Chemokine receptor expression on peripheral blood T-helper cells in Helicobacter pylori-associated diseases: chronic gastroduodenitis and peptic ulcer disease

Cover Page


Cite item

Full Text

Abstract

Helicobacter pylori represents a pathogen causing chronic infection in around a half of the global human population, which manifestations vary from asymptomatic infection to developing gastritis and peptic ulcer. The data accumulated suggest that overt clinical types of this infection are associated with lost immunoregulation and increased pro-inflammatory cell-mediated immune response triggered by H. pylori-specific T helper cells. Here, we examined the degree of peripheral blood CD4+ T cell maturity and related expression of chemokine receptors involved in migration to gastrointestinal tract (CCR9 and CCR6), as well as Тand B-cell zones of lymphoid organs (CCR7 and CXCR5). It was shown that overt H. pylori-infection was coupled to changes in expression pattern of chemokine receptors on T helper cells. In particular, percentage of mature CD4+CD45RO+ T cells bearing CCR9 and immature CD4+CD45RO Т cells expressing CXCR5 was increased in peripheral blood of patients with chronic gastroduodenitis. However, increased amount of activated mature CD4+CD45RO+ICOS+ T cells was observed in patients with chronic gastroduodenitis comorbid with peptic ulcer that was also associated with elevated amount of mature CCR6+ T helpers (mainly CD4+CD45RO+CCR7 CCR6+ cells) and follicular T helper cells as well as emerging minor CD4+CD45RO+CXCR5+CCR6+.T cell subset, not affecting CD4+CCR9+ Т cells. Thus, the data obtained evidence that tissue-specific T-helper cell migration is controlled separately in of H. pylori-associated diseases. 

About the authors

V. Yu. Talayev

I.N. Blokhina Nizhny Novgorod Scientific and Research Institute of Epidemiology and Microbiology

Author for correspondence.
Email: talaev@inbox.ru

PhD, MD (Medicine), Professor, Head of the Laboratory of Cellular Immunology 

Contacts: Vladimir Yu. Talayev 603950, Russian Federation, Nizhny Novgorod, Malaya Yamskaya str., 71, I.N. Blokhina Nizhny Novgorod Research Institute of Epidemiology and Microbiology. Phone: +7 (831) 469-79-48

Russian Federation

M. V. Talaeyva

I.N. Blokhina Nizhny Novgorod Scientific and Research Institute of Epidemiology and Microbiology

Email: marya.talaeva@yandex.ru
PhD (Biology), Senior Researcher, Laboratory of Cellular Immunology Russian Federation

E. V. Voronina

I.N. Blokhina Nizhny Novgorod Scientific and Research Institute of Epidemiology and Microbiology

Email: el2v@mail.ru
Junior Researcher, Laboratory of Cellular Immunology Russian Federation

I. Ye. Zaichenko

I.N. Blokhina Nizhny Novgorod Scientific and Research Institute of Epidemiology and Microbiology

Email: imm.irina@mail.ru
PhD (Biology), Leading Researcher, Laboratory of Cellular Immunology Russian Federation

N. V. Neumoina

I.N. Blokhina Nizhny Novgorod Scientific and Research Institute of Epidemiology and Microbiology

Email: tak1510@yandex.ru
PhD (Medicine), Head Physician, Infectious Diseases Clinic Russian Federation

K. M. Perfilova

I.N. Blokhina Nizhny Novgorod Scientific and Research Institute of Epidemiology and Microbiology

Email: tak1510@yandex.ru
PhD (Medicine), Deputy Head Physician, Infectious Diseases Clinic Russian Federation

O. N. Babaykina

I.N. Blokhina Nizhny Novgorod Scientific and Research Institute of Epidemiology and Microbiology

Email: olga_babaykina@inbox.ru
PhD (Medicine), Senior Researcher, Laboratory of Cellular Immunology Russian Federation

References

  1. Перфилова К.М., Неумоина Н.В., Бутина Т.Ю., Кузнецова И.В., Шутова И.В., Ларионова Т.В., Ефимова Е.И. Опыт использования метода полимеразной цепной реакции для исследования маркеров Heliсobacter pylori //Медицинский альманах. 2016. Т. 42, № 2. С. 52–56.
  2. Талаев В.Ю., Плеханова М.В., Бабайкина О.Н., Воронина Е.В. Характеристика малой субпопуляции наивных CD4+ Т-лимфоцитов, несущих хемокиновый рецептор CXCR5 //Иммунология. 2015. Т. 36, № 1. С. 9–13.
  3. Талаев В.Ю., Талаева М.В., Воронина Е.В., Талаева Е.Б., Заиченко И.Е., Бабайкина О.Н. Содержание и фенотип CCR6+ и CCR9+ Т-хелперов периферической крови у подростков с болезнью Крона //Иммунология. 2017. Т. 38, № 6. С. 313–320.
  4. Bimczok D., Kao J.Y., Zhang M., Cochrun S., Mannon P., Peter S. Wilcox C.M., Mönkemüller K.E., Harris P.R., Grams J.M., Stahl R.D., Smith P.D., Smythies L.E. Human gastric epithelial cells contribute to gastric immune regulation by providing retinoic acid to dendritic cells. Mucosal Immunol., 2016, vol. 8, no. 3, pp. 533–544. doi: 10.1038/mi.2014.86
  5. Carbo A., Olivares-Villagomez D., Hontecillas R., Bassaganya-Riera J., Chaturvedi R., Piazuelo M.B., Delgado A., Washington M.K., Wilson K.T., Algood H.M. Systems modeling of the role of interleukin-21 in the maintenance of effector CD4+ T cell responses during chronic Helicobacter pylori infection. MBio, 2014, vol. 5: e01243-14. doi: 10.1128/mBio.01243-14
  6. Caruso R., Fina D., Paoluzi O.A., Del Vecchio Blanco G., Stolfi C., Rizzo A., Caprioli F., Sarra M., Andrei F., Fantini M.C., MacDonald T.T., Pallone F., Monteleone G. IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur. J. Immunol., 2008, vol. 38, pp. 470–478. doi: 10.1002/eji.200737635
  7. Danesh J. Helicobacter pylori infection and gastric cancer: systematic review of the epidemiological studies. Aliment. Pharmacol. Ther., 1999, vol. 13, pp. 851–856. doi: 10.1038/sj.bjc.6690444
  8. Eaton K.A., Ringler S.R., Danon S.J. Murine splenocytes induce severe gastritis and delayed-type hypersensitivity and suppress bacterial colonization in Helicobacter pylori-infected SCID mice. Infect. Immun., 1999, vol. 67, no. 9, pp. 4594–4602.
  9. Evans-Marin H.L., Cao A.T., Yao S., Chen F., He C., Liu H., Wu W., Gonzalez M.G., Dann S.M., Cong Y. Unexpected regulatory role of CCR9 in regulatory T cell development. PLoS One, 2015, vol. 10, no. 7: e0134100. doi: 10.1371/journal.pone.0134100
  10. Graham D.Y., Opekun A.R., Osato M.S., El-Zimaity H.M., Lee C.K., Yamaoka Y., Qureshi W.A., Cadoz M., Monath T.P. Challenge model for Helicobacter pylori infection in human volunteers. Gut, 2004, vol. 53, pp. 1235–1243. doi: 10.1136/gut.2003.037499
  11. Gray B.M., Fontaine C.A., Poe S.A., Eaton K.A. Complex T cell interactions contribute to Helicobacter pylori gastritis in mice. Infect. Immun., 2013, vol. 81, pp. 740–752. doi: 10.1128/IAI.01269–12
  12. Hutloff A., Dittrich A.M., Beier K.C., Eljaschewitsch B., Kraft R., Anagnostopoulos I., Kroczek RA. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature, 1999, vol. 397, no. 6716, pp. 263–266. doi: 10.1038/16717
  13. Khamri W., Walker M.M., Clark P., Atherton J.C., Thursz M.R., Bamford K.B., Lechler R.I., Lombardi G. Helicobacter pylori stimulates dendritic cells to induce interleukin-17 expression from CD4+ T lymphocytes. Infect. Immun., 2010, vol. 78, pp. 845– 853. doi: 10.1128/IAI.00524–09
  14. Kiriya K., Watanabe N., Nishio A., Okazaki K., Kido M., Saga K., Tanaka J., Akamatsu T., Ohashi S., Asada M., Fukui T., Chiba T. Essential role of Peyer’s patches in the development of Helicobacter-induced gastritis. Int. Immunol., 2007, vol. 19, no. 4, pp. 435–446. doi: 10.1093/intimm/dxm008
  15. Kronsteiner B., Bassaganya-Riera J., Philipson C., Viladomiu M., Carbo A., Abedi V., Hontecillas R. Systems-wide analyses of mucosal immune responses to Helicobacter pylori at the interface between pathogenicity and symbiosis. Gut Microbes., 2016, vol. 7, no. 1, pp. 3–21. doi: 10.1080/19490976.2015.1116673
  16. Kunkel E.J., Campbell J.J., Haraldsen G., Pan J., Boisvert J., Roberts A.I., Ebert E.C., Vierra M.A., Goodman S.B., Genovese M.C., Wardlaw A.J., Greenberg H.B., Parker C.M., Butcher E.C., Andrew D.P., Agace W.W. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: Epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J. Exp. Med., 2000, vol. 192, no. 5, pp. 761–768. doi: 10.1084/jem.192.5.761
  17. Leber A., Abedi V., Hontecillas R., Viladomiu M., Hoops S., Ciupe S., Caughman J., Andrew T., Bassaganya-Riera J. Bistability analysis of CD4+ T follicular helper and regulatory cells during Helicobacter pylori infection. J. Theor. Biol., 2016, vol. 398, pp. 74–84. doi: 10.1016/j.jtbi.2016.02.036
  18. Lina T.T., Alzahrani S., Gonzalez J., Pinchuk I.V., Beswick E.J., Reyes V.E. Immune evasion strategies used by Helicobacter pylori. World J. Gastroenterol., 2014, vol. 20, no. 36, pp. 12753–12766. doi: 10.3748/wjg.v20.i36.12753
  19. Ma C.S., Deenick E.K., Batten M, Tangye S.G. The origins, function, and regulation of T follicular helper cells. J. Exp. Med., 2012, vol. 209, no. 7, pp. 1241–1253. doi: 10.1084/jem.20120994
  20. Marshall B.J., Warren J.R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet, 1984, vol. 1, no. 8390, pp. 1311–1315. doi: 10.1016/S0140–6736(84)91816-6
  21. Matsumoto M., Yokoyama H., Suzuki H., Shiraishi-Yokoyama H., Hibi T. Retinoic acid formation from retinol in the human gastric mucosa: role of class IV alcohol dehydrogenase and its relevance to morphological changes. Am. J. Physiol. Gastrointest. Liver Physiol., 2005, vol. 289, no. 3, pp. G429–433. doi: 10.1152/ajpgi.00502.2004
  22. Mora J.R., Iwata M., von Andrian U.H. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat. Rev. Immunol., 2008, vol. 8, no. 9, pp. 685–698. doi: 10.1038/nri2378
  23. Moyat M., Velin D. Immune responses to Helicobacter pylori infection. World J. Gastroenterol., 2014, vol. 20, no. 19, pp. 5583– 5593. doi: 10.3748/wjg.v20.i19.5583
  24. Nurgalieva Z.Z., Conner M.E., Opekun A.R., Zheng C.Q., Elliott S.N., Ernst P.B., Osato M., Estes M.K., Graham D.Y. B-cell and T-cell immune responses to experimental Helicobacter pylori infection in humans. Infect. Immun., 2005, vol. 73, pp. 2999– 3006. doi: 10.1128/IAI.73.5.2999-3006.2005
  25. Papadakis K.A., Landers C., Prehn J., Kouroumalis E.A., Moreno S.T., Gutierrez-Ramos J.C., Hodge M.R., Targan S.R. CC chemokine receptor 9 expression defines a subset of peripheral blood lymphocytes with mucosal T cell phenotype and Th1 or T-regulatory 1 cytokine profile. J. Immunol., 2003, vol. 171, no. 1, pp. 159–165. doi: 10.4049/jimmunol.171.1.159
  26. Shi Y., Liu X.F., Zhuang Y., Zhang J.Y., Liu T., Yin Z., Wu C., Mao X.H., Jia K.R., Wang F.J., Guo H., Flavell R.A., Zhao Z., Liu K.Y., Xiao B., Guo Y., Zhang W.J., Zhou W.Y., Guo G., Zou Q.M. Helicobacter pylori induced Th17 responses modulate Th1 cell responses, benefit bacterial growth, and contribute to pathology in mice. J. Immunol., 2010, vol. 184, pp. 5121–5129. doi: 10.4049/jimmunol.0901115
  27. Singh S.P., Zhang H.H., Tsang H., Gardina P.J., Myers T.G., Nagarajan V., Lee C.H., Farber J.M. PLZF regulates CCR6 and is critical for the acquisition and maintenance of the Th17 phenotype in human cells. J. Immunol., 2015, vol. 194, no. 9, pp. 4350– 4361. doi: 10.4049/jimmunol.1401093
  28. Suzuki T., Kato K., Ohara S., Noguchi K., Sekine H., Nagura H., Shimosegawa T. Localization of antigen-presenting cells in Helicobacter pylori-infected gastric mucosa. Pathol. Int., 2002, vol. 52, pp. 265–271.
  29. Villablanca E.J., Cassani B., von Andrian U.H., Mora J.R. Blocking lymphocyte localization to the gastrointestinal mucosa as a therapeutic strategy for inflammatory bowel diseases. Gastroenterology, 2011, vol. 140, no. 6, pp. 1776–1784. doi: 10.1053/j.gastro.2011.02.015
  30. Wang C., Kang S.G., Lee J., Sun Z., Kim C.H. The roles of CCR6 in migration of Th17 cells and regulation of effector T-cell balance in the gut. Mucosal Immunol., 2009, vol. 2, pp. 173–183. doi: 10.1038/mi.2008.84

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2019 Talayev V.Y., Talaeyva M.V., Voronina E.V., Zaichenko I.Y., Neumoina N.V., Perfilova K.M., Babaykina O.N.

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

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

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

About Cookies