Autophagy in prostate cancer and androgen suppression therapy

International Journal of Molecular Sciences

Volumn 14, Issue 6, 2013, Pages 12090-12106

  Ziparo, Elio ^a   Petrungaro, Simonetta ^a   Marini, Elettra Sara ^a   Starace, Donatella ^a   Conti, Silvia ^a   Facchiano, Antonio ^b   Filippini, Antonio ^a   Giampietri, Claudia ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Androgen deprivation therapy; Apoptosis; Autophagy; Prostate cancer

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANTIANDROGEN; BECLIN 1; CELL PROTEIN; CHLOROQUINE; GONADORELIN AGONIST; HYDROXYCHLOROQUINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNC 51 LIKE KINASE 1; UNCLASSIFIED DRUG;

ANDROGEN DEPRIVATION THERAPY; AUTOPHAGOSOME; AUTOPHAGY; CANCER HORMONE THERAPY; CANCER IMMUNOLOGY; CANCER RADIOTHERAPY; CANCER STAGING; CELL FUNCTION; CELL STIMULATION; CELL SURVIVAL; DRUG EFFICACY; HORMONE ACTION; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; NONHUMAN; ORCHIECTOMY; PROSTATE CANCER; PROTEIN FUNCTION; REVIEW; ANIMAL; BIOLOGICAL MODEL; DISEASE COURSE; DRUG EFFECTS; IMMUNITY; IMMUNOLOGY; MALE; PATHOLOGY; PROSTATIC NEOPLASMS;

ANDROGENS; ANIMALS; AUTOPHAGY; DISEASE PROGRESSION; HUMANS; IMMUNITY; MALE; MODELS, BIOLOGICAL; PROSTATIC NEOPLASMS;

EID: 84879019799     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140612090     Document Type: Review

References (77)

1. Borley, N.; Feneley, M.R. Prostate cancer: Diagnosis and staging. Asian J. Androl. 2009, 11, 74-80.
2. Tadros, N.N.; Garzotto, M. Androgen deprivation therapy for prostate cancer: Not so simple. Asian J. Androl. 2011, 13, 187-188.
3. Boccon-Gibod, L.; van der Meulen, E.; Persson, B.E. An update on the use of gonadotropin-releasing hormone antagonists in prostate cancer. Ther. Adv. Urol. 2011, 3, 127-140.
4. Oudard, S. Progress in emerging therapies for advanced prostate cancer. Cancer Treat. Rev. 2013, 39, 275-289.
5. Mostaghel, E.A.; Page, S.T.; Lin, D.W.; Fazli, L.; Coleman, I.M.; True, L.D.; Knudsen, B.; Hess, D.L.; Nelson, C.C.; Matsumoto, A.M.; et al. Intraprostatic androgens and androgen-regulated gene expression persist after testosterone suppression: Therapeutic implications for castration-resistant prostate cancer. Cancer Res. 2007, 67, 5033-5041.
6. Saraon, P.; Jarvi, K.; Diamandis, E.P. Molecular alterations during progression of prostate cancer to androgen independence. Clin. Chem. 2011, 57, 1366-1375.
7. Knudsen, K.E.; Scher, H.I. Starving the addiction: New opportunities for durable suppression of AR signaling in prostate cancer. Clin. Cancer Res. 2009, 15, 4792-4798.
8. Miyake, H.; Nelson, C.; Rennie, P.S.; Gleave, M.E. Overexpression of insulin-like growth factor binding protein-5 helps accelerate progression to androgen-independence in the human prostate LNCaP tumor model through activation of phosphatidylinositol 3'-kinase pathway. Endocrinology 2000, 141, 2257-2265.
9. Rocchi, P.; So, A.; Kojima, S.; Signaevsky, M.; Beraldi, E.; Fazli, L.; Hurtado-Coll, A.; Yamanaka, K.; Gleave, M. Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res. 2004, 64, 6595-6602.
10. Levine, B.; Klionsky, D.J. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev. Cell 2004, 6, 463-477.
11. Glick, D.; Barth, S.; Macleod, K.F. Autophagy: Cellular and molecular mechanisms. J. Pathol. 2010, 221, 3-12.
12. Shintani, T.; Klionsky, D.J. Autophagy in health and disease: A double-edged sword. Science 2004, 306, 990-995.
13. Horbinski, C.; Mojesky, C.; Kyprianou, N. Live free or die: Tales of homeless (cells) in cancer. Am. J. Pathol. 2010, 177, 1044-1052.
14. Corcelle, E.A.; Puustinen, P.; Jaattela, M. Apoptosis and autophagy: Targeting autophagy signalling in cancer cells-'Trick or treats'? FEBS J. 2009, 276, 6084-6096.
15. Hippert, M.M.; O'Toole, P.S.; Thorburn, A. Autophagy in cancer: Good, bad, or both? Cancer Res. 2006, 66, 9349-9351.
16. Kondo, Y.; Kanzawa, T.; Sawaya, R.; Kondo, S. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 2005, 5, 726-734.
17. Arico, S.; Petiot, A.; Bauvy, C.; Dubbelhuis, P.F.; Meijer, A.J.; Codogno, P.; Ogier-Denis, E. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 2001, 276, 35243-35246.
18. Pattingre, S.; Tassa, A.; Qu, X.; Garuti, R.; Liang, X.H.; Mizushima, N.; Packer, M.; Schneider, M.D.; Levine, B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122, 927-939.
19. Li, L.; Ishdorj, G.; Gibson, S.B. Reactive oxygen species regulation of autophagy in cancer: Implications for cancer treatment. Free Radic. Biol. Med. 2012, 53, 1399-1410.
20. Edinger, A.L.; Thompson, C.B. Defective autophagy leads to cancer. Cancer Cell 2003, 4, 422-424.
21. Aita, V.M.; Liang, X.H.; Murty, V.V.; Pincus, D.L.; Yu, W.; Cayanis, E.; Kalachikov, S.; Gilliam, T.C.; Levine, B. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 1999, 59, 59-65.
22. Qu, X.; Yu, J.; Bhagat, G.; Furuya, N.; Hibshoosh, H.; Troxel, A.; Rosen, J.; Eskelinen, E.L.; Mizushima, N.; Ohsumi, Y.; et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 2003, 112, 1809-1820.
23. Dalby, K.N.; Tekedereli, I.; Lopez-Berestein, G.; Ozpolat, B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 2010, 6, 322-329.
24. Kung, H.J. Targeting tyrosine kinases and autophagy in prostate cancer. Horm. Cancer 2011, 2, 38-46.
25. Guo, Z.; Dai, B.; Jiang, T.; Xu, K.; Xie, Y.; Kim, O.; Nesheiwat, I.; Kong, X.; Melamed, J.; Handratta, V.D.; et al. Regulation of androgen receptor activity by tyrosine phosphorylation. Cancer Cell 2006, 10, 309-319.
26. Wu, Z.; Chang, P.C.; Yang, J.C.; Chu, C.Y.; Wang, L.Y.; Chen, N.T.; Ma, A.H.; Desai, S.J.; Lo, S.H.; Evans, C.P.; et al. Autophagy blockade sensitizes prostate cancer cells towards Src family kinase inhibitors. Genes Cancer 2010, 1, 40-49.
27. Bristol, M.L.; Emery, S.M.; Maycotte, P.; Thorburn, A.; Chakradeo, S.; Gewirtz, D.A. Autophagy inhibition for chemosensitization and radiosensitization in cancer: Do the preclinical data support this therapeutic strategy? J. Pharmacol. Exp. Ther. 2013, 344, 544-552.
28. Kumano, M.; Furukawa, J.; Shiota, M.; Zardan, A.; Zhang, F.; Beraldi, E.; Wiedmann, R.M.; Fazli, L.; Zoubeidi, A.; Gleave, M.E. Cotargeting stress-activated Hsp27 and autophagy as a combinatorial strategy to amplify endoplasmic reticular stress in prostate cancer. Mol. Cancer Ther. 2012, 11, 1661-1671.
29. Lamoureux, F.; Thomas, C.; Crafter, C.; Kumano, M.; Zhang, F.; Davies, B.R.; Gleave, M.E.; Zoubeidi, A. Blocked autophagy using lysosomotropic agents sensitizes resistant prostate tumor cells to the novel Akt inhibitor AZD5363. Clin. Cancer Res. 2013, 19, 833-844.
30. Yu, L.; Tumati, V.; Tseng, S.F.; Hsu, F.M.; Kim, D.N.; Hong, D.; Hsieh, J.T.; Jacobs, C.; Kapur, P.; Saha, D. DAB2IP regulates autophagy in prostate cancer in response to combined treatment of radiation and a DNA-PKcs inhibitor. Neoplasia 2012, 14, 1203-1212.
31. Chen, R.J.; Hung, C.M.; Chen, Y.L.; Wu, M.D.; Yuan, G.F.; Wang, Y.J. Monascuspiloin induces apoptosis and autophagic cell death in human prostate cancer cells via the Akt and AMPK signaling pathways. J. Agric. Food Chem. 2012, 60, 7185-7193.
32. Tai, S.; Sun, Y.; Liu, N.; Ding, B.; Hsia, E.; Bhuta, S.; Thor, R.K.; Damoiseaux, R.; Liang, C.; Huang, J. Combination of Rad001 (everolimus) and propachlor synergistically induces apoptosis through enhanced autophagy in prostate cancer cells. Mol. Cancer Ther. 2012, 11, 1320-1331.
33. He, Z.; Mangala, L.S.; Theriot, C.A.; Rohde, L.H.; Wu, H.; Zhang, Y. Cell killing and radiosensitizing effects of atorvastatin in PC3 prostate cancer cells. J. Radiat. Res. 2012, 53, 225-233.
34. Jain, R.K.; Safabakhsh, N.; Sckell, A.; Chen, Y.; Jiang, P.; Benjamin, L.; Yuan, F.; Keshet, E. Endothelial cell death, angiogenesis, and microvascular function after castration in an androgen-dependent tumor: Role of vascular endothelial growth factor. Proc. Natl. Acad. Sci. USA 1998, 95, 10820-10825.
35. Chhipa, R.R.; Wu, Y.; Ip, C. AMPK-mediated autophagy is a survival mechanism in androgen-dependent prostate cancer cells subjected to androgen deprivation and hypoxia. Cell Signal. 2011, 23, 1466-1472.
36. Kaini, R.R.; Hu, C.A. Synergistic killing effect of chloroquine and androgen deprivation in LNCaP cells. Biochem. Biophys. Res. Commun. 2012, 425, 150-156.
37. Chhipa, R.R.; Wu, Y.; Mohler, J.L.; Ip, C. Survival advantage of AMPK activation to androgen-independent prostate cancer cells during energy stress. Cell Signal. 2010, 22, 1554-1561.
38. Meijer, A.J.; Codogno, P. AMP-activated protein kinase and autophagy. Autophagy 2007, 3, 238-240.
39. Park, H.U.; Suy, S.; Danner, M.; Dailey, V.; Zhang, Y.; Li, H.; Hyduke, D.R.; Collins, B.T.; Gagnon, G.; Kallakury, B.; et al. AMP-activated protein kinase promotes human prostate cancer cell growth and survival. Mol. Cancer Ther. 2009, 8, 733-741.
40. Schoenlein, P.V.; Periyasamy-Thandavan, S.; Samaddar, J.S.; Jackson, W.H.; Barrett, J.T. Autophagy facilitates the progression of ERalpha-positive breast cancer cells to antiestrogen resistance. Autophagy 2009, 5, 400-403.
41. Bennett, H.L.; Stockley, J.; Fleming, J.T.; Mandal, R.; O'Prey, J.; Ryan, K.M.; Robson, C.N.; Leung, H.Y. Does androgen-ablation therapy (AAT) associated autophagy have a pro-survival effect in LNCaP human prostate cancer cells? BJU Int. 2012, 111, 672-682.
42. Homewood, C.A.; Warhurst, D.C.; Peters, W.; Baggaley, V.C. Lysosomes, pH and the anti-malarial action of chloroquine. Nature 1972, 235, 50-52.
43. Amaravadi, R.K.; Lippincott-Schwartz, J.; Yin, X.M.; Weiss, W.A.; Takebe, N.; Timmer, W.; Dipaola, R.S.; Lotze, M.T.; White, E. Principles and current strategies for targeting autophagy for cancer treatment. Clin. Cancer Res. 2011, 17, 654-666.
44. Sotelo, J.; Briceno, E.; Lopez-Gonzalez, M.A. Adding chloroquine to conventional treatment for glioblastoma multiforme: A randomized, double-blind, placebo-controlled trial. Ann. Intern. Med. 2006, 144, 337-343.
45. Cheong, H.; Lu, C.; Lindsten, T.; Thompson, C.B. Therapeutic targets in cancer cell metabolism and autophagy. Nat. Biotechnol. 2012, 30, 671-678.
46. Tang, D.G.; Porter, A.T. Target to apoptosis: A hopeful weapon for prostate cancer. Prostate 1997, 32, 284-293.
47. Hesry, V.; Piquet-Pellorce, C.; Travert, M.; Donaghy, L.; Jegou, B.; Patard, J.J.; Guillaudeux, T. Sensitivity of prostate cells to TRAIL-induced apoptosis increases with tumor progression: DR5 and caspase 8 are key players. Prostate 2006, 66, 987-995.
48. Nakajima, Y.; DelliPizzi, A.M.; Mallouh, C.; Ferreri, N.R. TNF-mediated cytotoxicity and resistance in human prostate cancer cell lines. Prostate 1996, 29, 296-302.
49. D'Arcangelo, D.; Giampietri, C.; Facchiano, F.; Facchiano, A. BAMM: A preliminary Bibliometric Analysis on Melanoma Manuscripts. Pigment Cell Melanoma Res. 2013, 26, 415-417.
50. Giampietri, C.; Petrungaro, S.; Facchiano, A.; Filippini, A.; Ziparo, E. Therapeutic implications of autophagy modulation in prostate cancer. J. Endocrinol. Invest. 2012, 35, 945.
51. Giampietri, C.; Petrungaro, S.; Padula, F.; D'Alessio, A.; Marini, E.S.; Facchiano, A.; Filippini, A.; Ziparo, E. Autophagy modulators sensitize prostate epithelial cancer cell lines to TNF-alpha-dependent apoptosis. Apoptosis 2012, 17, 1210-1222.
52. He, W.; Wang, Q.; Xu, J.; Xu, X.; Padilla, M.T.; Ren, G.; Gou, X.; Lin, Y. Attenuation of TNFSF10/TRAIL-induced apoptosis by an autophagic survival pathway involving T. Autophagy 2012, 8, 1811-1821.
53. Zhu, K.; Dunner, K.,; McConkey, D.J. Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene 2010, 29, 451-462.
54. Lee, J.Y.; Koga, H.; Kawaguchi, Y.; Tang, W.X.; Wong, E.; Gao, Y.S.; Pandey, U.B.; Kaushik, S.; Tresse, E.; Lu, J.R.; et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 2010, 29, 969-980.
55. True, O.; Matthias, P. Interplay between histone deacetylases and autophagy-From cancer therapy to neurodegeneration. Immunol. Cell Biol. 2012, 90, 78-84.
56. Lu, J.V.; Walsh, C.M. Programmed necrosis and autophagy in immune function. Immunol. Rev. 2012, 249, 205-217.
57. Muzes, G.; Sipos, F. Anti-tumor immunity, autophagy and chemotherapy. World J. Gastroenterol. 2012, 18, 6537-6540.
58. Muranski, P.; Boni, A.; Antony, P.A.; Cassard, L.; Irvine, K.R.; Kaiser, A.; Paulos, C.M.; Palmer, D.C.; Touloukian, C.E.; Ptak, K.; et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 2008, 112, 362-373.
59. Ahn, G.O.; Tseng, D.; Liao, C.H.; Dorie, M.J.; Czechowicz, A.; Brown, J.M. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc. Natl. Acad. Sci. USA 2010, 107, 8363-8368.
60. Wildenberg, M.E.; Vos, A.C.; Wolfkamp, S.C.; Duijvestein, M.; Verhaar, A.P.; te Velde, A.A.; van den Brink, G.R.; Hommes, D.W. Autophagy attenuates the adaptive immune response by destabilizing the immunologic synapse. Gastroenterology 2012, 142, 1493-1503.
61. Barron, D.A.; Rowley, D.R. The reactive stroma microenvironment and prostate cancer progression. Endocr. Relat. Cancer 2012, 19, R187-R204.
62. Gerdes, M.J.; Dang, T.D.; Larsen, M.; Rowley, D.R. Transforming growth factor-beta1 induces nuclear to cytoplasmic distribution of androgen receptor and inhibits androgen response in prostate smooth muscle cells. Endocrinology 1998, 139, 3569-3577.
63. Jones, E.; Pu, H.; Kyprianou, N. Targeting TGF-beta in prostate cancer: Therapeutic possibilities during tumor progression. Expert. Opin. Ther. Targets. 2009, 13, 227-234.
64. Salm, S.N.; Burger, P.E.; Coetzee, S.; Goto, K.; Moscatelli, D.; Wilson, E.L. TGF-{beta} maintains dormancy of prostatic stem cells in the proximal region of ducts. J. Cell Biol. 2005, 170, 81-90.
65. Stover, D.G.; Bierie, B.; Moses, H.L. A delicate balance: TGF-beta and the tumor microenvironment. J. Cell Biochem. 2007, 101, 851-861.
66. Zhu, B.; Kyprianou, N. Transforming growth factor beta and prostate cancer. Cancer Treat. Res. 2005, 126, 157-173.
67. Alonso-Magdalena, P.; Brossner, C.; Reiner, A.; Cheng, G.; Sugiyama, N.; Warner, M.; Gustafsson, J.A. A role for epithelial-mesenchymal transition in the etiology of benign prostatic hyperplasia. Proc. Natl. Acad. Sci. USA 2009, 106, 2859-2863.
68. Ao, M.; Franco, O.E.; Park, D.; Raman, D.; Williams, K.; Hayward, S.W. Cross-talk between paracrine-acting cytokine and chemokine pathways promotes malignancy in benign human prostatic epithelium. Cancer Res. 2007, 67, 4244-4253.
69. Gann, P.H.; Klein, K.G.; Chatterton, R.T.; Ellman, A.E.; Grayhack, J.T.; Nadler, R.B.; Lee, C. Growth factors in expressed prostatic fluid from men with prostate cancer, BPH, and clinically normal prostates. Prostate 1999, 40, 248-255.
70. Shoskes, D.A.; Albakri, Q.; Thomas, K.; Cook, D. Cytokine polymorphisms in men with chronic prostatitis/chronic pelvic pain syndrome: Association with diagnosis and treatment response. J. Urol. 2002, 168, 331-335.
71. Kiyono, K.; Suzuki, H.I.; Matsuyama, H.; Morishita, Y.; Komuro, A.; Kano, M.R.; Sugimoto, K.; Miyazono, K. Autophagy is activated by TGF-beta and potentiates TGF-beta-mediated growth inhibition in human hepatocellular carcinoma cells. Cancer Res. 2009, 69, 8844-8852.
72. Lee, C.; Sintich, S.M.; Mathews, E.P.; Shah, A.H.; Kundu, S.D.; Perry, K.T.; Cho, J.S.; Ilio, K.Y.; Cronauer, M.V.; Janulis, L.; et al. Transforming growth factor-beta in benign and malignant prostate. Prostate 1999, 39, 285-290.
73. Reynolds, A.R.; Kyprianou, N. Growth factor signalling in prostatic growth: Significance in tumor development and therapeutic targeting. Br. J. Pharmacol. 2006, 147, S144-S152.
74. Fuzio, P.; Ditonno, P.; Rutigliano, M.; Battaglia, M.; Bettocchi, C.; Loverre, A.; Grandaliano, G.; Perlino, E. Regulation of TGF-beta1 expression by androgen deprivation therapy of prostate cancer. Cancer Lett. 2012, 318, 135-144.
75. Calone, I.; Souchelnytskyi, S. Inhibition of TGFbeta signaling and its implications in anticancer treatments. Exp. Oncol. 2012, 34, 9-16.
76. Mirochnik, Y.; Veliceasa, D.; Williams, L.; Maxwell, K.; Yemelyanov, A.; Budunova, I.; Volpert, O.V. Androgen receptor drives cellular senescence. PLoS One. 2012, 7, e31052.
77. White, E.; Lowe, S.W. Eating to exit: Autophagy-enabled senescence revealed. Genes Dev. 2009, 23, 784-787.