Rapamycin regulates iTreg function through CD39 and Runx1 pathways

Journal of Immunology Research

Volumn 2014, Issue , 2014, Pages

  Lu, Yunjie ^a   Wang, Jirong ^a   Gu, Jian ^a   Lu, Hao ^a   Li, Xiangcheng ^a   Qian, Xiaofeng ^a   Liu, Xiaoshan ^a   Wang, Xuehao ^a   Zhang, Feng ^a   Lu, Ling ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; CD39 ANTIGEN; MESSENGER RNA; RAPAMYCIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR RUNX1; APYRASE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 2; LEUKOCYTE ANTIGEN; RUNX1 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ARTICLE; BLOOD; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INDUCED REGULATORY T LYMPHOCYTE; LYMPHOCYTE FUNCTION; NORMAL HUMAN; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; UPREGULATION; AGONISTS; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

ANTIGENS, CD; APYRASE; CORE BINDING FACTOR ALPHA 2 SUBUNIT; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-2; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; SIROLIMUS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84899509739     PISSN: 23148861     EISSN: 23147156     Source Type: Journal    
DOI: 10.1155/2014/989434     Document Type: Article

References (35)

1. Shevach E. M., Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 2009 30 5 636 645 2-s2.0-65549136983 10.1016/j.immuni. 2009.04.010
2. Hippen K. L., Merkel S. C., Schirm D. K., Nelson C., Tennis N. C., Riley J. L., June C. H., Miller J. S., Wagner J. E., Blazar B. R., Generation and large-scale expansion of human inducible regulatory T cells that suppress graft-versus-host disease. American Journal of Transplantation 2011 11 6 1148 1157 2-s2.0-79958814636 10.1111/j.1600-6143.2011.03558.x
3. Heiber J. F., Geiger T. L., Context and location dependence of adaptive Foxp3(+) regulatory T cell formation during immunopathological conditions. Cellular Immunology 2012 279 1 60 65 10.1016/j.cellimm.2012.09.009
4. Kong N., Lan Q., Chen M., Antigen-specific transforming growth factor beta-induced Treg cells, but not natural Treg cells, ameliorate autoimmune arthritis in mice by shifting the Th17/Treg cell balance from Th17 predominance to Treg cell predominance. Arthritis & Rheumatism 2012 64 8 2548 2558 10.1002/art.34513
5. Bastid J., Cottalorda-Regairaz A., Alberici G., ENTPD1/CD39 is a promising therapeutic target in oncology. Oncogene 2013 32 14 1743 1751 10.1038/onc.2012.269
6. Schuler P. J., Harasymczuk M., Schilling B., Lang S., Whiteside T. L., Separation of human CD4+CD39+ T cells by magnetic beads reveals two phenotypically and functionally different subsets. Journal of Immunological Methods 2011 369 1-2 59 68 2-s2.0-79958781930 10.1016/j.jim.2011.04.004
7. Deaglio S., Dwyer K. M., Gao W., Friedman D., Usheva A., Erat A., Chen J., Enjyoji K., Linden J., Oukka M., Kuchroo V. K., Strom T. B., Robson S. C., Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. Journal of Experimental Medicine 2007 204 6 1257 1265 2-s2.0-34250351459 10.1084/jem.20062512
8. Nikolova M., Carriere M., Jenabian M., Limou S., Younas M., Kök A., Huë S., Seddiki N., Hulin A., Delaneau O., Schuitemaker H., Herbeck J. T., Mullins J. I., Muhtarova M., Bensussan A., Zagury J., Lelievre J., Lévy Y., CD39/adenosine pathway is involved in AIDS progression. PLoS Pathogens 2011 7 7 2-s2.0-79960931448 10.1371/journal.ppat.1002110 e1002110
9. Jenabian M. A., Seddiki N., Yatim A., Regulatory T cells negatively affect IL-2 production of effector T cells through CD39/adenosine pathway in HIV infection. PLOS Pathogens 2013 9 4 e1003319
10. Mandapathil M., Szczepanski M., Harasymczuk M., CD26 expression and adenosine deaminase activity in regulatory T cells (Treg) and CD4(+) T effector cells in patients with head and neck squamous cell carcinoma. Oncoimmunology 2012 1 5 659 669 10.4161/onci.20387
11. Hirschhorn R., Adenosine deaminase deficiency. Immunodeficiency Reviews 1990 2 3 175 198 2-s2.0-0025690483
12. Kaczorowski M., Jutel M., Human T regulatory cells: on the way to cognition. Archivum Immunologiae et Therapiae Experimentalis 2013 61 3 229 236 10.1007/s00005-013-0217-2
13. Bruno L., Mazzarella L., Hoogenkamp M., Hertweck A., Cobb B. S., Sauer S., Hadjur S., Leleu M., Naoe Y., Telfer J. C., Bonifer C., Taniuchi I., Fisher A. G., Merkenschlager M., Runx proteins regulate Foxp3 expression. Journal of Experimental Medicine 2009 206 11 2329 2337 2-s2.0-70449706325 10.1084/jem.20090226
14. Ono M., Yaguchi H., Ohkura N., Kitabayashi I., Nagamura Y., Nomura T., Miyachi Y., Tsukada T., Sakaguchi S., Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 2007 446 7136 685 689 2-s2.0-34247215187 10.1038/nature05673
15. Schaubach B. M., Wen H. Y., Kellems R. E., Regulation of murine Ada gene expression in the placenta by transcription factor RUNX1. Placenta 2006 27 2-3 269 277 2-s2.0-28844496048 10.1016/j.placenta.2005.03.001
16. Saunders R. N., Metcalfe M. S., Nicholson M. L., Rapamycin in transplantation: a review of the evidence. Kidney International 2001 59 1 3 16 2-s2.0-0035165578 10.1046/j.1523-1755.2001.00460.x
17. Sugiyama H., Maeda Y., Nishimori H., Mammalian target of rapamycin inhibitors permit regulatory T cell reconstitution and inhibit experimental chronic graft-versus-host disease. Biology of Blood and Marrow Transplantation 2014 20 2 183 191 10.1016/j.bbmt.2013.11.018
18. Battaglia M., Stabilini A., Roncarolo M., Rapamycin selectively expands CD4+CD25+FoxP3 + regulatory T cells. Blood 2005 105 12 4743 4748 2-s2.0-20444373376 10.1182/blood-2004-10-3932
19. Zhao T., Yang C., Qiu Y., Comparison of regulatory T cells and FoxP3-positive T-cell subsets in the peripheral blood of renal transplant recipients with sirolimus versus cyclosporine: a preliminary study. Transplantation Proceedings 2013 45 1 148 152 10.1016/j.transproceed.2012.06.067
20. Prevel N., Allenbach Y., Klatzmann D., Beneficial role of rapamycin in experimental autoimmune myositis. PLoS ONE 2013 8 11 e74450
21. Donia M., Mangano K., Amoroso A., Mazzarino M. C., Imbesi R., Castrogiovanni P., Coco M., Meroni P., Nicoletti F., Treatment with rapamycin ameliorates clinical and histological signs of protracted relapsing experimental allergic encephalomyelitis in Dark Agouti rats and induces expansion of peripheral CD4+CD25+Foxp3+ regulatory T cells. Journal of Autoimmunity 2009 33 2 135 140 2-s2.0-68249124611 10.1016/j.jaut.2009.06.003
22. Grant C. R., Liberal R., Holder B. S., Dysfunctional CD39 regulatory T cells and aberrant control of T helper type 17 cells in autoimmune hepatitis. Hepatology 2014 59 3 1007 1015 10.1002/hep.26583
23. Zeiser R., Leveson-Gower D. B., Zambricki E. A., Kambham N., Beilhack A., Loh J., Hou J., Negrin R. S., Differential impact of mammalian target of rapamycin inhibition on CD4 +CD25+Foxp3+ regulatory T cells compared with conventional CD4+ T cells. Blood 2008 111 1 453 462 2-s2.0-38049177784 10.1182/blood-2007-06-094482
24. Whiteside T. L., Regulatory T cell subsets in human cancer: are they regulating for or against tumor progression? Cancer Immunology, Immunotherapy 2014 63 1 67 72 10.1007/s00262-013-1490-y
25. Sauer A. V., Brigida I., Carriglio N., Hernandez R. J., Scaramuzza S., Clavenna D., Sanvito F., Poliani P. L., Gagliani N., Carlucci F., Tabucchi A., Roncarolo M. G., Traggiai E., Villa A., Aiuti A., Alterations in the adenosine metabolism and CD39/CD73 adenosinergic machinery cause loss of Treg cell function and autoimmunity in ADA-deficient SCID. Blood 2012 119 6 1428 1439 2-s2.0-84856838658 10.1182/blood-2011-07-366781
26. Borsellino G., Kleinewietfeld M., Di Mitri D., Sternjak A., Diamantini A., Giometto R., Höpner S., Centonze D., Bernardi G., Dell'Acqua M. L., Rossini P. M., Battistini L., Rötzschke O., Falk K., Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 2007 110 4 1225 1232 2-s2.0-34547098277 10.1182/blood-2006-12-064527
27. Mandapathil M., Lang S., Gorelik E., Whiteside T. L., Isolation of functional human regulatory T cells (Treg) from the peripheral blood based on the CD39 expression. Journal of Immunological Methods 2009 346 1-2 55 63 2-s2.0-67449128008 10.1016/j.jim.2009.05.004
28. Alam M. S., Kurtz C. C., Rowlett R. M., Reuter B. K., Wiznerowicz E., Das S., Linden J., Crowe S. E., Ernst P. B., CD73 is expressed by human regulatory T helper cells and suppresses proinflammatory cytokine production and Helicobacter felis-induced gastritis in mice. Journal of Infectious Diseases 2009 199 4 494 504 2-s2.0-61849104046 10.1086/596205
29. Schenk U., Frascoli M., Proietti M., Geffers R., Traggiai E., Buer J., Ricordi C., Westendorf A. M., Grassi F., ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Science Signaling 2011 4 162 ra12 2-s2.0-79952329655 10.1126/scisignal.2001270
30. Mandapathil M., Hilldorfer B., Szczepanski M. J., Czystowska M., Szajnik M., Ren J., Lang S., Jackson E. K., Gorelik E., Whiteside T. L., Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T Cells. Journal of Biological Chemistry 2010 285 10 7176 7186 2-s2.0-77951234655 10.1074/jbc.M109.047423
31. Battaglia M., Stabilini A., Migliavacca B., Horejs-Hoeck J., Kaupper T., Roncarolo M., Rapamycin promotes expansion of functional CD4+CD25 +FOXP3+ regulatory T cells of both healthy subjects and type 1 diabetic patients. Journal of Immunology 2006 177 12 8338 8347 2-s2.0-33845379986
32. Akimova T., Kamath B. M., Goebel J. W., Differing effects of rapamycin or calcineurin inhibitor on T-regulatory cells in pediatric liver and kidney transplant recipients. American Journal of Transplantation 2012 12 12 3449 3461 10.1111/j.1600-6143.2012.04269.x
33. Kitoh A., Ono M., Naoe Y., Ohkura N., Yamaguchi T., Yaguchi H., Kitabayashi I., Tsukada T., Nomura T., Miyachi Y., Taniuchi I., Sakaguchi S., Indispensable role of the Runx1-Cbf β transcription complex for in vivo -suppressive function of FoxP3+ regulatory T cells. Immunity 2009 31 4 609 620 2-s2.0-70349741295 10.1016/j.immuni.2009.09.003
34. Zhang F., Meng G., Strober W., Interactions among the transcription factors Runx1, ROR γ t and Foxp3 regulate the differentiation of interleukin 17-producing T cells. Nature Immunology 2008 9 11 1297 1306 2-s2.0-54549100120 10.1038/ni.1663
35. Yurchenko E., Shio M. T., Huang T. C., da Silva Martins M., Szyf M., Levings M. K., Olivier M., Piccirillo C. A., Inflammation-driven reprogramming of CD4+foxp3+ regulatory T cells into pathogenic Th1/Th17 t effectors is abrogated by mTOR inhibition in vivo. PLoS ONE 2012 7 4 2-s2.0-84860187314 10.1371/journal.pone.0035572 e35572