Age-related alterations of plasma glutathione and oxidation of redox potentials in chimpanzee (Pan troglodytes) and rhesus monkey (Macaca mulatta)

Anderson RM, Colman RJ (2011) Prospects and perspectives in primate aging research. Antioxid Redox Signal 14(2):203–205 Aquilano K, Baldelli S, Ciriolo MR (2011) Glutathione is a crucial guardian of protein integrity in the brain upon nitric oxide imbalance. Commun Integr Biol 4(4):477–479 Ashfaq S, Abramson JL, Jones DP, Rhodes SD, Weintraub WS, Hooper WC, Vaccarino V, Harrison DG, Quyyumi AA (2006) The Relationship between Plasma Levels of Oxidized and Reduced Thiols and Early Atherosclerosis in Healthy Adults. J Am Coll Cardiol 47(5):1005–1011. doi:10.1016/j.jacc.2005.09.063 Ashfaq S, Abramson JL, Jones DP, Rhodes SD, Weintraub WS, Hooper WC, Vaccarino V, Alexander RW, Harrison DG, Quyyumi AA (2008) Endothelial Function and Aminothiol Biomarkers of Oxidative Stress in Healthy Adults. Hypertension 52(1):80–85. doi:10.1161/hypertensionaha.107.097386 Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581 Blanco RA, Ziegler TR, Carlson BA, Cheng P-Y, Park Y, Cotsonis GA, Accardi CJ, Jones DP (2007) Diurnal variation in glutathione and cysteine redox states in human plasma. Am J Clin Nutr 86(4):1016–1023 Borras C, Gambini J, Vina J (2007) Mitochondrial oxidant generation is involved in determining why females live longer than males. Front Biosci 12:1008–1013 Candore G, Balistreri CR, Grimaldi MP, Vasto S, ListÌ F, Chiappelli M, Licastro F, Lio D, Caruso C (2006) Age-Related Inflammatory Diseases. Ann NY Acad Sci 1089(1):472–486. doi:10.1196/annals.1386.008 Chen F-C, Li W-H (2001) Genomic Divergences between Humans and Other Hominoids and the Effective Population Size of the Common Ancestor of Humans and Chimpanzees. Am J Hum Genet 68(2):444–456. doi:10.1086/318206 Chen X, Errangi B, Li L, Glasser MF, Westlye LT, Fjell AM, Walhovd KB, Hu X, Herndon JG, Preuss TM, Rilling JK (2013) Brain aging in humans, chimpanzees (Pan troglodytes), and rhesus macaques (Macaca mulatta): magnetic resonance imaging studies of macro- and microstructural changes. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2013.03.028 Colombo G, Dalle-Donne I, Giustarini D, Gagliano N, Portinaro N, Colombo R, Rossi R, Milzani A (2010) Cellular redox potential and hemoglobin S-glutathionylation in human and rat erythrocytes: A comparative study. Blood Cells Mol Dis 44(3):133–139. doi:10.1016/j.bcmd.2009.11.005 Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95 Dröge W (2003) Oxidative Stress and Aging. Adv Exp Med Biol 543:191–200 Evans JL, Maddux BA, Goldfine ID (2005) The Molecular Basis of Oxidative Stress-Induced Insulin Resistance. Antioxid Redox Signal 7(7–8):1040–1052 Finch CE, Austad SN (2012) Primate aging in the mammalian scheme: the puzzle of extreme variation in brain aging. Age (Dordrecht, Netherlands) 34(5):1075–1091. doi:10.1007/s11357-011-9355-9 Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408(6809):239–247 Forman HJ, Fukuto JM, Torres M (2004) Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol Cell Physiol 287(2):C246–C256. doi:10.1152/ajpcell.00516.2003 Go Y-M, Jones DP (2005) Intracellular Proatherogenic Events and Cell Adhesion Modulated by Extracellular Thiol/Disulfide Redox State. Circulation 111(22):2973–2980. doi:10.1161/circulationaha.104.515155 Go Y-M, Jones DP (2011) Cysteine/cystine redox signaling in cardiovascular disease. Free Radic Biol Med 50(4):495–509 Gueorguieva R, Krystal JH (2004) Move over ANOVA: progress in analyzing repeated-measures data and its reflection in papers published in the Archives of General Psychiatry. Arch Gen Psychiatry 61(3):310–317 Harman D (1956) Aging: a theory based on free radical and radiation chemistry. Gerontol 11:298–300 Hempe JM, Ory-Ascani J, Hsia D (2007) Genetic variation in mouse beta globin cysteine content modifies glutathione metabolism: implications for the use of mouse models. Exp Biol Med (Maywood) 232(3):437–444 Herculano-Houzel S (2012) The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost. Proc Natl Acad Sci U S A 109(Suppl 1):10661–10668. doi:10.1073/pnas.1201895109 Herndon JG (2010) The grandmother effect: implications for studies on aging and cognition. Gerontol 56(1):73–79. doi:10.1159/000236045 Herndon JG, Tigges J, Anderson DC, Klumpp SA, McClure HM (1999) Brain Weight Throughout the Life Span of the Chimpanzee. J Comp Neurol 409:567–572 Heuer E, Rosen RF, Cintron A, Walker LC (2012) Nonhuman primate models of Alzheimer-like cerebral proteopathy. Curr Pharm Des 18(8):1159–1169 Ide T, Tsutsui H, Ohashi N, Hayashidani S, Suematsu N, Tsuchihashi M, Tamai H, Takeshita A (2002) Greater Oxidative Stress in Healthy Young Men Compared With Premenopausal Women. Arterioscler Thromb Vasc Biol 22(3):438–442. doi:10.1161/hq0302.104515 Jiang S, Moriarty-Craige SE, Orr M, Cai J, Sternberg P, Jones DP (2005) Oxidant-Induced Apoptosis in Human Retinal Pigment Epithelial Cells: Dependence on Extracellular Redox State. Invest Ophthalmol Vis Sci 46(3):1054–1061. doi:10.1167/iovs.04-0949 Jonas CR, Ziegler TR, LiH G, Jones DP (2002) Extracellular thiol/disulfide redox state affects proliferation rate in a human colon carcinoma (Caco2) cell line. Free Radic Biol Med 33(11):1499–1506. doi:10.1016/s0891-5849(02)01081-x Jonas CR, Gu LH, Nkabyo YS, Mannery YO, Avissar NE, Sax HC, Jones DP, Ziegler TR (2003) Glutamine and KGF each regulate extracellular thiol/disulfide redox and enhance proliferation in Caco-2 cells. Am J Physiol Regul Integr Comp Physiol 285(6):R1421–R1429. doi:10.1152/ajpregu.00702.2002 Jones DP (2002) Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol 348:93–112 Jones DP (2006a) Extracellular Redox State: Refining the Definition of Oxidative Stress in Aging. Rejuvenation Res 9(2):169–181. doi:10.1089/rej.2006.9.169 Jones DP (2006b) Redefining oxidative stress. Antioxid Redox Signal 8(9–10):1865–1879. doi:10.1089/ars.2006.8.1865 Jones DP (2008) Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295(4):C849–C868. doi:10.1152/ajpcell.00283.2008 Jones DP, Liang Y (2009) Measuring the poise of thiol/disulfide couples in vivo. Free Radic Biol Med 47(10):1329–1338. doi:10.1016/j.freeradbiomed.2009.08.021 Jones DP, Carlson JL, Samiec PS, Sternberg P Jr, Mody VC Jr, Reed RL, Brown LAS (1998) Glutathione measurement in human plasma: Evaluation of sample collection, storage and derivatization conditions for analysis of dansyl derivatives by HPLC. Clin Chim Acta 275(2):175–184. doi:10.1016/s0009-8981(98)00089-8 Jones DP, Carlson JL, Mody VC, Cai J, Lynn MJ, Sternberg P (2000) Redox state of glutathione in human plasma. Free Radic Biol Med 28(4):625–635 Jones DP, Mody VC Jr, Carlson JL, Lynn MJ, Sternberg P (2002) Redox analysis of human plasma allows separation of pro-oxidant events of aging from decline in antioxidant defenses. Free Radic Biol Med 33(9):1290–1300 Jucker M (2010) The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nature medicine 16(11):1210–1214. doi:10.1038/nm.2224 Keaney JF Jr, Larson MG, Vasan RS, Wilson PWF, Lipinska I, Corey D, Massaro JM, Sutherland P, Vita JA, Benjamin EJ (2003) Obesity and Systemic Oxidative Stress: Clinical Correlates of Oxidative Stress in The Framingham Study. Arterioscler Thromb Vasc Biol 23(3):434–439. doi:10.1161/01.atv.0000058402.34138.11 Klepac N, Relja M, Klepac R, Hecimovic S, Babic T, Trkulja V (2007) Oxidative stress parameters in plasma of Huntington’s disease patients, asymptomatic Huntington’s disease gene carriers and healthy subjects: a cross-sectional study. J Neurol 254(12):1676–1683 Kondo T, Hirose M, Kageyama K (2009) Roles of oxidative stress and redox regulation in atherosclerosis. J Atheroscler Thromb 16(5):532–538 Lammey ML, Lee DR, Ely JJ, Sleeper MM (2008) Sudden cardiac death in 13 captive chimpanzees (Pan troglodytes). J Med Primatol 37:39–43. doi:10.1111/j.1600-0684.2007.00260.x Liu X, Somel M, Tang L, Yan Z, Jiang X, Guo S, Yuan Y, He L, Oleksiak A, Zhang Y, Li N, Hu Y, Chen W, Qiu Z, Paabo S, Khaitovich P (2012) Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome research 22(4):611–622. doi:10.1101/gr.127324.111 Lopez-Ruiz A, Sartori-Valinotti J, Yanes LL, Iliescu R, Reckelhoff JF (2008) Sex differences in control of blood pressure: role of oxidative stress in hypertension in females. Am J Physiol Heart Circ Physiol 295(2):H466–H474. doi:10.1152/ajpheart.01232.2007 Mendelsohn ME, Karas RH (2005) Molecular and Cellular Basis of Cardiovascular Gender Differences. Science 308(5728):1583–1587. doi:10.1126/science.1112062 Miller AA, De Silva TM, Jackman KA, Sobey CG (2007) Effect of gender and sex hormones on vascular oxidative stress. Clin Exp Pharmacol Physiol 34(10):1037–1043. doi:10.1111/j.1440-1681.2007.04732.x Nakamura E, Lane MA, Roth GS, Ingram DK (1998) A strategy for identifying biomarkers of aging: further evaluation of hematology and blood chemistry data from a calorie restriction study in rhesus monkeys. Exp Gerontol 33(5):421–443. doi:10.1016/s0531-5565(97)00134-4 Nkabyo YS, Go Y-M, Ziegler TR, Jones DP (2005) Extracellular cysteine/cystine redox regulates the p44/p42 MAPK pathway by metalloproteinase-dependent epidermal growth factor receptor signalling. Am J Physiol Gastrointest Liver Physiol 289(1):G70–G78 Nunamaker EA, Lee DR, Lamney ML (2012) Chronic diseases in captive geriatric female chimpanzees (Pan troglodytes). Comp Med 62(2):131–136 Olmez I, Ozyurt H (2012) Reactive oxygen species and ischemic cerebrovascular disease. Neurochem Int 60(2):208–212. doi:10.1016/j.neuint.2011.11.009 Patel RS, Al Mheid I, Morris AA, Ahmed Y, Kavtaradze N, Ali S, Dabhadkar K, Brigham K, Hooper WC, Alexander RW, Jones DP, Quyyumi AA (2011) Oxidative stress is associated with impaired arterial elasticity. Atherosclerosis 218(1):90–95. doi:10.1016/j.atherosclerosis.2011.04.033 Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441 (7097):1103–1108. doi:http://www.nature.com/nature/journal/v441/n7097/suppinfo/nature04789_S1.html Preuss TM (2011) The human brain: rewired and running hot. Ann N Y Acad Sci 1225(Suppl 1):E182–191. doi:10.1111/j.1749-6632.2011.06001.x Rebrin I, Sohal RS (2008) Pro-oxidant shift in glutathione redox state during aging. Adv Drug Deliv Rev 60(13–14):1545–1552. doi:10.1016/j.addr.2008.06.001 Rebrin I, Kamzalov S, Sohal RS (2003) Effects of age and caloric restriction on glutathione redox state in mice. Free Radic Biol Med 35(6):626–635. doi:10.1016/s0891-5849(03)00388-5 Rebrin I, Bayne AC, Mockett RJ, Orr WC, Sohal RS (2004) Free aminothiols, glutathione redox state and protein mixed disulphides in aging Drosophilia melanogaster. Biochem J 382(Pt 1):131–136 Rebrin I, Forster MJ, Sohal RS (2007) Effects of age and caloric intake on glutathione redox state in different brain regions of C57BL/6 and DBA/2 mice. Brain Res 1127:10–18. doi:10.1016/j.brainres.2006.10.040 Rebrin I, Forster MJ, Sohal RS (2011) Association between life-span extension by caloric restriction and thiol redox state in two different strains of mice. Free Radic Biol Med 51(1):225–233. doi:10.1016/j.freeradbiomed.2011.04.006 Reckelhoff JF (2001) Gender Differences in the Regulation of Blood Pressure. Hypertension 37(5):1199–1208. doi:10.1161/01.hyp.37.5.1199 Regitz-Zagrosek V, Lehmkuhl E, Weickert MO (2006) Gender differences in the metabolic syndrome and their role for cardiovascular disease. Clin Res Cardiol 95(3):136–147 Rhee SG (2006) H2O2, a Necessary Evil for Cell Signaling. Science 312(5782):1882–1883. doi:10.1126/science.1130481 Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37(2):191–223. doi:10.1006/jhev.1999.0313 Roth GS, Mattison JA, Ottinger MA, Chachich ME, Lane MA, Ingram DK (2004) Aging in rhesus monkeys: relevance to human health interventions. Science 305(5689):1423–1426. doi:10.1126/science.1102541 Samiec PS, Drews-Botsch C, Flagg EW, Kurtz JC, Sternberg P, Reed RL, Jones DP (1998) Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic Biol Med 24(5):699–704 Shukla V, Mishra SK, Pant HC (2011) Oxidative Stress in Neurodegeneration. Adv in Pharmacol Sci 2011:572–634 Sohal RS (2002) Oxidative stress hypothesis of aging. Free Radic Biol Med 33(5):573–574. doi:10.1016/s0891-5849(02)00885-7 Sohal RS, Orr WC (2012) The redox stress hypothesis of aging. Free Radic Biol Med 52(3):539–555. doi:10.1016/j.freeradbiomed.2011.10.445 Sohal RS, Weindruch R (1996) Oxidative Stress, Caloric Restriction, and Aging. Science 273(5271):59–63. doi:10.1126/science.273.5271.59 Sohal RS, Toy PL, Farmer KJ (1987) Age-related changes in the redox status of the housefly, Musca domestica. Arch Gerontol Geriatr 6(2):95–100. doi:10.1016/0167-4943(87)90001-x Takahata N, Satta Y (1997) Evolution of the primate lineage leading to modern humans: Phylogenetic and demographic inferences from DNA sequences. Proc Natl Acad Sci U S A 94(9):4811–4815 Tigges J, Gordan TP, McClure HM, Hall EC, Peters A (1988) Survival Rate and Life Span of Rhesus Monkeys at teh Yerkes Regional Primate Research Center. Am J Primatol 15:263–273 VandeBerg J, Zola S (2005) A unique biomedical resource at risk. Nature 437(7055):30–32 Veal E, Day A (2011) Hydrogen peroxide as a signaling molecule. Antioxid Redox Signal 15(1):147–151 Videan EN, Fritz J, Murphy J (2008) Effects of aging on hematology and serum clinical chemistry in chimpanzees (Pan troglodytes). Am J Primatol 70(4):327–338. doi:10.1002/ajp.20494 Zhu Y, Carvey PM, Ling Z (2006) Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res 1090(1):35–44. doi:10.1016/j.brainres.2006.03.063