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Prostate Cancer
Volume 2016, Article ID 8108549, 9 pages
http://dx.doi.org/10.1155/2016/8108549
Review Article

Hydrogen Sulfide Signaling Axis as a Target for Prostate Cancer Therapeutics

1Cardiovascular and Metabolic Research Unit, Lakehead University, Thunder Bay, ON, P7B 5E1, Canada
2Department of Health Sciences, Lakehead University, Thunder Bay, ON, P7B 5E1, Canada
3Department of Chemistry and Biochemistry, Laurentian University, Sudbury, ON, P3E 2C6, Canada

Received 19 October 2015; Accepted 28 January 2016

Academic Editor: David Nanus

Copyright © 2016 Mingzhe Liu 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. K. Ono, T. Akaike, T. Sawa et al., “Redox chemistry and chemical biology of H2S, hydropersulfides, and derived species: implications of their possible biological activity and utility,” Free Radical Biology and Medicine, vol. 77, pp. 82–94, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Li and P. K. Moore, “An overview of the biological significance of endogenous gases: new roles for old molecules,” Biochemical Society Transactions, vol. 35, no. 5, pp. 1138–1141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. B. Olas, “Hydrogen sulfide in signaling pathways,” Clinica Chimica Acta, vol. 439, pp. 212–218, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Wang, “Gasotransmitters: growing pains and joys,” Trends in Biochemical Sciences, vol. 39, no. 5, pp. 227–232, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Wang, “Physiological implications of hydrogen sulfide: a whiff exploration that blossomed,” Physiological Reviews, vol. 92, no. 2, pp. 791–896, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Wang, “Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter?” The FASEB Journal, vol. 16, no. 13, pp. 1792–1798, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. J. L. Wallace and R. Wang, “Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter,” Nature Reviews Drug Discovery, vol. 14, no. 5, pp. 329–345, 2015. View at Publisher · View at Google Scholar
  8. Y. Zhao, T. D. Biggs, and M. Xian, “Hydrogen sulfide (H2S) releasing agents: chemistry and biological applications,” Chemical Communications, vol. 50, no. 80, pp. 11788–11805, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. A. K. Mustafa, M. M. Gadalla, N. Sen et al., “H2S signals through protein S-sulfhydration,” Science Signaling, vol. 2, no. 96, p. ra72, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. A. K. Mustafa, G. Sikka, S. K. Gazi et al., “Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels,” Circulation Research, vol. 109, no. 11, pp. 1259–1268, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Zhao, Y. Ju, S. Li, Z. Altaany, R. Wang, and G. Yang, “S-sulfhydration of MEK1 leads to PARP-1 activation and DNA damage repair,” EMBO Reports, vol. 15, no. 7, pp. 792–800, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Yang, K. Zhao, Y. Ju et al., “Hydrogen sulfide protects against cellular senescence via s-sulfhydration of keap1 and activation of Nrf2,” Antioxidants and Redox Signaling, vol. 18, no. 15, pp. 1906–1919, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Zhang, I. MacInkovic, N. O. Devarie-Baez et al., “Detection of protein S-sulfhydration by a tag-switch technique,” Angewandte Chemie—International Edition, vol. 53, no. 2, pp. 575–581, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Yang, “Protein S-sulfhydration as a major sources of H2S bioactivity,” Receptors & Clinical Investigation, vol. 1, no. 4, article e337, 2014. View at Publisher · View at Google Scholar
  15. A. di Masi and P. Ascenzi, “H2S: a ‘double face’ molecule in health and disease,” BioFactors, vol. 39, no. 2, pp. 186–196, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Guo, J.-W. Gai, Y. Wang, H.-F. Jin, J.-B. Du, and J. Jin, “Characterization of hydrogen sulfide and its synthases, cystathionine β-synthase and cystathionine γ-lyase, in human prostatic tissue and cells,” Urology, vol. 79, no. 2, pp. 483.e1–483.e5, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. J.-W. Gai, W. Wahafu, H. Guo et al., “Further evidence of endogenous hydrogen sulphide as a mediator of relaxation in human and rat bladder,” Asian Journal of Andrology, vol. 15, no. 5, pp. 692–696, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Zhao, S. Li, L. Wu, C. Lai, and G. Yang, “Hydrogen sulfide represses androgen receptor transactivation by targeting at the second zinc finger module,” Journal of Biological Chemistry, vol. 289, no. 30, pp. 20824–20835, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Pei, B. Wu, Q. Cao, L. Wu, and G. Yang, “Hydrogen sulfide mediates the anti-survival effect of sulforaphane on human prostate cancer cells,” Toxicology and Applied Pharmacology, vol. 257, no. 3, pp. 420–428, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. P.-H. Lin, W. Aronson, and S. J. Freedland, “Nutrition, dietary interventions and prostate cancer: the latest evidence,” BMC Medicine, vol. 13, article 3, 2015. View at Publisher · View at Google Scholar
  21. E. Stone, “Prostatic intraepithelial neoplasia: will it help doctors pinpoint early prostate cancer?” Journal of the National Cancer Institute, vol. 88, no. 15, pp. 1023–1024, 1996. View at Publisher · View at Google Scholar · View at Scopus
  22. L. B. Valenca, C. J. Sweeney, and M. M. Pomerantz, “Sequencing current therapies in the treatment of metastatic prostate cancer,” Cancer Treatment Reviews, vol. 41, no. 4, pp. 332–340, 2015. View at Publisher · View at Google Scholar
  23. S. Stabler, T. Koyama, Z. Zhao et al., “Serum methionine metabolites are risk factors for metastatic prostate cancer progression,” PLoS ONE, vol. 6, no. 8, Article ID e22486, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. J. I. Toohey, “Sulfur signaling: is the agent sulfide or sulfane?” Analytical Biochemistry, vol. 413, no. 1, pp. 1–7, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. B. A. Vartapetov, N. V. Novikova, and G. M. Trandofilova, “Gonadal dysfunction and the thiol compound metabolism in the testes and prostate,” Zhurnal Eksperimental'noi i Klinicheskoi Meditsiny, vol. 17, no. 2, pp. 9–15, 1977. View at Google Scholar
  26. G. Chwatko, E. Forma, J. Wilkosz et al., “Thiosulfate in urine as a facilitator in the diagnosis of prostate cancer for patients with prostate-specific antigen less or equal 10 ng/mL,” Clinical Chemistry and Laboratory Medicine, vol. 51, no. 9, pp. 1825–1831, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Kimura, K. H. Franke, C. Steinhoff et al., “Methyl group metabolism gene polymorphisms and susceptibility to prostatic carcinoma,” Prostate, vol. 45, no. 3, pp. 225–231, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. W. Zhang, A. Braun, Z. Bauman, H. Olteanu, P. Madzelan, and R. Banerjee, “Expression profiling of homocysteine junction enzymes in the NCI60 panel of human cancer cell lines,” Cancer Research, vol. 65, no. 4, pp. 1554–1560, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. F. Al-Awadi, M. Yang, Y. Tan, Q. Han, S. Li, and R. M. Hoffman, “Human tumor growth in nude mice is associated with decreased plasma cysteine and homocysteine,” Anticancer Research, vol. 28, no. 5, pp. 2541–2544, 2008. View at Google Scholar · View at Scopus
  30. C. Stephan, K. Jung, K. Miller, and B. Ralla, “New biomarkers in serum and urine for detection of prostate cancer,” Aktuelle Urologie, vol. 46, no. 2, pp. 129–143, 2015. View at Publisher · View at Google Scholar
  31. M. R. Hellmich, C. Coletta, C. Chao, and C. Szabo, “The therapeutic potential of cystathionine β-synthetase/hydrogen sulfide inhibition in cancer,” Antioxidants and Redox Signaling, vol. 22, no. 5, pp. 424–448, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Kashfi, “Anti-cancer activity of new designer hydrogen sulfide-donating hybrids,” Antioxidants and Redox Signaling, vol. 20, no. 5, pp. 831–846, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. S. E. Lupold and R. Rodriguez, “Disulfide-constrained peptides that bind to the extracellular portion of the prostate-specific membrane antigen,” Molecular Cancer Therapeutics, vol. 3, no. 5, pp. 597–603, 2004. View at Google Scholar · View at Scopus
  34. S. M. Collin, “Folate and B12 in Prostate Cancer,” Advances in Clinical Chemistry, vol. 60, pp. 1–63, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Prasad, N. Kalra, and Y. Shukla, “Modulatory effects of diallyl sulfide against testosterone-induced oxidative stress in Swiss albino mice,” Asian Journal of Andrology, vol. 8, no. 6, pp. 719–723, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. A. I. Bhuiyan, V. T. Papajani, M. Paci, and S. Melino, “Glutathione-Garlic sulfur conjugates: slow hydrogen sulfide releasing agents for therapeutic applications,” Molecules, vol. 20, no. 1, pp. 1731–1750, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. K. L. Flannigan, T. A. Agbor, J.-P. Motta et al., “Proresolution effects of hydrogen sulfide during colitis are mediated through hypoxia-inducible factor-1α,” The FASEB Journal, vol. 29, no. 4, pp. 1591–1602, 2015. View at Publisher · View at Google Scholar
  38. D. Liang, C. Wang, R. Tocmo, H. Wu, L. Deng, and D. Huang, “Hydrogen sulphide (H2S) releasing capacity of essential oils isolated from organosulphur rich fruits and vegetables,” Journal of Functional Foods, vol. 14, pp. 634–640, 2015. View at Publisher · View at Google Scholar
  39. K. Ried and P. Fakler, “Potential of garlic (Allium sativum) in lowering high blood pressure: mechanisms of action and clinical relevance,” Integrated Blood Pressure Control, vol. 7, pp. 71–82, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. G. A. Benavides, G. L. Squadrito, R. W. Mills et al., “Hydrogen sulfide mediates the vasoactivity of garlic,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 46, pp. 17977–17982, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. M. H. Traka, A. Melchini, and R. F. Mithen, “Sulforaphane and prostate cancer interception,” Drug Discovery Today, vol. 19, no. 9, pp. 1488–1492, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Melchini, M. H. Traka, S. Catania et al., “Antiproliferative activity of the dietary isothiocyanate erucin, a bioactive compound from cruciferous vegetables, on human prostate cancer cells,” Nutrition and Cancer, vol. 65, no. 1, pp. 132–138, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Duan, Y. Li, L. Chen et al., “Sulfur inhibits the growth of androgen-independent prostate cancer in vivo,” Oncology Letters, vol. 9, no. 1, pp. 437–441, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Z. Amirov, V. T. Karpukhin, and N. I. Nesterov, “Changes in the state of the blood supply to the prostate gland in patients with chronic prostatitis under the influence of treatment with hydrogen sulfide water (according to rheovasographic findings),” Voprosy Kurortologii, Fizioterapii, i Lechebnoi Fizicheskoi Kultury, no. 1, pp. 69–72, 1976. View at Google Scholar · View at Scopus
  45. N. S. Nagaraj, K. R. Anilakumar, and O. V. Singh, “Diallyl disulfide causes caspase-dependent apoptosis in human cancer cells through a Bax-triggered mitochondrial pathway,” Journal of Nutritional Biochemistry, vol. 21, no. 5, pp. 405–412, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Y. Shin, G.-Y. Kim, J.-I. Kim et al., “Anti-invasive activity of diallyl disulfide through tightening of tight junctions and inhibition of matrix metalloproteinase activities in LNCaP prostate cancer cells,” Toxicology in Vitro, vol. 24, no. 6, pp. 1569–1576, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Arunkumar, M. R. Vijayababu, N. Srinivasan, M. M. Aruldhas, and J. Arunakaran, “Garlic compound, fiallyl disulfide induces cell cycle arrest in prostate cancer cell line PC-3,” Molecular and Cellular Biochemistry, vol. 288, no. 1, pp. 107–113, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Arunkumar, M. R. Vijayababu, N. Gunadharini, G. Krishnamoorthy, and J. Arunakaran, “Induction of apoptosis and histone hyperacetylation by diallyl disulfide in prostate cancer cell line PC-3,” Cancer Letters, vol. 251, no. 1, pp. 59–67, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Arunkumar, M. R. Vijayababu, P. Venkataraman, K. Senthilkumar, and J. Arunakaran, “Chemoprevention of rat prostate carcinogenesis by diallyl disulfide, an organosulfur compound of garlic,” Biological and Pharmaceutical Bulletin, vol. 29, no. 2, pp. 375–379, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Chen, B. Li, X. Zhao et al., “Effect of diallyl trisulfide derivatives on the induction of apoptosis in human prostate cancer PC-3 cells,” Molecular and Cellular Biochemistry, vol. 363, no. 1-2, pp. 75–84, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. D. N. Gunadharini, A. Arunkumar, G. Krishnamoorthy et al., “Antiproliferative effect of diallyl disulfide (DADS) on prostate cancer cell line LNCaP,” Cell Biochemistry and Function, vol. 24, no. 5, pp. 407–412, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Arunkumar, G. Sharmila, P. Elumalai et al., “Effect of diallyl disulfide on insulin-like growth factor signaling molecules involved in cell survival and proliferation of human prostate cancer cells in vitro and in silico approach through docking analysis,” Phytomedicine, vol. 19, no. 10, pp. 912–923, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Gayathri, D. N. Gunadharini, A. Arunkumar et al., “Effects of diallyl disulfide (DADS) on expression of apoptosis associated proteins in androgen independent human prostate cancer cells (PC-3),” Molecular and Cellular Biochemistry, vol. 320, no. 1-2, pp. 197–203, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Borkowska, N. Knap, and J. Antosiewicz, “Diallyl trisulfide is more cytotoxic to prostate cancer cells PC-3 than to noncancerous epithelial cell line PNT1A: a possible role of p66Shc signaling axis,” Nutrition and Cancer, vol. 65, no. 5, pp. 711–717, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Borkowska, A. Sielicka-Dudzin, A. Herman-Antosiewicz et al., “Diallyl trisulfide-induced prostate cancer cell death is associated with Akt/PKB dephosphorylation mediated by P-p66shc,” European Journal of Nutrition, vol. 51, no. 7, pp. 817–825, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Xiao, S. Choi, D. E. Johnson et al., “Diallyl trisulfide-induced apoptosis in human prostate cancer cells involves c-Jun N-terminal kinase and extracellular-signal regulated kinase-mediated phosphorylation of Bcl-2,” Oncogene, vol. 23, no. 33, pp. 5594–5606, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Xiao, A. Herman-Antosiewicz, J. Antosiewicz et al., “Diallyl trisulfide-induced G2-M phase cell cycle arrest in human prostate cancer cells is caused by reactive oxygen species-dependent destruction and hyperphosphorylation of Cdc25C,” Oncogene, vol. 24, no. 41, pp. 6256–6268, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Antosiewicz, A. Herman-Antosiewicz, S. W. Marynowski, and S. V. Singh, “c-Jun NH2-terminal kinase signaling axis regulates diallyl trisulfide-induced generation of reactive oxygen species and cell cycle arrest in human prostate cancer cells,” Cancer Research, vol. 66, no. 10, pp. 5379–5386, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. Y.-A. Kim, D. Xiao, H. Xiao et al., “Mitochondria-mediated apoptosis by diallyl trisulfide in human prostate cancer cells is associated with generation of reactive oxygen species and regulated by Bax/Bak,” Molecular Cancer Therapeutics, vol. 6, no. 5, pp. 1599–1609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Sielicka-Dudzin, A. Borkowska, A. Herman-Antosiewicz et al., “Impact of JNK1, JNK2, and ligase Itch on reactive oxygen species formation and survival of prostate cancer cells treated with diallyl trisulfide,” European Journal of Nutrition, vol. 51, no. 5, pp. 573–581, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Herman-Antosiewicz, Y.-A. Kim, S.-H. Kim, D. Xiao, and S. V. Singh, “Diallyl trisulfide-induced G2/M phase cell cycle arrest in DU145 cells is associated with delayed nuclear translocation of cyclin-dependent kinase 1,” Pharmaceutical Research, vol. 27, no. 6, pp. 1072–1079, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. W.-C. Chen, S.-S. Hsu, C.-T. Chou et al., “Effect of diallyl disulfide on Ca2+ movement and viability in PC3 human prostate cancer cells,” Toxicology in Vitro, vol. 25, no. 3, pp. 636–643, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. S. V. Singh, A. A. Powolny, S. D. Stan et al., “Garlic constituent diallyl trisulfide prevents development of poorly differentiated prostate cancer and pulmonary metastasis multiplicity in TRAMP mice,” Cancer Research, vol. 68, no. 22, pp. 9503–9511, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Xiao, K. L. Lew, Y.-A. Kim et al., “Diallyl trisulfide suppresses growth of PC-3 human prostate cancer xenograft in vivo in association with Bax and Bak induction,” Clinical Cancer Research, vol. 12, no. 22, pp. 6836–6843, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Shankar, Q. Chen, S. Ganapathy, K. P. Singh, and R. K. Srivastava, “Diallyl trisulfide increases the effectiveness of TRAIL and inhibits prostate cancer growth in an orthotopic model: molecular mechanisms,” Molecular Cancer Therapeutics, vol. 7, no. 8, pp. 2328–2338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. S. V. Singh, R. Warin, D. Xiao et al., “Sulforaphane inhibits prostate carcinogenesis and pulmonary metastasis in TRAMP mice in association with increased cytotoxicity of natural killer cells,” Cancer Research, vol. 69, no. 5, pp. 2117–2125, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. J. W. Chiao, F.-L. Chung, R. Kancherla, T. Ahmed, A. Mittelman, and C. C. Conaway, “Sulforaphane and its metabolite mediate growth arrest and apoptosis in human prostate cancer cells,” International journal of oncology, vol. 20, no. 3, pp. 631–636, 2002. View at Google Scholar · View at Scopus
  68. J. J. Alumkal, R. Slottke, J. Schwartzman et al., “A phase II study of sulforaphane-rich broccoli sprout extracts in men with recurrent prostate cancer,” Investigational New Drugs, vol. 33, pp. 480–489, 2015. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Prudova, M. Albin, Z. Bauman, A. Lin, V. Vitvitsky, and R. Banerjee, “Testosterone regulation of homocysteine metabolism modulates redox status in human prostate cancer cells,” Antioxidants and Redox Signaling, vol. 9, no. 11, pp. 1875–1881, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. S. D. Stan and S. V. Singh, “Transcriptional repression and inhibition of nuclear translocation of androgen receptor by diallyl trisulfide in human prostate cancer cells,” Clinical Cancer Research, vol. 15, no. 15, pp. 4895–4903, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Gibbs, J. Schwartzman, V. Deng, and J. Alumkal, “Sulforaphane destabilizes the androgen receptor in prostate cancer cells by inactivating histone deacetylase 6,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 39, pp. 16663–16668, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. M. C. Myzak, K. Hardin, R. Wang, R. H. Dashwood, and E. Ho, “Sulforaphane inhibits histone deacetylase activity in BPH-1, LnCaP and PC-3 prostate epithelial cells,” Carcinogenesis, vol. 27, no. 4, pp. 811–819, 2006. View at Publisher · View at Google Scholar · View at Scopus