The concentration of glutathione in human erythrocytes is a heritable trait

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 742-749

  Van 'T Erve, Thomas J ^a   Wagner, Brett A ^b   Ryckman, Kelli K ^a   Raife, Thomas J ^b   Buettner, Garry R ^b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

Author keywords

Free radicals; Glutathione; Heritability; Red blood cells; Twin study

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE;

ADULT; ARTICLE; DIZYGOTIC TWINS; ERYTHROCYTE; FEMALE; GENETIC DIFFERENCE; GENETIC TRAIT; HERITABILITY; HUMAN; HUMAN CELL; MALE; MONOZYGOTIC TWINS; NORMAL HUMAN; OXIDATION; PHENOTYPE; PRIORITY JOURNAL; TWINS; CHEMISTRY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MIDDLE AGED; QUANTITATIVE TRAIT; YOUNG ADULT;

ADULT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ERYTHROCYTES; FEMALE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; MALE; MIDDLE AGED; QUANTITATIVE TRAIT, HERITABLE; TWINS, DIZYGOTIC; TWINS, MONOZYGOTIC; YOUNG ADULT;

EID: 84883290132     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.08.002     Document Type: Article

References (59)

1. H. Song, C.A. Lang, and T.S. Chen The role of glutathione in p-aminophenol-induced nephrotoxicity in the mouse Drug Chem. Toxicol. 22 1999 529 544 (Pubitemid 29372671)
2. J.B. Adams, M. Baral, E. Geis, J. Mitchell, J. Ingram, A. Hensley, I. Zappia, S. Newmark, E. Gehn, R.A. Rubin, K. Mitchell, J. Bradstreet, and J. El-Dahr Safety and efficacy of oral DMSA therapy for children with autism spectrum disorders. Part A. Medical results BMC Clin. Pharmacol 9 2009
3. H. Diken, M. Kelle, C. Tumer, B. Deniz, Y. Baylan, and A. Sermet Effects of cigarette smoking on blood antioxidant status in short-term and long-term smokers Turk. J. Med. Sci. 31 2001 553 557 (Pubitemid 34136142)
4. J. Li, H. Wang, G.D. Stoner, and T.M. Bray Dietary supplementation with cysteine prodrugs selectively restores tissue glutathione levels and redox status in protein-malnourished mice J. Nutr. Biochem. 13 2002 625 633 (Pubitemid 35246553)
5. C.G. Taylor, L.E. Nagy, and T.M. Bray Nutritional and hormonal regulation of glutathione homeostasis Curr. Top. Cell Regul. 34 1996 189 208
6. C.A. Lang, B.J. Mills, W. Mastropaolo, and M.C. Liu Blood glutathione decreases in chronic diseases J. Lab. Clin. Med. 135 2000 402 405
7. S.J. Chinta, S. Rajagopalan, D.A. Butterfield, and J.K. Andersen In vitro and in vivo neuroprotection by γ-glutamylcysteine ethyl ester against MPTP: relevance to the role of glutathione in Parkinson′s disease Neurosci. Lett 402 2006 137 141 (Pubitemid 43766441)
8. G.R. Bernard, A.P. Wheeler, M.M. Arons, P.E. Morris, H.L. Paz, J.A. Russell, and P.E. Wright A trial of antioxidants N-acetyl cysteine and procysteine in ARDS Chest 112 1997 164 172 (Pubitemid 27343614)
9. T.E. Forrester, V. Badaloo, F.I. Bennett, and A.A. Jackson Excessive excretion and decreased levels of blood glutathione in type II diabetes mellitus Eur. J. Clin. Nutr. 44 1990 847 850
10. K. Murakami, T. Kondo, Y. Ohtsuka, M. Shimada, and Y. Kawakami Impairment of glutathione metabolism in erythrocytes from patients with diabetes mellitus Metabolism 38 1989 753 758 (Pubitemid 19205580)
11. E. Altomare, G. Vendemiale, and O. Albano Hepatic glutathione content in patients with alcoholic and non-alcoholic liver diseases Life Sci. 43 1988 991 998
12. R. Buhl, H.A. Jaffe, K.J. Holroyd, F.B. Wells, A. Mastrangli, A. Cantin, C. Saltini, A.M. Cantin, and R.G. Crystal Systemic glutathione deficiency in symptom free HIV-seropositive individuals Lancet 2 1989 1294 1298 (Pubitemid 20005670)
13. J.J. Harding Free and protein-bound glutathione in normal and cataractous human lenses Biochem. J. 117 1970 957 960
14. G.A. Hazelton, and C.A. Lang Glutathione biosynthesis in the aging adult yellow-fever mosquito [Aedes aegypti (Louisville)] Biochem. J. 210 1983 289 295 (Pubitemid 13124417)
15. G.A. Hazelton, and C.A. Lang Glutathione contents of tissues in the aging mouse Biochem. J. 188 1980 25 30 (Pubitemid 10092504)
16. J.P. Richie Jr, B.J. Mills, and C.A. Lang Correction of a glutathione deficiency in the aging mosquito increases its longevity Proc. Soc. Exp. Biol. Med. 184 1987 113 117 (Pubitemid 17007288)
17. I. Rebrin, M.J. Forster, and R.S. Sohal Association between life-span extension by caloric restriction and thiol redox state in two different strains of mice Free Radic. Biol. Med 51 2011 225 233
18. C.A. Lang, B.J. Mills, H.L. Lang, M.C. Liu, W.M. Usui, J.P. Richie Jr, W. Mastropaolo, and S.A. Murrell High blood glutathione levels accompany excellent physical and mental health in women ages 60 to 103 years J. Lab. Clin. Med. 140 2002 413 417 (Pubitemid 36017063)
19. J.P. Richie Jr, P. Abraham, and Y. Leutzinger Long-term stability of blood glutathione and cysteine in humans Clin. Chem. 42 1996 1100 1105 (Pubitemid 26231418)
20. B.J. Mills, J.P. Richie Jr, and C.A. Lang Glutathione disulfide variability in normal human blood Anal. Biochem. 222 1994 95 101 (Pubitemid 24319531)
21. H.H. Newman, F.N. Freeman, and J.J. Holzinger Twins: a Study of Heredity and Environment 1937 Univ. Chicago Press Chicago
22. D. Boomsma, A. Busjahn, and L. Peltonen Classical twin studies and beyond Nat. Rev. Genet. 3 2002 872 882 (Pubitemid 35303519)
23. P.E. Shrout, and J.L. Fleiss Intraclass correlations: uses in assessing rater reliability Psychol. Bull. 86 1979 420 428
24. K.W. Kang, J.C. Christian, and J.A. Norton Jr. Heritability estimates from twin studies. I. Formulae of heritability estimates Acta Genet. Med. Gemellol. (Roma) 27 1978 39 44 (Pubitemid 9107823)
25. H.J. Park, E. Mah, and R.S. Bruno Validation of high-performance liquid chromatography-boron-doped diamond detection for assessing hepatic glutathione redox status Anal. Biochem. 407 2010 151 159
26. F.Q. Schafer, and G.R. Buettner Redox state of the cell as viewed though the glutathione disulfide/glutathione couple Free Radic. Biol. Med. 30 2001 1191 1212 (Pubitemid 32463931)
27. P. Swietach, T. Tiffert, J.M.A. Mauritz, R. Seear, A. Esposito, C.F. Kaminski, V.L. Lew, and R.D. Vaughan-Jones Hydrogen ion dynamics in human red blood cells J. Physiol. 588 2010 4995 5014
28. K. Silventoinen, S. Sammalisto, M. Perola, D.I. Boomsma, B.K. Cornes, C. Davis, L. Dunkel, M. De Lange, J.R. Harris, J.V. Hjelmborg, M. Luciano, N.G. Martin, J. Mortensen, L. Nisticò, N.L. Pedersen, A. Skytthe, T.D. Spector, M.A. Stazi, G. Willemsen, and J. Kaprio Heritability of adult body height: a comparative study of twin cohorts in eight countries Twin Res. 6 2003 399 408 (Pubitemid 38019778)
29. H.H. Maes, M.C. Neale, and L.J. Eaves Genetic and environmental factors in relative body weight and human adiposity Behav. Genet. 27 1997 325 351 (Pubitemid 27415169)
30. E. Dimant, E. Landsberg, and I.M. London The metabolic behavior of reduced glutathione in human and avian erythrocytes J. Biol. Chem. 213 1955 769 776
31. O.W. Griffith Glutathione turnover in human erythrocytes: inhibition by buthionine sulfoximine and incorporation of glycine by exchange J. Biol. Chem 256 1981 4900 4904 (Pubitemid 11035342)
32. J.E. Raftos, S. Whillier, and P.W. Kuchel Glutathione synthesis and turnover in the human erythrocyte: alignment of a model based on detailed enzyme kinetics with experimental data J. Biol. Chem. 285 2010 23557 23567
33. A. Szeinberg, C. Sheba, and A. Adam Selective occurrence of glutathione instability in red blood corpuscles of the various Jewish tribes Blood 13 1958 1043 1053
34. C.A. Lang, A.P. Matheny Jr, W. Mastropaolo, and M.C. Liu Blood glutathione and cysteine concentrations in twin children Exp. Biol. Med. (Maywood) 226 2001 349 352
35. A. Küster, I. Tea, V. Ferchaud-Roucher, S. Le Borgne, C. Plouzennec, N. Winer, J.C. Rozé, R.J. Robins, and D. Darmaun Cord blood glutathione depletion in preterm infants: correlation with maternal cysteine depletion PLoS One 6 2011 e27626 2011
36. K. Broedbaek, R. Ribel-Madsen, T. Henriksen, A. Weimann, M. Petersen, J.T. Andersen, S. Afzal, B. Hjelvang, L.J. Roberts 2nd, A. Vaag, P. Poulsen, and H.E. Poulsen Genetic and environmental influences on oxidative damage assessed in elderly Danish twins Free Radic. Biol. Med. 50 2011 1488 1491
37. S. Chakraborty, and A.B.D. Chaudhuri Heritability of some important parameters of the antioxidant defense system like glucose-6-phosphate dehydrogenase, catalase, glutathione peroxidase and lipid peroxidation in red blood cells by twin study Int. J. Health Geogr 1 2001
38. D.P. Jones Redox sensing: orthogonal control in cell cycle and apoptosis signalling J. Intern. Med. 268 2010 432 448
39. M.C. Gruhlke, D. Portz, M. Stitz, A. Anwar, T. Schneider, C. Jacob, N.L. Schlaich, and A.J. Slusarenko Allicin disrupts the cell′s electrochemical potential and induces apoptosis in yeast Free Radic. Biol. Med. 49 2010 1916 1924
40. I. Kranner, S. Birtić, K.M. Anderson, and H.W. Pritchard Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radic. Biol. Med 40 2006 2155 2165 (Pubitemid 43932923)
41. C.E. Seal, R. Zammit, P. Scott, T.J. Flowers, and I. Kranner Glutathione half-cell reduction potential and alpha-tocopherol as viability markers during the prolonged storage of Suaeda maritima seeds Seed Sci. Res. 20 2010 47 53
42. C.E. Seal, R. Zammit, P. Scott, D.O. Nyamongo, M.I. Daws, and I. Kranner Glutathione half-cell reduction potential as a seed viability marker of the potential oilseed crop Vernonia galamensis Ind. Crops Prod 32 2010 687 691
43. I. Kranner, F.V. Minibayeva, R.P. Beckett, and C.E. Seal What is stress? Concepts; definitions and applications in seed science New Phytol. 188 2010 655 673
44. S. Birtić, L. Colville, H.W. Pritchard, S.R. Pearce, and I. Kranner Mathematically combined half-cell reduction potentials of low-molecular-weight thiols as markers of seed ageing Free Radic. Res. 45 2011 1093 1102
45. G.R. Buettner Superoxide dismutase in redox biology: the roles of superoxide and hydrogen peroxide Anticancer Agents Med. Chem 11 2011 341 346
46. S. Cui, C. Chesson, and R. Hope Genetic variation within and between strains of outbred Swiss mice Lab. Anim. 27 1993 116 123 (Pubitemid 23104419)
47. A. Szeinberg, Y. Asher, and C. Sheba Studies on glutathione stability in erythrocytes of cases with past history of favism or sulfa-drug-induced hemolysis Blood 13 1958 348 358
48. A. Szeinberg, C.H. Sheba, and A. Adam Selective occurrence of glutathione instability in red blood corpuscles of the various Jewish tribes Blood 13 1958 1043 1053
49. J.C. Sabine Glutathione concentration and stability in the red blood cells in various disease states; and some observations on the mechanism of action of acetyl-phenylhydrazine Br. J. Haematol 10 1964 477 484
50. D.G. Walker, and J.E. Bowman Glutathione stability of erythrocytes in Iranians Nature 184 1959 1325
51. L. Kum-Tatt, and I.K. Tan A new colorimetric method for the determination of glutathione in erythrocytes Clin. Chim. Acta 53 1974 153 161
52. V. Serru, B. Baudin, F. Ziegler, J.P. David, M.J. Cals, M. Vaubourdolle, and N. Mario Quantification of reduced and oxidized glutathione in whole blood samples by capillary electrophoresis Clin. Chem. 47 2001 1321 1324 (Pubitemid 32579128)
53. L.S. Matsubara, and P.E. Machado Age-related changes of glutathione content; glutathione reductase and glutathione peroxidase activity of human erythrocytes Braz. J. Med. Biol. Res. 24 1991 449 454
54. F. Michelet, R. Gueguen, P. Leroy, M. Wellman, A. Nicolas, and G. Siest Blood and plasma glutathione measured in healthy subjects by HPLC: relation to sex; aging; biological variables; and life habits Clin. Chem. 41 1995 1509 1517
55. J.P. Richie Jr, L. Skowronski, P. Abraham, and Y. Leutzinger Blood glutathione concentrations in a large-scale human study Clin. Chem. 42 1996 64 70 (Pubitemid 26030383)
56. W. Schroter, E. Schulz, and R. Bonn Die bedeutung de glutathione konzentration der erythrocyten fur die diagnose de osteomyelofibrose Klin. Wochenschr. 48 1970 1013 1014
57. D.T. Harwood, A.J. Kettle, S. Brennan, and C.C. Winterbourn Simultaneous determination of reduced glutathione; glutathione disulphide and glutathione sulphonamide in cells and physiological fluids by isotope dilution liquid chromatography-tandem mass spectrometry. J. Chromatogr B Anal. Technol. Biomed. Life Sci. 877 2009 3393 3399
58. M. Erden-Inal, E. Sunal, and G. Kanbak Age-related changes in the glutathione redox system Cell Biochem. Funct. 20 2002 61 66 (Pubitemid 34178183)
59. E. Buetler, M.J. Robson, and E. Buttenwieser The glutathione instability of drug-sensitive red cells; a new method for the in vitro detection of drug sensitivity J. Lab. Clin. Med. 49 1957 84 95