Metformin prevents LYRM1-induced insulin resistance in 3T3-L1 adipocytes via a mitochondrial-dependent mechanism

Experimental Biology and Medicine

Volumn 239, Issue 12, 2014, Pages 1567-1574

  Qin, Zhen Ying ^a   Zhang, Min ^b   Dai, Yong Mei ^b   Wang, Yu Mei ^c   Zhu, Guan Zhong ^d   Zhao, Ya Ping ^e   Ji, Chen Bo ^b   Qiu, Jie ^b   Cao, Xin Guo ^b   Guo, Xi Rong ^d  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b WOMEN S HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^c Huai'an Maternal and Child Health Care Center   (China)

^d NANJING MEDICAL UNIVERSITY   (China)

^e The 82nd Hospital of the People's Liberation Army   (China)

Author keywords

Insulin resistance; LYRM1; Metformin; Mitochondrial biogenesis

Indexed keywords

GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; METFORMIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; ANTIOXIDANT; APOPTOSIS REGULATORY PROTEIN; LYR MOTIF CONTAINING 1 PROTEIN, MOUSE;

3T3 CELL LINE; ADIPOCYTE; ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; BIOGENESIS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG EFFECT; FLOW CYTOMETRY; GENE; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC TRANSFECTION; GLUCOSE TRANSPORT; INSULIN RESISTANCE; LYR MOTIF CONTAINING 1 GENE; MITOCHONDRION; MOUSE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

ADIPOCYTES; ANIMALS; ANTIOXIDANTS; APOPTOSIS REGULATORY PROTEINS; CELL LINE; HYPOGLYCEMIC AGENTS; INSULIN RESISTANCE; METFORMIN; MICE; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 84918525766     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370214537746     Document Type: Article

References (40)

1. Bournat JC,Brown CW.Mitochondrial dysfunction in obesity.Curr Opin Endocrinol Diabetes Obes. 2010;17:446-52
2. 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
3. Kim JA,Wei Y,Sowers JR.Role of mitochondrial dysfunction in insulin resistance.Circ Res. 2008;102:401-14
4. Wang X,Gu C,He W,Ye X,Chen H,Zhang X,Hai C.Glucose oxidase induces insulin resistance via influencing multiple targets in vitro and in vivo: the central role of oxidative stress.Biochimie. 2012;94:1705-17
5. Bashan N,Kovsan J,Kachko I,Ovadia H,Rudich A.Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species.Physiol Rev. 2009;89:27-71
6. Houstis N,Rosen ED,Lander ES.Reactive oxygen species have a causal role in multiple forms of insulin resistance.Nature. 2006;440:944-8
7. Qin ZY,Zhang M,Guo XR,Wang YM,Zhu GZ,Ni YH,Zhao YP,Qiu J,Kou CZ,Qin R,Cao XG.α-Lipoic acid ameliorates impaired glucose uptake in LYRM1 overexpressing 3T3-L1 adipocytes through the IRS-1/Akt signaling pathway.J Bioenerg Biomembr. 2012;44:579-86
8. Rice S,Pellatt LJ,Bryan SJ,Whitehead SA,Mason HD.Action of metformin on the insulin-signaling pathway and on glucose transport in human granulosa cells.J Clin Endocrinol Metab. 2011;96:E427-35
9. Grisouard J,Timper K,Radimerski TM,Frey DM,Peterli R,Kola B,Korbonits M,Herrmann P,Krahenbuhl S,Zulewski H,Keller U,Muller B,Christ-Crain M.Mechanisms of metformin action on glucose transport and metabolism in human adipocytes.Biochem Pharmacol. 2010;80: 1736-45
10. Kukidome D,Nishikawa T,Sonoda K,Imoto K,Fujisawa K,Yano M,Motoshima H,Taguchi T,Matsumura T,Araki E.Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells.Diabetes. 2006;55:120-7
11. Qiu J,Ni YH,Gong HX,Fei L,Pan XQ,Guo M,Chen RH,Guo XR.Identification of differentially expressed genes in omental adipose tissues of obese patients by suppression subtractive hybridization.Biochem Biophys Res Commun. 2007;352:469-78
12. Cao XG,Kou CZ,Zhao YP,Gao CL,Zhu C,Zhang CM,Ji CB,Qin DN,Zhang M,Guo XR.Overexpression of LYRM1 induces mitochondrial impairment in 3T3-L1 adipocytes.Mol Genet Metab. 2010;101:395-9
13. Bailey CJ,Turner RC.Metformin.N Engl J Med. 1996;334:574-9
14. Hundal RS,Krssak M,Dufour S,Laurent D,Lebon V,Chandramouli V,Inzucchi SE,Schumann WC,Petersen KF,Landau BR,Shulman GI.Mechanism by which metformin reduces glucose production in type 2 diabetes.Diabetes. 2000;49:2063-9
15. Fujisawa K,Nishikawa T,Kukidome D,Imoto K,Yamashiro T,Motoshima H,Matsumura T,Araki E.TZDs reduce mitochondrial ROS production and enhance mitochondrial biogenesis.Biochem Biophys Res Commun. 2009;379: 43-8
16. Qiu J,Gao CL,Zhang M,Chen RH,Chi X,Liu F,Zhang CM,Ji CB,Chen XH,Zhao YP,Li XN,Tong ML,Ni YH,Guo XR.LYRM1, a novel gene promotes proliferation and inhibits apoptosis of preadipocytes.Eur J Endocrinol. 2009;160:177-84
17. Maxwell DP,Wang Y,McIntosh L.The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells.Proc Natl Acad Sci U S A. 1999;96:8271-6
18. Ceddia RB,Somwar R,Maida A,Fang X,Bikopoulos G,Sweeney G.Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells.Diabetologia. 2005;48:132-9
19. Kanzaki M.Insulin receptor signals regulating GLUT4 translocation and actin dynamics.Endocr J. 2006;53:267-93
20. Kou C,Cao X,Qin D,Ji C,Zhu J,Zhang C,Zhu C,Gao C,Chen R,Guo X,Zhang M.Over-expression of LYRM1 inhibits glucose transport in rat skeletal muscles via attenuated phosphorylation of PI3K (p85) and Akt.Mol Cell Biochem. 2011;348:149-54
21. Bonnard C,Durand A,Peyrol S,Chanseaume E,Chauvin MA,Morio B,Vidal H,Rieusset J.Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice.J Clin Invest. 2008;118:789-800
22. Scarpulla RC.Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network.Biochim Biophys Acta. 2011;1813:1269-78
23. Arduini A,Serviddio G,Escobar J,Tormos AM,Bellanti F,Vina J,Monsalve M,Sastre J.Mitochondrial biogenesis fails in secondary biliary cirrhosis in rats leading to mitochondrial DNA depletion and deletions.Am J Physiol Gastrointest Liver Physiol. 2011;301:G119-27
24. Patti ME,Corvera S.The role of mitochondria in the pathogenesis of type 2 diabetes.Endocr Rev. 2010;31:364-95
25. Kane DA,Anderson EJ,Price JW,Woodlief TL,Lin CT,Bikman BT,Cortright RN,Neufer PD.Metformin selectively attenuates mitochondrial H2O2 emission without affecting respiratory capacity in skeletal muscle of obese rats.Free Radic Biol Med. 2010;49:1082-7
26. Morales AI,Detaille D,Prieto M,Puente A,Briones E,Arevalo M,Leverve X,Lopez-Novoa JM,El-Mir MY.Metformin prevents experimental gentamicin-induced nephropathy by a mitochondria-dependent pathway.Kidney Int. 2010;77:861-9
27. Suwa M,Egashira T,Nakano H,Sasaki H,Kumagai S.Metformin increases the PGC-1alpha protein and oxidative enzyme activities possibly via AMPK phosphorylation in skeletal muscle in vivo.J Appl Physiol. 2006;101:1685-92
28. Ciaraldi TP,Kong AP,Chu NV,Kim DD,Baxi S,Loviscach M,Plodkowski R,Reitz R,Caulfield M,Mudaliar S,Henry RR.Regulation of glucose transport and insulin signaling by troglitazone or metformin in adipose tissue of type 2 diabetic subjects.Diabetes. 2002;51:30-6
29. Magnoni LJ,Vraskou Y,Palstra AP,Planas JV.AMP-activated protein kinase plays an important evolutionary conserved role in the regulation of glucose metabolism in fish skeletal muscle cells.PLoS One. 2012;7:e31219-e31219
30. Benton CR,Nickerson JG,Lally J,Han XX,Holloway GP,Glatz JF,Luiken JJ,Graham TE,Heikkila JJ,Bonen A.Modest PGC-1alpha overexpression in muscle in vivo is sufficient to increase insulin sensitivity and palmitate oxidation in subsarcolemmal, not intermyofibrillar, mitochondria.J Biol Chem. 2008;283:4228-40
31. Ikeuchi M,Matsusaka H,Kang D,Matsushima S,Ide T,Kubota T,Fujiwara T,Hamasaki N,Takeshita A,Sunagawa K,Tsutsui H.Overexpression of mitochondrial transcription factor a ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction.Circulation. 2005;112:683-90
32. Liang H,Balas B,Tantiwong P,Dube J,Goodpaster BH,O’Doherty RM,DeFronzo RA,Richardson A,Musi N,Ward WF.Whole body overexpression of PGC-1alpha has opposite effects on hepatic and muscle insulin sensitivity.Am J Physiol Endocrinol Metab. 2009;296:E945-54
33. Choi CS,Befroy DE,Codella R,Kim S,Reznick RM,Hwang YJ,Liu ZX,Lee HY,Distefano A,Samuel VT,Zhang D,Cline GW,Handschin C,Lin J,Petersen KF,Spiegelman BM,Shulman GI.Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism.Proc Natl Acad Sci U S A. 2008;105:19926-31
34. Miura S,Kai Y,Ono M,Ezaki O.Overexpression of peroxisome proliferator-activated receptor gamma coactivator-1alpha down-regulates GLUT4 mRNA in skeletal muscles.J Biol Chem. 2003;278:31385-90
35. Yang W,Lu J,Weng J,Jia W,Ji L,Xiao J,Shan Z,Liu J,Tian H,Ji Q,Zhu D,Ge J,Lin L,Chen L,Guo X,Zhao Z,Li Q,Zhou Z,Shan G,He J,China National D,Metabolic Disorders Study G.Prevalence of diabetes among men and women in China.N Engl J Med. 2010;362:1090-101
36. Giovannone B,Scaldaferri ML,Federici M,Porzio O,Lauro D,Fusco A,Sbraccia P,Borboni P,Lauro R,Sesti G.Insulin receptor substrate (IRS) transduction system: distinct and overlapping signaling potential.Diabetes Metab Res Rev. 2000;16:434-41
37. Shibata M,Hakuno F,Yamanaka D,Okajima H,Fukushima T,Hasegawa T,Ogata T,Toyoshima Y,Chida K,Kimura K,Sakoda H,Takenaka A,Asano T,Takahashi S.Paraquat-induced oxidative stress represses phosphatidylinositol 3-kinase activities leading to impaired glucose uptake in 3T3-L1 adipocytes.J Biol Chem. 2010;285:20915-25
38. Kumar N,Dey CS.Metformin enhances insulin signalling in insulin-dependent and-independent pathways in insulin resistant muscle cells.Br J Pharmacol. 2002;137:329-36
39. Yuan L,Ziegler R,Hamann A.Metformin modulates insulin post-receptor signaling transduction in chronically insulin-treated Hep G2 cells.Acta Pharmacol Sin. 2003;24:55-60
40. Bloch-Damti A,Potashnik R,Gual P,Le Marchand-Brustel Y,Tanti JF,Rudich A,Bashan N.Differential effects of IRS1 phosphorylated on Ser307 or Ser632 in the induction of insulin resistance by oxidative stress.Diabetologia. 2006;49:2463-73