In Vivo FRET Imaging Revealed a Regulatory Role of RanGTP in Kinetochore-Microtubule Attachments via Aurora B Kinase

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Lee, Yoke Peng ^a   Wong, Chi Hang ^a,b   Chan, Kheng Sze ^a   Lai, Soak Kuan ^a,c   Koh, Cheng Gee ^a   Li, Hoi Yeung ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; EXPORTIN 1; MST1 PROTEIN; NUCLEAR PROTEIN; RAN PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENOME; METAPHASE; METAPHASE CHROMOSOME; MICROTUBULE; MITOSIS SPINDLE; NUCLEAR EXPORT SIGNAL; POSTMETAPHASE; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TIME LAPSE IMAGING;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMES, MAMMALIAN; CRICETINAE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HEPATOCYTE GROWTH FACTOR; HUMANS; KARYOPHERINS; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; METAPHASE; MICROTUBULES; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS; RAN GTP-BINDING PROTEIN; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TIME-LAPSE IMAGING;

EID: 84867007519     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045836     Document Type: Article

References (39)

1. Maiato H, DeLuca J, Salmon ED, Earnshaw WC, (2004) The dynamic kinetochore-microtubule interface. Journal of cell science 117: 5461-5477.
2. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A, (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127: 983-997.
3. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, et al. (2006) Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127: 969-982.
4. Sundin LJ, Guimaraes GJ, Deluca JG, (2011) The NDC80 complex proteins Nuf2 and Hec1 make distinct contributions to kinetochore-microtubule attachment in mitosis. Molecular biology of the cell 22: 759-768.
5. McCleland ML, Kallio MJ, Barrett-Wilt GA, Kestner CA, Shabanowitz J, et al. (2004) The vertebrate Ndc80 complex contains Spc24 and Spc25 homologs, which are required to establish and maintain kinetochore-microtubule attachment. Current biology: CB 14: 131-137.
6. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, et al. (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468: 576-579.
7. Gaitanos TN, Santamaria A, Jeyaprakash AA, Wang B, Conti E, et al. (2009) Stable kinetochore-microtubule interactions depend on the Ska complex and its new component Ska3/C13Orf3. The EMBO journal 28: 1442-1452.
8. Kalab P, Pralle A, Isacoff EY, Heald R, Weis K, (2006) Analysis of a RanGTP-regulated gradient in mitotic somatic cells. Nature 440: 697-701.
9. Kalab P, Heald R, (2008) The RanGTP gradient- a GPS for the mitotic spindle. Journal of cell science 121: 1577-1586.
10. Wilde A, Lizarraga SB, Zhang L, Wiese C, Gliksman NR, et al. (2001) Ran stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nature cell biology 3: 221-227.
11. Ciciarello M, Mangiacasale R, Lavia P, (2007) Spatial control of mitosis by the GTPase Ran. Cellular and molecular life sciences: CMLS 64: 1891-1914.
12. Clarke PR, Zhang C, (2008) Spatial and temporal coordination of mitosis by Ran GTPase. Nature reviews Molecular cell biology 9: 464-477.
13. Kalab P, Weis K, Heald R, (2002) Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 295: 2452-2456.
14. Li HY, Ng WP, Wong CH, Iglesias PA, Zheng Y, (2007) Coordination of chromosome alignment and mitotic progression by the chromosome-based Ran signal. Cell cycle 6: 1886-1895.
15. Arnaoutov A, Dasso M, (2003) The Ran GTPase regulates kinetochore function. Developmental cell 5: 99-111.
16. Nishitani H, Ohtsubo M, Yamashita K, Iida H, Pines J, et al. (1991) Loss of RCC1, a nuclear DNA-binding protein, uncouples the completion of DNA replication from the activation of cdc2 protein kinase and mitosis. The EMBO journal 10: 1555-1564.
17. Lampson MA, Renduchitala K, Khodjakov A, Kapoor TM, (2004) Correcting improper chromosome-spindle attachments during cell division. Nature cell biology 6: 232-237.
18. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, et al. (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes & development 13: 532-544.
19. Brinkley BR, Cartwright J Jr, (1975) Cold-labile and cold-stable microtubules in the mitotic spindle of mammalian cells. Annals of the New York Academy of Sciences 253: 428-439.
20. Musacchio A, Hardwick KG, (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731-741.
21. Kulukian A, Han JS, Cleveland DW, (2009) Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev Cell 16: 105-117.
22. Fuller BG, Lampson MA, Foley EA, Rosasco-Nitcher S, Le KV, et al. (2008) Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature 453: 1132-1136.
23. Santaguida S, Tighe A, D'Alise AM, Taylor SS, Musacchio A, (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. The Journal of cell biology 190: 73-87.
24. Silverman-Gavrila RV, Wilde A, (2006) Ran is required before metaphase for spindle assembly and chromosome alignment and after metaphase for chromosome segregation and spindle midbody organization. Molecular biology of the cell 17: 2069-2080.
25. Bamba C, Bobinnec Y, Fukuda M, Nishida E, (2002) The GTPase Ran regulates chromosome positioning and nuclear envelope assembly in vivo. Current biology: CB 12: 503-507.
26. Stevens D, Gassmann R, Oegema K, Desai A, (2011) Uncoordinated loss of chromatid cohesion is a common outcome of extended metaphase arrest. PloS one 6: e22969.
27. Daum JR, Potapova TA, Sivakumar S, Daniel JJ, Flynn JN, et al. (2011) Cohesion fatigue induces chromatid separation in cells delayed at metaphase. Current biology: CB 21: 1018-1024.
28. Carazo-Salas RE, Gruss OJ, Mattaj IW, Karsenti E, (2001) Ran-GTP coordinates regulation of microtubule nucleation and dynamics during mitotic-spindle assembly. Nature cell biology 3: 228-234.
29. Funabiki H, Murray AW, (2000) The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell 102: 411-424.
30. Arnaoutov A, Azuma Y, Ribbeck K, Joseph J, Boyarchuk Y, et al. (2005) Crm1 is a mitotic effector of Ran-GTP in somatic cells. Nature cell biology 7: 626-632.
31. Torosantucci L, De Luca M, Guarguaglini G, Lavia P, Degrassi F, (2008) Localized RanGTP accumulation promotes microtubule nucleation at kinetochores in somatic mammalian cells. Molecular biology of the cell 19: 1873-1882.
32. Anand R, Kim AY, Brent M, Marmorstein R, (2008) Biochemical analysis of MST1 kinase: elucidation of a C-terminal regulatory region. Biochemistry 47: 6719-6726.
33. Cimini D, Wan X, Hirel CB, Salmon ED, (2006) Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Current biology: CB 16: 1711-1718.
34. Santaguida S, Vernieri C, Villa F, Ciliberto A, Musacchio A, (2011) Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. The EMBO journal 30: 1508-1519.
35. Maia AF, Feijao T, Vromans MJ, Sunkel CE, Lens SM, (2010) Aurora B kinase cooperates with CENP-E to promote timely anaphase onset. Chromosoma 119: 405-413.
36. Tatsuka M, Katayama H, Ota T, Tanaka T, Odashima S, et al. (1998) Multinuclearity and increased ploidy caused by overexpression of the aurora- and Ipl1-like midbody-associated protein mitotic kinase in human cancer cells. Cancer research 58: 4811-4816.
37. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, et al. (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. The Journal of cell biology 161: 267-280.
38. Nishitani H, Kobayashi H, Ohtsubo M, Nishimoto T, (1990) Cloning of Xenopus RCC1 cDNA, a homolog of the human RCC1 gene: complementation of tsBN2 mutation and identification of the product. Journal of biochemistry 107: 228-235.
39. Malkusch W (2004) Quantitative Measurements Of FRET Using Standard Fluorescence Microscopy. Bioscience Technology. 32-34.