Biomolecule Damage (DNA and Lipid) is Elevated in Patients with Type 1 Diabetes with and without Diabetic Complications
DOI:
https://doi.org/10.6000/1929-5634.2014.03.02.8Keywords:
DNA damage, Type 1 Diabetes, Lipid damage, Glycaemic control, oxidative stress.Abstract
There is strong evidence that oxidative stress is involved in the aetiology and pathogenesis of diabetes and its complications. Increased production of reactive oxygen species in vivo can lead to cellular biomolecule damage, such as lipid peroxidation and DNA damage.
The aim of this study was to determine the extent of this damage by measuring in vivo antioxidant status, levels of lipid peroxidation, and levels of neutrophil DNA damage in 50 participants with type 1 diabetes and 50 age- and sex-matched, healthy controls.
Gylcaemic control (%HbA1c) was relatively good with a group mean of 7.71% which increased to 8.12 % in those with complications. Compared to the control group there were significantly elevated levels of neutrophil DNA damage (% tail DNA, p<0.0001) and plasma MDA levels (p<0.05) in the Type 1 group as a whole, this significance rose to p<0.01 in those with complications. There were significant alterations in markers of antioxidant status including, reduced levels of superoxide dismutase (p<0.0001), uric acid (p<0.05) and Vitamin C (p<0.05) and elevated levels of catalase (p<0.001).
These results indicate that even with acceptable glycaemic control significant oxidative damage still occurs and this damage increases, in some indices, with the onset of complications.
References
[1] Kaneto H, Katakami N, Kawamori D, Miyatsuka T, Sakamoto K, Matsuoka TA, Matsuhisa M, Yamasaki Y. Involvement of oxidative stress in the pathogenesis of diabetes. Antioxid Redox Signal 2007; 9(3): 355-66.
http://dx.doi.org/10.1089/ars.2006.1465
[2] Giacco F, Brownlee M. Oxidative stress and diabetic complications Circ Res 2010; 107(9): 1058-70.
http://dx.doi.org/10.1161/CIRCRESAHA.110.223545
[3] Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: A summary of a Congress Series sponsored by UNESCO MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 2001; 17: 189-912.
http://dx.doi.org/10.1002/dmrr.196
[4] VanderJagt DJ, Harrison JM, Ratliff DM, Hunsaker LA, Vander Jagt DL. Oxidative stress indices in IDDM subjects with and without long-term diabetic complications. Clin Biochem 2001; 34(4): 265-70.
http://dx.doi.org/10.1016/S0009-9120(01)00204-1
[5] Maxwell SR, Thomason H, Sandler D, Leguen C, Baxter MA, Thorpe GH, Jones AF, Barnett, AH. Antioxidant status in patients with uncomplicated insulin-dependent and non-insulin-dependent diabetes mellitus. Eur J Clin Invest 1997; 27(6): 484-490.
http://dx.doi.org/10.1046/j.1365-2362.1997.1390687.x
[6] Wierusz-Wysocka B, Wykretowicz A, Byks H, Sadurska K, Wysocki H. Polymorphonuclear neutrophils adherence, superoxide anion (02-) production and HBA1 level in diabetic patients. Diabetes Res Clin Prac 1993; 21: 109-114.
http://dx.doi.org/10.1016/0168-8227(93)90057-C
[7] Zozulinska DA, Wierusz-Wysocka B, Wysocki H, Majchrzak AE, Wykretowicz A. The influence of insulin-dependent diabetes mellitus (IDDM) duration on superoxide anion and hydrogen peroxide production by polymorphonuclear neutrophils. Diabetes Res Clin Prac 1996; 33: 139-144.
http://dx.doi.org/10.1016/0168-8227(96)01289-2
[8] Ruiz C, Alegría A, Barberá R, Farré R, Lagarda MJ. Lipid peroxidation and antioxidant enzyme activities in patients with type 1 diabetes mellitus. Scand J Clin Lab Invest 1999, 59(2): 99-105.
http://dx.doi.org/10.1080/00365519950185823
[9] Sato Y, Hotta N, Sakamoto N, Matsuoka S, Ohishi N, Yagi, K. Lipid peroxide levels in plasma of diabetic patients. Biochem Med 1979; 21: 104-107.
http://dx.doi.org/10.1016/0006-2944(79)90061-9
[10] Matough FA, Budin SB, Hamid ZA, Alwahaibi N, Mohamed J. The role of oxidative stress and antioxidants in diabetic complications. Sultan Qaboos Univ Med J 2012; 12(1): 5-18.
[11] Biasi F, Vizio B, Mascia C, Gaia E, Zarkovic N, Chiarpotto E, Leonarduzzi G, Poli G. c-Jun N-terminal kinase upregulation as a key event in the proapoptotic interaction between transforming growth factor-beta1 and 4-hydroxynonenal in colon mucosa. Free Radic Biol Med 2006; 41(3): 443-54.
http://dx.doi.org/10.1016/j.freeradbiomed.2006.04.005
[12] Minko IG, Kozekov ID, Harris TM, Rizzo CJ, Lloyd RS, Stone MP Review Chemistry and biology of DNA containing 1,N(2)-deoxyguanosine adducts of the alpha,beta-unsaturated aldehydes acrolein, crotonaldehyde, and 4-hydroxynonenal. Chem Res Toxicol 2009; 22(5): 759-78.
http://dx.doi.org/10.1021/tx9000489
[13] Jaganjac M1, Cacev T, Cipak A, Kapitanovi? S, Gall Troselj K, Zarkovi? N. Even stressed cells are individuals: second messengers of free radicals in pathophysiology of cancer. Croat Med J 2012; 53(4): 304-9.
http://dx.doi.org/10.3325/cmj.2012.53.304
[14] Hannon-Fletcher MPA, Hughes C, Moles KW, Barnett CR, Barnett YA. An investigation of in vivo antioxidant status and DNA damage in patients with IDDM. In Basu TK, Temple NJ, Garg ML editors. Antioxidants in Human Health: Oxford: CABI Publishing, 1999; p259-269.
[15] Dandona P, Thusu K, Cook S, Snyder B, Makowski J, Armstrong D, Nicotera T. Oxidative damage to DNA in diabetes mellitus. Lancet 1996; 347: 444-445.
http://dx.doi.org/10.1016/S0140-6736(96)90013-6
[16] Collins AR, Raslová K, Somorovská M, Petrovská H, Ondrusová A, Vohnout B, Fábry R, Dusinská M. DNA
damage in diabetes: correlation with a clinical marker. Free Radic Biol Med 1998; 25(3): 373-7.
http://dx.doi.org/10.1016/S0891-5849(98)00053-7
[17] Lorenzi M, Montisano DF, Toledo S, Wong HC. Increased single strand breaks in DNA of lymphocytes from diabetic subjects. J Clin Invest 1897; 79: 653-656.
http://dx.doi.org/10.1172/JCI112863
[18] Anderson D, Yu TW, Wright J, Ioannides C. An examination of DNA strand breakage in the Comet Assay and antioxidant capacity in diabetic patients. Mutation Res 1998; 398: 151-161.
http://dx.doi.org/10.1016/S0027-5107(97)00271-6
[19] Böyum A. Isolation of mononuclear cells and granulocytes from human blood, in: Norwegian Defence Research establishment Division for Toxicology Kjeller Norway. 1980, Paper iv: pp. 77-89.
[20] Markert M, Particia CA, Babior BM. Measurement of O2- production by human neutrophils. The preparation and assay of NADPH oxidised containing particles from human neutrophils, Method. Enzymol 1984; 105: 358-362.
http://dx.doi.org/10.1016/S0076-6879(84)05048-5
[21] Allain CC, Poon LS, Chan CS, Richmond W, Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem 1974; 20(4): 470-475.
[22] Tietz NW. Specimen collection and processing; sources of biological variation. In Saunders W, editors. Textbook of Clinical Chemistry, 2nd ed. Philadelphia: 1994.
[23] Public Health Service Centers for Disease Control. A proposed method for determining glucose using hexokinase and glucose-6-phosphatase dehydrogenase. In Public Health Service, Centers for Disease Control 1976.
[24] John WG, Bullock DG, MacKenzie F. Methods for the analysis of glycated haemoglobins: what is being measured? Diabetic Med 1992; 9: 15-19.
http://dx.doi.org/10.1111/j.1464-5491.1992.tb01708.x
[25] Vuilleumier JP, Keck E. Flurometric assay of vitamin C in biological materials using a centrifugal analyser with fluorescence attachment. J Micronutr Anal 1989; 5: 25-34.
[26] Thurnham DI, Smith E, Flora PS. Concurrent liquid-chromatographic assay of retinol, ?-tocopherol, ?-carotene, ?-carotene, lycopene, and ?-cryptoxanthin in plasma, with tocopherol acetate as internal standard. Clin Chem 1988; 30(2): 377-381.
[27] Aebi HE. Catalase. Methods in Enzymatic Analysis 1974; 2: 121-126.
[28] Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70(1): 158-169.
[29] Jones DG, Suttle NF. Some effects of copper deficiency on leucocyte function in sheep and cattle. Res Vet Sci 1981; 31: 151-156.
[30] Fossati P, Prencipe L, Berti G. Use of 3,5-dichloro-2-hydroxybenzenesulfonic acid, 4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. Clin Chem 1980; 22(2): 227-231.
[31] Singh NP, McCoy MT, Trice RR, Schneider EL. A simple technique for quantification of low levels of DNA damage in individual cells. Exp Cell Res 1988; 175: 184-194.
http://dx.doi.org/10.1016/0014-4827(88)90265-0
[32] McKelvey-Martin VJ, Ho ET, McKeown SR, Johnston SR, McCarthy PJ, Rajab NF, Downes CS. Emerging applications of the single cell gel electrophoresis (Comet) assay. I. Management of invasive transitional cell human bladder carcinoma. II. Fluorescent in situ hybridization Comets for the identification of damaged and repaired DNA sequences in individual cells. Mutagenesis 1998; 13(1): 1-8.
http://dx.doi.org/10.1093/mutage/13.1.1
[33] Young IS, Trimble ER. Measurement of malondialdehyde in plasma by high performance liquid chromatography with fluorimetric detection. Ann Clin Biochem 1991; 28: 504-508.
http://dx.doi.org/10.1177/000456329102800514
[34] Kawamura N, Ookawara T, Suzuki K, Konoshi K, Mino M, Taniguchi N. Increased glycated Cu,Zn-superoxide dismutase levels in erythrocytes of patients with insulin-dependent diabetes mellitus. J Clin Endocrin Metab 1992; 74(6): 1352-1354.
[35] Olczyk K, Koscielniak-Kocurek E, Sonecki P, Zdenkowski W. The lipid peroxidation products and the enzymes of antioxidant system in patients with diabetes mellitus. Rocz Akad Med Bialymstoku 1994; 39: 93-99.
[36] Wolff SP. Diabetes mellitus and free radicals: free radicals, transition metals and oxidative stress in the aetiology of diabetes mellitus and complications. Br Med Bull 1993; 49: 642.
[37] Hägglöf B, Marklund SL, Holmgreen G. CuZn superoxide dismutase, Mn superoxide dismutase, catalase and glutathione peroxidase in lymphocytes and erythrocytes in insulin-dependent diabetic children. Acta Endocrinol 1983; 102: 235-239.
[38] Mann GV. Hypothesis: the role of vitamin C in diabetic angiopathy. Perspect Biol Med 1974; 210-217.
[39] Cunningham JJ. Altered vitamin C transport in diabetes mellitus. Med Hypotheses 1988; 26: 263-265.
http://dx.doi.org/10.1016/0306-9877(88)90131-4
[40] Cunningham JJ, Ellis SL, McVeigh KL, Levine RE, Calles-Escandon J. Reduced mononuclear leukocyte ascorbic acid content in adults with insulin-dependent diabetes mellitus consuming adequate dietary vitamin C. Metabolism 1991; 40(2): 146-149.
http://dx.doi.org/10.1016/0026-0495(91)90165-S
[41] Bode AM, Yavarow CR, Fry DA, Vargas T. Enzymatic basis for altered ascorbic acid and dehydroascorbic acid levels in diabetes. Biochem Biophys Res Commun 1993; 191(3): 1347-1353.
http://dx.doi.org/10.1006/bbrc.1993.1365
[42] Stankova L, Riddle M, Larned J, Burry K, Menashe D, Hart J, Bigley R. Plasma ascorbate concentrations and blood cell dehydroascorbate transport in patients with diabetes melltus. Metabolism 1984; 33(4): 347-353.
http://dx.doi.org/10.1016/0026-0495(84)90197-5
[43] The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993; 329(14): 977-986.
http://dx.doi.org/10.1056/NEJM199309303291401
[44] Ceriello A, Giugliano D, Quatraro A, Donzella C, Dipalo G, Lefebvre PJ. Vitamin E reduction of protein glycosylation in diabetes. Diabetes Care 1991; 14(1): 68-72.
http://dx.doi.org/10.2337/diacare.14.1.68
[45] Nishigaki I, Hagihara M, Tsunekawa H, Maseki M, Yagi K. Lipid peroxide levels of serum lipoprotein fractions of diabetic patients. Biochem Med 1981; 25: 373-378.
http://dx.doi.org/10.1016/0006-2944(81)90096-X
[46] Gallou G, Ruelland A, Legras B, Maugendre D, Allanic H, Cloarec L. Plasma malondialdehyde in type 1 and type 2 diabetic patients. Clinica Chim Acta 1993; 214: 227-234.
http://dx.doi.org/10.1016/0009-8981(93)90114-J
[47] Rimm EB, Stampfer MJ, Ascherio A, Giovannucci E, Colditz GA, Willett WC. Vitamin E consumption and the risk of coronary heart disease in men. N Engl J Med 1993; 322(20): 1450-1456.
http://dx.doi.org/10.1056/NEJM199305203282004
[48] Hannon-Fletcher MP, O'Kane MJ, Moles KW, Weatherup C, Barnett CR, Barnett YA. Levels of peripheral blood cell DNA damage in insulin dependent diabetes mellitus human subjects. Mutat Res 2000; 460(1): 53-60.
http://dx.doi.org/10.1016/S0921-8777(00)00013-6
[49] Collins AR1, Raslová K, Somorovská M, Petrovská H, Ondrusová A, Vohnout B, Fábry R, Dusinská M. DNA damage in diabetes: correlation with a clinical marker. Free Radic Biol Med 1998; 25(3): 373-7.
http://dx.doi.org/10.1016/S0891-5849(98)00053-7
[50] Lorenzi M, Montisano DF, Toledo S, Wong HC. Increased single strand breaks in DNA of lymphocytes from diabetic subjects, J Clin Invest 1987; 79: 653-656.
http://dx.doi.org/10.1172/JCI112863
[51] Dinçer Y, Akçay T, Ilkova H, Alademir Z, Ozbay G. DNA damage and antioxidant defense in peripheral leukocytes of patients with Type I diabetes mellitus. Mutat Res 2003; 527(1-2): 49-55.
http://dx.doi.org/10.1016/S0027-5107(03)00073-3
[52] Esman V. The polymorphonuclear leucocyte in diabetes, Fresen J Anal Chem 1982; 311: 344-348.
http://dx.doi.org/10.1007/BF00481709
[53] Weitzman SA, Gordon LI. Inflammation and cancer: Role of phagocyte-generated oxidants in carcinogenesis. Blood 1990; 76: 655-663.
[54] Ogino T, Packer L, Maguire JJ. Neutrophil antioxidant capacity during the respiratory burst: loss of glutathione induced by chloramines. Free Radical Biol Med 1997; 23: 445-452.
http://dx.doi.org/10.1016/S0891-5849(97)00115-9
http://dx.doi.org/10.1089/ars.2006.1465
[2] Giacco F, Brownlee M. Oxidative stress and diabetic complications Circ Res 2010; 107(9): 1058-70.
http://dx.doi.org/10.1161/CIRCRESAHA.110.223545
[3] Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: A summary of a Congress Series sponsored by UNESCO MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 2001; 17: 189-912.
http://dx.doi.org/10.1002/dmrr.196
[4] VanderJagt DJ, Harrison JM, Ratliff DM, Hunsaker LA, Vander Jagt DL. Oxidative stress indices in IDDM subjects with and without long-term diabetic complications. Clin Biochem 2001; 34(4): 265-70.
http://dx.doi.org/10.1016/S0009-9120(01)00204-1
[5] Maxwell SR, Thomason H, Sandler D, Leguen C, Baxter MA, Thorpe GH, Jones AF, Barnett, AH. Antioxidant status in patients with uncomplicated insulin-dependent and non-insulin-dependent diabetes mellitus. Eur J Clin Invest 1997; 27(6): 484-490.
http://dx.doi.org/10.1046/j.1365-2362.1997.1390687.x
[6] Wierusz-Wysocka B, Wykretowicz A, Byks H, Sadurska K, Wysocki H. Polymorphonuclear neutrophils adherence, superoxide anion (02-) production and HBA1 level in diabetic patients. Diabetes Res Clin Prac 1993; 21: 109-114.
http://dx.doi.org/10.1016/0168-8227(93)90057-C
[7] Zozulinska DA, Wierusz-Wysocka B, Wysocki H, Majchrzak AE, Wykretowicz A. The influence of insulin-dependent diabetes mellitus (IDDM) duration on superoxide anion and hydrogen peroxide production by polymorphonuclear neutrophils. Diabetes Res Clin Prac 1996; 33: 139-144.
http://dx.doi.org/10.1016/0168-8227(96)01289-2
[8] Ruiz C, Alegría A, Barberá R, Farré R, Lagarda MJ. Lipid peroxidation and antioxidant enzyme activities in patients with type 1 diabetes mellitus. Scand J Clin Lab Invest 1999, 59(2): 99-105.
http://dx.doi.org/10.1080/00365519950185823
[9] Sato Y, Hotta N, Sakamoto N, Matsuoka S, Ohishi N, Yagi, K. Lipid peroxide levels in plasma of diabetic patients. Biochem Med 1979; 21: 104-107.
http://dx.doi.org/10.1016/0006-2944(79)90061-9
[10] Matough FA, Budin SB, Hamid ZA, Alwahaibi N, Mohamed J. The role of oxidative stress and antioxidants in diabetic complications. Sultan Qaboos Univ Med J 2012; 12(1): 5-18.
[11] Biasi F, Vizio B, Mascia C, Gaia E, Zarkovic N, Chiarpotto E, Leonarduzzi G, Poli G. c-Jun N-terminal kinase upregulation as a key event in the proapoptotic interaction between transforming growth factor-beta1 and 4-hydroxynonenal in colon mucosa. Free Radic Biol Med 2006; 41(3): 443-54.
http://dx.doi.org/10.1016/j.freeradbiomed.2006.04.005
[12] Minko IG, Kozekov ID, Harris TM, Rizzo CJ, Lloyd RS, Stone MP Review Chemistry and biology of DNA containing 1,N(2)-deoxyguanosine adducts of the alpha,beta-unsaturated aldehydes acrolein, crotonaldehyde, and 4-hydroxynonenal. Chem Res Toxicol 2009; 22(5): 759-78.
http://dx.doi.org/10.1021/tx9000489
[13] Jaganjac M1, Cacev T, Cipak A, Kapitanovi? S, Gall Troselj K, Zarkovi? N. Even stressed cells are individuals: second messengers of free radicals in pathophysiology of cancer. Croat Med J 2012; 53(4): 304-9.
http://dx.doi.org/10.3325/cmj.2012.53.304
[14] Hannon-Fletcher MPA, Hughes C, Moles KW, Barnett CR, Barnett YA. An investigation of in vivo antioxidant status and DNA damage in patients with IDDM. In Basu TK, Temple NJ, Garg ML editors. Antioxidants in Human Health: Oxford: CABI Publishing, 1999; p259-269.
[15] Dandona P, Thusu K, Cook S, Snyder B, Makowski J, Armstrong D, Nicotera T. Oxidative damage to DNA in diabetes mellitus. Lancet 1996; 347: 444-445.
http://dx.doi.org/10.1016/S0140-6736(96)90013-6
[16] Collins AR, Raslová K, Somorovská M, Petrovská H, Ondrusová A, Vohnout B, Fábry R, Dusinská M. DNA
damage in diabetes: correlation with a clinical marker. Free Radic Biol Med 1998; 25(3): 373-7.
http://dx.doi.org/10.1016/S0891-5849(98)00053-7
[17] Lorenzi M, Montisano DF, Toledo S, Wong HC. Increased single strand breaks in DNA of lymphocytes from diabetic subjects. J Clin Invest 1897; 79: 653-656.
http://dx.doi.org/10.1172/JCI112863
[18] Anderson D, Yu TW, Wright J, Ioannides C. An examination of DNA strand breakage in the Comet Assay and antioxidant capacity in diabetic patients. Mutation Res 1998; 398: 151-161.
http://dx.doi.org/10.1016/S0027-5107(97)00271-6
[19] Böyum A. Isolation of mononuclear cells and granulocytes from human blood, in: Norwegian Defence Research establishment Division for Toxicology Kjeller Norway. 1980, Paper iv: pp. 77-89.
[20] Markert M, Particia CA, Babior BM. Measurement of O2- production by human neutrophils. The preparation and assay of NADPH oxidised containing particles from human neutrophils, Method. Enzymol 1984; 105: 358-362.
http://dx.doi.org/10.1016/S0076-6879(84)05048-5
[21] Allain CC, Poon LS, Chan CS, Richmond W, Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem 1974; 20(4): 470-475.
[22] Tietz NW. Specimen collection and processing; sources of biological variation. In Saunders W, editors. Textbook of Clinical Chemistry, 2nd ed. Philadelphia: 1994.
[23] Public Health Service Centers for Disease Control. A proposed method for determining glucose using hexokinase and glucose-6-phosphatase dehydrogenase. In Public Health Service, Centers for Disease Control 1976.
[24] John WG, Bullock DG, MacKenzie F. Methods for the analysis of glycated haemoglobins: what is being measured? Diabetic Med 1992; 9: 15-19.
http://dx.doi.org/10.1111/j.1464-5491.1992.tb01708.x
[25] Vuilleumier JP, Keck E. Flurometric assay of vitamin C in biological materials using a centrifugal analyser with fluorescence attachment. J Micronutr Anal 1989; 5: 25-34.
[26] Thurnham DI, Smith E, Flora PS. Concurrent liquid-chromatographic assay of retinol, ?-tocopherol, ?-carotene, ?-carotene, lycopene, and ?-cryptoxanthin in plasma, with tocopherol acetate as internal standard. Clin Chem 1988; 30(2): 377-381.
[27] Aebi HE. Catalase. Methods in Enzymatic Analysis 1974; 2: 121-126.
[28] Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70(1): 158-169.
[29] Jones DG, Suttle NF. Some effects of copper deficiency on leucocyte function in sheep and cattle. Res Vet Sci 1981; 31: 151-156.
[30] Fossati P, Prencipe L, Berti G. Use of 3,5-dichloro-2-hydroxybenzenesulfonic acid, 4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. Clin Chem 1980; 22(2): 227-231.
[31] Singh NP, McCoy MT, Trice RR, Schneider EL. A simple technique for quantification of low levels of DNA damage in individual cells. Exp Cell Res 1988; 175: 184-194.
http://dx.doi.org/10.1016/0014-4827(88)90265-0
[32] McKelvey-Martin VJ, Ho ET, McKeown SR, Johnston SR, McCarthy PJ, Rajab NF, Downes CS. Emerging applications of the single cell gel electrophoresis (Comet) assay. I. Management of invasive transitional cell human bladder carcinoma. II. Fluorescent in situ hybridization Comets for the identification of damaged and repaired DNA sequences in individual cells. Mutagenesis 1998; 13(1): 1-8.
http://dx.doi.org/10.1093/mutage/13.1.1
[33] Young IS, Trimble ER. Measurement of malondialdehyde in plasma by high performance liquid chromatography with fluorimetric detection. Ann Clin Biochem 1991; 28: 504-508.
http://dx.doi.org/10.1177/000456329102800514
[34] Kawamura N, Ookawara T, Suzuki K, Konoshi K, Mino M, Taniguchi N. Increased glycated Cu,Zn-superoxide dismutase levels in erythrocytes of patients with insulin-dependent diabetes mellitus. J Clin Endocrin Metab 1992; 74(6): 1352-1354.
[35] Olczyk K, Koscielniak-Kocurek E, Sonecki P, Zdenkowski W. The lipid peroxidation products and the enzymes of antioxidant system in patients with diabetes mellitus. Rocz Akad Med Bialymstoku 1994; 39: 93-99.
[36] Wolff SP. Diabetes mellitus and free radicals: free radicals, transition metals and oxidative stress in the aetiology of diabetes mellitus and complications. Br Med Bull 1993; 49: 642.
[37] Hägglöf B, Marklund SL, Holmgreen G. CuZn superoxide dismutase, Mn superoxide dismutase, catalase and glutathione peroxidase in lymphocytes and erythrocytes in insulin-dependent diabetic children. Acta Endocrinol 1983; 102: 235-239.
[38] Mann GV. Hypothesis: the role of vitamin C in diabetic angiopathy. Perspect Biol Med 1974; 210-217.
[39] Cunningham JJ. Altered vitamin C transport in diabetes mellitus. Med Hypotheses 1988; 26: 263-265.
http://dx.doi.org/10.1016/0306-9877(88)90131-4
[40] Cunningham JJ, Ellis SL, McVeigh KL, Levine RE, Calles-Escandon J. Reduced mononuclear leukocyte ascorbic acid content in adults with insulin-dependent diabetes mellitus consuming adequate dietary vitamin C. Metabolism 1991; 40(2): 146-149.
http://dx.doi.org/10.1016/0026-0495(91)90165-S
[41] Bode AM, Yavarow CR, Fry DA, Vargas T. Enzymatic basis for altered ascorbic acid and dehydroascorbic acid levels in diabetes. Biochem Biophys Res Commun 1993; 191(3): 1347-1353.
http://dx.doi.org/10.1006/bbrc.1993.1365
[42] Stankova L, Riddle M, Larned J, Burry K, Menashe D, Hart J, Bigley R. Plasma ascorbate concentrations and blood cell dehydroascorbate transport in patients with diabetes melltus. Metabolism 1984; 33(4): 347-353.
http://dx.doi.org/10.1016/0026-0495(84)90197-5
[43] The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993; 329(14): 977-986.
http://dx.doi.org/10.1056/NEJM199309303291401
[44] Ceriello A, Giugliano D, Quatraro A, Donzella C, Dipalo G, Lefebvre PJ. Vitamin E reduction of protein glycosylation in diabetes. Diabetes Care 1991; 14(1): 68-72.
http://dx.doi.org/10.2337/diacare.14.1.68
[45] Nishigaki I, Hagihara M, Tsunekawa H, Maseki M, Yagi K. Lipid peroxide levels of serum lipoprotein fractions of diabetic patients. Biochem Med 1981; 25: 373-378.
http://dx.doi.org/10.1016/0006-2944(81)90096-X
[46] Gallou G, Ruelland A, Legras B, Maugendre D, Allanic H, Cloarec L. Plasma malondialdehyde in type 1 and type 2 diabetic patients. Clinica Chim Acta 1993; 214: 227-234.
http://dx.doi.org/10.1016/0009-8981(93)90114-J
[47] Rimm EB, Stampfer MJ, Ascherio A, Giovannucci E, Colditz GA, Willett WC. Vitamin E consumption and the risk of coronary heart disease in men. N Engl J Med 1993; 322(20): 1450-1456.
http://dx.doi.org/10.1056/NEJM199305203282004
[48] Hannon-Fletcher MP, O'Kane MJ, Moles KW, Weatherup C, Barnett CR, Barnett YA. Levels of peripheral blood cell DNA damage in insulin dependent diabetes mellitus human subjects. Mutat Res 2000; 460(1): 53-60.
http://dx.doi.org/10.1016/S0921-8777(00)00013-6
[49] Collins AR1, Raslová K, Somorovská M, Petrovská H, Ondrusová A, Vohnout B, Fábry R, Dusinská M. DNA damage in diabetes: correlation with a clinical marker. Free Radic Biol Med 1998; 25(3): 373-7.
http://dx.doi.org/10.1016/S0891-5849(98)00053-7
[50] Lorenzi M, Montisano DF, Toledo S, Wong HC. Increased single strand breaks in DNA of lymphocytes from diabetic subjects, J Clin Invest 1987; 79: 653-656.
http://dx.doi.org/10.1172/JCI112863
[51] Dinçer Y, Akçay T, Ilkova H, Alademir Z, Ozbay G. DNA damage and antioxidant defense in peripheral leukocytes of patients with Type I diabetes mellitus. Mutat Res 2003; 527(1-2): 49-55.
http://dx.doi.org/10.1016/S0027-5107(03)00073-3
[52] Esman V. The polymorphonuclear leucocyte in diabetes, Fresen J Anal Chem 1982; 311: 344-348.
http://dx.doi.org/10.1007/BF00481709
[53] Weitzman SA, Gordon LI. Inflammation and cancer: Role of phagocyte-generated oxidants in carcinogenesis. Blood 1990; 76: 655-663.
[54] Ogino T, Packer L, Maguire JJ. Neutrophil antioxidant capacity during the respiratory burst: loss of glutathione induced by chloramines. Free Radical Biol Med 1997; 23: 445-452.
http://dx.doi.org/10.1016/S0891-5849(97)00115-9
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2014-06-16
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Hannon-Fletcher, M. P., Weatherup, C., O’Kane, M. J., Moles, K. W., & Barnett, Y. A. (2014). Biomolecule Damage (DNA and Lipid) is Elevated in Patients with Type 1 Diabetes with and without Diabetic Complications. Journal of Nutritional Therapeutics, 3(2), 95–102. https://doi.org/10.6000/1929-5634.2014.03.02.8
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