17β-Oestradiol enhances the expansion and activation of myeloid-derived suppressor cells via signal transducer and activator of transcription (STAT)−3 signalling in human pregnancy

Clinical and Experimental Immunology

Volumn 185, Issue 1, 2016, Pages 86-97

  Pan, T ^a,b   Zhong, L ^b   Wu, S ^b   Cao, Y ^b   Yang, Q ^b   Cai, Z ^b   Cai, X ^b   Zhao, W ^b   Ma, N ^c   Zhang, W ^c   Zhang, H ^b,d   Zhou, J ^a,b,d  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF SHENZHEN UNIVERSITY   (China)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

17 oestradiol; human pregnancy; MDSC; STAT 3

Indexed keywords

ACETYLCYSTEINE; ARGINASE; ARGININE; CHORIONIC GONADOTROPIN; CUCURBITACIN; ESTRADIOL; ESTROGEN RECEPTOR; FETAL ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROGESTERONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STAT PROTEIN;

ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL COMMUNICATION; CELL EXPANSION; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECT; ESTROGEN BLOOD LEVEL; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; MONOCYTE; MYELOID DERIVED SUPPRESSOR CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PREGNANCY; PREGNANT WOMAN; PRIMARY PREVENTION; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PUERPERIUM; REPRODUCTION; SIGNAL TRANSDUCTION; SPONTANEOUS ABORTION; SUPPRESSOR CELL; T LYMPHOCYTE;

EID: 84974803155     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12790     Document Type: Article

References (47)

1. Erlebacher A. Mechanisms of T cell tolerance towards the allogeneic fetus. Nat Rev Immunol 2013; 13:23–33.
2. Red-Horse K, Zhou Y, Genbacev O et al. Trophoblast differentiation during embryo implantation and formation of the maternal–fetal interface. J Clin Invest 2004; 114:744–54.
3. Erlebacher A. Immunology of the maternal–fetal interface. Annu Rev Immunol 2013; 31:387–411.
4. Makrigiannakis A, Karamouti M, Drakakis P, Loutradis D, Antsaklis A. Fetomaternal immunotolerance. Am J Reprod Immunol 2008; 60:482–96.
5. Arck PC, Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat Med 2013; 19:548–56.
6. Tafuri A, Alferink J, Moller P, Hammerling GJ, Arnold B. T cell awareness of paternal alloantigens during pregnancy. Science 1995; 270:630–3.
7. Lissauer D, Piper K, Goodyear O, Kilby MD, Moss PA. Fetal-specific CD8+ cytotoxic T cell responses develop during normal human pregnancy and exhibit broad functional capacity. J Immunol 2012; 189:1072–80.
8. Collins MK, Tay CS, Erlebacher A. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J Clin Invest 2009; 119:2062–73.
9. Madeja Z, Yadi H, Apps R et al. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc Natl Acad Sci USA 2011; 108:4012–7.
10. Rowe JH, Ertelt JM, Xin L, Way SS. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature 2012; 490:102–6.
11. Hanna J, Goldman-Wohl D, Hamani Y et al. Decidual NK cells regulate key developmental processes at the human fetal–maternal interface. Nat Med 2006; 12:1065–74.
12. Samstein RM, Josefowicz SZ, Arvey A, Treuting PM, Rudensky AY. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal–fetal conflict. Cell 2012; 150:29–38.
13. Bromley SK, Mempel TR, Luster AD. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat Immunol 2008; 9:970–80.
14. Movahedi K, Guilliams M, Van den Bossche J et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008; 111:4233–44.
15. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791–802.
16. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008; 8:618–31.
17. Goedegebuure P, Mitchem JB, Porembka MR et al. Myeloid-derived suppressor cells: general characteristics and relevance to clinical management of pancreatic cancer. Curr Cancer Drug Targets 2011; 11:734–51.
18. De Veirman K, Van Valckenborgh E, Lahmar Q et al. Myeloid-derived suppressor cells as n hematological malignancies. Front Oncol 2014; 4:349.
19. Wesolowski R, Markowitz J, Carson WE III. Myeloid derived suppressor cells – a new therapeutic target in the treatment of cancer. J Immunother Cancer 2013; 1:10.
20. Talmadge JE, Gabrilovich DI. History of myeloid-derived suppressor cells. Nat Rev Cancer 2013; 13:739–52.
21. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9:162–74.
22. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009; 182:4499–506.
23. Mauti LA, Le Bitoux MA, Baumer K et al. Myeloid-derived suppressor cells are implicated in regulating permissiveness for tumor metastasis during mouse gestation. J Clin Invest 2011; 121:2794–807.
24. Rieber N, Gille C, Kostlin N et al. Neutrophilic myeloid-derived suppressor cells in cord blood modulate innate and adaptive immune responses. Clin Exp Immunol 2013; 174:45–52.
25. Kostlin N, Kugel H, Spring B et al. Granulocytic myeloid derived suppressor cells expand in human pregnancy and modulate T-cell responses. Eur J Immunol 2014; 44:2582–91.
26. Gervassi A, Lejarcegui N, Dross S et al. Myeloid derived suppressor cells are present at high frequency in neonates and suppress in vitro T cell responses. PLOS ONE 2014; 9:e107816.
27. Nair RR, Sinha P, Khanna A, Singh K. Reduced myeloid-derived suppressor cells in the blood and endometrium is associated with early miscarriage. Am J Reprod Immunol 2015; 73:479–86.
28. Zhao H, Kalish F, Schulz S, Yang Y, Wong RJ, Stevenson DK. Unique roles of infiltrating myeloid cells in the murine uterus during early to midpregnancy. J Immunol 2015; 194:3713–22.
29. Grutzner E, Stirner R, Arenz L et al. Kinetics of human myeloid-derived suppressor cells after blood draw. J Transl Med 2016; 14:2.
30. Qin A, Cai W, Pan T et al. Expansion of monocytic myeloid-derived suppressor cells dampens T cell function in HIV-1-seropositive individuals. J Virol 2013; 87:1477–90.
31. Youn JI, Collazo M, Shalova IN, Biswas SK, Gabrilovich DI. Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J Leukoc Biol 2012; 91:167–81.
32. Zhou J, Cheng P, Youn JI, Cotter MJ, Gabrilovich DI. Notch and wingless signalling cooperate in regulation of dendritic cell differentiation. Immunity 2009; 30:845–59.
33. Lechner MG, Liebertz DJ, Epstein AL. Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J Immunol 2010; 185:2273–84.
34. Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S. Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res 2010; 70:68–77.
35. Rodriguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol Rev 2008; 222:180–91.
36. Sinha P, Okoro C, Foell D, Freeze HH, Ostrand-Rosenberg S, Srikrishna G. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol 2008; 181:4666–75.
37. Kujawski M, Kortylewski M, Lee H, Herrmann A, Kay H, Yu H. Stat-3 mediates myeloid cell-dependent tumor angiogenesis in mice. J Clin Invest 2008; 118:3367–77.
38. Parker KH, Beury DW, Ostrand-Rosenberg S. Myeloid-derived suppressor cells: critical cells driving immune suppression in the tumor microenvironment. Adv Cancer Res 2015; 128:95–139.
39. Vasquez-Dunddel D, Pan F, Zeng Q et al. STAT-3 regulates arginase-I in myeloid-derived suppressor cells from cancer patients. J Clin Invest 2013; 123:1580–9.
40. Ishdorj G, Johnston JB, Gibson SB. Inhibition of constitutive activation of STAT-3 by curcurbitacin-I (JSI-124) sensitized human B-leukemia cells to apoptosis. Mol Cancer Ther 2010; 9:3302–14.
41. Vollbrecht T, Stirner R, Tufman A et al. Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS 2012; 26:F31–37.
42. Yuk JM, Kim TS, Kim SY et al. Orphan nuclear receptor ERRalpha controls macrophage metabolic signalling and A20 expression to negatively regulate TLR-induced inflammation. Immunity 2015; 43:80–91.
43. Chen L, Li W, Qiu W et al. RSRC1 SUMOylation enhances SUMOylation and inhibits transcriptional activity of estrogen receptor beta. FEBS Lett 2015; 589:1476–84.
44. Maneix L, Antonson P, Humire P et al. Estrogen receptor beta exon 3-deleted mouse: the importance of non-ERE pathways in ERbeta signalling. Proc Natl Acad Sci USA 2015; 112:5135–40.
45. Yamamoto T, Matsuda T, Junicho A, Kishi H, Saatcioglu F, Muraguchi A. Cross-talk between signal transducer and activator of transcription 3 and estrogen receptor signalling. FEBS Lett 2000; 486:143–8.
46. Villa A, Rizzi N, Vegeto E, Ciana P, Maggi A. Estrogen accelerates the resolution of inflammation in macrophagic cells. Sci Rep 2015; 5:15224.
47. Liang XH, Deng WB, Li M et al. Egr1 protein acts downstream of estrogen–leukemia inhibitory factor (LIF)-STAT-3 pathway and plays a role during implantation through targeting Wnt4. J Biol Chem 2014; 289:23534–45.