Published online 25 December 2000. doi:10.1083/jcb.151.7.1575
© The Rockefeller University Press,
0021-9525/2000//1575 $5.00
The Journal of Cell Biology, Volume 151, Number 7,
, 2000 1575-1582
Human Survivin Is a Kinetochore-Associated Passenger Protein
Dimitrios A. Skoufiasa,
Cristiana Mollinaria,
Françoise B. Lacroixa, and
Robert L. Margolisa
a Institut de Biologie Structurale Jean-Pierre Ebel (Commissariat á l'Energie Atomique–Centre National de la Recherche Scientifique), 38027 Grenoble Cedex 1, France
Institut de Biologie Structurale Jean-Pierre Ebel (CEA-CNRS), 41 rue Jules Horowitz, 38027 Grenoble cedex 1, France.(33) 4 76 88 54 94(33) 4 76 88 96 16
margolis{at}ibs.fr
Survivin, a dimeric baculovirus inhibitor of apoptosis repeat (BIR) motif protein that is principally expressed in G2 and mitosis, has been associated with protection against apoptosis of cells that exit mitosis aberrantly. Mammalian survivin has been reported to associate with centrosomes and with the mitotic spindle. We have expressed a human hemagglutinin-tagged survivin plasmid to determine its localization, and find instead that it clearly acts as a passenger protein. In HeLa cells, survivin first associates with the kinetochores, and then translocates to the spindle midzone during anaphase and, finally, to the midbody during cell cleavage. Its localization is similar to that of TD-60, a known passenger protein. Both a point mutation in the baculovirus IAP repeat motif (C84A) and a COOH-terminal deletion mutant (
106) of survivin fail to localize to either kinetochores or midbodies, but neither interferes with cell cleavage. The interphase localization of survivin is cell cycle regulated since in permanently transfected NIH3T3 cells it is excluded from the nuclei until G2, where it localizes with centromeres. Survivin remains associated with mitotic kinetochores when microtubule assembly is disrupted and its localization is thus independent of microtubules. We conclude that human survivin is positioned to have an important function in the mechanism of cell cleavage.
Key Words: survivin mitosis kinetochore passenger protein cytokinesis
© 2000 The Rockefeller University Press
Abbreviations used in this paper: BIR, baculovirus IAP repeat; HA, hemagglutinin; IAP, inhibitor of apoptosis protein.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Fu, D.-H., Jiang, W., Zheng, J.-T., Zhao, G.-Y., Li, Y., Yi, H., Li, Z.-R., Jiang, J.-D., Yang, K.-Q., Wang, Y., Si, S.-Y.
(2008). Jadomycin B, an Aurora-B kinase inhibitor discovered through virtual screening. Molecular Cancer Therapeutics
7: 2386-2393
[Abstract]
[Full Text]
-
Hu, H., Shikama, Y., Matsuoka, I., Kimura, J.
(2008). Terminally differentiated neutrophils predominantly express Survivin-2{alpha}, a dominant-negative isoform of Survivin. J. Leukoc. Biol.
83: 393-400
[Abstract]
[Full Text]
-
Skoufias, D. A., Indorato, R.-L., Lacroix, F., Panopoulos, A., Margolis, R. L.
(2007). Mitosis persists in the absence of Cdk1 activity when proteolysis or protein phosphatase activity is suppressed. JCB
179: 671-685
[Abstract]
[Full Text]
-
Lechler, P., Wu, X., Bernhardt, W., Campean, V., Gastiger, S., Hackenbeck, T., Klanke, B., Weidemann, A., Warnecke, C., Amann, K., Engehausen, D., Willam, C., Eckardt, K.-U., Rodel, F., Wiesener, M. S.
(2007). The Tumor Gene Survivin Is Highly Expressed in Adult Renal Tubular Cells: Implications for a Pathophysiological Role in the Kidney. Am. J. Pathol.
171: 1483-1498
[Abstract]
[Full Text]
-
Niikura, Y., Dixit, A., Scott, R., Perkins, G., Kitagawa, K.
(2007). BUB1 mediation of caspase-independent mitotic death determines cell fate. JCB
178: 283-296
[Abstract]
[Full Text]
-
Leung, C. G., Xu, Y., Mularski, B., Liu, H., Gurbuxani, S., Crispino, J. D.
(2007). Requirements for survivin in terminal differentiation of erythroid cells and maintenance of hematopoietic stem and progenitor cells. JEM
204: 1603-1611
[Abstract]
[Full Text]
-
Colnaghi, R., Connell, C. M., Barrett, R. M. A., Wheatley, S. P.
(2006). Separating the Anti-apoptotic and Mitotic Roles of Survivin. J. Biol. Chem.
281: 33450-33456
[Abstract]
[Full Text]
-
Walter, D., Wissing, S., Madeo, F., Fahrenkrog, B.
(2006). The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J. Cell Sci.
119: 1843-1851
[Abstract]
[Full Text]
-
Lens, S. M.A., Rodriguez, J. A., Vader, G., Span, S. W., Giaccone, G., Medema, R. H.
(2006). Uncoupling the Central Spindle-associated Function of the Chromosomal Passenger Complex from Its Role at Centromeres. Mol. Biol. Cell
17: 1897-1909
[Abstract]
[Full Text]
-
Chang, C.-J., Goulding, S., Adams, R. R., Earnshaw, W. C., Carmena, M.
(2006). Drosophila Incenp is required for cytokinesis and asymmetric cell division during development of the nervous system. J. Cell Sci.
119: 1144-1153
[Abstract]
[Full Text]
-
Xia, W., Bisi, J., Strum, J., Liu, L., Carrick, K., Graham, K. M., Treece, A. L., Hardwicke, M. A., Dush, M., Liao, Q., Westlund, R. E., Zhao, S., Bacus, S., Spector, N. L.
(2006). Regulation of Survivin by ErbB2 Signaling: Therapeutic Implications for ErbB2-Overexpressing Breast Cancers. Cancer Res.
66: 1640-1647
[Abstract]
[Full Text]
-
Caldas, H, Holloway, M P, Hall, B M, Qualman, S J, Altura, R A
(2006). Survivin-directed RNA interference cocktail is a potent suppressor of tumour growth in vivo. J. Med. Genet.
43: 119-128
[Abstract]
[Full Text]
-
Huang, H.-K., Bailis, J. M., Leverson, J. D., Gomez, E. B., Forsburg, S. L., Hunter, T.
(2005). Suppressors of Bir1p (Survivin) Identify Roles for the Chromosomal Passenger Protein Pic1p (INCENP) and the Replication Initiation Factor Psf2p in Chromosome Segregation. Mol. Cell. Biol.
25: 9000-9015
[Abstract]
[Full Text]
-
Saffin, J.-M., Venoux, M., Prigent, C., Espeut, J., Poulat, F., Giorgi, D., Abrieu, A., Rouquier, S.
(2005). ASAP, a human microtubule-associated protein required for bipolar spindle assembly and cytokinesis. Proc. Natl. Acad. Sci. USA
102: 11302-11307
[Abstract]
[Full Text]
-
Jiang, Y., de Bruin, A., Caldas, H., Fangusaro, J., Hayes, J., Conway, E. M., Robinson, M. L., Altura, R. A.
(2005). Essential Role for Survivin in Early Brain Development. J. Neurosci.
25: 6962-6970
[Abstract]
[Full Text]
-
Mollinari, C., Kleman, J.-P., Saoudi, Y., Jablonski, S. A., Perard, J., Yen, T. J., Margolis, R. L.
(2005). Ablation of PRC1 by Small Interfering RNA Demonstrates that Cytokinetic Abscission Requires a Central Spindle Bundle in Mammalian Cells, whereas Completion of Furrowing Does Not. Mol. Biol. Cell
16: 1043-1055
[Abstract]
[Full Text]
-
Gerl, R., Vaux, D. L.
(2005). Apoptosis in the development and treatment of cancer. Carcinogenesis
26: 263-270
[Abstract]
[Full Text]
-
Scrittori, L., Skoufias, D. A., Hans, F., Gerson, V., Sassone-Corsi, P., Dimitrov, S., Margolis, R. L.
(2005). A Small C-Terminal Sequence of Aurora B Is Responsible for Localization and Function. Mol. Biol. Cell
16: 292-305
[Abstract]
[Full Text]
-
Johnson, M. E., Howerth, E. W.
(2004). Survivin: A Bifunctional Inhibitor of Apoptosis Protein. Vet Pathol
41: 599-607
[Abstract]
[Full Text]
-
Jiang, Y., Saavedra, H. I., Holloway, M. P., Leone, G., Altura, R. A.
(2004). Aberrant Regulation of Survivin by the RB/E2F Family of Proteins. J. Biol. Chem.
279: 40511-40520
[Abstract]
[Full Text]
-
Beardmore, V. A., Ahonen, L. J., Gorbsky, G. J., Kallio, M. J.
(2004). Survivin dynamics increases at centromeres during G2/M phase transition and is regulated by microtubule-attachment and Aurora B kinase activity. J. Cell Sci.
117: 4033-4042
[Abstract]
[Full Text]
-
Iurlaro, M., Demontis, F., Corada, M., Zanetta, L., Drake, C., Gariboldi, M., Peiro, S., Cano, A., Navarro, P., Cattelino, A., Tognin, S., Marchisio, P. C., Dejana, E.
(2004). VE-Cadherin Expression and Clustering Maintain Low Levels of Survivin in Endothelial Cells. Am. J. Pathol.
165: 181-189
[Abstract]
[Full Text]
-
Alsop, G. B., Zhang, D.
(2004). Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes. J. Cell Sci.
117: 1591-1602
[Abstract]
[Full Text]
-
Song, Z., Liu, S., He, H., Hoti, N., Wang, Y., Feng, S., Wu, M.
(2004). A Single Amino Acid Change (Asp 53-> Ala53) Converts Survivin from Anti-apoptotic to Pro-apoptotic. Mol. Biol. Cell
15: 1287-1296
[Abstract]
[Full Text]
-
Martinez, A., Bellosillo, B., Bosch, F., Ferrer, A., Marce, S., Villamor, N., Ott, G., Montserrat, E., Campo, E., Colomer, D.
(2004). Nuclear Survivin Expression in Mantle Cell Lymphoma Is Associated with Cell Proliferation and Survival. Am. J. Pathol.
164: 501-510
[Abstract]
[Full Text]
-
Fukuda, S., Mantel, C. R., Pelus, L. M.
(2004). Survivin regulates hematopoietic progenitor cell proliferation through p21WAF1/Cip1-dependent and -independent pathways. Blood
103: 120-127
[Abstract]
[Full Text]
-
Conway, E. M., Zwerts, F., Van Eygen, V., DeVriese, A., Nagai, N., Luo, W., Collen, D.
(2003). Survivin-Dependent Angiogenesis in Ischemic Brain: Molecular Mechanisms of Hypoxia-Induced Up-Regulation. Am. J. Pathol.
163: 935-946
[Abstract]
[Full Text]
-
Carvalho, A., Carmena, M., Sambade, C., Earnshaw, W. C., Wheatley, S. P.
(2003). Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J. Cell Sci.
116: 2987-2998
[Abstract]
[Full Text]
-
Song, Z., Yao, X., Wu, M.
(2003). Direct Interaction between Survivin and Smac/DIABLO Is Essential for the Anti-apoptotic Activity of Survivin during Taxol-induced Apoptosis. J. Biol. Chem.
278: 23130-23140
[Abstract]
[Full Text]
-
Guidotti, J.-E., Bregerie, O., Robert, A., Debey, P., Brechot, C., Desdouets, C.
(2003). Liver Cell Polyploidization: A Pivotal Role for Binuclear Hepatocytes. J. Biol. Chem.
278: 19095-19101
[Abstract]
[Full Text]
-
Chen, J., Jin, S., Tahir, S. K., Zhang, H., Liu, X., Sarthy, A. V., McGonigal, T. P., Liu, Z., Rosenberg, S. H., Ng, S.-C.
(2003). Survivin Enhances Aurora-B Kinase Activity and Localizes Aurora-B in Human Cells. J. Biol. Chem.
278: 486-490
[Abstract]
[Full Text]
-
Mollinari, C., Kleman, J.-P., Jiang, W., Schoehn, G., Hunter, T., Margolis, R. L.
(2002). PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. JCB
157: 1175-1186
[Abstract]
[Full Text]
-
Guertin, D. A., Trautmann, S., McCollum, D.
(2002). Cytokinesis in Eukaryotes. Microbiol. Mol. Biol. Rev.
66: 155-178
[Abstract]
[Full Text]
-
Blumer, J. B., Chandler, L. J., Lanier, S. M.
(2002). Expression Analysis and Subcellular Distribution of the Two G-protein Regulators AGS3 and LGN Indicate Distinct Functionality. LOCALIZATION OF LGN TO THE MIDBODY DURING CYTOKINESIS. J. Biol. Chem.
277: 15897-15903
[Abstract]
[Full Text]
-
Chen, F., Kamradt, M., Mulcahy, M., Byun, Y., Xu, H., McKay, M. J., Cryns, V. L.
(2002). Caspase Proteolysis of the Cohesin Component RAD21 Promotes Apoptosis. J. Biol. Chem.
277: 16775-16781
[Abstract]
[Full Text]
-
Giodini, A., Kallio, M. J., Wall, N. R., Gorbsky, G. J., Tognin, S., Marchisio, P. C., Symons, M., Altieri, D. C.
(2002). Regulation of Microtubule Stability and Mitotic Progression by Survivin. Cancer Res.
62: 2462-2467
[Abstract]
[Full Text]
-
Eda, M., Yonemura, S., Kato, T., Watanabe, N., Ishizaki, T., Madaule, P., Narumiya, S.
(2002). Rho-dependent transfer of Citron-kinase to the cleavage furrow of dividing cells. J. Cell Sci.
114: 3273-3284
[Abstract]
[Full Text]
-
Fortugno, P., Wall, N. R., Giodini, A., O'Connor, D. S., Plescia, J., Padgett, K. M., Tognin, S., Marchisio, P. C., Altieri, D. C.
(2002). Survivin exists in immunochemically distinct subcellular pools and is involved in spindle microtubule function. J. Cell Sci.
115: 575-585
[Abstract]
[Full Text]
-
Andreassen, P. R., Lacroix, F. B., Lohez, O. D., Margolis, R. L.
(2001). Neither p21WAF1 Nor 14-3-3{sigma} Prevents G2 Progression to Mitotic Catastrophe in Human Colon Carcinoma Cells after DNA Damage, But p21WAF1 Induces Stable G1 Arrest in Resulting Tetraploid Cells. Cancer Res.
61: 7660-7668
[Abstract]
[Full Text]
-
Oegema, K., Desai, A., Rybina, S., Kirkham, M., Hyman, A. A.
(2001). Functional Analysis of Kinetochore Assembly in Caenorhabditis elegans. JCB
153: 1209-1226
[Abstract]
[Full Text]
-
Adams, R. R., Maiato, H., Earnshaw, W. C., Carmena, M.
(2001). Essential Roles of Drosophila Inner Centromere Protein (Incenp) and Aurora B in Histone H3 Phosphorylation, Metaphase Chromosome Alignment, Kinetochore Disjunction, and Chromosome Segregation. JCB
153: 865-880
[Abstract]
[Full Text]
-
Silke, J, Vaux, D.
(2001). Two kinds of BIR-containing protein - inhibitors of apoptosis, or required for mitosis. J. Cell Sci.
114: 1821-1827
[Abstract]
-
Zeitlin, S. G., Shelby, R. D., Sullivan, K. F.
(2001). CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. JCB
155: 1147-1158
[Abstract]
[Full Text]
-
Leverson, J. D., Huang, H.-k., Forsburg, S. L., Hunter, T.
(2002). The Schizosaccharomyces pombe Aurora-related Kinase Ark1 Interacts with the Inner Centromere Protein Pic1 and Mediates Chromosome Segregation and Cytokinesis. Mol. Biol. Cell
13: 1132-1143
[Abstract]
[Full Text]
-
Murata-Hori, M., Tatsuka, M., Wang, Y.-L.
(2002). Probing the Dynamics and Functions of Aurora B Kinase in Living Cells during Mitosis and Cytokinesis. Mol. Biol. Cell
13: 1099-1108
[Abstract]
[Full Text]