Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained

Cancer Research

Volumn 70, Issue 9, 2010, Pages 3526-3536

  Ko, Jennifer S ^a   Rayman, Patricia ^a   Ireland, Joanna ^a   Swaidani, Shadi ^a   Li, Geqiang ^a   Bunting, Kevin D ^a   Rini, Brian ^a   Finke, James H ^a   Cohen, Peter A ^b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; STAT3 PROTEIN; STAT5A PROTEIN; STAT5B PROTEIN; SUNITINIB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CHEMOTHERAPY; CELL DIFFERENTIATION; DRUG ACTIVITY; DRUG EFFECT; DRUG POTENCY; DRUG SENSITIVITY; FEMALE; GROWTH INHIBITION; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CARCINOMA; LYMPHOCYTE FUNCTION; MICROENVIRONMENT; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; SPLEEN CELL; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; TUMOR GROWTH; TUMOR RESISTANCE;

ANIMALS; ANTIGENS, CD11B; CARCINOMA, RENAL CELL; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HUMANS; IMMUNOLOGIC FACTORS; INDOLES; KIDNEY NEOPLASMS; MICE; MICE, INBRED BALB C; MYELOID CELLS; PYRROLES; SUPPRESSOR FACTORS, IMMUNOLOGIC; T-LYMPHOCYTE SUBSETS;

EID: 77951754469     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-3278     Document Type: Article

References (47)

1. Motzer RJ, Rini BI, Bukowski RM, et al. Sunitinib in patients with metastatic renal cell carcinoma. JAMA 2006;295:2516-2524
2. Rini BI. Sunitinib. Expert Opin Pharmacother 2007;8:2359-2369
3. Roskoski R, Jr. Sunitinib: a VEGF and PDGF receptor protein kinase and angiogenesis inhibitor. Biochem Biophys Res Commun 2007; 356:323-328
4. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008;8:592-603.
5. Ebos JM, Lee CR, Cruz-Munoz W, et al. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-239
6. Paez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15:220-231
7. Shojaei F, Wu X, Malik AK, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol 2007;25:911-920
8. 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;106:6742-6747
9. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008; 8:618-631
10. Yang L, DeBusk LM, Fukuda K, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004;6:409-421
11. Yang L, Huang J, Ren X, et al. Abrogation of TGF β signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 2008;13:23-35.
12. Kujawski M, Kortylewski M, Lee H, et al. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J Clin Invest 2008;118: 3367-3377
13. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009;182:4499-4506
14. Rodriguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol Rev 2008;222:180-191
15. 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;179:977-983
16. Ko JS, Zea AH, Rini BI, et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res 2009;15:2148-2157
17. 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;135:234-243
18. Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res 2001;61:4756-4760
19. 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;65:3044-3048
20. 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;166:678-689
21. 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;25:2546-2553
22. Rodriguez PC, Ernstoff MS, Hernandez C, et al. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res 2009;69:1553-1560
23. Mandruzzato S, Solito S, Falisi E, et al. IL4Rα+ myeloid-derived suppressor cell expansion in cancer patients. J Immunol 2009;182: 6562-6568
24. Xin H, Zhang C, Herrmann A, et al. Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res 2009;69:2506-2513
25. Cohen PA, Koski GK, Czerniecki BJ, et al. STAT3- and STAT5-dependent pathways competitively regulate the pan-differentiation of CD34pos cells into tumor-competent dendritic cells. Blood 2008;112:1832-1843
26. Li G, Miskimen KL, Wang Z, et al. STAT5 requires the N-domain for suppression of miR15/16, induction of bcl-2, and survival signaling in myeloproliferative disease. Blood 2010;115:1416-1424
27. Peng L, Kjaergaard J, Plautz GE, et al. Tumor-induced L-selectinhigh suppressor T cells mediate potent effector T cell blockade and cause failure of otherwise curative adoptive immunotherapy. J Immunol 2002;169:4811-4821
28. Alexander JP, Kudoh S, Melsop KA, et al. T-cells infiltrating renal cell carcinoma display a poor proliferative response even though they can produce interleukin 2 and express interleukin 2 receptors. Cancer Res 1993;53:1380-1387
29. Ebert T, Bander NH, Finstad CL, Ramsawak RD, Old LJ. Establishment and characterization of human renal cancer and normal kidney cell lines. Cancer Res 1990;50:5531-5536
30. 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: 4233-4244
31. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791-5802
32. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-174
33. Faivre S, Delbaldo C, Vera K, et al. Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer. J Clin Oncol 2006;24:25-35.
34. Mendel DB, Laird AD, Xin X, et al. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 2003;9:327-337
35. Ozao-Choy J, Ma G, Kao J, et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res 2009;69:2514-2522
36. Steimer DA, Boyd K, Takeuchi O, et al. Selective roles for anti-apoptotic MCL-1 during granulocyte development and macrophage effector function. Blood 2009;113:2805-2815
37. Ebos JM, Lee CR, Christensen JG, Mutsaers AJ, Kerbel RS. Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc Natl Acad Sci U S A 2007;104:17069-17074
38. 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;111:219-228
39. Serafini P, Carbley R, Noonan KA, et al. High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells. Cancer Res 2004;64:6337-6343
40. Marigo I, Dolcetti L, Serafini P, Zanovello P, Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 2008;222:162-179
41. Cheng P, Corzo CA, Luetteke N, et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med 2008; 205:2235-2249
42. Corzo CA, Cotter MJ, Cheng P, et al. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 2009;182:5693-5701
43. Panopoulos AD, Zhang L, Snow JW, et al. STAT3 governs distinct pathways in emergency granulopoiesis and mature neutrophils. Blood 2006;108:3682-3690
44. Tatsumi T, Kierstead LS, Ranieri E, et al. Disease-associated bias in T helper type 1 (Th1)/Th2 CD4(+) T cell responses against MAGE-6 in HLA-DRB10401(+) patients with renal cell carcinoma or melanoma. J Exp Med 2002;196:619-628
45. Finn OJ. Cancer immunology. N Engl J Med 2008;358:2704-2715
46. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007; 25:267-296
47. Finke JH, Rini B, Ireland J, et al. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin Cancer Res 2008;14:6674-6682