The tumoral and stromal immune microenvironment in malignant pleural mesothelioma: A comprehensive analysis reveals prognostic immune markers

OncoImmunology

Volumn 4, Issue 6, 2015, Pages

  Ujiie, Hideki ^a,b   Kadota, Kyuichi ^a   Nitadori, Jun ichi ^a   Aerts, Joachim G ^c   Woo, Kaitlin M ^a   Sima, Camelia S ^a   Travis, William D ^a   Jones, David R ^a   Krug, Lee M ^a   Adusumilli, Prasad S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b CHIBA UNIVERSITY   (Japan)

^c ERASMUS MC CANCER INSTITUTE   (Netherlands)

Author keywords

B lymphocyte; Immune responses to cancer; Pleural malignancy; T lymphocytes; Tumor infiltrating lymphocytes

Indexed keywords

CD163 ANTIGEN; CD20 ANTIGEN; CD4 ANTIGEN; CYTOKINE RECEPTOR; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR;

ADULT; AGED; ANTIGEN DETECTION; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INFILTRATION; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; FEMALE; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PLEURA MESOTHELIOMA; TISSUE MICROARRAY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT;

EID: 84944458839     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1009285     Document Type: Article

References (44)

1. Robinson BW,Musk AW, Lake RA.Malignant mesothelioma. Lancet 2005; 366: 397-408; PMID:16054941; http://dx.doi.org/10.1016/S0140-6736(05)67025-0
2. Krug LM, Pass HI, Rusch VW, Kindler HL, Sugarbaker DJ, Rosenzweig KE, Flores R, Friedberg JS, Pisters K, Monberg M, et al. Multicenter phase II trial of neoadjuvant pemetrexed plus cisplatin followed by extrapleural pneumonectomy and radiation for malignant pleural mesothelioma. J Clin Oncol 2009; 27: 3007-13; PMID:19364962; http://dx.doi.org/ 10.1200/JCO.2008.20.3943
3. Flores RM, Krug LM, Rosenzweig KE, Venkatraman E, Vincent A, Heelan R, Akhurst T, Rusch VW. Induction chemotherapy, extrapleural pneumonectomy, and postoperative high-dose radiotherapy for locally advanced malignant pleural mesothelioma: a phase II trial. J Thorac Oncol 2006; 1: 289-95; PMID:17409872; http://dx.doi. org/10.1097/01243894-200605000-00004
4. Anraku M, Cunningham KS, Yun Z, Tsao MS, Zhang L, Keshavjee S, Johnston MR, de Perrot M. Impact of tumor-infiltrating T cells on survival in patients with malignant pleural mesothelioma. J Thorac Cardiovasc Surg 2008; 135: 823-9; PMID:18374762; http://dx. doi.org/10.1016/j.jtcvs.2007.10.026
5. Yamada N, Oizumi S, Kikuchi E, Shinagawa N, Konishi-Sakakibara J, Ishimine A, Aoe K,Gemba K, Kishimoto T, Torigoe T, et al. CD8+ tumor-infiltrating lymphocytes predict favorable prognosis in malignant pleural mesothelioma after resection. Cancer Immunol Immunother 2010; 59: 1543-9; PMID:20567822; http://dx.doi.org/ 10.1007/s00262-010-0881-6
6. Hegmans JP, Hemmes A, Hammad H, Boon L, Hoogsteden HC, Lambrecht BN. Mesothelioma environment comprises cytokines and T-regulatory cells that suppress immune responses. Eur Respir J 2006; 27: 1086-95; PMID:16540497; http://dx.doi.org/ 10.1183/09031936.06.00135305
7. Adusumilli PS, Cherkassky L, Villena-Vargas J, Colovos C, Servais E, Plotkin J, Jones DR, Sadelain M. Regional delivery of mesothelin-targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity. Sci Transl Med 2014; 6: 261ra151; PMID:25378643; http://dx.doi.org/ 10.1126/scitranslmed.3010162
8. Hassan R, Miller AC, Sharon E, Thomas A, Reynolds JC, Ling A, Kreitman RJ, Miettinen MM, Steinberg SM, Fowler DH, et al. Major cancer regressions in mesothelioma after treatment with an anti-mesothelin immunotoxin and immune suppression. Sci Transl Med 2013; 5: 208ra147; PMID:24154601; http://dx. doi.org/10.1126/scitranslmed.3006941
9. Kao SC, Klebe S, Henderson DW, Reid G, Chatfield M, Armstrong NJ, Yan TD, Vardy J, Clarke S, van Zandwijk N, et al. Low calretinin expression and high neutrophil-to-lymphocyte ratio are poor prognostic factors in patients with malignant mesothelioma undergoing extrapleural pneumonectomy. J Thorac Oncol 2011; 6: 1923-9; PMID:22011651; http://dx.doi.org/ 10.1097/JTO.0b013e31822a3740
10. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, CamusM, Berger A, Wind P, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313: 1960-4; PMID:17008531; http://dx. doi.org/10.1126/science.1129139
11. Bograd AJ, Suzuki K, Vertes E, Colovos C, Morales EA, Sadelain M, Adusumilli PS. Immune responses and immunotherapeutic interventions in malignant pleural mesothelioma. Cancer Immunol Immunother 2011; 60: 1509-27; PMID:21913025; http://dx.doi. org/10.1007/s00262-011-1103-6
12. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005; 353: 2654-66; PMID:16371631; http:// dx.doi.org/10.1056/NEJMoa051424
13. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003; 348: 203-13; PMID:12529460; http://dx.doi.org/10.1056/NEJMoa020177
14. Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, Ellis IO, Green AR. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol 2011; 29: 1949-55; PMID:21483002; http://dx.doi.org/10.1200/JCO. 2010.30.5037
15. Suzuki K, Kadota K, Sima CS, Sadelain M, Rusch VW, Travis WD, Adusumilli PS. Chronic inflammation in tumor stroma is an independent predictor of prolonged survival in epithelioid malignant pleural mesothelioma patients. Cancer Immunol Immunother 2011; 60: 1721-8; PMID:21769693; http://dx.doi.org/10.1007/ s00262-011-1073-8
16. Bouaziz JD, Yanaba K, Venturi GM, Wang Y, Tisch RM, Poe JC, Tedder TF. Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc Natl Acad Sci U S A 2007; 104: 20878-83; PMID:18093919; http://dx.doi.org/ 10.1073/pnas.0709205105
17. Coughlin CM, Vance BA, Grupp SA, Vonderheide RH. RNA-transfected CD40-activated B cells induce functional T-cell responses against viral and tumor antigen targets: implications for pediatric immunotherapy. Blood 2004; 103: 2046-54; PMID:14630810; http:// dx.doi.org/10.1182/blood-2003-07-2379
18. Schultz KR, Klarnet JP, Gieni RS, HayGlass KT, Greenberg PD. The role of B cells for in vivo T cell responses to a Friend virus-induced leukemia. Science 1990; 249: 921-3; PMID:2118273; http://dx.doi.org/ 10.1126/science.2118273
19. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005; 7: 411-23; PMID:15894262; http://dx.doi.org/10.1016/j. ccr.2005.04.014
20. Mahmoud SM, Lee AH, Paish EC, Macmillan RD, Ellis IO, Green AR. The prognostic significance of B lymphocytes in invasive carcinoma of the breast. Breast Cancer Res Treat 2012; 132: 545-53; PMID:21671016; http:// dx.doi.org/10.1007/s10549-011-1620-1
21. Al-Shibli KI, Donnem T, Al-Saad S, Persson M, Bremnes RM, Busund LT. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 2008; 14: 5220-7; PMID:18698040; http://dx.doi.org/10.1158/1078-0432.CCR-08-0133
22. Milne K, Kobel M, Kalloger SE, Barnes RO, Gao D, Gilks CB, Watson PH, Nelson BH. Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLoS One 2009; 4: e6412; PMID:19641607; http://dx.doi.org/10.1371/journal. pone.0006412
23. TewariN, Zaitoun AM, Arora A,Madhusudan S, IlyasM, LoboDN. The presence of tumour-associated lymphocytes confers a good prognosis in pancreatic ductal adenocarcinoma: an immunohistochemical study of tissue microarrays. BMC Cancer 2013; 13: 436; PMID:24063854; http://dx.doi.org/10.1186/1471-2407-13-436
24. Lissbrant IF, Stattin P, Wikstrom P, Damber JE, Egevad L, Bergh A. Tumor associated macrophages in human prostate cancer: relation to clinicopathological variables and survival. Int J Oncol 2000; 17: 445-51; PMID:10938382
25. Solinas G, Germano G, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 2009; 86: 1065-73; PMID:19741157; http://dx.doi. org/10.1189/jlb.0609385
26. Bingle L, Brown NJ, Lewis CE. The role of tumourassociated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002; 196: 254-65; PMID:11857487; http://dx.doi.org/ 10.1002/path.1027
27. Sica A, Larghi P, Mancino A, Rubino L, Porta C, Totaro MG, Rimoldi M, Biswas SK, Allavena P, Mantovani A. Macrophage polarization in tumour progression. Semin Cancer Biol 2008; 18: 349-55; PMID:18467122; http://dx.doi.org/10.1016/j. semcancer.2008.03.004
28. Brower V. Macrophages: cancer therapy's double-edged sword. J Natl Cancer Inst 2012; 104: 649-52; PMID:22517985; http://dx.doi.org/10.1093/jnci/djs235
29. Izzi V, Chiurchiu V, D'Aquilio F, Palumbo C, Tresoldi I, Modesti A, Baldini PM. Differential effects of malignant mesothelioma cells on THP-1 monocytes and macrophages. Int J Oncol 2009; 34: 543-50; PMID:19148491
30. Baratelli F, Lin Y, Zhu L, Yang SC, Heuze-Vourc'h N, Zeng G, Reckamp K,Dohadwala M, Sharma S, Dubinett SM. Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4+ T cells. J Immunol 2005; 175: 1483-90; PMID:16034085; http:// dx.doi.org/10.4049/jimmunol.175.3.1483
31. Chen C, Shen Y, Qu QX, Chen XQ, Zhang XG, Huang JA. Induced expression of B7-H3 on the lung cancer cells and macrophages suppresses T-cell mediating anti-tumor immune response. Exp Cell Res 2013; 319: 96-102; PMID:22999863; http://dx.doi.org/ 10.1016/j.yexcr.2012.09.006
32. Suzuki K, Kadota K, Sima CS, Nitadori J, Rusch VW, Travis WD, Sadelain M, Adusumilli PS. Clinical impact of immune microenvironment in stage I lung adenocarcinoma: tumor interleukin-12 receptor beta2 (IL-12Rbeta2), IL-7R, and stromal FoxP3/CD3 ratio are independent predictors of recurrence. J Clin Oncol 2013; 31: 490-8; PMID:23269987; http://dx.doi.org/ 10.1200/JCO.2012.45.2052
33. Kadota K,Nitadori JI, Adusumilli PS. Prognostic value of the immune microenvironment in lung adenocarcinoma. Oncoimmunology 2013; 2: e24036; PMID:23762792; http://dx.doi.org/10.4161/onci.24036
34. Ming J, Zhang Q, Qiu X, Wang E. Interleukin 7/interleukin 7 receptor induce c-Fos/c-Jun-dependent vascular endothelial growth factor-D up-regulation: a mechanism of lymphangiogenesis in lung cancer. Eur J Cancer 2009; 45: 866-73; PMID:19136250; http:// dx.doi.org/10.1016/j.ejca.2008.12.006
35. Al-Rawi MA, Watkins G, Mansel RE, Jiang WG. Interleukin 7 upregulates vascular endothelial growth factor D in breast cancer cells and induces lymphangiogenesis in vivo. Br J Surg 2005; 92: 305-10; PMID:15672426; http://dx.doi.org/10.1002/bjs.4832
36. Rochman Y, Spolski R, Leonard WJ. New insights into the regulation of T cells by gamma(c) family cytokines. Nature Reviews Immunology 2009; 9: 480-90; PMID:19543225; http://dx.doi.org/10.1038/nri2580
37. Kadota K, Suzuki K, Colovos C, Sima CS, Rusch VW, Travis WD, Adusumilli PS. A nuclear grading system is a strong predictor of survival in epitheloid diffuse malignant pleural mesothelioma. Mod Pathol 2012; 25: 260-71; PMID:21983936; http://dx.doi.org/ 10.1038/modpathol.2012.58
38. Kadota K, Suzuki K, Sima CS, Rusch VW, Adusumilli PS, Travis WD. Pleomorphic epithelioid diffuse malignant pleural mesothelioma: a clinicopathological review and conceptual proposal to reclassify as biphasic or sarcomatoid mesothelioma. J Thorac Oncol 2011; 6: 896-904; PMID:21358344; http://dx.doi.org/ 10.1097/JTO.0b013e318211127a
39. Servais EL, Colovos C, Rodriguez L, Bograd AJ, Nitadori J, Sima C, Rusch VW, Sadelain M, Adusumilli PS. Mesothelin overexpression promotes mesothelioma cell invasion and MMP-9 secretion in an orthotopic mouse model and in epithelioid pleural mesothelioma patients. Clin Cancer Res 2012; 18: 2478-89; PMID:22371455; http://dx.doi.org/10.1158/1078-0432.CCR-11-2614
40. Flores RM, Zakowski M, Venkatraman E, Krug L, Rosenzweig K, Dycoco J, Lee C, Yeoh C, Bains M, Rusch V. Prognostic factors in the treatment of malignant pleural mesothelioma at a large tertiary referral center. J Thorac Oncol 2007; 2: 957-65; PMID:17909360; http://dx.doi.org/10.1097/ JTO.0b013e31815608d9
41. Edge SB, American Joint Committee on Cancer. AJCC cancer stagingmanual. New York: Springer; 2010.
42. Kachala SS, Bograd AJ, Villena-Vargas J, Suzuki K, Servais EL, Kadota K, Chou J, Sima CS, Vertes E, Rusch VW, et al. Mesothelin overexpression is a marker of tumor aggressiveness and is associated with reduced recurrence-free and overall survival in earlystage lung adenocarcinoma. Clin Cancer Res 2014; 20: 1020-8; PMID:24334761; http://dx.doi.org/10.1158/ 1078-0432.CCR-13-1862
43. Yoshizawa A, Fukuoka J, Shimizu S, Shilo K, Franks TJ, Hewitt SM, Fujii T, Cordon-Cardo C, Jen J, Travis WD. Overexpression of phospho-eIF4E is associated with survival through AKT pathway in non-small cell lung cancer. Clin Cancer Res 2010; 16: 240-8; PMID:20008839; http://dx.doi.org/10.1158/1078-0432.CCR-09-0986
44. Mazumdar M, Glassman JR. Categorizing a prognostic variable: review of methods, code for easy implementation and applications to decision-making about cancer treatments. Stat Med 2000; 19: 113-32; PMID:10623917; http://dx.doi.org/10.1002/(SICI) 1097-0258(20000115)19:1%3c113::AID-SIM245%3e3.0. CO;2-O