Role of Zn2+ ions in host-virus interactions

Journal of Virology

Volumn 82, Issue 23, 2008, Pages 11486-11494

  Lazarczyk, Maciej ^a,b,c,d   Favre, Michel ^a  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; E5 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EVER PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; ZINC ION; CATION TRANSPORT PROTEIN; MEMBRANE PROTEIN; ONCOGENE PROTEIN E5, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN; SLC30A1 PROTEIN, HUMAN; TMC6 PROTEIN, HUMAN; TMC8 PROTEIN, HUMAN; TRANSCRIPTION FACTOR AP 1; ZINC;

CONCENTRATION (PARAMETERS); CONDYLOMA ACUMINATUM; DNA VIRUS; EPIDERMODYSPLASIA VERRUCIFORMIS; HOMEOSTASIS; HUMAN; INTRACELLULAR TRANSPORT; ION TRANSPORT; KERATINOCYTE; LIFE CYCLE; METAL BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; RNA VIRUS; SHORT SURVEY; SIGNAL TRANSDUCTION; VIROGENESIS; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; WART VIRUS; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; REVIEW; VIROLOGY;

ANIMALS; CATION TRANSPORT PROTEINS; EPIDERMODYSPLASIA VERRUCIFORMIS; HUMANS; KERATINOCYTES; MEMBRANE PROTEINS; ONCOGENE PROTEINS, VIRAL; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; VIRAL PROTEINS; ZINC;

EID: 56449102501     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01314-08     Document Type: Short Survey

References (78)

1. Barbosa, M. S., D. R. Lowy, and J. T. Schiller. 1989. Papillomavirus polypeptides E6 and E7 are zinc-binding proteins. J. Virol. 63:1404-1407.
2. Barthel, A., E. A. Ostrakhovitch, P. L. Walter, A. Kampkötter, and L. O. Klotz. 2007. Stimulation of phosphoinositide 3-kinase/Akt signaling by copper and zinc ions: mechanisms and consequences. Arch. Biochem. Biophys. 463:175-182.
3. Beerheide, W., H. U. Bernard, Y. J. Tan, A. Ganesan, W. G. Rice, and A. E. Ting. 1999. Potential drugs against cervical cancer: zinc-ejecting inhibitors of the human papillomavirus type 16 E6 oncoprotein. J. Natl. Cancer Inst. 91:1211-1220.
4. Bess, J. W., P. J. Powell, H. J. Issaq, L. J. Schumack, M. K. Grimes, L. E. Henderson, and L. O. Arthur. 1992. Tightly bound zinc in human immunodeficiency virus type 1, human T-cell leukemia virus type I, and other retroviruses. J. Virol. 66:840-847.
5. Boyle, W. J., T. Smeal, L. H. Defize, P. Angel, J. R. Woodgett, M. Karin, and T. Hunter. 1991. Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell 64:573-584.
6. +-ATPase function and stability in Saccharomyces cerevisiae. Virology 280:169-175.
7. Brottier, P., P. Nandi, M. Bremont, and J. Cohen. 1992. Bovine rotavirus segment 5 protein expressed in the baculovirus system interacts with zinc and RNA. J. Gen. Virol. 73:1931-1938.
8. Culp, J. S., L. C. Webster, D. J. Friedman, C. L. Smith, W. J. Huang, F. Y. Wu, M. Rosenberg, and R. P. Ricciardi. 1988. The 289-amino acid E1A protein of adenovirus binds zinc in a region that is important for transactivation. Proc. Natl. Acad. Sci. USA 85:6450-6454.
9. de Oliveira, W. R., C. Festa Neto, P. L. Rady, and S. K. Tyring. 2003. Clinical aspects of epidermodysplasia verruciformis. J. Eur. Acad. Dermatol. Venereol. 17:394-398.
10. de Villiers, E. M., C. Fauquet, T. R. Broker, H. U. Bernard, and H. zur Hausen. 2004. Classification of papillomaviruses. Virology 324:17-27.
11. Doorbar, J. 2006. Molecular biology of human papillomavirus infection and cervical cancer. Clin. Sci. (London) 110:525-541.
12. Eide, D. J. 2006. Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763:711-722.
13. 2+ induces stimulation of the c-Jun N-terminal kinase signaling pathway through phosphoinositide 3-kinase. Mol. Pharmacol. 59:981-986.
14. Erk, I., J. C. Huet, M. Duarte, S. Duquerroy, F. Rey, J. Cohen, and J. Lepault. 2003. A zinc ion controls assembly and stability of the major capsid protein of rotavirus. J. Virol. 77:3595-3601.
15. Favre, M., N. Ramoz, and G. Orth. 1997. Human papillomaviruses: general features. Clin. Dermatol. 15:181-198.
16. Fehrmann, F., D. J. Klumpp, and L. A. Laimins. 2003. Human papillomavirus type 31 E5 protein supports cell cycle progression and activates late viral functions upon epithelial differentiation. J. Virol. 77:2819-2831.
17. Fraefel, C., J. Zeng, Y. Choffat, M. Engels, M. Schwyzer, and M. Ackermann. 1994. Identification and zinc dependence of the bovine herpesvirus 1 transactivator protein BICP0. J. Virol. 68:3154-3162.
18. Frankel, A. D., D. S. Bredt, and C. O. Pabo. 1988. Tat protein from human immunodeficiency virus forms a metal-linked dimer. Science 240:70-73.
19. Frankel, A. D., L. Chen, R. J. Cotter, and C. O. Pabo. 1988. Dimerization of the tat protein from human immunodeficiency virus: a cysteine-rich peptide mimics the normal metal-linked dimer interface. Proc. Natl. Acad. Sci. USA 85:6297-6300.
20. Frazzini, V., E. Rockabrand, E. Mocchegiani, and S. L. Sensi. 2006. Oxidative stress and brain aging: is zinc the link? Biogerontology 7:307-314.
21. Garber, M. E., P. Wei, V. N. KewalRamani, T. P. Mayall, C. H. Herrmann, A. P. Rice, D. R. Littman, and K. A. Jones. 1998. The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes Dev. 12:3512-3527.
22. Genther, S. M., S. Sterling, S. Duensing, K. Münger, C. Sattler, and P. F. Lambert. 2003. Quantitative role of the human papillomavirus type 16 E5 gene during the productive stage of the viral life cycle. J. Virol. 77:2832-2842.
23. Goff, S. P. 2003. Death by deamination: a novel host restriction system for HIV-1. Cell 114:281-283.
24. Goswami, R., B. Turk, K. Enderle, A. Howe, and K. Rundell. 1992. Effect of zinc ions on the biochemical behavior of simian virus 40 small-t antigen expressed in bacteria. J. Virol. 66:1746-1751.
25. Grigorov, B., D. Décimo, F. Smagulova, C. Péchoux, M. Mougel, D. Muriaux, and J. L. Darlix. 2007. Intracellular HIV-1 Gag localization is impaired by mutations in the nucleocapsid zinc fingers. Retrovirology 4:54.
26. Grossman, S. R., and L. A. Laimins. 1989. E6 protein of human papillomavirus type 18 binds zinc. Oncogene 4:1089-1093.
27. Haase, H., and W. Maret. 2003. Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signaling. Exp. Cell Res. 291:289-298.
28. Han, R., N. M. Cladel, C. A. Reed, and N. D. Christensen. 1998. Characterization of transformation function of cottontail rabbit papillomavirus E5 and E8 genes. Virology 251:253-263.
29. Houzet, L., Z. Morichaud, L. Didierlaurent, D. Muriaux, J. L. Darlix, and M. Mougel. 2008. Nucleocapsid mutations turn HIV-1 into a DNA-containing virus. Nucleic Acids Res. 36:2311-2319.
30. Huang, H. W., and K. T. Wang. 1996. Structural characterization of the metal binding site in the cysteine-rich region of HIV-1 Tat protein. Biochem. Biophys. Res. Commun. 227:615-621.
31. Ilbäck, N. G., A. W. Glynn, L. Wikberg, E. Netzel, and U. Lindh. 2004. Metallothionein is induced and trace element balance changed in target organs of a common viral infection. Toxicology 199:241-250.
32. 2+-induced IL-8 expression involves AP-1, JNK, and ERK activities in human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 290:L1028-L1035.
33. Kitamura, H., H. Morikawa, H. Kamon, M. Iguchi, S. Hojyo, T. Fukada, S. Yamashita, T. Kaisho, S. Akira, M. Murakami, and T. Hirano. 2006. Tolllike receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat. Immunol. 7:971-977.
34. Kurima, K., Y. Yang, K. Sorber, and A. J. Griffith. 2003. Characterization of the transmembrane channel-like (TMC) gene family: functional clues from hearing loss and epidermodysplasia verruciformis. Genomics 82:300-308.
35. Kyo, S., D. J. Klumpp, M. Inoue, T. Kanaya, and L. A. Laimins. 1997. Expression of AP1 during cellular differentiation determines human papillomavirus E6/E7 expression in stratified epithelial cells. J. Gen. Virol. 78: 401-411.
36. Laity, J. H., B. M. Lee, and P. E. Wright. 2001. Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11:39-46.
37. Lazarczyk, M., C. Pons, J. A. Mendoza, P. Cassonnet, Y. Jacob, and M. Favre. 2008. Regulation of cellular zinc balance as a potential mechanism of EVER-mediated protection against pathogenesis by cutaneous oncogenic human papillomaviruses. J. Exp. Med. 205:35-42.
38. Lee, S. P., and M. K. Han. 1996. Zinc stimulates Mg2+-dependent 3′-processing activity of human immunodeficiency virus type 1 integrase in vitro. Biochemistry 35:3837-3844.
39. 2+ promotes the self-association of human immunodeficiency virus type-1 integrase in vitro. Biochemistry 36:173-180.
40. Liuzzi, J. P., and R. J. Cousins. 2004. Mammalian zinc transporters. Annu. Rev. Nutr. 24:151-172.
41. Luo, K., Z. Xiao, E. Ehrlich, Y. Yu, B. Liu, S. Zheng, and X. F. Yu. 2005. Primate lentiviral virion infectivity factors are substrate receptors that assemble with cullin 5-E3 ligase through a HCCH motif to suppress APOBEC3G. Proc. Natl. Acad. Sci. USA 102:11444-11449.
42. Majewski, S., S. Jablonska, and G. Orth. 1997. Epidermodysplasia verruciformis. Immunological and nonimmunological surveillance mechanisms: role in tumor progression. Clin. Dermatol. 15:321-334.
43. Margoshes, M., and B. L. Vallee. 1957. A cadmium protein from equine kidney cortex J. Am. Chem. Soc. 79:4813-4814.
44. Martin, P., W. C. Vass, J. T. Schiller, D. R. Lowy, and T. J. Velu. 1989. The bovine papillomavirus E5 transforming protein can stimulate the transforming activity of EGF and CSF-1 receptors. Cell 59:21-32.
45. Maufort, J. P., S. M. Williams, H. C. Pitot, and P. F. Lambert. 2007. Human papillomavirus 16 E5 oncogene contributes to two stages of skin carcinogenesis. Cancer Res. 67:6106-6112.
46. McEuen, A. R., B. Edwards, K. A. Koepke, A. E. Ball, B. A. Jennings, A. J. Wolstenholme, M. J. Danson, and D. W. Hough. 1992. Zinc binding by retroviral integrase. Biochem. Biophys. Res. Commun. 189:813-818.
47. 2+ binding to cysteine-rich domain of extracellular human immunodeficiency virus type 1 Tat protein is associated with Tat protein-induced apoptosis. AIDS Res. Hum. Retrovir. 20:297-304.
48. Miura, P., and B. J. Jasmin. 2006. Utrophin upregulation for treating Duchenne or Becker muscular dystrophy: how close are we? Trends Mol. Med. 12:122-129.
49. Nonnenmacher, M., J. Salmon, Y. Jacob, G. Orth, and F. Breitburd. 2006. Cottontail rabbit papillomavirus E8 protein is essential for wart formation and provides new insights into viral pathogenesis. J. Virol. 80:4890-4900.
50. Orth, G. 1987. Epidermodysplasia verruciformis, p. 199-243. In N.P. Salzman and P.M. Howley (ed.), The Papovaviridae: the papillomaviruses. Plenum Press, New York, NY.
51. Orth, G. 2006. Genetics of epidermodysplasia verruciformis: insights into host defense against papillomaviruses. Semin. Immunol. 18:362-374.
52. Palmiter, R. D. 1994. Regulation of metallothionein genes by heavy metals appears to be mediated by a zinc-sensitive inhibitor that interacts with a constitutively active transcription factor, MTF-1. Proc. Natl. Acad. Sci. USA 91:1219-1223.
53. Palmiter, R. D., and S. D. Findley. 1995. Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J. 14:639-649.
54. Paul, I., J. Cui, and E. L. Maynard. 2006. Zinc binding to the HCCH motif of HIV-1 virion infectivity factor induces a conformational change that mediates protein-protein interactions. Proc. Natl. Acad. Sci. USA 103:18475-18480.
55. Radtke, F., R. Heuchel, O. Georgiev, M. Hergersberg, M. Gariglio, Z. Dembic, and W. Schaffner. 1993. Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J. 12:1355-1362.
56. Ramoz, N., A. Taïeb, L. A. Rueda, L. S. Montoya, B. Bouadjar, M. Favre, and G. Orth. 2000. Evidence for a nonallelic heterogeneity of epidermodysplasia verruciformis with two susceptibility loci mapped to chromosome regions 2p21-p24 and 17q25. J. Investig. Dermatol. 114:1148-1153.
57. Ramoz, N., L. A. Rueda, B. Bouadjar, L. S. Montoya, G. Orth, and M. Favre. 2002. Mutations in two adjacent novel genes are associated with epidermodysplasia verruciformis. Nat. Genet. 32:579-581.
58. Rice, W. G., C. A. Schaeffer, B. Harten, F. Villinger, T. L. South, M. F. Summers, L. E. Henderson, J. W. Bess, L. O. Arthur, J. S. McDougal, S. L. Orloff, J. Mendeleyev, and E. Kun. 1993. Inhibition of HIV-1 infectivity by zinc-ejecting aromatic C-nitroso compounds. Nature 361:473-475.
59. Rice, W. G., C. A. Schaeffer, L. Graham, M. Bu, J. S. McDougal, S. L. Orloff, F. Villinger, M. Young, S. Oroszlan, M. R. Fesen, Y. Pomier, J. Mendeleyev, and E. Kun. 1993. The site of antiviral action of 3-nitrosobenzamide on the infectivity process of human immunodeficiency virus in human lymphocytes. Proc. Natl. Acad. Sci. USA 90:9721-9724.
60. Rodríguez, M. I., M. E. Finbow, and A. Alonso. 2000. Binding of human papillomavirus 16 E5 to the 16 kDa subunit c (proteolipid) of the vacuolar H+-ATPase can be dissociated from the E5-mediated epidermal growth factor receptor overactivation. Oncogene 19:3727-3732.
61. Schiffman, M., P. E. Castle, J. Jeronimo, A. C. Rodriguez, and S. Wacholder. 2007. Human papillomavirus and cervical cancer. Lancet 370:890-907.
62. Sekler, I., S. L. Sensi, M. Hershfinkel, and W. F. Silverman. 2007. Mechanism and regulation of cellular zinc transport. Mol. Med. 13:337-343.
63. 2+-induced ERK activation mediated by reactive oxygen species causes cell death in differentiated PC12 cells. J. Neurochem. 78:600-610.
64. Srinivas, S., A. Schönthal, and W. Eckhart. 1994. Polyomavirus middle-sized tumor antigen modulates c-Jun phosphorylation and transcriptional activity. Proc. Natl. Acad. Sci. USA 91:10064-10068.
65. Stöppler, M. C., S. W. Straight, G. Tsao, R. Schlegel, and D. J. McCance. 1996. The E5 gene of HPV-16 enhances keratinocyte immortalization by full-length DNA. Virology 223:251-254.
66. Straight, S. W., P. M. Hinkle, R. J. Jewers, and D. J. McCance. 1993. The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes. J. Virol. 67:4521-4532.
67. 2+ complex formation analysis with electrospray mass spectrometry. FEBS Lett. 311:259-262.
68. 2+. Toxicol. Appl. Pharmacol. 214:16-23.
69. Tsai, T. C., and S. L. Chen. 2003. The biochemical and biological functions of human papillomavirus type 16 E5 protein. Arch. Virol. 148:1445-1453.
70. Turk, B., A. Porras, M. C. Mumby, and K. Rundell. 1993. Simian virus 40 small-t antigen binds two zinc ions. J. Virol. 67:3671-3673.
71. Winnischofer, S. M., M. L. de Oliveira, and M. C. Sogayar. 2003. Suppression of AP-1 constitutive activity interferes with polyomavirus MT antigen transformation ability. J. Cell. Biochem. 90:253-266.
72. Xiao, Z., E. Ehrlich, K. Luo, Y. Xiong, and X. F. Yu. 2007. Zinc chelation inhibits HIV Vif activity and liberates antiviral function of the cytidine deaminase APOBEC3G. FASEB J. 21:217-222.
73. Yamasaki, S., K. Sakata-Sogawa, A. Hasegawa, T. Suzuki, K. Kabu, E. Sato, T. Kurosaki, S. Yamashita, M. Tokunaga, K. Nishida, and T. Hirano. 2007. Zinc is a novel intracellular second messenger. J. Cell Biol. 177:637-645.
74. Yoshimura, K., H. Aoki, Y. Ikeda, A. Furutani, K. Hamano, and M. Matsuzaki. 2006. Regression of abdominal aortic aneurysm by inhibition of c-Jun N-terminal kinase in mice. Ann. N. Y. Acad. Sci. 1085:74-81.
75. Young, M. R., L. Farrell, P. Lambert, P. Awasthi, and N. H. Colburn. 2002. Protection against human papillomavirus type 16-E7 oncogene-induced tumorigenesis by in vivo expression of dominant-negative c-jun. Mol. Carcinog. 34:72-77.
76. Zhang, B., A. Srirangam, D. A. Potter, and A. Roman. 2005. HPV16 E5 protein disrupts the c-Cbl-EGFR interaction and EGFR ubiquitination in human foreskin keratinocytes. Oncogene 24:2585-2588.
77. Zilliox, M. J., G. Parmigiani, and D. E. Griffin. 2006. Gene expression patterns in dendritic cells infected with measles virus compared with other pathogens. Proc. Natl. Acad. Sci. USA 103:3363-3368.
78. zur Hausen, H. 2000. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J. Natl. Cancer Inst. 92:690-698.