ClC-3 chloride channels are essential for cell proliferation and cell cycle progression in nasopharyngeal carcinoma cells

Acta Biochimica et Biophysica Sinica

Volumn 42, Issue 6, 2010, Pages 370-380

  Xu, Bin ^a   Mao, Jianwen ^a   Wang, Liwei ^b   Zhu, Linyan ^b   Li, Hongzhi ^a   Wang, Weizhang ^a   Jin, Xiaobao ^a   Zhu, Jiayong ^a   Chen, Lixin ^b  

^a GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^b MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

Author keywords

Antisense oligonucleotide; Cell cycle; Cell proliferation; Chloride channels; ClC 3

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CHLORIDE; CHLORIDE CHANNEL; CLC 3 CHANNEL; CLC-3 CHANNEL;

ARTICLE; BIOSYNTHESIS; CARCINOMA; CELL CYCLE; CELL PROLIFERATION; CELL SIZE; DRUG ANTAGONISM; HUMAN; MALE; METABOLISM; NASOPHARYNX TUMOR; PATCH CLAMP; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR CELL LINE; ANTAGONISTS AND INHIBITORS; PATCH CLAMP TECHNIQUE;

CARCINOMA; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SIZE; CHLORIDE CHANNELS; CHLORIDES; HUMANS; MALE; NASOPHARYNGEAL NEOPLASMS; OLIGONUCLEOTIDES, ANTISENSE; PATCH-CLAMP TECHNIQUES;

EID: 77952959961     PISSN: 16729145     EISSN: 17457270     Source Type: Journal    
DOI: 10.1093/abbs/gmq031     Document Type: Article

References (51)

1. Kunzelmann K. Ion channels and cancer. J Membr Biol 2005, 205: 159-173.
2. Fiske JL, Fomin VP, Brown ML, Duncan RL and Sikes RA. Voltage-sensitive ion channels and cancer. Cancer Metastasis Rev 2006, 25: 493-500.
3. Schreiber R. Ca2+ signaling, intracellular pH and cell volume in cell proliferation. J Membr Biol 2005, 205: 129-137.
4. Wang Z. Roles of K+ channels in regulating tumour cell proliferation and apoptosis. Pflugers Arch 2004, 448: 274-286.
5. Lu F, Chen H, Zhou C, Liu S, Guo M, Chen P and Zhuang H, et al. T-type Ca2+ channel expression in human esophageal carcinomas: a functional role in proliferation. Cell Calcium 2008, 43: 49-58.
6. Suh KS, Mutoh M, Gerdes M and Yuspa SH. CLIC4, an intracellular chloride channel protein, is a novel molecular target for cancer therapy. J Investig Dermatol Symp Proc 2005, 10: 105-109.
7. Beckley JR, Pauli BU and Elble RC. Re-expression of detachment-inducible chloride channel mCLCA5 suppresses growth of metastatic breast cancer cells. The J Biol Chem 2004, 279: 41634-41641.
8. Miyazaki H, Shiozaki A, Niisato N, Ohsawa R, Itoi H, Ueda Y and Otsuji E, et al. Chloride ions control the G1/S cell-cycle checkpoint by regulating the expression of p21 through a p53-independent pathway in human gastric cancer cells. Biochem Biophys Res Commun 2008, 366: 506-512.
9. Chen LX, Zhu LY, Jacob TJ and Wang LW. Roles of volume-activated Cl2 currents and regulatory volume decrease in the cell cycle and proliferation in nasopharyngeal carcinoma cells. Cell Prolif 2007, 40: 253-267.
10. Lang F, Shumilina E, Ritter M, Gulbins E, Vereninov A and Huber SM. Ion channels and cell volume in regulation of cell proliferation and apoptotic cell death. Contrib Nephrol 2006, 152: 142-160. (Pubitemid 44672106)
11. Sardini A, Amey JS, Weylandt KH, Nobles M, Valverde MA and Higgins CF. Cell volume regulation and swelling-activated chloride channels. Biochim Biophys Acta 2003, 1618: 153-162.
12. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E and Haussinger D. Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998, 78: 247-306. (Pubitemid 28070981)
13. Nilius B and Droogmans G. Amazing chloride channels: an overview. Acta Physiol Scand 2003, 177: 119-147.
14. Wondergem R, Gong W, Monen SH, Dooley SN, Gonce JL, Conner TD and Houser M, et al. Blocking swelling-activated chloride current inhibits mouse liver cell proliferation. J Physiol 2001, 532: 661-672.
15. Voets T, Szucs G, Droogmans G and Nilius B. Blockers of volume-activated Cl2 currents inhibit endothelial cell proliferation. Pflugers Arch 1995, 431: 132-134.
16. Ullrich N and Sontheimer H. Cell cycle-dependent expression of a glioma-specific chloride current: proposed link to cytoskeletal changes. Am J Physiol Cell Physiol 1997, 273: C1290-C1297.
17. Shen MR, Droogmans G, Eggermont J, Voets T, Ellory JC and Nilius B. Differential expression of volume-regulated anion channels during cell cycle progression of human cervical cancer cells. J Physiol 2000, 529: 385-394.
18. Ransom CB, O'Neal JT and Sontheimer H. Volume-activated chloride currents contribute to the resting conductance and invasive migration of human glioma cells. J Neurosci 2001, 21: 7674-7683.
19. Davies AR, Belsey MJ and Kozlowski RZ. Volume-sensitive organic osmolyte/anion channels in cancer: novel approaches to studying channel modulation employing proteomics technologies. Ann NY Acad Sci 2004, 1028: 38-55.
20. Chen L, Wang L, Zhu L, Nie S, Zhang J, Zhong P and Cai B, et al. Cell cycle-dependent expression of volume-activated chloride currents in nasopharyngeal carcinoma cells. Am J Physiol Cell Physiol 2002, 283: C1313-C1323.
21. Wang L, Chen L, Zhu L, Rawle M, Nie S, Zhang J and Ping Z, et al. Regulatory volume decrease is actively modulated during the cell cycle. J Cell Physiol 2002, 193: 110-119.
22. Uchida S, Kawasaki M, Sasaki S and Marumo F. Cloning and expression of a PKC-regulated chloride channel. Jpn J Physiol 1994, 44: S55-S62.
23. Duan D, Cowley S, Horowitz B and Hume JR. A serine residue in ClC-3 links phosphorylation-dephosphorylation to chloride channel regulation by cell volume. J Gen Physiol 1999, 113: 57-70.
24. Duan D, Winter C, Cowley S, Hume JR and Horowitz B. Molecular identification of a volume-regulated chloride channel. Nature 1997, 390: 417-421.
25. Wang L, Chen L and Jacob TJ. The role of ClC-3 in volume-activated chloride currents and volume regulation in bovine epithelial cells demonstrated by antisense inhibition. J Physiol 2000, 524: 63-75.
26. Duan D, Zhong J, Hermoso M, Satterwhite CM, Rossow CF, Hatton WJ and Yamboliev I, et al. Functional inhibition of native volume-sensitive outwardly rectifying anion channels in muscle cells and Xenopus oocytes by anti-ClC-3 antibody. J Physiol 2001, 531: 437-444.
27. Wang GX, Hatton WJ, Wang GL, Zhong J, Yamboliev I, Duan D and Hume JR. Functional effects of novel anti-ClC-3 antibodies on native volume-sensitive osmolyte and anion channels in cardiac and smooth muscle cells. Am J Physiol Heart Circ Physiol 2003, 285: H1453-H1463.
28. Jin NG, Kim JK, Yang DK, Cho SJ, Kim JM, Koh EJ and Jung HC, et al. Fundamental role of ClC-3 in volume-sensitive Cl2 channel function and cell volume regulation in AGS cells. Am J Physiol Gastrointest Liver Physiol 2003, 285: G938-G948.
29. Hermoso M, Satterwhite CM, Andrade YN, Hidalgo J, Wilson SM, Horowitz B and Hume JR. ClC-3 is a fundamental molecular component of volume-sensitive outwardly rectifying Cl2 channels and volume regulation in HeLa cells and Xenopus laevis oocytes. J Biol Chem 2002, 277: 40066-40074.
30. Wang GL, Wang XR, Lin MJ, He H, Lan XJ and Guan YY. Deficiency in ClC-3 chloride channels prevents rat aortic smooth muscle cell proliferation. Circ Res 2002, 91: E28-E32.
31. Qian JS, Pang RP, Zhu KS, Liu DY, Li ZR, Deng CY and Wang SM. Static pressure promotes rat aortic smooth muscle cell proliferation via upregulation of volume-regulated chloride channel. Cell Physiol Biochem 2009, 24: 461-470.
32. Tang YB, Liu YJ, Zhou JG, Wang GL, Qiu QY and Guan YY. Silence of ClC-3 chloride channel inhibits cell proliferation and the cell cycle via G/S phase arrest in rat basilar arterial smooth muscle cells. Cell Prolif 2008, 41: 775-785.
33. Habela CW, Olsen ML and Sontheimer H. ClC3 is a critical regulator of the cell cycle in normal and malignant glial cells. J Neurosci 2008, 28: 9205-9217.
34. Zhang HN, Zhou JG, Qiu QY, Ren JL and Guan YY. ClC-3 chloride channel prevents apoptosis induced by thapsigargin in PC12 cells. Apoptosis 2006, 11: 327-336.
35. Mao J, Chen L, Xu B, Wang L, Li H, Guo J and Li W, et al. Suppression of ClC-3 channel expression reduces migration of nasopharyngeal carcinoma cells. Biochem Pharmacol 2008, 75: 1706-1716.
36. Wang LW, Chen LX and Jacob T. ClC-3 expression in the cell cycle of nasopharyngeal carcinoma cells. Sheng Li Xue Bao 2004, 56: 230-236.
37. Doyle AGJ and Newell DG. Cell and Tissue Culture: Laboratory Procedures. Chichester: Wiley, 1993.
38. Gaffney EV. The accumulation and selective detachment of mitotic cells. Methods Cell Biol 1975, 9: 71-84.
39. Wu ZQ, Guo QL, You QD, Zhao L and Gu HY. Gambogic acid inhibits proliferation of human lung carcinoma SPC-A1 cells in vivo and in vitro and represses telomerase activity and telomerase reverse transcriptase mRNA expression in the cells. Biol Pharm Bull 2004, 27: 1769-1774.
40. Mao JW, Wang LW, Jacob T, Sun XR, Li H, Zhu LY and Li P, et al. Involvement of regulatory volume decrease in the migration of nasopharyngeal carcinoma cells. Cell Res 2005, 15: 371-378.
41. Aichberger KJ, Mayerhofer M, Gleixner KV, Krauth MT, Gruze A, Pickl WF and Wacheck V, et al. Identification of MCL1 as a novel target in neoplastic mast cells in systemic mastocytosis: inhibition of mast cell survival by MCL1 antisense oligonucleotides and synergism with PKC412. Blood 2007, 109: 3031-3041.
42. Tsang WP and Kwok TT. Riboregulator H19 induction of MDR1-associated drug resistance in human hepatocellular carcinoma cells. Oncogene 2007, 26: 4877-4881.
43. Iorns E, Lord CJ, Turner N and Ashworth A. Utilizing RNA interference to enhance cancer drug discovery. Nat Rev Drug Discov 2007, 6: 556-568.
44. Phipps DJ, Branch DR and Schlichter LC. Chloride-channel block inhibits T lymphocyte activation and signalling. Cell Signal 1996, 8: 141-149.
45. Nilius B, Prenen J, Kamouchi M, Viana F, Voets T and Droogmans G. Inhibition by mibefradil, a novel calcium channel antagonist, of Ca2+-and volume-activated Cl2 channels in macrovascular endothelial cells. Br J Pharmacol 1997, 121: 547-555.
46. Rouzaire-Dubois B, Milandri JB, Bostel S and Dubois JM. Control of cell proliferation by cell volume alterations in rat C6 glioma cells. Pflugers Arch 2000, 440: 881-888.
47. Jentsch TJ, Stein V, Weinreich F and Zdebik AA. Molecular structure and physiological function of chloride channels. Physiol Rev 2002, 82: 503-568.
48. Zhao Z, Li X, Hao J, Winston JH and Weinman SA. The ClC-3 chloride transport protein traffics through the plasma membrane via interaction of an N-terminal dileucine cluster with clathrin. J Biol Chem 2007, 282: 29022-29031.
49. Weylandt KH, Nebrig M, Jansen-Rosseck N, Amey JS, Carmena D, Wiedenmann B and Higgins CF, et al. ClC-3 expression enhances etoposide resistance by increasing acidification of the late endocytic compartment. Mol Cancer Ther 2007, 6: 979-986.
50. Hara-Chikuma M, Yang B, Sonawane ND, Sasaki S, Uchida S and Verkman AS. ClC-3 chloride channels facilitate endosomal acidification and chloride accumulation. J Biol Chem 2005, 280: 1241-1247.
51. Saurin AJ, Hamlett J, Clague MJ and Pennington SR. Inhibition of mitogen-induced DNA synthesis by bafilomycin A1 in Swiss 3T3 fibroblasts. Biochem J 1996, 313: 65-70.