Critical Role of a Survivin/TGF-β/mTORC1 Axis in IGF-I-Mediated Growth of Prostate Epithelial Cells

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Song, Kyung ^a,c   Shankar, Eswar ^a   Yang, Jiayi ^b,d   Bane, Kara L ^a   Wahdan Alaswad, Reema ^b,e   Danielpour, David ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Wonkwang University   (South Korea)

^d Eddingpharm   (United States)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; CELL PROTEIN; DOXYCYCLINE; KU 0063794; LUCIFERASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN RAPTOR; PROTEIN RICTOR; SHORT HAIRPIN RNA; SMAD2 PROTEIN; SMAD3 PROTEIN; SOMATOMEDIN C; SURVIVIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CDE GENE; CELL GROWTH; CELL STIMULATION; CELLULAR DISTRIBUTION; CHR GENE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG TARGETING; GENE; GENE ACTIVATION; GENE CONSTRUCT; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MTOR GENE; PROMOTER REGION; PROSTATE CANCER; PROSTATE EPITHELIUM; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAPTOR GENE; REPRESSOR GENE; RICTOR GENE; SIGNAL TRANSDUCTION; SURVIVIN GENE; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; AUTOCRINE COMMUNICATION; CELL PROLIFERATION; EPITHELIAL CELLS; HEK293 CELLS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MALE; MAP KINASE SIGNALING SYSTEM; MICROTUBULE-ASSOCIATED PROTEINS; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; PROSTATE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RETINOBLASTOMA PROTEIN; SMAD PROTEINS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA1;

RATTUS;

EID: 84877064816     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061896     Document Type: Article

References (64)

1. Liston P, Fong WG, Korneluk RG, (2003) The inhibitors of apoptosis: there is more to life than Bcl2. Oncogene 22: 8568-8580.
2. Salvesen GS, Duckett CS, (2002) IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 3: 401-410.
3. Altieri DC (2012) Targeting survivin in cancer. Cancer Lett.
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.
5. 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.
6. Altieri DC, (2003) Validating survivin as a cancer therapeutic target. Nat Rev Cancer 3: 46-54.
7. Jeyaprakash AA, Klein UR, Lindner D, Ebert J, Nigg EA, et al. (2007) Structure of a Survivin-Borealin-INCENP core complex reveals how chromosomal passengers travel together. Cell 131: 271-285.
8. Rosa J, Canovas P, Islam A, Altieri DC, Doxsey SJ, (2006) Survivin modulates microtubule dynamics and nucleation throughout the cell cycle. Mol Biol Cell 17: 1483-1493.
9. Altieri DC, (2003) Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 22: 8581-8589.
10. Shariat SF, Lotan Y, Saboorian H, Khoddami SM, Roehrborn CG, et al. (2004) Survivin expression is associated with features of biologically aggressive prostate carcinoma. Cancer 100: 751-757.
11. Sohn DM, Kim SY, Baek MJ, Lim CW, Lee MH, et al. (2006) Expression of survivin and clinical correlation in patients with breast cancer. Biomed Pharmacother 60: 289-292.
12. Vischioni B, van der Valk P, Span SW, Kruyt FA, Rodriguez JA, et al. (2004) Nuclear localization of survivin is a positive prognostic factor for survival in advanced non-small-cell lung cancer. Ann Oncol 15: 1654-1660.
13. Wang J, Yang L, Yang J, Kuropatwinski K, Wang W, et al. (2008) Transforming growth factor beta induces apoptosis through repressing the phosphoinositide 3-kinase/AKT/survivin pathway in colon cancer cells. Cancer Res 68: 3152-3160.
14. Khan S, Jutzy JM, Valenzuela MM, Turay D, Aspe JR, et al. (2012) Plasma-derived exosomal survivin, a plausible biomarker for early detection of prostate cancer. PLoS One 7: e46737.
15. Tang L, Ling X, Liu W, Das GM, Li F, (2012) Transcriptional inhibition of p21(WAF1/CIP1) gene (CDKN1) expression by survivin is at least partially p53-dependent: Evidence for survivin acting as a transcription factor or co-factor. Biochem Biophys Res Commun 421: 249-254.
16. Riolo MT, Cooper ZA, Holloway MP, Cheng Y, Bianchi C, et al. (2012) HDAC6 deacetylates survivin for its nuclear export in breast cancer. J Biol Chem.
17. Vaira V, Lee CW, Goel HL, Bosari S, Languino LR, et al. (2007) Regulation of survivin expression by IGF-1/mTOR signaling. Oncogene 26: 2678-2684.
18. Baserga R, Resnicoff M, Dews M, (1997) The IGF-I receptor and cancer. Endocrine 7: 99-102.
19. Danielpour D, Song K, (2006) Cross-talk between IGF-I and TGF-beta signaling pathways. Cytokine Growth Factor Rev 17: 59-74.
20. Pollak M, (2008) Targeting insulin and insulin-like growth factor signalling in oncology. Curr Opin Pharmacol 8: 384-392.
21. Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, et al. (1998) Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 279: 563-566.
22. DiGiovanni J, Kiguchi K, Frijhoff A, Wilker E, Bol DK, et al. (2000) Deregulated expression of insulin-like growth factor 1 in prostate epithelium leads to neoplasia in transgenic mice. Proc Natl Acad Sci U S A 97: 3455-3460.
23. Plymate SR, Haugk K, Coleman I, Woodke L, Vessella R, et al. (2007) An antibody targeting the type I insulin-like growth factor receptor enhances the castration-induced response in androgen-dependent prostate cancer. Clin Cancer Res 13: 6429-6439.
24. Yang J, Song K, Krebs TL, Jackson MW, Danielpour D, (2008) Rb/E2F4 and Smad2/3 link survivin to TGF-beta-induced apoptosis and tumor progression. Oncogene 27: 5326-5338.
25. Shi Y, Massague J, (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
26. Roberts AB, Wakefield LM, (2003) The two faces of transforming growth factor beta in carcinogenesis. Proc Natl Acad Sci U S A 100: 8621-8623.
27. ten Dijke P, Hill CS, (2004) New insights into TGF-beta-Smad signalling. Trends Biochem Sci 29: 265-273.
28. Massague J, Seoane J, Wotton D, (2005) Smad transcription factors. Genes Dev 19: 2783-2810.
29. Tang B, de Castro K, Barnes HE, Parks WT, Stewart L, et al. (1999) Loss of responsiveness to transforming growth factor beta induces malignant transformation of nontumorigenic rat prostate epithelial cells. Cancer Res 59: 4834-4842.
30. Song K, Cornelius SC, Danielpour D, (2003) Development and characterization of DP-153, a nontumorigenic prostatic cell line that undergoes malignant transformation by expression of dominant-negative transforming growth factor beta receptor type II. Cancer Res 63: 4358-4367.
31. Yang J, Wahdan-Alaswad R, Danielpour D, (2009) Critical role of Smad2 in tumor suppression and transforming growth factor-beta-induced apoptosis of prostate epithelial cells. Cancer Res 69: 2185-2190.
32. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, et al. (2004) TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303: 848-851.
33. Pu H, Collazo J, Jones E, Gayheart D, Sakamoto S, et al. (2009) Dysfunctional transforming growth factor-beta receptor II accelerates prostate tumorigenesis in the TRAMP mouse model. Cancer Res 69: 7366-7374.
34. Ding Z, Wu CJ, Chu GC, Xiao Y, Ho D, et al. (2011) SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 470: 269-273.
35. Hsing AY, Kadomatsu K, Bonham MJ, Danielpour D, (1996) Regulation of apoptosis induced by transforming growth factor-beta1 in nontumorigenic rat prostatic epithelial cell lines. Cancer Res 56: 5146-5149.
36. Lucibello FC, Liu N, Zwicker J, Gross C, Muller R, (1997) The differential binding of E2F and CDF repressor complexes contributes to the timing of cell cycle-regulated transcription. Nucleic Acids Res 25: 4921-4925.
37. Wahdan-Alaswad RS, Song K, Krebs TL, Shola DT, Gomez JA, et al. (2010) Insulin-like growth factor I suppresses bone morphogenetic protein signaling in prostate cancer cells by activating mTOR signaling. Cancer Res 70: 9106-9117.
38. Danielpour D, Kadomatsu K, Anzano MA, Smith JM, Sporn MB, (1994) Development and characterization of nontumorigenic and tumorigenic epithelial cell lines from rat dorsal-lateral prostate. Cancer Res 54: 3413-3421.
39. Bonham MJ, Danielpour D, (1996) Improved purification and yields of RNA by RNeasy. Biotechniques 21: 57-60.
40. Song K, Wang H, Krebs TL, Danielpour D, (2006) Novel roles of Akt and mTOR in suppressing TGF-beta/ALK5-mediated Smad3 activation. EMBO J 25: 58-69.
41. Song K, Wang H, Krebs TL, Kim SJ, Danielpour D, (2008) Androgenic control of transforming growth factor-beta signaling in prostate epithelial cells through transcriptional suppression of transforming growth factor-beta receptor II. Cancer Res 68: 8173-8182.
42. Song K, Krebs TL, Danielpour D, (2006) Novel permissive role of epidermal growth factor in transforming growth factor beta (TGF-beta) signaling and growth suppression. Mediation by stabilization of TGF-beta receptor type II. J Biol Chem 281: 7765-7774.
43. Chipuk JE, Cornelius SC, Pultz NJ, Jorgensen JS, Bonham MJ, et al. (2002) The androgen receptor represses transforming growth factor-beta signaling through interaction with Smad3. J Biol Chem 277: 1240-1248.
44. Stewart LV, Song K, Hsing AY, Danielpour D, (2003) Regulation of trespin expression by modulators of cell growth, differentiation, and apoptosis in prostatic epithelial cells. Exp Cell Res 284: 303-315.
45. Song K, Cornelius SC, Reiss M, Danielpour D, (2003) Insulin-like growth factor-I inhibits transcriptional responses of transforming growth factor-beta by phosphatidylinositol 3-kinase/Akt-dependent suppression of the activation of Smad3 but not Smad2. J Biol Chem 278: 38342-38351.
46. Nastiuk KL, Yoo K, Lo K, Su K, Yeung P, et al. (2008) FLICE-like inhibitory protein blocks transforming growth factor beta 1-induced caspase activation and apoptosis in prostate epithelial cells. Mol Cancer Res 6: 231-242.
47. Jiang Y, Saavedra HI, Holloway MP, Leone G, Altura RA, (2004) Aberrant regulation of survivin by the RB/E2F family of proteins. J Biol Chem 279: 40511-40520.
48. Gellibert F, Woolven J, Fouchet MH, Mathews N, Goodland H, et al. (2004) Identification of 1,5-naphthyridine derivatives as a novel series of potent and selective TGF-beta type I receptor inhibitors. J Med Chem 47: 4494-4506.
49. Megyesi K, Kahn CR, Roth J, Neville DM Jr, Nissley SP, et al. (1975) The NSILA-s receptor in liver plasma membranes. Characterization and comparison with the insulin receptor. J Biol Chem 250: 8990-8996.
50. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM, (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101.
51. Danielpour D, (1999) Transdifferentiation of NRP-152 rat prostatic basal epithelial cells toward a luminal phenotype: regulation by glucocorticoid, insulin-like growth factor-I and transforming growth factor-beta. J Cell Sci 112 (Pt 2): 169-179.
52. Hayward SW, Haughney PC, Lopes ES, Danielpour D, Cunha GR, (1999) The rat prostatic epithelial cell line NRP-152 can differentiate in vivo in response to its stromal environment. Prostate 39: 205-212.
53. Altieri DC, (2010) Survivin and IAP proteins in cell-death mechanisms. Biochem J 430: 199-205.
54. Chowdhury S, Howell GM, Rajput A, Teggart CA, Brattain LE, et al. (2011) Identification of a novel TGFbeta/PKA signaling transduceome in mediating control of cell survival and metastasis in colon cancer. PLoS One 6: e19335.
55. Dan HC, Sun M, Kaneko S, Feldman RI, Nicosia SV, et al. (2004) Akt phosphorylation and stabilization of X-linked inhibitor of apoptosis protein (XIAP). J Biol Chem 279: 5405-5412.
56. Kurimchak A, Grana X, (2012) PP2A holoenzymes negatively and positively regulate cell cycle progression by dephosphorylating pocket proteins and multiple CDK substrates. Gene 499: 1-7.
57. Davies MA, Koul D, Dhesi H, Berman R, McDonnell TJ, et al. (1999) Regulation of Akt/PKB activity, cellular growth, and apoptosis in prostate carcinoma cells by MMAC/PTEN. Cancer Res 59: 2551-2556.
58. McMenamin ME, Soung P, Perera S, Kaplan I, Loda M, et al. (1999) Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res 59: 4291-4296.
59. Chan JM, Stampfer MJ, Giovannucci E, Ma J, Pollak M (2000) Insulin-like growth factor I (IGF-I), IGF-binding protein-3 and prostate cancer risk: epidemiological studies. Growth Horm IGF Res 10 Suppl A: S32-33.
60. Nickerson T, Chang F, Lorimer D, Smeekens SP, Sawyers CL, et al. (2001) In vivo progression of LAPC-9 and LNCaP prostate cancer models to androgen independence is associated with increased expression of insulin-like growth factor I (IGF-I) and IGF-I receptor (IGF-IR). Cancer Res 61: 6276-6280.
61. Guha M, Plescia J, Leav I, Li J, Languino LR, et al. (2009) Endogenous tumor suppression mediated by PTEN involves survivin gene silencing. Cancer Res 69: 4954-4958.
62. Burgering BM, Medema RH, (2003) Decisions on life and death: FOXO Forkhead transcription factors are in command when PKB/Akt is off duty. J Leukoc Biol 73: 689-701.
63. Wahdan-Alaswad RS, Bane KL, Song K, Shola DT, Garcia JA, et al. (2012) Inhibition of mTORC1 kinase activates Smads 1 and 5 but not Smad8 in human prostate cancer cells, mediating cytostatic response to rapamycin. Mol Cancer Res 10: 821-833.
64. Song K, Wang H, Krebs TL, Wang B, Kelley TJ, et al. (2010) DHT selectively reverses Smad3-mediated/TGF-beta-induced responses through transcriptional down-regulation of Smad3 in prostate epithelial cells. Mol Endocrinol 24: 2019-2029.