Integrin-linked kinase is necessary for the development of diet-induced hepatic insulin resistance

Diabetes

Volumn 66, Issue 2, 2017, Pages 325-334

  Williams, Ashley S ^a   Trefts, Elijah ^a   Lantier, Louise ^a,b   Grueter, Carrie A ^b   Bracy, Deanna P ^a   James, Freyja D ^a   Pozzi, Ambra ^a,b,c   Zent, Roy ^b,c   Wasserman, David H ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL ACYLTRANSFERASE 1; DIACYLGLYCEROL ACYLTRANSFERASE 2; FAS ANTIGEN; FOCAL ADHESION KINASE; GLYCOGEN; INSULIN; INTEGRIN LINKED KINASE; PROTEIN; PROTEIN ACC1; PROTEIN IRS1; PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; UNCLASSIFIED DRUG; INTEGRIN-LINKED KINASE; PROTEIN SERINE THREONINE KINASE; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE DELETION; GENE EXPRESSION; GLUCOSE OXIDATION; GLYCOGEN LIVER LEVEL; IN VIVO STUDY; INSULIN RESISTANCE; LIPID DIET; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; GLUCOSE CLAMP TECHNIQUE; LIVER; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; DIET, HIGH-FAT; EXTRACELLULAR MATRIX; GENE DELETION; GLUCOSE CLAMP TECHNIQUE; INSULIN RESISTANCE; LIVER; MICE; MICE, TRANSGENIC; PROTEIN-SERINE-THREONINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; TRIGLYCERIDES;

EID: 85011636628     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db16-0484     Document Type: Article

References (49)

1. Pehling G, Tessari P, Gerich JE, Haymond MW, Service FJ, Rizza RA. Abnormal meal carbohydrate disposition in insulin-dependent diabetes. Relative contributions of endogenous glucose production and initial splanchnic uptake and effect of intensive insulin therapy. J Clin Invest 1984; 74:985-991
2. DeFronzo RA, Del Prato S. Insulin resistance and diabetes mellitus. J Diabetes Complications 1996;10:243-245
3. Puri P, Baillie RA, Wiest MM, et al. A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 2007;46:1081-1090
4. Samuel VT, Liu ZX, Qu X, et al. Mechanism of hepatic insulin resistance in non-Alcoholic fatty liver disease. J Biol Chem 2004;279:32345-32353
5. Li ZZ, Berk M, McIntyre TM, Feldstein AE. Hepatic lipid partitioning and liver damage in nonalcoholic fatty liver disease: role of stearoyl-CoA desaturase. J Biol Chem 2009;284:5637-5644
6. Williams AS, Kang L, Zheng J, et al. Integrin a1-null mice exhibit improved fatty liver when fed a high fat diet despite severe hepatic insulin resistance. J Biol Chem 2015;290:6546-6557
7. Hynes RO. The extracellular matrix: not just pretty fibrils. Science 2009;326: 1216-1219
8. Kang L, Ayala JE, Lee-Young RS, et al. Diet-induced muscle insulin resistance is associated with extracellular matrix remodeling and interaction with integrin alpha2beta1 in mice. Diabetes 2011;60:416-426
9. Williams AS, Kang L, Wasserman DH. The extracellular matrix and insulin resistance. Trends Endocrinol Metab 2015;26:357-366
10. Wickström SA, Lange A, Montanez E, Fässler R. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! EMBO J 2010;29:281-291
11. Legate KR, Fässler R. Mechanisms that regulate adaptor binding to betaintegrin cytoplasmic tails. J Cell Sci 2009;122:187-198
12. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, et al. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996;379:91-96
13. Lange A, Wickström SA, Jakobson M, Zent R, Sainio K, Fässler R. Integrinlinked kinase is an adaptor with essential functions during mouse development. Nature 2009;461:1002-1006
14. Fukuda K, Gupta S, Chen K, Wu C, Qin J. The pseudoactive site of ILK is essential for its binding to alpha-Parvin and localization to focal adhesions. Mol Cell 2009;36:819-830
15. Qian F, Zhang ZC, Wu XF, Li YP, Xu Q. Interaction between integrin alpha(5) and fibronectin is required for metastasis of B16F10 melanoma cells. Biochem Biophys Res Commun 2005;333:1269-1275
16. Hill MM, Feng J, Hemmings BA. Identification of a plasma membrane Raftassociated PKB Ser473 kinase activity that is distinct from ILK and PDK1. Curr Biol 2002;12:1251-1255
17. Persad S, Attwell S, Gray V, et al. Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase: critical roles for kinase activity and amino acids arginine 211 and serine 343. J Biol Chem 2001;276:27462-27469
18. Di-Poï N, Tan NS, Michalik L, Wahli W, Desvergne B. Antiapoptotic role of PPARbeta in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol Cell 2002;10:721-733
19. Plante I, Charbonneau M, Cyr DG. Activation of the integrin-linked kinase pathway downregulates hepatic connexin32 via nuclear Akt. Carcinogenesis 2006;27:1923-1929
20. Delcommenne M, Tan C, Gray V, Rue L, Woodgett J, Dedhar S. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc Natl Acad Sci U S A 1998;95:11211-11216
21. Troussard AA, Mawji NM, Ong C, Mui A, St-Arnaud R, Dedhar S. Conditional knock-out of integrin-linked kinase demonstrates an essential role in protein kinase B/Akt activation. J Biol Chem 2003;278:22374-22378
22. Zhang Y, Ikegami T, Honda A, et al. Involvement of integrin-linked kinase in carbon tetrachloride-induced hepatic fibrosis in rats. Hepatology 2006;44:612-622
23. Gkretsi V, Mars WM, Bowen WC, et al. Loss of integrin linked kinase from mouse hepatocytes in vitro and in vivo results in apoptosis and hepatitis. Hepatology 2007;45:1025-1034
24. Apte U, Gkretsi V, Bowen WC, et al. Enhanced liver regeneration following changes induced by hepatocyte-specific genetic ablation of integrin-linked kinase. Hepatology 2009;50:844-851
25. Shafiei MS, Rockey DC. The role of integrin-linked kinase in liver wound healing. J Biol Chem 2006;281:24863-24872
26. Gkretsi V, Bowen WC, Yang Y, Wu C, Michalopoulos GK. Integrin-linked kinase is involved in matrix-induced hepatocyte differentiation. Biochem Biophys Res Commun 2007;353:638-643
27. Sakai T, Li S, Docheva D, et al. Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev 2003;17:926-940
28. Terpstra L, Prud'homme J, Arabian A, et al. Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J Cell Biol 2003;162:139-148
29. Ayala JE, Bracy DP, McGuinness OP, Wasserman DH. Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 2006;55:390-397
30. Finegood DT, Bergman RN, Vranic M. Modeling error and apparent isotope discrimination confound estimation of endogenous glucose production during euglycemic glucose clamps. Diabetes 1988;37:1025-1034
31. Steele R, Wall JS, De Bodo RC, Altszuler N. Measurement of size and turnover rate of body glucose pool by the isotope dilution method. Am J Physiol 1956;187:15-24
32. 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
33. Koliwad SK, Streeper RS, Monetti M, et al. DGAT1-dependent triacylglycerol storage by macrophages protects mice from diet-induced insulin resistance and inflammation. J Clin Invest 2010;120:756-767
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-408
35. Gkretsi V, Apte U, Mars WM, et al. Liver-specific ablation of integrin-linked kinase in mice results in abnormal histology, enhanced cell proliferation, and hepatomegaly. Hepatology 2008;48:1932-1941
36. Moik D, Böttcher A, Makhina T, et al. Mutations in the paxillin-binding site of integrin-linked kinase (ILK) destabilize the pseudokinase domain and cause embryonic lethality in mice. J Biol Chem 2013;288:18863-18871
37. Wu C, Dedhar S. Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J Cell Biol 2001;155:505-510
38. Vial G, Dubouchaud H, Couturier K, et al. Effects of a high-fat diet on energy metabolism and ROS production in rat liver. J Hepatol 2011;54:348-356
39. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005;115:1343-1351
40. Postic C, Girard J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest 2008;118:829-838
41. Strömblad G, Björntorp P. Reduced hepatic insulin clearance in rats with dietary-induced obesity. Metabolism 1986;35:323-327
42. Svedberg J, Strömblad G, Wirth A, Smith U, Björntorp P. Fatty acids in the portal vein of the rat regulate hepatic insulin clearance. J Clin Invest 1991;88: 2054-2058
43. Yoshii H, Lam TK, Gupta N, et al. Effects of portal free fatty acid elevation on insulin clearance and hepatic glucose flux. Am J Physiol Endocrinol Metab 2006; 290:E1089-E1097
44. Lynch DK, Ellis CA, Edwards PA, Hiles ID. Integrin-linked kinase regulates phosphorylation of serine 473 of protein kinase B by an indirect mechanism. Oncogene 1999;18:8024-8032
45. Lebrun P, Mothe-Satney I, Delahaye L, Van Obberghen E, Baron V. Insulin receptor substrate-1 as a signaling molecule for focal adhesion kinase pp125(FAK) and pp60(src). J Biol Chem 1998;273:32244-32253
46. Bisht B, Srinivasan K, Dey CS. In vivo inhibition of focal adhesion kinase causes insulin resistance. J Physiol 2008;586:3825-3837
47. Cheung AT, Wang J, Ree D, Kolls JK, Bryer-Ash M. Tumor necrosis factoralpha induces hepatic insulin resistance in obese Zucker (fa/fa) rats via interaction of leukocyte antigen-related tyrosine phosphatase with focal adhesion kinase. Diabetes 2000;49:810-819
48. Huang D, Cheung AT, Parsons JT, Bryer-Ash M. Focal adhesion kinase (FAK) regulates insulin-stimulated glycogen synthesis in hepatocytes. J Biol Chem 2002;277:18151-18160
49. Murthy VK, Shipp JC. Synthesis and accumulation of triglycerides in liver of diabetic rats. Effects of insulin treatment. Diabetes 1979;28:472-478