BAD Dephosphorylation and Decreased Expression of MCL-1 Induce Rapid Apoptosis in Prostate Cancer Cells

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Yancey, Dana ^a   Nelson, Kyle C ^a   Baiz, Daniele ^a   Hassan, Sazzad ^a   Flores, Anabel ^a   Pullikuth, Ashok ^a   Karpova, Yelena ^a   Axanova, Linara ^a   Moore, Victoria ^b   Sui, Guangchao ^a   Kulik, George ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b ELON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 DIFLUOROMETHYLBENZIMIDAZOL 1 YL) 4,6 DIMORPHOLINO 1,3,5 TRIAZINE; CYCLOHEXIMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN MCL 1;

APOPTOSIS; ARTICLE; CANCER CELL; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; DRUG TARGETING; PROSTATE CANCER; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; CELL LINE, TUMOR; CULTURE MEDIA, SERUM-FREE; CYCLOHEXIMIDE; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN SYNTHESIS INHIBITORS; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; TRIAZINES;

EID: 84883546687     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074561     Document Type: Article

References (58)

1. Vivanco I, Sawyers CL, (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501.
2. Murillo H, Huang H, Schmidt LJ, Smith DI, Tindall DJ, (2001) Role of PI3K signaling in survival and progression of LNCaP prostate cancer cells to the androgen refractory state. Endocrinology 142: 4795-4805.
3. Gao N, Zhang Z, Jiang BH, Shi X, (2003) Role of PI3K/AKT/mTOR signaling in the cell cycle progression of human prostate cancer. Biochem Biophys Res Commun 310: 1124-1132.
4. Bayascas JR, Alessi DR, (2005) Regulation of Akt/PKB Ser473 phosphorylation. Mol Cell 18: 143-145.
5. Brazil DP, Yang ZZ, Hemmings BA, (2004) Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 29: 233-242.
6. Whang YE, Wu X, Suzuki H, Reiter RE, Tran C, et al. (1998) Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci U S A 95: 5246-5250.
7. Deocampo ND, Huang H, Tindall DJ, (2003) The role of PTEN in the progression and survival of prostate cancer. Minerva Endocrinol 28: 145-153.
8. Isaacs JT, Lundmo PI, Berges R, Martikainen P, Kyprianou N, et al. (1992) Androgen regulation of programmed death of normal and malignant prostatic cells. J Androl 13: 457-464.
9. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP, (1998) Pten is essential for embryonic development and tumour suppression. Nat Genet 19: 348-355.
10. 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.
11. Green DR, Kroemer G, (2004) The pathophysiology of mitochondrial cell death. Science 305: 626-629.
12. Kuwana T, Newmeyer DD, (2003) Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15: 691-699.
13. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, et al. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
14. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, et al. (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80: 285-291.
15. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, et al. (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17: 393-403.
16. Ren D, Tu HC, Kim H, Wang GX, Bean GR, et al. (2010) BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 330: 1390-1393.
17. Holmgreen SP, Huang DC, Adams JM, Cory S, (1999) Survival activity of Bcl-2 homologs Bcl-w and A1 only partially correlates with their ability to bind pro-apoptotic family members. Cell Death Differ 6: 525-532.
18. Dutta S, Gulla S, Chen TS, Fire E, Grant RA, et al. (2010) Determinants of BH3 binding specificity for Mcl-1 versus Bcl-xL. J Mol Biol 398: 747-762.
19. Smith AJ, Karpova Y, D'Agostino R Jr, Willingham M, Kulik G, (2009) Expression of the Bcl-2 protein BAD promotes prostate cancer growth. PLoS One 4: e6224.
20. Sastry KS, Smith AJ, Karpova Y, Datta SR, Kulik G, (2006) Diverse antiapoptotic signaling pathways activated by vasoactive intestinal polypeptide, epidermal growth factor, and phosphatidylinositol 3-kinase in prostate cancer cells converge on BAD. J Biol Chem 281: 20891-20901.
21. Fang X, Yu S, Eder A, Mao M, Bast RC, et al. (1999) Regulation of BAD phosphorylation at serine 112 by the Ras-mitogen-activated protein kinase pathway. Oncogene 18: 6635-6640.
22. Datta SR, Katsov A, Hu L, Petros A, Fesik SW, et al. (2000) 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol Cell 6: 41-51.
23. Tan Y, Demeter MR, Ruan H, Comb MJ, (2000) BAD Ser-155 phosphorylation regulates BAD/Bcl-XL interaction and cell survival. J Biol Chem 275: 25865-25869.
24. 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.
25. Datta SR, Dudek H, Tao X, Masters S, Fu H, et al. (1997) Akt phosphorylation of BAD couples survival signals to the cell- intrinsic death machinery. Cell 91: 231-241.
26. She QB, Solit DB, Ye Q, O'Reilly KE, et al. (2005) The BAD protein integrates survival signaling by EGFR/MAPK and PI3K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer Cell 8: 287-297.
27. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR, (2006) Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21: 749-760.
28. Krajewska M, Krajewski S, Epstein JI, Shabaik A, Sauvageot J, et al. (1996) Immunohistochemical analysis of bcl-2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol 148: 1567-1576.
29. Kim MH, Minton AZ, Agrawal V, (2009) C/EBPbeta regulates metastatic gene expression and confers TNF-alpha resistance to prostate cancer cells. Prostate 69: 1435-1447.
30. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, et al. (2008) BAX activation is initiated at a novel interaction site. Nature 455: 1076-1081.
31. Czabotar PE, Lee EF, van Delft MF, Day CL, Smith BJ, et al. (2007) Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci U S A 104: 6217-6222.
32. Song G, Ouyang G, Bao S, (2005) The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9: 59-71.
33. Castilla C, Congregado B, Chinchon D, Torrubia FJ, Japon MA, et al. (2006) Bcl-xL is overexpressed in hormone-resistant prostate cancer and promotes survival of LNCaP cells via interaction with proapoptotic Bak. Endocrinology 147: 4960-4967.
34. Tang DG, Li L, Chopra DP, Porter AT, (1998) Extended survivability of prostate cancer cells in the absence of trophic factors: increased proliferation, evasion of apoptosis, and the role of apoptosis proteins [published erratum appears in Cancer Res 1998 Nov 15;58(22):5260]. Cancer Res 58: 3466-3479.
35. Wei G, Margolin AA, Haery L, Brown E, Cucolo L, et al. (2012) Chemical genomics identifies small-molecule MCL1 repressors and BCL-xL as a predictor of MCL1 dependency. Cancer Cell 21: 547-562.
36. Osaki M, Oshimura M, Ito H, (2004) PI3K-Akt pathway: its functions and alterations in human cancer. Apoptosis 9: 667-676.
37. Pourmand G, Ziaee AA, Abedi AR, Mehrsai A, Alavi HA, et al. (2007) Role of PTEN gene in progression of prostate cancer. Urol J 4: 95-100.
38. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, et al. (2010) Integrative genomic profiling of human prostate cancer. Cancer Cell 18: 11-22.
39. Suzuki H, Freije D, Nusskern DR, Okami K, Cairns P, et al. (1998) Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res 58: 204-209.
40. Yoshimoto M, Cunha IW, Coudry RA, Fonseca FP, Torres CH, et al. (2007) FISH analysis of 107 prostate cancers shows that PTEN genomic deletion is associated with poor clinical outcome. Br J Cancer 97: 678-685.
41. Ayala G, Thompson T, Yang G, Frolov A, Li R, et al. (2004) High levels of phosphorylated form of Akt-1 in prostate cancer and non-neoplastic prostate tissues are strong predictors of biochemical recurrence. Clin Cancer Res 10: 6572-6578.
42. Zenyaku Kogyo Co., Ltd. (2012) A Phase 1b, Multi-Center, Open Label, Uncontrolled, Serial Cohort, Dose Escalation Study of the Safety, Tolerability, Pharmacokinetics and Preliminary Efficacy of Daily Oral Doses of ZSTK474 in Subjects With Advanced Solid Malignancies. Available: ClinicalTrials.gov. Dana Farber Cancer Institute. Accessed 2012 Sep 15.
43. Duke University (2012), BKM120 in Metastatic Castration-resistant Prostate Cancer. Available: ClinicalTrials.gov. Novartis Pharmaceuticals. Accessed 2012 Sep 15.
44. Sarah Cannon Research Institute. (2012). Study of PI3 Kinase/mTOR Inhibitor BEZ235 Twice Daily for Advanced Solid Tumors. Available: ClinicalTrials.gov. Novartis. Accessed 2012 Sep 15.
45. Bendell JC, Rodon J, Burris HA, de Jonge M, Verweij J, et al. (2012) Phase I, dose-escalation study of BKM120, an oral pan-Class I PI3K inhibitor, in patients with advanced solid tumors. J Clin Oncol 30: 282-290.
46. Shuttleworth SJ, Silva FA, Cecil AR, Tomassi CD, Hill TJ, et al. (2011) Progress in the preclinical discovery and clinical development of class I and dual class I/IV phosphoinositide 3-kinase (PI3K) inhibitors. Curr Med Chem 18: 2686-2714.
47. Ding Q, He X, Hsu JM, Xia W, Chen CT, et al. (2007) Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 27: 4006-4017.
48. Kitada S, Andersen J, Akar S, Zapata JM, Takayama S, et al. (1998) Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with In vitro and In vivo chemoresponses. Blood 91: 3379-3389.
49. Akgul C, Moulding DA, White MR, Edwards SW, (2000) In vivo localisation and stability of human Mcl-1 using green fluorescent protein (GFP) fusion proteins. FEBS Lett 478: 72-76.
50. Mott JL, Kobayashi S, Bronk SF, Gores GJ, (2007) mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26: 6133-6140.
51. Zhong Q, Gao W, Du F, Wang X, (2005) Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121: 1085-1095.
52. Cavarretta IT, Neuwirt H, Untergasser G, Moser PL, Zaki MH, et al. (2007) The antiapoptotic effect of IL-6 autocrine loop in a cellular model of advanced prostate cancer is mediated by Mcl-1. Oncogene 26: 2822-2832.
53. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR, (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant [see comments]. Nat Cell Biol 2: 156-162.
54. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, et al. (2011) A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 44: 517-531.
55. Wu HC, Hsieh JT, Gleave ME, Brown NM, Pathak S, et al. (1994) Derivation of androgen-independent human LNCaP prostatic cancer cell sublines: role of bone stromal cells. Int J Cancer 57: 406-412.
56. Axanova LS, Chen YQ, McCoy T, Sui G, Cramer SD, (2010) 1,25-dihydroxyvitamin D(3) and PI3K/AKT inhibitors synergistically inhibit growth and induce senescence in prostate cancer cells. Prostate 70: 1658-1671.
57. Sui G, Shi Y, (2005) Gene silencing by a DNA vector-based RNAi technology. Methods Mol Biol 309: 205-218.
58. Kulik G, Klippel A, Weber MJ, (1997) Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol Cell Biol 17: 1595-1606.