Resistance to inhibitors of cholinesterase (Ric)-8A and Gαi contribute to cytokinesis abscission by controlling Vacuolar protein-sorting (Vps)34 activity

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Boularan, Cedric ^a   Kamenyeva, Olena ^a   Cho, Hyeseon ^a   Kehrl, John H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHOLINESTERASE INHIBITOR; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; RIC 8A PROTEIN; UNCLASSIFIED DRUG;

ABSCISSION; ARTICLE; BIOSENSOR; CELL CYCLE; CELL DIVISION; CELL MEMBRANE; CELL SIGNALING ASSAY; CONFORMATIONAL TRANSITION; CYTOKINESIS; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; IMMUNOPRECIPITATION; MITOSIS; MOLECULAR MECHANICS; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; WESTERN BLOTTING;

CELL LINE, TUMOR; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; CYTOKINESIS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HELA CELLS; HUMANS; MITOSIS; NUCLEAR PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL;

EID: 84907033415     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086680     Document Type: Article

References (47)

1. Lambert NA (2008) Dissociation of heterotrimeric g proteins in cells. Sci Signal 1: re5.
2. Tall GG, Krumins AM, Gilman AG (2003) Mammalian Ric-8A (synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor. J Biol Chem 278: 8356-8362. (Pubitemid 36800584)
3. Gabay M, Pinter ME, Wright FA, Chan P, Murphy AJ, et al. (2011) Ric-8 proteins are molecular chaperones that direct nascent G protein alpha subunit membrane association. Sci Signal 4: ra79.
4. Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, et al. (1996) A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci U S A 93: 12593-12598. (Pubitemid 26367189)
5. Afshar K, Willard FS, Colombo K, Johnston CA, McCudden CR, et al. (2004) RIC-8 is required for GPR-1/2-dependent Galpha function during asymmetric division of C. elegans embryos. Cell 119: 219-230. (Pubitemid 39360904)
6. Afshar K, Willard FS, Colombo K, Siderovski DP, Gonczy P (2005) Cortical localization of the Galpha protein GPA-16 requires RIC-8 function during C. elegans asymmetric cell division. Development 132: 4449-4459. (Pubitemid 41632224)
7. Couwenbergs C, Spilker AC, Gotta M (2004) Control of embryonic spindle positioning and Galpha activity by C. elegans RIC-8. Curr Biol 14: 1871-1876. (Pubitemid 39408778)
8. Woodard GE, Huang NN, Cho H, Miki T, Tall GG, et al. (2010) Ric-8A and Gi alpha recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Mol Cell Biol 30: 3519-3530.
9. Siderovski DP, Willard FS (2005) The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int J Biol Sci 1: 51-66.
10. Parmentier ML, Woods D, Greig S, Phan PG, Radovic A, et al. (2000) Rapsynoid/partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J Neurosci 20: RC84.
11. Doherty D, Chudley AE, Coghlan G, Ishak GE, Innes AM, et al. (2012) GPSM2 mutations cause the brain malformations and hearing loss in Chudley-McCullough syndrome. Am J Hum Genet 90: 1088-1093.
12. Blumer JB, Chandler LJ, Lanier SM (2002) Expression analysis and subcellular distribution of the two G-protein regulators AGS3 and LGN indicate distinct functionality. Localization of LGN to the midbody during cytokinesis. J Biol Chem 277: 15897-15903. (Pubitemid 34967870)
13. Cho H, Kehrl JH (2007) Localization of Gi alpha proteins in the centrosomes and at the midbody: implication for their role in cell division. J Cell Biol 178: 245-255. (Pubitemid 47076461)
14. Lacroix B, Maddox AS (2012) Cytokinesis, ploidy and aneuploidy. J Pathol 226: 338-351.
15. Krumins AM, Gilman AG (2006) Targeted knockdown of G protein subunits selectively prevents receptor-mediated modulation of effectors and reveals complex changes in non-targeted signaling proteins. J Biol Chem 281: 10250-10262. (Pubitemid 43864563)
16. Steigemann P, Wurzenberger C, Schmitz MH, Held M, Guizetti J, et al. (2009) Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136: 473-484.
17. Yang F, Camp DG, 2nd, Gritsenko MA, Luo Q, Kelly RT, et al. (2007) Identification of a novel mitotic phosphorylation motif associated with protein localization to the mitotic apparatus. J Cell Sci 120: 4060-4070. (Pubitemid 350269411)
18. Moore NL, Narayanan R, Weigel NL (2007) Cyclin dependent kinase 2 and the regulation of human progesterone receptor activity. Steroids 72: 202-209. (Pubitemid 46273504)
19. Knockaert M, Greengard P, Meijer L (2002) Pharmacological inhibitors of cyclin-dependent kinases. Trends Pharmacol Sci 23: 417-425. (Pubitemid 35247771)
20. Koepp DM, Schaefer LK, Ye X, Keyomarsi K, Chu C, et al. (2001) Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294: 173-177. (Pubitemid 32952972)
21. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, et al. (2006) Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell 24: 355-366. (Pubitemid 44647901)
22. Dalrymple MB, Jaeger WC, Eidne KA, Pfleger KD (2011) Temporal profiling of orexin receptor-arrestin-ubiquitin complexes reveals differences between receptor subtypes. J Biol Chem 286: 16726-16733.
23. Perroy J, Pontier S, Charest PG, Aubry M, Bouvier M (2004) Real-time monitoring of ubiquitination in living cells by BRET. Nat Methods 1: 203-208.
24. Du Q, Macara IG (2004) Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell 119: 503-516. (Pubitemid 39482350)
25. Carmena M (2012) Abscission checkpoint control: stuck in the middle with Aurora B. Open Biol 2: 120095.
26. Sagona AP, Nezis IP, Pedersen NM, Liestol K, Poulton J, et al. (2010) PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nat Cell Biol 12: 362-371.
27. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, et al. (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19: 4577-4588.
28. Kavran JM, Klein DE, Lee A, Falasca M, Isakoff SJ, et al. (1998) Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J Biol Chem 273: 30497-30508. (Pubitemid 28545525)
29. Janetopoulos C, Borleis J, Vazquez F, Iijima M, Devreotes P (2005) Temporal and spatial regulation of phosphoinositide signaling mediates cytokinesis. Dev Cell 8: 467-477. (Pubitemid 40450737)
30. Toyoshima F, Matsumura S, Morimoto H, Mitsushima M, Nishida E (2007) PtdIns(3,4,5)P3 regulates spindle orientation in adherent cells. Dev Cell 13: 796-811. (Pubitemid 350163038)
31. Slessareva JE, Routt SM, Temple B, Bankaitis VA, Dohlman HG (2006) Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein alpha subunit at the endosome. Cell 126: 191-203.
32. Muggerud AA, Edgren H, Wolf M, Kleivi K, Dejeux E, et al. (2009) Data integration from two microarray platforms identifies bi-allelic genetic inactivation of RIC8A in a breast cancer cell line. BMC Med Genomics 2: 26.
33. Fukukawa C, Ueda K, Nishidate T, Katagiri T, Nakamura Y (2010) Critical roles of LGN/GPSM2 phosphorylation by PBK/TOPK in cell division of breast cancer cells. Genes Chromosomes Cancer 49: 861-872.
34. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, et al. (2009) Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 4: e6146.
35. Alexander J, Lim D, Joughin BA, Hegemann B, Hutchins JR, et al. (2011) Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for context-dependent mitotic signaling. Sci Signal 4: ra42.
36. Mayya V, Lundgren DH, Hwang SI, Rezaul K, Wu L, et al. (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci Signal 2: ra46.
37. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, et al. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143: 1174-1189.
38. Figueroa M, Hinrichs MV, Bunster M, Babbitt P, Martinez-Oyanedel J, et al. (2009) Biophysical studies support a predicted superhelical structure with armadillo repeats for Ric-8. Protein Sci 18: 1139-1145.
39. Wurmser AE, Gary JD, Emr SD (1999) Phosphoinositide 3-kinases and their FYVE domain-containing effectors as regulators of vacuolar/lysosomal membrane trafficking pathways. J Biol Chem 274: 9129-9132.
40. Oner SS, Maher E, Gabay M, Tall GG, Blumer JB, et al. (2012) Regulation of the GPR-Galphai Signaling Complex by non-receptor Guanine Nucleotide Exchange Factors. J Biol Chem.
41. Montagnac G, Echard A, Chavrier P (2008) Endocytic traffic in animal cell cytokinesis. Curr Opin Cell Biol 20: 454-461.
42. Neer EJ (1995) Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80: 249-257.
43. Zhang X, Bedigian AV, Wang W, Eggert US (2012) G protein-coupled receptors participate in cytokinesis. Cytoskeleton (Hoboken) 69: 810-818.
44. Funderburk SF, Wang QJ, Yue Z (2010) The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol 20: 355-362.
45. Garcia-Marcos M, Ghosh P, Farquhar MG (2009) GIV is a nonreceptor GEF for G alpha i with a unique motif that regulates Akt signaling. Proc Natl Acad Sci U S A 106: 3178-3183.
46. Mao JZ, Jiang P, Cui SP, Ren YL, Zhao J, et al. (2012) Girdin locates in centrosome and midbody and plays an important role in cell division. Cancer Sci.
47. Garcia-Marcos M, Ear J, Farquhar MG, Ghosh P (2011) A GDI (AGS3) and a GEF (GIV) regulate autophagy by balancing G protein activity and growth factor signals. Mol Biol Cell 22: 673-686.