Mitotic functions of the ran GTPase network: The importance of being in the right place at the right time

Cell Cycle

Volumn 3, Issue 3, 2004, Pages 305-313

  Di Fiore, Barbara ^a   Ciciarello, Marilena ^a   Lavia, Patrizia ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Cell transformation; Centrosome; Chromosome missegregation; Kinetochore; Ran GTPase network; Spindle pole

Indexed keywords

GUANOSINE TRIPHOSPHATASE; ONCOPROTEIN; RAN PROTEIN; VIRUS PROTEIN;

CARCINOGENESIS; CELL CYCLE; CELL NUCLEUS MEMBRANE; CENTROMERE; CENTROSOME; FUNGAL GENETICS; GENE INTERACTION; GENETIC STABILITY; GENOMIC INSTABILITY; MAMMAL CELL; MICROTUBULE; MITOSIS; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PROTEIN FUNCTION; REVIEW; RNA INTERFERENCE; SPINDLE POLE BODY; ANIMAL; HUMAN; METABOLISM; MITOSIS SPINDLE; NEOPLASM; PATHOLOGY;

MAMMALIA;

ANIMALS; CENTROSOME; HUMANS; MITOSIS; MITOTIC SPINDLE APPARATUS; NEOPLASMS; RAN GTP-BINDING PROTEIN;

EID: 4143086570     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: None     Document Type: Review

References (77)

1. Sazer S, Dasso M. The Ran decathlon: multiple roles of Ran. J Cell Sci 2000; 113:1111-8.
2. Clarke PR, Zhang C. Ran GTPase, a master regulator of nuclear structure and function during the eukaryotic cell division cycle? Trends Cell Biol 2001; 11:366-71.
3. Hetzer M, Gruss OJ, Mattaj IW. The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nat Cell Biol 2002; 4:E177-E184.
4. Weis K. Regulating access to the genome, nucleocytoplasmic transport throughout the cell cycle. Cell 2003; 112:441-51.
5. Ouspenski II, Mueller UW, Matynia A, Sazer S, Elledge SJ, Brinkley BR. Ran-binding protein-1 is an essential component of the Ran/RCC1 molecular switch system in budding yeast. J Biol Chem 1995; 270:1975-8.
6. Kirkpatrick D, Solomon F. Overexpression of yeast homologs of the mammalian checkpoint gene RCC1 suppresses the class of alpha-tubulin mutations that arrest with excess microtubules. Genetics 1994; 137:381-92.
7. Fleig U, Salus SS, Karig I, Sazer S. The fission yeast Ran GTPase is required for microtubule integrity. J Cell Biol 2000; 151:1101-1.
8. Salus SS, Demeter J, Sazer S. The Ran GTPase system in fission yeast affects microtubules and cytokinesis in cells that are competent for nucleocytoplasmic protein transport. Mol Cell Biol 2002; 22:8491-505.
9. Ouspenski II. A RanBP1 mutation which does not visibly affect nuclear import may reveal additional functions of the Ran GTPase system. Exp Cell Res 1998; 244:171-83.
10. Gonczy P, Echeverri C, Oegema K, Coulson A, Jones SJ, Copley RR et al. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 2000; 408:331-6.
11. Bamba C, Bobinnec Y, Fukuda M, Nishida E. The GTPase Ran regulates chromosome positioning and nuclear envelope assembly in vivo. Curr Biol 2002; 12:503-7.
12. Askjaer P, Galy V, Hannak E, Mattaj IW. Ran GTPase cycle and importing alpha and beta are essential for spindle formation and nuclear envelope assembly in living Caenorhabditis elegans embryos. Mol Biol Cell 2002; 13:4355-70.
13. Merdes A, Cleveland DW. Pathways of spindle pole formation, different mechanisms; conserved components. J Cell Biol 1997; 138:953-6.
14. Karsenti E, Vernos I. The mitotic spindle, a self-made machine. Science 2001; 294:543-7.
15. Carazo-Salas RE, Guarguaglini G, Gruss, OJ, Segref A, Karsenti E, Mattaj IW. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 1999; 400:178-81.
16. Kalab P, Pu RT, Dasso M. The Ran GTPase regulates mitotic spindle assembly. Curr Biol 1999; 9:481-4.
17. Ohba T, Nakamura M, Nishitani H, Nishimoto T. Self-organization of microtubule asters induced in Xenopus egg extracts by GTP-bound Ran. Science 1999; 284:1356-8.
18. Wilde A, Zheng Y. Stimulation of microtubule aster formation and spindle assembly by the small GTPase Ran. Science 1999; 284:1359-62.
19. Gruss OJ, Carazo-Salas, RE, Schatz CA, Guarguaglini G, Kast J, Wilm M et al. Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 2001; 104:83-93.
20. Nachury MV, Maresca TJ, Salmon WC, Waterman-Storer CM, Heald R, Weis K. Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 2001; 104:95-106.
21. Wiese C, Wilde A, Moore MS, Adam SA, Merdes A, Zheng Y. Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 2001; 291: 653-6.
22. Schatz CA, Santarella R, Hoenger A, Karsenti E, Mattaj IW, Gruss OJ, Carazo-Salas RE Importin alpha-regulated nucleation of microtubules by TPX2. EMBO J 2003; 22:2060-70.
23. Melchior F. Ran GTPase cycle: one mechanism, two functions. Curr Biol 2001; 11: R257-60.
24. Quimby BB, Dasso M. The small GTPase Ran: interpreting the signs. Curr Opin Cell Biol 2003; 15:338-44.
25. Khodjakov A, Rieder CL. Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J Cell Biol 2001; 153:237-42.
26. Hinchcliffe EH, Miller FJ, Cham M, Khodjakov A, Sluder G. Requirement of a centrosomal activity for cell cycle progression through G1 into S phase. Science 2001; 291:1547-50.
27. 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.
28. Sluder G, Thompson EA, Miller FJ, Hayes J, Rieder CL. The checkpoint control for anaphase onset does not monitor excess numbers of spindle poles or bipolar spindle symmetry. J Cell Sci 1997; 110:421-9.
29. Brinkley BR. Managing the centrosome numbers game, from chaos to stability in cancer cell division. Trends Cell Biol 2001; 11:18-21.
30. Doxsey SJ. Duplicating dangerously, linking centrosome duplication and aneuploidy. Mol. Cell. 2002; 10:439-40.
31. Nigg EA. Centrosome aberrations, cause or consequence of cancer progression? Nat Rev Cancer 2002; 2:815-25.
32. D'Assoro AB, Lingle WL, Salisbury JL. Centrosome amplification and the development of cancer. Oncogene 2002; 21:6146-53
33. De Luca A, Mangiacasale R, Severino A, Malquori L, Baldi A, Palena A et al. E1A deregulates the centrosome cycle in a Ran GTPase-dependent manner. Cancer Res 2003; 63:1430-7.
34. Duensing S, Lee LY, Duensing A, Basile J, Pibonniyom S, Gonzalez S, Crum CP, Munger K. The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. Proc Natl Acad Sci 2000; 97:10002-7.
35. Duensing S, Duensing A, Crum CP, Munger K. Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype. Cancer Res 2001; 61:2356-60.
36. Forgues M, Marrogi AJ, Spillare EA, Wu CG, Yang Q, Yoshida M, Wang XW. Interaction of the hepatitis B virus X protein with the Crm1-dependent nuclear export pathway. J Biol Chem 2001; 276:22797-803.
37. 'Forgues M, Difilippantonio MJ, Linke SP, Ried T, Nagashima K, Feden J et al. Involvement of Crm1 in hepatitis B virus X protein-induced aberrant centriole replication and abnormal mitotic spindles. Mol Cell Biol 2003; 23:5282-92.
38. 'Salisbury JL, Suino KM, Busby R, Springett M. Centrin-2 is required for centriole duplication in mammalian cells. Curr Biol 2002; 12:1287-92.
39. 'Doxsey SJ, Stein P, Evans L, Calarco PD. Kirschner M. Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 1994; 76:639-50.
40. Keryer G, Di Fiore B, Celati C, Lechtreck KF, Mogensen M, Delouvée A et al. Part of Ran is associated with AKAP450 at the centrosome. Involvement in microtubule organizing activity. Mol Biol Cell 2003; 14:4260-71.
41. Guarguaglini G, Renzi L, D'Ottavio F, Di Fiore B, Casenghi M, Cundari E, Lavia P. Regulated Ran-binding protein 1 activity is required for organization and function of the mitotic spindle in mammalian cells in vivo. Cell Growth Differ 2000; 11:455-65.
42. Moore W, Zhang C, Clarke PR. Targeting of RCC1 to chromosomes is required for proper mitotic spindle assembly in human cells. Curr Biol 2002; 12:1442-7.
43. Faruki S, Cole RW, Rieder CL. Separating centrosomes interact in the absence of associated chromosomes during mitosis in cultured vertebrate cells. Cell Motil Cytoskeleton 2002; 52:107-21.
44. Di Fiore B, Ciciarello M, Mangiacasale R, Palena A, Tassin AM, Cundari E, Lavia P. Mammalian RanBP1 regulates centrosome cohesion during mitosis. J Cell Sci 2003; 116:3399-411.
45. Smith AE, Slepchenko BM, Schaff JC, Loew LM, Macara IG. Systems analysis of Ran transport. Science 2002; 295:488-91.
46. Kalab P, Weis K, Heald R. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 2002; 295:2452-6.
47. Joseph J, Tan SH, Karpova TS, McNally JG, Dasso M. SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J Cell Biol 2002; 156:595-602.
48. Plafker K, Macara IG. Fluorescence resonance energy transfer biosensors that detect Ran conformational changes and a Ran x GDP-importin-beta -RanBP1 complex in vitro and in intact cells. J Biol Chem 2002; 277:30121-7.
49. Garrett S, Auer K, Compton DA, Kapoor TM. hTPX2 is required for normal spindle morphology and centrosome integrity during vertebrate cell division. Curr Biol 2002; 12:2055-59.
50. Gruss OJ, Wittmann M, Yokoyama H, Pepperkok R, Kufer T, Sillje H et al. Chromosome-induced microtubule assembly mediated by TPX2 is required for spindle formation in HeLa cells. Nat Cell Biol 2002; 4:871-9.
51. Hinkle B, Slepchenko B, Rolls MM, Walther TC, Stein PA, Mehlmann L et al. Chromosomal association of Ran during meiotic and mitotic divisions. J Cell Sci 2002; 115:4685-93.
52. Carazo-Salas RE, Gruss OJ, Mattaj IW, Karsenti E. Ran-GTP coordinates regulation of microtubule nucleation and dynamics during mitotic-spindle assembly. Nat Cell Biol 2001; 3:228-34.
53. Wilde A, Lizarraga SB, Zhang L, Wiese C, Gliksman NR, Walczak CE, Zheng Y. Ran stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nat Cell Biol 2001; 3:221-27.
54. Walczak CE, Vernos I, Mitchison TJ, Karsenti E, Heald R. A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity. Curr Biol 1998; 8:903-13.
55. Matunis MJ, Coutavas E, Blobel G. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP between the cytosol and the nuclear pore complex. J Cell Biol 1996; 135:1457-70.
56. Tsai MY, Wiese C, Cao K, Martin O, Donovan P, Ruderman J, Prigent C, Zheng Y. A Ran signaling pathway mediated by the mitotic Chinese Aurora A in spindle assembly. Nat Cell Biol 2003; 5:242-8.
57. Eyers PA, Erikson E, Chen LG, Maller JL. A novel mechanism for activation of the protein kinase Aurora A. Curr Biol 2003; 13:691-7.
58. Kufer TA, Sillje HH, Korner R, Gruss OJ, Meraldi P, Nigg EA. Human TPX2 is required for targeting Aurora-A kinase to the spindle. J Cell Biol 2002; 158:617-23.
59. Azuma Y, Hachiya T, Nishimoto T. Inhibition by anti-RCC1 monoclonal antibodies of RCC1-stimulated guanine nucleotide exchange on Ran GTPase. J Biochem (Tokyo) 1997; 122:1133-8.
60. Arnaoutov A, Dasso M. The Ran GTPase regulates kinetochore function. Dev Cell 2003; 5:99-111.
61. Salina D, Enarson P, Rattner JB, Burke B. Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J Cell Biol 2003; 162:991-1001.
62. Pichler A, Gast A, Seeler J S, Dejean A, Melchior F. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 2002; 108:109-20.
63. Saitoh H, Pu R, Cavenagh M, Dasso M. RanBP2 associates with Ubc9p and a modified form of RanGAP1. Proc Natl Acad Sci USA 1997; 94:3736-41.
64. Quimby BB, Wilson CA, Corbett AH. The interaction between Ran and NTF2 is required for cell cycle progression. Mol Biol Cell 2000; 11:2617-29.
65. Baumer M, Kunzler M, Steigemann P, Braus GH, Irniger S. Yeast Ran-binding protein Yrb1p is required for efficient proteolysis of cell cycle regulatory proteins Pds1p and Sic1p. J Biol Chem 2000; 275:38929-37.
66. Di Matteo G, Fuschi P, Zerfass K, Moretti S, Ricordy R, Cenciarelli C et al. Transcriptional control of the Htf9-a/RanBP-1 gene during the cell cycle. Cell Growth Differ 1995; 6:1213-24.
67. Di Fiore B, Guarguaglini G, Palena A, Kerkhoven RM, Bernards R, Lavia P. Two E2F sites control growth-regulated and cell cycle-regulated transcription of the Htf9-a/RanBP1 gene through functionally distinct mechanisms. J Biol Chem 1999; 274:10339-48.
68. Battistoni A, Guarguaglini G, Degrassi F, Pittoggi C, Palena A, Di Matteo G, et al Deregulated expression of the RanBP1 gene alters cell cycle progression in murine fibroblasts. J Cell Sci 1997; 110:2345-57.
69. Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M., Nevins JR. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cel. Biol 2001; 21:4684-99.
70. Guo QM, Malek RL, Kim S, Chiao C, He M, Ruffy M et al. Identification of c-myc responsive genes using rat cDNA microarray. Cancer Res 2000; 60: 5922-28.
71. Troyanskaya OG, Garber ME, Brown PO, Botstein D, Altman RB. Nonparametric methods for identifying differentially expressed genes in microarray data. Bioinformatics 2002; 18:1454-61.
72. Xu SH, Qian LJ, Mou HZ, Zhu CH, Zhou XM, Liu XL, et al. Difference of gene expression profiles between esophageal carcinoma and its pericancerous epithelium by gene chip. World J Gastroenterol 2003; 9:417-22.
73. Damm K, Hemmann U, Garin-Chesa P, Hauel N, Kauffmann I, Priepke H, et al. A highly selective telomerase inhibitor limiting human cancer cell proliferation. EMBO J 2001; 20: 6958-68.
74. Vanegas N, Garcia-Sacristan A, Lopez-Fernandez LA, Parraga M, del Mazo J, Hernandez P, et al. Differential expression of Ran GTPase during HMBA-induced differentiation in murine erythroleukemia cells. Leuk Res 2003; 27:607-15.
75. Tsuneoka M, Nakano F, Ohgusu H, Mekada E. c-myc activates RCC1 gene expression through E-box elements. Oncogene 1997; 14: 2301-11.
76. Tsuneoka M, Mekada E. N-myc transactivates RCC1 gene expression in rat fibroblast cells transformed by N-myc and v-ras. J Biochem (Tokyo) 1998; 124: 1013-19.
77. Fang CM, Shi C, Xu YH. Deregulated c-myc expression in quiescent CHO cells induces target gene transcription and subsequent apoptotic phenotype. Cell Res 1999; 9:305-14.