CXCR2-Expressing Myeloid-Derived Suppressor Cells Are Essential to Promote Colitis-Associated Tumorigenesis

Cancer Cell

Volumn 24, Issue 5, 2013, Pages 631-644

  Katoh, Hiroshi ^a   Wang, Dingzhi ^a   Daikoku, Takiko ^b   Sun, Haiyan ^a   Dey, Sudhansu K ^b   DuBois, Raymond N ^a,c  

^a ARIZONA STATE UNIVERSITY   (United States)

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GRANULOCYTE CHEMOTACTIC PROTEIN 2; INTERLEUKIN 6; INTERLEUKIN 8; STAT3 PROTEIN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CHEMOTAXIS; COLITIS; COLON CARCINOGENESIS; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DENDRITIC CELL; DISEASE ASSOCIATION; GENE LOSS; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPPRESSOR CELL;

MUS;

EID: 84887512876     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.10.009     Document Type: Article

References (61)

1. Abdallah Hajj Hussein I., Freund J.N., Reimund J.M., Shams A., Yamine M., Leone A., Jurjus A.R. Enteropathogenic e.coli sustains iodoacetamide-induced ulcerative colitis-like colitis in rats: modulation of IL-1β, IL-6, TNF-α, COX-2, and apoptosisi. J.Biol. Regul. Homeost. Agents 2012, 26:515-526.
2. Acharyya S., Oskarsson T., Vanharanta S., Malladi S., Kim J., Morris P.G., Manova-Todorova K., Leversha M., Hogg N., Seshan V.E., et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012, 150:165-178.
3. Alzoghaibi M.A., Al-Mofleh I.A., Al-Jebreen A.M. Neutrophil chemokines GCP-2 and GRO-alpha in patients with inflammatory bowel disease. J.Dig. Dis. 2008, 9:144-148.
4. Andres P.G., Beck P.L., Mizoguchi E., Mizoguchi A., Bhan A.K., Dawson T., Kuziel W.A., Maeda N., MacDermott R.P., Podolsky D.K., Reinecker H.C. Mice with a selective deletion of the CC chemokine receptors 5 or 2 are protected from dextran sodium sulfate-mediated colitis: lack of CC chemokine receptor 5 expression results in a NK1.1+ lymphocyte-associated Th2-type immune response in the intestine. J.Immunol. 2000, 164:6303-6312.
5. Asfaha S., Dubeykovskiy A.N., Tomita H., Yang X., Stokes S., Shibata W., Friedman R.A., Ariyama H., Dubeykovskaya Z.A., Muthupalani S., et al. Mice that express human interleukin-8 have increased mobilization of immature myeloid cells, which exacerbates inflammation and accelerates colon carcinogenesis. Gastroenterology 2013, 144:155-166.
6. Cho W.S., Chae C. Expression of cyclooxygenase-2 and nitric oxide synthase 2 in swine ulcerative colitis caused by Salmonella typhimurium. Vet. Pathol. 2004, 41:419-423.
7. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
8. Daley J.M., Thomay A.A., Connolly M.D., Reichner J.S., Albina J.E. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J.Leukoc. Biol. 2008, 83:64-70.
9. Diaz-Montero C.M., Salem M.L., Nishimura M.I., Garrett-Mayer E., Cole D.J., Montero A.J. 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.
10. Ekbom A., Helmick C., Zack M., Adami H.O. Ulcerative colitis and colorectal cancer. A population-based study. N.Engl. J. Med. 1990, 323:1228-1233.
11. Elson C.O., Cong Y., McCracken V.J., Dimmitt R.A., Lorenz R.G., Weaver C.T. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol. Rev. 2005, 206:260-276.
12. Feagins L.A., Souza R.F., Spechler S.J. Carcinogenesis in IBD: potential targets for the prevention of colorectal cancer. Nature reviews. Gastroenterol. Hepatol. 2009, 6:297-305.
13. Fegn L., Wang Z. Topical chemoprevention of skin cancer in mice, using combined inhibitors of 5-lipoxygenase and cyclo-oxygenase-2. J.Laryngol. Otol. 2009, 123:880-884.
14. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
15. Gabrilovich D.I., Ostrand-Rosenberg S., Bronte V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012, 12:253-268.
16. Garrido-Mesa N., Camuesco D., Arribas B., Comalada M., Bailon E., Cueto-Sola M., Utrilla P., Nieto A., Zarzuelo A., Rodriguez-Cabezas M.E., Galvez J. The intestinal anti-inflammatory effect of minocycline in experimental colitis involves both its immunomodulatory and antimicrobial properties. Pharmacol. Res. 2011, 63:308-319.
17. Garrido-Mesa N., Utrilla P., Comalada M., Zorrilla P., Garrido-Mesa J., Zarzuelo A., Rodríguez-Cabezas M.E., Gálvez J. The association of minocycline and the probiotic Escherichia coli Nissle 1917 results in an additive beneficial effect in a DSS model of reactivated colitis in mice. Biochem. Pharmacol. 2011, 82:1891-1900.
18. Gionchetti P., Rizzello F., Helwig U., Venturi A., Lammers K.M., Brigidi P., Vitali B., Poggioli G., Miglioli M., Campieri M. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology 2003, 124:1202-1209.
19. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
20. Grivennikov S.I., Wang K., Mucida D., Stewart C.A., Schnabl B., Jauch D., Taniguchi K., Yu G.Y., Osterreicher C.H., Hung K.E., et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 2012, 491:254-258.
21. Haile L.A., von Wasielewski R., Gamrekelashvili J., Kruger C., Bachmann O., Westendorf A.M., Buer J., Liblau R., Manns M.P., Korangy F., Greten T.F. Myeloid-derived suppressor cells in inflammatory bowel disease: a new immunoregulatory pathway. Gastroenterology 2008, 135:871-881.
22. Harrington L.E., Mangan P.R., Weaver C.T. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr. Opin. Immunol. 2006, 18:349-356.
23. Ijichi H., Chytil A., Gorska A.E., Aakre M.E., Bierie B., Tada M., Mohri D., Miyabayashi K., Asaoka Y., Maeda S., et al. Inhibiting Cxcr2 disrupts tumor-stromal interactions and improves survival in a mouse model of pancreatic ductal adenocarcinoma. J.Clin. Invest. 2011, 121:4106-4117.
24. Jamieson T., Clarke M., Steele C.W., Samuel M.S., Neumann J., Jung A., Huels D., Olson M.F., Das S., Nibbs R.J., Sansom O.J. Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J.Clin. Invest. 2012, 122:3127-3144.
25. Katoh H., Hosono K., Ito Y., Suzuki T., Ogawa Y., Kubo H., Kamata H., Mishima T., Tamaki H., Sakagami H., et al. COX-2 and prostaglandin EP3/EP4 signaling regulate the tumor stromal proangiogenic microenvironment via CXCL12-CXCR4 chemokine systems. Am. J. Pathol. 2010, 176:1469-1483.
26. Katoh H., Yamashita K., Waraya M., Margalit O., Ooki A., Tamaki H., Sakagami H., Kokubo K., Sidransky D., Watanabe M. Epigenetic silencing of HOPX promotes cancer progression in colorectal cancer. Neoplasia 2012, 14:559-571.
27. Khan W.I., Motomura Y., Wang H., El-Sharkawy R.T., Verdu E.F., Verma-Gandhu M., Rollins B.J., Collins S.M. Critical role of MCP-1 in the pathogenesis of experimental colitis in the context of immune and enterochromaffin cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 291:G803-G811.
28. Lakatos P.L., Lakatos L. Risk for colorectal cancer in ulcerativecolitis: changes, causes and management strategies. World J.Gastroenterol. 2008, 14:3937-3947.
29. Lauritsen K., Laursen L.S., Bukhave K., Rask-Madsen J. Effects of topical 5-aminosalicylic acid and prednisolone on prostaglandin E2 and leukotriene B4 levels determined by equilibrium invivo dialysis of rectum in relapsing ulcerative colitis. Gastroenterology 1986, 91:837-844.
30. Lee I.A., Kim D.H. Klebsiella pneumoniae increases the risk of inflammation and colitis in a murine model of intestinal bowel disease. Scand. J. Gastroenterol. 2011, 46:684-693.
31. Lu T., Ramakrishnan R., Altiok S., Youn J.I., Cheng P., Celis E., Pisarev V., Sherman S., Sporn M.B., Gabrilovich D. Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic Tcells in mice. J.Clin. Invest. 2011, 121:4015-4029.
32. Luan J., Shattuck-Brandt R., Haghnegahdar H., Owen J.D., Strieter R., Burdick M., Nirodi C., Beauchamp D., Johnson K.N., Richmond A. Mechanism and biological significance of constitutive expression of MGSA/GRO chemokines in malignant melanoma tumor progression. J.Leukoc. Biol. 1997, 62:588-597.
33. Mandruzzato S., Solito S., Falisi E., Francescato S., Chiarion-Sileni V., Mocellin S., Zanon A., Rossi C.R., Nitti D., Bronte V., Zanovello P. IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J.Immunol. 2009, 182:6562-6568.
34. Maxwell P.J., Gallagher R., Seaton A., Wilson C., Scullin P., Pettigrew J., Stratford I.J., Williams K.J., Johnston P.G., Waugh D.J. HIF-1 and NF-kappaB-mediated upregulation of CXCR1 and CXCR2 expressionpromotes cell survival in hypoxic prostate cancer cells. Oncogene 2007, 26:7333-7345.
35. Mitsuyama K., Tsuruta O., Tomiyasu N., Takaki K., Suzuki A., Masuda J., Yamasaki H., Toyonaga A., Sata M. Increased circulating concentrations of growth-related oncogene (GRO)-alpha in patients with inflammatory bowel disease. Dig. Dis. Sci. 2006, 51:173-177.
36. Monteleone I., Sarra M., Pallone F., Monteleone G. Th17-related cytokines in inflammatory bowel diseases: friends or foes?. Curr. Mol. Med. 2012, 12:592-597.
37. Oppenheim J.J., Zachariae C.O., Mukaida N., Matsushima K. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu. Rev. Immunol. 1991, 9:617-648.
38. Popivanova B.K., Kostadinova F.I., Furuichi K., Shamekh M.M., Kondo T., Wada T., Egashira K., Mukaida N. Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice. Cancer Res. 2009, 69:7884-7892.
39. Raccosta L., Fontana R., Maggioni D., Lanterna C., Villablanca E.J., Paniccia A., Musumeci A., Chiricozzi E., Trincavelli M.L., Daniele S., et al. The oxysterol-CXCR2 axis plays a key role in the recruitment of tumor-promoting neutrophils. J.Exp. Med. 2013, 210:1711-1728.
40. Rubie C., Frick V.O., Wagner M., Schuld J., Gräber S., Brittner B., Bohle R.M., Schilling M.K. ELR+ CXC chemokine expression in benign and malignant colorectal conditions. BMC Cancer 2008, 8:178.
41. Singer I.I., Kawka D.W., Schloemann S., Tessner T., Riehl T., Stenson W.F. Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology 1998, 115:297-306.
42. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of Tcell-mediated tissue damage. Nat. Med. 2007, 13:139-145.
43. Strober W., Fuss I., Mannon P. The fundamental basis of inflammatory bowel disease. J.Clin. Invest. 2007, 117:514-521.
44. Sutherland L., Singleton J., Sessions J., Hanauer S., Krawitt E., Rankin G., Summers R., Mekhjian H., Greenberger N., Kelly M., et al. Double blind, placebo controlled trial of metronidazole in Crohn's disease. Gut 1991, 32:1071-1075.
45. Tokuyama H., Ueha S., Kurachi M., Matsushima K., Moriyasu F., Blumberg R.S., Kakimi K. The simultaneous blockade of chemokine receptors CCR2, CCR5 and CXCR3 by a non-peptide chemokine receptor antagonist protects mice from dextran sodium sulfate-mediated colitis. Int. Immunol. 2005, 17:1023-1034.
46. Tosolini M., Kirilovsky A., Mlecnik B., Fredriksen T., Mauger S., Bindea G., Berger A., Bruneval P., Fridman W.H., Pagès F., Galon J. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 2011, 71:1263-1271.
47. Tsukamoto H., Nishikata R., Senju S., Nishimura Y. Myeloid-Derived Suppressor Cells Attenuate TH1 Development through IL-6 Production to Promote Tumor Progression. Cancer Immunol Res 2013, 1:64-76.
48. Uronis J.M., Mühlbauer M., Herfarth H.H., Rubinas T.C., Jones G.S., Jobin C. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS ONE 2009, 4:e6026.
49. Vetrano S., Borroni E.M., Sarukhan A., Savino B., Bonecchi R., Correale C., Arena V., Fantini M., Roncalli M., Malesci A., et al. The lymphatic system controls intestinal inflammation and inflammation-associated Colon Cancer through the chemokine decoy receptor D6. Gut 2010, 59:197-206.
50. Vezys V., Olson S., Lefrançois L. Expression of intestine-specific antigen reveals novel pathways of CD8 Tcell tolerance induction. Immunity 2000, 12:505-514.
51. Wang B., Hendricks D.T., Wamunyokoli F., Parker M.I. A growth-related oncogene/CXC chemokine receptor 2 autocrine loop contributes to cellular proliferation in esophageal cancer. Cancer Res. 2006, 66:3071-3077.
52. Wang D., Wang H., Brown J., Daikoku T., Ning W., Shi Q., Richmond A., Strieter R., Dey S.K., DuBois R.N. CXCL1 induced by prostaglandin E2 promotes angiogenesis in colorectal cancer. J.Exp. Med. 2006, 203:941-951.
53. Wang D., Dubois R.N., Richmond A. The role of chemokines in intestinal inflammation and cancer. Curr. Opin. Pharmacol. 2009, 9:688-696.
54. Wen Y., Giardina S.F., Hamming D., Greenman J., Zachariah E., Bacolod M.D., Liu H., Shia J., Amenta P.S., Barany F., et al. GROalpha is highly expressed in adenocarcinoma of the colon and down-regulates fibulin-1. Clin. Cancer Res. 2006, 12:5951-5959.
55. Yamashita K., Watanabe M. Clinical significance of tumor markers and an emerging perspective on colorectal cancer. Cancer Sci. 2009, 100:195-199.
56. Yang L., Huang J., Ren X., Gorska A.E., Chytil A., Aakre M., Carbone D.P., Matrisian L.M., Richmond A., Lin P.C., Moses H.L. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 2008, 13:23-35.
57. Yi H., Guo C., Yu X., Zuo D., Wang X.Y. Mouse CD11b+Gr-1+ myeloid cells can promote Th17 cell differentiation and experimental autoimmune encephalomyelitis. J.Immunol. 2012, 189:4295-4304.
58. Youn J.I., Nagaraj S., Collazo M., Gabrilovich D.I. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J.Immunol. 2008, 181:5791-5802.
59. Zauber A.G., Winawer S.J., O'Brien M.J., Lansdorp-Vogelaar I., van Ballegooijen M., Hankey B.F., Shi W., Bond J.H., Schapiro M., Panish J.F., et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N.Engl. J. Med. 2012, 366:687-696.
60. Zeng Z., Shi Y.X., Tsao T., Qiu Y., Kornblau S.M., Baggerly K.A., Liu W., Jessen K., Liu Y., Kantarjian H., et al. Targeting of mTORC1/2 by the mTOR kinase inhibitor PP242 induces apoptosis in AML cells under conditions mimicking the bone marrow microenvironment. Blood 2012, 120:2679-2689.
61. Zhao X., Rong L., Zhao X., Li X., Liu X., Deng J., Wu H., Xu X., Erben U., Wu P., et al. TNF signaling drives myeloid-derived suppressor cell accumulation. J.Clin. Invest. 2012, 122:4094-4104.