Pancreatic cancer cells isolated from Muc1-null tumors favor the generation of a mature less suppressive MDSC population

Frontiers in Immunology

Volumn 5, Issue FEB, 2014, Pages

  Kidiyoor, Amritha ^a   Schettini, Jorge ^a   Besmer, Dahlia Marie ^a   Rego, Stephen Lee ^a   Nath, Sritama ^a   Curry, Jennifer Marie ^a   Roy, Lopamudra Das ^a   Dréau, Didier ^a   Mukherjee, Pinku ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

COX 2; Immune suppression; MDSC; Mucin 1; Pancreatic cancer

Indexed keywords

ARGINASE 1; CD115 ANTIGEN; CD11B ANTIGEN; CELECOXIB; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; GLYCOPROTEIN P 15095; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; LYMPHOCYTE ANTIGEN; MUCIN 1; NITRIC OXIDE; PROSTAGLANDIN E2; UNCLASSIFIED DRUG; UREA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS CANCER; PROTEIN EXPRESSION; PROTEOMICS; SPLEEN CELL; SUPPRESSOR CELL; TUMOR GROWTH; UPREGULATION; WESTERN BLOTTING;

EID: 84895552952     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00067     Document Type: Article

References (49)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer (2010) 127(12):2893-917. doi:10.1002/ijc.25516.
2. American Cancer Society. Cancer Facts and Figures 2010. Atlanta: American Cancer Society (2010).
3. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell (2011) 144(5):646-74. doi:10.1016/j.cell.2011.02.013.
4. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, et al. HIF-1 alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med (2010) 207(11):2439-53. doi:10.1084/jem.20100587.
5. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol (2012) 12(4):253-68. doi:10.1038/nri3175.
6. Rhodes JM. Unifying hypothesis for inflammatory bowel disease and associated colon cancer: sticking the pieces together with sugar. Lancet (1996) 347(8993):40-4. doi:10.1016/S0140-6736(96)91563-9.
7. Kufe DW. Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer (2009) 9(12):874-85. doi:10.1038/nrc2761.
8. Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res (2009) 15(17):5323-37. doi:10.1158/1078-0432.CCR-09-0737.
9. Besmer DM, Curry JM, Roy LD, Tinder TL, Sahraei M, Schettini J, et al. Pancreatic ductal adenocarcinoma mice lacking mucin 1 have a profound defect in tumor growth and metastasis. Cancer Res (2011) 71(13):4432-42. doi:10.1158/0008-5472.CAN-10-4439.
10. Roy LD, Sahraei M, Subramani DB, Besmer D, Nath S, Tinder TL, et al. MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene (2011) 30(12):1449-59. doi:10.1038/onc.2010.526.
11. Ren J, Agata N, Chen D, Li Y, Yu WH, Huang L, et al. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell (2004) 5(2):163-75. doi:10.1016/S1535-6108(04)00020-0.
12. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell (2003) 4(6):437-50. doi:10.1016/S1535-6108(03)00309-X.
13. Tinder TL, Subramani DB, Basu GD, Bradley JM, Schettini J, Million A, et al. MUC1 enhances tumor progression and contributes toward immunosuppression in a mouse model of spontaneous pancreatic adenocarcinoma. J Immunol (2008) 181(5):3116-25.
14. Youn JI, Gabrilovich DI. The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol (2010) 40(11):2969-75. doi:10.1002/eji.201040895.
15. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol (2009) 9(3):162-74. doi:10.1038/nri2506.
16. Nagaraj S, Gabrilovich DI. Myeloid-derived suppressor cells. Adv Exp Med Biol (2007) 601:213-23. doi:10.1007/978-0-387-72005-0_22.
17. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol (2009) 182(8):4499-506. doi:10.4049/jimmunol.0802740.
18. Marigo I, Dolcetti L, Serafini P, Zanovello P, Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev (2008) 222:162-79. doi:10.1111/j.1600-065X.2008.00602.x.
19. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res (2007) 67(9):4507-13. doi:10.1158/0008-5472.CAN-06-4174.
20. 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(10):5728-37.
21. Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, 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):1123-31. doi:10.1158/0008-5472.CAN-05-1299.
22. 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):989-99.
23. Greten TF, Manns MP, Korangy F. Myeloid derived suppressor cells in human diseases. Int Immunopharmacol (2011) 11(7):802-7. doi:10.1016/j.intimp.2011.01.003.
24. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol (2008) 181(8):5791-802.
25. Bronte V, Zanovello P. Regulation of immune responses by l-arginine metabolism. Nat Rev Immunol (2005) 5(8):641-54. doi:10.1038/nri1668.
26. Rivoltini L, Carrabba M, Huber V, Castelli C, Novellino L, Dalerba P, et al. Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol Rev (2002) 188:97-113. doi:10.1034/j.1600-065X.2002.18809.x.
27. Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, et al. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med (2007) 13(7):828-35. doi:10.1038/nm1609.
28. Cheng P, Corzo CA, Luetteke N, Yu B, Nagaraj S, Bui MM, 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(10):2235-49. doi:10.1084/jem.20080132.
29. Poh TW, Bradley JM, Mukherjee P, Gendler SJ. Lack of Muc1-regulated beta-catenin stability results in aberrant expansion of CD11b+Gr1+ myeloid-derived suppressor cells from the bone marrow. Cancer Res (2009) 69(8):3554-62. doi:10.1158/0008-5472.CAN-08-3806.
30. Greifenberg V, Ribechini E, Rossner S, Lutz MB. Myeloid-derived suppressor cell activation by combined LPS and IFN-gamma treatment impairs DC development. Eur J Immunol (2009) 39(10):2865-76. doi:10.1002/eji.200939486.
31. Ribechini E, Leenen PJ, Lutz MB. Gr-1 antibody induces STAT signaling, macrophage marker expression and abrogation of myeloid-derived suppressor cell activity in BM cells. Eur J Immunol (2009) 39(12):3538-51. doi:10.1002/eji.200939530.
32. 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(8):4233-44. doi:10.1182/blood-2007-07-099226.
33. Poschke I, Mougiakakos D, Hansson J, Masucci GV, Kiessling R. Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res (2010) 70(11):4335-45. doi:10.1158/0008-5472.CAN-09-3767.
34. Serafini P, Mgebroff S, Noonan K, Borrello I. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res (2008) 68(13):5439-49. doi:10.1158/0008-5472.CAN-07-6621.
35. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science (2010) 327(5966):656-61. doi:10.1126/science.1178331.
36. Yang HS, Tamayo R, Almonte M, Horten B, DaSilva M, Gangi M, et al. Clinical significance of MUC1, MUC2 and CK17 expression patterns for diagnosis of pancreatobiliary carcinoma. Biotech Histochem (2012) 87(2):126-32. doi:10.3109/10520295.2011.570276.
37. Gabitass RF, Annels NE, Stocken DD, Pandha HA, Middleton GW. 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 (2011) 60(10):1419-30. doi:10.1007/s00262-011-1028-0.
38. Morse MA, Hall JR, Plate JM. Countering tumor-induced immunosuppression during immunotherapy for pancreatic cancer. Expert Opin Biol Ther (2009) 9(3):331-9. doi:10.1517/14712590802715756.
39. Chan AK, Lockhart DC, von Bernstorff W, Spanjaard RA, Joo HG, Eberlein TJ, et al. Soluble MUC1 secreted by human epithelial cancer cells mediates immune suppression by blocking T-cell activation. Int J Cancer (1999) 82(5):721-6. doi:10.1002/(SICI)1097-0215(19990827)82:5<::AID-IJC16>3.3.CO;2-E.
40. Agrawal B, Krantz MJ, Reddish MA, Longenecker BM. Cancer-associated MUC1 mucin inhibits human T-cell proliferation, which is reversible by IL-2. Nat Med (1998) 4(1):43-9. doi:10.1038/nm0198-043.
41. Obermajer N, Muthuswamy R, Lesnock J, Edwards RP, Kalinski P. Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells. Blood (2011) 118(20):5498-505. doi:10.1182/blood-2011-07-365825.
42. Ochoa AC, Zea AH, Hernandez C, Rodriguez PC. Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma. Clin Cancer Res (2007) 13(Pt 2):721s-6s. doi:10.1158/1078-0432.CCR-06-2197.
43. Jegerschold C, Pawelzik SC, Purhonen P, Bhakat P, Gheorghe KR, Gyobu N, et al. Structural basis for induced formation of the inflammatory mediator prostaglandin E2. Proc Natl Acad Sci USA (2008) 105(32):11110-5. doi:10.1073/pnas.0802894105.
44. Samuelsson B, Morgenstern R, Jakobsson PJ. Membrane prostaglandin E synthase-1: a novel therapeutic target. Pharmacol Rev (2007) 59(3):207-24. doi:10.1124/pr.59.3.1.
45. Veltman JD, Lambers ME, van Nimwegen M, Hendriks RW, Hoogsteden HC, Aerts JG, et al. COX-2 inhibition improves immunotherapy and is associated with decreased numbers of myeloid-derived suppressor cells in mesothelioma. Celecoxib influences MDSC function. BMC Cancer (2010) 10:464. doi:10.1186/1471-2407-10-464.
46. Iclozan C, Antonia S, Chiappori A, Chen DT, Gabrilovich D. Therapeutic regulation of myeloid-derived suppressor cells and immune response to cancer vaccine in patients with extensive stage small cell lung cancer. Cancer Immunol Immunother (2013) 62(5):909-18. doi:10.1007/s00262-013-1396-8.
47. Mace TA, Ameen Z, Collins A, Wojcik S, Mair M, Young GS, et al. Pancreatic cancer-associated stellate cells promote differentiation of myeloid-derived suppressor cells in a STAT3-dependent manner. Cancer Res (2013) 73(10):3007-18. doi:10.1158/0008-5472.CAN-12-4601.
48. Mukherjee P, Basu GD, Tinder TL, Subramani DB, Bradley JM, Arefayene M, et al. Progression of pancreatic adenocarcinoma is significantly impeded with a combination of vaccine and COX-2 inhibition. J Immunol (2009) 182(1):216-24.
49. Curry JM, Thompson KJ, Rao SG, Besmer DM, Murphy AM, Grdzelishvili VZ, et al. The use of a novel MUC1 antibody to identify cancer stem cells and circulating MUC1 in mice and patients with pancreatic cancer. J Surg Oncol (2013) 107(7):713-22. doi:10.1002/jso.23316.