Lipid metabolism and peroxisome proliferator-activated receptor signaling pathways participate in late-phase liver regeneration

Journal of Proteome Research

Volumn 10, Issue 3, 2011, Pages 1179-1190

  Yuan, Xing ^a   Yan, Shikai ^b   Zhao, Jing ^a,c   Shi, Duo ^a   Yuan, Bin ^a   Dai, Weixing ^a   Jiao, Binghua ^a   Zhang, Weidong ^a,b   Miao, Mingyong ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c Logistical Engineering University ^*  (China)

Author keywords

genomics; lipid metabolism pathway; liver regeneration; metabolomics; peroxisome proliferatoractivated receptor signaling pathway; proteomics

Indexed keywords

BIOLOGICAL MARKER; CARBOXYLIC ACID; COMPLEMENTARY DNA; FOLIC ACID; HYPOTAURINE; ISOLEUCINE; KETONE; LEUCINE; LIMONENE; LIPID; OXOACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PINENE; STEROID; TAURINE; TRYPTOPHAN; VALINE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BILE ACID SYNTHESIS; BIOINFORMATICS; CELL CYCLE REGULATION; CELL DEATH; CELL MEMBRANE; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENOMICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORMONE RESPONSE; HYPOXIA; LIPID METABOLISM; LIPOGENESIS; LIVER CELL; LIVER REGENERATION; MALE; MASS SPECTROMETRY; METABOLITE; METABOLOMICS; NONHUMAN; PARTIAL HEPATECTOMY; PRION DISEASE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEOMICS; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEROID METABOLISM; STRESS; TRYPTOPHAN METABOLISM; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION;

ANIMALS; GENE EXPRESSION PROFILING; LIPID METABOLISM; LIVER; LIVER DISEASES; LIVER REGENERATION; MALE; MASS SPECTROMETRY; MICROARRAY ANALYSIS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PROTEOME; PROTEOMICS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

RATTUS;

EID: 79952415541     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100960h     Document Type: Article

References (58)

1. Higgins, G. M.; Anderson, R. M. Experimental pathology of the liver: restoration of the Liver of the white rat following surgical removal Arch. Pathol. 1931, 12, 186-202
2. Lotz, G.; Kiss, A.; Novák, P. K.; Sobel, G.; Schaff, Z. Hepatitis viruses and hepatocarcinogenesis J. Physiol. Paris 2001, 95, 417-422 (Pubitemid 33020269)
3. Streetz, K. L.; Wustefeld, T.; Klein, C.; Manns, M. P.; Trautwein, C. Mediators of inflammation and acute phase response in the liver Cell. Mol. Biol. 2001, 47, 661-673
4. Michalopoulos, G. K.; DeFrances, M. C. Liver regeneration Science 1997, 276, 60-66
5. Drixler, T. A.; Vogten, M. J.; Ritchie, E. D.; van Vroonhoven, T. J.; Gebbink, M. F.; Voest, E. E.; Borel Rinkes, I. H. Liver regeneration is an angiogenesis-associated phenomenon Ann. Surg. 2002, 236, 703-711
6. Gaglio, P. J.; Liu, H.; Dash, S.; Cheng, S.; Dunne, B.; Ratterree, M.; Baskin, G.; Blanchard, J.; Bohm, R., Jr.; Theise, N. D.; LaBrecque, D. Liver regeneration investigated in a non-human primate model (Macaca mulatta) J. Hepatol. 2002, 37, 625-632 (Pubitemid 35305543)
7. Michalopoulos, G. K. Liver regeneration: Molecular mechanisms of growth control FASEB J. 1990, 4, 176-187
8. Fausto, N.; Riehle, K. J. Mechanisms of liver regeneration and their clinical implications J. Hepatobiliary Pancreat Surg. 2005, 12, 181-189 (Pubitemid 40975518)
9. Yamada, Y.; Webber, E. M.; Kirillova, I.; Peschon, J. J.; Fausto, N. Analysis of liver regeneration in mice lacking type 1 or type 2 tumor necrosis factor receptor:requirement for type 1 but not type 2 receptor Hepatology 1998, 28, 959-970 (Pubitemid 28450256)
10. Streetz, K. L.; Luedde, T.; Manns, M. P.; Trautwein, C. Interleukin 6 and liver regeneration Gut 2000, 47, 309-312 (Pubitemid 30489781)
11. Iimuro, Y.; Nishiura, T.; Hellerbrand, C.; Behrns, K. E.; Schoonhoven, R.; Grisham, J. W.; Brenner, D. A. NF-kappaB prevents apaptosis and liver dysfunction during liver regeneration J. Clin. Invest. 1998, 101, 802-811 (Pubitemid 28096077)
12. Chen, C.; Edelstein, L. C.; Gélinas, C. The Rel/NF-kappaB family directly activates expression of the apoptoais inhibitor Bcl-x(L) Mol. Cell. Biol. 2000, 20, 2687-2695 (Pubitemid 30183487)
13. Song, K. H.; Ellis, E.; Strom, S.; Chiang, J. Y. Hepatocyte Growth Factor Signaling Pathway Inhibits Cholesterol 7alpha-Hydroxylase and Bile Acid Synthesis in Human Hepatocytes Hepatology 2007, 46, 1993-2002
14. Monte, M. J.; Fernandez-Tagarro, M.; Marin, J. J. Transient changes in the expression pattern of key enzymes for bile acid synthesis during rat liver regeneration Biochim. Biophys. Acta 2005, 1734, 127-135 (Pubitemid 40724779)
15. Schmitz, K. J.; Wohlschlaeger, J.; Lang, H.; Sotiropoulos, G. C.; Malago, M.; Steveling, K.; Reis, H.; Cicinnati, V. R.; Schmid, K. W.; Baba, H. A. Activation of the ERK and AKT signalling pathway predicts poor prognosis in hepatocellular carcinoma and ERK activation in cancer tissue is associated with hepatitis C virus infection J. Hepatol. 2008, 48, 83-90 (Pubitemid 350191996)
16. Sun, Q.; Miao, M.; Jia, X.; Guo, W.; Wang, L.; Yao, Z.; Liu, C.; Jiao, B. Subproteomic Analysis of the Mitochondrial Proteins in Rats 24 h after Partial Hepatectomy J. Cell Biochem. 2008, 105, 176-184
17. Yang, F.; Yan, S.; He, Y.; Wang, F.; Song, S.; Guo, Y.; Zhou, Q.; Wang, Y.; Lin, Z.; Yang, Y.; Zhang, W.; Sun, S. Expression of hepatitis B virus proteins in transgenic mice alters lipid metabolism and induces oxidative stress in the liver J. Hepatol. 2008, 48, 12-19 (Pubitemid 350191981)
18. Bollard, M. E.; Contel, N. R.; Ebbels, T. M.; Smith, L.; Beckonert, O.; Cantor, G. H.; Lehman-McKeeman, L.; Holmes, E. C.; Lindon, J. C.; Nicholson, J. K.; Keun, H. C. NMR-based metabolic profiling identifies biomarkers of liver regeneration following partial hepatectomy in the rat J. Proteome Res. 2010, 9, 59-69
19. Yang, J.; Zhao, X.; Liu, X.; Wang, C.; Gao, P.; Wang, J.; Li, L.; Gu, J.; Yang, S.; Xu, G. High performance liquid chromatography-mass spectrometry for metabonomics: potential biomarkers for acute deterioration of liver function in chronic hepatitis B J. Proteome Res. 2006, 5, 554-561 (Pubitemid 43364095)
20. Lai, H. S.; Chen, Y.; Chen, W. J. Carnitine contents in remnant liver, kidney, and skeletal muscle after partial hepatectomy in rats: randomized trial World J. Surg. 1998, 22, 42-47 (Pubitemid 28027999)
21. Court, F. G.; Wemyss-Holden, S. A.; Dennison, A. R.; Maddern, G. J. The mystery of liver regeneration Br. J. Surg. 2002, 89, 1089-1095 (Pubitemid 34989213)
22. Mitsue, S.; Hamanoue, M.; Tanabe, G.; Ogura, Y.; Yoshidome, S.; Aikou, T.; Nakamura, T. Expression of HGF and TGF-beta 1 mRNA after partial hepatectomy in rats with liver cirrhosis Surg. Today 1995, 25, 237-243
23. Romero-Gallo, J.; Sozmen, E. G.; Chytil, A.; Russell, W. E.; Whitehead, R.; Parks, W. T.; Holdren, M. S.; Her, M. F.; Gautam, S.; Magnuson, M.; Moses, H. L.; Grady, W. M. Inactivation of TGF-beta signaling in hepatocytes results in an increased proliferative response after partial hepatectomy Oncogene 2005, 24, 3028-3041 (Pubitemid 40675534)
24. Chabicovsky, M.; Herkner, K.; Rossmanith, W. Overexpression of activin beta (C) or activin beta (E) in the mouse liver inhibits regenerative deoxyribonucleic acid synthesis of hepatic cells Endo 2003, 144, 3497-3504 (Pubitemid 36904428)
25. Wada, W.; Maeshima, A.; Zhang, Y. Q.; Hasegawa, Y.; Kuwano, H.; Kojima, I. Assessment of the function of the betaC-subunit of activin in cultured hepatocytes Am. J. Physiol. Endocrinol. Metab. 2004, 287, E247-254
26. Nguyen, L. N.; Furuya, M. H.; Wolfraim, L. A.; Nguyen, A. P.; Holdren, M. S.; Campbell, J. S.; Knight, B.; Yeoh, G. C.; Fausto, N.; Parks, W. T. Transforming growth factor-beta differentially regulates oval cell and hepatocyte proliferation Hepatology 2007, 45, 31-41 (Pubitemid 46144362)
27. Bouzahzah, B.; Fu, M.; Iavarone, A.; Factor, V. M.; Thorgeirsson, S. S.; Pestell, R. G. Transforming growth factor-beta1 recruits histone deacetylase 1 to a p130 repressor complex in transgenic mice in vivo Cancer Res. 2000, 60, 4531-4537 (Pubitemid 32103636)
28. Oe, S.; Lemmer, E. R.; Conner, E. A.; Factor, V. M.; Levéen, P.; Larsson, J.; Karlsson, S.; Thorgeirsson, S. S. Intact signaling by transforming growth factor beta is not required for termination of liver regeneration in mice Hepatology 2004, 40, 1098-1105 (Pubitemid 39425565)
29. Attisano, L.; Wrana, J. L. Signal transduction by the TGF-beta superfamily Science 2002, 296, 1646-1647
30. Kren, B. T.; Trembley, J. H.; Krajewski, S.; Behrens, T. W.; Reed, J. C.; Steer, C. J. Modulation of apoptosis-associated genes bcl-2, bcl-x, and bax during rat liver regeneration Cell Growth Differ. 1996, 7, 1633-1642 (Pubitemid 26415159)
31. Candiano, G.; Bruschi, M.; Musante, L.; Santucci, L.; Ghiggeri, G. M.; Carnemolla, B.; Orecchia, P.; Zardi, L.; Righetti, P. G. Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis Electrophoresis 2004, 25, 1327-1333 (Pubitemid 38801651)
32. Seong, J.; Kim, S. H.; Suh, C. O. Enhancement of tumor radioresponse by combined chemotheraphy in murine hepatocarcinoma J. Gastroenterol. Hepatol. 2001, 16, 883-889 (Pubitemid 32868633)
33. Seong, J.; Chung, E. J.; Kim, H.; Kim, G. E.; Kim, N. K.; Sohn, S. K.; Suh, C. O. Assessment of biomarkers in paired primary and recurrent colorectal adenocarcinomas Int. J. Radiat. Oncol. Biol. Phys. 1999, 45, 1167-1173
34. Craig, A.; Cloarec, O.; Holmes, E.; Nicholson, J. K.; Lindon, J. C. Scaling and normalization effects in NMR spectroscopic metabonomic data sets Anal. Chem. 2006, 78, 2262-2267
35. Curtis, R. K.; Oresic, M.; Vidal-Puig, A. Pathways to the analysis of microarray data Trends Biotechnol. 2005, 23, 429-435 (Pubitemid 41032923)
36. Schürer, N. Y. Implementation of fatty acid carriers to skin irritation and the epidermal barrier Contact Dermatitis 2002, 47, 199-205 (Pubitemid 36132484)
37. Schachtrup, C.; Emmler, T.; Bleck, B.; Sandqvist, A.; Spener, F. Functional analysis of peroxisome-proliferator-responsive element motifs in genes of fatty acid-binding proteins Biochem. J. 2004, 382 (Pt 1) 239-245 (Pubitemid 39141587)
38. Tan, N. S.; Shaw, N. S.; Vinckenbosch, N.; Liu, P.; Yasmin, R.; Desvergne, B.; Wahli, W.; Noy, N. Selective Cooperation between Fatty Acid Binding Proteins and Peroxisome Proliferator-Activated Receptors in Regulating Transcription Mol. Cell. Biol. 2002, 22, 5114-5127 (Pubitemid 34700702)
39. Veerkamp, J. H.; Maatman, R. G. Cytoplasmic fatty acid-binding proteins: their structure and genes Prog. Lipid Res. 1995, 34, 17-25
40. Saatian, B.; Zhao, Y.; He, D.; Georas, S. N.; Watkins, T.; Spannhake, E. W.; Natarajan, V. Transcriptional regulation of lysophosphatidic acid-induced interleukin-8 expression and secretion by p38 MAPK and JNK in human bronchial epithelial cells Biochem. J. 2006, 393 (Pt 3) 657-668 (Pubitemid 43168213)
41. Ikeda, H.; Yatomi, Y.; Yanase, M.; Satoh, H.; Nishihara, A.; Kawabata, M.; Fujiwara, K. Effects of Lysophosphatidic Acid on Proliferation of Stellate Cells and Hepatocytes in Culture Biochem. Biophys. Res. Commun. 1998, 248, 436-440 (Pubitemid 28386442)
42. Desvergne, B.; Wahli, W. Peroxisome proliferator-activated receptors: nuclear control of metabolism Endocr. Rev. 1999, 20, 649-688 (Pubitemid 30650602)
43. Rumi, M. A.; Sato, H.; Ishihara, S.; Kawashima, K.; Hamamoto, S.; Kazumori, H.; Okuyama, T.; Fukuda, R.; Nagasue, N.; Kinoshita, Y. Peroxisome proliferator-activated receptor gamma ligandinduced growth inhibition of human hepatocellular carcinoma Br. J. Cancer 2001, 84, 1640-1647 (Pubitemid 32612496)
44. Rocchi, S.; Auwerx, J. Peroxisome proliferator-activated receptor-gamma: a versatile metabolic regulator Ann. Med. 1999, 31, 342-351 (Pubitemid 29497696)
45. Everett, L.; Galli, A.; Crabb, D. The role of hepatic peroxisome proliferator-activated receptors (PPARs) in health and disease Liver 2000, 20, 191-199 (Pubitemid 30342716)
46. Quraishi, O.; Mancini, J. A.; Riendeau, D. Inhibition of inducible prostaglandin E(2) synthase by 15-deoxy-Delta(12,14)-prostaglandin J(2) and polyunsaturated fatty acids Biochem. Pharmacol. 2002, 63, 1183-1189 (Pubitemid 34267034)
47. Choi, K. C.; Lee, S. Y.; Yoo, H. J.; Ryu, O. H.; Lee, K. W.; Kim, S. M.; Baik, S. H.; Choi, K. M. Effect of PPAR-delta agonist on the expression of visfatin, adiponectin, and resistin in rat adipose tissue and 3T3-L1 adipocytes Biochem. Biophys. Res. Commun. 2007, 357, 62-67 (Pubitemid 46574500)
48. Escher, P.; Braissant, O.; Basu-Modak, S.; Michalik, L.; Wahli, W.; Desvergne, B. Rat PPARs: quantitative analysis in adult rat tissues and regulation in fasting and refeeding Endocrinology 2001, 142, 4195-4202 (Pubitemid 32907045)
49. Hellemans, K.; Michalik, L.; Dittie, A.; Knorr, A.; Rombouts, K.; De, Jong., J; Heirman, C.; Quartier, E.; Schuit, F.; Wahli, W.; Geerts, A. Peroxisome proliferator-activated receptor-beta signaling contributes to enhanced proliferation of hepatic stellate cells Gastroenterology 2003, 124, 184-201 (Pubitemid 36055351)
50. Odegaard, J. I.; Ricardo-Gonzalez, R. R.; Goforth, M. H.; Morel, C. R.; Subramanian, V.; Mukundan, L.; Red Eagle, A.; Vats, D.; Brombacher, F.; Ferrante, A. W.; Chawla, A. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance Nature 2007, 447, 1116-1120 (Pubitemid 47014427)
51. Moller, D. E.; Berger, J. P. Role of PPARs in the regulation of obesity-related insulin sensitivity and inflammation Int. J. Obes. Relat. Metab. Disord. 2003, 27 (Suppl 3) S17-21
52. Rao, M. S.; Peters, J. M.; Gonzalez, F. J.; Reddy, J. K. Hepatic regeneration in peroxisome proliferator-activated receptor alphanull mice after partial hepatectomy Hepatol. Res. 2002, 22, 52-57 (Pubitemid 34223634)
53. Anderson, S. P.; Yoon, L.; Richard, E. B.; Dunn, C. S.; Cattley, R. C.; Corton, J. C. Delayed liver regeneration in peroxisome proliferator-activated receptor-alpha-null mice Hepatology 2002, 36, 544-554 (Pubitemid 34977164)
54. Wheeler, M. D.; Smutney, O. M.; Check, J. F.; Rusyn, I.; Schulte-Hermann, R.; Thurman, R. G. Impaired Ras membrane association and activation in PPARalpha knockout mice after partial hepatectomy Am. J. Physiol. Gastrointest Liver Physiol. 2003, 284, G302-312
55. Ricote, M.; Li, A. C.; Willson, T. M.; Kelly, C. J.; Glass, C. K. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation Nature 1998, 391, 79-82 (Pubitemid 28079218)
56. Baek, S. J.; Wilson, L. C.; His, L. C.; Eling, T. E. Troglitazone, a peroxisome proliferator-activated receptor gamma (PPAR gamma) ligand, selectively induces the early growth response-1 gene independently of PPAR gamma. A novel mechanism for its anti-tumorigenic activity J. Biol. Chem. 2003, 278, 5845-5853 (Pubitemid 36800831)
57. Huang, W.; Ma, K.; Zhang, J.; Qatanani, M.; Cuvillier, J.; Liu., J.; Dong, B.; Huang, X.; Moore, D. D. Nuclear receptor-dependent bile acid signaling is required for normal liver regeneration Science 2006, 312, 233-236
58. Yang, J.; Li, Y.; Wu, L.; Zhang, Z.; Han, T.; Guo, H.; Jiang, N.; Tao, K.; Ti, Z.; Liu, X.; Yao, L.; Dou, K. NDRG2 in rat liver regeneration: role in proliferation and apoptosis Wound Repair Regen. 2010, 18, 524-531