DISC1 complexes with TRAK1 and Miro1 to modulate anterograde axonal mitochondrial trafficking

Human Molecular Genetics

Volumn 23, Issue 4, 2014, Pages 906-919

  Ogawa, Fumiaki ^a   Malavasi, Elise L V ^a   Crummie, Darragh K ^a   Eykelenboom, Jennifer E ^a,b   Soares, Dinesh C ^a   Mackie, Shaun ^a   Porteous, David J ^a   Millar, J Kirsty ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN 1; MIRO1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TRAFFICKING PROTEIN KINESIN BINDING 1; UNCLASSIFIED DRUG;

ANXIETY DISORDER; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DEPRESSION; DISRUPTED IN SCHIZOPHRENIA 1 GENE; GENE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL TRAFFICKING; MITOCHONDRION; NEUROTRANSMISSION; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROTEIN INTERACTION; SCHIZOPHRENIA;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; AXONS; CERCOPITHECUS AETHIOPS; COS CELLS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; KINESIN; MENTAL DISORDERS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; RHO GTP-BINDING PROTEINS;

EID: 84892980987     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt485     Document Type: Article

References (42)

1. Brandon, N.J. and Sawa, A. (2011) Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat. Rev. Neurosci., 12, 707-722.
2. Porteous, D.J., Millar, J.K., Brandon, N.J. and Sawa, A. (2011) DISC1 at 10: connecting psychiatric genetics and neuroscience. Trends Mol. Med., 17, 699-706.
3. Soares, D.C., Carlyle, B.C., Bradshaw, N.J. and Porteous, D.J. (2011) DISC1: structure, function, and therapeutic potential for major mental illness. ACS Chem. Neurosci., 2, 609-632.
4. James, R., Adams, R.R., Christie, S., Buchanan, S.R., Porteous, D.J. and Millar, J.K. (2004) Disrupted in Schizophrenia 1 (DISC1) is a multicompartmentalized protein that predominantly localizes to mitochondria. Mol. Cell. Neurosci., 26, 112-122.
5. Park, Y.U., Jeong, J., Lee, H., Mun, J.Y., Kim, J.H., Lee, J.S., Nguyen, M.D., Han, S.S., Suh, P.G. and Park, S.K. (2010) Disrupted-in-Schizophrenia 1 (DISC1) plays essential roles in mitochondria in collaboration with Mitofilin. Proc. Natl. Acad. Sci. USA, 107, 17785-17790.
6. Ramsey, A.J., Milenkovic, M., Oliveira, A.F., Escobedo-Lozoya, Y., Seshadri, S., Salahpour, A., Sawa, A., Yasuda, R. and Caron, M.G. (2011) Impaired NMDA receptor transmission alters striatal synapses and DISC1 protein in an age-dependent manner. Proc. Natl. Acad. Sci.USA, 108, 5795- 5800.
7. Paspalas, C.D., Wang, M. and Arnsten, A.F. (2012) Constellation of HCN channels and cAMP regulating proteins in dendritic spines of the primate prefrontal cortex: potential substrate for working memory deficits in schizophrenia. Cereb. Cortex, 23, 1643-1654.
8. Atkin, T.A., MacAskill, A.F., Brandon, N.J. and Kittler, J.T. (2011) Disrupted in Schizophrenia-1 regulates intracellular trafficking of mitochondria in neurons. Mol. Psychiatry, 16, 122-124.
9. Frederick, R.L. and Shaw, J.M. (2007) Moving mitochondria: establishing distribution of an essential organelle. Traffic, 8, 1668-1675.
10. Chen, S., Owens, G.C., Crossin, K.L. and Edelman, D.B. (2007) Serotonin stimulates mitochondrial transport in hippocampal neurons. Mol. Cell. Neurosci., 36, 472-483.
11. Chen, S., Owens, G.C. and Edelman, D.B. (2008) Dopamine inhibits mitochondrial motility in hippocampal neurons. PLoS ONE, 3, e2804.
12. Macaskill, A.F., Rinholm, J.E., Twelvetrees, A.E., Arancibia-Carcamo, I.L., Muir, J., Fransson, A., Aspenstrom, P., Attwell, D. and Kittler, J.T. (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron, 61, 541-555.
13. 2+ dependent regulation of kinesin-mediated mitochondrial motility. Cell, 136, 163-174.
14. Han, X.J., Tomizawa, K., Fujimura, A., Ohmori, I., Nishiki, T., Matsushita, M. and Matsui, H. (2011) Regulation of mitochondrial dynamics and neurodegenerative diseases. Acta Med. Okayama, 65, 1-10.
15. Cai, Q., Davis, M.L. and Sheng, Z.H. (2011) Regulation of axonal mitochondrial transport and its impact on synaptic transmission. Neurosci. Res., 70, 9-15.
16. Reis, K., Fransson, A. and Aspenstrom, P. (2009) The Miro GTPases: at the heart of the mitochondrial transport machinery. FEBS Lett., 583, 1391- 1398.
17. Boldogh, I.R. and Pon, L.A. (2007) Mitochondria on the move. Trends Cell Biol., 17, 502-510.
18. Brickley, K., Smith, M.J., Beck,M.and Stephenson, F.A. (2005)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, 14723- 14732.
19. Brickley, K. and Stephenson, F.A. (2011) Trafficking kinesin protein (TRAK)-mediated transport of mitochondria in axons of hippocampal neurons. J. Biol. Chem., 286, 18079-18092.
20. Webber, E., Li, L. and Chin, L.S. (2008) Hypertonia-associated protein Trak1 is a novel regulator of endosome-to-lysosome trafficking. J. Mol. Biol., 382, 638-651.
21. Gilbert, S.L., Zhang, L., Forster, M.L., Anderson, J.R., Iwase, T., Soliven, B., Donahue, L.R., Sweet, H.O., Bronson, R.T., Davisson, M.T. et al. (2006) Trak1 mutation disrupts GABA(A) receptor homeostasis in hypertonic mice. Nat. Genet., 38, 245-250.
22. Song, W., Li, W., Feng, J., Heston, L.L., Scaringe, W.A. and Sommer, S.S. (2008) Identification of high risk DISC1 structural variants with a 2% attributable risk for schizophrenia. Biochem. Biophys. Res. Commun., 367, 700-706.
23. Thomson, P.A., Parla, J.S., McRae, A.F., Kramer, M., Ramakrishnan, K., Yao, J., Soares, D.C., McCarthy, S., Morris, S.W., Cardone, L. et al. (2013) 708Commonand 2010 rareDISC1locus variants identified in 1542 subjects: analysis for association with psychiatric disorder and cognitive traits. Mol. Psychiatry. doi:10.1038/mp.2013.68.
24. Eykelenboom, J.E., Briggs, G.J., Bradshaw, N.J., Soares, D.C., Ogawa, F., Christie, S., Malavasi, E.L., Makedonopoulou, P., Mackie, S., Malloy, M.P. et al. (2012) A t(1;11) translocation linked to schizophrenia and affective disorders gives rise to aberrant chimeric DISC1 transcripts that encode structurally altered, deleterious mitochondrial proteins. Hum. Mol. Genet., 21, 3374-3386.
25. Millar, J.K., James, R., Christie, S. and Porteous, D.J. (2005) Disrupted in Schizophrenia 1 (DISC1): subcellular targeting and induction of ring mitochondria. Mol. Cell. Neurosci., 30, 477-484.
26. Camargo, L.M., Collura, V., Rain, J.C., Mizuguchi, K., Hermjakob, H., Kerrien, S., Bonnert, T.P., Whiting, P.J. and Brandon, N.J. (2007) Disrupted in Schizophrenia 1 interactome: evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia. Mol. Psychiatry, 12, 74-86.
27. Chubb, J.E., Bradshaw, N.J., Soares, D.C., Porteous, D.J. and Millar, J.K. (2008) The DISC locus in psychiatric illness. Mol. Psychiatry, 13, 36-64.
28. Sawamura, N., Ando, T., Maruyama, Y., Fujimuro, M., Mochizuki, H., Honjo, K., Shimoda, M., Toda, H., Sawamura-Yamamoto, T., Makuch, L.A. et al. (2008) Nuclear DISC1 regulates CRE-mediated gene transcription and sleep homeostasis in the fruit fly. Mol. Psychiatry, 13, 1138-1148.
29. Malavasi, E.L., Ogawa, F., Porteous, D.J. and Millar, J.K. (2012) DISC1 variants 37W and 607F disrupt its nuclear targeting and regulatory role in ATF4-mediated transcription. Hum. Mol. Genet., 21, 2779-2792.
30. Taya, S., Shinoda, T., Tsuboi, D., Asaki, J., Nagai, K., Hikita, T., Kuroda, S., Kuroda, K., Shimizu, M., Hirotsune, S. et al. (2007) DISC1 regulates the transport of the NUDEL/LIS1/14-3-3 epsilon complex through kinesin-1. J. Neurosci., 27, 15-26.
31. Koutsopoulos, O.S., Laine, D., Osellame, L., Chudakov, D.M., Parton, R.G., Frazier, A.E. and Ryan, M.T. (2010) Human Miltons associate with mitochondria and induce microtubule-dependent remodeling of mitochondrial networks. Biochim. Biophys. Acta, 1803, 564-574.
32. De Vos, K.J. and Sheetz, M.P. (2007) Visualization and quantification of mitochondrial dynamics in living animal cells. Methods Cell Biol., 80, 627- 682.
33. MacAskill, A.F., Brickley, K., Stephenson, F.A. and Kittler, J.T. (2009) GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol. Cell. Neurosci., 40, 301-312.
34. Millar, J.K., Wilson-Annan, J.C., Anderson, S., Christie, S., Taylor, M.S., Semple, C.A., Devon, R.S., St Clair, D.M., Muir, W.J., Blackwood, D.H. et al. (2000) Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet., 9, 1415-1423.
35. Blackwood, D.H., Fordyce, A., Walker, M.T., St Clair, D.M., Porteous, D.J. and Muir, W.J. (2001) Schizophrenia and affective disorders-cosegregation with a translocation atchromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am. J. Hum. Genet., 69, 428-433.
36. Millar, J.K., Pickard, B.S., Mackie, S., James, R., Christie, S., Buchanan, S.R., Malloy, M.P., Chubb, J.E., Huston, E., Baillie, G.S. et al. (2005)DISC1 And PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science, 310, 1187-1191.
37. Corti, O., Lesage, S. and Brice, A. (2011) What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol. Rev., 91, 1161-1218.
38. Wang, X., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y.L., Selkoe, D., Rice, S., Steen, J., LaVoie, M.J. and Schwarz, T.L. (2011)PINK1and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell, 147, 893-906.
39. Flores, R. III, Hirota, Y., Armstrong, B., Sawa, A. and Tomoda, T. (2011) DISC1 regulates synaptic vesicle transport via a lithium-sensitive pathway. Neurosci. Res., 71, 71-77.
40. Bradshaw, N.J., Ogawa, F., Antolin-Fontes, B., Chubb, J.E., Carlyle, B.C., Christie, S., Claessens, A., Porteous, D.J. and Millar, J.K. (2008) DISC1, PDE4B, and NDE1 at the centrosome and synapse. Biochem. Biophys. Res. Commun., 377, 1091-1096.
41. Li, Q., Lau, A., Morris, T.J., Guo, L., Fordyce, C.B. and Stanley, E.F. (2004) A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J. Neurosci., 24, 4070-4081.
42. Ogawa, F., Kasai, M. and Akiyama, T. (2005) A functional link between Disrupted-In-Schizophrenia 1 and the eukaryotic translation initiation factor 3. Biochem. Biophys. Res. Commun., 338, 771-776.