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Published in: Clinical and Experimental Medicine 3/2018

01-08-2018 | Original Article

Reduced mitochondrial DNA content in lymphocytes is associated with insulin resistance and inflammation in patients with impaired fasting glucose

Authors: Mohamad Hafizi Abu Bakar, Nany Hairunisa, Hasniza Zaman Huri

Published in: Clinical and Experimental Medicine | Issue 3/2018

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Abstract

Altered mitochondrial DNA (mtDNA) is the most common denominator to numerous metabolic diseases. The present study sought to investigate the correlation between mtDNA content in lymphocytes and associated clinical risk factors for impaired fasting glucose (IFG). We included 23 healthy control and 42 IFG participants in this cross-sectional study. The measurements of mtDNA content in lymphocytes and pro-inflammatory markers derived from both normal and diseased individuals were quantified. Spearman partial correlation and multivariate statistical analyses were employed to evaluate the association between mtDNA content and other metabolic covariates in IFG. Reduced mtDNA content was observed in the IFG group with microvascular complications than those without complications. The IFG patients with lowest median of mtDNA content had considerably elevated hyperglycemia, insulin resistance and inflammation. The adjusted partial correlation analysis showed that mtDNA content was positively correlated with HDL-cholesterol and IL-10 (P < 0.005 for all). Further, multiple linear regression analyses verified that reduced mtDNA content in lymphocytes was independently associated with HOMA-IR (β = 0.027, P = 0.003), HbA1c (β = 0.652, P = 0.002), HDL-cholesterol (β = − 1.056, P = 0.021), IL-6 (β = 0.423, P = 0.002), IL-10 (β = − 1.234, P = 0.043) and TNF-α (β = 0.542, P < 0.001) after adjustment for confounding factors. Our data show that reduced mtDNA content in lymphocytes was associated with insulin resistance and inflammation in individuals with IFG.
Literature
1.
go back to reference International Diabetes Federation. IDF Diabetes Atlas. 7th ed. Federation ID, editor. Brussels, Belgium: International Diabetes Federation; 2017. International Diabetes Federation. IDF Diabetes Atlas. 7th ed. Federation ID, editor. Brussels, Belgium: International Diabetes Federation; 2017.
2.
3.
go back to reference Lu H, Koshkin V, Allister EM, Gyulkhandanyan AV, Wheeler MB. Molecular and metabolic evidence for mitochondrial defects associated with beta-cell dysfunction in a mouse model of type 2 diabetes. Diabetes. 2010;59:448–59.CrossRefPubMed Lu H, Koshkin V, Allister EM, Gyulkhandanyan AV, Wheeler MB. Molecular and metabolic evidence for mitochondrial defects associated with beta-cell dysfunction in a mouse model of type 2 diabetes. Diabetes. 2010;59:448–59.CrossRefPubMed
4.
go back to reference Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med. 2004;350:664–71.CrossRefPubMedPubMedCentral Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med. 2004;350:664–71.CrossRefPubMedPubMedCentral
5.
go back to reference Serradas P, Giroix M-H, Saulnier C, Gangnerau M-N, Borg LA, Welsh M, et al. Mitochondrial deoxyribonucleic acid content is specifically decreased in adult, but not fetal, pancreatic islets of the Goto-Kakizaki rat, a genetic model of noninsulin-dependent diabetes. Endocrinology. 1995;136:5623–31.CrossRefPubMed Serradas P, Giroix M-H, Saulnier C, Gangnerau M-N, Borg LA, Welsh M, et al. Mitochondrial deoxyribonucleic acid content is specifically decreased in adult, but not fetal, pancreatic islets of the Goto-Kakizaki rat, a genetic model of noninsulin-dependent diabetes. Endocrinology. 1995;136:5623–31.CrossRefPubMed
6.
go back to reference Antonetti DA, Reynet C, Kahn CR. Increased expression of mitochondrial-encoded genes in skeletal muscle of humans with diabetes mellitus. J Clin Invest. 1995;95:1383.CrossRefPubMedPubMedCentral Antonetti DA, Reynet C, Kahn CR. Increased expression of mitochondrial-encoded genes in skeletal muscle of humans with diabetes mellitus. J Clin Invest. 1995;95:1383.CrossRefPubMedPubMedCentral
7.
go back to reference Widlansky ME, Wang J, Shenouda SM, Hagen TM, Smith AR, Kizhakekuttu TJ, et al. Altered mitochondrial membrane potential, mass, and morphology in the mononuclear cells of humans with type 2 diabetes. Transl Res. 2010;156:15–25.CrossRefPubMedPubMedCentral Widlansky ME, Wang J, Shenouda SM, Hagen TM, Smith AR, Kizhakekuttu TJ, et al. Altered mitochondrial membrane potential, mass, and morphology in the mononuclear cells of humans with type 2 diabetes. Transl Res. 2010;156:15–25.CrossRefPubMedPubMedCentral
8.
go back to reference Shenouda SM, Widlansky ME, Chen K, Xu G, Holbrook M, Tabit CE, et al. Altered mitochondrial dynamics contributes to endothelial dysfunction in diabetes mellitus. Circulation. 2011;124:444–53.CrossRefPubMedPubMedCentral Shenouda SM, Widlansky ME, Chen K, Xu G, Holbrook M, Tabit CE, et al. Altered mitochondrial dynamics contributes to endothelial dysfunction in diabetes mellitus. Circulation. 2011;124:444–53.CrossRefPubMedPubMedCentral
9.
go back to reference Perl A, Gergely P, Nagy G, Koncz A, Banki K. Mitochondrial hyperpolarization: a checkpoint of T-cell life, death and autoimmunity. Trends Immunol Elsevier. 2004;25:360–7.CrossRef Perl A, Gergely P, Nagy G, Koncz A, Banki K. Mitochondrial hyperpolarization: a checkpoint of T-cell life, death and autoimmunity. Trends Immunol Elsevier. 2004;25:360–7.CrossRef
10.
go back to reference Kim H-S, Park K-G, Koo TB, Huh S, Lee I-K. The modulating effects of the overexpression of uncoupling protein 2 on the formation of reactive oxygen species in vascular cells. Diabetes Res Clin Pract. 2007;77:S46–8.CrossRefPubMed Kim H-S, Park K-G, Koo TB, Huh S, Lee I-K. The modulating effects of the overexpression of uncoupling protein 2 on the formation of reactive oxygen species in vascular cells. Diabetes Res Clin Pract. 2007;77:S46–8.CrossRefPubMed
11.
go back to reference Khan S, Raghuram GV, Bhargava A, Pathak N, Chandra DH, Jain SK, et al. Role and clinical significance of lymphocyte mitochondrial dysfunction in type 2 diabetes mellitus. Transl Res. 2011;158:344–59.CrossRefPubMed Khan S, Raghuram GV, Bhargava A, Pathak N, Chandra DH, Jain SK, et al. Role and clinical significance of lymphocyte mitochondrial dysfunction in type 2 diabetes mellitus. Transl Res. 2011;158:344–59.CrossRefPubMed
12.
go back to reference Bakar MHA, Kian Kai C, Wan Hassan WN, Sarmidi MR, Yaakob H, Zaman Huri H. Mitochondrial dysfunction as a central event for mechanisms underlying insulin resistance: the roles of long chain fatty acids. Diabetes Metab Res Rev. 2015;31:453–75.CrossRef Bakar MHA, Kian Kai C, Wan Hassan WN, Sarmidi MR, Yaakob H, Zaman Huri H. Mitochondrial dysfunction as a central event for mechanisms underlying insulin resistance: the roles of long chain fatty acids. Diabetes Metab Res Rev. 2015;31:453–75.CrossRef
13.
go back to reference Malik AN, Czajka A. Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction? Mitochondrion. 2013;13:481–92.CrossRefPubMed Malik AN, Czajka A. Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction? Mitochondrion. 2013;13:481–92.CrossRefPubMed
14.
go back to reference American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2009;33:S62.CrossRef American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2009;33:S62.CrossRef
15.
go back to reference Abu Bakar MH, Sarmidi MR. Association of cultured myotubes and fasting plasma metabolite profiles with mitochondrial dysfunction in type 2 diabetes subjects. Mol BioSyst. 2017;13:1838–53.CrossRefPubMed Abu Bakar MH, Sarmidi MR. Association of cultured myotubes and fasting plasma metabolite profiles with mitochondrial dysfunction in type 2 diabetes subjects. Mol BioSyst. 2017;13:1838–53.CrossRefPubMed
16.
go back to reference Association AD. Standards of medical care in diabetes–2014. Diabetes Care. 2014;37:S14–80.CrossRef Association AD. Standards of medical care in diabetes–2014. Diabetes Care. 2014;37:S14–80.CrossRef
17.
go back to reference Piątkiewicz P, Czech A, Tatoń J. Glucose transport in human peripheral blood lymphocytes influenced by type 2 diabetes mellitus. Arch Immunol Ther Exp (Warsz). 2007;55:119–26.CrossRef Piątkiewicz P, Czech A, Tatoń J. Glucose transport in human peripheral blood lymphocytes influenced by type 2 diabetes mellitus. Arch Immunol Ther Exp (Warsz). 2007;55:119–26.CrossRef
18.
go back to reference Kramer PA, Ravi S, Chacko B, Johnson MS, Darley-Usmar VM. A review of the mitochondrial and glycolytic metabolism in human platelets and leukocytes: implications for their use as bioenergetic biomarkers. Redox Biol. 2014;2:206–10.CrossRefPubMedPubMedCentral Kramer PA, Ravi S, Chacko B, Johnson MS, Darley-Usmar VM. A review of the mitochondrial and glycolytic metabolism in human platelets and leukocytes: implications for their use as bioenergetic biomarkers. Redox Biol. 2014;2:206–10.CrossRefPubMedPubMedCentral
19.
go back to reference Hische M, Larhlimi A, Schwarz F, Fischer-Rosinský A, Bobbert T, Assmann A, et al. A distinct metabolic signature predicts development of fasting plasma glucose. J Clin Bioinforma. 2012;2:3.CrossRefPubMedPubMedCentral Hische M, Larhlimi A, Schwarz F, Fischer-Rosinský A, Bobbert T, Assmann A, et al. A distinct metabolic signature predicts development of fasting plasma glucose. J Clin Bioinforma. 2012;2:3.CrossRefPubMedPubMedCentral
20.
go back to reference Dagenais GR, Gerstein HC, Holman R, Budaj A, Escalante A, Hedner T, et al. Effects of ramipril and rosiglitazone on cardiovascular and renal outcomes in people with impaired glucose tolerance or impaired fasting glucose: results of the Diabetes REduction Assessment with ramipril and rosiglitazone Medication (DREAM) trial. Diabetes Care. 2008;31:1007–14.CrossRefPubMed Dagenais GR, Gerstein HC, Holman R, Budaj A, Escalante A, Hedner T, et al. Effects of ramipril and rosiglitazone on cardiovascular and renal outcomes in people with impaired glucose tolerance or impaired fasting glucose: results of the Diabetes REduction Assessment with ramipril and rosiglitazone Medication (DREAM) trial. Diabetes Care. 2008;31:1007–14.CrossRefPubMed
21.
go back to reference Garber AJ, Abrahamson MJ, Barzilay JI, Blonde L, Bloomgarden ZT, Bush MA, et al. Consensus statement by the American Association of Clinical Endocrinologists and American College of Endocrinology on the comprehensive type 2 diabetes management algorithm–2016 executive summary. Endocr Pract. 2016;22:84–113.CrossRefPubMed Garber AJ, Abrahamson MJ, Barzilay JI, Blonde L, Bloomgarden ZT, Bush MA, et al. Consensus statement by the American Association of Clinical Endocrinologists and American College of Endocrinology on the comprehensive type 2 diabetes management algorithm–2016 executive summary. Endocr Pract. 2016;22:84–113.CrossRefPubMed
22.
go back to reference Handelsman Y, Bloomgarden ZT, Grunberger G, Umpierrez G, Zimmerman RS, Bailey TS, et al. American Association of Clinical Endocrinologists and American College of Endocrinology–clinical practice guidelines for developing a diabetes mellitus comprehensive care plan–2015. Endocr Pract. 2015;21:1–87.CrossRefPubMedPubMedCentral Handelsman Y, Bloomgarden ZT, Grunberger G, Umpierrez G, Zimmerman RS, Bailey TS, et al. American Association of Clinical Endocrinologists and American College of Endocrinology–clinical practice guidelines for developing a diabetes mellitus comprehensive care plan–2015. Endocr Pract. 2015;21:1–87.CrossRefPubMedPubMedCentral
23.
go back to reference Lee JE, Park H, Ju YS, Kwak M, Kim J-I, Oh HY, et al. Higher mitochondrial DNA copy number is associated with lower prevalence of microalbuminuria. Exp Mol Med. 2009;41:253–8.CrossRefPubMedPubMedCentral Lee JE, Park H, Ju YS, Kwak M, Kim J-I, Oh HY, et al. Higher mitochondrial DNA copy number is associated with lower prevalence of microalbuminuria. Exp Mol Med. 2009;41:253–8.CrossRefPubMedPubMedCentral
24.
go back to reference Malik AN, Shahni R, Iqbal MM. Increased peripheral blood mitochondrial DNA in type 2 diabetic patients with nephropathy. Diabetes Res Clin Pract. 2009;86:e22–4.CrossRefPubMed Malik AN, Shahni R, Iqbal MM. Increased peripheral blood mitochondrial DNA in type 2 diabetic patients with nephropathy. Diabetes Res Clin Pract. 2009;86:e22–4.CrossRefPubMed
25.
go back to reference Madsen-Bouterse SA, Mohammad G, Kanwar M, Kowluru RA. Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with Its progression. Antioxid Redox Signal. 2010;13:797–805.CrossRefPubMedPubMedCentral Madsen-Bouterse SA, Mohammad G, Kanwar M, Kowluru RA. Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with Its progression. Antioxid Redox Signal. 2010;13:797–805.CrossRefPubMedPubMedCentral
26.
go back to reference Santos JM, Tewari S, Goldberg AFX, Kowluru RA. Mitochondrial biogenesis and the development of diabetic retinopathy. Free Radic Biol Med. 2011;51:1849–60.CrossRefPubMedPubMedCentral Santos JM, Tewari S, Goldberg AFX, Kowluru RA. Mitochondrial biogenesis and the development of diabetic retinopathy. Free Radic Biol Med. 2011;51:1849–60.CrossRefPubMedPubMedCentral
27.
go back to reference Vincent AM, Calabek B, Roberts L, Feldman EL. Biology of diabetic neuropathy. Handb Clin Neurol. 2012;115:591–606.CrossRef Vincent AM, Calabek B, Roberts L, Feldman EL. Biology of diabetic neuropathy. Handb Clin Neurol. 2012;115:591–606.CrossRef
28.
go back to reference Yagihashi S, Mizukami H, Sugimoto K. Mechanism of diabetic neuropathy: where are we now and where to go? J Diabetes Investig. 2011;2:18–32.CrossRefPubMed Yagihashi S, Mizukami H, Sugimoto K. Mechanism of diabetic neuropathy: where are we now and where to go? J Diabetes Investig. 2011;2:18–32.CrossRefPubMed
29.
go back to reference Fernyhough P, Roy Chowdhury SK, Schmidt RE. Mitochondrial stress and the pathogenesis of diabetic neuropathy. Expert Rev Endocrinol Metab. 2010;5:39–49.CrossRefPubMedPubMedCentral Fernyhough P, Roy Chowdhury SK, Schmidt RE. Mitochondrial stress and the pathogenesis of diabetic neuropathy. Expert Rev Endocrinol Metab. 2010;5:39–49.CrossRefPubMedPubMedCentral
30.
go back to reference Bogacka I, Xie H, Bray GA, Smith SR. Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes. 2005;54:1392–9.CrossRefPubMed Bogacka I, Xie H, Bray GA, Smith SR. Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes. 2005;54:1392–9.CrossRefPubMed
31.
go back to reference Wong J, McLennan SV, Molyneaux L, Min D, Twigg SM, Yue DK. Mitochondrial DNA content in peripheral blood monocytes: relationship with age of diabetes onsetand diabetic complications. Diabetologia. 2009;52:1953–61.CrossRefPubMed Wong J, McLennan SV, Molyneaux L, Min D, Twigg SM, Yue DK. Mitochondrial DNA content in peripheral blood monocytes: relationship with age of diabetes onsetand diabetic complications. Diabetologia. 2009;52:1953–61.CrossRefPubMed
32.
go back to reference Lee HK, Song JH, Shin CS, Park DJ, Park KS, Lee KU, et al. Decreased mitochondrial DNA content in peripheral blood precedes the development of non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract. 1998;42:161–7.CrossRefPubMed Lee HK, Song JH, Shin CS, Park DJ, Park KS, Lee KU, et al. Decreased mitochondrial DNA content in peripheral blood precedes the development of non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract. 1998;42:161–7.CrossRefPubMed
33.
go back to reference Madsen-Bouterse SA, Zhong Q, Mohammad G, Ho Y-S, Kowluru RA. Oxidative damage of mitochondrial DNA in diabetes and its protection by manganese superoxide dismutase. Free Radic Res. 2010;44:313–21.CrossRefPubMedPubMedCentral Madsen-Bouterse SA, Zhong Q, Mohammad G, Ho Y-S, Kowluru RA. Oxidative damage of mitochondrial DNA in diabetes and its protection by manganese superoxide dismutase. Free Radic Res. 2010;44:313–21.CrossRefPubMedPubMedCentral
34.
go back to reference Weng S-W, Lin T-K, Liou C-W, Chen S-D, Wei Y-H, Lee H-C, et al. Peripheral blood mitochondrial DNA content and dysregulation of glucose metabolism. Diabetes Res Clin Pract. 2009;83:94–9.CrossRefPubMed Weng S-W, Lin T-K, Liou C-W, Chen S-D, Wei Y-H, Lee H-C, et al. Peripheral blood mitochondrial DNA content and dysregulation of glucose metabolism. Diabetes Res Clin Pract. 2009;83:94–9.CrossRefPubMed
35.
go back to reference Lu Y, Xiao T, Zhang F, Chen Y, Liu Y, Li Y, et al. Effect of mitochondrial tRNA Lys mutation on the clinical and biochemical characteristics of Chinese essential hypertensive subjects. Biochem Biophys Res Commun. 2014;454:500–4.CrossRefPubMed Lu Y, Xiao T, Zhang F, Chen Y, Liu Y, Li Y, et al. Effect of mitochondrial tRNA Lys mutation on the clinical and biochemical characteristics of Chinese essential hypertensive subjects. Biochem Biophys Res Commun. 2014;454:500–4.CrossRefPubMed
36.
go back to reference Zhu H-Y, Wang S-W, Martin LJ, Liu L, Li Y-H, Chen R, et al. The role of mitochondrial genome in essential hypertension in a Chinese Han population. Eur J Hum Genet. 2009;17:1501–6.CrossRefPubMedPubMedCentral Zhu H-Y, Wang S-W, Martin LJ, Liu L, Li Y-H, Chen R, et al. The role of mitochondrial genome in essential hypertension in a Chinese Han population. Eur J Hum Genet. 2009;17:1501–6.CrossRefPubMedPubMedCentral
37.
go back to reference Singh R, Hattersley AT, Harries LW. Reduced peripheral blood mitochondrial DNA content is not a risk factor for Type 2 diabetes. Diabet Med. 2007;24:784–7.CrossRefPubMed Singh R, Hattersley AT, Harries LW. Reduced peripheral blood mitochondrial DNA content is not a risk factor for Type 2 diabetes. Diabet Med. 2007;24:784–7.CrossRefPubMed
38.
go back to reference Wilson PWF, Meigs JB, Sullivan L, Fox CS, Nathan DM, D’Agostino RB. Prediction of incident diabetes mellitus in middle-aged adults: the Framingham Offspring Study. Arch Intern Med. 2007;167:1068–74.CrossRefPubMed Wilson PWF, Meigs JB, Sullivan L, Fox CS, Nathan DM, D’Agostino RB. Prediction of incident diabetes mellitus in middle-aged adults: the Framingham Offspring Study. Arch Intern Med. 2007;167:1068–74.CrossRefPubMed
39.
go back to reference Schmidt MI, Duncan BB, Bang H, Pankow JS, Ballantyne CM, Golden SH, et al. Identifying individuals at high risk for diabetes. Diabetes Care. 2005;28:2013–8.CrossRefPubMed Schmidt MI, Duncan BB, Bang H, Pankow JS, Ballantyne CM, Golden SH, et al. Identifying individuals at high risk for diabetes. Diabetes Care. 2005;28:2013–8.CrossRefPubMed
40.
go back to reference Liu C-S, Kuo C-L, Cheng W-L, Huang C-S, Lee C-F, Wei Y-H. Alteration of the copy number of mitochondrial DNA in leukocytes of patients with hyperlipidemia. Ann N Y Acad Sci. 2005;1042:70–5.CrossRefPubMed Liu C-S, Kuo C-L, Cheng W-L, Huang C-S, Lee C-F, Wei Y-H. Alteration of the copy number of mitochondrial DNA in leukocytes of patients with hyperlipidemia. Ann N Y Acad Sci. 2005;1042:70–5.CrossRefPubMed
41.
go back to reference Romeo G, Liu W-H, Asnaghi V, Kern TS, Lorenzi M. Activation of nuclear factor-κB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes. 2002;51:2241–8.CrossRefPubMed Romeo G, Liu W-H, Asnaghi V, Kern TS, Lorenzi M. Activation of nuclear factor-κB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes. 2002;51:2241–8.CrossRefPubMed
42.
go back to reference Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014;105:141–50.CrossRefPubMed Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014;105:141–50.CrossRefPubMed
43.
go back to reference Malik AN, Parsade CK, Ajaz S, Crosby-Nwaobi R, Gnudi L, Czajka A, et al. Altered circulating mitochondrial DNA and increased inflammation in patients with diabetic retinopathy. Diabetes Res Clin Pract. 2015;110:257–65.CrossRefPubMed Malik AN, Parsade CK, Ajaz S, Crosby-Nwaobi R, Gnudi L, Czajka A, et al. Altered circulating mitochondrial DNA and increased inflammation in patients with diabetic retinopathy. Diabetes Res Clin Pract. 2015;110:257–65.CrossRefPubMed
44.
go back to reference Emanuela F, Grazia M, de Marco R, Maria Paola L, Giorgio F, Marco B. Inflammation as a link between obesity and metabolic syndrome. J Nutr Metab. 2012;2012:476380.CrossRefPubMedPubMedCentral Emanuela F, Grazia M, de Marco R, Maria Paola L, Giorgio F, Marco B. Inflammation as a link between obesity and metabolic syndrome. J Nutr Metab. 2012;2012:476380.CrossRefPubMedPubMedCentral
45.
46.
go back to reference Hong E-G, Ko HJ, Cho Y-R, Kim H-J, Ma Z, Yu TY, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes. 2009;58:2525–35.CrossRefPubMedPubMedCentral Hong E-G, Ko HJ, Cho Y-R, Kim H-J, Ma Z, Yu TY, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes. 2009;58:2525–35.CrossRefPubMedPubMedCentral
47.
go back to reference Dagdeviren S, Jung DY, Friedline RH, Noh HL, Kim JH, Patel PR, et al. IL-10 prevents aging-associated inflammation and insulin resistance in skeletal muscle. FASEB J. 2016;31:701–10.CrossRefPubMedPubMedCentral Dagdeviren S, Jung DY, Friedline RH, Noh HL, Kim JH, Patel PR, et al. IL-10 prevents aging-associated inflammation and insulin resistance in skeletal muscle. FASEB J. 2016;31:701–10.CrossRefPubMedPubMedCentral
Metadata
Title
Reduced mitochondrial DNA content in lymphocytes is associated with insulin resistance and inflammation in patients with impaired fasting glucose
Authors
Mohamad Hafizi Abu Bakar
Nany Hairunisa
Hasniza Zaman Huri
Publication date
01-08-2018
Publisher
Springer International Publishing
Published in
Clinical and Experimental Medicine / Issue 3/2018
Print ISSN: 1591-8890
Electronic ISSN: 1591-9528
DOI
https://doi.org/10.1007/s10238-018-0495-4

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