Interaction of dendritic cells with microorganisms capable of colonizing the intestine


Introduction. The use of bacterial vectors is one of the possible ways to deliver vaccine antigens to mucous membranes to induce mucosal immunity. In our opinion, microorganisms suitable for this purpose should cause safe and, preferably, temporary colonization of mucous membranes and effectively induce immune responses, in particular, be well absorbed by antigen-presenting cells and cause their maturation.

The aim of the study – search for microorganisms suitable for use as vectors for live oral vaccines.

Material and methods. 8 different bacteria and yeast capable of permanent or temporary persistence in the gastrointestinal tract were used. We compared the phagocytosis of microorganisms by human monocyte-derived dendritic cells, as well as the effect of these microorganisms on the expression of CD83, CD86, CCR7, and CXCR5 molecules on dendritic cells.

Results. Susceptibility to phagocytosis and the ability to induce the maturation of dendritic cells are independent properties of microorganisms. For example, Escherichia coli actively induce the phenotypic maturation of dendritic cells, but are relatively weakly phagocytosed and brings little microbial material into dendritic cells. Lactiplantibacillus plantarum and Limosilactobacillus fermentum, on the contrary, are well absorbed by dendritic cells, but have little effect on their maturation.

Conclusion. Based on the indicators of phagocytosis and the ability to stimulate the maturation of dendritic cells, Bacillus cereus seems to be the most acceptable candidate for the role of a bacterial vector among the microorganisms used in the work.

Keywords:dendritic cells; phagocytosis; maturation; intestinal microorganisms

For citation: Talayev V.Yu., Zaichenko I.Ye., Svetlova M.V., Voronina E.V., Babaykina О.N., Soloveva I.V., Belova I.V., Tochilina A.G. Interaction of dendritic cells with microorganisms capable of colonizing the intestine. Immunologiya. 2022; 43 (4): 412–22. DOI: (in Russian)

Funding. The study had no sponsorship.

Conflict of interests. The authors declare no conflict of interests.

Authorsʼ contribution: article writing – Talayev V.Yu.; work with dendritic cells – Zaichenko I.Ye., Voronina E.V.; flow cytometry – Svetlova M.V.; work with microorganisms – Zaichenko I.E., Babaykina O.N., Soloveva I.V., Belova I.V., Tochilina A.G.


1. Pinegin B.V., Pashchenkov M.V, Pinegin V.B., Khaitov R.M. Mucosal epithelial cells and novel approaches to immunoprophylaxy and immunotherapy of infectious diseases. Immunology. 2020; 41 (6): 486–500. DOI: (in Russian)

2. Logunov D.Y., Dolzhikova I.V., Shcheblyakov D.V., Tukhvatulin A.I., Zubkova O.V., Dzharullaeva A.S., Kovyrshina A.V., Lubenets N.L., Grousova D.M., Erokhova A.S., Botikov A.G., Izhaeva F.M., Popova O., Ozharovskaya T.A., Esmagambetov I.B., Favorskaya I.A., Zrelkin D.I., Voronina D.V., Shcherbinin D.N., Semikhin A.S., Simakova Y.V., Tokarskaya E.A., Egorova D.A., Shmarov M.M., Nikitenko N.A., Gushchin V.A., Smolyarchuk E.A., Zyryanov S.K., Borisevich S.V., Naroditsky B.S., Gintsburg A.L.; Gam-COVID-Vac Vaccine Trial Group. Safety and efficacy of an rAd26 and rAd5 vector-based heterologous prime-boost COVID-19 vaccine: an interim analysis of a randomised controlled phase 3 trial in Russia. Lancet. 2021; 397 (10 275): 671–81. DOI:

3. Andreev I.V., Nechay K.O., Andreev A.I., Zubareva A.P., Esaulova D.R., Alenova A.M., Nikolaeva I.A., Chernyavskaya O.P., Lomonosov K.S., Shul’zhenko A.E., Kurbacheva O.M., Latysheva E.A., Shartanova N.V., Nazarova E.V., Romanova L.V., Cherchenko N.G., Smirnov V.V., Averkov O.V., Martynov A.I., Vechorko V.I., Gudima G.O., Kudlay D.A., Khaitov M.R., Khaitov R.M. Post-vaccination and post-infection humoral immune response to the SARS-CoV-2 infection. Immunologiya. 2022; 43 (1): 18–32. DOI: (in Russian)

4. Dietrich G., Gentschev I., Hess J., Ulmer J.B., Kaufmann S.H., Goebel W. Delivery of DNA vaccines by attenuated intracellular bacteria. Immunol. Today. 1999; 20 (6): 251–3. DOI:

5. Spreng S., Dietrich G., Niewiesk S., ter Meulen V., Gentschev I., Goebel W. Novel bacterial systems for the delivery of recombinant protein or DNA. FEMS Immunol. Med. Microbiol. 2000; 27 (4): 299–304. DOI:

6. Gentschev I., Dietrich G., Spreng S., Kolb-Mäurer A., Daniels J., Hess J., Kaufmann S.H., Goebel W. Delivery of protein antigens and DNA by virulence-attenuated strains of Salmonella typhimurium and Listeria monocytogenes. J. Biotechnol. 2000; 83 (1–2): 19–26. DOI:

7. Gentschev I., Dietrich G., Spreng S., Pilgrim S., Stritzker J., Kolb-Mäurer A., Goebel W. Delivery of protein antigens and DNA by attenuated intracellular bacteria. J. Med. Microbiol. 2002; 291: 577–82. DOI:

8. Hess J., Grode L., Hellwig J., Conradt P., Gentschev I., Goebel W., Ladel C., Kaufmann S.H. Protection against murine tuberculosis by an attenuated recombinant Salmonella typhimurium vaccine strain that secretes the 30-kDa antigen of Mycobacterium bovis BCG. FEMS Immunol. Med. Microbiol. 2000; 27 (4): 283–9. DOI:

9. Spreng S., Gentschev I., Goebel W., Weidinger G., ter Meulen V., Niewiesk S. Salmonella vaccines secreting measles virus epitopes induce protective immune responses against measles virus encephalitis. Microbes Infect. 2000; 2 (14): 1687–92. DOI:

10. Parida S.K., Huygen K., Ryffel B., Chakraborty T. Novel bacterial delivery system with attenuated Salmonella typhimurium carrying plasmid encoding Mtb antigen 85A for mucosal immunization: establishment of proof of principle in TB mouse model. Ann. N. Y. Acad. Sci. 2005; 1056: 366–78. DOI:

11. Spreng S., Dietrich G., Goebel W., Gentschev I. Protection against murine listeriosis by oral vaccination with recombinant Salmonella expressing protective listerial epitopes within a surface-exposed loop of the TolC-protein. Vaccine. 2003; 21 (7–8): 746–52. DOI:

12. Sreerohini S., Balakrishna K., Parida M. Oral immunization of mice with Lactococcus lactis expressing Shiga toxin truncate confers enhanced protection against Shiga toxins of Escherichia coli O157:H7 and Shigella dysenteriae. APMIS. 2019; 127 (10): 671–80. DOI:

13. Craig K., Dai X., Li A., Lu M., Xue M., Rosas L., Gao T.Z., Niehaus A., Jennings R., Li J.A. Lactic Acid Bacteria (LAB)-based vaccine candidate for human norovirus. Viruses. 2019; 11 (3): E213. DOI:

14. Kuczkowska K., Copland A., Overland L., Mathiesen G., Tran A.C., Paul M.J., Eijsink V.G.H., Reljic R. Inactivated Lactobacillus plantarum carrying a surface-displayed Ag85B-ESAT-6 fusion antigen as a booster vaccine against Mycobacterium tuberculosis infection. Front. Immunol. 2019; 10: 1588. DOI:

15. Hiramatsu Y., Hosono A., Konno T., Nakanishi Y., Muto M., Suyama A., Hachimura S., Sato R., Takahashi K., Kaminogawa S. Orally administered Bifidobacterium triggers immune responses following capture by CD11c+ cells in Peyer’s patches and cecal patches. Cytotechnology. 2011; 63 (3): 307–17. DOI:

16. Mellman I., Steinman R.M. Dendritic cells: specialized and regulated antigen processing machines. Cell. 2001; 106: 255–8. DOI:

17. Guermonprez P., Valladeau J., Zitvogel L., Théry C., Amigorena S. Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 2002; 20: 621–67. DOI:

18. Savina A., Amigorena S. Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 2007; 219: 143–56. DOI:

19. Alvarez D., Vollmann E.H., von Andrian U.H. Mechanisms and consequences of dendritic cell migration. Immunity. 2008; 29 (3): 325–42. DOI:

20. Talaev V.Y., Talaeva М.V., Voronina Е.V., Babaykina О.N. Migration of human dendritic cells in vitro induced by vaccines stimulating humoral and cell immunity. Sovremennye tekhnologii v meditsine. 2016; 8 (3): 91–9. DOI: (in Russian)

All articles in our journal are distributed under the Creative Commons Attribution 4.0 International License (CC BY 4.0 license)

Musa R. Khaitov

Corresponding member of Russian Academy of Sciences, MD, Professor, Director of the NRC Institute of Immunology FMBA of Russia