Ubiquitin in regulation of spindle apparatus and its positioning: Implications in development and disease

Biochemistry and Cell Biology

Volumn 93, Issue 4, 2015, Pages 273-281

  Srivastava, Devika ^a   Chakrabarti, Oishee ^a  

^a SAHA INSTITUTE OF NUCLEAR PHYSICS   (India)

Author keywords

Cortical regulation; Mitosis; Spindle integrity; Spindle positioning; Ubiquitination

Indexed keywords

CELL PROLIFERATION; ENZYMES;

CORTICAL REGULATION; MITOSIS; SPINDLE INTEGRITY; SPINDLE POSITIONING; UBIQUITINATION;

PROTEINS;

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; DEUBIQUITINASE; DYNEIN ADENOSINE TRIPHOSPHATASE; HUNTINGTIN; MAHOGUNIN RING FINGER 1 PROTEIN; NEUROLIGIN 1; PARKIN; SIAH1 PROTEIN; SMAD SPECIFIC UBIQUITIN REGULATORY FACTOR 2; SMURF2 PROTEIN; TRIM E3 LIGASE; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

CELL DIVISION; DEVELOPMENTAL DISORDER; EMBRYO DEVELOPMENT; GERMLINE MUTATION; HUMAN; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; PROTEIN PROCESSING; PROTEIN STABILITY; REVIEW; RING FINGER MOTIF; SPINDLE APPARATUS; UBIQUITINATION; VON HIPPEL LINDAU DISEASE; METABOLISM; MICROTUBULE; PHYSIOLOGY;

HUMANS; MICROTUBULES; SPINDLE APPARATUS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84937865829     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/bcb-2015-0011     Document Type: Review

References (95)

1. Antonio C. Ferby I. Wilhelm H. Jones M. Karsenti E. Nebreda A.R. et al 2000. Xkid, a chromokinesin required for chromosome alignment on the metaphase plate. Cell, 102 (4): 425-435. 10.1016/S0092-8674(00)00048-9. 10966105.
2. Ban R. Matsuzaki H. Akashi T. Sakashita G. Taniguchi H. Park S.Y. 2009. Mitotic Regulation of the Stability of Microtubule Plus-end Tracking Protein EB3 by Ubiquitin Ligase SIAH-1 and Aurora Mitotic Kinases. J Biol. Chem. 284 (41): 28367-28381. 10.1074/jbc.M109.000273. 19696028.
3. Betarbet R. Sherer T.B. Greenamyre J.T. 2005. Ubiquitin proteasome system and Parkinson's diseases. Exp. Neurol. 191 (Suppl. 1): S17-S27. 10.1016/j.expneurol.2004.08.021. 15629758.
4. Bheda A. Gullapalli A. Caplow M. Pagano J.S. Shackelford J. 2010. Ubiquitin editing enzyme UCH L1 and microtubule dynamics Implication in mitosis. Cell Cycle, 9 (5): 980-994. 10.4161/cc.9.5.10934. 20160478.
5. Bird S.L. Heald R. Weis K. 2013. RanGTP and CLASP1 cooperate to position the mitotic spindle. Mol. Biol. Cell, 24 (16): 2506-2514. 10.1091/mbc.E13-03-0150. 23783028.
6. Blangy A. Lane H.A. d'Hérin P. Harper M. Kress M. Nigg E.A. 1995. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell, 83 (7): 1159-1169. 10.1016/0092-8674(95)90142-6. 8548803.
7. Cattaneo E. Zuccato C. Tartari M. 2005. Normal huntingtin function: an alternative approach to Huntington's disease. Nat. Rev. Neurosci. 6 (12): 919-930. 10.1038/nrn1806. 16288298.
8. Caviston J.P. Ross J.L. Antony S.M. Tokito M. Holzbaur E.L. 2007. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc. Natl. Acad. Sci. U.S.A. 104 (24): 10045-10050. 10.1073/pnas.0610628104. 17548833.
9. Chakrabarti O. Hegde R.S. 2009. Functional depletion of mahogunin by cytosolically exposed prion protein contributes to neurodegeneration. Cell, 137 (6): 1136-1147. 10.1016/j.cell.2009.03.042. 19524515.
10. Colin E. Zala D. Liot G. Rangone H. Borrell-Pagès M. Li X.J. et al 2008. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J. 27 (15): 2124-2134. 10.1038/emboj.2008.133. 18615096.
11. Cota C.D. Bagher P. Pelc P. Smith C.O. Bodner C.R. Gunn T.M. 2006. Mice with mutations in Mahogunin ring finger-1 (MGRN1) exhibit abnormal patterning of the left-right axis. Dev. Dyn. 235 (12): 3438-3447. 10.1002/dvdy.20992. 17075880.
12. Cox T.C. Allen L.R. Cox L.L. Hopwood B. Goodwin B. Haan E. et al 2000. New mutations in MID1 provide support for loss of function as the cause of X-linked Opitz syndrome. Hum. Mol. Genet. 9 (17): 2553-2562. 10.1093/hmg/9.17.2553. 11030761.
13. Daniels M.J. Wang Y. Lee M. Venkitaraman A.R. 2004. Abnormal cytokinesis in cells deficient in the breast cancer susceptibility protein BRCA2. Science, 306 (5697): 876-879. 10.1126/science.1102574. 15375219.
14. Delaval B. Ferrand A. Conte N. Larroque C. Hernandez-Verdun D. Prigent C. et al 2004. Aurora B-TACC1 protein complex in cytokinesis. Oncogene, 23 (26): 4516-4522. 10.1038/sj.onc.1207593. 15064709.
15. Delgehyr N. Wieland U. Rangone H. Pinson X. Mao G. Dzhindzhev N.S. et al 2012. Drosophila Mgr, a Prefoldin subunit cooperating with von HippelLindau to regulate tubulin stability. Proc. Natl. Acad. Sci. U.S.A. 109 (15): 5729-5734. 10.1073/pnas.1108537109. 22451918.
16. Deshaies R.J. Joazeiro C.A. 2009. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78: 399-434. 10.1146/annurev.biochem.78.101807.093809. 19489725.
17. Devenport D. 2014. The cell biology of planar cell polarity. J. Cell Biol. 207 (2): 171-179. 10.1083/jcb.201408039. 25349257.
18. Dickins R.A. Frew I.J. House C.M. O'Bryan M.K. Holloway A.J. Haviv I. et al 2002. The ubiquitin ligase component Siah1a is required for completion of meiosis I in male mice. Mol. Cell. Biol. 22 (7): 2294-2303. 10.1128/MCB.22.7.2294-2303.2002. 11884614.
19. Ding Q. Lewis J.J. Strum K.M. Dimayuga E. Bruce-Keller A.J. Dunn J.C. et al 2002. Polyglutamine expansion, protein, aggregation, proteasome activity, and neural survival. J. Biol. Chem. 277 (16): 13935-13942. 10.1074/jbc.M107706200. 11782460.
20. Du Q. Macara I.G. 2004. Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell, 119 (4): 503-516. 10.1016/j.cell.2004.10.028. 15537540.
21. El-Hodiri H.M. Shou W. Etkin L.D. 1997. xnf7 functions in dorsal-ventral patterning of the Xenopus embryo. Dev. Biol. 190 (1): 1-17. 10.1006/dbio.1997.8692. 9331327.
22. Elias S. Thion M.S. Yu H. Sousa C.M. Lasgi C. Morin X. et al 2014. Huntingtin Regulates Mammary Stem Cell Division and Differentiation. Stem Cell Reports, 2 (4): 491-506. 10.1016/j.stemcr.2014.02.011. 24749073.
23. Funabiki H. Murray A.W. 2000. The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell, 102 (4): 411-424. 10.1016/S0092-8674(00)00047-7. 10966104.
24. Gao J. Huo L. Sun X. Liu M. Li D. Dong J.T. et al 2008. The tumor suppressor CYLD regulates microtubule dynamics and plays a role in cell migration. J. Biol. Chem. 283 (14): 8802-8809. 10.1074/jbc.M708470200. 18222923.
25. Germani A. Bruzzoni-Giovanelli H. Fellous A. Gisselbrecht S. Varin-Blank N. Calvo F. 2000. SIAH-1 interacts with α-tubulin and degrades the kinesin Kid by the proteasome pathway during mitosis. Oncogene, 19 (52): 5997-6006. 10.1038/sj.onc.1204002. 11146551.
26. Gillies T.E. Cabernard C. 2011. Cell division orientation in animals. Curr. Biol. 21 (15): R599-R609. 10.1016/j.cub.2011.06.055. 21820628.
27. Godin J.D. Colombo K. Molina-Calavita M. Keryer G. Zala D. Charrin B.C. et al 2010. Huntingtin Is Required for Mitotic Spindle Orientation and Mammalian Neurogenesis. Neuron, 67 (3): 392-406. 10.1016/j.neuron.2010.06.027. 20696378.
28. Gönczy P. 2008. Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell Biol. 9 (5): 355-366. 10.1038/nrm2388. 18431399.
29. Harhaj E.W. Dixit V.M. 2011. Deubiquitinases in the regulation of NF-B signaling. Cell Res. 21 (1): 22-39. 10.1038/cr.2010.166. 21119682.
30. He L. Lu X.Y. Jolly A.F. Eldridge A.G. Watson S.J. Jackson P.K. et al 2003. Spongiform degeneration in mahoganoid mutant mice. Science, 299 (5607): 710-712. 10.1126/science.1079694. 12560552.
31. Hertwig O. 1884. Das Problem der Befruchtung und der Isotropie des Eies. EineTheorie der Vererbung. Jenaische Zeitschriftfür Naturwissenschaft, 18, 276-318.
32. Hoffner G. Kahlem P. Djian P. 2002. Perinuclear localization of huntingtin as a consequence of its binding to microtubules through an interaction with beta-tubulin: relevance to Huntington's disease. J. Cell Sci. 115 (5): 941-948. 11870213.
33. House C.M. Möller A. Bowtell DD. 2009. Siah proteins: novel drug targets in the Ras and hypoxia pathways. Cancer Res. 69 (23): 8835-8838. 10.1158/0008-5472.CAN-09-1676. 19920190.
34. Hristova V.A. Beasley S.A. Rylett R.J. Shaw G.S. 2009. Identification of a novel Zn2+-binding domain in the autosomal recessive juvenile Parkinson related E3 ligase parkin. J. Biol. Chem. 284 (22): 14978-14986. 10.1074/jbc.M808700200. 19339245.
35. Jaakkola P. Mole D.R. Tian Y.M. Wilson M.I. Gielbert J. Gaskell S.J. et al 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science, 292 (5516): 468-472. 10.1126/science.1059796. 11292861.
36. Jiao J. Kim H.Y. Liu R.R. Hogan C.A. Sun K. Tam L.M. et al 2009. Transgenic analysis of the physiological functions of Mahogunin Ring Finger-1 isoforms. Genesis, 47 (8): 524-534. 10.1002/dvg.20529. 19422019.
37. Joukov V. Groen A.C. Prokhorova T. 2006. The BRCA1/BARD1 Heterodimer Modulates Ran-Dependent Mitotic Spindle Assembly. Cell, 127 (3): 539-552. 10.1016/j.cell.2006.08.053. 17081976.
38. Kaelin W.G. Jr 2008. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat. Rev. Cancer, 8 (11): 865-873. 10.1038/nrc2502. 18923434.
39. Kaelin W.G. 2007. Von Hippel-Lindau disease. Annu. Rev. Pathol. 2: 145-173. 10.1146/annurev.pathol.2.010506.092049. 18039096.
40. Kafri M. Levy M. Pilpel Y. 2006. The regulatory utilization of genetic redundancy through responsive backup circuits. Proc. Natl. Acad. Sci. 103 (31): 11653-11658.
41. Kais Z. Chiba N. Ishioka C. Parvin J.D. 2012. Functional differences among BRCA1 missense mutations in the control of centrosome duplication. Oncogene, 31 (6): 799-804. 10.1038/onc.2011.271. 21725363.
42. Kalchman M.A. Graham R.K. Xia G. Koide H.B. Hodgson J.G. Graham K.C. et al 1996. Huntingtin is ubiquitinated and interacts with a specific ubiquitin-conjugating enzyme. J. Biol. Chem. 271 (32): 19385-19394. 10.1074/jbc.271.32.19385. 8702625.
43. Kapitein L.C. Peterman E.J. Kwok B.H. Kim J.H. Kapoor T.M. Schmidt C.F. 2005. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature, 435 (7038): 114-118. 10.1038/nature03503. 15875026.
44. Kim B.Y. Olzmann J.A. Barsh G.S. Chin L.S. Li L. 2007. Spongiform neurodegeneration-associated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol. Biol. Cell, 18 (4): 1129-1142. 10.1091/mbc.E06-09-0787. 17229889.
45. Knoblich J.A. 2008. Mechanisms of Asymmetric Stem Cell Division. Cell, 132 (4): 583-597. 10.1016/j.cell.2008.02.007. 18295577.
46. Kotak S. Busso C. Gönczy P. 2013. NuMA phosphorylation by CDK1 couples mitotic progression with cortical dynein function. EMBO J. 32 (18): 2517-2529. 10.1038/emboj.2013.172. 23921553.
47. Lancaster O.M. Baum B. 2011. Might makes right: Using force to align the mitotic spindle. Nat. Cell Biol. 13 (7): 736-738. 10.1038/ncb0711-736. 21725285.
48. Lin X. Liang M. Feng X.H. 2000. Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling. J. Biol. Chem. 275 (47): 36818-36822. 10.1074/jbc.C000580200. 11016919.
49. Liu M. Aneja R. Sun X. Xie S. Wang H. Wu X. et al 2008. Parkin regulates Eg5 expression by Hsp70 ubiquitination-dependent inactivation of c-Jun NH2-terminal kinase. J. Biol. Chem. 283 (51): 35783-35788. 10.1074/jbc.M806860200. 18845538.
50. Liu W. Xin H. Eckert D.T. Brown J.A. Gnarra J.R. 2011. Hypoxia and cell cycle regulation of the von Hippel-Lindau tumor suppressor. Oncogene, 30 (1): 21-31. 10.1038/onc.2010.395. 20802534.
51. Lu M.S. Johnston C.A. 2013. Molecular pathways regulating mitotic spindle orientation in animal cells. Development, 140 (9): 1843-1856. 10.1242/dev.087627. 23571210.
52. Maresca T.J. Niederstrasser H. Weis K. Heald R. 2005. Xnf7 Contributes to Spindle Integrity through Its Microtubule-Bundling Activity. Curr. Biol. 15 (19): 1755-1761. 10.1016/j.cub.2005.08.049. 16213823.
53. Massoumi R. 2011. CYLD: A deubiquitination enzyme with multiple roles in cancer. Future Oncol. 7 (2): 285-297. 10.2217/fon.10.187. 21345146.
54. McGuire J.R. Rong J. Li S.H. Li X.J. 2006. Interaction of Huntingtin associated protein-1 with kinesin light chain: implications in intracellular trafficking in neurons. J. Biol. Chem. 281 (6): 3552-3559. 10.1074/jbc.M509806200. 16339760.
55. McNally F.J. 2013. Mechanisms of spindle positioning. J. Cell Biol. 200 (2): 131-140. 10.1083/jcb.201210007. 23337115.
56. Metzger M.B. Hristova V.A. Weissman A.M. 2012. HECT and RING finger families of E3 ubiquitin ligases at a glance. J. Cell Sci. 125 (3): 531-537. 10.1242/jcs.091777. 22389392.
57. Miller K.A. Gunn T.M. Carrasquillo M.M. Lamoreux M.L. Galbraith D.B. Barsh G.S. 1997. Genetic Studies of the Mouse Mutations Mahogany and Mahoganoid. Genetics, 146 (4): 1407-1415. 9258683.
58. Molina-Calavita M. Barnat M. Elias S. Aparicio E. Piel M. Humbert S. 2014. Mutant huntingtin affects cortical progenitor cell division and development of the mouse neocortex. J. Neurosci. 34 (30): 10034-10040. 10.1523/JNEUROSCI.0715-14.2014. 25057205.
59. Morin X. Bellaïche Y. 2011. Mitotic Spindle Orientation in Asymmetric and Symmetric Cell Divisions during Animal Development. Dev. Cell, 21 (1): 102-119. 10.1016/j.devcel.2011.06.012. 21763612.
60. Nakayama K. Frew I.J. Hagensen M. Skals M. Habelhah H. Bhoumik A. et al 2004. Siah2 regulates stability of prolyl-hydroxylases, controls HIF1alpha abundance, and modulates physiological responses to hypoxia. Cell, 117 (7): 941-952. 10.1016/j.cell.2004.06.001. 15210114.
61. Narimatsu M. Bose R. Pye M. Zhang L. Miller B. Ching P. et al 2009. Regulation of Planar Cell Polarity by Smurf Ubiquitin Ligases. Cell, 137 (2): 295-307. 10.1016/j.cell.2009.02.025. 19379695.
62. Nasir J. Floresco S.B. O'Kusky J.R. Diewert V.M. Richman J.M. Zeisler J. et al 1995. Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell, 81 (5): 811-823. 10.1016/0092-8674(95)90542-1. 7774020.
63. Neumüller R.A. Knoblich J.A. 2009. Dividing cellular asymmetry: asymmetric cell division its implications for stem cells and cancer. Genes Dev. 23 (23): 2675-2699. 10.1101/gad.1850809. 19952104.
64. Osmundson E.C. Ray D. Moore F.E. Kiyokawa H. 2009. Smurf2 as a novel mitotic regulator: From the spindle assembly checkpoint to tumorigenesis. Cell Div. 4: 14. 10.1186/1747-1028-4-14. 19583833.
65. Parvin J.D. 2009. The BRCA1-dependent ubiquitin ligase, gamma-tubulin, and centrosomes. Environ. Mol. Mutagen. 50 (8): 649-653. 10.1002/em.20475. 19274767.
66. Peng C.Y. Manning L. Albertson R. Doe C.Q. 2000. The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature, 408 (6812): 596-600. 10.1038/35046094. 11117748.
67. Ryser S. Dizin E. Jefford C.E. Delaval B. Gagos S. Christodoulidou A. et al 2009. Distinct roles of BARD1 isoforms in mitosis: full-length BARD1 mediates Aurora B degradation, cancer-associated BARD1beta scaffolds Aurora B and BRCA2. Cancer Res. 69 (3): 1125-1134. 10.1158/0008-5472.CAN-08-2134. 19176389.
68. Sankaran S. Starita L.M. Groen A.C. Ko M.J. Parvin J.D. 2005. Centrosomal microtubule nucleation activity is inhibited by BRCA1-dependent ubiquitination. Mol. Cell. Biol. 25 (19): 8656-8668. 10.1128/MCB.25.19.8656-8668.2005. 16166645.
69. Sawin K.E. Mitchison T.J. 1995. Mutations in the kinesin-like protein Eg5 disrupting localization to the mitotic spindle. Proc. Natl. Acad. Sci. U.S.A. 92 (10): 4289-4293. 10.1073/pnas.92.10.4289. 7753799.
70. Schober M. Schaefer M. Knoblich J.A. 1999. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature, 402 (6761): 548-551. 10.1038/990135. 10591217.
71. Setsuie R. Wada K. 2007. The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem. Int. 51 (2-4): 105-111. 10.1016/j.neuint.2007.05.007. 17586089.
72. Sharp D.J. Yu K.R. Sisson J.C. Sullivan W. Scholey J.M. 1999. Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat. Cell Biol. 1 (1): 51-54. 10.1038/9025. 10559864.
73. Siller H.K. Doe C.Q. 2009. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11 (4): 365-374. 10.1038/ncb0409-365. 19337318.
74. Simons M. Mlodzik M. 2008. Planar cell polarity signaling: from fly development to human disease. Annu. Rev. Genet. 42: 517-540. 10.1146/annurev.genet.42.110807.091432. 18710302.
75. Srivastava D. Chakrabarti O. 2014. Mahogunin-mediated α-tubulin ubiquitination via noncanonical K6 linkage regulates microtubule stability and mitotic spindle orientation. Cell Death Dis. 5: e1064. 10.1038/cddis.2014.1. 24556679.
76. Stevermann L. Liakopoulos D. 2012. Molecular mechanisms in spindle positioning: structures and new concepts. Curr. Opin. Cell Biol. 24 (6): 816-824. 10.1016/j.ceb.2012.10.005. 23142476.
77. Stieglitz B. Morris-Davies A.C. Koliopoulos M.G. Christodoulou E. Rittinger K. 2012. LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep. 13 (9): 840-846. 10.1038/embor.2012.105. 22791023.
78. Stremlau M. Owens C.M. Perron M.J. Kiessling M. Autissier P. Sodroski J. 2004. The cytoplasmic body component TRIM5 alpha restricts HIV-1 infection in Old World monkeys. Nature, 427 (6977): 848-853. 10.1038/nature02343. 14985764.
79. Sun X. Liu M. Hao J. Li D. Luo Y. Wang X. et al 2013. Parkin deficiency contributes to pancreatic tumorigenesis by inducing spindle multipolarity and misorientation. Cell Cycle, 12 (7): 1133-1141. 10.4161/cc.24215. 23470638.
80. Tanenbaum M.E. Medema R.H. 2010. Mechanisms of centrosome separation and bipolar spindle assembly. Dev. Cell, 19 (6): 797-806. 10.1016/j.devcel.2010.11.011. 21145497.
81. Tanenbaum M.E. Macrek L. Janssen A. Geers E.F. Alvarez-Fernández M. Medema R.H. 2009. Kif15 cooperates with eg5 to promote bipolar spindle assembly. Curr. Biol. 19 (20): 1703-1711. 10.1016/j.cub.2009.08.027. 19818618.
82. Tang L.Y. Yamashita M. Coussens N.P. Tang Y. Wang X. Li C. et al 2011. Ablation of Smurf2 reveals an inhibition in TGF-β signaling through multiple mono-ubiquitination of Smad3. EMBO J. 30 (23): 4777-4789. 10.1038/emboj.2011.393. 22045334.
83. Tarapore P. Hanashiro K. Fukasawa K. 2012. Analysis of centrosome localization of BRCA1 and its activity in suppressing centrosomal aster formation. Cell Cycle, 11 (15): 2931-2946. 10.4161/cc.21396. 22833046.
84. Thoma C.R. Toso A. Gutbrodt K.L. Reggi S.P. Frew I.J. Schraml P. et al 2009. VHL loss causes spindle misorientation and chromosome instability. Nat. Cell Biol. 11 (8) 994-1001. 10.1038/ncb1912. 19620968.
85. van Heesbeen R.G. Tanenbaum M.E. Medema R.H. 2014. Balanced Activity of Three Mitotic Motors Is Required for Bipolar Spindle Assembly and Chromosome Segregation. Cell Rep. 8 (4): 948-956. 10.1016/j.celrep.2014.07.015. 25127142.
86. Waters J.C. Cole R.W. Rieder C.L. 1993. The force-producing mechanism for centrosome separation during spindle formation in vertebrates is intrinsic to each aster. J. Cell Biol. 122 (2): 361-372. 10.1083/jcb.122.2.361. 8320259.
87. Wenzel D.M. Lissounov A. Brzovic P.S. Klevit R.E. 2011. UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature, 474 (7349): 105-108. 10.1038/nature09966. 21532592.
88. Whitehead C.M. Winkfein R.J. Rattner J.B. 1996. The relationship of HsEg5 and the actin cytoskeleton to centrosome separation. Cell Motil. Cytoskeleton, 35 (4): 298-308. 10.1002/(SICI)1097-0169(1996)35:4%3C298::AID-CM3%3E3.0.CO;2-3. 8956002.
89. Williams S.E. Fuchs E. 2013. Oriented divisions, fate decisions. Curr. Opin. Cell Biol. 25 (6): 749-758. 10.1016/j.ceb.2013.08.003. 24021274.
90. Wodarz A. Ramrath A. Grimm A. Knust E. 2000. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150 (6): 1361-1374. 10.1083/jcb.150.6.1361. 10995441.
91. Wu L.C. Wang Z.W. Tsan J.T. Spillman M.A. Phung A. Xu X.L. et al 1996. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat. Genet. 14 (4): 430-440. 10.1038/ng1296-430. 8944023.
92. Yang Y. Liu M. Li D. Ran J. Gao J. Suo S. et al 2014. CYLD regulates spindle orientation by stabilizing astral microtubules and promoting dishevelled-NuMA-dynein/dynactin complex formation. Proc. Natl. Acad. Sci. U.S.A. 111 (6): 2158-2163. 10.1073/pnas.1319341111. 24469800.
93. Zeitlin S. Liu J.P. Chapman D.L. Papaioannou V.E. Efstratiadis A. 1995. Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nat. Genet. 11 (2): 155-163. 10.1038/ng1095-155. 7550343.
94. Zhang C. Hughes M. Clarke P.R. 1999. Ran-GTP stabilises microtubule asters and inhibits nuclear assembly in Xenopus egg extracts. J. Cell Sci. 112 (14): 2453-2461. 10381400.
95. Zhang J. Wang Y. Gao Z. Yun Z. Ye J. 2012. Hypoxia-inducible Factor 1 Activation from aP2 (Fabp4)-Cre Mediated Knockout of Von Hippel-Lindau Gene Leads to Embryonic Lethality. Clin. Exp. Pharmacol. Physiol. 39 (2): 145-150. 10.1111/j.1440-1681.2011.05656.x. 22150821.