Cisplatin and oxaliplatin inhibit gap junctional communication by direct action and by reduction of connexin expression, thereby counteracting cytotoxic efficacy

Journal of Pharmacology and Experimental Therapeutics

Volumn 333, Issue 3, 2010, Pages 903-911

  Wang, Qin ^a   You, Tianhui ^b   Yuan, Dongdong ^a   Han, Xu ^a   Hong, Xiaoting ^a   He, Bo ^a   Wang, Lingzhi ^a   Tong, Xuhui ^c   Tao, Liang ^a   Harris, Andrew L ^d  

^a SUN YAT SEN UNIVERSITY   (China)

^b GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^c BENGBU MEDICAL COLLEGE   (China)

^d RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; GAP JUNCTION PROTEIN; OXALIPLATIN;

ARTICLE; CELL COMMUNICATION; CELL CULTURE; CELL DENSITY; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CELL SURVIVAL; CLONOGENESIS; CONTROLLED STUDY; CYTOTOXICITY; DRUG EXPOSURE; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTINEOPLASTIC AGENTS; BIOLOGICAL TRANSPORT, ACTIVE; BLOTTING, WESTERN; CELL COMMUNICATION; CELL SURVIVAL; CISPLATIN; COLORING AGENTS; CONNEXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GAP JUNCTIONS; HELA CELLS; HUMANS; LIPOSOMES; ORGANOPLATINUM COMPOUNDS;

EID: 77952393802     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.109.165274     Document Type: Article

References (54)

1. Aasen T, Graham SV, Edward M, and Hodgins MB (2005) Reduced expression of multiple gap junction proteins is a feature of cervical dysplasia. Mol Cancer 4:31. (Pubitemid 41461193)
2. Ammerpohl O, Trauzold A, Schniewind B, Griep U, Pilarsky C, Grutzmann R, Saeger HD, Janssen O, Sipos B, Kloppel G, et al. (2007) Complementary effects of HDAC inhibitor 4-PB on gap junction communication and cellular export mechanisms support restoration of chemosensitivity of PDAC cells. Br J Cancer 96:73-81. (Pubitemid 46094642)
3. Azzam EI, de Toledo SM, Gooding T, and Little JB (1998) Intercellular communication is involved in the bystander regulation of gene expression in human cells exposed to very low fluences of alpha particles. Radiat Res 150:497-504. (Pubitemid 28499048)
4. Azzam EI, de Toledo SM, and Little JB (2001) Direct evidence for the participation of gap junction-mediated intercellular communication in the transmission of damage signals from alpha-particle irradiated to nonirradiated cells. Proc Natl Acad Sci USA 98:473-478.
5. Bevans CG and Harris AL (1999) Regulation of connexin channels by pH. Direct action of the protonated form of taurine and other aminosulfonates. J Biol Chem 274:3711-3719.
6. Brehm R, Marks A, Rey R, Kliesch S, Bergmann M, and Steger K (2002) Altered expression of connexins 26 and 43 in Sertoli cells in seminiferous tubules infiltrated with carcinoma-in-situ or seminoma. J Pathol 197:647-653.
7. Chen W, Yan C, Hou J, Pu J, Ouyang J, and Wen D (2008) ATRA enhances bystander effect of suicide gene therapy in the treatment of prostate cancer. Urol Oncol 26:397-405. (Pubitemid 351885374)
8. Cronier L, Crespin S, Strale PO, Defamie N, and Mesnil M (2009) Gap junctions and cancer: new functions for an old story. Antioxid Redox Signal 11:323-338.
9. Cruikshank SJ, Hopperstad M, Younger M, Connors BW, Spray DC, and Srinivas M (2004) Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc Natl Acad Sci USA 101:12364-12369. (Pubitemid 39145449)
10. Dobrowolski R and Willecke K (2009) Connexin-caused genetic diseases and corresponding mouse models. Antioxid Redox Signal 11:283-295.
11. Erdlenbruch B, Nier M, Kern W, Hiddemann W, Pekrun A, and Lakomek M (2001) Pharmacokinetics of cisplatin and relation to nephrotoxicity in paediatric patients. Eur J Clin Pharmacol 57:393-402. (Pubitemid 33787190)
12. Fiorini C, Tilloy-Ellul A, Chevalier S, Charuel C, and Pointis G (2004) Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod Toxicol 18:413-421. (Pubitemid 38479877)
13. Fuertesa MA, Castillab J, Alonsoa C, and Pérez JM (2003) Cisplatin biochemical mechanism of action: from cytotoxicity to induction of cell death through interconnections between apoptotic and necrotic pathways. Curr Med Chem 10:257-266.
14. Gershon E, Plaks V, and Dekel N (2008) Gap junctions in the ovary: expression, localization and function. Mol Cell Endocrinol 282:18-25.
15. Goldberg GS, Bechberger JF, and Naus CC (1995) A pre-loading method of evaluating gap junctional communication by fluorescent dye transfer. Biotechniques 18:490-497.
16. Green CR, Harfst E, Gourdie RG, and Severs NJ (1988) Analysis of the rat liver gap junction protein: clarification of anomalies in its molecular size. Proc R Soc Lond B Biol Sci 233:165-174. (Pubitemid 18084016)
17. Hanna EA, Umhauer S, Roshong SL, Piechocki MP, Fernstrom MJ, Fanning JD, and Ruch RJ (1999) Gap junctional intercellular communication and connexin43 expression in human ovarian surface epithelial cells and ovarian carcinomas in vivo and in vitro. Carcinogenesis 20:1369-1373. (Pubitemid 29341463)
18. Harris AL (2001) Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34:325-472.
19. Harris AL, Walter A, Paul D, Goodenough DA, and Zimmerberg J (1992) Ion channels in single bilayers induced by rat connexin32. Brain Res Mol Brain Res 15:269-280.
20. He B, Tong X, Wang L, Wang Q, Ye H, Liu B, Hong X, Tao L, and Harris AL (2009) Tramadol and flurbiprofen depress the cytotoxicity of cisplatin via their effects on gap junctions. Clin Cancer Res 15:5803-5810.
21. Isakson BE, Evans WH, and Boitano S (2001a) Intercellular Ca2+ signaling in alveolar epithelial cells through gap junctions and by extracellular ATP. Am J Physiol Lung Cell Mol Physiol 280:L221-L228. (Pubitemid 32473213)
22. Isakson BE, Lubman RL, Seedorf GJ, and Boitano S (2001b) Modulation of pulmonary alveolar type II cell phenotype and communication by extracellular matrix and KGF. Am J Physiol Cell Physiol 281:C1291-C1299. (Pubitemid 32948118)
23. Isakson BE, Seedorf GJ, Lubman RL, Evans WH, and Boitano S (2003) Cell-cell communication in heterocellular cultures of alveolar epithelial cells. Am J Respir Cell Mol Biol 29:552-561.
24. Jamieson ER and Lippard SJ (1999) Structure, recognition, and processing of cisplatin- DNA adducts. Chem Rev 99:2467-2498.
25. Jensen R and Glazer PM (2004) Cell-interdependent cisplatin killing by Ku/DNA-dependent protein kinase signaling transduced through gap junctions. Proc Natl Acad Sci USA 101:6134-6139. (Pubitemid 38520540)
26. Judson I and Kelland LR (2000) New developments and approaches in the platinum arena. Drugs 59 (Suppl 4):29-36; discussion 37-38. (Pubitemid 30344989)
27. Kalvelyte A, Imbrasaite A, Bukauskiene A, Verselis VK, and Bukauskas FF (2003) Connexins and apoptotic transformation. Biochem Pharmacol 66:1661-1672.
28. Koreen IV, Elsayed WA, Liu YJ, and Harris AL (2004) Tetracycline- regulated expression enables purification and functional analysis of recombinant connexin channels from mammalian cells. Biochem J 383:111-119.
29. Krutovskikh VA, Piccoli C, Yamasaki H, and Yamasaki H (2002) Gap junction intercellular communication propagates cell death in cancerous cells. Oncogene 21:1989-1999. (Pubitemid 34270887)
30. Lawrence TS, Rehemtulla A, Ng EY, Wilson M, Trosko JE, and Stetson PL (1998) Preferential cytotoxicity of cells transduced with cytosine deaminase compared to bystander cells after treatment with 5-flucytosine. Cancer Res 58:2588-2593. (Pubitemid 28275430)
31. Lin JH, Weigel H, Cotrina ML, Liu S, Bueno E, Hansen AJ, Hansen TW, Goldman S, and Nedergaard M (1998) Gap-junction-mediated propagation and amplification of cell injury. Nat Neurosci 1:494-500. (Pubitemid 128406060)
32. Locke D, Koreen IV, Liu JY, and Harris AL (2004a) Reversible pore block of connexin channels by cyclodextrins. J Biol Chem 279:22883-22892. (Pubitemid 38685589)
33. Locke D, Stein T, Davies C, Morris J, Harris AL, Evans WH, Monaghan P, and Gusterson B (2004b) Altered permeability and modulatory character of connexin channels during mammary gland development. Exp Cell Res 298:643-660. (Pubitemid 38950879)
34. Loewenstein WR and Rose B (1992) The cell-cell channel in the control of growth. Semin Cell Biol 3:59-79.
35. Mesnil M (2002) Connexins and cancer. Biol Cell 94:493-500.
36. Mesnil M, Crespin S, Avanzo JL, and Zaidan-Dagli ML (2005) Defective gap junctional intercellular communication in the carcinogenic process. Biochim Biophys Acta 1719:125-145. (Pubitemid 41785641)
37. Mesnil M, Piccoli C, Tiraby G, Willecke K, and Yamasaki H (1996) Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins. Proc Natl Acad Sci USA 93:1831-1835. (Pubitemid 26079840)
38. Omori Y, Zaidan Dagli ML, Yamakage K, and Yamasaki H (2001) Involvement of gap junctions in tumor suppression: analysis of genetically-manipulated mice. Mutat Res 477:191-196. (Pubitemid 32480202)
39. Peterson-Roth E, Brdlik CM, and Glazer PM (2009) Src-induced cisplatin resistance mediated by cell-to-cell communication. Cancer Res 69:3619-3624.
40. Pointis G, Fiorini C, Defamie N, and Segretain D (2005) Gap junctional communication in the male reproductive system. Biochim Biophys Acta 1719:102-116. (Pubitemid 41785639)
41. Pointis G and Segretain D (2005) Role of connexin-based gap junction channels in testis. Trends Endocrinol Metab 16:300-306. (Pubitemid 41206636)
42. Procházka L, Turánek J, Tesarík R, Knotigová P, Polásková P, Andrysík Z, Kozubík A, Zák F, Sova P, Neuzil J, et al. (2007) Apoptosis and inhibition of gap-junctional intercellular communication induced by LA-12, a novel hydrophobic platinum(IV) complex. Arch Biochem Biophys 462:54-61. (Pubitemid 46755141)
43. Rüttinger C, Bergmann M, Fink L, Pesch S, Seitz K, Trautmann A, Steger K, Konrad L, and Brehm R (2008) Expression of connexin 43 in normal canine testes and canine testicular tumors. Histochem Cell Biol 130:537-548.
44. Tanaka M and Grossman HB (2001) Connexin 26 gene therapy of human bladder cancer: induction of growth suppression, apoptosis, and synergy with Cisplatin. Hum Gene Ther 12:2225-2236. (Pubitemid 34075186)
45. Tao L and Harris AL (2004) Biochemical requirements for inhibition of Connexin26-containing channels by natural and synthetic taurine analogs. J Biol Chem 279:38544-38554. (Pubitemid 39296008)
46. Tao L and Harris AL (2007) 2-aminoethoxydiphenyl borate directly inhibits channels composed of connexin26 and/or connexin32. Mol Pharmacol 71:570-579. (Pubitemid 46147921)
47. Udaka N, Miyagi Y, and Ito T (2007) Connexin expression in mouse lung tumor. Cancer Lett 246:224-229. (Pubitemid 44959393)
48. Umhauer S, Ruch RJ, and Fanning J (2000) Gap junctional intercellular communication and connexin 43 expression in ovarian carcinoma. Am J Obstet Gynecol 182:999-1000. (Pubitemid 30353260)
49. van Dillen IJ, Mulder NH, Vaalburg W, de Vries EF, and Hospers GA (2002) Influence of the bystander effect on HSV-tk/GCV gene therapy. A review. Curr Gene Ther 2:307-322.
50. Wang D and Lippard SJ (2005) Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 4:307-320. (Pubitemid 41130944)
51. Wernyj RP and Morin PJ (2004) Molecular mechanisms of platinum resistance: still searching for the Achilles' heel. Drug Resist Updat 7:227-232.
52. Yamasaki H, Mesnil M, Omori Y, Mironov N, and Krutovskikh V (1995) Intercellular communication and carcinogenesis. Mutat Res 333:181-188.
53. Zhao W, Lin ZX, and Zhang ZQ (2004) Cisplatin-induced premature senescence with concomitant reduction of gap junctions in human fibroblasts. Cell Res 14:60-66. (Pubitemid 43231831)
54. Zoidl G and Dermietzel R (2010) Gap junctions in inherited human disease. Pflugers Arch. [Epub ahead of print].