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 (259.2 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alsharif N. Z., Lawson T., Stohs S. J. 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. doi: 10.1016/0300-483x(94)90166-x. [DOI] [PubMed] [Google Scholar]
- Altman J., Das G. D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 1965 Jun;124(3):319–335. doi: 10.1002/cne.901240303. [DOI] [PubMed] [Google Scholar]
- Alvarez-Buylla A. Neurogenesis and plasticity in the CNS of adult birds. Exp Neurol. 1992 Jan;115(1):110–114. doi: 10.1016/0014-4886(92)90232-f. [DOI] [PubMed] [Google Scholar]
- Anderson R., Theron A. J. 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. doi: 10.1159/000417534. [DOI] [PubMed] [Google Scholar]
- Apanius V., Penn D., Slev P. R., Ruff L. R., Potts W. K. The nature of selection on the major histocompatibility complex. Crit Rev Immunol. 1997;17(2):179–224. doi: 10.1615/critrevimmunol.v17.i2.40. [DOI] [PubMed] [Google Scholar]
- Auerbach J. M., Segal M. Peroxide modulation of slow onset potentiation in rat hippocampus. J Neurosci. 1997 Nov 15;17(22):8695–8701. doi: 10.1523/JNEUROSCI.17-22-08695.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Augustine P. C., Ruff M. D. 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] [Google Scholar]
- Baker M. S., Green S. P., Lowther D. A. Changes in the viscosity of hyaluronic acid after exposure to a myeloperoxidase-derived oxidant. Arthritis Rheum. 1989 Apr;32(4):461–467. doi: 10.1002/anr.1780320416. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1073/pnas.91.23.11217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. doi: 10.1210/endo.138.1.4835. [DOI] [PubMed] [Google Scholar]
- Beier R. C. Natural pesticides and bioactive components in foods. Rev Environ Contam Toxicol. 1990;113:47–137. doi: 10.1007/978-1-4612-3366-4_2. [DOI] [PubMed] [Google Scholar]
- Berenbaum M. R., Zangerl A. R. Chemical phenotype matching between a plant and its insect herbivore. Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13743–13748. doi: 10.1073/pnas.95.23.13743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Besedovsky H. O., del Rey A. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr Rev. 1996 Feb;17(1):64–102. doi: 10.1210/edrv-17-1-64. [DOI] [PubMed] [Google Scholar]
- Bingman V. P., Jones T. J. Sun compass-based spatial learning impaired in homing pigeons with hippocampal lesions. J Neurosci. 1994 Nov;14(11 Pt 1):6687–6694. doi: 10.1523/JNEUROSCI.14-11-06687.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Breimer L. H. Molecular mechanisms of oxygen radical carcinogenesis and mutagenesis: the role of DNA base damage. Mol Carcinog. 1990;3(4):188–197. doi: 10.1002/mc.2940030405. [DOI] [PubMed] [Google Scholar]
- Brenowitz E. A., Nalls B., Wingfield J. C., Kroodsma D. E. Seasonal changes in avian song nuclei without seasonal changes in song repertoire. J Neurosci. 1991 May;11(5):1367–1374. doi: 10.1523/JNEUROSCI.11-05-01367.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burton G. W., Ingold K. U. beta-Carotene: an unusual type of lipid antioxidant. Science. 1984 May 11;224(4649):569–573. doi: 10.1126/science.6710156. [DOI] [PubMed] [Google Scholar]
- Carney J. M., Starke-Reed P. E., Oliver C. N., Landum R. W., Cheng M. S., Wu J. F., Floyd R. A. 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. doi: 10.1073/pnas.88.9.3633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cerimele D., Celleno L., Serri F. Physiological changes in ageing skin. Br J Dermatol. 1990 Apr;122 (Suppl 35):13–20. doi: 10.1111/j.1365-2133.1990.tb16120.x. [DOI] [PubMed] [Google Scholar]
- Chainy G. B., Samantaray S., Samanta L. Testosterone-induced changes in testicular antioxidant system. Andrologia. 1997 Nov-Dec;29(6):343–349. doi: 10.1111/j.1439-0272.1997.tb00328.x. [DOI] [PubMed] [Google Scholar]
- Clark E. A., Ledbetter J. A. How B and T cells talk to each other. Nature. 1994 Feb 3;367(6462):425–428. doi: 10.1038/367425a0. [DOI] [PubMed] [Google Scholar]
- Clot F., Jager M., Simon-Bouy B., Serre J. L., 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. doi: 10.1007/BF00208293. [DOI] [PubMed] [Google Scholar]
- Cohen J. C., Cali J. J., Jelinek D. F., Mehrabian M., Sparkes R. S., Lusis A. J., Russell D. W., Hobbs H. H. Cloning of the human cholesterol 7 alpha-hydroxylase gene (CYP7) and localization to chromosome 8q11-q12. Genomics. 1992 Sep;14(1):153–161. doi: 10.1016/s0888-7543(05)80298-8. [DOI] [PubMed] [Google Scholar]
- Coyle J. T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 1993 Oct 29;262(5134):689–695. doi: 10.1126/science.7901908. [DOI] [PubMed] [Google Scholar]
- Daly A. K., Cholerton S., Gregory W., Idle J. R. Metabolic polymorphisms. Pharmacol Ther. 1993 Feb-Mar;57(2-3):129–160. doi: 10.1016/0163-7258(93)90053-g. [DOI] [PubMed] [Google Scholar]
- Deeble D. J., Bothe E., Schuchmann H. P., Parsons B. J., Phillips G. O., 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. doi: 10.1515/znc-1990-9-1016. [DOI] [PubMed] [Google Scholar]
- Devoogd T. J., Krebs J. R., Healy S. D., 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. doi: 10.1098/rspb.1993.0129. [DOI] [PubMed] [Google Scholar]
- Dieckmann U., Law R. The dynamical theory of coevolution: a derivation from stochastic ecological processes. J Math Biol. 1996;34(5-6):579–612. doi: 10.1007/BF02409751. [DOI] [PubMed] [Google Scholar]
- Dooley T. P., 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. doi: 10.1006/bbrc.1996.1628. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1007/BF00220466. [DOI] [PubMed] [Google Scholar]
- Getty T. Reliable signalling need not be a handicap. Anim Behav. 1998 Jul;56(1):253–255. doi: 10.1006/anbe.1998.0748. [DOI] [PubMed] [Google Scholar]
- Goedde H. W., Agarwal D. P., Fritze G., Meier-Tackmann D., Singh S., Beckmann G., Bhatia K., Chen L. Z., Fang B., Lisker R. Distribution of ADH2 and ALDH2 genotypes in different populations. Hum Genet. 1992 Jan;88(3):344–346. doi: 10.1007/BF00197271. [DOI] [PubMed] [Google Scholar]
- Gonzalez F. J., Nebert D. W. 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. doi: 10.1016/0168-9525(90)90174-5. [DOI] [PubMed] [Google Scholar]
- Grant D. F., Hammock B. D. 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. doi: 10.1007/BF00283836. [DOI] [PubMed] [Google Scholar]
- Grootveld M., Henderson E. B., Farrell A., Blake D. R., Parkes H. G., 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. doi: 10.1042/bj2730459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grubić Z., Zunec R., Naipal A., Kastelan A., Giphart M. J. Molecular analysis of HLA class II polymorphism in Croatians. Tissue Antigens. 1995 Oct;46(4):293–298. doi: 10.1111/j.1399-0039.1995.tb02495.x. [DOI] [PubMed] [Google Scholar]
- Gruner S., Volk H. D., 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. doi: 10.1002/eji.1830160219. [DOI] [PubMed] [Google Scholar]
- Haake A. R., Sawyer R. H. Differences in the histogenesis and keratin expression of avian extraembryonic ectoderm and endoderm recombined with dermis. Dev Biol. 1986 Feb;113(2):295–304. doi: 10.1016/0012-1606(86)90165-x. [DOI] [PubMed] [Google Scholar]
- Hamilton W. D., 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. doi: 10.1073/pnas.87.9.3566. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamilton W. D., Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982 Oct 22;218(4570):384–387. doi: 10.1126/science.7123238. [DOI] [PubMed] [Google Scholar]
- Hassoun E. A., Stohs S. J. 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. doi: 10.1016/s0742-8413(96)00116-8. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1111/j.1432-1033.1988.tb13993.x. [DOI] [PubMed] [Google Scholar]
- Hawkins C. L., Davies M. J. 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. doi: 10.1016/0891-5849(96)00042-1. [DOI] [PubMed] [Google Scholar]
- Hayes J. D., Pulford D. J. 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. doi: 10.3109/10409239509083491. [DOI] [PubMed] [Google Scholar]
- Healy S. D., Gwinner E., Krebs J. R. Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav Brain Res. 1996 Nov;81(1-2):61–68. doi: 10.1016/s0166-4328(96)00044-7. [DOI] [PubMed] [Google Scholar]
- Healy S. D., Krebs J. R. Development of hippocampal specialisation in a food-storing bird. Behav Brain Res. 1993 Feb 26;53(1-2):127–131. doi: 10.1016/s0166-4328(05)80272-4. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1099/0022-1317-73-1-39. [DOI] [PubMed] [Google Scholar]
- Hsu L. C., Chang W. C., Yoshida A. Human aldehyde dehydrogenase genes, ALDH7 and ALDH8: genomic organization and gene structure comparison. Gene. 1997 Apr 11;189(1):89–94. doi: 10.1016/s0378-1119(96)00839-6. [DOI] [PubMed] [Google Scholar]
- Hughes A. L., Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. doi: 10.1038/335167a0. [DOI] [PubMed] [Google Scholar]
- Hughes D. A., Wright A. J., Finglas P. M., Peerless A. C., Bailey A. L., Astley S. B., Pinder A. C., 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. doi: 10.1016/s0022-2143(97)90179-7. [DOI] [PubMed] [Google Scholar]
- Jaiswal A. K., Burnett P., Adesnik M., McBride O. W. 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. doi: 10.1021/bi00459a034. [DOI] [PubMed] [Google Scholar]
- Jialal I., Grundy S. M. 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. doi: 10.1172/JCI115035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalow W. Pharmacogenetics in biological perspective. Pharmacol Rev. 1997 Dec;49(4):369–379. [PubMed] [Google Scholar]
- Kirzhner V. M., Korol A. B., 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. doi: 10.1073/pnas.93.13.6532. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knight D. C., Eden J. A. Phytoestrogens--a short review. Maturitas. 1995 Nov;22(3):167–175. doi: 10.1016/0378-5122(95)00937-g. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1006/bbrc.1993.1714. [DOI] [PubMed] [Google Scholar]
- Lachman H. M., Morrow B., Shprintzen R., Veit S., Parsia S. S., Faedda G., Goldberg R., Kucherlapati R., Papolos D. F. 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. doi: 10.1002/(SICI)1096-8628(19960920)67:5<468::AID-AJMG5>3.0.CO;2-G. [DOI] [PubMed] [Google Scholar]
- Laurent T. C., Fraser J. R. Hyaluronan. FASEB J. 1992 Apr;6(7):2397–2404. [PubMed] [Google Scholar]
- Liebler D. C. Antioxidant reactions of carotenoids. Ann N Y Acad Sci. 1993 Dec 31;691:20–31. doi: 10.1111/j.1749-6632.1993.tb26154.x. [DOI] [PubMed] [Google Scholar]
- Maguire J. J., Wilson D. S., Packer L. Mitochondrial electron transport-linked tocopheroxyl radical reduction. J Biol Chem. 1989 Dec 25;264(36):21462–21465. [PubMed] [Google Scholar]
- Marez D., Legrand M., Sabbagh N., Lo Guidice J. M., Spire C., Lafitte J. J., Meyer U. A., 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. doi: 10.1097/00008571-199706000-00004. [DOI] [PubMed] [Google Scholar]
- Marler P., Peters S., Ball G. F., Dufty A. M., Jr, Wingfield J. C. The role of sex steroids in the acquisition and production of birdsong. Nature. 1988 Dec 22;336(6201):770–772. doi: 10.1038/336770a0. [DOI] [PubMed] [Google Scholar]
- McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
- McEwen B. S., Sapolsky R. M. Stress and cognitive function. Curr Opin Neurobiol. 1995 Apr;5(2):205–216. doi: 10.1016/0959-4388(95)80028-x. [DOI] [PubMed] [Google Scholar]
- McIntosh L. J., Cortopassi K. M., Sapolsky R. M. Glucocorticoids may alter antioxidant enzyme capacity in the brain: kainic acid studies. Brain Res. 1998 Apr 27;791(1-2):215–222. doi: 10.1016/s0006-8993(98)00104-8. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1007/BF01883711. [DOI] [PubMed] [Google Scholar]
- Nebert D. W., Goujon F. M., Gielen J. E. Aryl hydrocarbon hydroxylase induction by polycyclic hydrocarbons: simple autosomal dominant trait in the mouse. Nat New Biol. 1972 Mar 29;236(65):107–110. doi: 10.1038/newbio236107a0. [DOI] [PubMed] [Google Scholar]
- Nebert D. W., McKinnon R. A., Puga A. Human drug-metabolizing enzyme polymorphisms: effects on risk of toxicity and cancer. DNA Cell Biol. 1996 Apr;15(4):273–280. doi: 10.1089/dna.1996.15.273. [DOI] [PubMed] [Google Scholar]
- Nelson H. H., Wiencke J. K., Christiani D. C., Cheng T. J., Zuo Z. F., Schwartz B. S., Lee B. K., Spitz M. R., Wang M., Xu X. Ethnic differences in the prevalence of the homozygous deleted genotype of glutathione S-transferase theta. Carcinogenesis. 1995 May;16(5):1243–1245. doi: 10.1093/carcin/16.5.1243. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1126/science.7313697. [DOI] [PubMed] [Google Scholar]
- O'Toole E. A., Goel M., Woodley D. T. Hydrogen peroxide inhibits human keratinocyte migration. Dermatol Surg. 1996 Jun;22(6):525–529. doi: 10.1111/j.1524-4725.1996.tb00368.x. [DOI] [PubMed] [Google Scholar]
- Olanow C. W. A radical hypothesis for neurodegeneration. Trends Neurosci. 1993 Nov;16(11):439–444. doi: 10.1016/0166-2236(93)90070-3. [DOI] [PubMed] [Google Scholar]
- Orr W. C., Sohal R. S. 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. doi: 10.1016/0003-9861(92)90637-c. [DOI] [PubMed] [Google Scholar]
- doi: 10.1098/rstb.1997.0028. [DOI] [PMC free article] [Google Scholar]
- Parham P., Ohta T. Population biology of antigen presentation by MHC class I molecules. Science. 1996 Apr 5;272(5258):67–74. doi: 10.1126/science.272.5258.67. [DOI] [PubMed] [Google Scholar]
- Pemble S., Schroeder K. R., Spencer S. R., Meyer D. J., Hallier E., Bolt H. M., Ketterer B., Taylor J. B. 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. doi: 10.1042/bj3000271. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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] [Google Scholar]
- Prough R. A., Linder M. W., Pinaire J. A., Xiao G. H., Falkner K. C. Hormonal regulation of hepatic enzymes involved in foreign compound metabolism. FASEB J. 1996 Oct;10(12):1369–1377. doi: 10.1096/fasebj.10.12.8903507. [DOI] [PubMed] [Google Scholar]
- Rajewsky K. Clonal selection and learning in the antibody system. Nature. 1996 Jun 27;381(6585):751–758. doi: 10.1038/381751a0. [DOI] [PubMed] [Google Scholar]
- Rosvold E. A., McGlynn K. A., Lustbader E. D., Buetow K. H. Identification of an NAD(P)H:quinone oxidoreductase polymorphism and its association with lung cancer and smoking. Pharmacogenetics. 1995 Aug;5(4):199–206. doi: 10.1097/00008571-199508000-00003. [DOI] [PubMed] [Google Scholar]
- Roy N. K., 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. doi: 10.1006/abbi.1997.0238. [DOI] [PubMed] [Google Scholar]
- Roy S., Scherer M. T., Briner T. J., Smith J. A., Gefter M. L. Murine MHC polymorphism and T cell specificities. Science. 1989 May 5;244(4904):572–575. doi: 10.1126/science.2470147. [DOI] [PubMed] [Google Scholar]
- Ruff M. D., Reid W. M., Johnson J. K. Lowered blood carotenoid levels in chickens infected with coccidia. Poult Sci. 1974 Sep;53(5):1801–1809. doi: 10.3382/ps.0531801. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1098/rspb.1998.0482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saari H., Konttinen Y. T., 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. doi: 10.1007/BF00916581. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1007/BF00172267. [DOI] [PubMed] [Google Scholar]
- Saito K., Packianathan S., Longo L. D. Free radical-induced elevation of ornithine decarboxylase activity in developing rat brain slices. Brain Res. 1997 Jul 25;763(2):232–238. doi: 10.1016/s0006-8993(97)00414-9. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1016/0003-9861(90)90508-v. [DOI] [PubMed] [Google Scholar]
- Sherry D. F., Jacobs L. F., Gaulin S. J. Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci. 1992 Aug;15(8):298–303. doi: 10.1016/0166-2236(92)90080-r. [DOI] [PubMed] [Google Scholar]
- Smulders T. V., Sasson A. D., DeVoogd T. J. Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J Neurobiol. 1995 May;27(1):15–25. doi: 10.1002/neu.480270103. [DOI] [PubMed] [Google Scholar]
- Stam L. F., Laurie C. C. 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. doi: 10.1093/genetics/144.4.1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. doi: 10.1523/JNEUROSCI.16-10-03427.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tai H. L., Krynetski E. Y., Yates C. R., Loennechen T., Fessing M. Y., Krynetskaia N. F., Evans W. E. 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. [PMC free article] [PubMed] [Google Scholar]
- Trowsdale J. "Both man & bird & beast": comparative organization of MHC genes. Immunogenetics. 1995;41(1):1–17. doi: 10.1007/BF00188427. [DOI] [PubMed] [Google Scholar]
- Uchida K., Kanematsu M., Sakai K., Matsuda T., Hattori N., Mizuno Y., Suzuki D., Miyata T., Noguchi N., Niki E. Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4882–4887. doi: 10.1073/pnas.95.9.4882. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. doi: 10.1080/00071669508417801. [DOI] [PubMed] [Google Scholar]
- Vatsis K. P., Weber W. W., Bell D. A., Dupret J. M., Evans D. A., Grant D. M., Hein D. W., Lin H. J., Meyer U. A., Relling M. V. Nomenclature for N-acetyltransferases. Pharmacogenetics. 1995 Feb;5(1):1–17. doi: 10.1097/00008571-199502000-00001. [DOI] [PubMed] [Google Scholar]
- Vornov J. J., Park J., Thomas A. G. Regional vulnerability to endogenous and exogenous oxidative stress in organotypic hippocampal culture. Exp Neurol. 1998 Jan;149(1):109–122. doi: 10.1006/exnr.1997.6673. [DOI] [PubMed] [Google Scholar]
- Watt W. B., Carter P. A., Donohue K. Females' choice of "good genotypes" as mates is promoted by an insect mating system. Science. 1986 Sep 12;233(4769):1187–1190. doi: 10.1126/science.3738528. [DOI] [PubMed] [Google Scholar]
- Weitberg A. B., Weitzman S. A., Clark E. P., Stossel T. P. Effects of antioxidants on oxidant-induced sister chromatid exchange formation. J Clin Invest. 1985 Jun;75(6):1835–1841. doi: 10.1172/JCI111897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yao K. S., Godwin A. K., Johnson C., O'Dwyer P. J. 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] [Google Scholar]
- Yengi L., Inskip A., Gilford J., Alldersea J., Bailey L., Smith A., Lear J. T., Heagerty A. H., Bowers B., Hand P. 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] [Google Scholar]
- Yoshida A., Rzhetsky A., Hsu L. C., Chang C. Human aldehyde dehydrogenase gene family. Eur J Biochem. 1998 Feb 1;251(3):549–557. doi: 10.1046/j.1432-1327.1998.2510549.x. [DOI] [PubMed] [Google Scholar]
- Youngman L. D., Park J. Y., Ames B. N. 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. doi: 10.1073/pnas.89.19.9112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zachary A. A., Steinberg A. G., Bias W. B., Leffell M. S. 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. doi: 10.1097/00007890-199607270-00021. [DOI] [PubMed] [Google Scholar]
- Zahavi A. Mate selection-a selection for a handicap. J Theor Biol. 1975 Sep;53(1):205–214. doi: 10.1016/0022-5193(75)90111-3. [DOI] [PubMed] [Google Scholar]
- Zgombić-Knight M., Foglio M. H., 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. doi: 10.1074/jbc.270.9.4305. [DOI] [PubMed] [Google Scholar]
- Zhu X. D., Bonet B., Knopp R. H. 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. doi: 10.1016/s0002-9378(97)70462-9. [DOI] [PubMed] [Google Scholar]
- Zinkernagel R. M. Immunology taught by viruses. Science. 1996 Jan 12;271(5246):173–178. doi: 10.1126/science.271.5246.173. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1038/337166a0. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1098/rspb.1996.0041. [DOI] [PubMed] [Google Scholar]