Loss of Survivin in the Prostate Epithelium Impedes Carcinogenesis in a Mouse Model of Prostate Adenocarcinoma

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Adisetiyo, Helty ^a   Liang, Mengmeng ^b   Liao, Chun Peng ^b   Aycock Williams, Ari ^b   Cohen, Michael B ^c   Xu, Shili ^a   Neamati, Nouri ^a   Conway, Edward M ^d   Cheng, Chieh Yang ^e   Nikitin, Alexander Yu ^e   Roy Burman, Pradip ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SURVIVIN; X LINKED INHIBITOR OF APOPTOSIS;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GRADING; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DISEASE SEVERITY; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOSS; HETEROZYGOTE; HISTOPATHOLOGY; HOMOZYGOTE; MALE; MOUSE; NONHUMAN; PROSTATE ADENOCARCINOMA; PROSTATE EPITHELIUM; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN DEPLETION; PROTEIN EXPRESSION; SENESCENCE; SURVIVIN GENE;

ADENOCARCINOMA; ANIMALS; CARCINOGENESIS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EPITHELIUM; FEMALE; HISTONES; HUMANS; IMMUNOHISTOCHEMISTRY; INHIBITOR OF APOPTOSIS PROTEINS; MALE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; MICE, TRANSGENIC; PROSTATE; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE; REPRESSOR PROTEINS;

EID: 84881134854     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069484     Document Type: Article

References (43)

1. Altieri DC, (2008) Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 8: 61-70. doi:10.1038/nrc2293. PubMed: 18075512.
2. Altieri DC, (2006) The case for survivin as a regulator of microtubule dynamics and cell-death decisions. Curr Opin Cell Biol 18: 609-615. doi:10.1016/j.ceb.2006.08.015. PubMed: 16934447.
3. Srinivasula SM, Ashwell JD, (2008) IAPs: what's in a name? Mol Cell 30: 123-135. doi:10.1016/j.molcel.2008.03.008. PubMed: 18439892.
4. 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. doi:10.1074/jbc.C400236200. PubMed: 15218035.
5. Aoki Y, Feldman GM, Tosato G, (2003) Inhibition of STAT3 signaling induces apoptosis and decreases survivin expression in primary effusion lymphoma. Blood 101: 1535-1542. doi:10.1182/blood-2002-07-2130. PubMed: 12393476.
6. Roca H, Varsos ZS, Mizutani K, Pienta KJ, (2008) CCL2, survivin and autophagy: new links with implications in human cancer. Autophagy 4: 969-971. PubMed: 18758234.
7. Khan S, Aspe JR, Asumen MG, Almaguel F, Odumosu O, et al. (2009) Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential. Br J Cancer. 100: 1073-1086. doi:10.1038/sj.bjc.6604978. PubMed: 19293795.
8. Kobayashi K, Hatano M, Otaki M, Ogasawara T, Tokuhisa T, (1999) Expression of a murine homologue of the inhibitor of apoptosis protein is related to cell proliferation. Proc Natl Acad Sci U S A 96: 1457-1462. doi:10.1073/pnas.96.4.1457. PubMed: 9990045.
9. Carrasco RA, Stamm NB, Marcusson E, Sandusky G, Iversen P, et al. (2011) Antisense inhibition of survivin expression as a cancer theurapeutic. Mol Cancer Ther 10: 221-232. doi:10.1158/1535-7163.TARG-11-A221. PubMed: 21216939.
10. Stauber RH, Mann W, Knauer SK, (2007) Nuclear and cytoplasmic survivin: Molecular mechanism, prognostic, and therapeutic potential. Cancer Res 67: 5999-6002. doi:10.1158/0008-5472.CAN-07-0494. PubMed: 17616652.
11. 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. doi:10.1016/S0960-9822(00)00769-7. PubMed: 11084331.
12. 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. doi:10.1084/jem.20032092. PubMed: 14757745.
13. Jiang Y, de Bruin A, Caldas H, Fangusaro J, Hayes J, et al. (2005) Essential role for survivin in early brain development. J Neurosci 25: 6962-6970. doi:10.1523/JNEUROSCI.1446-05.2005. PubMed: 16049172.
14. Zwerts F, Lupu F, De Vriese A, Pollefeyt S, Moons L, et al. (2007) Lack of endothelial cell survivin causes embryonic defects in angiogenesis, cardiogenesis, and neural tube closure. Blood 109: 4742-4752. PubMed: 17299096.
15. Leung CG, Xu Y, Mularski B, Liu H, Gurbuxani S, et al. (2007) Requirements for survivin in terminal differentiation of erythroid cells and maintenance of hematopoietic stem and progenitor cells. J Exp Med 204: 1603-1611. PubMed: 17576776.
16. Yang S, Lim M, Pham LK, Kendall SE, Reddi AH, et al. (2006) Bone Morphogenetic Protein 7 protects prostate cancer cells from stress-induced apoptosis via both Smad and c-Jun NH2-terminal kinase pathways. Cancer Res 66: 4285-4290. doi:10.1158/0008-5472.CAN-05-4456. PubMed: 16618753.
17. Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, et al. (2003) Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 4: 209-221. doi:10.1016/S1535-6108(03)00215-0. PubMed: 14522255.
18. Trotman LC, Niki M, Dotan ZA, Koutcher JA, Di Cristofano A, et al. (2003) Pten dose dictates cancer progression in the prostate. PLOS Biol 1: 385-396. PubMed: 14691534.
19. Liao CP, Zhong C, Saribekyan G, Bading J, Park R, et al. (2007) Mouse models of prostate adenocarcinoma with the capacity to monitor spontaneous carcinogenesis by bioluminescence or fluorescence. Cancer Res 67: 7525-7533. doi:10.1158/0008-5472.CAN-07-0668. PubMed: 17671224.
20. Lim M, Zhong C, Yang S, Bell AM, Cohen MB, et al. (2010) Runx2 regulates survivin expression in prostate cancer cells. Lab Invest 90: 222-233. doi:10.1038/labinvest.2009.128. PubMed: 19949374.
21. Yang S, Zhong C, Frenkel B, Reddi AH, Roy-Burman P, (2005) Diverse biological effect and Smad signaling of bone morphogenetic protein 7 in prostate tumor cells. Cancer Res 65: 5769-5777. doi:10.1158/0008-5472.CAN-05-0289. PubMed: 15994952.
22. Xing Z, Conway EM, Kang C, Winoto A, (2003) Essential role of survivin, an inhibitor of apoptosis protein. T Cell Dev Maturation And Homeostasis J Exp Med 99: 69-80.
23. Wu X, Wu J, Huang J, Powell WC, Zhang J, et al. (2001) Generation of a prostate epithelial cell-specific Cre transgenic mouse model for tissue-specific gene ablation. Mech Dev 101: 61-69. doi:10.1016/S0925-4773(00)00551-7. PubMed: 11231059.
24. Zhou Z, Flesken-Nikitin A, Nikitin AY, (2007) Prostate cancer associated with p53 and Rb deficiency arises from the stem/progenitor cell-enriched proximal region of prostatic ducts. Cancer Res 67: 5683-5690. doi:10.1158/0008-5472.CAN-07-0768. PubMed: 17553900.
25. Zhou Z, Flesken-Nikitin A, Corney DC, Wang W, Goodrich DW, et al. (2006) Synergy of p53 and Rb deficiency in a conditional mouse model for metastatic prostate cancer. Cancer Res 66: 7889-7898. doi:10.1158/0008-5472.CAN-06-0486. PubMed: 16912162.
26. Bandyopadhyay D, Gatza C, Donehower LA, Medrano EE, (2005) Analysis of cellular senescence in culture in vivo: The senescence-associated β-galactosidase assay. Current Protoc Cell Biol 18.9: 1-18.9.9.
27. Zhang J, Thomas TZ, Kasper S, Matusik RJ, (2000) A small composite probasin promoter confers high levels of prostate-specific gene expression through regulation by androgens and glucocorticoids in vitro and in vivo. Endocrinology 141: 4698-4710. doi:10.1210/en.141.12.4698. PubMed: 11108285.
28. Park JH, Walls JE, Galvez JJ, Kim M, Abate-Shen C, et al. (2002) Prostatic intraepithelial neoplasia in genetically engineered mice. Am J Pathol 161: 725-735. PubMed: 12163397.
29. Couto SS, Cao M, Duarte PC, Banach-Petrosky W, Wang S, et al. (2009) Simultaneous haploinsufficiency of Pten and Trp53 tumor suppressor genes accelerates tumorigenesis in a mouse model of prostate cancer. Differentiation 77: 103-111. doi:10.1016/j.diff.2008.09.010. PubMed: 19281769.
30. Choi N, Zhang B, Zhang L, Ittmann M, Xin L, (2012) Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation. Cancer Cell 21: 253-265. doi:10.1016/j.ccr.2012.01.005. PubMed: 22340597.
31. Krajewska M, Krajewski S, Banares S, Huang X, Turner B, et al. (2003) Elevated expression of inhibitor of apoptosis proteins in prostate cancer. Clin Cancer Res 9: 4914-4925. PubMed: 14581366.
32. Dohi T, Xia F, Altieri DC, (2007) Compartmentalized phosphorylation of IAP by protein kinase A regulates cytoprotection. Mol Cell 27: 17-28. doi:10.1016/j.molcel.2007.06.004. PubMed: 17612487.
33. Cheung CH, Sun X, Kanwar JR, Bai JZ, Cheng L, et al. (2010) A cell-permeable dominant-negative survivin protein induces apoptosis and sensitizes prostate cancer cells to TNF-α therapy. Cancer Cell Int 10: 36. doi:10.1186/1475-2867-10-36. PubMed: 20920299.
34. Kanwar JR, Shen WP, Kanwar RK, Berg RW, Krissansen GW, (2001) Effects of survivin antagonists on growth of established tumors and B7-1 immunogene therapy. J Natl Cancer Inst 93: 1541-1552. doi:10.1093/jnci/93.20.1541. PubMed: 11604477.
35. Ambrosini G, Adida C, Sirugo G, Altieri DC, (1998) Induction of apoptosis and inhibition of cell proliferation by survivin gene targeting. J Biol Chem 273: 11177-11182. doi:10.1074/jbc.273.18.11177. PubMed: 9556606.
36. De Jesus BB, Blasco MA, (2012) Assessing cell and organ senescence biomarkers. Circ Res 111: 97-109. doi:10.1161/CIRCRESAHA.111.247866. PubMed: 22723221.
37. Mooi WJ, Peeper DS, (2006) Oncogene-induced cell senescence-halting on the road to cancer. N. Engl. J. Med. 355: 1037-1046. doi:10.1056/NEJMra062285. PubMed: 16957149.
38. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, et al. (2005) Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436: 725-730. doi:10.1038/nature03918. PubMed: 16079851.
39. Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, et al. (2005) Tumour biology: senescence in premalignant tumours. Nature 436: 642. doi:10.1038/436642a. PubMed: 16079833.
40. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444: 638-642. doi:10.1038/nature05327. PubMed: 17136094.
41. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, et al. (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444: 633-637. doi:10.1038/nature05268. PubMed: 17136093.
42. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434: 907-913. doi:10.1038/nature03485. PubMed: 15829965.
43. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM, (2000) Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275: 9390-9395. doi:10.1074/jbc.275.13.9390. PubMed: 10734083.