机体氧化/抗氧化状态与系统性红斑狼疮临床指标的相关性研究
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摘要
目的探讨系统性红斑狼疮(systemic lupus erythematosus, SLE)患者脂质过氧化、蛋白质氧化损伤程度以及氧化/抗氧化作用与临床疾病活动指标以及病程进展中组织和器官慢性损伤的关联性。
方法病例选用安徽医科大学附属医院风湿科门诊及住院确诊的SLE患者,以性别、年龄匹配的健康献血员为健康对照,参照系统性红斑狼疮疾病活动性指数(systemic lupus erythematosus disease activity index,SLEDAI)自行设计调查问卷,调查病例和对照的一般线性资料、以及病例组的疾病活动情况和临床/实验室资料。应用分光光度法测定SLE患者及正常对照者血浆中蛋白质氧化损伤相关指标(蛋白质羰基和巯基),脂质过氧化指标(丙二醛(malondialdehyde , MDA)),超氧化物歧化酶(superoxide dismutase, SOD)、髓过氧化酶(myeloperoxidase , MPO)和总抗氧化能力(total antioxidant capacity , TOAC)),采用酶联免疫吸附法定性测定SLE患者血浆抗ds-DNA抗体和抗核抗体的水平。病例组和对照组以及病例组间定量资料的比较,符合正态分布者采用t检验;不符合正态分布者,对其进行Mann-Whitney秩和检验。指标间相关分析,正态分布者采用Pearson相关,不符合正态分布者用Spearman等级相关。定性资料的组间比较采用χ2检验。以α=0.05作为检验水准。
结果系统性红斑狼疮患者脂质过氧化与蛋白质氧化产物与健康对照组相比差异显著,其中MDA、蛋白质羰基浓度以及MPO活性显著升高,蛋白质巯基浓度、活性显著降低,且与疾病活动相关指标有一定关联。抗dsDNA抗体阳性组血浆蛋白质巯基浓度、SOD活性显著低于阴性组,合并肾脏损伤或心血管损伤的SLE病人脂质过氧化和蛋白质氧化程度显著高于无上述合并症的SLE病人。
结论处于疾病活动状态的SLE患者,存在一定程度的脂质过氧化和蛋白质氧化损伤现象,且氧化损伤程度与疾病活动正相关。合并肾脏损伤以及心血管损伤与患者机体的氧化应激状态也存在一定关联,提示脂质过氧化以及蛋白质氧化损伤对以静脉微血管损伤、血管通透性改变为病理基础的SLE慢性器官损伤的发病机制可能存在一定的作用。
Objective To explore oxidative/anti-oxidative status(lipid oxidation, protein oxidative damage and antioxidant enzymes) in systemic lupus erythematosus (SLE), and to find the relationship between oxidation/anti-oxidation indexes and clinical indicators.
Method SLE patients were in- and out- patients of the Rheumatology Department in the First Affiliated Hospital, and health volunteers were recruited as controls. General information, chemical examination results and data of organ or system damage were collected by self-designed questionnaire. Here we have examined plasma oxidative damage indexs(such as malondialdehyde, protein carbonyl and protein thiol), superoxide dismutase(SOD), myeloperoxidase(MPO) and total antioxidant capacity (TOAC) in SLE patients and healthy controls. Levels of anti-double-stranded DNA (anti-dsDNA) and antinuclear antibody (ANA) were quantified by enzyme-linked immunosorbent assay. Variables were tested for skewness, and skewed continuous variables were logarithmically transformed. When appropriate, nonparametric tests (Mann-Whitney U test) were used for comparisons between the groups, whereas student’s t-test was used for normally distributed variables. Spearman’s rank correlation was used to calculate correlation coefficients between lipid Peroxidation, protein oxidation, anti-oxidation and clinical/laboratory indexes.
Results Compared with control subjects, SLE patients exhibited elevated levels of MDA(malondialdehyde) and protein carbonyls and decreased levels of protein thiols and activities of SOD. Plasma protein thiols levels and activities of SOD were lower in anti-dsDNA antibody(+) groups compared with anti-dsDNA antibody(-) groups in SLE patients. Lipid peroxidation and protein oxidation were significantly higher in SLE patients with nephropathy or cardiovascular complications than those without such complications patients.
Conclusion We found elevated levels of multiple markers of protein oxidation and degraded activities of antioxidant enzymes in plasma from SLE patients compared with controls, and these levels correlated with disease activity. The relationships between cardiac injury, nephropathy and oxidative stress were confrimed in SLE patients, which suggest oxidative stress may play a important role in the pathogenesis of chronic organ damage in SLE.
方法病例选用安徽医科大学附属医院风湿科门诊及住院确诊的SLE患者,以性别、年龄匹配的健康献血员为健康对照,参照系统性红斑狼疮疾病活动性指数(systemic lupus erythematosus disease activity index,SLEDAI)自行设计调查问卷,调查病例和对照的一般线性资料、以及病例组的疾病活动情况和临床/实验室资料。应用分光光度法测定SLE患者及正常对照者血浆中蛋白质氧化损伤相关指标(蛋白质羰基和巯基),脂质过氧化指标(丙二醛(malondialdehyde , MDA)),超氧化物歧化酶(superoxide dismutase, SOD)、髓过氧化酶(myeloperoxidase , MPO)和总抗氧化能力(total antioxidant capacity , TOAC)),采用酶联免疫吸附法定性测定SLE患者血浆抗ds-DNA抗体和抗核抗体的水平。病例组和对照组以及病例组间定量资料的比较,符合正态分布者采用t检验;不符合正态分布者,对其进行Mann-Whitney秩和检验。指标间相关分析,正态分布者采用Pearson相关,不符合正态分布者用Spearman等级相关。定性资料的组间比较采用χ2检验。以α=0.05作为检验水准。
结果系统性红斑狼疮患者脂质过氧化与蛋白质氧化产物与健康对照组相比差异显著,其中MDA、蛋白质羰基浓度以及MPO活性显著升高,蛋白质巯基浓度、活性显著降低,且与疾病活动相关指标有一定关联。抗dsDNA抗体阳性组血浆蛋白质巯基浓度、SOD活性显著低于阴性组,合并肾脏损伤或心血管损伤的SLE病人脂质过氧化和蛋白质氧化程度显著高于无上述合并症的SLE病人。
结论处于疾病活动状态的SLE患者,存在一定程度的脂质过氧化和蛋白质氧化损伤现象,且氧化损伤程度与疾病活动正相关。合并肾脏损伤以及心血管损伤与患者机体的氧化应激状态也存在一定关联,提示脂质过氧化以及蛋白质氧化损伤对以静脉微血管损伤、血管通透性改变为病理基础的SLE慢性器官损伤的发病机制可能存在一定的作用。
Objective To explore oxidative/anti-oxidative status(lipid oxidation, protein oxidative damage and antioxidant enzymes) in systemic lupus erythematosus (SLE), and to find the relationship between oxidation/anti-oxidation indexes and clinical indicators.
Method SLE patients were in- and out- patients of the Rheumatology Department in the First Affiliated Hospital, and health volunteers were recruited as controls. General information, chemical examination results and data of organ or system damage were collected by self-designed questionnaire. Here we have examined plasma oxidative damage indexs(such as malondialdehyde, protein carbonyl and protein thiol), superoxide dismutase(SOD), myeloperoxidase(MPO) and total antioxidant capacity (TOAC) in SLE patients and healthy controls. Levels of anti-double-stranded DNA (anti-dsDNA) and antinuclear antibody (ANA) were quantified by enzyme-linked immunosorbent assay. Variables were tested for skewness, and skewed continuous variables were logarithmically transformed. When appropriate, nonparametric tests (Mann-Whitney U test) were used for comparisons between the groups, whereas student’s t-test was used for normally distributed variables. Spearman’s rank correlation was used to calculate correlation coefficients between lipid Peroxidation, protein oxidation, anti-oxidation and clinical/laboratory indexes.
Results Compared with control subjects, SLE patients exhibited elevated levels of MDA(malondialdehyde) and protein carbonyls and decreased levels of protein thiols and activities of SOD. Plasma protein thiols levels and activities of SOD were lower in anti-dsDNA antibody(+) groups compared with anti-dsDNA antibody(-) groups in SLE patients. Lipid peroxidation and protein oxidation were significantly higher in SLE patients with nephropathy or cardiovascular complications than those without such complications patients.
Conclusion We found elevated levels of multiple markers of protein oxidation and degraded activities of antioxidant enzymes in plasma from SLE patients compared with controls, and these levels correlated with disease activity. The relationships between cardiac injury, nephropathy and oxidative stress were confrimed in SLE patients, which suggest oxidative stress may play a important role in the pathogenesis of chronic organ damage in SLE.
引文
1.叶冬青.红斑狼疮.北京:人民卫生出版社,2006.
2. Nishikawa M, Inoue M. Oxidative stress and tissue injury. Masui. 2008, 57(3): 321-6.
3.张肇,陈孝文,江黎明,等.狼疮肾炎患者白细胞介素13的血浆水平和基因表达.中华肾脏病杂志.2000,16(1):20 - 23.
4. Kovacic P, Jacintho JD. Systemic lupus erythematosus and other autoimmune diseases from endogenous and exogenous agents: unifying theme of oxidative stress. Mini Rev Med Chem. 2003,3(6):568-75.
5.李培峰,方允中,陈吉中等.活性氧对蛋白质抗原与其抗体反应性增强的效应.中国免疫学杂志,1993,10(2):84-86.
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2 Mohan IK, Das UN. Oxidant stress, anti-oxidants and essential fatty acids in systemic lupus erythematosus. Prostaglandins Leukot Essent Fatty Acids 1997; 56:193–8.
3 Avalos I, Chung CP, Oeser A, et al. Oxidative stress in systemic lupus erythematosus: relationship to disease activity and symptoms.Lupus. 2007; 16: 195-200
4 Ames PR, Alves J, Murat I, et al. Oxidative stress in systemic lupus erythematosus and allied conditions with vascular involvement. Rheumatology (Oxford). 1999, 38: 529-34.
5 Bergamo P, Maurano F, Rossi M. Phase 2 enzyme induction by conjugated linoleic acid improves lupus-associated oxidative stress. Free Radic Biol Med. 2007 Jul 1;43(1):71-9.
6 Platt AA, Gieseg SP. Inhibition of protein hydroperoxide formation by protein thiols. Redox Rep 2003; 8: 81–6.
7 Serban MG, Balanescu E, Nita V. Lipid peroxidase and erythrocyte redox system in systemic vasculitides treated with corticoids. Effect of vitamin E administration. Rom J Intern Med 1994; 32: 283–9.
8 Maeshima E, Liang XM, Goda M, et al. The efficacy of vitamin E against oxidative damage and autoantibody production in systemic lupus erythematosus: a preliminary study. Clin Rheumatol. 2007 Mar;26(3):401-4.
9 Hu ML.Measurement of protein thiol groups and glutathione in plasma.Methods Enzymol. 1994;233:380-5
10 Akio S, Yoneno T, et al. Trace analysis of carbonyl compounds by liquidchromatography-mass spectrometry after collection as 2,4-dinitrophenylhydrazine derivatives. J Chromatogr A. 1999, 4;844(1-2):403-8.
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15赵欣欣,赵丽娟,王晓非.系统性红斑狼疮患者血浆脂质过氧化物测定及分析.现代康复.1997,1 (3):189-190.
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26黄文,张学宁,孟如,等.系统性红斑狼疮患者自由基损伤的探讨.中国综合临床,1999,15:259-260.
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29 Scofield RH, Kurien BT, Ganick S,et al. Modification of lupus-associated 60-kDa Ro protein with the lipid oxidation product 4-hydroxy-2-nonenal increases antigenicity and facilitates epitope spreading. Free Radic Biol Med. 2005,38(6):719-28.
30 Morgan PE, Sturgess AD, Davies MJ. Increased levels of serum protein oxidation and correlation with disease activity in systemic lupus erythematosus. Arthritis Rheum. 2005,52(7):2069-79
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44张肇,陈孝文,江黎明,等.狼疮肾炎患者白细胞介素13的血浆水平和基因表达.中华肾脏病杂志.2000,16(1):20 - 23.
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1.叶冬青.红斑狼疮.北京:人民卫生出版社,2006.
2. Esdaile JM, Abrahamowicz M, Grodzicky T, et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001;44:2331–7.
3. Davies MJ, Fu S, Wang H, et al. Stable markers of oxidant damage to proteins and their application in study of human disease. Free Radic Biol Med. 1999; 27:1151–61
4. Kovacic P, Jacintho JD. Systemic Lupus Erythematosus and Other Autoimmune Diseases from Endogenous and Exogenous Agents: Unifying Theme of Oxidative Stress[J]. Mini Reviews in Medicinal Chemistry.2003,3(6):568-575.
5.赵欣欣,赵丽娟,王晓非.系统性红斑狼疮患者血浆脂质过氧化物测定及分析[J].现代康复.1997,1(3):189-190.
6. Frostegard J, Svenungsson E, Wu R, et al. Lipid peroxidation is enhanced in patients with systemic lupus erythematosus and is associated with arterial and renal disease manifestations[J]. Arthritis Rheum.2005,52(1):192-200.
7.吴赛珠,谭家余,吴迎星,等.女性性激素与血脂谱、丙二醛、超氧化物歧化酶及淋巴细胞亚群的相关性研究[J].中华核医学杂志. 2004,24(1):38-41.
8.章群,叶冬青.脂质和蛋白质过氧化与SLE临床指标的相关性研究[J].中华风湿病学杂志. 2008,
9. Scofield RH, Kurien BT, Ganick S,et al. Modification of lupus-associated 60-kDa Ro protein with the lipid oxidation product
4-hydroxy-2-nonenal increases antigenicity and facilitates epitope spreading. Free Radic Biol Med. 2005 Mar 15;38(6):719-28.
10.李培峰,方允中,陈吉中等.活性氧对蛋白质抗原与其抗体反应性增强的效应.中国免疫学杂志,1993,10(2):84-86.
11. Morgan PE, Sturgess AD, Davies MJ. Increased levels of serum protein oxidation and correlation with disease activity in systemic lupus erythematosus. Arthritis Rheum. 2005,52(7):2069-79
12.章群,叶冬青,陈国平.蛋白质氧化损伤与系统性红斑狼疮疾病活动的相关性研究[J].中华流行病学杂志. 2008
13. Tam LS, Li EK, Leung VY,et al. Effects of vitamins C and E on oxidative stress markers and endothelial function in patients with systemic lupus erythematosus: a double blind, placebo controlled pilot study. J Rheumatol. 2005 ,32(2):275-82.
14.董万群,叶冬青,潘海峰,等.机体氧化/抗氧化指标与SLE疾病活动相关性的研究.中华皮肤科杂志.2007,40(6):347-349
15. Avalos I, Chung CP, Oeser A, Oxidative stress in systemic lupus erythematosus: relationship to disease activity and symptoms. Lupus. 2007;16(3):195-200.
16.张肇,陈孝文,江黎明,等.狼疮肾炎患者白细胞介素13的血浆水平和基因表达[J].中华肾脏病杂志.2000,16(1):20 - 23.
17.姜红,王淑兰,罗钢,等.狼疮性肾炎中GSTμ基因缺失与氧化损伤的关系[J].中国医科大学学报. 2002,31(6):442-444.
18. Niessner A, Goronzy JJ, Weyand CM. Immune-mediated mechanisms in atherosclerosis: prevention and treatment of clinical manifestations. Curr Pharm Des. 2007;13(36):3701-10.
19. Lovell MA, Xie C, Gabbita SP, et al. Decreased thioredoxin and increased thioredoxin reductase levels in Alzheimer's disease brain. Free Radic Biol Med. 2000, 28(3):418-27.
2. Nishikawa M, Inoue M. Oxidative stress and tissue injury. Masui. 2008, 57(3): 321-6.
3.张肇,陈孝文,江黎明,等.狼疮肾炎患者白细胞介素13的血浆水平和基因表达.中华肾脏病杂志.2000,16(1):20 - 23.
4. Kovacic P, Jacintho JD. Systemic lupus erythematosus and other autoimmune diseases from endogenous and exogenous agents: unifying theme of oxidative stress. Mini Rev Med Chem. 2003,3(6):568-75.
5.李培峰,方允中,陈吉中等.活性氧对蛋白质抗原与其抗体反应性增强的效应.中国免疫学杂志,1993,10(2):84-86.
1 Esdaile JM, Abrahamowicz M, Grodzicky T, et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001;44:2331–7.
2 Mohan IK, Das UN. Oxidant stress, anti-oxidants and essential fatty acids in systemic lupus erythematosus. Prostaglandins Leukot Essent Fatty Acids 1997; 56:193–8.
3 Avalos I, Chung CP, Oeser A, et al. Oxidative stress in systemic lupus erythematosus: relationship to disease activity and symptoms.Lupus. 2007; 16: 195-200
4 Ames PR, Alves J, Murat I, et al. Oxidative stress in systemic lupus erythematosus and allied conditions with vascular involvement. Rheumatology (Oxford). 1999, 38: 529-34.
5 Bergamo P, Maurano F, Rossi M. Phase 2 enzyme induction by conjugated linoleic acid improves lupus-associated oxidative stress. Free Radic Biol Med. 2007 Jul 1;43(1):71-9.
6 Platt AA, Gieseg SP. Inhibition of protein hydroperoxide formation by protein thiols. Redox Rep 2003; 8: 81–6.
7 Serban MG, Balanescu E, Nita V. Lipid peroxidase and erythrocyte redox system in systemic vasculitides treated with corticoids. Effect of vitamin E administration. Rom J Intern Med 1994; 32: 283–9.
8 Maeshima E, Liang XM, Goda M, et al. The efficacy of vitamin E against oxidative damage and autoantibody production in systemic lupus erythematosus: a preliminary study. Clin Rheumatol. 2007 Mar;26(3):401-4.
9 Hu ML.Measurement of protein thiol groups and glutathione in plasma.Methods Enzymol. 1994;233:380-5
10 Akio S, Yoneno T, et al. Trace analysis of carbonyl compounds by liquidchromatography-mass spectrometry after collection as 2,4-dinitrophenylhydrazine derivatives. J Chromatogr A. 1999, 4;844(1-2):403-8.
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