Granulocytic myeloid derived suppressor cells expand in human pregnancy and modulate T-cell responses

European Journal of Immunology

Volumn 44, Issue 9, 2014, Pages 2582-2591

  Köstlin, Natascha ^a   Kugel, Hellen ^a   Spring, Bärbel ^a   Leiber, Anja ^a   Marmé, Alexander ^b   Henes, Melanie ^c   Rieber, Nikolaus ^a   Hartl, Dominik ^a   Poets, Christian F ^a   Gille, Christian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Am Lustnauer Tor   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Myeloid derived suppressor cells (MDSCs); Reproductive immunology; T cells; Tolerance

Indexed keywords

ARGINASE; ARGINASE I, HUMAN; INDUCIBLE NITRIC OXIDE SYNTHASE; NOS2 PROTEIN, HUMAN;

ADOLESCENT; ADULT; ARTICLE; BONE MARROW CELL; CLINICAL TRIAL; COMPARATIVE STUDY; CYTOLOGY; FEMALE; FETUS BLOOD; GENE EXPRESSION REGULATION; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MIDDLE AGED; MYELOID-DERIVED SUPPRESSOR CELLS (MDSCS); PHYSIOLOGY; PREGNANCY; REPRODUCTIVE IMMUNOLOGY; T LYMPHOCYTE; TOLERANCE;

MYELOID-DERIVED SUPPRESSOR CELLS (MDSCS); REPRODUCTIVE IMMUNOLOGY; T CELLS; TOLERANCE;

ADOLESCENT; ADULT; ARGINASE; FEMALE; FETAL BLOOD; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; IMMUNE TOLERANCE; MIDDLE AGED; MYELOID CELLS; NITRIC OXIDE SYNTHASE TYPE II; PREGNANCY; T-LYMPHOCYTES;

EID: 84907818476     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344200     Document Type: Article

References (48)

1. Goldenberg, R. L., Culhane, J. F., Iams, J. D. andRomero, R., Epidemiology and causes of preterm birth. Lancet 2008. 371: 75-84.
2. McCormick, M. C., The contribution of low birth weight to infantmortality and childhood morbidity. N. Engl. J. Med. 1985. 312: 82-90.
3. Bansal, A. S., Joining the immunological dots in recurrent miscarriage. Am. J. Reprod. Immunol. 2010. 64: 307-315.
4. Warning, J. C., McCracken, S. A. andMorris, J. M., A balancing act: mechanisms by which the fetus avoids rejection by the maternal immune system. Reproduction 2011. 141: 715-724.
5. Arck, P. C. and Hecher, K., Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat. Med. 2013. 19: 548- 556.
6. Erlebacher, A., Mechanisms of T cell tolerance towards the allogeneic fetus. Nat. Rev. Immunol. 2013. 13: 23-33.
7. Saito, S., Nakashima, A., Shima, T. and Ito, M., Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am. J. Reprod. Immunol. 2010. 63: 601-610.
8. Gabrilovich, D. I. and Nagaraj, S., Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009. 9: 162-174.
9. Rodriguez, P. C., Ernstoff, M. S., Hernandez, C., Atkins, M., Zabaleta, J., Sierra, R. and Ochoa, A. C., Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 2009. 69: 1553-1560.
10. Zea, A. H., Rodriguez, P. C., Atkins, M. B., Hernandez, C., Signoretti, S., Zabaleta, J., McDermott, D. et al., Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: amechanism of tumor evasion. Cancer Res. 2005. 65: 3044-3048.
11. Brandau, S., Trellakis, S., Bruderek, K., Schmaltz, D., Steller, G., Elian,M., Suttmann, H. et al., Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J. Leukoc. Biol. 2011. 89: 311-317.
12. Greten, T. F., Manns, M. P. and Korangy, F., Myeloid derived suppressor cells in human diseases. Int. Immunopharmacol. 2011. 11: 802-807.
13. Diaz-Montero, C. M., Salem, M. L., Nishimura, M. I., Garrett-Mayer, E., Cole, D. J. and Montero, A. J., Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol. Immunother. 2009. 58: 49-59.
14. Ochoa, A. C., Zea, A. H., Hernandez, C. and Rodriguez, P. C., Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma. Clin. Cancer Res. 2007. 13: 721s-726s.
15. Youn, J. I., Nagaraj, S., Collazo, M. and Gabrilovich, D. I., Subsets of myeloid-derived suppressor cells in tumor-bearingmice. J. Immunol. 2008. 181: 5791-5802.
16. Goni, O., Alcaide, P. and Fresno, M., Immunosuppression during acute Trypanosoma cruzi infection: involvement of Ly6G (Gr1(+))CD11b(+)immature myeloid suppressor cells. Int. Immunol. 2002. 14: 1125-1134.
17. Luyckx, A., Schouppe, E., Rutgeerts, O., Lenaerts, C., Koks, C., Fevery, S., Devos, T. et al., Subset characterization of myeloid-derived suppressor cells arising during induction of BM chimerism in mice. Bone Marrow Transplant. 2011. 47: 985-992.
18. Makarenkova, V. P., Bansal, V., Matta, B. M., Perez, L. A. and Ochoa, J. B., CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J. Immunol. 2006. 176: 2085-2094.
19. Zhu, B., Bando, Y., Xiao, S., Yang, K.,Anderson, A. C., Kuchroo, V. K. and Khoury, S. J., CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J. Immunol. 2007. 179: 5228-5237.
20. Rieber, N., Gille, C., Kostlin, N., Schafer, I., Spring, B., Ost, M., Spieles, H. et al., Neutrophilic myeloid-derived suppressor cells in cord blood modulate innate and adaptive immune responses. Clin. Exp. Immunol. 2013. 174: 45-52.
21. Teklenburg, G., Salker, M., Heijnen, C., Macklon, N. S. and Brosens, J. J., The molecular basis of recurrent pregnancy loss: impaired natural embryo selection. Mol. Hum. Reprod. 2010. 16: 886-895.
22. Delano, M. J., Scumpia, P. O., Weinstein, J. S., Coco, D., Nagaraj, S., Kelly-Scumpia, K. M., O'Malley, K. A. et al., MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med. 2007. 204: 1463-1474.
23. Mauti, L. A., Le Bitoux, M. A., Baumer, K., Stehle, J. C., Golshayan, D., Provero, P. and Stamenkovic, I., Myeloid-derived suppressor cells are implicated in regulating permissiveness for tumor metastasis during mouse gestation. J. Clin. Invest. 2011. 121: 2794-2807.
24. Andraweera, P. H., Dekker, G. A. and Roberts, C. T., The vascular endothelial growth factor family in adverse pregnancy outcomes. Hum. Reprod. Update 2012. 18: 436-457.
25. Dimitriadis, E., White, C. A., Jones, R. L. and Salamonsen, L. A., Cytokines, chemokines and growth factors in endometrium related to implantation. Hum. Reprod. Update 2005. 11: 613-630.
26. Hunt, J. S., Petroff, M. G., McIntire, R. H. and Ober, C., HLA-G and immune tolerance in pregnancy. FASEB J. 2005. 19: 681-693.
27. Agaugue, S., Carosella, E. D. and Rouas-Freiss, N., Role of HLA-G in tumor escape through expansion of myeloid-derived suppressor cells and cytokinic balance in favor of Th2 versus Th1/Th17. Blood 2011. 117: 7021-7031.
28. Filipazzi, P., Valenti, R., Huber, V., Pilla, L., Canese, P., Iero,M., Castelli, C. et al., Identification of a new subset ofmyeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocytemacrophage colony-stimulation factor-based antitumor vaccine. J. Clin. Oncol. 2007. 25: 2546-2553.
29. Lechner, M. G., Megiel, C., Russell, S. M., Bingham, B., Arger, N., Woo, T. and Epstein, A. L., Functional characterization of human Cd33+ and Cd11b+ myeloid-derived suppressor cell subsets induced from peripheral blood mononuclear cells co-cultured with a diverse set of human tumor cell lines. J. Transl. Med. 2011. 9: 90-110.
30. Obermajer, N., Wong, J. L., Edwards, R. P., Odunsi, K., Moysich, K. and Kalinski, P., PGE(2)-driven induction and maintenance of cancerassociated myeloid-derived suppressor cells. Immunol. Invest. 2012. 41: 635-657.
31. Corzo, C. A., Condamine, T., Lu, L., Cotter, M. J., Youn, J. I., Cheng, P., Cho, H. I. et al., HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp.Med. 2010. 207: 2439-2453.
32. Kusmartsev, S., Nefedova, Y., Yoder, D. and Gabrilovich, D. I., Antigenspecific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 2004. 172: 989-999.
33. Nagaraj, S., Gupta, K., Pisarev, V., Kinarsky, L., Sherman, S., Kang, L., Herber, D. L. et al., Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 2007. 13: 828-835.
34. Elghetany, M. T., Surface antigen changes during normal neutrophilic development: a critical review. Blood Cells Mol. Dis. 2002. 28: 260-274.
35. Conradi, S., Malzahn, U., Paul, F., Quill, S., Harms, L., Then Bergh, F., Ditzenbach, A. et al., Breastfeeding is associated with lower risk formultiple sclerosis. Mult. Scler. 2013. 19: 553-558.
36. Goldstein, A. L., New-onset Graves' disease in the postpartum period. J Midwifery Womens Health 2013. 58: 211-214.
37. Langer-Gould, A. and Beaber, B. E., Effects of pregnancy and breastfeeding on the multiple sclerosis disease course. Clin. Immunol. 2013. 149: 244-250.
38. Kropf, P., Baud, D., Marshall, S. E., Munder, M., Mosley, A., Fuentes, J. M., Bangham, C. R. et al., Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur. J. Immunol. 2007. 37: 935-945.
39. Conrad, K. P., Joffe, G. M., Kruszyna, H., Kruszyna, R., Rochelle, L. G., Smith, R. P., Chavez, J. E. et al., Identification of increased nitric oxide biosynthesis during pregnancy in rats. FASEB J. 1993. 7: 566-571.
40. Molnar, M., Suto, T., Toth, T. and Hertelendy, F., Prolonged blockade of nitric oxide synthesis in gravid rats produces sustained hypertension, proteinuria, thrombocytopenia, and intrauterine growth retardation. Am. J. Obstet. Gynecol. 1994. 170: 1458-1466.
41. Valdes, G., Kaufmann, P., Corthorn, J., Erices, R., Brosnihan, K. B. and Joyner-Grantham, J., Vasodilator factors in the systemic and local adaptations to pregnancy. Reprod. Biol. Endocrinol. 2009. 7: 79-99.
42. McCord, N., Ayuk, P., McMahon, M., Boyd, R. C., Sargent, I. and Redman, C., System y+ arginine transport and NO production in peripheral blood mononuclear cells in pregnancy and preeclampsia. Hypertension 2006. 47: 109-115.
43. Agarwal, A., Gupta, S., Sekhon, L. and Shah, R., Redox considerations in female reproductive function and assisted reproduction: frommolecular mechanisms to health implications. Antioxid. Redox Signal. 2008. 10: 1375- 1403.
44. Agarwal, A., Saleh, R. A. and Bedaiwy, M. A., Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril. 2003. 79: 829-843.
45. Woods, J. R., Jr., Reactive oxygen species and preterm premature rupture of membranes-a review. Placenta 2001. 22 Suppl A: S38-S44.
46. Feng, P. H., Lee, K. Y., Chang, Y. L., Chan, Y. F., Kuo, L. W., Lin, T. Y., Chung, F. T. et al., CD14(+)S100A9(+) monocytic myeloid-derived suppressor cells and their clinical relevance in non-small cell lung cancer. Am. J. Respir. Crit. CareMed. 2012. 186: 1025-1036.
47. Vadillo-Ortega, F., Perichart-Perera, O., Espino, S., Avila-Vergara, M. A., Ibarra, I., Ahued, R., Godines, M. et al., Effect of supplementation during pregnancy with L-arginine and antioxidant vitamins in medical food on pre-eclampsia in high risk population: randomised controlled trial. BMJ 2011. 342: d2901.
48. Wang, Y., Gu, X., Xiang, J. and Chen, Z., Myeloid-derived suppressor cells participate in preventing graft rejection. Clin. Dev. Immunol. 2012. 2012: 731486.