METASTASIS REGULATION IN PROSTATE CANCER: THE POSSIBLE ROLE OF IP3- AND CADPR-MEDIATED Ca2+ SIGNALING
Main Article Content
Keywords
Prostate cancer, Oxidative imbalance, Antioxidant barrier, Ca2+ influx pathways, Metastasis
Abstract
Background: Prostate cancer (PCa) is the second most prevalent cancer among males that are prone to the metastasis. The oxidative imbalance and Ca2+ influx are metastasis triggers and also crucial to understanding the pathogenesis of PCa. This study aimed to investigate the reciprocal relationship between Ca2+ up-regulation and oxidative stress by evaluation of the inositol-three-phosphate (IP3)- and cADPR-mediated Ca2+ influx in PCa tissue and marginal control. The possible correlation between Ca2+ up-regulation and matrix metalloproteinase 9 (MMP-9)/CD82 expressions which involve in tissue remodeling, cell proliferation and invasion was also evaluated.
References
1. Zhang Z, Zhanghuang C, Wang J, Mi T, Liu J, Tian X, et al. A Web-Based Prediction Model for Cancer-Specific Survival of Elderly Patients Undergoing Surgery With Prostate Cancer: A Population-Based Study. Front Public Health. 2022;10:935521.
2. Xing P, Chen L, Yang Q, Song T, Ma C, Grimm R, et al. Differentiating prostate cancer from benign prostatic hyperplasia using whole-lesion histogram and texture analysis of diffusion- and T2-weighted imaging. Cancer Imaging. 2021;21(1):54.
3. Jones J, Feger J, Bell D, et al. Gleason score. Reference article, Radiopaedia.org (Accessed on 11 Mar 2023) https://doi.org/10.53347/rID-9054.
4. Rawla P. Epidemiology of Prostate Cancer. World J Oncol. 2019;10(2):63-89.
5. Brawer MK. Prostatic intraepithelial neoplasia: an overview. Rev Urol. 2005;7 Suppl 3(Suppl 3):S11-8.
6. Minciullo PL, Inferrera A, Navarra M, Calapai G, Magno C, Gangemi S. Oxidative Stress in Benign Prostatic Hyperplasia: A Systematic Review. Urol Int 2015;94:249-254. doi: 10.1159/000366210
7. Srinivas US, Tan BWQ, Vellayappan BA, Jeyasekharan AD. ROS and the DNA damage response in cancer. Redox Biol. 2019;25:101084.
8. Rossi A, Pizzo P, Filadi R. Calcium, mitochondria and cell metabolism: A functional triangle in bioenergetics. Biochimica et biophysica acta Molecular cell research. 2019;1866(7):1068-78
9. Wei W, Graeff R, Yue J. Roles and mechanisms of the CD38/cyclic adenosine diphosphate ribose/Ca(2+) signaling pathway. World J Biol Chem. 2014 Feb 26;5(1):58-67. doi: 10.4331/wjbc.v5.i1.58. PMID: 24600514; PMCID: PMC3942542.
10. Courjaret, R., Machaca, K. Mid-range Ca2+ signalling mediated by functional coupling between store-operated Ca2+ entry and IP3-dependent Ca2+ release. Nat Commun 5, 3916 (2014). https://doi.org/10.1038/ncomms4916.
11. Ardura JA, Álvarez-Carrión L, Gutiérrez-Rojas I, Alonso V. Role of Calcium Signaling in Prostate Cancer Progression: Effects on Cancer Hallmarks and Bone Metastatic Mechanisms. Cancers (Basel). 2020 Apr 25;12(5):1071. doi: 10.3390/cancers12051071.
12. Manna F, Karkampouna S, Zoni E, De Menna M, Hensel J, Thalmann GN, Kruithof-de Julio M. Metastases in Prostate Cancer. Cold Spring Harb Perspect Med. 2019 Mar 1;9(3):a033688. doi: 10.1101/cshperspect.a033688.
13. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011 Oct 14;147(2):275-92. doi: 10.1016/j.cell.2011.09.024.
14. Liao, Z., Chua, D. & Tan, N.S. Reactive oxygen species: a volatile driver of field cancerization and metastasis. Mol Cancer 18, 65 (2019). https://doi.org/10.1186/s12943-019-0961-y
15. Yan W, Huang J, Zhang Q, Zhang J. Role of Metastasis Suppressor KAI1/e in Different Cancers. J Oncol. 2021 Jul 9;2021:9924473. doi: 10.1155/2021/9924473.
16. Reunanen N, Kähäri VM. Matrix Metalloproteinases in Cancer Cell Invasion. In: Madame Curie Bioscience Database [Internet]. Austin (TX): Landes Bioscience; 2000-2013. Available from: https://www.ncbi.nlm.nih.gov/books/NBK6598/
17. Aalinkeel R, Nair BB, Reynolds JL, Sykes DE, Mahajan SD, Chadha KC, et al. Overexpression of MMP-9 contributes to invasiveness of prostate cancer cell line LNCaP. Immunol Invest. 2011;40(5):447-64.
18. Webb AH, Gao BT, Goldsmith ZK, Irvine AS, Saleh N, Lee RP, Lendermon JB, Bheemreddy R, Zhang Q, Brennan RC, Johnson D, Steinle JJ, Wilson MW, Morales-Tirado VM. Inhibition of MMP-2 and MMP-9 decreases cellular migration, and angiogenesis in in vitro models of retinoblastoma. BMC Cancer. 2017 Jun 20;17(1):434. doi: 10.1186/s12885-017-3418-y.
19. Xiaohua Huang, Ying Li , Xin He , Yang Chen , Wei Wei , Xuesong Yang , Keli Ma. Gangliosides and CD82 inhibit the motility of colon cancer by downregulating the phosphorylation of EGFR at different tyrosine sites and signaling pathways. 2020. 22(5): 3994-4002. https://doi.org/10.3892/mmr.2020.11467.
20. Sadeghi L, Tanwir F, Yousefi Babadi V. Physiological and Biochemical Effects of Echium Amoenum Extract on Mn2+-Imposed Parkinson Like Disorder in Rats. Adv Pharm Bull. 2018 Nov;8(4):705-713. doi: 10.15171/apb.2018.079. Epub 2018 Nov 29.
21. Mittal M, Flora SJ. Vitamin E supplementation protects oxidative stress during arsenic and fluoride
antagonism in male mice. Drug Chem Toxicol 2007;30(3):263-81. doi:10.1080/01480540701380075.
22. Sadeghi, L., Rizvanov, A.A., Dabirmanesh, B. et al. Proteomic profiling of the rat hippocampus from the kindling and pilocarpine models of epilepsy: potential targets in calcium regulatory network. Sci Rep 11, 8252 (2021). https://doi.org/10.1038/s41598-021-87555-7
23. Zhou D, Shao L, Spitz DR. Reactive oxygen species in normal and tumor stem cells. Adv Cancer Res. 2014;122:1-67. doi: 10.1016/B978-0-12-420117-0.00001-3.
24. Zitka O, Skalickova S, Gumulec J, Masarik M, Adam V, Hubalek J, Trnkova L, Kruseova J, Eckschlager T, Kizek R. Redox status expressed as GSH:GSSG ratio as a marker for oxidative stress in paediatric tumour patients. Oncol Lett. 2012 Dec;4(6):1247-1253. doi: 10.3892/ol.2012.931.
25. Lee MS, Byun HJ, Lee J, Jeoung DI, Kim YM, Lee H. Tetraspanin CD82 represses Sp1-mediated Snail expression and the resultant E-cadherin expression interrupts nuclear signaling of β-catenin by increasing its membrane localization. Cell Signal. 2018 Dec;52:83-94. doi: 10.1016/j.cellsig.2018.09.001.
26. Geraldo, L.H.M., Spohr, T.C.L.d.S., Amaral, R.F.d. et al. Role of lysophosphatidic acid and its receptors in health and disease: novel therapeutic strategies. Sig Transduct Target Ther 6, 45 (2021). https://doi.org/10.1038/s41392-020-00367-5
27. Matuz-Mares D, González-Andrade M, Araiza-Villanueva MG, Vilchis-Landeros MM, Vázquez-Meza H. Mitochondrial Calcium: Effects of Its Imbalance in Disease. Antioxidants. 2022; 11(5):801. https://doi.org/10.3390/antiox11050801
28. Thiel G, Schmidt T, Rössler OG. Ca2+ Microdomains, Calcineurin and the Regulation of Gene Transcription. Cells. 2021 Apr 12;10(4):875. doi: 10.3390/cells10040875.
29. Morel Y, Barouki R. Repression of gene expression by oxidative stress. Biochem J. 1999 Sep 15;342 Pt 3(Pt 3):481-96.
30. Seabra Rodrigues Dias Ivo R., Mok Simon W. F., Gordillo-Martínez Flora, Khan Imran, Hsiao Wendy W. L., Law Betty Y. K., Wong Vincent K. W., Liu Liang. The Calcium-Induced Regulation in the Molecular and Transcriptional Circuitry of Human Inflammatory Response and Autoimmunity.Frontiers in Pharmacology. 2018; 8 https://doi.org/10.3389/fphar.2017.00962
31. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science. 2002;295(5564):2387-92.
32. Rhee JS, Coussens LM. RECKing MMP function: implications for cancer development. Trends Cell Biol. 2002;12(5):209-11.
33. Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res. 2010 May;44(5):479-96. doi: 10.3109/10715761003667554. PMID: 20370557; PMCID: PMC3880197.
34. Marilisa Galasso, Simona Gambino, Maria Grazia Romanelli, Massimo Donadelli, Maria Teresa Scupoli, Browsing the oldest antioxidant enzyme: catalase and its multiple regulation in cancer, Free Radical Biology and Medicine, 2012; 172 (264-272).
35. Che M, Wang R, Li X, Wang HY, Zheng XFS. Expanding roles of superoxide dismutases in cell regulation and cancer. Drug Discov Today. 2016 Jan;21(1):143-149. doi: 10.1016/j.drudis.2015.10.001. Epub 2015 Oct 19.
36. Hyoudou K, Nishikawa M, Ikemura M, Kobayashi Y, Mendelsohn A, Miyazaki N, et al. Prevention of pulmonary metastasis from subcutaneous tumors by binary system-based sustained delivery of catalase. J Control Release. 2009;137(2):110-5.
37. Aalinkeel R, Nair BB, Reynolds JL, Sykes DE, Mahajan SD, Chadha KC, et al. Overexpression of MMP-9 contributes to invasiveness of prostate cancer cell line LNCaP. Immunol Invest. 2011;40(5):447-64.
2. Xing P, Chen L, Yang Q, Song T, Ma C, Grimm R, et al. Differentiating prostate cancer from benign prostatic hyperplasia using whole-lesion histogram and texture analysis of diffusion- and T2-weighted imaging. Cancer Imaging. 2021;21(1):54.
3. Jones J, Feger J, Bell D, et al. Gleason score. Reference article, Radiopaedia.org (Accessed on 11 Mar 2023) https://doi.org/10.53347/rID-9054.
4. Rawla P. Epidemiology of Prostate Cancer. World J Oncol. 2019;10(2):63-89.
5. Brawer MK. Prostatic intraepithelial neoplasia: an overview. Rev Urol. 2005;7 Suppl 3(Suppl 3):S11-8.
6. Minciullo PL, Inferrera A, Navarra M, Calapai G, Magno C, Gangemi S. Oxidative Stress in Benign Prostatic Hyperplasia: A Systematic Review. Urol Int 2015;94:249-254. doi: 10.1159/000366210
7. Srinivas US, Tan BWQ, Vellayappan BA, Jeyasekharan AD. ROS and the DNA damage response in cancer. Redox Biol. 2019;25:101084.
8. Rossi A, Pizzo P, Filadi R. Calcium, mitochondria and cell metabolism: A functional triangle in bioenergetics. Biochimica et biophysica acta Molecular cell research. 2019;1866(7):1068-78
9. Wei W, Graeff R, Yue J. Roles and mechanisms of the CD38/cyclic adenosine diphosphate ribose/Ca(2+) signaling pathway. World J Biol Chem. 2014 Feb 26;5(1):58-67. doi: 10.4331/wjbc.v5.i1.58. PMID: 24600514; PMCID: PMC3942542.
10. Courjaret, R., Machaca, K. Mid-range Ca2+ signalling mediated by functional coupling between store-operated Ca2+ entry and IP3-dependent Ca2+ release. Nat Commun 5, 3916 (2014). https://doi.org/10.1038/ncomms4916.
11. Ardura JA, Álvarez-Carrión L, Gutiérrez-Rojas I, Alonso V. Role of Calcium Signaling in Prostate Cancer Progression: Effects on Cancer Hallmarks and Bone Metastatic Mechanisms. Cancers (Basel). 2020 Apr 25;12(5):1071. doi: 10.3390/cancers12051071.
12. Manna F, Karkampouna S, Zoni E, De Menna M, Hensel J, Thalmann GN, Kruithof-de Julio M. Metastases in Prostate Cancer. Cold Spring Harb Perspect Med. 2019 Mar 1;9(3):a033688. doi: 10.1101/cshperspect.a033688.
13. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011 Oct 14;147(2):275-92. doi: 10.1016/j.cell.2011.09.024.
14. Liao, Z., Chua, D. & Tan, N.S. Reactive oxygen species: a volatile driver of field cancerization and metastasis. Mol Cancer 18, 65 (2019). https://doi.org/10.1186/s12943-019-0961-y
15. Yan W, Huang J, Zhang Q, Zhang J. Role of Metastasis Suppressor KAI1/e in Different Cancers. J Oncol. 2021 Jul 9;2021:9924473. doi: 10.1155/2021/9924473.
16. Reunanen N, Kähäri VM. Matrix Metalloproteinases in Cancer Cell Invasion. In: Madame Curie Bioscience Database [Internet]. Austin (TX): Landes Bioscience; 2000-2013. Available from: https://www.ncbi.nlm.nih.gov/books/NBK6598/
17. Aalinkeel R, Nair BB, Reynolds JL, Sykes DE, Mahajan SD, Chadha KC, et al. Overexpression of MMP-9 contributes to invasiveness of prostate cancer cell line LNCaP. Immunol Invest. 2011;40(5):447-64.
18. Webb AH, Gao BT, Goldsmith ZK, Irvine AS, Saleh N, Lee RP, Lendermon JB, Bheemreddy R, Zhang Q, Brennan RC, Johnson D, Steinle JJ, Wilson MW, Morales-Tirado VM. Inhibition of MMP-2 and MMP-9 decreases cellular migration, and angiogenesis in in vitro models of retinoblastoma. BMC Cancer. 2017 Jun 20;17(1):434. doi: 10.1186/s12885-017-3418-y.
19. Xiaohua Huang, Ying Li , Xin He , Yang Chen , Wei Wei , Xuesong Yang , Keli Ma. Gangliosides and CD82 inhibit the motility of colon cancer by downregulating the phosphorylation of EGFR at different tyrosine sites and signaling pathways. 2020. 22(5): 3994-4002. https://doi.org/10.3892/mmr.2020.11467.
20. Sadeghi L, Tanwir F, Yousefi Babadi V. Physiological and Biochemical Effects of Echium Amoenum Extract on Mn2+-Imposed Parkinson Like Disorder in Rats. Adv Pharm Bull. 2018 Nov;8(4):705-713. doi: 10.15171/apb.2018.079. Epub 2018 Nov 29.
21. Mittal M, Flora SJ. Vitamin E supplementation protects oxidative stress during arsenic and fluoride
antagonism in male mice. Drug Chem Toxicol 2007;30(3):263-81. doi:10.1080/01480540701380075.
22. Sadeghi, L., Rizvanov, A.A., Dabirmanesh, B. et al. Proteomic profiling of the rat hippocampus from the kindling and pilocarpine models of epilepsy: potential targets in calcium regulatory network. Sci Rep 11, 8252 (2021). https://doi.org/10.1038/s41598-021-87555-7
23. Zhou D, Shao L, Spitz DR. Reactive oxygen species in normal and tumor stem cells. Adv Cancer Res. 2014;122:1-67. doi: 10.1016/B978-0-12-420117-0.00001-3.
24. Zitka O, Skalickova S, Gumulec J, Masarik M, Adam V, Hubalek J, Trnkova L, Kruseova J, Eckschlager T, Kizek R. Redox status expressed as GSH:GSSG ratio as a marker for oxidative stress in paediatric tumour patients. Oncol Lett. 2012 Dec;4(6):1247-1253. doi: 10.3892/ol.2012.931.
25. Lee MS, Byun HJ, Lee J, Jeoung DI, Kim YM, Lee H. Tetraspanin CD82 represses Sp1-mediated Snail expression and the resultant E-cadherin expression interrupts nuclear signaling of β-catenin by increasing its membrane localization. Cell Signal. 2018 Dec;52:83-94. doi: 10.1016/j.cellsig.2018.09.001.
26. Geraldo, L.H.M., Spohr, T.C.L.d.S., Amaral, R.F.d. et al. Role of lysophosphatidic acid and its receptors in health and disease: novel therapeutic strategies. Sig Transduct Target Ther 6, 45 (2021). https://doi.org/10.1038/s41392-020-00367-5
27. Matuz-Mares D, González-Andrade M, Araiza-Villanueva MG, Vilchis-Landeros MM, Vázquez-Meza H. Mitochondrial Calcium: Effects of Its Imbalance in Disease. Antioxidants. 2022; 11(5):801. https://doi.org/10.3390/antiox11050801
28. Thiel G, Schmidt T, Rössler OG. Ca2+ Microdomains, Calcineurin and the Regulation of Gene Transcription. Cells. 2021 Apr 12;10(4):875. doi: 10.3390/cells10040875.
29. Morel Y, Barouki R. Repression of gene expression by oxidative stress. Biochem J. 1999 Sep 15;342 Pt 3(Pt 3):481-96.
30. Seabra Rodrigues Dias Ivo R., Mok Simon W. F., Gordillo-Martínez Flora, Khan Imran, Hsiao Wendy W. L., Law Betty Y. K., Wong Vincent K. W., Liu Liang. The Calcium-Induced Regulation in the Molecular and Transcriptional Circuitry of Human Inflammatory Response and Autoimmunity.Frontiers in Pharmacology. 2018; 8 https://doi.org/10.3389/fphar.2017.00962
31. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science. 2002;295(5564):2387-92.
32. Rhee JS, Coussens LM. RECKing MMP function: implications for cancer development. Trends Cell Biol. 2002;12(5):209-11.
33. Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res. 2010 May;44(5):479-96. doi: 10.3109/10715761003667554. PMID: 20370557; PMCID: PMC3880197.
34. Marilisa Galasso, Simona Gambino, Maria Grazia Romanelli, Massimo Donadelli, Maria Teresa Scupoli, Browsing the oldest antioxidant enzyme: catalase and its multiple regulation in cancer, Free Radical Biology and Medicine, 2012; 172 (264-272).
35. Che M, Wang R, Li X, Wang HY, Zheng XFS. Expanding roles of superoxide dismutases in cell regulation and cancer. Drug Discov Today. 2016 Jan;21(1):143-149. doi: 10.1016/j.drudis.2015.10.001. Epub 2015 Oct 19.
36. Hyoudou K, Nishikawa M, Ikemura M, Kobayashi Y, Mendelsohn A, Miyazaki N, et al. Prevention of pulmonary metastasis from subcutaneous tumors by binary system-based sustained delivery of catalase. J Control Release. 2009;137(2):110-5.
37. Aalinkeel R, Nair BB, Reynolds JL, Sykes DE, Mahajan SD, Chadha KC, et al. Overexpression of MMP-9 contributes to invasiveness of prostate cancer cell line LNCaP. Immunol Invest. 2011;40(5):447-64.
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Jan 10, 2023
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Leila Sadeghi, Gholamreza Dehghan, & Tholfiqar Najah Ismeal. (2023). METASTASIS REGULATION IN PROSTATE CANCER: THE POSSIBLE ROLE OF IP3- AND CADPR-MEDIATED Ca2+ SIGNALING. Journal of Population Therapeutics and Clinical Pharmacology, 30(1), 503-513. https://doi.org/10.53555/jptcp.v30i1.2603
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Author Biographies
Leila Sadeghi
Department of Animal Biology, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran
Gholamreza Dehghan
Department of Animal Biology, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran
Tholfiqar Najah Ismeal
Department of Animal Biology, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran
How to Cite
Leila Sadeghi, Gholamreza Dehghan, & Tholfiqar Najah Ismeal. (2023). METASTASIS REGULATION IN PROSTATE CANCER: THE POSSIBLE ROLE OF IP3- AND CADPR-MEDIATED Ca2+ SIGNALING. Journal of Population Therapeutics and Clinical Pharmacology, 30(1), 503-513. https://doi.org/10.53555/jptcp.v30i1.2603