Cholesterol-induced activation of TRPM7 regulates cell proliferation, migration, and viability of human prostate cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 9, 2014, Pages 1839-1850

  Sun, Yuyang ^a   Sukumaran, Pramod ^a   Varma, Archana ^b   Derry, Susan ^b   Sahmoun, Abe E ^b   Singh, Brij B ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b UND School of Medicine & Health Sciences Southeast Campus   (United States)

Author keywords

Calcium and signal transduction; Cell proliferation and migration; Cholesterol; Prostate cancer; Statin; TRPM7

Indexed keywords

CALCIUM; CALPAIN; CHOLESTEROL; COMPACTIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SIMVASTATIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL M7; UVOMORULIN;

ARTICLE; CALCIUM TRANSPORT; CANCER CELL; CANCER GROWTH; CANCER PATIENT; CASE CONTROL STUDY; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; LNCAP CELL LINE; MALE; PILOT STUDY; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; SIGNAL TRANSDUCTION;

CALCIUM AND SIGNAL TRANSDUCTION; CELL PROLIFERATION AND MIGRATION; CHOLESTEROL; PROSTATE CANCER; STATIN; TRPM7;

AGED; CALCIUM; CALCIUM SIGNALING; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CHOLESTEROL; DEMOGRAPHY; GENE KNOCKOUT TECHNIQUES; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; ION CHANNEL GATING; MALE; MODELS, BIOLOGICAL; PROSTATE; PROSTATIC NEOPLASMS; TRPM CATION CHANNELS;

EID: 84902438481     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.04.019     Document Type: Article

References (56)

1. Center M.M., Jemal A., Lortet-Tieulent J., et al. International variation in prostate cancer incidence and mortality rates. Eur. Urol. 2012, 61:1079-1092.
2. Flourakis M., Prevarskaya N. Insights into Ca2+ homeostasis of advanced prostate cancer cells. Biochim. Biophys. Acta 2009, 1793:1105-1109.
3. Prevarskaya N., Skryma R., Shuba Y. Ca2+ homeostasis in apoptotic resistance of prostate cancer cells. Biochem. Biophys. Res. Commun. 2004, 322:1326-1335.
4. Wissenbach U., Niemeyer B., Himmerkus N., Fixemer T., Bonkhoff H., Flockerzi V. TRPV6 and prostate cancer: cancer growth beyond the prostate correlates with increased TRPV6 Ca2+ channel expression. Biochem. Biophys. Res. Commun. 2004, 322:1359-1363.
5. Pelton K., Freeman M.R., Solomon K.R. Cholesterol and prostate cancer. Curr. Opin. Pharmacol. 2012, 12:751-759.
6. Twiddy A.L., Leon C.G., Wasan K.M. Cholesterol as a potential target for castration-resistant prostate cancer. Pharm. Res. 2011, 28:423-437.
7. Loeb S., Kan D., Helfand B.T., Nadler R.B., Catalona W.J. Is statin use associated with prostate cancer aggressiveness?. BJU Int. 2010, 105:1222-1225.
8. Gutt R., Tonlaar N., Kunnavakkam R., Karrison T., Weichselbaum R.R., Liauw S.L. Statin use and risk of prostate cancer recurrence in men treated with radiation therapy. J. Clin. Oncol. 2010, 28:2653-2659.
9. Chen R., Zeng X., Zhang R., et al. Ca1.3 channel alpha protein is overexpressed and modulates androgen receptor transactivation in prostate cancers. Urol. Oncol. 2013, http://dx.doi.org/1 10.1016/j.urolonc.2013.05.011 (in press).
10. Datta M., Schwartz G.G. Calcium and vitamin D supplementation during androgen deprivation therapy for prostate cancer: a critical review. Oncologist 2012, 17:1171-1179.
11. Racioppi L. CaMKK2: a novel target for shaping the androgen-regulated tumor ecosystem. Trends Mol. Med. 2013, 19:83-88.
12. Sun Y., Selvaraj S., Varma A., Derry S., Sahmoun A.E., Singh B.B. Increase in serum Ca2+/Mg2+ ratio promote proliferation of prostate cancer cells by activating TRPM7 channel. J. Biol. Chem. 2012, 288(1):255-263.
13. Lee S.Y., Choi H.K., Kim S.T., et al. Cholesterol inhibits M-type K+channels via protein kinase C-dependent phosphorylation in sympathetic neurons. J. Biol. Chem. 2010, 285:10939-10950.
14. Chun Y.S., Shin S., Kim Y., et al. Cholesterol modulates ion channels via down-regulation of phosphatidylinositol 4,5-bisphosphate. J. Neurochem. 2010, 112:1286-1294.
15. Dopico A.M., Bukiya A.N., Singh A.K. Large conductance, calcium- and voltage-gated potassium (BK) channels: regulation by cholesterol. Pharmacol. Ther. 2012, 135:133-150.
16. Runnels L.W., Yue L., Clapham D.E. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 2001, 291:1043-1047.
17. Runnels L.W. TRPM6 and TRPM7: A Mul-TRP-PLIK-cation of channel functions. Curr. Pharm. Biotechnol. 2011, 12:42-53.
18. Lam D.H., Grant C.E., Hill C.E. Differential expression of TRPM7 in rat hepatoma and embryonic and adult hepatocytes. Can. J. Physiol. Pharmacol. 2012, 90:435-444.
19. Mishra R., Rao V., Ta R., Shobeiri N., Hill C.E. Mg2+- and MgATP-inhibited and Ca2+/calmodulin-sensitive TRPM7-like current in hepatoma and hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 297:G687-G694.
20. Guilbert A., Gautier M., Dhennin-Duthille I., Haren N., Sevestre H., Ouadid-Ahidouch H. Evidence that TRPM7 is required for breast cancer cell proliferation. Am. J. Physiol. Cell Physiol. 2009, 297:C493-C502.
21. Wang H.P., Pu X.Y., Wang X.H. Distribution profiles of transient receptor potential melastatin-related and vanilloid-related channels in prostatic tissue in rat. Asian J. Androl. 2007, 9:634-640.
22. Paravicini T.M., Chubanov V., Gudermann T. TRPM7: a unique channel involved in magnesium homeostasis. Int. J. Biochem. Cell Biol. 2012, 44:1381-1384.
23. Chen H.C., Su L.T., Gonzalez-Pagan O., Overton J.D., Runnels L.W. A key role for Mg(2+) in TRPM7's control of ROS levels during cell stress. Biochem. J. 2012, 445:441-448.
24. Jin J., Desai B.N., Navarro B., Donovan A., Andrews N.C., Clapham D.E. Deletion of Trpm7 disrupts embryonic development and thymopoiesis without altering Mg2+ homeostasis. Science 2008, 322:756-760.
25. Sun Y., Selvaraj S., Varma A., Derry S., Sahmoun A.E., Singh B.B. Increase in serum Ca2+/Mg2+ ratio promotes proliferation of prostate cancer cells by activating TRPM7 channels. J. Biol. Chem. 2013, 288:255-263.
26. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 2003, 4:517-529.
27. Braun A., Vogtle T., Varga-Szabo D., Nieswandt B. STIM and Orai in hemostasis and thrombosis. Front. Biosci. 2011, 16:2144-2160.
28. Jiang X., Newell E.W., Schlichter L.C. Regulation of a TRPM7-like current in rat brain microglia. J. Biol. Chem. 2003, 278:42867-42876.
29. Nadler M.J., Hermosura M.C., Inabe K., et al. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 2001, 411:590-595.
30. Runnels L.W., Yue L., Clapham D.E. The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat. Cell Biol. 2002, 4:329-336.
31. Voets T., Nilius B., Hoefs S., et al. TRPM6 forms the Mg2+ influx channel involved in intestinal and renal Mg2+ absorption. J. Biol. Chem. 2004, 279:19-25.
32. Li M., Du J., Jiang J., et al. Molecular determinants of Mg2+ and Ca2+ permeability and pH sensitivity in TRPM6 and TRPM7. J. Biol. Chem. 2007, 282:25817-25830.
33. Franco S.J., Huttenlocher A. Regulating cell migration: calpains make the cut. J. Cell Sci. 2005, 118:3829-3838.
34. Sukumaran P., Lof C., Pulli I., Kemppainen K., Viitanen T., Tornquist K. Significance of the transient receptor potential canonical 2 (TRPC2) channel in the regulation of rat thyroid FRTL-5 cell proliferation, migration, adhesion and invasion. Mol. Cell. Endocrinol. 2013, 374:10-21.
35. Rios-Doria J., Day K.C., Kuefer R., et al. The role of calpain in the proteolytic cleavage of E-cadherin in prostate and mammary epithelial cells. J. Biol. Chem. 2003, 278:1372-1379.
36. Roy M., Kung H.J., Ghosh P.M. Statins and prostate cancer: role of cholesterol inhibition vs. prevention of small GTP-binding proteins. Am. J. Cancer Res. 2011, 1:542-561.
37. Geybels M.S., Wright J.L., Holt S.K., Kolb S., Feng Z., Stanford J.L. Statin use in relation to prostate cancer outcomes in a population-based patient cohort study. Prostate 2013, 73(11):1214-1222.
38. Graham I., Cooney M.T., Bradley D., Dudina A., Reiner Z. Dyslipidemias in the prevention of cardiovascular disease: risks and causality. Curr. Cardiol. Rep. 2012, 14:709-720.
39. Critchley J.A., Capewell S. Withdrawn: smoking cessation for the secondary prevention of coronary heart disease. Cochrane Database Syst. Rev. 2012, 2:CD003041.
40. Pani B., Ong H.L., Liu X., Rauser K., Ambudkar I.S., Singh B.B. Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of store-operated Ca2+ entry (SOCE). J. Biol. Chem. 2008, 283:17333-17340.
41. Kannan K.B., Barlos D., Hauser C.J. Free cholesterol alters lipid raft structure and function regulating neutrophil Ca2+ entry and respiratory burst: correlations with calcium channel raft trafficking. J. Immunol. 2007, 178:5253-5261.
42. Dou Y., Li Y., Chen J., et al. Inhibition of cancer cell proliferation by midazolam by targeting transient receptor potential melastatin 7. Oncol. Lett. 2013, 5:1010-1016.
43. Kim B.J. Involvement of melastatin type transient receptor potential 7 channels in ginsenoside Rd-induced apoptosis in gastric and breast cancer cells. J. Ginseng Res. 2013, 37:201-209.
44. Solomon K.R., Freeman M.R. The complex interplay between cholesterol and prostate malignancy. Urol. Clin. North Am. 2011, 38:243-259.
45. Kitahara C.M., Berrington de Gonzalez A., Freedman N.D., et al. Total cholesterol and cancer risk in a large prospective study in Korea. J. Clin. Oncol. 2011, 29:1592-1598.
46. Brown M., Hart C., Tawadros T., et al. The differential effects of statins on the metastatic behaviour of prostate cancer. Br. J. Cancer 2012, 106:1689-1696.
47. Platz E.A., Leitzmann M.F., Visvanathan K., et al. Statin drugs and risk of advanced prostate cancer. J. Natl. Cancer Inst. 2006, 98:1819-1825.
48. Murtola T.J., Tammela T.L., Lahtela J., Auvinen A. Cholesterol-lowering drugs and prostate cancer risk: a population-based case-control study. Cancer Epidemiol. Biomarkers Prev. 2007, 16:2226-2232.
49. Platz E.A., Till C., Goodman P.J., et al. Men with low serum cholesterol have a lower risk of high-grade prostate cancer in the placebo arm of the prostate cancer prevention trial. Cancer Epidemiol. Biomarkers Prev. 2009, 18:2807-2813.
50. Khosropanah I., Falahatkar S., Farhat B., et al. Assessment of atorvastatin effectiveness on serum PSA level in hypercholesterolemic males. Acta Med. Iran. 2011, 49:789-794.
51. Rauthan M., Ranji P., Aguilera Pradenas N., Pitot C., Pilon M. The mitochondrial unfolded protein response activator ATFS-1 protects cells from inhibition of the mevalonate pathway. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:5981-5986.
52. Garcia-Ruiz C., Morales A., Fernandez-Checa J.C. Statins and protein prenylation in cancer cell biology and therapy. Anti Cancer Agents Med. Chem. 2012, 12:303-315.
53. Singh B.B., Lockwich T.P., Bandyopadhyay B.C., et al. VAMP2-dependent exocytosis regulates plasma membrane insertion of TRPC3 channels and contributes to agonist-stimulated Ca2+ influx. Mol. Cell 2004, 15:635-646.
54. Pani B., Cornatzer E., Cornatzer W., et al. Up-regulation of transient receptor potential canonical 1 (TRPC1) following sarco(endo)plasmic reticulum Ca2+ ATPase 2 gene silencing promotes cell survival: a potential role for TRPC1 in Darier's disease. Mol. Biol. Cell 2006, 17:4446-4458.
55. Pani B., Ong H.L., Brazer S.C., et al. Activation of TRPC1 by STIM1 in ER-PM microdomains involves release of the channel from its scaffold caveolin-1. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20087-20092.
56. Selvaraj S., Watt J.A., Singh B.B. TRPC1 inhibits apoptotic cell degeneration induced by dopaminergic neurotoxin MPTP/MPP(+). Cell Calcium 2009, 46:209-218.