Quantitative image analysis identifies pVHL as a key regulator of microtubule dynamic instability

Journal of Cell Biology

Volumn 190, Issue 6, 2010, Pages 991-1003

  Thoma, Claudio R ^a,d,e   Matov, Alexandre ^b   Gutbrodt, Katrin L ^a   Hoerner, Christian R ^a,c   Smole, Zlatko ^a   Krek, Wilhelm ^a   Danuser, Gaudenz ^b,e  

^a ETH ZURICH   (Switzerland)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; TUBULIN; VON HIPPEL LINDAU PROTEIN; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATE; HYBRID PROTEIN; MAPRE3 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; NOCODAZOLE;

ARTICLE; CANCER RISK; CELL GROWTH; ENZYME ACTIVITY; GENOTYPE PHENOTYPE CORRELATION; HUMAN; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CARCINOMA; MICROTUBULE ASSEMBLY; PHENOTYPIC VARIATION; POINT MUTATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; VON HIPPEL LINDAU DISEASE; AMINO ACID SEQUENCE; CHEMISTRY; CLUSTER ANALYSIS; DRUG EFFECTS; GENETICS; HYDROLYSIS; METABOLISM; MICROTUBULE; MOLECULAR GENETICS; PHENOTYPE; PROCEDURES; THREE DIMENSIONAL IMAGING;

AMINO ACID SEQUENCE; CLUSTER ANALYSIS; GREEN FLUORESCENT PROTEINS; GUANOSINE TRIPHOSPHATE; HUMANS; HYDROLYSIS; IMAGING, THREE-DIMENSIONAL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; NOCODAZOLE; PHENOTYPE; POINT MUTATION; RECOMBINANT FUSION PROTEINS; TUBULIN; VON HIPPEL-LINDAU DISEASE; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 77957198722     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201006059     Document Type: Article

References (34)

1. Chen, F., T. Kishida, M. Yao, T. Hustad, D. Glavac, M. Dean, J.R. Gnarra, M.L. Orcutt, F.M. Duh, G. Glenn, et al. 1995. Germline mutations in the von Hippel-Lindau disease tumor suppressor gene: correlations with phenotype. Hum. Mutat. 5:66-75. doi:10.1002/humu.1380050109
2. Crossey, P.A., F.M. Richards, K. Foster, J.S. Green, A. Prowse, F. Latif, M.I. Lerman, B. Zbar, N.A. Affara, M.A. Ferguson-Smith, et al. 1994. Identification of intragenic mutations in the von Hippel-Lindau disease tumour suppressor gene and correlation with disease phenotype. Hum. Mol. Genet. 3:1303-1308. doi:10.1093/hmg/3.8.1303
3. Dimitrov, A., M. Quesnoit, S. Moutel, I. Cantaloube, C. Poüs, and F. Perez. 2008. Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues. Science. 322:1353-1356. doi:10.1126/science.1165401
4. Frew, I.J., and W. Krek. 2008. pVHL: a multipurpose adaptor protein. Sci. Signal. 1:pe30. doi:10.1126/scisignal.124pe30
5. Frew, I.J., C.R. Thoma, S. Georgiev, A. Minola, M. Hitz, M. Montani, H. Moch, and W. Krek. 2008. pVHL and PTEN tumour suppressor proteins cooperatively suppress kidney cyst formation. EMBO J. 27:1747-1757. doi:10.1038/emboj.2008.96
6. Gallou, C., D. Chauveau, S. Richard, D. Joly, S. Giraud, S. Olschwang, N. Martin, C. Saquet, Y. Chrétien, A. Méjean, et al. 2004. Genotype-phenotype correlation in von Hippel-Lindau families with renal lesions. Hum. Mutat. 24:215-224. doi:10.1002/humu.20082
7. Hergovich, A., J. Lisztwan, R. Barry, P. Ballschmieter, and W. Krek. 2003. Regulation of microtubule stability by the von Hippel-Lindau tumour suppressor protein pVHL. Nat. Cell Biol. 5:64-70. doi:10.1038/ncb899
8. Hergovich, A., J. Lisztwan, C.R. Thoma, C. Wirbelauer, R.E. Barry, and W. Krek. 2006. Priming-dependent phosphorylation and regulation of the tumor suppressor pVHL by glycogen synthase kinase 3. Mol. Cell. Biol. 26:5784-5796. doi:10.1128/MCB.00232-06
9. Hesterberg, T.C., D.S. Moore, S. Monaghan, A. Clipson, and R. Epstein. 2005. Bootstrap methods and permutation tests. In Introduction to the Practice of Statistics. Fifth edition. D.S. Moore and G.P. McCabe, editors. W.H. Freeman and Co., New York. 14.1-14.70.
10. Hoffman, M.A., M. Ohh, H. Yang, J.M. Klco, M. Ivan, and W.G. Kaelin Jr. 2001. von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF. Hum. Mol. Genet. 10:1019-1027. doi:10.1093/hmg/10.10.1019
11. Iliopoulos, O., M. Ohh, and W.G. Kaelin Jr. 1998. pVHL19 is a biologically active product of the von Hippel-Lindau gene arising from internal translation initiation. Proc. Natl. Acad. Sci. USA. 95:11661-11666. doi:10.1073/pnas.95.20.11661
12. Jaqaman, K., J.F. Dorn, G.S. Jelson, J.D. Tytell, P.K. Sorger, and G. Danuser. 2006. Comparative autoregressive moving average analysis of kinetochore microtubule dynamics in yeast. Biophys. J. 91:2312-2325. doi:10.1529/biophysj. 106.080333
13. 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. doi:10.1038/nmeth.1237
14. Kaelin, W.G. Jr. 2008. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat. Rev. Cancer. 8:865-873. doi:10.1038/nrc2502
15. Kaelin, W.G. Jr., and P.J. Ratcliffe. 2008. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell. 30:393-402. doi:10.1016/j.molcel.2008.04.009
16. Keller, P.J., F. Pampaloni, and E.H. Stelzer. 2007. Three-dimensional preparation and imaging reveal intrinsic microtubule properties. Nat. Methods. 4:843-846. doi:10.1038/nmeth1087
17. Kishida, T., T.M. Stackhouse, F. Chen, M.I. Lerman, and B. Zbar. 1995. Cellular proteins that bind the von Hippel-Lindau disease gene product: mapping of binding domains and the effect of missense mutations. Cancer Res. 55:4544-4548.
18. Knauth, K., C. Bex, P. Jemth, and A. Buchberger. 2006. Renal cell carcinoma risk in type 2 von Hippel-Lindau disease correlates with defects in pVHL stability and HIF-1alpha interactions. Oncogene. 25:370-377.
19. Knauth, K., E. Cartwright, S. Freund, M. Bycroft, and A. Buchberger. 2009. VHL mutations linked to type 2C von Hippel-Lindau disease cause extensive structural perturbations in pVHL. J. Biol. Chem. 284:10514-10522. doi:10.1074/jbc.M809056200
20. Kondo, K., M. Yao, M. Yoshida, T. Kishida, T. Shuin, T. Miura, M. Moriyama, K. Kobayashi, N. Sakai, S. Kaneko, et al. 2002. Comprehensive mutational analysis of the VHL gene in sporadic renal cell carcinoma: relationship to clinicopathological parameters. Genes Chromosomes Cancer. 34:58-68. doi:10.1002/gcc.10054
21. Li, L., L. Zhang, X. Zhang, Q. Yan, Y.A. Minamishima, A.F. Olumi, M. Mao, S. Bartz, and W.G. Kaelin Jr. 2007. Hypoxia-inducible factor linked to differential kidney cancer risk seen with type 2A and type 2B VHL mutations. Mol. Cell. Biol. 27:5381-5392. doi:10.1128/MCB.00282-07
22. Matov, A., K. Applegate, P. Kumar, C.R. Thoma, W. Krek, G. Danuser, and T. Wittmann. 2010. Analysis of microtubule dynamic instability using a plus-end growth marker. Nat. Methods. 7:761-768. doi:10.1038/nmeth.1493
23. Mitchison, T., and M. Kirschner. 1984. Dynamic instability of microtubule growth. Nature. 312:237-242. doi:10.1038/312237a0
24. Ohh, M., Y. Takagi, T. Aso, C.E. Stebbins, N.P. Pavletich, B. Zbar, R.C. Conaway, J.W. Conaway, and W.G.J. Kaelin Jr. 1999. Synthetic peptides define critical contacts between elongin C, elongin B, and the von Hippel-Lindau protein. J. Clin. Invest. 104:1583-1591. doi:10.1172/JCI8161
25. Perez, F., G.S. Diamantopoulos, R. Stalder, and T.E. Kreis. 1999. CLIP-170 highlights growing microtubule ends in vivo. Cell. 96:517-527. doi:10.1016/S0092-8674(00)80656-X
26. Rosa, J., P. Canovas, A. Islam, D.C. Altieri, and S.J. Doxsey. 2006. Survivin modulates microtubule dynamics and nucleation throughout the cell cycle. Mol. Biol. Cell. 17:1483-1493. doi:10.1091/mbc.E05-08-0723
27. Schek, H.T. III, M.K. Gardner, J. Cheng, D.J. Odde, and A.J. Hunt. 2007. Microtubule assembly dynamics at the nanoscale. Curr. Biol. 17:1445-1455. doi:10.1016/j.cub.2007.07.011
28. Schermer, B., C. Ghenoiu, M. Bartram, R.U. Müller, F. Kotsis, M. Höhne, W. Kühn, M. Rapka, R. Nitschke, H. Zentgraf, et al. 2006. The von Hippel-Lindau tumor suppressor protein controls ciliogenesis by orienting microtubule growth. J. Cell Biol. 175:547-554. doi:10.1083/jcb.200605092
29. Schrijver, A. 2003. Combinatorial Optimization. Springer, Heidelberg. 1,800 pp.
30. Stepanova, T., J. Slemmer, C.C. Hoogenraad, G. Lansbergen, B. Dortland, C.I. De Zeeuw, F. Grosveld, G. van Cappellen, A. Akhmanova, and N. Galjart. 2003. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23:2655-2664.
31. Thoma, C.R., I.J. Frew, C.R. Hoerner, M. Montani, H. Moch, and W. Krek. 2007. pVHL and GSK3beta are components of a primary cilium-maintenance signalling network. Nat. Cell Biol. 9:588-595. doi:10.1038/ncb1579
32. Thoma, C.R., A. Toso, K.L. Gutbrodt, S.P. Reggi, I.J. Frew, P. Schraml, A. Hergovich, H. Moch, P. Meraldi, and W. Krek. 2009. VHL loss causes spindle misorientation and chromosome instability. Nat. Cell Biol. 11:994-1001. doi:10.1038/ncb1912
33. Vasquez, R.J., B. Howell, A.M.C. Yvon, P. Wadsworth, and L. Cassimeris. 1997. Nanomolar concentrations of nocodazole alter microtubule dynamic instability in vivo and in vitro. Mol. Biol. Cell. 8:973-985.
34. Weisenberg, R.C., W.J. Deery, and P.J. Dickinson. 1976. Tubulin-nucleotide interactions during the polymerization and depolymerization of microtubules. Biochemistry. 15:4248-4254. doi:10.1021/bi00664a018