Mast cells expressing interleukin 17 in the muscularis propria predict a favorable prognosis in esophageal squamous cell carcinoma

Cancer Immunology, Immunotherapy

Volumn 62, Issue 10, 2013, Pages 1575-1585

  Wang, Bo ^a   Li, Lian ^b   Liao, Yuan ^a   Li, Jinqing ^a   Yu, Xingjuan ^a   Zhang, Yi ^b   Xu, Jing ^a   Rao, Huilan ^b   Chen, Shupeng ^a   Zhang, Lanjun ^a,b   Zheng, Limin ^a,b  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Esophageal squamous cell carcinoma (ESCC); Interleukin 17 (IL 17); Mast cells; Muscularis propria; Overall survival

Indexed keywords

CD68 ANTIGEN; INTERLEUKIN 17; SIALOADHESIN;

ADULT; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL DENSITY; CONTROLLED STUDY; CYTOKINE RELEASE; EFFECTOR CELL; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS MUSCLE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MAST CELL; MUSCULARIS PROPRIA; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TUMOR INVASION; TUMOR MICROENVIRONMENT;

CARCINOMA, SQUAMOUS CELL; DISEASE PROGRESSION; ESOPHAGEAL NEOPLASMS; FEMALE; HUMANS; INTERLEUKIN-17; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MAST CELLS; MICROSCOPY, IMMUNOELECTRON; MIDDLE AGED; PROGNOSIS; SURVIVAL ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84885872268     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-013-1460-4     Document Type: Article

References (45)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69-90. doi: 10.3322/caac.20107
2. Enzinger PC, Mayer RJ (2003) Esophageal cancer. N Engl J Med 349(23):2241-2252. doi: 10.1056/NEJMra035010
3. Cooper SL, Russo JK, Chin S (2012) Definitive chemoradiotherapy for esophageal carcinoma. Surg Clin North Am 92(5):1213-1248. doi: 10.1016/j.suc.2012.07.013
4. Rice TW, Zuccaro G Jr, Adelstein DJ, Rybicki LA, Blackstone EH, Goldblum JR (1998) Esophageal carcinoma: depth of tumor invasion is predictive of regional lymph node status. Ann Thorac Surg 65(3):787-792
5. Mueller MM, Fusenig NE (2004) Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 4(11):839-849. doi: 10.1038/nrc1477
6. Hanahan D, Coussens LM (2012) Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21(3):309-322. doi: 10.1016/j.ccr.2012.02.022
7. Fridman WH, Pages F, Sautes-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12(4):298-306. doi: 10.1038/nrc3245
8. Cho Y, Miyamoto M, Kato K, Fukunaga A, Shichinohe T, Kawarada Y, Hida Y, Oshikiri T, Kurokawa T, Suzuoki M, Nakakubo Y, Hiraoka K, Murakami S, Shinohara T, Itoh T, Okushiba S, Kondo S, Katoh H (2003) CD4 + and CD8 + T cells cooperate to improve prognosis of patients with esophageal squamous cell carcinoma. Cancer Res 63(7):1555-1559
9. Liu J, Lu G, Li Z, Tang F, Liu Y, Cui G (2010) Distinct compartmental distribution of mature and immature dendritic cells in esophageal squamous cell carcinoma. Pathol Res Pract 206(9):602-606. doi: 10.1016/j.prp.2010.03.011
10. Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454(7203):436-444. doi: 10.1038/nature07205
11. Grivennikov SI, Greten FR, Karin M (2010) Immunity, inflammation, and cancer. Cell 140(6):883-899. doi: 10.1016/j.cell.2010.01.025
12. Murugaiyan G, Saha B (2009) Protumor vs antitumor functions of IL-17. J Immunol 183(7):4169-4175. doi: 10.4049/jimmunol.0901017
13. Zou W, Restifo NP (2010) T(H)17 cells in tumour immunity and immunotherapy. Nat Rev Immunol 10(4):248-256. doi: 10.1038/nri2742
14. Huang G, Wang Y, Chi H (2012) Regulation of TH17 cell differentiation by innate immune signals. Cell Mol Immunol 9(4):287-295. doi: 10.1038/cmi.2012.10
15. Cua DJ, Tato CM (2010) Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 10(7):479-489. doi: 10.1038/nri2800
16. de Boer OJ, van der Meer JJ, Teeling P, van der Loos CM, Idu MM, van Maldegem F, Aten J, van der Wal AC (2010) Differential expression of interleukin-17 family cytokines in intact and complicated human atherosclerotic plaques. J Pathol 220(4):499-508. doi: 10.1002/path.2667
17. Kuang DM, Zhao Q, Peng C, Xu J, Zhang JP, Wu C, Zheng L (2009) Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J Exp Med 206(6):1327-1337. doi: 10.1084/jem.20082173
18. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pages F (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313(5795):1960-1964. doi: 10.1126/science.1129139
19. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, Chen H, Omeroglu G, Meterissian S, Omeroglu A, Hallett M, Park M (2008) Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 14(5):518-527. doi: 10.1038/nm1764
20. Zhang JP, Yan J, Xu J, Pang XH, Chen MS, Li L, Wu C, Li SP, Zheng L (2009) Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients. J Hepatol 50(5):980-989. doi: 10.1016/j.jhep.2008.12.033
21. Kuang DM, Peng C, Zhao Q, Wu Y, Chen MS, Zheng L (2010) Activated monocytes in peritumoral stroma of hepatocellular carcinoma promote expansion of memory T helper 17 cells. Hepatology 51(1):154-164. doi: 10.1002/hep.23291
22. Kuang DM, Zhao Q, Wu Y, Peng C, Wang J, Xu Z, Yin XY, Zheng L (2011) Peritumoral neutrophils link inflammatory response to disease progression by fostering angiogenesis in hepatocellular carcinoma. J Hepatol 54(5):948-955. doi: 10.1016/j.jhep.2010.08.041
23. Lin SH, Chang JY (2010) Esophageal cancer: diagnosis and management. Chin J Cancer 29(10):843-854
24. Zhu ZH, Sun BY, Ma Y, Shao JY, Long H, Zhang X, Fu JH, Zhang LJ, Su XD, Wu QL, Ling P, Chen M, Xie ZM, Hu Y, Rong TH (2009) Three immunomarker support vector machines-based prognostic classifiers for stage IB non-small-cell lung cancer. J Clin Oncol 27(7):1091-1099. doi: 10.1200/JCO.2008.16.6991
25. Ding T, Xu J, Wang F, Shi M, Zhang Y, Li SP, Zheng L (2009) High tumor-infiltrating macrophage density predicts poor prognosis in patients with primary hepatocellular carcinoma after resection. Hum Pathol 40(3):381-389. doi: 10.1016/j.humpath.2008.08.011
26. Takahashi N, Vanlaere I, de Rycke R, Cauwels A, Joosten LA, Lubberts E, van den Berg WB, Libert C (2008) IL-17 produced by Paneth cells drives TNF-induced shock. J Exp Med 205(8):1755-1761. doi: 10.1084/jem.20080588
27. Lin AM, Rubin CJ, Khandpur R, Wang JY, Riblett M, Yalavarthi S, Villanueva EC, Shah P, Kaplan MJ, Bruce AT (2011) Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol 187(1):490-500. doi: 10.4049/jimmunol.1100123
28. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, Basham B, Smith K, Chen T, Morel F, Lecron JC, Kastelein RA, Cua DJ, McClanahan TK, Bowman EP, de Waal Malefyt R (2007) Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 8(9):950-957. doi: 10.1038/ni1497
29. Hueber AJ, Asquith DL, Miller AM, Reilly J, Kerr S, Leipe J, Melendez AJ, McInnes IB (2010) Mast cells express IL-17A in rheumatoid arthritis synovium. J Immunol 184(7):3336-3340. doi: 10.4049/jimmunol.0903566
30. Zhu X, Mulcahy LA, Mohammed RA, Lee AH, Franks HA, Kilpatrick L, Yilmazer A, Paish EC, Ellis IO, Patel PM, Jackson AM (2008) IL-17 expression by breast-cancer-associated macrophages: IL-17 promotes invasiveness of breast cancer cell lines. Breast Cancer Res 10(6):R95. doi: 10.1186/bcr2195
31. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, Bamba T, Fujiyama Y (2003) Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52(1):65-70
32. Abraham SN, St John AL (2010) Mast cell-orchestrated immunity to pathogens. Nat Rev Immunol 10(6):440-452. doi: 10.1038/nri2782
33. Galli SJ, Grimbaldeston M, Tsai M (2008) Immunomodulatory mast cells: negative, as well as positive, regulators of immunity. Nat Rev Immunol 8(6):478-486. doi: 10.1038/nri2327
34. Asano K, Nabeyama A, Miyake Y, Qiu CH, Kurita A, Tomura M, Kanagawa O, Fujii S, Tanaka M (2011) CD169-positive macrophages dominate antitumor immunity by crosspresenting dead cell-associated antigens. Immunity 34(1):85-95. doi: 10.1016/j.immuni.2010.12.011
35. Kryczek I, Banerjee M, Cheng P, Vatan L, Szeliga W, Wei S, Huang E, Finlayson E, Simeone D, Welling TH, Chang A, Coukos G, Liu R, Zou W (2009) Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 114(6):1141-1149. doi: 10.1182/blood-2009-03-208249
36. Khazaie K, Blatner NR, Khan MW, Gounari F, Gounaris E, Dennis K, Bonertz A, Tsai FN, Strouch MJ, Cheon E, Phillips JD, Beckhove P, Bentrem DJ (2011) The significant role of mast cells in cancer. Cancer Metastasis Rev 30(1):45-60. doi: 10.1007/s10555-011-9286-z
37. Kalesnikoff J, Galli SJ (2008) New developments in mast cell biology. Nat Immunol 9(11):1215-1223. doi: 10.1038/ni.f.216
38. Welsh TJ, Green RH, Richardson D, Waller DA, O'Byrne KJ, Bradding P (2005) Macrophage and mast-cell invasion of tumor cell islets confers a marked survival advantage in non-small-cell lung cancer. J Clin Oncol 23(35):8959-8967. doi: 10.1200/JCO.2005.01.4910
39. Noordenbos T, Yeremenko N, Gofita I, van de Sande M, Tak PP, Canete JD, Baeten D (2012) Interleukin-17-positive mast cells contribute to synovial inflammation in spondyloarthritis. Arthr Rheum 64(1):99-109. doi: 10.1002/art.33396
40. Connor SJ, Paraskevopoulos N, Newman R, Cuan N, Hampartzoumian T, Lloyd AR, Grimm MC (2004) CCR2 expressing CD4 + T lymphocytes are preferentially recruited to the ileum in Crohn's disease. Gut 53(9):1287-1294. doi: 10.1136/gut.2003.028225
41. Villablanca EJ, Cassani B, von Andrian UH, Mora JR (2011) Blocking lymphocyte localization to the gastrointestinal mucosa as a therapeutic strategy for inflammatory bowel diseases. Gastroenterology 140(6):1776-1784. doi: 10.1053/j.gastro.2011.02.015
42. Flores-Langarica A, Meza-Perez S, Calderon-Amador J, Estrada-Garcia T, Macpherson G, Lebecque S, Saeland S, Steinman RM, Flores-Romo L (2005) Network of dendritic cells within the muscular layer of the mouse intestine. Proc Natl Acad Sci U S A 102(52):19039-19044. doi: 10.1073/pnas.0504253102
43. Lv L, Pan K, Li XD, She KL, Zhao JJ, Wang W, Chen JG, Chen YB, Yun JP, Xia JC (2011) The accumulation and prognosis value of tumor infiltrating IL-17 producing cells in esophageal squamous cell carcinoma. PLoS ONE 6(3):e18219. doi: 10.1371/journal.pone.0018219
44. Sfanos KS, Bruno TC, Maris CH, Xu L, Thoburn CJ, DeMarzo AM, Meeker AK, Isaacs WB, Drake CG (2008) Phenotypic analysis of prostate-infiltrating lymphocytes reveals TH17 and Treg skewing. Clin Cancer Res: Off J Am Assoc Cancer Res 14(11):3254-3261. doi: 10.1158/1078-0432.CCR-07-5164
45. Jovanovic DV, Di Battista JA, Martel-Pelletier J, Jolicoeur FC, He Y, Zhang M, Mineau F, Pelletier JP (1998) IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J Immunol 160(7):3513-3521