Regulation of accumulation and function of myeloid derived suppressor cells in different murine models of hepatocellular carcinoma

Journal of Hepatology

Volumn 59, Issue 5, 2013, Pages 1007-1013

  Kapanadze, Tamar ^a,b   Gamrekelashvili, Jaba ^a,b   Ma, Chi ^a   Chan, Carmen ^a   Zhao, Fei ^a   Hewitt, Stephen ^a   Zender, Lars ^c   Kapoor, Veena ^d   Felsher, Dean W ^e   Manns, Michael P ^b   Korangy, Firouzeh ^a   Greten, Tim F ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer vaccine; Immunotherapy; Tumor immunology

Indexed keywords

CALGRANULIN A; CALGRANULIN B; DIETHYLNITROSAMINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; MONOCYTE CHEMOTACTIC PROTEIN 1; SORAFENIB; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CANCER GRAFT; CELL MIGRATION; COMPARATIVE STUDY; CONTROLLED STUDY; GENE; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MODEL; MOUSE; MURINE MODEL; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SUPPRESSOR CELL;

BLR; BODY WEIGHT/LIVER WEIGHT RATIO; CANCER VACCINE; DEN; DIETHYLNITROSOAMINE; G-CSF; GM-CSF; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE-MACROPHAGE COLONY STIMULATING FACTOR; HCC; HEPATOCELLULAR CARCINOMA; IL; IMMUNOTHERAPY; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; INTERLEUKIN; KC; KERATINOCYTE-DERIVED CHEMOKINE; L-NMMA; LAP; LIVER ACTIVATOR PROTEIN; MACROPHAGE CHEMOTACTIC PROTEIN; MCP; MDSC; MYELOID DERIVED SUPPRESSOR CELL; N(G)-METHYL-L-ARGININE; N(Ω)-HYDROXIL-NOR-L-ARGININE; N-NOHA; NATURAL KILLER; NK; OVA; OVALBUMIN; TUMOR IMMUNOLOGY; VASCULAR ENDOTHELIAL GROWTH FACTOR; VEGF; WILD TYPE; WT;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL MOVEMENT; CELL PROLIFERATION; DIETHYLNITROSAMINE; DISEASE MODELS, ANIMAL; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HETEROGRAFTS; HUMANS; LIVER NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID CELLS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTO-ONCOGENE PROTEINS C-MYC;

EID: 84885954039     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2013.06.010     Document Type: Article

References (41)

1. D.I. Gabrilovich, and S. Nagaraj Myeloid-derived suppressor cells as regulators of the immune system Nat Rev Immunol 9 2009 162 174
2. K. Movahedi, M. Guilliams, J. Van den Bossche, R. Van den Bergh, C. Gysemans, and A. Beschin Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity Blood 111 2008 4233 4244
3. J.I. Youn, S. Nagaraj, M. Collazo, and D.I. Gabrilovich Subsets of myeloid-derived suppressor cells in tumor-bearing mice J Immunol 181 2008 5791 5802
4. L.A. Haile, J. Gamrekelashvili, M.P. Manns, F. Korangy, and T.F. Greten CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice J Immunol 185 2010 203 210
5. D.I. Gabrilovich, V. Bronte, S.H. Chen, M.P. Colombo, A. Ochoa, and S. Ostrand-Rosenberg The terminology issue for myeloid-derived suppressor cells Cancer Res 67 2007 425 [author reply 426]
6. D. Ilkovitch, and D.M. Lopez The liver is a site for tumor-induced myeloid-derived suppressor cell accumulation and immunosuppression Cancer Res 69 2009 5514 5521
7. M.K. Connolly, J. Mallen-St Clair, A.S. Bedrosian, A. Malhotra, V. Vera, and J. Ibrahim Distinct populations of metastases-enabling myeloid cells expand in the liver of mice harboring invasive and preinvasive intra-abdominal tumor J Leukoc Biol 87 2010 713 725
8. D.I. Gabrilovich, M.P. Velders, E.M. Sotomayor, and W.M. Kast Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells J Immunol 166 2001 5398 5406
9. V. Bronte, D.B. Chappell, E. Apolloni, A. Cabrelle, M. Wang, and P. Hwu Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation J Immunol 162 1999 5728 5737
10. S. Kusmartsev, Y. Nefedova, D. Yoder, and D.I. Gabrilovich Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species J Immunol 172 2004 989 999
11. S. Nagaraj, and D.I. Gabrilovich Regulation of suppressive function of myeloid-derived suppressor cells by CD4(+) T cells Semin Cancer Biol 22 2012 282 288
12. B. Hoechst, T. Voigtlaender, L. Ormandy, J. Gamrekelashvili, F. Zhao, and H. Wedemeyer Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor Hepatology 50 2009 799 807
13. H. Li, Y. Han, Q. Guo, M. Zhang, and X. Cao Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1 J Immunol 182 2009 240 249
14. T.F. Greten, M.P. Manns, and F. Korangy Myeloid derived suppressor cells in human diseases Int Immunopharmacol 11 2011 802 807
15. B. Hoechst, L.A. Ormandy, M. Ballmaier, F. Lehner, C. Kruger, and M.P. Manns A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells Gastroenterology 135 2008 234 243
16. C.M. Shachaf, A.M. Kopelman, C. Arvanitis, A. Karlsson, S. Beer, and S. Mandl MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer Nature 431 2004 1112 1117
17. S.D. Vesselinovitch, and N. Mihailovich Kinetics of diethylnitrosamine hepatocarcinogenesis in the infant mouse Cancer Res 43 1983 4253 4259
18. L. Zender, W. Xue, C. Cordon-Cardo, G.J. Hannon, R. Lucito, and S. Powers Generation and analysis of genetically defined liver carcinomas derived from bipotential liver progenitors Cold Spring Harb Symp Quant Biol 70 2005 251 261
19. Z. Cao, H. Fan-Minogue, D.I. Bellovin, A. Yevtodiyenko, J. Arzeno, and Q. Yang MYC phosphorylation, activation, and tumorigenic potential in hepatocellular carcinoma are regulated by HMG-CoA reductase Cancer Res 71 2011 2286 2297
20. A. Kistner, M. Gossen, F. Zimmermann, J. Jerecic, C. Ullmer, and H. Lubbert Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice Proc Natl Acad Sci U S A 93 1996 10933 10938
21. C. Ma, T. Kapanadze, J. Gamrekelashvili, M.P. Manns, F. Korangy, and T.F. Greten Anti-Gr-1 antibody depletion fails to eliminate hepatic myeloid-derived suppressor cells in tumor-bearing mice J Leukoc Biol 92 2012 1199 1206
22. J.D. Waight, Q. Hu, A. Miller, S. Liu, and S.I. Abrams Tumor-derived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism PLoS One 6 2011 e27690
23. P. Sinha, C. Okoro, D. Foell, H.H. Freeze, S. Ostrand-Rosenberg, and G. Srikrishna Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells J Immunol 181 2008 4666 4675
24. P. Serafini, R. Carbley, K.A. Noonan, G. Tan, V. Bronte, and I. Borrello High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells Cancer Res 64 2004 6337 6343
25. L. Cheng, J. Wang, X. Li, Q. Xing, P. Du, and L. Su Interleukin-6 induces Gr-1+CD11b+ myeloid cells to suppress CD8+ T cell-mediated liver injury in mice PLoS One 6 2011 e17631
26. S.K. Bunt, P. Sinha, V.K. Clements, J. Leips, and S. Ostrand-Rosenberg Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression J Immunol 176 2006 284 290
27. F. Abe, A.J. Dafferner, M. Donkor, S.N. Westphal, E.M. Scholar, and J.C. Solheim Myeloid-derived suppressor cells in mammary tumor progression in FVB Neu transgenic mice Cancer Immunol Immunother 59 2010 47 62
28. Y. Sawanobori, S. Ueha, M. Kurachi, T. Shimaoka, J.E. Talmadge, and J. Abe Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice Blood 111 2008 5457 5466
29. M. Cao, Y. Xu, J.I. Youn, R. Cabrera, X. Zhang, and D. Gabrilovich Kinase inhibitor Sorafenib modulates immunosuppressive cell populations in a murine liver cancer model Lab Invest 91 2011 598 608
30. S. Ostrand-Rosenberg, P. Sinha, D.W. Beury, and V.K. Clements Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression Semin Cancer Biol 22 2012 275 281
31. E. Ribechini, V. Greifenberg, S. Sandwick, and M.B. Lutz Subsets, expansion and activation of myeloid-derived suppressor cells Med Microbiol Immunol 199 2010 273 281
32. F. Heindryckx, I. Colle, and H. Van Vlierberghe Experimental mouse models for hepatocellular carcinoma research Int J Exp Pathol 90 2009 367 386
33. P.A. Farazi, and R.A. DePinho Hepatocellular carcinoma pathogenesis: from genes to environment Nat Rev Cancer 6 2006 674 687
34. C. Schneider, A. Teufel, T. Yevsa, F. Staib, A. Hohmeyer, and G. Walenda Adaptive immunity suppresses formation and progression of diethylnitrosamine- induced liver cancer Gut 61 2012 1733 1743
35. C.M. Diaz-Montero, M.L. Salem, M.I. Nishimura, E. Garrett-Mayer, D.J. Cole, and A.J. Montero Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy Cancer Immunol Immunother 58 2009 49 59
36. R.F. Gabitass, N.E. Annels, D.D. Stocken, H.A. Pandha, and G.W. Middleton Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the Th2 cytokine interleukin-13 Cancer Immunol Immunother 60 2011 1419 1430
37. L.J. Bayne, G.L. Beatty, N. Jhala, C.E. Clark, A.D. Rhim, and B.Z. Stanger Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer Cancer Cell 21 2012 822 835
38. L. Dolcetti, E. Peranzoni, S. Ugel, I. Marigo, A. Fernandez Gomez, and C. Mesa Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF Eur J Immunol 40 2010 22 35
39. D. Gabrilovich, T. Ishida, T. Oyama, S. Ran, V. Kravtsov, and S. Nadaf Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo Blood 92 1998 4150 4166
40. F. Capone, S. Costantini, E. Guerriero, R. Calemma, M. Napolitano, and S. Scala Serum cytokine levels in patients with hepatocellular carcinoma Eur Cytokine Netw 21 2010 99 104
41. C.A. Corzo, T. Condamine, L. Lu, M.J. Cotter, J.I. Youn, and P. Cheng HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment J Exp Med 207 2010 2439 2453