Loss of SMAD4 promotes colorectal cancer progression by accumulation of myeloid-derived suppressor cells through the CCL15-CCR1 chemokine axis

Clinical Cancer Research

Volumn 22, Issue 2, 2016, Pages 492-501

  Inamoto, Susumu ^a   Itatani, Yoshiro ^a   Yamamoto, Takamasa ^a   Minamiguchi, Sachiko ^a   Hirai, Hideyo ^a   Iwamoto, Masayoshi ^a   Hasegawa, Suguru ^a   Taketo, Makoto Mark ^a   Sakai, Yoshiharu ^a   Kawada, Kenji ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CCL15 CHEMOKINE; CCR1 CHEMOKINE; CD11B ANTIGEN; CD33 ANTIGEN; CHEMOKINE; HLA DR ANTIGEN; SMAD4 PROTEIN; UNCLASSIFIED DRUG; BETA CHEMOKINE; CCL15 PROTEIN, HUMAN; CCR1 PROTEIN, HUMAN; CD33 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR1; MACROPHAGE INFLAMMATORY PROTEIN; SMAD4 PROTEIN, HUMAN;

ARTICLE; BIOACCUMULATION; BLOOD LEVEL; BONE MARROW CELL; CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUPPRESSOR CELL; TUMOR INVASION; COLORECTAL TUMOR; DISEASE COURSE; HT-29 CELL LINE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANTIGENS, CD11B; CELL LINE, TUMOR; CHEMOKINES; CHEMOKINES, CC; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; HLA-DR ANTIGENS; HT29 CELLS; HUMANS; MACROPHAGE INFLAMMATORY PROTEINS; MYELOID CELLS; RECEPTORS, CCR1; SIALIC ACID BINDING IG-LIKE LECTIN 3; SMAD4 PROTEIN;

EID: 84959016957     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-0726     Document Type: Article

References (28)

1. Weinberg RA. Multi-step tumorigenesis. Biol Cancer 2007;11:399-462.
2. Salovaara R, Roth S, Loukola A, Launonen V, Sistonen P, Avizienyte E, et al. Frequent loss of SMAD4/DPC4 protein in colorectal cancers. Gut 2002; 51:56-9.
3. Roth AD, Delorenzi M, Tejpar S, Yan P, Klingbiel D, Fiocca R, et al. Integrated analysis of molecular and clinical prognostic factors in stage II/III colon cancer. J Natl Cancer Inst 2012;104:1635-46.
4. Alazzouzi H, Alhopuro P, Salovaara R, Sammalkorpi H, Järvinen H, Mecklin JP, et al. SMAD4 as a prognostic marker in colorectal cancer. Clin Cancer Res 2005;11:2606-11.
5. Takaku K, Oshima M, Miyoshi H, Matsui M, Seldin MF, Taketo MM. Intestinal tumorigenesis in compound mutantmice of both Dpc4 (Smad4) and Apc genes. Cell 1998;92:645-56.
6. Kitamura T, Kometani K, Hashida H, Matsunaga A, Miyoshi H, Hosogi H, et al. SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion. Nat Genet 2007;39:467-75.
7. Kitamura T, Fujishita T, Loetscher P, Revesz L, Hashida H, Kizaka-Kondoh S, et al. Inactivation of chemokine (C-C motif) receptor 1 (CCR1) suppresses colon cancer liver metastasis by blocking accumulation of immature myeloid cells in a mouse model. Proc Natl Acad Sci U S A 2010; 107:13063-8.
8. Hirai H, Fujishita T, Kurimoto K, Miyachi H, Kitano S, Inamoto S, et al. CCR1-mediated accumulation of myeloid cells in the liver microenvironment promoting mouse colon cancer metastasis. Clin Exp Metastasis 2014;31:977-89.
9. Itatani Y, Kawada K, Fujishita T, Kakizaki F, Hirai H, Matsumoto T, et al. Loss of SMAD4 from colorectal cancer cells promotes CCL15 expression to recruit CCR1 +myeloid cells and facilitate liver metastasis. Gastroenterology 2013;145:1064-75.
10. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumor angiogenesis. Nat Rev Cancer 2008;8:618-31.
11. Joyce JA, Pollard JW.Microenvironmental regulation ofmetastasis. Nat Rev Cancer 2009;9:239-52.
12. Talmadge JE, Gabrilovich DI. History of myeloid-derived suppressor cells. Nat Rev Cancer 2013;13:739-52.
13. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12: 253-68.
14. BertagnolliMM, Niedzwiecki D, Compton CC,Hahn HP, Hall M,Damas B, et al. Microsatellite instability predicts improved response to adjuvant therapy with irinotecan, fluorouracil, and leucovorin in stage III colon cancer: Cancer and Leukemia Group B Protocol 89803. J Clin Oncol 2009;27:1814-21.
15. Lesokhin AM, Hohl TM, Kitano S, Cortez C, Hirschhorn-Cymerman D, Avogadri F, et al. Monocytic CCR2(+) myeloid-derived suppressor cells promote immune escape by limiting activated CD8 T-cell infiltration into the tumor microenvironment. Cancer Res 2012;72:876-86.
16. Li Y, Wu J, Zhang W, Zhang N, Guo H. Identification of serum CCL15 in hepatocellular carcinoma. Br J Cancer 2013;108:99-106.
17. Bodelon C, Polley MY, Kemp TJ, Pesatori AC, McShane LM, Caporaso NE, et al. Circulating levels of immune and inflammatory markers and long versus short survival in early-stage lung cancer. Ann Oncol 2013;24:2073-9.
18. Massagu-e J. TGFbeta in Cancer. Cell 2008;134:215-30.
19. Zhang B, Halder SK, Kashikar ND, Cho YJ, Datta A, Gorden DL, et al. Antimetastatic role of Smad4 signaling in colorectal cancer. Gastroenterology 2010;138:969-80.
20. Pino MS, Kikuchi H, Zeng M, Herraiz MT, Sperduti I, Berger D, et al. Epithelial to mesenchymal transition is impaired in colon cancer cells with microsatellite instability. Gastroenterology 2010;138:1406-17.
21. Voorneveld PW, Kodach LL, Jacobs RJ, Liv N, Zonnevylle AC, Hoogenboom JP, et al. Loss of SMAD4 alters BMP signaling to promote colorectal cancer cell metastasis via activation of Rho and ROCK. Gastroenterology 2014;147:196-208.
22. Calon A, Espinet E, Palomo-Ponce S, Tauriello DVF, Iglesias M, C-espedes MV, et al. Dependency of colorectal cancer on a TGF-b-driven program in stromal cells for metastasis initiation. Cancer Cell 2012; 22:571-84.
23. Katoh H, Wang D, Daikoku T, Sun H, Dey SK, DuBois RN. CXCR2-expressing myeloid-derived suppressor cells are essential to promote colitis-Associated tumorigenesis. Cancer Cell 2013;24:631-44.
24. Forssmann U,Magert HJ, Adermann K, Escher SE, Forssmann WG. Hemofiltrate CC chemokines with unique biochemical proterties: HCC-1/CCL14a and HCC2/CCL15. J Leukoc Biol 2001;70;357-66.
25. Starr AE, Dufour A, Maier J, Overall CM. Biochemical analysis of matrix metalloproteinase activation of chemokines CCL15 and CCL23 and increased glycosaminoglycan binding of CCL16. J Biol Chem 2012;287: 5848-60.
26. Youn BS, Zhang SM, Lee EK, Park DH, Broxmeyer HE, Murphy PM, et al. Molecular cloning of leukotactin-1: a novel human beta-chemokine, a chemoattractant for neutrophils, monocytes, and lymphocytes, and a potent agonist at CC chemokine receptors 1 and 3. J Immunol 1997; 159;5201-5.
27. Escher SE, ForssmannU, Frimpong-Boateng A, Adermann K, Vakili J, Sticht H, et al. Functional analysis of chemically synthesized derivatives of the human CC chemokine CCL15/HCC-2, a high affinity CCR1 ligand. J Pept Res 2004;63;36-47.
28. Gladue RP, Brown MF, Zwillich SH. CCR1 antagonists: what have we learned from clinical trials. Curr Top Med Chem 2010;10:1268-77.