Mitochondria dynamism: Of shape, transport and cell migration

Cellular and Molecular Life Sciences

Volumn 71, Issue 12, 2014, Pages 2313-2324

  Da Silva, André Ferreira ^a,b   Mariotti, Francesca Romana ^c   Máximo, Valdemar ^a,b   Campello, Silvia ^c  

^a UNIVERSITY OF PORTO   (Portugal)

^b University of Porto   (Portugal)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Fusion fission; Lymphocytes; Metastasis; Migration; Mitochondria; Neurons

Indexed keywords

CALCIUM; REACTIVE OXYGEN METABOLITE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

APOPTOSIS; CALCIUM SIGNALING; CANCER CELL; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CELL ORGANELLE; CELL SHAPE; CELL STRUCTURE; CELL TRANSPORT; CYTOPLASM; HUMAN; HUMAN CELL; IMMUNE SYSTEM; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; REVIEW; SUMOYLATION; TUMOR CELL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MOVEMENT; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; ORGANELLE SHAPE;

EID: 84901697443     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1557-8     Document Type: Review

References (101)

1. Otera H, Ishihara N, Mihara K (2013) New insights into the function and regulation of mitochondrial fission. Biochim Biophys Acta 1833:1256-1268. doi: 10.1016/j.bbamcr.2013.02.002
2. Tait SW, Green DR (2012) Mitochondria and cell signalling. J Cell Sci 125:807-815. doi: 10.1242/jcs.099234
3. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476:341-345. doi: 10.1038/nature10234
4. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476:336-340. doi: 10.1038/nature10230
5. Pizzo P, Drago I, Filadi R, Pozzan T (2012) Mitochondrial Ca(2)(+) homeostasis: mechanism, role, and tissue specificities. Pflugers Arch 464:3-17. doi: 10.1007/s00424-012-1122-y
6. 2+ transfer to mitochondria. Cell 142:270-283. doi: 10.1016/j.cell.2010.06.007
7. Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25:319-324 (Pubitemid 30421097)
8. Bereiter-Hahn J, Voth M (1994) Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Tech 27:198-219. doi: 10.1002/jemt.1070270303 (Pubitemid 24062014)
9. Campello S, Scorrano L (2010) Mitochondrial shape changes: orchestrating cell pathophysiology. EMBO Rep 11:678-684. doi: 10.1038/embor.2010.115
10. 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 103:2653-2658. doi: 10.1073/pnas.0511154103
11. Li Z, Okamoto K, Hayashi Y, Sheng M (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119:873-887. doi: 10.1016/j.cell.2004.11.003 (Pubitemid 40017692)
12. Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y, Milan G, Masiero E, Del Piccolo P, Foretz M, Scorrano L, Rudolf R, Sandri M (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29:1774-1785. doi: 10.1038/emboj.2010.60
13. Corrado M, Scorrano L, Campello S (2012) Mitochondrial dynamics in cancer and neurodegenerative and neuroinflammatory diseases. Int J Cell Biol 2012:729290. doi: 10.1155/2012/729290
14. Itoh K, Nakamura K, Iijima M, Sesaki H (2013) Mitochondrial dynamics in neurodegeneration. Trends Cell Biol 23:64-71. doi: 10.1016/j.tcb.2012.10.006
15. Ramonet D, Perier C, Recasens A, Dehay B, Bove J, Costa V, Scorrano L, Vila M (2013) Optic atrophy 1 mediates mitochondria remodeling and dopaminergic neurodegeneration linked to complex I deficiency. Cell Death Differ 20:77-85. doi: 10.1038/cdd.2012.95
16. Youle RJ, van der Bliek AM (2012) Mitochondrial fission, fusion, and stress. Science 337:1062-1065. doi: 10.1126/science.1219855
17. Elgass K, Pakay J, Ryan MT, Palmer CS (2013) Recent advances into the understanding of mitochondrial fission. Biochim Biophys Acta 1833:150-161. doi: 10.1016/j.bbamcr.2012.05.002
18. Cribbs JT, Strack S (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 8:939-944. doi: 10.1038/sj.embor.7401062 (Pubitemid 47500477)
19. Cereghetti GM, Stangherlin A, Martins de Brito O, Chang CR, Blackstone C, Bernardi P, Scorrano L (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci USA 105:15803-15808. doi: 10.1073/pnas.0808249105
20. Wasiak S, Zunino R, McBride HM (2007) Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J Cell Biol 177:439-450. doi: 10.1083/jcb.200610042 (Pubitemid 46718273)
21. Guo C, Hildick KL, Luo J, Dearden L, Wilkinson KA, Henley JM (2013) SENP3-mediated deSUMOylation of dynamin-related protein 1 promotes cell death following ischaemia. EMBO J 32:1514-1528. doi: 10.1038/emboj.2013.65
22. Wang H, Song P, Du L, Tian W, Yue W, Liu M, Li D, Wang B, Zhu Y, Cao C, Zhou J, Chen Q (2011) Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J Biol Chem 286:11649-11658. doi: 10.1074/jbc.M110.144238
23. Nakamura N, Kimura Y, Tokuda M, Honda S, Hirose S (2006) MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep 7:1019-1022. doi: 10.1038/sj.embor.7400790 (Pubitemid 44480517)
24. Yonashiro R, Ishido S, Kyo S, Fukuda T, Goto E, Matsuki Y, Ohmura-Hoshino M, Sada K, Hotta H, Yamamura H, Inatome R, Yanagi S (2006) A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J 25:3618-3626. doi: 10.1038/sj.emboj.7601249 (Pubitemid 44264872)
25. Karbowski M, Neutzner A, Youle RJ (2007) The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J Cell Biol 178:71-84. doi: 10.1083/jcb.200611064 (Pubitemid 47026403)
26. Fang L, Hemion C, Goldblum D, Meyer P, Orgul S, Frank S, Flammer J, Neutzner A (2012) Inactivation of MARCH5 prevents mitochondrial fragmentation and interferes with cell death in a neuronal cell model. PLoS ONE 7:e52637. doi: 10.1371/journal.pone.0052637
27. Park YY, Lee S, Karbowski M, Neutzner A, Youle RJ, Cho H (2010) Loss of MARCH5 mitochondrial E3 ubiquitin ligase induces cellular senescence through dynamin-related protein 1 and mitofusin 1. J Cell Sci 123:619-626. doi: 10.1242/jcs.061481
28. Lokireddy S, Wijesoma IW, Teng S, Bonala S, Gluckman PD, McFarlane C, Sharma M, Kambadur R (2012) The ubiquitin ligase Mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli. Cell Metab 16:613-624. doi: 10.1016/j.cmet.2012.10.005
29. Braschi E, Zunino R, McBride HM (2009) MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep 10:748-754. doi: 10.1038/embor.2009.86
30. Yoon Y, Krueger EW, Oswald BJ, McNiven MA (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol 23:5409-5420 (Pubitemid 36950895)
31. Tondera D, Czauderna F, Paulick K, Schwarzer R, Kaufmann J, Santel A (2005) The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J Cell Sci 118:3049-3059. doi: 10.1242/jcs.02415 (Pubitemid 41149909)
32. Karbowski M, Jeong SY, Youle RJ (2004) Endophilin B1 is required for the maintenance of mitochondrial morphology. J Cell Biol 166:1027-1039. doi: 10.1083/jcb.200407046 (Pubitemid 39304766)
33. Pedrola L, Espert A, Wu X, Claramunt R, Shy ME, Palau F (2005) GDAP1, the protein causing Charcot-Marie-Tooth disease type 4A, is expressed in neurons and is associated with mitochondria. Hum Mol Genet 14:1087-1094. doi: 10.1093/hmg/ddi121 (Pubitemid 40575884)
34. Otera H, Wang C, Cleland MM, Setoguchi K, Yokota S, Youle RJ, Mihara K (2010) Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 191:1141-1158. doi: 10.1083/jcb.201007152
35. Zhao J, Liu T, Jin S, Wang X, Qu M, Uhlen P, Tomilin N, Shupliakov O, Lendahl U, Nister M (2011) Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J 30:2762-2778. doi: 10.1038/emboj.2011.198
36. Palmer CS, Elgass KD, Parton RG, Osellame LD, Stojanovski D, Ryan MT (2013) MiD49 and MiD51 can act independently of Mff and Fis1 in Drp1 recruitment and are specific for mitochondrial fission. J Biol Chem. doi: 10.1074/jbc.M113.479873
37. Palmer CS, Osellame LD, Laine D, Koutsopoulos OS, Frazier AE, Ryan MT (2011) MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep 12:565-573. doi: 10.1038/embor.2011.54
38. Lackner LL, Ping H, Graef M, Murley A, Nunnari J (2013) Endoplasmic reticulum-associated mitochondria-cortex tether functions in the distribution and inheritance of mitochondria. Proc Natl Acad Sci USA 110:E458-E467. doi: 10.1073/pnas.1215232110
39. Pon LA (2013) Mitochondrial fission: rings around the organelle. Curr Biol 23:R279-R281. doi: 10.1016/j.cub.2013.02.042
40. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK (2011) ER tubules mark sites of mitochondrial division. Science 334:358-362. doi: 10.1126/science.1207385
41. Korobova F, Ramabhadran V, Higgs HN (2013) An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339:464-467. doi: 10.1126/science.1228360
42. Strack S, Wilson TJ, Cribbs JT (2013) Cyclin-dependent kinases regulate splice-specific targeting of dynamin-related protein 1 to microtubules. J Cell Biol 201:1037-1051. doi: 10.1083/jcb.201210045
43. Rugarli EI, Langer T (2012) Mitochondrial quality control: a matter of life and death for neurons. EMBO J 31:1336-1349. doi: 10.1038/emboj.2012.38
44. Chen H, Chan DC (2010) Physiological functions of mitochondrial fusion. Ann NY Acad Sci 1201:21-25. doi: 10.1111/j.1749-6632.2010.05615.x
45. Chen H, McCaffery JM, Chan DC (2007) Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130:548-562. doi: 10.1016/j.cell.2007.06.026 (Pubitemid 47198302)
46. Rojo M, Legros F, Chateau D, Lombes A (2002) Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J Cell Sci 115:1663-1674 (Pubitemid 34520596)
47. Escobar-Henriques M, Anton F (2013) Mechanistic perspective of mitochondrial fusion: tubulation versus fragmentation. Biochim Biophys Acta 1833:162-175. doi: 10.1016/j.bbamcr.2012.07.016
48. Ishihara N, Eura Y, Mihara K (2004) Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J Cell Sci 117:6535-6546. doi: 10.1242/jcs.01565 (Pubitemid 40214575)
49. Hoppins S, Edlich F, Cleland MM, Banerjee S, McCaffery JM, Youle RJ, Nunnari J (2011) The soluble form of Bax regulates mitochondrial fusion via MFN2 homotypic complexes. Mol Cell 41:150-160. doi: 10.1016/j.molcel.2010.11.030
50. de Brito OM, Scorrano L (2009) Mitofusin-2 regulates mitochondrial and endoplasmic reticulum morphology and tethering: the role of Ras. Mitochondrion 9:222-226. doi: 10.1016/j.mito.2009.02.005
51. Sugiura A, Nagashima S, Tokuyama T, Amo T, Matsuki Y, Ishido S, Kudo Y, McBride HM, Fukuda T, Matsushita N, Inatome R, Yanagi S (2013) MITOL regulates endoplasmic reticulum-mitochondria contacts via mitofusin2. Mol Cell. doi: 10.1016/j.molcel.2013.04.023
52. Eura Y, Ishihara N, Oka T, Mihara K (2006) Identification of a novel protein that regulates mitochondrial fusion by modulating mitofusin (Mfn) protein function. J Cell Sci 119:4913-4925. doi: 10.1242/jcs.03253 (Pubitemid 46017804)
53. Song Z, Chen H, Fiket M, Alexander C, Chan DC (2007) OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 178:749-755. doi: 10.1083/jcb.200704110 (Pubitemid 47347360)
54. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, Craessaerts K, Metzger K, Frezza C, Annaert W, D'Adamio L, Derks C, Dejaegere T, Pellegrini L, D'Hooge R, Scorrano L, De Strooper B (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126:163-175. doi: 10.1016/j.cell.2006.06.021
55. Yang RF, Zhao GW, Liang ST, Zhang Y, Sun LH, Chen HZ, Liu DP (2012) Mitofilin regulates cytochrome c release during apoptosis by controlling mitochondrial cristae remodeling. Biochem Biophys Res Commun 428:93-98. doi: 10.1016/j.bbrc.2012.10.012
56. An HJ, Cho G, Lee JO, Paik SG, Kim YS, Lee H (2013) Higd-1a interacts with Opa1 and is required for the morphological and functional integrity of mitochondria. Proc Natl Acad Sci USA 110:13014-13019. doi: 10.1073/pnas. 1307170110
57. Merkwirth C, Dargazanli S, Tatsuta T, Geimer S, Lower B, Wunderlich FT, von Kleist-Retzow JC, Waisman A, Westermann B, Langer T (2008) Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 22:476-488. doi: 10.1101/gad.460708 (Pubitemid 351272755)
58. Dimmer KS, Navoni F, Casarin A, Trevisson E, Endele S, Winterpacht A, Salviati L, Scorrano L (2008) LETM1, deleted in Wolf-Hirschhorn syndrome is required for normal mitochondrial morphology and cellular viability. Hum Mol Genet 17:201-214. doi: 10.1093/hmg/ddm297
59. Choi SY, Huang P, Jenkins GM, Chan DC, Schiller J, Frohman MA (2006) A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat Cell Biol 8:1255-1262. doi: 10.1038/ncb1487 (Pubitemid 44660590)
60. Saxton WM, Hollenbeck PJ (2012) The axonal transport of mitochondria. J Cell Sci 125:2095-2104. doi: 10.1242/jcs.053850
61. Schwarz TL (2013) Mitochondrial trafficking in neurons. Cold Spring Harb Perspect Biol 5. doi: 10.1101/cshperspect.a011304
62. Misgeld T, Kerschensteiner M, Bareyre FM, Burgess RW, Lichtman JW (2007) Imaging axonal transport of mitochondria in vivo. Nat Methods 4:559-561. doi: 10.1038/nmeth1055 (Pubitemid 47214773)
63. Court FA, Coleman MP (2012) Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci 35:364-372. doi: 10.1016/j.tins.2012.04. 001
64. Arnold B, Cassady SJ, VanLaar VS, Berman SB (2011) Integrating multiple aspects of mitochondrial dynamics in neurons: age-related differences and dynamic changes in a chronic rotenone model. Neurobiol Dis 41:189-200. doi: 10.1016/j.nbd.2010.09.006
65. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27:433-446. doi: 10.1038/sj.emboj.7601963 (Pubitemid 351161653)
66. Maday S, Wallace KE, Holzbaur EL (2012) Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol 196:407-417. doi: 10.1083/jcb.201106120
67. Calkins MJ, Manczak M, Mao P, Shirendeb U, Reddy PH (2011) Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease. Hum Mol Genet 20:4515-4529. doi: 10.1093/hmg/ddr381
68. Pilling AD, Horiuchi D, Lively CM, Saxton WM (2006) Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol Biol Cell 17:2057-2068. doi: 10.1091/mbc.E05-06-0526 (Pubitemid 44011618)
69. Boldogh IR, Pon LA (2007) Mitochondria on the move. Trends Cell Biol 17:502-510. doi: 10.1016/j.tcb.2007.07.008 (Pubitemid 47562767)
70. Hirokawa N, Nitta R, Okada Y (2009) The mechanisms of kinesin motor motility: lessons from the monomeric motor KIF1A. Nat Rev Mol Cell Biol 10:877-884. doi: 10.1038/nrm2807
71. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1:761-772
72. Avila J, Ulloa L, Gonzalez J, Moreno F, Diaz-Nido J (1994) Phosphorylation of microtubule-associated proteins by protein kinase CK2 in neuritogenesis. Cell Mol Biol Res 40:573-579
73. Jimenez-Mateos EM, Gonzalez-Billault C, Dawson HN, Vitek MP, Avila J (2006) Role of MAP1B in axonal retrograde transport of mitochondria. Biochem J 397:53-59. doi: 10.1042/BJ20060205 (Pubitemid 44032836)
74. Stroissnigg H, Trancikova A, Descovich L, Fuhrmann J, Kutschera W, Kostan J, Meixner A, Nothias F, Propst F (2007) S-nitrosylation of microtubule-associated protein 1B mediates nitric-oxide-induced axon retraction. Nat Cell Biol 9:1035-1045. doi: 10.1038/ncb1625 (Pubitemid 47338143)
75. Yonashiro R, Kimijima Y, Shimura T, Kawaguchi K, Fukuda T, Inatome R, Yanagi S (2012) Mitochondrial ubiquitin ligase MITOL blocks S-nitrosylated MAP1B-light chain 1-mediated mitochondrial dysfunction and neuronal cell death. Proc Natl Acad Sci USA 109:2382-2387. doi: 10.1073/pnas.1114985109
76. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143:777-794 (Pubitemid 28512571)
77. Mandelkow EM, Stamer K, Vogel R, Thies E, Mandelkow E (2003) Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol Aging 24:1079-1085 (Pubitemid 37487885)
78. Johnson GV, Stoothoff WH (2004) Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117:5721-5729. doi: 10.1242/jcs.01558 (Pubitemid 40123939)
79. Shahpasand K, Uemura I, Saito T, Asano T, Hata K, Shibata K, Toyoshima Y, Hasegawa M, Hisanaga S (2012) Regulation of mitochondrial transport and inter-microtubule spacing by tau phosphorylation at the sites hyperphosphorylated in Alzheimer's disease. J Neurosci 32:2430-2441. doi: 10.1523/JNEUROSCI.5927-11.2012
80. Shao CY, Zhu J, Xie YJ, Wang Z, Wang YN, Wang Y, Su LD, Zhou L, Zhou TH, Shen Y (2013) Distinct Functions of Nuclear Distribution Proteins LIS1, Ndel1 and NudCL in Regulating Axonal Mitochondrial Transport. Traffic 14:785-797. doi: 10.1111/tra.12070
81. Brickley K, Stephenson FA (2011) Trafficking kinesin protein (TRAK)-mediated transport of mitochondria in axons of hippocampal neurons. J Biol Chem 286:18079-18092. doi: 10.1074/jbc.M111.236018
82. Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61:541-555. doi: 10.1016/j.neuron.2009.01.030
83. Glater EE, Megeath LJ, Stowers RS, Schwarz TL (2006) Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J Cell Biol 173:545-557. doi: 10.1083/jcb.200601067 (Pubitemid 43765201)
84. Kang JS, Tian JH, Pan PY, Zald P, Li C, Deng C, Sheng ZH (2008) Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 132:137-148. doi: 10.1016/j.cell.2007.11.024
85. Courchet J, Lewis TLJ, Lee S, Courchet V, Liou DY, Aizawa S, Polleux F (2013) Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell 153:1510-1525. doi: 10.1016/j.cell.2013.05.021
86. 2+ -dependent regulation of kinesin-mediated mitochondrial motility. Cell 136:163-174. doi: 10.1016/j.cell.2008.11.046
87. Wang X, Winter D, Ashrafi G, Schlehe J, Wong YL, Selkoe D, Rice S, Steen J, LaVoie MJ, Schwarz TL (2011) PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147:893-906. doi: 10.1016/j.cell.2011.10.018
88. Dagda RK, Cherra SJ, Kulich SM, Tandon A, Park D, Chu CT (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 284:13843-13855. doi: 10.1074/jbc.M808515200
89. Matenia D, Hempp C, Timm T, Eikhof A, Mandelkow EM (2012) Microtubule affinity-regulating kinase 2 (MARK2) turns on phosphatase and tensin homolog (PTEN)-induced kinase 1 (PINK1) at Thr-313, a mutation site in Parkinson disease: effects on mitochondrial transport. J Biol Chem 287:8174-8186. doi: 10.1074/jbc.M111.262287
90. Mandelkow EM, Thies E, Trinczek B, Biernat J, Mandelkow E (2004) MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J Cell Biol 167:99-110. doi: 10.1083/jcb.200401085 (Pubitemid 39363418)
91. Thies E, Mandelkow EM (2007) Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J Neurosci 27:2896-2907. doi: 10.1523/JNEUROSCI.4674-06.2007 (Pubitemid 46438993)
92. Fransson S, Ruusala A, Aspenstrom P (2006) The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem Biophys Res Commun 344:500-510. doi: 10.1016/j.bbrc.2006.03.163
93. 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 (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11:958-966. doi: 10.1038/ncb1907
94. Pham AH, Meng S, Chu QN, Chan DC (2012) Loss of Mfn2 results in progressive, retrograde degeneration of dopaminergic neurons in the nigrostriatal circuit. Hum Mol Genet 21:4817-4826. doi: 10.1093/hmg/dds311
95. Campello S, Lacalle RA, Bettella M, Manes S, Scorrano L, Viola A (2006) Orchestration of lymphocyte chemotaxis by mitochondrial dynamics. J Exp Med 203:2879-2886. doi: 10.1084/jem.20061877 (Pubitemid 46026165)
96. Zhao J, Zhang J, Yu M, Xie Y, Huang Y, Wolff DW, Abel PW, Tu Y (2012) Mitochondrial dynamics regulates migration and invasion of breast cancer cells. Oncogene. doi: 10.1038/onc.2012.494
97. Desai SP, Bhatia SN, Toner M, Irimia D (2013) Mitochondrial localization and the persistent migration of epithelial cancer cells. Biophys J 104:2077-2088. doi: 10.1016/j.bpj.2013.03.025
98. Condeelis JS, Wyckoff JB, Bailly M, Pestell R, Lawrence D, Backer J, Segall JE (2001) Lamellipodia in invasion. Semin Cancer Biol 11:119-128. doi: 10.1006/scbi 2000.0363 (Pubitemid 32423287)
99. Anesti V, Scorrano L (2006) The relationship between mitochondrial shape and function and the cytoskeleton. Biochim Biophys Acta 1757:692-699. doi: 10.1016/j.bbabio.2006.04.013 (Pubitemid 43993860)
100. Krementsov DN, Krementsova EB, Trybus KM (2004) Myosin V: regulation by calcium, calmodulin, and the tail domain. J Cell Biol 164:877-886. doi: 10.1083/jcb.200310065 (Pubitemid 38366899)
101. Pathak D, Sepp KJ, Hollenbeck PJ (2010) Evidence that myosin activity opposes microtubule-based axonal transport of mitochondria. J Neurosci 30:8984-8992. doi: 10.1523/JNEUROSCI.1621-10.2010