BCL-2 in prostate cancer: A minireview

Springer Science and Business Media LLC - Tập 8 - Trang 29-37 - 2003
S. D. Catz1, J. L. Johnson1
1Biochemistry Division, Department of Molecular and Experimental Medicine, The Scripps Research Institute, La Jolla, USA

Tóm tắt

Prostate cancer progression and the development of androgen-independent prostate cancer have been largely related to a number of genetic abnormality that affect not only the androgen receptor but also crucial molecules involved in the regulation of survival or apoptotic pathways. One of these molecules, the pro-survival protein BCL-2, has been associated with the development of androgen-independent prostate cancer due to its high levels of expression in androgen-independent tumors in advanced stages of the pathology. The upregulation of BCL-2 after androgen ablation in prostate carcinoma cell lines and in a castrated-male rat model further established a connection between BCL-2 expression and prostate cancer progression. This review focuses on the experimental evidence that associates BCL-2 expression with prostate carcinogenesis and cancer progression, and analyzes the evidence that links the phosphatidylinositol 3-kinase (PI 3-kinase)/nuclear factor kappa B (NF-κB) survival pathway with the upregulation of BCL-2. The way in which hormone ablation influences this survival pathway and the potential application of novel therapeutic strategies to overcome this anti-apoptotic mechanism is examined.

Tài liệu tham khảo

Boring CC, Squires TS, Tong T, Montgomery S. Cancer statistics, 1994. CA Cancer J Clin 1994; 44: 7–26.

Tsujimoto Y, Cossman J, Jaffe E, Croce CM. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985; 228: 1440–1443.

Reed JC. Bcl-2 and the regulation of programmed cell death. J Cell Biol 1994; 124: 1–6.

Reed JC. Mechanisms of apoptosis. Am J Pathol 2000; 157: 1415–1430.

Adams JM, Cory S. The Bcl-2 protein family: Arbiters of cell survival. Science 1998; 281: 1322–1326.

Hanada M, Aime-Sempe C, Sato T, Reed JC. Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J Biol Chem 1995; 270: 11962–11969.

Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 1999; 13: 1899–1911.

Abate-Shen C, Shen MM. Molecular genetics of prostate cancer. Genes Dev 2000; 14: 2410–2434.

di Sant'Agnese PA. Neuroendocrine differentiation in carcinoma of the prostate. Diagnostic, prognostic, and therapeutic implications. Cancer 1992; 70: 254–268.

Abrahamsson PA. Neuroendocrine differentiation in prostatic carcinoma. Prostate 1999; 39: 135–148.

Hockenbery DM, Zutter M, Hickey W, Nahm M, Korsmeyer SJ. BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl Acad Sci USA 1991; 88: 6961–6965.

Colombel M, Symmans F, Gil S, et al. Detection of the apoptosis-suppressing oncoprotein bc1-2 in hormonerefractory human prostate cancers. Am J Pathol 1993; 143: 390–400.

Denmeade SR, Lin XS, Isaacs JT. Role of programmed (apoptotic) cell death during the progression and therapy for prostate cancer. Prostate 1996; 28: 251–265.

Huggins C. Endocrine-induced regression of cancers. Cancer Res 1967; 27: 1925–1930.

Grossmann ME, Huang H, Tindall DJ. Androgen receptor signaling in androgen-refractory prostate cancer. J Natl Cancer Inst 2001; 93: 1687–1697.

Feldman BJ, Feldman D. The development of androgenindependent prostate cancer. Nature Rev Cancer 2001; 1: 34–45.

Hyytinen ER, Thalmann GN, Zhau HE, et al. Genetic changes associated with the acquisition of androgen-independent growth, tumorigenicity and metastatic potential in a prostate cancer model. Br J Cancer 1997; 75: 190–195.

Kyprianou N. Apoptosis: Therapeutic significance in the treatment of androgen-dependent and androgen-independent prostate cancer. World J Urol 1994; 12: 299–303.

McDonnell TJ, Troncoso P, Brisbay SM, et al. Expression of the protooncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. Cancer Res 1992; 52: 6940–6944.

Krajewska M, Krajewski S, Epstein JI, et al. Immunohistochemical analysis of bcl-2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol 1996; 148: 1567–1576.

Furuya Y, Krajewski S, Epstein JI, Reed JC, Isaacs JT. Expression of bcl-2 and the progression of human and rodent prostatic cancers. Clin Cancer Res 1996; 2: 389–398.

Narla G, Heath KE, Reeves HL, et al. KLF6, a candidate tumor suppressor gene mutated in prostate cancer. Science 2001; 294: 2563–2566.

Fizazi K, Martinez LA, Sikes CR, et al. The association of p21((WAF-1/CIP1)) with progression to androgenindependent prostate cancer. Clin Cancer Res 2002; 8: 775–781.

Bookstein R, Rio P, Madreperla SA, et al. Promoter deletion and loss of retinoblastoma gene expression in human prostate carcinoma. Proc Natl Acad Sci USA 1990; 87: 7762–7766.

Bookstein R, Shew JY, Chen PL, Scully P, Lee WH. Suppression of tumorigenicity of human prostate carcinoma cells by replacing a mutated RB gene. Science 1990; 247: 712–715.

Bubendorf L, Sauter G, Moch H, et al. Prognostic significance of Bcl-2 in clinically localized prostate cancer. Am J Pathol 1996; 148: 1557–1565.

Johnson MI, Robinson MC, Marsh C, Robson CN, Neal DE, Hamdy FC. Expression of Bcl-2, Bax, and p53 in high-grade prostatic intraepithelial neoplasia and localized prostate cancer: Relationship with apoptosis and proliferation. Prostate 1998; 37: 223–229.

McDonnell TJ, Navone NM, Troncoso P, et al. Expression of bcl-2 oncoprotein and p53 protein accumulation in bone marrow metastases of androgen independent prostate cancer. J Urol 1997; 157: 569–574.

Apakama I, Robinson MC, Walter NM, et al. bcl-2 overexpression combined with p53 protein accumulation correlates with hormone-refractory prostate cancer. Br J Cancer 1996; 74: 1258–1262.

McConkey DJ, Greene G, Pettaway CA. Apoptosis resistance increases with metastatic potential in cells of the human LNCaP prostate carcinoma line. Cancer Res 1996; 56: 5594–5599.

Mackey TJ, Borkowski A, Amin P, Jacobs SC, Kyprianou N. bcl-2/bax ratio as a predictive marker for therapeutic response to radiotherapy in patients with prostate cancer. Urology 1998; 52: 1085–1090.

Taplin ME, Bubley GJ, Ko YJ, et al. Selection for androgen receptor mutations in prostate cancers treated with androgen antagonist. Cancer Res 1999; 59: 2511–2515.

Craft N, Chhor C, Tran C, et al. Evidence for clonal outgrowth of androgen-independent prostate cancer cells from androgendependent tumors through a two-step process. Cancer Res 1999; 59: 5030–5036.

English HF, Kyprianou N, Isaacs JT. Relationship between DNA fragmentation and apoptosis in the programmed cell death in the rat prostate following castration. Prostate 1989; 15: 233–250.

Lu S, Tsai SY, Tsai MJ. Molecular mechanisms of androgenindependent growth of human prostate cancer LNCaP-AI cells. Endocrinology 1999; 140: 5054–5059.

Catz SD, Johnson JL. Transcriptional regulation of bcl-2 by nuclear factor kappaB and its significance in prostate cancer. Oncogene 2001; 20: 7342–7351.

Gleave M, Tolcher A, Miyake H, et al. Progression to androgen independence is delayed by adjuvant treatment with antisense Bcl-2 oligodeoxynucleotides after castration in the LNCaP prostate tumor model. Clin Cancer Res 1999; 5: 2891–2898.

Raffo AJ, Perlman H, Chen MW, Day ML, Streitman JS, Buttyan R. Overexpression of bcl-2 protects prostate cancer cells from apoptosis in vitro and confers resistance to androgen depletion in vivo. Cancer Res 1995; 55: 4438–4445.

Di Cristofano A, Pandolfi PP. The multiple roles of PTEN in tumor suppression. Cell 2000; 100: 387–390.

Gray IC, Phillips SM, Lee SJ, Neoptolemos JP, Weissenbach J, Spurr NK. Loss of the chromosomal region 10q23-25 in prostate cancer. Cancer Res 1995; 55: 4800–4803.

Cantley LC, Neel BG. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc Natl Acad Sci USA 1999; 96: 4240–4245.

Feilotter HE, Nagai MA, Boag AH, Eng C, Mulligan LM. Analysis of PTEN and the 10q23 region in primary prostate carcinomas. Oncogene 1998; 16: 1743–1748.

Suzuki H, Freije D, Nusskern DR, et al. Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res 1998; 58: 204–209.

McMenamin ME, Soung P, Perera S, Kaplan I, Loda M, Sellers WR. Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res 1999; 59: 4291–4296.

Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1998; 273: 13375–13378.

Sun H, Lesche R, Li DM, et al. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc Natl Acad Sci USA 1999; 96: 6199–6204.

Tamura M, Gu J, Takino T, Yamada KM. Tumor suppressor PTEN inhibition of cell invasion, migration, and growth: Differential involvement of focal adhesion kinase and p130Cas. Cancer Res 1999; 59: 442–449.

Davies MA, Kim SJ, Parikh NU, Dong Z, Bucana CD, Gallick GE. Adenoviral-mediated Expression of MMAC/PTEN inhibits proliferation and metastasis of human prostate cancer cells. Clin Cancer Res 2002; 8: 1904–1914.

Roymans D, Slegers H. Phosphatidylinositol 3-kinases in tumor progression. Eur J Biochem 2001; 268: 487–498.

Chung LWK. LNCaP human prostate cancer progression model. Urologic Oncology 1996; 2: 126–128.

Gleave ME, Hsieh JT, Wu HC, von Eschenbach AC, Chung LW. Serum prostate specific antigen levels in mice bearing human prostate LNCaP tumors are determined by tumor volume and endocrine and growth factors. Cancer Res 1992; 52: 1598–1605.

Qiu Y, Robinson D, Pretlow TG, Kung HJ. Etk/Bmx, a tyrosine kinase with a pleckstrin-homology domain, is an effector of phosphatidylinositol 3'-kinase and is involved in interleukin 6-induced neuroendocrine differentiation of prostate cancer cells. Proc Natl Acad Sci USA 1998; 95: 3644–3649.

Umekita Y, Hiipakka RA, Kokontis JM, Liao S. Human prostate tumor growth in athymic mice: Inhibition by androgens and stimulation by finasteride. Proc Natl Acad Sci USA 1996; 93: 11802–11807.

Lin J, Adam RM, Santiestevan E, Freeman MR. The phosphatidylinositol 3'-kinase pathway is a dominant growth factor-activated cell survival pathway in LNCaP human prostate carcinoma cells. Cancer Res 1999; 59: 2891–2897.

Murillo H, Huang H, Schmidt LJ, Smith DI, Tindall DJ. Role of PI3K signaling in survival and progression of LNCaP prostate cancer cells to the androgen refractory state. Endocrinology 2001; 142: 4795–4805.

Saeed B, Zhang H, Ng SC. Apoptotic program is initiated but not completed in LNCaP cells in response to growth in charcoal-stripped media. Prostate 1997; 31: 145–152.

Heckman CA, Mehew JW, Boxer LM. NF-kappaB activates Bcl-2 expression in t(14;18) lymphoma cells. Oncogene 2002; 21: 3898–3908.

Khwaja A. Akt is more than just a Bad kinase. Nature 1999; 401: 33–34.

Romashkova JA, Makarov SS. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 1999; 401: 86–90.

Koul D, Yao Y, Abbruzzese JL, Yung WK, Reddy SA. Tumor suppressor MMAC/PTEN inhibits cytokine-induced NFkappaB activation without interfering with the IkappaB degradation pathway. J Biol Chem 2001; 276: 11402–11408.

Davies MA, Koul D, Dhesi H, et al. Regulation of Akt/PKB activity, cellular growth, and apoptosis in prostate carcinoma cells by MMAC/PTEN. Cancer Res 1999; 59: 2551–2556.

Yuan XJ, Whang YE. PTEN sensitizes prostate cancer cells to death receptor-mediated and drug-induced apoptosis through a FADD-dependent pathway. Oncogene 2002; 21: 319–327.

Huang H, Cheville JC, Pan Y, Roche PC, Schmidt LJ, Tindall DJ. PTENinduces chemosensitivity in PTEN-mutated prostate cancer cells by suppression of Bcl-2 expression. J Biol Chem 2001; 276: 38830–38836.

Pugazhenthi S, Nesterova A, Sable C, et al. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem 2000; 275: 10761–10766.

Leong KG, Karsan A. Signaling pathways mediated by tumor necrosis factor alpha. Histol Histopathol. 2000; 15: 1303–1325.

Nakajima Y, DelliPizzi AM, Mallouh C, Ferreri NR. TNF-mediated cytotoxicity and resistance in human prostate cancer cell lines. Prostate 1996; 29: 296–302.

Baldwin AS. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J Clin Invest 2001; 107: 241–246.

Claudio E, Segade F, Wrobel K, Ramos S, Bravo R, Lazo PS. Molecular mechanisms of TNFalpha cytotoxicity: Activation of NF-kappaB and nuclear translocation. Exp Cell Res 1996; 224: 63–71.

Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, Donner DB. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 1999; 401: 82–85.

Gustin JA, Maehama T, Dixon JE, Donner DB. The PTEN tumor suppressor protein inhibits tumor necrosis factor-induced nuclear factor kappa B activity. J Biol Chem 2001; 276: 27740–27744.

Kulik G, Carson JP, Vomastek T, et al. Tumor necrosis factor alpha induces BID cleavage and bypasses antiapoptotic signals in prostate cancer LNCaP cells. Cancer Res 2001; 61: 2713–2719.

Kreuz S, Siegmund D, Scheurich P, Wajant H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol Cell Biol 2001; 21: 3964–3973.

Muenchen HJ, Lin DL, Walsh MA, Keller ET, Pienta KJ. Tumor necrosis factor-alpha-induced apoptosis in prostate cancer cells through inhibition of nuclear factor-kappaB by an IkappaBalpha “super-repressor”. Clin Cancer Res 2000; 6: 1969–1977.

Sumitomo M, Tachibana M, Nakashima J, et al. An essential role for nuclear factor kappa B in preventing TNF-alpha-induced cell death in prostate cancer cells. J Urol 1999; 161: 674–679.

Gasparian AV, Yao YJ, Kowalczyk D, et al. The role of IKK in constitutive activation of NF-kappaB transcription factor in prostate carcinoma cells. J Cell Sci 2002; 115: 141–151.

Perlman H, Zhang X, Chen MW, Walsh K, Buttyan R. An elevated bax/bcl-2 ratio corresponds with the onset of prostate epithelial cell apoptosis. Cell Death Differ 1999; 6: 48–54.

Nakashima J, Tachibana M, Ueno M, Miyajima A, Baba S, Murai M. Association between tumor necrosis factor in serum and cachexia in patients with prostate cancer. Clin Cancer Res 1998; 4: 1743–1748.

Chaudhary KS, Abel PD, Lalani EN. Role of the Bcl-2 gene family in prostate cancer progression and its implications for therapeutic intervention. Environ Health Perspect 1999; 107: 49–57.

Scherr DS, Vaughan ED, Jr, Wei J, et al. BCL-2 and p53 expression in clinically localized prostate cancer predicts response to external beam radiotherapy. J Urol 1999; 162: 12–16.

Li P, Nicosia SV, Bai W. Antagonism between PTEN/ MMAC1/TEP-1 and androgen receptor in growth and apoptosis of prostatic cancer cells. J Biol Chem 2001; 276: 20444–20450.

Lapointe J, Fournier A, Richard V, Labrie C. Androgens down-regulate bcl-2 protooncogene expression in ZR-75-1 human breast cancer cells. Endocrinology 1999; 140: 416–421.

Chen CD, Sawyers CL. NF-kappa B activates prostate-specific antigen expression and is upregulated in androgenindependent prostate cancer. Mol Cell Biol 2002; 22: 2862–2870.

Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: A link between cancer genetics and chemotherapy. Cell 2002; 108: 153–164.

Baltaci S, Orhan D, Ozer G, Tolunay O, Gogous O. Bcl-2 proto-oncogene expression in low-and high-grade prostatic intraepithelial neoplasia. BJU Int 2000; 85: 155–159.

Huang A, Gandour-Edwards R, Rosenthal SA, Siders DB, Deitch AD, White RW. p53 and bcl-2 immunohistochemical alterations in prostate cancer treated with radiation therapy. Urology 1998; 51: 346–351.

Huang S, Pettaway CA, Uehara H, Bucana CD, Fidler IJ. Blockade of NF-kappaB activity in human prostate cancer cells is associated with suppression of angiogenesis, invasion, and metastasis. Oncogene 2001; 20: 4188–4197.

Dorai T, Olsson CA, Katz AE, Buttyan R. Development of a hammerhead ribozyme against bcl-2. I. Preliminary evaluation of a potential gene therapeutic agent for hormone-refractory human prostate cancer. Prostate 1997; 32: 246–258.

Miyake H, Tolcher A, Gleave ME. Antisense Bcl-2 oligodeoxynucleotides inhibit progression to androgen-independence after castration in the Shionogi tumor model. Cancer Res 1999; 59: 4030–4034.

Haldar S, Chintapalli J, Croce CM. Taxol induces bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res 1996; 56: 1253–1255.

Miayake H, Tolcher A, Gleave ME. Chemosensitization and delayed androgen-independent recurrence of prostate cancer with the use of antisense Bcl-2 oligodeoxynucleotides. J Natl Cancer Inst 2000; 92: 34–41.

Galderisi U, Cascino A, Giordano A. Antisense oligonucleotides as therapeutic agents. J Cell Physiol 1999; 181: 251–257.

Wang JL, Liu D, Zhang ZJ, et al. Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc Natl Acad Sci USA 2000; 97: 7124–7129.

Morris MJ, Tong WP, Cordon-Cardo C, et al. Phase I trial of BCL-2 antisense oligonucleotide (G3139) administered by continuous intravenous infusion in patients with advanced cancer. Clin Cancer Res 2002; 8: 679–683.

DiPaola RS, Rafi MM, Vyas V, et al. Phase I clinical and pharmacologic study of 13-cis-retinoic acid, interferon alfa, and paclitaxel in patients with prostate cancer and other advanced malignancies. J Clin Oncol 1999; 17: 2213–2218.

Friedland D, Cohen J, Miller R, Jr, et al. A phase II trial of docetaxel (Taxotere) in hormone-refractory prostate cancer: Correlation of antitumor effect to phosphorylation of Bcl-2. Semin Oncol 1999; 26: 19–23.

Shalev M, Thompson TC, Kadmon D, Ayala G, Kernen K, Miles BJ. Gene therapy for prostate cancer. Urology 2001; 57: 8–16.

Blutt SE, McDonnell TJ, Polek TC, Weigel NL. Calcitrioli-nduced apoptosis in LNCaP cells is blocked by overexpression of Bcl-2. Endocrinology 2000; 141: 10–17.

Szostak MJ, Kaur P, Amin P, Jacobs SC, Kyprianou N. Apoptosis and bcl-2 expression in prostate cancer: Significance in clinical outcome after brachytherapy. J Urol 2001; 165: 2126–2130.

Morris MJ, Scher HI. Novel strategies and therapeutics for the treatment of prostate carcinoma. Cancer 2000; 89: 1329–1348.

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