M CELLS ARE THE IMPORTANT POST IN THE INITIATION OF IMMUNE RESPONSE IN INTESTINE

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Abstract

Microfold cells (M cells) are specialized intestinal epithelial cells that initiate mucosal immune responses. These unique phagocytic epithelial cells are specialized for the transfer of a broad range of particulate antigens and microorganisms across the follicle-associated epithelium (FAE) into the gut-associated lymphoid tissue (GALT) by a process termed transcytosis. The molecular basis of antigen uptake by M cells has been gradually identified in the last decade. Active sampling of intestinal antigen initiates regulated immune responses that ensure intestinal homeostasis. The delivery of luminal substances across the intestinal epithelium to the immune system is a critical event in immune surveillance resulting in tolerance to dietary antigens and immunity to pathogens (e.g., bacteria, viruses, and parasites) and their toxins. Several specialized mechanisms transport luminal antigen across the gut epithelium. Discovery of M cell-specific receptors are of great interest, which could act as molecular tags for targeted delivery oral vaccine to M cells. Recent studies demonstrated that M cells utilize several receptors to recognize and transport specific luminal antigens. Vaccination through the mucosal immune system can induce effective systemic immune responses simultaneously with mucosal immunity. How this process is regulated is largely unknown. This review aims to show a new understanding of the factors that influence the development and function of M cells; to show the molecules expressed on M cells which appear to be used as immunosurveillance receptors to sample pathogenic microorganisms in the gut; to note how certain pathogens appear to exploit M cells to inject the host; and, finally, how this knowledge is used to specifically "target" antigens to M cells to attempt to improve the efficacy of mucosal vaccines. Recently, substantial progress has been made in our understanding of the factors that influence the development and function of M cells.

About the authors

A. S. Bykov

First Moscow State Medical University (Sechenov University).

Author for correspondence.
Email: bykov@imail.ru

PhD, MD (Medicine), Professor, Department of Microbiology, Virology and Immunology.

103009, Russian Federation, Moscow, Mokhovaya str., 11–10.

Phone: +7 916 494-35-43 (mobile).

Россия

A. V. Karaulov

First Moscow State Medical University (Sechenov University).

Email: fake@neicon.ru

RAS Full Member, PhD, MD (Medicine), Professor, Head of the Department of Clinical Immunology and Allergology.

Moscow. Россия

D. A. Tsomartova

First Moscow State Medical University (Sechenov University).

Email: fake@neicon.ru

PhD (Medicine), Associate Professor, Department of Histology, Cytology, Embryology. 

Moscow. Россия

N. L. Kartashkina

First Moscow State Medical University (Sechenov University).

Email: fake@neicon.ru

PhD (Medicine), Associate Professor, Department of Histology, Cytology, Embryology.

Moscow. Россия

V. L. Goriachkina

First Moscow State Medical University (Sechenov University).

Email: fake@neicon.ru

PhD (Biology), Associate Professor, Department of Histology, Cytology, Embryology.

Moscow. Россия

S. L. Kuznetsov

First Moscow State Medical University (Sechenov University).

Email: fake@neicon.ru

PhD, MD (Medicine), Professor, Head of the Department of Histology, Cytology, Embryology.

Moscow. Россия

D. A. Stonogina

First Moscow State Medical University (Sechenov University).

Email: fake@neicon.ru

5th Year Student.

Moscow.

Россия

Ye. V. Chereshneva

First Moscow State Medical University (Sechenov University).

Email: fake@neicon.ru

PhD (Medicine), Associate Professor, Department of Histology, Cytology, Embryology.

Moscow. Россия

References

  1. Быков А.С., Зверев В.В., Пашков Е.П., Караулов А.В., Быков С.А. Медицинская микробиология, вирусология и иммунология. Атлас-руководство. М.: МИА, 2018, 416 с.
  2. Akashi S., Saitoh S., Wakabayashi Y., Kikuchi T., Takamura N., Nagai Y., Kusumoto Y., Fukase K., Kusumoto S., Adachi Y., Kosugi A., Miyake K. Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14. J. Exp. Med., 2003, vol. 198, no. 7, pp. 1035–1042. doi: 10.1084/jem.20031076
  3. Amerongen H.M., Weltzin R., Farnet C.M., Michetti P., Haseltine W.A., Neutra M.R. Transepithelial transport of HIV by intestinal M cells: a mechanism for transmission of AIDS. J. Acquir. Immune Defic. Syndr., 1991, vol. 4, pp. 760–765.
  4. Asai T., Morrison S.L. The SRC family tyrosine kinase HCK and the ETS family transcription factors SPIB and EHF regulate transcytosis across a human follicle-associated epithelium model. J. Biol. Chem., 2013, vol. 288, pp. 10395–10405. doi: 10.1074/jbc.M112.437475
  5. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P.J., Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature, 2007, vol. 449, pp. 1003–1007. doi: 10.1038/nature06196
  6. Brandtzaeg P. Gate-keeper function of the intestinal epithelium. Benef. Microbes, 2013, vol. 4, pp. 67–82. doi: 10.3920/BM2012.0024
  7. Chen K., Cerutti A. Vaccination strategies to promote mucosal antibody responses. Immunity. 2010, vol. 33, no. 4. pp. 479–491. doi: 10.1016/j.immuni.2010.09.013
  8. Chiba S., Nagai T., Hayashi T., Baba Y., Nagai S., Koyasu S. Listerial invasion protein internalin B promotes entry into ileal Peyer’s patches in vivo. Microbiol. Immunol. 2011, vol. 55, no. 2, pp. 123–129. doi: 10.1111/j.1348-0421.2010.00292.x
  9. Cunningham A.L., Guentzel M.N., Yu J.J., Hung C.Y., Forsthuber T.G., Navara C.S., Yagita H., Williams I.R., Klose K.E., Eaves-Pyles T.D., Arulanandam B.P. M-cells contribute to the entry of an oral vaccine but are not essential for the subsequent induction of protective immunity against Francisella tularensis. PLoS One, 2016, vol. 11, no. 4: e0153402. doi: 10.1371/journal.pone.0153402
  10. De Lau W., Kujala P., Schneeberger K., Middendorp S., Li V.S., Barker N., Martens A., Hofhuis F., DeKoter R.P., Peters P.J., Nieuwenhuis E., Clevers H. Peyer’s patch M cells derive from Lgr5(+) stem cells, require SpiB and are induced by RankL in cultured “organoids”. Mol. Cell. Biol., 2012, vol. 32, no. 18, pp. 3639–3647. doi: 10.1128/MCB.00434-12
  11. Donaldson D.S, Sehgal A., Rios D, Williams I.R., Mabbott N.A. Increased abundance of M cells in the gut epithelium dramatically enhances oral prion disease susceptibility. PLoS Pathog., 2017, vol. 13, no. 2: e1006222. doi: 10.1371/journal.ppat.1006222
  12. Eugenin E.A., Gaskill P.J., Berman J.W. Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell. Immunol., 2009, vol. 254, no. 2, pp. 142–148. doi: 10.1016/j.cellimm.2008.08.005
  13. Fujimura Y., Takeda M., Ikai H., Haruma K., Akisada T., Harada T., Sakai T., Ohuchi M. The role of M cells of human nasopharyngeal lymphoid tissue in influenza virus sampling. Virchows Arch., 2004, vol. 444, no. 1, pp. 36–42.
  14. Gebert A., Pabst R. M cells at locations outside the gut. Semin. Immunol., 1999, vol. 11, no. 3, pp. 165–170. doi: 10.1006/smim.1999.0172
  15. Gonzalez-Hernandez M.B., Liu T., Payne H.C., Stencel-Baerenwald J.E., Ikizler M., Yagita H., Dermody T.S., Williams I.R., Wobus C.E. Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells. J. Virol., 2014, vol. 88, no. 12, pp. 6934–6943. doi: 10.1128/JVI.00204-14
  16. Gousset K., Schiff E., Langevin C., Marijanovic Z., Caputo A., Browman D.T., Chenouard N., de Chaumont F., Martino A., Enninga J., Olivo-Marin J.C., Männel D., Zurzolo C. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 2009, vol. 11, no. 3, pp. 328–336. doi: 10.1038/ncb1841
  17. Hase K., Kawano K., Nochi T., Pontes G.S., Fukuda S., Ebisawa M., Kadokura K., Tobe T., Fujimura Y., Kawano S., Yabashi A., Waguri S., Nakato G., Kimura S., Murakami T., Iimura M., Hamura K., Fukuoka S., Lowe A.W., Itoh K., Kiyono H., Ohno H. Uptake through glycoprotein 2 of FimH (+) bacteria by M cells initiates mucosal immune response. Nature, 2009, vol. 462, pp. 226–230. doi: 10.1038/nature08529
  18. Hase K., Ohshima S., Kawano K., Hashimoto N., Matsumoto K. Distinct gene expression profiles characterize cellular phenotypes of follicle-associated epithelium and M cells. DNA Res., 2005, vol. 12, pp. 127–137.
  19. Helander A., Silvey K.J., Mantis N.J., Hutchings A.B., Chandran K., Lucas W.T., Nibert M.L., Neutra M.R. The viral σ1 protein and glycoconjugates containing α2-3-linked sialic acid are involved in type I reovirus adherence to M cell apical surfaces. J. Virol., 2003, vol. 77, no. 14, pp. 7964–7977. doi: 10.1128/JVI.77.14
  20. Kanaja F., Ohno H. The Mechanisms of M-cell Differentiation. Biosci. Microbiota Food Health. 2014, vol. 33, no. 3, pp. 91–97. doi: 10.12938/bmfh.33.91
  21. Kanaya T., Hase K., Takahashi D., Fukuda S., Hoshino K., Sasaki I., Hemmi H., Knoop K.A., Kumar N., Sato M., Katsuno T., Yokosuka O., Toyooka K., Nakai K., Sakamoto A., Kitahara Y., Jinnohara T., McSorley S.J., Kaisho T., Williams I.R., Ohno H. The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells. Nat. Immunol., 2012, vol. 13, no. 8, pp. 729–736. doi: 10.1038/ni.2352
  22. Kim S.H., Jang Y.S. Antigen targeting to M cells for enhancing the efficacy of mucosal vaccines. Exp. Mol. Med., 2014, vol. 46, no. 3, pp. 1–14. doi: 10.1038/emm.2013.165
  23. Kim S.H., Jang Y.S. The development of mucosal vaccines for both mucosal and systemic immune induction and the roles played by adjuvants. Clin. Exp. Vaccine Res., 2017, vol. 6, pp. 15–21. doi: 10.7774/cevr.2017.6.1.15
  24. Kim S.H., Jung D.I., Yang I.Y., Kim J., Lee K.Y., Nochi T., Kiyono H., Jang Y.S. M cells expressing the complement C5a receptor are efficient targets for mucosal vaccine delivery. Eur J. Immunol., 2011, vol. 41, no.11, pp. 3219–3229. doi: 10.1002/eji.201141592
  25. Kim S.H., Lee H.Y., Jang Y.S. Expression of the ATP-gated P2X7 receptor on M cells and its modulating role in the mucosal immune environment. Immune Netw., 2015, vol. 15, no. 1, pp. 44–49. doi: 10.4110/in.2015.15.1.44
  26. Kishikawa S., Sato S., Kaneto S., Uchino S., Kohsaka S., Nakamura S., Kiyono H. Allograft inflammatory factor 1 is a regulator of transcytosis in M cells. Nat. Commun., 2017, vol. 8: 14509. doi: 10.1038/ncomms14509
  27. Knoop K.A., Kumar N., Butler B.R., Sakthivel S.K., Taylor R.T., Nochi T., Akiba H., Yagita H., Kiyono H, Williams I.R. RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium. J. Immunol., 2009, vol. 183, no. 9, pp. 5738–5747. doi: 10.4049/jimmunol.0901563
  28. Knoop K.A., McDonald K.G., McCrate S, McDole J.R., Newberry R.D. Microbial sensing by goblet cells controls immune surveillance of luminal antigens in the colon. Mucosal Immunol., 2015, vol. 8, no. 1, pp. 198–210. doi: 10.1038/mi.2014.58
  29. Kobayashi A., Donaldson D.S., Erridge C., Kanaya T., Williams I.R., Ohno H., Mahajan A., Mabbott N.A. The functional maturation of M cells is dramatically reduced in the Peyer’s patches of aged mice. Mucosal Immunol., 2013, vol. 6, no.5, pp. 1027–1037. doi: 10.1038/mi.2012.141
  30. Koga T., McGhee J. R., Kato H., Kato R, Kiyono H., Fujihashi K. Evidence for early aging in the mucosal immune system. J. Immunol., 2000, vol. 165, no. 9, pp. 5352–5359. doi: 10.4049/jimmunol.165.9.5352
  31. Kolawole A.O., Gonzalez-Hernandez M.B., Turula H., Yu C., Elftman M.D., Wobus C.E. Oral norovirus infection is blocked in mice lacking Peyer’s patches and mature M cells. J. Virol., 2016, vol. 90, no. 3, pp. 1499–1506. doi: 10.1128/JVI.02872-15
  32. Kujala P., Raymond C.R, Romeijn M., Godsave S.F., van Kasteren S.I., Wille H., Prusiner S.B., Mabbott N.A., Peters P.J. Prion uptake in the gut: identification of the first uptake and replication sites. PLoS Pathog., 2011, vol. 7 (12): e1002449. doi: 10.1371/journal.ppat.1002449
  33. Lelouard H., Fallet M., de Bovis B., Meresse S., Gorvel J.P. Peyer’s patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores. Gastroenterology, 2012, vol. 142, pp. 592–601.
  34. Ling J., Liao H., Clark R., Wong M.S., Lo D.D. Structural constraints for the binding of short peptides to Claudin 4 revealed by surface plasrion resonance. J. Biol. Chem., 2008, vol. 283, no. 45, pp. 30585–30595. doi: 10.1074/jbc.M803548200
  35. Lo D.D., Ling J., Eckelhoefer A.H. M cell targeting by a Claudin 4 targeting peptide can enhance mucosal IgA responses. BMC Biotechnol., 2012, vol. 12: 7. doi: 10.1186/1472-6750-12-7
  36. Lügering A., Floer M., Westphal S, Maaser C., Spahn T.W., Schmidt M.A., Domschke W., Williams I.R., Kucharzik T. Absence of CCR6 inhibits CD4+ regulatory T-cell development and M-cell formation inside Peyer’s patches. Am. J. Pathol., 2005, vol. 166, no. 6, pp. 1647–1654.
  37. Mabbott N.A., Donaldson D.S., Ohno H., Williams I.R., Mahajan A. Microfold (M) cells; important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol., 2013, vol. 6, no. 4, pp. 666–677. doi: 10.1038/mi.2013.30
  38. Mach J., Hshieh T., Hsieh D., Grubbs N., Chervonsky A. Development of intestinal M cells. Immunol. Rev., 2005, vol. 206, pp. 177–189. doi: 10.1111/j.0105-2896.2005.00281.x
  39. Maharjan S., Sing B., Jiang T., Yoon S.-Y., Li H.-S., Kim G., Gu M.J., Kim S.J., Park O.J., Han S.H., Kang S.K., Yun C.H., Choi Y.J., Cho C.S. Systemic administration of RANKL overcomes the bottleneck or oral vaccine delivery through microfold cells in the ileum. Biomaterials, 2016, vol. 84, pp. 286–300. doi: 10.1016/j.biomaterials.2016.01.043
  40. Manicassamy S., Pulendran B. Modulation of adaptive immunity with Toll-like receptors. Semin. Immunol., 2009, vol. 21, no. 4, pp. 185–193. doi: 10.1016/j.smim.2009.05.005
  41. Matsumura T., Sugawara Y., Yutani M., Amatsu S., Yagita H., Kohda T., Fukuoka S., Nakamura Y., Fukuda S., Hase K., Ohno H., Fujinaga Y. Botulinum toxin A complex exploits intestinal M cells to enter the host and exert neurotoxicity. Nat. Commun., 2015, vol. 6: 6255. doi: 10.1038/ncomms7255
  42. McDole J.R., Wheeler L.W., McDonald K.G., Wang B., Konjufca V., Knoop K.A., Newberry R.D., Miller M.J. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature, 2012, vol. 483, no. 7389, pp. 345–349. doi: 10.1038/nature10863
  43. Miller H., Zhang J., Kuolee R., Patel G.B., Chen W. Intestinal M cells: the fallible sentinels? World J. Gastroenterol., 2007, vol. 13, no. 10, pp. 1477–1486.
  44. Nagatake T., Fujita H., Minato N., Hamazaki Y. Enteroendocrine cells are specifically marked by cell surface expression of Claudin-4 in mouse small intestine. PLoS ONE, 2014, vol. 9, no. 3: e90638. doi: 10.1371/journal.pone.0090638
  45. Nakato G., Fukuda S., Hase K., Goitsuka R., Cooper M.D., Ohno H. New approach for m-cell-specific molecules by screening comprehensive transcriptome analysis. DNA Res. 2009, vol. 16, no. 4, pp. 227–235. doi: 10.1093/dnares/dsp013
  46. Nakato G., Hase K., Suzuki M., Kimura M., Ato M., Hanazato M., Tobiume M., Horiuchi M., Atarashi R., Nishida N., Watarai M., Imaoka K., Ohno H. Cutting edge: Brucella abortus exploits a cellular prion protein on intestinal M cells as an invasive receptor. J. Immunol., 2012, vol. 189, no. 4, pp. 1540–1544. doi: 10.4049/jimmunol.1103332
  47. Neutra M.R., Frey A., Kraehenuhl J.P. Epithelial M cells: gateways for mucosal infection and immunization. Cell, 1996, vol. 86, no. 3, pp. 345–348; PMID: 8756716; http://dx.doi.org/10.1016/S0092-8674(00)80106-3
  48. Nochi T., Yuki Y., Matsumura A., Mejima M., Terahara K., Kim D.Y., Fukuyama S., Iwatsuki-Horimoto K., Kawaoka Y., Kohda T., Kozaki S., Igarashi O., Kiyono H. A novel M cell-specific carbohydrate-targeted mucosal vaccine effectively induces antigen-specific immune responses. J. Exp. Med. 2007, vol. 204, no. 12, pp. 2789–2796.
  49. Owen R.L., Jones A.L. Epithelial cell specialization within human Peyer’s patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterol., 1974, vol. 66, no. 2, pp. 189–203. doi: 10.1016/S0016-5085(74)80102-2
  50. Pabst O., Mowat A.M. Oral tolerance to food protein. Mucosal Immunol., 2012, vol. 5, no. 3, pp. 232–239. doi: 10.1038/mi.2012
  51. Rand J.H., Wu X.X., Lin E.Y., Griffel A., Gialanella P., McKitrick J.C. Annexin A5 binds to lipopolysaccharide and reduces its endotoxin activity. MBio, 2012, vol. 3, no.11, pii: e00292-11. doi: 10.1128/mBio.00292-11
  52. Ren Z., Gay R., Thomas A., Pae M., Wu D., Logsdon L., Mecsas J., Meydani S.N. Effect of age on susceptibility to Salmonella Typhimurium infection in C57BL/6 mice. J. Med. Microbiol., 2009, vol. 58, pt. 12, pp. 1559–1567. doi: 10.1099/jmm.0.013250-0
  53. Rochereau N., Drocourt D., Perouzel E., Pavot V., Redelinghuys P., Brown G.D. Tiraby G., Roblin X., Verrier B., Genin C., Corthésy B., Paul S. Dectin-1 is essential for reverse transcytosis of glycosylated sIgA-antigen complexes by intestinal M cells. PLoS Biol., 2013, vol. 11, no. 9: e1001658. doi: 10.1371/journal.pbio.1001658
  54. Rouch J.D., Scott A., Lei N.Y., Solorzano-Vargas R.S., Wang J., Hanson E.M., Kobayashi M., Lewis M., Stelzner M.G., Dunn J.C.Y., Eckmann L., Martín M.G. Development of funetional microfold (M) cells from intestinal stem cells in primary human enteroids. PLOS one, 2016, vol. 11, no. 1, pp. 1–16. doi: 10.1371/journal.pone.0148216
  55. Rustom A., Saffrich R., Markovic I., Walther P., Gerdes H.H. Nanotubular highways for intercellular organelle transport. Science, 2004, vol. 303, pp. 1007–1010. doi: 10.1126/science.1093133
  56. Sato S., Kaneto S., Shibata N., Takahashi Y., Okura H., Yuki Y., Kunisawa J., Kiyono H. Transcription factor Spi-B-dependent and -independent pathways for the development of Peyer’s patch M cells. Mucosal Immunol., 2013, vol. 6, no. 4, pp. 838–846. doi: 10.1038/mi.2012.122
  57. Secott T.E., Lin T.L., Wu C.C. Mycobacterium avium subsp. paratuberculosis fibronectin attachment protein facilitates M-cell targeting and invasion through a fibronectin bridge with host integrins. Infect Immun. 2004, vol. 72, no. 7, pp. 3724–3732. doi: 10.1128/IAI.72.7.3724-3732.2004
  58. Siciński P., Rowiński J., Warchoł J.B., Jarzabek Z., Gut W., Szczygieł B., Bielecki K., Koch G. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology, 1990, vol. 98, pp. 56–58.
  59. Tahoun A., Mahajan S., Paxton E., Malterer G., Donaldson D.S., Wang D., Tan A, Gillespie T.L., O’Shea M., Roe A.J., Shaw D.J., Gally D.L., Lengeling A., Mabbott N.A., Haas J., Mahajan A. Salmonella transforms follicle-associated epithelial cells into M cells to promote intestinal invasion. Cell Host Microbe, 2012, vol. 12, no. 5, pp. 645–656. doi: 10.1016/j.chom.2012.10.009
  60. Terahara K., Yoshida M., Igarashi O., Nochi T., Pontes G.S., Hase K., Ohno H., Kurokawa S., Mejima M., Takayama N., Yuki Y., Lowe A.W., Kiyono H. Comprehensive gene expression profiling of Peyer’s patch M cells, villous M-like cells, and intestinal epithelial cells. J. Immunol., 2008, vol. 180, no. 12, pp. 7840–7846. doi: 10.4049/jimmunol.180.12.7840
  61. Travassos L.H., Girardin S.E., Philpott D.J., Blanot D., Nahori M.A., Werts C., Boneca I.G. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep., 2004, vol. 5, no. 10, pp. 1000–1006.
  62. Verbrugghe P., Kujala P., Waelput W., Peters P.J., Cuvelier C.A. Clusterin in human gut-associated lymphoid tissue, tonsils, and adenoids: localization to M cells and follicular dendritic cells. Histochem Cell Biol., 2008, vol. 129, no. 3, pp. 311–320. doi: 10.1007/s00418-007-0369-4
  63. Wang J., Gusti V., Saraswati A., Lo D.D. Convergent and divergent development among M cell lineages in mouse mucosal epithelium. J. Immunol., 2011, vol. 187, no. 10, pp. 5277–5285. doi: 10.4049/jimmunol.1102077
  64. Wang K.C., Huang C.H., Huang C.J., Fang S.B. Impacts of Salmonella enterica serovar Typhimurium and its speG gene on the transcriptomes of in vitro M cells and Caco-2 cells. PLOS ONE, 2016, vol. 11, no. 4, pp. 1–21. doi: 10.1371/journal.pone.0153444
  65. Wang M., Gao Z., Zhang Z., Pan L., Zhang Y. Roles of M cells in infection and mucosal vaccines. Human Vaccines & Immunother., 2014, vol. 10, no. 12, pp. 3544–3551. doi: 10.4161/hv.36174
  66. Westphal S., Lugering A, von Wedel J., von Eiff C, Maaser C., Spahn T., Heusipp G., Schmidt M.A., Herbst H., Williams I.R., Domschke W., Kucharzik T. Resistance of chemokine receptor 6-deficient mice to Yersinia enterocolitica infection: evidence on defective M-cell formation in vivo. Am. J. Pathol., 2008, vol. 172, no. 3, pp. 671–680. doi: 10.2353/ajpath.2008.070393
  67. Wobus C.E. Oral norovirus infection is blocked in mice lacking Peyer’s patches and mature M cells. J. Virol., 2016, vol. 90, no. 3, pp. 1499–1506. doi: 10.1128/JVI.02872-15

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Copyright (c) 2018 Bykov A.S., Karaulov A.V., Tsomartova D.A., Kartashkina N.L., Goriachkina V.L., Kuznetsov S.L., Stonogina D.A., Chereshneva Y.V.

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