UNC119a bridges the transmission of Fyn signals to RAB11, leading to the completion of cytokinesis

Cell Cycle

Volumn 12, Issue 8, 2013, Pages 1303-1315

  Lee, YuKyung ^a   Chung, Sunglan ^a   Baek, In Keol ^a   Lee, Tae H ^a   Paik, Soon Young ^b   Lee, JooHun ^a  

^a Yonsei University   (South Korea)

^b The Catholic University of Korea   (South Korea)

Author keywords

Cytokinesis; Cytokinesis failure; Fyn kinase; Rab11; SFKs signaling; UNC119

Indexed keywords

ENZYME ACTIVATOR; PARAFORMALDEHYDE; PROTEIN KINASE FYN; RAB11 PROTEIN; UNC119A PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CELL SYNCHRONIZATION; CELLS; CELLULAR DISTRIBUTION; CENTROSOME; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINESIS; ENZYME PHOSPHORYLATION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MAMMAL CELL; MITOSIS; MOLECULAR WEIGHT; NONHUMAN; SIGNAL TRANSDUCTION; SPINDLE CELL; T LYMPHOCYTE ACTIVATION; TELOPHASE;

EID: 84876277685     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24404     Document Type: Article

References (52)

1. Barr FA, Gruneberg U. Cytokinesis: Placing and making the final cut. Cell 2007; 131:847-60; PMID:18045532; http://dx.doi.org/10.1016/j.cell.2007.11.011
2. Fededa JP, Gerlich DW. Molecular control of animal cell cytokinesis. Nat Cell Biol 2012; 14:440-7; PMID:22552143; http://dx.doi.org/10.1038/ncb2482
3. Glotzer M. The molecular requirements for cytokinesis. Science 2005; 307:1735-9; PMID:15774750; http://dx.doi.org/10.1126/science.1096896
4. Normand G, King RW. Understanding cytokinesis failure. Adv Exp Med Biol 2010; 676:27-55; PMID:20687468; http://dx.doi.org/10.1007/978-1-4419-6199-0-3
5. Guarino M. Src signaling in cancer invasion. J Cell Physiol 2010; 223:14-26; PMID:20049846
6. Thomas SM, Brugge JS. Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 1997; 13:513-609; PMID:9442882; http://dx.doi.org/10. 1146/annurev.cellbio.13.1.513
7. Campbell KS, Cooper S, Dessing M, Yates S, Buder A. Interaction of p59fyn kinase with the dynein light chain, Tctex-1, and colocalization during cytokinesis. J Immunol 1998; 161:1728-37; PMID:9712037
8. Tominaga T, Sahai E, Chardin P, McCormick F, Courtneidge SA, Alberts AS. Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell 2000; 5:13-25; PMID:10678165; http://dx.doi.org/10.1016/S1097-2765(00) 803998
9. Yasunaga M, Yagi T, Hanzawa N, Yasuda M, Yamanashi Y, Yamamoto T, et al. Involvement of Fyn tyrosine kinase in progression of cytokinesis of B lymphocyte progenitor. J Cell Biol 1996; 132:91-9; PMID:8567733; http://dx.doi.org/10. 1083/jcb.132.1.91
10. Kasahara K, Nakayama Y, Nakazato Y, Ikeda K, Kuga T, Yamaguchi N. Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J Biol Chem 2007; 282:5327 PMID:17189253; http://dx.doi.org/10.1074/jbc. M608396200
11. Wilson GM, Fielding AB, Simon GC, Yu X, Andrews PD, Hames RS, et al. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol Biol Cell 2005; 16:849-60; PMID:15601896; http://dx.doi.org/10.1091/mbc.E04-10-0927
12. Pelissier A, Chauvin JP, Lecuit T. Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 2003; 13:1848-57; PMID:14588240; http://dx.doi.org/10.1016/j.cub.2003.10.023
13. Yu X, Prekeris R, Gould GW. Role of endosomal Rab GTPases in cytokinesis. Eur J Cell Biol 2007; 86:25-35; PMID:17157409; http://dx.doi.org/10.1016/j. ejcb.2006.10.002
14. Riggs B, Rothwell W, Mische S, Hickson GR, Matheson J, Hays TS, et al. Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J Cell Biol 2003; 163:143-54; PMID:14530382; http://dx.doi.org/10.1083/jcb.200305115
15. Maduro M, Pilgrim D. Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 1995; 141:977-88; PMID:8582641
16. Higashide T, Murakami A, McLaren MJ, Inana G. Cloning of the cDNA for a novel photoreceptor protein. J Biol Chem 1996; 271:1797-804; PMID:8576185; http://dx.doi.org/10.1074/jbc.271.3.1797
17. Chung S, Kang S, Paik S, Lee J. NgUNC-119, Naegleria homologue of UNC-119, localizes to the flagellar rootlet. Gene 2007; 389:45-51; PMID:17123749; http://dx.doi.org/10.1016/j.gene.2006.09.032
18. Ohshima S, Ohashi-Suzuki M, Miura Y, Yabu Y, Okada N, Ohta N, et al. TbUNC119 and its binding protein complex are essential for propagation, motility, and morphogenesis of Trypanosoma brucei procyclic form cells. PLoS ONE 2010; 5:e15577; PMID:21203515; http://dx.doi.org/10.1371/journal.pone.0015577
19. Maduro MF, Gordon M, Jacobs R, Pilgrim DB. The UNC-119 family of neural proteins is functionally conserved between humans, Drosophila and C. elegans. J Neurogenet 2000; 13:191-212; PMID:10858820; http://dx.doi.org/10.3109/ 01677060009084494
20. Manning AG, Crawford BD, Waskiewicz AJ, Pilgrim DB. unc-119 homolog required for normal development of the zebrafish nervous system. Genesis 2004; 40:223-30; PMID:15593328; http://dx.doi.org/10.1002/gene.20089
21. Kobayashi A, Higashide T, Hamasaki D, Kubota S, Sakuma H, An W, et al. HRG4 (UNC119) mutation found in cone-rod dystrophy causes retinal degeneration in a transgenic model. Invest Ophthalmol Vis Sci 2000; 41:3268-77; PMID:11006213
22. Higashide T, McLaren MJ, Inana G. Localization of HRG4, a photoreceptor protein homologous to Unc-119, in ribbon synapse. Invest Ophthalmol Vis Sci 1998; 39:690-8; PMID:9538874
23. Alpadi K, Magupalli VG, Käppel S, Köblitz L, Schwarz K, Seigel GM, et al. RIBEYE recruits Munc119, a mammalian ortholog of the Caenorhabditis elegans protein unc119, to synaptic ribbons of photoreceptor synapses. J Biol Chem 2008; 283:26461-7; PMID:18664567; http://dx.doi.org/10.1074/jbc.M801625200
24. Haeseleer F. Interaction and colocalization of CaBP4 and Unc119 (MRG4) in photoreceptors. Invest Ophthalmol Vis Sci 2008; 49:2366-75; PMID:18296658; http://dx.doi.org/10.1167/iovs.07-1166
25. Ishiba Y, Higashide T, Mori N, Kobayashi A, Kubota S, McLaren MJ, et al. Targeted inactivation of synaptic HRG4 (UNC119) causes dysfunction in the distal photoreceptor and slow retinal degeneration, revealing a new function. Exp Eye Res 2007; 84:473-85; PMID:17174953; http://dx.doi.org/10.1016/j.exer.2006.10.016
26. Kubota S, Kobayashi A, Mori N, Higashide T, McLaren MJ, Inana G. Changes in retinal synaptic proteins in the transgenic model expressing a mutant HRG4 (UNC119). Invest Ophthalmol Vis Sci 2002; 43:308-13; PMID:11818371
27. Mori N, Ishiba Y, Kubota S, Kobayashi A, Higashide T, McLaren MJ, et al. Truncation mutation in HRG4 (UNC119) leads to mitochondrial ANT-1-mediated photoreceptor synaptic and retinal degeneration by apoptosis. Invest Ophthalmol Vis Sci 2006; 47:1281-92; PMID:16565359; http://dx.doi.org/10.1167/iovs.05-0493
28. Kobayashi A, Kubota S, Mori N, McLaren MJ, Inana G. Photoreceptor synaptic protein HRG4 (UNC119) interacts with ARL2 via a putative conserved domain. FEBS Lett 2003; 534:26-32; PMID:12527357; http://dx.doi.org/10.1016/ S0014-5793(02)03766-3
29. Cen O, Gorska MM, Stafford SJ, Sur S, Alam R. Identification of UNC119 as a novel activator of SRCtype tyrosine kinases. J Biol Chem 2003; 278:8837-45; PMID:12496276; http://dx.doi.org/10.1074/jbc. M208261200
30. Gorska MM, Stafford SJ, Cen O, Sur S, Alam R. Unc119, a novel activator of Lck/Fyn, is essential for T cell activation. J Exp Med 2004; 199:369-79; PMID:14757743; http://dx.doi.org/10.1084/jem. 20030589
31. Vepachedu R, Gorska MM, Singhania N, Cosgrove GP, Brown KK, Alam R. Unc119 regulates myofibroblast differentiation through the activation of Fyn and the p38 MAPK pathway. J Immunol 2007; 179:682-90; PMID:17579091
32. Gorska MM, Liang Q, Karim Z, Alam R. Uncoordinated 119 protein controls trafficking of Lck via the Rab11 endosome and is critical for immunological synapse formation. J Immunol 2009; 183:1675-84; PMID:19592652; http://dx.doi.org/10.4049/jimmunol. 0900792
33. Karim Z, Vepachedu R, Gorska M, Alam R. UNC119 inhibits dynamin and dynamin-dependent endocytic processes. Cell Signal 2010; 22:128-37; PMID:19781630; http://dx.doi.org/10.1016/j.cellsig. 2009.09.022
34. Vepachedu R, Karim Z, Patel O, Goplen N, Alam R. Unc119 protects from Shigella infection by inhibiting the Abl family kinases. PLoS ONE 2009; 4:e5211; PMID:19381274; http://dx.doi.org/10.1371/journal. pone.0005211
35. Gopalakrishna KN, Doddapuneni K, Boyd KK, Masuho I, Martemyanov KA, Artemyev NO. Interaction of transducin with uncoordinated 119 protein (UNC119): Implications for the model of transducin trafficking in rod photoreceptors. J Biol Chem 2011; 286:28954-62; PMID:21712387; http://dx.doi.org/10.1074/jbc.M111. 268821
36. Zhang H, Constantine R, Vorobiev S, Chen Y, Seetharaman J, Huang YJ, et al. UNC119 is required for G protein trafficking in sensory neurons. Nat Neurosci 2011; 14:874-80; PMID:21642972; http://dx.doi.org/10.1038/nn.2835
37. Wright KJ, Baye LM, Olivier-Mason A, Mukhopadhyay S, Sang L, Kwong M, et al. An ARL3-UNC119-RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium. Genes Dev 2011; 25:2347-60; PMID:22085962; http://dx.doi.org/10.1101/ gad.173443.111
38. Gleeson PA, Anderson TJ, Stow JL, Griffiths G, Toh BH, Matheson F. p230 is associated with vesicles budding from the trans-Golgi network. J Cell Sci 1996; 109:2811-21; PMID:9013329
39. Pohl C, Jentsch S. Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 2008; 132:832-45; PMID:18329369; http://dx.doi.org/10.1016/j.cell.2008.01.012
40. Buck RC, Tisdale JM. The fine structure of the midbody of the rat erythroblast. J Cell Biol 1962; 13:109-15; PMID:13874303; http://dx.doi.org/10. 1083/jcb.13.1.109
41. Mullins JM, Biesele JJ. Terminal phase of cytokinesis in D-98s cells. J Cell Biol 1977; 73:672-84; PMID:873994; http://dx.doi.org/10.1083/jcb.73.3.672
42. Mullins JM, McIntosh Jr. Isolation and initial characterization of the mammalian midbody. J Cell Biol 1982; 94:654-61; PMID:7130277; http://dx.doi.org/10.1083/jcb.94.3.654
43. Fabbro M, Zhou BB, Takahashi M, Sarcevic B, Lal P, Graham ME, et al. Cdk1/Erk2-and Plk1-dependent phosphorylation of a centrosome protein, Cep55, is required for its recruitment to midbody and cytokinesis. Dev Cell 2005; 9:477-88; PMID:16198290; http://dx.doi.org/10.1016/j.devcel.2005.09.003
44. Gromley A, Jurczyk A, Sillibourne J, Halilovic E, Mogensen M, Groisman I, et al. A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase. J Cell Biol 2003; 161:535-45; PMID:12732615; http://dx.doi.org/10.1083/jcb.200301105
45. Chircop M, Oakes V, Graham ME, Ma MP, Smith CM, Robinson PJ, et al. The actin-binding and bundling protein, EPLIN, is required for cytokinesis. Cell Cycle 2009; 8:757-64; PMID:19221476; http://dx.doi.org/10.4161/cc.8.5.7878
46. van der Horst A, Simmons J, Khanna KK. Cep55 stabilization is required for normal execution of cytokinesis. Cell Cycle 2009; 8:3742-9; PMID:19855176; http://dx.doi.org/10.4161/cc.8.22.10047
47. Kuga T, Nakayama Y, Hoshino M, Higashiyama Y, Obata Y, Matsuda D, et al. Differential mitotic activation of endogenous c-Src, c-Yes, and Lyn in HeLa cells. Arch Biochem Biophys 2007; 466:116-24; PMID:17692281; http://dx.doi.org/10.1016/j.abb.2007.07.002
48. Ley SC, Marsh M, Bebbington CR, Proudfoot K, Jordan P. Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J Cell Biol 1994; 125:639-49; PMID:7513706; http://dx.doi.org/10. 1083/jcb.125.3.639
49. Jung J, Lee MK, Jin Y, Fu SB, Rosales JL, Lee KY. Clues for c-Yes involvement in the cell cycle and cytokinesis. Cell Cycle 2011; 10:1502-3; PMID:21566460; http://dx.doi.org/10.4161/cc.10.9.15495
50. Scapin SM, Carneiro FR, Alves AC, Medrano FJ, Guimarães BG, Zanchin NI. The crystal structure of the small GTPase Rab11b reveals critical differences relative to the Rab11a isoform. J Struct Biol 2006; 154:260-8; PMID:16545962; http://dx.doi.org/10.1016/j.jsb.2006.01.007
51. Lapierre LA, Dorn MC, Zimmerman CF, Navarre J, Burnette JO, Goldenring Jr. Rab11b resides in a vesicular compartment distinct from Rab11a in parietal cells and other epithelial cells. Exp Cell Res 2003; 290:322-31; PMID:14567990; http://dx.doi.org/10.1016/S0014-4827(03)00340-9
52. Khvotchev MV, Ren M, Takamori S, Jahn R, Südhof TC. Divergent functions of neuronal Rab11b in Ca2+-regulated versus constitutive exocytosis. J Neurosci 2003; 23:10531-9; PMID:14627637