Vascular smooth muscle cell polyploidization involves changes in chromosome passenger proteins and an endomitotic cell cycle

Experimental Cell Research

Volumn 305, Issue 2, 2005, Pages 277-291

  Nagata, Yuka ^a,b   Jones, Matthew R ^c   Nguyen, Hao G ^c   McCrann, Donald J ^c   St Hilaire, Cynthia ^c   Schreiber, Barbara M ^c   Hashimoto, Atsushi ^a,b   Inagaki, Masaki ^d   Earnshaw, William C ^e   Todokoro, Kazuo ^b   Ravid, Katya ^c  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b RIKEN   (Japan)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d AICHI CANCER CENTER HOSPITAL   (Japan)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Aurora B; Cell cycle; Chromosome passenger protein; Endomitosis; Polyploid; Survivin; Time lapse imaging; Vascular smooth muscle

Indexed keywords

AURORA B KINASE; CHROMOSOME PROTEIN; PROTEIN SUBUNIT; SURVIVIN; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL TISSUE; ARTICLE; CELL CYCLE; CENTROMERE; CHROMOSOME; CONTROLLED STUDY; CYTOKINESIS; IMMUNOFLUORESCENCE; MITOSIS; NONHUMAN; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SEGREGATION ANALYSIS; SEPARATION TECHNIQUE; SISTER CHROMATID; VASCULAR SMOOTH MUSCLE;

EID: 20144389459     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.12.028     Document Type: Article

References (48)

1. K. Ravid, J. Lu, J.M. Zimmet, and M.R. Jones Roads to polyploidy: the megakaryocyte example J. Cell. Physiol. 190 2002 7 20
2. T. Galitski, A.J. Saldanha, C.A. Styles, E.S. Lander, and G.R. Fink Ploidy regulation of gene expression Science 285 1999 251 254
3. M.R. Jones, and K. Ravid Vascular smooth muscle polyploidization as a biomarker for aging and its impact on differential gene expression J. Biol. Chem. 279 2004 5306 5313
4. J. Zimmet, and K. Ravid Polyploidy: occurrence in nature, mechanisms, and significance for the megakaryocyte-platelet system Exp. Hematol. 28 2000 3 16
5. B.A. Edgar, and T.L. Orr-Weaver Endoreplication cell cycles: more for less Cell 105 2001 297 306
6. L. Geitler Endomitose and endomitotische poltploidisierung Protoplasmatology 6 1953 1
7. Y. Nagata, Y. Muro, and K. Todokoro Thrombopoietin-induced polyploidization of bone marrow megakaryocytes is due to a unique regulatory mechanism in late mitosis J. Cell Biol. 139 1997 449 457
8. R.R. Adams, M. Carmena, and W.C. Earnshaw Chromosomal passengers and the (aurora) ABCs of mitosis Trends Cell Biol. 11 2001 49 54
9. C.A. Cooke, M.M. Heck, and W.C. Earnshaw The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis J. Cell Biol. 105 1987 2053 2067
10. Y. Terada, M. Tatsuka, F. Suzuki, Y. Yasuda, S. Fujita, and M. Otsu AIM-1: a mammalian midbody-associated protein required for cytokinesis EMBO J. 17 1998 667 676
11. J.R. Bischoff, and G.D. Plowman The Aurora/Ipl1p kinase family: regulators of chromosome segregation and cytokinesis Trends Cell Biol. 9 1999 454 459
12. R. Giet, and C. Prigent Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases J. Cell Sci. 112 Pt. 21 1999 3591 3601
13. G. Ambrosini, C. Adida, and D.C. Altieri A novel anti-apoptosis gene, Survivin, expressed in cancer and lymphoma Nat. Med. 3 1997 917 921
14. R. Gassmann, A. Carvalho, A.J. Henzing, S. Ruchaud, D.F. Hudson, R. Honda, E.A. Nigg, D.L. Gerloff, and W.C. Earnshaw Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle J. Cell Biol. 166 2004 179 191
15. S.C. Sampath, R. Ohi, O. Leismann, A. Salic, A. Pozniakovski, and H. Funabiki The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly Cell 118 2004 187 202
16. S.P. Wheatley, A. Carvalho, P. Vagnarelli, and W.C. Earnshaw INCENP is required for proper targeting of Survivin to the centromeres and the anaphase spindle during mitosis Curr. Biol. 11 2001 886 890
17. M. Murata-Hori, and Y.L. Wang The kinase activity of aurora B is required for kinetochore-microtubule interactions during mitosis Curr. Biol. 12 2002 894 899
18. M. Murata-Hori, M. Tatsuka, and Y.L. Wang Probing the dynamics and functions of aurora B kinase in living cells during mitosis and cytokinesis Mol. Biol. Cell 13 2002 1099 1108
19. Y.L. Wang The mechanism of cytokinesis: reconsideration and reconciliation Cell Struct. Funct. 26 2001 633 638
20. S.M. Cutts, K.J. Fowler, B.T. Kile, L.L. Hii, R.A. O'Dowd, D.F. Hudson, R. Saffery, P. Kalitsis, E. Earle, and K.H. Choo Defective chromosome segregation, microtubule bundling and nuclear bridging in inner centromere protein gene (Incenp)-disrupted mice Hum. Mol. Genet. 8 1999 1145 1155
21. A.G. Uren, L. Wong, M. Pakusch, K.J. Fowler, F.J. Burrows, D.L. Vaux, and K.H. Choo Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype Curr. Biol. 10 2000 1319 1328
22. R. Honda, R. Korner, and E.A. Nigg Exploring the functional interactions between Aurora B, INCENP, and Survivin in mitosis Mol. Biol. Cell 14 2003 3325 3341
23. M.P. McMahon, B. Faris, B.L. Wolfe, K.E. Brown, C.A. Pratt, P. Toselli, and C. Franzblau Aging effects on the elastin composition in the extracellular matrix of cultured rat aortic smooth muscle cells In Vitro Cell. Dev. Biol. 21 1985 674 680
24. R. Yaar, L.M. Cataldo, A. Tzatsos, C.E. Francis, Z. Zhao, and K. Ravid Regulation of the A3 adenosine receptor gene in vascular smooth muscle cells: role of a cAMP and GATA element Mol. Pharmacol. 62 2002 1167 1176
25. Y. Muro, K. Sugimoto, T. Okazaki, and M. Ohashi The heterogeneity of anticentromere antibodies in immunoblotting analysis J. Rheumatol. 17 1990 1042 1047
26. D.M. Eckley, A.M. Ainsztein, A.M. Mackay, I.G. Goldberg, and W.C. Earnshaw Chromosomal proteins and cytokinesis: patterns of cleavage furrow formation and inner centromere protein positioning in mitotic heterokaryons and mid-anaphase cells J. Cell Biol. 136 1997 1169 1183
27. Y. Yasui, H. Goto, S. Matsui, E. Manser, L. Lim, K. Nagata, and M. Inagaki Protein kinases required for segregation of vimentin filaments in mitotic process Oncogene 20 2001 2868 2876
28. Y. Zhang, Z. Wang, D.X. Liu, M. Pagano, and K. Ravid Ubiquitin-dependent degradation of cyclin B is accelerated in polyploid megakaryocytes J. Biol. Chem. 273 1998 1387 1392
29. E.H. Tate, M.E. Wilder, L.S. Cram, and W. Wharton A method for staining 3T3 cell nuclei with propidium iodide in hypotonic solution Cytometry 4 1983 211 215
30. R.M. Lee, R.B. Conyers, and C.Y. Kwan Incidence of multinucleated and polyploid aortic smooth muscle cells cultured from different age groups of spontaneously hypertensive rats Can. J. Physiol. Pharmacol. 70 1992 1496 1501
31. G.K. Owens Differential effects of antihypertensive drug therapy on vascular smooth muscle cell hypertrophy, hyperploidy, and hyperplasia in the spontaneously hypertensive rat Circ. Res. 56 1985 525 536
32. M.L. Hixon, C. Muro-Cacho, M.W. Wagner, C. Obejero-Paz, E. Millie, Y. Fujio, Y. Kureishi, T. Hassold, K. Walsh, and A. Gualberto Akt1/PKB upregulation leads to vascular smooth muscle cell hypertrophy and polyploidization J. Clin. Invest. 106 2000 1011 1020
33. J. Chen, S. Jin, S.K. Tahir, H. Zhang, X. Liu, A.V. Sarthy, T.P. McGonigal, Z. Liu, S.H. Rosenberg, and S.C. Ng Survivin enhances Aurora-B kinase activity and localizes Aurora-B in human cells J. Biol. Chem. 278 2003 486 490
34. M.A. Bolton, W. Lan, S.E. Powers, M.L. McCleland, J. Kuang, and P.T. Stukenberg Aurora B kinase exists in a complex with Survivin and INCENP and its kinase activity is stimulated by Survivin binding and phosphorylation Mol. Biol. Cell 13 2002 3064 3077
35. H. Goto, Y. Yasui, A. Kawajiri, E.A. Nigg, Y. Terada, M. Tatsuka, K. Nagata, and M. Inagaki Aurora-B regulates the cleavage furrow-specific vimentin phosphorylation in the cytokinetic process J. Biol. Chem. 278 2003 8526 8530
36. C. Crosio, G.M. Fimia, R. Loury, M. Kimura, Y. Okano, H. Zhou, S. Sen, C.D. Allis, and P. Sassone-Corsi Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases Mol. Cell. Biol. 22 2002 874 885
37. Y. Tintut, Z. Alfonso, T. Saini, K. Radcliff, K. Watson, K. Bostrom, and L.L. Demer Multilineage potential of cells from the artery wall Circulation 108 2003 2505 2510
38. A. Khodjakov, and C.L. Rieder Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression J. Cell Biol. 153 2001 237 242
39. J.K. Schweitzer, and C. D'Souza-Schorey Localization and activation of the ARF6 GTPase during cleavage furrow ingression and cytokinesis J. Biol. Chem. 277 2002 27210 27216
40. M.T. Parra, A. Viera, R. Gomez, J. Page, M. Carmena, W.C. Earnshaw, J.S. Rufas, and J.A. Suja Dynamic relocalization of the chromosomal passenger complex proteins inner centromere protein (INCENP) and aurora-B kinase during male mouse meiosis J. Cell Sci. 116 2003 961 974
41. A. Temme, M. Rieger, F. Reber, D. Lindemann, B. Weigle, P. Diestelkoetter-Bachert, G. Ehninger, M. Tatsuka, Y. Terada, and E.P. Rieber Localization, dynamics, and function of Survivin revealed by expression of functional SurvivinDsRed fusion proteins in the living cell Mol. Biol. Cell 14 2003 78 92
42. S. Kaitna, M. Mendoza, V. Jantsch-Plunger, and M. Glotzer Incenp and an aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis Curr. Biol. 10 2000 1172 1181
43. A. Carvalho, M. Carmena, C. Sambade, W.C. Earnshaw, and S.P. Wheatley Survivin is required for stable checkpoint activation in taxol-treated HeLa cells J. Cell Sci. 116 2003 2987 2998
44. Y. Zhang, Y. Nagata, G. Yu, H.G. Nguyen, M.R. Jones, P. Toselli, C.W. Jackson, M. Tatsuka, K. Todokoro, and K. Ravid Aberrant quantity and localization of Aurora-B/AIM-1 and Survivin during megakaryocyte polyploidization and the consequences of Aurora-B/AIM-1-deregulated expression Blood 103 2004 3717 3726
45. S.G. Zeitlin, R.D. Shelby, and K.F. Sullivan CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis J. Cell Biol. 155 2001 1147 1157
46. S.M. Lens, R.M. Wolthuis, R. Klompmaker, J. Kauw, R. Agami, T. Brummelkamp, G. Kops, and R.H. Medema Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension EMBO J. 22 2003 2934 2947
47. A.M. Mackay, A.M. Ainsztein, D.M. Eckley, and W.C. Earnshaw A dominant mutant of inner centromere protein (INCENP), a chromosomal protein, disrupts prometaphase congression and cytokinesis J. Cell Biol. 140 1998 991 1002
48. J. Zhao, T. Tenev, L.M. Martins, J. Downward, and N.R. Lemoine The ubiquitin-proteasome pathway regulates Survivin degradation in a cell cycle-dependent manner J. Cell Sci. 113 Pt. 23 2000 4363 4371