The dipeptidyl peptidase-4 inhibitor teneligliptin attenuates hepatic lipogenesis via AMPK activation in non-alcoholic fatty liver disease model mice

International Journal of Molecular Sciences

Volumn 16, Issue 12, 2015, Pages 29207-29218

  Ideta, Takayasu ^a   Shirakami, Yohei ^a   Miyazaki, Tsuneyuki ^a   Kochi, Takahiro ^a   Sakai, Hiroyasu ^a   Moriwaki, Hisataka ^a   Shimizu, Masahito ^a  

^a GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

AMPK; DPP 4 inhibitor; Lipogenesis; NAFLD; Non alcoholic fatty liver disease; SREBP1c; Teneligliptin

Indexed keywords

ALANINE AMINOTRANSFERASE; FATTY ACID; GLUCOSE; GLUTAMATE SODIUM; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; INSULIN; PHOSPHOPROTEIN; TENELIGLIPTIN; TRIACYLGLYCEROL; 3-(4-(4-(3-METHYL-1-PHENYL-1H-PYRAZOL-5-YL)PIPERAZIN-1-YL)PYRROLIDIN-2-YLCARBONYL)THIAZOLIDINE; BIOLOGICAL MARKER; DIPEPTIDYL PEPTIDASE IV INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PYRAZOLE DERIVATIVE; THIAZOLIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CLINICAL CHEMISTRY; CLINICAL TRIAL (TOPIC); CONTROLLED STUDY; DOWN REGULATION; FATTY LIVER; GENE EXPRESSION; HISTOPATHOLOGY; LIPID DIET; LIPOGENESIS; MALE; MESSENGER RNA; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; ENZYME ACTIVATION; LIPID METABOLISM; LIVER; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BIOMARKERS; DIPEPTIDYL-PEPTIDASE IV INHIBITORS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; LIPID METABOLISM; LIVER; MALE; MICE; NON-ALCOHOLIC FATTY LIVER DISEASE; PHOSPHORYLATION; PYRAZOLES; SIGNAL TRANSDUCTION; THIAZOLIDINES; TRIGLYCERIDES;

EID: 84949424443     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161226156     Document Type: Article

References (50)

1. Calle, E.E.; Rodriguez, C.; Walker-Thurmond, K.; Thun, M.J. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 2003, 348, 1625-1638. [CrossRef] [PubMed]
2. Chalasani, N.; Younossi, Z.; Lavine, J.E.; Diehl, A.M.; Brunt, E.M.; Cusi, K.; Charlton, M.; Sanyal, A.J. The diagnosis and management of non-alcoholic fatty liver disease: Practice guideline by the american association for the study of liver diseases, american college of gastroenterology, and the american gastroenterological association. Hepatology 2012, 55, 2005-2023. [CrossRef] [PubMed]
3. Sass, D.A.; Chang, P.; Chopra, K.B. Nonalcoholic fatty liver disease: A clinical review. Dig. Dis. Sci. 2005, 50, 171-180. [CrossRef] [PubMed]
4. Bacon, B.R.; Farahvash, M.J.; Janney, C.G.; Neuschwander-Tetri, B.A. Nonalcoholic steatohepatitis: An expanded clinical entity. Gastroenterology 1994, 107, 1103-1109. [PubMed]
5. Kim, C.H.; Younossi, Z.M. Nonalcoholic fatty liver disease: A manifestation of the metabolic syndrome. Clevel. Clin. J. Med. 2008, 75, 721-728.
6. Vanni, E.; Bugianesi, E.; Kotronen, A.; De Minicis, S.; Yki-Jarvinen, H.; Svegliati-Baroni, G. From the metabolic syndrome to NAFLD or vice versa? Dig. Liver Dis. 2010, 42, 320-330. [CrossRef] [PubMed]
7. Ascha, M.S.; Hanouneh, I.A.; Lopez, R.; Tamimi, T.A.; Feldstein, A.F.; Zein, N.N. The incidence and risk factors of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis. Hepatology 2010, 51, 1972-1978. [CrossRef] [PubMed]
8. Marchesini, G.; Brizi, M.; Morselli-Labate, A.M.; Bianchi, G.; Bugianesi, E.; McCullough, A.J.; Forlani, G.; Melchionda, N. Association of nonalcoholic fatty liver disease with insulin resistance. Am. J. Med. 1999, 107, 450-455. [CrossRef]
9. Sanyal, A.J.; American Gastroenterological, A. Aga technical review on nonalcoholic fatty liver disease. Gastroenterology 2002, 123, 1705-1725. [CrossRef] [PubMed]
10. Shimizu, M.; Yasuda, Y.; Sakai, H.; Kubota, M.; Terakura, D.; Baba, A.; Ohno, T.; Kochi, T.; Tsurumi, H.; Tanaka, T. et al. Pitavastatin suppresses diethylnitrosamine-induced liver preneoplasms in male C57BL/KsJ-db/db obese mice. BMC Cancer 2011, 11, 281. [CrossRef] [PubMed]
11. Shimizu, M.; Sakai, H.; Shirakami, Y.; Yasuda, Y.; Kubota, M.; Terakura, D.; Baba, A.; Ohno, T.; Hara, Y.; Tanaka, T. et al. Preventive effects of (_)-epigallocatechin gallate on diethylnitrosamine-induced liver tumorigenesis in obese and diabetic C57BL/KsJ-db/db mice. Cancer Prev. Res. 2011, 4, 396-403. [CrossRef] [PubMed]
12. Ohno, T.; Shimizu, M.; Shirakami, Y.; Baba, A.; Kochi, T.; Kubota, M.; Tsurumi, H.; Tanaka, T.; Moriwaki, H. Metformin suppresses diethylnitrosamine-induced liver tumorigenesis in obese and diabetic C57BL/KsJ-+Leprdb/+Leprdb mice. PLoS ONE 2015, 10, e0124081. [CrossRef] [PubMed]
13. Lonardo, A.; Ballestri, S.; Marchesini, G.; Angulo, P.; Loria, P. Nonalcoholic fatty liver disease: A precursor of the metabolic syndrome. Dig. Liver Dis. 2015, 47, 181-190. [CrossRef] [PubMed]
14. Zhang, Y.; Zhang, T.; Zhang, C.; Tang, F.; Zhong, N.; Li, H.; Song, X.; Lin, H.; Liu, Y.; Xue, F. Identification of reciprocal causality between non-alcoholic fatty liver disease and metabolic syndrome by a simplified bayesian network in a chinese population. BMJ Open 2015, 5, e008204. [CrossRef] [PubMed]
15. Aschner, P.; Kipnes, M.S.; Lunceford, J.K.; Sanchez, M.; Mickel, C.; Williams-Herman, D.E.; Sitagliptin Study, G. Effect of the dipeptidyl peptidase-4 inhibitor sitagliptin as monotherapy on glycemic control in patients with type 2 diabetes. Diabetes Care 2006, 29, 2632-2637. [CrossRef] [PubMed]
16. Pi-Sunyer, F.X.; Schweizer, A.; Mills, D.; Dejager, S. Efficacy and tolerability of vildagliptin monotherapy in drug-naive patients with type 2 diabetes. Diabetes Res. Clin. Pract. 2007, 76, 132-138. [CrossRef] [PubMed]
17. Gupta, N.A.; Mells, J.; Dunham, R.M.; Grakoui, A.; Handy, J.; Saxena, N.K.; Anania, F.A. 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 2010, 51, 1584-1592. [CrossRef] [PubMed]
18. Trevaskis, J.L.; Griffin, P.S.; Wittmer, C.; Neuschwander-Tetri, B.A.; Brunt, E.M.; Dolman, C.S.; Erickson, M.R.; Napora, J.; Parkes, D.G.; Roth, J.D. Glucagon-like peptide-1 receptor agonism improves metabolic, biochemical, and histopathological indices of nonalcoholic steatohepatitis in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302, G762-G772. [CrossRef] [PubMed]
19. Klein, T.; Fujii, M.; Sandel, J.; Shibazaki, Y.; Wakamatsu, K.; Mark, M.; Yoneyama, H. Linagliptin alleviates hepatic steatosis and inflammation in a mouse model of non-alcoholic steatohepatitis. Med. Mol. Morphol. 2014, 47, 137-149. [CrossRef] [PubMed]
20. Balaban, Y.H.; Korkusuz, P.; Simsek, H.; Gokcan, H.; Gedikoglu, G.; Pinar, A.; Hascelik, G.; Asan, E.; Hamaloglu, E.; Tatar, G. Dipeptidyl peptidase IV (DDP IV) in nash patients. Ann. Hepatol. 2007, 6, 242-250. [PubMed]
21. Schuppan, D.; Gorrell, M.D.; Klein, T.; Mark, M.; Afdhal, N.H. The challenge of developing novel pharmacological therapies for non-alcoholic steatohepatitis. Liver Int. 2010, 30, 795-808. [CrossRef] [PubMed]
22. Yilmaz, Y.; Atug, O.; Yonal, O.; Duman, D.; Ozdogan, O.; Imeryuz, N.; Kalayci, C. Dipeptidyl peptidase IV inhibitors: Therapeutic potential in nonalcoholic fatty liver disease. Med. Sci. Res. 2009, 15, HY1-5. [CrossRef]
23. Collison, K.S.; Makhoul, N.J.; Zaidi, M.Z.; Al-Rabiah, R.; Inglis, A.; Andres, B.L.; Ubungen, R.; Shoukri, M.; Al-Mohanna, F.A. Interactive effects of neonatal exposure to monosodium glutamate and aspartame on glucose homeostasis. Nutr. Metabol. 2012, 9, 58. [CrossRef] [PubMed]
24. Nagata, M.; Suzuki, W.; Iizuka, S.; Tabuchi, M.; Maruyama, H.; Takeda, S.; Aburada, M.; Miyamoto, K. Type 2 diabetes mellitus in obese mouse model induced by monosodium glutamate. Exp. Anim. Jpn. Assoc. Lab. Anim. Sci. 2006, 55, 109-115. [CrossRef]
25. Roman-Ramos, R.; Almanza-Perez, J.C.; Garcia-Macedo, R.; Blancas-Flores, G.; Fortis-Barrera, A.; Jasso, E.I.; Garcia-Lorenzana, M.; Campos-Sepulveda, A.E.; Cruz, M.; Alarcon-Aguilar, F.J. Monosodium glutamate neonatal intoxication associated with obesity in adult stage is characterized by chronic inflammation and increased mRNA expression of peroxisome proliferator-activated receptors in mice. Basic Clin. Pharmacol. Toxicol. 2011, 108, 406-413. [CrossRef] [PubMed]
26. Kleiner, D.E.; Brunt, E.M.; Van Natta, M.; Behling, C.; Contos, M.J.; Cummings, O.W.; Ferrell, L.D.; Liu, Y.C.; Torbenson, M.S.; Unalp-Arida, A. et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005, 41, 1313-1321. [CrossRef] [PubMed]
27. Li, Y.; Xu, S.; Mihaylova, M.M.; Zheng, B.; Hou, X.; Jiang, B.; Park, O.; Luo, Z.; Lefai, E.; Shyy, J.Y. et al. AMPK phosphorylates and inhibits Srebp activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metabol. 2011, 13, 376-388. [CrossRef] [PubMed]
28. Serviddio, G.; Bellanti, F.; Vendemiale, G. Free radical biology for medicine: Learning from nonalcoholic fatty liver disease. Free Radic. Biol. Med. 2013, 65, 952-968. [CrossRef] [PubMed]
29. Blaslov, K.; Bulum, T.; Zibar, K.; Duvnjak, L. Incretin based therapies: A novel treatment approach for non-alcoholic fatty liver disease. World J. Gastroenterol. 2014, 20, 7356-7365. [CrossRef] [PubMed]
30. Shimizu, M.; Sakai, H.; Shirakami, Y.; Iwasa, J.; Yasuda, Y.; Kubota, M.; Takai, K.; Tsurumi, H.; Tanaka, T.; Moriwaki, H. Acyclic retinoid inhibits diethylnitrosamine-induced liver tumorigenesis in obese and diabetic C57BLKS/J-+leprdb/+leprdb mice. Cancer Prev. Res. 2011, 4, 128-136. [CrossRef] [PubMed]
31. Misu, H.; Takamura, T.; Takayama, H.; Hayashi, H.; Matsuzawa-Nagata, N.; Kurita, S.; Ishikura, K.; Ando, H.; Takeshita, Y.; Ota, T. et al. A liver-derived secretory protein, selenoprotein p, causes insulin resistance. Cell Metabol. 2010, 12, 483-495. [CrossRef] [PubMed]
32. Choi, H.Y.; Hwang, S.Y.; Lee, C.H.; Hong, H.C.; Yang, S.J.; Yoo, H.J.; Seo, J.A.; Kim, S.G.; Kim, N.H.; Baik, S.H. et al. Increased selenoprotein p levels in subjects with visceral obesity and nonalcoholic fatty liver disease. Diabetes Metabol. J. 2013, 37, 63-71. [CrossRef] [PubMed]
33. Musso, G.; Gambino, R.; Cassader, M. Recent insights into hepatic lipid metabolism in non-alcoholic fatty liver disease (NAFLD). Progress Lipid Res. 2009, 48, 1-26. [CrossRef] [PubMed]
34. Higuchi, N.; Kato, M.; Shundo, Y.; Tajiri, H.; Tanaka, M.; Yamashita, N.; Kohjima, M.; Kotoh, K.; Nakamuta, M.; Takayanagi, R. et al. Liver X receptor in cooperation with Srebp-1c is a major lipid synthesis regulator in nonalcoholic fatty liver disease. Hepatol. Res. 2008, 38, 1122-1129. [CrossRef] [PubMed]
35. Kern, M.; Kloting, N.; Niessen, H.G.; Thomas, L.; Stiller, D.; Mark, M.; Klein, T.; Bluher, M. Linagliptin improves insulin sensitivity and hepatic steatosis in diet-induced obesity. PLoS ONE 2012, 7, e38744. [CrossRef] [PubMed]
36. Singh, S.; Khera, R.; Allen, A.M.; Murad, M.H.; Loomba, R. Comparative effectiveness of pharmacological interventions for nonalcoholic steatohepatitis: A systematic review and network meta-analysis. Hepatology 2015, 62, 1417-1432. [CrossRef] [PubMed]
37. Shirakami, Y.; Shimizu, M.; Kubota, M.; Ohno, T.; Kochi, T.; Nakamura, N.; Sumi, T.; Tanaka, T.; Moriwaki, H.; Seishima, M. Pentoxifylline prevents nonalcoholic steatohepatitis-related liver pre-neoplasms by inhibiting hepatic inflammation and lipogenesis. Eur. J. Cancer Prev. 2015. [CrossRef] [PubMed]
38. Hardie, D.G.; Ross, F.A.; Hawley, S.A. Ampk: A nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13, 251-262. [CrossRef] [PubMed]
39. Viollet, B.; Mounier, R.; Leclerc, J.; Yazigi, A.; Foretz, M.; Andreelli, F. Targeting AMP-activated protein kinase as a novel therapeutic approach for the treatment of metabolic disorders. Diabetes Metab. 2007, 33, 395-402. [CrossRef] [PubMed]
40. Ben-Shlomo, S.; Zvibel, I.; Shnell, M.; Shlomai, A.; Chepurko, E.; Halpern, Z.; Barzilai, N.; Oren, R.; Fishman, S. Glucagon-like peptide-1 reduces hepatic lipogenesis via activation of AMP-activated protein kinase. J. Hepatol. 2011, 54, 1214-1223. [CrossRef] [PubMed]
41. Svegliati-Baroni, G.; Saccomanno, S.; Rychlicki, C.; Agostinelli, L.; de Minicis, S.; Candelaresi, C.; Faraci, G.; Pacetti, D.; Vivarelli, M.; Nicolini, D. et al. Glucagon-like peptide-1 receptor activation stimulates hepatic lipid oxidation and restores hepatic signalling alteration induced by a high-fat diet in nonalcoholic steatohepatitis. Liver Int. 2011, 31, 1285-1297. [CrossRef] [PubMed]
42. Lee, J.; Hong, S.W.; Chae, S.W.; Kim, D.H.; Choi, J.H.; Bae, J.C.; Park, S.E.; Rhee, E.J.; Park, C.Y.; Oh, K.W.; et al. Exendin-4 improves steatohepatitis by increasing Sirt1 expression in high-fat diet-induced obese C57BL/6J mice. PLoS ONE 2012, 7, e31394. [CrossRef] [PubMed]
43. Samson, S.L.; Bajaj, M. Potential of incretin-based therapies for non-alcoholic fatty liver disease. J. Diabetes Complicat. 2013, 27, 401-406. [CrossRef] [PubMed]
44. Boschmann, M.; Engeli, S.; Dobberstein, K.; Budziarek, P.; Strauss, A.; Boehnke, J.; Sweep, F.C.; Luft, F.C.; He, Y.; Foley, J.E. et al. Dipeptidyl-peptidase-IV inhibition augments postprandial lipid mobilization and oxidation in type 2 diabetic patients. J. Clin. Endocrinol. Metab. 2009, 94, 846-852. [CrossRef] [PubMed]
45. The Japanese Association for Laboratory Animal Science (JALAS). Available online: http://www.jalas.jp/english/en_about_jalas.html (accessed on 26 July 2013).
46. Shimizu, M.; Shirakami, Y.; Iwasa, J.; Shiraki, M.; Yasuda, Y.; Hata, K.; Hirose, Y.; Tsurumi, H.; Tanaka, T.; Moriwaki, H. Supplementation with branched-chain amino acids inhibits azoxymethane-induced colonic preneoplastic lesions in male C57BL/KsJ-db/db mice. Clin. Cancer Res. 2009, 15, 3068-3075. [CrossRef] [PubMed]
47. Primer Blast. Available online: http://www.ncbi.nlm.nih.gov/tools/primer-blast/ (accessed on 26 July 2013).
48. Folch, J.; Lees, M.; Sloane Stanley, G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226, 497-509. [PubMed]
49. Iwasa, J.; Shimizu, M.; Shiraki, M.; Shirakami, Y.; Sakai, H.; Terakura, Y.; Takai, K.; Tsurumi, H.; Tanaka, T.; Moriwaki, H. Dietary supplementation with branched-chain amino acids suppresses diethylnitrosamine-induced liver tumorigenesis in obese and diabetic C57BL/KsJ-db/db mice. Cancer Sci. 2010, 101, 460-467. [CrossRef] [PubMed]
50. Miyazaki, M.; Kato, M.; Tanaka, K.; Tanaka, M.; Kohjima, M.; Nakamura, K.; Enjoji, M.; Nakamuta, M.; Kotoh, K.; Takayanagi, R. Increased hepatic expression of dipeptidyl peptidase-4 in non-alcoholic fatty liver disease and its association with insulin resistance and glucose metabolism. Mol. Med. Rep. 2012, 5, 729-733. [CrossRef] [PubMed]