Oligoadenylate synthetase 1 (OAS1) expression in human breast and prostate cancer cases, and its regulation by sex steroid hormones

Cláudio Jorge Maia, Sandra Moreira Rocha, Sílvia Socorro, Fernando Schmitt, Cecília Reis Santos

Abstract


Oligoadenylate synthetase 1 (OAS1) is an interferon-induced protein characterised by its capacity to catalyse the synthesis of 2ʹ-5ʹ-linked oligomers of adenosine from adenosine triphosphate (2-5A). The 2-5A binds to a latent Ribonuclease L (RNase L), which subsequently dimerises into its active form and may play an important role in the control of cell growth, differentiation and apoptosis. Previously, our research group identified OAS1 as a differentially-expressed gene in breast and prostate cancer cell lines when compared to normal cells. This study evaluates: i) the expression of OAS1 in human breast and prostate cancer specimens; and ii) the effect of sex steroid hormones in regulating the expression of OAS1 in breast (MCF-7) and prostate (LNCaP) cancer cell lines. The obtained results showed that OAS1expression was down-regulated in human infiltrative ductal carcinoma of breast, adenocarcinoma of prostate, and benign prostate hyperplasia, both at mRNA and protein level. In addition, OAS1 expression was negatively correlated with the progression of breast and prostate cancer. With regards to the regulation of OAS1 gene, it was demonstrated that 17β-estradiol (E2) down-regulates OAS1 gene in MCF-7 cell lines, an effect that seems to be dependent on the activation of oestrogen receptor (ER). On the other hand, 5α‑dihydrotestosterone (DHT) treatment showed no effect on the expression of OAS1 in LNCaP cell lines. The lower levels of OAS1 in breast and prostate cancer cases indicated that the OAS1/RNaseL apoptotic pathway may be compromised in breast and prostate tumours. Moreover, the present findings suggested that this effect may be enhanced by oestrogen in ER-positive breast cancers.

Keywords


OAS1; oestrogen; androgen; breast cancer; prostate cancer

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References


Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015; 65(2): 87–108. doi: 10.3322/caac.21262.

Knudson AG Jr. Genetics of human cancer. Annu Rev Genet 1986; 20: 231–251. doi: 10.1146/annurev.ge.20. 120186.001311.

López-Otín C, Diamandis EP. Breast and prostate cancer: an analysis of common epidemiological, genetic, and biochemical features. Endocr Rev 1998; 19(4): 365–396.

Risbridger GP, Davis ID, Birrell SN, Tilley WD. Breast and prostate cancer: more similar than different. Nat Rev Cancer 2010; 10(3): 205–212. doi: 10.1038/nrc2795.

Rauh-Adelmann C, Lau KM, Sabeti N, Long JP, Mok SC, Ho SM. Altered expression of BRCA1, BRCA2, and a newly identified BRCA2 exon 12 deletion variant in malignant human ovarian, prostate, and breast cancer cell lines. Mol Carcinog 2000; 28(4): 236–246. doi: 10.1002/1098-2744 (200008)28:4<236::AID-MC6>3.0.CO;2-H.

Signoretti S, Montironi R, Manola J, Altimari A, Tam C, Bubley G, Balk S, Thomas G, Kaplan I, Hlatky L, Hanhnfeldt P, Kantoff P, Loda M. Her-2-neu expression and progression toward androgen independence in human prostate cancer. J Natl Cancer Inst 2000; 92(23): 1918–1925. doi: 10.1093/jnci/92.23.1918.

Sauter ER, Klein G, Wagner-Mann C, Diamandis EP. Prostate-specific antigen expression in nipple aspirate fluid is associated with advanced breast cancer. Cancer Detect Prev 2004; 28(1): 27–31. doi: 10.1016/j.cdp.2003.11.003

Rebouillat D, Marie I, Hovanessian AG. Molecular cloning and characterization of two related and interferon- induced 56-kDa and 30-kDa proteins highly similar to 2ʹ-5ʹ oligoadenylate synthetase. Eur J Biochem 1998; 257(2): 319–330. doi: 10.1046/j.1432-1327.1998.257031 9.x.

Rebouillat D, Hovanessian AG. The human 2ʹ,5ʹ- oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. J Interferon Cytokine Res 1999; 19(4): 295–308. doi: 10.1089/107999099313992.

Benech P, Mory Y, Revel M, Chebath J. Structure of two forms of the interferon-induced (2ʹ-5ʹ) oligo A synthetase of human cells based on cDNAs and gene sequences. EMBO J 1985; 4(9): 2249–2256.

Hovanessian AG, Brown RE, Kerr IM. Synthesis of low molecular weight inhibitor of protein synthesis with enzyme from interferon-treated cells. Nature 1977; 268(5620): 537–540. doi: 10.1038/268537a0.

Kerr IM, Brown RE. pppA2ʹp5ʹA2ʹp5ʹA: an inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells. Proc Natl Acad Sci USA 1978; 75(1): 256–260. doi: 10.1073/pnas.75.1.256.

Dong B, Silverman RH. 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J Biol Chem 1995; 270(8): 4133–4137. doi: 10.1074/jbc.270.8.4133.

Zhou A, Hassel BA, Silverman RH. Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell 1993; 72(5): 753–765. doi: 10.1016/0092-8674(93)90403-D.

Naik S, Paranjape JM, Silverman RH. RNase L dimeriza-tion in a mammalian two-hybrid system in response to 2ʹ,5ʹ-oligoadenylates. Nucleic Acids Res 1998; 26(6): 1522–1527. doi: 10.1093/nar/26.6.1522.

Domingo-Gil E, Esteban M. Role of mitochondria in apoptosis induced by the 2-5A system and mechanisms involved. Apoptosis 2006; 11(5): 725–738. doi: 10.1007/ s10495-006-5541-0.

Castelli JC, Hassel BA, Maran A, Paranjape J, Hewitt JA, Li XL, Hsu YT, Silverman RH, Youle RJ. The role of 2ʹ-5ʹ oligoadenylate-activated ribonuclease L in apoptosis. Cell Death Differ 1998; 5(4): 313–320. doi: 10.1038/sj.cdd.4400352.

Xiang Y, Wang Z, Murakami J, Plummer S, Klein EA, Carpten JD, Trent JM, Isaacs WB, Casey G, Silverman RH. Effects of RNase L mutations associated with prostate cancer on apoptosis induced by 2ʹ,5ʹ-oligoadenylates. Cancer Res 2003; 63(20): 6795–6801.

Malathi K, Paranjape JM, Ganapathi R, Silverman RH. HPC1/ RNASEL mediates apoptosis of prostate cancer cells treated with 2ʹ,5ʹ-oligoadenylates, topoisomerase I inhibitors, and tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res 2004; 64(24): 9144–9151. doi: 10.1158/0008-5472.CAN-04-2226.

Viano I, Silvestro L, Giubertoni M, Dianzani C, Genazzani E, Di Carlo F. Induction of 2ʹ-5ʹ oligoadenylate synthetase and activation of ribonuclease in tamoxifen treated human breast cancer cell lines. J Biol Regul Homeost Agents 1989; 3(4): 167–174.

Zhang Z, Duan L, Du X, Ma H, Park I, Lee C, Zhang J, Shi J. The proliferative effect of estradiol on human prostate stromal cells is mediated through activation of ERK. Prostate 2008; 68(5): 508–516. doi: 10.1002/pros.20722.

Un-no T, Hayami S, Nobata S, Sudoko H, Honma S, Fujita K, Ozono S. Neonatal exposure to estrogen in the Wistar rat decreases estrogen receptor-beta and induces epithelial proliferation of the prostate in the adult. Urol Int 2007; 79(4): 345–351. doi: 10.1159/000109721.

Smekens M, Dumont JE, Degeyter A, Galand P. Effect of estrogen administration on rat liver 2-5A synthetase activity. Biochim Biophys Acta 1986; 887(3): 341–344. doi: 10.1016/0167-4889(86)90164-3.

Silvestro L, Viano I, Giubertoni M, Compagnoni G, Dianzani C, Di Carlo F, Genazzani E. Induction of 2ʹ-5ʹ oligoadenylate synthetase by 17 beta-oestradiol in a human breast cancer cell line. Pharmacol Res 1989; 21(1): 99–100. doi: 10.1016/1043-6618(89)90132-1.

Maia CJ, Socorro S, Schmitt F, Santos CR. Characterization of oligoadenylate synthetase-1 expression in rat mammary gland and prostate: effects of 17 beta-estradiol on the regulation of OAS1g in both tissues. Mol Cell Biochem 2008; 314(1-2): 113–121. doi: 10.1007/s11010-008-9771-z.

Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991; 19(5): 403–410. doi: 10.1111/j.1365-2559.1991.tb00229.x.

McNeal JE, Gleason DF. Gleason’s classification of prostatic adenocarcinomas. Ann Pathol 1991; 11(3): 163– 168.

Schmitt FC, Bento MJ, Amendoeira I. Estimation of estrogen receptor content in fine-needle aspirates from breast cancer using the monoclonal antibody 1D5 and microwave oven processing: correlation with paraffin embedded and frozen sections determinations. Diagn Cytopathol 1995; 13(4): 347–351. doi: 10.1002/dc.2840130417.

Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29(9): e45. doi: 10.1093/nar/29.9.e45.

Mandal S, Abebe F, Chaudhary J. 2ʹ-5ʹ oligoadenylate synthetase 1 polymorphism is associated with prostate cancer. Cancer 2011; 117(24): 5509–5518. doi: 10.10 02/cncr.26219.

Webb P, Nguyen P, Valentine C, Lopez GN, Kwok GR, McInerney E, Katzenellenbogen BS, Enmark E, Gustafsson JA, Nilsson S, Kushner PJ. The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirements for receptor transactivation functions. Mol Endocrinol 1999; 13(10): 1672–1685. doi: 10.1210/mend.13.10.0357.

Safe S. Transcriptional activation of genes by 17 beta-estradiol through estrogen receptor-Sp1 interactions. Vitam Horm 2001; 62: 231–252. doi: 10.1016/S0083-67 29(01)62006-5.

Harnish DC, Scicchitano MS, Adelman SJ, Lyttle CR, Karathanasis SK, Karathanasis SK. The role of CBP in estrogen receptor cross-talk with nuclear factor-kappaB in HepG2 cells. Endocrinology 2000; 141(9): 3403–3411.

Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005; 21(13): 2933–2942. doi: 10.1093/bioinformatics/bti473.




DOI: http://dx.doi.org/10.30564/amor.v2i2.44

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