The FLS (Fatty liver Shionogi) mouse reveals local expressions of lipocalin-2, CXCL1 and CXCL9 in the liver with non-alcoholic steatohepatitis

BMC Gastroenterology

Volumn 13, Issue 1, 2013, Pages

  Semba, Toshihisa ^a   Nishimura, Motoi ^a,b   Nishimura, Satomi ^a   Ohara, Osamu ^c   Ishige, Takayuki ^a   Ohno, Sayaka ^b   Nonaka, Ken ^c   Sogawa, Kazuyuki ^a,b   Satoh, Mamoru ^a,b   Sawai, Setsu ^a,b   Matsushita, Kazuyuki ^a,b   Imazeki, Fumio ^a   Yokosuka, Osamu ^a   Nomura, Fumio ^a,b  

^a CHIBA UNIVERSITY   (Japan)

^b CHIBA UNIVERSITY HOSPITAL   (Japan)

^c KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Adipokine; Chemokine; Immunohistochemistry; Non alcoholic steatohepatitis; Pathogenesis

Indexed keywords

CXCL1 CHEMOKINE; CXCL9 CHEMOKINE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CXCL1 CHEMOKINE GENE; CXCL9 CHEMOKINE GENE; DISEASE MODEL; DNA MICROARRAY; FATTY LIVER; FATTY LIVER SHIONOGI MODEL; GENE; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; IMMUNOHISTOCHEMISTRY; LIPOCALIN 2 GENE; LIVER CELL; LIVER NECROSIS; MOLECULAR PATHOLOGY; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ACUTE-PHASE PROTEINS; ANIMALS; CHEMOKINE CXCL1; CHEMOKINE CXCL9; DISEASE MODELS, ANIMAL; FATTY LIVER; GENE EXPRESSION PROFILING; HEPATOCYTES; IMMUNOHISTOCHEMISTRY; LIPOCALINS; LIVER; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENE PROTEINS; STATISTICS, NONPARAMETRIC; TRANSCRIPTOME; UP-REGULATION;

EID: 84880335250     PISSN: None     EISSN: 1471230X     Source Type: Journal    
DOI: 10.1186/1471-230X-13-120     Document Type: Article

References (45)

1. Ong JP, Younossi ZM. Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis 2007, 11(1):1-16. 10.1016/j.cld.2007.02.009, 17544968.
2. Marchesini G. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 2003, 37(4):917-923. 10.1053/jhep.2003.50161, 12668987.
3. Marchesini G, Brizi M, Bianchi G, Tomassetti S, Bugianesi E, Lenzi M, McCullough AJ, Natale S, Forlani G, Melchionda N. Nonalcoholic fatty liver disease. Diabetes 2001, 50(8):1844-1850. 10.2337/diabetes.50.8.1844, 11473047.
4. Angulo P, Lindor KD. Non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2002, 17:S186-S190.
5. Caldwell SH, Oelsner DH, Iezzoni JC, Hespenheide EE, Battle EH, Driscoll CJ. Cryptogenic cirrhosis: clinical characterization and risk factors for underlying disease. Hepatology 1999, 29(3):664-669. 10.1002/hep.510290347, 10051466.
6. Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, Angulo P. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 2005, 129(1):113-121. 10.1053/j.gastro.2005.04.014, 16012941.
7. Matteoni CA, Younossi ZM, Gramlich‡ T, Boparai§ N, Liu∥ YC, McCullough¶ AJ. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 1999, 116(6):1413-1419. 10.1016/S0016-5085(99)70506-8, 10348825.
8. Day CP. Natural history of NAFLD: remarkably benign in the absence of cirrhosis. Gastroenterology 2005, 129(1):375-378. 10.1053/j.gastro.2005.05.041, 16012969.
9. Day CP, James OFW. Steatohepatitis: a tale of two " hits" ?. Gastroenterology 1998, 114(4):842-845. 10.1016/S0016-5085(98)70599-2, 9547102.
10. Abiru S, Migita K, Maeda Y, Daikoku M, Ito M, Ohata K, Nagaoka S, Matsumoto T, Takii Y, Kusumoto K, et al. Serum cytokine and soluble cytokine receptor levels in patients with non-alcoholic steatohepatitis. Liver Int 2006, 26(1):39-45. 10.1111/j.1478-3231.2005.01191.x, 16420507.
11. Podrini C, Borghesan M, Greco A, Pazienza V, Mazzoccoli G, Vinciguerra M. Redox homeostasis and epigenetics in non-alcoholic fatty liver disease (NAFLD). Curr Pharm Des 2013, 19(15):2737-2746. 10.2174/1381612811319150009, 23092327.
12. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 2010, 52(5):1836-1846. 10.1002/hep.24001, 21038418.
13. Piccinino F, Sagnelli E, Pasquale G, Giusti G, Battocchia A, Bernardi M, Bertolazzi R, Bianchi FB, Brunelli E, Budillon G, et al. Complications following percutaneous liver biopsy: a multicentre retrospective study on 68 276 biopsies. J Hepatol 1986, 2(2):165-173. 10.1016/S0168-8278(86)80075-7, 3958472.
14. Austin BP, Garthwaite TL, Hagen TC, Stevens JO, Menahan LA. Hormonal, metabolic and morphologic studies of aged C57BL/6J obese mice. Exp Gerontol 1984, 19(2):121-132. 10.1016/0531-5565(84)90015-9, 6734767.
15. Coleman D, Hummel K. Studies with the mutation, diabetes, in the mouse. Diabetologia 1967, 3(2):238-248. 10.1007/BF01222201, 4907142.
16. Naggert JK, Fricker LD, Varlamov O, Nishina PM, Rouille Y, Steiner DF, Carroll RJ, Paigen BJ, Leiter EH. Hyperproinsulinaemia in obese fat/fat mice associated with a carboxypeptidase E mutation which reduces enzyme activity. Nat Genet 1995, 10(2):135-142. 10.1038/ng0695-135, 7663508.
17. Noben-Trauth K, Naggert JK, North MA, Nishina PM. A candidate gene for the mouse mutation tubby. Nature 1996, 380(6574):534-538. 10.1038/380534a0, 8606774.
18. Soga M, Kishimoto Y, Kawaguchi J, Nakai Y, Kawamura Y, Inagaki S, Katoh K, Oohara T, Makino S, Oshima I. The FLS mouse: a New inbred strain with spontaneous fatty liver. Comp Med 1999, 49(3):269-275.
19. Soga M, Kishimoto Y, Kawamura Y, Inagaki S, Makino S, Saibara T. Spontaneous development of hepatocellular carcinomas in the FLS mice with hereditary fatty liver. Cancer Lett 2003, 196(1):43-48. 10.1016/S0304-3835(03)00213-1, 12860288.
20. Harano Y, Yasui K, Toyama T, Nakajima T, Mitsuyoshi H, Mimani M, Hirasawa T, Itoh Y, Okanoue T. Fenofibrate, a peroxisome proliferator-activated receptor alpha agonist, reduces hepatic steatosis and lipid peroxidation in fatty liver shionogi mice with hereditary fatty liver. Liver Int 2006, 26(5):613-620. 10.1111/j.1478-3231.2006.01265.x, 16762007.
21. Oze-Fukai A, Fujisawa T, Sugimoto K, Nojima K, Shindo N, Shimoyoshi S, Yoshikawa Y, Sato Y, Shimomura I, Ikegami H, et al. A novel mouse model for type 2 diabetes and non-alcoholic fatty liver disease: spontaneous amelioration of diabetes by augmented beta cell mass. Endocr J 2009, 56(2):227-234. 10.1507/endocrj.K08E-315, 19088402.
22. Shindo N, Fujisawa T, Sugimoto K, Nojima K, Oze-Fukai A, Yoshikawa Y, Wang X, Yasuda O, Ikegami H, Rakugi H. Involvement of microsomal triglyceride transfer protein in nonalcoholic steatohepatitis in novel spontaneous mouse model. J Hepatol 2010, 52(6):903-912. 10.1016/j.jhep.2009.12.033, 20392512.
23. Tajima Y. Species and strains of laboratory animals developed in Japan Species and strains of laboratory animals developed in Japan. Exp Animals 1968, 17:27-39.
24. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci 2001, 98(1):31-36. 10.1073/pnas.98.1.31, 14539, 11134512.
25. Hübscher SG. Histological assessment of non-alcoholic fatty liver disease. Histopathology 2006, 49(5):450-465. 10.1111/j.1365-2559.2006.02416.x, 17064291.
26. Matsuo T, Ikura Y, Ohsawa M, Ogami M, Kayo S, Yoshimi N, Hai E, Naruko T, Ohishi M, Higuchi K, et al. Mast cell chymase expression in helicobacter pylori-associated gastritis. Histopathology 2003, 43(6):538-549. 10.1111/j.1365-2559.2003.01731.x, 14636254.
27. Satoh M, Haruta-Satoh E, Yamada M, Kado S, Nomura F. Overexpression of hydroxymethylglutaryl CoA synthase 2 and 2,4-dienoyl-CoA reductase in rat pancreas following chronic alcohol consumption. Pancreas 2012, in press.
28. Team RDC: R Development Core Team R: a language and environment for statistical computing 2011, Vienna: R Foundation for Statistical Computing, http://wwwr-projectorg/ 2011, Team RDC: R Development Core Team.
29. Kjeldsen L, Johnsen AH, Sengeløv H, Borregaard N. Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 1993, 268(14):10425-10432.
30. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, Strong RK, Akira S, Aderem A. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004, 432(7019):917-921. 10.1038/nature03104, 15531878.
31. Roudkenar MH, Kuwahara Y, Baba T, Roushandeh AM, Ebishima S, Abe S, Ohkubo Y, Fukumoto M. Oxidative stress induced lipocalin 2 gene expression: addressing its expression under the harmful conditions. J Radiat Res 2007, 48(1):39-44. 10.1269/jrr.06057, 17229997.
32. Roudkenar MH, Halabian R, Ghasemipour Z, Roushandeh AM, Rouhbakhsh M, Nekogoftar M, Kuwahara Y, Fukumoto M, Shokrgozar MA. Neutrophil gelatinase-associated lipocalin acts as a protective factor against H2O2 toxicity. Arch Med Res 2008, 39(6):560-566. 10.1016/j.arcmed.2008.05.003, 18662586.
33. Wang Y, Lam KSL, Kraegen EW, Sweeney G, Zhang J, Tso AWK, Chow WS, Wat NMS, Xu JY, Hoo RLC, et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem 2006, 53(1):34-41. 10.1373/clinchem.2006.075614, 17040956.
34. Catalán V, Gómez-Ambrosi J, Rodríguez A, Ramírez B, Silva C, Rotellar F, Gil MJ, Cienfuegos JA, Salvador J, Frühbeck G. Increased adipose tissue expression of lipocalin-2 in obesity is related to inflammation and matrix metalloproteinase-2 and metalloproteinase-9 activities in humans. J Mol Med 2009, 87(8):803-813. 10.1007/s00109-009-0486-8, 19466389.
35. Moser B, Clark-Lewis I, Zwahlen R, Baggiolini M. Neutrophil-activating properties of the melanoma growth-stimulatory activity. J Exp Med 1990, 171(5):1797-1802. 10.1084/jem.171.5.1797, 2187876, 2185333.
36. Maher JJ, Scott MK, Saito JM, Burton MC. Adenovirus-mediated expression of cytokine-induced neutrophil chemoattractant in rat liver induces a neutrophilic hepatitis. Hepatology 1997, 25(3):624-630. 10.1002/hep.510250322, 9049209.
37. Maltby J, Wright S, Bird G, Sheron N. Chemokine levels in human liver homogenates: associations between GRO α and histopathological evidence of alcoholic hepatitis. Hepatology 1996, 24(5):1156-1160.
38. Talukdar S, Oh DY, Bandyopadhyay G, Li D, Xu J, McNelis J, Lu M, Li P, Yan Q, Zhu Y, et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat Med 2012, 18(9):1407-1412. 10.1038/nm.2885, 3491143, 22863787.
39. Yamashita A, Soga Y, Iwamoto Y, Asano T, Li Y, Abiko Y, Nishimura F. DNA microarray analyses of genes expressed differentially in 3T3-L1 adipocytes co-cultured with murine macrophage cell line RAW264.7 In the presence of the toll-like receptor 4 ligand bacterial endotoxin. Int J Obes 2008, 32(11):1725-1729.
40. Feldstein AE, Canbay A, Guicciardi ME, Higuchi H, Bronk SF, Gores GJ. Diet associated hepatic steatosis sensitizes to Fas mediated liver injury in mice. J Hepatol 2003, 39(6):978-983. 10.1016/S0168-8278(03)00460-4, 14642615.
41. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004, 25(12):677-686. 10.1016/j.it.2004.09.015, 15530839.
42. Park J-W, Gruys ME, McCormick K, Lee J-K, Subleski J, Wigginton JM, Fenton RG, Wang J-M, Wiltrout RH. Primary hepatocytes from mice treated with IL-2/IL-12 produce T cell chemoattractant activity that is dependent on monokine induced by IFN-γ (Mig) and chemokine responsive to γ-2 (Crg-2). J Immunol 2001, 166(6):3763-3770.
43. Zeremski M, Petrovic LM, Chiriboga L, Brown QB, Yee HT, Kinkhabwala M, Jacobson IM, Dimova R, Markatou M, Talal AH. Intrahepatic levels of CXCR3-associated chemokines correlate with liver inflammation and fibrosis in chronic hepatitis C. Hepatology 2008, 48(5):1440-1450. 10.1002/hep.22500, 2579317, 18798334.
44. Wasmuth HE, Lammert F, Zaldivar MM, Weiskirchen R, Hellerbrand C, Scholten D, Berres M-L, Zimmermann H, Streetz KL, Tacke F, et al. Antifibrotic effects of CXCL9 and its receptor CXCR3 in livers of mice and humans. Gastroenterology 2009, 137(1):309-319. e303, 10.1053/j.gastro.2009.03.053, 2892869, 19344719.
45. Schrage A, Wechsung K, Neumann K, Schumann M, Schulzke J-D, Engelhardt B, Zeitz M, Hamann A, Klugewitz K. Enhanced T cell transmigration across the murine liver sinusoidal endothelium is mediated by transcytosis and surface presentation of chemokines. Hepatology 2008, 48(4):1262-1272. 10.1002/hep.22443, 18697212.