RABL6A, a novel RAB-like protein, controls centrosome amplification and chromosome instability in primary

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Zhang, Xuefeng ^a,e   Hagen, Jussara ^a   Muniz, Viviane P ^b   Smith, Tarik ^a   Coombs, Gary S ^c   Eischen, Christine M ^d   Mackie, Duncan I ^b   Roman, David L ^b   Van Rheeden, Richard ^a   Darbro, Benjamin ^a   Tompkins, Van S ^a   Quelle, Dawn E ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c Waldorf College   (United States)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; NUCLEAR PROTEIN; NUCLEOPHOSMIN; PROTEIN P53; RAB PROTEIN; RABL6A PROTEIN, MOUSE;

ANIMAL; CENTROSOME; CHROMOSOMAL INSTABILITY; FIBROBLAST; GENE INACTIVATION; GENE SILENCING; GENETICS; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY;

ADP-RIBOSYLATION FACTORS; ANIMALS; CENTROSOME; CHROMOSOMAL INSTABILITY; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; GENE SILENCING; HUMANS; MICE; NUCLEAR PROTEINS; RAB GTP-BINDING PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84894242838     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080228     Document Type: Article

References (54)

1. Nigg EA, Raff JW (2009) Centrioles, Centrosomes, and Cilia in Health and Disease. Cell 139: 663-678.
2. Pihan GA, Wallace J, Zhou Y, Doxsey SJ (2003) Centrosome Abnormalities and Chromosome Instability Occur Together in Pre-invasive Carcinomas. Cancer Research 63: 1398-1404. (Pubitemid 36348723)
3. Fukasawa K (2007) Oncogenes and tumour suppressors take on centrosomes. Nature Reviews Cancer 7: 911-924.
4. D'Assoro AB, Lingle WL, Salisbury JL (2002) Centrosome amplification and the development of cancer. Oncogene 21: 6146-6153.
5. Lingle WL, Barrett SL, Negron VC, D'Assoro AB, Boeneman K, et al. (2002) Centrosome amplification drives chromosomal instability in breast tumor development. Proceedings of the National Academy of Sciences of the United States of America 99: 1978-1983. (Pubitemid 34169000)
6. Doxsey S, Zimmerman W, Mikule K (2005) Chromosome segregation and aneuploidy series: Centrosome control of the cell. Trends in Cell Biology 15: 303-311.
7. Lengauer C, Kinzler KW, Vogelstein B (1998) Genetic instabilities in human cancers. Nature 396: 643-649. (Pubitemid 29003936)
8. Zeng X, Shaikh FY, Harrison MK, Adon AM, Trimboli AJ, et al. (2010) The Ras oncogene signals centrosome amplification in mammary epithelial cells through cyclin D1/Cdk4 and Nek2. Oncogene 29: 5103-5112.
9. Okuda M, Horn HF, Tarapore P, Tokuyama Y, Smulian AG, et al. (2000) Nucleophosmin/B23 is a target of CDK2/Cyclin E in centrosome duplication. Cell 103: 127-140.
10. Grisendi S, Mecucci C, Falini B, Pandolfi PP (2006) Nucleophosmin and cancer. Nature Reviews Cancer 6: 493-505. (Pubitemid 43980539)
11. Acilan C, Saunders WS (2008) A tale of too many centrosomes. Cell 134: 572-575.
12. Hainaut P, Soussi T, Shomer B, Hollstein M, Greenblatt M, et al. (1997) Database of p53 gene somatic mutations in human tumors and cell lines: updated compilation and future prospects. Nucleic Acids Research 25: 151-157. (Pubitemid 27303173)
13. Ruas M, Peters G (1998) The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochimica et Biophysica Acta 1378: F115-177. (Pubitemid 28530512)
14. Sherr CJ (2006) Divorcing ARF and p53: an unsettled case. Nature Reviews Cancer 6: 663-673.
15. Sherr CJ, McCormick F (2002) The RB and p53 pathways in cancer. Cancer Cell 2: 103-112. (Pubitemid 41039110)
16. Fukasawa K, Choi T, Kuriyama R, Rulong S, Vande Woude GF (1996) Abnormal centrosome amplification in the absence of p53. Science 271: 1744-1747. (Pubitemid 26102826)
17. di Tommaso A, Hagen J, Tompkins V, Muniz V, Dudakovic A, et al. (2009) Residues in the alternative reading frame tumor suppressor that influence its stability and p53-independent activities. Experimental Cell Research 315: 1326-1335.
18. Tompkins V, Hagen J, Zediak VP, Quelle DE (2006) Identification of novel ARF binding proteins by two-hybrid screening. Cell Cycle 5: 641-646.
19. Montalbano J, Jin WX, Sheikh MS, Huang Y (2007) RBEL1 is a novel gene that encodes a nucleocytoplasmic ras superfamily GTP-binding protein and is overexpressed in breast cancer. Journal of Biological Chemistry 282: 37640-37649.
20. Montalbano J, Lui K, Sheikh MS, Huang Y (2009) Identification and Characterization of RBEL1 Subfamily of GTPases in the Ras Superfamily Involved in Cell Growth Regulation. Journal of Biological Chemistry 284: 18129-18142.
21. Muniz VP, Askeland RW, Zhang X, Reed SM, Tompkins VS, et al. (2013) RABL6A Promotes Oxaliplatin Resistance in Tumor Cells and Is a New Marker of Survival for Resected Pancreatic Ductal Adenocarcinoma Patients. Genes & Cancer 4: 273-284.
22. Li Y-Y, Fu S, Wang X-P, Wang H-Y, Zeng M-S, et al. (2013) Down-Regulation of C9orf86 in Human Breast Cancer Cells Inhibits Cell Proliferation, Invasion and Tumor Growth and Correlates with Survival of Breast Cancer Patients. PLoS ONE 8: e71764.
23. Weber JD, Jeffers JR, Rehg JE, Randle DH, Lozano G, et al. (2000) p53-independent functions of the p19ARF tumor suppressor. Genes & Development 14: 2358-2365.
24. Tompkins VS, Hagen J, Frazier AA, Lushnikova T, Fitzgerald MP, et al. (2007) A Novel Nuclear Interactor of ARF and MDM2 (NIAM) That Maintains Chromosomal Stability. Journal of Biological Chemistry 282: 1322-1333. (Pubitemid 47076587)
25. Quelle DE, Zindy F, Ashmun RA, Sherr CJ (1995) Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 83: 993-1000. (Pubitemid 26006540)
26. Korgaonkar C, Zhao L, Modestou M, Quelle DE (2002) ARF function does not require p53 stabilization or Mdm2 relocalization. Molecular and Cellular Biology 22: 196-206. (Pubitemid 33144268)
27. Korgaonkar C, Hagen J, Tompkins V, Frazier AA, Allamargot C, et al. (2005) Nucleophosmin (B23) Targets ARF to Nucleoli and Inhibits Its Function. Molecular and Cellular Biology 25: 1258-1271. (Pubitemid 40204905)
28. Mendez J, Stillman B (2000) Chromatin Association of Human Origin Recognition Complex, Cdc6, and Minichromosome Maintenance Proteins during the Cell Cycle: Assembly of Prereplication Complexes in Late Mitosis. Mol Cell Biol 20: 8602-8612.
29. Prosser SL, Straatman KR, Fry AM (2009) Molecular Dissection of the Centrosome Overduplication Pathway in S-Phase-Arrested Cells. Molecular and Cellular Biology 29: 1760-1773.
30. Matsushime H, Quelle DE, Shurtleff SA, Shibuya M, Sherr CJ, et al. (1994) D-type cyclin-dependent kinase activity in mammalian cells. Molecular and Cellular Biology 14: 2066-2076. (Pubitemid 24074604)
31. Li M, Fang X, Wei Z, York JP, Zhang P (2009) Loss of spindle assembly checkpoint-mediated inhibition of Cdc20 promotes tumorigenesis in mice. The Journal of Cell Biology 185: 983-994.
32. Wang P, Greiner TC, Lushnikova T, Eischen CM (2006) Decreased Mdm2 expression inhibits tumor development induced by loss of ARF. Oncogene 25: 3708-3718. (Pubitemid 43980492)
33. Fukasawa K (2008) p53, cyclin-dependent kinase and abnormal amplification of centrosomes. Biochimica Et Biophysica Acta-Reviews on Cancer 1786: 15-23.
34. Itahana K, Bhat KP, Jin AW, Itahana Y, Hawke D, et al. (2003) Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Molecular Cell 12: 1151-1164. (Pubitemid 37487925)
35. Brady SN, Yu Y, Maggi LB Jr., Weber JD (2004) ARF Impedes NPM/B23 Shuttling in an Mdm2-Sensitive Tumor Suppressor Pathway. Molecular and Cellular Biology 24: 9327-9338. (Pubitemid 39391671)
36. Stewart S, Fang GW (2005) Destruction box-dependent degradation of Aurora B is mediated by the anaphase-promoting complex/cyclosome and Cdh1. Cancer Research 65: 8730-8735. (Pubitemid 41377361)
37. Lens SMA, Voest EE, Medema RH (2010) Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nature Reviews Cancer 10: 825-841.
38. Meraldi P, Honda R, Nigg EA (2002) Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53(-/-) cells. EMBO Journal 21: 483-492. (Pubitemid 34174030)
39. Tokuyama Y, Horn HF, Kawamura K, Tarapore P, Fukasawa K (2001) Specific phosphorylation of nucleophosmin on Thr(199) by cyclin-dependent kinase 2-cyclin E and its role in centrosome duplication. Journal of Biological Chemistry 276: 21529-21537.
40. Stott FJ, Bates S, James MC, McConnell BB, Starborg M, et al. (1998) The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO Journal 17: 5001-5014. (Pubitemid 28408466)
41. Llanos S, Clark PA, Rowe J, Peters G (2001) Stabilisation of p53 by p14ARF without relocalization of Mdm2 to the nucleolus. Nature Cell Biology 3: 445-452. (Pubitemid 32422079)
42. Reef S, Zalckvar E, Shifman O, Bialik S, Sabanay H, et al. (2006) A Short Mitochondrial Form of p19ARF Induces Autophagy and Caspase-Independent Cell Death. Molecular Cell 22: 463-475.
43. Itahana K, Zhang Y (2008) Mitochondrial p32 Is a Critical Mediator of ARF-Induced Apoptosis. Cancer Cell 13: 542-553. (Pubitemid 351763900)
44. Adon AM, Zeng XB, Harrison MK, Sannem S, Kiyokawa H, et al. (2010) Cdk2 and Cdk4 Regulate the Centrosome Cycle and Are Critical Mediators of Centrosome Amplification in p53-Null Cells. Molecular and Cellular Biology 30: 694-710.
45. Cui YP, Wang JB, Zhang XY, Bi MX, Guo LP, et al. (2003) Using yeast two-hybrid system to identify ECRG2 associated proteins and their possible interactions with ECRG2 gene. World Journal of Gastroenterology 9: 1892-1896.
46. Cheng XL, Shen Z, Yang JY, Lu SH, Cui YP (2008) ECRG2 disruption leads to centrosome amplification and spindle checkpoint defects contributing chromosome instability. Journal of Biological Chemistry 283: 5888-5898.
47. Song MS, Song SJ, Ayad NG, Chang JS, Lee JH, et al. (2004) The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex. Nature Cell Biology 6: 129-+.
48. Young J, Menetrey J, Goud B (2010) RAB6C Is a Retrogene that Encodes a Centrosomal Protein Involved in Cell Cycle Progression. Journal of Molecular Biology 397: 69-88.
49. Fukasawa K (2011) Aberrant Activation of Cell Cycle Regulators, Centrosome Amplification, and Mitotic Defects. Hormones and Cancer 2: 104-112.
50. Ma Z, Kanai M, Kawamura K, Kaibuchi K, Ye K, et al. (2006) Interaction between ROCK II and nucleophosmin/B23 in the regulation of centrosome duplication. Molecular and Cellular Biology 26: 9016-9034. (Pubitemid 44851958)
51. Hanashiro K, Brancaccio M, Fukasawa K (2011) Activated ROCK II by-passes the requirement of the CDK2 activity for centrosome duplication and amplification. Oncogene 30: 2188-2197.
52. Melo AN, Eischen CM (2012) Protecting the Genome from Mdm2 and Mdmx. Genes & Cancer 3: 283-290.
53. Matijasevic Z, Steinman HA, Hoover K, Jones SN (2008) MdmX Promotes Bipolar Mitosis To Suppress Transformation and Tumorigenesis in p53-Deficient Cells and Mice. Molecular and Cellular Biology 28: 1265-1273. (Pubitemid 351214129)
54. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, et al. (2007) Oncomine 3.0: Genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 9: 166-180.