Aberrant PGE2 metabolism in bladder tumor microenvironment promotes immunosuppressive phenotype of tumor-infiltrating myeloid cells

International Immunopharmacology

Volumn 11, Issue 7, 2011, Pages 848-855

  Eruslanov, Evgeniy ^a   Daurkin, Irina ^a   Vieweg, Johannes ^a   Daaka, Yehia ^a,b   Kusmartsev, Sergei ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Bladder cancer; Myeloid derived suppressor cells; Tumor microenvironment; Tumor associated macrophages; Tumor infiltrating myeloid cells

Indexed keywords

CD11B ANTIGEN; CHEMOKINE RECEPTOR CXCR4; PROSTAGLANDIN E2; CXCR4 PROTEIN, HUMAN;

ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; BLADDER TUMOR; BONE MARROW CELL; BONE MARROW CULTURE; CONTROLLED STUDY; HUMAN; IMMUNE DEFICIENCY; IMMUNOPHENOTYPING; INFLAMMATION; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN METABOLISM; PROSTAGLANDIN RELEASE; RECEPTOR UPREGULATION; SUPPRESSOR CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; ANIMAL; BIOSYNTHESIS; CARCINOMA; CELL DIFFERENTIATION; CELL MOTION; GENETICS; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR ESCAPE; XENOGRAFT;

ANIMALS; ANTIGENS, CD11B; CARCINOMA; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; DINOPROSTONE; HUMANS; IMMUNOSUPPRESSION; MICE; MICE, NUDE; MYELOID CELLS; RECEPTORS, CXCR4; TRANSPLANTATION, HETEROLOGOUS; TUMOR ESCAPE; TUMOR MICROENVIRONMENT; URINARY BLADDER NEOPLASMS;

EID: 80054109394     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2011.01.033     Document Type: Article

References (48)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin 2007;57:30-42.
2. Wang D, Dubois R. Eicosanoids and cancer. Nat Rev Cancer 2010;10:181-93.
3. Wu X-R. Urothelial tumorigenesis: a tale of divergent pathways. Nat Rev Cancer 2005;5:713-25. (Pubitemid 41486364)
4. Wang D, Dubois RN. Prostaglandins and cancer. Gut 2006;55:115-22. (Pubitemid 41820645)
5. Stolina M, Sharma S, Lin Y, Dohadwala M, Gardner B, Luo J, et al. Specific inhibition of cyclooxygenase 2 restores antitumor reactivity by altering the balance of IL-10 and IL-12 synthesis. J Immunol 2000;164:361-70. (Pubitemid 30013010)
6. Sombroek CC, Stam AGM, Masterson AJ, Lougheed SM, Schakel MJAG, Meijer CJLM, et al. Prostanoids play a major role in the primary tumor-induced inhibition of dendritic cell differentiation. J Immunol 2002;168:4333-43. (Pubitemid 34441333)
7. Rodriguez PC, Hernandez CP, Quiceno D David, Dubinett SM, Zabaleta J, Ochoa JB, et al. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med 2005;202:931-9. (Pubitemid 41396893)
8. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 2007;67:4507-13. (Pubitemid 46815102)
9. Eruslanov E, Kaliberov S, Daurkin I, Kaliberova L, Buchsbaum D, Vieweg J, et al. Altered expression of 15-hydroxyprostaglandin dehydrogenase in tumor-infiltrated CD11b myeloid cells: a mechanism for immune evasion in cancer. J Immunol 2009;182:7548-57.
10. Daurkin I, Eruslanov E, Vieweg J, Kusmartsev S. Generation of antigen-presenting cells from tumor-infiltrated CD11b myeloid cells with DNA demethylating agent 5-aza-2′-deoxycytidine. Cancer Immunol Immunother 2010;59:697-706.
11. Takayama K, García-Cardena G, Sukhova G, Comander J, Gimbrone M, Libby JP. Prostaglandin E2 suppresses chemokine production in human macrophages through the EP4 receptor. J Biol Chem 2002;277:44147-54. (Pubitemid 36157844)
12. Yao C, Sakata D, Esaki Y, Li Y, Matsuoka T, Kuroiwa K, et al. Prostaglandin E2-EP4 signaling promotes immune inflammation through Th1 cell differentiation and Th17 cell expansion. Nat Med 2009;15:633-40.
13. Vassiliou E, Sharma V, Jing H, Sheibanie F, Ganea D. Prostaglandin E2 promotes the survival of bone marrow-derived dendritic cells. J Immunol 2004;173:6955-64. (Pubitemid 39541084)
14. Sharma S, Stolina M, Yang SC, Baratelli F, Lin JF, Atianzar K, et al. Tumor cyclooxygenase 2-dependent suppression of dendritic cell function. Clin Cancer Res 2003;9:961-8. (Pubitemid 36323698)
15. Khayrullina T, Yen JH, Jing H, Ganea D. In vitro differentiation of dendritic cells in the presence of prostaglandin E2 alters the IL-12/IL-23 balance and promotes differentiation of Th17 cells. J Immunol 2008;181:721-35.
16. Sharma S, Yang SH, Zhu L, Reckamp K, Gardner B, Baratelli B, et al. Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res 2005;65:5211-20. (Pubitemid 40827331)
17. Zeddou M, Greimers R, Valensart N, Nayjib B, Tasken K, Boniver J, et al. Prostaglandin E2 induces the expression of functional inhibitory CD94/NKG2A receptors in human CD8+ T lymphocytes by a cAMP dependent protein kinase A type I pathway. Biochem Pharmacol 2005;70:714-24. (Pubitemid 41058706)
18. 2 catabolism in myeloid cells. J Leukoc Biol 2010;88:839-48.
19. Yang L, Yamagata N, Yadav R, Brandon S, Courtney RL, Morrow JD, et al. Cancer-associated immunodeficiency and dendritic cell abnormalities mediated by the prostaglandin EP2 receptor. J Clin Invest 2003;111:727-35. (Pubitemid 36278591)
20. Wülfing C, Eltze E, von Struensee D, Wülfing P, Hertle L, Piechota H. Cyclooxygenase-2 expression in bladder cancer: correlation with poor outcome after chemotherapy. Eur Urol 2004;45:46-52. (Pubitemid 37548993)
21. Wild P, Kunz-Schughart A, Stoehr R, Burger M, Blaszyk H, Simon R, et al. High-throughput tissue microarray analysis of COX2 expression in urinary bladder cancer. Int J Oncol 2005;27:385-91.
22. Pollard J. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 2004;4:71-8. (Pubitemid 38082155)
23. Mantovani A, Schioppa T, Porta C, Allavena P, Sica A Antonio. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev 2006;25:315-22. (Pubitemid 44922352)
24. Kusmartsev S, Gabriovich D. Effect of tumor-derived cytokines and growth factors on differentiation and immune suppressive features of myeloid cells in cancer. Cancer Rev Metastasis 2006;25:323-31. (Pubitemid 44922353)
25. Talmadge J, Donkor M, Scholar E. Inflammatory cell infiltration of tumors: Jekyll or Hyde. Cancer Metastasis Rev 2007;26:373-400. (Pubitemid 350115102)
26. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005;7:211-7. (Pubitemid 40568680)
27. Du R, Lu K, Petritsch C, Liu P, Ganss R, Passegue E, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008;13:206-20. (Pubitemid 351318372)
28. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005;438:820-7. (Pubitemid 41753060)
29. Nagaraj S, Gabrilovich D. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
30. Peranzoni E, Zilio S, Marigo I, Dolcetti L, Zanovello P, Mandruzzato S, et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 2010;22:238-44.
31. Kusmartsev S, Li Y, Chen SH. Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 co-stimulation. J Immunol 2000;165:779-85. (Pubitemid 30484744)
32. Bronte V, Chappell DB, Apolloni E, Cabrelle A, Wang M, Hwu P, 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;162:5728-37. (Pubitemid 29314923)
33. Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, Beschin A, et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008;111:4233-44.
34. Youn J, Nagaraj S, Collazo M, Gabrilovich D. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008;181:5791-802.
35. Kusmartsev S, Gabrilovich D. STAT1 signaling regulates tumor-associated macrophage-mediated T cell deletion. J Immunol 2005;174:4880-91.
36. Corzo C, Condamine T, Lu L, Cotter M, Youn J, Cheng P, et al. HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 2010;207:2439-53.
37. Movahedi K, Laoui D, Gyseman SC, Baeten M, Van den Bossche J, Mack M, et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C (high) monocytes. Cancer Res 2010;70:5728-39.
38. Burger J, Burger M, Kipps T. Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 1999;94:3658-67.
39. Mohle R, Bautz F, Rafii S, Moore M, Brugger W, Kanz L. The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood 1998;91:4523-30. (Pubitemid 28270300)
40. Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan M, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-6. (Pubitemid 32225831)
41. Geminder H, Sagi-Assif O, Goldberg L, Meshel T, Rechavi G, Witz I, et al. A possible role for CXCR4 and its ligand, the CXC chemokine stromal cell-derived factor-1, in the development of bone marrow metastases in neuroblastoma. J Immunol 2001;167:4747-57. (Pubitemid 32954357)
42. Zeelenberg I, Ruuls-Van Stalle L, Roos E. The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res 2003;63:3833-9. (Pubitemid 36793074)
43. Sakamoto N, Porvasnik S, Kusmartsev S, Eruslanov E, Cao W, Urbanek C, et al. Effects of CXCR4 antagonist CTCE-9908 on prostate tumor growth. Prostate 2009;69:1460-9.
44. Scala S, Ottaiano A, Ascierto P, Cavalli M, Simeone E, Giuliano P, et al. Expression of CXCR4 predicts poor prognosis in patients with malignant melanoma. Clin Cancer Res 2005;11:1835-41. (Pubitemid 40471847)
45. Scotton C, Wilson L, Scott K, Stamp G, Wilbanks D, Fricker S, et al. Multiple actions of the chemokine CXCL12 on epithelial tumor cells in human ovarian cancer. Cancer Res 2002;62:5930-8. (Pubitemid 35204756)
46. Devine S, Flomenberg N, Vesole D, Liesveld J, Weisdorf D, Badel K, et al. Rapid mobilization of CD34+ cells following administration of the CXCR4 antagonist AMD3100 to patients with multiple myeloma and non-Hodgkin's lymphoma. J Clin Oncol 2004;22:1095-102. (Pubitemid 41095043)
47. Tamamura H, Hori A, Kanzaki N, Hiramatsu K, Mizumoto M, Nakashima H, et al. T140 analogs as CXCR4 antagonists identified as antimetastatic agents in the treatment of breast cancer. FEBS Lett 2003;550:79-83. (Pubitemid 37281361)
48. Tseng-Rogenski S, Gee J, Ignatoski KW, Kunju LP, Bucheit A, Kintner HJ, et al. Loss of 15-hydroxyprostaglandin dehydrogenase expression contributes to bladder cancer progression. Am J Pathol 2010;176:1462-8.