Adaptive immunity suppresses formation and progression of diethylnitrosamine-induced liver cancer

Gut

Volumn 61, Issue 12, 2012, Pages 1733-1743

  Schneider, Carlo ^a   Teufel, Andreas ^b   Yevsa, Tetyana ^c,d   Staib, Frank ^b   Hohmeyer, Anja ^c,d   Walenda, Gudrun ^a   Zimmermann, Henning W ^a   Vucur, Mihael ^a   Huss, Sebastian ^e   Gassler, Nikolaus ^a   Wasmuth, Hermann E ^a   Lira, Sergio A ^f   Zender, Lars ^c,d   Luedde, Tom ^a   Trautwein, Christian ^a   Tacke, Frank ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e UNIVERSITY OF BONN   (Germany)

^f MOUNT SINAI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE SCAVENGING RECEPTOR D6; CXCL9 CHEMOKINE; DIETHYLNITROSAMINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CANCER GROWTH; CANCER PATIENT; CANCER PROGNOSIS; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL INFILTRATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENZYME REGULATION; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LEUKOCYTE; LIVER CELL CARCINOMA; LUNG CARCINOGENESIS; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ADAPTIVE IMMUNITY; ANIMALS; B-LYMPHOCYTES; BIOLOGICAL MARKERS; CARCINOGENS; CARCINOMA, HEPATOCELLULAR; CHEMOKINE CCL2; CHEMOKINE CCL5; CHEMOKINE CXCL9; DIETHYLNITROSAMINE; DISEASE PROGRESSION; HUMANS; LEUKOCYTES; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRECANCEROUS CONDITIONS; SURVIVAL ANALYSIS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84868706854     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2011-301116     Document Type: Article

References (54)

1. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007;132:2557-76. (Pubitemid 46890874)
2. Luedde T, Schwabe RF. NF-kappaB in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol 2011;8:108-18.
3. Maeda S, Kamata H, Luo JL, et al. IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 2005;121:977-90. (Pubitemid 40884391)
4. Pikarsky E, Porat RM, Stein I, et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004;431:461-6. (Pubitemid 39329586)
5. Vesely MD, Kershaw MH, Schreiber RD, et al. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011;29:235-71.
6. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006;6:24-37. (Pubitemid 43053650)
7. Korangy F, Hochst B, Manns MP, et al. Immune responses in hepatocellular carcinoma. Dig Dis 2010;28:150-4.
8. Newell P, Villanueva A, Friedman SL, et al. Experimental models of hepatocellular carcinoma. J Hepatol 2008;48:858-79.
9. Goldfarb S, Pugh TD, Koen H, et al. Preneoplastic and neoplastic progression during hepatocarcinogenesis in mice injected with diethylnitrosamine in infancy. Environ Health Perspect 1983;50:149-61. (Pubitemid 13040437)
10. Vucur M, Roderburg C, Bettermann K, et al. Mouse models of hepatocarcinogenesis: what can we learn for the prevention of human hepatocellular carcinoma? Oncotarget 2010;1:373-8.
11. Jamieson T, Cook DN, Nibbs RJ, et al. The chemokine receptor D6 limits the inflammatory response in vivo. Nat Immunol 2005;6:403-11. (Pubitemid 41716781)
12. Tacke F, Ginhoux F, Jakubzick C, et al. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J Exp Med 2006;203:583-97.
13. Bettermann K, Vucur M, Haybaeck J, et al. TAK1 suppresses a NEMO-dependent but NF-kappaB-independent pathway to liver cancer. Cancer Cell 2010;17:481-96.
14. Karlmark KR, Weiskirchen R, Zimmermann HW, et al. Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 2009;50:261-74.
15. Karlmark KR, Zimmermann HW, Roderburg C, et al. The fractalkine receptor CX3CR1 protects against liver fibrosis by controlling differentiation and survival of infiltrating hepatic monocytes. Hepatology 2010;52:1769-82.
16. Heymann F, Trautwein C, Tacke F. Monocytes and macrophages as cellular targets in liver fibrosis. Inflamm Allergy Drug Targets 2009;8:307-18.
17. Zimmermann HW, Seidler S, Nattermann J, et al. Functional contribution of elevated circulating and hepatic non-classical CD14CD16 monocytes to inflammation and human liver fibrosis. PLoS One 2010;5:e11049.
18. Baeck C, Wehr A, Karlmark KR, et al. Pharmacological inhibition of the chemokine CCL2 (MCP-1) diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury. Gut 2012. In press.
19. Kang TW, Yevsa T, Woller N, et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 2011;479:547-51.
20. Lee JS, Chu IS, Heo J, et al. Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. Hepatology 2004;40:667-76. (Pubitemid 39265589)
21. Lee JS, Heo J, Libbrecht L, et al. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 2006;12:410-16.
22. Shimokawa K, Mogushi K, Shoji S, et al. iCOD: an integrated clinical omics database based on the systems-pathology view of disease. BMC Genomics 2010;11(Suppl 4):S19.
23. Sander LE, Sackett SD, Dierssen U, et al. Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J Exp Med 2010;207:1453-64.
24. Hoechst B, Ormandy LA, Ballmaier M, et al. A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 2008;135:234-43. (Pubitemid 351899008)
25. Wasmuth HE, Tacke F, Trautwein C. Chemokines in liver inflammation and fibrosis. Semin Liver Dis 2010;30:215-25.
26. Shirabe K, Motomura T, Muto J, et al. Tumor-infiltrating lymphocytes and hepatocellular carcinoma: pathology and clinical management. Int J Clin Oncol 2010;15:552-8.
27. Chew V, Tow C, Teo M, et al. Inflammatory tumour microenvironment is associated with superior survival in hepatocellular carcinoma patients. J Hepatol 2010;52:370-9.
28. Heymann F, Hammerich L, Storch D, et al. Hepatic macrophage migration and differentiation critical for liver fibrosis is mediated by the chemokine receptor C-C motif chemokine receptor 8 in mice. Hepatology 2012. In press.
29. Mombaerts P, Iacomini J, Johnson RS, et al. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992;68:869-77.
30. Liu X, Zhan Z, Li D, et al. Intracellular MHC class II molecules promote TLR-triggered innate immune responses by maintaining activation of the kinase Btk. Nat Immunol 2011;12:416-24.
31. Fu C, Turck CW, Kurosaki T, et al. BLNK: a central linker protein in B cell activation. Immunity 1998;9:93-103. (Pubitemid 28361298)
32. van Spriel AB. Tetraspanins in the humoral immune response. Biochem Soc Trans 2011;39:512-17.
33. Mantovani A. B cells and macrophages in cancer: yin and yang. Nat Med 2011;17:285-6.
34. Koebel CM, Vermi W, Swann JB, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007;450:903-7. (Pubitemid 350231320)
35. Luedde T, Beraza N, Kotsikoris V, et al. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 2007;11:119-32. (Pubitemid 46209851)
36. Haybaeck J, Zeller N, Wolf MJ, et al. A lymphotoxin-driven pathway to hepatocellular carcinoma. Cancer Cell 2009;16:295-308.
37. Mauad TH, van Nieuwkerk CM, Dingemans KP, et al. Mice with homozygous disruption of the mdr2 P-glycoprotein gene. A novel animal model for studies of nonsuppurative inflammatory cholangitis and hepatocarcinogenesis. Am J Pathol 1994;145:1237-45.
38. Lee JS, Chu IS, Mikaelyan A, et al. Application of comparative functional genomics to identify best-fit mouse models to study human cancer. Nat Genet 2004;36:1306-11. (Pubitemid 39577940)
39. Roderfeld M, Rath T, Lammert F, et al. Innovative immunohistochemistry identifies MMP-9 expressing macrophages at the invasive front of murine HCC. World J Hepatol 2010;2:175-9.
40. Biswas SK, Sica A, Lewis CE. Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms. J Immunol 2008;180:2011-17.
41. Gao Q, Qiu SJ, Fan J, et al. Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 2007;25:2586-93. (Pubitemid 47041232)
42. Hoechst B, Voigtlaender T, Ormandy L, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009;50:799-807.
43. Nibbs RJ, Gilchrist DS, King V, et al. The atypical chemokine receptor D6 suppresses the development of chemically induced skin tumors. J Clin Invest 2007;117:1884-92. (Pubitemid 47036322)
44. Xue W, Zender L, Miething C, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007;445:656-60. (Pubitemid 46232886)
45. Ammirante M, Luo JL, Grivennikov S, et al. B cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010;464:302-5.
46. Andreu P, Johansson M, Affara NI, et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010;17:121-34.
47. Wilson NS, Yang B, Yang A, et al. An Fcgamma receptor-dependent mechanism drives antibody-mediated target-receptor signaling in cancer cells. Cancer Cell 2011;19:101-13.
48. Hoshida Y, Villanueva A, Kobayashi M, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med 2008;359:1995-2004.
49. Taniguchi CM, Winnay J, Kondo T, et al. The phosphoinositide 3-kinase regulatory subunit p85alpha can exert tumor suppressor properties through negative regulation of growth factor signaling. Cancer Res 2010;70:5305-15.
50. Fruman DA, Snapper SB, Yballe CM, et al. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85alpha. Science 1999;283:393-7.
51. Ruland J, Duncan GS, Wakeham A, et al. Differential requirement for Malt1 in T and B cell antigen receptor signaling. Immunity 2003;19:749-58. (Pubitemid 37490799)
52. Hikida M, Casola S, Takahashi N, et al. PLC-gamma2 is essential for formation and maintenance of memory B cells. J Exp Med 2009;206:681-9.
53. Caraux A, Kim N, Bell SE, et al. Phospholipase C-gamma2 is essential for NK cell cytotoxicity and innate immunity to malignant and virally infected cells. Blood 2006;107:994-1002. (Pubitemid 43156297)
54. Chew V, Chen J, Lee D, et al. Chemokine-driven lymphocyte infiltration: an early intratumoural event determining long-term survival in resectable hepatocellular carcinoma. Gut 2012. In press.