Miro sculpts mitochondrial dynamics in neuronal health and disease

Neurobiology of Disease

Volumn 90, Issue , 2016, Pages 27-34

  Devine, Michael J ^a   Birsa, Nicol ^a   Kittler, Josef T ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Calcium sensing; Miro; Mitochondria; Mitophagy; Trafficking

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE TRIPHOSPHATE; CALCIUM ION; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; MITOCHONDRIAL RHO GTPASE MIRO1; MITOCHONDRIAL RHO GTPASE MIRO2; MOLECULAR MOTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL TRANSPORT; DISEASE ASSOCIATION; HEALTH; HOMEOSTASIS; HUMAN; INTRACELLULAR SIGNALING; MIRO SIGNALLING DOMAIN; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL TRANSPORT; MITOPHAGY; MOLECULAR DYNAMICS; NEUROLOGIC DISEASE; NEURONAL HEALTH; NEURONAL HOMEOSTASIS; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; REVIEW; ANIMAL; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; HUMANS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; NEURONS; RHO GTP-BINDING PROTEINS;

EID: 84953232985     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.12.008     Document Type: Review

References (99)

1. Abou-Sleiman P.M., Muqit M.M.K., Wood N.W. Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat. Rev. Neurosci. 2006, 7:207-219. 10.1038/nrn1868.
2. Ashrafi G., Schlehe J.S., Lavoie M.J., Schwarz T.L. Mitophagy of damaged mitochondria occurs locally in distal neuronal axons and requires PINK1 and Parkin. J. Cell Biol. 2014, 206:655-670. 10.1083/jcb.201401070.
3. Atkin T.A., MacAskill A.F., Brandon N.J., Kittler J.T. Disrupted in schizophrenia-1 regulates intracellular trafficking of mitochondria in neurons. Mol. Psychiatry 2011, 16. (122-4- 121). 10.1038/mp.2010.110.
4. Babic M., Russo G.J., Wellington A.J., Sangston R.M., Gonzalez M., Zinsmaier K.E. Miro's N-terminal GTPase domain is required for transport of mitochondria into axons and dendrites. J. Neurosci. 2015, 35:5754-5771. 10.1523/JNEUROSCI.1035-14.2015.
5. Baughman J.M., Perocchi F., Girgis H.S., Plovanich M., Belcher-Timme C.A., Sancak Y., Bao X.R., Strittmatter L., Goldberger O., Bogorad R.L., Koteliansky V., Mootha V.K. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476:341-345. 10.1038/nature10234.
6. Birsa N., Norkett R., Wauer T., Mevissen T.E.T., Wu H.-C., Foltynie T., Bhatia K., Hirst W.D., Komander D., Plun-Favreau H., Kittler J.T. Lysine 27 ubiquitination of the mitochondrial transport protein Miro is dependent on serine 65 of the Parkin ubiquitin ligase. J. Biol. Chem. 2014, 289:14569-14582. 10.1074/jbc.M114.563031.
7. Brickley K., Stephenson F.A. Trafficking kinesin protein (TRAK)-mediated transport of mitochondria in axons of hippocampal neurons. J. Biol. Chem. 2011, 286:18079-18092. 10.1074/jbc.M111.236018.
8. Brickley K., Smith M.J., Beck M., Stephenson F.A. GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J. Biol. Chem. 2005, 280:14723-14732. 10.1074/jbc.M409095200.
9. Cai Q., Gerwin C., Sheng Z.-H. Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J. Cell Biol. 2005, 170:959-969. 10.1083/jcb.200506042.
10. Chada S.R., Hollenbeck P.J. Mitochondrial movement and positioning in axons: the role of growth factor signaling. J. Exp. Biol. 2003, 206:1985-1992. 10.1242/jeb.00263.
11. Chan N.C., Salazar A.M., Pham A.H., Sweredoski M.J., Kolawa N.J., Graham R.L.J., Hess S., Chan D.C. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum. Mol. Genet. 2011, 20:1726-1737. 10.1093/hmg/ddr048.
12. 2+ as an intrinsic signal regulating mitochondrial motility in axons. Proc. Natl. Acad. Sci. 2011, 108:15456-15461. 10.1073/pnas.1106862108.
13. Chen Y., Sheng Z.-H. Kinesin-1-syntaphilin coupling mediates activity-dependent regulation of axonal mitochondrial transport. J. Cell Biol. 2013, 202:351-364. 10.1083/jcb.201302040.
14. Cho K.-I., Cai Y., Yi H., Yeh A., Aslanukov A., Ferreira P.A. Association of the kinesin-binding domain of RanBP2 to KIF5B and KIF5C determines mitochondria localization and function. Traffic 2007, 8:1722-1735. 10.1111/j.1600-0854.2007.00647.x.
15. De Stefani D., Raffaello A., Teardo E., Szabò I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340. 10.1038/nature10230.
16. De Vos K.J., Mórotz G.M., Stoica R., Tudor E.L., Lau K.-F., Ackerley S., Warley A., Shaw C.E., Miller C.C.J. VAPB interacts with the mitochondrial protein PTPIP51 to regulate calcium homeostasis. Hum. Mol. Genet. 2012, 21:1299-1311. 10.1093/hmg/ddr559.
17. Deas E., Wood N.W., Plun-Favreau H. Mitophagy and Parkinson's disease: the PINK1-parkin link. Biochim. Biophys. Acta (BBA) - Mol. Cell Res. 2011, 1813:623-633. 10.1016/j.bbamcr.2010.08.007.
18. Ferree A.W., Trudeau K., Zik E., Benador I.Y., Twig G., Gottlieb R.A., Shirihai O.S. MitoTimer probe reveals the impact of autophagy, fusion, and motility on subcellular distribution of young and old mitochondrial protein and on relative mitochondrial protein age. Autophagy 2013, 9:1887-1896. 10.4161/auto.26503.
19. Fransson A., Ruusala A., Aspenstrom P. Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J. Biol. Chem. 2003, 278:6495-6502. 10.1074/jbc.M208609200.
20. Fransson A., Ruusala A., Aspenstrom P. The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem. Biophys. Res. Commun. 2006, 344:500-510. 10.1016/j.bbrc.2006.03.163.
21. Frederick R.L., Shaw J.M. Moving mitochondria: establishing distribution of an essential organelle. Traffic 2007, 8:1668-1675. 10.1111/j.1600-0854.2007.00644.x.
22. Frederick R.L., McCaffery J.M., Cunningham K.W., Okamoto K., Shaw J.M. Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J. Cell Biol. 2004, 167:87-98. 10.1083/jcb.200405100.
23. Fujita T., Maturana A.D., Ikuta J., Hamada J., Walchli S., Suzuki T., Sawa H., Wooten M.W., Okajima T., Tatematsu K., Tanizawa K., Kuroda S. Axonal guidance protein FEZ1 associates with tubulin and kinesin motor protein to transport mitochondria in neurites of NGF-stimulated PC12 cells. Biochem. Biophys. Res. Commun. 2007, 361:605-610. 10.1016/j.bbrc.2007.07.050.
24. Geisler S., Holmström K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J., Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12:119-131. 10.1038/ncb2012.
25. Giot L., Bader J.S., Brouwer C., Chaudhuri A., Kuang B., Li Y., Hao Y.L., Ooi C.E., Godwin B., Vitols E., Vijayadamodar G., Pochart P., Machineni H., Welsh M., Kong Y., Zerhusen B., Malcolm R., Varrone Z., Collis A., Minto M., Burgess S., McDaniel L., Stimpson E., Spriggs F., Williams J., Neurath K., Ioime N., Agee M., Voss E., Furtak K., Renzulli R., Aanensen N., Carrolla S., Bickelhaupt E., Lazovatsky Y., DaSilva A., Zhong J., Stanyon C.A., Finley R.L., White K.P., Braverman M., Jarvie T., Gold S., Leach M., Knight J., Shimkets R.A., McKenna M.P., Chant J., Rothberg J.M. A protein interaction map of Drosophila melanogaster. Science 2003, 302:1727-1736. 10.1126/science.1090289.
26. Glater E.E., Megeath L.J., Stowers R.S., Schwarz T.L. Axonal transport of mitochondria requires Milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol. 2006, 173:545-557. 10.1083/jcb.200601067.
27. Grishin A., Li H., Levitan E.S., Zaks-Makhina E. Identification of gamma-aminobutyric acid receptor-interacting factor 1 (TRAK2) as a trafficking factor for the K+ channel Kir2.1. J. Biol. Chem. 2006, 281:30104-30111. 10.1074/jbc.M602439200.
28. Guo X., Macleod G.T., Wellington A., Hu F., Panchumarthi S., Schoenfield M., Marin L., Charlton M.P., Atwood H.L., Zinsmaier K.E. The GTPase dMiro is required for axonal transport of mitochondria to drosophila synapses. Neuron 2005, 47:379-393. 10.1016/j.neuron.2005.06.027.
29. Hardy J. Genetic analysis of pathways to Parkinson disease. Neuron 2010, 68:201-206.
30. Harris J.J., Jolivet R., Attwell D. Synaptic energy use and supply. Neuron 2012, 75:762-777. 10.1016/j.neuron.2012.08.019.
31. Hirokawa N., Takemura R. Molecular motors and mechanisms of directional transport in neurons. Nat. Rev. Neurosci. 2005, 6:201-214. 10.1038/nrn1624.
32. Hirokawa N., Sato-Yoshitake R., Yoshida T., Kawashima T. Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J. Cell Biol. 1990, 111:1027-1037. 10.1083/jcb.111.3.1027.
33. Hirokawa N., Sato-Yoshitake R., Kobayashi N., Pfister K.K., Bloom G.S., Brady S.T. Kinesin associates with anterogradely transported membranous organelles in vivo. J. Cell Biol. 1991, 114:295-302. 10.1083/jcb.114.2.295.
34. Hollenbeck P.J., Saxton W.M. The axonal transport of mitochondria. J. Cell Sci. 2005, 118:5411-5419. 10.1242/jcs.02745.
35. Horiuchi D., Barkus R.V., Pilling A.D., Gassman A., Saxton W.M. APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in drosophila. Curr. Biol. 2005, 15:2137-2141. 10.1016/j.cub.2005.10.047.
36. Iijima-Ando K., Sekiya M., Maruko-Otake A., Ohtake Y., Suzuki E., Lu B., Iijima K.M. Loss of axonal mitochondria promotes tau-mediated neurodegeneration and Alzheimer's disease-related tau phosphorylation via PAR-1. PLoS Genet. 2012, 8:e1002918. 10.1371/journal.pgen.1002918.
37. Ikuta J., Maturana A., Fujita T., Okajima T., Tatematsu K., Tanizawa K., Kuroda S. Fasciculation and elongation protein zeta-1 (FEZ1) participates in the polarization of hippocampal neuron by controlling the mitochondrial motility. Biochem. Biophys. Res. Commun. 2007, 353:127-132. 10.1016/j.bbrc.2006.11.142.
38. Iyer S.P.N., Akimoto Y., Hart G.W. Identification and cloning of a novel family of coiled-coil domain proteins that interact with O-GlcNAc transferase. J. Biol. Chem. 2003, 278:5399-5409. 10.1074/jbc.M209384200.
39. Jouaville L.S., Pinton P., Bastianutto C., Rutter G.A., Rizzuto R. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13807-13812. 10.1073/pnas.96.24.13807.
40. Kalia L.V., Lang A.E. Parkinson's disease. Lancet 2015, 386:896-912. 10.1016/S0140-6736(14)61393-3.
41. Kane L.A., Lazarou M., Fogel A.I., Li Y., Yamano K., Sarraf S.A., Banerjee S., Youle R.J. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 2014, 205:143-153. 10.1083/jcb.201402104.
42. Kang J.-S., Tian J.-H., Pan P.-Y., Zald P., Li C., Deng C., Sheng Z.-H. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 2008, 132:137-148. 10.1016/j.cell.2007.11.024.
43. Kazlauskaite A., Kelly V., Johnson C., Baillie C., Hastie C.J., Peggie M., Macartney T., Woodroof H.I., Alessi D.R., Pedrioli P.G.A., Muqit M.M.K. Phosphorylation of Parkin at Serine65 is essential for activation: elaboration of a Miro1 substrate-based assay of Parkin E3 ligase activity. Open Biol. 2014, 4:130213. 10.1098/rsob.130213.
44. Kirk E., Chin L.-S., Li L. GRIF1 binds Hrs and is a new regulator of endosomal trafficking. J. Cell Sci. 2006, 119:4689-4701. 10.1242/jcs.03249.
45. Klosowiak J.L., Focia P.J., Chakravarthy S., Landahl E.C., Freymann D.M., Rice S.E. Structural coupling of the EF hand and C-terminal GTPase domains in the mitochondrial protein Miro. EMBO Rep. 2013, 14:968-974. 10.1038/embor.2013.151.
46. Kondapalli C., Kazlauskaite A., Zhang N., Woodroof H.I., Campbell D.G., Gourlay R., Burchell L., Walden H., Macartney T.J., Deak M., Knebel A., Alessi D.R., Muqit M.M.K. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol. 2012, 2:120080. 10.1098/rsob.120080.
47. Koutsopoulos O.S., Laine D., Osellame L., Chudakov D.M., Parton R.G., Frazier A.E., Ryan M.T. Human Miltons associate with mitochondria and induce microtubule-dependent remodeling of mitochondrial networks. Biochim. Biophys. Acta 2010, 1803:564-574. 10.1016/j.bbamcr.2010.03.006.
48. Koyano F., Okatsu K., Kosako H., Tamura Y., Go E., Kimura M., Kimura Y., Tsuchiya H., Yoshihara H., Hirokawa T., Endo T., Fon E.A., Trempe J.-F., Saeki Y., Tanaka K., Matsuda N. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 2014, 510:162-166. 10.1038/nature13392.
49. Li Y., Lim S., Hoffman D., Aspenstrom P., Federoff H.J., Rempe D.A. HUMMR, a hypoxia- and HIF-1alpha-inducible protein, alters mitochondrial distribution and transport. J. Cell Biol. 2009, 185:1065-1081. 10.1083/jcb.200811033.
50. Liu S., Sawada T., Lee S., Yu W., Silverio G., Alapatt P., Millan I., Shen A., Saxton W., Kanao T., Takahashi R., Hattori N., Imai Y., Lu B. Parkinson's disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet. 2012, 8:e1002537. 10.1371/journal.pgen.1002537.
51. Lopez-Domenech G., Serrat R., Mirra S., D'Aniello S., Somorjai I., Abad A., Vitureira N., García-Arumí E., Alonso M.T., Rodriguez-Prados M., Burgaya F., Andreu A.L., García-Sancho J., Trullas R., Garcia-Fernàndez J., Soriano E. The Eutherian Armcx genes regulate mitochondrial trafficking in neurons and interact with Miro and Trak2. Nat. Commun. 2012, 3:814. 10.1038/ncomms1829.
52. Loss O., Stephenson F.A. Localization of the kinesin adaptor proteins trafficking kinesin proteins 1 and 2 in primary cultures of hippocampal pyramidal and cortical neurons. J. Neurosci. Res. 2015, 93:1056-1066. 10.1002/jnr.23549.
53. MacAskill A.F., Kittler J.T. Control of mitochondrial transport and localization in neurons. Trends Cell Biol. 2010, 20:102-112. 10.1016/j.tcb.2009.11.002.
54. MacAskill A.F., Brickley K., Stephenson F.A., Kittler J.T. GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol. Cell. Neurosci. 2009, 40:301-312. 10.1016/j.mcn.2008.10.016.
55. MacAskill A.F., Rinholm J.E., Twelvetrees A.E., Arancibia-Carcamo I.L., Muir J., Fransson A., Aspenstrom P., Attwell D., Kittler J.T. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 2009, 61:541-555. 10.1016/j.neuron.2009.01.030.
56. MacAskill A.F., Atkin T.A., Kittler J.T. Mitochondrial trafficking and the provision of energy and calcium buffering at excitatory synapses. Eur. J. Neurosci. 2010, 32:231-240. 10.1111/j.1460-9568.2010.07345.x.
57. Martin M., Iyadurai S.J., Gassman A., Gindhart J.G., Hays T.S., Saxton W.M. Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol. Biol. Cell 1999, 10:3717-3728. 10.1091/mbc.10.11.3717.
58. 2+ in signal transduction in mammalian tissues. Biochim. Biophys. Acta 1990, 1018:287-291.
59. Miller K.E., Sheetz M.P. Axonal mitochondrial transport and potential are correlated. J. Cell Sci. 2004, 117:2791-2804. 10.1242/jcs.01130.
60. Misgeld T., Kerschensteiner M., Bareyre F.M., Burgess R.W., Lichtman J.W. Imaging axonal transport of mitochondria in vivo. Nat. Methods 2007, 4:559-561. 10.1038/nmeth1055.
61. Misko A., Jiang S., Wegorzewska I., Milbrandt J., Baloh R.H. Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 2010, 30:4232-4240. 10.1523/JNEUROSCI.6248-09.2010.
62. Morris R.L., Hollenbeck P.J. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 1995, 131:1315-1326. 10.1083/jcb.131.5.1315.
63. Nangaku M., Sato-Yoshitake R., Okada Y., Noda Y., Takemura R., Yamazaki H., Hirokawa N. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 1994, 79:1209-1220.
64. Nguyen T.T., Oh S.S., Weaver D., Lewandowska A., Maxfield D., Schuler M.-H., Smith N.K., Macfarlane J., Saunders G., Palmer C.A., Debattisti V., Koshiba T., Pulst S., Feldman E.L., Hajnóczky G., Shaw J.M. Loss of Miro1-directed mitochondrial movement results in a novel murine model for neuron disease. Proc. Natl. Acad. Sci. 2014, 111:E3631-E3640. 10.1073/pnas.1402449111.
65. Ogawa F., Malavasi E.L.V., Crummie D.K., Eykelenboom J.E., Soares D.C., Mackie S., Porteous D.J., Millar J.K. DISC1 complexes with TRAK1 and Miro1 to modulate anterograde axonal mitochondrial trafficking. Hum. Mol. Genet. 2014, 23:906-919. 10.1093/hmg/ddt485.
66. Pekkurnaz G., Trinidad J.C., Wang X., Kong D., Schwarz T.L. Glucose regulates mitochondrial motility via Milton modification by O-GlcNAc transferase. Cell 2014, 158:54-68. 10.1016/j.cell.2014.06.007.
67. Pilling A.D., Horiuchi D., Lively C.M., Saxton W.M. Kinesin-1 and dynein are the primary motors for fast transport of mitochondria in drosophila motor axons. Mol. Biol. Cell 2006, 17:2057-2068. 10.1091/mbc.E05-06-0526.
68. Plucińska G., Paquet D., Hruscha A., Godinho L., Haass C., Schmid B., Misgeld T. In vivo imaging of disease-related mitochondrial dynamics in a vertebrate model system. J. Neurosci. 2012, 32:16203-16212. 10.1523/JNEUROSCI.1327-12.2012.
69. Poole A.C., Thomas R.E., Yu S., Vincow E.S., Pallanck L. The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway. PLoS One 2010, 5:e10054. 10.1371/journal.pone.0010054.
70. Quintero O.A., DiVito M.M., Adikes R.C., Kortan M.B., Case L.B., Lier A.J., Panaretos N.S., Slater S.Q., Rengarajan M., Feliu M., Cheney R.E. Human Myo19 is a novel myosin that associates with mitochondria. Curr. Biol. 2009, 19:2008-2013. 10.1016/j.cub.2009.10.026.
71. Russo G.J., Louie K., Wellington A., Macleod G.T., Hu F., Panchumarthi S., Zinsmaier K.E. Drosophila Miro is required for both anterograde and retrograde axonal mitochondrial transport. J. Neurosci. 2009, 29:5443-5455. 10.1523/JNEUROSCI.5417-08.2009.
72. Sajic M., Mastrolia V., Lee C.Y., Trigo D., Sadeghian M., Mosley A.J., Gregson N.A., Duchen M.R., Smith K.J. Impulse conduction increases mitochondrial transport in adult mammalian peripheral nerves in vivo. PLoS Biol. 2013, 11:e1001754. 10.1371/journal.pbio.1001754.
73. 2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc. Natl. Acad. Sci. 2008, 105:20728-20733. 10.1073/pnas.0808953105.
74. Sarraf S.A., Raman M., Guarani-Pereira V., Sowa M.E., Huttlin E.L., Gygi S.P., Harper J.W. Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 2013, 496:372-376. 10.1038/nature12043.
75. Saxton W.M., Hollenbeck P.J. The axonal transport of mitochondria. J. Cell Sci. 2012, 125:2095-2104. 10.1242/jcs.053850.
76. Schiavo G., Greensmith L., Hafezparast M., Fisher E.M.C. Cytoplasmic dynein heavy chain: the servant of many masters. Trends Neurosci. 2013, 36:641-651. 10.1016/j.tins.2013.08.001.
77. Sepulveda-Falla D., Barrera-Ocampo A., Hagel C., Korwitz A., Vinueza-Veloz M.F., Zhou K., Schonewille M., Zhou H., Velazquez-Perez L., Rodriguez-Labrada R., Villegas A., Ferrer I., Lopera F., Langer T., De Zeeuw C.I., Glatzel M. Familial Alzheimer's disease-associated presenilin-1 alters cerebellar activity and calcium homeostasis. J. Clin. Invest. 2014, 124:1552-1567. 10.1172/JCI66407.
78. Serrat R., Mirra S., Figueiro-Silva J., Navas-Pérez E., Quevedo M., López-Doménech G., Podlesniy P., Ulloa F., Garcia-Fernàndez J., Trullas R., Soriano E. The Armc10/SVH gene: genome context, regulation of mitochondrial dynamics and protection against Aβ-induced mitochondrial fragmentation. Cell Death Dis. 2014, 5:e1163. 10.1038/cddis.2014.121.
79. Smith M.J., Pozo K., Brickley K., Stephenson F.A. Mapping the GRIF-1 binding domain of the kinesin, KIF5C, substantiates a role for GRIF-1 as an adaptor protein in the anterograde trafficking of cargoes. J. Biol. Chem. 2006, 281:27216-27228. 10.1074/jbc.M600522200.
80. Stowers R.S., Megeath L.J., Górska-Andrzejak J., Meinertzhagen I.A., Schwarz T.L. Axonal transport of mitochondria to synapses depends on Milton, a novel drosophila protein. Neuron 2002, 36:1063-1077.
81. Susalka S.J., Pfister K.K. Cytoplasmic dynein subunit heterogeneity: implications for axonal transport. J. Neurocytol. 2000, 29:819-829.
82. Suzuki M., Danilchanka O., Mekalanos J.J. Vibrio cholerae T3SS effector VopE modulates mitochondrial dynamics and innate immune signaling by targeting Miro GTPases. Cell Host Microbe 2014, 16:581-591. 10.1016/j.chom.2014.09.015.
83. 2+ signaling. Physiology 2008, 23:84-94. 10.1152/physiol.00046.2007.
84. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 1998, 93:1147-1158.
85. Tanaka K., Sugiura Y., Ichishita R., Mihara K., Oka T. KLP6: a newly identified kinesin that regulates the morphology and transport of mitochondria in neuronal cells. J. Cell Sci. 2011, 124:2457-2465. 10.1242/jcs.086470.
86. Trinidad J.C., Barkan D.T., Gulledge B.F., Thalhammer A., Sali A., Schoepfer R., Burlingame A.L. Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol. Cell. Proteomics 2012, 11:215-229. 10.1074/mcp.O112.018366.
87. Tsai P.-I., Course M.M., Lovas J.R., Hsieh C.-H., Babic M., Zinsmaier K.E., Wang X. PINK1-mediated phosphorylation of Miro inhibits synaptic growth and protects dopaminergic neurons in drosophila. Sci. Rep. 2014, 4:6962. 10.1038/srep06962.
88. van Spronsen M., Mikhaylova M., Lipka J., Schlager M.A., van den Heuvel D.J., Kuijpers M., Wulf P.S., Keijzer N., Demmers J., Kapitein L.C., Jaarsma D., Gerritsen H.C., Akhmanova A., Hoogenraad C.C. TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron 2013, 77:485-502. 10.1016/j.neuron.2012.11.027.
89. 2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009, 136:163-174. 10.1016/j.cell.2008.11.046.
90. Wang X., Winter D., Ashrafi G., Schlehe J., Wong Y.L., Selkoe D., Rice S., Steen J., Lavoie M.J., Schwarz T.L. PINK1 and parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 2011, 147:893-906. 10.1016/j.cell.2011.10.018.
91. Wang H., Song P., Du L., Tian W., Yue W., Liu M., Li D., Wang B., Zhu Y., Cao C., Zhou J., Chen Q. Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J. Biol. Chem. 2011, 286:11649-11658. 10.1074/jbc.M110.144238.
92. Wauer T., Simicek M., Schubert A., Komander D. Mechanism of phospho-ubiquitin-induced PARKIN activation. Nature 2015, 524:370-374. 10.1038/nature14879.
93. Webber E., Li L., Chin L.-S. Hypertonia-associated protein Trak1 is a novel regulator of endosome-to-lysosome trafficking. J. Mol. Biol. 2008, 382:638-651. 10.1016/j.jmb.2008.07.045.
94. Weihofen A., Thomas K.J., Ostaszewski B.L., Cookson M.R., Selkoe D.J. Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking. Biochemistry 2009, 48:2045-2052. 10.1021/bi8019178.
95. Wells L., Vosseller K., Hart G.W. A role for N-acetylglucosamine as a nutrient sensor and mediator of insulin resistance. Cell. Mol. Life Sci. 2003, 60:222-228.
96. Yoshii S.R., Kishi C., Ishihara N., Mizushima N. Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J. Biol. Chem. 2011, 286:19630-19640. 10.1074/jbc.M110.209338.
97. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117. 10.1038/35052055.
98. Zhang F., Wang W., Siedlak S.L., Liu Y., Liu J., Jiang K., Perry G., Zhu X., Wang X. Miro1 deficiency in amyotrophic lateral sclerosis. Front. Aging Neurosci. 2015, 7:100. 10.3389/fnagi.2015.00100.
99. Ziviani E., Tao R.N., Whitworth A.J. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. 2010, 107:5018-5023. 10.1073/pnas.0913485107.