Abstract
Under physiological conditions, regulatory processes can suppress the immune response after elimination of a pathogen and restore homeostasis through the destruction and suppression of obsolete effector cells of the immune system. The main players in this process are T-regulatory cells (Tregs) and immature dendritic cells, which suppress the immune response by their own products and/or by inducing synthesis of immunosuppressive interleukins IL-10, IL-35, and transforming growth factor (TGF-ß) by other cells. This mechanism is also used by widespread “successful” pathogens that are capable of chronically persisting in the human body — herpes virus, hepatitis viruses, human immunodeficiency virus, Mycobacterium tuberculosis, Helicobacter pylori, and others. During coevolution of microbial pathogens and the host immune system, the pathogens developed sophisticated strategies for evading the host defense, so-called immune evasion. In particular, molecular structures of pathogens during the interaction with dendritic cells via activating and inhibitory receptors can change intracellular signal transduction, resulting in block of maturation of dendritic cells. Immature dendritic cells become tolerogenic and cause differentiation of Tregs from the conventional T-cell CD4+. Microbial molecules can also react directly with Tregs through innate immune receptors. Costimulation of Toll-like receptor 5 (TLR5) by flagellin increases the expression of the transcription factor Foxp3, which increases the suppressive activity of Treg cells. From all evasion mechanisms, the induction of immunosuppression by Treg through IL-10, IL-35, and TGF-ß appears most effective. This results in the suppression of inflammation and of adaptive immune responses against pathogens, optimizing the conditions for the survival of bacteria and viruses.
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Abbreviations
- B7:
-
a costimulatory molecule expressed on the surface of antigen-presenting cells (APCs)
- CD4+ :
-
a marker expressed by helper and regulatory T-cells
- CD4+CD25highFoxp3+ :
-
markers expressed by regulatory T-cells
- CD4+Th2:
-
type 2 helper CD4+ T-cells
- CD4+Treg or CD8+Treg:
-
regulatory T-cells
- CD8+ :
-
a marker expressed by cytotoxic T-cells
- CTLA-4:
-
an inhibitory molecule expressed by T-cells
- FHA:
-
bacterial filamentous hemagglutinin adhesin
- HIV:
-
human immunodeficiency virus
- IL-10 and IL-35:
-
interleukins
- LFA-3 and ICAM-1:
-
cell adhesion molecules
- MHC I and II:
-
molecules of the major histocompatibility complex
- PD1:
-
an inhibitory molecule expressed on dendritic cells (programmed cell death protein 1)
- STAT:
-
intracellular signaling pathway (signal transducer and activator of transcription)
- TAP:
-
transporter associated with antigen processing expressed in APCs
- TCR:
-
T-cell receptor
- TGF-β:
-
transforming growth factor-β
- Th1:
-
type 1 helper CD4+ T-cells
- TLR:
-
Toll-like receptor
References
Playfair, J. H. L., and Bancroft, G. J. (2012) Infection and Immunity, 4th Edn., Oxford University Press, Oxford, pp. 115–120.
Tischler, A. D., and McKinney, J. D. (2011) in The Immune Response to Infection (Kaufmann, S. H. E., Rouse, B. T., and Sachs, D. L., eds.) ASM Press, Washington, DC, pp. 425–440.
Sansonetti, P. J., and Puhar, A. (2011) in The Immune Response to Infection (Kaufmann, S. H. E., Rouse, B. T., and Sachs, D. L., eds.) ASM Press, Washington, DC, pp. 133–142.
Garib, F. Yu. (2013) Interaction of Pathogens with Innate Immunity [in Russian], MSU, Moscow.
Garib, F. Yu., and Rizopulu, A. P. (2012) Interaction of pathogenic bacteria with host innate immunity, Infekts. Immun., 62, 581–596.
Gal-Mor, O., and Finlay, B. B. (2006) Pathogenicity islands: a molecular toolbox for bacterial virulence, Cell Microbiol., 8, 1707–1719.
Forsberg, A., Rosqvist, R., and Fallman, M. (2003) in Bacterial Evasion in Host Immune Responses (Henderson, B., and Oyston, P. C. E., eds.) Cambridge University Press, pp. 127–170.
Pritchard, D., Hooi, D., Watson, E., Chow, S., Telford, G., Bycroft, B., Chhabra, C., Harty, C., Camara, M., Diggle, S., and Williams, P. (2003) in Bacterial Evasion in Host Immune Responses (Henderson, B., and Oyston, P. C. E., eds.) Cambridge University Press, pp. 201–222.
Mesman, A. W., Zijlstra-Willems, E. M., Kaptein, T. M., de Swart, R. L., Davis, M. E., Ludlow, M., Duprex, W. P., Gack, M. U., Gringhuis, S. I., and Geijtenbeek, T. B. (2014) Measles virus suppresses RIG-I-like receptor activation in dendritic cells via DC-SIGN-mediated inhibition of PP1 phosphatases, Cell Host Microbe, 16, 31–42.
Murphy, K. P. (2012) Janeway’s Immunobiology, Garland Science, Taylor and Francis group, LLC.
Farrington, L., O’Neill, G., and Hill, A. B. (2011) in The Immune Response to Infection (Kaufmann, S. H. E., Rouse, B. T., and Sachs, D. L., eds.) ASM Press, Washington, DC, pp. 393–401.
Sakaguchi, S., Vignali, D. A., Rudensky, A. Y., Niec, R. E., and Waldmann, H. (2013) The plasticity and stability of regulatory T-cells, Nat. Rev. Immunol., 13, 461–467.
Shevach, E. M. (2013) in Fundamental Immunology (Paul, W. E., ed.) Lippincott Williams and Wilkins, pp. 795–832.
Buckner, J. H. (2010) Mechanisms of impaired regulation by CD4+CD25+FOXP3+ regulatory T-cells in human autoimmune diseases, Nat. Rev. Immunol., 10, 849–859.
Wang, R., Wan, Q., Kozhaya, L., Fujii, H., and Unutmaz, D. (2008) Identification of a regulatory T-cell specific cell surface molecule that mediates suppressive signals and induces Foxp3 expression, PLoS One, 3, e2705.
Collison, L. W., Chaturvedi, V., Henderson, A. L., Giacomin, P. R., Guy, C., Bankoti, J., Finkelstein, D., Forbes, K., Workman, C. J., Brown, S. A., Rehg, J. E., Jones, M. L., Ni, H. T., Artis, D., Turk, M. J., and Vignali, D. A. (2010) IL-35-mediated induction of a potent regulatory T-cell population, Nat. Immunol., 11, 1093–1101.
Jankovic, D., Kullberg, M. C., Feng, C. G., Goldszmid, R. S., Collazo, C. M., Wilson, M., Wynn, T. A., Kamanaka, M., Flavell, R. A., and Sher, A. (2007) Conventional T-bet+Foxp3–Th1-cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection, J. Exp. Med., 204, 273–283.
Nakagawa, T., Tsuruoka, M., Ogura, H., Okuyama, Y., Arima, Y., Hirano, T., and Murakami, M. (2010) IL-6 positively regulates Foxp3+CD8+ T-cells in vivo, Int. Immunol., 22, 129–139.
Rubtsov, Y. P., Niec, R. E., Josefowicz, S., Li, L., Darce, J., Mathis, D., Benoist, C., and Rudensky, A. Y. (2010) Stability of the regulatory T-cell lineage in vivo, Science, 329, 1667–1671.
Shevach, E. M. (2009) Mechanisms of Foxp3+ T-regulatory cell-mediated suppression, Immunity, 30, 636–645.
Gupta, N., Hegde, P., Lecerf, M., Nain, M., Kaur, M., Kalia, M., Vrati, S, Bayry, J., Lacroix-Desmazes, S., and Kaveri, S. V. (2014) Japanese encephalitis virus expands regulatory T-cells by increasing the expression of PD-L1 on dendritic cells, Eur. J. Immunol., 44, 1363–1374.
Chaturvedi, V., Collison, L. W., Guy, C. S., Workman, C. J., and Vignali, D. A. (2011) Cutting edge: human regulatory T-cells require IL-35 to mediate suppression and infectious tolerance, J. Immunol., 186, 6661–6666.
Vignali, D. A., Collison, L. W., and Workman, C. J. (2008) How regulatory T-cells work, Nature Rev. Immunol., 8, 523–532.
Cao, X., Cai, S. F., Fehniger, T. A., Song, J., Collins, L. I., Piwnica, D. R., and Ley, T. J. (2007) Granzyme B and perforin are important for regulatory T-cell-mediated suppression of tumor clearance, Immunity, 27, 635–646.
Garin, M. I., Chu, C. C., Golshayan, D., Cernuda-Morollon, E., Wait, R., and Lechler, R. I. (2007) Galectin-1: a key effector of regulation mediated by CD4+CD25+ T-cells, Blood, 109, 2058–2065.
Deaglio, S., Dwyer, K. M., Gao, W., Friedman, D., Usheva, A., Erat, A., Chen, J. F., Enjyoji, K., Linden, J., Oukka, M., Kuchroo, V. K., Strom, T. B., and Robson, S. C. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T-cells mediates immune suppression, J. Exp. Med., 204, 1257–1265.
Mandapathil, M., Hilldorfer, B., Szczepanski, M. J., Czystowska, M., Szajnik, M., Ren, J., Lang, S., Jackson, E. K., Gorelik, E., and Whiteside, T. L. (2010) Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T-cells, J. Biol. Chem., 285, 7176–7186.
Lukashev, D., Ohta, A., Apasov, S., Chen, J. F., and Sitkovsky, M. (2004) Cutting edge: physiologic attenuation of proinflammatory transcription by the Gs protein-coupled A2A adenosine receptor in vivo, J. Immunol., 173, 21–24.
Thammavongsa, V., Kern, J. W., Missiakas, D. M., and Schneewind, O. (2009) Staphylococcus aureus synthesizes adenosine to escape host immune responses, J. Exp. Med., 206, 2417–2427.
Zarek, P. E., Huang, C. T., Lutz, E. R., Kowalski, J., Horton, M. R., Linden, J., Drake, C. G., and Powell, J. D. (2008) A2A receptor signaling promotes peripheral tolerance by inducing T-cell energy and the generation of adaptive regulatory T-cells, Blood, 111, 251–259.
Liang, B. T., Workman, C., Lee, J., Chew, C., Dale, B. M., Colonna, L., Flores, M., Li, N. Y., Schweighoffer, E., Greenberg, S., Tybulewicz, V., Vignali, D., and Clynes, R. (2008) Regulatory T-cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II, J. Immunol., 180, 5916–5926.
Sarris, M., Anderson, K. G., Randow, F., Mayr, L., and Betz, A. G. (2008) Neuropilin-1 expression on regulatory T-cells enhances their interactions with dendritic cells during antigen recognition, Immunity, 28, 402–413.
Zhang, M., Liu, M., Luther, J., and Kao, J. Y. (2010) Helicobacter pylori directs tolerogenic programming of dendritic cells, Gut Microbes, 1, 325–329.
Kao, J. Y., Zhang, M., Miller, M. J., Mills, J. C., Wang, B., Liu, M., Eaton, K. A., Zou, W., Berndt, B. E., Cole, T. S., Takeuchi, T., Owyang, S. Y., and Luther, J. (2010) Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg-skewing and Th17 suppression in mice, Gastroenterology, 138, 1046–1054.
Balkow, S., Krux, F., Loser, K., Becker, J. U., Grabbe, S., and Dittmer, U. (2007) Friend retrovirus infection of myeloid dendritic cells impairs maturation, prolongs contact to naive T-cells, and favors expansion of regulatory T-cells, Blood, 110, 3949–3958.
McGuirk, P., McCann, C., and Mills, K. H. G. (2002) Pathogen-specific T-regulatory 1 cells induced in the respi-ratory tract by a bacterial molecule that stimulates inter-leukin 10 production by dendritic cells: a novel strategy for evasion of protective T-helper type 1 responses by Bordetella pertussis, J. Exp. Med., 195, 221–231.
Weber, M. S., Benkhoucha, M., Lehmann-Horn, K., Hertzenberg, D., Sellner, J., Santiago-Raber, M. L., Chofflon, M., Hemmer, B., Zamvil, S. S., and Lalive, P. H. (2010) Repetitive pertussis toxin promotes development of regulatory T-cells and prevents central nervous system autoimmune disease, PLoS One 5, e16009.
Van der Kleij, D., Latz, E., Brouwers, J. F., Kruize, Y. C., Schmitz, M., Kurt-Jones, E. A., Espevik, T., de Jong, E. C., Kapsenberg, M. L., Golenbock, D. T., Tielens, A. G., and Yazdanbakhsh, M. (2002) A novel host–parasite lipid cross talk: schistosomal lysophosphatidylserine activates Toll-like receptor 2 and affects immune polarization, J. Biol. Chem., 277, 48122–48129.
Cue’llar, C., Wu, W., and Mendez, S. (2009) The hookworm tissue inhibitor of metalloproteases (Ac-TMP-1) modifies dendritic cell function and induces generation of CD4 and CD8 suppressor T-cells, PLoS Negl. Trop. Dis., 3, e439.
Segura, M., Su, Z., Piccirillo, C., and Stevenson, M. M. (2007) Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression, Eur. J. Immunol., 37, 1887–1904.
Smith, K. A., Hochweller, K., Hammerling, G. J., Boon, L., Macdonald, A. S., and Maizels, R. M. (2011) Chronic helminth infection promotes immune regulation in vivo through dominance of CD11cloCD103- dendritic cells, J. Immunol., 186, 7098–7109.
Chieppa, M., Bianchi, G., Doni, A., Del Prete, A., Sironi, M., Laskarin, G., Monti, P., Piemonti, L., Biondi, A., Mantovani, A., Introna, M., and Allavena, P. (2003) Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program, J. Immunol., 171, 4552–4560.
Josefowicz, S. Z., Ni, R. E., Kim, H. Y., Treuting, P., Chinen, T., Zheng, Y., Umetsu, D. T., and Rudensky, A. Y. (2012) Extrathymically generated regulatory T-cells control mucosal TH2 inflammation, Nature, 482, 395–399.
Tanoue, T., and Honda, K. (2012) Induction of Treg-cells in the mouse colonic mucosa: a central mechanism to maintain host-microbiota homeostasis, Sem. Immunol., 24, 50–57.
Zaccone, P., Burton, O. T., Gibbs, S. E., Miller, N., Jones, F. M., Schramm, G., Haas, H., Doenhoff, M. J., Dunne, D. W., and Cooke, A. (2011) The S. mansoni glycoprotein ω-1 induces Foxp3 expression in NOD mouse CD4 T-cells, Eur. J. Immunol., 41, 2709–2718.
Liu, J. Y., Li, L. Y., Yang, X. Z., Li, J., Zhong, G., Wang, J., Li, L. J., Ji, B., Wu, Z. Q., Liu, H., Yang, X., and Liu, P. M. (2011) Adoptive transfer of DCs isolated from helminth-infected mice enhanced T-regulatory cell responses in airway allergic inflammation, Parasite Immunol., 33, 525–534.
Park, S. K., Cho, M. K., Park, H. K., Lee, K. H., Lee, S. J., Choi, S. H., Ock, M. S., Jeong, H. J., Lee, M. H., and Yu, H. S. (2009) Macrophage migration inhibitory factor homologs of anisakis simplex suppress Th2 response in allergic airway inflammation model via CD4+CD25+Foxp3+ T-cell recruitment, J. Immunol., 182, 6907–6914.
Sakaguchi, S., Wing, K., and Miara, M. (2013) in Clinical Immunology: Principles and Practice, Elsevier, pp. 193–202.
Sarangi, P. P., Sehrawat, S., Suvas, S., and Rouse, B. T. (2008) IL-10 and natural regulatory T-cells: two independent antiinflammatory mechanisms in herpes simplex virus-induced ocular immunopathology, J. Immunol., 180, 6297–6306.
Belkaid, Y., and Tarbell, K. (2009) Regulatory T-cells in the control of host-microorganism interactions, Ann. Rev. Immunol., 27, 551–589.
Ordway, D., Henao-Tamayo, M., Harton, M., Palanisamy, G., Troudt, J., Shanley, C., Basaraba, R. J., and Orme, I. M. (2007) The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation, J. Immunol., 179, 522–531.
Mahnke, K., Knop, J., and Enk, A. H. (2003) Induction of tolerogenic DCs: “you are what you eat”, Trends Immunol., 24, 646–651.
De Paolo, R. W., Tang, F., Kim, I., Han, M., Levin, N., Ciletti, N., Lin, A., Anderson, D., Schneewind, O., and Jabri, B. (2008) Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis, Cell Host Microbe, 4, 350–361.
Medzhitov, R. (2008) in Fundamental Immunology (Paul, W. E., ed.) Lippincott Williams and Wilkins, pp. 427–450.
Mion, F., Tonon, S., Toffoletto, B., Cesselli, D., Pucillo, C. E., and Vitale, G. (2014) IL-10 production by B-cells is differentially regulated by immune-mediated and infectious stimuli and requires p38 activation, Mol. Immunol., 62, 266–276.
Carey, A. J., Tan, C. K., and Ulett, G. C. (2012) Infectioninduced IL-10 and JAK-STAT: a review of the molecular circuitry controlling immune hyperactivity in response to pathogenic microbes, JAKSTAT, 1, 159–167.
Ketlinskiy, S. A., and Simbirtsev, A. S. (2008) Cytokines [in Russian], Izdatel’stvo Foliant, St. Petersburg.
Brubaker, R. R. (2003) Interleukin-10 and inhibition of innate immunity to Yersiniae: roles of Yops and LcrV (V-antigen), Infect. Immun., 71, 3673–3681.
Kopp, E., and Medzhitov, R. (2002) A plague on host defense, J. Exp. Med., 21, 1009–1012.
Stumhofer, J. S., Silver, J. S., Laurence, A., Porrett, P. M., Harris, T. H., Turka, L. A., Ernst, M., Saris, C. J., O’Shea, J. J., and Hunter, C. A. (2007) Interleukins 27 and 6 induce STAT3-mediated T-cell production of interleukin 10, Nat. Immunol., 8, 1363–1371.
Alcami, A., and Saraiva, M. (2009) Chemokine binding proteins encoded by pathogens, Adv. Exp. Med. Biol., 666, 167–179.
Taylor, A. L., and Llewelyn, M. J. (2010) Superantigen-induced proliferation of human CD4+CD25–T-cells is followed by a switch to a functional regulatory phenotype, J. Immunol., 185, 6591–6598.
Sutmuller, R. P. M., Morgan, M. E., Netea, M. G., Grauer, O., and Adema, G. J. (2006) Toll-like receptors on regulatory T-cells: expanding immune regulation, Trends Immunol., 27, 387–393.
Crellin, N. K., Garcia, R. V., Hadisfar, O., Allan, S. E., Steiner, T. S., and Levings, M. K. (2005) Human CD4+ T-cells express TLR5 and its ligand flagellin enhances the suppressive capacity and expression of FOXP3 in CD4+CD25+ T regulatory cells, J. Immunol., 175, 8051–8059.
Higgins, S. C., Lavelle, E. C., Mc Cann, C., Keogh, B., Mc Neela, E., Byrne, P., O’Gorman, B., Jarnicki, A., Mc Guirk, P., and Mills, K. H. (2003) Toll-like receptor 4-mediated innate IL-10 activates antigen-specific regulatory T-cells and confers resistance to Bordetella pertussis by inhibiting inflammatory pathology, J. Immunol., 171, 3119–3127.
Caramalho, I., Lopes-Carvalho, T., Ostler, D., Zelenay, S., Haury, M., and Demengeot, J. (2003) Regulatory T-cells selectively express toll-like receptors and are activated by lipopolysaccharide, J. Exp. Med., 197, 403–411.
Sing, A., Rost, D., Tvardovskaia, N., Roggenkamp, A., Wiedemann, A., Kirschning, C. J., Aepfelbacher, M., and Heesemann, J. (2002) Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression, J. Exp. Med., 196, 1017–1024.
Layland, L. E., Rad, R., Wagner, H., and da Costa, C. U. (2007) Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T-cells primed in the presence of TLR2, Eur. J. Immunol., 37, 2174–2184.
Wang, X., Zhou, S., Chi, Y., Wen, X., Hoellwarth, J., He, L., Liu, F., Wu, C., Dhesi, S., Zhao, J., Hu, W., and Su, C. (2009) CD4+CD25+Treg induction by an HSP60-derived peptide SJMHE1 from Schistosoma japonicum is TLR2 dependent, Eur. J. Immunol., 39, 3052–3065.
Chen, Q., Davidson, T. S., Huter, E. N., and Shevach, E. M. (2009) Engagement of TLR2 does not reverse the suppressor function of mouse regulatory T-cells, but promotes their survival, J. Immunol., 183, 4458–4466.
Oberg, H. H., Ly, T. T., Ussat, S., Meyer, T., Kabelitz, D., and Wesch, D. (2010) Differential but direct abolishment of human regulatory T-cell suppressive capacity by various TLR2 ligands, J. Immunol., 184, 4733–4740.
Van Maren, W. W., Nierkens, S., Toonen, L. W., Bolscher, J. M., Sutmuller, R. P., and Adema, G. J. (2011) Multifaceted effects of synthetic TLR2 ligand and Legionella pneumophilia on Treg-mediated suppression of T-cell activation, BMC Immunol., DOI: 10.1186/1471-2172-12-23.
Zanin-Zhorov, A., Cahalon, L., Tal, G., Margalit, R., Lider, O., and Cohen, I. R. (2006) Heat shock protein 60 enhances CD4+CD25+ regulatory T-cell function via innate TLR2 signaling, J. Clin. Invest., 116, 2022–2032.
Peng, G., Guo, Z., Kiniwa, Y., Voo, K. S., Peng, W., Fu, T., Wang, D. Y., Li, Y., Wang, H. Y., and Wang, R. F. (2005) Toll-like receptor 8-mediated reversal of CD4+ regulatory T-cell function, Science, 309, 1380–1384.
Chiffoleau, E., Heslan, J. M., Heslan, M., Louvet, C., Condamine, T., and Cuturi, M. C. (2007) TLR9 ligand enhances proliferation of rat CD4+ T-cell and modulates suppressive activity mediated by CD4+CD25+ T-cell, Int. Immunol., 19, 193–201.
Carlin, A. F., Uchiyama, S., Chang, Y. C., Lewis, A. L., Nizet, V., and Varki, A. (2009) Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response, Blood, 113, 3333–3336.
Wang, M., Krauss, J. L., Domon, H., Hosur, K. B., Liang, S., Magotti, P., Triantafilou, M., Triantafilou, K., Lambris, J. D., and Hajishengallis, G. (2010) Microbial hijacking of complement-Toll-like receptor crosstalk, Sci. Signal., 3, DOI: 10.1126.
Oliva, C., Turnbough, C. L., Jr., and Kearney, J. F. (2009) CD14–Mac-1 interactions in Bacillus anthracis spore internalization by macrophages, Proc. Natl. Acad. Sci. USA, 106, 13957–13962.
Hajishengallis, G., and Lambris, J. D. (2010) Crosstalk pathways between Toll-like receptors and the complement system, Trends Immunol., 31, 154–163.
Simmons, D. P., Canaday, D. H., Liu, Y., Li, Q., Huang, A., Boom, W. H., and Harding, C. V. (2010) Mycobacterium tuberculosis and TLR2 agonists inhibit induction of type I IFN and class I MHC antigen cross processing by TLR9, J. Immunol., 185, 2405–2415.
Melendez, A. J., Harnett, M. M., Pushparaj, P. N., Wong, W. S., Tay, H. K., Mc Sharry, C. P., and Harnett, W. (2007) Inhibition of FcεRI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes, Nat. Med., 13, 1375–1381.
Brodsky, I. E., and Medzhitov, R. (2009) Targeting of immune signaling networks by bacterial pathogens, Nat. Cell Biol., 11, 521–526.
Hajishengallis, G., and Lambris, J. D. (2011) Microbial manipulation of receptor crosstalk in innate immunity, Nat. Rev. Immunol., 11, 187–200.
Ivashkiv, L. B. (2009) Cross-regulation of signaling by ITAM associated receptors, Nat. Immunol., 10, 340–347.
Zak, D. E., and Aderem, A. (2009) Systems biology of innate immunity, Immunol. Rev., 227, 264–282.
Gringhuis, S. I., den Dunnen, J., Litjens, M., van Het Hof, B., van Kooyk, Y., and Geijtenbeek, T. B. (2007) C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-κB, Immunity, 26, 605–616.
Gringhuis, S. I., den Dunnen, J., Litjens, M., van der Vlist, M., and Geijtenbeek, T. B. (2009) Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori, Nat. Immunol., 10, 1081–1088.
Bergman, M. P., Engering, A., Smits, H. H., van Vliet, S. J., van Bodegraven, A. A., Wirth, H. P., Kapsenberg, M. L., Vandenbroucke-Grauls, C. M., van Kooyk, Y., and Appelmelk, B. J. (2004) Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN, J. Exp. Med., 200, 979–990.
Hovius, J. W., de Jong, M. A., den Dunnen, J., Litjens, M., Fikrig, E., van der Poll, T., Gringhuis, S. I., and Geijtenbeek, T. B. (2008) Salp15 binding to DC-SIGN inhibits cytokine expression by impairing both nucleosome remodeling and mRNA stabilization, PLoS Pathog., 4, e31.
Hedrick, S. M. (2004) The acquired immune system: a vantage from beneath, Immunity, 21, 607–615.
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Original Russian Text © F. Yu. Garib, A. P. Rizopulu, 2015, published in Biokhimiya, 2015, Vol. 80, No. 8, pp. 1141–1159.
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Garib, F.Y., Rizopulu, A.P. T-regulatory cells as part of strategy of immune evasion by pathogens. Biochemistry Moscow 80, 957–971 (2015). https://doi.org/10.1134/S0006297915080015
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DOI: https://doi.org/10.1134/S0006297915080015