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In the defence against hyperglycamiea: an avian strategy

Published online by Cambridge University Press:  18 September 2007

H. Klandorf ,
I.L. Probert  and
M. Iqbal
H. Klandorf*
Affiliation:
Division of Animal and veterinary Sciences, West Virginia University, P.O. Box 6108, Morgantown, WV 26506–6108, USA
I.L. Probert
Affiliation:
Division of Animal and veterinary Sciences, West Virginia University, P.O. Box 6108, Morgantown, WV 26506–6108, USA
M. Iqbal
Affiliation:
Division of Animal and veterinary Sciences, West Virginia University, P.O. Box 6108, Morgantown, WV 26506–6108, USA Center of Excellence for poultry, University of Arkansas, Fayetteville, AR 72701, USA
*
Correspondence to Dr Hillar Klandorf.
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Abstract

Birds live longer than mammals of comparable sizes, contrary to what their metabolic rates, plasma gulcose concentrations and body tempratures, all of which are higher than mammalian norms, would suggest. Although these factors should predispose them to accelerated tissue degeneration, this has been shown not to happen. In this paper the possible mechanism whereby birds limit the accelerated tissue damage that should be associated with the above characteristics are explored. Specifically, this review will focus on the relationship in chickens between the raised concentrations of plasma glucose and the lack of associated tissue complications. We propose that the role of uric acid in birds should be re-examined. Until now uric acid has been considered to be little more than an excretory by-product where its role as an antioxidant can be directly linked to the resistance of birds to glucose-mediated tissue damage. It is suggested that, compared with mammals, the lower rate of generation of reactive oxygen species in birds in association with their stronger antioxidant-defence system contributes to their longevity.

Keywords

Birdshyperglycamieafree radicalsoxidative stresslongevityutric acidAGEspentosidine

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Type
Research Article
Information
World's Poultry Science Journal , Volume 55 , Issue 3 , September 1999 , pp. 251 - 268
Copyright
Copyright © Cambridge University Press 1999

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References

Ames, B.N., Cathcart, R., Schwiers, E. and Hochstein, P. (1981) Uric acid provides an antioxidant defence in humans against oxidant- and radical-caused aging and cancer: a hypothesis. Proceedings of the National Academy of Sciences, USA 78: 6858–6862CrossRefGoogle ScholarPubMed
Ames, B.N., Shigenaga, M.K. and Hagen, T.M. (1993) Oxidants, antioxidants, and the degenerative diseases of ageing. Proceedings of the National Academy of Sciences, USA 90: 7915CrossRefGoogle Scholar
Andreassen, T.T. and Oxlund, H. (1987) Changes in collagen and elastin of rat aorta induced by experimental diabetes and food restriction. Acta Endocrinology 98: 432–436Google Scholar
Andreassen, T.T., Seyer-Hansen, K. and Oxlund, H. (1981) Biomechanical changes in connective tissues induced by experimental diabetes. Acta Endocrinologia 98: 432–436Google ScholarPubMed
Aoki, Y., Yanagisawa, Y., Yazaki, K., Oguchi, H., Kiyosawa, K. and Furuta, S. (1992) Protective effect of vitamin E supplementation on increased thermal stability of collagen in diabetic rats. Diabetologia 35: 913–916CrossRefGoogle ScholarPubMed
Austad, S. and Fischer, K. (1991) Mammalian aging, metabolism, and ecology: evidence from bats and marsupials. Journal of Gerontology: Biological Science 46: B47–B53CrossRefGoogle ScholarPubMed
Bandy, B. and Davison, A. (1990) Mitochondria1 mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radical Biology and Medicine 8: 523CrossRefGoogle Scholar
Barja De Quiroga, G., Lopez-Torres, M. and Perez-Campo, R. (1992) Relationship between antioxidants, lipid peroxidation and aging. In: Free Radicals and Aging (Emerit, I. and Chance, B., Eds), Birkauser Verlag, Basel, pp. 109–123CrossRefGoogle ScholarPubMed
Baynes, J.W. (1991) Role of oxidative stress on development to complications in diabetes. Diabetes 40: 405–412CrossRefGoogle ScholarPubMed
Becker, F.B. (1993) Towards the physiological function of uric acid. Free Radical Biology and Medicine 14: 615–631CrossRefGoogle ScholarPubMed
Berg, T.J., Dahl-Jorgensen, K., Torjesen, P.A. and Hunnsen, K.F. (1997) Increased serum levels of advanced glycosylation end products (AGES) in children and adolescents with IDDM. Diabetes Care 20: 1006–1008CrossRefGoogle ScholarPubMed
Beuchat, C.A. and Chong, C.R. (1997) Hyperglycemia in hummingbirds: implications for hummingbird ecology and human health. Federation of American Societies for Experimental Biology Journal 11: A91Google Scholar
Bilous, R.W., Mauer, S.M., Sutherland, E.R. and Steffes, M.W. (1989) Mean glomerular volume and rate of development of diabetic nephropathy. Diabetes 38: 1142–1147CrossRefGoogle ScholarPubMed
Bishop, M.L., Duben-Engelkink, J.L. and Fody, E.P. (1992) Clinical Chemistry, Principles, Procedures, Correlations. 2nd Edition, Lippincott, PhiladelphiaGoogle Scholar
Bottje, W.G. and Wideman, R.F. (1995) Potential role of free radicals in the pathogenesis of pulmonary hypertension syndrome. Poultry and Avian Biology 6: 211–231Google Scholar
Bottje, W. G., Wang, S., Beers, K.W. and Cawthon, D. (1998) Lung lining fluid antioxidants in male broilers: age-related changes under thermoneutral and cold temperature conditions. Poultry Science 77: 1905–1912CrossRefGoogle ScholarPubMed
Braun, E.J. and Dantzler, W.H. (1997) Vertebrate renal system. In: Handbook of Physiology: Comparative Physiology (Dantzler, W.H., Ed.), Volume 1, Oxford University Press, New York, pp. 481–576CrossRefGoogle Scholar
Brownlee, M., Vlassara, H. and Cerami, A. (1984) Nonenzymatic glycosylation and the pathogenesis of diabetic complication. Annals of Internal Medicine 101: 527–537CrossRefGoogle Scholar
Brownlee, M., Vlassara, H., Kooney, A., Ulrich, P. and Cerami, A. (1986) Aminoguani-dine prevents diabetes-induced arterial wall protein cross-linking. Science 232: 1629–1632CrossRefGoogle ScholarPubMed
Brownlee, M., Cerami, A. and Vlassara, H. (1988a) Advanced products of nonenzymatic glycosylation and the pathogenesis of diabetic vascular disease. Diabetes Metabolism Reviews. 4: 437–451CrossRefGoogle ScholarPubMed
Brownler, M., Cerami, A. and Vlassara, H. (1988b) Advanced glycosylation end products in tissue and the boichemical basis of diabetic complicatoins. Science 318: 1315–1321Google Scholar
Bucala, R. and Cerami, A. (1992) Advanced glycosylation: chemistry, biology, and implications for diabetes and aging. Advances in Pharmacology 23: 1–33CrossRefGoogle Scholar
Cefalu, W.T., Bell-Farrow, A.D., Wang, Z.Q., Sonntag, W.E., Fu, M., Baynes, J.W. and Thorpe, S.R. (1995) Caloric restriction decreases age-dependent accumulation of the glycoxidation products, N-(carboxymethyl)lysine and pentosidine, in rat skin collagen. Journal of Gerontology: Biological Science, 50A: B337–B341Google Scholar
Ceriello, A., Guigliano, D., Quataro, A., Donzella, C. and Leeebvre, P.J. (1991) Vitamin E reduction of protein glycosylastion in diabetes. Diabetes Care 14: 68–72CrossRefGoogle ScholarPubMed
Chandler, M.I., Shannon, W.A. and Desantis, L. (1984) Prevention of capillary basement membrane thickening in diabetic rats by aldose reductase inhibitors. Investigative Ophthalmology and Visual Science 25 (Supplement): 159Google Scholar
Conlon, P., Smith, D. and Gowlett, T. (1991) Oxygen radical production by avian leukocytes. Canadian Journal of Veterinary Research 55: 193–195Google ScholarPubMed
Cutler, R.G. (1984a) Antioxidants, aging, and longevity. In: Free Radicals in Biology (Pryor, W.A., Ed.), Volume VI, Academic Press, Orlando, pp.371–428CrossRefGoogle Scholar
Cutler, R.G. (1984b) Urate and ascorbate: their possible roles as antioxidants in determining longevity of mammalian species. Archives of Gerontology and Geriatrics 3: 321–348CrossRefGoogle ScholarPubMed
Danby, R., Bluff, L., Deheny, T.P. and Gibson, W.R. (1981) Effects of alloxan and streptozotocin at high doses on blood glucose levels, glucose tolerance, and responsiveness to sulphonylureas in chickens. General Comparative Endocrinology 47: 159–169CrossRefGoogle Scholar
Davie, S.J., Gould, B.J. and Yadkin, J.S. (1992) Effect of vitamin C on glycosylation of protein. Diabetes 41: 167–173CrossRefGoogle Scholar
Dunn, J.S., Patrick, J.S., Thorpe, S.R. and Bayens, J.W. (1989) Oxidation of glycated protein: age dependent accumulation of N-(carboxymethy1)lysine in lens proteins. Biochemisty 28: 9464–9468CrossRefGoogle Scholar
Dunn, F.A., Mccance, D.R., Thorpe, S.R., Lyons, T.J. and Baynes, J.W. (1991) Age-dependent accumulation of N-(carboxymethy1)lysine and N-(carboxymethy1)hydroxylysine in human skin collagen. Biochemistry 30: 1205–1210CrossRefGoogle Scholar
Dyer, D.G., Blackledge, J.A., Thorpe, S.R. and Baynes, J.W. (1991a) Formation of pentosidine during nonenzymatic browning of proteins by glucose. Journal of Biological Chemisty 266: 11554–11560Google ScholarPubMed
Dyer, D.G., Blackledge, J.A., Thorpe, S.R. and Baynes, J.W. (1991b) Formation of pentosidine during nonenzymatic browning of proteins by glucose: identification of glucose and other carbohydrates as possible precursors of pentosidine in vivo. Journal of Biological Chemistry 266: 11654–11660CrossRefGoogle ScholarPubMed
Dyer, D.G., Dunn, J.A., Thorpe, S.R. and Lyons, T.J. (1992) Accumulation of Maillard reaction products in skin collagen in diabetes and aging. Annals of the New York Academy of Science 663: 421–422CrossRefGoogle Scholar
Edelstein, D. and Brownlee, M. (1992a) Mechanistic studies of advanced glycosylation end product inhibition by aminoguanidine. Diabetes 41: 26–29CrossRefGoogle ScholarPubMed
Edelstein, D. and Brownlee, M. (1992b) Aminoguanidine ameliorates albuminuria in diabetic hypertensive rats. Diabetologia 35: 96–97CrossRefGoogle ScholarPubMed
Fraga, C.G., Shigenaga, M.K., Park, J.W., Deagan, P. and Ames, B.N. (1990) Oxidative damage to DNA during aging; 8-hydroxyguanosine in rat organ DNA and urine. Proceedings of the National Academy of Sciences, USA 87: 55–63CrossRefGoogle Scholar
Frei, B. (1994) Reactive oxygen species and antioxidant vitamins: mechanisms of action, American Journal of Medicine 97: 5CrossRefGoogle ScholarPubMed
Galeski, A., Kastelic, J., Baer, E. and Kohn, R.R. (1977) Mechanical and structural changes in rat tail tendon induced by alloxan diabetes and aging. Journal of Biomechanics 10: 775–782CrossRefGoogle Scholar
Grandhee, S.K. and Monnier, V.M. (1991) Mechanisms of formation of the Maillard protein cross-link pentosidine: ribose, glucose, fructose and ascorbate as pentosidine precursors. Journal of Biological Chemisty 266: 11649–53CrossRefGoogle ScholarPubMed
Grgic, A., Rosenbloom, A.L., Weber, F.T. and Giordano, B. (1975) Joint contract in childhood diabetes. New England Journal of Medicine 292: 372–379Google Scholar
Guarnieri, C., Muscari, C. and Caldarera, C.M. (1993) Mitochondria1 production of oxygen free radicals in the heart muscle during the life-span of the rat peak at middle age. Experientia Supplementia 62: 47Google Scholar
Hadley, E.C. (1993) Morbid consequences of aging processes: methodologic issues. In: Musculoskeletal Soft-Tissue Aging: Impact on Mobility (Buckwalter, J.A., Goldberg, B.M. and Woo, S.L., Eds), American Academy of Orthopedic Surgeons, Rosemont, IL, pp. 35–47Google Scholar
Halliwell, B. and Gutteridge, J.M.C. (1989) Free Radicals in Biology and Medicine, 2nd edition, Clarendon Press, OxfordGoogle Scholar
Hayase, F., Kim, Y.H. and Kato, H. (1991) Inhibition of the protein crosslinking in a Maillard reaction by aminoguanidine and semicarbazide. Agricultural Biological Chemistry 55: 1435–1436Google Scholar
Hazelwood, R.L. (1986) Carbohydrate metabolism. In: Avian Physiology (Sturkie, P.D., Ed.), 4th Edition, Springer-Verlag, New York, pp. 303–325CrossRefGoogle Scholar
Hazelwood, R.L. and Lorenz, F. (1959) Effects of fasting and insulin on carbohydrate metabolism of the domestic fowl. American Journal of Physiology 197: 47–51CrossRefGoogle ScholarPubMed
Hellerstorm, C., Andersson, A., Sandler, S. and Swenne, I. (1986) Mechanisms of destruction and repair of the pancreatic β-cell. Transplant Proceedings 18: 1509–1512Google Scholar
Hellsten, Y., Tullson, P.C., Richter, E.A. and Bangsbo, J. (1997) Oxidation of urate in human skeletal muscle during exercise. Free Radical Biology and Medicine 22: 169–174CrossRefGoogle ScholarPubMed
Herrero, A. and Barja, G. (1998) H2O2, production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved. Mechanism of Aging and Development 103: 133–146CrossRefGoogle ScholarPubMed
Holmes, D. and Austad, S. (1995) Birds as animal models for the comparative biology of aging: a prospectus. Journal of Gerontology: Biological Science 50A: 859–866Google Scholar
Ikebe, S., Tanaka, M., Ohno, K., Sato, W., Hattori, K., Kondo, T., Mizuno, Y. and Ozawa, T. (1990) Increase of deleted mitochondrial DNA in the striatum in Parkinson's disease and senescence. Biochemistry Biophysics Research Communications 170: 1044–1048CrossRefGoogle ScholarPubMed
Iqbal, M., Probert, L.L. and Klandorf, H. (1997) Effect of dietary aminoguanidine on tissue pentosidine and reproductive performance in broiler breeder hens. Poultry Science 76: 1574–1579CrossRefGoogle ScholarPubMed
Iqbal, M., Probert, L.L., Al-Humadi, N.H. and Klandorf, H. (1999a) Protein glycosylationand advanced glycosylation end products (AGES): an avian solution. Journal of Gerontology: Biological Science 54A: B171–B176Google Scholar
Iqbal, M., Kenney, P. B. Al-Humadi, N.H. and Klandorf, H. (1999b) Relationship between mechanical properties and pentosidine in tendon: effect of age, diet restriction and aminoguanidine in broiler breeder hens. Journal of Gerontology: Biological Science (submitted for publication)CrossRefGoogle Scholar
James, V.J., Delbridge, L., Mclennan, S.V. and Yue, D.K. (1991) Use of X-ray diffraction in study of human diabetic and aging collagen. Diabetes 40: 391–394CrossRefGoogle ScholarPubMed
Junad, A., Lambert, A., Stauffacher, W. and Renold, A. (1969) Diabetogenic action of streptozotocin: relationship of dose to metabolic response. Journal of Clinical Investigation 48: 2129CrossRefGoogle Scholar
Kawada, J., Toide, J., Nishida, M., Yoshimura, Y. and Tsujihara, K. (1986) New diabetogenic streptozotocin analogue, 3-0-methyl-2{[(methylnitrosoamino)carbonyl[amino}- D-glucopyranose: evidence for a glucose recognition site on pancreatic β-cells. Diabetes 35: 74CrossRefGoogle ScholarPubMed
Kilo, C. Volger, N. and Williamson, J.R. (1972) Muscle capillary basement membrane charges related to aging and to diabetes mellitus. Diabetes 2: 881–905CrossRefGoogle Scholar
Klandorf, H., Holt, S., Mcgowan, J., Pinchasov, Y., Deyette, D. and Peterson, R. (1995) Hyperglycemia and non-enzymatic glycation of serum and tissue proteins in chickens. Comparative Biochemistry and Physiology 110C: 215–220Google Scholar
Klandorf, H., Zhou, Q. and Sams, A. R. (1996) Inhibition by aminoguanidine of glucose- derived collagen cross-linking in skeletal muscle of broiler breeder hens. Poulty Science 75: 432–437CrossRefGoogle ScholarPubMed
Kohn, R.R. and Schnider, S.L. (1982) Glycosylation of human collagen. Diabetes 31: 47–51CrossRefGoogle Scholar
Kristal, B. and Yu, B. (1992) An emerging hypothesis: synergistic induction of aging by free radicals and Maillard reactions. Journal of Gerontology: Biological Science 47: B107–B114CrossRefGoogle ScholarPubMed
Ku, H. and Sohal, R.S. (1993) Comparison of mitochondria1 prooxidant generation and antioxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential. Mechanism of Aging Development 72: 67–76CrossRefGoogle Scholar
Lindstedt, S. L. and Calde, W. A. (1976) Body size and longevity in birds. Condor 78: 91–94CrossRefGoogle Scholar
Masoro, E., Katz, M. and Mcmahan, C. (1989) Evidence for the glycation hypothesis of aging from the food-restricted rodent model. Journal of Gerontology: Biological Science 44: B820–B22CrossRefGoogle ScholarPubMed
Meadows, J., Smith, R.C. and Reeves, J. (1986) Uric acid protects membranes and linolenic acid from ozone-induced oxidation. Biochemistry Biophysics Research Communications 137: 536–541CrossRefGoogle ScholarPubMed
Merriwether, A.A., Clark, A.G., Ballinger, S.W., Schyrr, T.G., Soodyall, H., Jendkins, T., Sheny, T.T. and Wallace, D.C. (1991) The structure of human mitochondrial DNA variation. Journal of Molecular Evolution 33: 543–555CrossRefGoogle ScholarPubMed
Minaker, K.L. (1987) Aging and diabetes mellitus are risk factors for vascular disease. American Journal of Medicine 82 (Supplement 1B): 47–53CrossRefGoogle ScholarPubMed
Monnier, V., Glomb, M., Elgawish, A. and Sell, D. (1996) The mechanism of collagen crosslinking in diabetes: a puzzle nearing resolution. Diabetes 45: S67–S72CrossRefGoogle ScholarPubMed
Munscher, C., Rieger, T., Muller-HOCKER, J. and Kadenbach, B. (1993) The point mutation of mitochondria1 DNA characteristic for MERRF disease is found also in healthy people of different ages. Federation of Experimental Biology Societies Lucent 317: 27–30CrossRefGoogle Scholar
Nagaraj, R.H., Timothy, T.S., Sell, D.R., Forgarty, J., Engerman, R.L. and Monnier, V.M. (1996) Evidence of a glycemic threshold for the formation of pentosidine in diabetic dog lens but not in collagen. Diabetes 45: 587–594CrossRefGoogle ScholarPubMed
Nohal, H. and Hegner, D. (1990) Do mitochondria produce oxygen radicals in vivo? European Journal of Biochemistry 82: 563CrossRefGoogle Scholar
Odetti, P.R., Borgoflio, A.A., Pascale, D., Polandi, R. and Adezati, L. (1990) Prevention of diabetes-increased aging effect on rat collagen-linked fluorescence by aminoguanidine and rutin. Diabetes 39: 796–801CrossRefGoogle ScholarPubMed
Oxuland, H. and Andreassen, T. (1992) Aminoguanidine treatment reduces increase in collagen stability of rats with experimental diabetes mellitus. Diabetologia 35a: 19–25CrossRefGoogle Scholar
Parmley, L., Mufti, A.G. and Downey, J.M. (1992) Allopurinol therapy of ischemic heart disease with infarct extension. Canadian Journal of Cardiology 8: 280–286Google ScholarPubMed
Pierrefiche, G. and Laborit, H. (1995) Oxygen free radicals, melatonin, and aging. Experimental Gerontology 30: 213–227CrossRefGoogle ScholarPubMed
Pillsbury, H.C., Hung, W., Kyle, M.C. and Freis, E.D. (1974) Arterial pulse wave velocity and systolic time intervals in diabetic children. American Heart Journal 87: 783–790CrossRefGoogle Scholar
Rammamurthy, N.S., Zebrowski, E.J. and Golub, L.M. (1972) The effects of alloxan diabetes on gingival collagen metabolism in rats. Archive of Oral Biology 17: 1551–1560CrossRefGoogle Scholar
Reagan, T.J., Lyons, M.M., Ahmed, S.S., Levinson, G.E., Oldewurtel, H.A., Ahmed, M.R. and Haider, B. (1977) Evidence for cardiomyopathy in familial diabetes mellitus. Journal of Clinical Investigation 60: 885–899CrossRefGoogle Scholar
Reiser, K. M. (1991) Nonenzymatic glycation of collagen in aging and diabetes. Proceedings of the Society of Experimental Biology and Medicine 196: 17–29CrossRefGoogle ScholarPubMed
Reiser, K. M. (1994) Influence of age and long-term dietarv restriction on enzvmaticallv mediated crosslinks and nonenzymatic glyckon of coGagen in mice. Journal of Gerontolgy: Biological Science 49: B71–B79CrossRefGoogle Scholar
Rendell, M., Stephen, P.M., Paulsen, R., Valentine, J.L., Rasbold, K.,Hestorff, T., Eastberg, S. and Shint, D. (1985) An interspecies comparison of normal levels of glycosylated hemoglobin and glycosylated albumin. Comparative Biochemistry and Physiology 81B: 819–822Google Scholar
Robinson, W.G., Kador, P.F. and Kinoshita, J.H. (1983) Retinal capillaries: basement membrane thickening by galactosemia prevented with aldose reductase inhibitor. Science 221: 1177–1179CrossRefGoogle Scholar
Rosenthal, M. and Olenick, L.J. (1988) Evaluation of a single color reading method for determining fructosamine. Clinical Chemistry 34: 360–363CrossRefGoogle ScholarPubMed
Rossini, A.A. and Dubin, W.E. (1976) Studies of streptozotocin anomers on pancreatic beta cell toxicity. Diabetes 35: 384Google Scholar
Scheynius, A. and Taljedal, I.B. (1971) On the mechanism of glucose protection against alloxan toxicity. Diabetologia 7: 252–255CrossRefGoogle ScholarPubMed
Schnider, S.L. and Kohn, R.R. (1982) Effects of age and diabetes mellitus on the solubility of collagen from human skin, tracheal cartilage and dura mater. Experimental Gerontology 17: 185–194CrossRefGoogle ScholarPubMed
Schwler, M.R., Niewohner, D., Inkley, S.R. and Kohn, R.R. (1976) Abnormal lung elasticity in juvenile diabetes mellitus. American Review of Respiratory Diseases 13: 37–41Google Scholar
Schweiger, F.F., Uehlein-HARRELL, S., Von Hegel, G. and Wiesner, H. (1991) Vitamin A (retinol and retinyl esters), α-tocopherol and lipid levels in plasma of captive wild mammals and birds. Xentralblatt fur Veterinarmedizin-Reihe A38: 35–42CrossRefGoogle Scholar
Sell, D.R. and Monnier, V.M. (1989) Structure elucidation of a senescence cross-link from human extracellular matrix: Impiication of pentoses in the aging process. Journal of Biological Chemisty 264: 21597–21602CrossRefGoogle ScholarPubMed
Sell, D.R., Lapolla, A., Odetti, P., Forgarty, J. and Monnier, V.M. (1992) Pentosidine formation in skin correlates with severity of complications in individuals with long-standing IDDM. Diabetes 41: 1286–1291CrossRefGoogle ScholarPubMed
Sevanian, A., Davies, K.J.A. and Hochstein, P. (1991) Serum urate as an antioxidant for ascorbic acid. American Journal of Clinical Nutrition 54: 1129S–1143SCrossRefGoogle ScholarPubMed
Shapiro, F., Mahagna, M. and Nir, I. (1997) Stunting syndrome in broilers: effect of glucose or maltose supplementation on digestive organs, intestinal disaccharidases, and some blood metabolites. Poulty Science 76: 369–380CrossRefGoogle ScholarPubMed
Short, R., Williams, D.D. and Bowden, D.M. (1997) Circulating antioxidants as determinants of the rate of biological aging in pigtailed macaques (Macaca nemestrina). Journal of Gerontology: Biological Science 52A: B26–B30Google Scholar
Simon, H. and Dubois, M.P. (1980) Failure of a sublethal streptozotocin dose to induce diabetes in the chicken. Hormone Metabolism Research 12: 631–632CrossRefGoogle ScholarPubMed
Souza, A.V.G., Petretski, J.H., Demasi, M., Bechara, E.J.H. and Oliveira, P.L. (1996) Urate protects a blood-sucking insect against hemin-induced oxidative stress. Free Radical Biology and Medicine 22: 209–214CrossRefGoogle Scholar
Stellenwerf, W.A. and Hazelwood, R.L. (1979) Peripheral utilization of a glucose load after alloxan and streptozotocin in the rat and chicken: a comparison. General Comparative Endocrinology 39: 131–140CrossRefGoogle ScholarPubMed
Velasquez, M.T., Kimmel, P.L. and Michaelis, O.E. (1990) Animal models of spontaneously diabetic kidney disease. Federation of American Societies for Experimental Biology Journal 4: 2850–2859CrossRefGoogle ScholarPubMed
Wei, Y.H. (1992) Mitochondria1 DNA alterations as ageing-associated molecular events. Mutation Research 275: 145–155CrossRefGoogle Scholar
Wei, Y.H. (1998) Oxidative stress and mitochondrial DNA mutations in human aging. Experimental Biology and Medicine 127: 53–63CrossRefGoogle Scholar
Wu, J. (1993) Advanced glycosylation end products: a new disease marker for diabetes and aging. Journal of Clinical Laboratory Animals 7: 252–255CrossRefGoogle Scholar
Wu, J. (1995) Nitric oxide synthesis and effect of aminoguanidine and N-monomethyl-L-arginine on the onset of diabetes in spontaneously diabetic BB rats. Diabetes 44: 364–365CrossRefGoogle Scholar
Yagihashi, S., Kamigo, M., Babal, M., Yahishi, N. and Nagai, N. (1992) Effect of aminoguanidine on functional and structural abnormalities in peripheral nerve of STZ-induced diabetic rats. Diabetes 41: 47–52CrossRefGoogle ScholarPubMed
Yen, T.C., Su, H., King, K.L. and Wei, Y.G. (1991) Ageing-associated 5-kb deletion in human liver mitochondrial DNA. Biochemistry Biophysics Research Communications 178: 124–131CrossRefGoogle Scholar
Yosla, S.F., Elden, F.R., Rabionoveitch, A., Mintz, D.H. and Boueckm, J. (1983) Experimental diabetes mellitus and age-stimulated changes in intact rat dermal collagen. Diabetes 32: 739–742Google Scholar
Yu, B.P. (1993) Oxidative damage by free radicals and lipid peroxidation in aging. In: Free Radicals in Aging (Yu, B.P., Ed.), CRC Press, Boca Raton, FL, pp. 57–88Google Scholar
Yue, D.K., Mclennan, S., Delbridge, L., Handlesman, D.J., Reeve, T. and Turtle, J.R. (1983) The thermal stability of collagen in diabetic rats: correlation with severity of diabetes and nonenzymatic glycosylation. Diabetologia 24: 282–285CrossRefGoogle Scholar