Excess centrosomes disrupt endothelial cell migration via centrosome scattering

Journal of Cell Biology

Volumn 206, Issue 2, 2014, Pages 257-272

  Kushner, Erich J ^a   Ferro, Luke S ^a   Liu, Jie Yu ^a   Durrant, Jessica R ^a   Rogers, Stephen L ^a   Dudley, Andrew C ^a,b   Bautch, Victoria L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA TUBULIN; PERICENTRIN; POLO LIKE KINASE 1;

ANIMAL CELL; ARTICLE; BLOOD VESSEL; CELL FUNCTION; CELL MIGRATION; CELL POLARITY; CENTROSOME; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERPHASE; MICROTUBULE; MITOSIS; MOUSE; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BLOOD VESSELS; CELL MOVEMENT; CENTROSOME; ENDOTHELIAL CELLS; GOLGI APPARATUS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERPHASE; MICE; MICE, TRANSGENIC; MICROTUBULES; TUMOR CELLS, CULTURED;

EID: 84904695566     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201311013     Document Type: Article

References (58)

1. Aird, W.C. 2012. Endothelial cell heterogeneity. Cold Spring Harb Perspect Med. 2:a006429. http://dx.doi.org/10.1101/cshperspect.a006429
2. Applegate, K.T., S. Besson, A. Matov, M.H. Bagonis, K. Jaqaman, and G. Danuser. 2011. plusTipTracker: Quantitative image analysis software for the measurement of microtubule dynamics. J. Struct. Biol. 176:168-184. http://dx.doi.org/10.1016/j.jsb.2011.07.009
3. Badano, J.L., T.M. Teslovich, and N. Katsanis. 2005. The centrosome in human genetic disease. Nat. Rev. Genet. 6:194-205. http://dx.doi.org/10.1038/nrg1557
4. Balconi, G., R. Spagnuolo, and E. Dejana. 2000. Development of endothelial cell lines from embryonic stem cells: A tool for studying genetically manipulated endothelial cells in vitro. Arterioscler. Thromb. Vasc. Biol. 20:1443-1451. http://dx.doi.org/10.1161/01.ATV.20.6.1443
5. Berginski, M.E., E.A. Vitriol, K.M. Hahn, and S.M. Gomez. 2011. High-resolution quantification of focal adhesion spatiotemporal dynamics in living cells. PLoS ONE. 6:e22025. http://dx.doi.org/10.1371/journal.pone.0022025
6. Bettencourt-Dias, M., and D.M. Glover. 2007. Centrosome biogenesis and function: centrosomics brings new understanding. Nat. Rev. Mol. Cell Biol. 8:451-463. http://dx.doi.org/10.1038/nrm2180
7. Bornens, M. 2012. The centrosome in cells and organisms. Science. 335:422- 426. http://dx.doi.org/10.1126/science.1209037
8. Boveri, T. 1888. Zellen-Studien II: Die Befruchtung und Teilung des Eies von Ascaris megalocephala. Gustav Fischer Verlag, Jena, Germany. 198 pp.
9. Boveri, T. 1901. Uber die natur der centrosomen. Jena Z Med. Naturw. 28: 1-220.
10. Carmeliet, P., and R.K. Jain. 2011. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 10:417-427. http://dx.doi.org/10.1038/nrd3455
11. Casenghi, M., P. Meraldi, U. Weinhart, P.I. Duncan, R. Körner, and E.A. Nigg. 2003. Polo-like kinase 1 regulates Nlp, a centrosome protein involved in microtubule nucleation. Dev. Cell. 5:113-125. http://dx.doi.org/10.1016/S1534-5807(03)00193-X
12. Chen, H., Z. Huang, K. Dutta, S. Blais, T.A. Neubert, X. Li, D. Cowburn, N.J. Traaseth, and M. Mohammadi. 2013. Cracking the molecular origin of intrinsic tyrosine kinase activity through analysis of pathogenic gain-of-function mutations. Cell Reports. 4:376-384. http://dx.doi.org/10.1016/j.celrep.2013.06.025
13. Dudley, A.C., Z.A. Khan, S.-C. Shih, S.-Y. Kang, B.M.M. Zwaans, J. Bischoff, and M. Klagsbrun. 2008. Calcification of multipotent prostate tumor endothelium. Cancer Cell. 14:201-211. http://dx.doi.org/10.1016/j.ccr.2008.06.017
14. Elowe, S., S. Hümmer, A. Uldschmid, X. Li, and E.A. Nigg. 2007. Tensionsensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev. 21:2205-2219. http://dx.doi.org/10.1101/gad.436007
15. Eot-Houllier, G., M. Venoux, S. Vidal-Eychenié, M.T. Hoang, D. Giorgi, and S. Rouquier. 2010. Plk1 regulates both ASAP localization and its role in spindle pole integrity. J. Biol. Chem. 285:29556-29568. http://dx.doi.org/10.1074/jbc.M110.144220
16. Fu, J., and D.M. Glover. 2012. Structured illumination of the interface between centriole and peri-centriolar material. Open Biol. 2:120104. http://dx.doi.org/10.1098/rsob.120104
17. Ganem, N.J., S.A. Godinho, and D. Pellman. 2009. A mechanism linking extra centrosomes to chromosomal instability. Nature. 460:278-282. http://dx.doi.org/10.1038/nature08136
18. Golsteyn, R.M., S.J. Schultz, J. Bartek, A. Ziemiecki, T. Ried, and E.A. Nigg. 1994. Cell cycle analysis and chromosomal localization of human Plk1, a putative homologue of the mitotic kinases Drosophila polo and Saccharomyces cerevisiae Cdc5. J. Cell Sci. 107:1509-1517.
19. Habedanck, R., Y.D. Stierhof, C.J. Wilkinson, and E.A. Nigg. 2005. The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7:1140-1146. http://dx.doi.org/10.1038/ncb1320
20. Hanisch, A., A. Wehner, E.A. Nigg, and H.H.W. Silljé. 2006. Different Plk1 functions show distinct dependencies on Polo-Box domain-mediated targeting. Mol. Biol. Cell. 17:448-459. http://dx.doi.org/10.1091/mbc.E05-08-0801
21. Haren, L., T. Stearns, and J. Lüders. 2009. Plk1-dependent recruitment of gamma-tubulin complexes to mitotic centrosomes involves multiple PCM components. PLoS ONE. 4:e5976. http://dx.doi.org/10.1371/journal.pone.0005976
22. Hida, K., Y. Hida, D.N. Amin, A.F. Flint, D. Panigrahy, C.C. Morton, and M. Klagsbrun. 2004. Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res. 64:8249-8255. http://dx.doi.org/10.1158/0008-5472.CAN-04-1567
23. Holland, A.J., W. Lan, and D.W. Cleveland. 2010. Centriole duplication: A lesson in self-control. Cell Cycle. 9:2731-2736. http://dx.doi.org/10.4161/cc.9.14.12184
24. Hurtado, L., C. Caballero, M.P. Gavilan, J. Cardenas, M. Bornens, and R.M. Rios. 2011. Disconnecting the Golgi ribbon from the centrosome prevents directional cell migration and ciliogenesis. J. Cell Biol. 193:917- 933. http://dx.doi.org/10.1083/jcb.201011014
25. Jaqaman, K., D. Loerke, M. Mettlen, H. Kuwata, S. Grinstein, S.L. Schmid, and G. Danuser. 2008. Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods. 5:695-702. http://dx.doi.org/10.1038/nmeth.1237
26. Kappas, N.C., G. Zeng, J.C. Chappell, J.B. Kearney, S. Hazarika, K.G. Kallianos, C. Patterson, B.H. Annex, and V.L. Bautch. 2008. The VEGF receptor Flt-1 spatially modulates Flk-1 signaling and blood vessel branching. J. Cell Biol. 181:847-858. http://dx.doi.org/10.1083/jcb.200709114
27. Kaverina, I., and A. Straube. 2011. Regulation of cell migration by dynamic microtubules. Semin. Cell Dev. Biol. 22:968-974. http://dx.doi.org/10.1016/j.semcdb.2011.09.017
28. Kiyomitsu, T., and I.M. Cheeseman. 2012. Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat. Cell Biol. 14:311-317. http://dx.doi.org/10.1038/ncb2440
29. Kollman, J.M., A. Merdes, L. Mourey, and D.A. Agard. 2011. Microtubule nucleation by γ-tubulin complexes. Nat. Rev. Mol. Cell Biol. 12:709-721. http://dx.doi.org/10.1038/nrm3209
30. Koonce, M.P., J. Köhler, R. Neujahr, J.-M. Schwartz, I. Tikhonenko, and G. Gerisch. 1999. Dynein motor regulation stabilizes interphase microtubule arrays and determines centrosome position. EMBO J. 18:6786-6792. http://dx.doi.org/10.1093/emboj/18.23.6786
31. Kuijpers, M., and C.C. Hoogenraad. 2011. Centrosomes, microtubules and neuronal development. Mol. Cell. Neurosci. 48:349-358. http://dx.doi.org/10.1016/j.mcn.2011.05.004
32. Kwon, M., S.A. Godinho, N.S. Chandhok, N.J. Ganem, A. Azioune, M. Thery, and D. Pellman. 2008. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 22:2189-2203. http://dx.doi.org/10.1101/gad.1700908
33. Lawo, S., M. Hasegan, G.D. Gupta, and L. Pelletier. 2012. Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat. Cell Biol. 14:1148-1158. http://dx.doi.org/10.1038/ncb2591
34. Levy, J.R., and E.L.F. Holzbaur. 2008. Dynein drives nuclear rotation during forward progression of motile fibroblasts. J. Cell Sci. 121:3187-3195. http://dx.doi.org/10.1242/jcs.033878
35. Lindon, C., and J. Pines. 2004. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 164:233-241. http://dx.doi.org/10.1083/jcb.200309035
36. Lingle, W.L., W.H. Lutz, J.N. Ingle, N.J. Maihle, and J.L. Salisbury. 1998. Centrosome hypertrophy in human breast tumors: implications for genomic stability and cell polarity. Proc. Natl. Acad. Sci. USA. 95:2950- 2955. http://dx.doi.org/10.1073/pnas.95.6.2950
37. Luxton, G.W.G., and G.G. Gundersen. 2011. Orientation and function of the nuclear-centrosomal axis during cell migration. Curr. Opin. Cell Biol. 23:579-588. http://dx.doi.org/10.1016/j.ceb.2011.08.001
38. Magidson, V., J. Lončarek, P. Hergert, C.L. Rieder, and A. Khodjakov. 2007. Laser microsurgery in the GFP era: a cell biologist's perspective. Methods Cell Biol. 82:239-266. http://dx.doi.org/10.1016/S0091-679X(06)82007-8
39. Mahjoub, M.R., and T. Stearns. 2012. Supernumerary centrosomes nucleate extra cilia and compromise primary cilium signaling. Curr. Biol. 22:1628- 1634. http://dx.doi.org/10.1016/j.cub.2012.06.057
40. Mennella, V., B. Keszthelyi, K.L. McDonald, B. Chhun, F. Kan, G.C. Rogers, B. Huang, and D.A. Agard. 2012. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat. Cell Biol. 14:1159-1168. http://dx.doi.org/10.1038/ncb2597
41. Mikhailov, A., and G.G. Gundersen. 1998. Relationship between microtubule dynamics and lamellipodium formation revealed by direct imaging of microtubules in cells treated with nocodazole or taxol. Cell Motil. Cytoskeleton. 41:325-340. http://dx.doi.org/10.1002/(SICI)1097-0169(1998)41:4<325::AID-CM5>3.0.CO;2-D
42. Miller, P.M., A.W. Folkmann, A.R. Maia, N. Efimova, A. Efimov, and I. Kaverina. 2009. Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat. Cell Biol. 11:1069- 1080. http://dx.doi.org/10.1038/ncb1920
43. Myers, K.A., K.T. Applegate, G. Danuser, R.S. Fischer, and C.M. Waterman. 2011. Distinct ECM mechanosensing pathways regulate microtubule dynamics to control endothelial cell branching morphogenesis. J. Cell Biol. 192:321-334. http://dx.doi.org/10.1083/jcb.201006009
44. Nakatsu, M.N., J. Davis, and C.C. Hughes. 2007. Optimized fibrin gel bead assay for the study of angiogenesis. J. Vis. Exp. 3:186.
45. Neef, R., U. Gruneberg, R. Kopajtich, X. Li, E.A. Nigg, H. Sillje, and F.A. Barr. 2007. Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat. Cell Biol. 9:436-444. http://dx.doi.org/10.1038/ncb1557
46. Petrie, R.J., A.D. Doyle, and K.M. Yamada. 2009. Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 10:538-549. http://dx.doi.org/10.1038/nrm2729
47. Robinson, J.T., E.J. Wojcik, M.A. Sanders, M. McGrail, and T.S. Hays. 1999. Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. J. Cell Biol. 146:597-608. http://dx.doi.org/10.1083/jcb.146.3.597
48. Sathasivam, K., B. Woodman, A. Mahal, F. Bertaux, E.E. Wanker, D.T. Shima, and G.P. Bates. 2001. Centrosome disorganization in fibroblast cultures derived from R6/2 Huntington's disease (HD) transgenic mice and HD patients. Hum. Mol. Genet. 10:2425-2435. http://dx.doi.org/10.1093/hmg/10.21.2425
49. Silkworth, W.T., I.K. Nardi, L.M. Scholl, and D. Cimini. 2009. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS ONE. 4:e6564. http://dx.doi.org/10.1371/journal.pone.0006564
50. Sluder, G., and A. Khodjakov. 2010. Centriole duplication: analogue control in a digital age. Cell Biol. Int. 34:1239-1245. http://dx.doi.org/10.1042/CBI20100612
51. Sonnen, K.F., L. Schermelleh, H. Leonhardt, and E.A. Nigg. 2012. 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol. Open. 1:965-976. http://dx.doi.org/10.1242/bio.20122337
52. Tanaka, T., F.F. Serneo, C. Higgins, M.J. Gambello, A. Wynshaw-Boris, and J.G. Gleeson. 2004. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165:709-721. http://dx.doi.org/10.1083/jcb.200309025
53. Tapley, E.C., and D.A. Starr. 2013. Connecting the nucleus to the cytoskeleton by SUN-KASH bridges across the nuclear envelope. Curr. Opin. Cell Biol. 25:57-62. http://dx.doi.org/10.1016/j.ceb.2012.10.014
54. Taylor, S.M., K.R. Nevis, H.L. Park, G.C. Rogers, S.L. Rogers, J.G. Cook, and V.L. Bautch. 2010. Angiogenic factor signaling regulates centrosome duplication in endothelial cells of developing blood vessels. Blood. 116: 3108-3117. http://dx.doi.org/10.1182/blood-2010-01-266197
55. Vinogradova, T., R. Paul, A.D. Grimaldi, J. Loncarek, P.M. Miller, D. Yampolsky, V. Magidson, A. Khodjakov, A. Mogilner, and I. Kaverina. 2012. Concerted effort of centrosomal and Golgi-derived microtubules is required for proper Golgi complex assembly but not for maintenance. Mol. Biol. Cell. 23:820-833. http://dx.doi.org/10.1091/mbc.E11-06-0550
56. Waterman-Storer, C.M., R.A. Worthylake, B.P. Liu, K. Burridge, and E.D. Salmon. 1999. Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat. Cell Biol. 1:45-50. http://dx.doi.org/10.1038/9018
57. Wu, J., H.P. Cho, D.B. Rhee, D.K. Johnson, J. Dunlap, Y. Liu, and Y. Wang. 2008. Cdc14B depletion leads to centriole amplification, and its overexpression prevents unscheduled centriole duplication. J. Cell Biol. 181:475-483. http://dx.doi.org/10.1083/jcb.200710127
58. Yadav, S., S. Puri, and A.D. Linstedt. 2009. A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Mol. Biol. Cell. 20:1728-1736. http://dx.doi.org/10.1091/mbc.E08-10-1077