Skip to main content

Advertisement

SpringerLink
Log in

Immune-suppressive properties of the tumor microenvironment

  • Review
  • Published:
Cancer Immunology, Immunotherapy Aims and scope Submit manuscript

Abstract

Solid tumors are more than an accumulation of cancer cells. Indeed, cancerous cells create a permissive microenvironment by exploiting non-transformed host cells. Thus, solid tumors rather resemble abnormal organs composed of the cancerous cells itself and the stroma providing the supportive framework. The stroma can be divided into the extracellular matrix consisting of proteoglycans, hyaluronic acid, and fibrous proteins, as well as stromal cells including mesenchymal and immune cells; moreover, it contains various peptide factors and metabolites. Here, we will focus on immune-modulating capacities of the tumor microenvironment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674. doi:10.1016/j.cell.2011.02.013

    Article  PubMed  CAS  Google Scholar 

  2. Pietras K, Östman A (2010) Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res 316:1324–1331. doi:10.1016/j.yexcr.2010.02.045

    Article  PubMed  CAS  Google Scholar 

  3. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860–867. doi:10.1038/nature01322

    Article  PubMed  CAS  Google Scholar 

  4. de Visser KE, Korets LV, Coussens LM (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7:411–423. doi:10.1016/j.ccr.2005.04.014

    Article  PubMed  Google Scholar 

  5. Colotta F, Allavena P, Sica A et al (2009) Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30:1073–1081. doi:10.1093/carcin/bgp127

    Article  PubMed  CAS  Google Scholar 

  6. Egeblad M, Nakasone ES, Werb Z (2010) Tumors as organs: complex tissues that interface with the entire organism. Dev Cell 18:884–901. doi:10.1016/j.devcel.2010.05.012

    Article  PubMed  CAS  Google Scholar 

  7. Rosenberg SA (2012) Raising the bar: the curative potential of human cancer immunotherapy. Sci Transl Med 4:127ps8. doi:10.1126/scitranslmed.3003634

    Article  PubMed  Google Scholar 

  8. Kerkar SP, Restifo NP (2012) Cellular constituents of immune escape within the tumor microenvironment. Cancer Res 72:3125–3130. doi:10.1158/0008-5472.CAN-11-4094

    Article  PubMed  CAS  Google Scholar 

  9. Bronte V, Mocellin S (2009) Suppressive influences in the immune response to cancer. J Immunother 32:1–11. doi:10.1097/CJI.0b013e3181837276

    Article  PubMed  Google Scholar 

  10. Andersen MH, Schrama D, thor Straten P, Becker JC (2006) PS_JID_5700001.indd. J Invest Dermatol 126:32–41. doi:10.1038/sj.jid.5700001

    Article  PubMed  CAS  Google Scholar 

  11. Hajishengallis G, Chavakis T (2013) Endogenous modulators of inflammatory cell recruitment. Trends Immunol 34:1–6. doi:10.1016/j.it.2012.08.003

    Article  PubMed  CAS  Google Scholar 

  12. Brennan PJ, Brigl M, Brenner MB (2013) Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 13:101–117. doi:10.1038/nri3369

    Article  PubMed  CAS  Google Scholar 

  13. Mantovani A (2009) The yin-yang of tumor-associated neutrophils. Cancer Cell 16:173–174. doi:10.1016/j.ccr.2009.08.014

    Article  PubMed  CAS  Google Scholar 

  14. Matzinger P, Kamala T (2011) Tissue-based class control: the other side of tolerance. Nat Rev Immunol 11:221–230. doi:10.1038/nri2940

    Article  PubMed  CAS  Google Scholar 

  15. Hofmann UB, Houben R, Bröcker E-B, Becker JC (2005) Role of matrix metalloproteinases in melanoma cell invasion. Biochimie 87:307–314. doi:10.1016/j.biochi.2005.01.013

    Article  PubMed  CAS  Google Scholar 

  16. Yu Q, Stamenkovic I (2000) Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Gen Dev 14:163–176

    Google Scholar 

  17. Sheu BC, Hsu SM, Ho HN et al (2001) A novel role of metalloproteinase in cancer-mediated immunosuppression. Cancer Res 61:237–242

    PubMed  CAS  Google Scholar 

  18. Boutet P, Agüera-González S, Atkinson S et al (2009) Cutting edge: the metalloproteinase ADAM17/TNF-alpha-converting enzyme regulates proteolytic shedding of the MHC class I-related chain B protein. J Immunol 182:49–53

    PubMed  CAS  Google Scholar 

  19. Scheller J, Chalaris A, Garbers C, Rose-John S (2011) ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol 32:380–387. doi:10.1016/j.it.2011.05.005

    Article  PubMed  CAS  Google Scholar 

  20. Godefroy E, Manches O, Dréno B et al (2011) Matrix metalloproteinase-2 conditions human dendritic cells to prime inflammatory TH2 cells via an IL-12- and OX40L-dependent pathway. Cancer Cell 19:333–346. doi:10.1016/j.ccr.2011.01.037

    Article  PubMed  CAS  Google Scholar 

  21. Godin-Ethier J, Hanafi LA, Piccirillo CA, Lapointe R (2011) Indoleamine 2,3-dioxygenase expression in human cancers: clinical and immunologic perspectives. Clin Cancer Res 17:6985–6991. doi:10.1158/1078-0432.CCR-11-1331

    Article  PubMed  CAS  Google Scholar 

  22. Platten M, Wick W, Van den Eynde BJ (2012) Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion. Cancer Res 72:5435–5440. doi:10.1158/0008-5472.CAN-12-0569

    Article  PubMed  CAS  Google Scholar 

  23. Zou W, Restifo NP (2010) TH17 cells in tumour immunity and immunotherapy. Nat Rev Immunol 10:248–256. doi:10.1038/nri2742

    Article  PubMed  CAS  Google Scholar 

  24. Weinlich G, Murr C, Richardsen L et al (2007) Decreased serum tryptophan concentration predicts poor prognosis in malignant melanoma patients. Dermatology 214:8–14. doi:10.1159/000096906

    Article  PubMed  Google Scholar 

  25. Smith C, Chang MY, Parker KH et al (2012) IDO is a nodal pathogenic driver of lung cancer and metastasis development. Cancer Discov 2:722–735. doi:10.1158/2159-8290.CD-12-0014

    Article  PubMed  CAS  Google Scholar 

  26. Andersen MH (2012) The specific targeting of immune regulation: T-cell responses against indoleamine 2,3-dioxygenase. Cancer Immunol Immunother 61:1289–1297. doi:10.1007/s00262-012-1234-4

    Article  PubMed  CAS  Google Scholar 

  27. Pilotte L, Larrieu P, Stroobant V et al (2012) Reversal of tumoral immune resistance by inhibition of tryptophan 2,3-dioxygenase. Proc Nat Acad Sci 109:2497–2502. doi:10.1073/pnas.1113873109

    Article  PubMed  CAS  Google Scholar 

  28. Nowak EC, de Vries VC, Wasiuk A et al (2012) Tryptophan hydroxylase-1 regulates immune tolerance and inflammation. J Exp Med 209:2127–2135. doi:10.1084/jem.20120408

    Article  PubMed  CAS  Google Scholar 

  29. Bronte V, Zanovello P (2005) Regulation of immune responses by l-arginine metabolism. Nat Rev Immunol 5:641–654. doi:10.1038/nri1668

    Article  PubMed  CAS  Google Scholar 

  30. Rundhaug JE, Simper MS, Surh I, Fischer SM (2011) The role of the EP receptors for prostaglandin E2 in skin and skin cancer. Cancer Metastasis Rev 30:465–480. doi:10.1007/s10555-011-9317-9

    Article  PubMed  CAS  Google Scholar 

  31. Chouaib S, Messai Y, Couve S et al (2012) Hypoxia promotes tumor growth in linking angiogenesis to immune escape. Front Immunol 3:21. doi:10.3389/fimmu.2012.00021

    Article  PubMed  Google Scholar 

  32. Wink DA, Hines HB, Cheng RYS et al (2011) Nitric oxide and redox mechanisms in the immune response. J Leuk Biol 89:873–891. doi:10.1189/jlb.1010550

    Article  CAS  Google Scholar 

  33. Jayaraman P, Parikh F, Lopez-Rivera E et al (2012) Tumor-expressed inducible nitric oxide synthase controls induction of functional myeloid-derived suppressor cells through modulation of vascular endothelial growth factor release. J Immunol 188:5365–5376. doi:10.4049/jimmunol.1103553

    Article  PubMed  CAS  Google Scholar 

  34. Singer K, Gottfried E, Kreutz M, Mackensen A (2011) Suppression of T-cell responses by tumor metabolites. Cancer Immunol Immunother 60:425–431. doi:10.1007/s00262-010-0967-1

    Article  PubMed  CAS  Google Scholar 

  35. Hirschhaeuser F, Sattler UGA, Mueller-Klieser W (2011) Lactate: a metabolic key player in cancer. Cancer Res 71:6921–6925. doi:10.1158/0008-5472.CAN-11-1457

    Article  PubMed  CAS  Google Scholar 

  36. Shime H, Yabu M, Akazawa T et al (2008) Tumor-secreted lactic acid promotes IL-23/IL-17 proinflammatory pathway. J Immunol 180:7175–7183

    PubMed  CAS  Google Scholar 

  37. Cham CM, Gajewski TF (2005) Glucose availability regulates IFN-gamma production and p70S6 kinase activation in CD8+ effector T cells. J Immunol 174:4670–4677

    PubMed  CAS  Google Scholar 

  38. Mandapathil M, Szczepanski MJ, Szajnik M et al (2010) Adenosine and prostaglandin E2 cooperate in the suppression of immune responses mediated by adaptive regulatory T cells. J Biol Chem 285:27571–27580. doi:10.1074/jbc.M110.127100

    Article  PubMed  CAS  Google Scholar 

  39. Stagg J, Smyth MJ (2010) Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29:5346–5358. doi:10.1038/onc.2010.292

    Article  PubMed  CAS  Google Scholar 

  40. Haskó G, Linden J, Cronstein B, Pacher P (2008) Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov 7:759–770. doi:10.1038/nrd2638

    Article  PubMed  Google Scholar 

  41. Waickman AT, Alme A, Senaldi L et al (2012) Enhancement of tumor immunotherapy by deletion of the A2A adenosine receptor. Cancer Immunol Immunother 61:917–926. doi:10.1007/s00262-011-1155-7

    Article  PubMed  CAS  Google Scholar 

  42. Su Y, Jackson EK, Gorelik E (2011) Receptor desensitization and blockade of the suppressive effects of prostaglandin E(2) and adenosine on the cytotoxic activity of human melanoma-infiltrating T lymphocytes. Cancer Immunol Immunother 60:111–122. doi:10.1007/s00262-010-0924-z

    Article  PubMed  CAS  Google Scholar 

  43. Häusler SFM, Montalbán del Barrio I, Strohschein J et al (2011) Ectonucleotidases CD39 and CD73 on OvCA cells are potent adenosine-generating enzymes responsible for adenosine receptor 2A-dependent suppression of T cell function and NK cell cytotoxicity. Cancer Immunol Immunother 60:1405–1418. doi:10.1007/s00262-011-1040-4

    Article  PubMed  Google Scholar 

  44. Kryczek I, Wu K, Zhao E et al (2011) IL-17+ regulatory T Cells in the microenvironments of chronic inflammation and cancer. J Immunol 186:4388–4395. doi:10.4049/jimmunol.1003251

    Article  PubMed  CAS  Google Scholar 

  45. Ryzhov S, Novitskiy SV, Goldstein AE et al (2011) Adenosinergic regulation of the expansion and immunosuppressive activity of CD11b+ Gr1+ Cells. J Immunol 187:6120–6129. doi:10.4049/jimmunol.1101225

    Article  PubMed  CAS  Google Scholar 

  46. Beavis PA, Stagg J, Darcy PK, Smyth MJ (2012) CD73: a potent suppressor of antitumor immune responses. Trends Immunol 33:231–237. doi:10.1016/j.it.2012.02.009

    Article  PubMed  CAS  Google Scholar 

  47. Jin D, Fan J, Wang L et al (2010) CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression. Cancer Res 70:2245–2255. doi:10.1158/0008-5472.CAN-09-3109

    Article  PubMed  CAS  Google Scholar 

  48. Garber K (2011) Beyond ipilimumab: new approaches target the immunological synapse. J Nat Cancer Inst 103:1079–1082. doi:10.1093/jnci/djr281

    Article  PubMed  CAS  Google Scholar 

  49. Cameron F, Whiteside G, Perry C (2011) Ipilimumab: first global approval. Drugs 71:1093–1104. doi:10.2165/11594010-000000000-00000

    Article  PubMed  Google Scholar 

  50. Callahan MK, Wolchok JD, Allison JP (2010) Anti-CTLA-4 antibody therapy: immune monitoring during clinical development of a novel immunotherapy. Semin Oncol 37:473–484. doi:10.1053/j.seminoncol.2010.09.001

    Article  PubMed  CAS  Google Scholar 

  51. Robert C, Thomas L, Bondarenko I et al (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364:2517–2526. doi:10.1056/NEJMoa1104621

    Article  PubMed  CAS  Google Scholar 

  52. Reck M, Bondarenko I, Luft A et al (2013) Ipilimumab in combination with paclitaxel and carboplatin as first-line therapy in extensive-disease-small-cell lung cancer: results from a randomized, double-blind, multicenter phase 2 trial. Ann Oncol 24:75–83. doi:10.1093/annonc/mds213

    Article  PubMed  CAS  Google Scholar 

  53. Di Giacomo AM, Ascierto PA, Pilla L et al (2012) Ipilimumab and fotemustine in patients with advanced melanoma (NIBIT-M1): an open-label, single-arm phase 2 trial. Lancet Oncol 13:879–886. doi:10.1016/S1470-2045(12)70324-8

    Article  PubMed  Google Scholar 

  54. Postow MA, Callahan MK, Barker CA et al (2012) Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 366:925–931. doi:10.1056/NEJMoa1112824

    Article  PubMed  CAS  Google Scholar 

  55. Santegoets SJAM, Stam AGM, Lougheed SM et al (2012) T cell profiling reveals high CD4(+)CTLA-4 (+) T cell frequency as dominant predictor for survival after prostate GVAX/ipilimumab treatment. Cancer Immunol Immunother. doi:10.1007/s00262-012-1330-5

    PubMed  Google Scholar 

  56. Hodis R, Watson IR, Kryukov GV et al (2012) A landscape of driver mutations in melanoma. Cell 150:251–263. doi:10.1016/j.cell.2012.06.024

    Article  PubMed  CAS  Google Scholar 

  57. Downey SG, Klapper JA, Smith FO et al (2007) Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade. Clin Cancer Res 13:6681–6688. doi:10.1158/1078-0432.CCR-07-0187

    Article  PubMed  CAS  Google Scholar 

  58. Liakou CI, Kamat A, Tang DN et al (2008) CTLA-4 blockade increases IFNgamma-producing CD4+ ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients. Proc Nat Acad Sci 105:14987–14992. doi:10.1073/pnas.0806075105

    Article  PubMed  CAS  Google Scholar 

  59. Ji R-R, Chasalow SD, Wang L et al (2012) An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother 61:1019–1031. doi:10.1007/s00262-011-1172-6

    Article  PubMed  CAS  Google Scholar 

  60. Hamid O, Schmidt H, Nissan A et al (2011) A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J Transl Med 9:204. doi:10.1186/1479-5876-9-204

    Article  PubMed  CAS  Google Scholar 

  61. Shahabi V, Whitney G, Hamid O et al (2012) Assessment of association between BRAF-V600E mutation status in melanomas and clinical response to ipilimumab. Cancer Immunol Immunother 61:733–737. doi:10.1007/s00262-012-1227-3

    Article  PubMed  CAS  Google Scholar 

  62. la Fuente de H, Cibrián D, Sánchez-Madrid F (2012) Immunoregulatory molecules are master regulators of inflammation during the immune response. FEBS Lett 586:2897–2905. doi:10.1016/j.febslet.2012.07.032

    Article  Google Scholar 

  63. Topalian SL, Hodi FS, Brahmer JR et al (2012) Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366:2443–2454. doi:10.1056/NEJMoa1200690

    Article  PubMed  CAS  Google Scholar 

  64. Brahmer JR, Tykodi SS, Chow LQM et al (2012) Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366:2455–2465. doi:10.1056/NEJMoa1200694

    Article  PubMed  CAS  Google Scholar 

  65. Hobo W, Novobrantseva TI, Fredrix H et al (2012) Improving dendritic cell vaccine immunogenicity by silencing PD-1 ligands using siRNA-lipid nanoparticles combined with antigen mRNA electroporation. Cancer Immunol Immunother. doi:10.1007/s00262-012-1334-1

    PubMed  Google Scholar 

  66. Seliger B, Quandt D (2012) The expression, function, and clinical relevance of B7 family members in cancer. Cancer Immunol Immunother 61:1327–1341. doi:10.1007/s00262-012-1293-6

    Article  PubMed  CAS  Google Scholar 

  67. Yi KH, Chen L (2009) Fine tuning the immune response through B7-H3 and B7-H4. Immunol Rev 229:145–151. doi:10.1111/j.1600-065X.2009.00768.x

    Article  PubMed  CAS  Google Scholar 

  68. Textor S, Fiegler N, Arnold A et al (2011) Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res 71:5998–6009. doi:10.1158/0008-5472.CAN-10-3211

    Article  PubMed  CAS  Google Scholar 

  69. Vetter CS, Groh V, thor Straten P et al (2002) Expression of stress-induced MHC class I related chain molecules on human melanoma. J Invest Dermatol 118:600–605. doi:10.1046/j.1523-1747.2002.01700.x

    Article  PubMed  CAS  Google Scholar 

  70. Champsaur M, Lanier LL (2010) Effect of NKG2D ligand expression on host immune responses. Immunol Rev 235:267–285. doi:10.1111/j.0105-2896.2010.00893.x

    PubMed  CAS  Google Scholar 

  71. Waldhauer I, Goehlsdorf D, Gieseke F et al (2008) Tumor-associated MICA is shed by ADAM proteases. Cancer Res 68:6368–6376. doi:10.1158/0008-5472.CAN-07-6768

    Article  PubMed  CAS  Google Scholar 

  72. Siemens DR, Hu N, Sheikhi AK et al (2008) Hypoxia increases tumor cell shedding of MHC class I chain-related molecule: role of nitric oxide. Cancer Res 68:4746–4753. doi:10.1158/0008-5472.CAN-08-0054

    Article  PubMed  CAS  Google Scholar 

  73. Barsoum IB, Hamilton TK, Li X et al (2011) Hypoxia induces escape from innate immunity in cancer cells via increased expression of ADAM10: role of nitric oxide. Cancer Res 71:7433–7441. doi:10.1158/0008-5472.CAN-11-2104

    Article  PubMed  CAS  Google Scholar 

  74. Pruessmeyer J, Ludwig A (2009) The good, the bad and the ugly substrates for ADAM10 and ADAM17 in brain pathology, inflammation and cancer. Semin Cell Dev Biol 20:164–174. doi:10.1016/j.semcdb.2008.09.005

    Article  PubMed  CAS  Google Scholar 

  75. Paschen A, Sucker A, Hill B et al (2009) Differential clinical significance of individual NKG2D ligands in melanoma: soluble ULBP2 as an indicator of poor prognosis superior to S100B. Clin Cancer Res 15:5208–5215. doi:10.1158/1078-0432.CCR-09-0886

    Article  PubMed  CAS  Google Scholar 

  76. Benitez AC, Dai Z, Mann HH et al (2011) Expression, signaling proficiency, and stimulatory function of the NKG2D lymphocyte receptor in human cancer cells. Proc Nat Acad Sci 108:4081–4086. doi:10.1073/pnas.1018603108

    Article  PubMed  CAS  Google Scholar 

  77. Rak J (2013) Extracellular vesicles—biomarkers and effectors of the cellular interactome in cancer. Front Pharmacol 4:21. doi:10.3389/fphar.2013.00021

    Article  PubMed  Google Scholar 

  78. Taylor DD, Doellgast GJ (1979) Quantitation of peroxidase-antibody binding to membrane fragments using column chromatography. Anal Biochem 98:53–59

    Article  PubMed  CAS  Google Scholar 

  79. Taylor DD, Gercel-Taylor C (2011) Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol 33:441–454. doi:10.1007/s00281-010-0234-8

    Article  PubMed  CAS  Google Scholar 

  80. Filipazzi P, Bürdek M, Villa A et al (2012) Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Sem Cancer Biol 22:342–349. doi:10.1016/j.semcancer.2012.02.005

    Article  CAS  Google Scholar 

  81. Huber V, Filipazzi P, Iero M et al (2008) More insights into the immunosuppressive potential of tumor exosomes. J Transl Med 6:63. doi:10.1186/1479-5876-6-63

    Article  PubMed  Google Scholar 

  82. van der Heyde HC, Gramaglia I, Combes V et al (2011) Flow cytometric analysis of microparticles. Methods Mol Biol 699:337–354. doi:10.1007/978-1-61737-950-5_16

    Article  PubMed  Google Scholar 

  83. Whiteside TL (2013) Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes). Biochem Soc Trans 41:245–251. doi:10.1042/BST20120265

    Article  PubMed  CAS  Google Scholar 

  84. Xiang X, Poliakov A, Liu C et al (2009) Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 124:2621–2633. doi:10.1002/ijc.24249

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of interest

Jürgen C. Becker is a paid Advisor for and Member of the Speakers Bureau of Bristol-Myers Squibb, Glaxo-Smith-Kline, Leo Pharma, and Novartis. All other authors do not have any conflict of interest.

Author information

Authors and Affiliations

  1. Department of General Dermatology, Medical University of Graz, Auenbruggerplatz 8, 8010, Graz, Austria

    Jürgen C. Becker & David Schrama

  2. Department of Hematology, Center for Cancer Immune Therapy (CCIT), University Hospital Herlev, Herlev Ringvej 75, 2730, Herlev, Denmark

    Mads Hald Andersen & Per thor Straten

Authors
  1. Jürgen C. Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mads Hald Andersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Schrama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Per thor Straten
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jürgen C. Becker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Becker, J.C., Andersen, M.H., Schrama, D. et al. Immune-suppressive properties of the tumor microenvironment. Cancer Immunol Immunother 62, 1137–1148 (2013). https://doi.org/10.1007/s00262-013-1434-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00262-013-1434-6

Keywords

Search

Navigation