Mutant p53 in concert with an interleukin-27 receptor alpha deficiency causes spontaneous liver inflammation, fibrosis, and steatosis in mice

Hepatology

Volumn 63, Issue 3, 2016, Pages 1000-1012

  Dibra, Denada ^a   Xia, Xueqing ^a   Mitra, Abhisek ^a   Cutrera, Jeffry J ^a   Lozano, Guillermina ^a   Li, Shulin ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; ENDOTHELIN A RECEPTOR; INTERLEUKIN 27 RECEPTOR ALPHA; INTERLEUKIN RECEPTOR; PROTEIN P53; UNCLASSIFIED DRUG; ZIBOTENTAN; CYTOKINE RECEPTOR; IL27RA PROTEIN, MOUSE;

AGE; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL INFILTRATION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FATTY LIVER; FLOW CYTOMETRY; GENE MUTATION; GENE TARGETING; GENOTYPE; HEPATITIS; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INTERLEUKIN 27 RECEPTOR ALPHA DEFICIENCY; LIPID STORAGE; LIVER CELL; LIVER FIBROSIS; MACROPHAGE; MOUSE; MOUSE MODEL; NATURAL KILLER CELL; NONALCOHOLIC FATTY LIVER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; IMMUNOLOGY; METABOLISM; TUMOR SUPPRESSOR GENE;

ANIMALS; GENES, P53; MACROPHAGES; MICE, INBRED C57BL; MICE, TRANSGENIC; NON-ALCOHOLIC FATTY LIVER DISEASE; RECEPTOR, ENDOTHELIN A; RECEPTORS, CYTOKINE;

EID: 84955454341     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.28379     Document Type: Article

References (36)

1. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT, et al. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004;119:847-860.
2. Lang GA, Iwakuma T, Suh YA, Liu G, Rao VA, Parant JM, et al. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 2004;119:861-872.
3. Dibra D, Mishra L, Li S. Molecular mechanisms of oncogene-induced inflammation and inflammation-sustained oncogene activation in gastrointestinal tumors: an underappreciated symbiotic relationship. Biochim Biophys Acta 2014;1846:152-160.
4. Cooks T, Pateras IS, Tarcic O, Solomon H, Schetter AJ, Wilder S, et al. Mutant p53 prolongs NF-kappaB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell 2013;23:634-646.
5. Abiru S, Migita K, Maeda Y, Daikoku M, Ito M, Ohata K, et al. Serum cytokine and soluble cytokine receptor levels in patients with non-alcoholic steatohepatitis. Liver Int 2006;26:39-45.
6. Weisz L, Damalas A, Liontos M, Karakaidos P, Fontemaggi G, Maor-Aloni R, et al. Mutant p53 enhances nuclear factor kappaB activation by tumor necrosis factor alpha in cancer cells. Cancer Res 2007;67:2396-2401.
7. Scian MJ, Stagliano KE, Anderson MA, Hassan S, Bowman M, Miles MF, et al. Tumor-derived p53 mutants induce NF-kappaB2 gene expression. Mol Cell Biol 2005;25:10097-10110.
8. Schneider G, Henrich A, Greiner G, Wolf V, Lovas A, Wieczorek M, et al. Cross talk between stimulated NF-kappaB and the tumor suppressor p53. Oncogene 2010;29:2795-2806.
9. Akyol G, Dursun A, Poyraz A, Uluoglu O, Ataoglu O, Edaly N, Memis L. P53 and proliferating cell nuclear antigen (PCNA) expression in non-tumoral liver diseases. Pathol Int 1999;49:214-221.
10. Panasiuk A, Dzieciol J, Panasiuk B, Prokopowicz D. Expression of p53, Bax and Bcl-2 proteins in hepatocytes in non-alcoholic fatty liver disease. World J Gastroenterol 2006;12:6198-6202.
11. Attallah AM, Shiha GE, Ismail H, Mansy SE, El-Sherbiny R, El-Dosoky I. Expression of p53 protein in liver and sera of patients with liver fibrosis, liver cirrhosis or hepatocellular carcinoma associated with chronic HCV infection. Clin Biochem 2009;42:455-461.
12. Loguercio C, Cuomo A, Tuccillo C, Gazzerro P, Cioffi M, Molinari AM, Del Vecchio Blanco C. Liver p53 expression in patients with HCV-related chronic hepatitis. J Viral Hepat 2003;10:266-270.
13. Kodama T, Takehara T, Hikita H, Shimizu S, Shigekawa M, Tsunematsu H, et al. Increases in p53 expression induce CTGF synthesis by mouse and human hepatocytes and result in liver fibrosis in mice. J Clin Invest 2011;121:3343-3356.
14. Lujambio A, Akkari L, Simon J, Grace D, Tschaharganeh DF, Bolden JE, et al. Non-cell-autonomous tumor suppression by p53. Cell 2013;153:449-460.
15. Hunter CA, Kastelein R. Interleukin-27: balancing protective and pathological immunity. Immunity 2012;37:960-969.
16. Chen Y, Jiang G, Yang HR, Gu X, Wang L, Hsieh CC, et al. Distinct response of liver myeloid dendritic cells to endotoxin is mediated by IL-27. J Hepatol 2009;51:510-519.
17. Yamanaka A, Hamano S, Miyazaki Y, Ishii K, Takeda A, Mak TW, et al. Hyperproduction of proinflammatory cytokines by WSX-1-deficient NKT cells in concanavalin A-induced hepatitis. J Immunol 2004;172:3590-3596.
18. Nagy ZS, LeBaron MJ, Ross JA, Mitra A, Rui H, Kirken RA. STAT5 regulation of BCL10 parallels constitutive NFkappaB activation in lymphoid tumor cells. Mol Cancer 2009;8:67.
19. Dibra D, Cutrera J, Xia X, Kallakury B, Mishra L, Li S. Interleukin-30: a novel antiinflammatory cytokine candidate for prevention and treatment of inflammatory cytokine-induced liver injury. Hepatology 2012;55:1204-1214.
20. Dibra D, Cutrera JJ, Xia X, Birkenbach MP, Li S. Expression of WSX1 in tumors sensitizes IL-27 signaling-independent natural killer cell surveillance. Cancer Res 2009;69:5505-5513.
21. Mitra A, Satelli A, Yan J, Xueqing X, Gagea M, Hunter CA, et al. IL-30 (IL27p28) attenuates liver fibrosis through inducing NKG2D-rae1 interaction between NKT and activated hepatic stellate cells in mice. Hepatology 2014;60:2027-2039.
22. Stienstra R, Saudale F, Duval C, Keshtkar S, Groener JE, van Rooijen N, et al. Kupffer cells promote hepatic steatosis via interleukin-1beta-dependent suppression of peroxisome proliferator-activated receptor alpha activity. Hepatology 2010;51:511-522.
23. Wolf MJ, Adili A, Piotrowitz K, Abdullah Z, Boege Y, Stemmer K, et al. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell 2014;26:549-564.
24. Gandhi CR, Nemoto EM, Watkins SC, Subbotin VM. An endothelin receptor antagonist TAK-044 ameliorates carbon tetrachloride-induced acute liver injury and portal hypertension in rats. Liver 1998;18:39-48.
25. Pinzani M, Milani S, DeFranco R, Grappone C, Caligiuri A, Gentilini A, et al. Endothelin 1 is overexpressed in human cirrhotic liver and exerts multiple effects on activated hepatic stellate cells. Gastroenterology 1996;110:534-548.
26. Bahcecioglu IH, Yalniz M, Ataseven H, Ilhan N, Ozercan IH, Seckin D, Sahin K. Levels of serum hyaluronic acid, TNF-alpha and IL-8 in patients with nonalcoholic steatohepatitis. Hepatogastroenterology 2005;52:1549-1553.
27. Suh YA, Post SM, Elizondo-Fraire AC, Maccio DR, Jackson JG, El-Naggar AK, et al. Multiple stress signals activate mutant p53 in vivo. Cancer Res 2011;71:7168-7175.
28. Terzian T, Suh YA, Iwakuma T, Post SM, Neumann M, Lang GA, et al. The inherent instability of mutant p53 is alleviated by Mdm2 or p16INK4a loss. Genes Dev 2008;22:1337-1344.
29. Melnikova VO, Santamaria AB, Bolshakov SV, Ananthaswamy HN. Mutant p53 is constitutively phosphorylated at Serine 15 in UV-induced mouse skin tumors: involvement of ERK1/2 MAP kinase. Oncogene 2003;22:5958-5966.
30. Day CP, James OF. Steatohepatitis: a tale of two "hits"? Gastroenterology 1998;114:842-845.
31. Tilg H, Moschen AR. Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 2010;52:1836-1846.
32. Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol 2010;5:145-171.
33. Li Z, Yang S, Lin H, Huang J, Watkins PA, Moser AB, et al. Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatology 2003;37:343-350.
34. Vermeulen L, Morrissey E, van der Heijden M, Nicholson AM, Sottoriva A, Buczacki S, et al. Defining stem cell dynamics in models of intestinal tumor initiation. Science 2013;342:995-998.
35. Suh YA, Post SM, Elizondo-Fraire AC, Maccio DR, Jackson JG, El-Naggar AK, et al. Multiple stress signals activate mutant p53 in vivo. Cancer Res 2011;71:7168-7175.
36. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997;387:296-299.