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PMID: 24060865 Published · ppublish English Historical Article Review

History of myeloid-derived suppressor cells.

Nature reviews. Cancer ·Vol. 13 ·No. 10 ·2013-00-00 ·Pages 739-52

Talmadge JE, Gabrilovich DI

Abstract

Tumour-induced granulocytic hyperplasia is associated with tumour vasculogenesis and escape from immunity via T cell suppression. Initially, these myeloid cells were identified as granulocytes or monocytes; however, recent studies have revealed that this hyperplasia is associated with populations of multipotent progenitor cells that have been identified as myeloid-derived suppressor cells (MDSCs). The study of MDSCs has provided a wealth of information regarding tumour pathobiology, has extended our understanding of neoplastic progression and has modified our approaches to immune adjuvant therapy. In this Timeline article, we discuss the history of MDSCs, their influence on tumour progression and metastasis, and the crosstalk between tumour cells, MDSCs and the host macroenvironment.

MeSH Terms
Animals Antigens, Differentiation/analysis Antigens, Neoplasm/analysis Cell Biology/history Cell Differentiation Cell Lineage Chemokines/physiology Hematopoiesis, Extramedullary Hematopoietic Stem Cell Mobilization/adverse effects History, 20th Century History, 21st Century Humans Leukemoid Reaction/pathology Medical Oncology/history Mice Molecular Targeted Therapy Multipotent Stem Cells/cytology,drug effects,physiology Myeloid Cells/cytology,drug effects,physiology Myeloid Progenitor Cells/cytology,drug effects,physiology Neoplasm Invasiveness/physiopathology Neoplasm Metastasis Neoplasms/immunology,pathology Neovascularization, Pathologic/physiopathology Tumor Burden Tumor Escape Tumor Microenvironment
Chemicals
Antigens, Differentiation Antigens, Neoplasm Chemokines
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Talmadge James E
University of Nebraska Medical Center, Department of Pathology and Microbiology, 986495 Nebraska Medical Center, Omaha NE 68198-6495, USA.
Gabrilovich Dmitry I
References (191)
191 references, click to expand
  1. Anti-IL-6 receptor mAb eliminates myeloid-derived suppressor cells and inhibits tumor growth by enhancing T-cell responses.
    Eur J Immunol. 2012 Aug;42(8):2060-72 PMID: 22653638
  2. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1.
    J Biol Chem. 2001 Nov 23;276(47):43503-8 PMID: 11571304
  3. Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign.
    Cancer Res. 2010 Jun 1;70(11):4335-45 PMID: 20484028
  4. Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice.
    Blood. 2008 Jun 15;111(12):5457-66 PMID: 18375791
  5. Combination of p53 cancer vaccine with chemotherapy in patients with extensive stage small cell lung cancer.
    Clin Cancer Res. 2006 Feb 1;12(3 Pt 1):878-87 PMID: 16467102
  6. Integrin alpha4beta1 promotes monocyte trafficking and angiogenesis in tumors.
    Cancer Res. 2006 Feb 15;66(4):2146-52 PMID: 16489015
  7. Vascular endothelial growth factor-trap overcomes defects in dendritic cell differentiation but does not improve antigen-specific immune responses.
    Clin Cancer Res. 2007 Aug 15;13(16):4840-8 PMID: 17699863
  8. The effect of zoledronic acid on the function and differentiation of myeloid cells.
    Haematologica. 2006 Sep;91(9):1165-71 PMID: 16956814
  9. Systemic bacillus Calmette-Guérin (BCG) activates natural suppressor cells.
    Proc Natl Acad Sci U S A. 1978 Oct;75(10):5142-4 PMID: 283421
  10. MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis.
    J Exp Med. 2007 Jun 11;204(6):1463-74 PMID: 17548519
  11. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients.
    Cancer Immunol Immunother. 2012 Feb;61(2):255-263 PMID: 22120756
  12. A novel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers.
    Clin Cancer Res. 2010 Sep 15;16(18):4583-94 PMID: 20702612
  13. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function.
    J Exp Med. 2006 Nov 27;203(12):2691-702 PMID: 17101732
  14. Progression of pancreatic adenocarcinoma is significantly impeded with a combination of vaccine and COX-2 inhibition.
    J Immunol. 2009 Jan 1;182(1):216-24 PMID: 19109152
  15. Myelopoiesis-associated suppressor-cell activity in mice with Lewis lung carcinoma tumors: interferon-gamma plus tumor necrosis factor-alpha synergistically reduce suppressor cell activity.
    Int J Cancer. 1990 Aug 15;46(2):245-50 PMID: 2143498
  16. Granulocyte colony-stimulating factor promotes tumor angiogenesis via increasing circulating endothelial progenitor cells and Gr1+CD11b+ cells in cancer animal models.
    Int Immunol. 2006 Jan;18(1):1-9 PMID: 16352631
  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. Metastasis: quantitative analysis of distribution and fate of tumor emboli labeled with 125 I-5-iodo-2'-deoxyuridine.
    J Natl Cancer Inst. 1970 Oct;45(4):773-82 PMID: 5513503
  19. Isolation of putative progenitor endothelial cells for angiogenesis.
    Science. 1997 Feb 14;275(5302):964-7 PMID: 9020076
  20. Altered macrophage differentiation and immune dysfunction in tumor development.
    J Clin Invest. 2007 May;117(5):1155-66 PMID: 17476345
  21. 1 alpha,25-dihydroxyvitamin D3 plus gamma-interferon blocks lung tumor production of granulocyte-macrophage colony-stimulating factor and induction of immunosuppressor cells.
    Cancer Res. 1993 Dec 15;53(24):6006-10 PMID: 8261414
  22. Mammary tumor latency is increased in mice lacking the inducible nitric oxide synthase.
    Int J Cancer. 2003 Aug 10;106(1):1-7 PMID: 12794750
  23. Characterization of iNOS(+) Neutrophil-like ring cell in tumor-bearing mice.
    J Transl Med. 2012 Jul 30;10:152 PMID: 22846631
  24. Myeloid derived suppressor cells in human diseases.
    Int Immunopharmacol. 2011 Jul;11(7):802-7 PMID: 21237299
  25. Tumor secretion of VEGF induces endothelial cells to suppress T cell functions through the production of PGE2.
    J Immunother. 2010 Feb-Mar;33(2):126-35 PMID: 20145550
  26. Pathways mediating the expansion and immunosuppressive activity of myeloid-derived suppressor cells and their relevance to cancer therapy.
    Clin Cancer Res. 2007 Sep 15;13(18 Pt 1):5243-8 PMID: 17875751
  27. Heterogeneity of splenic natural suppressor cells induced in mice by treatment with cyclophosphamide.
    Immunopharmacology. 1993 Mar-Apr;25(2):117-29 PMID: 8500984
  28. Indomethacin sensitive suppressor-cell activity in head and neck cancer patients. The role of the adherent mononuclear cell.
    Cancer. 1988 Feb 1;61(3):462-74 PMID: 2962730
  29. CCR2 mediates hematopoietic stem and progenitor cell trafficking to sites of inflammation in mice.
    J Clin Invest. 2010 Apr;120(4):1192-203 PMID: 20234092
  30. Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation.
    J Immunol. 2000 Jul 15;165(2):779-85 PMID: 10878351
  31. Tricks tumors use to escape from immune control.
    Oral Oncol. 2009 Oct;45(10):e119-23 PMID: 19467917
  32. Regulation of immune responses by L-arginine metabolism.
    Nat Rev Immunol. 2005 Aug;5(8):641-54 PMID: 16056256
  33. Induction of allograft tolerance after total lymphoid irradiation (TLI): development of suppressor cells of the mixed leukocyte reaction (MLR).
    J Immunol. 1979 Aug;123(2):942-6 PMID: 156766
  34. The immunoregulatory role of bone marrow. I. Suppression of the induction of antibody responses to T-dependent and T-independent antigens by cells in the bone marrow.
    Cell Immunol. 1979 Mar 15;43(2):362-71 PMID: 314345
  35. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells.
    J Immunol. 2008 Oct 1;181(7):4666-75 PMID: 18802069
  36. Splenic macrophages from tumor-bearing mice co-expressing MAC-1 and MAC-2 antigens exert immunoregulatory functions via two distinct mechanisms.
    J Leukoc Biol. 1991 Feb;49(2):126-38 PMID: 1991996
  37. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity.
    Blood. 2008 Apr 15;111(8):4233-44 PMID: 18272812
  38. Role of beta2-integrins for homing and neovascularization capacity of endothelial progenitor cells.
    J Exp Med. 2005 Jan 3;201(1):63-72 PMID: 15623573
  39. Direct evidence that bevacizumab, an anti-VEGF antibody, up-regulates SDF1alpha, CXCR4, CXCL6, and neuropilin 1 in tumors from patients with rectal cancer.
    Cancer Res. 2009 Oct 15;69(20):7905-10 PMID: 19826039
  40. Myeloid-derived suppressor cells in mammary tumor progression in FVB Neu transgenic mice.
    Cancer Immunol Immunother. 2010 Jan;59(1):47-62 PMID: 19449184
  41. Functional differentiation of normal human neutrophils.
    Blood. 1987 Mar;69(3):937-44 PMID: 3814822
  42. Characterization of the MDSC proteome associated with metastatic murine mammary tumors using label-free mass spectrometry and shotgun proteomics.
    PLoS One. 2011;6(8):e22446 PMID: 21853032
  43. 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
  44. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism.
    J Immunol. 2002 Jan 15;168(2):689-95 PMID: 11777962
  45. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide.
    J Clin Invest. 2003 Jan;111(2):187-96 PMID: 12531874
  46. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells.
    Nat Biotechnol. 2007 Aug;25(8):911-20 PMID: 17664940
  47. Depletion of lymphocyte subpopulations in primary and secondary lymphoid organs of mice by a transplanted granulocytosis-inducing mammary carcinoma.
    Cancer Res. 1982 Apr;42(4):1255-60 PMID: 7060002
  48. Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes.
    Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21248-55 PMID: 21081700
  49. Tumor-derived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism.
    PLoS One. 2011;6(11):e27690 PMID: 22110722
  50. The iSBTc/SITC primer on tumor immunology and biological therapy of cancer: a summary of the 2010 program.
    J Transl Med. 2011 Jan 31;9:18 PMID: 21281484
  51. Role of organ selectivity in the determination of metastatic patterns of B16 melanoma.
    Cancer Res. 1980 Jul;40(7):2281-7 PMID: 7388794
  52. Chemoprevention by cyclooxygenase-2 inhibition reduces immature myeloid suppressor cell expansion.
    Int Immunopharmacol. 2007 Feb;7(2):140-51 PMID: 17178380
  53. Resection of the primary tumor improves survival in metastatic breast cancer by reducing overall tumor burden.
    Surgery. 2013 Jun;153(6):771-8 PMID: 23489938
  54. Anti-LFA-1 blocking antibodies prevent mobilization of hematopoietic progenitor cells induced by interleukin-8.
    Blood. 1998 Jun 1;91(11):4099-105 PMID: 9596655
  55. 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
  56. Subsets of myeloid-derived suppressor cells in tumor-bearing mice.
    J Immunol. 2008 Oct 15;181(8):5791-802 PMID: 18832739
  57. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein.
    J Exp Med. 2008 Sep 29;205(10):2235-49 PMID: 18809714
  58. FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy?
    Nat Rev Cancer. 2008 Dec;8(12):942-56 PMID: 19029957
  59. Induction of suppressor cells by intravenous administration of Bacillus Calmette-Guérin and its modulation by cyclophosphamide.
    Biochem Pharmacol. 1979 Jun 15;28(12):1947-52 PMID: 313210
  60. Antibodies to colony-stimulating factors block Lewis lung carcinoma cell stimulation of immune-suppressive bone marrow cells.
    Cancer Immunol Immunother. 1991;33(3):146-52 PMID: 1675153
  61. Effect of conditional knockout of the type II TGF-beta receptor gene in mammary epithelia on mammary gland development and polyomavirus middle T antigen induced tumor formation and metastasis.
    Cancer Res. 2005 Mar 15;65(6):2296-302 PMID: 15781643
  62. GM-CSF is one of the main breast tumor-derived soluble factors involved in the differentiation of CD11b-Gr1- bone marrow progenitor cells into myeloid-derived suppressor cells.
    Breast Cancer Res Treat. 2010 Aug;123(1):39-49 PMID: 19898981
  63. Myeloid-derived suppressor cells as regulators of the immune system.
    Nat Rev Immunol. 2009 Mar;9(3):162-74 PMID: 19197294
  64. Phase IB study of 25-hydroxyvitamin D(3) treatment to diminish suppressor cells in head and neck cancer patients.
    Hum Immunol. 2001 Nov;62(11):1282-93 PMID: 11704292
  65. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer.
    Cancer Cell. 2012 Jun 12;21(6):822-35 PMID: 22698406
  66. Tumor- and organ-dependent infiltration by myeloid-derived suppressor cells.
    Int Immunopharmacol. 2011 Jul;11(7):816-26 PMID: 21376153
  67. Murine neonatal spleen contains natural T and non-T suppressor cells capable of inhibiting adult alloreactive and newborn autoreactive T-cell proliferation.
    Cell Immunol. 1986 May;99(2):461-75 PMID: 2944626
  68. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity.
    Clin Cancer Res. 2005 Sep 15;11(18):6713-21 PMID: 16166452
  69. The tumor microenvironment and its role in promoting tumor growth.
    Oncogene. 2008 Oct 6;27(45):5904-12 PMID: 18836471
  70. Tumor necrosis factor-α blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation.
    Immunity. 2013 Mar 21;38(3):541-54 PMID: 23477736
  71. 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
  72. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models.
    Proc Natl Acad Sci U S A. 2009 Apr 21;106(16):6742-7 PMID: 19346489
  73. Epigenetic silencing of retinoblastoma gene regulates pathologic differentiation of myeloid cells in cancer.
    Nat Immunol. 2013 Mar;14(3):211-20 PMID: 23354483
  74. Inhibition of tumor growth by elimination of granulocytes.
    J Exp Med. 1995 Jan 1;181(1):435-40 PMID: 7807024
  75. Extramedullary hematopoiesis: a new look at the underlying stem cell niche, theories of development, and occurrence in animals.
    Vet Pathol. 2012 May;49(3):508-23 PMID: 22262354
  76. Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo.
    J Exp Med. 2003 Jul 21;198(2):305-13 PMID: 12874263
  77. Bone marrow stem and progenitor cell contribution to neovasculogenesis is dependent on model system with SDF-1 as a permissive trigger.
    Blood. 2009 Nov 5;114(19):4310-9 PMID: 19717647
  78. Mouse neutrophilic granulocytes express mRNA encoding the macrophage colony-stimulating factor receptor (CSF-1R) as well as many other macrophage-specific transcripts and can transdifferentiate into macrophages in vitro in response to CSF-1.
    J Leukoc Biol. 2007 Jul;82(1):111-23 PMID: 17438263
  79. Regulation of dendritic cell differentiation and antitumor immune response in cancer by pharmacologic-selective inhibition of the janus-activated kinase 2/signal transducers and activators of transcription 3 pathway.
    Cancer Res. 2005 Oct 15;65(20):9525-35 PMID: 16230418
  80. CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice.
    J Immunol. 2010 Jul 1;185(1):203-10 PMID: 20525890
  81. The distribution of secondary growths in cancer of the breast. 1889.
    Cancer Metastasis Rev. 1989 Aug;8(2):98-101 PMID: 2673568
  82. Molecular mechanisms and clinical applications of angiogenesis.
    Nature. 2011 May 19;473(7347):298-307 PMID: 21593862
  83. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy.
    Cancer Discov. 2011 Jun;1(1):54-67 PMID: 22039576
  84. A STUDY OF THE LEUKEMOID RESPONSE TO TRANSPLANTABLE A-280 TUMOR IN MICE.
    Cancer Res. 1964 Feb;24:302-11 PMID: 14115699
  85. Mechanism of T cell tolerance induced by myeloid-derived suppressor cells.
    J Immunol. 2010 Mar 15;184(6):3106-16 PMID: 20142361
  86. CD11b+/Gr-1+ immature myeloid cells mediate suppression of T cells in mice bearing tumors of IL-1beta-secreting cells.
    J Immunol. 2005 Dec 15;175(12):8200-8 PMID: 16339559
  87. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF.
    Eur J Immunol. 2010 Jan;40(1):22-35 PMID: 19941314
  88. Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization.
    Genes Dev. 2007 Jun 15;21(12):1546-58 PMID: 17575055
  89. 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
  90. Microenvironmental regulation of metastasis.
    Nat Rev Cancer. 2009 Apr;9(4):239-52 PMID: 19279573
  91. Bone marrow-derived cells contribute to tumor neovasculature and, when modified to express an angiogenesis inhibitor, can restrict tumor growth in mice.
    Clin Cancer Res. 2001 Sep;7(9):2870-9 PMID: 11555605
  92. 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
  93. Inhibition of the graft-versus-host response by BCGcw-induced suppressor cells or prostaglandin E1.
    Cell Immunol. 1983 Mar;76(2):361-71 PMID: 6220811
  94. Immunologic attributes of cytokine mobilized peripheral blood stem cells and recovery following transplantation.
    Bone Marrow Transplant. 1996 Jan;17(1):101-9 PMID: 8673041
  95. HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment.
    J Exp Med. 2010 Oct 25;207(11):2439-53 PMID: 20876310
  96. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination.
    Proc Natl Acad Sci U S A. 2005 Mar 15;102(11):4185-90 PMID: 15753302
  97. ADAM10 overexpression shifts lympho- and myelopoiesis by dysregulating site 2/site 3 cleavage products of Notch.
    J Immunol. 2011 Apr 1;186(7):4244-52 PMID: 21368228
  98. Spleen but not tumor infiltration by dendritic and T cells is increased by intravenous adenovirus-Flt3 ligand injection.
    Cancer Gene Ther. 2007 Apr;14(4):364-71 PMID: 17235356
  99. The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity.
    Eur J Immunol. 2010 Nov;40(11):2969-75 PMID: 21061430
  100. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth.
    Nat Med. 2001 Nov;7(11):1194-201 PMID: 11689883
  101. MDSC as a mechanism of tumor escape from sunitinib mediated anti-angiogenic therapy.
    Int Immunopharmacol. 2011 Jul;11(7):856-61 PMID: 21315783
  102. Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine.
    J Clin Oncol. 2007 Jun 20;25(18):2546-53 PMID: 17577033
  103. Circulating stem cells in mice treated with cyclophosphamide.
    Blood. 1992 Jul 1;80(1):264-9 PMID: 1611093
  104. Tumor-induced immune dysfunctions caused by myeloid suppressor cells.
    J Immunother. 2001 Nov-Dec;24(6):431-46 PMID: 11759067
  105. Mammary tumor heterogeneity in the expansion of myeloid-derived suppressor cells.
    Int Immunopharmacol. 2009 Jul;9(7-8):937-48 PMID: 19362167
  106. Suppression of cytotoxic T-cell generation by natural suppressor cells from mice with GVHD is partially reversed by indomethacin.
    Cell Immunol. 1988 Apr 1;112(2):271-8 PMID: 2965616
  107. Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology.
    Cancer Immunol Immunother. 2012 Aug;61(8):1155-67 PMID: 22692756
  108. Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells.
    J Immunol. 2001 May 1;166(9):5398-406 PMID: 11313376
  109. Overexpression of matrix metalloproteinase-7 and -9 in NSCLC tumor and stromal cells: correlation with a favorable clinical outcome.
    Lung Cancer. 2012 Feb;75(2):235-41 PMID: 21764478
  110. Neutrophil homeostasis: a new role for stromal cell-derived factor-1.
    Immunol Res. 2005;32(1-3):169-78 PMID: 16106067
  111. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer.
    Clin Cancer Res. 2000 Aug;6(8):3282-9 PMID: 10955814
  112. The biology of cancer invasion and metastasis.
    Adv Cancer Res. 1978;28:149-250 PMID: 360795
  113. Immune cell migration in inflammation: present and future therapeutic targets.
    Nat Immunol. 2005 Dec;6(12):1182-90 PMID: 16369557
  114. Natural suppressor (NS) cells found in the spleen of neonatal mice and adult mice given total lymphoid irradiation (TLI) express the null surface phenotype.
    J Immunol. 1984 Jan;132(1):101-10 PMID: 6228575
  115. 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
  116. Tumor heterogeneity and the biology of cancer invasion and metastasis.
    Cancer Res. 1978 Sep;38(9):2651-60 PMID: 354778
  117. Identification and clinical significance of circulating endothelial progenitor cells in human non-small cell lung cancer.
    Cancer Res. 2006 Jul 15;66(14):7341-7 PMID: 16849585
  118. CC chemokine ligand 2 (CCL2) promotes prostate cancer tumorigenesis and metastasis.
    Cytokine Growth Factor Rev. 2010 Feb;21(1):41-8 PMID: 20005149
  119. Resection of solid tumors reverses T cell defects and restores protective immunity.
    J Immunol. 2000 Feb 15;164(4):2214-20 PMID: 10657677
  120. Stimulation of immune-suppressive bone marrow cells by colony-stimulating factors.
    Exp Hematol. 1990 Aug;18(7):806-11 PMID: 2143138
  121. All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients.
    Cancer Res. 2006 Sep 15;66(18):9299-307 PMID: 16982775
  122. Granulocyte colony-stimulating factor: molecular mechanisms of action during steady state and 'emergency' hematopoiesis.
    Cytokine. 2008 Jun;42(3):277-88 PMID: 18400509
  123. Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice.
    J Leukoc Biol. 2012 Jan;91(1):167-81 PMID: 21954284
  124. A case of cervical cancer with aggressive tumor growth: possible autocrine growth stimulation by G-CSF and Il-6.
    Gynecol Oncol. 2000 Sep;78(3 Pt 1):383-7 PMID: 10985899
  125. Myeloid-derived suppressor cell heterogeneity and subset definition.
    Curr Opin Immunol. 2010 Apr;22(2):238-44 PMID: 20171075
  126. Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells.
    J Immunol. 1998 Nov 15;161(10):5313-20 PMID: 9820504
  127. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity.
    Blood. 2003 Sep 15;102(6):2138-45 PMID: 12750171
  128. Fas-FasL-mediated CD4+ T-cell apoptosis following stem cell transplantation.
    Cancer Res. 1999 Jul 1;59(13):3107-11 PMID: 10397252
  129. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1.
    Nature. 1996 Aug 15;382(6592):635-8 PMID: 8757135
  130. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity.
    Cancer Res. 2010 Apr 15;70(8):3052-61 PMID: 20388795
  131. Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained.
    Cancer Res. 2010 May 1;70(9):3526-36 PMID: 20406969
  132. Suppression of alloantigen-induced T-cell proliferation by CD14+ cells derived from granulocyte colony-stimulating factor-mobilized peripheral blood mononuclear cells.
    Blood. 1997 Mar 1;89(5):1629-34 PMID: 9057645
  133. Bv8 regulates myeloid-cell-dependent tumour angiogenesis.
    Nature. 2007 Dec 6;450(7171):825-31 PMID: 18064003
  134. Low levels of tumor necrosis factor alpha increase tumor growth by inducing an endothelial phenotype of monocytes recruited to the tumor site.
    Cancer Res. 2009 Jan 1;69(1):338-48 PMID: 19118019
  135. Increased myeloid-derived suppressor cells in gastric cancer correlate with cancer stage and plasma S100A8/A9 proinflammatory proteins.
    J Immunol. 2013 Jan 15;190(2):794-804 PMID: 23248262
  136. Mobilization by either cyclophosphamide or granulocyte colony-stimulating factor transforms the bone marrow into a highly proteolytic environment.
    Exp Hematol. 2002 May;30(5):440-9 PMID: 12031650
  137. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo.
    Blood. 1998 Dec 1;92(11):4150-66 PMID: 9834220
  138. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis.
    Cancer Cell. 2004 Oct;6(4):409-21 PMID: 15488763
  139. Production of colony-stimulating factor by tumor cells and the factor-mediated induction of suppressor cells.
    J Immunol. 1988 Jul 15;141(2):699-708 PMID: 2968407
  140. Myeloid-derived suppressor cells: linking inflammation and cancer.
    J Immunol. 2009 Apr 15;182(8):4499-506 PMID: 19342621
  141. Granulocyte colony-stimulating factor and its receptor.
    Blood. 1991 Dec 1;78(11):2791-808 PMID: 1720034
  142. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion.
    Cancer Res. 2005 Apr 15;65(8):3044-8 PMID: 15833831
  143. Murine mammary carcinoma 4T1 induces a leukemoid reaction with splenomegaly: association with tumor-derived growth factors.
    Exp Mol Pathol. 2007 Feb;82(1):12-24 PMID: 16919266
  144. Suppression of T cell proliferation by tumor-induced granulocyte-macrophage progenitor cells producing transforming growth factor-beta and nitric oxide.
    J Immunol. 1996 Mar 1;156(5):1916-22 PMID: 8596044
  145. Preparing the "soil": the premetastatic niche.
    Cancer Res. 2006 Dec 1;66(23):11089-93 PMID: 17145848
  146. S100A9 a new marker for monocytic human myeloid-derived suppressor cells.
    Immunology. 2012 Jun;136(2):176-83 PMID: 22304731
  147. MicroRNA-494 is required for the accumulation and functions of tumor-expanded myeloid-derived suppressor cells via targeting of PTEN.
    J Immunol. 2012 Jun 1;188(11):5500-10 PMID: 22544933
  148. Mechanisms of immune suppression in patients with head and neck cancer: presence of CD34(+) cells which suppress immune functions within cancers that secrete granulocyte-macrophage colony-stimulating factor.
    Clin Cancer Res. 1995 Jan;1(1):95-103 PMID: 9815891
  149. Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal.
    Nature. 2008 May 15;453(7193):306-13 PMID: 18480811
  150. 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
  151. Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function.
    Blood. 2008 Jan 1;111(1):219-28 PMID: 17885078
  152. Granulocyte colony-stimulating factor: a novel mediator of T cell tolerance.
    J Immunol. 2005 Dec 1;175(11):7085-91 PMID: 16301609
  153. Subsets, expansion and activation of myeloid-derived suppressor cells.
    Med Microbiol Immunol. 2010 Aug;199(3):273-81 PMID: 20376485
  154. GM-CSF-mobilized peripheral blood CD34+ cells differ from steady-state bone marrow CD34+ cells in adhesion molecule expression.
    Bone Marrow Transplant. 1997 Jun;19(12):1175-81 PMID: 9208110
  155. High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells.
    Cancer Res. 2004 Sep 1;64(17):6337-43 PMID: 15342423
  156. Granulocytosis in neoplasia.
    Ann N Y Acad Sci. 1974;230:212-8 PMID: 4522870
  157. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer.
    J Immunol. 2001 Jan 1;166(1):678-89 PMID: 11123353
  158. Effect of recombinant granulocyte colony-stimulating factor on neutrophil kinetics in normal young and elderly humans.
    Blood. 1996 Jul 1;88(1):335-40 PMID: 8704192
  159. Mononuclear phagocyte heterogeneity in cancer: different subsets and activation states reaching out at the tumor site.
    Immunobiology. 2011 Nov;216(11):1192-202 PMID: 21803441
  160. Distinct populations of metastases-enabling myeloid cells expand in the liver of mice harboring invasive and preinvasive intra-abdominal tumor.
    J Leukoc Biol. 2010 Apr;87(4):713-25 PMID: 20042467
  161. 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
  162. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation.
    J Immunol. 1999 May 15;162(10):5728-37 PMID: 10229805
  163. AACR centennial series: the biology of cancer metastasis: historical perspective.
    Cancer Res. 2010 Jul 15;70(14):5649-69 PMID: 20610625
  164. Degradation of BM SDF-1 by MMP-9: the role in G-CSF-induced hematopoietic stem/progenitor cell mobilization.
    Bone Marrow Transplant. 2008 Nov;42(9):581-8 PMID: 18679363
  165. Tumor regulation of myeloid-derived suppressor cell proliferation and trafficking.
    Int Immunopharmacol. 2012 Jul;13(3):245-56 PMID: 22609473
  166. Interleukin-8 mediates resistance to antiangiogenic agent sunitinib in renal cell carcinoma.
    Cancer Res. 2010 Feb 1;70(3):1063-71 PMID: 20103651
  167. 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
  168. Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas.
    Clin Cancer Res. 1999 May;5(5):1107-13 PMID: 10353745
  169. Proteomic pathway analysis reveals inflammation increases myeloid-derived suppressor cell resistance to apoptosis.
    Mol Cell Proteomics. 2011 Mar;10(3):M110.002980 PMID: 21191032
  170. Myeloid-derived suppressor cells in human cancer.
    Cancer J. 2010 Jul-Aug;16(4):348-53 PMID: 20693846
  171. All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination.
    Cancer Res. 2003 Aug 1;63(15):4441-9 PMID: 12907617
  172. 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
  173. Sunitinib-induced myeloid lineage redistribution in renal cell cancer patients: CD1c+ dendritic cell frequency predicts progression-free survival.
    Clin Cancer Res. 2008 Sep 15;14(18):5884-92 PMID: 18794101
  174. Myelopoiesis-associated immune suppressor cells in mice bearing metastatic Lewis lung carcinoma tumors: gamma interferon plus tumor necrosis factor alpha synergistically reduces immune suppressor and tumor growth-promoting activities of bone marrow cells and diminishes tumor recurrence and metastasis.
    Cancer Res. 1992 Nov 15;52(22):6335-40 PMID: 1423279
  175. Mechanisms underlying hematopoietic stem cell mobilization induced by the CXC chemokine interleukin-8.
    Curr Opin Hematol. 1999 May;6(3):152-8 PMID: 10226735
  176. Mobilization of endothelial progenitor cells in patients with hematological malignancies after treatment with filgrastim and chemotherapy for autologous transplantation.
    Eur J Haematol. 2007 May;78(5):374-80 PMID: 17331127
  177. A homing mechanism for bone marrow-derived progenitor cell recruitment to the neovasculature.
    J Clin Invest. 2006 Mar;116(3):652-62 PMID: 16498499
  178. Inhibition of PPARγ in myeloid-lineage cells induces systemic inflammation, immunosuppression, and tumorigenesis.
    Blood. 2012 Jan 5;119(1):115-26 PMID: 22053106
  179. The metastatic niche: adapting the foreign soil.
    Nat Rev Cancer. 2009 Apr;9(4):285-93 PMID: 19308068
  180. Myeloid-derived suppressor cells in cancer patients: a clinical perspective.
    J Immunother. 2012 Feb-Mar;35(2):107-15 PMID: 22306898
  181. Cytoreduction surgery reduces systemic myeloid suppressor cell populations and restores intratumoral immunotherapy effectiveness.
    J Hematol Oncol. 2012 Jun 28;5:34 PMID: 22742411
  182. On the armament and appearances of human myeloid-derived suppressor cells.
    Clin Immunol. 2012 Sep;144(3):250-68 PMID: 22858650
  183. Immune suppression with supraoptimal doses of antigen in contact sensitivity. I. Demonstration of suppressor cells and their sensitivity to cyclophosphamide.
    J Immunol. 1977 Jul;119(1):240-4 PMID: 68972
  184. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells.
    EMBO J. 1999 Jul 15;18(14):3964-72 PMID: 10406801
  185. The kinship of neutrophils and granulocytic myeloid-derived suppressor cells in cancer: cousins, siblings or twins?
    Semin Cancer Biol. 2013 Jun;23(3):171-82 PMID: 23459190
  186. The terminology issue for myeloid-derived suppressor cells.
    Cancer Res. 2007 Jan 1;67(1):425; author reply 426 PMID: 17210725
  187. Macrophages, innate immunity and cancer: balance, tolerance, and diversity.
    Curr Opin Immunol. 2010 Apr;22(2):231-7 PMID: 20144856
  188. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1.
    J Immunol. 2009 Jan 1;182(1):240-9 PMID: 19109155
  189. Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma.
    Cancer Res. 2007 Dec 1;67(23):11438-46 PMID: 18056472
  190. Chemoattraction of femoral CD34+ progenitor cells by tumor-derived vascular endothelial cell growth factor.
    Clin Exp Metastasis. 1999;17(10):881-8 PMID: 11089887
  191. Clinical significance of defective dendritic cell differentiation in cancer.
    Clin Cancer Res. 2000 May;6(5):1755-66 PMID: 10815894
Article Info
Journal
Nature reviews. Cancer
Abbr.
Nat Rev Cancer
ISSN
1474-1768
Published
2013-00-00
Pages
739-52
Language
English
Region
England
NLM ID
101124168
PMCID
PMC4358792
Subset
IM
Grants
NCI NIH HHS · R01 CA084488 · United States
NCI NIH HHS · R01 CA100062 · United States
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