Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13

Blood

Volumn 116, Issue 25, 2010, Pages 5738-5747

  Highfill, Steven L ^a   Rodriguez, Paulo C ^b   Zhou, Qing ^a   Goetz, Christine A ^a   Koehn, Brent H ^a   Veenstra, Rachelle ^a   Taylor, Patricia A ^a   Panoskaltsis Mortari, Angela ^a   Serody, Jonathan S ^c   Munn, David H ^d   Tolar, Jakub ^a   Ochoa, Augusto C ^b   Blazar, Bruce R ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; ARGININE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 13; PEGYLATED RECOMBINANT ARGINASE 1; RECOMBINANT ENZYME; RECOMBINANT INTERLEUKIN 13; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL ACTIVATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; HUMAN; IN VIVO CULTURE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUPPRESSOR CELL; T LYMPHOCYTE; TREATMENT RESPONSE; UPREGULATION;

EID: 78650474985     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-06-287839     Document Type: Article

References (30)

1. Nagaraj S, Gabrilovich DI. Myeloid-derived suppressor cells. Adv Exp Med Biol. 2007;601:213-223.
2. Movahedi K, Guilliams M, Van den Bossche J, et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood. 2008;111(8):4233-4244.
3. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol. 2008;181(8):5791-5802.
4. Gallina G, Dolcetti L, Serafini P, et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest. 2006;116(10):2777-2790. (Pubitemid 44511641)
5. 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(2):1123-1131. (Pubitemid 43165981)
6. Bronte V, Zanovello P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol. 2005;5(8):641-654. (Pubitemid 41113195)
7. Rodriguez PC, Quiceno DG, Ochoa AC. L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood. 2007;109(4):1568-1573.
8. Rodriguez PC, Zea AH, Culotta KS, Zabaleta J, Ochoa JB, Ochoa AC. Regulation of T cell receptor CD3zeta chain expression by L-arginine. J Biol Chem. 2002;277(24):21123-21129. (Pubitemid 34952247)
9. Ghansah T, Paraiso KH, Highfill S, et al. Expansion of myeloid suppressor cells in SHIP-deficient mice represses allogeneic T cell responses. J Immunol. 2004;173(12):7324-7330. (Pubitemid 39628170)
10. Zhou Z, French DL, Ma G, et al. Development and function of myeloid-derived suppressor cells generated from mouse embryonic and hematopoietic stem cells. Stem Cells. 2010;28(3):620-632.
11. Munn DH, Sharma MD, Baban B, et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity. 2005;22(5):633-642. (Pubitemid 40719198)
12. Serody JS, Burkett SE, Panoskaltsis-Mortari A, et al. T-lymphocyte production of macrophage inflammatory protein-1alpha is critical to the recruitment of CD8(+) T cells to the liver, lung, and spleen during graft-versus-host disease. Blood. 2000;96(9):2973-2980.
13. Cheng PN, Lam TL, Lam WM, et al. Pegylated recombinant human arginase (rhArg-peg5,000mw) inhibits the in vitro and in vivo proliferation of human hepatocellular carcinoma through arginine depletion. Cancer Res. 2007;67(1):309-317.
14. Abe F, Dafferner AJ, Donkor M, et al. Myeloid-derived suppressor cells in mammary tumor progression in FVB Neu transgenic mice. Cancer Immunol Immunother. 2010;59(1):47-62.
15. Bronte V, Chappell DB, Apolloni E, et al. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation. J Immunol. 1999;162(10):5728-5737. (Pubitemid 29314923)
16. Shojaei F, Wu X, Qu X, et al. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc Natl Acad Sci U S A. 2009;106(16):6742-6747.
17. Taylor PA, Panoskaltsis-Mortari A, Swedin JM, et al. L-Selectin(hi) but not the L-selectin(lo) CD4+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood. 2004;104(12):3804-3812.
18. Highfill SL, Kelly RM, O'Shaughnessy MJ, et al. Multipotent adult progenitor cells can suppress graft-versus-host disease via prostaglandin E2 synthesis and only if localized to sites of allopriming. Blood. 2009;114(3):693-701.
19. Munder M, Eichmann K, Modolell M. Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J Immunol. 1998;160(11):5347-5354. (Pubitemid 28267823)
20. Munn DH, Mellor AL. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest. 2007;117(5):1147-1154.
21. Xia Y, Roman LJ, Masters BS, Zweier JL. Inducible nitric-oxide synthase generates superoxide from the reductase domain. J Biol Chem. 1998;273(35):22635-22639. (Pubitemid 28399833)
22. Squadrito GL, Pryor WA. The formation of peroxynitrite in vivo from nitric oxide and superoxide. Chem Biol Interact. 1995;96(2):203-206.
23. Groves JT. Peroxynitrite: reactive, invasive and enigmatic. Curr Opin Chem Biol. 1999;3(2):226-235.
24. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol. 2004;172(2):989-999. (Pubitemid 38113758)
25. Rodriguez PC, Quiceno DG, Zabaleta J, et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res. 2004;64(16):5839-5849. (Pubitemid 39095585)
26. Zea AH, Rodriguez PC, Atkins MB, et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 2005;65(8):3044-3048.
27. Rodriguez PC, Zea AH, DeSalvo J, et al. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol. 2003;171(3):1232-1239. (Pubitemid 36900052)
28. Freeman GJ, Long AJ, Iwai Y, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med. 2000;192(7):1027-1034.
29. Ash DE. Structure and function of arginases. J Nutr. 2004;134(10)[suppl]: 2760S-2764S; discussion 2765S-2767S.
30. Hernandez CP, Morrow K, Lopez-Barcons LA, et al. Pegylated arginase I: a potential therapeutic approach in T-ALL. Blood. 2010;115(25):5214-5221.