The glucagon-like peptide-1 receptor agonist exendin 4 has a protective role in ischemic injury of lean and steatotic liver by inhibiting cell death and stimulating lipolysis

American Journal of Pathology

Volumn 181, Issue 5, 2012, Pages 1693-1701

  Gupta, Nitika A ^a,b   Kolachala, Vasantha L ^a   Jiang, Rong ^a   Abramowsky, Carlos ^a   Romero, Rene ^a,b   Fifadara, Nimita ^a   Anania, Frank ^a   Knechtle, Stuart ^a,b   Kirk, Allan ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHILDREN'S HEALTHCARE OF ATLANTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; EXENDIN 4; FAT DROPLET; HORMONE SENSITIVE LIPASE; PERILIPIN; TRIACYLGLYCEROL;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; FAT CONTENT; LIPOLYSIS; LIVER CELL; LIVER INJURY; LIVER NECROSIS; LIVER PROTECTION; LIVER TRANSPLANTATION; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PERIOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; TREATMENT DURATION; TRIACYLGLYCEROL BLOOD LEVEL;

3T3-L1 CELLS; ADIPOSITY; ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL LINE, TUMOR; FATTY LIVER; HEPATOCYTES; HUMANS; LIPOLYSIS; LIVER; MALE; MICE; MICE, INBRED C57BL; NECROSIS; PEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTECTIVE AGENTS; RECEPTORS, GLUCAGON; REPERFUSION INJURY; STEROL ESTERASE; THINNESS; VENOMS;

EID: 84868120544     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.07.015     Document Type: Article

References (50)

1. C.P. Day Non-alcoholic fatty liver disease: a massive problem Clinical Med 11 2011 176 178
2. I.A. Hanouneh, N.N. Zein Metabolic syndrome and liver transplantation Minerva Gastroenterol Dietol 56 2010 297 304
3. M. Selzner, P.A. Clavien Fatty liver in liver transplantation and surgery Semin Liver Dis 21 2001 105 113 (Pubitemid 32240490)
4. D. Gomez, H.Z. Malik, G.K. Bonney, V. Wong, G.J. Toogood, J.P. Lodge, K.R. Prasad Steatosis predicts postoperative morbidity following hepatic resection for colorectal metastasis Br J Surg 94 2007 1395 1402 (Pubitemid 350144389)
5. R. Vetelainen, A. van Vliet, D.J. Gouma, T.M. van Gulik Steatosis as a risk factor in liver surgery Ann Surg 245 2007 20 30 (Pubitemid 46035431)
6. K.D. Chavin, R.N. Fiorini, S. Shafizadeh, G. Cheng, C. Wan, Z. Evans, D. Rodwell, C. Polito, J.K. Haines, G.M. Baillie, M.G. Schmidt Fatty acid synthase blockade protects steatotic livers from warm ischemia reperfusion injury and transplantation Am J Transplant 4 2004 1440 1447 (Pubitemid 39159058)
7. A. Marcos, J.M. Ham, R.A. Fisher, A.T. Olzinski Posner: Single-center analysis of the first 40 adult-to-adult living donor liver transplants using the right lobe Liver Transpl 6 2000 296 301 (Pubitemid 30317224)
8. P.J. Matheson, R.T. Hurt, G.A. Franklin, C.J. McClain, R.N. Garrison Obesity-induced hepatic hypoperfusion primes for hepatic dysfunction after resuscitated hemorrhagic shock Surgery 146 2009 739 748
9. M. Selzner, P.A. Clavien Failure of regeneration of the steatotic rat liver: disruption at two different levels in the regeneration pathway Hepatology 31 2000 35 42 (Pubitemid 30033686)
10. P.A. Clavien, M. Selzner Hepatic steatosis and transplantation Liver Transpl 8 2002 980
11. F.E. Sharkey, I. Lytvak, T.J. Prihoda, K.V. Speeg, W.K. Washburn, G.A. Halff High-grade microsteatosis and delay in hepatic function after orthotopic liver transplantation Hu Pathol 42 2011 1337 1342
12. Y. Cheng, C. Chen, C.Y. Lai, T. Chen, T. Huang, T. Lee, C. Lin, R. Lord, Y. Chen, H. Eng, T.L. Pan, T.H. Lee, Y.H. Wang, Y. Iwashita, Kitano, S. Goto Assessment of donor fatty livers for liver transplantation Transplantation 71 2001 1206 1207
13. P. Sorrentino, L. Terracciano, S. D'Angelo, U. Ferbo, A. Bracigliano, L. Tarantino, A. Perrella, O. Perrella, G. De Chiara, L. Panico, N. De Stefano, M. Lepore, Mariolina, R. Vecchione Oxidative stress and steatosis are cofactors of liver injury in primary biliary cirrhosis J Gastroenterol 45 2010 1053 1062
14. B. Thorens, G. Waeber Glucagon-like peptide-I and the control of insulin secretion in the normal state and in NIDDM Diabetes 42 1993 1219 1225 (Pubitemid 23259839)
15. A. Acitores, N. Gonzalez, V. Sancho, I. Valverde, M.L. Villanueva-Penacarrillo Cell signalling of glucagon-like peptide-1 action in rat skeletal muscle J Endocrinol 180 2004 389 398 (Pubitemid 38443391)
16. D.J. Drucker Biological actions and therapeutic potential of the glucagon-like peptides Gastroenterology 122 2002 531 544 (Pubitemid 34117003)
17. K. Ban, M.H. Noyan-Ashraf, J. Hoefer, S.S. Bolz, D.J. Drucker, M. Husain Cardioprotective and vasodilatory actions of glucagon-like peptide 1 receptor are mediated through both glucagon-like peptide 1 receptor-dependent and -independent pathways Circulation 117 2008 2340 2350 (Pubitemid 351653542)
18. L.L. Baggio, D. Holland, J. Wither, D.J. Drucker Lymphocytic infiltration and immune activation in metallothionein promoter-exendin-4 (MT-Exendin) transgenic mice Diabetes 55 2006 1562 1570 (Pubitemid 44324108)
19. E. Alvarez, I. Roncero, J.A. Chowen, B. Thorens, E. Blazquez Expression of the glucagon-like peptide-1 receptor gene in rat brain J Neurochem 66 1996 920 927 (Pubitemid 26065887)
20. N.A. Gupta, J. Mells, R.M. Dunham, A. Grakoui, J. Handy, N.K. Saxena, F.A. Anania Glucagon-like peptide-1 receptor is present on human hepatocytes and has a direct role in decreasing hepatic steatosis in vitro by modulating elements of the insulin signaling pathway Hepatology 51 2010 1584 1592
21. X. Ding, N.K. Saxena, S. Lin, N.A. Gupta, F.A. Anania Exendin-4, a glucagon-like protein-1 (GLP-1) receptor agonist, reverses hepatic steatosis in ob/ob mice Hepatology 43 2006 173 181 (Pubitemid 43733604)
22. L. Li, W. El-Kholy, C.J. Rhodes, P.L. Brubaker Glucagon-like peptide-1 protects beta cells from cytokine-induced apoptosis and necrosis: role of protein kinase B Diabetologia 48 2005 1339 1349 (Pubitemid 41186100)
23. R. Cursio, P. Colosetti, M.C. Saint-Paul, S. Pagnotta, P. Gounon, A. Iannelli, P. Auberger, J. Gugenheim Induction of different types of cell death after normothermic liver ischemia-reperfusion Transplant Proc 42 2010 3977 3980
24. A. Marcinkiewicz, D. Gauthier, A. Garcia, D.L. Brasaemle The phosphorylation of serine 492 of perilipin a directs lipid droplet fragmentation and dispersion J Biol Chem 281 2006 11901 11909 (Pubitemid 43855452)
25. P.M. McDonough, R.S. Ingermanson, P.A. Loy, E.D. Koon, R. Whittaker, C.A. Laris, J.M. Hilton, J.B. Nicoll, B.M. Buehrer, J.H. Price Quantification of hormone sensitive lipase phosphorylation and colocalization with lipid droplets in murine 3T3L1 and human subcutaneous adipocytes via automated digital microscopy and high-content analysis Assay Drug Dev Technol 9 2011 262 280
26. S. Ali, B.J. Lamont, M.J. Charron, D.J. Drucker Dual elimination of the glucagon and GLP-1 receptors in mice reveals plasticity in the incretin axis J Clin Invest 121 2011 1917 1929
27. B.J. Lamont, Y. Li, E. Kwan, T.J. Brown, H. Gaisano, D.J. Drucker Pancreatic GLP-1 receptor activation is sufficient for incretin control of glucose metabolism in mice J ClinI Invest 122 2012 388 402
28. C. Cabou, C. Vachoux, G. Campistron, D.J. Drucker, R. Burcelin Brain GLP-1 signaling regulates femoral artery blood flow and insulin sensitivity through hypothalamic PKC-delta Diabetes 60 2011 2245 2256
29. L. Axelsen, W. Keung, H. Pedersen, E. Meier, D. Riber, A. Kjolbye, J. Petersen, S. Proctor, N.H. Holstein-Rathlou, G. Lopaschuk Glucagon and a glucagon-GLP-1 dual-agonist increases cardiac performance with different metabolic effects in insulin-resistant hearts Br J Clin Pharmacol 165 2012 2736 2748
30. L. Chaykovska, K. von Websky, J. Rahnenfuhrer, M. Alter, S. Heiden, H. Fuchs, F. Runge, T. Klein, B. Hocher Effects of DPP-4 inhibitors on the heart in a rat model of uremic cardiomyopathy PloS One 6 2011 e27861
31. J. Hlebowicz, S. Lindstedt, O. Bjorgell, M. Dencker The effect of endogenously released glucose, insulin, glucagon-like peptide 1, ghrelin on cardiac output, heart rate, stroke volume, and blood pressure Cardiovasc Ultrasound 9 2011 43
32. T. Suzuki, H. Yoshidome, F. Kimura, H. Shimizu, M. Ohtsuka, D. Takeuchi, A. Kato, K. Furukawa, H. Yoshitomi, A. Iida, T. Dochi, M. Miyazaki Hepatocyte apoptosis is enhanced after ischemia/reperfusion in the steatotic liver J Clin Biochem Nutr 48 2011 142 148
33. A.V. Savateev, T.N. Savateeva-Liubimova [Apoptosis-universal mechanisms of cell death and survival in ischemia and reperfusion: ways to pharmacological control] Eksp Klin Farmakol 73 2010 44 49
34. W.H. Xu, Q.F. Ye, S.S. Xia Apoptosis and proliferation of intrahepatic bile duct after ischemia-reperfusion injury Hepatobiliary Pancreat Dis Int 3 2004 428 432 (Pubitemid 39173080)
35. H. Jaeschke, J.S. Gujral, M.L. Bajt Apoptosis and necrosis in liver disease Liver Int 24 2004 85 89 (Pubitemid 38584992)
36. M. Marzioni, G. Alpini, S. Saccomanno, C. Candelaresi, J. Venter, C. Rychlicki, G. Fava, H. Francis, L. Trozzi, A. Benedetti Exendin-4, a glucagon-like peptide 1 receptor agonist, protects cholangiocytes from apoptosis Gut 58 2009 990 997
37. A.K. Bose, M.M. Mocanu, R.D. Carr, D.M. Yellon Myocardial ischaemia-reperfusion injury is attenuated by intact glucagon like peptide-1 (GLP-1) in the in vitro rat heart and may involve the p70s6K pathway Cardiovasc Drugs Ther 21 2007 253 256 (Pubitemid 47387464)
38. S. Martin, R.G. Parton Lipid droplets: a unified view of a dynamic organelle Nat Rev Mol Cell Biol 7 2006 373 378
39. N. Krahmer, Y. Guo, R.V. Farese Jr, T.C. Walther SnapShot: lipid droplets Cell 139 2009 1024-1024
40. N. Selzner, M. Selzner, W. Jochum, B. Amann-Vesti, R. Graf, P.A. Clavien Mouse livers with macrosteatosis are more susceptible to normothermic ischemic injury than those with microsteatosis J Hepatol 44 2006 694 701
41. A. Marcinkiewicz, D. Gauthier, A. Garcia, D.L. Brasaemle The phosphorylation of serine 492 of perilipin a directs lipid droplet fragmentation and dispersion J Biol Chem 281 2006 11901 11909 (Pubitemid 43855452)
42. Y. Guo, T.C. Walther, M. Rao, N. Stuurman, G. Goshima, K. Terayama, J.S. Wong, R.D. Vale, P. Walter, R.V. Farese Functional genomic screen reveals genes involved in lipid-droplet formation and utilization Nature 453 2008 657 661 (Pubitemid 351769298)
43. J.T. Tansey, C. Sztalryd, E.M. Hlavin, A.R. Kimmel, C. Londos The central role of perilipin a in lipid metabolism and adipocyte lipolysis IUBMB Life 56 2004 379 385 (Pubitemid 39564301)
44. C. Londos, C. Sztalryd, J.T. Tansey, A.R. Kimmel Role of PAT proteins in lipid metabolism Biochimie 87 2005 45 49 (Pubitemid 40305232)
45. C. Sztalryd, G. Xu, H. Dorward, J.T. Tansey, J.A. Contreras, A.R. Kimmel, C. Londos Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation J Cell Biol 161 2003 1093 1103 (Pubitemid 36870171)
46. R. Zechner, P.C. Kienesberger, G. Haemmerle, R. Zimmermann, A. Lass Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores J Lipid Res 50 2009 3 21
47. D.L. Brasaemle, V. Subramanian, A. Garcia, A. Marcinkiewicz, A. Rothenberg Perilipin A and the control of triacylglycerol metabolism Mol Cell Biochem 326 2009 15 21
48. W.J. Shen, S. Patel, H. Miyoshi, A.S. Greenberg, F.B. Kraemer Functional interaction of hormone-sensitive lipase and perilipin in lipolysis J Lipid Res 50 2009 2306 2313
49. C. Londos, C. Sztalryd, J.T. Tansey, A.R. Kimmel Role of PAT proteins in lipid metabolism Biochimie 87 2005 45 49 (Pubitemid 40305232)
50. R.V. Farese Jr., T.C. Walther Lipid droplets finally get a little R-E-S-P-E-C-T Cell 139 2009 855 860