Cohen syndrome-associated protein COH1 physically and functionally interacts with the small GTPase RAB6 at the Golgi complex and directs neurite outgrowth

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3349-3358

  Seifert, Wenke ^a   Kühnisch, Jirko ^a,b   Maritzen, Tanja ^c   Lommatzsch, Stefanie ^a   Hennies, Hans Christian ^d,e,f   Bachmann, Sebastian ^a   Horn, Denise ^a   Haucke, Volker ^c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY OF COLOGNE   (Germany)

^f INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

NEURONS; PROTEINS;

AXONAL OUTGROWTH; CONSTITUTIVELY ACTIVES; INTELLECTUAL DISABILITY; LIPID MEMBRANES; NEURITE OUTGROWTH; PHYSICAL INTERACTIONS; SCAFFOLD PROTEIN; STRUCTURAL MAINTENANCE;

SCAFFOLDS (BIOLOGY);

MEMBRANE PROTEIN; PROTEIN COH1; PROTEIN RAB6; RAB PROTEIN; UNCLASSIFIED DRUG; PROTEIN BINDING; RAB6 PROTEIN; VESICULAR TRANSPORT PROTEIN; VPS13B PROTEIN, HUMAN;

ARTICLE; AUTOSOMAL RECESSIVE DISORDER; COHEN SYNDROME; CONTROLLED STUDY; GOLGI COMPLEX; HUMAN; LIPID MEMBRANE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURITOGENESIS; PATHOGENESIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SOLUBILIZATION; ANIMAL; CELL CULTURE; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; NEURITE; PROTEIN TRANSPORT; RAT;

ANIMALS; CELLS, CULTURED; GOLGI APPARATUS; HEK293 CELLS; HELA CELLS; HUMANS; NEURITES; PROTEIN BINDING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RATS; VESICULAR TRANSPORT PROTEINS;

EID: 84922422473     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.608174     Document Type: Article

References (38)

1. Cohen, M. M., Jr., Hall, B. D., Smith, D. W., Graham, C. B., and Lampert, K. J. (1973) A new syndrome with hypotonia, obesity, mental deficiency, and facial, oral, ocular, and limb anomalies. J. Pediatr 83, 280-284
2. Kolehmainen, J., Black, G. C., Saarinen, A., Chandler, K., Clayton-Smith, J., Träskelin, A. L., Perveen, R., Kivitie-Kallio, S., Norio, R., Warburg, M., Fryns, J. P., de la Chapelle, A., and Lehesjoki, A. E. (2003) Cohen syndrome is causedbymutations ina novel gene, COH1, encoding atransmembrane protein with a presumed role in vesicle-mediated sorting and intracellular protein transport. Am. J. Hum. Genet. 72, 1359-1369
3. Seifert, W., Holder-Espinasse, M., Kühnisch, J., Kahrizi, K., Tzschach, A., Garshasbi, M., Najmabadi, H., Walter Kuss, A., Kress, W., Laureys, G., Loeys, B., Brilstra, E., Mancini, G. M., Dollfus, H., Dahan, K., Apse, K., Hennies, H. C., and Horn, D. (2009) Expanded mutational spectrum in Cohen syndrome, tissue expression, and transcript variants of COH1. Hum. Mutat. 30, E404-E420
4. Mochida, G. H., Rajab, A., Eyaid, W., Lu, A., Al-Nouri, D., Kosaki, K., Noruzinia, M., Sarda, P., Ishihara, J., Bodell, A., Apse, K., and Walsh, C. A. (2004) Broader geographical spectrum of Cohen syndrome due to COH1 mutations. J. Med. Genet. 41, e87
5. Hennies, H. C., Rauch, A., Seifert, W., Schumi, C., Moser, E., Al-Taji, E., Tariverdian, G., Chrzanowska, K. H., Krajewska-Walasek, M., Rajab, A., Giugliani, R., Neumann, T. E., Eckl, K. M., Karbasiyan, M., Reis, A., and Horn, D. (2004) Allelic heterogeneity in the COH1 gene explains clinical variability in Cohen syndrome. Am. J. Hum. Genet. 75, 138-145
6. Velayos-Baeza, A., Vettori, A., Copley, R. R., Dobson-Stone, C., and Monaco, A. P. (2004) Analysis of the human VPS13 gene family. Genomics 84, 536-549
7. Redding, K., Brickner, J. H., Marschall, L. G., Nichols, J. W., and Fuller, R. S. (1996) Allele-specific suppression of a defective trans-Golgi network (TGN) localization signal in Kex2p identifies three genes involved in localization of TGN transmembrane proteins. Mol. Cell. Biol. 16, 6208-6217
8. Brickner, J. H., and Fuller, R. S. (1997) SOI1 encodes a novel, conserved protein that promotes TGN-endosomal cycling of Kex2p and other membrane proteins by modulating the function of two TGN localization signals. J. Cell Biol. 139, 23-36
9. Kilmartin, J. V. (2003) Sfi1p has conserved centrin-binding sites and an essential function in budding yeast spindle pole body duplication. J. Cell Biol. 162, 1211-1221
10. Meriin, A. B., Zhang, X., Miliaras, N. B., Kazantsev, A., Chernoff, Y. O., McCaffery, J. M., Wendland, B., and Sherman, M. Y. (2003) Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis. Mol. Cell. Biol. 23, 7554-7565
11. Park, J. S., Okumura, Y., Tachikawa, H., and Neiman, A. M. SPO71 encodes a developmental stage-specific partner for Vps13 in Saccharomyces cerevisiae. Eukaryot Cell 12, 1530-1537
12. Park, J. S., and Neiman, A. M. VPS13 regulates membrane morphogenesis during sporulation in Saccharomyces cerevisiae. J. Cell Sci. 125, 3004-3011
13. Seifert, W., Kühnisch, J., Maritzen, T., Horn, D., Haucke, V., and Hennies, H. C. (2011) Cohen syndrome-associated protein, COH1, is a novel, giant Golgi matrix protein required for Golgi integrity. J. Biol. Chem. 286, 37665-37675
14. Del Nery, E., Miserey-Lenkei, S., Falguières, T., Nizak, C., Johannes, L., Perez, F., and Goud, B. (2006) Rab6A and Rab6A' GTPases play nonoverlapping roles in membrane trafficking. Traffic 7, 394-407
15. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-AAC (T)) Method. Methods 25, 402-408
16. Kaech, S., and Banker, G. (2006) Culturing hippocampal neurons. Nat. Protoc. 1, 2406-2415
17. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E. D., Sevier, C. S., Ding, H., Koh, J. L., Toufighi, K., Mostafavi, S., Prinz, J., St Onge, R. P., Van der Sluis, B., Makhnevych, T., Vizeacoumar, F. J., Alizadeh, S., Bahr, S., Brost, R. L., Chen, Y., Cokol, M., Deshpande, R., Li, Z., Lin, Z. Y., Liang, W., Marback, M., Paw, J., San Luis, B. J., Shuteriqi, E., Tong, A. H., van Dyk, N, Wallace, I. M., Whitney, J. A., Weirauch, M. T., Zhong, G., Zhu, H., Houry, W. A., Brudno, M., Ragibizadeh, S., Papp, B., Pál, C, Roth, F. P., Giaever, G., Nislow, C, Troyanskaya, O. G., Bussey, H., Bader, G. D., Gingras, A. C, Morris, Q. D., Kim, P. M., Kaiser, C. A., Myers, C. L., Andrews, B. J., and Boone, C. (2010) The genetic landscape of a cell. Science 327, 425-431
18. Hoppins, S., Collins, S. R., Cassidy-Stone, A., Hummel, E., Devay, R. M., Lackner, L. L., Westermann, B., Schuldiner, M., Weissman, J. S., and Nunnari, J. (2011) A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J. Cell Biol. 195, 323-340
19. Martinez, O., Antony, C, Pehau-Arnaudet, G., Berger, E. G., Salamero, J., and Goud, B. (1997) GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 94, 1828-1833
20. Martinez, O., Schmidt, A., Salaméro, J., Hoflack, B., Roa, M., and Goud, B. (1994) The small GTP-binding protein rab6 functions in intra-Golgi transport. J. Cell Biol. 127, 1575-1588
21. Grigoriev, I., Splinter, D., Keijzer, N, Wulf, P. S., Demmers, J., Ohtsuka, T., Modesti, M., Maly, I. V., Grosveld, F., Hoogenraad, C. C, and Akhmanova, A. (2007) Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 13, 305-314
22. Seifert, W., Holder-Espinasse, M., Spranger, S., Hoeltzenbein, M., Rossier, E., Dollfus, H., Lacombe, D., Verloes, A., Chrzanowska, K. H., Maegawa, G. H., Chitayat, D., Kotzot, D., Huhle, D., Meinecke, P., Albrecht, B., Mathijssen, I., Leheup, B., Raile, K., Hennies, H. C, and Horn, D. (2006) Mutational spectrum of COH1 and clinical heterogeneity in Cohen syndrome. J Med. Genet. 43, e22
23. Barkovich, A. J., Kuzniecky, R. I., Jackson, G. D., Guerrini, R., and Dobyns, W. B. (2005) A developmental and genetic classification for malformations of cortical development. Neurology 65, 1873-1887
24. Bielas, S., Higginbotham, H., Koizumi, H., Tanaka, T., and Gleeson, J. G. (2004) Cortical neuronal migration mutants suggest separate but intersecting pathways. Annu. Rev. Cell Dev. Biol. 20, 593-618
25. Guerrini, R., Dobyns, W. B., and Barkovich, A. J. (2008) Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends Neurosci. 31, 154-162
26. Jackson, A. P., Eastwood, H., Bell, S. M., Adu, J., Toomes, C., Carr, I. M., Roberts, E., Hampshire, D. J., Crow, Y. J., Mighell, A. J., Karbani, G., Jafri, H., Rashid, Y., Mueller, R. F., Markham, A. F., and Woods, C. G. (2002) Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 71, 136-142
27. Rauch, A., Thiel, C. T., Schindler, D., Wick, U., Crow, Y. J., Ekici, A. B., van Essen, A. J., Goecke, T. O., Al-Gazali, L., Chrzanowska, K. H., Zweier, C., Brunner, H. G., Becker, K., Curry, C. J., Dallapiccola, B., Devriendt, K., Dörfler, A., Kinning, E., Megarbane, A., Meinecke, P., Semple, R. K., Spranger, S., Toutain, A., Trembath, R. C., Voss, E., Wilson, L., Hennekam, R., de Zegher, F., Dörr, H. G., and Reis, A. (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319, 816-819
28. Sheen, V. L., Ganesh, V. S., Topcu, M., Sebire, G., Bodell, A., Hill, R. S., Grant, P. E., Shugart, Y. Y., Imitola, J., Khoury, S. J., Guerrini, R., and Walsh, C. A. (2004) Mutationsin ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex. Nat. Genet. 36, 69-76
29. Pfenninger, K. H. (2009) Plasma membrane expansion: a neuron's Herculean task. Nat Rev. Neurosci. 10, 251-261
30. Kivitie-Kallio, S., Autti, T., Salonen, O., and Norio, R. (1998) MRI of the brain in the Cohen syndrome: a relatively large corpus callosum in patients with mental retardation and microcephaly. Neuropediatrics 29, 298-301
31. Schlager, M. A., Kapitein, L. C., Grigoriev, I., Burzynski, G. M., Wulf, P. S., Keijzer, N., de Graaff, E., Fukuda, M., Shepherd, I. T., Akhmanova, A., and Hoogenraad, C. C. (2010) Pericentrosomal targeting of Rab6 secretory vesicles by Bicaudal-D-related protein 1 (BICDR-1) regulates neuritogenesis. EMBO J. 29, 1637-1651
32. Zmuda, J. F., and Rivas, R. J. (1998) The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. Cell Motil. Cytoskeleton 41, 18-38
33. Rosnoblet, C., Peanne, R., Legrand, D., and Foulquier, F. (2013) Glycosylation disorders of membrane trafficking. Glycoconj. J. 30, 23-31
34. Miller, V. J., and Ungar, D. (2012) Re'COG'nition at the Golgi. Traffic 13, 891-897
35. Majeed, W., Liu, S., and Storrie, B. (2014) Distinct sets of Rab6 effectors contribute to ZW10- and COG-dependent Golgi homeostasis. Traffic 15, 630-647
36. Sun, Y., Shestakova, A., Hunt, L., Sehgal, S., Lupashin, V., and Storrie, B. (2007) Rab6 regulates both ZW10/RINT-1 and conserved oligomeric Golgi complex-dependent Golgi trafficking and homeostasis. Mol. Biol. Cell 18, 4129-4142
37. Fukuda, M., Kanno, E., Ishibashi, K., and Itoh, T. (2008) Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol. Cell Proteomics 7, 1031-1042
38. Lubbehusen, J., Thiel, C., Rind, N., Ungar, D., Prinsen, B. H., de Koning, T. J., van Hasselt, P. M., and Korner, C. (2010) Fatal outcome due to deficiency of subunit 6 of the conserved oligomeric Golgi complex leading to a new type of congenital disorders of glycosylation. Hum. Mol. Genet. 19, 3623-3633