The role of the immune system in non-small cell lung carcinoma and potential for therapeutic intervention

Translational Lung Cancer Research

Volumn 4, Issue 2, 2015, Pages 177-190

  Domagala Kulawik, Joanna ^a  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

Cytotoxic cells; Immune response; Immunotherapy; Lung cancer; Regulation; Vaccines

Indexed keywords

ANTINEOPLASTIC AGENT; CANCER VACCINE; IMMUNOMODULATING AGENT; TUMOR ANTIGEN;

CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CELL MEDIATED CYTOTOXICITY; DRUG TARGETING; HUMAN; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; LUNG CARCINOGENESIS; NON SMALL CELL LUNG CANCER; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; VACCINE PRODUCTION;

EID: 84938078422     PISSN: 22186751     EISSN: 22264477     Source Type: Journal    
DOI: 10.3978/j.issn.2218-6751.2015.01.11     Document Type: Review

References (111)

1. Adler IA. Classics in oncology: Primary malignant growths of the lung. CA Cancer J Clin 1980;30:295-301.
2. Alberg AJ, Brock MV, Ford JG, et al. Epidemiology of lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidencebased clinical practice guidelines. Chest 2013;143:e1S-29S.
3. European Respiratory Society. eds. European Lung White Book. Washington, DC: European Respiratory Society, 2014.
4. Howington JA, Blum MG, Chang AC, et al. Treatment of stage I and II non-small cell lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e278S-313S.
5. Thunnissen E, van der Oord K, den Bakker M. Prognostic and predictive biomarkers in lung cancer. A review. Virchows Arch 2014;464:347-58.
6. Dempke WC, Suto T, Reck M. Targeted therapies for non-small cell lung cancer. Lung Cancer 2010;67:257-74.
7. Thunnissen E, Bubendorf L, Dietel M, et al. EML4-ALK testing in non-small cell carcinomas of the lung: a review with recommendations. Virchows Arch 2012;461:245-57.
8. Lindeman NI, Cagle PT, Beasley MB, et al. Molecular testing guideline for selection of lung cancer patients for EGFR and ALK tyrosine kinase inhibitors: guideline from the College of American Pathologists, International Association for the Study of Lung Cancer, and Association for Molecular Pathology. J Mol Diagn 2013;15:415-53.
9. Thunnissen E, Boers E, Heideman DA, et al. Correlation of immunohistochemical staining p63 and TTF-1 with EGFR and K-ras mutational spectrum and diagnostic reproducibility in non small cell lung carcinoma. Virchows Arch 2012;461:629-38.
10. Travis WD, Brambilla E, Riely GJ. New pathologic classification of lung cancer: relevance for clinical practice and clinical trials. J Clin Oncol 2013;31:992-1001.
11. Krawczyk P, Ramlau R, Chorostowska-Wynimko J, et al. The efficacy of EGFR gene mutation testing in various samples from non-small cell lung cancer patients: a multicenter retrospective study. J Cancer Res Clin Oncol 2015;141:61-8.
12. Franceschi C, Bonafè M, Valensin S, et al. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 2000;908:244-54.
13. Gonçalves RB, Coletta RD, Silvério KG, et al. Impact of smoking on inflammation: overview of molecular mechanisms. Inflamm Res 2011;60:409-24.
14. Domagala-Kulawik J. Effects of cigarette smoke on the lung and systemic immunity. J Physiol Pharmacol 2008;59:19-34.
15. Domagala-Kulawik J, Hoser G, Safianowska A, et al. Elevated TGF-beta1 concentration in bronchoalveolar lavage fluid from patients with primary lung cancer. Arch Immunol Ther Exp (Warsz) 2006;54:143-7.
16. Hoser G, Kawiak J, Domagala-Kulawik J, et al. Flow cytometric evaluation of lymphocyte subpopulations in BALF of healthy smokers and nonsmokers. Folia Histochem Cytobiol 1999;37:25-30.
17. Hoser G, Domagala-Kulawik J, Droszcz P, et al. Lymphocyte subsets differences in smokers and nonsmokers with primary lung cancer: a flow cytometry analysis of bronchoalveolar lavage fluid cells. Med Sci Monit 2003;9:BR310-5.
18. Poletti V, Poletti G, Murer B, et al. Bronchoalveolar lavage in malignancy. Semin Respir Crit Care Med 2007;28:534-45.
19. Klech H, Pohl W. Technical recommendations and guidelines for bronchoalveolar lavage (BAL). Report of the European Society of Pneumology Task Group. Eur Respir J 1989;2:561-85.
20. Linder J, Rennard SI. eds. Bronchoalveolar Lavage. Chicago: The American Society for Clinical Pathology, 1992.
21. Chcialowski A, Chorostowska-Wynimko J, Fal A, et al. Recommendation of the Polish Respiratory Society for bronchoalveolar lavage (BAL) sampling, processing and analysis methods. Pneumonol Alergol Pol 2011;79:75-89.
22. Bronchoalveolar lavage constituents in healthy individuals, idiopathic pulmonary fibrosis, and selected comparison groups. The BAL Cooperative Group Steering Committee. Am Rev Respir Dis 1990;141:S169-202.
23. Domagala-Kulawik J, Hoser G, Droszcz P, et al. T-cell subtypes in bronchoalveolar lavage fluid and in peripheral blood from patients with primary lung cancer. Diagn Cytopathol 2001;25:208-13.
24. Domagala-Kulawik J, Guzman J, Costabel U. Immune cells in bronchoalveolar lavage in peripheral lung cancer-analysis of 140 cases. Respiration 2003;70:43-8.
25. Domagala-Kulawik J, Hoser G, Safianowska A, et al. Elevated TGF-beta1 concentration in bronchoalveolar lavage fluid from patients with primary lung cancer. Arch Immunol Ther Exp (Warsz) 2006;54:143-7.
26. Bingle CD. Thyroid transcription factor-1. Int J Biochem Cell Biol 1997;29:1471-3.
27. Solis LM, Behrens C, Raso MG, et al. Histologic patterns and molecular characteristics of lung adenocarcinoma associated with clinical outcome. Cancer 2012;118:2889-99.
28. Wu X, Chen H, Wang X. Can lung cancer stem cells be targeted for therapies? Cancer Treat Rev 2012;38:580-8.
29. Kim CF, Jackson EL, Woolfenden AE, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121:823-35.
30. Kim CF. Paving the road for lung stem cell biology: bronchioalveolar stem cells and other putative distal lung stem cells. Am J Physiol Lung Cell Mol Physiol 2007;293:L1092-8.
31. Szypowska A, Stelmaszczyk-Emmel A, Demkow U, et al. Low frequency of regulatory T cells in the peripheral blood of children with type 1 diabetes diagnosed under the age of five. Arch Immunol Ther Exp (Warsz) 2012;60:307-13.
32. Wang P, Gao Q, Suo Z, et al. Identification and characterization of cells with cancer stem cell properties in human primary lung cancer cell lines. PLoS One 2013;8:e57020.
33. Yoshino I, Yano T, Murata M, et al. Phenotypes of lymphocytes infiltrating non-small cell lung cancer tissues and its variation with histological types of cancer. Lung Cancer 1993;10:13-9.
34. Al-Shibli KI, Donnem T, Al-Saad S, et al. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 2008;14:5220-7.
35. Allavena P, Mantovani A. Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 2012;167:195-205.
36. Través PG, Luque A, Hortelano S. Macrophages, inflammation, and tumor suppressors: ARF, a new player in the game. Mediators Inflamm 2012;2012:568783.
37. Fridlender ZG, Albelda SM. Tumor-associated neutrophils: friend or foe? Carcinogenesis 2012;33:949-55.
38. Gatault S, Legrand F, Delbeke M, et al. Involvement of eosinophils in the anti-tumor response. Cancer Immunol Immunother 2012;61:1527-34.
39. Aerts JG, Hegmans JP. Tumor-specific cytotoxic T cells are crucial for efficacy of immunomodulatory antibodies in patients with lung cancer. Cancer Res 2013;73:2381-8.
40. Salagianni M, Baxevanis CN, Papamichail M, et al. New insights into the role of NK cells in cancer immunotherapy. Oncoimmunology 2012;1:205-7.
41. Motohashi S, Okamoto Y, Yoshino I, et al. Antitumor immune responses induced by iNKT cell-based immunotherapy for lung cancer and head and neck cancer. Clin Immunol 2011;140:167-76.
42. Vermaelen K, Pauwels R. Pulmonary dendritic cells. Am J Respir Crit Care Med 2005;172:530-51.
43. Bright RK. Immunology of lung cancer. In: Pass HI, Mitchel IB, Johnson DH, et al. eds. Lung Cancer. Lippincott W&W, 2000:304-18.
44. Tartour E, Zitvogel L. Lung cancer: potential targets for immunotherapy. Lancet Respir Med 2013;1:551-63.
45. Kris MG, Natale RB, Herbst RS, et al. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. JAMA 2003;290:2149-58.
46. Brahmer JR. PD-1-targeted immunotherapy: recent clinical findings. Clin Adv Hematol Oncol 2012;10:674-5.
47. Dasanu CA, Sethi N, Ahmed N. Immune alterations and emerging immunotherapeutic approaches in lung cancer. Expert Opin Biol Ther 2012;12:923-37.
48. Declerck S, Vansteenkiste J. Immunotherapy for lung cancer: ongoing clinical trials. Future Oncol 2014;10:91-105.
49. Shih K, Arkenau HT, Infante JR. Clinical impact of checkpoint inhibitors as novel cancer therapies. Drugs 2014;74:1993-2013.
50. Hoser G, Wasilewska D, Domagala-Kulawik J. Expression of Fas receptor on peripheral blood lymphocytes from patients with non-small cell lung cancer. Folia Histochem Cytobiol 2004;42:249-52.
51. Gajewski TF, Meng Y, Harlin H. Immune suppression in the tumor microenvironment. J Immunother 2006;29:233-40.
52. Erfani N, Mehrabadi SM, Ghayumi MA, et al. Increase of regulatory T cells in metastatic stage and CTLA-4 over expression in lymphocytes of patients with non-small cell lung cancer (NSCLC). Lung Cancer 2012;77:306-11.
53. Erfani N, Khademi B, Haghshenas MR, et al. Intracellular CTLA4 and regulatory T cells in patients with laryngeal squamous cell carcinoma. Immunol Invest 2013;42:81-90.
54. Mocellin S, Nitti D. CTLA-4 blockade and the renaissance of cancer immunotherapy. Biochim Biophys Acta 2013;1836:187-96.
55. Baecher-Allan C, Viglietta V, Hafler DA. Human CD4+CD25+ regulatory T cells. Semin Immunol 2004;16:89-98.
56. Chambers CA, Kuhns MS, Egen JG, et al. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu Rev Immunol 2001;19:565-94.
57. Egen JG, Kuhns MS, Allison JP. CTLA-4: new insights into its biological function and use in tumor immunotherapy. Nat Immunol 2002;3:611-8.
58. Iida T, Ohno H, Nakaseko C, et al. Regulation of cell surface expression of CTLA-4 by secretion of CTLA-4-containing lysosomes upon activation of CD4+ T cells. J Immunol 2000;165:5062-8.
59. Wang XB, Zheng CY, Giscombe R, et al. Regulation of surface and intracellular expression of CTLA-4 on human peripheral T cells. Scand J Immunol 2001;54:453-8.
60. Hall RD, Gray JE, Chiappori AA. Beyond the standard of care: a review of novel immunotherapy trials for the treatment of lung cancer. Cancer Control 2013;20:22-31.
61. Becker C, Kubach J, Wijdenes J, et al. CD4-mediated functional activation of human CD4+CD25+ regulatory T cells. Eur J Immunol 2007;37:1217-23.
62. D'Ambrosio D. Regulatory T cells: how do they find their space in the immunological arena? Semin Cancer Biol 2006;16:91-7.
63. Sainz-Perez A, Lim A, Lemercier B, et al. The T-cell receptor repertoire of tumor-infiltrating regulatory T lymphocytes is skewed toward public sequences. Cancer Res 2012;72:3557-69.
64. Orentas RJ, Kohler ME, Johnson BD. Suppression of anticancer immunity by regulatory T cells: back to the future. Semin Cancer Biol 2006;16:137-49.
65. Shigematsu Y, Hanagiri T, Shiota H, et al. Immunosuppressive effect of regulatory T lymphocytes in lung cancer, with special reference to their effects on the induction of autologous tumor-specific cytotoxic T lymphocytes. Oncol Lett 2012;4:625-30.
66. Simonetta F, Chiali A, Cordier C, et al. Increased CD127 expression on activated FOXP3+CD4+ regulatory T cells. Eur J Immunol 2010;40:2528-38.
67. Douglass S, Ali S, Meeson AP, et al. The role of FOXP3 in the development and metastatic spread of breast cancer. Cancer Metastasis Rev 2012;31:843-54.
68. Petersen RP, Campa MJ, Sperlazza J, et al. Tumor infiltrating Foxp3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients. Cancer 2006;107:2866-72.
69. Wolf AM, Wolf D, Steurer M, et al. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res 2003;9:606-12.
70. Xue L, Lu HQ, He J, et al. Expression of FOXP3 in esophageal squamous cell carcinoma relating to the clinical data. Dis Esophagus 2010;23:340-6.
71. Schneider T, Kimpfler S, Warth A, et al. Foxp3(+) regulatory T cells and natural killer cells distinctly infiltrate primary tumors and draining lymph nodes in pulmonary adenocarcinoma. J Thorac Oncol 2011;6:432-8.
72. Muranski P, Restifo NP. Essentials of Th17 cell commitment and plasticity. Blood 2013;121:2402-14.
73. Romagnani S. Human Th17 cells. Arthritis Res Ther 2008;10:206.
74. Kryczek I, Banerjee M, Cheng P, et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 2009;114:1141-9.
75. Kryczek I, Wu K, Zhao E, et al. IL-17+ regulatory T cells in the microenvironments of chronic inflammation and cancer. J Immunol 2011;186:4388-95.
76. Numasaki M, Watanabe M, Suzuki T, et al. IL-17 enhances the net angiogenic activity and in vivo growth of human non-small cell lung cancer in SCID mice through promoting CXCR-2-dependent angiogenesis. J Immunol 2005;175:6177-89.
77. Devaud C, John LB, Westwood JA, et al. Immune modulation of the tumor microenvironment for enhancing cancer immunotherapy. Oncoimmunology 2013;2:e25961.
78. Dabrowska M, Grubek-Jaworska H, Hoser G, et al. Effect of IFN-gamma stimulation on expression of intercellular adhesion molecule-1 (ICAM-1) on alveolar macrophages in patients with non-small cell lung cancer. J Interferon Cytokine Res 2006;26:190-5.
79. Cassetta L, Cassol E, Poli G. Macrophage polarization in health and disease. ScientificWorldJournal 2011;11:2391-402.
80. Mantovani A, Sozzani S, Locati M, et al. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002;23:549-55.
81. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008;8:958-69.
82. Osinska I, Wolosz D, Domagala-Kulawik J. Association between M1 and M2 macrophages in bronchoalveolar lavage fluid and tobacco smoking in patients with sarcoidosis. Pol Arch Med Wewn 2014;124:359-64.
83. Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 2014;6:13.
84. Ma J, Liu L, Che G, et al. The M1 form of tumorassociated macrophages in non-small cell lung cancer is positively associated with survival time. BMC Cancer 2010;10:112.
85. Serafini P. Myeloid derived suppressor cells in physiological and pathological conditions: the good, the bad, and the ugly. Immunol Res 2013;57:172-84.
86. Ino Y, Yamazaki-Itoh R, Oguro S, et al. Arginase II expressed in cancer-associated fibroblasts indicates tissue hypoxia and predicts poor outcome in patients with pancreatic cancer. PLoS One 2013;8:e55146.
87. Solito S, Marigo I, Pinton L, et al. Myeloid-derived suppressor cell heterogeneity in human cancers. Ann N Y Acad Sci 2014;1319:47-65.
88. Srivastava MK, Andersson Å, Zhu L, et al. Myeloid suppressor cells and immune modulation in lung cancer. Immunotherapy 2012;4:291-304.
89. Witz IP. Tumor-microenvironment interactions: the selectin-selectin ligand axis in tumor-endothelium cross talk. Cancer Treat Res 2006;130:125-40.
90. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54.
91. Fridlender ZG, Jassar A, Mishalian I, et al. Using macrophage activation to augment immunotherapy of established tumours. Br J Cancer 2013;108:1288-97.
92. Fridlender ZG, Albelda SM. Modifying tumor-associated macrophages: An important adjunct to immunotherapy. Oncoimmunology 2013;2:e26620.
93. Doedens AL, Stockmann C, Rubinstein MP, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res 2010;70:7465-75.
94. Beatty GL, Chiorean EG, Fishman MP, et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011;331:1612-6.
95. Gajewski TF, Meng Y, Harlin H. Immune suppression in the tumor microenvironment. J Immunother 2006;29:233-40.
96. Quatromoni JG, Suzuki E, Okusanya O, et al. The timing of TGF-β inhibition affects the generation of antigenspecific CD8+ T cells. BMC Immunol 2013;14:30.
97. Wallace A, Kapoor V, Sun J, et al. Transforming growth factor-beta receptor blockade augments the effectiveness of adoptive T-cell therapy of established solid cancers. Clin Cancer Res 2008;14:3966-74.
98. Wahl SM. Transforming growth factor beta: the good, the bad, and the ugly. J Exp Med 1994;180:1587-90.
99. Cuppens K, Vansteenkiste J. Vaccination therapy for nonsmall-cell lung cancer. Curr Opin Oncol 2014;26:165-70.
100. Vansteenkiste J, Zielinski M, Linder A, et al. Adjuvant MAGE-A3 immunotherapy in resected non-small-cell lung cancer: phase II randomized study results. J Clin Oncol 2013;31:2396-403.
101. Thomas A, Hassan R. Immunotherapies for non-smallcell lung cancer and mesothelioma. Lancet Oncol 2012;13:e301-10.
102. Roulois D, Grégoire M, Fonteneau JF. MUC1-specific cytotoxic T lymphocytes in cancer therapy: induction and challenge. Biomed Res Int 2013;2013:871936.
103. Zhu WF, Li J, Yu LC, et al. Prognostic value of EpCAM/MUC1 mRNA-positive cells in non-small cell lung cancer patients. Tumour Biol 2014;35:1211-9.
104. Kris MG, Johnson BE, Berry LD, et al. Using multiplexed assays of oncogenic drivers in lung cancers to select targeted drugs. JAMA 2014;311:1998-2006.
105. Mellstedt H, Vansteenkiste J, Thatcher N. Vaccines for the treatment of non-small cell lung cancer: investigational approaches and clinical experience. Lung Cancer 2011;73:11-7.
106. Cuppens K, Vansteenkiste J. Vaccination therapy for nonsmall-cell lung cancer. Curr Opin Oncol 2014;26:165-70.
107. Wojas-Krawczyk K, Krawczyk P, Buczkowski J, et al. Immunotherapy of lung adenocarcinoma patient with Peptide-pulsed dendritic cells: a case report. Arch Immunol Ther Exp (Warsz) 2012;60:69-77.
108. Wolchok JD, Hoos A, O'Day S, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009;15:7412-20.
109. Luedke E, Jaime-Ramirez AC, Bhave N, et al. Cetuximab therapy in head and neck cancer: immune modulation with interleukin-12 and other natural killer cell-activating cytokines. Surgery 2012;152:431-40.
110. Luedke E, Jaime-Ramirez AC, Bhave N, et al. Monoclonal antibody therapy of pancreatic cancer with cetuximab: potential for immune modulation. J Immunother 2012;35:367-73.
111. Declerck S, Vansteenkiste J. Immunotherapy for lung cancer: ongoing clinical trials. Future Oncol 2014;10:91-105.