The role of zinc in genomic stability

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 733, Issue 1-2, 2012, Pages 111-121

  Sharif, Razinah ^a,b,c   Thomas, Philip ^a   Zalewski, Peter ^b   Fenech, Michael ^a  

^a CSIRO   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

Author keywords

DNA damage; Genomic stability; Methylation; Micronuclei; Telomere; Zinc

Indexed keywords

METALLOTHIONEIN; UNCLASSIFIED DRUG; ZINC; ZINC ACETATE; ZINC CHROMATE;

CANCER RISK; CHROMOSOMAL INSTABILITY; DNA DAMAGE; DNA METHYLATION; GENE MUTATION; GENOMIC INSTABILITY; GENOTOXICITY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TELOMERE; ZINC DEFICIENCY;

ANIMALS; ANTIOXIDANTS; CELL LINE; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, DRUG; GENOMIC INSTABILITY; HUMANS; NEOPLASMS; OXIDATIVE STRESS; POLYMORPHISM, GENETIC; TELOMERE; TRACE ELEMENTS; ZINC;

EID: 84860571781     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2011.08.009     Document Type: Review

References (140)

1. W. World Health Organizations Cancer, World Health Organizations, 2009, pp. WHO - Media Centre - Fact Sheet.
2. A.I.C.R. AICR Food, Nutrition, Physical Activity, and the Prevention of Cancer 2007, American Institute for Cancer Research, Washington, DC.
3. Milner J.A. Molecular targets for bioactive food components. J. Nutr. 2004, 134:2492S-2498S.
4. Finley J.W. Proposed criteria for assessing the efficacy of cancer reduction by plant foods enriched in carotenoids glucosinolates, polyphenols and selenocompounds. Ann. Bot. (London) 2005, 95:1075-1096.
5. Fenech M., Ferguson L.R. Vitamins/minerals and genomic stability in humans. Mutat. Res. 2001, 475:1-6.
6. Ames B.N. Micronutrients prevent cancer and delay aging. Toxicol. Lett. 1998, 102-103:5-18.
7. Ames B.N. Micronutrient deficiencies. A major cause of DNA damage. Ann. N. Y. Acad. Sci. 1999, 889:87-106.
8. Fenech M. Chromosomal biomarkers of genomic instability relevant to cancer. Drug Discov. Today 2002, 7:1128-1137.
9. Ames B.N., Wakimoto P. Are vitamin and mineral deficiencies a major cancer risk?. Nat. Rev. Cancer 2002, 2:694-704.
10. Ames B.N. DNA damage from micronutrient deficiencies is likely to be a major cause of cancer. Mutat. Res. 2001, 475:7-20.
11. Ames B.N., Gold L.S. Paracelsus to parascience: the environmental cancer distraction. Mutat. Res. 2000, 447:3-13.
12. Blount B.C., Mack M.M., Wehr C.M., MacGregor J.T., Hiatt R.A., Wang G., Wickramasinghe S.N., Everson R.B., Ames B.N. Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:3290-3295.
13. Dreosti I.E. Zinc and the gene. Mutat. Res. 2001, 475:161-167.
14. Ho E. Zinc deficiency, DNA damage and cancer risk. J. Nutr. Biochem. 2004, 15:572-578.
15. Falchuk K.H. The molecular basis for the role of zinc in developmental biology. Mol. Cell. Biochem. 1998, 188:41-48.
16. Bray T.M., Bettger W.J. The physiological role of zinc as an antioxidant. Free Radic. Biol. Med. 1990, 8:281-291.
17. Powell S.R. The antioxidant properties of zinc. J. Nutr. 2000, 130:1447S-1454S.
18. Cousins R.J., Blanchard R.K., Moore J.B., Cui L., Green C.L., Liuzzi J.P., Cao J., Bobo J.A. Regulation of zinc metabolism and genomic outcomes. J. Nutr. 2003, 133:1521S-1526S.
19. Oteiza P.I., Adonaylo V.N., Keen C.L. Cadmium-induced testes oxidative damage in rats can be influenced by dietary zinc intake. Toxicology 1999, 137:13-22.
20. Oteiza P.I., Clegg M.S., Keen C.L. Short-term zinc deficiency affects nuclear factor-kappa B nuclear binding activity in rat testes. J. Nutr. 2001, 131:21-26.
21. Oteiza P.I., Olin K.L., Fraga C.G., Keen C.L. Zinc deficiency causes oxidative damage to proteins, lipids and DNA in rat testes. J. Nutr. 1995, 125:823-829.
22. Oteiza P.L, Olin K.L., Fraga C.G., Keen C.L. Oxidant defense systems in testes from zinc-deficient rats. Proc. Soc. Exp. Biol. Med. 1996, 213:85-91.
23. Hennig B., Meerarani P., Ramadass P., Toborek M., Malecki A., Slim R., McClain C.J. Zinc nutrition and apoptosis of vascular endothelial cells: implications in atherosclerosis. Nutrition 1999, 15:744-748.
24. Hennig B., Toborek M., McClain C.J. Antiatherogenic properties of zinc: implications in endothelial cell metabolism. Nutrition 1996, 12:711-717.
25. Meerarani P., Ramadass P., Toborek M., Bauer H.C., Bauer H., Hennig B. Zinc protects against apoptosis of endothelial cells induced by linoleic acid and tumor necrosis factor alpha. Am. J. Clin. Nutr. 2000, 71:81-87.
26. 2+ induces DNA fragmentation and cell condensation in cultured human Chang liver cells. Biol. Trace Elem. Res. 1997, 58:135-147.
27. Clegg M.S., Hanna L.A., Niles B.J., Momma T.Y., Keen C.L. Zinc deficiency-induced cell death. IUBMB Life 2005, 57:661-669.
28. Bae S.N., Lee Y.S., Kim M.Y., Kim J.D., Park L.O. Antiproliferative and apoptotic effects of zinc-citrate compound (CIZAR(R)) on human epithelial ovarian cancer cell line, OVCAR-3. Gynecol. Oncol. 2006, 103:127-136.
29. 2-induced cytotoxicity. Toxicol. Appl. Pharmacol. 2005, 205:225-236.
30. Chimienti F., Jourdan E., Favier A., Seve M. Zinc resistance impairs sensitivity to oxidative stress in HeLa cells: protection through metallothioneins expression. Free Radic. Biol. Med. 2001, 31:1179-1190.
31. Chang K.L., Hung T.C., Hsieh B.S., Chen Y.H., Chen T.F., Cheng H.L. Zinc at pharmacologic concentrations affects cytokine expression and induces apoptosis of human peripheral blood mononuclear cells. Nutrition 2006, 22:465-474.
32. Hainaut P., Mann K. Zinc binding and redox control of p53 structure and function. Antioxid. Redox Signal. 2001, 3:611-623.
33. Marchenko N.D., Zaika A., Moll U.M. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J. Biol. Chem. 2000, 275:16202-16212.
34. King K.L., Cidlowski J.A. Cell cycle regulation and apoptosis. Annu. Rev. Physiol. 1998, 60:601-617.
35. Ho E., Courtemanche C., Ames B.N. Zinc deficiency induces oxidative DNA damage and increases p53 expression in human lung fibroblasts. J. Nutr. 2003, 133:2543-2548.
36. Ho E., Ames B.N. Low intracellular zinc induces oxidative DNA damage, disrupts p53 NFkappa B, and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:16770-16775.
37. Ra H., Kim H.L., Lee H.W., Kim Y.H. Essential role of p53 in TPEN-induced neuronal apoptosis. FEBS Lett. 2009, 583:1516-1520.
38. Petrucco S., Percudani R. Structural recognition of DNA by poly(ADP-ribose)polymerase-like zinc finger families. FEBS J. 2008, 275:883-893.
39. Kunzmann A., Dedoussis G., Jajte J., Malavolta M., Mocchegiani E., Burkle A. Effect of zinc on cellular poly(ADP-ribosyl)ation capacity. Exp. Gerontol. 2008, 43:409-414.
40. Oka S., Ohno M., Tsuchimoto D., Sakumi K., Furuichi M., Nakabeppu Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J. 2008, 27:421-432.
41. Boiteux S., Radicella J.P. The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch. Biochem. Biophys. 2000, 377:1-8.
42. Song Y., Elias V., Loban A., Scrimgeour A.G., Ho E. Marginal zinc deficiency increases oxidative DNA damage in the prostate after chronic exercise. Free Radic. Biol. Med. 2009, 48:82-88.
43. Song Y., Leonard S.W., Traber M.G., Ho E. Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats. J. Nutr. 2009, 139:1626-1631.
44. Fritz G. Human APE/Ref-1 protein. Int. J. Biochem. Cell Biol. 2000, 32:925-929.
45. Hegde M.L., Hazra T.K., Mitra S. Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res. 2008, 18:27-47.
46. Puglisi F., Aprile G., Minisini A.M., Barbone F., Cataldi P., Tell G., Kelley M.R., Damante G., Beltrami C.A., Di Loreto C. Prognostic significance of Ape1/ref-1 subcellular localization in non-small cell lung carcinomas. Anticancer Res. 2001, 21:4041-4049.
47. Prasad A.S. Zinc in human health: effect of zinc on immune cells. Mol. Med. 2008, 14:353-357.
48. Chinenov Y., Kerppola K.T. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 2001, 20:2438-2452.
49. Shaulian E., Karin M. AP-1 in cell proliferation and survival. Oncogene 2001, 20:2390-2400.
50. Karin M., Shaulian E. AP-1: linking hydrogen peroxide and oxidative stress to the control of cell proliferation and death. IUBMB Life 2001, 52:17-24.
51. Mackenzie G.G., Zago M.P., Keen C.L., Oteiza P.I. Low intracellular zinc impairs the translocation of activated NF-kappa B to the nuclei in human neuroblastoma IMR-32 cells. J. Biol. Chem. 2002, 277:34610-34617.
52. Olin K.L., Shigenaga M.K., Ames B.N., Golub M.S., Gershwin M.E., Hendrickx A.G., Keen C.L. Maternal dietary zinc influences DNA strand break and 8-hydroxy-2'-deoxyguanosine levels in infant rhesus monkey liver. Proc. Soc. Exp. Biol. Med. 1993, 203:461-466.
53. Jourdan E., Emonet-Piccardi N., Didier C., Beani J.C., Favier A., Richard M.J. Effects of cadmium and zinc on solar-simulated light-irradiated cells: potential role of zinc-metallothionein in zinc-induced genoprotection. Arch. Biochem. Biophys. 2002, 405:170-177.
54. Jourdan E., Marie Jeanne R., Regine S., Pascale G. Zinc-metallothionein genoprotective effect is independent of the glutathione depletion in HaCaT keratinocytes after solar light irradiation. J. Cell. Biochem. 2004, 92:631-640.
55. Krezel A., Hao Q., Maret W. The zinc/thiolate redox biochemistry of metallothionein and the control of zinc ion fluctuations in cell signaling. Arch. Biochem. Biophys. 2007, 463:188-200.
56. Bell S.G., Vallee B.L. The metallothionein/thionein system: an oxidoreductive metabolic zinc link. Chembiochem 2009, 10:55-62.
57. Vasak M. Advances in metallothionein structure and functions. J. Trace Elem. Med. Biol. 2005, 19:13-17.
58. Mocchegiani E., Muzzioli M., Giacconi R., Cipriano C., Gasparini N., Franceschi C., Gaetti R., Cavalieri E., Suzuki H. Metallothioneins/PARP-1/IL-6 interplay on natural killer cell activity in elderly: parallelism with nonagenarians and old infected humans. Effect of zinc supply. Mech. Ageing Dev. 2003, 124:459-468.
59. Fenech M. The Genome Health Clinic and Genome Health Nutrigenomics concepts: diagnosis and nutritional treatment of genome and epigenome damage on an individual basis. Mutagenesis 2005, 20:255-269.
60. Thompson L.H., Schild D. Recombinational DNA repair and human disease. Mutat. Res. 2002, 509:49-78.
61. Rajagopalan H., Lengauer C. Aneuploidy and cancer. Nature 2004, 432:338-341.
62. Hambridge K.M. Zinc and chromium in human nutrition. J. Hum. Nutr. 1978, 32:99-110.
63. Federico A., Iodice P., Federico P., Del Rio A., Mellone M.C., Catalano G., Federico P. Effects of selenium and zinc supplementation on nutritional status in patients with cancer of digestive tract. Eur. J. Clin. Nutr. 2001, 55:293-297.
64. Prasad A.S. Zinc deficiency in humans: a neglected problem. J. Am. Coll. Nutr. 1998, 17:542-543.
65. Prasad A.S. Zinc and immunity. Mol. Cell. Biochem. 1998, 188:63-69.
66. Prasad A.S., Beck F.W., Doerr T.D., Shamsa F.H., Penny H.S., Marks S.C., Kaplan J., Kucuk O., Mathog R.H. Nutritional and zinc status of head and neck cancer patients: an interpretive review. J. Am. Coll. Nutr. 1998, 17:409-418.
67. Fong L.Y., Lau K.M., Huebner K., Magee P.N. Induction of esophageal tumors in zinc-deficient rats by single low doses of N-nitrosomethylbenzylamine (NMBA): analysis of cell proliferation, and mutations in H-ras and p53 genes. Carcinogenesis 1997, 18:1477-1484.
68. Zhang Z.F, Kurtz R.C., Yu G.P., Sun M., Gargon N., Karpeh M., Fein J.S., Harlap S. Adenocarcinomas of the esophagus and gastric cardia: the role of diet. Nutr. Cancer 1997, 27:298-309.
69. Lipman T.O., Diamond A., Mellow M.H., Patterson K.Y. Esophageal zinc content in human squamous esophageal cancer. J. Am. Coll. Nutr. 1987, 6:41-46.
70. Newberne P.M., Broitman S., Schrager T.F. Esophageal carcinogenesis in the rat: zinc deficiency, DNA methylation and alkyltransferase activity. Pathobiology 1997, 65:253-263.
71. Donahue T., Hines O.J. The ZIP4 pathway in pancreatic cancer. Cancer Biol. Ther. 2010, 9:243-245.
72. Hogstrand C., Kille P., Nicholson R.I., Taylor K.M. Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends Mol. Med. 2009, 15:101-111.
73. Franklin R.B., Feng P., Milon B., Desouki M.M., Singh K.K., Kajdacsy-Balla A., Bagasra O., Costello L.C. hZIP1 zinc uptake transporter down regulation and zinc depletion in prostate cancer. Mol. Cancer 2005, 4:32.
74. Hansen C.R., Malecha M., Mackenzie T.B., Kroll J. Copper and zinc deficiencies in association with depression and neurological findings. Biol. Psychiatry 1983, 18:395-401.
75. Black M.M. Zinc deficiency and child development. Am. J. Clin. Nutr. 1998, 68:464S-469S.
76. Black R.E. Therapeutic and preventive effects of zinc on serious childhood infectious diseases in developing countries. Am. J. Clin. Nutr. 1998, 68:476S-479S.
77. Sandstead H.H., Frederickson C.J., Penland J.G. History of zinc as related to brain function. J. Nutr. 2000, 130:496S-502S.
78. Salgueiro M.J., Weill R., Zubillaga M., Lysionek A., Caro R., Goldman C., Barrado D., Sarrasague M.M., Ridolfi A., Boccio J. Zinc deficiency and growth: current concepts in relationship to two important points: intellectual and sexual development. Biol. Trace Elem. Res. 2004, 99:49-69.
79. Salgueiro M.J., Zubillaga M.B., Lysionek A.E., Caro R.A., Weill R., Boccio J.R. The role of zinc in the growth and development of children. Nutrition 2002, 18:510-519.
80. Yan M., Song Y., Wong C.P., Hardin K., Ho E. Zinc deficiency alters DNA damage response genes in normal human prostate epithelial cells. J. Nutr. 2008, 138:667-673.
81. Sharif R., Thomas P., Zalewski P., Graham R.D., Fenech M. The effect of zinc sulphate and zinc carnosine on genome stability and cytotoxicity in the WIL2-NS human lymphoblastoid cell line. Mutat. Res. 2011, 720:22-33.
82. Fenech M.F. Dietary reference values of individual micronutrients and nutriomes for genome damage prevention: current status and a road map to the future. Am. J. Clin. Nutr. 2010, 91:1438S-1454S.
83. Fenech M. Cytokinesis-block micronucleus cytome assay. Nat. Protoc. 2007, 2:1084-1104.
84. Fenech M., Kirsch-Volders M., Natarajan A.T., Surralles J., Crott J.W., Parry J., Norppa H., Eastmond D.A., Tucker J.D., Thomas P. Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis 2011, 26:125-132.
85. Xu B., Sun Z., Liu Z., Guo H., Liu Q., Jiang H., Zou Y., Gong Y., Tischfield J.A., Shao C. Replication stress induces micronuclei comprising of aggregated DNA double-strand breaks. PLoS One 2011, 6:e18618.
86. Kimura M., Umegaki K., Higuchi M., Thomas P., Fenech M. Methylenetetrahydrofolate reductase C677T polymorphism, folic acid and riboflavin are important determinants of genome stability in cultured human lymphocytes. J. Nutr. 2004, 134:48-56.
87. Wu J., Lyons G.H., Graham R.D., Fenech M.F. The effect of selenium, as selenomethionine, on genome stability and cytotoxicity in human lymphocytes measured using the cytokinesis-block micronucleus cytome assay. Mutagenesis 2009, 24:225-232.
88. Leopardi P., Marcon F., Caiola S., Cafolla A., Siniscalchi E., Zijno A., Crebelli R. Effects of folic acid deficiency and MTHFR C677T polymorphism on spontaneous and radiation-induced micronuclei in human lymphocytes. Mutagenesis 2006, 21:327-333.
89. Zenzen V., Fauth E., Zankl H., Janzowski C., Eisenbrand G. Mutagenic and cytotoxic effectiveness of zinc dimethyl and zinc diisononyldithiocarbamate in human lymphocyte cultures. Mutat. Res. 2001, 497:89-99.
90. Santra M., Das S.K., Talukder G., Sharma A. Induction of micronuclei by zinc in human leukocytes: a study using cytokinesis-block micronucleus assay. Biol. Trace Elem. Res. 2002, 88:139-144.
91. Bruno R.S., Song Y., Leonard S.W., Mustacich D.J., Taylor A.W., Traber M.G., Ho E. Dietary zinc restriction in rats alters antioxidant status and increases plasma F2 isoprostanes. J. Nutr. Biochem. 2007, 18:509-518.
92. Shibuya K., Suzuki J.S., Kito H., Naganuma A., Tohyama C., Satoh M. Protective role of metallothionein in bone marrow injury caused by X-irradiation. J. Toxicol. Sci. 2008, 33:479-484.
93. Song Y., Chung C.S., Bruno R.S., Traber M.G., Brown K.H., King J.C., Ho E. Dietary zinc restriction and repletion affects DNA integrity in healthy men. Am. J. Clin. Nutr. 2009, 90:321-328.
94. Xie H., Holmes A.L., Young J.L., Qin Q., Joyce K., Pelsue S.C., Peng C., Wise S.S., Jeevarajan A.S., Wallace W.T., Hammond D., Wise J.P. Zinc chromate induces chromosome instability and DNA double strand breaks in human lung cells. Toxicol. Appl. Pharmacol. 2009, 234:293-299.
95. Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300:1542-1548.
96. Falck J., Coates J., Jackson S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005, 434:605-611.
97. Wise S.S., Holmes A.L., Qin Q., Xie H., Katsifis S.P., Thompson W.D., Wise J.P. Comparative genotoxicity and cytotoxicity of four hexavalent chromium compounds in human bronchial cells. Chem. Res. Toxicol. 2010, 23:365-372.
98. Bae S.N., Kim J., Lee Y.S., Kim J.D., Kim M.Y., Park L.O. Cytotoxic effect of zinc-citrate compound on choriocarcinoma cell lines. Placenta 2007, 28:22-30.
99. Sliwinski T., Czechowska A., Kolodziejczak M., Jajte J., Wisniewska-Jarosinska M., Blasiak J. Zinc salts differentially modulate DNA damage in normal and cancer cells. Cell Biol. Int. 2009, 33:542-547.
100. Tapisso J.T., Marques C.C., Mathias Mda L., Ramalhinho Mda G. Induction of micronuclei and sister chromatid exchange in bone-marrow cells and abnormalities in sperm of Algerian mice (Mus spretus) exposed to cadmium, lead and zinc. Mutat. Res. 2009, 678:59-64.
101. W. World Health Organization Environment Health Criteria 221: Zinc 2001, World Health Organization, Geneva, p. 360.
102. Domingo J.L., Llobet J.M., Paternain J.L., Corbella J. Acute zinc intoxication: comparison of the antidotal efficacy of several chelating agents. Vet. Hum. Toxicol. 1988, 30:224-228.
103. Wang P., Guliaev A.B., Hang B. Metal inhibition of human N-methylpurine-DNA glycosylase activity in base excision repair. Toxicol. Lett. 2006, 166:237-247.
104. Egger G., Liang G., Aparicio A., Jones P.A. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004, 429:457-463.
105. Richardson B. Impact of aging on DNA methylation. Ageing Res. Rev. 2003, 2:245-261.
106. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J. Mol. Biol. 1987, 196:261-282.
107. Okano M., Xie S., Li E. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res. 1998, 26:2536-2540.
108. Bestor T. Structure of mammalian DNA methyltransferase as deduced from the inferred amino acid sequence and direct studies of the protein. Biochem. Soc. Trans. 1988, 16:944-947.
109. Duerre J.A., Wallwork J.C. Methionine metabolism in isolated perfused livers from rats fed on zinc-deficient and restricted diets. Br. J. Nutr. 1986, 56:395-405.
110. Wallwork J.C., Duerre J.A. Effect of zinc deficiency on methionine metabolism, methylation reactions and protein synthesis in isolated perfused rat liver. J. Nutr. 1985, 115:252-262.
111. Breksa A.P., Garrow T.A. Recombinant human liver betaine-homocysteine S-methyltransferase: identification of three cysteine residues critical for zinc binding. Biochemistry 1999, 38:13991-13998.
112. Maret W., Sandstead H.H. Possible roles of zinc nutriture in the fetal origins of disease. Exp. Gerontol. 2008, 43:378-381.
113. Evans J.C., Huddler D.P., Jiracek J., Castro C., Millian N.S., Garrow T.A., Ludwig M.L. Betaine-homocysteine methyltransferase: zinc in a distorted barrel. Structure 2002, 10:1159-1171.
114. Koutmos M., Pejchal R., Bomer T.M., Matthews R.G., Smith J.L., Ludwig M.L. Metal active site elasticity linked to activation of homocysteine in methionine synthases. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3286-3291.
115. Matthews R.G., Goulding C.W. Enzyme-catalyzed methyl transfers to thiols: the role of zinc. Curr. Opin. Chem. Biol. 1997, 1:332-339.
116. Blasco M.A. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 2005, 6:611-622.
117. Callen E., Surralles J. Telomere dysfunction in genome instability syndromes. Mutat. Res. 2004, 567:85-104.
118. Rodier F., Kim S.H., Nijjar T., Yaswen P., Campisi J. Cancer and aging: the importance of telomeres in genome maintenance. Int. J. Biochem. Cell Biol. 2005, 37:977-990.
119. Bull C., Fenech M. Genome-health nutrigenomics and nutrigenetics: nutritional requirements or 'nutriomes' for chromosomal stability and telomere maintenance at the individual level. Proc. Nutr. Soc. 2008, 67:146-156.
120. Liu Q., Wang H., Hu D., Ding C., Xu H., Tao D. Effects of trace elements on the telomere lengths of hepatocytes L-02 and hepatoma cells SMMC-7721. Biol. Trace Elem. Res. 2004, 100:215-227.
121. Cipriano C., Tesei S., Malavolta M., Giacconi R., Muti E., Costarelli L., Piacenza F., Pierpaoli S., Galeazzi R., Blasco M., Vera E., Canela A., Lattanzio F., Mocchegiani E. Accumulation of cells with short telomeres is associated with impaired zinc homeostasis and inflammation in old hypertensive participants. J. Gerontol. A: Biol. Sci. Med. Sci. 2009, 64:745-751.
122. Lehtio L., Collins R., van den Berg S., Johansson A., Dahlgren L.G., Hammarstrom M., Helleday T., Holmberg-Schiavone L., Karlberg T., Weigelt J. Zinc binding catalytic domain of human tankyrase 1. J. Mol. Biol. 2008, 379:136-145.
123. Smith S., Giriat I., Schmitt A., de Lange T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 1998, 282:1484-1487.
124. Smith S., de Lange T. Tankyrase promotes telomere elongation in human cells. Curr. Biol. 2000, 10:1299-1302.
125. van Steensel B., de Lange T. Control of telomere length by the human telomeric protein TRF1. Nature 1997, 385:740-743.
126. d'Adda di Fagagna F., Hande M.P., Tong W.M., Lansdorp P.M., Wang Z.Q., Jackson S.P. Functions of poly(ADP-ribose) polymerase in controlling telomere length and chromosomal stability. Nat. Genet. 1999, 23:76-80.
127. Fenech M. Micronutrients and genomic stability: a new paradigm for recommended dietary allowances (RDAs). Food Chem. Toxicol. 2002, 40:1113-1117.
128. Fenech M. Nutrition and genome health. Forum Nutr. 2007, 60:49-65.
129. Liuzzi J.P., Cousins R.J. Mammalian zinc transporters. Annu. Rev. Nutr. 2004, 24:151-172.
130. Sekler I., Sensi S.L., Hershfinkel M., Silverman W.F. Mechanism and regulation of cellular zinc transport. Mol. Med. 2007, 13:337-343.
131. Lichten L.A., Cousins R.J. Mammalian zinc transporters: nutritional and physiologic regulation. Annu. Rev. Nutr. 2009, 29:153-176.
132. Maret W., Sandstead H.H. Zinc requirements and the risks and benefits of zinc supplementation. J. Trace Elem. Med. Biol. 2006, 20:3-18.
133. Mocchegiani E., Giacconi R., Costarelli L., Muti E., Cipriano C., Tesei S., Pierpaoli S., Giuli C., Papa R., Marcellini F., Gasparini N., Pierandrei R., Piacenza F., Mariani E., Monti D., Dedoussis G., Kanoni S., Herbein G., Fulop T., Rink L., Jajte J., Malavolta M. Zinc deficiency and IL-6-174G/C polymorphism in old people from different European countries: effect of zinc supplementation. ZINCAGE study. Exp. Gerontol. 2008, 43:433-444.
134. Mariani E., Neri S., Cattini L., Mocchegiani E., Malavolta M., Dedoussis G.V., Kanoni S., Rink L., Jajte J., Facchini A. Effect of zinc supplementation on plasma IL-6 and MCP-1 production and NK cell function in healthy elderly: interactive influence of +647 MT1a and -174 IL-6 polymorphic alleles. Exp. Gerontol. 2008, 43:462-471.
135. Vasto S., Mocchegiani E., Malavolta M., Cuppari I., Listi F., Nuzzo D., Ditta V., Candore G.C. Caruso Zinc and inflammatory/immune response in aging. Ann. N. Y. Acad. Sci. 2007, 1100:111-122.
136. Giacconi R., Cipriano C., Albanese F., Boccoli G., Saba V., Olivieri F., Franceschi C.E., Mocchegiani E. The -174G/C polymorphism of IL-6 is useful to screen old subjects at risk for atherosclerosis or to reach successful ageing. Exp. Gerontol. 2004, 39:621-628.
137. Cipriano C., Malavolta M., Costarelli L., Giacconi R., Muti E., Gasparini N., Cardelli M., Monti D., Mariani E., Mocchegiani E. Polymorphisms in MT1a gene coding region are associated with longevity in Italian Central female population. Biogerontology 2006, 7:357-365.
138. Mocchegiani E., Giacconi R., Cipriano C., Muzzioli M., Gasparini N., Moresi R., Stecconi R., Suzuki H., Cavalieri E., Mariani E. MtmRNA gene expression, via IL-6 and glucocorticoids, as potential genetic marker of immunosenescence: lessons from very old mice and humans,. Exp. Gerontol. 2002, 37:349-357.
139. Mariani E., Mangialasche F., Feliziani F.T., Cecchetti R., Malavolta M., Bastiani P., Baglioni M., Dedoussis G., Fulop T., Herbein G., Jajte J., Monti D., Rink L., Mocchegiani E., Mecocci P. Effects of zinc supplementation on antioxidant enzyme activities in healthy old subjects. Exp. Gerontol. 2008, 43:445-451.
140. Mocchegiani E., Giacconi R., Cipriano C., Costarelli L., Muti E., Tesei S., Giuli C., Papa R., Marcellini F., Mariani E., Rink L., Herbein G., Varin A., Fulop T., Monti D., Jajte J., Dedoussis G., Gonos E.S., Trougakos I.P., Malavolta M. Zinc, metallothioneins, and longevity - effect of zinc supplementation: zincage study. Ann. N. Y. Acad. Sci. 2007, 1119:129-146.