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PMID: 24100804 Published · ppublish English Journal Article

Clinical evaluation of systemic and local immune responses in cancer: time for integration.

Cancer immunology, immunotherapy : CII ·Vol. 63 ·No. 1 ·2014-01-00 ·Pages 45-57

Gutkin DW, Shurin MR

Abstract

The immune system has a dual role in cancer development and progression. On the one hand, it can eradicate emerging malignant cells, but on the other hand, it can actively promote growth of malignant cells, their invasive capacities and their ability to metastasize. Immune cells with predominantly anti-tumor functionality include cells of the innate immune system, such as natural killer cells, and cells of adaptive immunity, such as conventional dendritic cells and cytotoxic T lymphocytes. Immune cells with predominantly pro-tumor functionality include a broad spectrum of cells of the innate and adaptive immune system, such as type 2 neutrophils and macrophages, plasmacytoid DC, myeloid-derived suppressor cells and regulatory T lymphocytes. The presence of immune cells with tumor-suppressive and tumor-promoting activity in the cancer microenvironment and in peripheral blood is usually associated with good clinical outcomes and poor clinical outcomes, respectively. Significant advances in experimental and clinical oncoimmunology achieved in the last decade open an opportunity for the use of modern morphologic, flow cytometric and functional tests in clinical practice. In this review, we describe an integrated approach to clinical evaluation of the immune status of cancer patients for diagnostic purposes, prognostic/predictive purposes (evaluation of patient prognosis and response to treatment) and for therapeutic purposes.

MeSH Terms
Adaptive Immunity Animals Dendritic Cells/cytology Flow Cytometry Humans Immunity, Innate Killer Cells, Natural/cytology Lymphocytes, Tumor-Infiltrating/cytology Macrophages/cytology Neoplasms/immunology,pathology Neutrophils/cytology Predictive Value of Tests Prognosis T-Lymphocytes/cytology Tumor Microenvironment/immunology
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gutkin Dmitriy W
Departments of Pathology, University of Pittsburgh, Pittsburgh, PA, USA, [email protected].
Shurin Michael R
References (138)
138 references, click to expand
  1. The prognostic value of intraepithelial and stromal innate immune system cells in non-small cell lung carcinoma.
    Histopathology. 2009 Sep;55(3):301-12 PMID: 19723145
  2. Circulating and tumor-infiltrating myeloid-derived suppressor cells in patients with colorectal carcinoma.
    PLoS One. 2013;8(2):e57114 PMID: 23437326
  3. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity.
    Adv Immunol. 2006;90:1-50 PMID: 16730260
  4. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures.
    J Clin Oncol. 2008 Sep 20;26(27):4410-7 PMID: 18802153
  5. Blood CD33(+)HLA-DR(-) myeloid-derived suppressor cells are increased with age and a history of cancer.
    J Leukoc Biol. 2013 Apr;93(4):633-7 PMID: 23341539
  6. Prognostic significance of CD3+ tumor-infiltrating lymphocytes in ovarian carcinoma.
    Gynecol Oncol. 2008 Feb;108(2):415-20 PMID: 18037158
  7. Natural killer lymphocytes: biology, development, and function.
    Cancer Immunol Immunother. 2004 Mar;53(3):176-86 PMID: 14685782
  8. Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma: role in tumor progression and death.
    Cancer Res. 2003 Mar 15;63(6):1405-12 PMID: 12649206
  9. Distribution of dendritic cell subtypes in primary oral squamous cell carcinoma is inconsistent with a functional response.
    Cancer Lett. 2007 Sep 18;255(1):145-52 PMID: 17574329
  10. Pediatric cancers are infiltrated predominantly by macrophages and contain a paucity of dendritic cells: a major nosologic difference with adult tumors.
    Clin Cancer Res. 2006 Apr 1;12(7 Pt 1):2049-54 PMID: 16609014
  11. T regulatory cells in cancer: recent advances and therapeutic potential.
    Expert Opin Biol Ther. 2010 Nov;10(11):1573-86 PMID: 20955112
  12. Prognostic significance of p53, bcl-2, vimentin, and S100 protein-positive Langerhans cells in endometrial carcinoma.
    Hum Pathol. 1998 May;29(5):455-62 PMID: 9596268
  13. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients.
    Cancer Immunol Immunother. 2012 Feb;61(2):255-263 PMID: 22120756
  14. Clinical perspectives on targeting of myeloid derived suppressor cells in the treatment of cancer.
    Front Oncol. 2013 Mar 15;3:49 PMID: 23508517
  15. In breast carcinoma tissue, immature dendritic cells reside within the tumor, whereas mature dendritic cells are located in peritumoral areas.
    J Exp Med. 1999 Nov 15;190(10):1417-26 PMID: 10562317
  16. Quantitative and functional alterations of plasmacytoid dendritic cells contribute to immune tolerance in ovarian cancer.
    Cancer Res. 2011 Aug 15;71(16):5423-34 PMID: 21697280
  17. Increased frequency and clinical significance of myeloid-derived suppressor cells in human colorectal carcinoma.
    World J Gastroenterol. 2012 Jul 7;18(25):3303-9 PMID: 22783056
  18. Role of Foxp3-positive tumor-infiltrating lymphocytes in the histologic features and clinical outcomes of hepatocellular carcinoma.
    Am J Surg Pathol. 2012 Jul;36(7):980-6 PMID: 22446942
  19. Stromal macrophage expressing CD204 is associated with tumor aggressiveness in lung adenocarcinoma.
    J Thorac Oncol. 2010 Oct;5(10):1507-15 PMID: 20802348
  20. The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis.
    Br J Cancer. 2011 Jun 28;105(1):93-103 PMID: 21629244
  21. Distribution of Langerhans cells and HLA class II molecules in prostatic carcinomas of different histopathological grade.
    Prostate. 1991;19(1):73-87 PMID: 1876538
  22. Immunosuppressive CD14+HLA-DRlow/- monocytes in prostate cancer.
    Prostate. 2010 Mar 1;70(4):443-55 PMID: 19902470
  23. Natural killer cells in human health and disease.
    Clin Immunol. 2006 Jan;118(1):1-10 PMID: 16337194
  24. Tolerogenic plasmacytoid DC.
    Eur J Immunol. 2010 Oct;40(10):2667-76 PMID: 20821731
  25. Prognostic impact of CD57, CD68, M-CSF, CSF-1R, Ki67 and TGF-beta in soft tissue sarcomas.
    BMC Clin Pathol. 2012 May 03;12:7 PMID: 22554285
  26. Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers.
    Clin Cancer Res. 2003 Oct 1;9(12):4404-8 PMID: 14555512
  27. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome.
    Science. 2006 Sep 29;313(5795):1960-4 PMID: 17008531
  28. An immunohistochemical study of CD1a and CD83-positive infiltrating dendritic cell density in cervical neoplasia.
    Int J Gynecol Pathol. 2007 Jan;26(1):83-8 PMID: 17197902
  29. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse.
    J Clin Oncol. 2006 Dec 1;24(34):5373-80 PMID: 17135638
  30. CD8 tumor-infiltrating lymphocytes are predictive of survival in muscle-invasive urothelial carcinoma.
    Proc Natl Acad Sci U S A. 2007 Mar 6;104(10):3967-72 PMID: 17360461
  31. Myeloid derived suppressor cells and their role in tolerance induction in cancer.
    J Dermatol Sci. 2010 Jul;59(1):1-6 PMID: 20570112
  32. CD1a dendritic cells predominate in transitional cell carcinoma of bladder and kidney but are minimally activated.
    J Urol. 1999 Jun;161(6):1962-7 PMID: 10332481
  33. Effect of head and neck cancer supernatant and CpG-oligonucleotides on migration and IFN-alpha production of plasmacytoid dendritic cells.
    Anticancer Res. 2009 Aug;29(8):3019-25 PMID: 19661310
  34. Phase- and stage-related proportions of T cells bearing the transcription factor FOXP3 infiltrate primary melanoma.
    J Invest Dermatol. 2008 Mar;128(3):676-84 PMID: 17851585
  35. Distribution of S-100 protein-positive dendritic cells and expression of HLA-DR antigen in transitional cell carcinoma of the urinary bladder in relation to tumour progression and prognosis.
    Virchows Arch A Pathol Anat Histopathol. 1993;422(5):351-5 PMID: 8322450
  36. Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the Th2 cytokine interleukin-13.
    Cancer Immunol Immunother. 2011 Oct;60(10):1419-30 PMID: 21644036
  37. Plasmacytoid dendritic cells and cancer.
    J Leukoc Biol. 2011 Oct;90(4):681-90 PMID: 21730085
  38. The prognostic value of peritumoral regulatory T cells and its correlation with intratumoral cyclooxygenase-2 expression in clear cell renal cell carcinoma.
    BJU Int. 2009 Feb;103(3):399-405 PMID: 19021626
  39. Macrophage infiltration and its prognostic relevance in clear cell renal cell carcinoma.
    Cancer Sci. 2011 Jul;102(7):1424-31 PMID: 21453387
  40. Tumor-associated neutrophils: new targets for cancer therapy.
    Cancer Res. 2011 Apr 1;71(7):2411-6 PMID: 21427354
  41. The influence of dendritic cell infiltration and vascular endothelial growth factor expression on the prognosis of non-small cell lung cancer.
    Clin Cancer Res. 2002 Nov;8(11):3480-6 PMID: 12429638
  42. Paucity of dendritic cells in pancreatic cancer.
    Surgery. 2002 Feb;131(2):135-8 PMID: 11854690
  43. The prognostic value of tumor-infiltrating neutrophils in gastric adenocarcinoma after resection.
    PLoS One. 2012;7(3):e33655 PMID: 22442706
  44. FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer.
    J Clin Invest. 2011 Apr;121(4):1361-72 PMID: 21436588
  45. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer.
    Cancer Res. 2001 Jun 15;61(12):4766-72 PMID: 11406550
  46. Cancer classification using the Immunoscore: a worldwide task force.
    J Transl Med. 2012 Oct 03;10:205 PMID: 23034130
  47. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells.
    J Clin Invest. 2005 Dec;115(12):3623-33 PMID: 16308572
  48. The prognostic value of intraepithelial and stromal CD3-, CD117- and CD138-positive cells in non-small cell lung carcinoma.
    APMIS. 2010 May;118(5):371-82 PMID: 20477813
  49. S100 positive dendritic cells in human lung tumors associated with cell differentiation and enhanced survival.
    Pathology. 1993 Oct;25(4):338-43 PMID: 8164994
  50. Targeting myeloid regulatory cells in cancer by chemotherapeutic agents.
    Immunol Res. 2011 Aug;50(2-3):276-85 PMID: 21717082
  51. Role of cytokines in distribution and differentiation of dendritic cell/Langerhans' cell lineage in human primary carcinomas of the lung.
    Hum Pathol. 1995 Aug;26(8):866-72 PMID: 7635448
  52. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase.
    J Clin Invest. 2007 Sep;117(9):2570-82 PMID: 17710230
  53. CD4+CD25high T cells are enriched in the tumor and peripheral blood of prostate cancer patients.
    J Immunol. 2006 Nov 15;177(10):7398-405 PMID: 17082659
  54. Exploring the full spectrum of macrophage activation.
    Nat Rev Immunol. 2008 Dec;8(12):958-69 PMID: 19029990
  55. Increased prevalence of regulatory T-cells in the peripheral blood of patients with gastrointestinal cancer.
    Anticancer Res. 2009 May;29(5):1527-32 PMID: 19443361
  56. Tumor-infiltrating Foxp3+ regulatory T cells are correlated with cyclooxygenase-2 expression and are associated with recurrence in resected non-small cell lung cancer.
    J Thorac Oncol. 2010 May;5(5):585-90 PMID: 20234320
  57. Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer.
    Lung Cancer. 2002 Jan;35(1):23-8 PMID: 11750709
  58. Prognostic significance of mature dendritic cells and factors associated with their accumulation in metastatic liver tumors from colorectal cancer.
    Hum Pathol. 2004 Nov;35(11):1392-6 PMID: 15668897
  59. Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection.
    J Clin Oncol. 2007 Jun 20;25(18):2586-93 PMID: 17577038
  60. Prognostic significance of macrophage infiltration in leiomyosarcomas.
    Clin Cancer Res. 2008 Mar 1;14(5):1423-30 PMID: 18316565
  61. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation.
    J Leukoc Biol. 2009 Nov;86(5):1065-73 PMID: 19741157
  62. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma.
    Cancer. 1997 Jun 15;79(12):2320-8 PMID: 9191519
  63. Prognostic significance of activated CD8(+) T cell infiltrations within esophageal carcinomas.
    Cancer Res. 2001 May 15;61(10):3932-6 PMID: 11358808
  64. Prognostic value of intratumoral neutrophils in advanced gastric carcinoma in a high-risk area in northern Italy.
    Mod Pathol. 2002 Aug;15(8):831-7 PMID: 12181268
  65. Characterization of macrophage subpopulations in colon cancer using tissue microarrays.
    Histopathology. 2005 May;46(5):515-21 PMID: 15842633
  66. Phase 2 study of neoadjuvant treatment with NOV-002 in combination with doxorubicin and cyclophosphamide followed by docetaxel in patients with HER-2 negative clinical stage II-IIIc breast cancer.
    Breast Cancer Res Treat. 2012 Feb;132(1):215-23 PMID: 22138748
  67. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells.
    Blood. 2011 Aug 25;118(8):2254-65 PMID: 21734236
  68. Immunological monitoring of the tumor immunoenvironment for clinical trials.
    Cancer Immunol Immunother. 2012 Feb;61(2):239-247 PMID: 22080408
  69. Human small cell lung carcinoma and carcinoid tumor regulate dendritic cell maturation and function.
    Mod Pathol. 2001 Jan;14(1):40-5 PMID: 11211308
  70. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer.
    Clin Cancer Res. 2008 Aug 15;14(16):5220-7 PMID: 18698040
  71. Tumor-associated tissue eosinophilia in human esophageal squamous cell carcinoma.
    Anticancer Res. 2006 Mar-Apr;26(2B):1419-24 PMID: 16619553
  72. Independent prognostic value of eosinophil and mast cell infiltration in colorectal cancer tissue.
    J Pathol. 1999 Dec;189(4):487-95 PMID: 10629548
  73. Prognostic value of intratumoral natural killer cells in gastric carcinoma.
    Cancer. 2000 Feb 1;88(3):577-83 PMID: 10649250
  74. Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma.
    Neuro Oncol. 2011 Jun;13(6):591-9 PMID: 21636707
  75. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients.
    Clin Cancer Res. 2009 Mar 15;15(6):2148-57 PMID: 19276286
  76. CD1a-positive infiltrating-dendritic cell density and 5-year survival from human breast cancer.
    Br J Cancer. 2003 Aug 4;89(3):533-8 PMID: 12888826
  77. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy.
    Cancer Immunol Immunother. 2009 Jan;58(1):49-59 PMID: 18446337
  78. FOXP3+ cell density in primary tumor has no prognostic impact in patients with cutaneous malignant melanoma.
    Pathol Oncol Res. 2010 Sep;16(3):303-9 PMID: 20306313
  79. Dendritic cell density and activation status in human breast cancer -- CD1a, CMRF-44, CMRF-56 and CD-83 expression.
    Br J Cancer. 2002 Feb 12;86(4):546-51 PMID: 11870535
  80. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival.
    Nat Med. 2004 Sep;10(9):942-9 PMID: 15322536
  81. Enhanced functionality of CD4+CD25(high)FoxP3+ regulatory T cells in the peripheral blood of patients with prostate cancer.
    Clin Cancer Res. 2008 Feb 15;14(4):1032-40 PMID: 18281535
  82. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction.
    J Clin Oncol. 2011 Feb 20;29(6):610-8 PMID: 21245428
  83. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells.
    J Immunol. 2004 Jul 15;173(2):1444-53 PMID: 15240741
  84. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18538-43 PMID: 16344461
  85. Significance of M2-polarized tumor-associated macrophage in pancreatic cancer.
    J Surg Res. 2011 May 15;167(2):e211-9 PMID: 19765725
  86. Distinct role of macrophages in different tumor microenvironments.
    Cancer Res. 2006 Jan 15;66(2):605-12 PMID: 16423985
  87. Tumor microenvironment: a main actor in the metastasis process.
    Clin Exp Metastasis. 2012 Apr;29(4):381-95 PMID: 22322279
  88. Distribution of tumor-infiltrating dendritic cells in human non-small cell lung carcinoma in relation to apoptosis.
    Pathol Int. 2004 May;54(5):302-10 PMID: 15086834
  89. Dendritic cell infiltration and prognosis of early stage breast cancer.
    Clin Cancer Res. 2004 Nov 15;10(22):7466-74 PMID: 15569976
  90. Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth.
    Cancer Immunol Immunother. 2012 Sep;61(9):1373-85 PMID: 22215137
  91. Increased intratumoral neutrophil in colorectal carcinomas correlates closely with malignant phenotype and predicts patients' adverse prognosis.
    PLoS One. 2012;7(1):e30806 PMID: 22295111
  92. Phenotypic characterisation of the dendritic cell infiltrate in prostate cancer.
    J Urol. 1998 Jul;160(1):214-9 PMID: 9628653
  93. Tumor-infiltrating macrophages and dendritic cells in human colorectal cancer: relation to local regulatory T cells, systemic T-cell response against tumor-associated antigens and survival.
    J Transl Med. 2007 Nov 29;5:62 PMID: 18047662
  94. Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma.
    J Clin Oncol. 2009 Oct 1;27(28):4709-17 PMID: 19720929
  95. Prognostic value of intratumoral CD8+ T lymphocyte in extrahepatic bile duct carcinoma as essential immune response.
    J Surg Oncol. 2003 Dec;84(4):224-8 PMID: 14756433
  96. Expression of Foxp3 in non-small cell lung cancer patients is significantly higher in tumor tissues than in normal tissues, especially in tumors smaller than 30 mm.
    Oncol Rep. 2006 May;15(5):1315-9 PMID: 16596204
  97. Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors.
    Am J Pathol. 2010 Apr;176(4):1564-76 PMID: 20167863
  98. Gastric carcinoma with prominent neutrophil infiltration.
    Histopathology. 2000 Sep;37(3):289-90 PMID: 10971710
  99. Dual role of immunomodulation by anticancer chemotherapy.
    Nat Med. 2013 Jan;19(1):20-2 PMID: 23296003
  100. High expression of CD20+ lymphocytes in soft tissue sarcomas is a positive prognostic indicator.
    Oncoimmunology. 2012 Jan 1;1(1):75-77 PMID: 22720216
  101. CD14(+)S100A9(+) monocytic myeloid-derived suppressor cells and their clinical relevance in non-small cell lung cancer.
    Am J Respir Crit Care Med. 2012 Nov 15;186(10):1025-36 PMID: 22955317
  102. Cytotoxic markers and frequency predict functional capacity of natural killer cells infiltrating renal cell carcinoma.
    Clin Cancer Res. 2006 Feb 1;12(3 Pt 1):718-25 PMID: 16467081
  103. Higher intratumoral infiltrated Foxp3+ Treg numbers and Foxp3+/CD8+ ratio are associated with adverse prognosis in resectable gastric cancer.
    J Cancer Res Clin Oncol. 2010 Oct;136(10):1585-95 PMID: 20221835
  104. Granzyme B produced by human plasmacytoid dendritic cells suppresses T-cell expansion.
    Blood. 2010 Feb 11;115(6):1156-65 PMID: 19965634
  105. CD4+ T cells in cancer stroma, not CD8+ T cells in cancer cell nests, are associated with favorable prognosis in human non-small cell lung cancers.
    Cancer Sci. 2003 Nov;94(11):1003-9 PMID: 14611679
  106. The number and microlocalization of tumor-associated immune cells are associated with patient's survival time in non-small cell lung cancer.
    BMC Cancer. 2010 May 20;10:220 PMID: 20487543
  107. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes.
    Cancer Res. 2009 Feb 15;69(4):1553-60 PMID: 19201693
  108. Neutrophils: key mediators of tumour angiogenesis.
    Int J Exp Pathol. 2009 Jun;90(3):222-31 PMID: 19563607
  109. New vistas on macrophage differentiation and activation.
    Eur J Immunol. 2007 Jan;37(1):14-6 PMID: 17183610
  110. Myometrial invasion and lymph node metastasis in endometrioid carcinomas: tumor-associated macrophages, microvessel density, and HIF1A have a crucial role.
    Am J Surg Pathol. 2010 Nov;34(11):1708-14 PMID: 20962622
  111. Immune infiltration in human cancer: prognostic significance and disease control.
    Curr Top Microbiol Immunol. 2011;344:1-24 PMID: 20512556
  112. Cancer dormancy: a model of early dissemination and late cancer recurrence.
    Clin Cancer Res. 2012 Feb 1;18(3):645-53 PMID: 22156560
  113. Inflammatory cell infiltration of tumors: Jekyll or Hyde.
    Cancer Metastasis Rev. 2007 Dec;26(3-4):373-400 PMID: 17717638
  114. Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome.
    Am J Pathol. 1998 Jan;152(1):83-92 PMID: 9422526
  115. Intratumoral CD8(+) T/FOXP3 (+) cell ratio is a predictive marker for survival in patients with colorectal cancer.
    Cancer Immunol Immunother. 2010 May;59(5):653-61 PMID: 19908042
  116. Prognostic significance of CD83 positive, mature dendritic cells in the gallbladder carcinoma.
    Oncol Rep. 2005 Aug;14(2):353-6 PMID: 16012714
  117. Dendritic cell infiltration and prognosis of human hepatocellular carcinoma.
    J Cancer Res Clin Oncol. 2006 May;132(5):293-301 PMID: 16421755
  118. Prognostic impact of lymphocytes in soft tissue sarcomas.
    PLoS One. 2011 Jan 27;6(1):e14611 PMID: 21298041
  119. Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review.
    J Pathol. 2010 Dec;222(4):350-66 PMID: 20927778
  120. Tumor-infiltrating regulatory dendritic cells inhibit CD8+ T cell function via L-arginine metabolism.
    Cancer Res. 2009 Apr 1;69(7):3086-94 PMID: 19293186
  121. Recruitment of immature plasmacytoid dendritic cells (plasmacytoid monocytes) and myeloid dendritic cells in primary cutaneous melanomas.
    J Pathol. 2003 Jun;200(2):255-68 PMID: 12754747
  122. Prognostic value of CD83-positive mature dendritic cells and their relation to vascular endothelial growth factor in advanced human gastric cancer.
    Oncol Rep. 2005 Aug;14(2):369-75 PMID: 16012717
  123. Prognostic markers in resectable non-small cell lung cancer: a multivariate analysis.
    Can J Surg. 2001 Jun;44(3):180-8 PMID: 11407827
  124. Tumour-educated macrophages promote tumour progression and metastasis.
    Nat Rev Cancer. 2004 Jan;4(1):71-8 PMID: 14708027
  125. Dendritic cells in human squamous cell carcinoma of the oral cavity.
    Anticancer Res. 2002 Mar-Apr;22(2A):545-57 PMID: 12014622
  126. Characteristics of CD4+CD25+ regulatory T cells in the peripheral circulation of patients with head and neck cancer.
    Br J Cancer. 2005 Mar 14;92(5):913-20 PMID: 15714205
  127. Concurrent infiltration by CD8+ T cells and CD4+ T cells is a favourable prognostic factor in non-small-cell lung carcinoma.
    Br J Cancer. 2006 Jan 30;94(2):275-80 PMID: 16421594
  128. CD4+ and CD8+ T cells cooperate to improve prognosis of patients with esophageal squamous cell carcinoma.
    Cancer Res. 2003 Apr 1;63(7):1555-9 PMID: 12670904
  129. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma.
    J Immunol. 2002 Sep 1;169(5):2756-61 PMID: 12193750
  130. Intratumoral CD8+ T lymphocytes as a prognostic factor of survival in endometrial carcinoma.
    Clin Cancer Res. 2004 Jul 1;10(13):4450-6 PMID: 15240536
  131. Behavior of circulating CD4+CD25+Foxp3+ regulatory T cells in colon cancer patients undergoing surgery.
    J Clin Immunol. 2011 Dec;31(6):1095-104 PMID: 21915633
  132. Utility of tumour-infiltrating CD25+FOXP3+ regulatory T cell evaluation in predicting local recurrence in vertical growth phase cutaneous melanoma.
    Oncol Rep. 2007 Nov;18(5):1115-22 PMID: 17914561
  133. Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity.
    Cancer Immunol Immunother. 2010 Oct;59(10):1593-600 PMID: 20414655
  134. Increased prevalence of regulatory T cells (Treg) is induced by pancreas adenocarcinoma.
    J Immunother. 2006 Jul-Aug;29(4):416-24 PMID: 16799337
  135. Tumor-infiltrating dendritic cells in adenocarcinomas of the breast: a study of 143 neoplasms with a correlation to usual prognostic factors and to clinical outcome.
    Int J Cancer. 1999 Jun 21;84(3):309-14 PMID: 10371352
  136. The number of intratumoral dendritic cells and zeta-chain expression in T cells as prognostic and survival biomarkers in patients with oral carcinoma.
    Cancer. 2001 Jun 1;91(11):2136-47 PMID: 11391595
  137. Coordinated regulation of myeloid cells by tumours.
    Nat Rev Immunol. 2012 Mar 22;12(4):253-68 PMID: 22437938
  138. In melanoma changes of immature and mature dendritic cell expression correlate with tumor thickness:an immunohistochemical study.
    Int J Immunopathol Pharmacol. 2007 Apr-Jun;20(2):325-33 PMID: 17624244
Article Info
Journal
Cancer immunology, immunotherapy : CII
Abbr.
Cancer Immunol Immunother
ISSN
1432-0851
DOI
10.1007/s00262-013-1480-0
Email
[email protected]
Published
2014-01-00
Epub
2013-00-08
Pages
45-57
Language
English
Region
Germany
NLM ID
8605732
PMCID
PMC4018188
Subset
IM
Grants
NCI NIH HHS · R01 CA154369 · United States
External Links
PubMed source DOI: 10.1007/s00262-013-1480-0 PMC Full Text View journal details
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