Learning about cancer from frogs: Analysis of mitotic spindles in Xenopus egg extracts

DMM Disease Models and Mechanisms

Volumn 2, Issue 11-12, 2009, Pages 541-547

  Cross, Marie K ^a   Powers, Maureen A ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; BUB3 PROTEIN; HEPATOMA UPREGULATED PROTEIN; KINESIN; MASKIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN EG5; PROTEIN MAD1; PROTEIN MAD2; PROTEIN RHAMM; PROTEIN TPX2; SECURIN; SURVIVIN; UNCLASSIFIED DRUG; XENOPUS PROTEIN;

ANAPHASE; CELL CYCLE REGULATION; CENTROMERE; DNA REPLICATION; HUMAN; METAPHASE; MITOSIS SPINDLE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; XENOPUS LAEVIS;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; MITOTIC SPINDLE APPARATUS; MODELS, BIOLOGICAL; NEOPLASMS; OOCYTES; XENOPUS LAEVIS;

ANURA;

EID: 70549100921     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.002022     Document Type: Review

References (90)

1. Abrieu, A., Kahana, J. A., Wood, K. W. and Cleveland, D. W. (2000). CENP-E as an essential component of the mitotic checkpoint in vitro. Cell 102, 817-826.
2. Altieri, D. C. (2008a). New wirings in the survivin networks. Oncogene 27, 6276-6284.
3. Altieri, D. C. (2008b). Survivin, cancer networks and pathway-directed drug discovery. Nat. Rev. Cancer 8, 61-70.
4. Arias, E. E. and Walter, J. C. (2004). Initiation of DNA replication in Xenopus egg extracts. Front Biosci. 9, 3029-3045.
5. Arnaoutov, A. and Dasso, M. (2005). Ran-GTP regulates kinetochore attachment in somatic cells. Cell Cycle 4, 1161-1165. (Pubitemid 41365383)
6. Blower, M. D., Nachury, M., Heald, R. and Weis, K. (2005). A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 121, 223-234. (Pubitemid 40546390)
7. Brunet, S., Sardon, T., Zimmerman, T., Wittmann, T., Pepperkok, R., Karsenti, E. and Vernos, I. (2004). Characterization of the TPX2 domains involved in microtubule nucleation and spindle assembly in Xenopus egg extracts. Mol. Biol. Cell 15, 5318-5328. (Pubitemid 39564727)
8. Carazo-Salas, R. E., Guarguaglini, G., Gruss, O. J., Segref, A., Karsenti, E. and Mattaj, I. W. (1999). Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 400, 178-181. (Pubitemid 29327548)
9. Casanova, C. M., Rybina, S., Yokoyama, H., Karsenti, E. and Mattaj, I. W. (2008). Hepatoma up-regulated protein is required for chromatin-induced microtubule assembly independently of TPX2. Mol. Biol. Cell 19, 4900-4908.
10. Castillo, A., Morse, H. C., 3rd, Godfrey, V. L., Naeem, R. and Justice, M. J. (2007). Overexpression of Eg5 causes genomic instability and tumor formation in mice. Cancer Res. 67, 10138-10147.
11. Chan, G. K., Liu, S. T. and Yen, T. J. (2005). Kinetochore structure and function. Trends Cell. Biol. 15, 589-598.
12. Chan, R. C. and Forbes, D. I. (2006). In vitro study of nuclear assembly and nuclear import using Xenopus egg extracts. Methods Mol. Biol. 322, 289-300.
13. Clarke, P. R. and Sanderson, H. S. (2006). A mitotic role for BRCA1/BARD1 in tumor suppression? Cell 127, 453-455.
14. Coe, B. P., Lee, E. H., Chi, B., Girard, L., Minna, J. D., Gazdar, A. F., Lam, S., MacAulay, C. and Lam, W. L. (2006). Gain of a region on 7p22.3, containing MAD1L1, is the most frequent event in small-cell lung cancer cell lines. Genes Chromosomes Cancer 45, 11-19. (Pubitemid 46930857)
15. Conte, N., Delaval, B., Ginestier, C., Ferrand, A., Isnardon, D., Larroque, C., Prigent, C., Seraphin, B., Jacquemier, J. and Birnbaum, D. (2003). TACC1- chTOG-Aurora A protein complex in breast cancer. Oncogene 22, 8102-8116. (Pubitemid 37487301)
16. Desai, A., Murray, A., Mitchison, T. J. and Walczak, C. E. (1999). The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. Methods Cell Biol. 61, 385-412.
17. Dhonukshe, P., Vischer, N. and Gadella, T. W., Jr (2006). Contribution of microtubule growth polarity and flux to spindle assembly and functioning in plant cells. J. Cell Sci. 119, 3193-3205.
18. Giet, R., Uzbekov, R., Cubizolles, F., Le Guellec, K. and Prigent, C. (1999). The Xenopus laevis aurora-related protein kinase pEg2 associates with and phosphorylates the kinesin-related protein XlEg5. J. Biol. Chem. 274, 15005-15013. (Pubitemid 129518834)
19. Grabsch, H., Takeno, S., Parsons, W. J., Pomjanski, N., Boecking, A., Gabbert, H. E. and Mueller, W. (2003). Overexpression of the mitotic checkpoint genes BUB1, BUBR1, and BUB3 in gastric cancer - association with tumour cell proliferation. J. Pathol. 200, 16-22. (Pubitemid 36592631)
20. Groen, A. C., Cameron, L. A., Coughlin, M., Miyamoto, D. T., Mitchison, T. J. and Ohi, R. (2004). XRHAMM functions in ran-dependent microtubule nucleation and pole formation during anastral spindle assembly. Curr. Biol. 14, 1801-1811. (Pubitemid 39408769)
21. Groen, A. C., Needleman, D., Brangwynne, C., Gradinaru, C., Fowler, B., Mazitschek, R. and Mitchison, T. J. (2008). A novel small-molecule inhibitor reveals a possible role of kinesin-5 in anastral spindle-pole assembly. J. Cell Sci. 121, 2293-2300.
22. Gruss, O. J., Carazo-Salas, R. E., Schatz, C. A., Guarguaglini, G., Kast, J., Wilm, M., Le Bot, N., Vernos, I., Karsenti, E. and Mattaj, I. W. (2001). Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 104, 83-93. (Pubitemid 32144974)
23. Hansen, G. M. and Justice, M. J. (1999). Activation of Hex and mEg5 by retroviral insertion may contribute to mouse B-cell leukemia. Oncogene 18, 6531-6539.
24. Heald, R., Tournebize, R., Blank, T., Sandaltzopoulos, R., Becker, P., Hyman, A. and Karsenti, E. (1996). Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382, 420-425. (Pubitemid 26264851)
25. Holland, A. J. and Cleveland, D. W. (2009). Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat. Rev. Mol. Cell. Biol. 10, 478-487.
26. Hoyt, M. A., Totis, L. and Roberts, B. T. (1991). S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66, 507-517. (Pubitemid 121001387)
27. Huang, Y. L., Chiu, A. W., Huan, S. K., Wang, Y. C., Ju, J. P. and Lu, C. L. (2003). Prognostic significance of hepatoma-up-regulated protein expression in patients with urinary bladder transitional cell carcinoma. Anticancer Res. 23, 2729-2733. (Pubitemid 36897151)
28. Jeganathan, K. B., Baker, D. J. and van Deursen, J. M. (2006). Securin associates with APCCdh1 in prometaphase but its destruction is delayed by Rae1 and Nup98 until the metaphase/anaphase transition. Cell Cycle 5, 366-370.
29. Joukov, V., Groen, A. C., Prokhorova, T., Gerson, R., White, E., Rodriguez, A., Walter, J. C. and Livingston, D. M. (2006). The BRCA1/BARD1 heterodimer modulates ran-dependent mitotic spindle assembly. Cell 127, 539-552. (Pubitemid 44647427)
30. Kalab, P. and Heald, R. (2008). The RanGTP gradient-a GPS for the mitotic spindle. J. Cell Sci. 121, 1577-1586. (Pubitemid 351911814)
31. Kalab, P., Pu, R. T. and Dasso, M. (1999). The ran GTPase regulates mitotic spindle assembly. Curr. Biol. 9, 481-484. (Pubitemid 29228620)
32. Karsenti, E., Newport, J. W., Hubble, R. and Kirschner, M. (1984). Interconversion of metaphase and interphase microtubule arrays, as studied by the injection of centrosomes and nuclei into Xenopus eggs. J. Cell Biol. 98, 1730-1745. (Pubitemid 14102599)
33. Kasai, T., Iwanaga, Y., Iha, H. and Jeang, K. T. (2002). Prevalent loss of mitotic spindle checkpoint in adult Tcell leukemia confers resistance to microtubule inhibitors. J. Biol. Chem. 277, 5187-5193. (Pubitemid 34968562)
34. Khodjakov, A., Cole, R. W., Oakley, B. R. and Rieder, C. L. (2000). Centrosome-independent mitotic spindle formation in vertebrates. Curr. Biol. 10, 59-67. (Pubitemid 30079190)
35. Kim, H. S., Park, K. H., Kim, S. A., Wen, J., Park, S. W., Park, B., Gham, C. W., Hyung, W. J., Noh, S. H., Kim, H. K. et al. (2005). Frequent mutations of human Mad2, but not Bub1, in gastric cancers cause defective mitotic spindle checkpoint. Mutat. Res. 578, 187-201. (Pubitemid 41395324)
36. Kinoshita, K., Noetzel, T. L., Pelletier, L., Mechtler, K., Drechsel, D. N., Schwager, A., Lee, M., Raff, J. W. and Hyman, A. A. (2005). Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J. Cell Biol. 170, 1047-1055. (Pubitemid 41362637)
37. Kirschner, M. and Mitchison, T. (1986). Beyond self-assembly: from microtubules to morphogenesis. Cell 45, 329-342.
38. Knauer, S. K., Bier, C., Habtemichael, N. and Stauber, R. H. (2006). The Survivin-Crm1 interaction is essential for chromosomal passenger complex localization and function. EMBO Rep. 7, 1259-1265. (Pubitemid 44835095)
39. Koffa, M. D., Casanova, C. M., Santarella, R., Kocher, T., Wilm, M. and Mattaj, I. W. (2006). HURP is part of a Ran-dependent complex involved in spindle formation. Curr. Biol. 16, 743-754.
40. Kops, G. J., Kim, Y., Weaver, B. A., Mao, Y., McLeod, I., Yates, J. R., 3rd, Tagaya, M. and Cleveland, D. W. (2005). ZW10 links mitotic checkpoint signaling to the structural kinetochore. J. Cell Biol. 169, 49-60.
41. Kufer, T. A., Sillje, H. H., Korner, R., Gruss, O. J., Meraldi, P. and Nigg, E. A. (2002). Human TPX2 is required for targeting Aurora-A kinase to the spindle. J. Cell Biol. 158, 617-623. (Pubitemid 34920101)
42. Lange, A., Mills, R. E., Lange, C. J., Stewart, M., Devine, S. E. and Corbett, A. H. (2007). Classical nuclear localization signals: definition, function, and interaction with importin alpha. J. Biol. Chem. 282, 5101-5105. (Pubitemid 47093710)
43. Li, M., Fang, X., Wei, Z., York, J. P. and Zhang, P. (2009). Loss of spindle assembly checkpoint-mediated inhibition of Cdc20 promotes tumorigenesis in mice. J. Cell Biol. 185, 983-994.
44. Liu, M., Yu, H., Huo, L., Liu, J., Li, M. and Zhou, J. (2008). Validating the mitotic kinesin Eg5 as a therapeutic target in pancreatic cancer cells and tumor xenografts using a specific inhibitor. Biochem. Pharmacol. 76, 169-178.
45. Lohka, M. J. and Masui, Y. (1983). The germinal vesicle material required for sperm pronuclear formation is located in the soluble fraction of egg cytoplasm. Exp. Cell Res. 148, 481-491.
46. Lohka, M. J. and Maller, J. L. (1985). Induction of nuclear envelope breakdown, chromosome condensation, and spindle formation in cell-free extracts. J. Cell Biol. 101, 518-523.
47. Lu, Y., Wang, Z., Ge, L., Chen, N. and Liu, H. (2009). The RZZ complex and the spindle assembly checkpoint. Cell Struct. Funct. 34, 31-45.
48. Masui, Y. and Markert, C. L. (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177, 129-145.
49. Maxwell, C. A., McCarthy, J. and Turley, E. (2008). Cell-surface and mitotic-spindle RHAMM: moonlighting or dual oncogenic functions? J. Cell Sci. 121, 925-932. (Pubitemid 351639411)
50. Mayer, T. U., Kapoor, T. M., Haggarty, S. J., King, R. W., Schreiber, S. L. and Mitchison, T. J. (1999). Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974. (Pubitemid 33594038)
51. Mita, A. C., Mita, M. M., Nawrocki, S. T. and Giles, F. J. (2008). Survivin: key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin. Cancer Res. 14, 5000-5005.
52. Mitchison, T. J., Maddox, P., Groen, A., Cameron, L., Perlman, Z., Ohi, R., Desai, A., Salmon, E. D. and Kapoor, T. M. (2004). Bipolarization and poleward flux correlate during Xenopus extract spindle assembly. Mol. Biol. Cell 15, 5603-5615. (Pubitemid 39564751)
53. Miyamoto, D. T., Perlman, Z. E., Burbank, K. S., Groen, A. C. and Mitchison, T. J. (2004). The kinesin Eg5 drives poleward microtubule flux in Xenopus laevis egg extract spindles. J. Cell Biol. 167, 813-818.
54. Morgan-Lappe, S. E., Tucker, L. A., Huang, X., Zhang, Q., Sarthy, A. V., Zakula, D., Vernetti, L., Schurdak, M., Wang, J. and Fesik, S. W. (2007). Identification of Ras-related nuclear protein, targeting protein for xenopus kinesin-like protein 2, and stearoyl-CoA desaturase 1 as promising cancer targets from an RNAi-based screen. Cancer Res. 67, 4390-4398. (Pubitemid 46815088)
55. Murray, A. W. (1991). Coordinating cell cycle events. Cold Spring Harb. Symp. Quant. Biol. 56, 399-408.
56. Musacchio, A. and Salmon, E. D. (2007). The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell. Biol. 8, 379-393.
57. Nachury, M. V., Maresca, T. J., Salmon, W. C., Waterman-Storer, C. M., Heald, R. and Weis, K. (2001). Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104, 95-106. (Pubitemid 32144975)
58. Nakai, R., Iida, S., Takahashi, T., Tsujita, T., Okamoto, S., Takada, C., Akasaka, K., Ichikawa, S., Ishida, H., Kusaka, H. et al. (2009). K858, a novel inhibitor of mitotic kinesin Eg5 and antitumor agent, induces cell death in cancer cells. Cancer Res. 69, 3901-3909.
59. O'Brien, L. L., Albee, A. J., Liu, L., Tao, W., Dobrzyn, P., Lizarraga, S. B. and Wiese, C. (2005). The Xenopus TACC homologue, maskin, functions in mitotic spindle assembly. Mol. Biol. Cell 16, 2836-2847. (Pubitemid 40741228)
60. O'Connell, C. B. and Khodjakov, A. L. (2007). Cooperative mechanisms of mitotic spindle formation. J. Cell Sci. 120, 1717-1722.
61. Ohba, T., Nakamura, M., Nishitani, H. and Nishimoto, T. (1999). Self-organization of microtubule asters induced in Xenopus egg extracts by GTP-bound Ran. Science 284, 1356-1358. (Pubitemid 29289661)
62. Pesin, J. A. and Orr-Weaver, T. L. (2008). Regulation of APC/C activators in mitosis and meiosis. Annu. Rev. Cell Dev. Biol. 24, 475-499.
63. Philpott, A. and Yew, P. R. (2008). The Xenopus cell cycle: an overview. Mol. Biotechnol. 39, 9-19.
64. Pollard, J. R. and Mortimore, M. (2009). Discovery and development of aurora kinase inhibitors as anticancer agents. J. Med. Chem. 52, 2629-2651.
65. Rello-Varona, S., Vitale, I., Kepp, O., Senovilla, L., Jemaa, M., Metivier, D., Castedo, M. and Kroemer, G. (2009). Preferential killing of tetraploid tumor cells by targeting the mitotic kinesin Eg5. Cell Cycle 8, 1030-1035.
66. Ruben, L. N., Clothier, R. H. and Balls, M. (2007). Cancer resistance in amphibians. Altern. Lab. Anim. 35, 463-470.
67. Ruchaud, S., Carmena, M. and Earnshaw, W. C. (2007). Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell. Biol. 8, 798-812. (Pubitemid 47462135)
68. Ryan, B. M., O'Donovan, N. and Duffy, M. J. (2009). Survivin: A new target for anti-cancer therapy. Cancer Treat. Rev. Jun 24 [Epub ahead of print] [doi:10.1016/j.ctrv.2009.05.003].
69. Salehi, F., Kovacs, K., Scheithauer, B. W., Lloyd, R. V. and Cusimano, M. (2008). Pituitary tumortransforming gene in endocrine and other neoplasms: a review and update. Endocr. Relat. Cancer 15, 721-743.
70. Sawin, K. E. and Mitchison, T. J. (1991). Poleward microtubule flux mitotic spindles assembled in vitro. J. Cell Biol. 112, 941-954.
71. Sawin, K. E., LeGuellec, K., Philippe, M. and Mitchison, T. J. (1992). Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359, 540-543.
72. Shirasu-Hiza, M., Perlman, Z. E., Wittmann, T., Karsenti, E. and Mitchison, T. J. (2004). Eg5 causes elongation of meiotic spindles when flux-associated microtubule depolymerization is blocked. Curr. Biol. 14, 1941-1945. (Pubitemid 39464818)
73. Sudakin, V., Chan, G. K. and Yen, T. J. (2001). Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J. Cell Biol. 154, 925-936. (Pubitemid 34286173)
74. Tonon, G., Wong, K. K., Maulik, G., Brennan, C., Feng, B., Zhang, Y., Khatry, D. B., Protopopov, A., You, M. J., Aguirre, A. J. et al. (2005). High-resolution genomic profiles of human lung cancer. Proc. Natl. Acad. Sci. USA 102, 9625-9630. (Pubitemid 40981731)
75. Toole, B. P. (2004). Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 4, 528-539.
76. Tsai, M. Y., Wiese, C., Cao, K., Martin, O., Donovan, P., Ruderman, J., Prigent, C. and Zheng, Y. (2003). A Ran signalling pathway mediated by the mitotic kinase Aurora A in spindle assembly. Nat. Cell Biol. 5, 242-248. (Pubitemid 36322252)
77. Tsou, A. P., Yang, C. W., Huang, C. Y., Yu, R. C., Lee, Y. C., Chang, C. W., Chen, B. R., Chung, Y. F., Fann, M. J., Chi, C. W. et al. (2003). Identification of a novel cell cycle regulated gene, HURP, overexpressed in human hepatocellular carcinoma. Oncogene 22, 298-307.
78. Walczak, C. E. and Heald, R. (2008). Mechanisms of mitotic spindle assembly and function. Int. Rev. Cytol. 265, 111-158. (Pubitemid 351215987)
79. Walczak, C. E., Mitchison, T. J. and Desai, A. (1996). XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell 84, 37-47.
80. Wang, Y. C., Lee, Y. H., Huang, G. C., Lin, Y. H., Fan-Chiang, M. H., Chiu, A. W. and Huang, Y. L. (2006). Enhanced transformation and chemosensitivity of NIH3T3 cells transduced with hepatoma up-regulated protein. Biochem. Biophys. Res. Commun. 340, 244-249.
81. Wiese, C., Wilde, A., Moore, M. S., Adam, S. A., Merdes, A. and Zheng, Y. (2001). Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 291, 653-656. (Pubitemid 32150424)
82. Wilde, A. and Zheng, Y. (1999). Stimulation of microtubule aster formation and spindle assembly by the small GTPase Ran. Science 284, 1359-1362. (Pubitemid 29289662)
83. Wilde, A., Lizarraga, S. B., Zhang, L., Wiese, C., Gliksman, N. R., Walczak, C. E. and Zheng, Y. (2001). Ran stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nat. Cell. Biol. 3, 221-227. (Pubitemid 32201316)
84. Wittmann, T., Wilm, M., Karsenti, E. and Vernos, I. (2000). TPX2, A novel xenopus MAP involved in spindle pole organization. J. Cell Biol. 149, 1405-1418. (Pubitemid 30437615)
85. Wong, J., Lerrigo, R., Jang, C. Y. and Fang, G. (2008). Aurora A regulates the activity of HURP by controlling the accessibility of its microtubule-binding domain. Mol. Biol. Cell 19, 2083-2091.
86. Wood, K. W., Sakowicz, R., Goldstein, L. S. and Cleveland, D. W. (1997). CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment. Cell 91, 357-366. (Pubitemid 27467966)
87. Wu, J. Q. and Kornbluth, S. (2008). Across the meiotic divide-CSF activity in the post-Emi2/XErp1 era. J. Cell Sci. 121, 3509-3514.
88. Yu, C. T., Hsu, J. M., Lee, Y. C., Tsou, A. P., Chou, C. K. and Huang, C. Y. (2005). Phosphorylation and stabilization of HURP by Aurora-A: implication of HURP as a transforming target of Aurora-A. Mol. Cell. Biol. 25, 5789-5800.
89. Yuan, B., Xu, Y., Woo, J. H., Wang, Y., Bae, Y. K., Yoon, D. S., Wersto, R. P., Tully, E., Wilsbach, K. and Gabrielson, E. (2006). Increased expression of mitotic checkpoint genes in breast cancer cells with chromosomal instability. Clin. Cancer Res. 12, 405-410. (Pubitemid 43166128)
90. Zhang, C., Hughes, M. and Clarke, P. R. (1999). Ran- GTP stabilises microtubule asters and inhibits nuclear assembly in Xenopus egg extracts. J. Cell Sci. 112, 2453-2461. (Pubitemid 29381035)