PKA knockdown enhances cell killing in response to radiation and androgen deprivation

International Journal of Cancer

Volumn 128, Issue 4, 2011, Pages 962-973

  Hensley, Harvey H ^a   Hannoun Levi, Jean Michel ^b   Hachem, Paul ^c   Mu, Zhaomei ^a   Stoyanova, Radka ^c   Khor, Li Yan ^a   Agrawal, Sudhir ^d   Pollack, Alan ^c  

^a FOX CHASE CANCER CENTER   (United States)

^b CENTRE ANTOINE LACASSAGNE   (France)

^c UNIVERSITY OF MIAMI   (United States)

^d HYBRIDON INC   (United States)

Author keywords

androgen deprivation; antisense; prostate cancer; protein kinase A; radiation

Indexed keywords

CASPASE 3; CASPASE 7; CYCLIC AMP DEPENDENT PROTEIN KINASE; GENE EXPRESSION MODULATOR 231; MITOGEN ACTIVATED PROTEIN KINASE;

ANDROGEN DEPRIVATION THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER RADIOTHERAPY; CELL SURVIVAL; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DRUG EFFICACY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ORCHIECTOMY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN PHOSPHORYLATION; TUMOR VOLUME; TUMOR XENOGRAFT;

ANDROGEN ANTAGONISTS; ANDROGENS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GAMMA RAYS; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MICE; MICE, NUDE; OLIGONUCLEOTIDES, ANTISENSE; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 78650621031     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25634     Document Type: Article

References (50)

1. Pilepich MV, Winter K, John MJ, Mesic JB, Sause W, Rubin P, Lawton C, Machtay M, Grignon D,. Phase III radiation therapy oncology group (RTOG) trial 86-10 of androgen deprivation adjuvant to definitive radiotherapy in locally advanced carcinoma of the prostate. Int J Radiat Oncol Biol Phys 2001; 50: 1243-52.
2. D'Amico AV, Manola J, Loffredo M, Renshaw AA, DellaCroce A, Kantoff PW,. 6-month androgen suppression plus radiation therapy vs radiation therapy alone for patients with clinically localized prostate cancer: a randomized controlled trial. JAMA 2004; 292: 821-7.
3. Denham JW, Steigler A, Lamb DS, Joseph D, Mameghan H, Turner S, Matthews J, Franklin I, Atkinson C, North J, Poulsen M, Christie D, Spry NA, Tai KH, Wynne C, Duchesne G, Kovacev O, D'Este C,. Short-term androgen deprivation and radiotherapy for locally advanced prostate cancer: results from the Trans-Tasman Radiation Oncology Group 96.01 randomised controlled trial. Lancet Oncol 2005; 6: 841-50.
4. Vance W, Tucker SL, de Crevoisier R, Kuban DA, Cheung MR,. The predictive value of 2-year posttreatment biopsy after prostate cancer radiotherapy for eventual biochemical outcome. Int J Radiat Oncol Biol Phys 2007; 67: 828-33.
5. Morgan PB, Hanlon AL, Horwitz EM, Buyyounouski MK, Uzzo RG, Pollack A,. Radiation dose and late failures in prostate cancer. Int J Radiat Oncol Biol Phys 2007; 67: 1074-81.
6. Miyake H, Hara I, Gleave ME,. Antisense oligodeoxynucleotide therapy targeting clusterin gene for prostate cancer: Vancouver experience from discovery to clinic. Int J Urol 2005; 12: 785-94.
7. Mu Z, Hachem P, Agrawal S, Pollack A,. Antisense MDM2 sensitizes prostate cancer cells to androgen deprivation, radiation, and the combination. Int J Radiat Oncol Biol Phys 2004; 58: 336-43. (Pubitemid 38142457)
8. Stoyanova R, Hachem P, Hensley HH, Khor L, Mu Z, Hammond MH, Agrawal S, Pollack A,. Antisense MDM2 sensitizes LNCaP prostate cancer cells to androgen deprivation, radiation and the combination in vivo. Int J Radiat Oncol Biol Phys 2007; 68: 1151-60.
9. Mellon PL, Clegg CH, Correll LA, McKnight GS,. Regulation of transcription by cyclic AMP-dependent protein kinase. Proc Natl Acad Sci USA 1989; 86: 4887-91.
10. Cho-Chung YS,. Role of cyclic AMP receptor proteins in growth, differentiation, and suppression of malignancy: new approaches to therapy. Cancer Res 1990; 50: 7093-100.
11. Cho-Chung YS, Clair T,. The regulatory subunit of cAMP-dependent protein kinase as a target for chemotherapy of cancer and other cellular dysfunctional-related diseases. Pharmacol Ther 1993; 60: 265-88.
12. Nesterova M, Cho-Chung YS,. A single-injection protein kinase A-directed antisense treatment to inhibit tumour growth. Nat Med 1995; 1: 528-33.
13. Tortora G, Yokozaki H, Pepe S, Clair T, Cho-Chung YS,. Differentiation of HL-60 leukemia by type I regulatory subunit antisense oligodeoxynucleotide of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 1991; 88: 2011-5.
14. Bradbury AW, Carter DC, Miller WR, Cho-Chung YS, Clair T,. Protein kinase A (PK-A) regulatory subunit expression in colorectal cancer and related mucosa. Br J Cancer 1994; 69: 738-42.
15. Tortora G, Caputo R, Damiano V, Bianco R, Pepe S, Bianco AR, Jiang Z, Agrawal S, Ciardiello F,. Synergistic inhibition of human cancer cell growth by cytotoxic drugs and mixed backbone antisense oligonucleotide targeting protein kinase A. Proc Natl Acad Sci USA 1997; 94: 12586-91.
16. Shi SS, He ZG, Shao K, Zhou F, Xiong MH, Huang W, Mu BD, Zhang CY, Zhang S, Sun YT, He J,. [Relationship between overexpression of the RIalpha subunit of the cAMP-dependent protein kinase and clinicopathological features of lung cancer.]. Zhonghua Zhong Liu Za Zhi 2004; 26: 547-50.
17. Miller WR, Hulme MJ, Cho-Chung YS, Elton RA,. Types of cyclic AMP binding proteins in human breast cancers. Eur J Cancer 1993; 29: 989-91.
18. Nesterova M, Cho-Chung YS,. Oligonucleotide sequence-specific inhibition of gene expression, tumor growth inhibition, and modulation of cAMP signaling by an RNA-DNA hybrid antisense targeted to protein kinase A RIalpha subunit. Antisense Nucleic Acid Drug Dev 2000; 10: 423-33.
19. Agrawal S, Kandimalla ER, Yu D, Ball R, Lombardi G, Lucas T, Dexter DL, Hollister BA, Chen SF,. GEM 231, a second-generation antisense agent complementary to protein kinase A RIalpha subunit, potentiates antitumor activity of irinotecan in human colon, pancreas, prostate and lung cancer xenografts. Int J Oncol 2002; 21: 65-72.
20. Bianco C, Bianco R, Tortora G, Damiano V, Guerrieri P, Montemaggi P, Mendelsohn J, De Placido S, Bianco AR, Ciardiello F,. Antitumor activity of combined treatment of human cancer cells with ionizing radiation and anti-epidermal growth factor receptor monoclonal antibody C225 plus type I protein kinase A antisense oligonucleotide. Clin Cancer Res 2000; 6: 4343-50.
21. Chin C, Bae JH, Kim MJ, Hwang JY, Kim SJ, Yoon MS, Lee MK, Kim DW, Chung BS, Kang CD, Kim SH,. Radiosensitization by targeting radioresistance-related genes with protein kinase A inhibitor in radioresistant cancer cells. Exp Mol Med 2005; 37: 608-18.
22. Ciardiello F, Tortora G,. Interactions between the epidermal growth factor receptor and type I protein kinase A: biological significance and therapeutic implications. Clin Cancer Res 1998; 4: 821-8. (Pubitemid 28183381)
23. Mimeault M, Pommery N, Henichart JP,. Synergistic antiproliferative and apoptotic effects induced by epidermal growth factor receptor and protein kinase a inhibitors in human prostatic cancer cell lines. Int J Cancer 2003; 106: 116-24. (Pubitemid 36750397)
24. Cho YS, Kim MK, Tan L, Srivastava R, Agrawal S, Cho-Chung YS,. Protein kinase A RIalpha antisense inhibition of PC3M prostate cancer cell growth: Bcl-2 hyperphosphorylation, Bax up-regulation, and Bad-hypophosphorylation. Clin Cancer Res 2002; 8: 607-14.
25. Khor L-Y, Bae K, Al-Saleem T, Hammond EH, Grignon DJ, Sause WT, Pilepich MV, Okunieff PP, Sandler HM, Pollack A,. Protein kinase A RI-alpha (PKA) predicts prostate cancer outcome: an analysis of radiation therapy Oncology Group Trial 86-10. Int J Radiat Oncol Biol Phys 2008; 71: 1309-15.
26. Chen T, Cho RW, Stork PJ, Weber MJ,. Elevation of cyclic adenosine 3′,5′-monophosphate potentiates activation of mitogen-activated protein kinase by growth factors in LNCaP prostate cancer cells. Cancer Res 1999; 59: 213-8.
27. Gioeli D, Mandell JW, Petroni GR, Frierson HF, Jr, Weber MJ,. Activation of mitogen-activated protein kinase associated with prostate cancer progression. Cancer Res 1999; 59: 279-84.
28. Segawa N, Nakamura M, Nakamura Y, Mori I, Katsuoka Y, Kakudo K,. Phosphorylation of mitogen-activated protein kinase is inhibited by calcitonin in DU145 prostate cancer cells. Cancer Res 2001; 61: 6060-3.
29. Wang G, Jones SJ, Marra MA, Sadar MD,. Identification of genes targeted by the androgen and PKA signaling pathways in prostate cancer cells. Oncogene 2006; 25: 7311-23.
30. Chen HX, Marshall JL, Ness E, Martin RR, Dvorchik B, Rizvi N, Marquis J, McKinlay M, Dahut W, Hawkins MJ,. A safety and pharmacokinetic study of a mixed-backbone oligonucleotide (GEM231) targeting the type I protein kinase A by two-hour infusions in patients with refractory solid tumors. Clin Cancer Res 2000; 6: 1259-66.
31. Cowen D, Salem N, Ashoori F, Meyn R, Meistrich ML, Roth JA, Pollack A,. Prostate cancer radiosensitization in vivo with adenovirus-mediated p53 gene therapy. Clin Cancer Res 2000; 6: 4402-8.
32. Mu Z, Hachem P, Agrawal S, Pollack A,. Antisense MDM2 oligonucleotides restore the apoptotic response of prostate cancer cells to androgen deprivation. Prostate 2004; 60: 187-96. (Pubitemid 38971830)
33. Pollack A, Salem N, Ashoori F, Hachem P, Sangha M, von Eschenbach AC, Meistrich ML,. Lack of prostate cancer radiosensitization by androgen deprivation. Int J Radiat Oncol Biol Phys 2001; 51: 1002-7.
34. Kestin LL, Vicini FA, Martinez AA,. Practical application of biochemical failure definitions: what to do and when to do it. Int J Radiat Oncol Biol Phys 2002; 53: 304-15.
35. Roach M, III, Hanks G, Thames H, Jr, Schellhammer P, Shipley WU, Sokol GH, Sandler H,. Defining biochemical failure following radiotherapy with or without hormonal therapy in men with clinically localized prostate cancer: recommendations of the RTOG-ASTRO Phoenix Consensus Conference. Int J Radiat Oncol Biol Phys 2006; 65: 965-74.
36. Kim J, Jia L, Stallcup MR, Coetzee GA,. The role of protein kinase A pathway and cAMP responsive element-binding protein in androgen receptor-mediated transcription at the prostate-specific antigen locus. J Mol Endocrinol 2005; 34: 107-18.
37. Culig Z,. Androgen receptor cross-talk with cell signalling pathways. Growth Factors 2004; 22: 179-84.
38. Sadar MD,. Androgen-independent induction of prostate-specific antigen gene expression via cross-talk between the androgen receptor and protein kinase A signal transduction pathways. J Biol Chem 1999; 274: 7777-83.
39. Nesterova MV, Cho-Chung YS,. Antisense protein kinase A RIalpha inhibits 7,12-dimethylbenz(a)anthracene-induction of mammary cancer: blockade at the initial phase of carcinogenesis. Clin Cancer Res 2004; 10: 4568-77.
40. Nesterova MV, Cho-Chung YS,. Chemoprevention with protein kinase A RIalpha antisense in DMBA-mammary carcinogenesis. Ann N Y Acad Sci 2005; 1058: 255-64.
41. Tortora G, Caputo R, Damiano V, Fontanini G, Melisi D, Veneziani BM, Zunino F, Bianco AR, Ciardiello F,. Oral administration of a novel taxane, an antisense oligonucleotide targeting protein kinase A, and the epidermal growth factor receptor inhibitor Iressa causes cooperative antitumor and antiangiogenic activity. Clin Cancer Res 2001; 7: 4156-63.
42. Tortora G, Caputo R, Damiano V, Melisi D, Bianco R, Fontanini G, Veneziani BM, De Placido S, Bianco AR, Ciardiello F,. Combination of a selective cyclooxygenase-2 inhibitor with epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 and protein kinase A antisense causes cooperative antitumor and antiangiogenic effect. Clin Cancer Res 2003; 9: 1566-72.
43. Wang H, Hang J, Shi Z, Li M, Yu D, Kandimalla ER, Agrawal S, Zhang R,. Antisense oligonucleotide targeted to RIalpha subunit of cAMP-dependent protein kinase (GEM231) enhances therapeutic effectiveness of cancer chemotherapeutic agent irinotecan in nude mice bearing human cancer xenografts: in vivo synergistic activity, pharmacokinetics and host toxicity. Int J Oncol 2002; 21: 73-80.
44. Fujino M, Ohnishi K, Asahi M, Wang X, Takahashi A, Ohnishi T,. Effects of protein kinase inhibitors on radiation-induced WAF1 accumulation in human cultured melanoma cells. Br J Dermatol 1999; 141: 652-7.
45. Mani S, Goel S, Nesterova M, Martin RM, Grindel JM, Rothenberg ML, Zhang R, Tortora G, Cho-Chung YS,. Clinical studies in patients with solid tumors using a second-generation antisense oligonucleotide (GEM 231) targeted against protein kinase A type I. Ann N Y Acad Sci 2003; 1002: 252-62.
46. Culig Z, Steiner H, Bartsch G, Hobisch A,. Mechanisms of endocrine therapy-responsive and -unresponsive prostate tumours. Endocr Relat Cancer 2005; 12: 229-44.
47. Wang G, Sadar MD,. Amino-terminus domain of the androgen receptor as a molecular target to prevent the hormonal progression of prostate cancer. J Cell Biochem 2006; 98: 36-53.
48. Cheng H, Snoek R, Ghaidi F, Cox ME, Rennie PS,. Short hairpin RNA knockdown of the androgen receptor attenuates ligand-independent activation and delays tumor progression. Cancer Res 2006; 66: 10613-20.
49. Ueda T, Bruchovsky N, Sadar MD,. Activation of the androgen receptor N-terminal domain by interleukin-6 via MAPK and STAT3 signal transduction pathways. J Biol Chem 2002; 277: 7076-85.
50. Qiao L, Yacoub A, McKinstry R, Park JS, Caron R, Fisher PB, Hagan MP, Grant S, Dent P,. Pharmocologic inhibitors of the mitogen activated protein kinase cascade have the potential to interact with ionizing radiation exposure to induce cell death in carcinoma cells by multiple mechanisms. Cancer Biol Ther 2002; 1: 168-76.