Immunotropic and Immunogenic Properties of Nonspecific Yersinia Porins
https://doi.org/10.35825/2587-5728-2019-3-4-350-372
EDN: afixlb
Abstract
The purpose of the study is to summarize our own data and literature data on the significance of poreforming proteins of the outer membrane of Yersinia as factors of their pathogenicity and as diagnostic and protective antigens, and their role in pathological processes considered non-infectious. In the last decades of the last century, the epidemic significance of intestinal yersiniosis caused by the bacteria of Yersinia genus, Yersinia pseudotuberculosis and Yersinia enterocolitica, which are the «doubles» of the plague pathogen (Yersinia pestis) by genetic, cultural, biochemical, and other properties, has significantly increased. It has been established that acute yersiniosis infections without effective treatment can pass into secondary focal forms, leading to the development of systemic diseases that were not previously considered infectious (for example, Grave’s disease). They are characterized by multiple organ lesions, dysfunctions of the cardiovascular and nervous systems, musculoskeletal system, urinary system and gastrointestinal tract, which is a consequence of autoimmune processes based on the ability of Yersinia to molecular mimicry. The paper shows that porins play a significant role in the development of the infectious process and can be considered as pathogenic factors of bacteria. Together with other components of the outer membrane of gram negative bacteria, they provide adhesion, invasion and colonization of the cells of the host organism by bacteria. Porins can affect a number of eukaryotic cell functions, including cytokine expression, receptor activation, apoptosis induction, and regulation of the actin cytoskeleton. It has been established that pore-forming Yersinia proteins are protective antigens. The administration of them to laboratory animals induces the formation of species-specific immunity, which allows us to recommend porin protein as a component of chemical and genetic engineering vaccines. Porins are promising for the development of ELISA test systems for the diagnosis of pseudotuberculosis and intestinal yersiniosis, as well as immunopathologies caused by Yersinia bacteria. Given the high degree of similarity of the primary structures of Yersinia porins, it can be assumed that protective preparations created on their basis will protect against infections caused by intestinal yersiniosis, pseudotuberculosis and plague pathogens.
About the Authors
O. D. NovikovaRussian Federation
Olga Daniilovna Novikova. Chief Researcher. Doctor of Chemical Sciences
Prospect 100 let Vladivostoku, 159, Vladivostok 690022
O. Yu. Portnyagina
Russian Federation
Olga Yurievna Portnyagina. Senior Researcher. Candidate of Biological Sciences
Prospect 100 let Vladivostoku, 159, Vladivostok 690022
O. P. Vostrikova
Russian Federation
Olga Pavlovna Vostricova. Senior Researcher. Candidate of Chemical Sciences
Prospect 100 let Vladivostoku, 159, Vladivostok 690022
V. A. Ivanis
Russian Federation
Viktoria Alersandrovna Ivanis. Professjr. Doctor of Medicine
Prospect Ostryakova, 2, Vladivostok, 690002
References
1. Onishchenko G. G. The epidemiological situation and the main directions of the fight against infectious diseases in the Russian Federation for the period 1991-1996 // Epidemiol. Infect. Dis. 1997. №3. P.4–13 (in Russian).
2. Pokrovsky V.M., Onishchenko G.G., Cherkassky B.L. The evolution of infectious diseases in Russia in the XX century. M.: 2003 (in Russian).
3. Onishchenko G.G. On government measures to prevent the spread of infectious hepatitis in the Russian Federation // Epidemiol. Infect. Dis. 2002. №3. Р. 4–8 (in Russian).
4. Pokrovsky V.M., Maleev V.V. Actual problems of infectious pathology // Epidemiol. Infect. Dis. 1999. № 2. P. 17–20 (in Russian).
5. Infectious morbidity in the Russian Federation for January – September 1996: Official information // Epidemiology and Infectious Diseases / Goskomsanepidnadzor of Russia, Russian Information and Analytical Center. 1997. № 1. Р. 64 (in Russian).
6. Сhesnokova M.V., Klimov V.T., Nikitin A.Ya., Yarygina M.B., Innokentieva T.I., Balakhonov S.V. Analysis of the epidemiological situation of pseudotuberculosis and intestinal yersiniosis in Russia and the prognosis of morbidity for the mediumterm // Public Health and Habitat. 2018. № 9. P. 59–64 (in Russian).
7. Cherkassky B.L. Modern features of the epidemiology of intestinal infections in the Russian Federation // Epidemiol. Infect. Dis. 1997. № 5. Р. 12–15 (in Russian).
8. Kutyrev V.V. Actual problems of especially dangerous infectious diseases and sanitary protection of the territory in modern conditions // Zh. Microbiol., Epidemiol., Immunobiol. 2008. № 1. Р. 17–23 (in Russian).
9. Kosilko S.A., Balakhonov S.V., Brenyova N.V. et al. Epidemiological situation of zoonotic, natural focal infectious diseases in Siberia and the Far East in 2013 and forecast for 2014 // Problems of Particularly Dangerous Infections. 2014. Issue. 2. Р. 53–57 (in Russian).
10. Somov G.P. Yersiniosis infection at the present stage // Zh. Microbiol., Epidemiol., Immunobiol. 1997. № 5. Р. 7–11 (in Russian).
11. Tseneva G.Ya., Solodovnikova N.Yu., Voskresenskaya E.A. Molecular aspects of Yersinia virulence // Clin. Microbiol. Antimicrobial Chemother. 2002. Vol. 4, №. 3. Р. 248–266 (in Russian).
12. Somov G.P., Pokrovsky V.I., Besednova N.N., Antonenko F.F. Pseudotuberculosis. M.: 2001 (in Russian).
13. Tseneva G.Ya., Voskresenskaya E.A., Solodovnikova N. Yu. et al. Biological properties of Yersinia and laboratory diagnosis of pseudotuberculosis and yersiniosis. Manual for doctors. Pasteur Institute of Epidemiology and Microbiology, St. Petersburg: 2001 (in Russian).
14. Sidelnikova S. M., Yushchenko G. V., Aseeva E. I. Yersiniosis as a therapeutic problem // Therapeutic Archive. 2000. № 11. Р. 27-30 (in Russian).
15. Tseneva G.Ya. Yersinia and yersiniosis. St. Petersburg. Media: 2006 (in Russian).
16. Granfors K., Merilahti-Palo R., Luukkainen R. et al. Persistence of Yersinia antigens in peripheral blood cells from patients with Yersinia enterocolitica O:3 infection with or without reactive arthritis // Arthritis & Rheum. 1998. V. 41. P. 855-862.
17. Obert A.S., Khilchuk V.P., Goncharenko A.I. The prognostic value of immunological reactivity in children with pseudotuberculosis // G.N. Speransky Pediatrics. Zhurn. 1996. № 2. P. 35–38 (in Russian).
18. Voskresenskaya E.A., Tseneva G.Ya. Immunological parameters in pathology due to yersiniosis // Zh. Microbiol., Epidemiol. Immunobiol. 1996. № 5. Р. 68–73 (in Russian).
19. Zheleznikova G.F., Ivanova V.V., Monakhova N.E. Immunopathogenesis options for acute infections in children. St. Petersburg Tome: 2007 (in Russian).
20. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited // Microbiol. Mol. Biol. Rev. 2003. V. 67, №. 4. Р. 593–656.
21. Achouak W., Heulin T., Pages J.P. Multiple facets of bacterial porins // FEMS Microbiol. Lett. 2001. V. 199, № 1. P. 1–7.
22. Rawling E.G., Martin N.L., Hancock R.E.W. Epitope mapping of the Pseudomonas aeruginosa major outer membrane porin protein OprF // Infect. Immun. 1995. V. 63, № 1. P. 38–42.
23. Supotnitsky M.V. Effective patenting of means of specific prophylaxis of infectious diseases // Biotechnology. 1997. № 9-10. Р. 56–79 (in Russian).
24. Novikova O.D., Soloviev. T.F. Nonspecific porins of the outer membrane of gram negative bacteria: structure and properties // Biol. membrany. 2009. V. 26, № 1. Р. 6–20 (in Russian).
25. Portnyagina O.Yu., Novikova O.D., Solovieva T.F. Immunological properties of non-specific porins of the outer membrane of gram negative bacteria // Biol. membrany. 2005. V. 22, № 5. Р. 357–365 (in Russian).
26. Vostrikova O.P., Kim N.Yu., Likhatskaya G.N. et al. The structure and function of pore-forming proteins of bacteria of the genus Yersinia. 1. Isolation and comparative characteristics of the physicochemical properties and functional activity of Yersinia porins // Bioorgan. Khimiya. 2006. V. 32, № 4. P. 371–383 (in Russian).
27. Chistyulin D.K., Novikova O.D., Portnyagina O. Yu. et al. Isolation and characterization of an OmpF-like porin of the outer membrane of Yersinia ruckeri // Biol. membrany. 2012. V. 29, №. 3. Р. 1–9 (in Russian).
28. Novikova O.D., Khomenko V.A., Emelyanenko V.I. et al. OmpC-like porin fromYersinia pseudotuberculosis: molecular characterization, physicochemical and functional properties // Biol. membrany. 2011. V. 28, №. 1. Р. 1–16 (in Russian).
29. Vostrikova O.P., Isaeva M.P., Likhatskaya G.N. et al. OmpС – like porins of the outer membrane of Yersinia entrocolitica: molecular structure and functional activity // Biokhimiya. 2013. V. 78, №. 5. P. 550–560 (in Russian).
30. Novikova O.D., Fedoreeva L.I., Khomenko V.A. et al. Effect of the method of extraction of a poreforming protein from Yersinia pseudotuberculosis on its macromolecular organization // Bioorgan. Khimiya. 1993. V. 19, № 5. Р. 536–547 (in Russian).
31. Khomenko V.A., Novikova O.D., Fedoreeva L.I. et al. Porin from Yersinia enterocolitica 0: 3. Isolation and characterization // Biol. membrany. 1994. V. 11, № 1. Р. 68– 79 (in Russian).
32. Novikova O.D., Chistyulin D.K., Khomenko V.A. еt al. Peculiarities of thermal denaturation of OmpF porin from Yersinia ruckeri // Molecular BioSystems. 2017. V. 13. P. 1854–1862.
33. Chistyulin D.K., Novikova O.D., Zelepuga E.A. et al. Abnormally high closing potential of the porin channel OmpF from Yersinia ruckeri: the role of charged residues and intramolecular bonds // Acta Naturae. 2019. V. 11, № 3. P. 89–98 (in Russian).
34. Bystritskaya E., Stenkova A., Chistuylin D. et. al. Adaptive responses of outer membrane porin balance of Yersinia ruckeri under different incubation temperature, osmolarity, and oxygen availability // Microbiology Open. 2016. V. 5, № 4. P. 597–603.
35. Selinsky B.S. Protein-lipid interactions and membrane function // In: The structure of biological membranes. Yeagle P., ed. Boca Raton: CRC Press. 1992. P. 603–651.
36. Novikova O.D., Vakorina T.I., Khomenko V.A. et al. Influence of cultivation conditions on the spatial structure of OmpF-like porin from the outer membrane of Yersinia pseudotuberculosis // Biokhimiya. 2008. V. 73. P. 173–184 (in Russian).
37. Bogdanov M., Dowhan W., Vitrac H. Lipids and topological rules governing membrane protein assembly // Biochim. Biophys. Acta. 2014. V. 1843, № 8. P. 1475–1488.
38. Krasikova I.N., Bakholdina S.I., Solovyova T.F. Glucose as a growth medium factor regulating the lipid composition of Yersinia pseudotuberculosis // Biokhimiya. 2001. V. 66, № 8. P. 1122–1127 (in Russian).
39. Bystritskaya E.P., Stenkova A.M., Portnyagina O.Yu. et al. Regulation of expression of the main porin of Yersinia pseudotuberculosis under conditions of antibiotic stress // Mol. Gen., Microbiol.Virol. 2014. № 2. Р. 17–21 (in Russian).
40. Achtman M., Zurth K., Morelli G. et al. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis // Proc. Natl. Acad. Sci. U.S.A. 1999. V. 96. P. 14043–14048.
41. Kleinschmidt J.H. Membrane proteins – Introduction // Cell Mol. Life Sci. 2003. V. 60, № 8. P. 1527–1528.
42. Likhatskaya G.N., Solov’eva T.F., Novikova O.D. et al. Homology models of the Yersinia pseudotuberculosis and Yersinia pestis general porins and comperative analysis of their functional and antigenic regions // J. Biomol. Struct. Dyn. V. 23, № 2. P. 163–174.
43. Patent RF № 98122085/14 (in Russian).
44. Patent RF № 98122085/14 (in Russian).
45. Portnyagina O.Yu., Vostrikova O.P., Khomenko V.A. et al. Testing an enzyme-linked immunosorbent assay system based on the porin protein from Yersinia pseudotuberculosis for the diagnosis of pseudotuberculosis (extraintestinal yersiniosis) in children // Immunology. 2000. № 2. Р. 59–61 (in Russian).
46. Vostrikova O.P., Portnyagina O.Yu., Khomenko V.A. andothers. A new approach in the diagnosis of yersiniosis // Cytokines and inflammation. 2005. V. 4, № 3.P. 132–133 (in Russian).
47. Portnyagina O.Yu., Sidorova O.V., Khomenko V.A. et al. Study of the immunogenic properties of recombinant OmpF-like porin from the outer membrane of Yersinia pseudotuberculosis // Bull. Exp. Biol. Med. 2009. № 7. Р. 85– 88 (in Russian).
48. Vostrikova O.P., Portnyagina O.Yu., Novikova O.D. et al. Clinical and immunological characteristics of patients with rheumatoid arthritis associated with yersiniosis infection // Ros. Allerg. Zh. 2012. № 5, issue 1. Р. 55–57 (in Russian).
49. Vostrikova O.P., Portnyagina O.Yu., Khomenko V.A. et al. A new approach in the diagnosis of yersiniosis // Cytokines and inflammation. 2005. V. 4, № 3. P. 132−133 (in Russian).
50. Vostrikova O.P., Portnyagina O.Yu., Novikova O.D. et al. Immunological characteristics of secondary immunodeficiencies associated with yersiniosis infection // Ros. Allerg. Zh. 2013. № 2, part 2. P. 61−63 (in Russian).
51. Vostrikova O.P., Portnyagina O.Yu., Khomenko V.A. et al. Clinical and immunological characteristic of the diffusion nodale of nontoxic goiter of Yersinia etiology // European Science and Technology: materials of the 4th international research and practice conference, Munich, Germany, Apr. 10th−11th, 2013. Munich: Vela-Verlag Waldkraiburg, 2013. V. 2. P. 536−544.
52. Darmov I.V., Marakulin I.V., Pogorelsky I.P. et al. Prevention of experimental pseudotuberculosis infection by immunization with porin from Yersinia pseudotuberculosis // Bull. Exp Biol. Med. 1999. V. 127, № 2. Р. 221–223 (in Russian).
53. Portnyagina O.Yu., Sidorova O.V., Novikova O.D. et al. Immunochemical characterization of synthetic peptides, including T- and B-cell epitopes of nonspecific porins of pathogenic yersinia // Bioorgan. Khimiya. 2010. V. 36, № 6. Р. 779–788 (in Russian).
54. Antonets D.V., Bakulina A.Yu., Portnyagina O.Yu. et al. Prediction of antigenically active regions of OmpFlike porin Yersinia pseudotuberculosis // Dokl. Biochem. Biophys. 2007. V. 414, № 4. Р. 1–3 (in Russian).
55. Timchenko N.F., Novikova O.D., Pavlova T.N. et al. Protective properties of porin from the outer membrane of Yersinia pseudotuberculosis // Zh. Microbiol., Epidemiol. Immunobiol. 1990. № 11. P. 48–50 (in Russian).
56. Novikova O.D., Likhatskaya G.N., Frolova G.M. et al. Molecular organization and biological properties of yersinin – porin from the pseudotuberculosis microbe Yersinia pseudotuberculosis // Biol. Membrany. 1990. V. 7, № 5. С. 453–461 (in Russian).
57. Byvalov A.A., Konyshev I.V., Novikova O.D. et al. Adhesion of OmpF and OmpC porins of Yersinia pseudotuberculosis to macrophages J774 // Biophysics. 2018. V. 63, № 5, Р. 913–922 (in Russian).
58. Portnyagina O.Yu., Kuzmich A.S., Khomenko V.A. et al. Induction of the synthesis of interleukins and chemotaxis activators under the influence of OmpF porin from Yersinia pseudotuberculosis in an in vivo model // Cytokines and inflammation. 2019. № 1(in Russian).
59. Cusick M.F., Libbey J.E., Fujinami R.S. et. al., Molecular mimicry as a mechanism of autoimmune disease // Clin. Rev. Allergy Immunol. 2012 V. 42. № 1. Р. 102–111.
60. Fujinami R.S. Viruses and autoimmune disease– two sides of the same coin? // Trends Microbiol. 2001. V. 9. P. 377–381.
61. Damian R.T. Molecular mimicry: antigen sharing by parasite and host and its consequences // Am. Nat. 1964. V. 98. P. 129–149.
62. Blank M. Molecular Mimicry and Auto-Immunity // Clin. Rev. Allergy Immunol. 2007. V. 32. Р.111–118.
63. Corapçioğlu D., Tonyukuk V., Kiyan M. et al. Relationship between thyroid autoimmunity and Yersinia enterocolitica antibodies // Thyroid. 2002. V. 12, № 7. Р. 613–617.
64. Wenzel B.E., Strieder T.M., Gaspar. E. et al. Chronic infection with Yersinia enterocolitica in patients with clinical or latent hyperthyroidism // Adv. Exp. Med. Biol. 2003. V. 529. Р. 463– 466.
65. Kunihiko T., Chazenbalk G.D., MeLaehlan S.M., Rapoport B. Subunit structure of thyrotropin receptors expressed on the cell surface // J. Biol. Chem. 1999. V. 274, № 48. Р. 33979–33984.
66. Timchenko N.F., Andryukov B.G. Detection of antibodies to Yersinia enterocolitica in patients with autoimmune thyroidopathy // Infect. Dis. 2012. V. 10, №. 4. P. 37–40 (in Russian).
67. Vostrikova O.P., Portnyagina O.Yu., Khomenko V.A. et. al. Clinical and immunological characteristic of the diffusion nodale of nontoxic goiter of Yersinia etiology // European Science and Technology: materials of the 4thinternational research and practice conference, Munich, Germany, Apr. 10th-11th, 2013. Munich: VelaVerlag Waldkraiburg, 2013; 2:536–544.
68. Wang Z., Zhang Q., Lu J. et. al. Identification of outer membrane porin F protein of Yersinia enterocolitica recognized by antithyrotopin receptor antibodies in Grave’s disease and determination of its epitope using mass spectrometry and bioinformatics tools // J. Clin. Endocrinol. Metab. 2010. V. 95, № 8. Р. 4012–4020.
69. Portnyagina O., Zelepuga E., Khomenko V. et al. In silico and in vitro analysis of cross-reactivity between Yersinia pseudotuberculosis OmpF porin and thyroid stimulating hormone receptor // Int. J. Biol. Macromol. 2018. V. 107(Pt B). P. 2484–2491.
70. Portnyagina O.Yu., Golotin V.A., Zelepuga E.A. et al. Nonspecific porins of Yersinia pseudotuberculosis as inducers of experimental hyperthyroidism in mice // Bull. Exp. Biol. Med. 2018. V. 166, № 12. Р. 714–717 (in Russian).
Review
For citations:
Novikova O.D., Portnyagina O.Yu., Vostrikova O.P., Ivanis V.A. Immunotropic and Immunogenic Properties of Nonspecific Yersinia Porins. Journal of NBC Protection Corps. 2019;3(4):350-372. (In Russ.) https://doi.org/10.35825/2587-5728-2019-3-4-350-372. EDN: afixlb