Respiratory chain dysfunction in skeletal muscle does not cause insulin resistance

Biochemical and Biophysical Research Communications

Volumn 350, Issue 1, 2006, Pages 202-207

  Wredenberg, Anna ^a   Freyer, Christoph ^a   Sandström, Marie E ^b   Katz, Abram ^b   Wibom, Rolf ^a   Westerblad, Håkan ^b   Larsson, Nils Göran ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Diabetes; Insulin resistance; Mitochondria; mtDNA; Oxidative phosphorylation; Respiratory chain

Indexed keywords

GLUCOSE; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; HYPOTHESIS; INSULIN RESISTANCE; KNOCKOUT MOUSE; MITOCHONDRIAL RESPIRATION; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; SKELETAL MUSCLE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ELECTRON TRANSPORT; ENZYME ACTIVATION; GLUCOSE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; INSULIN RESISTANCE; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MULTIENZYME COMPLEXES; MUSCLE, SKELETAL; PROTEIN-SERINE-THREONINE KINASES;

ANIMALIA;

EID: 33749041269     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.09.029     Document Type: Article

References (35)

1. Petersen K.F., and Shulman G.I. Etiology of insulin resistance. Am. J. Med. 119 (2006) S10-S16
2. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstrale M., Laurila E., Houstis N., Daly M.J., Patterson N., Mesirov J.P., Golub T.R., Tamayo P., Spiegelman B., Lander E.S., Hirschhorn J.N., Altshuler D., and Groop L.C. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34 (2003) 267-273
3. Patti M.E., Butte A.J., Crunkhorn S., Cusi K., Berria R., Kashyap S., Miyazaki Y., Kohane I., Costello M., Saccone R., Landaker E.J., Goldfine A.B., Mun E., DeFronzo R., Finlayson J., Kahn C.R., and Mandarino L.J. 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 100 (2003) 8466-8471
4. Petersen K.F., and Shulman G.I. New insights into the pathogenesis of insulin resistance in humans using magnetic resonance spectroscopy. Obesity (Silver Spring) 14 Suppl. 1 (2006) 34S-40S
5. Petersen K.F., Befroy D., Dufour S., Dziura J., Ariyan C., Rothman D.L., DiPietro L., Cline G.W., and Shulman G.I. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300 (2003) 1140-1142
6. Petersen K.F., Dufour S., Befroy D., Garcia R., and Shulman G.I. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350 (2004) 664-671
7. Smeitink J., van den Heuvel L., and DiMauro S. The genetics and pathology of oxidative phosphorylation. Nat. Rev. Genet. 2 (2001) 342-352
8. Knowler W.C., Barrett-Connor E., Fowler S.E., Hamman R.F., Lachin J.M., Walker E.A., and Nathan D.M. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N. Engl. J. Med. 346 (2002) 393-403
9. Wredenberg A., Wibom R., Wilhelmsson H., Graff C., Wiener H.H., Burden S.J., Oldfors A., Westerblad H., and Larsson N.G. Increased mitochondrial mass in mitochondrial myopathy mice. Proc. Natl. Acad. Sci. USA 99 (2002) 15066-15071
10. Shashkin P., Koshkin A., Langley D., Ren J.M., Westerblad H., and Katz A. Effects of CGS 9343B (a putative calmodulin antagonist) on isolated skeletal muscle. Dissociation of signaling pathways for insulin-mediated activation of glycogen synthase and hexose transport. J. Biol. Chem. 270 (1995) 25613-25618
11. Lowry O.H., and Passonneau J.V. A Flexible System of Enzymatic Analysis (1972), Academic Press, New York
12. Sandstrom M.E., Zhang S.J., Bruton J., Silva J.P., Reid M.B., Westerblad H., and Katz A. Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J. Physiol. 575 (2006) 251-262
13. Karlsson H.K., Zierath J.R., Kane S., Krook A., Lienhard G.E., and Wallberg-Henriksson H. Insulin-stimulated phosphorylation of the Akt substrate AS160 is impaired in skeletal muscle of type 2 diabetic subjects. Diabetes 54 (2005) 1692-1697
14. Hansson A., Hance N., Dufour E., Rantanen A., Hultenby K., Clayton D.A., Wibom R., and Larsson N.G. A switch in metabolism precedes increased mitochondrial biogenesis in respiratory chain-deficient mouse hearts. Proc. Natl. Acad. Sci. USA 101 (2004) 3136-3141
15. Bothe G.W., Haspel J.A., Smith C.L., Wiener H.H., and Burden S.J. Selective expression of Cre recombinase in skeletal muscle fibers. Genesis 26 (2000) 165-166
16. Hayashi T., Hirshman M.F., Fujii N., Habinowski S.A., Witters L.A., and Goodyear L.J. Metabolic stress and altered glucose transport: activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49 (2000) 527-531
17. Wojtaszewski J.F., Jorgensen S.B., Hellsten Y., Hardie D.G., and Richter E.A. Glycogen-dependent effects of 5-aminoimidazole-4-carboxamide (AICA)-riboside on AMP-activated protein kinase and glycogen synthase activities in rat skeletal muscle. Diabetes 51 (2002) 284-292
18. Halse R., Fryer L.G., McCormack J.G., Carling D., and Yeaman S.J. Regulation of glycogen synthase by glucose and glycogen: a possible role for AMP-activated protein kinase. Diabetes 52 (2003) 9-15
19. Kelley D.E., He J., Menshikova E.V., and Ritov V.B. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51 (2002) 2944-2950
20. Ritov V.B., Menshikova E.V., He J., Ferrell R.E., Goodpaster B.H., and Kelley D.E. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54 (2005) 8-14
21. Kobayashi T., Nakanishi K., Nakase H., Kajio H., Okubo M., Murase T., and Kosaka K. In situ characterization of islets in diabetes with a mitochondrial DNA mutation at nucleotide position 3243. Diabetes 46 (1997) 1567-1571
22. Maassen J.A., LM T.H., Van Essen E., Heine R.J., Nijpels G., Jahangir Tafrechi R.S., Raap A.K., Janssen G.M., and Lemkes H.H. Mitochondrial diabetes: molecular mechanisms and clinical presentation. Diabetes 53 Suppl. 1 (2004) S103-S109
23. Otabe S., Yasuda K., Mori Y., Shimokawa K., Kadowaki H., Jimi A., Nonaka K., Akanuma Y., Yazaki Y., and Kadowaki T. Molecular and histological evaluation of pancreata from patients with a mitochondrial gene mutation associated with impaired insulin secretion. Biochem. Biophys. Res. Commun. 259 (1999) 149-156
24. Silva J.P., Kohler M., Graff C., Oldfors A., Magnuson M.A., Berggren P.O., and Larsson N.G. Impaired insulin secretion and beta-cell loss in tissue-specific knockout mice with mitochondrial diabetes. Nat. Genet. 26 (2000) 336-340
25. Kennedy E.D., Maechler P., and Wollheim C.B. Effects of depletion of mitochondrial DNA in metabolism secretion coupling in INS-1 cells. Diabetes 47 (1998) 374-380
26. Soejima A., Inoue K., Takai D., Kaneko M., Ishihara H., Oka Y., and Hayashi J.I. Mitochondrial DNA is required for regulation of glucose-stimulated insulin secretion in a mouse pancreatic beta cell line, MIN6. J. Biol. Chem. 271 (1996) 26194-26199
27. Becker R., Laube H., Linn T., and Damian M.S. Insulin resistance in patients with the mitochondrial tRNA(Leu(UUR)) gene mutation at position 3243. Exp. Clin. Endocrinol. Diabetes 110 (2002) 291-297
28. Hardie D.G., and Carling D. The AMP-activated protein kinase-fuel gauge of the mammalian cell?. Eur. J. Biochem. 246 (1997) 259-273
29. Hardie D.G., Salt I.P., Hawley S.A., and Davies S.P. AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem. J. 338 Pt. 3 (1999) 717-722
30. Winder W.W. Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle. J. Appl. Physiol. 91 (2001) 1017-1028
31. Hudson E.R., Pan D.A., James J., Lucocq J.M., Hawley S.A., Green K.A., Baba O., Terashima T., and Hardie D.G. A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr. Biol. 13 (2003) 861-866
32. Polekhina G., Gupta A., Michell B.J., van Denderen B., Murthy S., Feil S.C., Jennings I.G., Campbell D.J., Witters L.A., Parker M.W., Kemp B.E., and Stapleton D. AMPK beta subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13 (2003) 867-871
33. Davies S.P., Sim A.T., and Hardie D.G. Location and function of three sites phosphorylated on rat acetyl-CoA carboxylase by the AMP-activated protein kinase. Eur. J. Biochem. 187 (1990) 183-190
34. Ha J., Daniel S., Broyles S.S., and Kim K.H. Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 269 (1994) 22162-22168
35. Ruderman N.B., Saha A.K., Vavvas D., and Witters L.A. Malonyl-CoA, fuel sensing, and insulin resistance. Am. J. Physiol. 276 (1999) E1-E18