FAP Promotes immunosuppression by cancer-associated fibroblasts in the tumor microenvironment via STAT3-CCL2 Signaling

Cancer Research

Volumn 76, Issue 14, 2016, Pages 4124-4135

  Yang, Xuguang ^a   Lin, Yuli ^a   Shi, Yinghong ^a   Li, Bingji ^a,b   Liu, Weiren ^a   Yin, Wei ^a,b   Dang, Yongjun ^a   Chu, Yiwei ^a   Fan, Jia ^a   He, Rui ^a,b,c  

^a FUDAN UNIVERSITY   (China)

^b ZHONGSHAN HOSPITAL OF FUDAN UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; JANUS KINASE 2; MONOCYTE CHEMOTACTIC PROTEIN 1; SEPRASE; STAT3 PROTEIN; CCL2 PROTEIN, MOUSE; FOCAL ADHESION KINASE; GELATINASE; JAK2 PROTEIN, MOUSE; MEMBRANE PROTEIN; SERINE PROTEINASE; STAT3 PROTEIN, MOUSE; UROKINASE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT CARCINOMA; CANCER ASSOCIATED FIBROBLAST; CANCER INHIBITION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; FIBROBLAST; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; LIVER CANCER; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; C57BL MOUSE; CELL MOTION; IMMUNOLOGICAL TOLERANCE; PHYSIOLOGY;

ANIMALS; CANCER-ASSOCIATED FIBROBLASTS; CELL MOVEMENT; CHEMOKINE CCL2; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GELATINASES; IMMUNE TOLERANCE; JANUS KINASE 2; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TUMOR MICROENVIRONMENT;

EID: 84978476944     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2973     Document Type: Article

References (44)

1. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6: 392-401.
2. Ohlund D, Elyada E, Tuveson D. Fibroblast heterogeneity in the cancer wound. J Exp Med 2014;211:1503-23.
3. Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 2014;25:735-47.
4. Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 2014;25:719-34.
5. Desmouliere A, Guyot C, Gabbiani G. The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol 2004; 48:509-17.
6. Santos AM, Jung J, Aziz N, Kissil JL, Pure E. Targeting fibroblast activation protein inhibits tumor stromagenesis and growth in mice. J Clin Invest 2009;119:3613-25.
7. Trimboli AJ, Cantemir-Stone CZ, Li F, Wallace JA, Merchant A, Creasap N, et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 2009;461:1084-91.
8. Erez N, Truitt M, Olson P, Arron ST, Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010;17:135-47.
9. Cortez E, Roswall P, Pietras K. Functional subsets of mesenchymal cell types in the tumor microenvironment. Semin Cancer Biol 2014;25:3-9.
10. Osterreicher CH, Penz-Osterreicher M, Grivennikov SI, Guma M, Koltsova EK, Datz C, et al. Fibroblast-specific protein 1 identifies an inflammatory subpopulation of macrophages in the liver. Proc Natl Acad Sci U S A 2011;108:308-13.
11. Scanlan MJ, Raj BK, Calvo B, Garin-Chesa P, Sanz-Moncasi MP, Healey JH, et al. Molecular cloning of fibroblast activation protein alpha, a member of the serine protease family selectively expressed in stromal fibroblasts of epithelial cancers. Proc Natl Acad Sci U S A 1994;91: 5657-61.
12. Levy MT, McCaughan GW, Abbott CA, Park JE, Cunningham AM, Muller E, et al. Fibroblast activation protein: a cell surface dipeptidyl peptidase and gelatinase expressed by stellate cells at the tissue remodelling interface in human cirrhosis. Hepatology 1999;29:1768-78.
13. Cheng JD, Dunbrack RL Jr., Valianou M, Rogatko A, Alpaugh RK, Weiner LM.Promotionoftumorgrowth bymurinefibroblast activation protein, a serine protease, in an animal model. Cancer Res 2002;62:4767-72.
14. Lo A, Wang LCS, Scholler J, Monslow J, Avery D, Newick K, et al. Tumorpromoting desmoplasia is disrupted by depleting FAP-expressing stromal cells. Cancer Res 2015;75:2800-10.
15. Kraman M, Bambrough PJ, Arnold JN, Roberts EW, Magiera L, Jones JO, et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 2010;330:827-30.
16. Feig C, Jones JO, Kraman M, Wells RJ, Deonarine A, Chan DS, et al. Targeting CXCL12 from FAP-expressing carcinoma-associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer. Proc Natl Acad Sci U S A 2013;110:20212-7.
17. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
18. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009;9:798-809.
19. Artym VV, Kindzelskii AL, Chen WT, Petty HR. Molecular proximity of seprase and the urokinase-type plasminogen activator receptor on malignant melanoma cell membranes: dependence on beta(1) integrins and the cytoskeleton. Carcinogenesis 2002;23:1593-601.
20. Sulzmaier FJ, Jean C, Schlaepfer DD. FAK in cancer: mechanistic findings and clinical applications. Nat Rev Cancer 2014;14:598-610.
21. Smith HW, Marshall CJ. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Bio 2010;11:23-36.
22. Bowman T, Broome MA, Sinibaldi D, Wharton W, Pledger WJ, Sedivy JM, et al. Stat3-mediated Myc expression is required for Src transformation and PDGF-induced mitogenesis. Proc Natl Acad Sci U S A 2001;98:7319-24.
23. Bai KJ, Chen BC, Pai HC, Weng CM, Yu CC, Hsu MJ, et al. Thrombininduced CCN2 expression in human lung fibroblasts requires the c-Src/ JAK2/STAT3 pathway. J Leukoc Biol 2013;93:101-12.
24. Christiansen VJ, Jackson KW, Lee KN, Downs TD, McKee PA. Targeting inhibition of fibroblast activation protein-alpha and prolyl oligopeptidase activities on cells common to metastatic tumor microenvironments. Neoplasia 2013;15:348-58.
25. Adams S, Miller GT, Jesson MI, Watanabe T, Jones B, Wallner BP. PT-100, a small molecule dipeptidyl peptidase inhibitor, has potent antitumor effects and augments antibody-mediated cytotoxicity via a novel immune mechanism. Cancer Res 2004;64:5471-80.
26. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12:253-68.
27. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009;182:4499-506.
28. Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 2009; 29:313-26.
29. Tsuyada A, Chow A, Wu J, Somlo G, Chu P, Loera S, et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res 2012;72:2768-79.
30. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nat Rev Immunol 2011;11:762-74.
31. Sirica AE, Campbell DJ, Dumur CI. Cancer-associated fibroblasts in intrahepatic cholangiocarcinoma. Curr Opin Gastroenterol 2011;27: 276-84.
32. Deng J, Liu Y, Lee H, Herrmann A, Zhang W, Zhang C, et al. S1PR1-STAT3 signaling is crucial for myeloid cell colonization at future metastatic sites. Cancer Cell 2012;21:642-54.
33. Wang L, Yi T, Kortylewski M, Pardoll DM, Zeng D, Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med 2009; 206:1457-64.
34. Wong VW, Rustad KC, Akaishi S, Sorkin M, Glotzbach JP, Januszyk M, et al. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med 2012;18:148-52.
35. Cui TX, Kryczek I, Zhao L, Zhao E, Kuick R, Roh MH, et al. Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing micro-RNA101 and suppressing the corepressor CtBP2. Immunity 2013;39: 611-21.
36. Wan S, Zhao E, Kryczek I, Vatan L, Sadovskaya A, Ludema G, et al. Tumorassociated macrophages produce interleukin 6 and signal via STAT3 topromote expansion of human hepatocellular carcinoma stem cells. Gastroenterology 2014;147:1393-404.
37. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011;475:222-5.
38. Brown CE, Vishwanath RP, Aguilar B, Starr R, Najbauer J, Aboody KS, et al. Tumor-derived chemokine MCP-1/CCL2 is sufficientfor mediatingtumor tropism of adoptively transferred T cells. J Immunol 2007;179:3332-41.
39. Molon B, Ugel S, Del Pozzo F, Soldani C, Zilio S, Avella D, et al. Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. J Exp Med 2011;208:1949-62.
40. Augsten M, Sjoberg E, Frings O, Vorrink SU, Frijhoff J, Olsson E, et al. Cancer-associated fibroblasts expressing CXCL14 Rely upon NOS1-derived nitric oxide signaling for their tumor-supporting properties. Cancer Res 2014;74:2999-3010.
41. Sander LE, Sackett SD, Dierssen U, Beraza N, Linke RP, Muller M, et al. Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J Exp Med 2010;207:1453-64.
42. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012;150:165-78.
43. Roberts EW, Deonarine A, Jones JO, Denton AE, Feig C, Lyons SK, et al. Depletion of stromal cells expressing fibroblast activation protein-alpha from skeletal muscle and bone marrow results in cachexia and anemia. J Exp Med 2013;210:1137-51.
44. Tran E, Chinnasamy D, Yu Z, Morgan RA, Lee CC, Restifo NP, et al. Immune targeting of fibroblast activation protein triggers recognition of multipotent bone marrow stromal cells and cachexia. J Exp Med 2013;210: 1125-35.