PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of procbThe Royal Society PublishingProceedings BAboutBrowse by SubjectAlertsFree Trial
 
Proc Biol Sci. 1999 January 7; 266(1414): 1–12.
PMCID: PMC1689644

Good genes, oxidative stress and condition-dependent sexual signals.

Abstract

The immune and the detoxication systems of animals are characterized by allelic polymorphisms, which underlie individual differences in ability to combat assaults from pathogens and toxic compounds. Previous studies have shown that females may improve offspring survival by selecting mates on the basis of sexual ornaments and signals that honestly reveal health. In many cases the expression of these ornaments appears to be particularly sensitive to oxidative stress. Activated immune and detoxication systems often generate oxidative stress by an extensive production of reactive metabolites and free radicals. Given that tolerance or resistance to toxic compounds and pathogens can be inherited, female choice should promote the evolution of male ornaments that reliably reveal the status of the bearers' level of oxidative stress. Hence, oxidative stress may be one important agent linking the expression of sexual ornaments to genetic variation in fitness-related traits, thus promoting the evolution of female mate choice and male sexual ornamentation, a controversial issue in evolutionary biology ever since Darwin.

Full Text

The Full Text of this article is available as a PDF (259K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Alsharif NZ, Lawson T, Stohs SJ. Oxidative stress induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin is mediated by the aryl hydrocarbon (Ah) receptor complex. Toxicology. 1994 Sep 6;92(1-3):39–51. [PubMed]
  • Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 1965 Jun;124(3):319–335. [PubMed]
  • Alvarez-Buylla A. Neurogenesis and plasticity in the CNS of adult birds. Exp Neurol. 1992 Jan;115(1):110–114. [PubMed]
  • Anderson R, Theron AJ. Physiological potential of ascorbate, beta-carotene and alpha-tocopherol individually and in combination in the prevention of tissue damage, carcinogenesis and immune dysfunction mediated by phagocyte-derived reactive oxidants. World Rev Nutr Diet. 1990;62:27–58. [PubMed]
  • Apanius V, Penn D, Slev PR, Ruff LR, Potts WK. The nature of selection on the major histocompatibility complex. Crit Rev Immunol. 1997;17(2):179–224. [PubMed]
  • Auerbach JM, Segal M. Peroxide modulation of slow onset potentiation in rat hippocampus. J Neurosci. 1997 Nov 15;17(22):8695–8701. [PubMed]
  • Augustine PC, Ruff MD. Changes in carotenoid and vitamin A levels in young turkeys infected with Eimeria meleagrimitis or E. adenoeides. Avian Dis. 1983 Oct-Dec;27(4):963–971. [PubMed]
  • Baker MS, Green SP, Lowther DA. Changes in the viscosity of hyaluronic acid after exposure to a myeloperoxidase-derived oxidant. Arthritis Rheum. 1989 Apr;32(4):461–467. [PubMed]
  • Barnea A, Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11217–11221. [PubMed]
  • Behl C, Lezoualc'h F, Trapp T, Widmann M, Skutella T, Holsboer F. Glucocorticoids enhance oxidative stress-induced cell death in hippocampal neurons in vitro. Endocrinology. 1997 Jan;138(1):101–106. [PubMed]
  • Beier RC. Natural pesticides and bioactive components in foods. Rev Environ Contam Toxicol. 1990;113:47–137. [PubMed]
  • Berenbaum MR, Zangerl AR. Chemical phenotype matching between a plant and its insect herbivore. Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13743–13748. [PubMed]
  • Besedovsky HO, del Rey A. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr Rev. 1996 Feb;17(1):64–102. [PubMed]
  • Bingman VP, Jones TJ. Sun compass-based spatial learning impaired in homing pigeons with hippocampal lesions. J Neurosci. 1994 Nov;14(11 Pt 1):6687–6694. [PubMed]
  • Breimer LH. Molecular mechanisms of oxygen radical carcinogenesis and mutagenesis: the role of DNA base damage. Mol Carcinog. 1990;3(4):188–197. [PubMed]
  • Brenowitz EA, Nalls B, Wingfield JC, Kroodsma DE. Seasonal changes in avian song nuclei without seasonal changes in song repertoire. J Neurosci. 1991 May;11(5):1367–1374. [PubMed]
  • Burton GW, Ingold KU. beta-Carotene: an unusual type of lipid antioxidant. Science. 1984 May 11;224(4649):569–573. [PubMed]
  • Carney JM, Starke-Reed PE, Oliver CN, Landum RW, Cheng MS, Wu JF, Floyd RA. Reversal of age-related increase in brain protein oxidation, decrease in enzyme activity, and loss in temporal and spatial memory by chronic administration of the spin-trapping compound N-tert-butyl-alpha-phenylnitrone. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3633–3636. [PubMed]
  • Cerimele D, Celleno L, Serri F. Physiological changes in ageing skin. Br J Dermatol. 1990 Apr;122 (Suppl 35):13–20. [PubMed]
  • Chainy GB, Samantaray S, Samanta L. Testosterone-induced changes in testicular antioxidant system. Andrologia. 1997 Nov-Dec;29(6):343–349. [PubMed]
  • Clark EA, Ledbetter JA. How B and T cells talk to each other. Nature. 1994 Feb 3;367(6462):425–428. [PubMed]
  • Clot F, Jager M, Simon-Bouy B, Serre JL, Aupetit-Faisant B, Mornet E. A polymorphic poly-A sequence in the 5' region of the aldosynthase (CYP11B2) gene may be useful in genetic diagnosis of 11 beta-hydroxylase genes defects. Hum Genet. 1994 Sep;94(3):316–317. [PubMed]
  • Cohen JC, Cali JJ, Jelinek DF, Mehrabian M, Sparkes RS, Lusis AJ, Russell DW, Hobbs HH. Cloning of the human cholesterol 7 alpha-hydroxylase gene (CYP7) and localization to chromosome 8q11-q12. Genomics. 1992 Sep;14(1):153–161. [PubMed]
  • Coyle JT, Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 1993 Oct 29;262(5134):689–695. [PubMed]
  • Daly AK, Cholerton S, Gregory W, Idle JR. Metabolic polymorphisms. Pharmacol Ther. 1993 Feb-Mar;57(2-3):129–160. [PubMed]
  • Deeble DJ, Bothe E, Schuchmann HP, Parsons BJ, Phillips GO, von Sonntag C. The kinetics of hydroxyl-radical-induced strand breakage of hyaluronic acid. A pulse radiolysis study using conductometry and laser-light-scattering. Z Naturforsch C. 1990 Sep-Oct;45(9-10):1031–1043. [PubMed]
  • Devoogd TJ, Krebs JR, Healy SD, Purvis A. Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds. Proc Biol Sci. 1993 Nov 22;254(1340):75–82. [PubMed]
  • Dieckmann U, Law R. The dynamical theory of coevolution: a derivation from stochastic ecological processes. J Math Biol. 1996;34(5-6):579–612. [PubMed]
  • Dooley TP, Huang Z. Genomic organization and DNA sequences of two human phenol sulfotransferase genes (STP1 and STP2) on the short arm of chromosome 16. Biochem Biophys Res Commun. 1996 Nov 1;228(1):134–140. [PubMed]
  • Edman K, Maret W. Alcohol dehydrogenase genes: restriction fragment length polymorphisms for ADH4 (pi-ADH) and ADH5 (chi-ADH) and construction of haplotypes among different ADH classes. Hum Genet. 1992 Dec;90(4):395–401. [PubMed]
  • Getty T. Reliable signalling need not be a handicap. Anim Behav. 1998 Jul;56(1):253–255. [PubMed]
  • Goedde HW, Agarwal DP, Fritze G, Meier-Tackmann D, Singh S, Beckmann G, Bhatia K, Chen LZ, Fang B, Lisker R, et al. Distribution of ADH2 and ALDH2 genotypes in different populations. Hum Genet. 1992 Jan;88(3):344–346. [PubMed]
  • Gonzalez FJ, Nebert DW. Evolution of the P450 gene superfamily: animal-plant 'warfare', molecular drive and human genetic differences in drug oxidation. Trends Genet. 1990 Jun;6(6):182–186. [PubMed]
  • Grant DF, Hammock BD. Genetic and molecular evidence for a trans-acting regulatory locus controlling glutathione S-transferase-2 expression in Aedes aegypti. Mol Gen Genet. 1992 Aug;234(2):169–176. [PubMed]
  • Grootveld M, Henderson EB, Farrell A, Blake DR, Parkes HG, Haycock P. Oxidative damage to hyaluronate and glucose in synovial fluid during exercise of the inflamed rheumatoid joint. Detection of abnormal low-molecular-mass metabolites by proton-n.m.r. spectroscopy. Biochem J. 1991 Jan 15;273(Pt 2):459–467. [PubMed]
  • Grubić Z, Zunec R, Naipal A, Kastelan A, Giphart MJ. Molecular analysis of HLA class II polymorphism in Croatians. Tissue Antigens. 1995 Oct;46(4):293–298. [PubMed]
  • Gruner S, Volk HD, Falck P, Von Baehr R. The influence of phagocytic stimuli on the expression of HLA-DR antigens; role of reactive oxygen intermediates. Eur J Immunol. 1986 Feb;16(2):212–215. [PubMed]
  • Haake AR, Sawyer RH. Differences in the histogenesis and keratin expression of avian extraembryonic ectoderm and endoderm recombined with dermis. Dev Biol. 1986 Feb;113(2):295–304. [PubMed]
  • Hamilton WD, Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982 Oct 22;218(4570):384–387. [PubMed]
  • Hamilton WD, Axelrod R, Tanese R. Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci U S A. 1990 May;87(9):3566–3573. [PubMed]
  • Hassoun EA, Stohs SJ. TCDD, endrin and lindane induced oxidative stress in fetal and placental tissues of C57BL/6J and DBA/2J mice. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 1996 Sep;115(1):11–18. [PubMed]
  • Hata R, Sunada H, Arai K, Sato T, Ninomiya Y, Nagai Y, Senoo H. Regulation of collagen metabolism and cell growth by epidermal growth factor and ascorbate in cultured human skin fibroblasts. Eur J Biochem. 1988 Apr 15;173(2):261–267. [PubMed]
  • Hawkins CL, Davies MJ. Direct detection and identification of radicals generated during the hydroxyl radical-induced degradation of hyaluronic acid and related materials. Free Radic Biol Med. 1996;21(3):275–290. [PubMed]
  • Hayes JD, Pulford DJ. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol. 1995;30(6):445–600. [PubMed]
  • Healy SD, Krebs JR. Development of hippocampal specialisation in a food-storing bird. Behav Brain Res. 1993 Feb 26;53(1-2):127–131. [PubMed]
  • Healy SD, Gwinner E, Krebs JR. Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav Brain Res. 1996 Nov;81(1-2):61–68. [PubMed]
  • Hennet T, Peterhans E, Stocker R. Alterations in antioxidant defences in lung and liver of mice infected with influenza A virus. J Gen Virol. 1992 Jan;73(Pt 1):39–46. [PubMed]
  • Hsu LC, Chang WC, Yoshida A. Human aldehyde dehydrogenase genes, ALDH7 and ALDH8: genomic organization and gene structure comparison. Gene. 1997 Apr 11;189(1):89–94. [PubMed]
  • Hughes AL, Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. [PubMed]
  • Hughes DA, Wright AJ, Finglas PM, Peerless AC, Bailey AL, Astley SB, Pinder AC, Southon S. The effect of beta-carotene supplementation on the immune function of blood monocytes from healthy male nonsmokers. J Lab Clin Med. 1997 Mar;129(3):309–317. [PubMed]
  • Jaiswal AK, Burnett P, Adesnik M, McBride OW. Nucleotide and deduced amino acid sequence of a human cDNA (NQO2) corresponding to a second member of the NAD(P)H:quinone oxidoreductase gene family. Extensive polymorphism at the NQO2 gene locus on chromosome 6. Biochemistry. 1990 Feb 20;29(7):1899–1906. [PubMed]
  • Jialal I, Grundy SM. Preservation of the endogenous antioxidants in low density lipoprotein by ascorbate but not probucol during oxidative modification. J Clin Invest. 1991 Feb;87(2):597–601. [PMC free article] [PubMed]
  • Kalow W. Pharmacogenetics in biological perspective. Pharmacol Rev. 1997 Dec;49(4):369–379. [PubMed]
  • Kirzhner VM, Korol AB, Nevo E. Complex dynamics of multilocus systems subjected to cyclical selection. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6532–6535. [PubMed]
  • Knight DC, Eden JA. Phytoestrogens--a short review. Maturitas. 1995 Nov;22(3):167–175. [PubMed]
  • Kvam C, Granese D, Flaibani A, Pollesello P, Paoletti S. Hyaluronan can be protected from free-radical depolymerisation by 2,6-diisopropylphenol, a novel radical scavenger. Biochem Biophys Res Commun. 1993 Jun 30;193(3):927–933. [PubMed]
  • Lachman HM, Morrow B, Shprintzen R, Veit S, Parsia SS, Faedda G, Goldberg R, Kucherlapati R, Papolos DF. Association of codon 108/158 catechol-O-methyltransferase gene polymorphism with the psychiatric manifestations of velo-cardio-facial syndrome. Am J Med Genet. 1996 Sep 20;67(5):468–472. [PubMed]
  • Laurent TC, Fraser JR. Hyaluronan. FASEB J. 1992 Apr;6(7):2397–2404. [PubMed]
  • Liebler DC. Antioxidant reactions of carotenoids. Ann N Y Acad Sci. 1993 Dec 31;691:20–31. [PubMed]
  • McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. [PubMed]
  • McEwen BS, Sapolsky RM. Stress and cognitive function. Curr Opin Neurobiol. 1995 Apr;5(2):205–216. [PubMed]
  • McIntosh LJ, Cortopassi KM, Sapolsky RM. Glucocorticoids may alter antioxidant enzyme capacity in the brain: kainic acid studies. Brain Res. 1998 Apr 27;791(1-2):215–222. [PubMed]
  • Maguire JJ, Wilson DS, Packer L. Mitochondrial electron transport-linked tocopheroxyl radical reduction. J Biol Chem. 1989 Dec 25;264(36):21462–21465. [PubMed]
  • Marez D, Legrand M, Sabbagh N, Lo Guidice JM, Spire C, Lafitte JJ, Meyer UA, Broly F. Polymorphism of the cytochrome P450 CYP2D6 gene in a European population: characterization of 48 mutations and 53 alleles, their frequencies and evolution. Pharmacogenetics. 1997 Jun;7(3):193–202. [PubMed]
  • Marler P, Peters S, Ball GF, Dufty AM, Jr, Wingfield JC. The role of sex steroids in the acquisition and production of birdsong. Nature. 1988 Dec 22;336(6201):770–772. [PubMed]
  • Nakagawa Y, Takeuchi H, Kubota A, Nakahori Y, Nakagome Y, Igarashi Y, Yamada M. Restriction fragment length polymorphisms of the CYP11B1 gene in the Japanese population. Jpn J Hum Genet. 1993 Jun;38(2):203–207. [PubMed]
  • Nebert DW, Goujon FM, Gielen JE. Aryl hydrocarbon hydroxylase induction by polycyclic hydrocarbons: simple autosomal dominant trait in the mouse. Nat New Biol. 1972 Mar 29;236(65):107–110. [PubMed]
  • Nebert DW, McKinnon RA, Puga A. Human drug-metabolizing enzyme polymorphisms: effects on risk of toxicity and cancer. DNA Cell Biol. 1996 Apr;15(4):273–280. [PubMed]
  • Nelson HH, Wiencke JK, Christiani DC, Cheng TJ, Zuo ZF, Schwartz BS, Lee BK, Spitz MR, Wang M, Xu X, et al. Ethnic differences in the prevalence of the homozygous deleted genotype of glutathione S-transferase theta. Carcinogenesis. 1995 May;16(5):1243–1245. [PubMed]
  • Nevo E, Kirzhner V, Beiles A, Korol A. Selection versus random drift: long-term polymorphism persistence in small populations (evidence and modelling) Philos Trans R Soc Lond B Biol Sci. 1997 Mar 29;352(1351):381–389. [PMC free article]
  • Nottebohm F. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science. 1981 Dec 18;214(4527):1368–1370. [PubMed]
  • Olanow CW. A radical hypothesis for neurodegeneration. Trends Neurosci. 1993 Nov;16(11):439–444. [PubMed]
  • Orr WC, Sohal RS. The effects of catalase gene overexpression on life span and resistance to oxidative stress in transgenic Drosophila melanogaster. Arch Biochem Biophys. 1992 Aug 15;297(1):35–41. [PubMed]
  • O'Toole EA, Goel M, Woodley DT. Hydrogen peroxide inhibits human keratinocyte migration. Dermatol Surg. 1996 Jun;22(6):525–529. [PubMed]
  • Parham P, Ohta T. Population biology of antigen presentation by MHC class I molecules. Science. 1996 Apr 5;272(5258):67–74. [PubMed]
  • Pemble S, Schroeder KR, Spencer SR, Meyer DJ, Hallier E, Bolt HM, Ketterer B, Taylor JB. Human glutathione S-transferase theta (GSTT1): cDNA cloning and the characterization of a genetic polymorphism. Biochem J. 1994 May 15;300(Pt 1):271–276. [PubMed]
  • Poland A, Palen D, Glover E. Analysis of the four alleles of the murine aryl hydrocarbon receptor. Mol Pharmacol. 1994 Nov;46(5):915–921. [PubMed]
  • Prough RA, Linder MW, Pinaire JA, Xiao GH, Falkner KC. Hormonal regulation of hepatic enzymes involved in foreign compound metabolism. FASEB J. 1996 Oct;10(12):1369–1377. [PubMed]
  • Råberg L, Grahn M, Hasselquist D, Svensson E. On the adaptive significance of stress-induced immunosuppression. Proc Biol Sci. 1998 Sep 7;265(1406):1637–1641. [PMC free article] [PubMed]
  • Rajewsky K. Clonal selection and learning in the antibody system. Nature. 1996 Jun 27;381(6585):751–758. [PubMed]
  • Rosvold EA, McGlynn KA, Lustbader ED, Buetow KH. Identification of an NAD(P)H:quinone oxidoreductase polymorphism and its association with lung cancer and smoking. Pharmacogenetics. 1995 Aug;5(4):199–206. [PubMed]
  • Roy NK, Wirgin I. Characterization of the aromatic hydrocarbon receptor gene and its expression in Atlantic tomcod. Arch Biochem Biophys. 1997 Aug 15;344(2):373–386. [PubMed]
  • Roy S, Scherer MT, Briner TJ, Smith JA, Gefter ML. Murine MHC polymorphism and T cell specificities. Science. 1989 May 5;244(4904):572–575. [PubMed]
  • Ruff MD, Reid WM, Johnson JK. Lowered blood carotenoid levels in chickens infected with coccidia. Poult Sci. 1974 Sep;53(5):1801–1809. [PubMed]
  • Saari H, Konttinen YT, Friman C, Sorsa T. Differential effects of reactive oxygen species on native synovial fluid and purified human umbilical cord hyaluronate. Inflammation. 1993 Aug;17(4):403–415. [PubMed]
  • Saika S, Kanagawa R, Uenoyama K, Hiroi K, Hiraoka J. L-ascorbic acid 2-phosphate, a phosphate derivative of L-ascorbic acid, enhances the growth of cultured rabbit keratocytes. Graefes Arch Clin Exp Ophthalmol. 1991;229(1):79–83. [PubMed]
  • Saito K, Packianathan S, Longo LD. Free radical-induced elevation of ornithine decarboxylase activity in developing rat brain slices. Brain Res. 1997 Jul 25;763(2):232–238. [PubMed]
  • Sato K, Niki E, Shimasaki H. Free radical-mediated chain oxidation of low density lipoprotein and its synergistic inhibition by vitamin E and vitamin C. Arch Biochem Biophys. 1990 Jun;279(2):402–405. [PubMed]
  • von Schantz T, Göransson G, Andersson G, Fröberg I, Grahn M, Helgée A, Wittzell H. Female choice selects for a viability-based male trait in pheasants. Nature. 1989 Jan 12;337(6203):166–169. [PubMed]
  • von Schantz T, Wittzell H, Göransson G, Grahn M, Persson K. MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc Biol Sci. 1996 Mar 22;263(1368):265–271. [PubMed]
  • Sherry DF, Jacobs LF, Gaulin SJ. Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci. 1992 Aug;15(8):298–303. [PubMed]
  • Smulders TV, Sasson AD, DeVoogd TJ. Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J Neurobiol. 1995 May;27(1):15–25. [PubMed]
  • Stam LF, Laurie CC. Molecular dissection of a major gene effect on a quantitative trait: the level of alcohol dehydrogenase expression in Drosophila melanogaster. Genetics. 1996 Dec;144(4):1559–1564. [PubMed]
  • Sugaya K, Chouinard M, Greene R, Robbins M, Personett D, Kent C, Gallagher M, McKinney M. Molecular indices of neuronal and glial plasticity in the hippocampal formation in a rodent model of age-induced spatial learning impairment. J Neurosci. 1996 May 15;16(10):3427–3443. [PubMed]
  • Tai HL, Krynetski EY, Yates CR, Loennechen T, Fessing MY, Krynetskaia NF, Evans WE. Thiopurine S-methyltransferase deficiency: two nucleotide transitions define the most prevalent mutant allele associated with loss of catalytic activity in Caucasians. Am J Hum Genet. 1996 Apr;58(4):694–702. [PubMed]
  • Trowsdale J. "Both man & bird & beast": comparative organization of MHC genes. Immunogenetics. 1995;41(1):1–17. [PubMed]
  • Uchida K, Kanematsu M, Sakai K, Matsuda T, Hattori N, Mizuno Y, Suzuki D, Miyata T, Noguchi N, Niki E, et al. Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4882–4887. [PubMed]
  • Uni Z, Sklan D, Haklay N, Yonash N, Heller D. Response of three class-IV major histocompatibility complex haplotypes to Eimeria acervulina in meat-type chickens. Br Poult Sci. 1995 Sep;36(4):555–561. [PubMed]
  • Vatsis KP, Weber WW, Bell DA, Dupret JM, Evans DA, Grant DM, Hein DW, Lin HJ, Meyer UA, Relling MV, et al. Nomenclature for N-acetyltransferases. Pharmacogenetics. 1995 Feb;5(1):1–17. [PubMed]
  • Vornov JJ, Park J, Thomas AG. Regional vulnerability to endogenous and exogenous oxidative stress in organotypic hippocampal culture. Exp Neurol. 1998 Jan;149(1):109–122. [PubMed]
  • Watt WB, Carter PA, Donohue K. Females' choice of "good genotypes" as mates is promoted by an insect mating system. Science. 1986 Sep 12;233(4769):1187–1190. [PubMed]
  • Weitberg AB, Weitzman SA, Clark EP, Stossel TP. Effects of antioxidants on oxidant-induced sister chromatid exchange formation. J Clin Invest. 1985 Jun;75(6):1835–1841. [PMC free article] [PubMed]
  • Yao KS, Godwin AK, Johnson C, O'Dwyer PJ. Alternative splicing and differential expression of DT-diaphorase transcripts in human colon tumors and in peripheral mononuclear cells in response to mitomycin C treatment. Cancer Res. 1996 Apr 15;56(8):1731–1736. [PubMed]
  • Yengi L, Inskip A, Gilford J, Alldersea J, Bailey L, Smith A, Lear JT, Heagerty AH, Bowers B, Hand P, et al. Polymorphism at the glutathione S-transferase locus GSTM3: interactions with cytochrome P450 and glutathione S-transferase genotypes as risk factors for multiple cutaneous basal cell carcinoma. Cancer Res. 1996 May 1;56(9):1974–1977. [PubMed]
  • Youngman LD, Park JY, Ames BN. Protein oxidation associated with aging is reduced by dietary restriction of protein or calories. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9112–9116. [PubMed]
  • Yoshida A, Rzhetsky A, Hsu LC, Chang C. Human aldehyde dehydrogenase gene family. Eur J Biochem. 1998 Feb 1;251(3):549–557. [PubMed]
  • Zachary AA, Steinberg AG, Bias WB, Leffell MS. The frequencies of HLA alleles and haplotypes and their distribution among donors and renal patients in the UNOS registry. Transplantation. 1996 Jul 27;62(2):272–283. [PubMed]
  • Zahavi A. Mate selection-a selection for a handicap. J Theor Biol. 1975 Sep;53(1):205–214. [PubMed]
  • Zgombić-Knight M, Foglio MH, Duester G. Genomic structure and expression of the ADH7 gene encoding human class IV alcohol dehydrogenase, the form most efficient for retinol metabolism in vitro. J Biol Chem. 1995 Mar 3;270(9):4305–4311. [PubMed]
  • Zhu XD, Bonet B, Knopp RH. 17beta-Estradiol, progesterone, and testosterone inversely modulate low-density lipoprotein oxidation and cytotoxicity in cultured placental trophoblast and macrophages. Am J Obstet Gynecol. 1997 Jul;177(1):196–209. [PubMed]
  • Zinkernagel RM. Immunology taught by viruses. Science. 1996 Jan 12;271(5246):173–178. [PubMed]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society