The TRPC channel blocker SKF 96365 inhibits glioblastoma cell growth by enhancing reverse mode of the Na+/Ca2+ exchanger and increasing intracellular Ca2+

British Journal of Pharmacology

Volumn 171, Issue 14, 2014, Pages 3432-3447

  Song, M ^a   Chen, D ^a   Yu, Shan Ping ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

calcium; cell cycle; cell death; glioblastoma; SKF 96365; TRPC channel

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; CALCIUM ION; EGTAZIC ACID; MITOGEN ACTIVATED PROTEIN KINASE P38; SMALL INTERFERING RNA; SODIUM CALCIUM EXCHANGE PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; 1-(2-METHYLPHENYL)-4-METHYLAMINO-6-METHYL-2,3-DIHYDROPYRROLO(3,2-C)QUINOLINE; AMINOQUINOLINE DERIVATIVE; ANTINEOPLASTIC AGENT; CALCIUM;

ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; GLIOBLASTOMA; GLIOBLASTOMA CELL; HUMAN; HUMAN CELL; IMAGING; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; METABOLISM; PATHOLOGY; STRUCTURE ACTIVITY RELATION; TUMOR CELL CULTURE;

AMINOQUINOLINES; ANTINEOPLASTIC AGENTS; CALCIUM; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; GLIOBLASTOMA; HUMANS; SODIUM-CALCIUM EXCHANGER; STRUCTURE-ACTIVITY RELATIONSHIP; TRPC CATION CHANNELS; TUMOR CELLS, CULTURED;

EID: 84903208768     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12691     Document Type: Article

References (60)

1. Abramowitz J, Yildirim E, Birnbaumer L, (2007). The TRPC family of ion channels: relation to the TRP superfamily and role in receptor- and store-operated calcium entry. In:, Liedtke WB, Heller S, (eds). TRP Ion Channel Function in Sensory Transduction and Cellular Signaling Cascades. CRC Press: Boca Raton, FL, pp. 1-26.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: Transporters. Br J Pharmacol 170: 1706-1796.
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Ion Channels. Br J Pharmacol 170: 1607-1651.
4. Amaral MD, Pozzo-Miller L, (2007). BDNF induces calcium elevations associated with IBDNF, a non-selective cationic current mediated by TRPC channels. J Neurophysiol 98: 2476-2482.
5. 2+ exchanger: from molecular biology to therapeutic perspectives. Pharmacol Rev 56: 633-654.
6. Antigny F, Jousset H, Konig S, Frieden M, (2011). Thapsigargin activates Ca(2)+ entry both by store-dependent, STIM1/Orai1-mediated, and store-independent, TRPC3/PLC/PKC-mediated pathways in human endothelial cells. Cell Calcium 49: 115-127.
7. Ashwell JD, (2006). The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nat Rev Immunol 6: 532-540.
8. Berridge MJ, Bootman MD, Lipp P, (1998). Calcium-a life and death signal. Nature 395: 645-648.
9. Berridge MJ, Lipp P, Bootman MD, (2000). The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11-21.
10. Blaustein MP, Juhaszova M, Golovina VA, Church PJ, Stanley EF, (2002). Na/Ca exchanger and PMCA localization in neurons and astrocytes: functional implications. Ann N Y Acad Sci 976: 356-366.
11. Bomben VC, Sontheimer HW, (2008). Inhibition of transient receptor potential canonical channels impairs cytokinesis in human malignant gliomas. Cell Prolif 41: 98-121.
12. Brat DJ, Prayson RA, Ryken TC, Olson JJ, (2008). Diagnosis of malignant glioma: role of neuropathology. J Neurooncol 89: 287-311.
13. Cai R, Ding X, Zhou K, Shi Y, Ge R, Ren G, et al. (2009). Blockade of TRPC6 channels induced G2/M phase arrest and suppressed growth in human gastric cancer cells. Int J Cancer 125: 2281-2287.
14. Cheng KT, Ong HL, Liu X, Ambudkar IS, (2013). Contribution and regulation of TRPC channels in store-operated Ca(2+) entry. Curr Top Membr 71: 149-179.
15. Chigurupati S, Venkataraman R, Barrera D, Naganathan A, Madan M, Paul L, et al. (2010). Receptor channel TRPC6 is a key mediator of Notch-driven glioblastoma growth and invasiveness. Cancer Res 70: 418-427.
16. Clapham DE, (2007). Calcium signaling. Cell 131: 1047-1058.
17. Ding X, He Z, Zhou K, Cheng J, Yao H, Lu D, et al. (2010). Essential role of TRPC6 channels in G2/M phase transition and development of human glioma. J Natl Cancer Inst 102: 1052-1068.
18. DiPolo R, Beauge L, (2006). Sodium/calcium exchanger: influence of metabolic regulation on ion carrier interactions. Physiol Rev 86: 155-203.
19. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, et al. (2007). Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 21: 2683-2710.
20. Gutierrez GJ, Tsuji T, Cross JV, Davis RJ, Templeton DJ, Jiang W, et al. (2010). JNK-mediated phosphorylation of Cdc25C regulates cell cycle entry and G(2)/M DNA damage checkpoint. J Biol Chem 285: 14217-14228.
21. Harmar AJ, Hills RA, Rosser EM, Jones M, Buneman OP, Dunbar DR, et al. (2009). IUPHAR-DB: the IUPHAR database of G protein-coupled receptors and ion channels. Nucleic Acids Res 37 (Database issue): D680-D685.
22. 2+ exchanger expressed in human cell lines. J Physiol 548 (Pt 3): 677-689.
23. Hotta A, Kim YC, Nakamura E, Kito Y, Yamamoto Y, Suzuki H, (2005). Effects of inhibitors of nonselective cation channels on the acetylcholine-induced depolarization of circular smooth muscle from the guinea-pig stomach antrum. J Smooth Muscle Res 41: 313-327.
24. 2+ concentration without production of nitric oxide and von Willebrand factor. Cell Calcium 20: 501-508.
25. 2+ exchange inhibitor that preferentially inhibits NCX3, efficiently protects against hypoxia/reoxygenation-induced SH-SY5Y neuronal cell damage. Mol Pharmacol 70: 2075-2083.
26. 2+ entry. Naunyn Schmiedebergs Arch Pharmacol 359: 92-101.
27. Jia Y, Zhou J, Tai Y, Wang Y, (2007). TRPC channels promote cerebellar granule neuron survival. Nat Neurosci 10: 559-567.
28. 2+ influx in cerebellar Purkinje neurons. Neuroscience 131: 589-599.
29. Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, Simon M, et al. (2007). Long-term survival with glioblastoma multiforme. Brain 130 (Pt 10): 2596-2606.
30. Kuhn SA, Mueller U, Hanisch UK, Regenbrecht CR, Schoenwald I, Brodhun M, et al. (2009). Glioblastoma cells express functional cell membrane receptors activated by daily used medical drugs. J Cancer Res Clin Oncol 135: 1729-1745.
31. Labelle D, Jumarie C, Moreau R, (2007). Capacitative calcium entry and proliferation of human osteoblast-like MG-63 cells. Cell Prolif 40: 866-884.
32. 2+ channel antagonists. Mol Chem Neuropathol 22: 81-95.
33. Leung YM, Kwan CY, Loh TT, (1996). Dual effects of SK&F 96365 in human leukemic HL-60 cells. Inhibition of calcium entry and activation of a novel cation influx pathway. Biochem Pharmacol 51: 605-612.
34. Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, et al. (2005). Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434: 894-898.
35. Liu H, Hughes JD, Rollins S, Chen B, Perkins E, (2011). Calcium entry via ORAI1 regulates glioblastoma cell proliferation and apoptosis. Exp Mol Pathol 91: 753-760.
36. Lytton J, Westlin M, Hanley MR, (1991). Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem 266: 17067-17071.
37. Merritt JE, Armstrong WP, Benham CD, Hallam TJ, Jacob R, Jaxa-Chamiec A, et al. (1990). SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem J 271: 515-522.
38. 2+ exchanger protein isoforms, NCX1, NCX2, and NCX3 in cerebral cortex and hippocampus of adult rat. Cell Calcium 41: 221-234.
39. 2+ exchanger 3 (NCX3) gene leads to a worsening of ischemic brain damage. J Neurosci 28: 1179-1184.
40. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. (2008). An integrated genomic analysis of human glioblastoma multiforme. Science 321: 1807-1812.
41. Rahman M, Inman M, Kiss L, Janssen LJ, (2012). Reverse-mode NCX current in mouse airway smooth muscle: Na(+) and voltage dependence, contributions to Ca(2+) influx and contraction, and altered expression in a model of allergen-induced hyperresponsiveness. Acta Physiol (Oxf) 205: 279-291.
42. Rao JS, (2003). Molecular mechanisms of glioma invasiveness: the role of proteases. Nat Rev Cancer 3: 489-501.
43. 2+ for cancer cell proliferation and survival. Nat Rev Cancer 8: 361-375.
44. Rosen LB, Ginty DD, Weber MJ, Greenberg ME, (1994). Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12: 1207-1221.
45. Schwarz G, Droogmans G, Nilius B, (1994). Multiple effects of SK&F 96365 on ionic currents and intracellular calcium in human endothelial cells. Cell Calcium 15: 45-54.
46. See V, Rajala NK, Spiller DG, White MR, (2004). Calcium-dependent regulation of the cell cycle via a novel MAPK-NF-kappaB pathway in Swiss 3T3 cells. J Cell Biol 166: 661-672.
47. 2+ entry: roles of Orai, Stim and TRP. Biochim Biophys Acta 1763: 1147-1160.
48. Sokolow S, Luu SH, Headley AJ, Hanson AY, Kim T, Miller CA, et al. (2011). High levels of synaptosomal Na(+)-Ca(2+) exchangers (NCX1, NCX2, NCX3) co-localized with amyloid-beta in human cerebral cortex affected by Alzheimer's disease. Cell Calcium 49: 208-216.
49. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. (2005). Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352: 987-996.
50. Thurneysen T, Nicoll DA, Philipson KD, Porzig H, (2002). Sodium/calcium exchanger subtypes NCX1, NCX2 and NCX3 show cell-specific expression in rat hippocampus cultures. Brain Res Mol Brain Res 107: 145-156.
51. Van Meir E, Sawamura Y, Diserens AC, Hamou MF, de Tribolet N, (1990). Human glioblastoma cells release interleukin 6 in vivo and in vitro. Cancer Res 50: 6683-6688.
52. Van Meir E, Ceska M, Effenberger F, Walz A, Grouzmann E, Desbaillets I, et al. (1992). Interleukin-8 is produced in neoplastic and infectious diseases of the human central nervous system. Cancer Res 52: 4297-4305.
53. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ, (2010). Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 60: 166-193.
54. Varnai P, Hunyady L, Balla T, (2009). STIM and Orai: the long-awaited constituents of store-operated calcium entry. Trends Pharmacol Sci 30: 118-128.
55. Verkhratsky A, Orkand RK, Kettenmann H, (1998). Glial calcium: homeostasis and signaling function. Physiol Rev 78: 99-141.
56. Verkhratsky A, Rodriguez JJ, Parpura V, (2012). Calcium signalling in astroglia. Mol Cell Endocrinol 353: 45-56.
57. Wang GX, Poo MM, (2005). Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434: 898-904.
58. Yang S, Zhang JJ, Huang XY, (2009). Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 15: 124-134.
59. 2+ exchange currents in cortical neurons: concomitant forward and reverse operation and effect of glutamate. Eur J Neurosci 9: 1273-1281.
60. Zhou X, Wei J, Song M, Francis K, Yu SP, (2011). Novel role of KCNQ2/3 channels in regulating neuronal cell viability. Cell Death Differ 18: 493-505.