Mitochondrial metabolism and diabetes

Journal of Diabetes Investigation

Volumn 1, Issue 5, 2010, Pages 161-169

  Kwak, Soo Heon ^a   Park, Kyong Soo ^a,b   Lee, Ki Up ^c   Lee, Hong Kyu ^d  

^a Internal Medicine   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

^c University of Ulsan College of Medicine   (South Korea)

^d Eulji University   (South Korea)

Author keywords

Insulin resistance; Mitochondrial dysfunction; Type 2 diabetes mellitus

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CELL NUCLEUS DNA; COPPER ZINC SUPEROXIDE DISMUTASE; CYTIDINE; GAMMA GLUTAMYLTRANSFERASE; GLITAZONE DERIVATIVE; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HEPATOCYTE NUCLEAR FACTOR 1BETA; HEPATOCYTE NUCLEAR FACTOR 4; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; REACTIVE OXYGEN METABOLITE; SIRTUIN 1; THIOCTIC ACID; THYMIDINE; TRICARBOXYLIC ACID;

AUTOPHAGY; CALORIC RESTRICTION; CAUSAL ATTRIBUTION; CELL DIVISION; CELL FUNCTION; CELL FUSION; CELL STRUCTURE; COPY NUMBER VARIATION; DIABETES MELLITUS; DIABETOGENESIS; DISEASE CLASSIFICATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG TARGETING; ENERGY METABOLISM; ENVIRONMENTAL FACTOR; ETHNIC DIFFERENCE; FETAL MALNUTRITION; GENE STRUCTURE; GENETIC VARIABILITY; HUMAN; INSULIN RELEASE; INSULIN RESISTANCE; MITOCHONDRIAL RESPIRATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; OXIDATIVE PHOSPHORYLATION; PANCREAS ISLET BETA CELL; PANCREAS ISLET DISEASE; POLLUTION; PRIORITY JOURNAL; PROTEIN MALNUTRITION; REVIEW;

EID: 79953738071     PISSN: 20401116     EISSN: 20401124     Source Type: Journal    
DOI: 10.1111/j.2040-1124.2010.00047.x     Document Type: Review

References (106)

1. Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature 2001; 414: 782-787.
2. Yoon KH, Lee JH, Kim JW, et al. Epidemic obesity and type 2 diabetes in Asia. Lancet 2006; 368: 1681-1688.
3. American Diabetes Association. Economic costs of diabetes in the U.S. in 2007. Diabetes Care 2008; 31: 596-615.
4. Wiederkehr A, Wollheim CB. Minireview: implication of mitochondria in insulin secretion and action. Endocrinology 2006; 147: 2643-2649.
5. Wallace DC. Mitochondrial diseases in man and mouse. Science 1999; 283: 1482-1488.
6. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 2005; 39: 359-407.
7. Anderson S, Bankier AT, Barrell BG, et al. Sequence and organization of the human mitochondrial genome. Nature 1981; 290: 457-465.
8. Larsson NG, Wang J, Wilhelmsson H, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 1998; 18: 231-236.
9. Berman SB, Pineda FJ, Hardwick JM. Mitochondrial fission and fusion dynamics: the long and short of it. Cell Death Differ 2008; 15: 1147-1152.
10. Finck BN, Kelly DP. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 2006; 116: 615-622.
11. Kelly DP, Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 2004; 18: 357-368.
12. Canto C, Auwerx J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 2009; 20: 98-105.
13. Wikstrom JD, Twig G, Shirihai OS. What can mitochondrial heterogeneity tell us about mitochondrial dynamics and autophagy? Int J Biochem Cell Biol 2009; 41: 1914-1927.
14. Saraste M. Oxidative phosphorylation at the fin de siecle. Science 1999; 283: 1488-1493.
15. Raha S, Robinson BH. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 2000; 25: 502-508.
16. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13.
17. Greaves LC, Turnbull DM. Mitochondrial DNA mutations and ageing. Biochim Biophys Acta 2009; 1790: 1015-1020.
18. Kokoszka JE, Waymire KG, Levy SE, et al. The ADP/ATP trans-locator is not essential for the mitochondrial permeability transition pore. Nature 2004; 427: 461-465.
19. Ballinger SW, Shoffner JM, Hedaya EV, et al. Maternally transmitted diabetes and deafness associated with a 10.4 kb mitochondrial DNA deletion. Nat Genet 1992; 1: 11-15.
20. van den Ouweland JM, Lemkes HH, Ruitenbeek W, et al. Mutation in mitochondrial tRNA(Leu)(UUR) gene in a large pedigree with maternally transmitted type II diabetes mellitus and deafness. Nat Genet 1992; 1: 368-371.
21. Lee HK, Song JH, Shin CS, et al. Decreased mitochondrial DNA content in peripheral blood precedes the development of non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract 1998; 42: 161-167.
22. Petersen KF, Dufour S, Befroy D, et al. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 2004; 350: 664-671.
23. Maechler P, Wollheim CB. Mitochondrial function in normal and diabetic beta-cells. Nature 2001; 414: 807-812.
24. Maassen JA, Jahangir Tafrechi RS, Janssen GM, et al. New insights in the molecular pathogenesis of the maternally inherited diabetes and deafness syndrome. Endocrinol Metab Clin North Am 2006; 35: 385-396, x-xi.
25. Kadowaki T, Kadowaki H, Mori Y, et al. A subtype of diabetes mellitus associated with a mutation of mitochondrial DNA. N Engl J Med 1994; 330: 962-968.
26. Murphy R, Turnbull DM, Walker M, et al. Clinical features, diagnosis and management of maternally inherited diabetes and deafness (MIDD) associated with the 3243A>G mitochondrial point mutation. Diabet Med 2008; 25: 383-399.
27. Kim SK, Park KS, Shin CS, et al. Mitochondrial DNA point mutations in Korean NIDDM patients. J Korean Diabetes Assoc 1997; 21: 147-155.
28. Lee WJ, Lee HW, Palmer JP, et al. Islet cell autoimmunity and mitochondrial DNA mutation in Korean subjects with typical and atypical Type I diabetes. Diabetologia 2001; 44: 2187-2191.
29. van den Ouweland JM, Lemkes HH, Trembath RC, et al. Maternally inherited diabetes and deafness is a distinct subtype of diabetes and associates with a single point mutation in the mitochondrial tRNA(Leu(UUR)) gene. Diabetes 1994; 43: 746-751.
30. Goto Y, Nonaka I, Horai S. A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature 1990; 348: 651-653.
31. Laloi-Michelin M, Meas T, Ambonville C, et al. The clinical variability of maternally inherited diabetes and deafness is associated with the degree of heteroplasmy in blood leukocytes. J Clin Endocrinol Metab 2009; 94: 3025-3030.
32. Maassen JA, Janssen GM, 't Hart LM. Molecular mechanisms of mitochondrial diabetes (MIDD). Ann Med 2005; 37: 213-221.
33. van den Ouweland JM, Maechler P, Wollheim CB, et al. Functional and morphological abnormalities of mitochondria harbouring the tRNA(Leu)(UUR) mutation in mitochondrial DNA derived from patients with maternally inherited diabetes and deafness (MIDD) and progressive kidney disease. Diabetologia 1999; 42: 485-492.
34. King MP, Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 1989; 246: 500-503.
35. Vaxillaire M, Froguel P. Genetic basis of maturity-onset diabetes of the young. Endocrinol Metab Clin North Am 2006; 35: 371-384, x.
36. Li J, Ning G, Duncan SA. Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev 2000; 14: 464-474.
37. Wang H, Maechler P, Antinozzi PA, et al. Hepatocyte nuclear factor 4alpha regulates the expression of pancreatic beta-cell genes implicated in glucose metabolism and nutrient-induced insulin secretion. J Biol Chem 2000; 275: 35953-35959.
38. Boj SF, Parrizas M, Maestro MA, et al. A transcription factor regulatory circuit in differentiated pancreatic cells. Proc Natl Acad Sci USA 2001; 98: 14481-14486.
39. Pongratz RL, Kibbey RG, Kirkpatrick CL, et al. Mitochondrial dysfunction contributes to impaired insulin secretion in INS-1 cells with dominant-negative mutations of HNF-1alpha and in HNF-1alpha-deficient islets. J Biol Chem 2009; 284: 16808-16821.
40. Gauthier BR, Wiederkehr A, Baquie M, et al. PDX1 deficiency causes mitochondrial dysfunction and defective insulin secretion through TFAM suppression. Cell Metab 2009; 10: 110-118.
41. Fuku N, Park KS, Yamada Y, et al. Mitochondrial haplogroup N9a confers resistance against type 2 diabetes in Asians. Am J Hum Genet 2007; 80: 407-415.
42. Kim JH, Park KS, Cho YM, et al. The prevalence of the mito-chondrial DNA 16189 variant in non-diabetic Korean adults and its association with higher fasting glucose and body mass index. Diabet Med 2002; 19: 681-684.
43. Park KS, Chan JC, Chuang LM, et al. A mitochondrial DNA variant at position 16189 is associated with type 2 diabetes mellitus in Asians. Diabetologia 2008; 51: 602-608.
44. Poulton J, Brown MS, Cooper A, et al. A common mito-chondrial DNA variant is associated with insulin resistance in adult life. Diabetologia 1998; 41: 54-58.
45. Chinnery PF, Elliott HR, Patel S, et al. Role of the mitochondrial DNA 16184-16193 poly-C tract in type 2 diabetes. Lancet 2005; 366: 1650-1651.
46. Ruiz-Pesini E, Mishmar D, Brandon M, et al. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 2004; 303: 223-226.
47. Prokopenko I, McCarthy MI, Lindgren CM. Type 2 diabetes: new genes, new understanding. Trends Genet 2008; 24: 613-621.
48. Sandhu MS, Weedon MN, Fawcett KA, et al. Common variants in WFS1 confer risk of type 2 diabetes. Nat Genet 2007; 39: 951-953.
49. Winckler W, Weedon MN, Graham RR, et al. Evaluation of common variants in the six known maturity-onset diabetes of the young (MODY) genes for association with type 2 diabetes. Diabetes 2007; 56: 685-693.
50. Smith CJ, Crock PA, King BR, et al. Phenotype-genotype correlations in a series of wolfram syndrome families. Diabetes Care 2004; 27: 2003-2009.
51. Takeda K, Inoue H, Tanizawa Y, et al. WFS1 (Wolfram syndrome 1) gene product: predominant subcellular localization to endoplasmic reticulum in cultured cells and neuronal expression in rat brain. Hum Mol Genet 2001; 10: 477-484.
52. Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab 2009; 34: 465-472.
53. Wicks KL, Hood DA. Mitochondrial adaptations in denervated muscle: relationship to muscle performance. Am J Physiol 1991; 260: C841-C850.
54. Anderson EJ, Lustig ME, Boyle KE, et al. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009; 119: 573-581.
55. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 1992; 35: 595-601.
56. Lee YY, Park KS, Pak YK, et al. The role of mitochondrial DNA in the development of type 2 diabetes caused by fetal malnutrition. J Nutr Biochem 2005; 16: 195-204.
57. Park KS, Kim SK, Kim MS, et al. Fetal and early postnatal protein malnutrition cause long-term changes in rat liver and muscle mitochondria. J Nutr 2003; 133: 3085-3090.
58. Park HK, Jin CJ, Cho YM, et al. Changes of mitochondrial DNA content in the male offspring of protein-malnourished rats. Ann N Y Acad Sci 2004; 1011: 205-216.
59. Fisher BE. Most unwanted. Environ Health Perspect 1999; 107: A18-A23.
60. Lee DH, Ha MH, Kim JH, et al. Gamma-glutamyltransferase and diabetes - a 4 year follow-up study. Diabetologia 2003; 46: 359-364.
61. Strange RC, Spiteri MA, Ramachandran S, et al. Glutathione-S-transferase family of enzymes. Mutat Res 2001; 482: 21-26.
62. Lee DH, Jacobs DR Jr. Association between serum concentrations of persistent organic pollutants and gamma glutamyl-transferase: results from the National Health and Examination Survey 1999-2002. Clin Chem 2006; 52: 1825-1827.
63. Pardini RS, Heidker JC, Baker TA, et al. Toxicology of various pesticides and their decomposition products on mitochondrial electron transport. Arch Environ Contam Toxicol 1980; 9: 87-97.
64. Lim S, Ahn SY, Song IC, et al. Chronic exposure to the herbicide, atrazine, causes mitochondrial dysfunction and insulin resistance. PLoS ONE 2009; 4: e5186.
65. Chen SC, Liao TL, Wei YH, et al. Endocrine disruptor, dioxin (TCDD)-induced mitochondrial dysfunction and apoptosis in human trophoblast-like JAR cells. Mol Hum Reprod 2010; 16: 361-372.
66. Song J, Oh JY, Sung YA, et al. Peripheral blood mitochondrial DNA content is related to insulin sensitivity in offspring of type 2 diabetic patients. Diabetes Care 2001; 24: 865-869.
67. 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: 784-787.
68. Weng SW, Lin TK, Liou CW, et al. Peripheral blood mitochondrial DNA content and dysregulation of glucose metabolism. Diabetes Res Clin Pract 2009; 83: 94-99.
69. Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003; 300: 1140-1142.
70. Kim CH, Kim MS, Youn JY, et al. Lipolysis in skeletal muscle is decreased in high-fat-fed rats. Metabolism 2003; 52: 1586-1592.
71. Koh EH, Lee WJ, Kim MS, et al. Intracellular fatty acid metabolism in skeletal muscle and insulin resistance. Curr Diabetes Rev 2005; 1: 331-336.
72. Mootha VK, Lindgren CM, Eriksson KF, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34: 267-273.
73. Patti ME, Butte AJ, Crunkhorn S, et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 2003; 100: 8466-8471.
74. Holland WL, Brozinick JT, Wang LP, et al. Inhibition of cera-mide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 2007; 5: 167-179.
75. Liu L, Zhang Y, Chen N, et al. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest 2007; 117: 1679-1689.
76. Lee WJ, Song KH, Koh EH, et al. Alpha-lipoic acid increases insulin sensitivity by activating AMPK in skeletal muscle. Biochem Biophys Res Commun 2005; 332: 885-891.
77. Kahn BB, Alquier T, Carling D, et al. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 2005; 1: 15-25.
78. Minokoshi Y, Kim YB, Peroni OD, et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 2002; 415: 339-343.
79. Reznick RM, Zong H, Li J, et al. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 2007; 5: 151-156.
80. Lee WJ, Kim M, Park HS, et al. AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPARalpha and PGC-1. Biochem Biophys Res Commun 2006; 340: 291-295.
81. Soriano FX, Liesa M, Bach D, et al. Evidence for a mitochon-drial regulatory pathway defined by peroxisome prolifera-tor-activated receptor-gamma coactivator-1 alpha, estrogen-related receptor-alpha, and mitofusin 2. Diabetes 2006; 55: 1783-1791.
82. Chan DC. Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol 2006; 22: 79-99.
83. Wredenberg A, Freyer C, Sandstrom ME, et al. Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance. Biochem Biophys Res Commun 2006; 350: 202-207.
84. Pospisilik JA, Knauf C, Joza N, et al. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 2007; 131: 476-491.
85. Nair KS, Bigelow ML, Asmann YW, et al. Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance. Diabetes 2008; 57: 1166-1175.
86. Liu S, Okada T, Assmann A, et al. Insulin signaling regulates mitochondrial function in pancreatic beta-cells. PLoS ONE 2009; 4: e7983.
87. Ashcroft FM, Proks P, Smith PA, et al. Stimulus-secretion coupling in pancreatic beta cells. J Cell Biochem 1994; 55(Suppl.): 54-65.
88. Lang J. Molecular mechanisms and regulation of insulin exocytosis as a paradigm of endocrine secretion. Eur J Biochem 1999; 259: 3-17.
89. Lu H, Koshkin V, Allister EM, et al. Molecular and metabolic evidence for mitochondrial defects associated with beta-cell dysfunction in a mouse model of type 2 diabetes. Diabetes 2010; 59: 448-459.
90. Koh EH, Kim MS, Park JY, et al. Peroxisome proliferator-activated receptor (PPAR)-alpha activation prevents diabetes in OLETF rats: comparison with PPAR-gamma activation. Diabetes 2003; 52: 2331-2337.
91. Deng S, Vatamaniuk M, Huang X, et al. Structural and functional abnormalities in the islets isolated from type 2 diabetic subjects. Diabetes 2004; 53: 624-632.
92. Anello M, Lupi R, Spampinato D, et al. Functional and morphological alterations of mitochondria in pancreatic beta cells from type 2 diabetic patients. Diabetologia 2005; 48: 282-289.
93. Twig G, Elorza A, Molina AJ, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 2008; 27: 433-446.
94. Jung HS, Chung KW, Won Kim J, et al. Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab 2008; 8: 318-324.
95. Imai S, Armstrong CM, Kaeberlein M, et al. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 2000; 403: 795-800.
96. Moynihan KA, Grimm AA, Plueger MM, et al. Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. Cell Metab 2005; 2: 105-117.
97. Kitamura YI, Kitamura T, Kruse JP, et al. FoxO1 protects against pancreatic beta cell failure through NeuroD and MafA induction. Cell Metab 2005; 2: 153-163.
98. Rodgers JT, Lerin C, Haas W, et al. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005; 434: 113-118.
99. Lagouge M, Argmann C, Gerhart-Hines Z, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006; 127: 1109-1122.
100. Milne JC, Lambert PD, Schenk S, et al. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 2007; 450: 712-716.
101. Coletta DK, Sriwijitkamol A, Wajcberg E, et al. Pioglitazone stimulates AMP-activated protein kinase signalling and increases the expression of genes involved in adiponectin signalling, mitochondrial function and fat oxidation in human skeletal muscle in vivo: a randomised trial. Diabetologia 2009; 52: 723-732.
102. Schrauwen-Hinderling VB, Mensink M, Hesselink MK, et al. The insulin-sensitizing effect of rosiglitazone in type 2 diabetes mellitus patients does not require improved in vivo muscle mitochondrial function. J Clin Endocrinol Metab 2008; 93: 2917-2921.
103. Song KH, Lee WJ, Koh JM, et al. Alpha-Lipoic acid prevents diabetes mellitus in diabetes-prone obese rats. Biochem Biophys Res Commun 2005; 326: 197-202.
104. Lee WJ, Lee IK, Kim HS, et al. Alpha-lipoic acid prevents endothelial dysfunction in obese rats via activation of AMP-activated protein kinase. Arterioscler Thromb Vasc Biol 2005; 25: 2488-2494.
105. Park KG, Min AK, Koh EH, et al. Alpha-lipoic acid decreases hepatic lipogenesis through adenosine monophosphate-activated protein kinase (AMPK)-dependent and AMPK-independent pathways. Hepatology 2008; 48: 1477-1486.
106. Kim MS, Park JY, Namkoong C, et al. Anti-obesity effects of alpha-lipoic acid mediated by suppression of hypothalamic AMP-activated protein kinase. Nat Med 2004; 10: 727-733.