T-type calcium channels blockers as new tools in cancer therapies

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 4, 2014, Pages 801-810

  Dziegielewska, Barbara ^a   Gray, Lloyd S ^b   Dziegielewski, Jaroslaw ^a,c  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Tau Therapeutics LLC   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Apoptosis; Cancer; Mibefradil; Proliferation; T type calcium channels; Targeted therapy

Indexed keywords

ANTINEOPLASTIC AGENT; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL T TYPE;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER MORTALITY; CANCER RESISTANCE; CANCER SURVIVAL; CANCER THERAPY; CARCINOGENESIS; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CHEMORADIOTHERAPY; DOWN REGULATION; DRUG SAFETY; HUMAN; NEUROPATHIC PAIN; NEUROSECRETORY CELL; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; STEM CELL; TARGET CELL; TUMOR MICROENVIRONMENT; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; DRUG EFFECTS; GENE THERAPY; GENETICS; METABOLISM; NEOPLASMS; PHYSIOLOGY; TRENDS;

ANIMALS; ANTINEOPLASTIC AGENTS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, T-TYPE; CELL DIFFERENTIATION; GENETIC THERAPY; HUMANS; NEOPLASMS;

EID: 84896543008     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1444-z     Document Type: Review

References (91)

1. Alison MR, Lin W-R, Lim SML, Nicholson LJ (2012) Cancer stem cells: in the line of fire. Cancer Treat Rev 38(6):589-598
2. Amorino GP, Parsons SJ (2004) Neuroendocrine cells in prostate cancer. Crit Rev Eukaryot Gene Expr 14(4):287-300 (Pubitemid 40221058)
3. Atlas D (2010) Signaling role of the voltage-gated calcium channel as themolecular on/off-switch of secretion. Cell Signal 22(11):1597-1603
4. Balk SD (1971) Calciumas a regulator of the proliferation of normal, but not of transformed, chicken fibroblasts in a plasma-containing medium. Proc Natl Acad Sci U S A 68(2):271-275
5. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 357(9255):539-545 (Pubitemid 32173595)
6. Bertolesi GE, Jollimore CAB, Shi C, Elbaum L, Denovan-Wright EM, Barnes S, Kelly MEM (2003) Regulation of alpha1G T-type calcium channel gene (CACNA1G) expression during neuronal differentiation. Eur J Neurosci 17(9):1802-1810 (Pubitemid 36645330)
7. Bertolesi GE, Shi C, Elbaum L, Jollimore C, Rozenberg G, Barnes S, Kelly MEM (2002) The Ca(2+) channel antagonists mibefradil and pimozide inhibit cell growth via different cytotoxicmechanisms. Mol Pharmacol 62(2):210-219 (Pubitemid 34804099)
8. Bilici D, Akpinar E, Gürsan N, Dengiz GO, Bilici S, Alta̧ S (2001) Protective effect of T-type calcium channel blocker in histamineinduced paw inflammation in rat. Pharmacol Res Off J Ital Pharmacol Soc 44(6):527-531 (Pubitemid 34014334)
9. Boynton AL, Whitfield JF, Isaacs RJ, Tremblay RG (1977) Different extracellular calcium requirements for proliferation of nonneoplastic, preneoplastic, and neoplastic mouse cells. Cancer Res 37(8 Pt 1): 2657-2661
10. Bringmann A, Schopf S, Reichenbach A (2000) Developmental regulation of calcium channel-mediated currents in retinal glial (Müller) cells. J Neurophysiol 84(6):2975-2983
11. Capiod T (2011) Cell proliferation, calcium influx and calcium channels. Biochimie 93(12):2075-2079
12. Carbone E, Lux HD (1984) A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature 310(5977):501-502 (Pubitemid 14052412)
13. Chemin J, Nargeot J, Lory P (2004) Ca(v)3.2 calcium channels control an autocrine mechanism that promotes neuroblastoma cell differentiation. Neuroreport 15(4):671-675 (Pubitemid 38457158)
14. Clapham DE (2007) Calcium signaling. Cell 131(6):1047-1058 (Pubitemid 350258556)
15. Das A, Pushparaj C, Bahí N, Sorolla A, Herreros J, Pamplona R, Vilella R, Matias-Guiu X, Martí RM, Cantí C (2012) Functional expression of voltage-gated calcium channels in human melanoma. Pigment Cell Melanoma Res 25(2):200-212
16. Das A, Pushparaj C, Herreros J, Nager M, Vilella R, Portero M, Pamplona R, Matias-Guiu X, Martí R, Cantí C (2013) T-type calcium channel blockers inhibit autophagy and promote apoptosis of malignant melanoma cells. Pigment Cell Melanoma Res 26(6):874-85
17. Del Toro R, Levitsky KL, López-Barneo J, Chiara MD (2003) Induction of T-type calcium channel gene expression by chronic hypoxia. J Biol Chem 278(25):22316-22324 (Pubitemid 36833255)
18. Di Sant'Agnese PA (2001) Neuroendocrine differentiation in prostatic carcinoma: an update on recent developments. Ann Oncol Off J Eur Soc Med Oncol / ESMO 12(Suppl 2):S135-140
19. Dziegielewska B, Brautigan DL, Larner JM, Dziegielewski J (2013) T-type Ca2+ channel inhibition induces p53 dependent cell growth arrest and apoptosis through activation of p38-MAPKin colon cancer cells. Molecular Cancer Research: MCR. http://mcr.aacrjournals.org/content/early/2013/12/20/1541-7786.MCR-13-0485. abstract. Accessed 30 Dec 2013
20. Eller P, Berjukov S, Wanner S, Huber I, Hering S, Knaus HG, Toth G, Kimball SD, Striessnig J (2000) High affinity interaction of mibefradil with voltage-gated calcium and sodium channels. Br J Pharmacol 130(3):669-677 (Pubitemid 30332987)
21. Fallon MT (2013) Neuropathic pain in cancer. Br J Anaesth 111(1):105-111
22. Fearon IM, Randall AD, Perez-Reyes E, Peers C (2000) Modulation of recombinant T-type Ca2+ channels by hypoxia and glutathione. Pflügers Archiv Eur J Physiol 441(2-3):181-188 (Pubitemid 32128156)
23. Fisseler-Eckhoff A, Demes M (2012) Neuroendocrine tumors of the lung. Cancers 4(3):777-798
24. Fixemer T, Remberger K, Bonkhoff H (2002) Apoptosis resistance of neuroendocrine phenotypes in prostatic adenocarcinoma. Prostate 53(2):118-123
25. Flatters SJL, Bennett GJ (2004) Ethosuximide reverses paclitaxel-and vincristine-induced painful peripheral neuropathy. Pain 109(1-2):150-161 (Pubitemid 38479781)
26. Gackière F, Bidaux G, Delcourt P, Van Coppenolle F, Katsogiannou M, Dewailly E, Bavencoffe A, Van Chuoï-Mariot MT, Mauroy B, Prevarskaya N, Mariot P (2008) CaV3.2 T-type calcium channels are involved in calcium-dependent secretion of neuroendocrine prostate cancer cells. J Biol Chem 283(15):10162-10173
27. Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, Jain RK (2011) Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 91(3):1071-1121
28. Gray LS, Macdonald TL (2006) The pharmacology and regulation of T type calcium channels: new opportunities for unique therapeutics for cancer. Cell Calcium 40(2):115-120 (Pubitemid 43942296)
29. Gray LS, Schiff D, Macdonald TL (2013) A model for the regulation of T-type Ca(2+) channels in proliferation: roles in stem cells and cancer. Expert Rev Anticancer Ther 13(5):589-595
30. Haverstick DM, Heady TN, Macdonald TL, Gray LS (2000) Inhibition of human prostate cancer proliferation in vitro and in a mouse model by a compound synthesized to block Ca2+ entry. Cancer Res 60(4):1002-1008 (Pubitemid 30129537)
31. Heady TN, Gomora JC, Macdonald TL, Perez-Reyes E (2001) Molecular pharmacology of T-type Ca2+ channels. Jpn J Pharmacol 85(4):339-350
32. Heo JH, Seo HN, Choe YJ, Kim S, Oh CR, Kim YD, Rhim H, Choo DJ, Kim J, Lee JY (2008) T-type Ca2+ channel blockers suppress the growth of human cancer cells. Bioorg Med Chem Lett 18(14):3899-3901
33. Hirooka K, Bertolesi GE, Kelly MEM, Denovan-Wright EM, Sun X, Hamid J, Zamponi GW, Juhasz AE, Haynes LW, Barnes S (2002) T-Type calcium channel alpha1G and alpha1H subunits in human retinoblastoma cells and their loss after differentiation. J Neurophysiol 88(1):196-205 (Pubitemid 34755343)
34. Huang L, Keyser BM, Tagmose TM, Hansen JB, Taylor JT, Zhuang H, ZhangM, Ragsdale DS, LiM(2004) NNC 55-0396 [(1S,2S)-2-(2-(N-[(3-benzimidazol-2-yl) propyl]-N-methylamino)ethyl)-6-fluoro-1, 2,3,4-tetrahydro-1-isopropyl-2-naphtyl cyclopropanecarboxylate dihydrochloride]: a new selective inhibitor of T-type calcium channels. J Pharmacol Exp Ther 309(1):193-199 (Pubitemid 38393130)
35. Ischenko I, Seeliger H, Schaffer M, Jauch K-W, Bruns CJ (2008) Cancer stem cells: how can we target them? Curr Med Chem 15(30): 3171-3184
36. Jaggi AS, Singh N (2012) Mechanisms in cancer-chemotherapeutic drugs-induced peripheral neuropathy. Toxicology 291(1-3):1-9
37. Jang, SJ, Choi HW, Choi DL, Cho S, Rim H.-K, Choi H.-E, Kim KS, Huang M, Rhim H, Lee K-T, Lee JY (2013) In vitro cytotoxicity on human ovarian cancer cells by T-type calcium channel blockers. Bioorg Med Chem Lett 23(24):6656-62
38. 2+ channels in the rat and mouse thalamus. J Physiol 574(2):415-430
39. Kahl CR, Means AR (2003) Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr Rev 24(6):719-736 (Pubitemid 38067696)
40. Kang HB, Rim H-K, Park JY, Choi HW, Choi DL, Seo J-H, Chung K-S, Huh G, Kim J, Choo DJ, Lee K-T, Lee JY (2012) In vivo evaluation of oral anti-tumoral effect of 3,4-dihydroquinazoline derivative on solid tumor. Bioorg Med Chem Lett 22(2):1198-1201
41. Keir ST, Friedman HS, Reardon DA, Bigner DD, Gray LA (2013) Mibefradil, a novel therapy for glioblastoma multiforme: cell cycle synchronization and interlaced therapy in a murine model. J Neurooncol 111(2):97-102
42. Knut and Alice Wallenberg Foundation (2013) Human protein atlas. www.proteinatlas.org. Accessed 15 Nov 2013
43. Kundu JK, Surh Y-J (2008) Inflammation: gearing the journey to cancer. Mutat Res 659(1-2):15-30
44. Kwon SY, Bae YK, Gu MJ, Choi JE, Kang SH, Lee SJ, Kim A, Jung HR, Kang SH, Oh HK, Park JY (2013) Neuroendocrine differentiation correlates with hormone receptor expression and decreased survival in patients with invasive breast carcinoma. http://onlinelibrary.wiley.com/doi/10.1111/his.12306/abstract. Accessed 30 Dec 2013
45. Lijnen P, Fagard R, Petrov V (1999)Mibefradil-induced inhibition of proliferation of human peripheral blood mononuclear cells. J Cardiovasc Pharmacol 33(4):595-604 (Pubitemid 29164823)
46. Li W, Zhang S-L, Wang N, Zhang B-B, Li M (2011) Blockade of Ttype Ca(2+) channels inhibits human ovarian cancer cell proliferation. Cancer Investig 29(5):339-346
47. Li Y, Liu S, Lu F, Zhang T, Chen H, Wu S, Zhuang H (2009) Arole of functional T-type Ca2+ channel in hepatocellular carcinoma cell proliferation. Oncol Rep 22(5):1229-1235
48. Life Technologies Corporation (2013) https://www.oncomine.com/resource/ main.html#d:212;dso:geneOverex;dt:dataset;ec[2]; epv:150001.151078,3508;et: over;f:2502825;g:8912;gt:boxplot;p: 77321987;pg:1;pvf:3518,7696;scr:datasets;ss: all;v:17. Accessed 15 Nov 2013
49. Lory P, Bidaud I, Chemin J (2006) T-type calcium channels in differentiation and proliferation. Cell Calcium 40(2):135-146 (Pubitemid 43964483)
50. Louhivuori LM, Louhivuori V, Wigren H-K, Hakala E, Jansson LC, Nordström T, Castrén ML, Akerman KE (2013) Role of low voltage activated calcium channels in neuritogenesis and active migration of embryonic neural progenitor cells. Stem Cells Dev 22(8):1206-1219
51. Lu F, Chen H, Zhou C, Liu S, Guo M, Chen P, Zhuang H, Xie D, Wu S (2008) T-type Ca2+ channel expression in human esophageal carcinomas: a functional role in proliferation. Cell Calcium 43(1):49-58
52. Lu F, Chen H, Zhou C, Wu S (2005) Is there a role for T-type Ca2+ channel in glioma cell proliferation? Cell Calcium 38(6):593-595, author reply 597
53. Mariot P, Vanoverberghe K, Lalevee N, Rossier MF, Prevarskaya N (2002) Overexpression of an alpha 1H (Cav3.2) T-type calcium channel during neuroendocrine differentiation of human prostate cancer cells. J Biol Chem 277(13):10824-10833 (Pubitemid 34952836)
54. Mehrke G, Zong XG, Flockerzi V, Hofmann F (1994) The Ca(++)- channel blocker Ro 40-5967 blocks differently T-type and L-type Ca++ channels. J Pharmacol Exp Ther 271(3):1483-1488 (Pubitemid 24382661)
55. Mishra SK, Hermsmeyer K (1994) Selective inhibition of T-type Ca2+ channels by Ro 40-5967. Circ Res 75(1):144-148
56. Moncharmont C, Levy A, Gilormini M, Bertrand G, Chargari C, Alphonse G, Ardail D, Rodriguez-Lafrasse C, Magné N (2012) Targeting a cornerstone of radiation resistance: cancer stem cell. Cancer Lett 322(2):139-147
57. Monteith GR, Davis FM, Roberts-Thomson SJ (2012) Calcium channels and pumps in cancer: changes and consequences. J Biol Chem 287(38):31666-31673
58. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ (2007) Calcium and cancer: targeting Ca2+ transport. Nat Rev Cancer 7(7):519-530 (Pubitemid 46985398)
59. Nebe B, Kunz F, Peters A, Rychly J, Noack T, Beck R (2004) Induction of apoptosis by the calcium antagonist mibefradil correlates with depolarization of the membrane potential and decreased integrin expression in human lens epithelial cells. Graefe's Arch Clin Exp Ophthalmol = Albrecht Von Graefes Archiv Für Klinische Und Experimentelle Ophthalmologie 242(7):597-604 (Pubitemid 39157689)
60. Nilius B, Hess P, Lansman JB, Tsien RW (1985) A novel type of cardiac calcium channel in ventricular cells. Nature 316(6027): 443-446 (Pubitemid 16238453)
61. Nilius B, Talavera K, Verkhratsky A (2006) T-type calcium channels: the never ending story. Cell Calcium 40(2):81-88 (Pubitemid 43942293)
62. Nowycky MC, Fox AP, Tsien RW (1985) Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316(6027):440-443 (Pubitemid 16197073)
63. Oguri A, Tanaka T, Iida H, Meguro K, Takano H, Oonuma H, Nishimura S, Morita T, Yamasoba T, Nagai R, Nakajima T (2010) Involvement of CaV3.1 T-type calcium channels in cell proliferation in mouse preadipocytes. Am J Physiol Cell Physiol 298(6):C1414-1423
64. Ohkubo T, Yamazaki J (2012) T-type voltage-activated calcium channel Cav3.1, but not Cav3.2, is involved in the inhibition of proliferation and apoptosis in MCF-7 human breast cancer cells. Int J Oncol 41(1):267-275
65. Panner A, Cribbs LL, Zainelli GM, Origitano TC, Singh S, Wurster RD (2005) Variation of T-type calcium channel protein expression affects cell division of cultured tumor cells. Cell Calcium 37(2):105-119 (Pubitemid 40017369)
66. Panner A, Wurster RD (2006) T-type calcium channels and tumor proliferation. Cell Calcium 40(2):253-259 (Pubitemid 43942305)
67. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83(1):117-161
68. Perez-Reyes E, Van Deusen AL, Vitko I (2009) Molecular pharmacology of human Cav3.2 T-type Ca2+ channels: block by antihypertensives, antiarrhythmics, and their analogs. J Pharmacol Exp Ther 328(2):621-627
69. Pluteanu F, Cribbs LL (2009) T-type calcium channels are regulated by hypoxia/reoxygenation in ventricular myocytes. Am J Physiol Heart Circ Physiol 297(4):H1304-1313
70. Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146(6):873-887
71. Pottle J, Sun C, Gray L, Li M (2013) Exploiting MCF-7 cells' calcium dependence with Interlaced Therapy. J Cancer Ther 04(07): 32-40
72. Rim H-K, Lee H-W, Choi IS, Park JY, Choi HW, Choi J-H, Cho Y-W, Lee JY, Lee K-T (2012) T-type Ca2+ channel blocker, KYS05047 induces G1 phase cell cycle arrest by decreasing intracellular Ca2+ levels in human lung adenocarcinoma A549 cells. Bioorg Med Chem Lett 22(23):7123-7126
73. Rodríguez-Gómez JA, Levitsky KL, López-Barneo J (2012) T-type Ca2+ channels in mouse embryonic stem cells: modulation during cell cycle and contribution to self-renewal. Am J Physiol Cell physiol 302(3):C494-504
74. Santoni G, Santoni M, Nabissi M (2012) Functional role of T-type calcium channels in tumour growth and progression: prospective in cancer therapy. Br J Pharmacol 166(4):1244-1246
75. Schmitt R, Clozel JP, Iberg N, Bühler FR (1996) Prevention of neointima formation by mibefradil after vascular injury in rats: comparison with ACE inhibition. Cardiovasc Drugs Ther / Sponsored Int Soc Cardiovasc Pharmacother 10(2):101-105
76. Seigel GM, Hackam AS, Ganguly A, Mandell LM, Gonzalez-Fernandez F (2007) Human embryonic and neuronal stem cell markers in retinoblastoma. Mol Vis 13(2007):823-832 (Pubitemid 46908324)
77. Sekiguchi F, Kawabata A (2013) T-type calcium channels: functional regulation and implication in pain signaling. J Pharmacol Sci 122(4):244-250
78. Sheehan JP, Xu Z, Popp B, Kowalski L, Schlesinger D (2013) Inhibition of glioblastoma and enhancement of survival via the use of mibefradil in conjunction with radiosurgery. J Neurosurg 118(4):830-837
79. Su AI, Welsh JB, Sapinoso LM, Kern SG, Dimitrov P, Lapp H, Schultz PG, Powell SM, Moskaluk CA, Frierson HF Jr, Hampton GM (2001) Molecular classification of human carcinomas by use of gene expression signatures. Cancer Res 61(20):7388-7393 (Pubitemid 32995021)
80. Taylor JT, Huang L, Pottle JE, Liu K, Yang Y, Zeng X, Keyser BM, Agrawal KC, Hansen JB, Li M (2008) Selective blockade of T-type Ca2+ channels suppresses human breast cancer cell proliferation. Cancer Lett 267(1):116-124
81. Taylor JT, Zeng X-B, Pottle JE, Lee K, Wang AR, Yi SG, Scruggs JAS, Sikka SS, Li M (2008) Calciumsignaling and T-type calcium channels in cancer cell cycling. World J Gastroenterol WJG 14(32):4984-4991
82. Toyota M, Ho C, Ohe-Toyota M, Baylin SB, Issa JP (1999) Inactivation of CACNA1G, a T-type calcium channel gene, by aberrant methylation of its 5′ CpG island in human tumors. Cancer Res 59(18):4535-4541 (Pubitemid 29428953)
83. Trepel JB (2003) Ion channels as molecular targets in prostate cancer. Clin Prostate Cancer 2(3):188-189
84. Valerie NCK, Dziegielewska B, Hosing AS, Augustin E, Gray LS, Brautigan DL, Larner JM, Dziegielewski J (2013) Inhibition of T-type calcium channels disrupts Akt signaling and promotes apoptosis in glioblastoma cells. Biochem Pharmacol 85(7):888-897
85. Vanoverberghe K, Vanden Abeele F, Mariot P, Lepage G, Roudbaraki M, Bonnal JL, Mauroy B, Shuba Y, Skryma R, Prevarskaya N (2004) Ca2+ homeostasis and apoptotic resistance of neuroendocrine differentiated prostate cancer cells. Cell Death Differ 11(3):321-330 (Pubitemid 38313141)
86. Viana F, Van den Bosch L, Missiaen L, Vandenberghe W, Droogmans G, Nilius B, Robberecht W (1997) Mibefradil (Ro 40-5967) blocks multiple types of voltage-gated calcium channels in cultured rat spinal motoneurones. Cell Calcium 22(4):299-311 (Pubitemid 27490309)
87. Wang D, Hirase T, Inoue T, Node K (2006) Atorvastatin inhibits angiotensin II-induced T-type Ca2+ channel expression in endothelial cells. Biochem Biophys Res Commun 347(2):394-400 (Pubitemid 44041429)
88. Wang L, Bhattacharjee A, Zuo Z, Hu F, Honkanen RE, Berggren PO, Li M (1999) A low voltage-activated Ca2+ current mediates cytokine-induced pancreatic beta-cell death. Endocrinology 140(3):1200-1204 (Pubitemid 29104221)
89. Wilson WR, Hay MP (2011) Targeting hypoxia in cancer therapy. Nat Rev Cancer 11(6):393-410
90. Zhang Y, Cribbs LL, Satin J (2000) Arachidonic acid modulation of alpha1H, a cloned human T-type calcium channel. Am J Physiol Heart Circ Physiol 278(1):H184-193 (Pubitemid 30101870)
91. Zhang Y, Zhang J, Jiang D, Zhang D, Qian Z, Liu C, Tao J (2012) Inhibition of T-type Ca(2+) channels by endostatin attenuates human glioblastoma cell proliferation and migration. Br J Pharmacol 166(4):1247-1260