Activation of Wnt/β-catenin signaling increases insulin sensitivity through a reciprocal regulation of Wnt10B and SREBP-1c in skeletal muscle cells

PLoS ONE

Volumn 4, Issue 12, 2009, Pages

  Abiola, Mounira ^a,b   Favier, Maryline ^a,b   Christodoulou Vafeiadou, Eleni ^a,b   Pichard, Anne Lise ^a,b   Martelly, Isabelle ^c   Guillet Deniau, Isabelle ^a,b,d  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

^c Université Paris 12 ^*  (France)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; WNT PROTEIN; WNT10B PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; GENE SILENCING; GLUCOSE TRANSPORT; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID STORAGE; MALE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; RAT; REGENERATIVE MEDICINE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL;

ADENYLATE KINASE; ANIMALS; BETA CATENIN; BIOLOGICAL TRANSPORT; CELLS, CULTURED; DEOXYGLUCOSE; DOWN-REGULATION; GENE SILENCING; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; GLYCOGEN SYNTHASE KINASE 3; INDOLES; INSULIN; LIPID METABOLISM; MAP KINASE SIGNALING SYSTEM; MICE; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MYOBLASTS; OXIMES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RNA, MESSENGER; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; WNT PROTEINS;

EID: 77954036677     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008509     Document Type: Article

References (46)

1. Kanazawa A, Tsukada S, Sekine A, Tsunoda T, Takahashi A, et al. (2004) Association of the gene encoding wingless-type mammary tumor virus integration-site family member 5B (WNT5B) with type 2 diabetes. Am J Hum Genet 75: 832-843.
2. Welters HJ, Kulkarni RN (2008) Wnt signaling: relevance to beta-cell biology and diabetes. Trends Endocrinol Metab 19: 349-355.
3. Anagnostou SH, Shepherd PR (2008) Glucose induces an autocrine activation of the Wnt/beta-catenin pathway in macrophage cell lines. Biochem J 416: 211-218.
4. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R (1997) beta-catenin is a target for the ubiquitin-proteasome pathway. Embo J 16: 3797-3804.
5. Cossu G, Borello U (1999) Wnt signaling and the activation of myogenesis in mammals. Embo J 18: 6867-6872.
6. Ridgeway AG, Petropoulos H, Wilton S, Skerjanc IS (2000) Wnt signaling regulates the function of MyoD and myogenin. J Biol Chem 275: 32398-32405.
7. Miller JR (2002) The Wnts. Genome Biol 3: REVIEWS3001.
8. Unger RH, Orci L (2001) Diseases of liporegulation: new perspective on obesity and related disorders. Faseb J 15: 312-321.
9. Virkamaki A, Korsheninnikova E, Seppala-Lindroos A, Vehkavaara S, Goto T, et al. (2001) Intramyocellular lipid is associated with resistance to in vivo insulin actions on glucose uptake, antilipolysis, and early insulin signaling pathways in human skeletal muscle. Diabetes 50: 2337-2343.
10. Machann J, Haring H, Schick F, Stumvoll M (2004) Intramyocellular lipids and insulin resistance. Diabetes Obes Metab 6: 239-248.
11. Shimomura I, Bashmakov Y, Ikemoto S, Horton JD, Brown MS, et al. (1999) Insulin selectively increases SREBP-1c mRNA in the livers of rats with streptozotocin-induced diabetes. Proc Natl Acad Sci U S A 96: 13656-13661.
12. Foretz M, Guichard C, Ferre P, Foufelle F (1999) Sterol regulatory element binding protein-1c is a major mediator of insulin action on the hepatic expression of glucokinase and lipogenesis-related genes [see comments]. Proc Natl Acad Sci U S A 96: 12737-12742.
13. Foretz M, Pacot C, Dugail I, Lemarchand P, Guichard C, et al. (1999) ADD1/SREBP-1c is required in the activation of hepatic lipogenic gene expression by glucose. Mol Cell Biol 19: 3760-3768.
14. Ducluzeau PH, Perretti N, Laville M, Andreelli F, Vega N, et al. (2001) Regulation by insulin of gene expression in human skeletal muscle and adipose tissue. Evidence for specific defects in type 2 diabetes. Diabetes 50: 1134-1142.
15. Guillet-Deniau I, Mieulet V, Le Lay S, Achouri Y, Carre D, et al. (2002) Sterol regulatory element binding protein-1c expression and action in rat muscles: insulin-like effects on the control of glycolytic and lipogenic enzymes and UCP3 gene expression. Diabetes 51: 1722-1728.
16. Taylor-Jones JM, McGehee RE, Rando TA, Lecka-Czernik B, Lipschitz DA, et al. (2002) Activation of an adipogenic program in adult myoblasts with age. Mech Ageing Dev 123: 649-661.
17. Prestwich TC, Macdougald OA (2007) Wnt/beta-catenin signaling in adipogenesis and metabolism. Curr Opin Cell Biol 19: 612-617.
18. Sabourin LA, Rudnicki MA (2000) The molecular regulation of myogenesis. Clin Genet 57: 16-25.
19. Grimaldi PA, Teboul L, Inadera H, Gaillard D, Amri EZ (1997) Transdifferentiation of myoblasts to adipoblasts: triggering effects of fatty acids and thiazolidinediones. Prostaglandins Leukot Essent Fatty Acids 57: 71-75.
20. Teboul L, Gaillard D, Staccini L, Inadera H, Amri EZ, et al. (1995) Thiazolidinediones and fatty acids convert myogenic cells into adipose-like cells. J Biol Chem 270: 28183-28187.
21. Aguiari P, Leo S, Zavan B, Vindigni V, Rimessi A, et al. (2008) High glucose induces adipogenic differentiation of muscle-derived stem cells. Proc Natl Acad Sci U S A 105: 1226-1231.
22. Bassaglia Y, Gautron J (1995) Fast and slow rat muscles degenerate and regenerate differently after whole crush injury. J Muscle Res Cell Motil 16: 420-429.
23. Bhat RV, Shanley J, Correll MP, Fieles WE, Keith RA, et al. (2000) Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc Natl Acad Sci U S A 97: 11074-11079.
24. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specificinhibitor. Nat Med 10: 55-63.
25. Guillet-Deniau I, Pichard AL, Kone A, Esnous C, Nieruchalski M, et al. (2004) Glucose induces de novo lipogenesis in rat muscle satellite cells through a sterolregulatory-element-binding-protein-1c-dependent pathway. J Cell Sci 117: 1937-1944.
26. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, et al. (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. Embo J 15: 6541-6551.
27. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101.
28. Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1: 15-25.
29. Jensen TE, Schjerling P, Viollet B, Wojtaszewski JF, Richter EA (2008) AMPK alpha1 activation is required for stimulation of glucose uptake by twitch contraction, but not by H2O2, in mouse skeletal muscle. PLoS ONE 3: e2102.
30. Meijer L, Skaltsounis AL, Magiatis P, Polychronopoulos P, Knockaert M, et al. (2003) GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 10: 1255-1266.
31. Takata H, Terada K, Oka H, Sunada Y, Moriguchi T, et al. (2007) Involvement of Wnt4 signaling during myogenic proliferation and differentiation of skeletal muscle. Dev Dyn 236: 2800-2807.
32. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, et al. (2000) Inhibition of adipogenesis by Wnt signaling. Science 289: 950-953.
33. Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, et al. (2002) Regulation of Wnt signaling during adipogenesis. J Biol Chem 277: 30998-31004.
34. Bizeau ME, MacLean PS, Johnson GC, Wei Y (2003) Skeletal muscle sterol regulatory element binding protein-1c decreases with food deprivation and increases with feeding in rats. J Nutr 133: 1787-1792.
35. Vertino AM, Taylor-Jones JM, Longo KA, Bearden ED, Lane TF, et al. (2005) Wnt10b deficiency promotes coexpression of myogenic and adipogenic programs in myoblasts. Mol Biol Cell 16: 2039-2048.
36. Simoneau JA, Colberg SR, Thaete FL, Kelley DE (1995) Skeletal muscle glycolytic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women. Faseb J 9: 273-278.
37. Miyake K, Ogawa W, Matsumoto M, Nakamura T, Sakaue H, et al. (2002) Hyperinsulinemia, glucose intolerance, and dyslipidemia induced by acute inhibition of phosphoinositide 3-kinase signaling in the liver. J Clin Invest 110: 1483-1491.
38. Cusi K, Maezono K, Osman A, Pendergrass M, Patti ME, et al. (2000) Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 105: 311-320.
39. Nadeau KJ, Leitner JW, Gurerich I, Draznin B (2004) Insulin regulation of sterol regulatory element-binding protein-1 expression in L-6 muscle cells and 3T3 L1 adipocytes. J Biol Chem 279: 34380-34387.
40. Hara K, Yonezawa K, Sakaue H, Ando A, Kotani K, et al. (1994) 1- Phosphatidylinositol 3-kinase activity is required for insulin-stimulated glucose transport but not for RAS activation in CHO cells. Proc Natl Acad Sci U S A 91: 7415-7419.
41. Etgen GJ Jr, Fryburg DA, Gibbs EM (1997) Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction- and phosphatidylinositol-3-kinase-independent pathway. Diabetes 46: 1915-1919.
42. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ (1998) Evidence for 59 AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes 47: 1369-1373.
43. Zahler S, Tietze S, Totzke F, Kubbutat M, Meijer L, et al. (2007) Inverse in silico screening for identification of kinase inhibitor targets. Chem Biol 14: 1207-1214.
44. Bouzakri K, Zachrisson A, Al-Khalili L, Zhang BB, Koistinen HA, et al. (2006) siRNA-based gene silencing reveals specialized roles of IRS-1/Akt2 and IRS-2/ Akt1 in glucose and lipid metabolism in human skeletal muscle. Cell Metab 4: 89-96.
45. Guillet-Deniau I, Leturque A, Girard J (1994) Expression and cellular localization of glucose transporters (GLUT1, GLUT3, GLUT4) during differentiation of myogenic cells isolated from rat foetuses. J Cell Sci 107: 487-496.
46. Koopman R, Schaart G, Hesselink MK (2001) Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol 116: 63-68.