GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons

Molecular and Cellular Neuroscience

Volumn 40, Issue 3, 2009, Pages 301-312

  MacAskill, Andrew F ^a   Brickley, Kieran ^b   Stephenson, F Anne ^b   Kittler, Josef T ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

GTPase; Mitochondria; Neuron; Signalling; Trafficking

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR INTERACTING FACTOR 1; ADAPTOR PROTEIN; KINESIN; MITOCHONDRIAL RHO GUANINE NUCLEOTIDE BINDING PROTEIN 1; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BRAIN NERVE CELL; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

ANIMALS; CARRIER PROTEINS; CELL LINE; GTP PHOSPHOHYDROLASES; HIPPOCAMPUS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR MOTOR PROTEINS; NERVE TISSUE PROTEINS; NEURONS; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 60149097713     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.10.016     Document Type: Article

References (46)

1. Alexander C., Votruba M., Pesch U.E., Thiselton D.L., Mayer S., Moore A., Rodriguez M., Kellner U., Leo-Kottler B., Auburger G., Bhattacharya S.S., and Wissinger B. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26 (2000) 211-215
2. Baloh R.H., Schmidt R.E., Pestronk A., and Milbrandt J. Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J. Neurosci. 27 (2007) 422-430
3. Beck M., Brickley K., Wilkinson H.L., Sharma S., Smith M., Chazot P.L., Pollard S., and Stephenson F.A. Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J. Biol. Chem. 277 (2002) 30079-30090
4. Bernardi P., Petronilli V., Di Lisa F., and Forte M. A mitochondrial perspective on cell death. Trends Biochem. Sci. 26 (2001) 112-117
5. Brickley K., Smith M.J., Beck M., and 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. 280 (2005) 14723-14732
6. Brodin L., Bakeeva L., and Shupliakov O. Presynaptic mitochondria and the temporal pattern of neurotransmitter release. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354 (1999) 365-372
7. Cai Q., Gerwin C., and Sheng Z.H. Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J. Cell Biol. 170 (2005) 959-969
8. Cai Q., Pan P.Y., and Sheng Z.H. Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J. Neurosci. 27 (2007) 7284-7296
9. Chada S.R., and Hollenbeck P.J. Mitochondrial movement and positioning in axons: the role of growth factor signaling. J. Exp. Biol. 206 (2003) 1985-1992
10. Chan D.C. Mitochondria: dynamic organelles in disease, aging, and development. Cell 125 (2006) 1241-1252
11. Chang D.T., Honick A.S., and Reynolds I.J. Mitochondrial trafficking to synapses in cultured primary cortical neurons. J. Neurosci. 26 (2006) 7035-7045
12. Chen H., and Chan D.C. Critical dependence of neurons on mitochondrial dynamics. Curr. Opin. Cell Biol. 18 (2006) 453-459
13. Choi S.Y., Huang P., Jenkins G.M., Chan D.C., Schiller J., and Frohman M.A. A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat. Cell Biol. 8 (2006) 1255-1262
14. Darcy K.J., Staras K., Collinson L.M., and Goda Y. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat. Neurosci. 9 (2006) 315-321
15. David G., and Barrett E.F. Stimulation-evoked increases in cytosolic [Ca(2+)] in mouse motor nerve terminals are limited by mitochondrial uptake and are temperature-dependent. J. Neurosci. 20 (2000) 7290-7296
16. Davis A.F., and Clayton D.A. In situ localization of mitochondrial DNA replication in intact mammalian cells. J. Cell Biol. 135 (1996) 883-893
17. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., and Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1 (2001) 515-525
18. Fransson A., Ruusala A., and Aspenstrom P. Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J. Biol. Chem. 278 (2003) 6495-6502
19. Fransson S., Ruusala A., and Aspenstrom P. The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem. Biophys. Res. Commun. 344 (2006) 500-510
20. Frederick R.L., McCaffery J.M., Cunningham K.W., Okamoto K., and Shaw J.M. Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J. Cell Biol. 167 (2004) 87-98
21. Glater E.E., Megeath L.J., Stowers R.S., and Schwarz T.L. Axonal transport of mitochondria requires Milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol. 173 (2006) 545-557
22. Gorska-Andrzejak J., Stowers R.S., Borycz J., Kostyleva R., Schwarz T.L., and Meinertzhagen I.A. Mitochondria are redistributed in Drosophila photoreceptors lacking Milton, a kinesin-associated protein. J. Comp. Neurol. 463 (2003) 372-388
23. Goslin, K., Banker, G., 1991. Culturing Nerve Cells.
24. Guo X., Macleod G.T., Wellington A., Hu F., Panchumarthi S., Schoenfield M., Marin L., Charlton M.P., Atwood H.L., and Zinsmaier K.E. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47 (2005) 379-393
25. Hollenbeck P.J. The pattern and mechanism of mitochondrial transport in axons. Front. Biosci. 1 (1996) d91-d102
26. Hollenbeck P.J., and Saxton W.M. The axonal transport of mitochondria. J. Cell. Sci. 118 (2005) 5411-5419
27. Horiuchi D., Barkus R.V., Pilling A.D., Gassman A., and 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. 15 (2005) 2137-2141
28. Kirk E., Chin L.S., and Li L. GRIF1 binds Hrs and is a new regulator of endosomal trafficking. J. Cell. Sci. 119 (2006) 4689-4701
29. Kittler J.T., Thomas P., Tretter V., Bogdanov Y.D., Haucke V., Smart T.G., and Moss S.J. Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 12736-12741
30. Komada M., Masaki R., Yamamoto A., and Kitamura N. Hrs, a tyrosine kinase substrate with a conserved double zinc finger domain, is localized to the cytoplasmic surface of early endosomes. J. Biol. Chem. 272 (1997) 20538-20544
31. Li Z., Okamoto K., Hayashi Y., and Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119 (2004) 873-887
32. Otsuga D., Keegan B.R., Brisch E., Thatcher J.W., Hermann G.J., Bleazard W., and Shaw J.M. The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J. Cell Biol. 143 (1998) 333-349
33. Palmer C.L., Lim W., Hastie P.G., Toward M., Korolchuk V.I., Burbidge S.A., Banting G., Collingridge G.L., Isaac J.T., and Henley J.M. Hippocalcin functions as a calcium sensor in hippocampal LTD. Neuron 47 (2005) 487-494
34. Pilling A.D., Horiuchi D., Lively C.M., and Saxton W.M. Kinesin-1 and dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol. Biol. Cell 17 (2006) 2057-2068
35. Pitts K.R., Yoon Y., Krueger E.W., and McNiven M.A. The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol. Biol. Cell 10 (1999) 4403-4417
36. Pozo K., and Stephenson F.A. GRIF-1-kinesin-1 interactions: a confocal microscopy study. Biochem. Soc. Trans. 34 (2006) 48-50
37. Raiborg C., Bache K.G., Mehlum A., Stang E., and Stenmark H. Hrs recruits clathrin to early endosomes. EMBO J. 20 (2001) 5008-5021
38. Sesaki H., and Jensen R.E. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147 (1999) 699-706
39. Smirnova E., Griparic L., Shurland D.L., and van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12 (2001) 2245-2256
40. Smith M.J., Pozo K., Brickley K., and 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. 281 (2006) 27216-27228
41. Stowers R.S., Megeath L.J., Gorska-Andrzejak J., Meinertzhagen I.A., and Schwarz T.L. Axonal transport of mitochondria to synapses depends on Milton, a novel Drosophila protein. Neuron 36 (2002) 1063-1077
42. Su Q., Cai Q., Gerwin C., Smith C.L., and Sheng Z.H. Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat. Cell Biol. 6 (2004) 941-953
43. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., and Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93 (1998) 1147-1158
44. Tang Y., and Zucker R.S. Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18 (1997) 483-491
45. Verstreken P., Ly C.V., Venken K.J., Koh T.W., Zhou Y., and Bellen H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47 (2005) 365-378
46. Xia Z., Dudek H., Miranti C.K., and Greenberg M.E. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16 (1996) 5425-5436