ, et al. 2007. Role of mitochondrial remodeling in programmed cell death in Drosophila melanogaster. Dev Cell 12: 807-16.
22. Shenouda SM, Widlansky ME, Chen K, Xu G, et al. 2011. Altered mitochondrial dynamics contributes to endothelial dysfunction in diabetes mellitus. Circulation 124: 444-53.
23. Yu T, Robotham JL, Yoon Y. 2006. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci USA 103: 2653-8.
24. Mitra K, Wunder C, Roysam B, Lin G, et al. 2009. A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase. Proc Natl Acad Sci USA 106: 11960-5.
25. Taguchi N, Ishihara N, Jofuku A, Oka T, et al. 2007. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282: 11521-9.
26. Tondera D, Grandemange S, Jourdain A, Karbowski M, et al. 2009. SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J 28: 1589-600.
27. Mitra K, Rikhy R, Lilly M, Lippincott-Schwartz J. 2012. DRP1-dependent mitochondrial fission initiates follicle cell differentiation during Drosophila oogenesis. J Cell Biol 197: 487-97.
28. Wang C, Li Z, Lu Y, Du R, et al. 2006. Cyclin D1 repression of nuclear respiratory factor 1 integrates nuclear DNA synthesis and mitochondrial function. Proc Natl Acad Sci USA 103: 11567-72.
29. Kashatus DF, Lim KH, Brady DC, Pershing NL, et al. 2011. RALA and RALBP1 regulate mitochondrial fission at mitosis. Nat Cell Biol 13: 1108 11-15.
30. Zunino R, Braschi E, Xu L, McBride HM. 2009. Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J Biol Chem 284: 17783-95.
31. Horn SR, Thomenius MJ, Johnson ES, Freel CD, et al. 2011. Regulation of mitochondrial morphology by APC/CCdh1-mediated control of Drp1 stability. Mol Biol Cell 22: 1207-16.
32. Qiao X, Zhang L, Gamper AM, Fujita T, et al. 2010. APC/C-Cdh1: from cell cycle to cellular differentiation and genomic integrity. Cell Cycle 9: 3904-12.
33. Colombo SL, Palacios-Callender M, Frakich N, De Leon J, et al. 2010. Anaphase-promoting complex/cyclosome-Cdh1 coordinates glycolysis and glutaminolysis with transition to S phase in human T lymphocytes. Proc Natl Acad Sci USA 107: 18868-73.
34. Gomes LC, Di Benedetto G, Scorrano L. 2011. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13: 589-98.
35. Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J. 2011. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci USA 108: 10190-5.
36. Jones RG, Plas DR, Kubek S, Buzzai M, et al. 2005. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 18: 283-93.
37. Margineantu DH, Gregory Cox W, Sundell L, Sherwood SW, et al. 2002. Cell cycle dependent morphology changes and associated mitochondrial DNA redistribution in mitochondria of human cell lines. Mitochondrion 1: 425-35.
38. Nagaraj R, Gururaja-Rao S, Jones KT, Slattery M, et al. 2012. Control of mitochondrial structure and function by the Yorkie/YAP oncogenic pathway. Genes Dev 26: 2027-37.
39. Qian W, Choi S, Gibson GA, Watkins SC, et al. 2012. Mitochondrial hyperfusion induced by loss of fission protein Drp1 causes ATM-dependent G2/M arrest and aneuploidy through DNA replication stress. J Cell Sci 125: 5745-57.
40. Hwang HC, Clurman BE. 2005. Cyclin E in normal and neoplastic cell cycles. Oncogene 24: 2776-86.
41. Meignin C, Alvarez-Garcia I, Davis I, Palacios IM. 2007. The salvador-warts-hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr Biol 17: 1871-8.
42. Zhao B, Tumaneng K, Guan KL. 2011. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol 13: 877-83.
43. Ohsawa S, Sato Y, Enomoto M, Nakamura M, et al. 2012. Mitochondrial defect drives non-autonomous tumour progression through Hippo signalling in Drosophila. Nature 490: 547-51.
44. Ashrafian H, Docherty L, Leo V, Towlson C, et al. 2010. A mutation in the mitochondrial fission gene Dnm1l leads to cardiomyopathy. PLoS Genet 6: e1001000.
45. DuBoff B, Gotz J, Feany MB. 2012. Tau promotes neurodegeneration via DRP1 mislocalization in vivo. Neuron 75: 618-32.
46. Kageyama Y, Zhang Z, Roda R, Fukaya M, et al. 2012. Mitochondrial division ensures the survival of postmitotic neurons by suppressing oxidative damage. J Cell Biol 197: 535-51.
47. Ishihara N, Nomura M, Jofuku A, Kato H, et al. 2009. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11: 958-66.
48. Miller JP, Yeh N, Vidal A, Koff A. 2007. Interweaving the cell cycle machinery with cell differentiation. Cell Cycle 6: 2932-8.
49. Buttitta LA, Edgar BA. 2007. Mechanisms controlling cell cycle exit upon terminal differentiation. Curr Opin Cell Biol 19: 697-704.
50. Chen H, Chomyn A, Chan DC. 2005. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 280: 26185-92.
51. Hom JR, Quintanilla RA, Hoffman DL, de Mesy Bentley KL, et al. 2011. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev Cell 21: 469-78.
52. Varum S, Rodrigues AS, Moura MB, Momcilovic O, et al. 2011. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS ONE 6: e20914.
53. De Palma C, Falcone S, Pisoni S, Cipolat S, et al. 2010. Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation. Cell Death Differ 17: 1684-96.
54. Ali SH, DeCaprio JA. 2001. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin Cancer Biol 11: 15-23.
55. Ollmann M, Young LM, Di Como CJ, Karim F, et al. 2000. Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101: 91-101.
56. Chen KH, Guo X, Ma D, Guo Y, et al. 2004. Dysregulation of HSG triggers vascular proliferative disorders. Nat Cell Biol 6: 872-83.
57. Marsboom G, Toth PT, Ryan JJ, Hong Z, et al. 2012. Dynamin-related protein 1-mediated mitochondrial mitotic fission permits hyperproliferation of vascular smooth muscle cells and offers a novel therapeutic target in pulmonary hypertension. Circ Res 110: 1484-97.
58. Park YY, Lee S, Karbowski M, Neutzner A, et al. 2010. Loss of MARCH5 mitochondrial E3 ubiquitin ligase induces cellular senescence through dynamin-related protein 1 and mitofusin 1. J Cell Sci 123: 619-26.
59. Mandal S, Guptan P, Owusu-Ansah E, Banerjee U. 2005. Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev Cell 9: 843-54.
60. Mandal S, Freije WA, Guptan P, Banerjee U. 2010. Metabolic control of G1-S transition: cyclin E degradation by p53-induced activation of the ubiquitin-proteasome system. J Cell Biol 188: 473-9.
61. Schieke SM, McCoy JP, Jr, Finkel T. 2008. Coordination of mitochondrial bioenergetics with G1 phase cell cycle progression. Cell Cycle 7: 1782-7.
62. Crider DG, Garcia-Rodriguez LJ, Srivastava P, Peraza-Reyes L, et al. 2012. Rad53 is essential for a mitochondrial DNA inheritance checkpoint regulating G1 to S progression. J Cell Biol 198: 793-8.
63. Macleod KF. 2008. The role of the RB tumour suppressor pathway in oxidative stress responses in the haematopoietic system. Nat Rev Cancer 8: 769-81.
64. Havens CG, Ho A, Yoshioka N, Dowdy SF. 2006. Regulation of late G1/S phase transition and APC Cdh1 by reactive oxygen species. Mol Cell Biol 26: 4701-11.
65. Menon SG, Sarsour EH, Kalen AL, Venkataraman S, et al. 2007. Superoxide signaling mediates N-acetyl-L-cysteine-induced G1 arrest: regulatory role of cyclin D1 and manganese superoxide dismutase. Cancer Res 67: 6392-9.
66. Finkel T. 2011. Signal transduction by reactive oxygen species. J Cell Biol 194: 7-15.
67. Matoba S, Kang JG, Patino WD, Wragg A, et al. 2006. p53 regulates mitochondrial respiration. Science 312: 1650-3.
68. Blanchet E, Annicotte JS, Lagarrigue S, Aguilar V, et al. 2011. E2F transcription factor-1 regulates oxidative metabolism. Nat Cell Biol 13: 1146-52.
69. Galloway CA, Lee H, Yoon Y. 2012. Mitochondrial morphology-emerging role in bioenergetics. Free Radic Biol Med 53: 2218-28.
70. Perciavalle RM, Stewart DP, Koss B, Lynch J, et al. 2012. Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nat Cell Biol 14: 575-83.
71. Youle RJ, Karbowski M. 2005. Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 6: 657-63.
72. Shim SH, Xia C, Zhong G, Babcock HP, et al. 2012. Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes. Proc Natl Acad Sci USA 109: 13978-83.
73. Wurm CA, Neumann D, Lauterbach MA, Harke B, et al. 2011. Nanoscale distribution of mitochondrial import receptor Tom20 is adjusted to cellular conditions and exhibits an inner-cellular gradient. Proc Natl Acad Sci USA 108: 13546-51.
74. Chen H, Detmer SA, Ewald AJ, Griffin EE, et al. 2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200.
75. Verstreken P, Ly CV, Venken KJ, Koh TW, et al. 2005. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47: 365-78.
76. Labrousse AM, Zappaterra MD, Rube DA, van der Bliek AM. 1999. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell 4: 815-26.
77. Bleazard W, McCaffery JM, King EJ, Bale S, et al. 1999. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1: 298-304.
78. Hermann GJ, Thatcher JW, Mills JP, Hales KG, et al. 1998. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J Cell Biol 143: 359-73.
79. Tu BP, Kudlicki A, Rowicka M, McKnight SL. 2005. Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310: 1152-8.
80. Engelman JA, Luo J, Cantley LC. 2006. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7: 606-19.
81. Tondera D, Santel A, Schwarzer R, Dames S, et al. 2004. Knockdown of MTP18, a novel phosphatidylinositol 3-kinase-dependent protein, affects mitochondrial morphology and induces apoptosis. J Biol Chem 279: 31544-55.
82. Tondera D, Czauderna F, Paulick K, Schwarzer R, et al. 2005. The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J Cell Sci 118: 3049-59.
83. Sebastian D, Hernandez-Alvarez MI, Segales J, Sorianello E, et al. 2012. Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis. Proc Natl Acad Sci USA 109: 5523-8.
84. Chen H, Vermulst M, Wang YE, Chomyn A, et al. 2010. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141: 280-9.
85. Romanello V, Guadagnin E, Gomes L, Roder I, et al. 2010. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29: 1774-85.
86. Hardie DG, Ross FA, Hawley SA. 2012. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13: 251-62.
87. Graef M, Nunnari J. 2011. Mitochondria regulate autophagy by conserved signalling pathways. EMBO J 30: 2101-14.
88. Vander Heiden MG, Cantley LC, Thompson CB. 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-33.
89. Folmes CD, Dzeja PP, Nelson TJ, Terzic A. 2012. Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 11: 596-606.
90. Moyes CD, Mathieu-Costello OA, Tsuchiya N, Filburn C, et al. 1997. Mitochondrial biogenesis during cellular differentiation. Am J Physiol 272: C1345-51.
91. Wilson-Fritch L, Burkart A, Bell G, Mendelson K, et al. 2003. Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone. Mol Cell Biol 23: 1085-94.
92. Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, et al. 2007. Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 120: 4025-34.
93. Sankaran VG, Orkin SH, Walkley CR. 2008. Rb intrinsically promotes erythropoiesis by coupling cell cycle exit with mitochondrial biogenesis. Genes Dev 22: 463-75.
94. Ciavarra G, Zacksenhaus E. 2010. Rescue of myogenic defects in Rb-deficient cells by inhibition of autophagy or by hypoxia-induced glycolytic shift. J Cell Biol 191: 291-301.
95. Evan GI, Vousden KH. 2001. Proliferation, cell cycle and apoptosis in cancer. Nature 411: 342-8.
96. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, et al. 2011. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell stem cell 8: 59-71.
97. Weinberg F, Hamanaka R, Wheaton WW, Weinberg S, et al. 2010. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci USA 107: 8788-93.
98. Zhao J, Zhang J, Yu M, Xie Y, et al. 2013. Mitochondrial dynamics regulates migration and invasion of breast cancer cells. Oncogene in press, DOI: 10.1038/onc.2012.494
99. Rehman J, Zhang HJ, Toth PT, Zhang Y, et al. 2012. Inhibition of mitochondrial fission prevents cell cycle progression in lung cancer. FASEB J 26: 2175-86.
100. Ward PS, Thompson CB. 2012. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 21: 297-308.
101. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144: 646-74.
102. Gottlieb E, Tomlinson IP. 2005. Mitochondrial tumour suppressors: a genetic and biochemical update. Nat Rev Cancer 5: 857-66.
103. Yen KE, Bittinger MA, Su SM, Fantin VR. 2010. Cancer-associated IDH mutations: biomarker and therapeutic opportunities. Oncogene 29: 6409-17.
104. Iglesias-Bartolome R, Gutkind JS. 2011. Signaling circuitries controlling stem cell fate: to be or not to be. Curr Opin Cell Biol 23: 716-23.
105. Todd LR, Damin MN, Gomathinayagam R, Horn SR, et al. 2010. Growth factor erv1-like modulates Drp1 to preserve mitochondrial dynamics and function in mouse embryonic stem cells. Mol Biol Cell 21: 1225-36.
106. Zhou W, Choi M, Margineantu D, Margaretha L, et al. 2012. HIF1alpha induced switch from bivalent to exclusively glycolytic metabolism during ESC-to-EpiSC/hESC transition. EMBO J 31: 2103-16.
107. Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, et al. 2011. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 14: 264-71.
108. Agathocleous M, Love NK, Randlett O, Harris JJ, et al. 2012. Metabolic differentiation in the embryonic retina. Nat Cell Biol 14: 859-64.
109. Aubry L, Firtel R. 1999. Integration of signaling networks that regulate Dictyostelium differentiation. Annu Rev Cell Dev Biol 15: 469-517.