RNA stimulates Aurora B kinase activity during mitosis

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Jambhekar, Ashwini ^a,b   Emerman, Amy B ^a,b   Schweidenback, Caterina T H ^a,b   Blower, Michael D ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CYCLIN DEPENDENT KINASE; MCAK PROTEIN; MESSENGER RNA; MICROTUBULE PROTEIN; RIBONUCLEASE; RIBONUCLEOPROTEIN; RIBOSOME RNA; RNA; SURVIVIN; UNCLASSIFIED DRUG; KINESIN; MITOTIC CENTROMERE-ASSOCIATED KINESIN, XENOPUS; XENOPUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CATALYSIS; CELL VIABILITY; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; GENE CONTROL; IMMUNOPRECIPITATION; IN VITRO STUDY; INTERPHASE; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PROTEIN LOCALIZATION; RNA BINDING; RNA SEQUENCE; RNA TRANSLATION; XENOPUS; ANIMAL; CENTROMERE; ENZYME SPECIFICITY; GENETICS; HUMAN; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PROTEIN TRANSPORT; SPINDLE APPARATUS; XENOPUS LAEVIS;

ANIMALS; AURORA KINASE B; BASE SEQUENCE; CENTROMERE; ENZYME ACTIVATION; HUMANS; KINESIN; MICE; MITOSIS; PROTEIN TRANSPORT; RNA; SPINDLE APPARATUS; SUBSTRATE SPECIFICITY; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84903553148     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100748     Document Type: Article

References (77)

1. Mitchison T, Kirschner M (1984) Microtubule assembly nucleated by isolated centrosomes. Nature 312: 232-237. (Pubitemid 15201997)
2. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, et al. (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382: 420-425. (Pubitemid 26264851)
3. Karsenti E, Newport J, Kirschner M (1984) Respective roles of centrosomes and chromatin in the conversion of microtubule arrays from interphase to metaphase. J Cell Biol 99: 47s-54s. (Pubitemid 14074763)
4. Gadde S, Heald R (2004) Mechanisms and molecules of the mitotic spindle. Curr Biol 14: R797-805. (Pubitemid 39239355)
5. Nachury MV, Maresca TJ, Salmon WC, Waterman-Storer CM, Heald R, et al. (2001) Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104: 95-106. (Pubitemid 32144975)
6. Wiese C, Wilde A, Moore MS, Adam SA, Merdes A, et al. (2001) Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 291: 653-656. (Pubitemid 32150424)
7. Gruss OJ, Carazo-Salas RE, Schatz CA, Guarguaglini G, Kast J, et al. (2001) Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 104: 83-93. (Pubitemid 32144974)
8. Koffa MD, Casanova CM, Santarella R, Kocher T, Wilm M, et al. (2006) HURP is part of a Ran-dependent complex involved in spindle formation. Curr Biol 16: 743-754.
9. Sillje HH, Nagel S, Korner R, Nigg EA (2006) HURP is a Ran-importin beta-regulated protein that stabilizes kinetochore microtubules in the vicinity of chromosomes. Curr Biol 16: 731-742.
10. Ribbeck K, Groen AC, Santarella R, Bohnsack MT, Raemaekers T, et al. (2006) NuSAP, a mitotic RanGTP target that stabilizes and cross-links microtubules. Mol Biol Cell 17: 2646-2660. (Pubitemid 43825502)
11. Carmena M, Wheelock M, Funabiki H, Earnshaw WC (2012) The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol 13: 789-803.
12. Earnshaw WC, Bernat RL (1991) Chromosomal passengers: toward an integrated view of mitosis. Chromosoma 100: 139-146.
13. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812. (Pubitemid 47462135)
14. Gadea BB, Ruderman JV (2006) Aurora B is required for mitotic chromatin-induced phosphorylation of Op18/Stathmin. Proc Natl Acad Sci U S A 103: 4493-4498.
15. Belmont LD, Mitchison TJ (1996) Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84: 623-631. (Pubitemid 26071742)
16. Andrews PD, Ovechkina Y, Morrice N, Wagenbach M, Duncan K, et al. (2004) Aurora B regulates MCAK at the mitotic centromere. Dev Cell 6: 253-268. (Pubitemid 38190365)
17. Lan W, Zhang X, Kline-Smith SL, Rosasco SE, Barrett-Wilt GA, et al. (2004) Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr Biol 14: 273-286. (Pubitemid 38300205)
18. Desai A, Verma S, Mitchison TJ, Walczak CE (1999) Kin I kinesins are microtubule-destabilizing enzymes. Cell 96: 69-78. (Pubitemid 29044154)
19. Tournebize R, Popov A, Kinoshita K, Ashford AJ, Rybina S, et al. (2000) Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat Cell Biol 2: 13-19.
20. Walczak CE, Mitchison TJ, Desai A (1996) XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell 84: 37-47. (Pubitemid 26031459)
21. Ohi R, Sapra T, Howard J, Mitchison TJ (2004) Differentiation of cytoplasmic and meiotic spindle assembly MCAK functions by Aurora B-dependent phosphorylation. Mol Biol Cell 15: 2895-2906. (Pubitemid 38691877)
22. Blower MD, Feric E, Weis K, Heald R (2007) Genome-wide analysis demonstrates conserved localization of messenger RNAs to mitotic microtubules. J Cell Biol 179: 1365-1373.
23. Eliscovich C, Peset I, Vernos I, Mendez R (2008) Spindle-localized CPE-mediated translation controls meiotic chromosome segregation. Nat Cell Biol 10: 858-865. (Pubitemid 351927714)
24. Groisman I, Huang YS, Mendez R, Cao Q, Theurkauf W, et al. (2000) CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: implications for local translational control of cell division. Cell 103: 435-447.
25. Sharp JA, Plant JJ, Ohsumi TK, Borowsky M, Blower MD (2011) Functional analysis of the microtubule-interacting transcriptome. Mol Biol Cell 22: 4312-4323.
26. Kingsley EP, Chan XY, Duan Y, Lambert JD (2007) Widespread RNA segregation in a spiralian embryo. Evol Dev 9: 527-539. (Pubitemid 350045751)
27. Lambert JD, Nagy LM (2002) Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature 420: 682-686. (Pubitemid 36764501)
28. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, et al. (2007) Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187. (Pubitemid 47498530)
29. Rabinowitz JS, Lambert JD (2010) Spiralian quartet developmental potential is regulated by specific localization elements that mediate asymmetric RNA segregation. Development 137: 4039-4049.
30. Raff JW, Whitfield WG, Glover DM (1990) Two distinct mechanisms localise cyclin B transcripts in syncytial Drosophila embryos. Development 110: 1249-1261. (Pubitemid 120009494)
31. Audhya A, Hyndman F, McLeod IX, Maddox AS, Yates JR 3rd, et al. (2005) A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans. J Cell Biol 171: 267-279. (Pubitemid 41540019)
32. Goshima G, Wollman R, Goodwin SS, Zhang N, Scholey JM, et al. (2007) Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316: 417-421. (Pubitemid 46651486)
33. Hussain S, Benavente SB, Nascimento E, Dragoni I, Kurowski A, et al. (2009) The nucleolar RNA methyltransferase Misu (NSun2) is required for mitotic spindle stability. J Cell Biol 186: 27-40.
34. Squirrell JM, Eggers ZT, Luedke N, Saari B, Grimson A, et al. (2006) CAR-1, a protein that localizes with the mRNA decapping component DCAP-1, is required for cytokinesis and ER organization in Caenorhabditis elegans embryos. Mol Biol Cell 17: 336-344. (Pubitemid 43049486)
35. Blower MD, Nachury M, Heald R, Weis K (2005) A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 121: 223-234. (Pubitemid 40546390)
36. Ferri F, Bouzinba-Segard H, Velasco G, Hube F, Francastel C (2009) Noncoding murine centromeric transcripts associate with and potentiate Aurora B kinase. Nucleic Acids Res 37: 5071-5080.
37. Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, et al. (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 17: 1146-1160. (Pubitemid 47204858)
38. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, et al. (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102: 279-291.
39. Bolton MA, LanW, Powers SE, McCleland ML, Kuang J, et al. (2002) 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: 3064-3077. (Pubitemid 35034246)
40. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
41. Edwards NS, Murray AW (2005) Identification of xenopus CENP-A and an associated centromeric DNA repeat. Mol Biol Cell 16: 1800-1810. (Pubitemid 40471950)
42. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-208.
43. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, et al. (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141.
44. Hafner M, Max KE, Bandaru P, Morozov P, Gerstberger S, et al. (2013) Identification of mRNAs bound and regulated by human LIN28 proteins and molecular requirements for RNA recognition. RNA 19: 613-626.
45. Ince-Dunn G, Okano HJ, Jensen KB, Park WY, Zhong R, et al. (2012) Neuronal Elav-like (Hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability. Neuron 75: 1067-1080.
46. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, et al. (2008) HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456: 464-469. (Pubitemid 352759008)
47. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, et al. (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 40: 939-953.
48. Davidovich C, Zheng L, Goodrich KJ, Cech TR (2013) Promiscuous RNA binding by Polycomb repressive complex 2. Nat Struct Mol Biol 20: 1250-1257.
49. Makino DL, Baumgartner M, Conti E (2013) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495: 70-75.
50. Klein UR, Nigg EA, Gruneberg U (2006) Centromere targeting of the chromosomal passenger complex requires a ternary subcomplex of Borealin, Survivin, and the N-terminal domain of INCENP. Mol Biol Cell 17: 2547-2558. (Pubitemid 43825493)
51. Kelly AE, Sampath SC, Maniar TA, Woo EM, Chait BT, et al. (2007) Chromosomal enrichment and activation of the aurora B pathway are coupled to spatially regulate spindle assembly. Dev Cell 12: 31-43. (Pubitemid 46002596)
52. Rosasco-Nitcher SE, Lan W, Khorasanizadeh S, Stukenberg PT (2008) Centromeric Aurora-B activation requires TD-60, microtubules, and substrate priming phosphorylation. Science 319: 469-472. (Pubitemid 351160581)
53. Tseng BS, Tan L, Kapoor TM, Funabiki H (2010) Dual detection of chromosomes and microtubules by the chromosomal passenger complex drives spindle assembly. Dev Cell 18: 903-912.
54. Zhang X, Lan W, Ems-McClung SC, Stukenberg PT, Walczak CE (2007) Aurora B phosphorylates multiple sites on mitotic centromere-associated kinesin to spatially and temporally regulate its function. Mol Biol Cell 18: 3264-3276. (Pubitemid 47378669)
55. Knowlton AL, Lan W, Stukenberg PT (2006) Aurora B is enriched at merotelic attachment sites, where it regulates MCAK. Curr Biol 16: 1705-1710. (Pubitemid 44691788)
56. Cimini D (2007) Detection and correction of merotelic kinetochore orientation by Aurora B and its partners. Cell Cycle 6: 1558-1564.
57. Sampath SC, Ohi R, Leismann O, Salic A, Pozniakovski A, et al. (2004) The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly. Cell 118: 187-202. (Pubitemid 38962575)
58. Mitchison TJ, Maddox P, Gaetz J, Groen A, Shirasu M, et al. (2005) Roles of polymerization dynamics, opposed motors, and a tensile element in governing the length of Xenopus extract meiotic spindles. Mol Biol Cell 16: 3064-3076. (Pubitemid 40741248)
59. Groen AC, Maresca TJ, Gatlin JC, Salmon ED, Mitchison TJ (2009) Functional overlap of microtubule assembly factors in chromatin-promoted spindle assembly. Mol Biol Cell 20: 2766-2773.
60. Chan FL, Marshall OJ, Saffery R, Kim BW, Earle E, et al. (2012) Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc Natl Acad Sci U S A 109: 1979-1984.
61. Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, et al. (2008) Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 14: 507-522. (Pubitemid 351492128)
62. Gent JI, Dawe RK (2012) RNA as a structural and regulatory component of the centromere. Annu Rev Genet 46: 443-453.
63. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30: 687-696. (Pubitemid 13204658)
64. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30: 675-686. (Pubitemid 13204657)
65. Tan MH, Au KF, Yablonovitch AL, Wills AE, Chuang J, et al. (2013) RNA sequencing reveals a diverse and dynamic repertoire of the Xenopus tropicalis transcriptome over development. Genome Res 23: 201-216.
66. Darnell RB (2010) HITS-CLIP: panoramic views of protein-RNA regulation in living cells. Wiley Interdiscip Rev RNA 1: 266-286.
67. Baltz AG, Munschauer M, Schwanhausser B, Vasile A, Murakawa Y, et al. (2012) The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 46: 674-690.
68. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, et al. (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149: 1393-1406.
69. Castello A, Horos R, Strein C, Fischer B, Eichelbaum K, et al. (2013) System-wide identification of RNA-binding proteins by interactome capture. Nat Protoc 8: 491-500.
70. Kwon SC, Yi H, Eichelbaum K, Fohr S, Fischer B, et al. (2013) The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol 20: 1122-1130.
71. Kennedy MC, Mende-Mueller L, Blondin GA, Beinert H (1992) Purification and characterization of cytosolic aconitase from beef liver and its relationship to the iron-responsive element binding protein. Proc Natl Acad Sci U S A 89: 11730-11734. (Pubitemid 23004717)
72. Nagy E, Rigby WF (1995) Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold). J Biol Chem 270: 2755-2763.
73. Ciesla J (2006) Metabolic enzymes that bind RNA: yet another level of cellular regulatory network? Acta Biochim Pol 53: 11-32.
74. Hannak E, Heald R (2006) Investigating mitotic spindle assembly and function in vitro using Xenopus laevis egg extracts. Nat Protoc 1: 2305-2314.
75. Kim Y, Heuser JE, Waterman CM, Cleveland DW (2008) CENP-E combines a slow, processive motor and a flexible coiled coil to produce an essential motile kinetochore tether. J Cell Biol 181: 411-419. (Pubitemid 351645031)
76. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
77. Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18: 6097-6100.