Cover Page

Cite item


Review covers modern data on relationships of normal intestinal microbiota and immune system. Possibility to maintain the residence of large numbers of symbiotic bateria at mucosal surfaces of the body is regarded as a separate and independent immunological function named acceptive immunity. Basic effector arms of protective (defense against pathogens) and acceptive immunity (symbiotic relationships) are compared. Acceptive immunity differs from protective one in the absence of inflammation where all complex of immune reactions occurs in the context of physiological process. Several homeostatic mechanisms that provide crosstalk with symbiotic bacteria at the epithelial surfaces, innate and adaptive immunity are described. The main immunological strategies towards symbiotic bacteria are support of microbial community from one hand, and providing of host defense, from the other hand. The key step of this interaction is sensing of soluble microbial products via pattern-recognition receptors on the host cells. Basic innate immune response consists of mucus production and synthesis of antimicrobial peptides by barrier epithelial cells as well as maintenance of specific anti-inflammatory microenvironment. The main adaptive response is synthesis of secretory immunoglobulin A that is produced to the intestinal lumen and interacts with bacteria. At the same time, immunoglobulin A does not make any damage for commensals. Moreover this factor plays important role in symbiotic relationships. The following promicrobial functions of immunoglobulin A are suggested: participation in biofilm formation, discrimination of intestinal bacteria for fixed and free-living populations as well as facilitation of microbial transport through M cells. Mucosal homeostasis is supported by the development of immunological tolerance with participation of T regulatory cells. Main mechanisms of the development and maintenance of specific tolerance towards antigens of normal microbiota are discussed. Modern data on the participation of two main populations of T-regulatory cells are cited — thymic cells and cells induced in periphery. It is now accepted, that development of specific tolerance to microbial and food antigens plays important role in prevention of autoimmune and allergic diseases.

About the authors

E. P. Kisseleva

North-West Branch of the Russian Academy of Medical Sciences

Author for correspondence.
PhD, MD (Medicine), Head of the Laboratory of Immunoregulation, Department of Immunology, St. Petersburg State Pediatric Medical University, 191119, Russian Federation, St. Petersburg, Dostoevskiy str., 32, 4 Russian Federation


  1. Климович В.Б. Актуальные проблемы эволюционной иммунологии // Журнал эволюционной биохимии и физиологии. 2002. Т. 38, № 5. С. 442–451. [Klimovich V.B. Actual problems of evolutionary immunology. Zhurnal evolyutsionnoi biokhimii i fiziologii = J. Evol. Biochem. Physiol., 2002, vol. 38, no. 5, pp. 562–574. (In Russ.)]
  2. Климович В.Б., Самойлович М.П. Иммуноглобулин А (IgA) и его рецепторы // Медицинская иммунология. 2006. Т. 8, № 4. С. 483–500. [Klimovich V.B., Samoilovich M.P. Immunoglobulin A (IgA) and its receptors. Meditsinskaya Immunologiya = Medical Immunology (Russia), 2006, vol. 8, no. 4, pp. 483–500. doi: 10.15789/1563-0625-2006-4-483-500 (In Russ.)]
  3. Кокряков В.Н. Очерки о врожденном иммунитете. СПб.: Наука, 2006. 261 с. [Kokryakov V.N. Ocherki o vrozhdennom immunitete [Essays on innate immunity]. St. Petersburg: NAUKA, 2006. 261 p.]
  4. Bevins C.L., Ganz T. Antimicrobial peptides of the alimentary tract of mammals / Mammalian host defense peptides; eds. Devine D.A., Hancock R.E.W. UK: Cambridge University Press, 2004, pp. 161–188.
  5. Biesbrock A.R., Reddy M.S., Levine M.J. Interaction of salivary mucin-secretory immunoglobulin A complex with mucosal patho gens. Infect. Immun., 1991, vol. 59, no. 10, pp. 3492–3497.
  6. Bilate A.M., Lafaille J.J. Induced CD4+Foxp3+ regulatory T-cells in immune tolerance. Annu. Rev. Immunol., 2012, vol. 30, pp. 733–758. doi: 10.1146/annurev-immunol-020711-075043
  7. Boehm T. Evolution of vertebrate immunity. Curr. Biol., 2012, vol. 22, pp. R722–R732. doi: 10.1016/j.cub.2012.07.003
  8. Boullier S., Tanguy M., Kadaoui K.A., Caubet C., Sansonetti P., Corthesy B., Phalipon A. Secretory IgA-mediated neutralization of Shigella flexneri prevents intestinal tissue destruction by down-regulating inflammatory circuits. J. Immunol., 2009, vol. 183, pp. 5879–5885. doi: 10.4049/jimmunol.0901838
  9. Brandl K., Pitas G., Schnabl B., DeMatteo R.P., Pamer E.G. MyD88-mediated signals induce the bacterial lectin RegIII gamma and protect mice against intestinal Listeria monocytogenes infection. J. Exp. Med., 2007, vol. 204, pp. 1891–1900. doi: 10.1084/jem.20070563
  10. Brandtzaeg P. Secretory IgA: designed for anti-microbial defense. Front. Immunol., 2013, vol. 4, pp. 1–17. doi: 10.3389/fimmu.2013.00222
  11. Brown E.M., Sadarangani M., Finlay B.B. The role of the immune system in governing host-microbe interactions in the intestine. Nature Immunol., 2013, vol. 14, no. 7, pp. 660–667. doi: 10.1038/ni.2611
  12. Burger-Van Paassen N., Vincent A., Puiman P.J., Van der Sluis M., Bouma J., Boehm G., Van Goudoever J.B., Van Seuningen I., Renes I.B. The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem. J., 2009, vol. 420, pp. 211–219. doi: 10.1042/BJ20082222
  13. Cash H.L., Whitham C.V., Behrendt C.L., Hooper L.V. Symbiotic bacteria direct expression of an intestinal bacterial lectin. Science, 2006, vol. 313, pp. 1052–1054. doi: 10.1126/science.1127119
  14. Cebula A., Seweryn M., Rempala G.A., Pabla S.S., McIndoe R.A., Denning T.L., Bry L., Kraj P., Kisielow P., Ignatowicz L. Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota. Nature, 2013, vol. 497, no. 7448, pp. 258–262. doi: 10.1038/nature12079
  15. De Goër de Herve M.G., Jaafoura S., Vallee M., Taoufik Y. Foxp3+ regulatory CD4 T cells control the generation of functional CD8 memory. Nat. Commun., 2012, vol. 3, no. 986. doi: 10.1038/ncomms1992 doi: 10.1038/ncomms1992
  16. Eberl G. A new vision of immunity: homeostasis of the superorganism. Mucosal Immunol., 2010, vol. 3, no. 5, pp. 450–460. doi: 10.1038/mi.2010.20
  17. Everett M.L., Palestrant D., Miller S.E., Bollinger R.R., Parker W. Immune exclusion and immune inclusion: a new model of hostbacterial interactions in the gut. Clin. Appl. Immunol. Rev., 2004, vol. 4, pp. 321–332. doi: 10.1016/j.cair.2004.03.001
  18. Faria A.M.C., Weiner H.W. Oral tolerance. Immunol. Rev., 2005, vol. 206, pp. 232–259.
  19. Fontenot J.D., Gavin M.A., Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol., 2003, vol. 4, no. 4, pp. 330–336. doi: 10.1038/ni904
  20. Frantz A.L., Rogier E.W., Weber C.R., Shen L., Cohen D.A., Fenton L.F., Bruno M.E.C., Kaetzel C.S. Targeted deletion of MyD88 in intestinal epithelial cells results in compromised antibacterial immunity associated with down-regulation of polymeric immunoglobulin receptor, mucin-2, and antibacterial peptides. Mucosal Immunology, 2012, vol. 5, no. 5, pp. 501–512. doi: 10.1038/mi.2012.23
  21. Han D., Walsh M.C., Cejas P.J., Dang N.N., Kim Y.F., Kim J., Charrier-Hisamuddin L., Chau L., Zhang Q., Bittinger K., Bushman F.D., Turka L.A., Shen H., Reizis B., DeFranco A.L., Wu G.D., Choi Y. Dendritic cell expression of the signaling molecule TRAF6 is critical for gut microbiota-dependent immune tolerance. Immunity, 2013, vol. 38, pp. 1211–1222. doi: 10.1016/j.immuni.2013.05.012
  22. He B., Xu W., Santini P.A., Polydorides A.D., Chiu A., Estrella J., Shan M., Shadbun A., Villanacci V., Plebani A., Knowles D.M., Rescigno M., Cerutti A. Intestinal bacteria trigger T-cell-independent IgA2 class switching by inducing epithelial cell secretion of the cytokine APRIL. Immunity, 2007, vol. 26, pp. 812–826. doi: 10.1016/j.immuni.2007.04.014
  23. Herr A.B., Ballister E.R., Bjorkman P.J. Insights into IgA-mediated immune responses from the crystal structures of human FcalphaR1 and its complex with IgA1-Fc. Nature, 2003, vol. 423, pp. 614–620.
  24. Hill D.A., Artis D. Intestinal bacteria and the regulation of immune cell homeostasis. Annu. Rev. Immunol., 2010, vol. 28, pp. 623–667. doi: 10.1146/annurev-immunol-030409-101330
  25. Honda K., Takeda K. Regulatory mechanisms of immune responses to intestinal bacteria. Mucosal Immunol., 2009, vol. 2, no. 3, pp. 187–196. doi: 10.1038/mi.2009.8
  26. Hooper J.V., Littman D.R., Macpherson A.J. Interactions between the microbiota and the immune system. Science, 2012, vol. 336, pp. 1268–1273. doi: 10.1126/science.1223490
  27. Hooper L.V., Stappenbeck T.S., Hong C.V., Gordon J.I. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat. Immunol., 2003, vol. 4, pp. 269–273. doi: 10.1038/ni888
  28. Hori S., Nomura N., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science, 2003, vol. 299, pp. 1057–1061. doi: 10.1126/science.1079490
  29. Iliev I.D., Mileti E., Matteoli G., Chieppa M., Rescigno M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol., 2009, vol. 2, pp. 340–350. doi: 10.1038/mi.2009.13
  30. Johansson M.E.V., Holmen Larsson J.M., Hansson G.C. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl. Acad. Sci. USA, 2011, vol. 108, suppl. 1, pp. 4659–4665. doi: 10.1073/pnas.1006451107
  31. Josefowicz S.Z., Lu L.-F., Rudensky A.Y. Regulatory T cells: mechanism of differentiation and function. Annu. Rev. Immunol., 2012, vol. 30, pp. 531–564. doi: 10.1146/annurev.immunol.25.022106.141623
  32. 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, 2012, vol. 482, pp. 395–399. doi: 10.1038/nature10772
  33. Kadaoui K.A., Corthesy B. Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer’s patches with restriction to mucosal compartment. J. Immunol., 2007, vol. 179, no. 11, pp. 7751–7757. doi: 10.4049/ jimmunol.179.11.7751
  34. Kaetzel C.S. Coevolution of mucosal immunoglobulins and the polymeric immunoglobulin receptor: evidence that the commensal microbiota provided the driving force. ISRN Immunology, 2014, vol. 2014, pp. 1–20. doi: 10.1155/2014/541537
  35. Karlsson J., Pütsep K., Chu H., Kays R.J., Bevins C.L., Andersson M. Regional variations in Paneth cell antimicrobial peptide expression along mouse intestinal tract. BMC Immunol., 2008, vol. 9, no. 37. doi: 10.1186/1471-2172-9-37
  36. Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nunez G., Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science, 2005, vol. 307, no. 5710, pp. 731–734. doi: 10.1126/science.1104911
  37. Koropatnick T.A., Engle J.T., Apicella M.A., Stabb E.V., Goldman W.E., McFall-Ngai M.J. Microbial factor-mediated development in a host-bacterial mutualism. Science, 2004, vol. 306, pp. 1186–1188. doi: 10.1126/science.1102218
  38. Kruglov A.A., Grivennikov S.I., Kuprash D.V., Winsauer C., Prepens S., Seleznik G.M., Ebert G., Littman D.R., Heikenwalder M., Tumanov A.V., Nedospasov S.A. Nonredundant function of soluble LTα3 produced by innate lymphoid cells in intestinal homeostasis. Science, 2013, vol. 342, pp. 1243–1246. doi: 10.1126/science.1243364
  39. Lathrop S.K., Bloom S.M., Rao S.M., Nutsch K., Lio C.-W., Santakruz N., Peterson D.A., Stappenbeck T.S., Hsieh C.S. Peripheral education of the immune system by colonic commensal microbiota. Nature, 2011, vol. 478, pp. 251–254. doi: 10.1038/nature10434
  40. Laurin M., Everett M.L., Parker W. The cecal appendix: one more immune component with a function disturbed by post-industrial culture. Anat. Rec., 2011, vol. 294, pp. 567–579. doi: 10.1002/ar.21357
  41. Licona-Limon P., Henao-Mejia J., Temann A.U., Gagliani N., Licona-Limon I., Ishigame H., Hao L., Herbert D.R., Flavell R.A. Th9 cells drive host immunity against gastrointestinal worm infection. Immunity, 2013, vol. 39, no. 4, pp. 744–757. doi: 10.1016/j.immuni.2013.07.020
  42. Louahed J., Toda M., Jen J., Hamid Q., Renauld J.C., Levitt R.C., Nicolaides N.C. Interleukin-9 upregulates mucus expression in the airways. Am. J. Respir. Cell. Mol. Biol., 2000, vol. 22, pp. 649–656. doi: 10.1165/ajrcmb.22.6.3927
  43. Macia L., Thorburn A.N., Binge L.C., Marino E., Rogers K.E., Maslowski K.M., Vieira A.T., Kranich J., Mackay C.R. Microbial influences on epithelial integrity and immune function as a basis for inflammatory diseases. Immunol. Rev., 2012, vol. 245, no. 1, pp. 164–176. doi: 10.1111/j.1600-065X.2011.01080.x
  44. Macpherson A.J., Geuking M.B., McCoy K.D. Homeland security: IgA immunity at the frontiers of the body. Trends Immunol., 2012, vol. 33, no. 4, pp. 160–167. doi: 10.1016/
  45. Mantis N.J., Rol N., Corthesy B. Secretory IgA’s complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol., 2011, vol. 4, no. 6, pp. 603–611. doi: 10.1038/mi.2011.41
  46. Masuda K., Nakamura K., Yoshioka S., Fukaya R., Sakai N., Ayabe T. Regulation of microbiota by antimicrobial peptides in the gut. Adv. Otorhinolaryngol., 2011, vol. 72, pp. 97–99. doi: 10.1159/000324625
  47. Mathias A., Corthesy B. N-glycans on secretory component. Mediators of the interaction between secretory IgA and Grampositive commensals sustaining intestinal homeostasis. Gut Microbes, 2011, vol. 2, no. 5, pp. 287–293. doi: 10.4161/gmic.2.5.18269
  48. Matzinger P. Friendly and dangerous signals: is the tissue in control? Nat. Immunol., 2007, vol. 8, no. 1, pp. 11–13. doi: 10.1038/ni0107-11
  49. Maynard C.L., Elson C.O., Hatton R.D., Weaver C.T. Reciprocal interactions of the intestinal microbiota and immune system. Nature, 2012, vol. 489, no. 7415, pp. 231–241. doi: 10.1038/nature11551
  50. McFall-Ngai M. Care for the community. Nature, 2007, vol. 445, p. 153. doi: 10.1038/445153a
  51. Medzhitov R., Janeway C.A. Decoding the patterns of self and nonself by innate immune system. Science, 2002, vol. 296, pp. 298–300. doi: 10.1126/science.1068883
  52. Menendez A., Willing B.P., Montero M., Wlodarska M., So C.C., Bhinder G., Vallance B.A., Finlay B.B. Bacterial stimulation of the TLR-MyD88 pathway modulates the homeostatic expression of ileal Paneth cell α-defensins. J. Innate. Immun., 2013, vol. 5, no. 1, pp. 39–49. doi: 10.1159/000341630
  53. Mestecky J., Russell M.W. Specific antibody activity, glycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces. Immunol. Lett., 2009, vol. 124, pp. 57–62. doi: 10.1016/j.imlet.2009.03.013
  54. Mkaddem S.B., Rossato E., Heming N., Monteiro R.C. Anti-inflammatory role of the IgA Fc receptor (CD89): from autoimmunity to therapeutic perspectives. Autoimmun. Rev., 2013, vol. 12, pp. 666–669. doi: 10.1016/j.autrev.2012.10.011
  55. Morgan X.C., Segata N., Huttenhower C. Biodiversity and functional genomics in the human microbiome. Trends Genet., 2013, vol. 29, pp. 51–58. doi: 10.1016/j.tig.2012.09.005
  56. Pabst O. New concepts in the generation and functions of IgA. Nat. Rev. Immunol., 2012, vol. 12, no. 12, pp. 821–832. doi: 10.1038/nri3322
  57. Pabst O. Traffiking of regulatory T cells in the intestinal immune system. Int. Immunol., 2013, vol. 25, no. 3, pp. 139–143. doi: 10.1093/intimm/dxs113
  58. Pearson C., Uhlig H.H., Powrie F. Lymphoid microenvironments and innate lymphoid cells in the gut. Trends Immunol., 2012, vol. 33, no. 6, pp. 289–296. doi: 10.1016/
  59. Pena J.A., Versalovic J. Lactobacillus rhamnosus GG decreases TNF-alpha production in lipopolysaccharide-activated murine macrophages by contact-independent mechanism. Cell. Microbiol., 2003, vol. 5, pp. 277–285. doi: 10.1046/j.1462-5822.2003.t01-1-00275.x
  60. Peterson D.A., McNulty N.P., Guruge J.L., Gordon J.I. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe, 2007, vol. 2, pp. 328–339. doi: 10.1016/j.chom.2007.09.013
  61. Phalipon A., Cardona A., Kraehenbuhl J.-P., Edelman L., Sansonetti P.J., Corthesy B. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity, 2002, vol. 17, pp. 107–115. doi: 10.1016/S1074-7613(02)00341-2
  62. Putsep K., Axelsson L.G., Boman A., Midtvedt T., Normark S., Boman H.G., Andersson M. Germ-free and colonized mice generate the same products from enteric prodefensins. J. Biol. Chem., 2000, vol. 275, no. 51, pp. 40478–40482. doi: 10.1074/jbc.M007816200
  63. Renz H., Brandtzaeg P., Hornef M. The impact of perinatal immune development of mucosal homeostasis and chronic inflammation. Nat. Rev. Immunol., 2012, vol. 12, pp. 9–23. doi: 10.1038/nri3112
  64. Sakaguchi S., Vignali D.A.A., Rudensky A.Y., Niec R.E., Waldman H. The plasticity and stability of regulatory T cells. Nat. Rev. Immunol., 2013, vol. 13, no. 6, pp. 461–467. doi: 10.1038/nri3464
  65. Salzman N.H. Microbiota-immune system interaction: an uneasy alliance. Curr. Opin. Microbiol., 2011, vol. 14, no. 1, pp. 99–105. doi: 10.1016/j.mib.2010.09.018
  66. Sansonetti P.J., Medzhitov R. Learning tolerance while fighting ignorance. Cell, 2009, vol. 138, pp. 416–420. doi: 10.1016/j.cell.2009.07.024
  67. Savage P.A., Malchow S., Leventhal D.S. Basic principles of tumor-associated T cell biology. Trends Immunol., 2013, vol. 34, no. 1, pp. 33–40. doi: 10.1016/
  68. Schmitt E., Klein M., Bopp T. Th9, new players in adaptive immunity. Trends Immunol., 2014, vol. 35, no. 2, pp. 61–68. doi: 10.1016/
  69. Shan M., Gentile M., Yeiser J.R., Walland A.C., Bornstein V.U., Chen K., He B., Cassis L., Bigas A., Cols M., Comerma L., Huang B., Blander J.M., Xiong H., Mayer L., Berin C., Augenlicht L.H., Velcich A., Cerutti A. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science, 2013, vol. 342, no. 6157, pp. 447–453. doi: 10.1126/science.1237910
  70. Smith P.D., Smythies L.E., Shen R., Greenwell-Wild T., Gliozzi M., Wahl S.M. Intestinal macrophages and response to microbial encroachment. Mucosal. Immunol., 2011, vol. 4, no. 1, pp. 31–42. doi: 10.1038/mi.2010.66
  71. Snoeck V., Peters I.E., Cox E. The IgA system: a comparison of structure and function in different species. Vet. Res., 2006, vol. 37, pp. 455–467. doi: 10.1051/vetres:2006010
  72. Sonnenberg G.F., Fouser L.A., Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol., 2011, vol. 12, pp. 383–390. doi: 10.1038/ni.2025
  73. Stappenbeck T.S., Hooper L.V., Gordon J.I. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 24, pp. 15451–15455. doi: 10.1073/pnas.202604299
  74. Steenwinckel V., Louahed J., Lemaire M.M., Sommereyns C., Warnier G., McKenzie A., Brombacher F., Van Snick J., Renauld J.-C. IL-9 promotes IL-13-dependent Paneth cell hyperplasia and up-regulation of innate immunity mediators in intestinal mucosa. J. Immunol., 2009, vol. 182, pp. 4737–4743. doi: 10.4049/jimmunol.0801941
  75. Suzuki K., Meek B., Doi Y., Muramatsu M., Chiba T., Honjo T., Fagarasan S. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 1981–1986. doi: 10.1073/pnas.0307317101
  76. Turner J.R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol., 2009, vol. 9, pp. 799–809. doi: 10.1038/nri2653
  77. Weaver C.T., Hatton R.D. Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective. Nat. Rev. Immunol., 2009, vol. 9, pp. 883–889. doi: 10.1038/nri2660
  78. Wei M., Shinkura R., Doi Y., Maruya M., Fagarasan S., Honjo T. Mice carrying a knock-in mutation of Aicda resulting in a defect in somatic hypermutation have impaired gut homeostasis and compromised mucosal defense. Nat. Immunol., 2011, vol. 12, pp. 264–270. doi: 10.1038/ni.1991
  79. Whitman W.B., Coleman D.C., Wiebe W.J. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 6578–6583.
  80. Williams R.C., Gibbons R.J. Inhibition of bacterial adherence by secretory immunoglobulin A: a mechanism of antigen disposal. Science, 1972, vol. 177, pp. 697–699. doi: 10.1126/science.177.4050.697
  81. Woof J.M., Kerr M.A. IgA function — variations on a theme. Immunology, 2004, vol. 113, pp. 175–177. doi: 10.1111/j.1365-2567.2004.01958.x
  82. Zhang N., Bevan M.J. Transforming growth factor-β signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity, 2013, vol. 39, no. 4, pp. 687–696. doi: 10.1016/j.immuni.2013.08.019
  83. Zhao P., Xiao X., Ghobrial R.M., Li X.C. IL-9 and Th9 cells: progress and challenges. Intern. Immunol., 2013, vol. 25, no. 10, pp. 547–551. doi: 10.1093/intimm/dxt039
  84. Zhu Z., Homer R.J., Wang Z., Chen Q., Geba G.P., Wang J., Zhang Y., Elias J.A. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest., 1999, vol. 103, pp. 779–788. doi: 10.1172/JCI5909

Copyright (c) 2015 Kisseleva E.P.

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

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies