Metallothionein polymorphisms in pathological processes

Metallomics

Volumn 6, Issue 1, 2014, Pages 55-68

  Raudenska, Martina ^a,b   Gumulec, Jaromir ^a,b   Podlaha, Ondrej ^c   Sztalmachova, Marketa ^a,d   Babula, Petr ^e   Eckschlager, Tomas ^f   Adam, Vojtech ^b,d   Kizek, Rene ^b,d   Masarik, Michal ^a,b  

^a MASARYK UNIVERSITY   (Czech Republic)

^b BRNO UNIVERSITY OF TECHNOLOGY   (Czech Republic)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d MENDEL UNIVERSITY IN BRNO   (Czech Republic)

^e UNIVERSITY OF VETERINARY AND PHARMACEUTICAL SCIENCES   (Czech Republic)

^f UNIVERSITY HOSPITAL MOTOL   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DETOXIFICATION; FREE RADICALS;

ANTIOXIDANT DEFENSE; GENETIC CHARACTERISTICS; GENETIC POLYMORPHISMS; LOW MOLECULAR WEIGHT; METAL-BINDING PROTEIN; OXYGEN FREE RADICALS; PATHOLOGICAL PROCESS; TYPE 2 DIABETES MELLITUS;

DISEASES;

ALKYLATING AGENT; METALLOTHIONEIN; METALLOTHIONEIN 4; METALLOTHIONEIN I; METALLOTHIONEIN II; METALLOTHIONEIN III; OXYGEN RADICAL; UNCLASSIFIED DRUG;

AGING; ATHEROSCLEROSIS; CANCER RISK; DETOXIFICATION; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETIC TRAIT; HUMAN; LIFESTYLE; METAL METABOLISM; MULTIGENE FAMILY; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

CARDIOMYOPATHIES; DIABETES MELLITUS, TYPE 2; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; METALLOTHIONEIN; MULTIGENE FAMILY; NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN ISOFORMS;

EID: 84890911633     PISSN: 17565901     EISSN: 1756591X     Source Type: Journal    
DOI: 10.1039/c3mt00132f     Document Type: Review

References (119)

1. J. Busciglio B. A. Yankner Apoptosis and increased generation of reactive oxygen species in Downs-syndrome neurons in-vitro Nature 1995 378 776 779 10.1038/378776a0
2. J. C. A. Marr H. L. Bergman J. Lipton C. Hogstrand Differences in relative sensitivity of naive and metals-acclimated brown and rainbow-trout exposed to metals representative of the clark-fork river, montana Can. J. Fish. Aquat. Sci. 1995 52 2016 2030 10.1139/f95-793
3. S. Silver Bacterial resistances to toxic metal ions-a review Gene 1996 179 9 19 10.1016/s0378-1119(96)00323-x
4. T. K. S. Janssens D. Roelofs N. M. van Straalen Molecular mechanisms of heavy metal tolerance and evolution in invertebrates Insect Sci. 2009 16 3 18 10.1111/j.1744-7917.2009.00249.x
5. V. Adam I. Fabrik T. Eckschlager M. Stiborova L. Trnkova R. Kizek Vertebrate metallothioneins as target molecules for analytical techniques TrAC, Trends Anal. Chem. 2010 29 409 418 10.1016/j.trac.2010.02.004
6. V. Adam J. Petrlova J. Wang T. Eckschlager L. Trnkova R. Kizek Zeptomole electrochemical detection of metallothioneins PLoS One 2010 5 e11441 10.1371/journal.pone.0011441
7. S. Krizkova I. Fabrik V. Adam P. Hrabeta T. Eckschlager R. Kizek Metallothionein-a promising tool for cancer diagnostics Br. Med. J. 2009 110 93 97
8. B. Y. Lee D. H. Shin S. Cho K. S. Seo H. Kim Genome-wide analysis of copy number variations reveals that aging processes influence body fat distribution in Korea Associated Resource (KARE) cohorts Hum. Genet. 2012 131 1795 1804 10.1007/s00439-012-1203-1
9. P. Seibold R. Hein P. Schmezer P. Hall J. J. Liu N. Dahmen D. Flesch-Janys O. Popanda J. Chang-Claude Polymorphisms in oxidative stress-related genes and postmenopausal breast cancer risk Int. J. Cancer 2011 129 1467 1476 10.1002/ijc.25761
10. Y. Koga M. Pelizzola E. Cheng M. Krauthammer M. Sznol S. Ariyan D. Narayan A. M. Molinaro R. Halaban S. M. Weissman Genome-wide screen of promoter methylation identifies novel markers in melanoma Genome Res. 2009 19 1462 1470 10.1101/gr.091447.109
11. L. Marselli J. Thorne S. Dahiya D. C. Sgroi A. Sharma S. Bonner-Weir P. Marchetti G. C. Weir Gene expression profiles of beta-cell enriched tissue obtained by laser capture microdissection from subjects with type 2 diabetes PLoS One 2010 5 e11499 10.1371/journal.pone.0011499
12. M. Hlavna M. Raudenska K. Hudcova J. Gumulec M. Sztalmachova V. Tanhauserova P. Babula V. Adam T. Eckschlager R. Kizek M. Masarik MicroRNAs and zinc metabolism-related gene expression in prostate cancer cell lines treated with zinc(ii) ions Int. J. Oncol. 2012 41 2237 2244 10.3892/ijo.2012.1655
13. J. T. den Dunnen S. E. Antonarakis Mutation nomenclature extensions and suggestions to describe complex mutations: a discussion Hum. Mutat. 2000 15 7 12 10.1002/(SICI)1098-1004(200001)15:1<7::AID-HUMU4>3.0.CO;2-N
14. F. S. Collins L. D. Brooks A. Chakravarti A DNA polymorphism discovery resource for research on human genetic variation Genome Res. 1998 8 1229 1231
15. E. Alexov Numerical calculations of the pH of maximal protein stability-the effect of the sequence composition and three-dimensional structure Eur. J. Biochem. 2004 271 173 185 10.1046/j.1432-1033.2003.03917.x
16. V. Chelliah L. Chen T. L. Blundell S. C. Lovell Distinguishing structural and functional restraints in evolution in order to identify interaction sites J. Mol. Biol. 2004 342 1487 1504 10.1016/j.jmb.2004.08.022
17. D. Gilis M. Rooman Predicting protein stability changes upon mutation using database-derived potentials: solvent accessibility determines the importance of local versus non-local interactions along the sequence J. Mol. Biol. 1997 272 276 290 10.1006/jmbi.1997.1237
18. J. V. Chamary J. L. Parmley L. D. Hurst Hearing silence: non-neutral evolution at synonymous sites in mammals Nat. Rev. Genet. 2006 7 98 108 10.1038/nrg1770
19. H. Akashi Synonymous codon usage in Drosophila-melanogaster-natural- selection and translational accuracy Genetics 1994 136 927 935
20. Y. Xing C. Lee Assessing the application of Ka/Ks ratio test to alternatively spliced exons Bioinformatics 2005 21 3701 3703 10.1093/bioinformatics/bit613
21. A. G. Nackley S. A. Shabalina I. E. Tchivileva K. Satterfield O. Korchynskyi S. S. Makarov W. Maixner L. Diatchenko Human catechol-O- methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure Science 2006 314 1930 1933 10.1126/science.1131262
22. C. C. Chang P. C. Huang Semi-empirical simulation of Zn/Cd binding site preference in the metal binding domains of mammalian metallothionein Protein Eng. 1996 9 1165 1172 10.1093/protein/9.12.1165
23. M. Fedurco I. Sestakova Adsorption of Cd,Zn-metallothionein on covered Hg electrodes and its voltammetric determination Bioelectrochem. Bioenerg. 1996 40 223 232 10.1016/0302-4598(96)01914-9
24. X. L. Yu M. Wojciechowski C. Fenselau Assessment of metals in reconstituted metallothioneins by electrospray mass-spectrometry Anal. Chem. 1993 65 1355 1359 10.1021/ac00058a010
25. J. Abel N. Deruiter Inhibition of hydroxyl-radical-generated DNA-degradation by metallothionein Toxicol. Lett. 1989 47 191 196 10.1016/0378-4274(89)90075-1
26. L. Cai J. B. Klein Y. J. Kang Metallothionein inhibits peroxynitrite-induced DNA and lipoprotein damage J. Biol. Chem. 2000 275 38957 38960 10.1074/jbc.C000593200
27. P. J. Thornalley M. Vasak Possible role for metallothionein in protection against radiation-induced oxidative stress-kinetics and mechanism of its reaction with superoxide and hydroxyl radicals Biochim. Biophys. Acta 1985 827 36 44 10.1016/0167-4838(85)90098-6
28. P. Babula M. Masarik V. Adam T. Eckschlager M. Stiborova L. Trnkova H. Skutkova I. Provaznik J. Hubalek R. Kizek Mammalian metallothioneins: properties and functions Metallomics 2012 4 739 750 10.1039/c2mt20081c
29. E. Tokuda S. I. Ono K. Ishige A. Naganuma Y. Ito T. Suzuki Metallothionein proteins expression, copper and zinc concentrations, and lipid peroxidation level in a rodent model for amyotrophic lateral sclerosis Toxicology 2007 229 33 41 10.1016/j.tox.2006.09.011
30. J. W. Bauman J. Liu Y. P. Liu C. D. Klaassen Increase in metallothionein produced by chemicals that induce oxidative stress Toxicol. Appl. Pharmacol. 1991 110 347 354 10.1016/s0041-008x(05)80017-1
31. G. K. Andrews Regulation of metallothionein gene expression by oxidative stress and metal ions Biochem. Pharmacol. 2000 59 95 104 10.1016/s0006-2952(99) 00301-9
32. M. Karin R. L. Eddy W. M. Henry L. L. Haley M. G. Byers T. B. Shows Human metallothionein genes are clustered on chromosome-16 Proc. Natl. Acad. Sci. U. S. A. 1984 81 5494 5498 10.1073/pnas.81.17.5494
33. F. A. Stennard A. F. Holloway J. Hamilton A. K. West Characterization of 6 additional human metallothionein genes Biochim. Biophys. Acta, Gene Struct. Expression 1994 1218 357 365 10.1016/0167-4781(94)90189-9
34. A. K. West R. Stallings C. E. Hildebrand R. Chiu M. Karin R. I. Richards Human metallothionein genes-structure of the functional locus at 16q13 Genomics 1990 8 513 518 10.1016/0888-7543(90)90038-v
35. Z. M. Liu G. G. Chen C. K. Y. Shum A. C. Vlantis M. G. Cherlan J. Koropatnick C. A. van Hasselta Induction of functional MT1 and MT2 isoforms by calcium in anaplastic thyroid carcinoma cells FEBS Lett. 2007 581 2465 2472 10.1016/j.febslet.2007.04.049
36. Y. Uchida F. Gomi T. Masumizu Y. Miura Growth inhibitory factor prevents neurite extension and the death of cortical neurons caused by high oxygen exposure through hydroxyl radical scavenging J. Biol. Chem. 2002 277 32353 32359 10.1074/jbc.M111263200
37. G. Meloni K. Zovo J. Kazantseva P. Palumaa M. Vasak Organization and assembly of metal-thiolate clusters in epithelium-specific metallothionein-4 J. Biol. Chem. 2006 281 14588 14595 10.1074/jbc.M601724200
38. R. Faraonio P. Moffatt O. LaRochelle H. M. Schipper R. S-Arnaud C. Seguin Characterization of cis-acting elements in the promoter of the mouse metallothionein-3 gene-activation of gene expression during neuronal differentiation of P19 embryonal carcinoma cells Eur. J. Biochem. 2000 267 1743 1753 10.1046/j.1432-1327.2000.01167.x
39. Z. Y. Huang Q. Zhang J. Chen Z. X. Zhuang X. R. Wang Bioaccumulation of metals and induction of metallothioneins in selected tissues of common carp (Cyprinus carpio L.) co-exposed to cadmium, mercury and lead Appl. Organomet. Chem. 2007 21 101 107 10.1002/aoc.1167
40. M. F. McAleer R. S. Tuan Metallothionein overexpression in human trophoblastic cells protects against cadmium-induced apoptosis In Vitro Mol. Toxicol. 2001 14 25 42
41. Y. P. Liu J. Liu S. M. Habeebu M. P. Waalkes C. D. Klaassen Metallothionein-I/II null mice are sensitive to chronic oval cadmium-induced nephrotoxicity Toxicol. Sci. 2000 57 167 176 10.1093/toxsci/57.1.167
42. A. U. R. Memon T. G. Kazi H. I. Afridi M. K. Jamali M. B. Arain N. Jalbani N. Syed Evaluation of zinc status in whole blood and scalp hair of female cancer patients Clin. Chim. Acta 2007 379 66 70 10.1016/j.cca.2006.12.009
43. Z. Kayaalti V. Aliyev T. Soylemezogiu The potential effect of metallothionein 2A-5 A/G single nucleotide polymorphism on blood cadmium, lead, zinc and copper levels Toxicol. Appl. Pharmacol. 2011 256 1 7 10.1016/j.taap.2011.06.023
44. T. Eckschlager V. Adam J. Hrabeta K. Figova R. Kizek Metallothioneins and cancer Curr. Protein Pept. Sci. 2009 10 360 375 10.2174/138920309788922243
45. H. Goulding B. Jasani H. Pereira A. Reid M. Galea J. A. Bell C. W. Elston J. F. Robertson R. W. Blamey R. A. Nicholson K. W. Schmid I. O. Ellis Metallothionein expression in human breast-cancer Br. J. Cancer 1995 72 968 972 10.1038/bjc.1995.443
46. H. G. Kim J. Y. Kim E. H. Han Y. P. Hwang J. H. Choi B. H. Park H. G. Jeong Metallothionein-2A overexpression increases the expression of matrix metalloproteinase-9 and invasion of breast cancer cells FEBS Lett. 2011 585 421 428 10.1016/j.febslet.2010.12.030
47. J. I. Izawa M. Moussa M. G. Cherian G. Doig J. L. Chin Metallothionein expression in renal cancer Urology 1998 52 767 772 10.1016/s0090-4295(98)00323-9
48. J. Gumulec M. Masarik S. Krizkova M. Hlavna P. Babula R. Hrabec A. Rovny M. Masarikova J. Sochor V. Adam T. Eckschlager R. Kizek Evaluation of alpha-methylacyl-CoA racemase, metallothionein and prostate specific antigen as prostate cancer prognostic markers Neoplasma 2012 59 191 200 10.4149/neo-2012-025
49. H. Wei M. M. Desouki S. Lin D. Xiao R. B. Franklin P. Feng Differential expression of metallothioneins (MTs) 1, 2, and 3 in response to zinc treatment in human prostate normal and malignant cells and tissues Mol. Cancer 2008 7 10.1186/1476-4598-7-7
50. J. Gumulec M. Masarik S. Krizkova V. Adam J. Hubalek J. Hrabeta T. Eckschlager M. Stiborova R. Kizek Insight to physiology and pathology of zinc(ii) ions and their actions in breast and prostate carcinoma Curr. Med. Chem. 2011 18 5041 5051 10.2174/092986711797636126
51. M. Masarik J. Gumulec M. Hlavna M. Sztalmachova P. Babula M. Raudenska M. Pavkova-Goldbergova N. Cernei J. Sochor O. Zitka B. Ruttkay-Nedecky S. Krizkova V. Adam R. Kizek Monitoring of the prostate tumour cells redox state and real-time proliferation by novel biophysical techniques and fluorescent staining Integr. Biol. 2012 4 672 684 10.1039/c2ib00157h
52. M. Masarik J. Gumulec M. Sztalmachova M. Hlavna P. Babula S. Krizkova M. Ryvolova M. Jurajda J. Sochor V. Adam R. Kizek Isolation of metallothionein from cells derived from aggressive form of high-grade prostate carcinoma using paramagnetic antibody-modified microbeads off-line coupled with electrochemical and electrophoretic analysis Electrophoresis 2011 32 3576 3588 10.1002/elps.201100301
53. S. Krizkova M. Ryvolova J. Hrabeta V. Adam M. Stiborova T. Eckschlager R. Kizek Metallothioneins and zinc in cancer diagnosis and therapy Drug Metab. Rev. 2012 44 287 301 10.3109/03602532.2012.725414
54. V. Pekarik J. Gumulec M. Masarik R. Kizek V. Adam Prostate cancer, miRNAs, metallothioneins and resistance to cytostatic drugs Curr. Med. Chem. 2013 20 534 544 10.2174/092986713804910102
55. J. K. Choi U. S. Yu O. J. Yoo S. Kim Differential coexpression analysis using microarray data and its application to human cancer Bioinformatics 2005 21 4348 4355 10.1093/bioinformatics/bti722
56. S. Suemori M. Shimazawa K. Kawase M. Satoh H. Nagase T. Yamamoto H. Hara Metallothionein, an endogenous antioxidant, protects against retinal neuron damage in mice Invest. Ophthalmol. Visual Sci. 2006 47 3975 3982 10.1167/iovs.06-0275
57. K. Wakida M. Shimazawa I. Hozumi M. Satoh H. Nagase T. Inuzuka H. Hara Neuroprotective effect of erythropoietin, and role of metallothionein-1 and -2, in permanent focal cerebral ischemia Neuroscience 2007 148 105 114 10.1016/j.neuroscience.2007.04.063
58. M. Penkowa S. Florit M. Giralt A. Quintana A. Molinero J. Carrasco J. Hidalgo Metallothionein reduces central nervous system inflammation, neuro degeneration, and cell death following kainic acid-induced epileptic seizures J. Neurosci. Res. 2005 79 522 534 10.1002/jnr.20387
59. A. E. Michalska K. H. A. Choo Targeting and germ-line transmission of a null mutation at the metallothionein I-loci and II-loci in mouse Proc. Natl. Acad. Sci. U. S. A. 1993 90 8088 8092 10.1073/pnas.90.17.8088
60. B. A. Masters E. J. Kelly C. J. Quaife R. L. Brinster R. D. Palmiter Targeted disruption of metallothionein-I and metallothionein-II genes increases sensitivity to cadmium Proc. Natl. Acad. Sci. U. S. A. 1994 91 584 588 10.1073/pnas.91.2.584
61. L. L. Pearce R. E. Gandley W. P. Han K. Wasserloos M. Stitt A. J. Kanai M. K. McLaughlin B. R. Pitt E. S. Levitan Role of metallothionein in nitric oxide signaling as revealed by a green fluorescent fusion protein Proc. Natl. Acad. Sci. U. S. A. 2000 97 477 482 10.1073/pnas.97.1.477
62. J. Carrasco M. Penkowa H. Hadberg A. Molinero J. Hidalgo Enhanced seizures and hippocampal neurodegeneration following kainic acid-induced seizures in metallothionein-I plus II-deficient mice Eur. J. Neurosci. 2000 12 2311 2322 10.1046/j.1460-9568.2000.00128.x
63. Y. Y. Yang P. D. Robbins J. S. Lazo Differential transactivation of human metallothionein-IIa in cisplatin-resistant and -sensitive cells Oncol. Res. 1998 10 85 98
64. M. Karin A. Haslinger A. Heguy T. Dietlin T. Cooke Metal-responsive elements act as positive modulators of human metallothionein-IIA enhancer activity Mol. Cell. Biol. 1987 7 606 613
65. M. P. Waalkes M. J. Harvey C. D. Klaassen Relative in vitro affinity of hepatic metallothionein for metals Toxicol. Lett. 1984 20 33 39 10.1016/0378-4274(84)90179-6
66. R. D. Palmiter 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. U. S. A. 1994 91 1219 1223 10.1073/pnas.91.4.1219
67. L. J. Hager R. D. Palmiter Transcriptional regulation of mouse-liver metallothionein-I gene by glucocorticoids Nature 1981 291 340 342 10.1038/291340a0
68. W. Lee A. Haslinger M. Karin R. Tjian Activation of transcription by two factors that bind promoter and enhancer sequences of the human metallothionein gene and SV40 Nature 1987 325 368 372 10.1038/325368a0
69. A. Haslinger M. Karin Upstream promoter element of the human metallothionein-IIA gene can act like an enhancer element Proc. Natl. Acad. Sci. U. S. A. 1985 82 8572 8576 10.1073/pnas.82.24.8572
70. F. Otsuka A. Iwamatsu K. Suzuki M. Ohsawa D. H. Hamer S. Koizumi Purification and characterization of a protein that binds to metal-responsive elements of the human metallothionein II(A) gene J. Biol. Chem. 1994 269 23700 23707
71. M. Karin A. Haslinger H. Holtgreve R. I. Richards P. Krauter H. M. Westphal M. Beato Characterization of DNA-sequences through which cadmium and glucocorticoid hormones induce human metallothionein-IIa gene Nature 1984 308 513 519 10.1038/308513a0
72. K. Suzuki S. Koizumi Individual metal responsive elements of the human metallothionein-IIA gene independently mediate responses to various heavy metal signals Ind. Health 2000 38 87 90 10.2486/indhealth.38.87
73. M. Ohtsuji F. Katsuoka A. Kobayashi H. Aburatani J. D. Hayes M. Yamamoto Nrf1 and Nrf2 Play distinct roles in activation of antioxidant response element-dependent genes J. Biol. Chem. 2008 283 33554 33562 10.1074/jbc. M804597200
74. Z. Kayaalti G. Mergen T. Soylemezoglu Effect of metallothionein core promoter region polymorphism on cadmium, zinc and copper levels in autopsy kidney tissues from a Turkish population Toxicol. Appl. Pharmacol. 2010 245 252 255 10.1016/j.taap.2010.03.007
75. C. Cipriano M. Malavolta L. Costarelli R. Giacconi E. Muti N. Gasparini M. Cardelli D. Monti E. Mariani E. Mocchegiani Polymorphisms in MT1a gene coding region are associated with longevity in Italian central female population Biogerontology 2006 7 357 365 10.1007/s10522-006-9050-x
76. L. Yang H. Y. Li T. Yu H. J. Zhao M. G. Cherian L. Cai Y. Liu Polymorphisms in metallothionein-1 and -2 genes associated with the risk of type 2 diabetes mellitus and its complications Am. J. Physiol.: Endocrinol. Metab. 2008 294 E987 E992 10.1152/ajpendo.90234.2008
77. A. I. Zavras A. J. Yoon M. K. Chen C. W. Lin S. F. Yang Metallothionein-1 genotypes in the risk of oral squamous cell carcinoma Ann. Surg. Oncol. 2011 18 1478 1483 10.1245/s10434-010-1431-3
78. Y. Wang J. M. Goodrich B. Gillespie R. Werner N. Basu A. Franzblau An investigation of modifying effects of metallothionein single-nucleotide polymorphisms on the association between mercury exposure and biomarker levels Environ. Health Perspect. 2012 120 530 534 10.1289/ehp.1104079
79. F. R. DeRubertis P. A. Craven M. F. Melhem Acceleration of diabetic renal injury in the superoxide dismutase knockout mouse: effects of tempol Metab., Clin. Exp. 2007 56 1256 1264 10.1016/j.metabol.2007.04.024
80. T. Nishikawa D. Edelstein X. L. Du S. Yamagishi T. Matsumura Y. Kaneda M. A. Yorek D. Beebe P. J. Oates H. P. Hammes I. Giardino M. Brownlee Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage Nature 2000 404 787 790 10.1038/35008121
81. V. Elangovan E. Shohami I. Gati R. Kohen Increased hepatic lipid soluble antioxidant capacity as compared to other organs of streptozotocin-induced diabetic rats: a cyclic voltammetry study Free Radical Res. 2000 32 125 134 10.1080/10715760000300131
82. R. H. Wong C. H. Huang C. B. Yeh H. S. Lee M. H. Chien S. F. Yang Effects of metallothionein-1 genetic polymorphism and cigarette smoking on the development of hepatocellular carcinoma Ann. Surg. Oncol. 2012 20 2088 2095 10.1245/s10434-012-2456-6
83. L. Sun X. Zhang Y. Kong L. Yu Effect of MT1M gene on the cell cycle and signaling pathway of Hep-G2 Int. J. Androl. 2004 10 932 934
84. K. Kita N. Miura M. Yoshida K. Yamazaki T. Ohkubo Y. Imai A. Naganuma Potential effect on cellular response to cadmium of a single-nucleotide A → G polymorphism in the promoter of the human gene for metallothionein IIA Hum. Genet. 2006 120 553 560 10.1007/s00439-006-0238-6
85. Z. Kayaalti T. Soylemezoglu The polymorphism of core promoter region on metallothionein 2A-metal binding protein in Turkish population Mol. Biol. Rep. 2010 37 185 190 10.1007/s11033-009-9586-3
86. E. Forma A. Krzeslak J. Wilkosz P. Jozwiak A. Szymczyk W. Rozanski M. Brys Metallothionein 2A genetic polymorphisms and risk of prostate cancer in a Polish population Cancer Genet. 2012 205 432 435 10.1016/j.cancergen.2012.05.005
87. D. Tekin Z. Kayaalti V. Aliyev T. Soylemezoglu The effects of metallothionein 2A polymorphism on placental cadmium accumulation: is metallothionein a modifiying factor in transfer of micronutrients to the fetus? J. Appl. Toxicol. 2012 32 270 275 10.1002/jat.1661
88. E. Mocchegiani R. Giacconi C. Cipriano M. Muzzioli N. Gasparini R. Moresi R. Stecconi H. Suzuki E. Cavalieri E. Mariani 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 10.1016/s0531-5565(01)00202-9
89. M. G. Cherian A. Jayasurya B. H. Bay Metallothioneins in human tumors and potential roles in carcinogenesis Mutat. Res., Fundam. Mol. Mech. Mutagen. 2003 533 201 209 10.1016/j.mrfmmm.2003.07.013
90. C. Gundacker K. J. Wittmann M. Kukuckova G. Komarnicki I. Hikkel M. Gencik Genetic background of lead and mercury metabolism in a group of medical students in Austria Environ. Res. 2009 109 786 796 10.1016/j.envres.2009.05.003
91. R. Giacconi C. Cipriano E. Muti L. Costarelli C. Maurizio V. Saba N. Gasparini M. Malavolta E. Mocchegiani Novel-209A/G MT2A polymorphism in old patients with type 2 diabetes and atherosclerosis: relationship with inflammation (IL-6) and zinc Biogerontology 2005 6 407 413 10.1007/s10522-005- 4907-y
92. R. Giacconi E. Muti M. Malavolta C. Cipriano L. Costarelli G. Bernardini N. Gasparini E. Mariani V. Saba G. Boccoli E. Mocchegiani The +838 C/G MT2A polymorphism, metals, and the inflammatory/immune response in carotid artery stenosis in elderly people Mol. Med. 2007 13 388 395 10.2119/2007-00045.Giacconi
93. X. Chen L. J. Lei L. T. Tian G. Y. Zhu T. Y. Jin Bone mineral density and polymorphisms in metallothionein 1A and 2A in a Chinese population exposed to cadmium Sci. Total Environ. 2012 423 12 17 10.1016/j.scitotenv.2012.02.020
94. R. Kozarova A. Postadzhiyan B. Finkov M. Apostolova Association of copy number variations and single nucleotide polymorphisms in metallothionein genes with pathogenesis of diabetes and coronary artery disease Atheroscler. Suppl. 2011 12 107 10.1016/S1567-5688(11)70504-9
95. J. A. McElroy E. C. Bryda S. D. McKay R. D. Schnabel J. F. Taylor Genetic variation at a metallothionein 2A promoter single-nucleotide polymorphism in white and black females in midwestern United States J. Toxicol. Environ. Health, Part A 2010 73 1283 1287 10.1080/15287394.2010.485067
96. N. Miura Individual susceptibility to cadmium toxicity and metallothionein gene polymorphisms: with references to current status of occupational cadmium exposure Ind. Health 2009 47 487 494
97. Y. Hayashi T. Hashizume K. Wakida M. Satoh Y. Uchida K. Watabe Z. Matsuyama A. Kimura T. Inuzuka I. Hozumi Association between metallothionein genes polymorphisms and sporadic amyotrophic lateral sclerosis in a Japanese population Amyotrophic Lateral Scler. Other Mot. Neuron Disord. 2006 7 22 26 10.1080/14660820600618766
98. Z. Kayaalti D. Tekin T. Soylemezoglu Role of metallothionein 2A polymorphism on lead metabolism: are pregnant women with a heterozygote genotype for metallothionein 2A polymorphism and their newborns at risk of having higher blood lead levels? Toxicol. Lett. 2011 205 S106 10.1016/j.toxlet.2011.05.383
99. K. Shibuya N. Nishimura J. S. Suzuki C. Tohyama A. Naganuma M. Satoh Role of metallothionein as a protective factor against radiation carcinogenesis J. Toxicol. Sci. 2008 33 651 655 10.2131/jts.33.651
100. M. P. Waalkes J. Liu K. S. Kasprzak B. A. Diwan Minimal influence of metallothionein over-expression on nickel carcinogenesis in mice Toxicol. Lett. 2004 153 357 364 10.1016/j.toxlet.2004.06.003
101. J. Zeng B. L. Vallee J. H. R. Kagi Zinc transfer from transcription factor-IIIA fingers to thionein clusters Proc. Natl. Acad. Sci. U. S. A. 1991 88 9984 9988 10.1073/pnas.88.22.9984
102. R. Shimoda W. E. Achanzar W. Qu T. Nagamine H. Takagi M. Mori M. P. Waalkes Metallothionein is a potential negative regulator of apoptosis Toxicol. Sci. 2003 73 294 300 10.1093/toxsci/kfg095
103. B. Werynska B. Pula B. Muszczynska-Bernhard A. Gomulkiewicz A. Jethon M. Podhorska-Okolow R. Jankowska P. Dziegiel Expression of metallothionein-III in patients with non-small cell lung cancer Anticancer Res. 2013 33 965 974
104. A. M. L. Janssen W. van Duijn F. Kubben G. Griffioen C. Lamers J. van Krieken C. J. H. van de Velde H. W. Verspaget Prognostic significance of metallothionein in human gastrointestinal cancer Clin. Cancer Res. 2002 8 1889 1896
105. M. Moussa D. Kloth G. Peers M. G. Cherian J. V. Frei J. L. Chin Metallothionein expression in prostatic carcinoma: correlation with Gleason grade, pathologic stage, DNA content and serum level of prostate-specific antigen Clin. Invest. Med. 1997 20 371 380
106. Q. R. Liang E. C. Carlson R. V. Donthi P. M. Kralik X. Shen P. N. Epstein Overexpression of metallothionein reduces diabetic cardiomyopathy Diabetes 2002 51 174 181
107. S. R. Zheng E. C. Carlson L. Yang P. M. Kralik Y. Huang P. N. Epstein Podocyte-specific overexpression of the antioxidant metallothionein reduces diabetic nephropathy J. Am. Soc. Nephrol. 2008 19 2077 2085 10.1681/asn. 2007080967
108. M. D. Apostolova K. H. A. Choo A. E. Michalska C. Tohyama Analysis of the possible protective role of metallothionein in streptozotocin-induced diabetes using metallothionein-null mice J. Trace Elem. Med. Biol. 1997 11 1 7
109. P. Palumaa I. Tammiste K. Kruusel L. Kangur H. Jornvall R. Sillard Metal binding of metallothionein-3 versus metallothionein-2: lower affinity and higher plasticity Biochim. Biophys. Acta, Proteins Proteomics 2005 1747 205 211 10.1016/j.bbapap.2004.11.007
110. J. Hidalgo M. Aschner P. Zatta M. Vasak Roles of the metallothionein family of proteins in the central nervous system Brain Res. Bull. 2001 55 133 145 10.1016/s0361-9230(01)00452-x
111. A. K. Sewell L. T. Jensen J. C. Erickson R. D. Palmiter D. R. Winge Bioactivity of metallothionein-3 correlates with its novel beta-domain sequence rather than metal-binding properties Biochemistry 1995 34 4740 4747 10.1021/bi00014a031
112. Y. Manso J. Carrasco G. Comes G. Meloni P. A. Adlard A. I. Bush M. Vasak J. Hidalgo Characterization of the role of metallothionein-3 in an animal model of Alzheimer's disease Cell. Mol. Life Sci. 2012 69 3683 3700 10.1007/s00018-012-1047-9
113. M. C. Amoureux D. Van Gool M. T. Herrero R. Dom F. C. Colpaert P. J. Pauwels Regulation of metallothionein-III (GIF) mRNA in the brain of patients with Alzheimer disease is not impaired Mol. Chem. Neuropathol. 1997 32 101 121 10.1007/bf02815170
114. D. A. Drum Are toxic biometals destroying your children's future? Biometals 2009 22 697 700 10.1007/s10534-009-9212-9
115. H. Fusheng X. Feiyan X. Han Z. Fang Study on the relationship between gene polymorphism of metallothionein 3 and childhood autism Chin. J. Clin. 2011 5 2559 2562
116. C. J. Quaife S. D. Findley J. C. Erickson G. J. Froelick E. J. Kelly B. P. Zambrowicz R. D. Palmiter Induction of a new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia Biochemistry 1994 33 7250 7259 10.1021/bi00189a029
117. L. Tio L. Villarreal S. Atrian M. Capdevila Functional differentiation in the mammalian metallothionein gene family-metal binding features of mouse MT4 and comparison with its paralog MT1 J. Biol. Chem. 2004 279 24403 24413 10.1074/jbc.M401346200
118. H. I. Chen Y. W. Chiu Y. K. Hsu W. F. Li Y. C. Chen H. Y. Chuang The association of metallothionein-4 gene polymorphism and renal function in long-term lead-exposed workers Biol. Trace Elem. Res. 2010 137 55 62 10.1007/s12011-009-8564-x
119. Z. Kayaalti L. Sahiner M. E. Durakoglugil T. Soylemezoglu Distributions of interleukin-6 (IL-6) promoter and metallothionein 2A (MT2A) core promoter region gene polymorphisms and their associations with aging in Turkish population Arch. Gerontol. Geriatr. 2011 53 354 358 10.1016/j.archger.2011.01. 001