AURKB-mediated effects on chromatin regulate binding versus release of XIST RNA to the inactive chromosome

Journal of Cell Biology

Volumn 186, Issue 4, 2009, Pages 491-507

  Hall, Lisa L ^a   Byron, Meg ^a   Pageau, Gayle ^a   Lawrence, Jeanne B ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CHROMOSOME PROTEIN; HISTONE H3; RNA;

ARTICLE; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; HUMAN; HUMAN CELL; MALE; MITOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA BINDING; RNA INTERFERENCE; STAINING; UBIQUITINATION;

ANIMALS; CELL CYCLE; CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; HUMANS; INDOLES; MALE; MODELS, MOLECULAR; PROTEIN PHOSPHATASE 1; PROTEIN-SERINE-THREONINE KINASES; RNA; RNA INTERFERENCE; RNA, UNTRANSLATED; SULFONAMIDES; TRANSCRIPTION FACTORS; TRANSGENES;

EID: 69449101751     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200811143     Document Type: Article

References (68)

1. Agnese, V., V. Bazan, F.P. Fiorentino, D. Fanale, G. Badalamenti, G. Colucci, V. Adamo, D. Santini, and A. Russo. 2007. The role of Aurora-A inhibitors in cancer therapy. Ann. Oncol. 18:vi47-vi52.
2. Ajiro, K., K. Yoda, K. Utsumi, and Y. Nishikawa. 1996. Alteration of cell cycle-dependent histone phosphorylations by okadaic acid. Induction of mitosis-specific H3 phosphorylation and chromatin condensation in mammalian interphase cells. J. Biol. Chem. 271:13197-13201. (Pubitemid 26175900)
3. Andrews, P.D., E. Knatko, W.J. Moore, and J.R. Swedlow. 2003. Mitotic mechanics: the auroras come into view. Curr. Opin. Cell Biol. 15:672-683.
4. Barber, C.M., F.B. Turner, Y. Wang, K. Hagstrom, S.D. Taverna, S. Mollah, B. Ueberheide, B.J. Meyer, D.F. Hunt, P. Cheung, and C.D. Allis. 2004. The enhancement of histone H4 and H2A serine 1 phosphorylation during mitosis and S-phase is evolutionarily conserved. Chromosoma. 112:360-371.
5. Bernstein, E., and C.D. Allis. 2005. RNA meets chromatin. Genes Dev. 19:1635-1655.
6. Bialojan, C., and A. Takai. 1988. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem. J. 256:283-290. (Pubitemid 18273473)
7. Brockdorff, N. 2002. X-chromosome inactivation: closing in on proteins that bind Xist RNA. Trends Genet. 18:352-358. (Pubitemid 34804447)
8. Brown, C.J., and S.E. Baldry. 1996. Evidence that heteronuclear proteins interact with XIST RNA in vitro. Somat. Cell Mol. Genet. 22:403-417.
9. Brown, C.J., B.D. Hendrich, J.L. Rupert, R.G. Lafrenière, Y. Xing, J.B. Lawrence, and H.F. Willard. 1992. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell. 71:527-542.
10. Chadwick, B.P., and H.F. Willard. 2002. Cell cycle-dependent localization of macroH2A in chromatin of the inactive X chromosome. J. Cell Biol. 157:1113-1123.
11. Chadwick, B.P., and H.F. Willard. 2003. Chromatin of the Barr body: histone and non-histone proteins associated with or excluded from the inactive X chromosome. Hum. Mol. Genet. 12:2167-2178.
12. Clemson, C.M., J.A. McNeil, H.F. Willard, and J.B. Lawrence. 1996. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132:259-275.
13. Clemson, C.M., L.L. Hall, M. Byron, J. McNeil, and J.B. Lawrence. 2006. The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. Proc. Natl. Acad. Sci. USA. 103:7688-7693.
14. Crosio, C., G.M. Fimia, R. Loury, M. Kimura, Y. Okano, H. Zhou, S. Sen, C.D. Allis, and P. Sassone-Corsi. 2002. Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol. Cell. Biol. 22:874-885. (Pubitemid 34053065)
15. Csankovszki, G., A. Nagy, and R. Jaenisch. 2001. Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J. Cell Biol. 153:773-784. (Pubitemid 34286109)
16. Dawson, J.F., and C.F. Holmes. 1999. Molecular mechanisms underlying inhibition of protein phosphatases by marine toxins. Front. Biosci. 4:D646-D658.
17. de Napoles, M., J.E. Mermoud, R. Wakao, Y.A. Tang, M. Endoh, R. Appanah, T.B. Nesterova, J. Silva, A.P. Otte, M. Vidal, et al. 2004. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell. 7:663-676. (Pubitemid 39462687)
18. Dormann, H.L., B.S. Tseng, C.D. Allis, H. Funabiki, and W. Fischle. 2006. Dynamic regulation of effector protein binding to histone modifications: the biology of HP1 switching. Cell Cycle. 5:2842-2851.
19. Duthie, S.M., T.B. Nesterova, E.J. Formstone, A.M. Keohane, B.M. Turner, S.M. Zakian, and N. Brockdorff. 1999. Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Hum. Mol. Genet. 8:195-204.
20. Edmondson, D.G., J.K. Davie, J. Zhou, B. Mirnikjoo, K. Tatchell, and S.Y. Dent. 2002. Site-specific loss of acetylation upon phosphorylation of histone H3. J. Biol. Chem. 277:29496-29502. (Pubitemid 41079236)
21. Esteller, M. 2007. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8:286-298. (Pubitemid 46439286)
22. Fang, J., T. Chen, B. Chadwick, E. Li, and Y. Zhang. 2004. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J. Biol. Chem. 279:52812-52815. (Pubitemid 40051779)
23. Favre, B., P. Turowski, and B.A. Hemmings. 1997. Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J. Biol. Chem. 272:13856-13863. (Pubitemid 27224826)
24. Feinberg, A.P., and B. Tycko. 2004. The history of cancer epigenetics. Nat. Rev. Cancer. 4:143-153.
25. Fischle, W., B.S. Tseng, H.L. Dormann, B.M. Ueberheide, B.A. Garcia, J. Shabanowitz, D.F. Hunt, H. Funabiki, and C.D. Allis. 2005. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature. 438:1116-1122. (Pubitemid 41831675)
26. Giet, R., and C. Prigent. 1999. Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases. J. Cell Sci. 112:3591-3601. (Pubitemid 129783931)
27. Girdler, F., K.E. Gascoigne, P.A. Eyers, S. Hartmuth, C. Crafter, K.M. Foote, N.J. Keen, and S.S. Taylor. 2006. Validating Aurora B as an anti-cancer drug target. J. Cell Sci. 119:3664-3675. (Pubitemid 44501870)
28. Goto, H., Y. Tomono, K. Ajiro, H. Kosako, M. Fujita, M. Sakurai, K. Okawa, A. Iwamatsu, T. Okigaki, T. Takahashi, and M. Inagaki. 1999. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274:25543-25549. (Pubitemid 129530724)
29. Hall, L.L., M. Byron, K. Sakai, L. Carrel, H.F. Willard, and J.B. Lawrence. 2002. An ectopic human XIST gene can induce chromosome inactivation in postdifferentiation human HT-1080 cells. Proc. Natl. Acad. Sci. USA. 99:8677-8682.
30. Hauf, S., R.W. Cole, S. LaTerra, C. Zimmer, G. Schnapp, R. Walter, A. Heckel, J. van Meel, C.L. Rieder, and J.M. Peters. 2003. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J. Cell Biol. 161:281-294. (Pubitemid 36529847)
31. Hauf, S., E. Roitinger, B. Koch, C.M. Dittrich, K. Mechtler, and J.M. Peters. 2005. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol. 3:e69. (Pubitemid 40605292)
32. He, S., K.L. Dunn, P.S. Espino, B. Drobic, L. Li, J. Yu, J.M. Sun, H.Y. Chen, S. Pritchard, and J.R. Davie. 2008. Chromatin organization and nuclear microenvironments in cancer cells. J. Cell. Biochem. 104:2004-2015.
33. Hendzel, M.J., Y. Wei, M.A. Mancini, A. Van Hooser, T. Ranalli, B.R. Brinkley, D.P. Bazett-Jones, and C.D. Allis. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma. 106:348-360.
34. Hirota, T., J.J. Lipp, B.H. Toh, and J.M. Peters. 2005. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature. 438:1176-1180. (Pubitemid 41831689)
35. Honkanen, R.E., and T. Golden. 2002. Regulators of serine/threonine protein phosphatases at the dawn of a clinical era? Curr. Med. Chem. 9:2055-2075.
36. Huang, Y., and J.A. Steitz. 2005. SRprises along a messenger's journey. Mol. Cell. 17:613-615.
37. Johnson, C.V., R.H. Singer, and J.B. Lawrence. 1991. Fluorescent detection of nuclear RNA and DNA: implications for genome organization. Methods Cell Biol. 35:73-99.
38. Johnson, C.V., D. Primorac, M. McKinstry, J.A. McNeil, D. Rowe, and J.B. Lawrence. 2000. Tracking COL1A1 RNA in osteogenesis imperfecta: splice-defective transcripts initiate transport from the gene but are retained within the SC35 domain. J. Cell Biol. 150:417-432.
39. Joo, H.Y., L. Zhai, C. Yang, S. Nie, H. Erdjument-Bromage, P. Tempst, C. Chang, and H. Wang. 2007. Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature. 449:1068-1072. (Pubitemid 350014605)
40. Karachentsev, D., K. Sarma, D. Reinberg, and R. Steward. 2005. PR-Set7- dependent methylation of histone H4 Lys 20 functions in repression of gene expression and is essential for mitosis. Genes Dev. 19:431-435. (Pubitemid 40256274)
41. Knapp, J., P. Bokník, S. Huke, H. Lüss, F.U. Müller, T. Müller, P. Nacke, W. Schmitz, U. Vahlensieck, and J. Neumann. 1998. The mechanism of action of cantharidin in smooth muscle. Br. J. Pharmacol. 123:911-919. (Pubitemid 28085392)
42. Lee, J.T., and R. Jaenisch. 1997. Long-range cis effects of ectopic X-inactivation centres on a mouse autosome. Nature. 386:275-279.
43. Lipp, J.J., T. Hirota, I. Poser, and J.M. Peters. 2007. Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes. J. Cell Sci. 120:1245-1255.
44. Maison, C., D. Bailly, A.H. Peters, J.P. Quivy, D. Roche, A. Taddei, M. Lachner, T. Jenuwein, and G. Almouzni. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329-334. (Pubitemid 34887695)
45. Marston, A.L., and A. Amon. 2004. Meiosis: cell-cycle controls shuffle and deal. Nat. Rev. Mol. Cell Biol. 5:983-997.
46. Misteli, T., and D.L. Spector. 1999. RNA polymerase II targets pre-mRNA splicing factors to transcription sites in vivo. Mol. Cell. 3:697-705. (Pubitemid 29323048)
47. Muchardt, C., M. Guilleme, J.S. Seeler, D. Trouche, A. Dejean, and M. Yaniv. 2002. Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep. 3:975-981. (Pubitemid 35256472)
48. Murnion, M.E., R.R. Adams, D.M. Callister, C.D. Allis, W.C. Earnshaw, and J.R. Swedlow. 2001. Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J. Biol. Chem. 276:26656-26665. (Pubitemid 37412889)
49. Nowak, S.J., and V.G. Corces. 2004. Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet. 20:214-220.
50. Pageau, G.J., L.L. Hall, S. Ganesan, D.M. Livingston, and J.B. Lawrence. 2007a. The disappearing Barr body in breast and ovarian cancers. Nat. Rev. Cancer. 7:628-633.
51. Pageau, G.J., L.L. Hall, and J.B. Lawrence. 2007b. BRCA1 does not paint the inactive X to localize XIST RNA but may contribute to broad changes in cancer that impact XIST and Xi heterochromatin. J. Cell. Biochem. 100:835-850.
52. Plath, K., J. Fang, S.K. Mlynarczyk-Evans, R. Cao, K.A. Worringer, H. Wang, C.C. de la Cruz, A.P. Otte, B. Panning, and Y. Zhang. 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science. 300:131-135. (Pubitemid 36423045)
53. Richardson, A.L., Z.C. Wang, A. De Nicolo, X. Lu, M. Brown, A. Miron, X. Liao, J.D. Iglehart, D.M. Livingston, and S. Ganesan. 2006. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell. 9:121-132. (Pubitemid 43202662)
54. Rodriguez, J.A., S.M. Lens, S.W. Span, G. Vader, R.H. Medema, F.A. Kruyt, and G. Giaccone. 2006. Subcellular localization and nucleocytoplasmic transport of the chromosomal passenger proteins before nuclear envelope breakdown. Oncogene. 25:4867-4879.
55. Ruchaud, S., M. Carmena, and W.C. Earnshaw. 2007. The chromosomal passenger complex: one for all and all for one. Cell. 131:230-231. (Pubitemid 47577519)
56. Sasai, K., H. Katayama, D.L. Stenoien, S. Fujii, R. Honda, M. Kimura, Y. Okano, M. Tatsuka, F. Suzuki, E.A. Nigg, et al. 2004. Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil. Cytoskeleton. 59:249-263. (Pubitemid 40012993)
57. Schoeftner, S., A.K. Sengupta, S. Kubicek, K. Mechtler, L. Spahn, H. Koseki, T. Jenuwein, and A. Wutz. 2006. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25:3110-3122. (Pubitemid 44121103)
58. Smith, K.P., M. Byron, C.M. Clemson, and J.B. Lawrence. 2004. Ubiquitinated proteins including uH2A on the human and mouse inactive X chromosome: enrichment in gene rich bands. Chromosoma. 113:324-335.
59. Sugiyama, K., K. Sugiura, T. Hara, K. Sugimoto, H. Shima, K. Honda, K. Furukawa, S. Yamashita, and T. Urano. 2002. Aurora-B associated protein phosphatases as negative regulators of kinase activation. Oncogene. 21:3103-3111. (Pubitemid 34548081)
60. Tam, R., L.S. Shopland, C.V. Johnson, J. McNeil, and J.B. Lawrence. 2002. Applications of RNA FISH for visualizing gene expression and nuclear architecture. In FISH: A Practical Approach. B.G. Beatty, S. Mai, and J. Squire, editors. Oxford University Press, New York. 93-118.
61. Terada, Y. 2006. Aurora-B/AIM-1 regulates the dynamic behavior of HP1alpha at the G2-M transition. Mol. Biol. Cell. 17:3232-3241. (Pubitemid 43993523)
62. Vader, G., R.H. Medema, and S.M. Lens. 2006. The chromosomal passenger complex: guiding Aurora-B through mitosis. J. Cell Biol. 173:833-837. (Pubitemid 43920690)
63. Wreggett, K.A., F. Hill, P.S. James, A. Hutchings, G.W. Butcher, and P.B. Singh. 1994. A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet. Cell Genet. 66:99-103. (Pubitemid 24042839)
64. Wutz, A., T.P. Rasmussen, and R. Jaenisch. 2002. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 30:167-174. (Pubitemid 34887710)
65. Xiao, C., J.A. Sharp, M. Kawahara, A.R. Davalos, M.J. Difilippantonio, Y. Hu, W. Li, L. Cao, K. Buetow, T. Ried, et al. 2007. The XIST noncoding RNA functions independently of BRCA1 in X inactivation. Cell. 128:977-989. (Pubitemid 46350785)
66. Xing, Y., C.V. Johnson, P.T. Moen Jr., J.A. McNeil, and J.B. Lawrence. 1995. Nonrandom gene organization: structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains. J. Cell Biol. 131:1635-1647. (Pubitemid 26007964)
67. Yang, H., T. Burke, J. Dempsey, B. Diaz, E. Collins, J. Toth, R. Beckmann, and X. Ye. 2005. Mitotic requirement for aurora A kinase is bypassed in the absence of aurora B kinase. FEBS Lett. 579:3385-3391.
68. Zhang, R., M.V. Poustovoitov, X. Ye, H.A. Santos, W. Chen, S.M. Daganzo, J.P. Erzberger, I.G. Serebriiskii, A.A. Canutescu, R.L. Dunbrack, et al. 2005. Formation of MacroH2A-containing senescence-associated hetero-chromatin foci and senescence driven by ASF1a and HIRA. Dev. Cell. 8:19-30. (Pubitemid 40058002)