The liver is a site for tumor-induced myeloid-derived suppressor cell accumulation and immunosuppression

Cancer Research

Volumn 69, Issue 13, 2009, Pages 5514-5521

  Ilkovitch, Dan ^a   Lopez, Diana M ^a,b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MIAMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; PD L1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CELL INTERACTION; CONTROLLED STUDY; HEMATOPOIESIS; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; KUPFFER CELL; LIVER; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; SUPPRESSOR CELL; T LYMPHOCYTE; UPREGULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; HEMATOPOIESIS; IMMUNOSUPPRESSION; KUPFFER CELLS; LIVER; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASMS; T-LYMPHOCYTES;

EID: 67650422616     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-4625     Document Type: Article

References (44)

1. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol 2004;22:329-60.
2. Fu YX, Watson G, Jimenez JJ, Wang Y, Lopez DM. Expansion of immunoregulatory macrophages by granulocyte-macrophage colony-stimulating factor derived from a murine mammary tumor. Cancer Res 1990;50:227-34.
3. Watson GA, Fu YX, Lopez DM. Splenic macrophages from tumor-bearing mice co-expressing MAC-1 and MAC-2 antigens exert immunoregulatory functions via two distinct mechanisms. J Leukoc Biol 1991;49:126-38.
4. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
5. Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol 2006;16:53-65.
6. Ochoa AC, Zea AH, Hernandez C, Rodriguez PC. Arginase, prostaglandins, andmyeloid-derived suppressor cells in renal cell carcinoma. Clin Cancer Res 2007;13:721-6s.
7. Haile LA, von Wasielewski R, Gamrekelashvili J, et al. Myeloid-derived suppressor cells in inflammatory bowel disease: a new immunoregulatory pathway. Gastroenterology 2008;135:871-81, 81 e1-5.
8. Makarenkova VP, Bansal V, Matta BM, Perez LA, Ochoa JB. CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J Immunol 2006;176:2085-94.
9. Noel JG, Osterburg A, Wang Q, et al. Thermal injury elevates the inflammatory monocyte subpopulation in multiple compartments. Shock 2007;28:684-93.
10. Delano MJ, Scumpia PO, Weinstein JS, et al. MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J Exp Med 2007;204:1463-74.
11. Dugast AS, Haudebourg T, Coulon F, et al. Myeloid-derived suppressor cells accumulate in kidney allograft tolerance and specifically suppress effector T cell expansion. J Immunol 2008;180:7898-906.
12. Ilkovitch D, Lopez DM. Immune modulation by melanoma-derived factors. Exp Dermatol 2008;17:977-85.
13. Liu C, Yu S, Kappes J, et al. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood 2007;109:4336-42.
14. Sinha P, Clements VK, Bunt SK, Albelda SM, Ostrand-Rosenberg S. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 2007;179:977-83.
15. Huang B, Pan PY, Li Q, et al. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 2006;66:1123-31.
16. Saio M, Radoja S, Marino M, Frey AB. Tumor-infiltrating macrophages induce apoptosis in activated CD8(+) T cells by a mechanism requiring cell contact and mediated by both the cell-associated form of TNF and nitric oxide. J Immunol 2001;167:5583-93.
17. Kalchenko V, Shivtiel S, Malina V, et al. Use of lipophilic near-infrared dye in whole-body optical imaging of hematopoietic cell homing. J Biomed Opt 2006;11:050507-1-050507-3.
18. Fu YX, Watson GA, Kasahara M, Lopez DM. The role of tumor-derived cytokines on the immune system of mice bearing a mammary adenocarcinoma. I. Induction of regulatory macrophages in normal mice by the in vivo administration of rGM-CSF. J Immunol 1991;146:783-9.
19. Melani C, Chiodoni C, Forni G, Colombo MP. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood 2003;102:2138-45.
20. Callery MP, Kamei T, Flye MW. Kupffer cell blockade inhibits induction of tolerance by the portal venous route. Transplantation 1989;47:1092-4.
21. Kryczek I, Zou L, Rodriguez P, et al. B7-4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 2006;203:871-81.
22. Maier H, Isogawa M, Freeman GJ, Chisari FV. PD-1:PD-L1 interactions contribute to the functional suppression of virus-specific CD8+ T lymphocytes in the liver. J Immunol 2007;178:2714-20.
23. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008;26:677-704.
24. Li B, VanRoey M, Wang C, et al. Anti-programmed death-1 synergizes with granulocyte macrophage colony-stimulating factor-secreting tumor cell immunotherapy providing therapeutic benefit to mice with established tumors. Clin Cancer Res 2009;15:1623-34.
25. Wei S, Shreiner AB, Takeshita N, et al. Tumor-induced immune suppression of in vivo effector T-cell priming is mediated by the B7-1/PD-1 axis and transforming growth factor h. Cancer Res 2008;68:5432-8.
26. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008;181:5791-802.
27. Filipazzi P, Valenti R, Huber V, et al. Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J Clin Oncol 2007;25:2546-53.
28. Diaz-Montero CM, Salem ML, Nishimura MI, et al. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 2009;58:49-59.
29. Almand B, Clark JI, Nikitina E, et al. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 2001;166:678-89.
30. Kusmartsev S, Su Z, Heiser A, et al. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin Cancer Res 2008;14:8270-8.
31. 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.
32. Rodriguez PC, Hernandez CP, Quiceno D, et al. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med 2005;202:931-9.
33. Bronte V, Apolloni E, Cabrelle A, et al. Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood 2000;96:3838-46.
34. Ilkovitch D, Lopez DM. Urokinase-mediated recruitment of myeloid-derived suppressor cells and their suppressive mechanisms are blocked by MUC1/sec. Blood 2009;113:4729-39.
35. Pan PY, Wang GX, Yin B, et al. Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood 2008;111:219-28.
36. DuPre SA, Redelman D, Hunter KW, Jr. The mouse mammary carcinoma 4T1: characterization of the cellular landscape of primary tumours and metastatic tumour foci. Int J Exp Pathol 2007;88:351-60.
37. Tao K, Fang M, Alroy J, Sahagian GG. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 2008;8:228.
38. Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-h1. J Immunol 2009;182:240-9.
39. Dinapoli MR, Calderon CL, Lopez DM. The altered tumoricidal capacity of macrophages isolated from tumor-bearing mice is related to reduce expression of the inducible nitric oxide synthase gene. J Exp Med 1996;183:1323-9.
40. Watson GA, Lopez DM. Aberrant antigen presentation by macrophages from tumor-bearing mice is involved in the down-regulation of their T cell responses. J Immunol 1995;155:3124-34.
41. Sotomayor EM, Fu YX, Lopez-Cepero M, et al. Role of tumor-derived cytokines on the immune system of mice bearing a mammary adenocarcinoma. II. Downregulation of macrophage-mediated cytotoxicity by tumor-derived granulocyte-macrophage colony-stimulating factor. J Immunol 1991;147:2816-23.
42. Iwai Y, Terawaki S, Ikegawa M, Okazaki T, Honjo T. PD-1 inhibits antiviral immunity at the effector phase in the liver. J Exp Med 2003;198:39-50.
43. Wahl C, Bochtler P, Chen L, Schirmbeck R, Reimann J. B7-1 on hepatocytes facilitates priming of specific CD8 T cells but limits the specific recall of primed responses. Gastroenterology 2008;135:980-8.
44. Liu Y, Zeng B, Zhang Z, Zhang Y, Yang R. B7-1 on myeloid-derived suppressor cells in immune suppression by a mouse model of ovarian cancer. Clin Immunol 2008;129:471-81.