The expanding role of fish models in understanding non-alcoholic fatty liver disease

DMM Disease Models and Mechanisms

Volumn 6, Issue 4, 2013, Pages 905-914

  Asaoka, Yoichi ^a   Terai, Shuji ^b   Sakaida, Isao ^b   Nishina, Hiroshi ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; CHEMICAL AGENT; CYTOKINE; EZETIMIBE; HERBACEOUS AGENT; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; OMEGA 3 FATTY ACID; TAURINE; TELMISARTAN; TRIACYLGLYCEROL;

DIET; DRUG EFFECT; DRUG EFFICACY; DRUG SCREENING; ENDOPLASMIC RETICULUM STRESS; EXPERIMENTAL MODEL; FISH; GENE MUTATION; GENETIC SCREENING; LIPID METABOLISM; MITOCHONDRION; MOLECULAR PATHOLOGY; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; ORYZIAS; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TOMATO; TRANSGENICS; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; FATTY LIVER; FISHES; HUMANS;

DANIO RERIO; MAMMALIA; ORYZIAS LATIPES; ORYZIINAE; RODENTIA;

EID: 84880008350     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.011981     Document Type: Review

References (80)

1. Amali, A. A., Rekha, R. D., Lin, C. J., Wang, W. L., Gong, H. Y., Her, G. M. and Wu, J. L. (2006). Thioacetamide induced liver damage in zebrafish embryo as a disease model for steatohepatitis. J. Biomed. Sci. 13, 225-232.
2. Aoki, K. and Matsudaira, H. (1977). Induction of hepatic tumors in a teleost (Oryzias latipes) after treatment with methylazoxymethanol acetate: brief communication. J. Natl. Cancer Inst. 59, 1747-1749. (Pubitemid 8255052)
3. Balkan, J., Doǧru-Abbasoǧlu, S., Kanbaǧli, O., Cevikbaş, U., Aykaç-Toker, G. and Uysal, M. (2001). Taurine has a protective effect against thioacetamide-induced liver cirrhosis by decreasing oxidative stress. Hum. Exp. Toxicol. 20, 251-254.
4. Balthasar, N., Dalgaard, L. T., Lee, C. E., Yu, J., Funahashi, H., Williams, T., Ferreira, M., Tang, V., McGovern, R. A., Kenny, C. D. et al. (2005). Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123, 493-505. (Pubitemid 41546678)
5. Boorman, G. A., Botts, S., Bunton, T. E., Fournie, J. W., Harshbarger, J. C., Hawkins, W. E., Hinton, D. E., Jokinen, M. P., Okihiro, M. S. and Wolfe, M. J. (1997). Diagnostic criteria for degenerative, inflammatory, proliferative nonneoplastic and neoplastic liver lesions in medaka (Oryzias latipes): consensus of a National Toxicology Program Pathology Working Group. Toxicol. Pathol. 25, 202-210. (Pubitemid 27175213)
6. Braunbeck, T., Görge, G., Storch, V. and Nagel, R. (1990). Hepatic steatosis in zebra fish (Brachydanio rerio) induced by long-term exposure to gamma-hexachlorocyclohexane. Ecotoxicol. Environ. Saf. 19, 355-374. (Pubitemid 20236341)
7. Brown-Peterson, N. J., Krol, R. M., Zhu, Y. and Hawkins, W. E. (1999). N-nitrosodiethylamine initiation of carcinogenesis in Japanese medaka (Oryzias latipes): hepatocellular proliferation, toxicity, and neoplastic lesions resulting from short term, low level exposure. Toxicol. Sci. 50, 186-194. (Pubitemid 29407080)
8. Brunt, E. M., Janney, C. G., Di Bisceglie, A. M., Neuschwander-Tetri, B. A. and Bacon, B. R. (1999). Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am. J. Gastroenterol. 94, 2467-2474. (Pubitemid 29420675)
9. Bugianesi, E., Pagotto, U., Manini, R., Vanni, E., Gastaldelli, A., de Iasio, R., Gentilcore, E., Natale, S., Cassader, M., Rizzetto, M. et al. (2005). Plasma adiponectin in nonalcoholic fatty liver is related to hepatic insulin resistance and hepatic fat content, not to liver disease severity. J. Clin. Endocrinol. Metab. 90, 3498-3504. (Pubitemid 41014319)
10. Bunton, T. E. (1990). Hepatopathology of diethylnitrosamine in the medaka (Oryzias latipes) following short-term exposure. Toxicol. Pathol. 18, 313-323.
11. Capanni, M., Calella, F., Biagini, M. R., Genise, S., Raimondi, L., Bedogni, G., Svegliati-Baroni, G., Sofi, F., Milani, S., Abbate, R. et al. (2006). Prolonged n-3 polyunsaturated fatty acid supplementation ameliorates hepatic steatosis in patients with non-alcoholic fatty liver disease: a pilot study. Aliment. Pharmacol. Ther. 23, 1143-1151. (Pubitemid 43779354)
12. Carten, J. D., Bradford, M. K. and Farber, S. A. (2011). Visualizing digestive organ morphology and function using differential fatty acid metabolism in live zebrafish. Dev. Biol. 360, 276-285.
13. Chalasani, N., Deeg, M. A. and Crabb, D. W. (2004). Systemic levels of lipid peroxidation and its metabolic and dietary correlates in patients with nonalcoholic steatohepatitis. Am. J. Gastroenterol. 99, 1497-1502. (Pubitemid 39193189)
14. Chalasani, N., Younossi, Z., Lavine, J. E., Diehl, A. M., Brunt, E. M., Cusi, K., Charlton, M. and Sanyal, A. J. (2012). The diagnosis and management of nonalcoholic 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 55, 2005-2023.
15. Chen, S. W., Chen, Y. X., Shi, J., Lin, Y. and Xie, W. F. (2006). The restorative effect of taurine on experimental nonalcoholic steatohepatitis. Dig. Dis. Sci. 51, 2225-2234.
16. Cinaroglu, A., Gao, C., Imrie, D. and Sadler, K. C. (2011). Activating transcription factor 6 plays protective and pathological roles in steatosis due to endoplasmic reticulum stress in zebrafish. Hepatology 54, 495-508.
17. Colak, Y., Ozturk, O., Senates, E., Tuncer, I., Yorulmaz, E., Adali, G., Doganay, L. and Enc, F. Y. (2011). SIRT1 as a potential therapeutic target for treatment of nonalcoholic fatty liver disease. Med. Sci. Monit. 17, HY5-HY9.
18. Day, C. P. (2006). From fat to inflammation. Gastroenterology 130, 207-210.
19. Day, C. P. and James, O. F. (1998). Steatohepatitis: a tale of two "hits"? Gastroenterology 114, 842-845.
20. Deng, Q. G., She, H., Cheng, J. H., French, S. W., Koop, D. R., Xiong, S. and Tsukamoto, H. (2005). Steatohepatitis induced by intragastric overfeeding in mice. Hepatology 42, 905-914. (Pubitemid 41401129)
21. Diehl, A. M. (2002). Nonalcoholic steatosis and steatohepatitis IV. Nonalcoholic fatty liver disease abnormalities in macrophage function and cytokines. Am. J. Physiol. Gastrointest. Liver Physiol. 282, G1-G5.
22. Dixon, J. B. (2010). The effect of obesity on health outcomes. Mol. Cell. Endocrinol. 316, 104-108.
23. Ekstedt, M., Franzén, L. E., Mathiesen, U. L., Thorelius, L., Holmqvist, M., Bodemar, G. and Kechagias, S. (2006). Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 44, 865-873. (Pubitemid 46489550)
24. Engelhard, Y. N., Gazer, B. and Paran, E. (2006). Natural antioxidants from tomato extract reduce blood pressure in patients with grade-1 hypertension: a double-blind, placebo-controlled pilot study. Am. Heart J. 151, 100.
25. Goldsmith, J. R. and Jobin, C. (2012). Think small: zebrafish as a model system of human pathology. J. Biomed. Biotechnol. 2012, 817341.
26. Gut, P., Baeza-Raja, B., Andersson, O., Hasenkamp, L., Hsiao, J., Hesselson, D., Akassoglou, K., Verdin, E., Hirschey, M. D. and Stainier, D. Y. (2013). Whole-organism screening for gluconeogenesis identifies activators of fasting metabolism. Nat. Chem. Biol. 9, 97-104.
27. Hammes, T. O., Pedroso, G. L., Hartmann, C. R., Escobar, T. D., Fracasso, L. B., da Rosa, D. P., Marroni, N. P., Porawski, M. and da Silveira, T. R. (2012). The effect of taurine on hepatic steatosis induced by thioacetamide in zebrafish (Danio rerio). Dig. Dis. Sci. 57, 675-682.
28. Her, G. M., Hsu, C. C., Hong, J. R., Lai, C. Y., Hsu, M. C., Pang, H. W., Chan, S. K. and Pai, W. Y. (2011). Overexpression of gankyrin induces liver steatosis in zebrafish (Danio rerio). Biochim. Biophys. Acta 1811, 536-548.
29. Her, G. M., Pai, W. Y., Lai, C. Y., Hsieh, Y. W. and Pang, H. W. (2013). Ubiquitous transcription factor YY1 promotes zebrafish liver steatosis and lipotoxicity by inhibiting CHOP-10 expression. Biochim. Biophys. Acta 1831, 1037-1051.
30. Higashitsuji, H., Itoh, K., Nagao, T., Dawson, S., Nonoguchi, K., Kido, T., Mayer, R. J., Arii, S. and Fujita, J. (2000). Reduced stability of retinoblastoma protein by gankyrin, an oncogenic ankyrin-repeat protein overexpressed in hepatomas. Nat. Med. 6, 96-99. (Pubitemid 30048534)
31. Howarth, D. L., Vacaru, A. M., Tsedensodnom, O., Mormone, E., Nieto, N., Costantini, L. M., Snapp, E. L. and Sadler, K. C. (2012). Alcohol disrupts endoplasmic reticulum function and protein secretion in hepatocytes. Alcohol. Clin. Exp. Res. 36, 14-23.
32. Huang, X. D., Fan, Y., Zhang, H., Wang, P., Yuan, J. P., Li, M. J. and Zhan, X. Y. (2008). Serum leptin and soluble leptin receptor in non-alcoholic fatty liver disease. World J. Gastroenterol. 14, 2888-2893.
33. Huang, P., Zhu, Z., Lin, S. and Zhang, B. (2012). Reverse genetic approaches in zebrafish. J. Genet. Genomics 39, 421-433.
34. Hugo, S. E., Cruz-Garcia, L., Karanth, S., Anderson, R. M., Stainier, D. Y. and Schlegel, A. (2012). A monocarboxylate transporter required for hepatocyte secretion of ketone bodies during fasting. Genes Dev. 26, 282-293.
35. Ishikawa, T., Shimamine, T. and Takayama, S. (1975). Histologic and electron microscopy observations on diethylnitrosamine-induced hepatomas in small aquarium fish (Oryzias latipes). J. Natl. Cancer Inst. 55, 909-916.
36. Itoh, M., Suganami, T., Nakagawa, N., Tanaka, M., Yamamoto, Y., Kamei, Y., Terai, S., Sakaida, I. and Ogawa, Y. (2011). Melanocortin 4 receptor-deficient mice as a novel mouse model of nonalcoholic steatohepatitis. Am. J. Pathol. 179, 2454-2463.
37. 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.; Nonalcoholic Steatohepatitis Clinical Research Network (2005). Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321. (Pubitemid 40770284)
38. Kuwashiro, S., Terai, S., Oishi, T., Fujisawa, K., Matsumoto, T., Nishina, H. and Sakaida, I. (2011). Telmisartan improves nonalcoholic steatohepatitis in medaka (Oryzias latipes) by reducing macrophage infiltration and fat accumulation. Cell Tissue Res. 344, 125-134.
39. Lemoine, M., Ratziu, V., Kim, M., Maachi, M., Wendum, D., Paye, F., Bastard, J. P., Poupon, R., Housset, C., Capeau, J. et al. (2009). Serum adipokine levels predictive of liver injury in non-alcoholic fatty liver disease. Liver Int. 29, 1431-1438.
40. Li, Z., Huang, X., Zhan, H., Zeng, Z., Li, C., Spitsbergen, J. M., Meierjohann, S., Schartl, M. and Gong, Z. (2012). Inducible and repressable oncogene-addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. J. Hepatol. 56, 419-425.
41. Li, Z., Zheng, W., Wang, Z., Zeng, Z., Zhan, H., Li, C., Zhou, L., Yan, C., Spitsbergen, J. M. and Gong, Z. (2013). A transgenic zebrafish liver tumor model with inducible Myc expression reveals conserved Myc signatures with mammalian liver tumors. Dis. Model. Mech. 6, 414-423.
42. Lu, J. W., Yang, W. Y., Lin, Y. M., Jin, S. L. and Yuh, C. H. (2013). Hepatitis B virus X antigen and aflatoxin B1 synergistically cause hepatitis, steatosis and liver hyperplasia in transgenic zebrafish. Acta Histochem. (in press)
43. Matsumoto, T., Terai, S., Oishi, T., Kuwashiro, S., Fujisawa, K., Yamamoto, N., Fujita, Y., Hamamoto, Y., Furutani-Seiki, M., Nishina, H. et al. (2010). Medaka as a model for human nonalcoholic steatohepatitis. Dis. Model. Mech. 3, 431-440.
44. Matteoni, C. A., Younossi, Z. M., Gramlich, T., Boparai, N., Liu, Y. C. and McCullough, A. J. (1999). Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 116, 1413-1419. (Pubitemid 29258890)
45. Matthews, R. P., Lorent, K., Mañoral-Mobias, R., Huang, Y., Gong, W., Murray, I. V., Blair, I. A. and Pack, M. (2009). TNFalpha-dependent hepatic steatosis and liver degeneration caused by mutation of zebrafish S-adenosylhomocysteine hydrolase. Development 136, 865-875.
46. Menescal, L. A., Schmidt, C., Liedtke, D. and Schartl, M. (2012). Liver hyperplasia after tamoxifen induction of Myc in a transgenic medaka model. Dis. Model. Mech. 5, 492-502.
47. Mensenkamp, A. R., van Luyn, M. J., van Goor, H., Bloks, V., Apostel, F., Greeve, J., Hofker, M. H., Jong, M. C., van Vlijmen, B. J., Havekes, L. M. et al. (2000). Hepatic lipid accumulation, altered very low density lipoprotein formation and apolipoprotein E deposition in apolipoprotein E3-Leiden transgenic mice. J. Hepatol. 33, 189-198. (Pubitemid 30485222)
48. Miyake, A., Higashijima, S., Kobayashi, D., Narita, T., Jindo, T., Setiamarga, D. H., Ohisa, S., Orihara, N., Hibiya, K., Konno, S. et al. (2008). Mutation in the abcb7 gene causes abnormal iron and fatty acid metabolism in developing medaka fish. Dev. Growth Differ. 50, 703-716.
49. Monk, K. R., Voas, M. G., Franzini-Armstrong, C., Hakkinen, I. S. and Talbot, W. S. (2013). Mutation of sec63 in zebrafish causes defects in myelinated axons and liver pathology. Dis. Model. Mech. 6, 135-145.
50. Nagarajan, P., Mahesh Kumar, M. J., Venkatesan, R., Majundar, S. S. and Juyal, R. C. (2012). Genetically modified mouse models for the study of nonalcoholic fatty liver disease. World J. Gastroenterol. 18, 1141-1153.
51. Neuschwander-Tetri, B. A. and Caldwell, S. H. (2003). Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology 37, 1202-1219. (Pubitemid 36538699)
52. Nguyen, A. T., Emelyanov, A., Koh, C. H., Spitsbergen, J. M., Lam, S. H., Mathavan, S., Parinov, S. and Gong, Z. (2011). A high level of liver-specific expression of oncogenic Kras(V12) drives robust liver tumorigenesis in transgenic zebrafish. Dis. Model. Mech. 4, 801-813.
53. Nguyen, A. T., Emelyanov, A., Koh, C. H., Spitsbergen, J. M., Parinov, S. and Gong, Z. (2012). An inducible kras(V12) transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis. Model. Mech. 5, 63-72.
54. Oishi, T., Terai, S., Kuwashiro, S., Fujisawa, K., Matsumoto, T., Nishina, H. and Sakaida, I. (2012). Ezetimibe reduces fatty acid quantity in liver and decreased inflammatory cell infiltration and improved NASH in medaka model. Biochem. Biophys. Res. Commun. 422, 22-27.
55. Oka, T., Nishimura, Y., Zang, L., Hirano, M., Shimada, Y., Wang, Z., Umemoto, N., Kuroyanagi, J., Nishimura, N. and Tanaka, T. (2010). Diet-induced obesity in zebrafish shares common pathophysiological pathways with mammalian obesity. BMC Physiol. 10, 21.
56. Pai, W. Y., Hsu, C. C., Lai, C. Y., Chang, T. Z., Tsai, Y. L. and Her, G. M. (2013). Cannabinoid receptor 1 promotes hepatic lipid accumulation and lipotoxicity through the induction of SREBP-1c expression in zebrafish. Transgenic Res. (in press)
57. Passeri, M. J., Cinaroglu, A., Gao, C. and Sadler, K. C. (2009). Hepatic steatosis in response to acute alcohol exposure in zebrafish requires sterol regulatory element binding protein activation. Hepatology 49, 443-452.
58. Pessayre, D. and Fromenty, B. (2005). NASH: a mitochondrial disease. J. Hepatol. 42, 928-940. (Pubitemid 40693212)
59. Postic, C. and Girard, J. (2008). Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J. Clin. Invest. 118, 829-838. (Pubitemid 351364588)
60. Puri, P., Mirshahi, F., Cheung, O., Natarajan, R., Maher, J. W., Kellum, J. M. and Sanyal, A. J. (2008). Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology 134, 568-576. (Pubitemid 351173040)
61. Rekha, R. D., Amali, A. A., Her, G. M., Yeh, Y. H., Gong, H. Y., Hu, S. Y., Lin, G. H. and Wu, J. L. (2008). Thioacetamide accelerates steatohepatitis, cirrhosis and HCC by expressing HCV core protein in transgenic zebrafish Danio rerio. Toxicology 243, 11-22. (Pubitemid 350258587)
62. Sadler, K. C., Amsterdam, A., Soroka, C., Boyer, J. and Hopkins, N. (2005). A genetic screen in zebrafish identifies the mutants vps18, nf2 and foie gras as models of liver disease. Development 132, 3561-3572. (Pubitemid 41246129)
63. Sanyal, A. J., Campbell-Sargent, C., Mirshahi, F., Rizzo, W. B., Contos, M. J., Sterling, R. K., Luketic, V. A., Shiffman, M. L. and Clore, J. N. (2001). Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 120, 1183-1192. (Pubitemid 32246672)
64. Schlegel, A. and Stainier, D. Y. (2007). Lessons from "lower" organisms: what worms, flies, and zebrafish can teach us about human energy metabolism. PLoS Genet. 3, e199.
65. Schwarz, J. M., Linfoot, P., Dare, D. and Aghajanian, K. (2003). Hepatic de novo lipogenesis in normoinsulinemic and hyperinsulinemic subjects consuming high-fat, low-carbohydrate and low-fat, high-carbohydrate isoenergetic diets. Am. J. Clin. Nutr. 77, 43-50. (Pubitemid 36015371)
66. Scrivens, P. J., Noueihed, B., Shahrzad, N., Hul, S., Brunet, S. and Sacher, M. (2011). C4orf41 and TTC-15 are mammalian TRAPP components with a role at an early stage in ER-to-Golgi trafficking. Mol. Biol. Cell 22, 2083-2093.
67. Sekiya, M., Yahagi, N., Matsuzaka, T., Najima, Y., Nakakuki, M., Nagai, R., Ishibashi, S., Osuga, J., Yamada, N. and Shimano, H. (2003). Polyunsaturated fatty acids ameliorate hepatic steatosis in obese mice by SREBP-1 suppression. Hepatology 38, 1529-1539. (Pubitemid 37466979)
68. Shieh, Y. S., Chang, Y. S., Hong, J. R., Chen, L. J., Jou, L. K., Hsu, C. C. and Her, G. M. (2010). Increase of hepatic fat accumulation by liver specific expression of Hepatitis B virus X protein in zebrafish. Biochim. Biophys. Acta 1801, 721-730.
69. Steiling, H., Wüstefeld, T., Bugnon, P., Brauchle, M., Fässler, R., Teupser, D., Thiery, J., Gordon, J. I., Trautwein, C. and Werner, S. (2003). Fibroblast growth factor receptor signalling is crucial for liver homeostasis and regeneration. Oncogene 22, 4380-4388. (Pubitemid 36897968)
70. Stewart, S. T., Cutler, D. M. and Rosen, A. B. (2009). Forecasting the effects of obesity and smoking on U.S. life expectancy. N. Engl. J. Med. 361, 2252-2260.
71. Tainaka, T., Shimada, Y., Kuroyanagi, J., Zang, L., Oka, T., Nishimura, Y., Nishimura, N. and Tanaka, T. (2011). Transcriptome analysis of anti-fatty liver action by Campari tomato using a zebrafish diet-induced obesity model. Nutr. Metab. (Lond) 8, 88.
72. Tanaka, N., Sano, K., Horiuchi, A., Tanaka, E., Kiyosawa, K. and Aoyama, T. (2008). Highly purified eicosapentaenoic acid treatment improves nonalcoholic steatohepatitis. J. Clin. Gastroenterol. 42, 413-418. (Pubitemid 351450629)
73. Thakur, P. C., Stuckenholz, C., Rivera, M. R., Davison, J. M., Yao, J. K., Amsterdam, A., Sadler, K. C. and Bahary, N. (2011). Lack of de novo phosphatidylinositol synthesis leads to endoplasmic reticulum stress and hepatic steatosis in cdipt-deficient zebrafish. Hepatology 54, 452-462.
74. Tomita, K., Oike, Y., Teratani, T., Taguchi, T., Noguchi, M., Suzuki, T., Mizutani, A., Yokoyama, H., Irie, R., Sumimoto, H. et al. (2008). Hepatic AdipoR2 signaling plays a protective role against progression of nonalcoholic steatohepatitis in mice. Hepatology 48, 458-473.
75. Tsai, S. M., Liu, D. W. and Wang, W. P. (2013). Fibroblast growth factor (Fgf) signaling pathway regulates liver homeostasis in zebrafish. Transgenic Res. 22, 301-314.
76. van der Velden, Y. U., Wang, L., Zevenhoven, J., van Rooijen, E., van Lohuizen, M., Giles, R. H., Clevers, H. and Haramis, A. P. (2011). The serine-threonine kinase LKB1 is essential for survival under energetic stress in zebrafish. Proc. Natl. Acad. Sci. USA 108, 4358-4363.
77. Wang, Y., Ausman, L. M., Greenberg, A. S., Russell, R. M. and Wang, X. D. (2010). Dietary lycopene and tomato extract supplementations inhibit nonalcoholic steatohepatitis-promoted hepatocarcinogenesis in rats. Int. J. Cancer 126, 1788-1796.
78. Whitehead, J. P., Richards, A. A., Hickman, I. J., Macdonald, G. A. and Prins, J. B. (2006). Adiponectin - a key adipokine in the metabolic syndrome. Diabetes Obes. Metab. 8, 264-280.
79. Xu, A., Wang, Y., Keshaw, H., Xu, L. Y., Lam, K. S. and Cooper, G. J. (2003). The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in mice. J. Clin. Invest. 112, 91-100. (Pubitemid 38056380)
80. Yee, N. S., Lorent, K. and Pack, M. (2005). Exocrine pancreas development in zebrafish. Dev. Biol. 284, 84-101. (Pubitemid 41096726)