Gap junctions propagate opposite effects in normal and tumor testicular cells in response to cisplatin

Cancer Letters

Volumn 317, Issue 2, 2012, Pages 165-171

  Hong, Xiaoting ^a   Wang, Qin ^a   Yang, Yan ^a   Zheng, Suping ^a   Tong, Xuhui ^b   Zhang, Suzhi ^a   Tao, Liang ^a   Harris, Andrew L ^c  

^a SUN YAT SEN UNIVERSITY   (China)

^b BENGBU MEDICAL COLLEGE   (China)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Bystander effect; Cancer; Chemotherapy; Cisplatin; Gap junction

Indexed keywords

CISPLATIN;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CELL DENSITY; CELL FUNCTION; CELL JUNCTION; CELL PROTECTION; CELL TYPE; CONTROLLED STUDY; CYTOTOXICITY; DNA CROSS LINKING; GAP JUNCTION; GAP JUNCTIONAL INTERCELLULAR COMMUNICATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL COMMUNICATION; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; CONNEXIN 43; GAP JUNCTIONS; GLYCYRRHETINIC ACID; LEYDIG CELLS; MALE; MICE; RNA INTERFERENCE; SERTOLI CELLS; TESTICULAR NEOPLASMS; TESTIS;

EID: 84856625041     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.11.019     Document Type: Article

References (56)

1. Sosinsky G.E., Nicholson B.J. Structural organization of gap junction channels. Biochim. Biophys. Acta 2005, 1711:99-125.
2. Harris A.L. Connexin channel permeability to cytoplasmic molecules. Prog. Biophys. Mol. Biol. 2007, 94:120-143.
3. Vinken M., Vanhaecke T., Papeleu P., Snykers S., Henkens T., Rogiers V. Connexins and their channels in cell growth and cell death. Cell Signal 2006, 18:592-600.
4. Kandouz M., Batist G. Gap junctions and connexins as therapeutic targets in cancer. Expert Opin. Ther. Targets 2010, 14:681-692.
5. Naus C.C., Laird D.W. Implications and challenges of connexin connections to cancer. Nat. Rev. Cancer 2010, 10:435-441.
6. Cronier L., Crespin S., Strale P.O., Defamie N., Mesnil M. Gap junctions and cancer: new functions for an old story. Antioxid. Redox. Signal 2009, 11:323-338.
7. Loewenstein W.R., Kanno Y. Intercellular communication and the control of tissue growth: lack of communication between cancer cells. Nature 1966, 209:1248-1249.
8. Leithe E., Sirnes S., Omori Y., Rivedal E. Downregulation of gap junctions in cancer cells. Crit. Rev. Oncog. 2006, 12:225-256.
9. Enomoto T., Yamasaki H. Lack of intercellular communication between chemically transformed and surrounding nontransformed BALB/c 3T3 cells. Cancer Res. 1984, 44:5200-5203.
10. Trosko J.E., Chang C.C., Madhukar B.V., Klaunig J.E. Chemical, oncogene and growth factor inhibition gap junctional intercellular communication: an integrative hypothesis of carcinogenesis. Pathobiology 1990, 58:265-278.
11. Krutovskikh V.A., Piccoli C., Yamasaki H. Gap junction intercellular communication propagates cell death in cancerous cells. Oncogene 2002, 21:1989-1999.
12. el-Sabban M.E., Pauli B.U. Adhesion-mediated gap junctional communication between lung-metastatatic cancer cells and endothelium. Invas. Metast. 1994, 14:164-176.
13. Oliveira R., Christov C., Guillamo J.S., de Bouard S., Palfi S., Venance L., et al. BMC Cell Biol. 2005, 6:7.
14. Ito A., Katoh F., Kataoka T.R., Okada M., Tsubota N., Asada H., et al. A role for heterologous gap junctions between melanoma and endothelial cells in metastasis. J. Clin. Invest. 2000, 105:1189-1197.
15. Czyz J. The stage-specific function of gap junctions during tumourigenesis. Cell Mol. Biol. Lett. 2008, 13:92-102.
16. Kapoor P., Saunders M.M., Li Z., Zhou Z., Sheaffer N., Kunze E.L., et al. Breast cancer metastatic potential: correlation with increased heterotypic gap junctional intercellular communication between breast cancer cells and osteoblastic cells. Int. J. Cancer 2004, 111:693-697.
17. Elzarrad M.K., Haroon A., Willecke K., Dobrowolski R., Gillespie M.N., Al-Mehdi A.B. Connexin-43 upregulation in micrometastases and tumor vasculature and its role in tumor cell attachment to pulmonary endothelium. BMC Med. 2008, 6:20.
18. McLachlan E., Shao Q., Laird D.W. Connexins and gap junctions in mammary gland development and breast cancer progression. J. Membr. Biol. 2007, 218:107-121.
19. Ito A., Koma Y., Uchino K., Okada T., Ohbayashi C., Tsubota N., et al. Increased expression of connexin 26 in the invasive component of lung squamous cell carcinoma: significant correlation with poor prognosis. Cancer Lett. 2006, 234:239-248.
20. He B., Tong X., Wang L., Wang Q., Ye H., Liu B., et al. Tramadol and flurbiprofen depress the cytotoxicity of cisplatin via their effects on gap junctions. Clin. Cancer Res. 2009, 15:5803-5810.
21. Huang R.P., Hossain M.Z., Huang R., Gano J., Fan Y., Boynton A.L. Connexin 43 (cx43) enhances chemotherapy-induced apoptosis in human glioblastoma cells. Int. J. Cancer 2001, 92:130-138.
22. Jensen R., Glazer P.M. Cell-interdependent cisplatin killing by Ku/DNA-dependent protein kinase signaling transduced through gap junctions. Proc. Natl. Acad. Sci. USA 2004, 101:6134-6139.
23. Wang Q., You T., Yuan D., Han X., Hong X., He B., et al. thereby counteracting cytotoxic efficacy. J. Pharmacol. Exp. Ther. 2010, 333:903-911.
24. Harada K., Nonaka T., Hamada N., Sakurai H., Hasegawa M., Funayama T., et al. Heavy-ion-induced bystander killing of human lung cancer cells: role of gap junctional intercellular communication. Cancer Sci. 2009, 100:684-688.
25. Carystinos G.D., Alaoui-Jamali M.A., Phipps J., Yen L., Batist G. Upregulation of gap junctional intercellular communication and connexin 43 expression by cyclic-AMP and all-trans-retinoic acid is associated with glutathione depletion and chemosensitivity in neuroblastoma cells. Cancer Chemother. Pharmacol. 2001, 47:126-132.
26. Mesnil M., Piccoli C., Tiraby G., Willecke K., Yamasaki H. Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins. Proc. Natl. Acad. Sci. USA 1996, 93:1831-1835.
27. Vrionis F.D., Wu J.K., Qi P., Waltzman M., Cherington V., Spray D.C. The bystander effect exerted by tumor cells expressing the herpes simplex virus thymidine kinase (HSVtk) gene is dependent on connexin expression and cell communication via gap junctions. Gene Ther. 1997, 4:577-585.
28. Trosko J.E., Ruch R.J. Gap junctions as targets for cancer chemoprevention and chemotherapy. Curr. Drug Targets 2002, 3:465-482.
29. Burrows F.J., Gore M., Smiley W.R., Kanemitsu M.Y., Jolly D.J., Read S.B., et al. Purified herpes simplex virus thymidine kinase retroviral particles: III. Characterization of bystander killing mechanisms in transfected tumor cells. Cancer Gene Ther. 2002, 9:87-95.
30. Cottin S., Gould P.V., Cantin L., Caruso M. Gap junctions in human glioblastomas: implications for suicide gene therapy. Cancer Gene Ther. 2011.
31. Garcia-Rodriguez L., Perez-Torras S., Carrio M., Cascante A., Garcia-Ribas I., Mazo A., et al. Connexin-26 is a key factor mediating gemcitabine bystander effect. Mol. Cancer Ther. 2011, 10:505-517.
32. Matuskova M., Hlubinova K., Pastorakova A., Hunakova L., Altanerova V., Altaner C., et al. HSV-tk expressing mesenchymal stem cells exert bystander effect on human glioblastoma cells. Cancer Lett. 2010, 290:58-67.
33. Hutnik C.M., Pocrnich C.E., Liu H., Laird D.W., Shao Q. The protective effect of functional connexin43 channels on a human epithelial cell line exposed to oxidative stress. Invest. Ophthalmol. Vis. Sci. 2008, 49:800-806.
34. Nakase T., Fushiki S., Naus C.C. Astrocytic gap junctions composed of connexin 43 reduce apoptotic neuronal damage in cerebral ischemia. Stroke 2003, 34:1987-1993.
35. Contreras J.E., Sanchez H.A., Veliz L.P., Bukauskas F.F., Bennett M.V., Saez J.C. Role of connexin-based gap junction channels and hemichannels in ischemia-induced cell death in nervous tissue. Brain Res. Brain Res. Rev. 2004, 47:290-303.
36. Ozog M.A., Siushansian R., Naus C.C. Blocked gap junctional coupling increases glutamate-induced neurotoxicity in neuron-astrocyte co-cultures. J. Neuropathol. Exp. Neurol. 2002, 61:132-141.
37. Goldberg G.S., Bechberger J.F., Naus C.C. A pre-loading method of evaluating gap junctional communication by fluorescent dye transfer. Biotechniques 1995, 18:490-497.
38. de Jong S., Zijlstra J.G., Timmer-Bosscha H., Mulder N.H., de Vries E.G. Detection of DNA cross-links in tumor cells with the ethidium bromide fluorescence assay. Int. J. Cancer 1986, 37:557-561.
39. Davidson J.S., Baumgarten I.M., Harley E.H. Reversible inhibition of intercellular junctional communication by glycyrrhetinic acid. Biochem. Biophys. Res. Commun. 1986, 134:29-36.
40. Ye Z.C., Wyeth M.S., Baltan-Tekkok S., Ransom B.R. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J. Neurosci. 2003, 23:3588-3596.
41. Pointis G., Segretain D. Role of connexin-based gap junction channels in testis. Trends Endocrinol. Metab. 2005, 16:300-306.
42. Jamieson E.R., Lippard S.J. Structure, recognition, and processing of cisplatin-DNA adducts. Chem. Rev. 1999, 99:2467-2498.
43. Wang D., Lippard S.J. Cellular processing of platinum anticancer drugs. Nat. Rev. Drug Discov. 2005, 4:307-320.
44. Goldberg G.S., Lampe P.D., Nicholson B.J. Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat. Cell. Biol. 1999, 1:457-459.
45. Nakamura T.Y., Yamamoto I., Kanno Y., Shiba Y., Goshima K. Metabolic coupling of glutathione between mouse and quail cardiac myocytes and its protective role against oxidative stress. Circ. Res. 1994, 74:806-816.
46. Zhang K., Mack P., Wong K.P. Glutathione-related mechanisms in cellular resistance to anticancer drugs. Int. J. Oncol. 1998, 12:871-882.
47. Lin J.H., Weigel H., Cotrina M.L., Liu S., Bueno E., Hansen A.J., et al. Gap-junction-mediated propagation and amplification of cell injury. Nat. Neurosci. 1998, 1:494-500.
48. Azzam E.I., de Toledo S.M., Little J.B. Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene 2003, 22:7050-7057.
49. Mandic A., Hansson J., Linder S., Shoshan M.C. Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J. Biol. Chem. 2003, 278:9100-9106.
50. Choi M.K., Kim D.D. Platinum transporters and drug resistance. Arch. Pharm. Res. 2006, 29:1067-1073.
51. Segretain D., Decrouy X., Dompierre J., Escalier D., Rahman N., Fiorini C., et al. Sequestration of connexin43 in the early endosomes: an early event of Leydig cell tumor progression. Mol. Carcinog. 2003, 38:179-187.
52. Ammerpohl O., Thormeyer D., Khan Z., Appelskog I.B., Gojkovic Z., Almqvist P.M., et al. HDACi phenylbutyrate increases bystander killing of HSV-tk transfected glioma cells. Biochem. Biophys. Res. Commun. 2004, 324:8-14.
53. Huang T., Zhu Y., Fang X., Chi Y., Kitamura M., Yao J. Gap junctions sensitize cancer cells to proteasome inhibitor MG132-induced apoptosis. Cancer Sci. 2010, 101:713-721.
54. Takano Y., Iwata H., Yano Y., Miyazawa M., Virgona N., Sato H., et al. Up-regulation of connexin 32 gene by 5-aza-2'-deoxycytidine enhances vinblastine-induced cytotoxicity in human renal carcinoma cells via the activation of JNK signalling. Biochem. Pharmacol. 2010, 80:463-470.
55. Heiniger B., Gakhar G., Prasain K., Hua D.H., Nguyen T.A. Second-generation substituted quinolines as anticancer drugs for breast cancer. Anticancer Res. 2010, 30:3927-3932.
56. Hernandez M., Shao Q., Yang X.J., Luh S.P., Kandouz M., Batist G., et al. A histone deacetylation-dependent mechanism for transcriptional repression of the gap junction gene cx43 in prostate cancer cells. Prostate 2006, 66:1151-1161.