Regulatory T cells orchestrate similar immune evasion of fetuses and tumors in mice

Journal of Immunology

Volumn 196, Issue 2, 2016, Pages 678-690

  Nehar Belaid, Djamel ^a,b   Courau, Tristan ^a,b   Derian, Nicolas ^a,b   Florez, Laura ^a,b   Ruocco, Maria Grazia ^a,b   Klatzmann, David ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b UMR S 959 ^*  (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FETUS; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T CELL DEPLETION; TRANSCRIPTOMICS; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; FETUS DEVELOPMENT; IMMUNOLOGY; NEOPLASM; TUMOR ESCAPE;

ANIMALS; FEMALE; FETAL DEVELOPMENT; FETUS; IMMUNE TOLERANCE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASMS; T-LYMPHOCYTES, REGULATORY; TRANSCRIPTOME; TUMOR ESCAPE;

EID: 84954115963     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501834     Document Type: Article

References (61)

1. Ferretti, C., L. Bruni, V. Dangles-Marie, A. P. Pecking, and D. Bellet. 2007. Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts. Hum. Reprod. Update 13: 121-141.
2. Holtan, S. G., D. J. Creedon, P. Haluska, and S. N. Markovic. 2009. Cancer and pregnancy: parallels in growth, invasion, and immune modulation and implications for cancer therapeutic agents. Mayo Clin. Proc. 84: 985-1000.
3. Ohlsson, R. 1989. Growth factors, protooncogenes and human placental development. Cell Differ. Dev. 28: 1-15.
4. Strickland, S., and W. G. Richards. 1992. Invasion of the trophoblasts. Cell 71: 355-357.
5. Genbacev, O., Y. Zhou, J. W. Ludlow, and S. J. Fisher. 1997. Regulation of human placental development by oxygen tension. Science 277: 1669-1672.
6. Houghton, A. N. 1994. Cancer antigens: immune recognition of self and altered self. J. Exp. Med. 180: 1-4.
7. Preiss, S., T. Kammertoens, C. Lampert, G. Willimsky, and T. Blankenstein. 2005. Tumor-induced antibodies resemble the response to tissue damage. Int. J. Cancer 115: 456-462.
8. Schumacher, T. N., and R. D. Schreiber. 2015. Neoantigens in cancer immu-notherapy. Science 348: 69-74.
9. Arck, P. C., and K. Hecher. 2013. Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat. Med. 99: 548-556.
10. Barber, E. M., and J. W. Pollard. 2003. The uterine NK cell population requires IL-15 but these cells are not required for pregnancy nor the resolution of a Listeria monocytogenes infection. J. Immunol. 171: 37-46.
11. Fauve, R. M., B. Hevin, H. Jacob, J. A. Gaillard, and F. Jacob. 1974. Antiin-flammatory effects of murine malignant cells. Proc. Natl. Acad. Sci. USA 71: 4052-4056.
12. Ruocco, M. G., G. Chaouat, L. Florez, A. Bensussan, and D. Klatzmann. 2014. Regulatory T-cells in pregnancy: historical perspective, state of the art, and burning questions. Front. Immunol. 5: 389.
13. + regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 10: 347-353.
14. Heikkinen, J., M. Möttönen, A. Alanen, and O. Lassila. 2004. Phenotypic characterization of regulatory T cells in the human decidua. Clin. Exp. Immunol. 136: 373-378.
15. bright regulatory T cells and CTLA-4 expression in peripheral and decidual lymphocytes are down-regulated in human miscarriage. Clin. Immunol. 133: 402-410.
16. bright regulatory T cells in pre-eclampsia. Clin. Exp. Immunol. 149: 139-145.
17. Piccinni, M. P., L. Beloni, C. Livi, E. Maggi, G. Scarselli, and S. Romagnani. 1998. Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat. Med. 4: 1020-1024.
18. Saito, S. 2000. Cytokine network at the feto-maternal interface. J. Reprod. Immunol. 47: 87-103.
19. Curiel, T. J., G. Coukos, L. Zou, X. Alvarez, P. Cheng, P. Mottram, M. Evdemon-Hogan, J. R. Conejo-Garcia, L. Zhang, M. Burow, et al. 2004. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10: 942-949.
20. Galon, J., A. Costes, F. Sanchez-Cabo, A. Kirilovsky, B. Mlecnik, C. Lagorce-Pagès, M. Tosolini, M. Camus, A. Berger, P. Wind, et al. 2006. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964.
21. hi memory Tregs that create a dominant tolerogenic environment for tumors in mice. J. Clin. Invest. 119: 2648-2662.
22. Aluvihare, V. R., M. Kallikourdis, and A. G. Betz. 2004. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5: 266-271.
23. + regulatory/suppressor T cells prevent allogeneic fetus rejection in mice. Immunol. Lett. 102: 106-109.
24. + T cells: a common basis between tumor immunity and autoimmunity. J. Immunol. 163: 5211-5218.
25. Chen, T., G. Darrasse-Jèze, A.-S. Bergot, T. Courau, G. Churlaud, K. Valdivia, J. L. Strominger, M. G. Ruocco, G. Chaouat, and D. Klatzmann. 2013. Self-specific memory regulatory T cells protect embryos at implantation in mice. J. Immunol. 191: 2273-2281.
26. Benoist, C., R. N. Germain, and D. Mathis. 2006. A plaidoyer for "systems immunology". Immunol. Rev. 210: 229-234.
27. Chaussabel, D., C. Quinn, J. Shen, P. Patel, C. Glaser, N. Baldwin, D. Stichweh, D. Blankenship, L. Li, I. Munagala, et al. 2008. A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 29: 150-164.
28. Querec, T. D., R. S. Akondy, E. K. Lee, W. Cao, H. I. Nakaya, D. Teuwen, A. Pirani, K. Gernert, J. Deng, B. Marzolf, et al. 2009. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol. 10: 116-125.
29. Brandes, M., F. Klauschen, S. Kuchen, and R. N. Germain. 2013. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154: 197-212.
30. Pham, H.-P., N. Dérian, W. Chaara, B. Bellier, D. Klatzmann, and A. Six. 2014. A novel strategy for molecular signature discovery based on independent component analysis. Int. J. Data Min. Bioinform. 9: 277-304.
31. Hyvärinen, A., and E. Oja. 2000. Independent component analysis: algorithms and applications. Neural Netw. 13: 411-430.
32. Subramanian, A., P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R. Golub, E. S. Lander, and J. P. Mesirov. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102: 15545-15550.
33. Shannon, P., A. Markiel, O. Ozier, N. S. Baliga, J. T. Wang, D. Ramage, N. Amin, B. Schwikowski, and T. Ideker. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13: 2498-2504.
34. Merico, D., R. Isserlin, O. Stueker, A. Emili, and G. D. Bader. 2010. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One 5: e13984.
35. Jaccard, P. 1901. Bull. Soc. Vaud. Sci. Nat.
36. Yu, G., F. Li, Y. Qin, X. Bo, Y. Wu, and S. Wang. 2010. GOSemSim: an R package for measuring semantic similarity among GO terms and gene products. Bioinformatics 26: 976-978.
37. Tzachanis, D., and V. A. Boussiotis. 2009. Tob, a member of the APRO family, regulates immunological quiescence and tumor suppression. Cell Cycle 8: 1019-1025.
38. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, et al. 2000. Gene ontology: tool for the unification of biology. Nat. Genet. 25: 25-29.
39. Zheng, Y., S. Z. Josefowicz, A. Kas, T.-T. Chu, M. A. Gavin, and A. Y. Rudensky. 2007. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445: 936-940.
40. Marson, A., K. Kretschmer, G. M. Frampton, E. S. Jacobsen, J. K. Polansky, K. D. MacIsaac, S. S. Levine, E. Fraenkel, H. von Boehmer, and R. A. Young. 2007. Foxp3 occupancy and regulation of key target genes during T-cell stim ulation. Nature 445: 931-935.
41. Karlsson, G., Y. Liu, J. Larsson, M.-J. Goumans, J.-S. Lee, S. S. Thorgeirsson, M. Ringnér, and S. Karlsson. 2005. Gene expression profiling demonstrates that TGF-b1 signals exclusively through receptor complexes involving Alk5 and identifies targets of TGF-b signaling. Physiol. Genomics 21: 396-403.
42. + cutaneous T-cell lymphoma cells. Cancer Res. 68: 1083-1091.
43. Medawar, P. 1953. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 7: 320-338.
44. Gobert, M., and J. J. Lafaille. 2012. Maternal-fetal immune tolerance, block by block. Cell 150: 7-9.
45. Erlebacher, A. 2013. Mechanisms of T cell tolerance towards the allogeneic fetus. Nat. Rev. Immunol. 13: 23-33.
46. Smyth, M. J., Y. Hayakawa, K. Takeda, and H. Yagita. 2002. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat. Rev. Cancer 2: 850-861.
47. Liotta, L. A., and E. C. Kohn. 2001. The microenvironment of the tumour-host interface. Nature 411: 375-379.
48. Schumacher, A., S.-D. Costa, and A. C. Zenclussen. 2014. Endocrine factors modulating immune responses in pregnancy. Front. Immunol. 5: 196.
49. Gavin, M. A., J. P. Rasmussen, J. D. Fontenot, V. Vasta, V. C. Manganiello, J. A. Beavo, and A. Y. Rudensky. 2007. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 445: 771-775.
50. + regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198: 235-247.
51. + T cells. Immunity 19: 877-889.
52. Gardner, L., and A. Moffett. 2003. Dendritic cells in the human decidua. Biol. Reprod. 69: 1438-1446.
53. Blois, S., M. Tometten, J. Kandil, E. Hagen, B. F. Klapp, R. A. Margni, and P. C. Arck. 2005. Intercellular adhesion molecule-1/LFA-1 cross talk is a proximate mediator capable of disrupting immune integration and tolerance mechanism at the feto-maternal interface in murine pregnancies. J. Immunol. 174: 1820-1829.
54. Habbeddine, M., P. Verbeke, S. Karaz, P. Bobé, and C. Kanellopoulos-Langevin. 2014. Leukocyte population dynamics and detection of IL-9 as a major cytokine at the mouse fetal-maternal interface. PLoS One 9: e107267.
55. + T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol. Reprod. 80: 1036-1045.
56. Kim, B.-J., Y.-M. Choi, S.-Y. Rah, D.-R. Park, S.-A. Park, Y.-J. Chung, S.-M. Park, J. K. Park, K. Y. Jang, and U.-H. Kim. 2015. Seminal CD38 is a pivotal regulator for fetomaternal tolerance. Proc. Natl. Acad. Sci. USA 112: 1559-1564.
57. Youn, J.-I., M. Collazo, I. N. Shalova, S. K. Biswas, and D. I. Gabrilovich. 2012. Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J. Leukoc. Biol. 91: 167-181.
58. Samstein, R. M., S. Z. Josefowicz, A. Arvey, P. M. Treuting, and A. Y. Rudensky. 2012. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 150: 29-38.
59. Sontag, S. 1978. Illness as Metaphor. Farrar, Straus and Giroux, New York.
60. Saadoun, D., M. Rosenzwajg, F. Joly, A. Six, F. Carrat, V. Thibault, D. Sene, P. Cacoub, and D. Klatzmann. 2011. Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N. Engl. J. Med. 365: 2067-2077.
61. Klatzmann, D., and A. K. Abbas. 2015. The promise of low-dose interleukin-2 therapy for autoimmune and inflammatory diseases. Nat. Rev. Immunol. 15: 283-294.