Nonalcoholic steatohepatitis and hepatocellular carcinoma in galectin-3 knockout mice

Hepatology Research

Volumn 38, Issue 12, 2008, Pages 1241-1251

  Nakanishi, Yuko ^a   Tsuneyama, Koichi ^a   Nomoto, Kazuhiro ^a   Fujimoto, Makoto ^a   Salunga, Thucydides L ^a   Nakajima, Takahiko ^a   Miwa, Shigeharu ^a   Murai, Yoshihiro ^a   Hayashi, Shinichi ^a   Kato, Ichiro ^b   Hiraga, Koichi ^b   Hsu, Daniel K ^c   Liu, Fu Tong ^c   Takano, Yasuo ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b University of the Philippines Diliman   (Philippines)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Computed tomography; Galectin 3; Hepatocellular carcinoma; Nonalcoholic fatty liver disease; nonalcoholic steatohepatitis

Indexed keywords

GALECTIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MORPHOLOGY; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; DISEASE ASSOCIATION; HISTOPATHOLOGY; KNOCKOUT MOUSE; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER HYPERPLASIA; LIVER NODULE; LONGITUDINAL STUDY; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBSERVATIONAL STUDY; PRIORITY JOURNAL;

EID: 55449125261     PISSN: 13866346     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1872-034X.2008.00395.x     Document Type: Article

References (68)

1. Bugianesi E. Non-alcoholic steatohepatitis and cancer. Clin Liver Dis 2007; 11: 191-207, x-xi.
2. Anstee QM, Goldin RD. Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol 2006; 87: 1-16.
3. Nomoto K, Tsuneyama K, Abdel Aziz HO et al. Disrupted galectin-3 causes non-alcoholic fatty liver disease in male mice. J Pathol 2006; 210: 469-77.
4. Kuwabara I, Liu FT. Galectin-3 promotes adhesion of human neutrophils to laminin. J Immunol 1996; 156: 3939-44.
5. Inohara H, Akahani S, Koths K, Raz A. Interactions between galectin-3 and Mac-2-binding protein mediate cell-cell adhesion. Cancer Res 1996; 56: 4530-4.
6. Ochieng J, Warfield P, Green-Jarvis B, Fentie I. Galectin-3 regulates the adhesive interaction between breast carcinoma cells and elastin. J Cell Biochem 1999; 75: 505-14.
7. Sato S, Ouellet N, Pelletier I, Simard M, Rancourt A, Bergeron MG. Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J Immunol 2002; 168: 1813-22.
8. Zou J, Glinsky VV, Landon LA, Matthews L, Deutscher SL. Peptides specific to the galectin-3 carbohydrate recognition domain inhibit metastasis-associated cancer cell adhesion. Carcinogenesis 2005; 26: 309-18.
9. Sano H, Hsu DK, Yu L et al. Human galectin-3 is a novel chemoattractant for monocytes and macrophages. J Immunol 2000; 165: 2156-64.
10. Dagher SF, Wang JL, Patterson RJ. Identification of galectin-3 as a factor in pre-mRNA splicing. Proc Nat Acad Sci USA 1995; 92: 1213-17.
11. Yang RY, Hsu DK, Liu FT. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Nat Acad Sci USA 1996; 93: 6737-42.
12. Nagata M, Suzuki W, Iizuka S et al. Type 2 diabetes mellitus in obese mouse model induced by monosodium glutamate. Exp Anim 2006; 55: 109-15.
13. Nakanishi Y, Tsuneyama K, Fujimoto M et al. Monosodium glutamate (MSG): a villain and promoter of liver inflammation and dysplasia. J Autoimmun 2008; 30: 42-50.
14. Hsu DK, Yang RY, Pan Z et al. Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am J Pathol 2000; 156: 1073-83.
15. Kumada T, Tsuneyama K, Hatta H, Ishizawa S, Takano Y. Improved 1-h rapid immunostaining method using intermittent microwave irradiation: practicability based on 5 years application in Toyama Medical and Pharmaceutical University Hospital. Mod Pathol 2004; 17: 1141-9.
16. Kleiner DE, Brunt EM, Van Natta M et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005; 41: 1313-21.
17. Flotte TJ, Springer TA, Thorbecke GJ. Dendritic cell and macrophage staining by monoclonal antibodies in tissue sections and epidermal sheets. Am J Pathol 1983; 111: 112-24.
18. Hsu DK, Dowling CA, Jeng KC, Chen JT, Yang RY, Liu FT. Galectin-3 expression is induced in cirrhotic liver and hepatocellular carcinoma. Int J Cancer 1999; 81: 519-26.
19. Kim H, Lee J, Hyun JW, Park JW, Joo HG, Shin T. Expression and immunohistochemical localization of galectin-3 in various mouse tissues. Cell Biol Int 2007; 31: 655-62.
20. Paine-Saunders S, Viviano BL, Saunders S. GPC6, a novel member of the glypican gene family, encodes a product structurally related to GPC4 and is colocalized with GPC5 on human chromosome 13. Genomics 1999; 57: 455-8.
21. Zhu ZW, Friess H, Wang L et al. Enhanced glypican-3 expression differentiates the majority of hepatocellular carcinomas from benign hepatic disorders. Gut 2001; 48: 558-64.
22. Capurro M, Wanless IR, Sherman M et al. Glypican-3: A novel serum and histochemical marker for hepatocellular carcinoma. Gastroenterology 2003; 125: 89-97.
23. Nakatsura T, Yoshitake Y, Senju S et al. Glypican-3, overexpressed specifically in human hepatocellular carcinoma, is a novel tumor marker. Biochem Biophys Res Commun 2003; 306: 16-25.
24. Sung YK, Hwang SY, Park MK et al. Glypican-3 is overexpressed in human hepatocellular carcinoma. Cancer Sci 2003; 94: 259-62.
25. Libbrecht L, Severi T, Cassiman D et al. Glypican-3 expression distinguishes small hepatocellular carcinomas from cirrhosis, dysplastic nodules, and focal nodular hyperplasia-like nodules. Am J Surg Pathol 2006; 30: 1405-11.
26. Wang XY, Degos F, Dubois S et al. Glypican-3 expression in hepatocellular tumors: Diagnostic value for preneoplastic lesions and hepatocellular carcinomas. Hum Pathol 2006; 37: 1435-41.
27. Di Tommaso L, Franchi G, Park YN et al. Diagnostic value of HSP70, glypican 3, and glutamine synthetase in hepatocellular nodules in cirrhosis. Hepatology 2007; 45: 725-34.
28. Ong JP, Younossi ZM. Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis 2007; 11: 1-16, vii.
29. Charlton M. Nonalcoholic fatty liver disease: A review of current understanding and future impact. Clin Gastroenterol Hepatol 2004; 2: 1048-58.
30. Liu FT, Hsu DK, Zuberi RI et al. Expression and function of galectin-3, a beta-galactoside-binding lectin, in human monocytes and macrophages. Am J Pathol 1995; 147: 1016-28.
31. Almkvist J, Karlsson A. Galectins as inflammatory mediators. Glycoconj J 2004; 19: 575-81.
32. Fan J, Zhong L, Wang G et al. The role of Kupffer cells in non-alcoholic steatohepatitis of rats chronically fed with high-fat diet. Zhonghua Gan Zang Bing Za Zhi 2001; 9: 16-18.
33. Diehl AM. Nonalcoholic steatosis and steatohepatitis IV. Nonalcoholic fatty liver disease abnormalities in macrophage function and cytokines. Am J Physiol Gastrointest Liver Physiol 2002; 282: G1-5.
34. Yoshimatsu M, Terasaki Y, Sakashita N et al. Induction of macrophage scavenger receptor MARCO in nonalcoholic steatohepatitis indicates possible involvement of endotoxin in its pathogenic process. Int J Exp Pathol 2004; 85: 335-43.
35. Shen J, Sakaida I, Uchida K, Terai S, Okita K. Leptin enhances TNF-alpha production via p38 and JNK MAPK in LPS-stimulated Kupffer cells. Life Sci 2005; 77: 1502-15.
36. Malaguarnera L, Di Rosa M, Zambito AM, Ombra N, Nicoletti F, Malaguarnera M. Chitotriosidase gene expression in Kupffer cells from patients with non-alcoholic fatty liver disease. Gut 2006; 55: 1313-20.
37. Tomita K, Tamiya G, Ando S et al. Tumour necrosis factor alpha signalling through activation of Kupffer cells plays an essential role in liver fibrosis of non-alcoholic steatohepatitis in mice. Gut 2006; 55: 415-24.
38. Kawada N, Otogawa K. Role of oxidative stress and Kupffer cells in hepatic fibrosis. J Gastroenterol Hepatol 2007; 22 (Suppl 1): S85-6.
39. Kiki I, Altunkaynak BZ, Altunkaynak ME, Vuraler O, Unal D, Kaplan S. Effect of high fat diet on the volume of liver and quantitative feature of Kupffer cells in the female rat: A stereological and ultrastructural study. Obes Surg 2007; 17: 1381-8.
40. Kolak M, Westerbacka J, Velagapudi VR et al. Adipose tissue inflammation and increased ceramide content characterize subjects with high liver fat content independent of obesity. Diabetes 2007; 56: 1960-8.
41. Otogawa K, Kinoshita K, Fujii H et al. Erythrophagocytosis by liver macrophages (Kupffer cells) promotes oxidative stress, inflammation, and fibrosis in a rabbit model of steatohepatitis: Implications for the pathogenesis of human nonalcoholic steatohepatitis. Am J Pathol 2007; 170: 967-80.
42. Park JW, Jeong G, Kim SJ, Kim MK, Park SM. Predictors reflecting the pathological severity of non-alcoholic fatty liver disease: comprehensive study of clinical and immunohistochemical findings in younger Asian patients. J Gastroenterol Hepatol 2007; 22: 491-7.
43. Strissel KJ, Stancheva Z, Miyoshi H et al. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007; 56: 2910-18.
44. Mey A, Leffler H, Hmama Z, Normier G, Revillard JP. The animal lectin galectin-3 interacts with bacterial lipopolysaccharides via two independent sites. J Immunol 1996; 156: 1572-7.
45. Matarrese P, Tinari N, Semeraro ML, Natoli C, Iacobelli S, Malorni W. Galectin-3 overexpression protects from cell damage and death by influencing mitochondrial homeostasis. FEBS Lett 2000; 473: 311-15.
46. Day CP, James OF. Steatohepatitis: A tale of two "hits"? Gastroenterology 1998; 114: 842-5.
47. Yamazaki K, Kawai A, Kawaguchi M et al. Simultaneous induction of galectin-3 phosphorylated on tyrosine residue, p21(WAF1/Cip1/Sdi1), and the proliferating cell nuclear antigen at a distinctive period of repair of hepatocytes injured by CCl4. Biochem Biophys Res Commun 2001; 280: 1077-84.
48. Kiwaki K, Novak CM, Hsu DK, Liu FT, Levine JA. Galectin-3 stimulates preadipocyte proliferation and is up-regulated in growing adipose tissue. Obesity (Silver Spring) 2007; 15: 32-9.
49. Shimura T, Takenaka Y, Fukumori T etal. Implication of galectin-3 in Wnt signaling. Cancer Res 2005; 65: 3535-7.
50. Sutherland C, Leighton IA, Cohen P. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: New kinase connections in insulin and growth-factor signalling. Biochem J 1993; 296 (Pt 1): 15-19.
51. Martin M, Rehani K, Jope RS, Michalek SM. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat Immunol 2005; 6: 777-84.
52. Woodgett JR, Ohashi PS. GSK3: An in-Toll-erant protein kinase? Nat Immunol 2005; 6: 751-2.
53. Maeda N, Kawada N, Seki S et al. Stimulation of proliferation of rat hepatic stellate cells by galectin-1 and galectin-3 through different intracellular signaling pathways. J Biol Chem 2003; 278: 18938-44.
54. Henderson NC, Mackinnon AC, Farnworth SL et al. Galectin-3 regulates myofibroblast activation and hepatic fibrosis. Proc Nat Acad Sci USA 2006; 103: 5060-5.
55. Powell EE, Cooksley WG, Hanson R, Searle J, Halliday JW, Powell LW. The natural history of nonalcoholic steatohepatitis: A follow-up study of forty-two patients for up to 21 years. Hepatology 1990; 11: 74-80.
56. Yoshioka Y, Hashimoto E, Yatsuji S et al. Nonalcoholic steatohepatitis: cirrhosis, hepatocellular carcinoma, and burnt-out NASH. J Gastroenterol 2004; 39: 1215-18.
57. Abdelmalek M, Ludwig J, Lindor KD. Two cases from the spectrum of nonalcoholic steatohepatitis. J Clin Gastroenterol 1995; 20: 127-30.
58. Shimada M, Hashimoto E, Taniai M et al. Hepatocellular carcinoma in patients with non-alcoholic steatohepatitis. J Hepatol 2002; 37: 154-60.
59. Hui JM, Kench JG, Chitturi S et al. Long-term outcomes of cirrhosis in nonalcoholic steatohepatitis compared with hepatitis C. Hepatology 2003; 38: 420-7.
60. Schoeppner HL, Raz A, Ho SB, Bresalier RS. Expression of an endogenous galactose-binding lectin correlates with neoplastic progression in the colon. Cancer 1995; 75: 2818-26.
61. Xu XC, El-Naggar AK, Lotan R. Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications. Am J Pathol 1995; 147: 815-22.
62. Fernandez PL, Merino MJ, Gomez M et al. Galectin-3 and laminin expression in neoplastic and non-neoplastic thyroid tissue. J Pathol 1997; 181: 80-6.
63. Chung EJ, Sung YK, Farooq M et al. Gene expression profile analysis in human hepatocellular carcinoma by cDNA microarray. Mol Cells 2002; 14: 382-7.
64. Lotz MM, Andrews CW Jr, Korzelius CA et al. Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its nuclear localization are associated with the neoplastic progression of colon carcinoma. Proc Nat Acad Sci USA 1993; 90: 3466-70.
65. Castronovo V, Van Den Brule FA, Jackers P et al. Decreased expression of galectin-3 is associated with progression of human breast cancer. J Pathol 1996; 179: 43-8.
66. Pacis RA, Pilat MJ, Pienta KJ et al. Decreased galectin-3 expression in prostate cancer. Prostate 2000; 44: 118-23.
67. Ellerhorst JA, Stephens LC, Nguyen T, Xu XC. Effects of galectin-3 expression on growth and tumorigenicity of the prostate cancer cell line LNCaP. Prostate 2002; 50: 64-70.
68. Lee JW, Song SY, Choi JJ et al. Decreased galectin-3 expression during the progression of cervical neoplasia. J Cancer Res Clin Oncol 2006; 132: 241-7.