Foxp3+ regulatory T cells ensure B lymphopoiesis by inhibiting the granulopoietic activity of effector T cells in mouse bone marrow

European Journal of Immunology

Volumn 45, Issue 1, 2015, Pages 167-179

  Kim, Sunghoon ^a   Park, Kyungsoo ^b   Choi, Jinwook ^b   Jang, Eunkyeong ^a   Paik, Doo Jin ^a   Seong, Rho H ^b   Youn, Jeehee ^a  

^a Hanyang University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

B lymphopoiesis; Foxp3; Granulopoietins; Hematopoiesis; Regulatory T cells

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; NEUTRALIZING ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BONE MARROW; BONE MARROW CELL; CELL COUNT; CELL DIFFERENTIATION; CELL EXPANSION; CELL POPULATION; CYTOKINE PRODUCTION; EFFECTOR CELL; ERYTHROID CELL; GRANULOPOIESIS; HOMEOSTASIS; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; LYMPHOCYTIC INFILTRATION; LYMPHOID PROGENITOR CELL; LYMPHOPOIESIS; MALE; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINEAGE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; GENETICS; GRANULOCYTE; IMMUNOLOGY; PRIMARY CELL CULTURE; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, NEUTRALIZING; B-LYMPHOCYTES; BONE MARROW CELLS; CELL LINEAGE; CELL PROLIFERATION; FORKHEAD TRANSCRIPTION FACTORS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; GRANULOCYTES; HOMEOSTASIS; INTERFERON-GAMMA; INTERLEUKIN-6; MALE; MICE; MICE, TRANSGENIC; PRIMARY CELL CULTURE; STEM CELLS; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84921061600     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444532     Document Type: Article

References (43)

1. Brunkow, M. E., Jeffery, E. W., Hjerrild, K. A., Paeper, B., Clark, L. B., Yasayko, S. A., Wilkinson, J. E. et al., Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 2001. 27: 68-73.
2. Bennett, C. L., Christie, J., Ramsdell, F., Brunkow, M. E., Ferguson, P. J., Whitesell, L., Kelly, T. E. et al., The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 2001. 27: 20-21.
3. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M. and Toda, M., Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995. 155: 1151-1164.
4. Tadokoro, C. E., Shakhar, G., Shen, S., Ding, Y., Lino, A. C., Maraver, A., Lafaille, J. J. et al., Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J. Exp. Med. 2006. 203: 505-511.
5. Tang, Q., Adams, J. Y., Tooley, A. J., Bi, M., Fife, B. T., Serra, P., Santamaria, P. et al., Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 2006. 7: 83-92.
6. Huehn, J., Siegmund, K., Lehmann, J. C., Siewert, C., Haubold, U., Feuerer, M., Debes, G. F. et al., Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J. Exp. Med. 2004. 199: 303-313.
7. Dudda, J. C., Perdue, N., Bachtanian, E. and Campbell, D. J., Foxp3+ regulatory T cells maintain immune homeostasis in the skin. J. Exp. Med. 2008. 205: 1559-1565.
8. Eksteen, B., Miles, A., Curbishley, S. M., Tselepis, C., Grant, A. J., Walker, L. S. and Adams, D. H., Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10. J. Immunol. 2006. 177: 593-603.
9. Lim, H. W., Broxmeyer, H. E. and Kim, C. H., Regulation of trafficking receptor expression in human forkhead box P3+ regulatory T cells. J. Immunol. 2006. 177: 840-851.
10. Sather, B. D., Treuting, P., Perdue, N., Miazgowicz, M., Fontenot, J. D., Rudensky, A. Y. and Campbell, D. J., Altering the distribution of Foxp3(+) regulatory T cells results in tissue-specific inflammatory disease. J. Exp. Med. 2007. 204: 1335-1347.
11. Wei, S., Kryczek, I., Edwards, R. P., Zou, L., Szeliga, W., Banerjee, M., Cost, M. et al., Interleukin-2 administration alters the CD4+FOXP3+ T-cell pool and tumor trafficking in patients with ovarian carcinoma. Cancer Res. 2007. 67: 7487-7494.
12. Zou, L., Barnett, B., Safah, H., Larussa, V. F., Evdemon-Hogan, M., Mottram, P., Wei, S. et al., Bone marrow is a reservoir for CD4+CD25+ regulatory T cells that traffic through CXCL12/CXCR4 signals. Cancer Res. 2004. 64: 8451-8455.
13. Kondo, M., Wagers, A. J., Manz, M. G., Prohaska, S. S., Scherer, D. C., Beilhack, G. F., Shizuru, J. A. et al., Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu. Rev. Immunol. 2003. 21: 759-806.
14. Arinobu, Y., Mizuno, S., Chong, Y., Shigematsu, H., Iino, T., Iwasaki, H., Graf, T. et al., Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 2007. 1: 416-427.
15. Nagasawa, T., Microenvironmental niches in the bone marrow required for B-cell development. Nat. Rev. Immunol. 2006. 6: 107-116.
16. Basu, S., Hodgson, G., Zhang, H. H., Katz, M., Quilici, C. and Dunn, A. R., Emergency granulopoiesis in G-CSF-deficient mice in response to Candida albicans infection. Blood 2000. 95: 3725-3733.
17. Hirai, H., Zhang, P., Dayaram, T., Hetherington, C. J., Mizuno, S., Imanishi, J., Akashi, K. et al., C/EBPbeta is required for 'emergency' granulopoiesis. Nat. Immunol. 2006. 7: 732-739.
18. Maeda, K., Malykhin, A., Teague-Weber, B. N., Sun, X. H., Farris, A. D. and Coggeshall, K. M., Interleukin-6 aborts lymphopoiesis and elevates production of myeloid cells in systemic lupus erythematosus-prone B6.Sle1.Yaa animals. Blood 2009. 113: 4534-4540.
19. Iwasaki-Arai, J., Iwasaki, H., Miyamoto, T., Watanabe, S. and Akashi, K., Enforced granulocyte/macrophage colony-stimulating factor signals do not support lymphopoiesis, but instruct lymphoid to myelomonocytic lineage conversion. J. Exp. Med. 2003. 197: 1311-1322.
20. Pronk, C. J., Veiby, O. P., Bryder, D. and Jacobsen, S. E., Tumor necrosis factor restricts hematopoietic stem cell activity in mice: involvement of two distinct receptors. J. Exp. Med. 2011. 208: 1563-1570.
21. Lee, J. H., Wang, C. and Kim, C. H., FoxP3+ regulatory T cells restrain splenic extramedullary myelopoiesis via suppression of hemopoietic cytokine-producing T cells. J. Immunol. 2009. 183: 6377-6386.
22. Leonardo, S. M., Josephson, J. A., Hartog, N. L. and Gauld, S. B., Altered B cell development and anergy in the absence of Foxp3. J. Immunol. 2010. 185: 2147-2156.
23. Chang, S. E., Guo, L., Tian, J., Liu, Y., Guo, Z., Zheng, B. and Han, S., Autoimmune bone marrow environment severely inhibits B cell development by inducing extensive cell death and inhibiting proliferation. Autoimmunity 2012. 45: 210-217.
24. Urbieta, M., Barao, I., Jones, M., Jurecic, R., Panoskaltsis-Mortari, A., Blazar, B. R., Murphy, W. J. et al., Hematopoietic progenitor cell regulation by CD4+CD25+ T cells. Blood 2010. 115: 4934-4943.
25. Riewaldt, J., Duber, S., Boernert, M., Krey, M., Dembinski, M., Weiss, S., Garbe, A. I. et al., Severe developmental B lymphopoietic defects in Foxp3-deficient mice are refractory to adoptive regulatory T cell therapy. Front Immunol. 2012. 3: 141.
26. Chang, X., Gao, J. X., Jiang, Q., Wen, J., Seifers, N., Su, L., Godfrey, V. L. et al., The Scurfy mutation of FoxP3 in the thymus stroma leads to defective thymopoiesis. J. Exp. Med. 2005. 202: 1141-1151.
27. Zuo, T., Wang, L., Morrison, C., Chang, X., Zhang, H., Li, W., Liu, Y. et al., FOXP3 is an X-linked breast cancer suppressor gene and an important repressor of the HER-2/ErbB2 oncogene. Cell 2007. 129: 1275-1286.
28. Sundin, M., D'Arcy, P., Johansson, C. C., Barrett, A. J., Lonnies, H., Sundberg, B., Nava, S. et al., Multipotent mesenchymal stromal cells express FoxP3: a marker for the immunosuppressive capacity? J. Immunother. 2011. 34: 336-342.
29. Seder, R. A. and Paul, W. E., Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annu. Rev. Immunol. 1994. 12: 635-673.
30. Monteiro, J. P., Benjamin, A., Costa, E. S., Barcinski, M. A. and Bonomo, A., Normal hematopoiesis is maintained by activated bone marrow CD4+ T cells. Blood 2005. 105: 1484-1491.
31. Rolink, A., ten Boekel, E., Melchers, F., Fearon, D. T., Krop, I. and Andersson, J., A subpopulation of B220+ cells in murine bone marrow does not express CD19 and contains natural killer cell progenitors. J. Exp. Med. 1996. 183: 187-194.
32. Adolfsson, J., Mansson, R., Buza-Vidas, N., Hultquist, A., Liuba, K., Jensen, C. T., Bryder, D. et al., Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 2005. 121: 295-306.
33. Chen, C., Liu, Y., Liu, Y. and Zheng, P., Mammalian target of rapamycin activation underlies HSC defects in autoimmune disease and inflammation in mice. J. Clin. Invest. 2010. 120: 4091-4101.
34. Grawunder, U., Melchers, F. and Rolink, A., Interferon-gamma arrests proliferation and causes apoptosis in stromal cell/interleukin-7-dependent normal murine pre-B cell lines and clones in vitro, but does not induce differentiation to surface immunoglobulin-positive B cells. Eur. J. Immunol. 1993. 23: 544-551.
35. Garvy, B. A. and Riley, R. L., IFN-gamma abrogates IL-7-dependent proliferation in pre-B cells, coinciding with onset of apoptosis. Immunology 1994. 81: 381-388.
36. Zhou, X., Bailey-Bucktrout, S. L., Jeker, L. T., Penaranda, C., Martinez-Llordella, M., Ashby, M., Nakayama, M. et al., Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 2009. 10: 1000-1007.
37. Yang, X. O., Nurieva, R., Martinez, G. J., Kang, H. S., Chung, Y., Pappu, B. P., Shah, B. et al., Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 2008. 29: 44-56.
38. Valencia, X., Stephens, G., Goldbach-Mansky, R., Wilson, M., Shevach, E. M. and Lipsky, P. E., TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 2006. 108: 253-261.
39. Jang, E., Kim, H. R., Cho, S. H., Paik, D. J., Kim, J. M., Lee, S. K. and Youn J., Prevention of spontaneous arthritis by inhibiting homeostatic expansion of autoreactive CD4+ T cells in the K/BxN mouse model. Arthritis Rheum. 2006. 54: 492-498.
40. Haribhai, D., Lin, W., Relland, L. M., Truong, N., Williams, C. B. and Chatila, T. A., Regulatory T cells dynamically control the primary immune response to foreign antigen. J. Immunol. 2007. 178: 2961-2972.
41. Kouskoff, V., Korganow, A. S., Duchatelle, V., Degott, C., Benoist, C. and Mathis, D., Organ-specific disease provoked by systemic autoimmunity. Cell 1996. 87: 811-822.
42. Jang, E., Cho, W. S., Cho, M. L., Park, H. J., Oh, H. J., Kang, S. M., Paik, D. J. et al., Foxp3+ regulatory T cells control humoral autoimmunity by suppressing the development of long-lived plasma cells. J. Immunol. 2011. 186: 1546-1553.
43. Choi, J., Ko, M., Jeon, S., Jeon, Y., Park, K., Lee, C., Lee, H. and Seong, R. H., The SWI/SNF-like BAF complex is essential for early B cell development. J. Immunol. 2012. 188: 3791-3803.