Forced expression of fibroblast growth factor 21 reverses the sustained impairment of liver regeneration in PPARαPAC mice due to dysregulated bile acid synthesis

Oncotarget

Volumn 6, Issue 12, 2015, Pages 9686-9700

  Liu, Hui Xin ^a   Hu, Ying ^a   French, Samuel W ^b   Gonzalez, Frank J ^c   Wan, Yu Jui Yvonne ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARBOR UCLA MEDICAL CENTER   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Bile acid; Metabolism; Nuclear receptor; Proliferation; Species differences

Indexed keywords

ADENOVIRUS VECTOR; ALPHA SMOOTH MUSCLE ACTIN; BILE ACID; CARNITINE PALMITOYLTRANSFERASE I; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA 1; CYCLIN A; CYCLIN B; CYCLIN D; CYCLIN E; CYTOKERATIN 1; CYTOKERATIN 19; CYTOKERATIN 6; FIBROBLAST GROWTH FACTOR 21; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MYC PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; FIBROBLAST GROWTH FACTOR; KI 67 ANTIGEN; MICRORNA; MIRNLET7 MICRORNA, MOUSE;

ALPHASMA GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHROPOMETRIC PARAMETERS; ARTICLE; BILE; BILE ACID SYNTHESIS; CDK1 GENE; CDK6 GENE; CELL PROLIFERATION; CK19 GENE; COL1A1 GENE; CONTROLLED STUDY; CPT1 GENE; CYCLIN A GENE; CYCLIN B GENE; CYCLIN D GENE; CYCLIN E GENE; CYP4A10 GENE; CYP4A14 GENE; DIET RESTRICTION; DOWN REGULATION; DRUG ACTIVITY; FATTY LIVER; FOCAL NECROSIS; GENE; GENE EXPRESSION REGULATION; GENE TARGETING; HUMAN; HUMAN CELL; HYDROPHOBICITY; IL 6 GENE; IL6 GENE; INFLAMMATION; LET 7C GENE; LIPID HOMEOSTASIS; LIVER; LIVER FIBROSIS; LIVER GROWTH; LIVER NECROSIS; LIVER REGENERATION; LIVER SIZE; LIVER TO BODY WEIGHT RATIO; MCP1 GENE; MOUSE; NONHUMAN; NRF2 GENE; ONCOGENE C MYC; PARTIAL HEPATECTOMY; PATHOGENESIS; PEPCK GENE; PGC1A GENE; PROTEIN EXPRESSION; PROTEIN METABOLISM; SIGNAL TRANSDUCTION; TISSUE GROWTH; TNFA GENE; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT; ADENOVIRIDAE; ANIMAL; BODY WEIGHT; CHEMISTRY; FIBROSIS; GENETICS; HOMEOSTASIS; LIVER RESECTION; MALE; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ADENOVIRIDAE; ANIMALS; BILE ACIDS AND SALTS; BODY WEIGHT; FATTY LIVER; FIBROBLAST GROWTH FACTORS; FIBROSIS; GENE EXPRESSION REGULATION; HEPATECTOMY; HOMEOSTASIS; HUMANS; INFLAMMATION; KI-67 ANTIGEN; LIVER; LIVER REGENERATION; MALE; MICE; MICE, TRANSGENIC; MICRORNAS; POLYMERASE CHAIN REACTION; PPAR ALPHA; SIGNAL TRANSDUCTION;

EID: 84929590429     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3531     Document Type: Article

References (49)

1. Liu HX, Fang Y, Hu Y, Gonzalez FJ, Fang J, Wan YJ. PPARbeta Regulates Liver Regeneration by Modulating Akt and E2f Signaling. PLoS One. 2013;8:e65644.
2. Gazit V, Huang J, Weymann A, Rudnick DA. Analysis of the role of hepatic PPARgammaexpression during mouse liver regeneration. Hepatology. 2012;56:1489-1498.
3. Shteyer E, Liao YJ, Muglia LJ, Hruz PW, Rudnick DA. Disruption of hepatic adipogenesis is associated with impaired liver regeneration in mice. Hepatology. 2004;40:1322-1332.
4. Yang SQ, Lin HZ, Mandal AK, Huang JW, Diehl AM. Disrupted signaling and inhibited regeneration in obese mice with fatty livers: Implications for nonalcoholic fatty liver disease pathophysiology. Hepatology. 2001;34:694-706.
5. Leclercq IA, Field J, Farrell GC. Leptin-specific mechanisms for impaired liver regeneration in ob/ob mice after toxic injury. Gastroenterology. 2003;124:1451-1464.
6. Anderson SP, Yoon L, Richard EB, Dunn CS, Cattley RC, Corton JC. Delayed liver regeneration in peroxisome proliferator-activated receptor-alpha-null mice. Hepatology. 2002;36:544-554.
7. Wheeler MD, Smutney OM, Check JF, Rusyn I, Schulte-Hermann R, Thurman RG. Impaired Ras membrane association and activation in PPAR alpha knockout mice after partial hepatectomy. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2003;284:G302-G312.
8. Yang Q, Nagano T, Shah Y, Cheung C, Ito S, Gonzalez FJ. The PPAR alpha-humanized mouse: A model to investigate species differences in liver toxicity mediated by PPAR alpha. Toxicological Sciences. 2008;101:132-139.
9. Klaunig JE, Babich MA, Baetcke KP, Cook JC, Corton JC, David RM, DeLuca JG, Lai DY, McKee RH, Peters JM, Roberts RA, Fenner-Crisp PA. PPARalpha agonist-induced rodent tumors: modes of action and human relevance. Crit Rev Toxicol. 2003;33:655-780.
10. Elias-Miro M, Jimenez-Castro MB, Mendes-Braz M, Casillas-Ramirez A, Peralta C. The Current Knowledge of the Role of PPAR in Hepatic Ischemia-Reperfusion Injury. Ppar Research. 2012; 2012:802384.
11. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, Maratos-Flier E. Hepatic fibroblast growth factor 21 is regulated by PPAR alpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metabolism. 2007;5:426-437.
12. Owen BM, Ding XS, Morgan DA, Coate KC, Bookout AL, Rahmouni K, Kliewer SA, Mangelsdorf DJ. FGF21 Acts Centrally to Induce Sympathetic Nerve Activity, Energy Expenditure, and Weight Loss. Cell Metabolism. 2014;20:670-677.
13. Kliewer SA, Mangelsdorf DJ. Fibroblast growth factor 21:from pharmacology to physiology. American Journal of Clinical Nutrition. 2010;91:254s-257s.
14. Johnson CL, Weston JY, Chadi SA, Fazio EN, Huff MW, Kharitonenkov A, Koester A, et al. Fibroblast Growth Factor 21 Reduces the Severity of Cerulein-Induced Pancreatitis in Mice. Gastroenterology. 2009;137:1795-1804.
15. Feingold KR, Grunfeld C, Heuer JG, Gupta A, Cramer M, Zhang TH, Shigenaga JK, Patzek SM, Chan ZW, Moser A, Bina H, Kharitonenkov A. FGF21 Is Increased by Inflammatory Stimuli and Protects Leptin-Deficient ob/ob Mice from the Toxicity of Sepsis. Endocrinology. 2012;153:2689-2700.
16. Ye DW, Wang YD, Li HT, Jia WP, Man K, Lo CM, Wang Y, Lam KS, Xu A. Fibroblast Growth Factor 21 Protects Against Acetaminophen-Induced Hepatotoxicity by Potentiating Peroxisome Proliferator-Activated Receptor Coactivator Protein-1 alpha-Mediated Antioxidant Capacity in Mice. Hepatology. 2014;60:977-989.
17. Huang WD, Ma K, Zhang J, Qatanani M, Cuvillier J, Liu J, Dong BN, Huang X, Moore DD. Nuclear receptordependent bile acid signaling is required for normal liver regeneration. Science. 2006;312:233-236.
18. Pean N, Doignon I, Garcin I, Besnard A, Julien B, Liu BK, Branchereau S, Spraul A, Guettier C, Humbert L, Schoonjans K, Rainteau D, Tordjmann T. The Receptor TGR5 Protects the Liver From Bile Acid Overload During Liver Regeneration in Mice. Hepatology. 2013;58:1451-1460.
19. Bai HB, Zhang NL, Xu Y, Chen Q, Khan M, Potter JJ, Nayar SK, Cornish T, Alpini G, Bronk S, Pan D, Anders RA. Yes-associated protein regulates the hepatic response after bile duct ligation. Hepatology. 2012;56:1097-1107.
20. Shah YA, Morimura K, Yang Q, Tanabe T, Takagi M, Gonzalez FJ. Peroxisome proliferator-activated receptor alpha regulates a microRNA-mediated signaling cascade responsible for hepatocellular proliferation. Molecular and Cellular Biology. 2007;27:4238-4247.
21. Potthoff MJ, Inagaki T, Satapati S, Ding XS, He TT, Goetz R, Mohammadi M, Finck BN, Mangelsdorf DJ, Kliewer SA, Burgess SC. FGF21 induces PGC-1 alpha and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc Natl Acad Sci U S A. 2009;106:10853-10858.
22. Smith JL, Lewindon PJ, Hoskins AC, Pereira TN, Setchell KDR, O'Connell NC, Shepherd RW, Ramm GA. Endogenous ursodeoxycholic acid and cholic acid in liver disease due to cystic fibrosis. Hepatology. 2004;39:1673-1682.
23. Huang WM, Gowda M, Donnelly JG. Bile Acid Ratio in Diagnosis of Intrahepatic Cholestasis of Pregnancy. American Journal of Perinatology. 2009;26:291-294.
24. Shimada T, Nakanishi T, Toyama A, Yamauchi S, Kanzaki A, Fujiwake H, Sato TA, Ikegawa M. Potential Implications for Monitoring Serum Bile Acid Profiles in Circulation with Serum Proteome for Carbon Tetrachloride-Induced Liver Injury/Regeneration Model in Mice. Journal of Proteome Research. 2010;9:4490-4500.
25. Terpstra AHM. Differences between humans and mice in efficacy of the body fat lowering effect of conjugated linoleic acid: Role of metabolic rate. Journal of Nutrition. 2001;131:2067-2068.
26. Nagasue N, Yukaya H, Ogawa Y, Kohno H, Nakamura T. Human-Liver Regeneration after Major Hepatic Resection - a Study of Normal Liver and Livers with Chronic Hepatitis and Cirrhosis. Annals of Surgery. 1987;206:30-39.
27. Palmer CNA, Hsu MH, Griffin KJ, Raucy JL, Johnson EF. Peroxisome proliferator activated receptor-alpha expression in human liver. Molecular Pharmacology. 1998;53:14-22.
28. Rakhshandehroo M, Hooiveld G, Muller M, Kersten S. Comparative analysis of gene regulation by the transcription factor PPARalpha between mouse and human. PLoS One. 2009;4:e6796.
29. Oishi K, Shirai H, Ishida N. CLOCK is involved in the circadian transactivation of peroxisome-proliferatoractivated receptor alpha (PPAR alpha) in mice. Biochemical Journal. 2005;386:575-581.
30. Li Y, Wong K, Walsh K, Gao B, Zang M. Retinoic acid receptor beta stimulates hepatic induction of fibroblast growth factor 21 to promote fatty acid oxidation and control whole-body energy homeostasis in mice. J Biol Chem. 2013;288:10490-10504.
31. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, Maratos-Flier E. Hepatic fibroblast growth factor 21 is regulated by PPAR alpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab. 2007;5:426-437.
32. Wang Y, Solt LA, Burris TP. Regulation of FGF21 expression and secretion by retinoic acid receptor-related orphan receptor alpha. J Biol Chem. 2010;285:15668-15673.
33. Cyphert HA, Ge X, Kohan AB, Salati LM, Zhang Y, Hillgartner FB. Activation of the farnesoid X receptor induces hepatic expression and secretion of fibroblast growth factor 21. J Biol Chem. 2012;287:25123-25138.
34. Chau MD, Gao J, Yang Q, Wu Z, Gromada J. Fibroblast growth factor 21 regulates energy metabolism by activating the AMPK-SIRT1-PGC-1alpha pathway. Proc Natl Acad Sci U S A. 2010;107:12553-12558.
35. García-Rodríguez JL, Barbier-Torres L, FernándezÁlvarez S, Gutiérrez-de Juan V, Monte MJ, Halilbasic E, Herranz D, Álvarez L, Aspichueta P, Marín JJ,Trauner M, Mato JM, Serrano M, Beraza N, Martínez-Chantar ML. SIRT1 controls liver regeneration by regulating bile acid metabolism through farnesoid X receptor and mammalian target of rapamycin signaling. Hepatology. 2014;59:1972-1983.
36. Varela-Rey M, Beraza N, Lu SC, Mato JM, Martinez Chantar ML. Role of AMP-activated protein kinase in the control of hepatocyte priming and proliferation during liver regeneration. Exp Biol Med. 2011;236:402-408.
37. Kong B, Huang J, Zhu Y, Li G, Williams J, Shen S, Aleksunes LM, Richardson JR, Apte U, Rudnick DA, Guo GL. Am J Physiol Gastrointest Liver Physiol. 2014;306:G893-902.
38. Raschzok N, Werner W, Sallmon H, Billecke N, Dame C, Neuhaus P, Sauer IM. Temporal expression profiles indicate a primary function for microRNA during the peak of DNA replication after rat partial hepatectomy. American Journal of Physiology-Regulatory Integrative and Comparative Physiology. 2011;300:R1363-R1372.
39. Li TG, Chiang JYL. Regulation of Bile Acid and Cholesterol Metabolism by PPARs. Ppar Research 2009;2009:501739.
40. Henkel AS, Anderson KA, Dewey AM, Kavesh MH, Green RM. A chronic high-cholesterol diet paradoxically suppresses hepatic CYP7A1 expression in FVB/NJ mice. Journal of Lipid Research. 2011;52:289-298.
41. Landrier JF, Eloranta JJ, Vavricka SR, Kullak-Ublick GA. The nuclear receptor for bile acids, FXR, transactivates human organic solute transporter-alpha and -beta genes. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2006;290:G476-G485.
42. Wagner M, Fickert P, Zollner G, Fuchsbichler A, Silbert D, Tsybrovskyy O, Zatloukal K, Guo GL, Schuetz JD, Gonzalez FJ, Marschall HU, Denk H, Trauner M. Role of farnesoid X receptor in determining hepatic ABC transporter expression and liver injury in bile duct-ligated mice. Gastroenterology. 2003;125:825-838.
43. Dai GL, He L, Bu PL, Wan YJY. Pregnane X receptor is essential for normal progression of liver regeneration. Hepatology. 2008;47:1277-1287.
44. Yang XX, Guo ML, Wan YJY. Deregulation of Growth Factor, Circadian Clock, and Cell Cycle Signaling in Regenerating Hepatocyte RXR alpha-Deficient Mouse Livers. American Journal of Pathology. 2010;176:733-743.
45. Garcia-Canaveras JC, Donato MT, Castell JV, Lahoz A. Targeted profiling of circulating and hepatic bile acids in human, mouse, and rat using a UPLC-MRM-MS-validated method. Journal of Lipid Research. 2012;53:2231-2241.
46. Yang F, Xu Y, Xiong AZ, He YG, Yang L, Wan YJY, Wang ZT. Evaluation of the protective effect of Rhei Radix et Rhizoma against alpha-naphthylisothiocyanate induced liver injury based on metabolic profile of bile acids. Journal of Ethnopharmacology. 2012;144:599-604.
47. Inagaki T, Dutchak P, Zhao G, Ding X, Gautron L, Parameswara V, Li Y, Goetz R, Mohammadi M, Esser V, Elmquist JK, Gerard RD, Burgess SC, Hammer RE, Mangelsdorf DJ, Kliewer RA. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 2007;5:415-425.
48. Yang F, He YQ, Liu HX, Tsuei J, Jiang XY, Yang L, Wang ZT, Wan YJY. All-trans retinoic acid regulates hepatic bile acid homeostasis. Biochemical Pharmacology. 2014;91:483-489.
49. Hu Y, Liu HX, He YQ, Fang YP, Fang JW, Wan YJY. Transcriptome profiling and genome-wide DNA binding define the differential role of fenretinide and all-trans RA in regulating the death and survival of human hepatocellular carcinoma Huh7 cells. Biochemical Pharmacology. 2013;85:1007-1017.