Low-voltage-activated T-type Ca2+ channel inhibitors as new tools in the treatment of glioblastoma: The role of endostatin

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 4, 2014, Pages 811-818

  Zhang, Yuan ^a,c   Wang, Hua ^b,c   Qian, Zhiyuan ^a   Feng, Bo ^b   Zhao, Xianyang ^c   Jiang, Xinghong ^c   Tao, Jin ^a,c  

^a SOOCHOW UNIVERSITY   (China)

^b TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^c MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

Endostatin; Glioblastoma; Proliferation

Indexed keywords

CALCIUM CHANNEL T TYPE; ENDOSTATIN; SMALL INTERFERING RNA; CALCIUM CHANNEL BLOCKING AGENT;

BREAST CARCINOMA; CANCER CELL CULTURE; CELL PROLIFERATION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINOBLASTOMA; REVIEW; TUMOR GROWTH; ANIMAL; BRAIN NEOPLASMS; METABOLISM; PHYSIOLOGY; TREATMENT OUTCOME; TUMOR CELL LINE;

ANIMALS; BRAIN NEOPLASMS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, T-TYPE; CELL LINE, TUMOR; ENDOSTATINS; GLIOBLASTOMA; HUMANS; TREATMENT OUTCOME;

EID: 84896544445     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1427-5     Document Type: Review

References (80)

1. Belardetti F, Zamponi GW(2008) Linking calcium-channel isoforms to potential therapies. Curr Opin Investig Drugs 9:707-715 (Pubitemid 351950867)
2. Bertolesi GE, Shi C, Elbaum L, Jollimore C, Rozenberg G, Barnes S, Kelly ME (2002) The Ca(2+) channel antagonists mibefradil and pimozide inhibit cell growth via different cytotoxicmechanisms.Mol Pharmacol 62:210-219 (Pubitemid 34804099)
3. Bourinet E, Alloui A, Monteil A, Barrere C, Couette B, Poirot O, Pages A, McRory J, Snutch TP, Eschalier A, Nargeot J (2005) Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. EMBO J 24: 315-324 (Pubitemid 40216136)
4. Cain SM, Snutch TP (2010) Contributions of T-type calcium channel isoforms to neuronal firing. Channels (Austin) 4:475-482
5. Carbone E, Giancippoli A, Marcantoni A, Guido D, Carabelli V (2006) A new role for T-type channels in fast "low-threshold" exocytosis. Cell Calcium 40:147-154 (Pubitemid 43964484)
6. Catterall WA (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16:521-555
7. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J (2005) International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57:411-425 (Pubitemid 43036432)
8. Chemin J, Monteil A, Bourinet E, Nargeot J, Lory P (2001) Alternatively spliced alpha(1G) (Ca(V)3.1) intracellular loops promote specific T-type Ca(2+) channel gating properties. Biophys J 80: 1238-1250 (Pubitemid 32182151)
9. Chemin J, Monteil A, Briquaire C, Richard S, Perez-Reyes E, Nargeot J, Lory P (2000) Overexpression of T-type calcium channels in HEK-293 cells increases intracellular calcium without affecting cellular proliferation. FEBS Lett 478:166-172 (Pubitemid 30462279)
10. Chemin J,Monteil A, Dubel S, Nargeot J, Lory P (2001) The alpha1I T-type calcium channel exhibits faster gating properties when overexpressed in neuroblastoma/glioma NG 108-15 cells. Eur J Neurosci 14:1678-1686 (Pubitemid 35478036)
11. Chemin J, Nargeot J, Lory P (2007) Chemical determinants involved in anandamide-induced inhibition of T-type calcium channels. J Biol Chem 282:2314-2323 (Pubitemid 47076786)
12. Chemin J, Traboulsie A, Lory P (2006) Molecular pathways underlying themodulation of T-type calciumchannels by neurotransmitters and hormones. Cell Calcium 40:121-134 (Pubitemid 43942297)
13. Ciapa B, Pesando D, Wilding M, Whitaker M (1994) Cell-cycle calcium transients driven by cyclic changes in inositol trisphosphate levels. Nature 368:875-878
14. Cribbs LL (2006) T-type Ca2+ channels in vascular smooth muscle: multiple functions. Cell Calcium 40:221-230
15. Cribbs L (2010) T-type calcium channel expression and function in the diseased heart. Channels (Austin) 4:447-452
16. Garber SS, Hoshi T, Aldrich RW(1990) Interaction of forskolin with voltage-gated K+channels in PC12 cells. J Neurosci 10:3361-3368
17. Giordanetto F, Knerr L, Wallberg A (2011) T-type calcium channels inhibitors: a patent review. Expert Opin Ther Patent 21:85-101
18. Gray LS,Macdonald TL (2006) The pharmacology and regulation of T type calcium channels: new opportunities for unique therapeutics for cancer. Cell Calcium 40:115-120 (Pubitemid 43942296)
19. Gray LS, Perez-Reyes E, Gomora JC, Haverstick DM, Shattock M, McLatchie L, Harper J, Brooks G, Heady T, Macdonald TL (2004) The role of voltage gated T-type Ca2+ channel isoforms in mediating "capacitative" Ca2+ entry in cancer cells. Cell Calcium 36:489-497 (Pubitemid 39366137)
20. 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 60:1002-1008 (Pubitemid 30129537)
21. 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 309:193-199 (Pubitemid 38393130)
22. Huang JB, Kindzelskii AL, Clark AJ, Petty HR (2004) Identification of channels promoting calcium spikes and waves in HT1080 tumor cells: their apparent roles in cell motility and invasion. Cancer Res 64: 2482-2489 (Pubitemid 38523903)
23. Iftinca MC, Zamponi GW (2009) Regulation of neuronal T-type calcium channels. Trends Pharmacol Sci 30:32-40
24. Kim YM, Hwang S, Pyun BJ, Kim TY, Lee ST, Gho YS, Kwon YG (2002) Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J Biol Chem 277:27872-27879 (Pubitemid 34966733)
25. Kim D, Song I, Keum S, Lee T, Jeong MJ, Kim SS, McEnery MW, Shin HS (2001) Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels. Neuron 31:35-45 (Pubitemid 32757087)
26. Kunzelmann K (2005) Ion channels and cancer. J Membr Biol 205: 159-173
27. Lacinova L (2004) Pharmacology of recombinant low-voltage activated calcium channels. Curr Drug Targets CNS Neurol Disord 3: 105-111
28. Latour I, Louw DF, Beedle AM, Hamid J, Sutherland GR, Zamponi GW (2004) Expression of T-type calcium channel splice variants in human glioma. Glia 48:112-119 (Pubitemid 39545943)
29. Lee JH, Daud AN, Cribbs LL, Lacerda AE, Pereverzev A, Klockner U, Schneider T, Perez-Reyes E (1999) Cloning and expression of a novel member of the low voltage-activated T-type calcium channel family. J Neurosci 19:1912-1921 (Pubitemid 29133369)
30. Lee GL, Hait WN (1985) Inhibition of growth of C6 astrocytoma cells by inhibitors of calmodulin. Life Sci 36:347-354 (Pubitemid 15193339)
31. Lee YS, Lee BH, Park SJ, Kang SB, RhimH, Park JY, Lee JH, Jeong SW, Lee JY (2004) 3,4-Dihydroquinazoline derivatives as novel selective T-type Ca2+ channel blockers. Bioorg Med Chem Lett 14: 3379-3384 (Pubitemid 38737132)
32. LiM, Xiong ZG (2011) Ion channels as targets for cancer therapy. Int J Physiol Pathophysiol Pharmacol 3:156-166
33. Li W, Zhang SL, Wang N, Zhang BB, Li M (2011) Blockade of Ttype Ca(2+) channels inhibits human ovarian cancer cell proliferation. Cancer Invest 29:339-346
34. Lory P, Bidaud I, Chemin J (2006) T-type calcium channels in differentiation and proliferation. Cell Calcium 40:135-146 (Pubitemid 43964483)
35. Lu F, Chen H, Zhou C, Liu S, GuoM, 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 43:49-58
36. Lu F, Chen H, Zhou C, Wu S (2005) Is there a role for T-type Ca2+ channel in glioma cell proliferation? Cell Calcium 38:593-595, author reply 597
37. Machaca K (2011) Ca(2+) signaling, genes and the cell cycle. Cell Calcium 49:323-330
38. 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 277:10824-10833 (Pubitemid 34952836)
39. Marshall E (2002) Cancer therapy. Setbacks for endostatin. Science 295:2198-2199
40. McCalmont WF, Heady TN, Patterson JR, Lindenmuth MA, Haverstick DM, Gray LS, Macdonald TL (2004) Design, synthesis, and biological evaluation of novel T-Type calcium channel antagonists. Bioorg Med Chem Lett 14:3691-3695 (Pubitemid 38760064)
41. McGivern JG (2006) Pharmacology and drug discovery for T-type calcium channels. CNS Neurol Disord Drug Targets 5:587-603
42. McRory JE, Santi CM, Hamming KS, Mezeyova J, Sutton KG, Baillie DL, Stea A, Snutch TP (2001) Molecular and functional characterization of a family of rat brain T-type calcium channels. J Biol Chem 276:3999-4011
43. Minor DL Jr, Findeisen F (2010) Progress in the structural understanding of voltage-gated calcium channel (CaV) function and modulation. Channels (Austin) 4:459-474
44. Monteil A, Chemin J, Bourinet E, Mennessier G, Lory P, Nargeot J (2000) Molecular and functional properties of the human alpha(1G) subunit that forms T-type calcium channels. J Biol Chem 275:6090-6100 (Pubitemid 30129892)
45. Monteil A, Chemin J, Leuranguer V, Altier C, Mennessier G, Bourinet E, Lory P, Nargeot J (2000) Specific properties of T-type calcium channels generated by the human alpha 1I subunit. J Biol Chem 275:16530-16535 (Pubitemid 30398876)
46. Monteith GR, Davis FM, Roberts-Thomson SJ (2012) Calcium channels and pumps in cancer: changes and consequences. J Biol Chem 287:31666-31673
47. Murbartian J, Arias JM, Lee JH, Gomora JC, Perez-Reyes E (2002) Alternative splicing of the rat Ca(v)3.3 T-type calcium channel gene produces variants with distinct functional properties(1). FEBS Lett 528:272-278 (Pubitemid 35258038)
48. Nilius B, Prenen J, Kamouchi M, Viana F, Voets T, Droogmans G (1997) Inhibition by mibefradil, a novel calcium channel antagonist, of Ca(2+)- and volume-activated Cl- channels in macrovascular endothelial cells. Br J Pharmacol 121:547-555 (Pubitemid 27226309)
49. 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 Calcium37:105-119 (Pubitemid 40017369)
50. Panner A, Wurster RD (2006) T-type calcium channels and tumor proliferation. Cell Calcium 40:253-259 (Pubitemid 43942305)
51. Park SJ, LeeMJ, Rhim H, Kim Y, Lee JH, Chung BY, Lee JY (2006) Synthesis and SAR studies of a novel series of T-type calcium channel blockers. Bioorg Med Chem 14:3502-3511
52. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83:117-161
53. Perez-Reyes E, Cribbs LL, Daud A, Lacerda AE, Barclay J, Williamson MP, Fox M, Rees M, Lee JH (1998) Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature 391:896-900 (Pubitemid 28157667)
54. Perez-Reyes E, Lory P (2006) Molecular biology of T-type calcium channels. CNS Neurol Disord Drug Targets 5:605-609 (Pubitemid 44890572)
55. Peroulis I, Jonas N, Saleh M (2002) Antiangiogenic activity of endostatin inhibits C6 glioma growth. Int J Cancer 97:839-845 (Pubitemid 34106342)
56. Richard S, Neveu D, Carnac G, Bodin P, Travo P, Nargeot J (1992) Differential expression of voltage-gated Ca(2+)-currents in cultivated aortic myocytes. Biochim Biophys Acta 1160:95-104
57. Rouzaire-Dubois B, Dubois JM (1998) K+channel block-induced mammalian neuroblastoma cell swelling: a possible mechanism to influence proliferation. J Physiol 510(Pt 1):93-102 (Pubitemid 28351927)
58. 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 166:1244-1246
59. Schmidt NO, Ziu M, Carrabba G, Giussani C, Bello L, Sun Y, Schmidt K, Albert M, Black PM, Carrol l RS (2004) Antiangiogenic therapy by local intracerebral microinfusion improves treatment efficiency and survival in an orthotopic human glioblastoma model. Clin Cancer Res 10:1255-1262 (Pubitemid 38365215)
60. Schmitt R, Clozel JP, Iberg N, Buhler FR (1995)Mibefradil prevents neointima formation after vascular injury in rats. Possible role of the blockade of the T-type voltage-operated calcium channel. Arterioscler Thromb Vasc Biol 15:1161-1165
61. Singh A, Hildebrand ME, Garcia E, Snutch TP (2010) The transient receptor potential channel antagonist SKF96365 is a potent blocker of low-voltage-activated T-type calcium channels. Br J Pharmacol 160:1464-1475
62. Skovseth DK, Veuger MJ, Sorensen DR, De Angelis PM, Haraldsen G (2005) Endostatin dramatically inhibits endothelial cell migration, vascular morphogenesis, and perivascular cell recruitment in vivo. Blood 105:1044-1051 (Pubitemid 40170874)
63. Talavera K, Nilius B (2006) Biophysics and structure-function relationship of T-type Ca2+ channels. Cell Calcium 40:97-114 (Pubitemid 43942295)
64. Talavera K, Staes M, Janssens A, Droogmans G, Nilius B (2004) Mechanism of arachidonic acid modulation of the T-type Ca2+ channel alpha1G. J Gen Physiol 124:225-238 (Pubitemid 39244523)
65. Taylor JT, Zeng XB, Pottle JE, Lee K,Wang AR, Yi SG, Scruggs JA, Sikka SS, Li M (2008) Calcium signaling and T-type calcium channels in cancer cell cycling. World J Gastroenterol 14:4984-4991
66. 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 59:4535-4541 (Pubitemid 29428953)
67. Trimarchi T, Pachuau J, Shepherd A, Dey D, Martin-Caraballo M (2009) CNTF-evoked activation of JAK and ERK mediates the functional expression of T-type Ca2+ channels in chicken nodose neurons. J Neurochem 108:246-259
68. Turner RW, Anderson D, Zamponi GW(2011) Signaling complexes of voltage-gated calcium channels. Channels (Austin) 5:440-448
69. Vassort G, Talavera K, Alvarez JL (2006) Role of T-type Ca2+ channels in the heart. Cell Calcium 40:205-220 (Pubitemid 43942302)
70. Wang YQ, Brooks G, Zhu CB, Yuan WZ, Li YQ, Wu XS (2002) Functional analysis of the human T-type calcium channel alpha 1H subunit gene in cellular proliferation. Yi Chuan Xue Bao 29:659-665
71. Wang Z, Estacion M, Mordan LJ (1993) Ca2+ influx via T-type channels modulates PDGF-induced replication of mouse fibroblasts. Am J Physiol 265:C1239-C1246
72. Wang G, Lemos JR, Iadecola C (2004) Herbal alkaloid tetrandrine: from an ion channel blocker to inhibitor of tumor proliferation. Trends Pharmacol Sci 25:120-123 (Pubitemid 38264500)
73. Wickstrom SA, Alitalo K, Keski-Oja J (2002) Endostatin associates with integrin alpha5beta1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells. Cancer Res 62:5580-5589
74. Wondergem R, GongW, Monen SH, Dooley SN, Gonce JL, Conner TD, Houser M, Ecay TW, Ferslew KE (2001) Blocking swelling-activated chloride current inhibits mouse liver cell proliferation. J Physiol 532:661-672 (Pubitemid 32427882)
75. Xu XP, Best PM (1990) Increase in T-type calcium current in atrial myocytes from adult rats with growth hormone-secreting tumors. Proc Natl Acad Sci U S A 87:4655-4659
76. Yang L, Lin Z, Lin J, Weng S, Huang Q, Zhang P, Fu J (2011) Antitumor effect of endostatin overexpressed in C6 glioma cells is associated with the down-regulation of VEGF. Int J Oncol 38:465-471
77. Yoshida M, Nosaka K, Yasunaga J, Nishikata I, Morishita K, Matsuoka M (2004) Aberrant expression of the MEL1S gene identified in association with hypomethylation in adult T-cell leukemia cells. Blood 103:2753-2760 (Pubitemid 38393034)
78. Zhang Y, Jiang X, Snutch TP, Tao J (2013) Modulation of low-voltage- activated T-type Ca(2)(+) channels. Biochim Biophys Acta 1828:1550-1559
79. 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 166:1247-1260
80. Zhong X, Liu JR, Kyle JW, Hanck DA, AgnewWS (2006) A profile of alternative RNA splicing and transcript variation of CACNA1H, a human T-channel gene candidate for idiopathic generalized epilepsies. Hum Mol Genet 15:1497-1512