Home LiteratureArticle Details
PMID: 25035953 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Tumor-associated macrophages: from mechanisms to therapy.

Immunity ·Vol. 41 ·No. 1 ·2014-07-17 ·Pages 49-61

Noy R, Pollard JW

Abstract

The tumor microenvironment is a complex ecology of cells that evolves with and provides support to tumor cells during the transition to malignancy. Among the innate and adaptive immune cells recruited to the tumor site, macrophages are particularly abundant and are present at all stages of tumor progression. Clinical studies and experimental mouse models indicate that these macrophages generally play a protumoral role. In the primary tumor, macrophages can stimulate angiogenesis and enhance tumor cell invasion, motility, and intravasation. During monocytes and/or metastasis, macrophages prime the premetastatic site and promote tumor cell extravasation, survival, and persistent growth. Macrophages are also immunosuppressive, preventing tumor cell attack by natural killer and T cells during tumor progression and after recovery from chemo- or immunotherapy. Therapeutic success in targeting these protumoral roles in preclinical models and in early clinical trials suggests that macrophages are attractive targets as part of combination therapy in cancer treatment.

MeSH Terms
Animals Cell Lineage/immunology Cell Movement Cell Proliferation Cell Survival Cell Transformation, Neoplastic/immunology Humans Immunosuppression Therapy Macrophages/immunology Mice Neoplasm Invasiveness Neoplasm Metastasis Neoplasms/immunology,pathology,therapy Neovascularization, Pathologic/immunology Tumor Microenvironment
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Noy Roy
Department of Developmental and Molecular Biology, Center for the Study of Reproductive Biology and Women's Health, Albert Einstein College of Medicine, New York, NY 10461, USA.
Pollard Jeffrey W
Department of Developmental and Molecular Biology, Center for the Study of Reproductive Biology and Women's Health, Albert Einstein College of Medicine, New York, NY 10461, USA; MRC Centre for Reproductive Health, Queen's Medical Research Institute, The University of Edinburgh, Edinburgh EH16 4TJ, UK. Electronic address: jeff.pollard@ed.ac.uk.
References (132)
132 references, click to expand
  1. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth.
    PLoS One. 2009 Aug 10;4(8):e6562 PMID: 19668347
  2. The cellular and molecular origin of tumor-associated macrophages.
    Science. 2014 May 23;344(6186):921-5 PMID: 24812208
  3. Negative co-receptors on lymphocytes.
    Curr Opin Immunol. 2002 Jun;14(3):391-6 PMID: 11973140
  4. A novel mouse model of inflammatory bowel disease links mammalian target of rapamycin-dependent hyperproliferation of colonic epithelium to inflammation-associated tumorigenesis.
    Am J Pathol. 2010 Feb;176(2):952-67 PMID: 20042677
  5. Regulation of T helper cell responses in experimental murine schistosomiasis by IL-10. Effect on expression of B7 and B7-2 costimulatory molecules by macrophages.
    J Immunol. 1994 Dec 1;153(11):5190-9 PMID: 7525726
  6. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors.
    Cancer Cell. 2005 Sep;8(3):211-26 PMID: 16169466
  7. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells.
    Cancer Cell. 2011 Apr 12;19(4):512-26 PMID: 21481792
  8. Cancer-related inflammation: common themes and therapeutic opportunities.
    Semin Cancer Biol. 2012 Feb;22(1):33-40 PMID: 22210179
  9. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs.
    Cancer Cell. 2011 Oct 18;20(4):538-49 PMID: 22014578
  10. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy.
    J Exp Med. 2001 Mar 19;193(6):727-40 PMID: 11257139
  11. Inactivation of chemokine (C-C motif) receptor 1 (CCR1) suppresses colon cancer liver metastasis by blocking accumulation of immature myeloid cells in a mouse model.
    Proc Natl Acad Sci U S A. 2010 Jul 20;107(29):13063-8 PMID: 20616008
  12. Macrophage diversity enhances tumor progression and metastasis.
    Cell. 2010 Apr 2;141(1):39-51 PMID: 20371344
  13. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  14. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages.
    Cancer Cell. 2009 Aug 4;16(2):91-102 PMID: 19647220
  15. Therapeutic PD-1 pathway blockade augments with other modalities of immunotherapy T-cell function to prevent immune decline in ovarian cancer.
    Cancer Res. 2013 Dec 1;73(23):6900-12 PMID: 23975756
  16. Low surface expression of B7-1 (CD80) is an immunoescape mechanism of colon carcinoma.
    Cancer Res. 2006 Feb 15;66(4):2442-50 PMID: 16489051
  17. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes.
    J Immunol. 2003 Aug 1;171(3):1232-9 PMID: 12874210
  18. TGF-β: guardian of T cell function.
    J Immunol. 2013 Oct 15;191(8):3973-9 PMID: 24098055
  19. PD-1 blockage delays murine squamous cell carcinoma development.
    Carcinogenesis. 2014 Feb;35(2):424-31 PMID: 24031027
  20. Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells.
    Blood. 2007 Mar 1;109(5):2040-8 PMID: 17077329
  21. Tumor-associated macrophages press the angiogenic switch in breast cancer.
    Cancer Res. 2007 Jun 1;67(11):5064-6 PMID: 17545580
  22. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses.
    Nat Immunol. 2007 Oct;8(10):1086-94 PMID: 17873879
  23. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis.
    Cancer Cell. 2008 Jan;13(1):23-35 PMID: 18167337
  24. Contribution of the PD-1 ligands/PD-1 signaling pathway to dendritic cell-mediated CD4+ T cell activation.
    Eur J Immunol. 2006 Sep;36(9):2472-82 PMID: 16917960
  25. Regulation of adaptive immunity; the role of interleukin-10.
    Front Immunol. 2013 May 31;4:129 PMID: 23755052
  26. Stromal cell-derived CSF-1 blockade prolongs xenograft survival of CSF-1-negative neuroblastoma.
    Int J Cancer. 2010 Mar 15;126(6):1339-52 PMID: 19711348
  27. Microenvironmental regulation of tumor progression and metastasis.
    Nat Med. 2013 Nov;19(11):1423-37 PMID: 24202395
  28. Tumor-associated macrophages: functional diversity, clinical significance, and open questions.
    Semin Immunopathol. 2013 Sep;35(5):585-600 PMID: 23657835
  29. Neutralizing tumor-promoting chronic inflammation: a magic bullet?
    Science. 2013 Jan 18;339(6117):286-91 PMID: 23329041
  30. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion.
    Cancer Cell. 2008 Mar;13(3):206-20 PMID: 18328425
  31. Regulation of macrophage arginase expression and tumor growth by the Ron receptor tyrosine kinase.
    J Immunol. 2011 Sep 1;187(5):2181-92 PMID: 21810604
  32. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts.
    Semin Cancer Biol. 2011 Apr;21(2):139-46 PMID: 21251983
  33. Myeloid WNT7b mediates the angiogenic switch and metastasis in breast cancer.
    Cancer Res. 2014 Jun 1;74(11):2962-73 PMID: 24638982
  34. Myeloid-derived suppressor cells as regulators of the immune system.
    Nat Rev Immunol. 2009 Mar;9(3):162-74 PMID: 19197294
  35. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited.
    Nat Rev Cancer. 2003 Jun;3(6):453-8 PMID: 12778135
  36. Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice.
    Blood. 2012 Mar 29;119(13):3164-75 PMID: 22327225
  37. Role of macrophage targeting in the antitumor activity of trabectedin.
    Cancer Cell. 2013 Feb 11;23(2):249-62 PMID: 23410977
  38. VCAM-1 and VAP-1 recruit myeloid cells that promote pulmonary metastasis in mice.
    Blood. 2013 Apr 18;121(16):3289-97 PMID: 23407548
  39. Alternative activation of macrophages.
    Nat Rev Immunol. 2003 Jan;3(1):23-35 PMID: 12511873
  40. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes.
    Cancer Res. 2010 Jul 15;70(14):5728-39 PMID: 20570887
  41. Colony-stimulating factor-1 in immunity and inflammation.
    Curr Opin Immunol. 2006 Feb;18(1):39-48 PMID: 16337366
  42. TIE2-expressing macrophages limit the therapeutic efficacy of the vascular-disrupting agent combretastatin A4 phosphate in mice.
    J Clin Invest. 2011 May;121(5):1969-73 PMID: 21490397
  43. Tumor progression stage and anatomical site regulate tumor-associated macrophage and bone marrow-derived monocyte polarization.
    Am J Pathol. 2010 Jun;176(6):2972-85 PMID: 20431028
  44. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors.
    Cancer Res. 2007 Mar 15;67(6):2649-56 PMID: 17363585
  45. A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis.
    Cancer Cell. 2014 May 12;25(5):605-20 PMID: 24823638
  46. Macrophage polarization in tumour progression.
    Semin Cancer Biol. 2008 Oct;18(5):349-55 PMID: 18467122
  47. Gliomas promote immunosuppression through induction of B7-H1 expression in tumor-associated macrophages.
    Clin Cancer Res. 2013 Jun 15;19(12):3165-75 PMID: 23613317
  48. Macrophage regulation of tumor responses to anticancer therapies.
    Cancer Cell. 2013 Mar 18;23(3):277-86 PMID: 23518347
  49. Tumor-associated macrophages: effectors of angiogenesis and tumor progression.
    Biochim Biophys Acta. 2009 Aug;1796(1):11-8 PMID: 19269310
  50. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.
    Cell. 2006 Jan 27;124(2):263-6 PMID: 16439202
  51. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression.
    Cancer Res. 2010 Oct 1;70(19):7465-75 PMID: 20841473
  52. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy.
    Cancer Discov. 2011 Jun;1(1):54-67 PMID: 22039576
  53. Increased B7-H1 and B7-H4 Expressions on Circulating Monocytes and Tumor-Associated Macrophages are Involved in Immune Evasion in Patients with Gastric Cancer.
    Yonago Acta Med. 2011 Mar;54(1):1-10 PMID: 24031123
  54. CD8+ tumor-infiltrating T cells are trapped in the tumor-dendritic cell network.
    Neoplasia. 2013 Jan;15(1):85-94 PMID: 23359264
  55. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses.
    Cancer Res. 2013 Feb 1;73(3):1128-41 PMID: 23221383
  56. CSF-1R inhibition alters macrophage polarization and blocks glioma progression.
    Nat Med. 2013 Oct;19(10):1264-72 PMID: 24056773
  57. Tumor-associated macrophages recruit CCR6+ regulatory T cells and promote the development of colorectal cancer via enhancing CCL20 production in mice.
    PLoS One. 2011 Apr 29;6(4):e19495 PMID: 21559338
  58. Human anti-inflammatory macrophages induce Foxp3+ GITR+ CD25+ regulatory T cells, which suppress via membrane-bound TGFbeta-1.
    J Immunol. 2008 Aug 1;181(3):2220-6 PMID: 18641362
  59. PD-L1 is a novel direct target of HIF-1α, and its blockade under hypoxia enhanced MDSC-mediated T cell activation.
    J Exp Med. 2014 May 5;211(5):781-90 PMID: 24778419
  60. Tumor microenvironment of metastasis and risk of distant metastasis of breast cancer.
    J Natl Cancer Inst. 2014 Jun 03;106(8): PMID: 24895374
  61. Macrophage colony-stimulating factor augments Tie2-expressing monocyte differentiation, angiogenic function, and recruitment in a mouse model of breast cancer.
    PLoS One. 2014 Jun 03;9(6):e98623 PMID: 24892425
  62. CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8+ T cells.
    Oncoimmunology. 2013 Dec 1;2(12):e26968 PMID: 24498562
  63. Natural and induced T regulatory cells in cancer.
    Front Immunol. 2013 Jul 11;4:190 PMID: 23874336
  64. Microenvironmental regulation of metastasis.
    Nat Rev Cancer. 2009 Apr;9(4):239-52 PMID: 19279573
  65. Origins of tumor-associated macrophages and neutrophils.
    Proc Natl Acad Sci U S A. 2012 Feb 14;109(7):2491-6 PMID: 22308361
  66. Macrophage therapy of cancer metastasis.
    Ciba Found Symp. 1988;141:211-22 PMID: 3075934
  67. Vascular endothelial growth factor-induced skin carcinogenesis depends on recruitment and alternative activation of macrophages.
    J Pathol. 2012 May;227(1):17-28 PMID: 22262122
  68. Human neuroblastoma cells trigger an immunosuppressive program in monocytes by stimulating soluble HLA-G release.
    Cancer Res. 2007 Jul 1;67(13):6433-41 PMID: 17616704
  69. Reactive nitrogen species in the chemical biology of inflammation.
    Arch Biochem Biophys. 2004 Mar 1;423(1):12-22 PMID: 14989259
  70. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion.
    Genes Dev. 2010 Feb 1;24(3):241-55 PMID: 20080943
  71. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses.
    Immunity. 2007 Jul;27(1):111-22 PMID: 17629517
  72. 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
  73. Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1.
    J Exp Med. 2009 Jun 8;206(6):1327-37 PMID: 19451266
  74. Tumor-associated macrophages mediate immunosuppression in the renal cancer microenvironment by activating the 15-lipoxygenase-2 pathway.
    Cancer Res. 2011 Oct 15;71(20):6400-9 PMID: 21900394
  75. SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion.
    Nat Genet. 2007 Apr;39(4):467-75 PMID: 17369830
  76. Tumor-associated macrophages in glioma: friend or foe?
    J Oncol. 2013;2013:486912 PMID: 23737783
  77. M1 and M2 Macrophages: Oracles of Health and Disease.
    Crit Rev Immunol. 2012;32(6):463-88 PMID: 23428224
  78. Expression of functional B7-H2 and B7.2 costimulatory molecules and their prognostic implications in de novo acute myeloid leukemia.
    Clin Cancer Res. 2005 Aug 15;11(16):5708-17 PMID: 16115907
  79. Low-dose irradiation programs macrophage differentiation to an iNOS⁺/M1 phenotype that orchestrates effective T cell immunotherapy.
    Cancer Cell. 2013 Nov 11;24(5):589-602 PMID: 24209604
  80. Molecular pathways: adipose inflammation as a mediator of obesity-associated cancer.
    Clin Cancer Res. 2013 Nov 15;19(22):6074-83 PMID: 23958744
  81. A clinical study assessing the tolerability and biological effects of infliximab, a TNF-alpha inhibitor, in patients with advanced cancer.
    Ann Oncol. 2008 Jul;19(7):1340-1346 PMID: 18325912
  82. Colorectal cancer: looking for answers in the microbiota.
    Cancer Discov. 2013 Apr;3(4):384-7 PMID: 23580283
  83. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation).
    Blood. 2006 Mar 1;107(5):2112-22 PMID: 16269622
  84. Bv8 regulates myeloid-cell-dependent tumour angiogenesis.
    Nature. 2007 Dec 6;450(7171):825-31 PMID: 18064003
  85. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis.
    Nature. 2011 Jun 08;475(7355):222-5 PMID: 21654748
  86. Inflammation and cancer.
    Nature. 2002 Dec 19-26;420(6917):860-7 PMID: 12490959
  87. Targeting tumor-stromal interactions in bone metastasis.
    Pharmacol Ther. 2014 Feb;141(2):222-33 PMID: 24140083
  88. Smoldering and polarized inflammation in the initiation and promotion of malignant disease.
    Cancer Cell. 2005 Mar;7(3):211-7 PMID: 15766659
  89. The clinical significance of inflammatory cytokines in primary cell culture in endometrial carcinoma.
    Mol Oncol. 2013 Feb;7(1):41-54 PMID: 22944067
  90. The interplay between macrophages and angiogenesis in development, tissue injury and regeneration.
    Int J Dev Biol. 2011;55(4-5):495-503 PMID: 21732273
  91. Leukocytes in mammary development and cancer.
    Cold Spring Harb Perspect Biol. 2011 Mar 01;3(3): PMID: 21123394
  92. Immune modulation in cancer with antibodies.
    Annu Rev Med. 2014;65:185-202 PMID: 24188664
  93. The role of B7 family molecules in hematologic malignancy.
    Blood. 2013 Jan 31;121(5):734-44 PMID: 23223433
  94. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET.
    Nat Med. 2012 Jun;18(6):883-91 PMID: 22635005
  95. PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5336-41 PMID: 12697896
  96. Macrophage plasticity and polarization: in vivo veritas.
    J Clin Invest. 2012 Mar;122(3):787-95 PMID: 22378047
  97. Therapeutic activation of macrophages and microglia to suppress brain tumor-initiating cells.
    Nat Neurosci. 2014 Jan;17(1):46-55 PMID: 24316889
  98. Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase.
    Int Immunol. 2004 Oct;16(10):1391-401 PMID: 15351783
  99. A multi-targeted approach to treating bone metastases.
    Cancer Metastasis Rev. 2014 Sep;33(2-3):545-53 PMID: 24390423
  100. Metastasis to bone: causes, consequences and therapeutic opportunities.
    Nat Rev Cancer. 2002 Aug;2(8):584-93 PMID: 12154351
  101. Tumor-infiltrating monocytic myeloid-derived suppressor cells mediate CCR5-dependent recruitment of regulatory T cells favoring tumor growth.
    J Immunol. 2012 Dec 15;189(12):5602-11 PMID: 23152559
  102. Vascular endothelial growth factor restores delayed tumor progression in tumors depleted of macrophages.
    Mol Oncol. 2007 Dec;1(3):288-302 PMID: 18509509
  103. Tumour-educated macrophages promote tumour progression and metastasis.
    Nat Rev Cancer. 2004 Jan;4(1):71-8 PMID: 14708027
  104. Recombinant HLA-G5 and -G6 drive U937 myelomonocytic cell production of TGF-beta1.
    J Leukoc Biol. 2004 Dec;76(6):1220-8 PMID: 15459235
  105. The LILR family: modulators of innate and adaptive immune pathways in health and disease.
    Tissue Antigens. 2004 Sep;64(3):215-25 PMID: 15304001
  106. Leukocyte composition of human breast cancer.
    Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):2796-801 PMID: 21825174
  107. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis.
    J Exp Med. 1998 Mar 2;187(5):813-8 PMID: 9480992
  108. Intratumoral macrophages contribute to epithelial-mesenchymal transition in solid tumors.
    BMC Cancer. 2012 Jan 24;12:35 PMID: 22273460
  109. Targeting distinct tumor-infiltrating myeloid cells by inhibiting CSF-1 receptor: combating tumor evasion of antiangiogenic therapy.
    Blood. 2010 Feb 18;115(7):1461-71 PMID: 20008303
  110. Macrophage biology in development, homeostasis and disease.
    Nature. 2013 Apr 25;496(7446):445-55 PMID: 23619691
  111. Macrophage-secreted cytokines drive pancreatic acinar-to-ductal metaplasia through NF-κB and MMPs.
    J Cell Biol. 2013 Aug 5;202(3):563-77 PMID: 23918941
  112. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm.
    Nat Immunol. 2010 Oct;11(10):889-96 PMID: 20856220
  113. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression.
    J Immunol. 1993 Aug 1;151(3):1224-34 PMID: 7687627
  114. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses.
    Cancer Res. 2004 Aug 15;64(16):5839-49 PMID: 15313928
  115. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions.
    Int J Dev Biol. 2011;55(7-9):861-7 PMID: 22161841
  116. Immunity, inflammation, and cancer.
    Cell. 2010 Mar 19;140(6):883-99 PMID: 20303878
  117. Induction of tumor-specific T cell memory by NK cell-mediated tumor rejection.
    Nat Immunol. 2002 Jan;3(1):83-90 PMID: 11743585
  118. Myeloid-derived suppressor cells in cancer patients: a clinical perspective.
    J Immunother. 2012 Feb-Mar;35(2):107-15 PMID: 22306898
  119. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition.
    Cancer Res. 2012 Mar 15;72(6):1384-94 PMID: 22282653
  120. Langerhans cells facilitate epithelial DNA damage and squamous cell carcinoma.
    Science. 2012 Jan 6;335(6064):104-8 PMID: 22223807
  121. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy.
    Cancer Cell. 2014 Jun 16;25(6):846-59 PMID: 24898549
  122. Tracking of intertissue migration reveals the origins of tumor-infiltrating monocytes.
    Proc Natl Acad Sci U S A. 2014 May 27;111(21):7771-6 PMID: 24825888
  123. The metastatic niche: adapting the foreign soil.
    Nat Rev Cancer. 2009 Apr;9(4):285-93 PMID: 19308068
  124. Innate and adaptive immune cells in the tumor microenvironment.
    Nat Immunol. 2013 Oct;14(10):1014-22 PMID: 24048123
  125. The macrophage growth factor CSF-1 in mammary gland development and tumor progression.
    J Mammary Gland Biol Neoplasia. 2002 Apr;7(2):147-62 PMID: 12465600
  126. Production of immune-modulatory nonclassical molecules HLA-G and HLA-E by tumor infiltrating ameboid microglia/macrophages in glioblastomas: a role in innate immunity?
    J Neuroimmunol. 2010 Mar 30;220(1-2):131-5 PMID: 20167379
  127. Marginating dendritic cells of the tumor microenvironment cross-present tumor antigens and stably engage tumor-specific T cells.
    Cancer Cell. 2012 Mar 20;21(3):402-17 PMID: 22439936
  128. Increase of circulating B7-H4-expressing CD68+ macrophage correlated with clinical stage of lung carcinomas.
    J Immunother. 2012 May;35(4):354-8 PMID: 22495393
  129. Macrophage-derived SPARC bridges tumor cell-extracellular matrix interactions toward metastasis.
    Cancer Res. 2008 Nov 1;68(21):9050-9 PMID: 18974151
  130. B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma.
    J Exp Med. 2006 Apr 17;203(4):871-81 PMID: 16606666
  131. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells.
    Proc Natl Acad Sci U S A. 2004 May 4;101(18):7064-9 PMID: 15103024
  132. Coordinated regulation of myeloid cells by tumours.
    Nat Rev Immunol. 2012 Mar 22;12(4):253-68 PMID: 22437938
Article Info
Journal
Immunity
Abbr.
Immunity
ISSN
1097-4180
DOI
10.1016/j.immuni.2014.06.010
Email
jeff.pollard@ed.ac.uk
Published
2014-07-17
Pages
49-61
Language
English
Region
United States
NLM ID
9432918
PMCID
PMC4137410
Subset
IM
Grants
NCI NIH HHS · P01 CA100324 · United States
Wellcome Trust · 101067 · United Kingdom
NCI NIH HHS · R01 CA172451 · United States
NCATS NIH HHS · UL1 TR001073 · United States
Medical Research Council · G1002033 · United Kingdom
Corrections
ErratumIn
-
External Links
PubMed source DOI: 10.1016/j.immuni.2014.06.010 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2