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Immunologic Interpretation of Cancer Biology: Impact on Clinical Outcome

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The Tumor Immunoenvironment

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Abstract

The biology of tumors cannot be understood by simply studying the traits of the neoplastic cells in isolation. Instead, the contributions of the “tumor microenvironment” to tumor genesis must be considered. The complexity of the interaction between not transformed host cells with cancer cells and the molecular pathways involved in such interaction could be recently appreciated by high-throughput tools capable of providing a global view of biological processes. Based on this approach numerous studies have defined a new portrait of cancer, describing a linkage between the immune infiltrate, prognosis and response to therapy. Here, we provide an overview of the current status of the field describing the immune cells involved in this phenomenon. Molecular events and biomarkers associated with the favorable clinic outcome will be described, analyzing also commonalities and discrepancies among studies.

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References

  • Ahmadzadeh M, Johnson LA, Heemskerk B, Wunderlich JR, Dudley ME, White DE et al (2009) Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 114:44–1537

    Article  CAS  Google Scholar 

  • Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A et al (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403:11–503

    Article  CAS  Google Scholar 

  • Allavena P, Sica A, Solinas G, Porta C, Mantovani A (2008) The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev Oncol Hematol 66:1–9

    Article  PubMed  Google Scholar 

  • Andreu P, Johansson M, Affara NI, Pucci F, Tan T, Junankar S et al (2010) FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 17:121–134

    Article  PubMed  CAS  Google Scholar 

  • Ascierto ML, De Giorgi V, Liu Q, Bedognetti D, Spivey TL, Murtas D et al (2011) An immunologic portrait of cancer. J Transl Med 9:146

    Google Scholar 

  • Ascierto ML, Kmieciak M, Idowu MO, Manjili R, Zhao YD, Grimes M et al (2012) A signature of immune function genes associated with recurrence-free survival in breast cancer patients. Breast Cancer Res Tr 131:871–880

    Article  CAS  Google Scholar 

  • Badoual C, Hans S, Rodriguez J, Peyrard S, Klein C, Agueznay Nel H et al (2006) Prognostic value of tumor-infiltrating CD4 + T-cell subpopulations in head and neck cancers. Clin Cancer Res 12:72–465

    Article  CAS  Google Scholar 

  • Bedognetti D, Wang E, Sertoli MR, Marincola FM (2010) Gene-expression profiling in vaccine therapy and immunotherapy for cancer. Expert Rev Vaccines 9:65–555

    Article  Google Scholar 

  • Broussard EK, Disis ML (2011) TNM staging in colorectal cancer: T is for T cell and M is for memory. J Clin Oncol 29:601–603

    Article  PubMed  Google Scholar 

  • Carreras J, Lopez-Guillermo A, Fox BC, Colomo L, Martinez A, Roncador G et al (2006) High numbers of tumor-infiltrating FOXP3-positive regulatory T cells are associated with improved overall survival in follicular lymphoma. Blood 108:64–2957

    Article  CAS  Google Scholar 

  • Chaput N, Conforti R, Viaud S, Spatz A, Zitvogel L (2008) The Janus face of dendritic cells in cancer. Oncogene 27:5920–5931

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Wan J, Liu J, Xie W, Diao X, Xu J et al (2010) Increased IL-17-producing cells correlate with poor survival and lymphangiogenesis in NSCLC patients. Lung Cancer 69:348–354

    Article  PubMed  Google Scholar 

  • Clemente CG, Mihm MC Jr, Bufalino R, Zurrida S, Collini P, Cascinelli N (1996) Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 77:10–1303

    Article  Google Scholar 

  • Coca S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez MA, Vallejo C et al (1997) The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 79:2320–2328

    Article  PubMed  CAS  Google Scholar 

  • Cochran AJ (1969) Histology and prognosis in malignant melanoma. J Pathol 97:68–459

    Article  Google Scholar 

  • Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P et al (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10:9–942

    Article  CAS  Google Scholar 

  • De Monte L, Reni M, Tassi E, Clavenna D, Papa I, Recalde H et al (2011) Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J Exp Med 208:469–478

    Article  PubMed  CAS  Google Scholar 

  • Delahaye NF, Rusakiewicz S, Martins I, Menard C, Roux S, Lyonnet L et al (2011) Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med 17:700–707

    Article  PubMed  CAS  Google Scholar 

  • Disis ML (2010) Immune regulation of cancer. J Clin Oncol 28:8–4531

    Article  CAS  Google Scholar 

  • Donskov F, von der Maase H (2006) Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J Clin Oncol 24:1997–2005

    Article  PubMed  Google Scholar 

  • Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ et al (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298:850–854

    Article  PubMed  CAS  Google Scholar 

  • Eckl J, Buchner A, Prinz PU, Riesenberg R, Siegert SI, Kammerer R et al (2012) Transcript signature predicts tissue NK cell content and defines renal cell carcinoma subgroups independent of TNM staging. J Mol Med 90:55–66 (Berl)

    Article  PubMed  CAS  Google Scholar 

  • Emens LA, Silverstein SC, Khleif S, Marincola FM, Galon J (2012) Toward integrative cancer immunotherapy: targeting the tumor microenvironment. J Transl Med 10:70

    Article  PubMed  CAS  Google Scholar 

  • Frey DM, Droeser RA, Viehl CT, Zlobec I, Lugli A, Zingg U et al (2010) High frequency of tumor-infiltrating FOXP3(+) regulatory T cells predicts improved survival in mismatch repair-proficient colorectal cancer patients. Int J Cancer 126:2635–2643

    PubMed  CAS  Google Scholar 

  • Fridman WH, Pages F, Sautes-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12:298–306

    Article  PubMed  CAS  Google Scholar 

  • Gajewski TF (2011) Molecular profiling of melanoma and the evolution of patient-specific therapy. Semin Oncol 38:42–236

    Article  CAS  Google Scholar 

  • Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C et al (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313:4–1960

    Article  CAS  Google Scholar 

  • Galon J, Pages F, Marincola FM, Thurin M, Trinchieri G, Fox BA et al (2012) The immune score as a new possible approach for the classification of cancer. J Transl Med 3:10–11

    Google Scholar 

  • Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, Xiao YS et al (2007) Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 25:93–2586

    Article  Google Scholar 

  • Gogas H, Ioannovich J, Dafni U, Stavropoulou-Giokas C, Frangia K, Tsoutsos D et al (2006) Prognostic significance of autoimmunity during treatment of melanoma with interferon. N Engl J Med 354:709–718

    Article  PubMed  CAS  Google Scholar 

  • Guidoboni M, Gafa R, Viel A, Doglioni C, Russo A, Santini A et al (2001) Microsatellite instability and high content of activated cytotoxic lymphocytes identify colon cancer patients with a favorable prognosis. Am J Pathol 159:297–304

    Article  PubMed  CAS  Google Scholar 

  • Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70

    Article  PubMed  CAS  Google Scholar 

  • Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:74–646

    Article  CAS  Google Scholar 

  • Heimberger AB, Abou-Ghazal M, Reina-Ortiz C, Yang DS, Sun W, Qiao W et al (2008) Incidence and prognostic impact of FoxP3 + regulatory T cells in human gliomas. Clin Cancer Res 14:72–5166

    Article  Google Scholar 

  • Herberman RB, Nunn ME, Holden HT, Lavrin DH (1975) Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int J Cancer 16:230–239

    Article  PubMed  CAS  Google Scholar 

  • Hillen F, Baeten CI, van de Winkel A, Creytens D, van der Schaft DW, Winnepenninckx V et al (2008) Leukocyte infiltration and tumor cell plasticity are parameters of aggressiveness in primary cutaneous melanoma. Cancer Immunol Immunother 57:97–106

    Article  PubMed  Google Scholar 

  • Hoffmann P, Boeld TJ, Eder R, Huehn J, Floess S, Wieczorek G et al (2009) Loss of FOXP3 expression in natural human CD4 + CD25 + regulatory T cells upon repetitive in vitro stimulation. Eur J Immunol 39:1088–1097

    Article  PubMed  CAS  Google Scholar 

  • Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Che X, Iwashige H et al (2000) Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 88:577–583

    Article  PubMed  CAS  Google Scholar 

  • Ito T, Saga S, Nagayoshi S, Imai M, Aoyama A, Yokoi T et al (1986) Class distribution of immunoglobulin-containing plasma cells in the stroma of medullary carcinoma of breast. Breast Cancer Res Treat 7:97–103

    Article  PubMed  CAS  Google Scholar 

  • Jensen TO, Schmidt H, Moller HJ, Donskov F, Hoyer M, Sjoegren P et al (2012) Intratumoral neutrophils and plasmacytoid dendritic cells indicate poor prognosis and are associated with pSTAT3 expression in AJCC stage I/II melanoma. Cancer 118(9):2476–2485

    Article  PubMed  CAS  Google Scholar 

  • Jochems C, Schlom J (2011) Tumor-infiltrating immune cells and prognosis: the potential link between conventional cancer therapy and immunity. Exp Biol Med 236:567–579 (Maywood)

    Article  CAS  Google Scholar 

  • Kelley T, Beck R, Absi A, Jin T, Pohlman B, Hsi E (2007) Biologic predictors in follicular lymphoma: importance of markers of immune response. Leuk Lymphoma 48:2403–2411

    Article  PubMed  Google Scholar 

  • Kiessling R, Klein E, Pross H, Wigzell H (1975) “Natural” killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 5:117–121

    Article  PubMed  CAS  Google Scholar 

  • Kryczek I, Wei S, Zou L, Zhu G, Mottram P, Xu H et al (2006) Cutting edge: induction of B7–H4 on APCs through IL-10: novel suppressive mode for regulatory T cells. J Immunol 177:40–44

    PubMed  CAS  Google Scholar 

  • Kryczek I, Banerjee M, Cheng P, Vatan L, Szeliga W, Wei S et al (2009) Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 114:1141–1149

    Article  PubMed  CAS  Google Scholar 

  • Lossos IS, Alizadeh AA, Eisen MB, Chan WC, Brown PO, Botstein D et al (2000) Ongoing immunoglobulin somatic mutation in germinal center B cell-like but not in activated B cell-like diffuse large cell lymphomas. Proc Natl Acad Sci U S A 97:13–10209

    Article  Google Scholar 

  • Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Lee AH, Ellis IO et al (2011) An evaluation of the clinical significance of FOXP3 + infiltrating cells in human breast cancer. Breast Cancer Res Treat 127:99–108

    Article  PubMed  CAS  Google Scholar 

  • Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R et al (2011) Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest 121:3609–3622

    Article  PubMed  CAS  Google Scholar 

  • Mantovani A, Romero P, Palucka AK, Marincola FM (2008) Tumour immunity: effector response to tumour and role of the microenvironment. Lancet 371:83–771

    Article  CAS  Google Scholar 

  • Marincola FM (2005) A balanced review of the status T cell-based therapy against cancer. J Transl Med 3:16

    Google Scholar 

  • Martuza RL, Malick A, Markert JM, Ruffner KL, Coen DM (1991) Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science 252:854–856

    Article  PubMed  CAS  Google Scholar 

  • Masferrer JL, Leahy KM, Koki AT, Zweifel BS, Settle SL, Woerner BM et al (2000) Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors. Cancer Res 60:11–1306

    Google Scholar 

  • Milne K, Kobel M, Kalloger SE, Barnes RO, Gao D, Gilks CB et al (2009) Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLoS ONE 4:e6412

    Article  PubMed  CAS  Google Scholar 

  • Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T et al (2011) Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 29:610–618

    Article  PubMed  Google Scholar 

  • Mocellin S, Panelli MC, Wang E, Nagorsen D, Marincola FM (2003) The dual role of IL-10. Trends Immunol 24:36–43

    Article  PubMed  CAS  Google Scholar 

  • Mocellin S, Panelli M, Wang E, Rossi CR, Pilati P, Nitti D et al (2004) IL-10 stimulatory effects on human NK cells explored by gene profile analysis. Genes Immun 5:621–630

    Article  PubMed  CAS  Google Scholar 

  • Moretta L, Moretta A (2004) Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J 23:255–259

    Article  PubMed  CAS  Google Scholar 

  • Moretta L, Ciccone E, Mingari MC, Biassoni R, Moretta A (1994) Human natural killer cells: origin, clonality, specificity, and receptors. Adv Immunol 55:341–380

    Article  PubMed  CAS  Google Scholar 

  • Nielsen JS, Sahota RA, Milne K, Kost SE, Nesslinger NJ, Watson PH et al (2012) CD20 + tumor-infiltrating lymphocytes have an atypical CD27- memory phenotype and together with CD8 + T cells promote favorable prognosis in ovarian cancer. Clin Cancer Res 18:3281–3292

    Article  PubMed  CAS  Google Scholar 

  • Oldham RK, Herberman RB (1973) Evaluation of cell-mediated cytotoxic reactivity against tumor associated antigens with 125I-iododeoxyuridine labeled target cells. J Immunol 111:862–871

    PubMed  CAS  Google Scholar 

  • Ostrand-Rosenberg S, Sinha P (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182:4499–4506

    Article  PubMed  CAS  Google Scholar 

  • Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R et al (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353:66–2654

    Article  Google Scholar 

  • Pages F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G et al (2009) In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 27:5944–5951

    Article  PubMed  CAS  Google Scholar 

  • Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA et al (2000) Molecular portraits of human breast tumours. Nature 406:52–747

    Article  Google Scholar 

  • Qiu X, Zhu X, Zhang L, Mao Y, Zhang J, Hao P et al (2003) Human epithelial cancers secrete immunoglobulin g with unidentified specificity to promote growth and survival of tumor cells. Cancer Res 63:6488–6495

    PubMed  CAS  Google Scholar 

  • Rossi CR, Testori A, Mocellin S, Campana L, Lejeune F (2004) Melanoma—what is new in sentinel node biopsy and locoregional treatments in 2003? Report of a workshop at the third research meeting on Melanoma, Milan, Italy, May 2003. Melanoma Res 14:329–332

    Article  PubMed  Google Scholar 

  • Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D et al (2009) Tumor-infiltrating FOXP3 + T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 27:186–192

    Article  PubMed  Google Scholar 

  • Schmidt M, Hellwig B, Hammad S, Othman A, Lohr M, Chen Z et al (2012) A comprehensive analysis of human gene expression profiles identifies stromal immunoglobulin kappa C as a compatible prognostic marker in human solid tumors. Clin Cancer Res 18:2695–2703

    Article  PubMed  CAS  Google Scholar 

  • Schreck S, Friebel D, Buettner M, Distel L, Grabenbauer G, Young LS et al (2009) Prognostic impact of tumour-infiltrating Th2 and regulatory T cells in classical Hodgkin lymphoma. Hematol Oncol 27:31–39

    Article  PubMed  CAS  Google Scholar 

  • Schwartzentruber DJ, Lawson DH, Richards JM, Conry RM, Miller DM, Treisman J et al (2011) Gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med 364:2119–2127

    Article  PubMed  CAS  Google Scholar 

  • Shanker A, Marincola FM (2011) Cooperativity of adaptive and innate immunity: implications for cancer therapy. Cancer Immunol Immunother 60:1061–1074

    Article  PubMed  CAS  Google Scholar 

  • Shanker A, Verdeil G, Buferne M, Inderberg-Suso EM, Puthier D, Joly F et al (2007) CD8 T cell help for innate antitumor immunity. J Immunol 179:6651–6662

    PubMed  CAS  Google Scholar 

  • Shanker A, Buferne M, Schmitt-Verhulst AM (2010) Cooperative action of CD8 T lymphocytes and natural killer cells controls tumour growth under conditions of restricted T-cell receptor diversity. Immunology 129:41–54

    Article  PubMed  CAS  Google Scholar 

  • Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S (2007) Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 67:13–4507

    Article  CAS  Google Scholar 

  • Tassi E, Gavazzi F, Albarello L, Senyukov V, Longhi R, Dellabona P et al (2008) Carcinoembryonic antigen-specific but not antiviral CD4 + T cell immunity is impaired in pancreatic carcinoma patients. J Immunol 181:6595–6603

    PubMed  CAS  Google Scholar 

  • Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G et al (2011) Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res 71:1263–1271

    Article  PubMed  CAS  Google Scholar 

  • Uccellini L, De Giorgi V, Zhao Y, Tumaini B, Erdenebileg N, Dudley ME et al (2012) IRF5 gene polymorphisms in melanoma. J Transl Med 10:170

    Article  PubMed  CAS  Google Scholar 

  • Villegas FR, Coca S, Villarrubia VG, Jimenez R, Chillon MJ, Jareno J et al (2002) Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 35:23–28

    Article  PubMed  Google Scholar 

  • Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL et al (2011) Innate or adaptive immunity? The example of natural killer cells. Science 331:44–49

    Article  PubMed  CAS  Google Scholar 

  • Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L (2012) Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 12:239–252

    Article  PubMed  CAS  Google Scholar 

  • Walker MR, Kasprowicz DJ, Gersuk VH, Benard A, Van Landeghen M, Buckner JH et al (2003) Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4 + CD25- T cells. J Clin Invest 112:1437–1443

    PubMed  CAS  Google Scholar 

  • Wang E, Worschech A, Marincola FM (2008) The immunologic constant of rejection. Trends Immunol 29:62–256

    Article  CAS  Google Scholar 

  • Wang XY, Han M, Xiao ZP, Chen L, Kong LH, Fu K et al (2009) The comparison of CD4(+);CD25(high); Foxp3(+); regulatory T cells between neonatal cord blood and adult peripheral blood. Bao X, Yu Fen Zi Mian Yi Xue Za Zhi. 25:1152–1154

    Google Scholar 

  • Wang E, Uccellini L, Marincola FM (2012) A genetic inference on cancer immune responsiveness. Oncoimmunology 1:520–525

    Article  PubMed  Google Scholar 

  • Wilke CM, Kryczek I, Wei S, Zhao E, Wu K, Wang G et al (2011) Th17 cells in cancer: help or hindrance? Carcinogenesis 32:643–649

    Article  PubMed  CAS  Google Scholar 

  • Wong SC, Puaux AL, Chittezhath M, Shalova I, Kajiji TS, Wang X et al (2010) Macrophage polarization to a unique phenotype driven by B cells. Eur J Immunol 40:2296–2307

    Article  PubMed  CAS  Google Scholar 

  • Worschech A, Chen N, Yu YA, Zhang Q, Pos Z, Weibel S et al (2009) Systemic treatment of xenografts with vaccinia virus GLV-1h68 reveals the immunologic facet of oncolytic therapy. BMC Genomics 10:301

    Article  PubMed  CAS  Google Scholar 

  • Yoon NK, Maresh EL, Shen D, Elshimali Y, Apple S, Horvath S et al (2010) Higher levels of GATA3 predict better survival in women with breast cancer. Hum Pathol 41:1794–1801

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G et al (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348:13–203

    Article  Google Scholar 

  • Zhang JP, Yan J, Xu J, Pang XH, Chen MS, Li L et al (2009) Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients. J Hepatol 50:980–989

    Article  PubMed  CAS  Google Scholar 

  • Zhu XD, Zhang JB, Zhuang PY, Zhu HG, Zhang W, Xiong YQ et al (2008) High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J Clin Oncol 26:2707–2716

    Article  PubMed  Google Scholar 

  • Zuo T, Wang L, Morrison C, Chang X, Zhang H, Li W et al (2007) FOXP3 is an X-linked breast cancer suppressor gene and an important repressor of the HER-2/ErbB2 oncogene. Cell 129:1275–1286

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Researcher in the Infectious Disease and Immunogenetics Section (FM Marincola’s laboratory) are supported by NIH Intramural Research Program. ML Ascierto thanks Dr. Ermelinda Ascierto and Dr. Domenico Ascierto for insightful suggestions.

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Authors and Affiliations

  1. National Institutes of Health, Building 10, Room 1N224, 10 Center Drive, Bethesda, MD, 20892, USA

    Maria Libera Ascierto & Ena Wang

  2. Infectious Disease and Immunogenetics Section (IDIS), Department of Transfusion Medicine, Clinical Center and Trans-NIH Center for Human Immunology (CHI), National Institutes of Health, Bethesda, MD, 20892, USA

    Maria Libera Ascierto, Francesco M. Marincola & Ena Wang

  3. Department of Internal Medicine, University of Genoa, Genoa, Italy

    Maria Libera Ascierto

Authors
  1. Maria Libera Ascierto
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  2. Francesco M. Marincola
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  3. Ena Wang
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Correspondence to Maria Libera Ascierto or Ena Wang .

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Editors and Affiliations

  1. Department of Pathology, University of Pittsburgh Medical Center, 3550 Terrace Street Scaife Hal, Pittsburgh, 15213, Pennsylvania, USA

    Michael R. Shurin

  2. , Clinical Cooperation Unit Dermato-Oncolo, German Cancer Research Center, Im Neuenheimer Feld 280, Heidelberg, 69120, Germany

    Viktor Umansky

  3. , SAIC-Frederick, Inc., National Cancer Institute at Frederick, Post Office B, Frederick, 21702, Maryland, USA

    Anatoli Malyguine

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Ascierto, M.L., Marincola, F.M., Wang, E. (2013). Immunologic Interpretation of Cancer Biology: Impact on Clinical Outcome. In: Shurin, M., Umansky, V., Malyguine, A. (eds) The Tumor Immunoenvironment. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6217-6_4

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