Mycobacteria-responsive sonic hedgehog signaling mediates programmed death-ligand 1-and prostaglandin e 2-induced regulatory T cell expansion

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Holla, Sahana ^a   Stephen Victor, Emmanuel ^b,c,d   Prakhar, Praveen ^a   Sharma, Meenu ^b,c   Saha, Chaitrali ^b,c,e   Udupa, Vibha ^a   Kaveri, Srinivas V ^b,c,d,f   Bayry, Jagadeesh ^b,c,d,f   Balaji, Kithiganahalli Narayanaswamy ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b INSERM   (France)

^c CENTRE DE RECHERCHE DES CORDELIERS   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITÉ DE TECHNOLOGIE DE COMPIÈGNE   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOTCH RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROGRAMMED DEATH 1 LIGAND 1; PROSTAGLANDIN E2; SONIC HEDGEHOG PROTEIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD274; CYCLOOXYGENASE 2; DINOPROSTONE; HEDGEHOG PROTEINS; HUMANS; LYMPHOCYTE ACTIVATION; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TOR SERINE-THREONINE KINASES;

EID: 84964407533     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24193     Document Type: Article

References (62)

1. Sakaguchi, S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22, 531-562 (2004).
2. Sakaguchi, S., Miyara, M., Costantino, C. M., Hafler, D. A. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 10, 490-500 (2010).
3. Rouse, B. T., Suvas, S. Regulatory cells and infectious agents: detentes cordiale and contraire. J Immunol 173, 2211-2215 (2004).
4. Mills, K. H. Regulatory T cells: friend or foe in immunity to infection? Nat Rev Immunol 4, 841-855 (2004).
5. Kursar, M. et al. Cutting Edge: Regulatory T cells prevent efficient clearance of Mycobacterium tuberculosis. J Immunol 178, 2661-2665 (2007).
6. Scott-Browne, J. P. et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J Exp Med 204, 2159-2169 (2007).
7. Shafiani, S. et al. Pathogen-specific Treg cells expand early during mycobacterium tuberculosis infection but are later eliminated in response to Interleukin-12. Immunity 38, 1261-1270 (2013).
8. Mahan, C. S., Thomas, J. J., Boom, W. H., Rojas, R. E. CD4+ CD25(high) Foxp3+ regulatory T cells downregulate human Vdelta2+ T-lymphocyte function triggered by anti-CD3 or phosphoantigen. Immunology 127, 398-407 (2009).
9. Li, L., Lao, S. H., Wu, C. Y. Increased frequency of CD4(+ )CD25(high) Treg cells inhibit BCG-specific induction of IFN-gamma by CD4(+ ) T cells from TB patients. Tuberculosis (Edinb) 87, 526-534 (2007).
10. Quinn, K. M. et al. Inactivation of CD4+ CD25+ regulatory T cells during early mycobacterial infection increases cytokine production but does not affect pathogen load. Immunol Cell Biol 84, 467-474 (2006).
11. Shafiani, S., Tucker-Heard, G., Kariyone, A., Takatsu, K., Urdahl, K. B. Pathogen-specific regulatory T cells delay the arrival of effector T cells in the lung during early tuberculosis. J Exp Med 207, 1409-1420 (2010).
12. Josefowicz, S. Z., Lu, L. F., Rudensky, A. Y. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol 30, 531-564 (2012).
13. Vignali, D. A., Collison, L. W., Workman, C. J. How regulatory T cells work. Nat Rev Immunol 8, 523-532 (2008).
14. Barber, D. L., Mayer-Barber, K. D., Feng, C. G., Sharpe, A. H., Sher, A. CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J Immunol 186, 1598-1607 (2011).
15. Periasamy, S. et al. Programmed death 1 and cytokine inducible SH2-containing protein dependent expansion of regulatory T cells upon stimulation With Mycobacterium tuberculosis. J Infect Dis 203, 1256-1263 (2011).
16. Trinath, J., Maddur, M. S., Kaveri, S. V., Balaji, K. N., Bayry, J. Mycobacterium tuberculosis promotes regulatory T-cell expansion via induction of programmed death-1 ligand 1 (PD-L1, CD274) on dendritic cells. J Infect Dis 205, 694-696 (2012).
17. Garg, A. et al. Mannose-capped lipoarabinomannan-and prostaglandin E2-dependent expansion of regulatory T cells in human Mycobacterium tuberculosis infection. Eur J Immunol 38, 459-469 (2008).
18. Narayana, Y., Balaji, K. N. NOTCH1 up-regulation and signaling involved in Mycobacterium bovis BCG-induced SOCS3 expression in macrophages. J Biol Chem 283, 12501-12511 (2008).
19. Bansal, K., Trinath, J., Chakravortty, D., Patil, S. A., Balaji, K. N. Pathogen-specific TLR2 protein activation programs macrophages to induce Wnt-beta-catenin signaling. J Biol Chem 286, 37032-37044 (2011).
20. Ghorpade, D. S. et al. Sonic hedgehog-dependent induction of microRNA 31 and microRNA 150 regulates Mycobacterium bovis BCG-driven toll-like receptor 2 signaling. Mol Cell Biol 33, 543-556 (2013).
21. Holla, S., Kurowska-Stolarska, M., Bayry, J., Balaji, K. N. Selective inhibition of IFNG-induced autophagy by Mir155-and Mir31-responsive WNT5A and SHH signaling. Autophagy 10, 311-330 (2014).
22. Ghorpade, D. S., Kaveri, S. V., Bayry, J., Balaji, K. N. Cooperative regulation of NOTCH1 protein-phosphatidylinositol 3-kinase (PI3K) signaling by NOD1, NOD2, and TLR2 receptors renders enhanced refractoriness to transforming growth factor-beta (TGFbeta)-or cytotoxic T-lymphocyte antigen 4 (CTLA-4)-mediated impairment of human dendritic cell maturation. J Biol Chem 286, 31347-31360 (2011).
23. Bansal, K. et al. PE-PGRS antigens of Mycobacterium tuberculosis induce maturation and activation of human dendritic cells. J Immunol 184, 3495-3504 (2010).
24. Bansal, K. et al. Src homology 3-interacting domain of Rv1917c of Mycobacterium tuberculosis induces selective maturation of human dendritic cells by regulating PI3K-MAPK-NF-kappaB signaling and drives Th2 immune responses. J Biol Chem 285, 36511-36522 (2010).
25. Billiard, F. et al. Dll4-Notch signaling in Flt3-independent dendritic cell development and autoimmunity in mice. J Exp Med 209, 1011-1028 (2012).
26. Asano, N., Watanabe, T., Kitani, A., Fuss, I. J., Strober, W. Notch1 signaling and regulatory T cell function. J Immunol 180, 2796-2804 (2008).
27. Manicassamy, S. et al. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329, 849-853 (2010).
28. van Loosdregt, J. et al. Canonical Wnt signaling negatively modulates regulatory T cell function. Immunity 39, 298-310 (2013).
29. Koyasu, S. The role of PI3K in immune cells. Nat Immunol 4, 313-319 (2003).
30. Koorella, C. et al. Novel regulation of CD80/CD86-induced phosphatidylinositol 3-kinase signaling by NOTCH1 protein in interleukin-6 and indoleamine 2,3-dioxygenase production by dendritic cells. J Biol Chem 289, 7747-7762 (2014).
31. Varjosalo, M., Taipale, J. Hedgehog: functions and mechanisms. Genes Dev 22, 2454-2472 (2008).
32. Fu, Y., Yi, Z., Wu, X., Li, J., Xu, F. Circulating microRNAs in patients with active pulmonary tuberculosis. J Clin Microbiol 49, 4246-4251 (2011).
33. Furci, L., Schena, E., Miotto, P., Cirillo, D. M. Alteration of human macrophages microRNA expression profile upon infection with Mycobacterium tuberculosis. International Journal of Mycobacteriology 2, 128-134 (2013).
34. Hoyne, G. F. et al. Serrate1-induced notch signalling regulates the decision between immunity and tolerance made by peripheral CD4(+ ) T cells. Int Immunol 12, 177-185 (2000).
35. Yvon, E. S. et al. Overexpression of the Notch ligand, Jagged-1, induces alloantigen-specific human regulatory T cells. Blood 102, 3815-3821 (2003).
36. Tsukumo, S., Yasutomo, K. Notch governing mature T cell differentiation. J Immunol 173, 7109-7113 (2004).
37. Bassil, R. et al. Notch ligand delta-like 4 blockade alleviates experimental autoimmune encephalomyelitis by promoting regulatory T cell development. J Immunol 187, 2322-2328 (2011).
38. Riella, L. V. et al. Jagged2-signaling promotes IL-6-dependent transplant rejection. Eur J Immunol 43, 1449-1458 (2013).
39. Kared, H. et al. Jagged2-expressing hematopoietic progenitors promote regulatory T cell expansion in the periphery through notch signaling. Immunity 25, 823-834 (2006).
40. Yuan, J. S., Kousis, P. C., Suliman, S., Visan, I., Guidos, C. J. Functions of notch signaling in the immune system: consensus and controversies. Annu Rev Immunol 28, 343-365 (2010).
41. Amsen, D. et al. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117, 515-526 (2004).
42. Minter, L. M. et al. Inhibitors of gamma-secretase block in vivo and in vitro T helper type 1 polarization by preventing Notch upregulation of Tbx21. Nat Immunol 6, 680-688 (2005).
43. Gentle, M. E., Rose, A., Bugeon, L., Dallman, M. J. Noncanonical Notch signaling modulates cytokine responses of dendritic cells to inflammatory stimuli. J Immunol 189, 1274-1284 (2012).
44. Rutz, S. et al. Notch regulates IL-10 production by T helper 1 cells. Proc Natl Acad Sci USA 105, 3497-3502 (2008).
45. Tu, L. et al. Notch signaling is an important regulator of type 2 immunity. J Exp Med 202, 1037-1042 (2005).
46. Fang, T. C. et al. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27, 100-110 (2007).
47. Mukherjee, S., Schaller, M. A., Neupane, R., Kunkel, S. L., Lukacs, N. W. Regulation of T cell activation by Notch ligand, DLL4, promotes IL-17 production and Rorc activation. J Immunol 182, 7381-7388 (2009).
48. Bugeon, L., Gardner, L. M., Rose, A., Gentle, M., Dallman, M. J. Cutting edge: Notch signaling induces a distinct cytokine profile in dendritic cells that supports T cell-mediated regulation and IL-2-dependent IL-17 production. J Immunol 181, 8189-8193 (2008).
49. Francisco, L. M., Sage, P. T., Sharpe, A. H. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev 236, 219-242 (2010).
50. Amarnath, S. et al. The PDL1-PD1 axis converts human TH1 cells into regulatory T cells. Sci Transl Med 3, 111-120 (2011).
51. Lazar-Molnar, E. et al. Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc Natl Acad Sci USA 107, 13402-13407 (2010).
52. Stephen-Victor, E. et al. Inhibition of Programmed Death 1 Ligand 1 on Dendritic Cells Enhances Mycobacterium-Mediated Interferon gamma (IFN-gamma) Production Without Modulating the Frequencies of IFN-gamma-Producing CD4+ T Cells. J Infect Dis (2014).
53. Trinath, J. et al. Intravenous immunoglobulin expands regulatory T cells via induction of cyclooxygenase-2-dependent prostaglandin E2 in human dendritic cells. Blood 122, 1419-1427 (2013).
54. Baratelli, F. et al. PGE(2) contributes to TGF-beta induced T regulatory cell function in human non-small cell lung cancer. Am J Transl Res 2, 356-367 (2010).
55. Baratelli, F. et al. Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4+ T cells. J Immunol 175, 1483-1490 (2005).
56. Zelenay, S. et al. Cyclooxygenase-Dependent Tumor Growth through Evasion of Immunity. Cell 162, 1257-1270 (2015).
57. Ghorpade, D. S., Leyland, R., Kurowska-Stolarska, M., Patil, S. A., Balaji, K. N. MicroRNA-155 is required for Mycobacterium bovis BCG-mediated apoptosis of macrophages. Mol Cell Biol 32, 2239-2253 (2012).
58. Wang, C. et al. Comparative miRNA expression profiles in individuals with latent and active tuberculosis. PLoS One 6, e25832 (2011).
59. Ceppi, M. et al. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci USA 106, 2735-2740 (2009).
60. Turner, M. L., Schnorfeil, F. M., Brocker, T. MicroRNAs regulate dendritic cell differentiation and function. J Immunol 187, 3911-3917 (2011).
61. Basu, J., Shin, D. M., Jo, E. K. Mycobacterial signaling through toll-like receptors. Front Cell Infect Microbiol 2, 145 (2012).
62. Kapoor, N., Narayana, Y., Patil, S. A., Balaji, K. N. Nitric oxide is involved in Mycobacterium bovis bacillus Calmette-Guerinactivated Jagged1 and Notch1 signaling. J Immunol 184, 3117-3126 (2010).