Preview

Medical Immunology (Russia)

Advanced search

MOLECULAR AND CELLULAR MECHANISMS MEDIATED BY DENDRITIC CELLS INVOLVED IN THE INDUCTION OF TOLERANCE

https://doi.org/10.15789/1563-0625-2017-4-359-374

Abstract

Autoimmune diseases  and  complications  after  transplantation  operations are  major   public health  problem, as they often  lead to deterioration in the quality  of life, reduce  work capacity  and  disability in the  population. To date, the  induction of antigen-specific tolerance is the  promising method of therapy. During this process dendritic cells play important role.  In  this review current data  of tolerogenic dendritic cells characterization, of factors inducing tolerogenic properties in dendritic cells, development of central  and peripheral tolerance by dendritic cells, role of tolerogenic dendritic cells in the formation of regulatory B cells, molecular and cellular mechanisms that are involved in the formation of an immunological tolerance depending on tolerogenic dendritic cells were analyzed. Tolerogenic dendritic cells play a key role in maintaining of immune homeostasis by inducing immunological tolerance mechanisms which  are associated with the  generation of regulatory T cells, induction of anergy or apoptosis of T cells. Formation of tolerogenic properties in dendritic cells is occurred by various factors that regulate the maturation and differentiation of dendritic cells and induce anti-inflammatory agents synthesis of them. Because of their ability to induce natural and peripheral regulatory T cells, dendritic cells contribute to the development of the central  and peripheral tolerance in the organism. Analysis of the results  of experimental work demonstrates that  in addition to induction of regulatory T cells tolerogenic dendritic cells participate in generating of regulatory B cells that  play a role in the  formation of tolerance and  have the  ability  to affect  the  population of regulatory T cells. However, the  mechanisms that lead to the formation of B cell population by tolerogenic dendritic cells have not been completely established yet. Review of published data showed that the molecular and cellular mechanisms of immunological tolerance induction by tolerogenic dendritic cells and other regulatory cell subpopulations interacting with each other are similar to a large extent.  Currently, the role of tolerogenic dendritic cells in maintaining of immune tolerance is determined generally, however, some aspects  require  further  investigation. Subsequent experimental studies will lead to a better understanding of the signaling mechanisms and the realization of immunological functions of tolerogenic dendritic cells, which provide additional information for application approaches development of tolerogenic dendritic cells for the control of autoimmune diseases and transplant complications.

About the Authors

S. V. Sennikov
Research Institute of Fundamental and Clinical Immunology
Russian Federation

Sennikov  Sergey V. - PhD, MD (Medicine), Professor, Head, Laboratory of Molecular Immunology.

630099, Novosibirsk, Yandrintsevskaya str., 14, room 301-309. Phone: 7 (383) 222-19-10. Fax: 7 (383) 222-70-28



E. V. Kulikova
Research Institute of Fundamental and Clinical Immunology
Russian Federation

PhD (Biology), Research Associate, Laboratory of Molecular Immunology.

Novosibirsk



N. Yu. Knauer
Research Institute of Fundamental and Clinical Immunology
Russian Federation

Junior Research Associate, Laboratory of Clinical Immunopathology.

Novosibirsk



Yu. N. Khantakova
Research Institute of Fundamental and Clinical Immunology
Russian Federation

PhD (Medicine), Research Associate, Laboratory of Molecular Immunology.

Novosibirsk 



References

1. Сенников С.В., Облеухова И.А. Методы индукции толерогенных дендритных клеток у животных и человека // Иммунология, 2016. Т. 37, № 5. С. 291-296. [Sennikov S.V., Obleukhova I.A. Methods of induction tolerogenic dendritic cells in animals and humans. Immunologiya = Immunology, 2016, Vol. 37, no. 5, pp. 291-296. (In Russ.)]

2. Фрейдлин И.С. Регуляторные Т-клетки: происхождение и функции // Медицинская иммунология, 2005. Т. 7. № 4. С. 347-354. [Freidlin I.S. Regulatory T-cells: origin and function. Meditsinskaya immunologiya = Medical Immunology (Russia), 2005, Vol. 7, no. 4, pp. 347-354. (In Russ.)] doi:10.15789/1563-0625-2005-4-347-354.

3. Ahmed M.S., Bae Y.S. Dendritic Cell-based Immunotherapy for Rheumatoid Arthritis: from Bench to Bedside. Immune Netw., 2016, Vol. 16, no. 1, pp. 44-51.

4. Amu S., Tarkowski A., Dörner T., Bokarewa M., Brisslert M. The human immunomodulatory CD25+ B cell population belongs to the memory B cell pool. Scand. J. Immunol., 2007, Vol. 66, no. 1, pp. 77-86.

5. Anderson A.E., Isaacs J.D. Tregs and rheumatoid arthritis. Acta Reumatol. Port., 2008, Vol. 33, no. 1, pp. 17-33.

6. Apostolopoulos V., Pietersz G.A., Tsibanis A., Tsikkinis A., Stojanovska L., McKenzie I.F., Vassilaros S. Dendritic cell immunotherapy: clinical outcomes. Clin. Transl. Immunology, 2014, Vol. 3, no. 7, e21. doi: 10.1038/cti.2014.14.

7. Aschenbrenner K., D’Cruz L.M., Vollmann E.H., Hinterberger M., Emmerich J., Swee L.K., Rolink A., Klein L. Selection of Foxp3+ regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat. Immunol., 2007, Vol. 8, no. 4, pp. 351-358.

8. Awasthi A., Carrier Y., Peron J.P., Bettelli E., Kamanaka M., Flavell R.A., Kuchroo V.K., Oukka M., Weiner H.L. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat. Immunol., 2007, Vol. 8, no. 12, pp. 1380-1389.

9. Bar-On L., Birnberg T., Ki K.W., Jun S. Dendritic cell-restricted CD80/86 deficiency results in peripheral regulatory T-cell reduction but is not associated with lymphocyte hyperactivation. Eur. J. Immunol., 2011, Vol. 41, no. 2, pp. 291-298.

10. Belladonna M.L., Grohmann U., Guidetti P., Volpi C., Bianchi R., Fioretti M.C., Schwarcz R., Fallarino F., Puccetti P. Kynurenine pathway enzymes in dendritic cells initiate tolerogenesis in the absence of functional IDO. J. Immunol. 2006, Vol. 177, no. 1, pp. 130-137.

11. Berthelot J.M., Jamin C., Amrouche K., Le Goff B., Maugars Y., Youinou P. Regulatory B cells play a key role in immune system balance. Joint Bone Spine, 2013, Vol. 80, no. 1, pp. 18-22.

12. Birnberg T., Bar-On L., Sapoznikov A., Caton M.L., Cervantes-Barragan L., Makia D., Krauthgamer R., Brenner O., Ludewig B., Brockschnieder D., Riethmacher D., Reizis B., Jung S. Lack of conventional dendritic cells is compatible with normal development and T cell homeostasis, but causes myeloid proliferative syndrome. Immunity, 2008, Vol. 29, no. 6, pp. 986-997.

13. Blair P.A., Noreña L.Y., Flores-Borja F., Rawlings D.J., Isenberg D.A., Ehrenstein M.R., Mauri C. CD19(+) CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity, 2010, Vol. 32, no. 1, pp. 129-140.

14. Bonifaz L., Bonnyay D., Mahnke K., Rivera M., Nussenzweig M.C., Steinman R.M. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med., 2002, Vol. 196, no. 12, pp. 1627-1638.

15. Brenk M., Scheler M., Koch S., Neumann J., Takikawa O., Hacker G., Bieber T., von Bubnoff D. Tryptophan deprivation induces inhibitory receptors ILT3 and ILT4 on dendritic cells favoring the induction of human CD4+CD25+Foxp3+T regulatory cells. J. Immunol., 2009, Vol. 183, no. 1, pp. 145-154.

16. Brown J.A., Dorfman D.M., Ma F.R., Sullivan E.L., Munoz O., Wood C.R., Greenfield E.A., Freeman G.J. Blockade of programmed death-1 ligands on dendritic cells enhances T cell activation and cytokine production. J. Immunol., 2003, Vol. 170, no. 3, pp. 1257-1266.

17. Brusko T.M., Wasserfall C.H., Agarwal A., Kapturczak M.H., Atkinson M.A. An integral role for heme oxygenase-1 and carbon monoxide in maintaining peripheral tolerance by CD4+CD25+ regulatory T cells. J. Immunol., 2005, Vol. 174, no. 9, pp. 5181-5186.

18. Caielli S., Conforti-Andreoni C., Di Pietro C., Usuelli V., Badami E., Malosio M.L., Falcone M. On/off TLR signaling decides proinflammatory or tolerogenic dendritic cell maturation upon CD1d-mediated interaction with invariant NKT cells. J. Immunol., 2010, Vol. 185, no. 12, pp. 7317-7329.

19. Chauveau C., Remy S., Royer P.J., Hill M., Tanguy-Royer S., Hubert F.X., Tesson L., Brion R., Beriou G., Gregoire M., Josien R., Cuturi M.C., Anegon I. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood, 2005, Vol. 106, no. 5, pp. 1694-1702.

20. Chen Z.M., O’Shaughnessy M.J., Gramaglia I., Panoskaltsis-Mortari A., Murphy W.J., Narula S., Roncarolo M.G., Blazar B.R. IL-10 and TGF-β induce alloreactive CD4+CD25+ T cells to acquire regulatory cell function. Blood, 2003, Vol. 101, no. 12, pp. 5076-5083.

21. Colonna M., Nakajima H., Cella M. A family of inhibitory and activating Ig-like receptors that modulate function of lymphoid and myeloid cells. Semin. Immunol., 2000, Vol. 12, no. 2, pp. 121-127.

22. Colonna M., Nakajima H., Navarro F., Lopez-Botet M. A novel family of Ig-like receptors for HLA class I molecules that modulate function of lymphoid and myeloid cells. J. Leukoc. Biol., 1999, Vol. 66, no. 3, pp. 375-381.

23. Cook C.H., Bickerstaff A.A., Wang J.J., Nadasdy T., Della Pelle P., Colvin R.B., Orosz C.G. Spontaneous renal allograft acceptance associated with “regulatory” dendritic cells and IDO. J. Immunol., 2008, Vol. 180, no. 5, pp. 3103-3112.

24. Coombes J.L., Siddiqui K.R., Arancibia-Carcamo C.V., Hall J., Sun C.M., Belkaid Y., Powrie F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med., 2007, Vol. 204, no. 8, pp. 1757-1764.

25. Coquet J.M., Ribot J.C., Bąbała N., Middendorp S., van der Horst G., Xiao Y., Neves J.F., Fonseca-Pereira D., Jacobs H., Pennington D.J., Silva-Santos B., Borst J. Epithelial and dendritic cells in the thymic medulla promote CD4+Foxp3+ regulatory T cell development via the CD27-CD70 pathway. J. Exp. Med., 2013, Vol. 210, no. 4, pp. 715-728.

26. Curti A., Trabanelli S., Salvestrini V., Baccarani M., Lemoli R.M. The role of indoleamine 2,3-dioxygenase in the induction of immune tolerance: focus on hematology. Blood, 2009, Vol. 113, no. 11, pp. 2394-2401.

27. Darrasse-Jeze G., Deroubaix S., Mouquet H., Victora G.D., Eisenreich T., Yao K.H., Masilamani R.F., Dustin M.L., Rudensky A., Liu K., Nussenzweig M.C. Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J. Exp. Med., 2009, Vol. 206, no. 9, pp. 1853-1862.

28. Di Caro V., Phillips B., Engman C., Harnaha J., Trucco M., Giannoukakis N. Involvement of suppressive B-lymphocytes in the mechanism of tolerogenic dendritic cell reversal of type 1 diabetes in NOD mice. PLoS One, 2014, Vol. 9, no. 1, e83575. doi: 10.1371/journal.pone.0083575.

29. Di Caro V., Phillips B., Engman C., Harnaha J., Trucco M., Giannoukakis N. Retinoic acid-producing, exvivo-generated human tolerogenic dendritic cells induce the proliferation ofimmunosuppressive B lymphocytes. Clin. Exp. Immunol., 2013, Vol. 174, no. 2, pp. 302-317.

30. Ezzelarab M, Thomson A.W. Tolerogenic dendritic cells and their role in transplantation. Semin. Immunol., 2011, Vol. 23, no. 4, pp. 252-263.

31. Fife B.T., Pauken K.E., Eagar T.N., Obu T., Wu J., Tang Q., Azuma M., Krummel M.F., Bluestone J.A. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol., 2009, Vol. 10, no. 11, pp. 1185-1192.

32. Fitzgerald D.C., Zhang G.X., El-Behi M., Fonseca-Kelly Z., Li H., Yu S., Saris C.J., Gran B., Ciric B., Rostami A. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat. Immunol., 2007, Vol. 8, no. 12, pp. 1372-1379.

33. Fontenot J.D., Rasmussen J.P., Gavin M.A., Rudensky A.Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol., 2005, Vol. 6, no. 11, pp. 1142-1151.

34. Fryer M., Grahammer J., Khalifian S., Furtmüller G.J , Lee W.P., Raimondi G, Brandacher G. Exploring cell-based tolerance strategies for hand and face transplantation. Expert Rev. Clin. Immunol., 2015, Vol. 11, no. 11, pp. 1189-1204.

35. García-González P., Ubilla-Olguín G., Catalán D., Schinnerling K., Aguillón J.C. Tolerogenic dendritic cells for reprogramming of lymphocyte responses in autoimmune diseases. Autoimmun. Rev., 2016, Vol. 15, no. 11, pp. 1071-1080.

36. Giannoukakis N., Phillips B., Finegold D., Harnaha J., Trucco M. Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients. Diabetes Care, 2011, Vol. 34, no. 9, pp. 2026-2032.

37. Giannoukakis N., Trucco M. A role for tolerogenic dendritic cell-induced B-regulatory cells in type 1 diabetes mellitus. Curr. Opin. Endocrinol. Diabetes Obes., 2012, Vol. 19, no. 4, pp. 279-287.

38. Guilliams M., Crozat K., Henri S., Tamoutounour S., Grenot P., Devilard E., de Bovis B., Alexopoulou L., Dalod M., Malissen B. Skin-draining lymph nodes contain dermis-derived CD103(-) dendritic cells that constitutively produce retinoic acid and induce Foxp3(+) regulatory T cells. Blood, 2010, Vol. 115, no. 10, pp. 1958-1968.

39. Guillonneau C., Aubry V., Renaudin K., Seveno C., Usal C., Tezuka K., Anegon I. Inhibition of chronic rejection and development of tolerogenic T cells after ICOS-ICOSL and CD40-CD40L co-stimulation blockade. Transplantation, 2005, Vol. 80, no. 2, pp. 255-263.

40. Hanabuchi S., Ito T., Park W.R., Watanabe N., Shaw J.L., Roman E., Arima K., Wang Y.H., Voo K.S., Cao W., Liu Y.J. Thymic stromal lymphopoietin-activated plasmacytoid dendritic cells induce the generation of FoxP3+regulatory T cells in human thymus. J. Immunol., 2010, Vol. 184, no. 6, pp. 2999-3007.

41. Hawiger D., Inaba K., Dorsett Y., Guo M., Mahnke K., Rivera M., Ravetch J.V., Steinman R.M., Nussenzweig M.C. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med., 2001, Vol. 194, no. 6, pp. 769-779.

42. Hutloff A., Dittrich A.M., Beier K.C., Eljaschewitsch B., Kraft R., Anagnostopoulos I., Kroczek R.A. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature, 1999, Vol. 397, no. 6716, pp. 263-266.

43. Idoyaga J., Fiorese C., Zbytnuik L., Lubkin A., Miller J., Malissen B., Mucida D., Merad M., Steinman R.M. Specialized role of migratory dendritic cells in peripheral tolerance induction. J. Clin. Invest., 2013, Vol. 123, no. 2, pp. 844-854.

44. Iliev I.D., Spadoni I., Mileti E., Matteoli G., Sonzogni A., Sampietro G.M., Foschi D., Caprioli F., Viale G., Rescigno M. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut, 2009, Vol. 58, no. 11, pp. 1481-1489.

45. Iwata Y., Matsushita T., Horikawa M., DiLillo D.J., Yanaba K., Venturi G.M., Szabolcs P.M., Bernstein S.H., Magro C.M., Williams A.D., Hall R.P., St Clair E.W., Tedder T.F. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood, 2011, Vol. 117, no. 2, pp. 530-541.

46. Jordan M.S., Boesteanu A., Reed A.J., Petrone A.L., Holenbeck A.E., Lerman M.A., Naji A., Caton A.J. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol., 2001, Vol. 2, no. 4, pp. 301-306.

47. Josefowicz S.Z., Niec R.E., Kim H.Y., Treuting P., Chinen T., Zheng Y., Umetsu D.T., Rudensky A.Y. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature, 2011, Vol. 482, no. 7385, pp. 395-399.

48. Kessel A., Haj T., Peri R., Snir A., Melamed D., Sabo E. Human CD19(+)CD25(high) B regulatory cells suppress proliferation of CD4(+) T cells and enhance Foxp3 and CTLA-4 expression in T regulatory cells. Autoimmun. Rev., 2012, Vol. 11, no. 9, pp. 670-677.

49. Koble C., Kyewski B. The thymic medulla: a unique microenvironment for intercellular self-antigen transfer. J. Exp. Med., 2009, Vol. 206, no. 7, pp. 1505-1513.

50. Kretschmer K., Apostolou I., Hawiger D., Khazaie K., Nussenzweig M.C., von Boehmer H. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol., 2005, Vol. 6, no. 12, pp. 1219-1227.

51. Lan Z., Ge W., Arp J., Jiang J., Liu W., Gordon D., Healey D., DeBenedette M., Nicolette C., Garcia B., Wang H. Induction of kidney allograft tolerance by soluble CD83 associated with prevalence of tolerogenic dendritic cells and indoleamine 2,3-dioxygenase. Transplantation, 2010, Vol. 90, no. 12, pp. 1286-1293.

52. Le Friec G., Laupeze B., Fardel O., Sebti Y., Pangault C., Guilloux V., Beauplet A., Fauchet R., Amiot L. Soluble HLA-G inhibits human dendritic cell-triggered allogeneic T-cell proliferation without altering dendritic differentiation and maturation processes. Hum. Immunol., 2003, Vol. 64, no. 8, pp. 752-761.

53. Levings M.K., Gregori S., Tresoldi E., Cazzaniga S., Bonini C., Roncarolo M.G. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood, 2005, Vol. 105, no. 3, pp. 1162-1169.

54. Liang S., Baibakov B., Horuzsko A. HLA-G inhibits the functions of murine dendritic cells via the PIR-B immune inhibitory receptor. Eur. J. Immunol., 2002, Vol. 32, no. 9, pp. 2418-2426.

55. Lio C.W., Hsieh C.S. A two-step process for thymic regulatory T cell development. Immunity, 2008, Vol. 28, no. 1, pp. 100-111.

56. Liston A., Nutsch K.M., Farr A.G., Lund J.M., Rasmussen J.P., Koni P.A., Rudensky A.Y. Differentiation of regulatory Foxp3+ T cells in the thymic cortex. Proc. Natl. Acad. Sci. U.S.A., 2008, Vol. 105, no. 33, pp. 11903-11908.

57. Liu J., Cao X. Regulatory dendritic cells in autoimmunity: a comprehensive review. J. Autoimmun., 2015, Vol. 63, pp. 1-12.

58. Liu Y.J., Soumelis V., Watanabe N., Ito T., Wang Y.H., MalefytRde W., Omori M., Zhou B., Ziegler S.F. TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu. Rev. Immunol., 2007, Vol. 25, pp. 193-219.

59. Luo X., Tarbell K.V., Yang H., Pothoven K., Bailey S.L., Ding R., Steinman R.M, Suthanthiran M. Dendritic cells with TGF-beta1 differentiate naive CD4+CD25T cells into islet-protective Foxp3+ regulatory T cells. Proc. Natl. Acad. Sci. U.S.A., 2007, Vol. 104, no. 8, pp. 2821-2826.

60. Lv H., Havari E., Pinto S., Gottumukkala R.V., Cornivelli L., Raddassi K., Matsui T., Rosenzweig A., Bronson R.T., Smith R., Fletcher A.L., Turley S.J., Wucherpfennig K., Kyewski B., Lipes M.A. Impaired thymic tolerance to alpha-myosin directs autoimmunity to the heart in mice and humans. J. Clin. Invest. 2011, Vol. 121, no. 4, pp. 1561-1573.

61. Mahmud S.A., Manlove L.S., Schmitz H.M., Xing Y., Wang Y., Owen D.L., Schenkel J.M., Boomer J.S., Green J.M., Yagita H., Chi H., Hogquist K.A., Farrar M.A. Costimulation via the tumor-necrosis factor receptor superfamily couples TCR signal strength to the thymic differentiation of regulatory T cells. Nat. Immunol, 2014, Vol. 15, no. 5, pp. 473-481.

62. Mahnke K., Schmitt E., Bonifaz L., Henk A., Jonuleit H. Immature, but not inactive: the tolerogenic function of immature dendritic cells. Immunol. Cell Biol., 2002, Vol. 80, no. 5, pp. 477-483.

63. Manavalan J.S., Rossi P.C., Vlad G., Piazza F., Yarilina A., Cortesini R., Mancini D., Suciu-Foca N. High expression of ILT3 and ILT4 is a general feature of tolerogenic dendritic cells. Transpl. Immunol., 2003, Vol. 11, no. 3-4, pp. 245-258.

64. Mauri C., Menon M. The expanding family of regulatory B cells. Int. Immunol., 2015, Vol. 27, no. 10, pp. 479-486.

65. Mazzucchelli R., Hixon J.A., Spolski R., Chen X., Li W.Q., Hall V.L., Willette-Brown J., Hurwitz A.A., Leonard W.J., Durum S.K. Development of regulatory T cells requires IL-7Ralpha stimulation by IL-7 or TSLP. Blood, 2008, Vol. 112, no. 8, pp. 3283-3292.

66. Mellor A.L., Munn, D.H. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol., 2004, Vol. 4, no. 10, pp. 762-774.

67. Moreau A., Hill M., Thebault P., Deschamps J.Y., Chiffoleau E., Chauveau C., Moullier P., Anegon I., AlliotLicht B., Cuturi M.C. Tolerogenic dendritic cells actively inhibit T cells through heme oxygenase-1 in rodents and in nonhuman primates. FASEB J., 2009, Vol. 23, no. 9, pp. 3070-3077.

68. Morelli A.E., Thomson A.W. Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol. Rev, 2003, Vol. 196, pp. 125-146.

69. Nencioni A., Beck J., Werth D., Grünebach F., Patrone F., Ballestrero A., Brossart P. Histone deacetylase inhibitors affect dendritic cell differentiation and immunogenicity. Clin. Cancer Res., 2007, Vol. 13, no. 13, pp. 3922-3941.

70. Oh J., Shin J.S. The Role of Dendritic Cells in Central Tolerance. Immune Netw., 2015, Vol. 15, no. 3, pp. 111-120.

71. Ohnmacht C., Pullner A., King S.B., Drexler I., Meier S., Brocker T., Voehringer D. Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J. Exp. Med., 2009, Vol. 206, no. 3, pp. 549-559.

72. Pallotta M.T., Orabona C., Volpi C., Vacca C., Belladonna M.L., Bianchi R., Servillo G., Brunacci C., Calvitti M., Bicciato S., Mazza E.M., Boon L., Grassi F., Fioretti M.C., Fallarino F., Puccetti P., Grohmann U. Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat. Immunol., 2011, Vol. 12, no. 9, pp. 870-878.

73. Park J.H., Choi A.J., Kim S.J., Jeong S.Y. 3,3’-Diindolylmethane Inhibits Flt3L/GM-CSF-induced-bone Marrow-derived CD103(+) Dendritic Cell Differentiation Regulating Phosphorylation of STAT3 and STAT5. Immune Netw., 2015, Vol. 15, no. 6, pp. 278-290.

74. Probst H.C., Muth S., Schild H. Regulation of the tolerogenic function of steady-state DCs. Eur. J. Immunol., 2014, Vol. 44, no. 4, pp. 927-933.

75. Qian L., Qian C., Chen Y., Bai Y., Bao Y., Lu L., Cao X. Regulatory dendritic cells program B cells to differentiate into CD19hiFcγIIbhi regulatory B cells through IFN-β and CD40L. Blood, 2012, Vol. 120, no. 3, pp. 581-591.

76. Ristich V., Liang S., Zhang W., Wu J., Horuzsko A. Tolerization of dendritic cells by HLA-G. Eur. J. Immunol., 2005, Vol. 35, no. 4, pp. 1133-1142.

77. Ronet C., Hauyon-La Torre Y., Revaz-Breton M., Mastelic B., Tacchini-Cottier F., Louis J., Launois P. Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J. Immunol., 2010, Vol. 184, no. 2, pp. 886-894.

78. Salomon B., Lenschow D. J., Rhee L., Ashourian N., Singh B., Sharpe A., Bluestone J.A. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity, 2000, Vol. 12, no. 4, pp. 431-440.

79. Soares M.P., Bach F.H. Heme oxygenase-1: from biology to therapeutic potential. Trends Mol. Med., 2009, Vol. 15, no. 2, pp. 50-58.

80. Steinman R.M., Hawiger D., Nussenzweig M.C. Tolerogenic dendritic cells. Annu. Rev. Immunol., 2003, Vol. 21, pp. 685-711.

81. Strainic M.G., Shevach E.M., An F., Lin F., Medof M.E. Absence of signaling into CD4(+) cells via C3aR and C5aR enables autoinductive TGF-beta1 signaling and induction of Foxp3(+) regulatory T cells. Nat. Immunol., 2012, Vol. 14, no. 2, pp. 162-171.

82. Stuart L.M., Lucas M., Simpson C., Lamb J., Savill J., Lacy-Hulbert A., Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J. Immunol., 2002, Vol. 168, no. 4, pp. 1627-1635.

83. Su X., Qian C., Zhang Q., Hou J., Gu Y., Han Y., Chen Y., Jiang M., Cao X. miRNomes of haematopoietic stem cells and dendritic cells identify miR-30b as a regulator of Notch1. Nat. Commun., 2013, Vol. 4, p. 2903.

84. Suffner J., Hochweller K., Kuhnle M.C., Li X., Kroczek R.A., Garbi N., Hammerling G.J. Dendritic cells support homeostatic expansion of Foxp3+ regulatory T cells in Foxp3.LuciDTR mice. J. Immunol., 2010, Vol. 184, no. 4, pp. 1810-1820.

85. Švajger U., Rožman P. Tolerogenic dendritic cells: molecular and cellular mechanisms in transplantation. J. Leukoc. Biol., 2014, Vol. 95, no. 1, pp. 53-69.

86. van Herk E.H., Te Velde A.A. Treg subsets in inflammatory bowel disease and colorectal carcinoma. Characteristics, role and therapeutic targets. J. Gastroenterol. Hepatol., 2016, Vol. 31, no. 8, pp. 1393-1404.

87. van Meerwijk J.P., Marguerat S., Lees R.K., Germain R.N., Fowlkes B.J., MacDonald H.R. Quantitative impact of thymic clonal deletion on the T cell repertoire. J. Exp. Med., 1997, Vol. 185, no. 3, pp. 377-383.

88. Vitali C., Mingozzi F., Broggi A., Barresi S., Zolezzi F., Bayry J., Raimondi G., Zanoni I., Granucci F. Migratory, and not lymphoid-resident, dendritic cells maintain peripheral self-tolerance and prevent autoimmunity via induction of iTreg cells. Blood, 2012, Vol. 120, no. 6, pp. 1237-1245.

89. Vlad G., Piazza F., Colovai A., Cortesini R., Della Pietra F., Suciu-Foca N., Manavalan J.S. Interleukin-10 induces the upregulation of the inhibitory receptor ILT4 in monocytes from HIV positive individuals. Hum. Immunol., 2003, Vol. 64, no. 5, pp. 483-489.

90. Volchenkov R., Karlsen M., Jonsson R., Appel S. Type 1 regulatory T cells and regulatory B cells induced by tolerogenic dendritic cells. Scand. J. Immunol., 2013, Vol. 77, no. 4, pp. 246-254.

91. Voll R.E., Herrmann M., Roth E.A., Stach C., Kalden J.R., Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature, 1997, Vol. 390, no. 6658, pp. 350-351.

92. Wang P., Xue Y., Han Y., Lin L., Wu C., Xu S., Jiang Z., Xu J., Liu Q., Cao X. The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science, 2014, Vol. 344, no. 6181, pp. 310-313.

93. Wang Y., Han X. B Cells with Regulatory Function in Human Disease. Autoimmune Dis. Ther. Approaches, 2014, Vol. 1, no. 2, pp. 9-17.

94. Watanabe N., Wang Y.H., Lee H.K., Ito T., Wang Y.H., Cao W., Liu Y.J. Hassall’s corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus. Nature, 2005, Vol. 436, no. 7054, pp. 1181-1185.

95. Wei S., Kryczek I., Zou L., Daniel B., Cheng P., Mottram P., Curiel T., Lange A., Zou W. Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res., 2005, Vol. 65, no. 12, pp. 5020-5026.

96. Wolach O., Shpilberg O., Lahav M. Neutropenia after rituximab treatment: new insights on a late complication. Curr. Opin. Hematol., 2012, Vol. 19, no. 1, pp. 32-38.

97. Xing C., Ma N., Xiao H., Wang X., Zheng M., Han G., Chen G., Hou C., Shen B., Li Y., Wang R. Critical role for thymic CD19+CD5+CD1dhiIL-10+ regulatory B cells in immune homeostasis. J. Leukoc. Biol., 2015, Vol. 97, no. 3, pp. 547-556.

98. Yamazaki S., Steinman R.M. Dendritic cells as controllers of antigen-specific Foxp3+ regulatory T cells. J. Dermatol. Sci., 2009, Vol. 54, no. 2, pp. 69-75.

99. Yamazaki T., Akiba H., Iwai H., Matsuda H., Aoki M., Tanno Y., Shin T., Tsuchiya H., Pardoll D.M., Okumura K., Azuma M., Yagita H. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol., 2002, Vol. 169, no. 10, pp. 5538-5545.

100. Zhang J. Yin and yang interplay of IFN-γ in inflammation and autoimmune disease. J. Clin. Invest. 2007, Vol. 117, no. 4, pp. 871-873.

101. Zhang M., Zheng X., Zhang J., Zhu Y., Zhu X., Liu H., Zeng M., Graner M.W., Zhou B., Chen X. CD19(+) CD1d(+)CD5(+) B cell frequencies are increased in patients with tuberculosis and suppress Th17 responses. Cell Immunol., 2012, Vol. 274, no. 1-2, pp. 89-97.


Review

For citations:


Sennikov S.V., Kulikova E.V., Knauer N.Yu., Khantakova Yu.N. MOLECULAR AND CELLULAR MECHANISMS MEDIATED BY DENDRITIC CELLS INVOLVED IN THE INDUCTION OF TOLERANCE. Medical Immunology (Russia). 2017;19(4):359-374. (In Russ.) https://doi.org/10.15789/1563-0625-2017-4-359-374

Views: 2086


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1563-0625 (Print)
ISSN 2313-741X (Online)