Abstract
In this series of experiments, we found that Sanguisorbae Radix extract possesses strong free radical-scavenging activity in vitro and in vivo. This crude drug protected against renal disease, which is closely associated with excessive generation of reactive oxygen species. We also showed that Sanguisorbae Radix extract can suppress lipid peroxidation and stimulate an antioxidant defense ability in SAM, suggesting that this crude drug may be an effective agent for ameliorating the pathological conditions related to excessive generation of free radicals and oxidant damage, particularly in the aging process.
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References
- 1.Lynch M.A. Analysis of the mechanisms underlying the age-related impairment in long-term potentiation in the rat. Reviews in the Neurosciences. 1998;9:169–201. doi: 10.1515/revneuro.1998.9.3.169. [DOI] [PubMed] [Google Scholar]
- 2.Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol. Rev. 1998;78:547–581. doi: 10.1152/physrev.1998.78.2.547. [DOI] [PubMed] [Google Scholar]
- 3.Mecocci P., Fano G., Fulle S., MacGarvey U., Shinobu L., Polidori M.C., Cherubini A., Vecchiet J., Senin U., Beal M.F. Age-dependent increases in oxidative damage to DNA, lipids, and protein in human skeletal muscle. Free Rad. Biol. Med. 1999;26:303–308. doi: 10.1016/S0891-5849(98)00208-1. [DOI] [PubMed] [Google Scholar]
- 4.Tian L., Cai Q., Wei H. Alterations of antioxidant enzymes and oxidative damage to macromolecules in different organs of rats during aging. Free Rad. Biol. Med. 1998;24:1477–1484. doi: 10.1016/S0891-5849(98)00025-2. [DOI] [PubMed] [Google Scholar]
- 5.Kakkar R., Bains J.S., Sharma S.P. Effect of vitamin E on life span, malondialdehyde content and antioxidant enzymes in aging Zaprionus paravittiger. Gerontology. 1996;42:312–321. doi: 10.1159/000213809. [DOI] [PubMed] [Google Scholar]
- 6.Kumari M.V., Yoneda T., Hiramatsu M. Effect of “beta CATECHIN” on the life span of senescence accelerated mice (SAM-P8 strain) Biochem. Mol. Biol. Intern. 1997;41:1005–1011. doi: 10.1080/15216549700202071. [DOI] [PubMed] [Google Scholar]
- 7.Brack C., Bechter-Thuring E., Labuhn M. N-Acetylcysteine slows down ageing and increases the life span of Drosophila melanogaster. Cell. Mol. Life Sci. 1997;53:960–966. doi: 10.1007/PL00013199. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Youdim K.A., Deans S.G. Beneficial effects of thyme oil on age-related changes in the phospholipid C20 and C22 polyunsaturated fatty acid composition of various rat tissues. Biochim. Biophys. Acta. 1999;1438:140–146. doi: 10.1016/s1388-1981(99)00045-1. [DOI] [PubMed] [Google Scholar]
- 9.Barber D.A., Harris S.R. Oxygen free radicals and antioxidants: a review. Am. Pharm. 1994;NS34:26–35. doi: 10.1016/s0160-3450(15)30310-x. [DOI] [PubMed] [Google Scholar]
- 10.Rikans L.E., Hornbrook K.R. Lipid peroxidation, antioxidant protection and aging. Biochim. Biophys. Acta. 1997;1362:116–127. doi: 10.1016/s0925-4439(97)00067-7. [DOI] [PubMed] [Google Scholar]
- 11.Das D.K., Maulik N. Antioxidant effectiveness in ischemia-reperfusion tissue injury. Methods Enzymol. 1994;233:601–610. doi: 10.1016/s0076-6879(94)33063-8. [DOI] [PubMed] [Google Scholar]
- 12.Chapple I.L. Reactive oxygen species and antioxidants in inflammatory diseases. J. Clin. Periodontol. 1997;24:287–296. doi: 10.1111/j.1600-051X.1997.tb00760.x. [DOI] [PubMed] [Google Scholar]
- 13.Hatano T., Edamatsu R., Hiramatsu M., Mori A., Fujita Y., Yasuhara T., Yoshida T., Okuda T. Effects of the interaction of tannins with co-existing substances. VI. Effects of tannins and related polyphenols and superoxide anion radical, and on 1,1-diphenyl-2-picrylhydrazyl radical. Chem. Pharm. Bull. 1989;37:2016–2021. [Google Scholar]
- 14.Zhao Y., Wang X., Kawai M., Liu J., Liu M., Mori A. Antioxidant activity of Chinese ant extract preparations. Acta Med. Okayama. 1995;49:275–279. doi: 10.18926/AMO/30386. [DOI] [PubMed] [Google Scholar]
- 15.Robak J., Gryglewski R.J. Bioactivity of flavonoids. Pol. J. Pharmacol. 1996;48:555–564. [PubMed] [Google Scholar]
- 16.Yokozawa T., Dong E., Liu Z.W., Oura H. Antiperoxidation activity of traditional Chinese prescriptions and their main crude drugs in vitro. Nat. Med. 1997;51:92–97. [Google Scholar]
- 17.Yokozawa T., Dong E., Liu Z.W., Shimizu M. Antioxidative activity of flavones and flavonols in vitro. Phytother. Res. 1997;11:446–449. doi: 10.1002/(SICI)1099-1573(199709)11:6<446::AID-PTR128>3.0.CO;2-8. [DOI] [Google Scholar]
- 18.Yokozawa T., Chen C.P., Liu Z.W. Effect of traditional Chinese prescriptions and their main crude drugs on 1,1-diphenyl-2-picrylhydrazyl radical. Phytother. Res. 1998;12:94–97. doi: 10.1002/(SICI)1099-1573(199803)12:2<94::AID-PTR194>3.0.CO;2-U. [DOI] [Google Scholar]
- 19.Yokozawa T., Chen C.P., Dong E., Tanaka T., Nonaka G., Nishioka I. Study on the inhibitory effect of tannins and flavonoids against the 1,1-diphenyl-2-picrylhydrazyl radical. Biochem. Pharmacol. 1998;56:213–222. doi: 10.1016/S0006-2952(98)00128-2. [DOI] [PubMed] [Google Scholar]
- 20.Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 1991;43:109–142. [PubMed] [Google Scholar]
- 21.Gross S.S., Wolin M.S. Nitric oxide: pathophysiological mechanisms. Annu. Rev. Physiol. 1995;57:737–769. doi: 10.1146/annurev.ph.57.030195.003513. [DOI] [PubMed] [Google Scholar]
- 22.Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 1992;6:3051–3064. [PubMed] [Google Scholar]
- 23.Harrison D.G. Perspective series: nitric oxide and nitric oxide synthases. Cellular and molecular mechanisms of endothelial cell dysfunction. J. Clin. Invest. 1997;100:2153–2157. doi: 10.1172/JCI119751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 1991;288:481–487. doi: 10.1016/0003-9861(91)90224-7. [DOI] [PubMed] [Google Scholar]
- 25.Akaike T., Suga M., Maeda H. Free radicals in viral pathogenesis: molecular mechanisms involving superoxide and NO. Proc. Soc. Exp. Biol. Med. 1998;217:64–73. doi: 10.3181/00379727-217-44206. [DOI] [PubMed] [Google Scholar]
- 26.Kunchandy E., Rao M.N.A. Oxygen radical scavenging activity of curcumin. Int. J. Pharm. 1990;58:237–240. doi: 10.1016/0378-5173(90)90201-E. [DOI] [Google Scholar]
- 27.Hu J.P., Calomme M., Lasure A., De Bruyne T., Pieters L., Vlietinck A., Vanden Berghe D.A. Structure-activity relationship of flavonoids with superoxide scavenging activity. Biol. Trace Element Res. 1995;47:327–331. doi: 10.1007/BF02790134. [DOI] [PubMed] [Google Scholar]
- 28.Yokozawa T., Chen C.P., Tanaka T. Direct scavenging of nitric oxide by traditional crude drugs. Phytomed. 1999;6:453–463. doi: 10.1016/S0944-7113(00)80074-4. [DOI] [PubMed] [Google Scholar]
- 29.Chen C.P., Yokozawa T., Kitani K. Beneficial effects of Sanguisorbae Radix in renal dysfunction caused by endotoxin in vivo. Biol. Pharm. Bull. 1999;22:1327–1330. doi: 10.1248/bpb.22.1327. [DOI] [PubMed] [Google Scholar]
- 30.Chen, C.P., Yokozawa, T., Sekiya, M., Hattori, M., Tanaka, T.: Protective effect of Sanguisorbae Radix against peroxynitrite-mediated renal injury. J. Trad. Med., in press.
- 31.Yokozawa T., Chen C.P., Kitani K. Chiyu extract stimulates antioxidant defense ability in senescence-accelerated mice. J. Trad. Med. 2000;17:73–79. [Google Scholar]
- 32.Gold M.E. Pharmacology of the nitrovasodilators. Antianginal, antihypertensive, and antiplatelet actions. Nursing Clin. North Am. 1991;26:437–450. [PubMed] [Google Scholar]
- 33.Wink D.A., Cook J.A., Pacelli R., DeGraff W., Gamson J., Liebmann J., Krishna M.C., Mitchell J.B. The effect of various nitric oxide-donor agents on hydrogen peroxide-mediated toxicity: a direct correlation between nitric oxide formation and protection. Arch. Biochem. Biophys. 1996;331:241–248. doi: 10.1006/abbi.1996.0304. [DOI] [PubMed] [Google Scholar]
- 34.Green L.C., Wagner D.A., Glogowski J., Skipper P.L., Wishnok J.S., Tannenbaum S.R. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 1982;126:131–138. doi: 10.1016/0003-2697(82)90118-X. [DOI] [PubMed] [Google Scholar]
- 35.Tanaka, T., Nonaka, G., Nishioka, I.: Tannins and related compounds. Part 28. Revision of the structures of sanguiins H-6, H-2, and H-3, and isolation and characterization of sanguiin H-11, a novel tetrameric hydrolyzable tannin, and seven related tannins, from Sanguisorba officinalis. J. Chem. Research (S) 176–177, (M) 2001–2029, 1985.
- 36.Nonaka G., Nishioka I., Nagasawa T., Oura H. Tannins and related compounds. I. Rhubarb (1) Chem. Pharm. Bull. 1981;29:2862–2870. [Google Scholar]
- 37.Kashiwada Y., Nonaka G., Nishioka I. Tannins and related compounds. XLVlII. Rhubarb (7). Isolation and characterization of new dimeric and trimeric procyanidins. Chem. Pharm. Bull. 1986;34:4083–4091. doi: 10.1248/cpb.34.4083. [DOI] [PubMed] [Google Scholar]
- 38.Cooper S.F., Mockle J.A., Beliveau J. Alkaloids of Coptis groenlandica. Planta Medica. 1970;19:23–29. doi: 10.1055/s-0028-1099800. [DOI] [PubMed] [Google Scholar]
- 39.Valencia E., Weiss I., Firdous S., Freyer A.J., Shamma M., Urzua A., Fajardo V. The isoindolobenzazepine alkaloids. Tetrahedron. 1984;40:3957–3962. doi: 10.1016/0040-4020(84)85073-5. [DOI] [Google Scholar]
- 40.Li X.J., Tian X.H., Chen Y.X., Li F., Duan M.S., Zhou Y.Y. Separation and identification of epiberberine in coptis (Coptis chinensis) Chin. Trad. Herb. Drugs. 1986;17:2–3. [Google Scholar]
- 41.Ikuta A., Itokawa H. Protoberberine alkaloids from Coptis quinquefolia. Shoyakugaku Zasshi. 1989;43:81–82. [Google Scholar]
- 42.Hong C.Y., Wang C.P., Huang S.S., Hsu F.L. The inhibitory effect of tannins on lipid peroxidation of rat heart mitochondria. J. Pharm. Pharmacol. 1995;47:138–142. doi: 10.1111/j.2042-7158.1995.tb05766.x. [DOI] [PubMed] [Google Scholar]
- 43.Yoshida T., Mori K., Hatano T., Okumura T., Uehara I., Komagoe K., Fujita Y., Okuda T. Studies on inhibition mechanism of autoxidation by tannins and flavonoids. V. Radical-scavenging effects of tannins and related polyphenols on 1,1-diphenyl-2-picrylhydrazyl radical. Chem. Pharm. Bull. 1989;37:1919–1921. [Google Scholar]
- 44.Otsuka H., Tsukui M., Matsuoka T., Goto M., Fujimura H., Hiramatsu Y., Sawada T. Studies on anti-inflammatory agents. Anti-inflammatory screening by fertile egg method. Yakugaku Zasshi. 1974;94:796–801. doi: 10.1248/yakushi1947.94.7_796. [DOI] [PubMed] [Google Scholar]
- 45.Otsuka H., Fujimura H., Sawada T., Goto M. Studies on anti-inflammatory constituents from Rhizome of Coptis japonicaMAKINO. Yakugaku Zasshi. 1981;101:883–890. doi: 10.1248/yakushi1947.101.10_883. [DOI] [PubMed] [Google Scholar]
- 46.Kubo M., Matsuda H., Tanaka M., Kimura Y., Okuda H., Higashino M., Tani T., Namba K., Arichi S. Studies on Scutellariae Radix. VII. Anti-arthritic and anti-inflammatory actions of methanolic extract and flavonoid components from Scutellariae Radix. Chem. Pharm. Bull. 1984;32:2724–2729. doi: 10.1248/cpb.32.2724. [DOI] [PubMed] [Google Scholar]
- 47.Yamahara J., Matsuda H., Sawada T., Mibu H., Fujimura H. Biologically active principles of crude drugs. Pharmacological evaluation of Artemisiae capillarisFLOS. Yakugaku Zasshi. 1982;102:285–291. [PubMed] [Google Scholar]
- 48.Zhang Y.D., Wang Y.L., Shen J.P., Li D.X. Hypotensive and antiinflammatory effects of Astragalus saponin 1. Acta Pharm. Sin. 1984;19:333–337. [Google Scholar]
- 49.Rice-Evans C.A., Miller N.J., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Rad. Biol. Med. 1996;20:933–956. doi: 10.1016/0891-5849(95)02227-9. [DOI] [PubMed] [Google Scholar]
- 50.Cao G., Sofic E., Prior R.L. Antioxidant and prooxidant behavior of flavonoids: structure-activity relationship. Free Rad. Biol. Med. 1997;22:749–760. doi: 10.1016/S0891-5849(96)00351-6. [DOI] [PubMed] [Google Scholar]
- 51.Rao M.N.A. Nitric oxide scavenging by curcuminoids. J. Pharm. Pharmacol. 1997;49:105–107. doi: 10.1111/j.2042-7158.1997.tb06761.x. [DOI] [PubMed] [Google Scholar]
- 52.Kone B.C., Baylis C. Biosynthesis and homeostatic roles of nitric oxide in the normal kidney. Am. J. Physiol. 1997;272:F561–F578. doi: 10.1152/ajprenal.1997.272.5.F561. [DOI] [PubMed] [Google Scholar]
- 53.Bachmann S., Mundel P. Nitric oxide in the kidney: synthesis, localization, and function. Am. J. Kidney Diseases. 1994;24:112–129. doi: 10.1016/s0272-6386(12)80170-3. [DOI] [PubMed] [Google Scholar]
- 54.Yu L., Gengaro P.E., Niederberger M., Burke T.J., Schrier R.W. Nitric oxide: a mediator in rat tubular hypoxia/reoxygenation injury. Proc. Natl. Acad. Sci. USA. 1994;91:1691–1695. doi: 10.1073/pnas.91.5.1691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Cattell V., Cook T., Moncada S. Glomeruli synthesize nitrite in experimental nephrotoxic nephritis. Kidney Int. 1990;38:1056–1060. doi: 10.1038/ki.1990.312. [DOI] [PubMed] [Google Scholar]
- 56.Suh N., Honda T., Finlay H.J., Barchowsky A., Williams C., Benoit N.E., Xie Q., Nathan C., Gribble G.W., Sporn M.B. Novel triterpenoids suppress inducible nitric oxide synthase (iNOS) and inducible cyclooxygenase (COX-2) in mouse macrophages. Cancer Res. 1998;58:717–723. [PubMed] [Google Scholar]
- 57.Weinberg J.B., Granger D.L., Pisetsky D.S., Seldin M.F., Misukonis M.A., Mason S.N., Pippen A.M., Ruiz P., Wood E.R., Gilkeson G.S. The role of nitric oxide in the pathogenesis of spontaneous murine autoimmune disease: increased nitric oxide production and nitric oxide synthase expression in MRL-lpr/lpr mice, and reduction of spontaneous glomerulonephritis and arthritis by orally administered NG-monomethyl-L-arginine. J. Exp. Med. 1994;179:651–660. doi: 10.1084/jem.179.2.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Mashiach E., Sela S., Winaver J., Shasha S.M., Kristal B. Renal ischemia-reperfusion injury: contribution of nitric oxide and renal blood flow. Nephron. 1998;80:458–467. doi: 10.1159/000045220. [DOI] [PubMed] [Google Scholar]
- 59.Schwartz D., Blum M., Peer G., Wollman Y., Maree A., Serban I., Grosskopf I., Cabili S., Levo Y., Iaina A. Role of nitric oxide (EDRF) in radiocontrast acute renal failure in rats. Am. J. Physiol. 1994;267:F374–F379. doi: 10.1152/ajprenal.1994.267.3.F374. [DOI] [PubMed] [Google Scholar]
- 60.Yokozawa T., Chen C.P., Tanaka T., Kitani K. A study on the nitric oxide production-suppressing activity of Sanguisorbae Radix components. Biol. Pharm. Bull. 2000;23:717–722. doi: 10.1248/bpb.23.717. [DOI] [PubMed] [Google Scholar]
- 61.Halliwell B. Oxidants and human disease: some new concepts. FASEB J. 1987;1:358–364. [PubMed] [Google Scholar]
- 62.Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. J. Biol. Chem. 1991;266:4244–4250. [PubMed] [Google Scholar]
- 63.Koppenol W.H., Moreno J.J., Pryor W.A., Ischiropoulos H., Beckman J.S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 1992;5:834–842. doi: 10.1021/tx00030a017. [DOI] [PubMed] [Google Scholar]
- 64.Brown G.C. Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta. 1999;1411:351–369. doi: 10.1016/S0005-2728(99)00025-0. [DOI] [PubMed] [Google Scholar]
- 65.Herce-Pagliai C., Kotecha S., Shuker D.E. Analytical methods for 3-nitrotyrosine as a marker of exposure to reactive nitrogen species: a review. Nitric Oxide. 1998;2:324–336. doi: 10.1006/niox.1998.0192. [DOI] [PubMed] [Google Scholar]
- 66.Di Stasi A.M.M., Mallozzi C., Macchia G., Petrucci T.C., Minetti M. Peroxynitrite induces tyrosine nitration and modulates tyrosine phosphorylation of synaptic proteins. J. Neurochem. 1999;73:727–735. doi: 10.1046/j.1471-4159.1999.0730727.x. [DOI] [PubMed] [Google Scholar]
- 67.Yasmin W., Strynadka K.D., Schulz R. Generation of peroxynitrite contributes to ischemia-reperfusion injury in isolated rat hearts. Cardiovasc. Res. 1997;33:422–432. doi: 10.1016/S0008-6363(96)00254-4. [DOI] [PubMed] [Google Scholar]
- 68.Eliasson M.J.L., Huang Z., Ferrante R.J., Sasamata M., Molliver M.E., Snyder S.H., Moskowitz M.A. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J. Neurosci. 1999;19:5910–5918. doi: 10.1523/JNEUROSCI.19-14-05910.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69.Virag L., Scott G.S., Antal-Szalmas P., O’Connor M., Ohshima H., Szabo C. Requirement of intracellular calcium mobilization for peroxynitrite-induced poly(ADP-ribose) synthetase activation and cytotoxicity. Mol. Pharmacol. 1999;56:824–833. [PubMed] [Google Scholar]
- 70.Chen C.P., Yokozawa T., Tanaka T. Protective effect of Sanguisorbae Radix against apoptosis and function of renal tissues subjected to ischemia-reperfusion. J. Trad. Med. 1999;16:97–101. [Google Scholar]
- 71.Nishioka I. The chemistry of tannins (1) J. Tradit. Sino-Jpn. Med. 1990;11:75–81. [Google Scholar]
- 72.Yokozawa T., Fujioka K., Oura H., Nonaka G., Nishioka I. Effects of rhubarb tannins on uremic toxins. Nephron. 1991;58:155–160. doi: 10.1159/000186406. [DOI] [PubMed] [Google Scholar]
- 73.Yokozawa T., Fujioka K., Oura H., Nonaka G., Nishioka I. Effects of rhubarb tannins on renal function in rats with renal failure. Jpn. J. Nephrol. 1993;35:13–18. [PubMed] [Google Scholar]
- 74.Yokozawa T., Oura H., Hattori M., Iwano M., Dohi K., Sakanaka S., Kim M. Inhibitory effect of tannin in green tea on the proliferation of mesangial cells. Nephron. 1993;65:596–600. doi: 10.1159/000187570. [DOI] [PubMed] [Google Scholar]
- 75.Yokozawa T., Oura H., Sakanaka S., Ishigaki S., Kim M. Depressor effect of tannin in green tea on rats with renal hypertension. Biosci. Biotech. Biochem. 1994;58:855–858. doi: 10.1271/bbb.58.855. [DOI] [Google Scholar]
- 76.Yokozawa T., Fujioka K., Oura H., Tanaka T., Nonaka G., Nishioka I. Uraemic toxin reduction: a newly found effect of hydrolysable-type tannin-containing crude drug and gallotannin. Phytother. Res. 1995;9:327–330. [Google Scholar]
- 77.Yokozawa T., Fujioka K., Oura H., Tanaka T., Nonaka G., Nishioka I. Decrease in uraemic toxins, a newly found beneficial effect of Ephedrae Herba. Phytother. Res. 1995;9:382–384. [Google Scholar]
- 78.Knight J.A. Free radicals: their history and current status in aging and disease. Ann. Clin. Lab. Sci. 1998;28:331–346. [PubMed] [Google Scholar]
- 79.Kretzschmar M. Regulation of hepatic glutathione metabolism and its role in hepatotoxicity. Exp. Toxicol. Pathol. 1996;48:439–446. doi: 10.1016/S0940-2993(96)80054-6. [DOI] [PubMed] [Google Scholar]
- 80.Stabel-Burow J., Kleu A., Schuchmann S., Heinemann U. Glutathione levels and nerve cell loss in hippocampal cultures from trisomy 16 mouse — a model of Down syndrome. Brain Res. 1997;765:313–318. doi: 10.1016/S0006-8993(97)00480-0. [DOI] [PubMed] [Google Scholar]
- 81.Munkres K.D., Rana R.S., Goldstein E. Genetically determined conidial longevity is positively correlated with superoxide dismutase, catalase, glutathione peroxidase, cytochrome c peroxidase, and ascorbate free radical reductase activities in Neurospora crassa. Mechan. Ageing Develop. 1984;24:83–100. doi: 10.1016/0047-6374(84)90177-5. [DOI] [PubMed] [Google Scholar]
- 82.Kellogg E.W., Fridovich I. Superoxide dismutase in the rat and mouse as a function of age and longevity. J. Gerontol. 1976;31:405–408. doi: 10.1093/geronj/31.4.405. [DOI] [PubMed] [Google Scholar]
- 83.Tolmasoff J.M., Ono T., Cutler R.G. Superoxide dismutase: correlation with life-span and specific metabolic rate in primate species. Proc. Natl. Acad. Sci. USA. 1980;77:2777–2781. doi: 10.1073/pnas.77.5.2777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84.Cestaro B., Giuliani A., Fabris F., Scarafiotti C. Free radicals, atherosclerosis, ageing and related dysmetabolic pathologies: biochemical and molecular aspects. Eur. J. Cancer Prevent. 1997;6:S25–S30. doi: 10.1097/00008469-199703001-00006. [DOI] [PubMed] [Google Scholar]