The Detergent-Soluble Cytoplasmic Pool of Survivin Suppresses Anoikis and Its Expression Is Associated with Metastatic Disease of Human Colon Cancer

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Hori, Masato ^a   Miki, Tomoharu ^a   Okamoto, Mayumi ^a   Yazama, Futoshi ^a   Konishi, Hiroaki ^a   Kaneko, Hiroshi ^a   Shimamoto, Fumio ^a   Ota, Takahide ^b   Temme, Achim ^c   Tatsuka, Masaaki ^a  

^a PREFECTURAL UNIVERSITY OF HIROSHIMA   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN C JUN; SURVIVIN; X LINKED INHIBITOR OF APOPTOSIS;

AGED; ANIMAL CELL; ANOIKIS; ARTICLE; CELL ADHESION; CELL FATE; CELL INTERACTION; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CLINICAL ARTICLE; COLON CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DISTANT METASTASIS; EMBRYO; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR VOLUME;

ANIMALS; ANOIKIS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; CHO CELLS; COLON; COLORECTAL NEOPLASMS; CRICETINAE; CYTOPLASM; DETERGENTS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; I-KAPPA B PROTEINS; IMMUNOPRECIPITATION; INHIBITOR OF APOPTOSIS PROTEINS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NF-KAPPA B; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECTUM; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84873563496     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055710     Document Type: Article

References (70)

1. Chaffer CL, Weinberg RA, (2011) A perspective on cancer cell metastasis. Science 331: 1559-1564.
2. Ruchaud S, Carmena M, Earnshaw WC, (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812.
3. Bolton MA, Lan W, Powers SE, McCleland ML, Kuang J, et al. (2002) Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol Biol Cell 13: 3064-3077.
4. Petersen J, Hagan IM, (2003) S. pombe aurora kinase/survivin is required for chromosome condensation and the spindle checkpoint attachment response. Curr Biol 13: 590-597.
5. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, et al. (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330: 235-239.
6. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, et al. (2010) Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330: 231-235.
7. Yamagishi Y, Honda T, Tanno Y, Watanabe Y, (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330: 239-243.
8. Li F, Ambrosini G, Chu EY, Plescia J, Tognin S, et al. (1998) Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 396: 580-584.
9. Hoffman WH, Biade S, Zilfou JT, Chen J, Murphy M, (2002) Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J Biol Chem 277: 3247-3257.
10. Mirza A, McGuirk M, Hockenberry TN, Wu Q, Ashar H, et al. (2002) Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway. Oncogene 21: 2613-2622.
11. Ambrosini G, Adida C, Altieri DC, (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3: 917-921.
12. Velculescu VE, Madden SL, Zhang L, Lash AE, Yu J, et al. (1999) Analysis of human transcriptomes. Nat Genet 23: 387-388.
13. Altieri DC, (2003) Validating survivin as a cancer therapeutic target. Nat Rev Cancer 3: 46-54.
14. Xia F, Altieri DC, (2006) Mitosis-independent survivin gene expression in vivo and regulation by p53. Cancer Res 66: 3392-3395.
15. Kawasaki H, Altieri DC, Lu CD, Toyoda M, Tenjo T, et al. (1998) Inhibition of apoptosis by survivin predicts shorter survival rates in colorectal cancer. Cancer Res 58: 5071-5074.
16. Sarela AI, Macadam RC, Farmery SM, Markham AF, Guillou PJ, (2000) Expression of the antiapoptosis gene, survivin, predicts death from recurrent colorectal carcinoma. Gut 46: 645-650.
17. Sarela AI, Scott N, Ramsdale J, Markham AF, Guillou PJ, (2001) Immunohistochemical detection of the anti-apoptosis protein, survivin, predicts survival after curative resection of stage II colorectal carcinomas. Ann Surg Oncol 8: 305-310.
18. Chu XY, Chen LB, Wang JH, Su QS, Yang JR, et al. (2012) Overexpression of survivin is correlated with increased invasion and metastasis of colorectal cancer. J Surg Oncol 105: 520-528.
19. Miura K, Fujibuchi W, Ishida K, Naitoh T, Ogawa H, et al. (2011) Inhibitor of apoptosis protein family as diagnostic markers and therapeutic targets of colorectal cancer. Surg Today 41: 175-182.
20. Kalliakmanis JG, Kouvidou C, Latoufis C, Kouvatseas G, Anagnostakis D, et al. (2010) Survivin expression in colorectal carcinomas: correlations with clinicopathological parameters and survival. Dig Dis Sci 55: 2958-2964.
21. Altieri DC, (2006) The case for survivin as a regulator of microtubule dynamics and cell-death decisions. Curr Opin Cell Biol 18: 609-615.
22. Reed JC, (2001) The Survivin saga goes in vivo. J Clin Invest 108: 965-969.
23. Wheatley SP, McNeish IA, (2005) Survivin: a protein with dual roles in mitosis and apoptosis. Int Rev Cytol 247: 35-88.
24. Altieri DC, (2010) Survivin and IAP proteins in cell-death mechanisms. Biochem J 430: 199-205.
25. Li F, Ackermann EJ, Bennett CF, Rothermel AL, Plescia J, et al. (1999) Pleiotropic cell-division defects and apoptosis induced by interference with survivin function. Nat Cell Biol 1: 461-466.
26. Temme A, Rieger M, Reber F, Lindemann D, Weigle B, et al. (2003) Localization, dynamics, and function of survivin revealed by expression of functional survivinDsRed fusion proteins in the living cell. Mol Biol Cell 14: 78-92.
27. Beltrami E, Plescia J, Wilkinson JC, Duckett CS, Altieri DC, (2004) Acute ablation of survivin uncovers p53-dependent mitotic checkpoint functions and control of mitochondrial apoptosis. J Biol Chem 279: 2077-2084.
28. Hendruschk S, Wiedemuth R, Aigner A, Topfer K, Cartellieri M, et al. (2011) RNA interference targeting survivin exerts antitumoral effects in vitro and in established glioma xenografts in vivo. Neuro Oncol 13: 1074-1089.
29. Yue Z, Carvalho A, Xu Z, Yuan X, Cardinale S, et al. (2008) Deconstructing Survivin: comprehensive genetic analysis of Survivin function by conditional knockout in a vertebrate cell line. J Cell Biol 183: 279-296.
30. Lackinger D, Eichhorn U, Kaina B, (2001) Effect of ultraviolet light, methyl methanesulfonate and ionizing radiation on the genotoxic response and apoptosis of mouse fibroblasts lacking c-Fos, p53 or both. Mutagenesis 16: 233-241.
31. Christmann M, Tomicic MT, Origer J, Kaina B, (2005) Fen1 is induced p53 dependently and involved in the recovery from UV-light-induced replication inhibition. Oncogene 24: 8304-8313.
32. Tomicic MT, Christmann M, Kaina B, (2005) Apoptosis in UV-C light irradiated p53 wild-type, apaf-1 and p53 knockout mouse embryonic fibroblasts: interplay of receptor and mitochondrial pathway. Apoptosis 10: 1295-1304.
33. Tamm I, Wang Y, Sausville E, Scudiero DA, Vigna N, et al. (1998) IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res 58: 5315-5320.
34. 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.
35. McNeish IA, Lopes R, Bell SJ, McKay TR, Fernandez M, et al. (2005) Survivin interacts with Smac/DIABLO in ovarian carcinoma cells but is redundant in Smac-mediated apoptosis. Exp Cell Res 302: 69-82.
36. Dohi T, Okada K, Xia F, Wilford CE, Samuel T, et al. (2004) An IAP-IAP complex inhibits apoptosis. J Biol Chem 279: 34087-34090.
37. Mehrotra S, Languino LR, Raskett CM, Mercurio AM, Dohi T, et al. (2010) IAP regulation of metastasis. Cancer Cell 17: 53-64.
38. Golubovskaya VM, Gross S, Kaur AS, Wilson RI, Xu LH, et al. (2003) Simultaneous inhibition of focal adhesion kinase and SRC enhances detachment and apoptosis in colon cancer cell lines. Mol Cancer Res 1: 755-764.
39. Sakurai S, Sonoda Y, Koguchi E, Shinoura N, Hamada H, et al. (2002) Mutated focal adhesion kinase induces apoptosis in a human glioma cell line, T98G. Biochem Biophys Res Commun 293: 174-181.
40. Dohi T, Beltrami E, Wall NR, Plescia J, Altieri DC, (2004) Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J Clin Invest 114: 1117-1127.
41. Fortugno P, Wall NR, Giodini A, O'Connor DS, Plescia J, et al. (2002) Survivin exists in immunochemically distinct subcellular pools and is involved in spindle microtubule function. J Cell Sci 115: 575-585.
42. Qi G, Tuncel H, Aoki E, Tanaka S, Oka S, et al. (2009) Intracellular localization of survivin determines biological behavior in colorectal cancer. Oncol Rep 22: 557-562.
43. 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 Res 58: 4811-4816.
44. Temme A, Herzig E, Weigle B, Morgenroth A, Schmitz M, et al. (2005) Inhibition of malignant glioma cell growth by a survivin mutant retrovirus. Hum Gene Ther 16: 209-222.
45. Kaur H, Bekier ME, Taylor WR, (2010) Regulation of Borealin by phosphorylation at serine 219. J Cell Biochem 111: 1291-1298.
46. Uren AG, Beilharz T, O'Connell MJ, Bugg SJ, van Driel R, et al. (1999) Role for yeast inhibitor of apoptosis (IAP)-like proteins in cell division. Proc Natl Acad Sci U S A 96: 10170-10175.
47. Rajagopalan S, Balasubramanian MK, (2002) Schizosaccharomyces pombe Bir1p, a nuclear protein that localizes to kinetochores and the spindle midzone, is essential for chromosome condensation and spindle elongation during mitosis. Genetics 160: 445-456.
48. Fraser AG, James C, Evan GI, Hengartner MO, (1999) Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr Biol 9: 292-301.
49. Speliotes EK, Uren A, Vaux D, Horvitz HR, (2000) The survivin-like C. elegans BIR-1 protein acts with the Aurora-like kinase AIR-2 to affect chromosomes and the spindle midzone. Mol Cell 6: 211-223.
50. Uren AG, Wong L, Pakusch M, Fowler KJ, Burrows FJ, et al. (2000) Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr Biol 10: 1319-1328.
51. 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.
52. Jones G, Jones D, Zhou L, Steller H, Chu Y, (2000) Deterin, a new inhibitor of apoptosis from Drosophila melanogaster. J Biol Chem 275: 22157-22165.
53. Okada H, Bakal C, Shahinian A, Elia A, Wakeham A, et al. (2004) Survivin loss in thymocytes triggers p53-mediated growth arrest and p53-independent cell death. J Exp Med 199: 399-410.
54. Yang D, Welm A, Bishop JM, (2004) Cell division and cell survival in the absence of survivin. Proc Natl Acad Sci U S A 101: 15100-15105.
55. Okamoto M, Koga S, Tatsuka M, (2010) Differential regulation of caspase-9 by ionizing radiation- and UV-induced apoptotic pathways in thymic cells. Mutat Res 688: 78-87.
56. Shimizu T, Kato MV, Nikaido O, Suzuki F, (1995) A specific chromosome change and distinctive transforming genes are necessary for malignant progression of spontaneous transformation in cultured Chinese hamster embryo cells. Jpn J Cancer Res 86: 546-554.
57. Ota T, Suto S, Katayama H, Han ZB, Suzuki F, et al. (2002) Increased mitotic phosphorylation of histone H3 attributable to AIM-1/Aurora-B overexpression contributes to chromosome number instability. Cancer Res 62: 5168-5177.
58. Banks DP, Plescia J, Altieri DC, Chen J, Rosenberg SH, et al. (2000) Survivin does not inhibit caspase-3 activity. Blood 96: 4002-4003.
59. Conway EM, Pollefeyt S, Cornelissen J, DeBaere I, Steiner-Mosonyi M, et al. (2000) Three differentially expressed survivin cDNA variants encode proteins with distinct antiapoptotic functions. Blood 95: 1435-1442.
60. Shin S, Sung BJ, Cho YS, Kim HJ, Ha NC, et al. (2001) An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and-7. Biochemistry 40: 1117-1123.
61. Dohi T, Xia F, Altieri DC, (2007) Compartmentalized phosphorylation of IAP by protein kinase A regulates cytoprotection. Mol Cell 27: 17-28.
62. Suzuki Y, Nakabayashi Y, Takahashi R, (2001) Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc Natl Acad Sci U S A 98: 8662-8667.
63. Suzuki Y, Nakabayashi Y, Nakata K, Reed JC, Takahashi R, (2001) X-linked inhibitor of apoptosis protein (XIAP) inhibits caspase-3 and-7 in distinct modes. J Biol Chem 276: 27058-27063.
64. Schile AJ, Garcia-Fernandez M, Steller H, (2008) Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes Dev 22: 2256-2266.
65. Jacobs MD, Harrison SC, (1998) Structure of an IkappaBalpha/NF-kappaB complex. Cell 95: 749-758.
66. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, Miyamoto S, (1995) Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation. Genes Dev 9: 2723-2735.
67. Pavlyukov MS, Antipova NV, Balashova MV, Vinogradova TV, Kopantzev EP, et al. (2011) Survivin monomer plays an essential role in apoptosis regulation. J Biol Chem 286: 23296-23307.
68. Kelly RJ, Lopez-Chavez A, Citrin D, Janik JE, Morris JC, (2011) Impacting tumor cell-fate by targeting the inhibitor of apoptosis protein survivin. Mol Cancer 10: 35.
69. Kawai H, Kitamura Y, Nikaido O, Tatsuka M, Hama-Inaba H, et al. (1998) Isolation and characterization of apoptosis-resistant mutants from a radiosensitive mouse lymphoma cell line. Radiat Res 149: 41-51.
70. Ota T, Maeda M, Sakita-Suto S, Zhou X, Murakami M, et al. (2006) RhoGDIbeta lacking the N-terminal regulatory domain suppresses metastasis by promoting anoikis in v-src-transformed cells. Clin Exp Metastasis 23: 323-334.