Genetic susceptibility to chronic hepatitis is inherited codominantly in Helicobacter hepaticus-infected AB6F1 and B6AF1 hybrid male mice, and progression to hepatocellular carcinoma is linked to hepatic expression of lipogenic genes and immune function-associated networks

Infection and Immunity

Volumn 76, Issue 5, 2008, Pages 1866-1876

  García, Alexis ^a   Ihrig, Melanie M ^a   Fry, Rebecca C ^b   Feng, Yan ^a   Xu, Sandy ^a   Boutin, Samuel R ^a   Rogers, Arlin B ^a   Muthupalani, Suresh ^a   Samson, Leona D ^b   Fox, James G ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COENZYME A; FATTY ACID SYNTHASE; TRANSCRIPTOME; ACYL COENZYME A DESATURASE; SCD1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CHRONIC HEPATITIS; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; EUTHANASIA; FATTY LIVER; FEMALE; GENE EXPRESSION; GENETIC ENGINEERING; GENETIC SUSCEPTIBILITY; HELICOBACTER HEPATICUS; HELICOBACTER INFECTION; HISTOLOGY; HYBRID; IMMUNE FUNCTION TEST; IMMUNOPATHOLOGY; INOCULATION; LIPOGENESIS; LIVER CELL CARCINOMA; LIVER INJURY; LIVER TUMOR; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; A J MOUSE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION; GENETICS; HOSPITALIZATION; IMMUNOLOGY; INHERITANCE; LIVER; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; UPREGULATION;

ANIMALS; CARCINOMA, HEPATOCELLULAR; FATTY ACID SYNTHETASE COMPLEX; FATTY LIVER; FEMALE; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; HELICOBACTER HEPATICUS; HELICOBACTER INFECTIONS; HEPATITIS, CHRONIC; INHERITANCE PATTERNS; LIVER; MALE; MICE; MICE, INBRED A; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEVERITY OF ILLNESS INDEX; STEAROYL-COA DESATURASE; UP-REGULATION;

EID: 42949091932     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01044-07     Document Type: Article

References (67)

1. Avenaud, P., A. Marais, L. Monteiro, B. Le Bail, P. Bioulac Sage, C. Balabaud, and F. Megraud. 2000. Detection of Helicobacter species in the liver of patients with and without primary liver carcinoma. Cancer 89:1431-1439.
2. Bosch, F. X., J. Ribes, R. Cleries, and M. Diaz. 2005. Epidemiology of hepatocellular carcinoma. Clin. Liver Dis. 9:191-211.
3. Boutin, S. R., A. B. Rogers, Z. Shen, R. C. Fry, J. A. Love, P. R. Nambiar, S. Suerbaum, and J. G. Fox. 2004. Hepatic temporal gene expression profiling in Helicobacter hepaticus-infected A/JCr mice. Toxicol. Pathol. 32:678-693.
4. Bucher, J. R., J. R. Hailey, J. R. Roycroft, J. K. Haseman, R. C. Sills, S. L. Grumbein, P. W. Mellick, and B. J. Chou. 1999. Inhalation toxicity and carcinogenicity studies of cobalt sulfate. Toxicol. Sci. 49:56-67.
5. Caldwell, S. H., D. M. Crespo, H. S. Rang, and A. M. Al-Osaimi. 2004. Obesity and hepatocellular carcinoma. Gastroenterology 127:S97-S103.
6. Chang, Y., J. Wang, X. Lu, D. P. Thewke, and R. J. Mason. 2005. KGF induces lipogenic genes through a PI3K and JNK/SREBP-1 pathway in H292 cells. J. Lipid Res. 46:2624-2635.
7. Correa, P. 2004. The biological model of gastric carcinogenesis. IARC Sci. Publ. 2004:301-310.
8. Davila, J. A., N. J. Petersena, H. A. Nelson, and H. B. El-Serag. 2003. Geographic variation within the United States in the incidence of hepatocellular carcinoma. J. Clin. Epidemiol. 56:487-493.
9. Dore, M. P., G. Realdi, D. Mura, D. Y. Graham, and A. R. Sepulveda. 2002. Helicobacter infection in patients with HCV-related chronic hepatitis, cirrhosis, and hepatocellular carcinoma. Dig. Dis. Sci. 47:1638-1643.
10. Downey, T. 2006. Analysis of a multifactor microarray study using Partek genomics solution. Methods Enzymol. 411:256-270.
11. El-Serag, H. B. 2004. Hepatocellular carcinoma: recent trends in the United States. Gastroenterology 127:S27-S34.
12. Eppinger, M., C. Baar, G. Raddatz, D. H. Huson, and S. C. Schuster. 2004. Comparative analysis of four Campylobacterales. Nat. Rev. Microbiol. 2:872-885.
13. + regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res. 63:6042-6050.
14. Evert, M., R. Schneider-Stock, and F. Dombrowski. 2005. Overexpression of fatty acid synthase in chemically and hormonally induced hepatocarcinogenesis of the rat. Lab. Investig. 85:99-108.
15. Falvella, F. S., R. M. Pascale, M. Gariboldi, G. Manenti, M. R. De Miglio, M. M. Simile, T. A. Dragani, and F. Feo. 2002. Stearoyl-CoA desaturase 1 (Scd1) gene overexpression is associated with genetic predisposition to hepatocarcinogenesis in mice and rats. Carcinogenesis 23:1933-1936.
16. Fan, X. G., X. N. Peng, Y. Huang, J. Yakoob, Z. M. Wang, and Y. P. Chen. 2002. Helicobacter species ribosomal DNA recovered from the liver tissue of Chinese patients with primary hepatocellular carcinoma. Clin. Infect. Dis. 35:1555-1557.
17. Farinha, P., and R. D. Gascoyne. 2005. Helicobacter pylori and MALT lymphoma. Gastroenterology 128:1579-1605.
18. Fox, J. G., F. E. Dewhirst, Z. Shen, Y. Feng, N. S. Taylor, B. J. Paster, R. L. Ericson, C. N. Lau, P. Correa, J. C. Araya, and I. Roa. 1998. Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 114:755-763.
19. Fox, J. G., F. E. Dewhirst, J. G. Tully, B. J. Paster, L. Yan, N. S. Taylor, M. J. Collins, Jr., P. L. Gorelick, and J. M. Ward. 1994. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J. Clin. Microbiol. 32:1238-1245.
20. Fox, J. G., X. Li, L. Yan, R. J. Cahill, R. Hurley, R. Lewis, and J. C. Murphy. 1996. Chronic proliferative hepatitis in A/JCr mice associated with persistent Helicobacter hepaticus infection: a model of Helicobacter-induced carcinogenesis. Infect. Immun. 64:1548-1558.
21. Fox, J. G., A. B. Rogers, M. Ihrig, N. S. Taylor, M. T. Whary, G. Dockray, A. Varro, and T. C. Wang. 2003. Helicobacter pylori-associated gastric cancer in INS-GAS mice is gender specific. Cancer Res. 63:942-950.
22. Fox, J. G., T. C. Wang, A. B. Rogers, T. Poutahidis, Z. Ge, N. Taylor, C. A. Dangler, D. A. Israel, U. Krishna, K. Gaus, and R. M. Peek, Jr. 2003. Host and microbial constituents influence Helicobacter pylori-induced cancer in a murine model of hypergastrinemia. Gastroenterology 124:1879-1890.
23. Ge, Z., A. B. Rogers, Y. Feng, A. Lee, S. Xu, N. S. Taylor, and J. G. Fox. 2007. Bacterial cytolethal distending toxin promotes the development of dysplasia in a model of microbially induced hepatocarcinogenesis. Cell Microbiol. 9:2070-2080.
24. Gutierrez-Juarez, R., A. Pocai, C. Mulas, H. Ono, S. Bhanot, B. P. Monia, and L. Rossetti. 2006. Critical role of stearoyl-CoA desaturase-1 (SCD1) in the onset of diet-induced hepatic insulin resistance. J. Clin. Investig. 116:1686-1695.
25. Hailey, J. R., J. K. Haseman, J. R. Bucher, A. E. Radovsky, D. E. Malarkey, R. T. Miller, A. Nyska, and R. R. Maronpot. 1998. Impact of Helicobacter hepaticus infection in B6C3F1 mice from twelve National Toxicology Program two-year carcinogenesis studies. Toxicol. Pathol. 26:602-611.
26. Herkel, J., M. Schuchmann, G. Tiegs, and A. W. Lohse. 2005. Immune-mediated liver injury. J. Hepatol. 42:920-923.
27. Hohler, T., G. Gerken, A. Notghi, P. Knolle, R. Lubjuhn, H. Taheri, P. M. Schneider, K. H. Meyer zum Buschenfelde, and C. Rittner. 1997. MHC class II genes influence the susceptibility to chronic active hepatitis C. J. Hepatol. 27:259-264.
28. Huang, Y., X. G. Fan, Z. M. Wang, J. H. Zhou, X. F. Tian, and N. Li. 2004. Identification of Helicobacter species in human liver samples from patients with primary hepatocellular carcinoma. J. Clin. Pathol. 57:1273-1277.
29. Ihrig, M., M. D. Schrenzel, and J. G. Fox. 1999. Differential susceptibility to hepatic inflammation and proliferation in AXB recombinant inbred mice chronically infected with Helicobacter hepaticus. Am. J. Pathol. 155:571-582.
30. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, and T. P. Speed. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31:e15.
31. Jiang, G., Z. Li, F. Liu, K. Ellsworth, Q. Dallas-Yang, M. Wu, J. Ronan, C. Esau, C. Murphy, D. Szalkowski, R. Bergeron, T. Doebber, and B. B. Zhang. 2005. Prevention of obesity in mice by antisense oligonucleotide inhibitors of stearoyl-CoA desaturase-1. J. Clin. Investig. 115:1030- 1038.
32. Kim, H. S., and M. S. Lee. 2007. STAT1 as a key modulator of cell death. Cell Signal. 19:454-465.
33. Lacroix-Triki, M., L. Lacoste-Collin, S. Jozan, J. P. Charlet, C. Caratero, and M. Courtade. 2003. Histiocytic sarcoma in C57BL/6J female mice is associated with liver hematopoiesis: review of 41 cases. Toxicol. Pathol. 31:304-309.
34. Luedde, T., N. Beraza, V. Kotsikoris, G. van Loo, A. Nenci, R. De Vos, T. Roskams, C. Trautwein, and M. Pasparakis. 2007. Deletion of NEMO/IKKγ in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 11:119-132.
35. Matsukura, N., S. Yokomuro, S. Yamada, T. Tajiri, T. Sundo, T. Hadama, S. Kamiya, Z. Naito, and J. G. Fox. 2002. Association between Helicobacter bilis in bile and biliary tract malignancies: H. bilis in bile from Japanese and Thai patients with benign and malignant diseases in the biliary tract. Jpn. J. Cancer Res. 93:842-847.
36. Maurer, K. J., M. M. Ihrig, A. B. Rogers, V. Ng, G. Bouchard, M. R. Leonard, M. C. Carey, and J. G. Fox. 2005. Identification of cholelithogenic enterohepatic Helicobacter species and their role in murine cholesterol gallstone formation. Gastroenterology 128:1023-1033.
37. Maurer, K. J., V. P. Rao, Z. Ge, A. B. Rogers, T. J. Oura, M. C. Carey, and J. G. Fox. 2007. T-cell function is critical for murine cholesterol gallstone formation. Gastroenterology 133:1304-1315.
38. Maurer, K. J., A. B. Rogers, Z. Ge, A. J. Wiese, M. C. Carey, and J. G. Fox. 2006. Helicobacter pylori and cholesterol gallstone formation in C57L/J. mice: a prospective study. Am. J. Physiol. Gastrointest. Liver Physiol. 290:G175-G182.
39. Nilsson, H. O., J. Taneera, M. Castedal, E. Glatz, R. Olsson, and T. Wadstrom. 2000. Identification of Helicobacter pylori and other Helicobacter species by PCR, hybridization, and partial DNA sequencing in human liver samples from patients with primary sclerosing cholangitis or primary biliary cirrhosis. J. Clin. Microbiol. 38:1072-1076.
40. Nyska, A., R. R. Maronpot, S. R. Eldridge, J. K. Haseman, and J. R. Hailey. 1997. Alteration in cell kinetics in control B6C3F1 mice infected with Helicobacter hepaticus. Toxicol. Pathol. 25:591-596.
41. Ohtani, M., A. Garcia, A. B. Rogers, Z. Ge, N. S. Taylor, S. Xu, K. Watanabe, R. P. Marini, M. T. Whary, T. C. Wang, and J. G. Fox. 2007. Protective role of 17β-estradiol against the development of Helicobacter pylori-induced gastric cancer in INS-GAS mice. Carcinogenesis 28:2597-2604.
42. Pellicano, R., V. Mazzaferro, W. F. Grigioni, M. A. Cutufia, S. Fagoonee, L. Silengo, M. Rizzetto, and A. Ponzetto. 2004. Helicobacter species sequences in liver samples from patients with or without hepatocellular carcinoma. World J. Gastroenterol. 10:598-601.
43. Rao, V. P., T. Poutahidis, Z. Ge, P. R. Nambiar, C. Boussahmain, Y. Y. Wang, B. H. Horwitz, J. G. Fox, and S. E. Erdman. 2006. Innate immune inflammatory response against enteric bacteria Helicobacter hepaticus induces mammary adenocarcinoma in mice. Cancer Res. 66:7395-7400.
44. Reddy, J. K., and M. S. Rao. 2006. Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation. Am. J. Physiol. Gastrointest Liver Physiol. 290:G852-G858.
45. Rocha, M., P. Avenaud, A. Menard, B. Le Bail, C. Balabaud, P. Bioulac-Sage, D. M. de Magalhaesq Ueiroz, and F. Megraud. 2005. Association of Helicobacter species with hepatitis C cirrhosis with or without hepatocellular carcinoma. Gut 54:396-401.
46. Rogers, A. B., S. R. Boutin, M. T. Whary, N. Sundina, Z. Ge, K. Cormier, and J. G. Fox. 2004. Progression of chronic hepatitis and preneoplasia in Helicobacter hepaticus-infected A/JCr mice. Toxicol. Pathol. 32:668-677.
47. Rogers, A. B., and J. G. Fox. 2004. Inflammation and Cancer I. Rodent models of infectious gastrointestinal and liver cancer. Am. J. Physiol. Gastrointest. Liver Physiol. 286:G361-G366.
48. Rogers, A. B., E. J. Theve, Y. Feng, R. C. Fry, K. Taghizadeh, K. M. Clapp, C. Bonssahmain, K. S. Cormier, and J. G. Fox. 2007. Hepatocellular carcinoma associated with liver-gender disruption in male mice. Cancer Res. 67:11536-11546.
49. Scaglia, N., and R. A. Igal. 2005. Stearoyl-CoA desaturase is involved in the control of proliferation, anchorage-independent growth, and survival in human transformed cells. J. Biol. Chem. 280:25339-25349.
50. Schramm, C., M. Protschka, H. H. Kohler, J. Podlech, M. J. Reddehase, P. Schirmacher, P. R. Galle, A. W. Lohse, and M. Blessing. 2003. Impairment of TGF-β signaling in T cells increases susceptibility to experimental autoimmune hepatitis in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 284:G525-G535.
51. Shames, B., J. G. Fox, F. Dewhirst, L. Yan, Z. Shen, and N. S. Taylor. 1995. Identification of widespread Helicobacter hepaticus infection in feces in commercial mouse colonies by culture and PCR assay. J. Clin. Microbiol. 33:2968-2972.
52. Sheppard, F. R., M. R. Kelher, E. E. Moore, N. J. McLaughlin, A. Banerjee, and C. C. Silliman. 2005. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J. Leukoc. Biol. 78:1025-1042.
53. Shi, X., L. Leng, T. Wang, W. Wang, X. Du, J. Li, C. McDonald, Z. Chen, J. W. Murphy, E. Lolis, P. Noble, W. Knudson, and R. Bucala. 2006. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 25:595-606.
54. Singh, R., C. Leuratti, S. Josyula, M. A. Sipowicz, B. A. Diwan, K. S. Kasprzak, H. A. Schut, L. J. Marnett, L. M. Anderson, and D. E. Shuker. 2001. Lobe-specific increases in malondialdehyde DNA adduct formation in the livers of mice following infection with Helicobacter hepaticus. Carcinogenesis 22:1281-1287.
55. Sipowicz, M. A., P. Chomarat, B. A. Diwan, M. A. Anver, Y. C. Awasthi, J. M. Ward, J. M. Rice, K. S. Kasprzak, C. P. Wild, and L. M. Anderson. 1997. Increased oxidative DNA damage and hepatocyte overexpression of specific cytochrome P450 isoforms in hepatitis of mice infected with Helicobacter hepaticus. Am. J. Pathol. 151:933-941.
56. Stafforini, D. M., J. R. Sheller, T. S. Blackwell, A. Sapirstein, F. E. Yull, T. M. McIntyre, J. V. Bonventre, S. M. Prescott, and L. J. Roberts, 2nd. 2006. Release of free F2-isoprostanes from esterified phospholipids is catalyzed by intracellular and plasma platelet-activating factor acetylhydrolases. J. Biol. Chem. 281:4616-4623.
57. Stoicov, C., R. Saffari, X. Cai, C. Hasyagar, and J. Houghton. 2004. Molecular biology of gastric cancer: Helicobacter infection and gastric adenocarcinoma: bacterial and host factors responsible for altered growth signaling. Gene 341:1-17.
58. Suerbaum, S., C. Josenhans, T. Sterzenbach, B. Drescher, P. Brandt, M. Bell, M. Droge, B. Fartmann, H. P. Fischer, Z. Ge, A. Horster, R. Holland, K. Klein, J. Konig, L. Macko, G. L. Mendz, G. Nyakatura, D. B. Schauer, Z. Shen, J. Weber, M. Frosch, and J. G. Fox. 2003. The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc. Natl. Acad. Sci. USA 100:7901-7906.
59. Sutton, P., T. Kolesnikow, S. Danon, J. Wilson, and A. Lee. 2000. Dominant nonresponsiveness to Helicobacter pylori infection is associated with production of interleukin 10 but not gamma interferon. Infect. Immun. 68:4802-4804.
60. Takaki, H., Y. Minoda, K. Koga, G. Takaesu, A. Yoshimura, and T. Kobayashi. 2006. TGF-β1 suppresses IFN-γ-induced NO production in macrophages by suppressing STAT1 activation and accelerating iNOS protein degradation. Genes Cells 11:871-882.
61. Vorobjova, T., I. Nilsson, S. Terjajev, M. Granholm, M. Lyyra, T. Porkka, T. Prukk, R. Salupere, H. I. Maaroos, T. Wadstrom, and R. Uibo. 2006. Serum antibodies to enterohepatic Helicobacter spp. in patients with chronic liver diseases and in a population with high prevalence of H. pylori infection. Dig. Liver Dis. 38:171-176.
62. Wang, G., Y. Hong, M. K. Johnson, and R. J. Maier. 2006. Lipid peroxidation as a source of oxidative damage in Helicobacter pylori: protective roles of peroxiredoxins. Biochim. Biophys. Acta 1760:1596- 1603.
63. Ward, J. M., M. R. Anver, D. C. Haines, and R. E. Benveniste. 1994. Chronic active hepatitis in mice caused by Helicobacter hepaticus. Am. J. Pathol. 145:959-968.
64. Ward, J. M., J. G. Fox, M. R. Anver, D. C. Haines, C. V. George, M. J. Collins, Jr., P. L. Gorelick, K. Nagashima, M. A. Gonda, R. V. Gilden, et al. 1994. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J. Natl. Cancer Inst. 86:1222-1227.
65. Whary, M. T., J. Cline, A. King, Z. Ge, Z. Shen, B. Sheppard, and J. G. Fox. 2001. Long-term colonization levels of Helicobacter hepaticus in the cecum of hepatitis-prone A/JCr mice are significantly lower than those in hepatitis-resistant C57BL/6 mice. Comp. Med. 51:413-417.
66. Whary, M. T., T. J. Morgan, C. A. Dangler, K. J. Gaudes, N. S. Taylor, and J. G. Fox. 1998. Chrome active hepatitis induced by Helicobacter hepaticus in the A/JCr mouse is associated with a Th1 cell-mediated immune response. Infect. Immun. 66:3142-3148.
67. Zhang, B., S. Kirov, and J. Snoddy. 2005. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 33:W741-W748.