Calmodulin protects Aurora B on the midbody to regulate the fidelity of cytokinesis

Cell Cycle

Volumn 12, Issue 4, 2013, Pages 663-673

  Mallampalli, Rama K ^a,c   Glasser, Jennifer R ^a   Coon, Tiffany A ^a   Chen, Bill B ^a,b  

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

^b UNIVERSITY OF PITTSBURGH   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Aurora B; Calmodulin; FBXL2; Midbody; Mitosis

Indexed keywords

AURORA B KINASE; CALMIDAZOLIUM; CALMODULIN; F BOX PROTEIN; UBIQUITIN PROTEIN LIGASE E3;

ABSCISSION; ANIMAL CELL; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CHROMOSOME SEGREGATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINESIS; IC 50; MITOSIS; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; NUDE MOUSE; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TELOPHASE; TETRAPLOIDY; TUMOR CELL; UBIQUITINATION;

EID: 84874611872     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.23586     Document Type: Article

References (65)

1. Margolis RL. Tetraploidy and tumor development. Cancer Cell 2005; 8:353-4; PMID:16286243; http://dx.doi.org/10.1016/j.ccr.2005.10.017
2. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005; 437:1043-7; PMID:16222300; http://dx.doi. org/10.1038/nature04217
3. Gortchakov AA, Eggert H, Gan M, Mattow J, Zhimulev IF, Saumweber H. Chriz, a chromodomain protein specific for the interbands of Drosophila melanogaster polytene chromosomes. Chromosoma 2005; 114:54-66; PMID:15821938; http://dx.doi. org/10.1007/s00412-005-0339-3
4. Cimini D, Wan X, Hirel CB, Salmon ED. Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr Biol 2006; 16:1711-8; PMID:16950108; http://dx.doi. org/10.1016/j.cub.2006.07.022
5. Wilsker D, Chung JH, Bunz F. Chk1 suppresses bypass of mitosis and tetraploidization in p53-deficient cancer cells. Cell Cycle 2012; 11:1564-72; PMID:22433954; http://dx.doi.org/10.4161/cc.19944
6. Bannon JH, O'Donovan DS, Kennelly SM, Mc Gee MM. The peptidyl prolyl isomerase cyclophilin A localizes at the centrosome and the midbody and is required for cytokinesis. Cell Cycle 2012; 11:1340-53; PMID:22421161; http://dx.doi.org/10.4161/cc.19711
7. Vazquez-Martin A, Sauri-Nadal T, Menendez OJ, Oliveras-Ferraros C, Cufí S, Corominas-Faja B, et al. Ser2481-autophosphorylated mTOR colocalizes with chromosomal passenger proteins during mammalian cell cytokinesis. Cell Cycle 2012; 11:4211-21; PMID:23095638; http://dx.doi.org/10. 4161/cc.22551
8. Weaver BA, Silk AD, Cleveland DW. Cell biology: nondisjunction, aneuploidy and tetraploidy. [discussion E.]. Nature 2006; 442:E9-10, discussion E10; PMID:16915240; http://dx.doi.org/10.1038/nature05139
9. Li Y, Xu FL, Lu J, Saunders WS, Prochownik EV. Widespread genomic instability mediated by a pathway involving glycoprotein Ib alpha and Aurora B kinase. J Biol Chem 2010; 285:13183-92; PMID:20157117; http://dx.doi.org/10. 1074/jbc.M109.084913
10. Nicholson JM, Cimini D. Doubling the deck: Tetraploidy induces chromosome shuffling and cancer. Cell Cycle 2012; 11:3354-5; PMID:22918235; http://dx.doi.org/10.4161/cc.21850
11. Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, Barral Y. The No Cut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 2006; 125:85-98; PMID:16615892; http://dx.doi.org/10.1016/j. cell.2006.01.045
12. Steigemann P, Wurzenberger C, Schmitz MH, Held M, Guizetti J, Maar S, et al. Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 2009; 136:473-84; PMID:19203582; http://dx.doi. org/10.1016/j.cell.2008.12. 020
13. Guse A, Mishima M, Glotzer M. Phosphorylation of ZEN-4/MKLP1 by aurora B regulates completion of cytokinesis. Curr Biol 2005; 15:778-86; PMID:15854913; http://dx.doi.org/10.1016/j. cub.2005.03.041
14. Chen CT, Doxsey S. A last-minute rescue of trapped chromatin. Cell 2009; 136:397-9; PMID:19203574; http://dx.doi.org/10.1016/j.cell.2009.01.028
15. Shao H, Ma C, Zhang X, Li R, Miller AL, Bement WM, et al. Aurora B regulates spindle bipolarity in meiosis in vertebrate oocytes. Cell Cycle 2012; 11:2672-80; PMID:22751439; http://dx.doi.org/10.4161/cc.21016
16. Yabuta N, Mukai S, Okada N, Aylon Y, Nojima H. The tumor suppressor Lats2 is pivotal in Aurora A and Aurora B signaling during mitosis. Cell Cycle 2011; 10:2724-36; PMID:21822051; http://dx.doi. org/10.4161/cc.10.16.16873
17. Archambault V, Carmena M. Polo-like kinase-activating kinases: Aurora A, Aurora B and what else? Cell Cycle 2012; 11:1490-5; PMID:22433949; http://dx.doi.org/10.4161/cc.19724
18. Bolton MA, Lan W, Powers SE, McCleland ML, Kuang J, Stukenberg PT. 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 2002; 13:3064-77; PMID:12221116; http://dx.doi.org/10.1091/mbc.E02-02-0092
19. Yasui Y, Urano T, Kawajiri A, Nagata K, Tatsuka M, Saya H, et al. Autophosphorylation of a newly identified site of Aurora-B is indispensable for cytokinesis. J Biol Chem 2004; 279:12997-3003; PMID:14722118; http://dx.doi.org/10.1074/jbc.M311128200
20. Sun L, Gao J, Dong X, Liu M, Li D, Shi X, et al. EB1 promotes Aurora-B kinase activity through blocking its inactivation by protein phosphatase 2A. Proc Natl Acad Sci U S A 2008; 105:7153-8; PMID:18477699; http://dx.doi.org/10. 1073/pnas.0710018105
21. Nguyen HG, Chinnappan D, Urano T, Ravid K. Mechanism of Aurora-B degradation and its dependency on intact KEN and A-boxes: identification of an aneuploidy-promoting property. Mol Cell Biol 2005; 25:4977-92; PMID:15923616; http://dx.doi. org/10.1128/MCB.25.12.4977-4992.2005
22. Sumara I, Quadroni M, Frei C, Olma MH, Sumara G, Ricci R, et al. A Cul3-based E3 ligase removes Aurora B from mitotic chromosomes, regulating mitotic progression and completion of cytokinesis in human cells. Dev Cell 2007; 12:887-900; PMID:17543862; http://dx.doi.org/10.1016/j.devcel.2007.03.019
23. Maerki S, Olma MH, Staubli T, Steigemann P, Gerlich DW, Quadroni M, et al. The Cul3-KLHL21 E3 ubiquitin ligase targets aurora B to midzone microtubules in anaphase and is required for cytokinesis. J Cell Biol 2009; 187:791-800; PMID:19995937; http://dx.doi. org/10.1083/jcb.200906117
24. Tyers M, Willems AR. One ring to rule a superfamily of E3 ubiquitin ligases. Science 1999; 284:601, 603-4; PMID:10328744; http://dx.doi.org/10.1126/ science.284.5414.601
25. Guardavaccaro D, Frescas D, Dorrello NV, Peschiaroli A, Multani AS, Cardozo T, et al. Control of chromosome stability by the beta-TrCP-REST-Mad2 axis. Nature 2008; 452:365-9; PMID:18354482; http://dx.doi.org/10.1038/ nature06641
26. rd, Fang G. Plk1-and beta-TrCP-dependent degradation of Bora controls mitotic progression. J Cell Biol 2008; 181:65-78; PMID:18378770; http://dx.doi. org/10.1083/jcb. 200712027
27. Gusti A, Baumberger N, Nowack M, Pusch S, Eisler H, Potuschak T, et al. The Arabidopsis thaliana F-box protein FBL17 is essential for progression through the second mitosis during pollen development. PLoS One 2009; 4:e4780; PMID:19277118; http://dx.doi. org/10.1371/journal.pone.0004780
28. D'Angiolella V, Donato V, Vijayakumar S, Saraf A, Florens L, Washburn MP, et al. SCF(Cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 2010; 466:138-42; PMID:20596027; http://dx.doi.org/10.1038/nature09140
29. Coon TA, Glasser JR, Mallampalli RK, Chen BB. Novel E3 ligase component FBXL7 ubiquitinates and degrades Aurora A, causing mitotic arrest. Cell Cycle 2012; 11:721-9; PMID:22306998; http://dx.doi. org/10.4161/cc.11.4.19171
30. Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, Wang P, et al. Structure of the Cul1-Rbx1-Skp1-F box Skp2 SCF ubiquitin ligase complex. Nature 2002; 416:703-9; PMID:11961546; http://dx.doi. org/10.1038/416703a
31. Cardozo T, Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol 2004; 5:739-51; PMID:15340381; http://dx.doi. org/10.1038/nrm1471
32. Cenciarelli C, Chiaur DS, Guardavaccaro D, Parks W, Vidal M, Pagano M. Identification of a family of human F-box proteins. Curr Biol 1999; 9:1177-9; PMID:10531035; http://dx.doi.org/10.1016/S0960-9822(00)80020-2
33. Ilyin GP, Rialland M, Glaise D, Guguen-Guillouzo C. Identification of a novel Skp2-like mammalian protein containing F-box and leucine-rich repeats. FEBS Lett 1999; 459:75-9; PMID:10508920; http://dx.doi. org/10.1016/S0014- 5793(99)01211-9
34. Liu D, Zhang N, Du J, Cai X, Zhu M, Jin C, et al. Interaction of Skp1 with CENP-E at the midbody is essential for cytokinesis. Biochem Biophys Res Commun 2006; 345:394-402; PMID:16682006; http://dx.doi.org/10.1016/j.bbrc.2006. 04.062
35. Chen BB, Glasser JR, Coon TA, Mallampalli RK. F-box protein FBXL2 exerts human lung tumor suppressor-like activity by ubiquitin-mediated degradation of cyclin D3 resulting in cell cycle arrest. Oncogene 2012; 31:2566-79; PMID:22020328; http://dx.doi. org/10.1038/onc.2011.432
36. Chen BB, Glasser JR, Coon TA, Mallampalli RK. FBXL2 is a ubiquitin E3 ligase subunit that triggers mitotic arrest. Cell Cycle 2011; 10:3487-94; PMID:22024926; http://dx.doi.org/10.4161/cc.10.20.17742
37. Rhoads AR, Friedberg F. Sequence motifs for calmodulin recognition. FASEB J 1997; 11:331-40; PMID:9141499
38. Moser MJ, Flory MR, Davis TN. Calmodulin localizes to the spindle pole body of Schizosaccharomyces pombe and performs an essential function in chromosome segregation. J Cell Sci 1997; 110:1805-12; PMID:9264467
39. Zhu Q, Liu T, Clarke M. Calmodulin and the contractile vacuole complex in mitotic cells of Dictyostelium discoideum. J Cell Sci 1993; 104:1119-27; PMID:8314896
40. Sweet SC, Rogers CM, Welsh MJ. Calmodulin is associated with microtubules forming in PTK1 cells upon release from nocodazole treatment. Cell Motil Cytoskeleton 1989; 12:113-22; PMID:2713899; http://dx.doi.org/10.1002/cm. 970120206
41. Welsh MJ, Dedman JR, Brinkley BR, Means AR. Tubulin and calmodulin. Effects of microtubule and microfilament inhibitors on localization in the mitotic apparatus. J Cell Biol 1979; 81:624-34; PMID:379022; http://dx.doi.org/10.1083/jcb.81.3.624
42. Liu T, Williams JG, Clarke M. Inducible expression of calmodulin antisense RNA in Dictyostelium cells inhibits the completion of cytokinesis. Mol Biol Cell 1992; 3:1403-13; PMID:1493336
43. Yu YY, Dai G, Pan FY, Chen J, Li CJ. Calmodulin regulates the post-anaphase reposition of centrioles during cytokinesis. Cell Res 2005; 15:548-52; PMID:16045818; http://dx.doi.org/10.1038/sj.cr.7290324
44. Tsang WY, Spektor A, Luciano DJ, Indjeian VB, Chen Z, Salisbury JL, et al. CP110 cooperates with two calcium-binding proteins to regulate cytokinesis and genome stability. Mol Biol Cell 2006; 17:3423-34; PMID:16760425; http://dx.doi.org/10.1091/mbc. E06-04-0371
45. Chen BB, Coon TA, Glasser JR, Mallampalli RK. Calmodulin antagonizes a calcium-activated SCF ubiquitin E3 ligase subunit, FBXL2, to regulate surfactant homeostasis. Mol Cell Biol 2011; 31:1905-20; PMID:21343341; http://dx.doi.org/10.1128/MCB.00723-10
46. Liu C, Kato Y, Zhang Z, Do VM, Yankner BA, He X. beta-Trcp couples beta-catenin phosphorylation-degradation and regulates Xenopus axis formation. Proc Natl Acad Sci U S A 1999; 96:6273-8; PMID:10339577; http://dx.doi.org/10. 1073/pnas.96.11.6273
47. Hansen DV, Loktev AV, Ban KH, Jackson PK. Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCFbeta TrCP dependent destruction of the APC Inhibitor Emi1. Mol Biol Cell 2004; 15:5623-34; PMID:15469984; http://dx.doi.org/10.1091/mbc.E04-07-0598
48. Watanabe N, Arai H, Iwasaki J, Shiina M, Ogata K, Hunter T, et al. Cyclin-dependent kinase (CDK) phosphorylation destabilizes somatic Weel via multiple pathways. Proc Natl Acad Sci U S A 2005; 102:11663-8; PMID:16085715; http://dx.doi.org/10.1073/pnas.0500410102
49. Green MR, Woolery JE, Mahadevan D. Update on Aurora Kinase Targeted Therapeutics in Oncology. Expert Opin Drug Discov 2011; 6:291-307; PMID:21556291; http://dx.doi.org/10.1517/174604 41.2011.555395
50. Stirling DA, Welch KA, Stark MJ. Interaction with calmodulin is required for the function of Spc110p, an essential component of the yeast spindle pole body. EMBO J 1994; 13:4329-42; PMID:7925277
51. Sundberg HA, Goetsch L, Byers B, Davis TN. Role of calmodulin and Spc110p interaction in the proper assembly of spindle pole body compenents. J Cell Biol 1996; 133:111-24; PMID:8601600; http://dx.doi. org/10.1083/jcb.133.1.111
52. Sanhaji M, Friel CT, Wordeman L, Louwen F, Yuan J. Mitotic centromere-associated kinesin (MCAK): a potential cancer drug target. Oncotarget 2011; 2:935-47; PMID:22249213
53. Blanchard Z, Malik R, Mullins N, Maric C, Luk H, Horio D, et al. Geminin overexpression induces mammary tumors via suppressing cytokinesis. Oncotarget 2011; 2:1011-27; PMID:22184288
54. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T, et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 2004; 10:262-7; PMID:14981513; http://dx.doi. org/10.1038/nm1003
55. Gadea BB, Ruderman JV. Aurora kinase inhibitor ZM447439 blocks chromosome-induced spindle assembly, the completion of chromosome condensation, and the establishment of the spindle integrity checkpoint in Xenopus egg extracts. Mol Biol Cell 2005; 16:1305-18; PMID:15616188; http://dx.doi. org/10.1091/mbc.E04-10-0891
56. Soncini C, Carpinelli P, Gianellini L, Fancelli D, Vianello P, Rusconi L, et al. PHA-680632, a novel Aurora kinase inhibitor with potent antitumoral activity. Clin Cancer Res 2006; 12:4080-9; PMID:16818708; http://dx.doi.org/10. 1158/1078-0432.CCR-05-1964
57. Hardwicke MA, Oleykowski CA, Plant R, Wang J, Liao Q, Moss K, et al. GSK1070916, a potent Aurora B/C kinase inhibitor with broad antitumor activity in tissue culture cells and human tumor xenograft models. Mol Cancer Ther 2009; 8:1808-17; PMID:19567821; http://dx.doi.org/10.1158/1535-7163.MCT-09-0041
58. Hoellein A, Pickhard A, von Keitz F, Schoeffmann S, Piontek G, Rudelius M, et al. Aurora kinase inhibition overcomes cetuximab resistance in squamous cell cancer of the head and neck. Oncotarget 2011; 2:599-609; PMID:21865609
59. Marxer M, Foucar CE, Man WY, Chen Y, Ma HT, Poon RY. Tetraploidization increases sensitivity to Aurora B kinase inhibition. Cell Cycle 2012; 11:2567-77; PMID:22722494; http://dx.doi.org/10.4161/cc.20947
60. Ray NB, Durairaj L, Chen BB, McVerry BJ, Ryan AJ, Donahoe M, et al. Dynamic regulation of cardiolipin by the lipid pump Atp8b1 determines the severity of lung injury in experimental pneumonia. Nat Med 2010; 16:1120-7; PMID:20852622; http://dx.doi. org/10.1038/nm.2213
61. Chen BB, Mallampalli RK. Calmodulin binds and stabilizes the regulatory enzyme, CTP: phosphocholine cytidylyltransferase. J Biol Chem 2007; 282:33494-506; PMID:17804406; http://dx.doi.org/10.1074/jbc. M706472200
62. Agassandian M, Chen BB, Schuster CC, Houtman JC, Mallampalli RK. 14-3-3zeta escorts CCTalpha for calcium-activated nuclear import in lung epithelia. FASEB J 2010; 24:1271-83; PMID:20007511; http://dx.doi.org/10.1096/ fj.09-136044
63. Chen BB, Mallampalli RK. Masking of a nuclear signal motif by monoubiquitination leads to mislocalization and degradation of the regulatory enzyme cytidylyltransferase. Mol Cell Biol 2009; 29:3062-75; PMID:19332566; http://dx.doi.org/10.1128/MCB.01824-08
64. Mallampalli RK, Ryan AJ, Salome RG, Jackowski S. Tumor necrosis factor-alpha inhibits expression of CTP:phosphocholine cytidylyltransferase. J Biol Chem 2000; 275:9699-708; PMID:10734122; http://dx.doi. org/10.1074/jbc.275. 13.9699
65. Butler PL, Mallampalli RK. Cross-talk between remodeling and de novo pathways maintains phospholipid balance through ubiquitination. J Biol Chem 2010; 285:6246-58; PMID:20018880; http://dx.doi. org/10.1074/jbc.M109.017350