Abstract
We recently demonstrated that human BM cells can be treated in vitro with defined growth factors to induce the rapid generation of myeloid-derived suppressor cells (MDSCs), hereafter defined as BM-MDSCs. Indeed, combination of G-CSF + GM-CSF led to the development of a heterogeneous mixture of immature myeloid cells ranging from myeloblasts to band cells that were able to suppress alloantigen- and mitogen-stimulated T lymphocytes. Here, we further investigate the mechanism of suppression and define the cell subset that is fully responsible for BM-MDSC-mediated immune suppression. This population, which displays the structure and markers of promyelocytes, is however distinct from physiologic promyelocytes that, instead, are devoid of immuosuppressive function. In addition, we demonstrate that promyelocyte-like cells proliferate in the presence of activated lymphocytes and that, when these cells exert suppressive activity, they do not differentiate but rather maintain their immature phenotype. Finally, we show that promyelocyte-like BM-MDSCs are equivalent to MDSCs present in the blood of patients with breast cancer and patients with colorectal cancer and that increased circulating levels of these immunosuppressive myeloid cells correlate with worse prognosis and radiographic progression.
MeSH Terms
Breast Neoplasms/immunology,pathology
CD11b Antigen/metabolism
CD3 Complex/metabolism
CD8-Positive T-Lymphocytes/immunology,pathology
Cell Differentiation
Cell Proliferation
Colorectal Neoplasms/immunology,pathology
Female
GPI-Linked Proteins/metabolism
Humans
Immune Tolerance
In Vitro Techniques
Leukemia, Lymphoid/immunology,pathology
Lymphocyte Activation
Male
Myeloid Cells/classification,immunology,pathology
Myelopoiesis/immunology
Prognosis
Receptors, IgG/metabolism
Chemicals
CD11b Antigen
CD3 Complex
CD3 antigen, zeta chain
FCGR3B protein, human
GPI-Linked Proteins
ITGAM protein, human
Receptors, IgG
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Solito Samantha
Department of Oncology and Surgical Sciences, Oncology Section, University of Padova, Padova, Italy.
Falisi Erika
Diaz-Montero Claudia Marcela
Doni Andrea
Pinton Laura
Rosato Antonio
Francescato Samuela
Basso Giuseppe
Zanovello Paola
Onicescu Georgiana
Garrett-Mayer Elizabeth
Montero Alberto J
Bronte Vincenzo
Mandruzzato Susanna
References (28)
28 references, click to expand
-
Circulating tumor cells, disease progression, and survival in metastatic breast cancer.
N Engl J Med. 2004 Aug 19;351(8):781-91
PMID: 15317891
-
Down-regulation of the CD3-zeta chain in sentinel node biopsies from breast cancer patients.
Breast Cancer Res Treat. 2002 Jul;74(1):33-40
PMID: 12150450
-
Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression.
J Exp Med. 2007 Jun 11;204(6):1257-65
PMID: 17502665
-
Circulating tumor cells in metastatic breast cancer: biologic staging beyond tumor burden.
Clin Breast Cancer. 2007 Feb;7(6):471-9
PMID: 17386124
-
Immortalized myeloid suppressor cells trigger apoptosis in antigen-activated T lymphocytes.
J Immunol. 2000 Dec 15;165(12):6723-30
PMID: 11120790
-
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
-
Severe combined immunodeficiency caused by deficiency in either the delta or the epsilon subunit of CD3.
J Clin Invest. 2004 Nov;114(10):1512-7
PMID: 15546002
-
Tumor-educated tolerogenic dendritic cells induce CD3epsilon down-regulation and apoptosis of T cells through oxygen-dependent pathways.
J Immunol. 2008 Sep 1;181(5):3089-98
PMID: 18713979
-
Myeloid-derived suppressor cells accumulate in kidney allograft tolerance and specifically suppress effector T cell expansion.
J Immunol. 2008 Jun 15;180(12):7898-906
PMID: 18523253
-
Products of anti-CD3/anti-CD28 activated lymphocytes induce differentiation and maturation of dendritic cells and have adjuvant-like activity in vitro and in vivo.
Clin Immunol. 2008 Oct;129(1):58-68
PMID: 18691939
-
Granules of the human neutrophilic polymorphonuclear leukocyte.
Blood. 1997 May 15;89(10):3503-21
PMID: 9160655
-
Lung carcinomas do not induce T-cell apoptosis via the Fas/Fas ligand pathway but down-regulate CD3 epsilon expression.
Cancer Immunol Immunother. 2008 Mar;57(3):325-36
PMID: 17668204
-
PD-L2 is a second ligand for PD-1 and inhibits T cell activation.
Nat Immunol. 2001 Mar;2(3):261-8
PMID: 11224527
-
Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 zeta chain of T-cell receptor complex and antigen-specific T-cell responses.
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13119-24
PMID: 8917554
-
Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity.
Blood. 2005 Mar 15;105(6):2549-56
PMID: 15546957
-
Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor.
Immunity. 2010 Jun 25;32(6):790-802
PMID: 20605485
-
IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients.
J Immunol. 2009 May 15;182(10):6562-8
PMID: 19414811
-
Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells.
J Immunol. 2010 Aug 15;185(4):2273-84
PMID: 20644162
-
Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives.
Immunol Rev. 2008 Apr;222:180-91
PMID: 18364002
-
Myeloid-derived suppressor cells as regulators of the immune system.
Nat Rev Immunol. 2009 Mar;9(3):162-74
PMID: 19197294
-
Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer.
J Clin Oncol. 2005 Mar 1;23(7):1420-30
PMID: 15735118
-
Functional analysis of monocyte MHC class II compartments.
FASEB J. 2009 Jan;23(1):164-71
PMID: 18815360
-
Flow cytometric study of neutrophilic granulopoiesis in normal bone marrow using an expanded panel of antibodies: correlation with morphologic assessments.
J Clin Lab Anal. 2004;18(1):36-41
PMID: 14730556
-
Myeloid-derived suppressor cell heterogeneity and subset definition.
Curr Opin Immunol. 2010 Apr;22(2):238-44
PMID: 20171075
-
Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells.
J Clin Invest. 2006 Oct;116(10):2777-90
PMID: 17016559
-
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
-
Reciprocal functional modulation of the activation of T lymphocytes and fibroblasts derived from human solid tumors.
J Immunol. 2010 Sep 1;185(5):2681-92
PMID: 20686130
-
Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells.
Immunol Rev. 2008 Apr;222:162-79
PMID: 18364001