Hepatic retinoid stores are required for normal liver regeneration

Journal of Lipid Research

Volumn 54, Issue 4, 2013, Pages 893-908

  Shmarakov, Igor O ^a,b   Jiang, Hongfeng ^a   Yang, Kryscilla Jian Zhang ^a   Goldberg, Ira J ^a   Blaner, William S ^a  

^a Howard Hughes Medical Institute   (United States)

^b CHERNIVTSI NATIONAL UNIVERSITY   (Ukraine)

Author keywords

Cell cycle; Cell proliferation; Lipid droplet; Nuclear hormone receptor; Retinyl ester; Vitamin A

Indexed keywords

ALANINE AMINOTRANSFERASE; BROXURIDINE; CYCLIN A2; CYCLIN B1; CYCLIN E; CYCLIN E1; CYTOKINE; GROWTH FACTOR; INTERLEUKIN 6; LECITHIN RETINOL ACYLTRANSFERASE; MESSENGER RNA; PROTEIN P21; RETINOID; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE; GENE EXPRESSION; HEPATIC RETINOID STORE; LIVER; LIVER INJURY; LIVER REGENERATION; LIVER SURGERY; LIVER WEIGHT; LRAT GENE; MALE; MITOSIS; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINOID RESPONSE GENE; STORAGE;

ANIMALS; ENDOCANNABINOIDS; IMMUNOHISTOCHEMISTRY; LIVER; LIVER REGENERATION; MICE; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RETINOIDS; TANDEM MASS SPECTROMETRY; TRETINOIN; TRIGLYCERIDES;

EID: 84875833440     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M029801     Document Type: Article

References (60)

1. Gudas, L. J. 2012. Emerging roles for retinoids in regeneration and differentiation in normal and disease states. Biochim. Biophys. Acta. 1821 : 213-221.
2. Noy, N. 2010. Between death and survival: retinoic acid in regulation of apoptosis. Annu. Rev. Nutr. 30 : 201-217.
3. Balmer, J. E., and R. Blomhoff. 2002. Gene expression regulation by retinoic acid. J. Lipid Res. 43 : 1773-1808.
4. Chawla, A., J. J. Repa, R. M. Evans, and D. J. Mangelsdorf. 2001. Nuclear receptors and lipid physiology: opening the X-fi les. Science. 294 : 1866-1870.
5. Duong, V., and C. Rochette-Egly. 2011. The molecular physiology of nuclear retinoic acid receptors. From health to disease. Biochim. Biophys. Acta. 1812 : 1023-1031.
6. Wagner, M., G. Zollner, and M. Trauner. 2011. Nuclear receptors in liver disease. Hepatology. 53 : 1023-1034.
7. Goodman, D. W., H. S. Huang, and T. Shiratori. 1965. Tissue distribution and metabolism of newly absorbed vitamin A in the rat. J. Lipid Res. 6 : 390-396.
8. Blaner, W. S., S. M. O'Byrne, N. Wongsiriroj, J. Kluwe, D. M. D'Ambrosio, H. Jiang, R. F. Schwabe, E. M. Hillman, R. Piantedosi, and J. Libien. 2009. Hepatic stellate cell lipid droplets: a specialized lipid droplet for retinoid storage. Biochim. Biophys. Acta. 1791 :467-473.
9. Leo, M. A., and C. S. Lieber. 1999. Alcohol, vitamin A, and betacarotene: adverse interactions, including hepatotoxicity and carcinogenicity. Am. J. Clin. Nutr. 69 : 1071-1085.
10. Fausto, N., J. S. Campbell, and K. J. Riehle. 2006. Liver regeneration. Hepatology. 43 : S45-S53.
11. Taub, R. 2004. Liver regeneration: from myth to mechanism. Nat. Rev. Mol. Cell Biol. 5 : 836-847.
12. Michalopoulos, G. K. 2010. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am. J. Pathol. 176 : 2-13.
13. Kurinna, S., and M. C. Barton. 2011. Cascades of transcription regulation during liver regeneration. Int. J. Biochem. Cell Biol. 43 : 189-197.
14. Utoh, R., C. Tateno, M. Kataoka, A. Tachibana, N. Masumoto, C. Yamasaki, T. Shimada, T. Itamoto, T. Asahara, and K. Yoshizato. 2010. Hepatic hyperplasia associated with discordant xenogeneic parenchymal-nonparenchymal interactions in human hepatocyterepopulated mice. Am. J. Pathol. 177 : 654-665.
15. Mabuchi, A., I. Mullaney, P. Sheard, P. Hessian, A. Zimmermann, H. Senoo, and A. M. Wheatley. 2004. Role of hepatic stellate cells in the early phase of liver regeneration in rat: formation of tight adhesion to parenchymal cells. Comp. Hepatol. 3 (Suppl. 1) : S29.
16. Mabuchi, A., I. Mullaney, P. W. Sheard, P. A. Hessian, B. L. Mallard, M. N. Tawadrous, A. Zimmermann, H. Senoo, and A. M. Wheatley. 2004. Role of hepatic stellate cell/hepatocyte interaction and activation of hepatic stellate cells in the early phase of liver regeneration in the rat. J. Hepatol. 40 : 910-916.
17. Zhang, W., X. P. Chen, W. G. Zhang, F. Zhang, S. Xiang, H. H. Dong, and L. Zhang. 2009. Hepatic non-parenchymal cells and extracellular matrix participate in oval cell-mediated liver regeneration. World J. Gastroenterol. 15 : 552-560.
18. Ezaki, H., Y. Yoshida, Y. Saji, T. Takemura, J. Fukushima, H. Matsumoto, Y. Kamada, A. Wada, T. Igura, S. Kihara, et al. 2009. Delayed liver regeneration after partial hepatectomy in adiponectin knockout mice. Biochem. Biophys. Res. Commun. 378 : 68-72.
19. DeAngelis, R. A., M. M. Markiewski, R. Taub, and J. D. Lambris. 2005. A high-fat diet impairs liver regeneration in C57BL/6 mice through overexpression of the NF-kappaB inhibitor, IkappaBalpha. Hepatology. 42 : 1148-1157.
20. Hu, Z., K. Fujio, E. R. Marsden, S. S. Thorgeirsson, and R. P. Evarts. 1994. Hepatic regeneration in vitamin A-defi cient rats: changes in the expression of transforming growth factor alpha/epidermal growth factor receptor and retinoic acid receptors alpha and beta. Cell Growth Differ. 5 : 503-508.
21. Weiss, B., I. Barshack, N. Onaca, I. Goldberg, Z. Berkovich, E. Melzer, A. Jonas, and R. Reifen. 2010. Vitamin A defi ciency associated with enhanced proliferation of bile duct epithelial cells in the rat. Isr. Med. Assoc. J. 12 : 82-86.
22. Kimura, M., M. Watanabe, N. Ishibashi, S. Yanagida, and M. Ogihara. 2010. Acyclic retinoid NIK-333 accelerates liver regeneration and lowers serum transaminase activities in 70% partially hepatectomized rats, in vivo. Eur. J. Pharmacol. 643 : 267-273.
23. O'Byrne, S. M., N. Wongsiriroj, J. Libien, S. Vogel, I. J. Goldberg, W. Baehr, K. Palczewski, and W. S. Blaner. 2005. Retinoid absorption and storage is impaired in mice lacking lecithin:retinol acyltransferase (LRAT). J. Biol. Chem. 280 : 35647-35657.
24. Mitchell, C., and H. Willenbring. 2008. A reproducible and welltolerated method for 2/3 partial hepatectomy in mice. Nat. Protoc. 3 : 1167-1170.
25. Fischer, A. H., K. A. Jacobson, J. Rose, and R. Zeller. 2008. Paraffi n embedding tissue samples for sectioning. CSH Protoc. 2008: pdb. prot4989.
26. Penney, D. P., J. M. Powers, M. Frank, C. Willis, and C. Churukian. 2002. Analysis and testing of biological stains-The Biological Stain Commission Procedures. Biotech. Histochem. 77 : 237-275.
27. Kane, M. A., A. E. Folias, C. Wang, and J. L. Napoli. 2008. Quantitative profi ling of endogenous retinoic acid in vivo and in vitro by tandem mass spectrometry. Anal. Chem. 80 : 1702-1708.
28. Clugston, R. D., H. Jiang, M. X. Lee, R. Piantedosi, J. J. Yuen, R. Ramakrishnan, M. J. Lewis, M. E. Gottesman, L. S. Huang, I. J. Goldberg, et al. 2011. Altered hepatic lipid metabolism in C57BL/6 mice fed alcohol: a targeted lipidomic and gene expression study. J. Lipid Res. 52 : 2021-2031.
29. Borowiak, M., A. N. Garratt, T. Wustefeld, M. Strehle, C. Trautwein, and C. Birchmeier. 2004. Met provides essential signals for liver regeneration. Proc. Natl. Acad. Sci. USA. 101 : 10608-10613.
30. Su, A. I., L. G. Guidotti, J. P. Pezacki, F. V. Chisari, and P. G. Schultz. 2002. Gene expression during the priming phase of liver regeneration after partial hepatectomy in mice. Proc. Natl. Acad. Sci. USA. 99 : 11181-11186.
31. Chauhan, A., S. Lorenzen, H. Herzel, and S. Bernard. 2011. Regulation of mammalian cell cycle progression in the regenerating liver. J. Theor. Biol. 283 : 103-112.
32. Wang, X., H. Kiyokawa, M. B. Dennewitz, and R. H. Costa. 2002. The Forkhead Box m1b transcription factor is essential for hepatocyte DNA replication and mitosis during mouse liver regeneration. Proc. Natl. Acad. Sci. USA. 99 : 16881-16886.
33. Kalin, T. V., V. Ustiyan, and V. V. Kalinichenko. 2011. Multiple faces of FoxM1 transcription factor: lessons from transgenic mouse models. Cell Cycle. 10 : 396-405.
34. Shmarakov, I., M. K. Fleshman, D. N. D'Ambrosio, R. Piantedosi, K. M. Riedl, S. J. Schwartz, R. W. Curley, Jr. ., J. von Lintig, L. P. Rubin, E. H. Harrison, et al. 2010. Hepatic stellate cells are an important cellular site for beta-carotene conversion to retinoid. Arch. Biochem. Biophys. 504 : 3-10.
35. Newberry, E. P., S. M. Kennedy, Y. Xie, J. Luo, S. E. Stanley, C. F. Semenkovich, R. M. Crooke, M. J. Graham, and N. O. Davidson. 2008. Altered hepatic triglyceride content after partial hepatectomy without impaired liver regeneration in multiple murine genetic models. Hepatology. 48 : 1097-1105.
36. Shteyer, E., Y. Liao, L. J. Muglia, P. W. Hruz, and D. A. Rudnick. 2004. Disruption of hepatic adipogenesis is associated with impaired liver regeneration in mice. Hepatology. 40 : 1322-1332.
37. Mukhopadhyay, B., R. Cinar, S. Yin, J. Liu, J. Tam, G. Godlewski, J. Harvey-White, I. Mordi, B. F. Cravatt, S. Lotersztajn, et al. 2011. Hyperactivation of anandamide synthesis and regulation of cellcycle progression via cannabinoid type 1 (CB1) receptors in the regenerating liver. Proc. Natl. Acad. Sci. USA. 108 : 6323-6328.
38. Tam, J., J. Liu, B. Mukhopadhyay, R. Cinar, G. Godlewski, and G. Kunos. 2011. Endocannabinoids in liver disease. Hepatology. 53 : 346-355.
39. Mukhopadhyay, B., J. Liu, D. Osei-Hyiaman, G. Godlewski, P. Mukhopadhyay, L. Wang, W. I. Jeong, B. Gao, G. Duester, K. Mackie, et al. 2010. Transcriptional regulation of cannabinoid receptor-1 expression in the liver by retinoic acid acting via retinoic acid receptor-gamma. J. Biol. Chem. 285 : 19002-19011.
40. Batten, M. L., Y. Imanishi, T. Maeda, D. C. Tu, A. R. Moise, D. Bronson, D. Possin, R. N. Van Gelder, W. Baehr, and K. Palczewski. 2004. Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J. Biol. Chem. 279 : 10422-10432.
41. Liu, L., and L. J. Gudas. 2005. Disruption of the lecithin:retinol acyltransferase gene makes mice more susceptible to vitamin A defi ciency. J. Biol. Chem. 280 : 40226-40234.
42. Yang, X., M. Guo, and Y. J. Wan. 2010. Deregulation of growth factor, circadian clock, and cell cycle signaling in regenerating hepatocyte RXRalpha-defi cient mouse livers. Am. J. Pathol. 176 : 733-743.
43. Imai, T., M. Jiang, P. Kastner, P. Chambon, and D. Metzger. 2001. Selective ablation of retinoid X receptor alpha in hepatocytes impairs their lifespan and regenerative capacity. Proc. Natl. Acad. Sci. USA. 98 : 4581-4586.
44. Ledda-Columbano, G. M., M. Pibiri, F. Molotzu, C. Cossu, L. Sanna, G. Simbula, A. Perra, and A. Columbano. 2004. Induction of hepatocyte proliferation by retinoic acid. Carcinogenesis. 25 : 2061-2066.
45. Ohtake, Y., A. Maruko, N. Ohishi, M. Kawaguchi, T. Satoh, and Y. Ohkubo. 2008. Effect of retinoic acid on transglutaminase and ornithine decarboxylase activities during liver regeneration. Cell Biochem. Funct. 26 : 359-365.
46. López-Valencia, V., P. Rangel, S. Rodriguez, and R. Hernandez-Munoz. 2007. Involvement of alcohol and aldehyde dehydrogenase activities on hepatic retinoid metabolism and its possible participation in the progression of rat liver regeneration. Biochem. Pharmacol. 73 : 586-596.
47. Omori, M., Y. Muto, and T. Nagao. 1981. Cellular retinoid-binding proteins in reginerating rat liver: demonstration of a novel cellular retinoid-binding protein. J. Lipid Res. 22 : 899-904.
48. Kwon, H. S., B. Huang, N. Ho Jeoung, P. Wu, C. N. Steussy, and R. A. Harris. 2006. Retinoic acids and trichostatin A (TSA), a histone deacetylase inhibitor, induce human pyruvate dehydrogenase kinase 4 (PDK4) gene expression. Biochim. Biophys. Acta. 1759 : 141-151.
49. Liu, M., A. Iavarone, and L. P. Freedman. 1996. Transcriptional activation of the human p21(WAF1/CIP1) gene by retinoic acid receptor. Correlation with retinoid induction of U937 cell differentiation. J. Biol. Chem. 271 : 31723-31728.
50. Ray, W. J., G. Bain, M. Yao, and D. I. Gottlieb. 1997. CYP26, a novel mammalian cytochrome P450, is induced by retinoic acid and defi nes a new family. J. Biol. Chem. 272 : 18702-18708.
51. Yamamoto, Y., R. Zolfaghari, and A. C. Ross. 2000. Regulation of CYP26 (cytochrome P450RAI) mRNA expression and retinoic acid metabolism by retinoids and dietary vitamin A in liver of mice and rats. FASEB J. 14 : 2119-2127.
52. Sherr, C. J., and J. M. Roberts. 2004. Living with or without cyclins and cyclin-dependent kinases. Genes Dev. 18 : 2699-2711.
53. Weymann, A., E. Hartman, V. Gazit, C. Wang, M. Glauber, Y. Turmelle, and D. A. Rudnick. 2009. p21 is required for dextrose-mediated inhibition of mouse liver regeneration. Hepatology. 50 : 207-215.
54. Albrecht, J. H., R. Y. Poon, C. L. Ahonen, B. M. Rieland, C. Deng, and G. S. Crary. 1998. Involvement of p21 and p27 in the regulation of CDK activity and cell cycle progression in the regenerating liver. Oncogene. 16 : 2141-2150.
55. Estep, J. M., L. O'Reilly, G. Grant, J. Piper, J. Jonsson, A. Afendy, V. Chandhoke, and Z. M. Younossi. 2010. Hepatic stellate cell and myofi broblast-like cell gene expression in the explanted cirrhotic livers of patients undergoing liver transplantation. Dig. Dis. Sci. 55 : 496-504.
56. Makino, H., H. Shimizu, H. Ito, F. Kimura, S. Ambiru, A. Togawa, M. Ohtsuka, H. Yoshidome, A. Kato, H. Yoshitomi, et al. 2006. Changes in growth factor and cytokine expression in biliary obstructed rat liver and their relationship with delayed liver regeneration after partial hepatectomy. World J. Gastroenterol. 12 : 2053-2059.
57. Schirmacher, P., A. Geerts, A. Pietrangelo, H. P. Dienes, and C. E. Rogler. 1992. Hepatocyte growth factor/hepatopoietin A is expressed in fat-storing cells from rat liver but not myofi broblast-like cells derived from fat-storing cells. Hepatology. 15 : 5-11.
58. Kwon, H. S., and R. A. Harris. 2004. Mechanisms responsible for regulation of pyruvate dehydrogenase kinase 4 gene expression. Adv. Enzyme Regul. 44 : 109-121.
59. Shaw, N., M. Elholm, and N. Noy. 2003. Retinoic acid is a high affi nity selective ligand for the peroxisome proliferator-Activated receptor beta/delta. J. Biol. Chem. 278 : 41589-41592.
60. Blaner, W. S., and J. A. Olson. 1994. Retinol and retinoic acid metabolism. In The Retinoids: Biology, Chemistry, and Medicine. 2nd edition. M. B. Sporn, A. B. Roberts, and D. S. Goodman, editors. Raven Press, New York. 229-256.