Inhibition of gap junctional intercellular communication by toxic metals

Chemical Research in Toxicology

Volumn 23, Issue 12, 2010, Pages 1862-1867

  Vinken, Mathieu ^a   Ceelen, Liesbeth ^a   Vanhaecke, Tamara ^a   Rogiers, Vera ^a  

^a FACULTY OF MEDICINE AND PHARMACY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM; ARSENIC; CADMIUM; INDIUM; LEAD; MERCURY; NICKEL;

ARTICLE; CELL COMMUNICATION; DOWN REGULATION; EXPOSURE; GAP JUNCTION; HUMAN; IN VITRO STUDY; SCREENING;

CELL COMMUNICATION; CONNEXINS; ENVIRONMENTAL POLLUTANTS; GAP JUNCTIONS; HUMANS; METALS;

EID: 78650507833     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx100276f     Document Type: Article

References (77)

1. Buchwalter, D. (2008) Metals. In Molecular and Biochemical Toxicology (Smart, R. H. E., Ed.) 4th ed., pp 413 - 440, Wiley, Singapore.
2. Merrill, J. C., Morton, J. J. P., and Soileau, S. D. (2008) Metals. In Principles and Methods of Toxicology (Hayes, A., Ed.) 5th ed., pp 841 - 896, CRC Press, London.
3. Schäfer, S. D., Elsenhans, B., Forth, W., and Schümann, K. (1999) Metals. In Toxicology (Marquardt, H. S., McClellan, R., and Welsch, F., Eds.) pp 755 - 804, Academic Press, London.
4. Summer, K.-H. H., Kappus, H., and Greim, H. (2009) Metals. In Toxicology and risk assessment: A comprehensive introduction (Greim, H. S. R., Ed.) pp 534 - 564, John Wiley & Sons Ltd., Chichester, U.K.
5. Decrock, E., Vinken, M., De Vuyst, E., Krysko, D. V., DHerde, K., Vanhaecke, T., Vandenabeele, P., Rogiers, V., and Leybaert, L. (2009) Connexin-related signaling in cell death: To live or let die Cell Death Differ. 16, 524-536
6. Vinken, M., De Rop, E., Decrock, E., De Vuyst, E., Leybaert, L., Vanhaecke, T., and Rogiers, V. (2009) Epigenetic regulation of gap junctional intercellular communication: More than a way to keep cells quiet Biochim. Biophys. Acta 1795, 53-61
7. Vinken, M., Doktorova, T., Decrock, E., Leybaert, L., Vanhaecke, T., and Rogiers, V. (2009) Gap junctional intercellular communication as a target for liver toxicity and carcinogenicity Crit. Rev. Biochem. Mol. Biol. 44, 201-222
8. Vinken, M., Henkens, T., De Rop, E., Fraczek, J., Vanhaecke, T., and Rogiers, V. (2008) Biology and pathobiology of gap junctional channels in hepatocytes Hepatology 47, 1077-1088
9. Vinken, M., Vanhaecke, T., Papeleu, P., Snykers, S., Henkens, T., and Rogiers, V. (2006) Connexins and their channels in cell growth and cell death Cell. Signalling 18, 592-600
10. Hanner, F., Sorensen, C. M., Holstein-Rathlou, N. H., and Peti-Peterdi, J. (2010) Connexins and the kidney Am. J. Physiol. 298, R1143-R1155
11. Talhouk, R. S., Zeinieh, M. P., Mikati, M. A., and El-Sabban, M. E. (2008) Gap junctional intercellular communication in hypoxia-ischemia-induced neuronal injury Prog. Neurobiol. 84, 57-76
12. Johnson, L. N. and Koval, M. (2009) Cross-talk between pulmonary injury, oxidant stress, and gap junctional communication Antioxid. Redox Signaling 11, 355-367
13. DHondt, C., Ponsaerts, R., De Smedt, H., Bultynck, G., and Himpens, B. (2009) Pannexins, distant relatives of the connexin family with specific cellular functions BioEssays 31, 953-974
14. Alexander, D. B. and Goldberg, G. S. (2003) Transfer of biologically important molecules between cells through gap junction channels Curr. Med. Chem. 10, 2045-2058
15. Goldberg, G. S., Moreno, A. P., and Lampe, P. D. (2002) Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and ATP J. Biol. Chem. 277, 36725-36730
16. Evans, W. H., De Vuyst, E., and Leybaert, L. (2006) The gap junction cellular internet: Connexin hemichannels enter the signalling limelight Biochem. J. 397, 1-14
17. Dbouk, H. A., Mroue, R. M., El-Sabban, M. E., and Talhouk, R. S. (2009) Connexins: A myriad of functions extending beyond assembly of gap junction channels Cell Commun. Signaling 7, 4
18. Laird, D. W. (2010) The gap junction proteome and its relationship to disease Trends Cell Biol. 20, 92-101
19. Oyamada, M., Oyamada, Y., and Takamatsu, T. (2005) Regulation of connexin expression Biochim. Biophys. Acta 1719, 6-23
20. Sohl, G. and Willecke, K. (2004) Gap junctions and the connexin protein family Cardiovasc. Res. 62, 228-232
21. Anderson, C., Catoe, H., and Werner, R. (2006) MIR-206 regulates connexin43 expression during skeletal muscle development Nucleic Acids Res. 34, 5863-5871
22. Kim, H. K., Lee, Y. S., Sivaprasad, U., Malhotra, A., and Dutta, A. (2006) Muscle-specific microRNA miR-206 promotes muscle differentiation J. Cell Biol. 174, 677-687
23. Yang, B., Lin, H., Xiao, J., Lu, Y., Luo, X., Li, B., Zhang, Y., Xu, C., Bai, Y., Wang, H., Chen, G., and Wang, Z. (2007) The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2 Nat. Med. 13, 486-491
24. Chipman, J. K., Mally, A., and Edwards, G. O. (2003) Disruption of gap junctions in toxicity and carcinogenicity Toxicol. Sci. 71, 146-153
25. Naus, C. C. and Laird, D. W. (2010) Implications and challenges of connexin connections to cancer Nat. Rev. Cancer 10, 435-441
26. Czyz, J. (2008) The stage-specific function of gap junctions during tumourigenesis Cell. Mol. Biol. Lett. 13, 92-102
27. Leithe, E., Sirnes, S., Omori, Y., and Rivedal, E. (2006) Downregulation of gap junctions in cancer cells Crit. Rev. Oncog. 12, 225-256
28. Mesnil, M., Crespin, S., Avanzo, J. L., and Zaidan-Dagli, M. L. (2005) Defective gap junctional intercellular communication in the carcinogenic process Biochim. Biophys. Acta 1719, 125-145
29. Trosko, J. E. and Ruch, R. J. (2002) Gap junctions as targets for cancer chemoprevention and chemotherapy Curr. Drug Targets 3, 465-482
30. Krutovskikh, V., Mazzoleni, G., Mironov, N., Omori, Y., Aguelon, A. M., Mesnil, M., Berger, F., Partensky, C., and Yamasaki, H. (1994) Altered homologous and heterologous gap-junctional intercellular communication in primary human liver tumors associated with aberrant protein localization but not gene mutation of connexin 32 Int. J. Cancer 56, 87-94
31. Oyamada, M., Krutovskikh, V. A., Mesnil, M., Partensky, C., Berger, F., and Yamasaki, H. (1990) Aberrant expression of gap junction gene in primary human hepatocellular carcinomas: Increased expression of cardiac-type gap junction gene connexin 43 Mol. Carcinog. 3, 273-278
32. Kandouz, M. and Batist, G. (2010) Gap junctions and connexins as therapeutic targets in cancer Expert Opin. Ther. Targets 14, 681-692
33. Pointis, G., Fiorini, C., Gilleron, J., Carette, D., and Segretain, D. (2007) Connexins as precocious markers and molecular targets for chemical and pharmacological agents in carcinogenesis Curr. Med. Chem. 14, 2288-2303
34. Trosko, J. E., Chang, C. C., Upham, B., and Wilson, M. (1998) Epigenetic toxicology as toxicant-induced changes in intracellular signalling leading to altered gap junctional intercellular communication Toxicol. Lett. 102-103, 71-78
35. Aleo, M. F., Morandini, F., Bettoni, F., Tanganelli, S., Vezzola, A., Giuliani, R., Steimberg, N., Apostoli, P., and Mazzoleni, G. (2002) Antioxidant potential and gap junction-mediated intercellular communication as early biological markers of mercuric chloride toxicity in the MDCK cell line Toxicol. in Vitro 16, 457-465
36. Guzzi, G. and La Porta, C. A. (2008) Molecular mechanisms triggered by mercury Toxicology 244, 1-12
37. Taber, K. H. and Hurley, R. A. (2008) Mercury exposure: Effects across the lifespan J. Neuropsychiatry Clin. Neurosci. 20, 384-389
38. Yoshida, M., Kujiraoka, T., Hara, M., Nakazawa, H., and Sumi, Y. (1998) Methylmercury inhibits gap junctional intercellular communication in primary cultures of rat proximal tubular cells Arch. Toxicol. 72, 192-196
39. i in bone cells Calcif. Tissue Int. 63, 134-139
40. Zefferino, R., Elia, G., Lasalvia, M., Piccoli, C., Boffoli, D., Capitanio, N., and Ambrosi, L. (2005) The study of gap junctional intercellular communication in keratinocytes as screening of promoter effect induced by industrial and environmental toxic substances Med. Lav. 96, 222-230
41. Zefferino, R., Elia, G., Petrozzi, M. T., Leone, A., Corsi, P., and Ambrosi, L. (2002) Promoter effect of mercury chloride and methyl-mercury on human keratinocytes in culture Giornale Italiano di Medicina del Lavoro ed Ergonomia 24, 372-375
42. Zefferino, R., Leone, A., Piccaluga, S., Cincione, R., and Ambrosi, L. (2008) Mercury modulates interplay between IL-1β, TNF-α, and gap junctional intercellular communication in keratinocytes: Mitigation by lycopene J. Immunotoxicol. 5, 353-360
43. Zefferino, R., Piccaluga, S., Lasalvia, M., DAndrea, G., Margaglione, M., and Ambrosi, L. (2006) Role of tumour necrosis factor α and interleukin 1β in promoter effect induced by mercury in human keratinocytes Int. J. Immunopathol. Pharmacol. 19, 15-20
44. Fukumoto, M., Kujiraoka, T., Hara, M., Shibasaki, T., Hosoya, T., and Yoshida, M. (2001) Effect of cadmium on gap junctional intercellular communication in primary cultures of rat renal proximal tubular cells Life Sci. 69, 247-254
45. Jeong, S. H., Habeebu, S. S., and Klaassen, C. D. (2000) Cadmium decreases gap junctional intercellular communication in mouse liver Toxicol. Sci. 57, 156-166
46. Joseph, P. (2009) Mechanisms of cadmium carcinogenesis Toxicol. Appl. Pharmacol. 238, 272-279
47. Thevenod, F. (2009) Cadmium and cellular signaling cascades: To be or not to be Toxicol. Appl. Pharmacol. 238, 221-239
48. Jeon, S. H., Cho, M. H., and Cho, J. H. (2001) Effects of cadmium on gap junctional intercellular communication in WB-F344 rat liver epithelial cells Hum. Exp. Toxicol. 20, 577-583
49. 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
50. Fang, M. Z., Mar, W. C., and Cho, M. H. (2001) Cadmium-induced alterations of connexin expression in the promotion stage of in vitro two-stage transformation Toxicology 161, 117-127
51. Ghosh, P., Banerjee, M., Giri, A. K., and Ray, K. (2008) Toxicogenomics of arsenic: Classical ideas and recent advances Mutat. Res. 659, 293-301
52. Salnikow, K. and Zhitkovich, A. (2008) Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: Nickel, arsenic, and chromium Chem. Res. Toxicol. 21, 28-44
53. Chou, Y., Tsai, C. H., Ueng, K. C., Tian, T. Y., Chen, S. C., and Yeh, H. I. (2007) Endothelial gap junctions are down-regulated by arsenic trioxide Eur. J. Pharmacol. 569, 29-36
54. Vasudevaraju, P., Govindaraju, M., Palanisamy, A. P., Sambamurti, K., and Rao, K. S. (2008) Molecular toxicity of aluminium in relation to neurodegeneration Indian J. Med. Res. 128, 545-556
55. Verstraeten, S. V., Aimo, L., and Oteiza, P. I. (2008) Aluminium and lead: Molecular mechanisms of brain toxicity Arch. Toxicol. 82, 789-802
56. Theiss, C. and Meller, K. (2002) Aluminum impairs gap junctional intercellular communication between astroglial cells in vitro Cell Tissue Res. 310, 143-154
57. Loch-Caruso, R., Corcos, I. A., and Trosko, J. E. (1991) Inhibition of metabolic coupling by metals J. Toxicol. Environ. Health 32, 33-48
58. Mikalsen, S. O. (1990) Effects of heavy metal ions on intercellular communication in Syrian hamster embryo cells Carcinogenesis 11, 1621-1626
59. Tsuchiya, T. (2000) A useful marker for evaluating tissue-engineered products: Gap-junctional communication for assessment of the tumor-promoting action and disruption of cell differentiation in tissue-engineered products J. Biomater. Sci., Polym. Ed. 11, 947-959
60. Rivedal, E., Roseng, L. E., and Sanner, T. (1990) Vanadium compounds promote the induction of morphological transformation of hamster embryo cells with no effect on gap junctional cell communication Cell Biol. Toxicol. 6, 303-314
61. Nakajima, M., Usami, M., Nakazawa, K., Arishima, K., and Yamamoto, M. (2008) Developmental toxicity of indium: Embryotoxicity and teratogenicity in experimental animals Congenital Anomalies 48, 145-150
62. Guo, X. B., Ohno, Y., Kawanishi, T., Sunouchi, M., and Takanaka, A. (1992) Indium inhibits gap junctional communication between rat hepatocytes in primary culture Toxicol. Lett. 60, 99-106
63. Beyersmann, D. and Hartwig, A. (2008) Carcinogenic metal compounds: Recent insight into molecular and cellular mechanisms Arch. Toxicol. 82, 493-512
64. Chung, N. P. and Cheng, C. Y. (2001) Is cadmium chloride-induced inter-sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis? Endocrinology 142, 1878-1888
65. 2+-dependent cell-cell junctions and alters the pattern of E-cadherin immunofluorescence in LLC-PK1 cells Biochem. Biophys. Res. Commun. 181, 1118-1124
66. 2+) disrupts intercellular junctions and actin filaments in LLC-PK1 cells Toxicol. Appl. Pharmacol. 107, 81-97
67. Prozialeck, W. C., Wellington, D. R., and Lamar, P. C. (1993) Comparison of the cytotoxic effects of cadmium chloride and cadmium-metallothionein in LLC-PK1 cells Life Sci. 53, PL337-PL342
68. Yoon, S., Han, S. S., and Rana, S. V. (2008) Molecular markers of heavy metal toxicity: A new paradigm for health risk assessment J. Environ. Biol. 29, 1-14
69. Thukral, S. K., Nordone, P. J., Hu, R., Sullivan, L., Galambos, E., Fitzpatrick, V. D., Healy, L., Bass, M. B., Cosenza, M. E., and Afshari, C. A. (2005) Prediction of nephrotoxicant action and identification of candidate toxicity-related biomarkers Toxicol. Pathol. 33, 343-355
70. Chappell, R. L., Qian, H., Zakevicius, J., and Ripps, H. (2004) Histidine suppresses zinc modulation of connexin hemichannels Biol. Bull. 207, 188-190
71. Chappell, R. L., Zakevicius, J., and Ripps, H. (2003) Zinc modulation of hemichannel currents in Xenopus oocytes Biol. Bull. 205, 209-211
72. Sun, Z., Zhang, D. Q., and McMahon, D. G. (2009) Zinc modulation of hemi-gap-junction channel currents in retinal horizontal cells J. Neurophysiol. 101, 1774-1780
73. Brough, D., Pelegrin, P., and Rothwell, N. J. (2009) Pannexin-1-dependent caspase-1 activation and secretion of IL-1β is regulated by zinc Eur. J. Immunol. 39, 352-358
74. Tang, Q., Dowd, T. L., Verselis, V. K., and Bargiello, T. A. (2009) Conformational changes in a pore-forming region underlie voltage-dependent "loop gating" of an unapposed connexin hemichannel J. Gen. Physiol. 133, 555-570
75. Bhabra, G., Sood, A., Fisher, B., Cartwright, L., Saunders, M., Evans, W. H., Surprenant, A., Lopez-Castejon, G., Mann, S., Davis, S. A., Hails, L. A., Ingham, E., Verkade, P., Lane, J., Heesom, K., Newson, R., and Case, C. P. (2009) Nanoparticles can cause DNA damage across a cellular barrier Nat. Nanotechnol. 4, 876-883
76. Legare, M. E., Barhoumi, R., Burghardt, R. C., and Tiffany-Castiglioni, E. (1993) Low-level lead exposure in cultured astroglia: Identification of cellular targets with vital fluorescent probes Neurotoxicology 14, 267-272
77. Mikalsen, S. O. and Kaalhus, O. (1996) A characterization of pervanadate, an inducer of cellular tyrosine phosphorylation and inhibitor of gap junctional intercellular communication Biochim. Biophys. Acta 1290, 308-318