Deficiency of PDK1 in liver results in glucose intolerance, impairment of insulin-regulated gene expression and liver failure

Biochemical Journal

Volumn 385, Issue 3, 2005, Pages 639-648

  Mora, Alfonso ^a   Lipina, Christopher ^b   Tronche, François ^c   Sutherland, Calum ^b   Alessi, Dario R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c l'alimentation et l'Environnement   (France)

Author keywords

3 phospho inositide dependent kinase 1 (PDK1); Gluconeogenesis; Glucose; Insulin; Liver; Phosphorylation

Indexed keywords

BLOOD; DISEASES; GENES; GLUCOSE; INSULIN; LIVING SYSTEMS STUDIES; PROTEINS;

BLOOD GLUCOSE LEVELS; LITTERMATES; MICE;

BIOLOGICAL ORGANS;

GLUCOKINASE; GLUCOSE; GLUCOSE 6 PHOSPHATASE; GLYCOGEN; INSULIN; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); SOMATOMEDIN BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; FEEDING; GENE EXPRESSION REGULATION; GENETIC CODE; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; KNOCKOUT MOUSE; LIVER FAILURE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPECIES COMPARISON;

ANIMALS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GLUCONEOGENESIS; GLUCOSE; GLUCOSE INTOLERANCE; HEPATOCYTES; HOMEOSTASIS; INSULIN; LIVER; LIVER FAILURE; MICE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SURVIVAL RATE;

ANIMALIA;

EID: 13444252573     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041782     Document Type: Article

References (43)

1. Pilkis, S. J. and Granner, D. K. (1992) Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu. Rev. Physiol. 54, 885-909
2. Cherrington, A. D. (1999) Banting Lecture 1997. Control of glucose uptake and release by the liver in vivo. Diabetes 48, 1198-1214
3. Armstrong, C. G., Doherty, M. J. and Cohen, P. T. W. (1998) Identification of the separate domains in the hepatic glycogen-targeting subunit of protein phosphatase 1 that interact with phosphorylase a, glycogen and protein phosphatase 1. Biochem. J. 336, 699-704
4. Bollen, M., Keppens, S. and Stalmans, W. (1998) Specific features of glycogen metabolism in the liver. Biochem. J. 336, 19-31
5. Barthel, A. and Schmoll, D. (2003) Novel concepts in insulin regulation of hepatic gluconeogenesis. Am. J. Physiol. Endocrinol. Metab. 285, E685-E692
6. Michael, M. D., Kulkarni, R. N., Postic, C., Previs, S. F., Shulman, G. I., Magnuson, M. A. and Kahn, C. R. (2000) Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol. Cell. 6, 87-97
7. Kubota, N., Tobe, K., Terauchi, Y., Eto, K., Yamauchi, T., Suzuki, R., Tsubamoto, Y., Komeda, K., Nakano, R., Miki, H. et al. (2000) Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory β-cell hyperplasia. Diabetes 49, 1880-1889
8. Withers, D. J., Gutierrez, J. S., Towery, H., Burks, D. J., Ren, J. M., Previs, S., Zhang, Y., Bernal, D., Pons, S., Shulman, G. I. et al. (1998) Disruption of IRS-2 causes type 2 diabetes in mice. Nature (London) 391, 900-904
9. Miyake, K., Ogawa, W., Matsumoto, M., Nakamura, T., Sakaue, H. and Kasuga, M. (2002) Hyperinsulinemia, glucose intolerance, and dyslipidemia induced by acute inhibition of phosphoinositide 3-kinase signaling in the liver. J. Clin. Invest. 110, 1483-1491
10. Scheid, M. P. and Woodgett, J. R. (2003) Unravelling the activation mechanisms of protein kinase B/Akt. FEBS Lett. 546, 10B-112
11. Avruch, J., Belham, C., Weng, Q., Hara, K. and Yonezawa, K. (2001) The p70 S6 kinase integrates nutrient and growth signals to control translational capacity. Prog. Mol. Subcell. Biol. 26, 115-154
12. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, 3rd, E. B., Kaestner, K. H., Bartolomei, M. S., Shulman, G. I. and Birnbaum, M. J. (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKBβ). Science 292, 1728-1731
13. Mora, A., Komander, D., Van Aalten, D. M. and Alessi, D. R. (2004) PDK1, the master regulator of AGC kinase signal transduction. Semin. Cell. Dev. Biol. 15, 161-170
14. Williams, M. R., Arthur, J. S., Balendran, A., van der Kaay, J., Poli. V., Cohen, P. and Alessi, D. R. (2000) The role of 3-phosphoinositide-dependent protein kinase 1 in activating AGC kinases defined in embryonic stem cells. Curr. Biol. 10, 439-448
15. Sakaue, H., Nishizawa, A., Ogawa, W., Teshigawara, K., Mori, T., Takashima, Y., Noda, T. and Kasuga, M. (2003) Requirement for 3-phosphoinositide-dependent kinase-1 (PDK-1) in insulin-induced glucose uptake in immortalized brown adipocytes. J. Biol. Chem. 278, 38870-38874
16. Mora, A., Davies, A. M., Bertrand, L., Sharif, I., Budas, G. R., Jovanovic, S., Mouton, V., Kahn, C. R., Lucocq, J. M., Gray, G. A. et al. (2003) Deficiency of PDK1 in cardiac muscle results in heart failure and increased sensitivity to hypoxia. EMBO J. 22, 4666-4676
17. Roe, J. H. and Dailey, R. E. (1966) Determination of glycogen with the anthrone reagent. Anal. Biochem. 15, 245-250
18. Lang, G. and Michal, G. (1974) in Methods of Enzymatic Analysis (Bergmeyer, H. U., ed.), pp. 1238-1242, Academic Press, New York
19. Gundersen, H. J. and Jensen, E. B. (1987) The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147, 229-263
20. Lawlor, M. A., Mora, A., Ashby, P. R., Williams, M. R., Murray-Tail, V., Malone, L., Prescott, A. R., Lucocq, J. M. and Alessi, D. R. (2002) Essential role of PDK1 in regulating cell size and development in mice. EMBO J. 21, 3728-3738
21. Kellendonk, C., Opherk, C., Anlag, K., Schutz, G. and Tronche, F. (2000) Hepatocyte-specific expression of Cre recombinase. Genesis 26, 151-153
22. Patel, S., Lochhead, P. A., Rena, G., Fumagalli, S., Pende, M., Kozma, S. C., Thomas, G. and Sutherland, C. (2002) Insulin regulation of insulin-like growth factor-binding protein-1 gene expression is dependent on the mammalian target of rapamycin, but independent of ribosomal S6 kinase activity. J. Biol. Chem. 277, 9889-9895
23. Hall, R. K. and Granner, D. K. (1999) Insulin regulates expression of metabolic genes through divergent signaling pathways. J. Basic Clin. Physiol. Pharmacol. 10, 119-133
24. Ide, T., Shimano, H., Yahagi, N., Matsuzaka, T., Nakakuki, M., Yamamoto, T., Nakagawa, Y., Takahashi, A., Suzuki, H., Sone, H. et al. (2004) SREBPs suppress IRS-2-mediated insulin signalling in the liver. Nat. Cell Biol. 6, 351-357
25. Sutherland, C., O'Brien, R. M. and Granner, D. K. (1997) The regulation of gene transcription by insulin and the search tor diabetogenes. In International Textbook of Diabetes Mellitus, vol. 1 (Alberti, K. G. M. M., Zimmet, R. A., DeFronzo, R. A. and Keen, H., eds.), pp. 489-504, John Wiley & Sons, Chichester
26. Duckworth, W. C. (1988) Insulin degradation: mechanisms, products, and significance. Endocr. Rev. 9, 319-345
27. George, S., Rochford, J. J., Wolfrum, C., Gray, S. L., Schinner, S., Wilson, J. C., Soos, M. A., Murgatroyd, P. R., Williams, R. M., Acerini, C. L. et al. (2004) A family with severe insulin resistance and diabetes due to a mutation in AKT2. Science 304, 1325-1328
28. Kalhan, S. C., Mahajan, S., Burkett, E., Reshef, L. and Hanson, R. W. (2001) Glyceroneogenesis and the source of glycerol for hepatic triacylglycerol synthesis in humans. J. Biol. Chem. 276, 12928-12931
29. O'Brien, R. M., Lucas, P. C., Forest, C. D., Magnuson, M. A. and Granner, D. K. (1990) Identification of a sequence in the PEPCK gene that mediates a negative effect of insulin on transcription. Science 249, 533-537
30. Sutherland, C., O'Brien, R. M. and Granner, D. K. (1995) Phosphatidylinositol 3-kinase, but not p70/p85 ribosomal S6 protein kinase, is required for the regulation of phosphoenolpyruvate carboxykinase (PEPCK) gene expression by insulin: dissociation of signaling pathways for insulin and phorbol ester regulation of PEPCK gene expression. J. Biol. Chem. 270, 15501-15506
31. Band, C. J. and Posner, B. I. (1997) Phosphalidylinositol 3′-kinase and p70s6k are required for insulin but not bisperoxovanadium 1,10-phenanthroline (bpV(phen)) inhibition of insulin-like growth factor binding protein gene expression: evidence for MEK-independent activation of mitogen-activated protein kinase by bpV(phen). J. Biol. Chem. 272, 138-145
32. Dickens, M., Svitek, C. A., Culbert, A. A., O'Brien, R. M. and Tavaré, J. M. (1998) Central role for phosphatidylinositide 3-kinase in the repression of glucose-6-phosphatase gene transcription by insulin. J. Biol. Chem. 273, 20144-20149
33. Zhang, J., Ou, J., Bashmakov, Y., Horlon, J. D., Brown, M. S. and Goldstein, J. L. (2001) Insulin inhibits transcription of IRS-2 gene in rat liver through an insulin response element (IRE) that resembles IREs of other insulin-repressed genes. Proc. Natl. Acad. Sci. U.S.A. 98, 3756-3761
34. Ribaux, P. G. and Iynedjian, P. B. (2003) 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. 376, 697-705
35. Guo, S., Rena, G., Cichy, S., He, X., Cohen, P. and Unlerman, T. (1999) Phosphorylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274, 17184-17192
36. Vander Kooi, B. T., Streeper, R. S., Svitek, C. A., Oeser, J. K., Powell, D. R. and D'Brien, R. M. (2003) The three insulin response sequences in the glucose-6-phosphatase catalytic subunit gene promoter are functionally distinct. J. Biol. Chem. 278, 11782-11793
37. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J. and Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiling a Forkhead transcription factor. Cell 96, 857-868
38. Rena, G., Guo, S., Cichy, S. C., Unterman, T. G. and Cohen, P. (1999) Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274, 17179-17183
39. Chakravarty, K., Wu, S. Y., Chiang, C. M., Samols, D. and Hanson, R. W. (2004) SREBP-1c and Sp1 interact to regulate transcription of the gene for phosphoenolpyruvate carboxykinase (GTP) in the liver. J. Biol. Chem. 279, 15385-15395
40. Frame, S. and Cohen, P. (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359, 1-16
41. Finlay, D., Patel, S., Dickson, L. M., Shpiro, N., Marquez, R., Rhodes, C. J. and Sutherland, C. (2004) Glycogen synthase kinase-3 regulates IGFBP-1 gene transcription through the thymine-rich insulin response element. BMC Mol. Biol. 5, 15
42. Postic, C., Shiota, M., Niswender, K. D., Jelton, T. L., Chen, Y., Moates, J. M., Shelton, K. D., Lindner, J., Cherrington, A. D. and Magnuson, M. A. (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic β-cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem. 274, 305-315
43. Lawlor, M. A. and Alessi, D. R. (2001) PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114, 2903-2910