Higher protein kinase C Ζ in fatty rat liver and its effect on insulin actions in primary hepatocytes

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Chen, Wei ^a   Goff, Matthew Ray ^a   Kuang, Heqian ^a   Chen, Guoxun ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GLUCOKINASE; GLUCOSE 6 PHOSPHATASE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; PHOSPHOENOLPYRUVATE CARBOXYKINASE (PYROPHOSPHATE); PROTEIN KINASE B; PROTEIN KINASE C ZETA; SERINE; SOMATOMEDIN BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; THREONINE; ISOENZYME; MESSENGER RNA; PROTEIN KINASE C; PROTEIN KINASE C LAMBDA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME PHOSPHORYLATION; FATTY LIVER; G6PC GENE; GENE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SEQUENCE; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HYPERINSULINEMIA; IGFBP1 GENE; IMMUNOBLOTTING; INSULIN RESISTANCE; LIPID METABOLISM; LIPOGENESIS; LIVER CELL; NONHUMAN; PCK1 GENE; PRKCZ GENE; PROTEIN DEPHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SIGNAL TRANSDUCTION; SREBP 1C GENE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; UPREGULATION; ZUCKER RAT;

ADENOVIRIDAE; RATTUS;

ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FATTY LIVER; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEPATOCYTES; INSULIN; INSULIN RESISTANCE; ISOENZYMES; MALE; PROTEIN KINASE C; RATS; RATS, ZUCKER; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84926628933     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121890     Document Type: Article

References (43)

1. Guan HP, Chen G. Factors Affecting Insulin-Regulated Hepatic Gene Expression. In: Ya-Xiong T, editors. Progress in Molecular Biology and Translational Science: Glucose Homeostatis and the Pathogenesis of Diabetes Mellitus. Academic Press; 2014. pp. 165-215.
2. O'Brien RM, Granner DK. Regulation of gene expression by insulin. Physiol Rev. 1996; 76: 1109-1161. PMID: 8874496
3. White MF. Insulin Signaling in Health and Disease. Science. 2003; 302: 1710-1711. PMID: 14657487
4. Pearce LR, Komander D, Alessi DR The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol. 2010; 11: 9-22. doi: 10.1038/nrm2822 PMID: 20027184
5. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO Journal. 1996; 15: 6541-6551. PMID: 8978681
6. Farese RV, Sajan MP. Metabolic functions of atypical protein kinase C: "good" and "bad" as defined by nutritional status. Am J Physiol Endocrinol Metab. 2010; 298: E385-E394. doi: 10.1152/ajpendo. 00608.2009 PMID: 19996389
7. Sajan MP, Standaert ML, Miura A, Kahn CR, Farese RV. Tissue-Specific Differences in Activation of Atypical Protein Kinase C and Protein Kinase B in Muscle, Liver, and Adipocytes of Insulin Receptor Substrate-1 Knockout Mice. Mol Endocrinol. 2004; 18: 2513-2521. PMID: 15256535
8. Taniguchi CM, Kondo T, Sajan M, Luo J, Bronson R, Asano T, et al. Divergent regulation of hepatic glucose and lipid metabolism by phosphoinositide 3-kinase via Akt and PKC[lambda]/[zeta]. Cell Metab. 2006; 3: 343-353. PMID: 16679292
9. Iynedjian PB, Roth RA, Fleischmann M, Gjinovci A. Activation of protein kinase B/cAkt in hepatocytes is sufficient for the induction of expression of the gene encoding glucokinase. Biochem J. 2000; 351: 621-627. PMID: 11042116
10. Fleischmann M, Iynedjian PB. Regulation of sterol regulatory-element binding protein 1 gene expression in liver: role of insulin and protein kinase B/cAkt. Biochem J. 2000; 349: 13-17. PMID: 10861205
11. Ribaux PG, Iynedjian PB. Analysis of the role of protein kinase B (cAKT) in insulin-dependent induction of glucokinase and sterol regulatory element-binding protein 1 (SREBP1) mRNAs in hepatocytes. Biochem J. 2003; 376: 697-705. PMID: 14505487
12. Matsumoto M, Ogawa W, Akimoto K, Inoue H, Miyake K, Furukawa K, et al. PKCl in liver mediates insulin-induced SREBP-1c expression and determines both hepatic lipid content and overall insulin sensitivity. J Clin Invest, 2003; 112: 935-944. PMID: 12975478
13. Sajan MP, Standaert ML, Nimal S, Varanasi U, Pastoor T, Mastorides S, et al. The critical role of atypical protein kinase C in activating hepatic SREBP-1c and NFkB in obesity. J Lipid Res. 2009; 50: 1133-1145. doi: 10.1194/jlr.M800520-JLR200 PMID: 19202134
14. Farese RV, Sajan MP. Atypical protein kinase C in cardiometabolic abnormalities. Curr Opin Lipidol. 2012; 23: 175-181. doi: 10.1097/MOL.0b013e328352c4c7 PMID: 22449812
15. Sajan M, Standaert M, Rivas J, Miura A, Kanoh Y, Soto J, et al. Role of atypical protein kinase C in activation of sterol regulatory element binding protein-1c and nuclear factor kappa B (NFkB) in liver of rodents used as a model of diabetes, and relationships to hyperlipidaemia and insulin resistance. Diabetologia. 2009; 52: 1197-1207. doi: 10.1007/s00125-009-1336-5 PMID: 19357831
16. Standaert ML, Sajan MP, Miura A, Kanoh Y, Chen HC, Farese RV, et al. Insulin-induced Activation of Atypical Protein Kinase C, but Not Protein Kinase B, Is Maintained in Diabetic (ob/ob and Goto-Kakazaki) Liver. Contrasting insulin signaling patterns in liver versus muscle define phenotypes of type 2 diabetic and high fat-induced insulin-resistant states. J Biol Chem. 2004; 279: 24929-24934. PMID: 15069067
17. Sajan MP, Farese RV. Insulin signalling in hepatocytes of humans with type 2 diabetes: excessive production and activity of protein kinase C-i (PKC-i) and dependent processes and reversal by PKC-i inhibitors. Diabetologia. 2012; 55: 1446-1457. doi: 10.1007/s00125-012-2477-5 PMID: 22349071
18. Sajan MP, Nimal S, Mastorides S, Acevedo-Duncan M, Kahn CR, Fields AP, et al. Correction of metabolic abnormalities in a rodent model of obesity, metabolic syndrome, and type 2 diabetes mellitus by inhibitors of hepatic protein kinase C-i. Metabolism. 2012; 61: 459-469. doi: 10.1016/j.metabol.2011.12.008 PMID: 22225955
19. Sajan M, Ivey R, Farese R. Metformin action in human hepatocytes: coactivation of atypical protein kinase C alters 5'-AMP-activated protein kinase effects on lipogenic and gluconeogenic enzyme expression. Diabetologia. 2013; 56: 2507-2516. doi: 10.1007/s00125-013-3010-1 PMID: 23933835
20. Zucker LM, Antoniades HN. Insulin and Obesity in the Zucker Genetically Obese Rat "Fatty". Endocrinology. 1972; 90: 1320-1330. PMID: 5012744
21. Zhang Y, Chen W, Li R, Li Y, Ge Y, Chen G. Insulin-Regulated Srebp-1c and Pck1 mRNA Expression in Primary Hepatocytes from Zucker Fatty but Not Lean Rats Is Affected by Feeding Conditions. PLoS ONE. 2011; 6: e21342. doi: 10.1371/journal.pone.0021342 PMID: 21731709
22. Chen G, Liang G, Ou J, Goldstein JL, Brown MS. Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc Natl Acad Sci. USA. 2004; 101: 11245-11250. PMID: 15266058
23. Li Y, Zhang Y, Li R, Chen W, Howell M, Zhang R, et al. The Hepatic Raldh1 Expression Is elevated in Zucker Fatty Rats and Its Over-Expression Introduced the Retinal-Induced Srebp-1c Expression in INS-1 Cells. PLoS ONE. 2012; 7: e45210. doi: 10.1371/journal.pone.0045210 PMID: 23028851
24. Iynedjian P. Molecular Physiology of Mammalian Glucokinase. Cell. Mol. Life Sci. 2009; 66: 27-42. doi: 10.1007/s00018-008-8322-9 PMID: 18726182
25. Liu YF, Paz K, Hershkowitz A, Alt A, Tenenboim T, Sampson S, et al. Insulin stimulates PKCzetamediated phosphorylation of insulin receptor substrate-1 (IRS-1): A self-attenuated mechanism to negatively regulate IRS proteins function. J Biol Chem. 2001; 276: 14459-14465. PMID: 11278339
26. Moeschel K, Beck A, Weigert C, Lammers R, Kalbacher H, Voelter W, et al. Protein Kinase C-zetainduced 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: 25157-25163. PMID: 15069075
27. Ravichandran LV, Esposito DL, Chen J, Quon MJ. Protein Kinase C-z Phosphorylates Insulin Receptor Substrate-1 and Impairs Its Ability to Activate Phosphatidylinositol 3-Kinase in Response to Insulin. J Biol Chem. 2001; 276: 3543-3549. PMID: 11063744
28. Hirota K, Sakamaki Ji, Ishida J, Shimamoto Y, Nishihara S, Kodama N, et al. A Combination of HNF-4 and Foxo1 Is Required for Reciprocal Transcriptional Regulation of Glucokinase and Glucose-6-phosphatase Genes in Response to Fasting and Feeding. J Biol Chem. 2008; 283: 32432-32441. doi: 10.1074/jbc.M806179200 PMID: 18805788
29. Kim TH, Kim H, Park JM, Im SS, Bae JS, Kim MY, et al. Interrelationship between Liver X Receptor a, Sterol Regulatory Element-binding Protein-1c, Peroxisome Proliferator-activated Receptor g, and Small Heterodimer Partner in the Transcriptional Regulation of Glucokinase Gene Expression in Liver. J Biol Chem. 2009; 284: 15071-15083. doi: 10.1074/jbc.M109.006742 PMID: 19366697
30. Li R, Zhang R, Li Y, Zhu B, Chen W, Zhang Y, et al. A RARE of hepatic Gck promoter interacts with RARa, HNF4a and COUP-TFII that affect retinoic acid- and insulin-induced Gck expression. J Nut Biochem. 2014; 25: 964-976. doi: 10.1016/j.jnutbio.2014.04.009 PMID: 24973045
31. Roth U, Curth K, Unterman TG, Kietzmann T. The Transcription Factors HIF-1 and HNF-4 and the Coactivator p300 Are Involved in Insulin-regulated Glucokinase Gene Expression via the Phosphatidylinositol 3-Kinase/Protein Kinase B Pathway. J Biol Chem. 2004; 279: 2623-2631. PMID: 14612449
32. Yang J, Reshef L, Cassuto H, Aleman G, Hanson RW. Aspects of the Control of Phosphoenolpyruvate Carboxykinase Gene Transcription. J Biol Chem. 2009; 284: 27031-27035. doi: 10.1074/jbc.R109.040535 PMID: 19636079
33. Barthel A, Schmoll D. Novel concepts in insulin regulation of hepatic gluconeogenesis. Am J Physiol Endocrinol Metab. 2003; 285: E685-E692. PMID: 12959935
34. Matsumoto M, Pocai A, Rossetti L, DePinho RA, Accili D. Impaired Regulation of Hepatic Glucose Production in Mice Lacking the Forkhead Transcription Factor Foxo1 in Liver. Cell Metab. 2007; 6: 208-216. PMID: 17767907
35. Puigserver P, Rhee J, Donovan J, Walkey CJ, Yoon JC, Oriente F, et al. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1[alpha] interaction. Nature. 2003; 423: 550-555. PMID: 12754525
36. He L, Sabet A, Djedjos S, Miller R, Sun X, Hussain MA, et al. Metformin and Insulin Suppress Hepatic Gluconeogenesis through Phosphorylation of CREB Binding Protein. Cell. 2009; 137: 635-646. doi: 10.1016/j.cell.2009.03.016 PMID: 19450513
37. Zhou XY, Shibusawa N, Naik K, Porras D, Temple K, Ou H, et al. Insulin regulation of hepatic gluconeogenesis through phosphorylation of CREB-binding protein. Nat Med. 2004; 10: 633-637. PMID: 15146178
38. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest. 2002; 109: 1125-1131. PMID: 11994399
39. Li S, Brown MS, Goldstein JL. Bifurcation of insulin signaling pathway in rat liver: mTORC1 required for stimulation of lipogenesis, but not inhibition of gluconeogenesis. Proc Natl Acad Sci. USA. 2010; 107: 3441-3446. doi: 10.1073/pnas.0914798107 PMID: 20133650
40. Owen JL, Zhang Y, Bae SH, Farooqi MS, Liang G, Hammer RE, et al. Insulin stimulation of SREBP-1c processing in transgenic rat hepatocytes requires p70 S6-kinase. Proc Natl Acad Sci. USA. 2012; 109: 16184-16189. doi: 10.1073/pnas.1213343109 PMID: 22927400
41. Chen W, Howell ML, Li Y, Li R, Chen G. Vitamin A and Feeding Statuses Modulate the Insulin-Regulated Gene Expression in Zucker Lean and Fatty Primary Rat Hepatocytes. PLoS ONE 2014; 9: e100868. doi: 10.1371/journal.pone.0100868 PMID: 25105869
42. Liu HY, Hong T, Wen GB, Han J, Zuo D, Liu Z, et al. Increased basal level of Akt-dependent insulin signaling may be responsible for the development of insulin resistance. Am J Physiol Endocrinol Metab. 2009; 297: E898-E906. doi: 10.1152/ajpendo.00374.2009 PMID: 19638508
43. Sajan MP, Acevedo-Duncan ME, Standaert ML, Ivey RA, Lee M, Farese RV. Akt-Dependent Phosphorylation of Hepatic FoxO1 Is Compartmentalized on a WD40/ProF Scaffold and Is Selectively Inhibited by aPKC in Early Phases of Diet-Induced Obesity. Diabetes 2014; 63: 2690-2701. doi: 10.2337/db13-1863 PMID: 24705403