Enforced expression of protein kinase C in skeletal muscle causes physical inactivity, fatty liver and insulin resistance in the brain

Journal of Cellular and Molecular Medicine

Volumn 14, Issue 4, 2010, Pages 903-913

  Hennige, Anita M ^a   Heni, Martin ^a   Machann, Jürgen ^a   Staiger, Harald ^a   Sartorius, Tina ^a   Hoene, Miriam ^a   Lehmann, Rainer ^a   Weigert, Cora ^a   Peter, Andreas ^a   Bornemann, Antje ^a   Kroeber, Stefan ^b   Pujol, Anna ^c   Franckhauser, Sylvie ^c   Bosch, Fatima ^c   Schick, Fritz ^a   Lammers, Reiner ^a   Häring, Hans Ulrich ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Fatty acid oxidation; Insulin action; Intramyocellular lipid deposition; Lipolysis; NAFLD; Physical activity; Protein kinase C

Indexed keywords

INSULIN; PROTEIN KINASE C; PROTEIN KINASE C BETA;

ANIMAL; ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ARTICLE; BRAIN; C57BL MOUSE; ENZYMOLOGY; FATTY LIVER; GENETICS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; METABOLISM; MOTOR ACTIVITY; MOUSE; OXIDATION REDUCTION REACTION; PATHOLOGY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; BRAIN; FATTY LIVER; INSULIN; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; MUSCLE, SKELETAL; ORGAN SPECIFICITY; OXIDATION-REDUCTION; PHYSICAL CONDITIONING, ANIMAL; PROTEIN KINASE C; SIGNAL TRANSDUCTION; UP-REGULATION;

MUS MUSCULUS;

EID: 77953928057     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00629.x     Document Type: Article

References (49)

1. Roden M. Mechanisms of Disease: hepatic steatosis in type 2 diabetes-pathogenesis and clinical relevance. Nat Clin Pract Endocrinol Metab. 2006, 2:335-48.
2. Michael MD, Kulkarni RN, Postic C. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell. 2000, 6:87-97.
3. Biddinger SB, Hernandez-Ono A, Rask-Madsen C. Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab. 2008, 7:125-34.
4. Tschritter O, Preissl H, Hennige AM. The cerebrocortical response to hyperinsulinemia is reduced in overweight humans: a magnetoencephalographic study. Proc Natl Acad Sci USA. 2006, 103:12103-8.
5. Bruning JC, Gautam D, Burks DJ. Role of brain insulin receptor in control of body weight and reproduction. Science. 2000, 289:2122-25.
6. Nandi A, Kitamura Y, Kahn CR. Mouse models of insulin resistance. Physiol Rev. 2004, 84:623-47.
7. Bruning JC, Michael MD, Winnay JN. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell. 1998, 2:559-69.
8. Charron MJ, Gorovits N, Laidlaw JS. Use of GLUT-4 null mice to study skeletal muscle glucose uptake. Clin Exp Pharmacol Physiol. 2005, 32:308-13.
9. Cariou B, Postic C, Boudou P. Cellular and molecular mechanisms of adipose tissue plasticity in muscle insulin receptor knockout mice. Endocrinology. 2004, 145:1926-32.
10. Mellor H, Parker PJ. The extended protein kinase C superfamily. Biochem J. 1998, 332:281-92.
11. Bandyopadhyay GK, Yu JG, Ofrecio J. Increased p85/55/50 expression and decreased phosphotidylinositol 3-kinase activity in insulin-resistant human skeletal muscle. Diabetes. 2005, 54:2351-59.
12. Farese RV, Sajan MP, Standaert ML. Atypical protein kinase C in insulin action and insulin resistance. Biochem Soc Trans. 2005, 33:350-3.
13. Liberman Z, Plotkin B, Tennenbaum T. Coordinated phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 and protein kinase C{beta}II in the diabetic fat tissue. Am J Physiol Endocrinol Metab 2008, 294:E1169-77.
14. Rajasekar P, Palanisamy N, Anuradha CV. Increase in nitric oxide and reductions in blood pressure, protein kinase C beta II and oxidative stress by L-carnitine: a study in the fructose-fed hypertensive rat. Clin Exp Hypertens. 2007, 29:517-30.
15. Strack V, Hennige AM, Krutzfeldt J. Serine residues 994 and 1023/25 are important for insulin receptor kinase inhibition by protein kinase C isoforms beta2 and theta. Diabetologia. 2000, 43:443-9.
16. Bossenmaier B, Mosthaf L, Mischak H. Protein kinase C isoforms beta 1 and beta 2 inhibit the tyrosine kinase activity of the insulin receptor. Diabetologia. 1997, 40:863-6.
17. Moeschel K, Beck A, Weigert C. Protein kinase C-zeta-induced phosphorylation of Ser318 in insulin receptor substrate-1 (IRS-1) attenuates the interaction with the insulin receptor and the tyrosine phosphorylation of IRS-1. J Biol Chem. 2004, 279:25157-63.
18. Nawaratne R, Gray A, Jorgensen CH. Regulation of insulin receptor substrate 1 pleckstrin homology domain by protein kinase C: role of serine 24 phosphorylation. Mol Endocrinol. 2006, 20:1838-52.
19. Hennige AM, Stefan N, Kapp K. Leptin down-regulates insulin action through phosphorylation of serine-318 in insulin receptor substrate 1. FASEB J. 2006, 20:1206-8.
20. Mussig K, Staiger H, Fiedler H. Shp2 is required for protein kinase c-dependent phosphorylation of serine 307 in insulin receptor substrate-1. J Biol Chem. 2005, 280:32693-9.
21. Rosenthal N, Kornhauser JM, Donoghue M. Myosin light chain enhancer activates muscle-specific, developmentally regulated gene expression in transgenic mice. Proc Natl Acad Sci USA. 1989, 86:7780-4.
22. Donoghue MJ, Merlie JP, Rosenthal N. Rostrocaudal gradient of transgene expression in adult skeletal muscle. Proc Natl Acad Sci USA. 1991, 88:5847-51.
23. Otaegui PJ, Ferre T, Pujol A. Expression of glucokinase in skeletal muscle: a new approach to counteract diabetic hyperglycemia. Hum Gene Ther. 2000, 20:1543-52.
24. Hogan B, Costantini F, Lacy E. Manipulating the mouse embryo. A laboratory manual. 2006, Cold Spring Harbor, New York
25. Chirgwin JM, Przybyla AE, MacDonald RJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979, 18:5294-99.
26. Stefan N, Hennige AM, Staiger H. Alpha2-Heremans-Schmid glycoprotein/fetuin-A is associated with insulin resistance and fat accumulation in the liver in humans. Diabetes Care. 2006, 29:853-7.
27. Hennige AM, Lehmann R, Weigert C. Insulin glulisine: insulin receptor signaling characteristics in vivo. Diabetes. 2005, 54:361-6.
28. Kellerer M, Koch M, Metzinger E. Leptin activates PI-3 kinase in C2C12 myotubes via janus kinase-2 (JAK-2) and insulin receptor substrate-2 (IRS-2)dependent pathways. Diabetologia. 1997, 40:1358-62.
29. Chan TM, Exton JH. A rapid method for the determination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes. Anal Biochem. 1976, 71:96-105.
30. Pirola L, Johnston AM, Van Obberghen E. Modulation of insulin action. Diabetologia. 2004, 47:170-84.
31. Lee YH, White MF. Insulin receptor substrate proteins and diabetes. Arch Pharm Res. 2004, 27:361-70.
32. Hribal ML, Tornei F, Pujol A. Transgenic mice overexpressing human G972R IRS-1 show impaired insulin action and insulin secretion. J Cell Mol Med. 2008, 12:2096-106.
33. Oh YS, Khil LY, Cho KA. A potential role for skeletal muscle caveolin-1 as an insulin sensitivity modulator in ageing-dependent non-obese type 2 diabetes: studies in a new mouse model. Diabetologia. 2008, 51:1025-34.
34. Hennige AM, Staiger H, Wicke C. Fetuin-A induces cytokine expression and suppresses adiponectin production. PLoS ONE. 2008, 3:e1765.
35. Chin JE, Liu F, Roth RA. Activation of protein kinase C alpha inhibits insulin-stimulated tyrosine phosphorylation of insulin receptor substrate-1. Mol Endocrinol. 1994, 8:51-8.
36. Formisano P, Oriente F, Fiory F. Insulin-activated protein kinase Cbeta bypasses Ras and stimulates mitogen-activated protein kinase activity and cell proliferation in muscle cells. Mol Cell Biol. 2000, 20:6323-33.
37. Kim JK, Michael MD, Previs SF. Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J Clin Invest. 2000, 105:1791-7.
38. Cariou B, Postic C, Boudou P. Cellular and molecular mechanisms of adipose tissue plasticity in muscle insulin receptor knockout mice. Endocrinology. 2004, 145:1926-32.
39. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK. Intramyocellular lipid content and molecular adaptations in response to a 1-week high-fat diet. Obes Res. 2005, 13:2088-94.
40. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest. 2000, 106:171-6.
41. Perseghin G, Scifo P, De Cobelli F. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes. 1999, 48:1600-6.
42. Jacob S, Machann J, Rett K. Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes. 1999, 48:1113-9.
43. Patti ME, Butte AJ, Crunkhorn S. 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, 100:8466-71.
44. Arany Z, Lebrasseur N, Morris C. The transcriptional coactivator PGC-1beta drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab. 2007, 5:35-46.
45. Richardson DK, Kashyap S, Bajaj M. Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J Biol Chem. 2005, 280:10290-7.
46. Deng T, Shan S, Li PP. Peroxisome proliferator-activated receptor-gamma transcriptionally up-regulates hormone-sensitive lipase via the involvement of specificity protein-1. Endocrinology. 2006, 147:875-84.
47. Kamei Y, Miura S, Suganami T. Regulation of SREBP1c gene expression in skeletal muscle: role of RXR/LXR and FOXO1. Endocrinology. 2008, 149:2293-330.
48. Mingrone G, Rosa G, Greco AV. Intramyocitic lipid accumulation and SREBP-1c expression are related to insulin resistance and cardiovascular risk in morbid obesity. Atherosclerosis. 2003, 170:155-61.
49. Taguchi A, Wartschow LM, White MF. Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science. 2007, 317:369-72.