HIF2α Is an essential molecular brake for postprandial hepatic glucagon response independent of insulin signaling

Cell Metabolism

Volumn 23, Issue 3, 2016, Pages 505-516

  Ramakrishnan, Sadeesh K ^a   Zhang, Huabing ^a   Takahashi, Shogo ^b   Centofanti, Brook ^a   Periyasamy, Sarvesh ^a   Weisz, Kevin ^a   Chen, Zheng ^a   Uhler, Michael D ^a   Rui, Liangyou ^a   Gonzalez, Frank J ^b   Shah, Yatrik M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CREB; ERK; glucagon; HIF2 ; hypoxia; PKA; VHL

Indexed keywords

CYCLIC AMP PHOSPHODIESTERASE; GLUCAGON; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHODIESTERASE IV; PROTEIN KINASE B; PYRUVIC ACID; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; GLUCOSE BLOOD LEVEL; VHL PROTEIN, MOUSE; VON HIPPEL LINDAU PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DRUG MECHANISM; ENZYME ACTIVITY; FEEDING; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HYPERGLYCEMIA; INSULIN SENSITIVITY; LIVER; LIVER CELL; LIVER ISCHEMIA; MOUSE; NONHUMAN; POSTPRANDIAL STATE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; EXPERIMENTAL DIABETES MELLITUS; GENETICS; METABOLISM; PHYSIOLOGY; PRIMARY CELL CULTURE; TRANSGENIC MOUSE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOOD GLUCOSE; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIABETES MELLITUS, EXPERIMENTAL; GLUCAGON; GLUCONEOGENESIS; HEPATOCYTES; HYPERGLYCEMIA; INSULIN; LIVER; MICE, INBRED C57BL; MICE, TRANSGENIC; POSTPRANDIAL PERIOD; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84960809487     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.01.004     Document Type: Article

References (45)

1. M. Abdollahi, T.S. Chan, V. Subrahmanyam, and P.J. O'Brien Effects of phosphodiesterase 3,4,5 inhibitors on hepatocyte cAMP levels, glycogenolysis, gluconeogenesis and susceptibility to a mitochondrial toxin Mol. Cell. Biochem. 252 2003 205 211
2. D. Ackerman, and M.C. Simon Hypoxia, lipids, and cancer: surviving the harsh tumor microenvironment Trends Cell Biol. 24 2014 472 478
3. E.R. Anderson, M. Taylor, X. Xue, A. Martin, D.S. Moons, M.B. Omary, and Y.M. Shah The hypoxia-inducible factor-C/EBPα axis controls ethanol-mediated hepcidin repression Mol. Cell. Biol. 32 2012 4068 4077
4. S.O. Ang, H. Chen, K. Hirota, V.R. Gordeuk, J. Jelinek, Y. Guan, E. Liu, A.I. Sergueeva, G.Y. Miasnikova, D. Mole, and et al. Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia Nat. Genet. 32 2002 614 621
5. A.D. Baron, L. Schaeffer, P. Shragg, and O.G. Kolterman Role of hyperglucagonemia in maintenance of increased rates of hepatic glucose output in type II diabetics Diabetes 36 1987 274 283
6. C. Cherrin, K. Haskell, B. Howell, R. Jones, K. Leander, R. Robinson, A. Watkins, M. Bilodeau, J. Hoffman, P. Sanderson, and et al. An allosteric Akt inhibitor effectively blocks Akt signaling and tumor growth with only transient effects on glucose and insulin levels in vivo Cancer Biol. Ther. 9 2010 493 503
7. S.L. Conarello, G. Jiang, J. Mu, Z. Li, J. Woods, E. Zycband, J. Ronan, F. Liu, R.S. Roy, L. Zhu, and et al. Glucagon receptor knockout mice are resistant to diet-induced obesity and streptozotocin-mediated beta cell loss and hyperglycaemia Diabetologia 50 2007 142 150
8. D.E. Cummings, E.P. Brandon, J.V. Planas, K. Motamed, R.L. Idzerda, and G.S. McKnight Genetically lean mice result from targeted disruption of the RII beta subunit of protein kinase A Nature 382 1996 622 626
9. D. D'Alessio The role of dysregulated glucagon secretion in type 2 diabetes Diabetes Obes. Metab. 13 Suppl 1 2011 126 132
10. R. Dentin, Y. Liu, S.H. Koo, S. Hedrick, T. Vargas, J. Heredia, J. Yates 3rd, and M. Montminy Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2 Nature 449 2007 366 369
11. B.E. Dunning, and J.E. Gerich The role of alpha-cell dysregulation in fasting and postprandial hyperglycemia in type 2 diabetes and therapeutic implications Endocr. Rev. 28 2007 253 283
12. C. Eipel, K. Abshagen, and B. Vollmar Regulation of hepatic blood flow: the hepatic arterial buffer response revisited World J. Gastroenterol. 16 2010 6046 6057
13. J.H. Exton, J.G. Corbin, and S.C. Harper Control of gluconeogenesis in liver. V. Effects of fasting, diabetes, and glucagon on lactate and endogenous metabolism in the perfused rat liver J. Biol. Chem. 247 1972 4996 5003
14. F. Formenti, D. Constantin-Teodosiu, Y. Emmanuel, J. Cheeseman, K.L. Dorrington, L.M. Edwards, S.M. Humphreys, T.R. Lappin, M.F. McMullin, C.J. McNamara, and et al. Regulation of human metabolism by hypoxia-inducible factor Proc. Natl. Acad. Sci. USA 107 2010 12722 12727
15. R.H. Gallavan Jr., and C.C. Chou Possible mechanisms for the initiation and maintenance of postprandial intestinal hyperemia Am. J. Physiol. 249 1985 G301 G308
16. R.W. Gelling, X.Q. Du, D.S. Dichmann, J. Romer, H. Huang, L. Cui, S. Obici, B. Tang, J.J. Holst, C. Fledelius, and et al. Lower blood glucose, hyperglucagonemia, and pancreatic alpha cell hyperplasia in glucagon receptor knockout mice Proc. Natl. Acad. Sci. USA 100 2003 1438 1443
17. V.R. Gordeuk, G.Y. Miasnikova, A.I. Sergueeva, X. Niu, M. Nouraie, D.J. Okhotin, L.A. Polyakova, T. Ammosova, S. Nekhai, T. Ganz, and J.T. Prchal Chuvash polycythemia VHLR200W mutation is associated with down-regulation of hepcidin expression Blood 118 2011 5278 5282
18. K.M. Habegger, K.M. Heppner, N. Geary, T.J. Bartness, R. DiMarchi, and M.H. Tschöp The metabolic actions of glucagon revisited Nat. Rev. Endocrinol. 6 2010 689 697
19. S. Herzig, F. Long, U.S. Jhala, S. Hedrick, R. Quinn, A. Bauer, D. Rudolph, G. Schutz, C. Yoon, P. Puigserver, and et al. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1 Nature 413 2001 179 183
20. M.M. Hickey, J.C. Lam, N.A. Bezman, W.K. Rathmell, and M.C. Simon von Hippel-Lindau mutation in mice recapitulates Chuvash polycythemia via hypoxia-inducible factor-2alpha signaling and splenic erythropoiesis J. Clin. Invest. 117 2007 3879 3889
21. T. Jenssen, N. Nurjhan, A. Consoli, and J.E. Gerich Failure of substrate-induced gluconeogenesis to increase overall glucose appearance in normal humans. Demonstration of hepatic autoregulation without a change in plasma glucose concentration J. Clin. Invest. 86 1990 489 497
22. C. Kim, C.Y. Cheng, S.A. Saldanha, and S.S. Taylor PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation Cell 130 2007 1032 1043
23. S.H. Koo, L. Flechner, L. Qi, X. Zhang, R.A. Screaton, S. Jeffries, S. Hedrick, W. Xu, F. Boussouar, P. Brindle, and et al. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism Nature 437 2005 1109 1111
24. Y. Lee, M.Y. Wang, X.Q. Du, M.J. Charron, and R.H. Unger Glucagon receptor knockout prevents insulin-deficient type 1 diabetes in mice Diabetes 60 2011 391 397
25. G.F. Lewis, M. Vranic, and A. Giacca Glucagon enhances the direct suppressive effect of insulin on hepatic glucose production in humans Am. J. Physiol. 272 1997 E371 E378
26. Y. Liang, M.C. Osborne, B.P. Monia, S. Bhanot, W.A. Gaarde, C. Reed, P. She, T.L. Jetton, and K.T. Demarest Reduction in glucagon receptor expression by an antisense oligonucleotide ameliorates diabetic syndrome in db/db mice Diabetes 53 2004 410 417
27. S.J. MacKenzie, G.S. Baillie, I. McPhee, G.B. Bolger, and M.D. Houslay ERK2 mitogen-activated protein kinase binding, phosphorylation, and regulation of the PDE4D cAMP-specific phosphodiesterases. The involvement of COOH-terminal docking sites and NH2-terminal UCR regions J. Biol. Chem. 275 2000 16609 16617
28. D.A. McClain, K.A. Abuelgasim, M. Nouraie, J. Salomon-Andonie, X. Niu, G. Miasnikova, L.A. Polyakova, A. Sergueeva, D.J. Okhotin, R. Cherqaoui, and et al. Decreased serum glucose and glycosylated hemoglobin levels in patients with Chuvash polycythemia: a role for HIF in glucose metabolism J. Mol. Med. 91 2013 59 67
29. K. Omori, and J. Kotera Overview of PDEs and their regulation Circ. Res. 100 2007 309 327
30. S. Pörksen, L.B. Nielsen, A. Kaas, M. Kocova, F. Chiarelli, C. Orskov, J.J. Holst, K.B. Ploug, P. Hougaard, L. Hansen, H.B. Mortensen Hvidøre Study Group on Childhood Diabetes Meal-stimulated glucagon release is associated with postprandial blood glucose level and does not interfere with glycemic control in children and adolescents with new-onset type 1 diabetes J. Clin. Endocrinol. Metab. 92 2007 2910 2916
31. N.R. Prabhakar, and G.L. Semenza Oxygen Sensing and Homeostasis Physiology (Bethesda) 30 2015 340 348
32. A. Qu, M. Taylor, X. Xue, T. Matsubara, D. Metzger, P. Chambon, F.J. Gonzalez, and Y.M. Shah Hypoxia-inducible transcription factor 2α promotes steatohepatitis through augmenting lipid accumulation, inflammation, and fibrosis Hepatology 54 2011 472 483
33. P. Ramadoss, N.E. Unger-Smith, F.S. Lam, and A.N. Hollenberg STAT3 targets the regulatory regions of gluconeogenic genes in vivo Mol. Endocrinol. 23 2009 827 837
34. S.K. Ramakrishnan, E.R. Anderson, A. Martin, B. Centofanti, and Y.M. Shah Maternal intestinal HIF-2α is necessary for sensing iron demands of lactation in mice Proc. Natl. Acad. Sci. USA 112 2015 E3738 E3747
35. B. Ren, Y. Deng, A. Mukhopadhyay, A.A. Lanahan, Z.W. Zhuang, K.L. Moodie, M.J. Mulligan-Kehoe, T.V. Byzova, R.T. Peterson, and M. Simons ERK1/2-Akt1 crosstalk regulates arteriogenesis in mice and zebrafish J. Clin. Invest. 120 2010 1217 1228
36. M. Schuler, A. Dierich, P. Chambon, and D. Metzger Efficient temporally controlled targeted somatic mutagenesis in hepatocytes of the mouse Genesis 39 2004 167 172
37. Y.M. Shah, S. Ito, K. Morimura, C. Chen, S.H. Yim, V.H. Haase, and F.J. Gonzalez Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade Gastroenterology 134 2008 2036 2048, 2048.e1-2048.e3
38. C.M. Taniguchi, E.C. Finger, A.J. Krieg, C. Wu, A.N. Diep, E.L. LaGory, K. Wei, L.M. McGinnis, J. Yuan, C.J. Kuo, and A.J. Giaccia Cross-talk between hypoxia and insulin signaling through Phd3 regulates hepatic glucose and lipid metabolism and ameliorates diabetes Nat. Med. 19 2013 1325 1330
39. T.F. Tse, W.E. Clutter, S.D. Shah, and P.E. Cryer Mechanisms of postprandial glucose counterregulation in man. Physiologic roles of glucagon and epinephrine vis-a-vis insulin in the prevention of hypoglycemia late after glucose ingestion J. Clin. Invest. 72 1983 278 286
40. R.H. Unger, A.M. Eisentraut, and L.L. Madison The effects of total starvation upon the levels of circulating glucagon and insulin in man J. Clin. Invest. 42 1963 1031 1039
41. J.N. Walker, R. Ramracheya, Q. Zhang, P.R. Johnson, M. Braun, and P. Rorsman Regulation of glucagon secretion by glucose: paracrine, intrinsic or both? Diabetes Obes. Metab. 13 Suppl 1 2011 95 105
42. X. Wang, and A. Schneider HIF-2alpha-mediated activation of the epidermal growth factor receptor potentiates head and neck cancer cell migration in response to hypoxia Carcinogenesis 31 2010 1202 1210
43. K. Wei, S.M. Piecewicz, L.M. McGinnis, C.M. Taniguchi, S.J. Wiegand, K. Anderson, C.W. Chan, K.X. Mulligan, D. Kuo, J. Yuan, and et al. A liver Hif-2α-Irs2 pathway sensitizes hepatic insulin signaling and is modulated by Vegf inhibition Nat. Med. 19 2013 1331 1337
44. T.A. Yap, L. Yan, A. Patnaik, I. Fearen, D. Olmos, K. Papadopoulos, R.D. Baird, L. Delgado, A. Taylor, L. Lupinacci, and et al. First-in-man clinical trial of the oral pan-AKT inhibitor MK-2206 in patients with advanced solid tumors J. Clin. Oncol. 29 2011 4688 4695
45. L. Zheng, C.J. Kelly, and S.P. Colgan Physiologic hypoxia and oxygen homeostasis in the healthy intestine. A Review in the Theme: Cellular Responses to Hypoxia Am. J. Physiol. Cell Physiol. 309 2015 C350 C360