Survivin-induced Aurora-B kinase activation: A mechanism by which APC mutations contribute to increased mitoses during colon cancer development

American Journal of Pathology

Volumn 177, Issue 6, 2010, Pages 2816-2826

  Zhang, Tao ^a,b   Fields, Jeremy Z ^e   Opdenaker, Lynn ^a   Otevrel, Tomas ^b   Masuda, Emi ^b   Palazzo, Juan P ^c   Isenberg, Gerald A ^b   Goldstein, Scott D ^b   Brand, Marc ^f   Boman, Bruce M ^a,b,d,g  

^a UNIVERSITY OF DELAWARE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e CATX Biotechnology Inc   (United States)

^f RUSH UNIVERSITY   (United States)

^g HELEN F GRAHAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; AURORA B KINASE; CENTROMERE PROTEIN A; HISTONE H3; KI 67 ANTIGEN; SURVIVIN;

ARTICLE; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; CRYPT CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE CONTROL; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

EID: 78650206080     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100047     Document Type: Article

References (35)

1. Zhang T, Otevrel T, Gao Z, Ehrlich SM, Fields JZ, Boman BM: Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 2001, 61:8664-8667 (Pubitemid 34013874)
2. Boman B, Kopelovich L, Siracusa LD, Zhang T, Henderson K, Cofer Z, Buchberg AM, Fields JZ, Otevrel T: A GFP-Tcf4 reporter mouse model for monitoring effects of Apc mutations during intestinal tumorigenesis. Mol Carcinog 2009, 48:821-831
3. Boman B, Walters R, Fields JZ, Kovatich AJ, Zhang T, Isenberg GA, Goldstein SD, Palazzo JP: Colonic crypt changes during adenoma development in familial adenomatous polyposis: immunohistochemical evidence for expansion of the crypt base cell population. Am J Pathol 2004, 165:1489-1498
4. Chen J, Jin S, Tahir SK, Zhang H, Liu X, Sarthy AV, McGonigal TP, Liu Z, Rosenberg SH, Ng SC: Survivin enhances Aurora-B kinase activity and localizes Aurora-B in human cells. J Biol Chem 2003, 278:486-490
5. Bolton MA, Lan W, Powers SE, McCleland ML, Kuang J, Stukenberg PT: 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 2002, 13:3064-3077
6. Katayama H, Ota T, Jisaki F, Ueda Y, Tanaka T, Odashima S, Suzuki F, Terada Y, Tatsuka M: Mitotic kinase expression and colorectal cancer progression. J Natl Cancer Inst 1999, 91:1160-1162
7. Tatsuka M, Katayama H, Ota T, Tanaka T, Odashima S, Suzuki F, Terada Y: Multinuclearity and increased ploidy caused by overexpression of the aurora- and Ipl1-like midbody-associated protein mitotic kinase in human cancer cells. Cancer Res 1998, 58:4811-4816 (Pubitemid 28503674)
8. Adams RR, Eckley DM, Vagnarelli P, Wheatley SP, Gerloff DL, Mackay AM, Svingen PA, Kaufmann SH, Earnshaw WC: Human INCENP colocalizes with the Aurora-B/AIRK2 kinase on chromosomes and is overexpressed in tumour cells. Chromosoma 2001, 110:65-74
9. Ota T, Suto S, Katayama H, Han ZB, Suzuki F, Maeda M, Tanino M, Terada Y, Tatsuka M: Increased mitotic phosphorylation of histone H3 attributable to AIM-1/Aurora-B overexpression contributes to chromosome number instability. Cancer Res 2002, 62:5168-5177
10. Boman BM, Zhang T, Fields JZ: Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. (letter to the editor) Cancer Res 2004, 64:776-779
11. Smith KJ, Johnson KA, Bryan TM, Hill DE, Markowitz S, Willson JK, Paraskeva C, Petersen GM, Hamilton SR, Vogelstein B: The APC gene product in normal and tumor cells. Proc Natl Acad Sci USA 1993, 90:2846-2850
12. Kim PJ, Plescia J, Clevers H, Fearon ER, Altieri DC: Survivin and molecular pathogenesis of colorectal cancer. Lancet 2003, 362:205-209
13. Ma H, Nguyen C, Lee KS, Kahn M: Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene 2005, 24:3619-3631 (Pubitemid 40756231)
14. Boman BM, Fields JZ, Bonham-Carter O, Runquist OA: Computer modeling implicates stem cell overproduction in colon cancer initiation. Cancer Res 2001, 61:8408-8411
15. Boman BM, Wicha MS, Fields JZ, Runquist OA: Symmetric division of cancer stem cells-a key mechanism in tumor growth that should be targeted in future therapeutic approaches. Clin Pharmacol Ther 2007, 81:893-898
16. Boman BM, Fields JZ, Cavanaugh KL, Gujetter A, Runquist OA: How dysregulated colonic crypt dynamics cause stem cell overpopulation and initiate colon cancer. Cancer Res 2008, 6:3304-3313
17. Deschner E, Lewis CM, Lipkin M: In vitro study of human rectal epithelial cells. I atypical zone of H3 thymidine incorporation in mucosa of multiple polyposis. J Clin Invest 1963, 42:1922-1928
18. Lightdale C, Lipkin M, Deschner E: In vivo measurements in familial polyposis: kinetics and location of proliferating cells in colonic adenomas. Cancer Res 1982, 42:4280-4283
19. Potten CS: Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci 1998, 353:821-830
20. Potten CS, Kellett M, Rew DA, Roberts SA: Proliferation in human gastrointestinal epithelium using bromodeoxyuridine in vivo: data for different sites, proximity to a tumour, and polyposis coli. Gut 1992, 33:524-529
21. Wildrick DM, Lointier P, Nichols DH, Roll R, Quintanilla B, Boman BM: Isolation of normal human colonic mucosa: comparison of methods. In Vitro Cell Dev Biol Anim 1997, 33:18-27
22. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha M, Boman BM: ALDH1 is a marker for normal and malignant human colonic stem cells and tracks stem cell overpopulation during colon tumorigenesis. Cancer Res 2009, 69:3382-3389
23. Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP: Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 2003, 116:2987-2998
24. Zeitlin SG, Shelby RD, Sullivan KF: CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J Cell Biol 2001, 155:1147-1157
25. Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD: Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 1999, 97:99-109
26. Adams RR, Maiato H, Earnshaw WC, Carmena M: Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J Cell Biol 2001, 153:865-880
27. Wheatley SP, Carvalho A, Vagnarelli P, Earnshaw WC: INCENP is required for proper targeting of Survivin to the centromeres and the anaphase spindle during mitosis. Curr Biol 2001, 11:886-890
28. Romano A, Guse A, Krascenicova I, Schnabel H, Schnabel R, Glotzer M: CSC-1: a subunit of the Aurora B kinase complex that binds to the survivin-like protein BIR-1 and the incenp-like protein ICP-1. J Cell Biol 2003, 161:229-236
29. Juan G, Traganos F, James WM, Ray JM, Roberge M, Sauve DM, Anderson H, Darzynkiewicz Z: Histone H3 phosphorylation and expression of cyclins A and B1 measured in individual cells during their progression through G2 and mitosis. Cytometry 1998, 32:71-77 (Pubitemid 28246753)
30. Crosio C, Heitz E, Allis CD, Borrelli E, Sassone-Corsi P: Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J Cell Sci 2003, 116:4905-4914
31. Leverson JD, Huang HK, Forsburg SL, Hunter T: The Schizosaccharomyces pombe aurora-related kinase Ark1 interacts with the inner centromere protein Pic1 and mediates chromosome segregation and cytokinesis. Mol Biol Cell 2002, 13:1132-1143
32. Girdler F, Gascoigne KE, Eyers PA, Hartmuth S, Crafter C, Foote KM, Keen NJ, Taylor SS: Validating Aurora B as an anti-cancer drug target. J Cell Sci 2006, 119:3664-3675
33. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS: Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol, 2003, 161:267-280
34. Morin PJ, Vogelstein B, Kinzler KW: Apoptosis and APC in colorectal tumorigenesis. Proc Natl Acad Sci USA 1996, 93:7950-7954
35. Takahashi T, Futamura M, Yoshimi N, Sano J, Katada M, Takagi Y, Kimura M, Yoshioka T, Okano Y, Saji S: Centrosomal kinases. HsAIRK1 and HsAIRK3, are overexpressed in primary colorectal cancers. Jpn J Cancer Res 2000, 91:1007-1014