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BioMed Research International
Volume 2018, Article ID 1439712, 10 pages
https://doi.org/10.1155/2018/1439712
Research Article

In Vivo Study of the Effects of ER on Apoptosis and Proliferation of Hormone-Independent Prostate Cancer Cell Lines PC-3M

1School of Nursing, Jilin University, 965 Xinjiang Street, Changchun, Jilin 130020, China
2Basic Medical School, Jilin University, 126 Xinmin Street, Changchun, Jilin 130020, China

Correspondence should be addressed to Feng Li; nc.ude.ulj@ilf

Received 2 December 2017; Revised 9 April 2018; Accepted 19 April 2018; Published 19 June 2018

Academic Editor: Bo Zhao

Copyright © 2018 Changli Zhou et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. Y. Chang and G. S. Prins, “Estrogen receptor-β: Implications for the prostate gland,” The Prostate, vol. 40, no. 2, pp. 115–124, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. S. M. Ho, “Estrogens and anti-estrogens: Key mediators of prostate carcinogenesis and new therapeutic candidates,” Journal of Cellular Biochemistry, vol. 91, no. 3, pp. 491–503, 2004. View at Publisher · View at Google Scholar
  3. G. G. Kuiper, E. Enmark, M. Pelto-Huikko, S. Nilsson, and J.-A. Gustafsson, “Cloning of a novel receptor expressed in rat prostate and ovary,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 93, no. 12, pp. 5925–5930, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Mosselman, J. Polman, and R. Dijkema, “ERβ: Identification and characterization of a novel human estrogen receptor,” FEBS Letters, vol. 392, no. 1, pp. 49–53, 1996. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Pylkkanen, S. Makela, and R. Santti, “Animal models for the preneoplastic lesions of the prostate,” European Urology, vol. 30, no. 2, pp. 243–248, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. C. M. Armstrong, K. F. Allred, B. R. Weeks, R. S. Chapkin, and C. D. Allred, “Estradiol Has Differential Effects on Acute Colonic Inflammation in the Presence and Absence of Estrogen Receptor β Expression,” Digestive Diseases and Sciences, vol. 62, no. 8, pp. 1977–1984, 2017. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Bonkhoff, T. Fixemer, I. Hunsicker, and K. Remberger, “Estrogen receptor expression in prostate cancer and premalignant prostatic lesions,” The American Journal of Pathology, vol. 155, no. 2, pp. 641–647, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. I. Leav, K. Lau, J. Y. Adams et al., “Comparative Studies of the Estrogen Receptors β and α and the Androgen Receptor in Normal Human Prostate Glands, Dysplasia, and in Primary and Metastatic Carcinoma,” The American Journal of Pathology, vol. 159, no. 1, pp. 79–92, 2001. View at Publisher · View at Google Scholar
  9. T. Fixemer, K. Remberger, and H. Bonkhoff, “Differential expression of the estrogen receptor beta (ERβ) in human prostate tissue, premalignant changes, and in primary, metastatic, and recurrent prostatic adenocarcinoma,” The Prostate, vol. 54, no. 2, pp. 79–87, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Bonkhoff and K. Remberger, “Differentiation pathways and histogenetic aspects of normal and abnormal prostatic growth: A stem cell model,” The Prostate, vol. 28, no. 2, pp. 98–106, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Asgari and A. Morakabati, “Estrogen receptor beta expression in prostate adenocarcinoma,” Diagnostic Pathology, vol. 6, no. 1, article no. 61, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. L. G. Horvath, S. M. Henshall, C. S. Lee et al., “Frequent Loss of Estrogen Receptor-ß Expression in prostate Cancer,” Cancer Resesrch, vol. 61, no. 15, pp. 5331–5335, 2001. View at Google Scholar
  13. A. Latil, I. Bieche, D. Vidaud et al., “Evaluation of androgen, estrogen (ERα and ERβ), and progesterone receptor expression in human prostate cancer by real-time quantitative reverse transcription-polymerase chain reaction assays,” Cancer Research, vol. 61, no. 5, pp. 1919–1926, 2001. View at Google Scholar · View at Scopus
  14. D. Pasquali, S. Staibano, and D. Prezioso, “Estrogen receptor beta expression in human prostate tissue,” Mol Cell Endocrinol, vol. 178, no. 1-2, pp. 47–50, 2001. View at Publisher · View at Google Scholar
  15. G. Poelzl, Y. Kasai, N. Mochizuki, P. W. Shaul, M. Brown, and M. E. Mendelsohn, “Specific association of estrogen receptor beta with the cell cycle spindle assembly checkpoint protein, MAD2,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 97, no. 6, pp. 2836–2839, 2000. View at Publisher · View at Google Scholar
  16. S. Signoretti and M. Loda, “Estrogen receptor beta in prostate cancer: brake pedal or accelerator?” The American Journal of Pathology, vol. 159, no. 1, pp. 13–16, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Weihua, R. Lathe, M. Warner, and J. Gustafsson, “An endocrine pathway in the prostate, ER , AR, 5 -androstane-3 ,17 -diol, and CYP7B1, regulates prostate growth,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 99, no. 21, pp. 13589–13594, 2002. View at Publisher · View at Google Scholar
  18. J. H. Krege, J. B. Hodgin, J. F. Couse et al., “Generation and reproductive phenotypes of mice lacking estrogen receptor,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 95, no. 26, pp. 15677–15682, 1998. View at Publisher · View at Google Scholar
  19. S. J. McPherson, S. J. Ellem, and G. P. Risbridger, “Estrogen-regulated development and differentiation of the prostate,” Differentiation, vol. 76, no. 6, pp. 660–670, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. O. Imamov, A. Morani, G. J. Shim et al., “Estrogen receptor beta regulates epithelial cellular differentiation in the mouse ventral prostate,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 21, p. 8298, 2006. View at Google Scholar
  21. J. Bektic, A. P. Berger, K. Pfeil, G. Dobler, G. Bartsch, and H. Klocker, “Androgen Receptor Regulation by Physiological Concentrations of the Isoflavonoid Genistein in Androgen-Dependent LNCaP Cells Is Mediated by Estrogen Receptor β,” European Urology, vol. 45, no. 2, pp. 245–251, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. I. Y. Kim, D. H. Seong, B.-C. Kim et al., “Raloxifene, a selective estrogen receptor modulator, induces apoptosis in androgen-responsive human prostate cancer cell line LNCaP through an androgen-independent pathway,” Cancer Research, vol. 62, no. 13, pp. 3649–3653, 2002. View at Google Scholar · View at Scopus
  23. R. Xiang, H. N. Lode, T.-H. Chao et al., “An autologous oral DNA vaccine protects against murine melanoma,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 97, no. 10, pp. 5492–5497, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. S. O. Lee, W. Lou, K. M. Qureshi, F. Mehraein-Ghomi, D. L. Trump, and A. C. Gao, “RNA interference targeting Stat3 inhibits growth and induces apoptosis of human prostate cancer cells,” The Prostate, vol. 60, no. 4, pp. 303–309, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Zhang, K. Wen, J. Shen et al., “Characterization of immune responses following intranasal immunization with the Mycobacterium bovis CFP-10 protein expressed by attenuated salmonella typhimurium,” Scandinavian Journal of Immunology, vol. 72, no. 4, pp. 277–283, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Agarwala and R. E. Kalil, “Axotomy-induced neuronal death and reactive astrogliosis in the lateral geniculate nucleus following a lesion of the visual cortex in the rat,” Journal of Comparative Neurology, vol. 392, no. 2, pp. 252–263, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Zhang, L. Gao, Y. Li et al., “Effects of plasmid-based Stat3-specific short hairpin RNA and GRIM-19 on PC-3M tumor cell growth,” Clinical Cancer Research, vol. 14, no. 2, pp. 559–568, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Cancel-Tassin and O. Cussenot, “Genetic susceptibility to prostate cancer,” BJU International, vol. 96, no. 9, pp. 1380–1385, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Jemal, R. C. Tiwari, and T. Murray, “Cancer statistics, 2004,” CA: A Cancer Journal for Clinicians, vol. 54, no. 1, pp. 8–29, 2004. View at Publisher · View at Google Scholar
  30. C. L. Amling, C. J. Kane, R. H. Riffenburgh et al., “Relationship between obesity and race in predicting adverse pathologic variables in patients undergoing radical prostatectomy.,” Urology, vol. 58, no. 5, pp. 723–728, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. K. E. Knudsen and H. I. Scher, “Starving the addiction: New opportunities for durable suppression of AR signaling in prostate cancer,” Clinical Cancer Research, vol. 15, no. 15, pp. 4792–4798, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. Z. Weihua, M. Warner, and J.-Å. Gustafsson, “Estrogen receptor beta in the prostate,” Molecular and Cellular Endocrinology, vol. 193, no. 1-2, pp. 1–5, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. L. G. Horvath, S. M. Henshall, C. S. Lee et al., “Frequent loss of estrogen receptor-beta expression in prostate cancer,” Cancer Res, vol. 61, no. 14, pp. 5331–5335, 2001. View at Google Scholar
  34. W. A. Ricke, S. J. McPherson, J. J. Bianco, G. R. Cunha, Y. Wang, and G. P. Risbridger, “Prostatic hormonal carcinogenesis is mediated by in situ estrogen production and estrogen receptor alpha signaling,” The FASEB Journal, vol. 22, no. 5, pp. 1512–1520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. T. V. Agthoven, A. M. Sieuwerts, M. E. Meijer-van Gelder et al., “Relevance of breast cancer antiestrogen resistance genes in human breast cancer progression and tamoxifen resistance,” Journal of Clinical Oncology, vol. 27, no. 4, pp. 542–549, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Lazennec, D. Bresson, A. Lucas, C. Chauveau, and F. Vignon, “ERβ inhibits proliferation and invasion of breast cancer cells,” Endocrinology, vol. 142, no. 9, pp. 4120–4130, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Paruthiyil, H. Parmar, V. Kerekatte, G. R. Cunha, G. L. Firestone, and D. C. Leitmant, “Estrogen receptor β inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest,” Cancer Research, vol. 64, no. 1, pp. 423–428, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Iwao, Y. Miyoshi, C. Egawa, N. Ikeda, and S. Noguchi, “Quantitative analysis of estrogen receptor-β mRNA and its variants in human breast cancers,” International Journal of Cancer, vol. 88, no. 5, pp. 733–736, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. K. B. Low, M. Ittensohn, T. Le et al., “Lipid a mutant Salmonella with suppressed virulence and TNFα induction retain tumor-targeting in vivo,” Nature Biotechnology, vol. 17, no. 1, pp. 37–41, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. J. M. Pawelek, K. B. Low, and D. Bermudes, “Tumor-targeted Salmonella as a novel anticancer vector,” Cancer Research, vol. 57, no. 20, pp. 4537–4544, 1997. View at Google Scholar · View at Scopus
  41. L. Yuhua, G. Kunyuan, C. Hui et al., “Oral cytokine gene therapy against murine tumor using attenuated Salmonella typhimurium,” International Journal of Cancer, vol. 94, no. 3, pp. 438–443, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Zhao, M. Yang, H. Ma et al., “Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice,” Cancer Research, vol. 66, no. 15, pp. 7647–7652, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Dietrich, C. Andersen, R. Rappuoli, T. M. Doherty, C. G. Jensen, and P. Andersen, “Mucosal Administration of Ag85B-ESAT-6 Protects against Infection with Mycobacterium tuberculosis and Boosts Prior Bacillus Calmette-Guerin Immunity,” The Journal of Immunology, vol. 177, no. 9, pp. 6353–6360, 2006. View at Publisher · View at Google Scholar
  44. L. Chen, J. Wang, A. Zganiacz, and Z. Xing, “Single Intranasal Mucosal Mycobacterium bovis BCG Vaccination Confers Improved Protection Compared to Subcutaneous Vaccination against Pulmonary Tuberculosis,” Infection and Immunity, vol. 72, no. 1, pp. 238–246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Zhang, L. Gao, L. Zhao et al., “Intratumoral delivery and suppression of prostate tumor growth by attenuated Salmonella enterica serovar typhimurium carrying plasmid-based small interfering RNAs,” Cancer Research, vol. 67, no. 12, pp. 5859–5864, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. S. I. Miller, A. M. Kukral, and J. J. Mekalanos, “A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 86, no. 13, pp. 5054–5058, 1989. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Angelakopoulos and E. L. Hohmann, “Pilot study of phoP/phoQ-deleted Salmonella enterica serovar typhimurium expressing Helicobacter priori urease in adult volunteers,” Infection and Immunity, vol. 68, no. 4, pp. 2135–2141, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. X.-G. Qin, Z. Hua, W. Shuang, Y.-H. Wang, and Y.-D. Cui, “Effects of matrine on HepG2 cell proliferation and expression of tumor relevant proteins in vitro,” Pharmaceutical Biology, vol. 48, no. 3, pp. 275–281, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Bardin, N. Boulle, G. Lazennec, F. Vignon, and P. Pujol, “Loss of ERβ expression as a common step in estrogen-dependent tumor progression,” Endocrine-Related Cancer, vol. 11, no. 3, pp. 537–551, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. R. A. Jarred, S. J. McPherson, J. J. Bianco, J. F. Couse, K. S. Korach, and G. P. Risbridger, “Prostate phenotypes in estrogen-modulated transgenic mice,” Trends in Endocrinology & Metabolism, vol. 13, no. 4, pp. 163–168, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. S. R. Datta, A. Brunet, and M. E. Greenberg, “Cellular survival: a play in three akts,” Genes & Development, vol. 13, no. 22, pp. 2905–2927, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. R. A. Segal and M. E. Greenberg, “Intracellular signaling pathways activated by neurotrophic factors,” Annual Review of Neuroscience, vol. 19, pp. 463–489, 1996. View at Publisher · View at Google Scholar · View at Scopus
  53. K. M. Nicholson and N. G. Anderson, “The protein kinase B/Akt signalling pathway in human malignancy,” Cellular Signalling, vol. 14, no. 5, pp. 381–395, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. S. R. Datta, H. Dudek, T. Xu et al., “Akt phosphorylation of BAD couples survival signals to the cell- intrinsic death machinery,” Cell, vol. 91, no. 2, pp. 231–241, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Lindberg, L. A. Helguero, Y. Omoto, J. Gustafsson, and L. Haldosén, “Estrogen receptor β represses Akt signaling in breast cancer cells via downregulation of HER2/HER3 and upregulation of PTEN: implications for tamoxifen sensitivity,” Breast Cancer Research, vol. 13, no. 2, article R43, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Jun, X. Dan, L. Jin-Dan, and P. Wang, “Exogenous p27KIP1 expression induces anti-tumour effects and inhibits the EGFR/PI3K/Akt signalling pathway in PC3 cells,” Asian Journal of Andrology, vol. 11, no. 6, pp. 669–677, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. O. Al-Bazz, J. C. E. Underwood, B. L. Brown, and P. R. M. Dobson, “Prognostic significance of Akt, phospho-Akt and BAD expression in primary breast cancer,” European Journal of Cancer, vol. 45, no. 4, pp. 694–704, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. B. S. Finlin, C.-L. Gau, G. A. Murphy et al., “RERG Is a Novel ras-related, Estrogen-regulated and Growth-inhibitory Gene in Breast Cancer,” The Journal of Biological Chemistry, vol. 276, no. 45, pp. 42259–42267, 2001. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Guo and G. E. Sonenshein, “Forkhead box transcription factor FOXO3a regulates estrogen receptor alpha expression and is repressed by the Her-2/neu/phosphatidylinositol 3-kinase/Akt signaling pathway,” Molecular and Cellular Biology, vol. 24, no. 19, pp. 8681–8690, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. V. Kirkin, S. Joos, and M. Zörnig, “The role of Bcl-2 family members in tumorigenesis,” Biochimica et Biophysica Acta (BBA)—Molecular Cell Research, vol. 1644, no. 2-3, pp. 229–249, 2004. View at Publisher · View at Google Scholar
  61. M. O. Hengartner, “The biochemistry of apoptosis,” Nature, vol. 407, no. 6805, pp. 770–776, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Enari, H. Sakahira, H. Yokoyama, K. Okawa, A. Iwamatsu, and S. Nagata, “A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD,” Nature, vol. 391, no. 6662, pp. 43–50, 1998. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Chen, R. J. Lin, R. Schiltz et al., “Nuclear Receptor Coactivator ACTR Is a Novel Histone Acetyltransferase and Forms a Multimeric Activation Complex with P/CAF and CBP/p300,” Cell, vol. 90, no. 3, pp. 569–580, 1997. View at Publisher · View at Google Scholar