Preview

Medical Immunology (Russia)

Advanced search

INFLUENCE OF PROBIOTICS ON CYTOKINE PRODUCTION IN THE IN VITRO AND IN VIVO SYSTEMS

https://doi.org/10.15789/1563-0625-2015-5-443-454

Abstract

Modulatory effects of three probiotic bacterial strains (Lactobacillus rhamnosus K32 (L), Bifidobacterium longum GT15 (B, Enterococcus faecium L-3 (E) on expression level and contents of key cytokines were studied using PCR techniques with reverse transcription, and enzyme-linked immunosorbent assay. Both cell cultures and an experimental model of intestinal dysbiosis were used in this study.

The genes encoding bacteriocins, surface membrane component, pili and exopolysaccharides involved in host immune system modulation were previously identified in the B and Ebacterial strains.

Investigation of probiotic strains and effects of their supernatants expression of cytokines in cell cultures of promonocyte origin (HTP-1) showed increased expression of TNFα, due to E and L supernatants. Moreover, the Bl culture induced IL-8 and IL-10 expression.

In a model of Wistar rats with ampicillinand metronidazole-induced intestinal dysbiosis corrected with probiotics we have shown that the dysbiosis was accompanied by sufficient alterations in microbiota composition (Klebsiella spp. overgrowth and low contents of Faecalobacterium prausnitzii) that were observed only in the animals untreated with probiotics (control), or after administration of L.

In contrast to these results, the animals treated with E and B, the following changes were revealed: 1) low expression of proinflammatory cytokines IL-8, TNFα, MCP-1 inmesenteric lymph nodes and appropriate changes of their serum contents, 2) increased serum content of the anti-inflammatory TGFβ cytokine. Hence, the present study, having used two complementary models, has detected some individual features of immune modulation produced by the probiotictic strains of L. rhamnosus K32, B. longum GT15 и E. faecium L-3 which exert differential effects upon the intestinal microbiota. 

About the Authors

O. V. Averina
N.I. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow
Russian Federation
PhD, MD (Biology), Senior Research Associate, Laboratory of Genetics of Microorganisms


E. I. Ermolenko
Institute of Experimental Medicine, St. Petersburg; Saint Petersburg State University
Russian Federation

PhD, MD (Medicine), Head, Laboratory of Biomedical Microecology, Research Institute of Experimental Medicine; Professor, Faculty of Medicine, St. Petersburg State University.

Address for correspondence: Ermolenko Elena I. Research Institute of Experimental Medicine 197376, Russian Federation, St. Petersburg, Acad. Pavlov str., 12. Phone: 7 (812) 234-05-42. Fax: 7 (812) 234-94-77. E-mail: lermolenko1@yandex.ru

 



A. Yu. Ratushniy
N.I. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow
Russian Federation
Student Moscow State University, Research Institute of General Genetics, Russian Academy of Sciences Petersburg State University
Competing Interests: Cтудент 5 курса МГУ, ФГБУН «Институт общей генетики им. Н.И. Вавилова» РАН


E. A. Tarasova
Institute of Experimental Medicine, St. Petersburg
Russian Federation
Research Associate, Department of Normal Physiology


Yu. Yu. Borschev
Institute of Experimental Medicine, St. Petersburg
Russian Federation
PhD (Biology), Research Associate, Department of Molecular Microbiology


G. F. Leontieva
Institute of Experimental Medicine, St. Petersburg
Russian Federation
PhD (Biology), Leading Research Associate, Department of Molecular Microbiology Petersburg State University


T. A. Kramskaya
Institute of Experimental Medicine, St. Petersburg
Russian Federation
PhD (Biology), Senior Research Associate, Department of Molecular Microbiology Petersburg State University


M. P. Kotyleva
Institute of Experimental Medicine, St. Petersburg; Saint Petersburg State University
Russian Federation
Research Associate, Department of Molecular Microbiology, Research Institute of Experimental Medicine; St. Petersburg State University


V. N. Danilenko
N.I. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow
Russian Federation
PhD, MD (Biology), Professor, Chief, Laboratory of Genetics of Microorganisms Petersburg State University


A. N. Suvorov
Institute of Experimental Medicine, St. Petersburg; Saint Petersburg State University
Russian Federation
PhD, MD (Medicine), Professor, Chief of Department of Molecular Microbiology, Research Institute of Experimental Medicine; head of the Department of Fundamental medicine and medical technologies in Saint Petersburg State University


References

1. Бельтюков П.П., Абдурасулова И.Н., Тарасова Е.А., Суворов А.Н., Захарова Е.Т., Соколов А.В., Карпенко М.Н., Ермоленко Е.И. Исследование влияния пробиотических эшерихий и энтерококков на иммунную систему здоровых крыс // Ученые записки Санкт-Петербургского государственного медицинского университета имени академика И.П. Павлова, 2009. Вып. 16, № 2. С. 54-58. [Beltyukov P.P., Abdurasulova I.N., Tarasova E.A., Suvorov A.N., Zakharova E.T., Sokolov A.V., Karpenko M.N., Ermolenko E.I. Influence of probiotic Escherichia and Enterococci on the immune system of healthy rats. The Record of the I.P. Pavlov St. Petersburg State Medical University, 2009, Vol. 16, no. 2, pp. 54-58. (In Russ.)]

2. Волошина Е.В., Зубова С.В., Прохоренко С.В. Сравнение эффектов разных хемотипов липополисахаридов из Escherichia coli и Salmonella на синтез TNFα и IL-6 макрофагоподобными клетками ТНР-1 // Медицинская иммунология, 2009. Т. 11, № 6. C. 509-514. [VoloshinaE.V., Zubova S.V., Prokhorenko S.V.A comparison of different lipopolysaccharide chemotypes from Escherichia coli and Salmonella upon synthesis of TNFα and IL-6 by macrophagelike THP-1 cells. Meditsinskaya Immunologiya = Medical Immunology (Russia), 2009, Vol. 11, no. 6, pp. 509-514. doi: 10.15789/1563-0625-2009-6-509-514 (In Russ.)]

3. Грачева Н.М., Бондаренко В.М. Пробиотические препараты в терапии и профилактике дисбактериоза кишечника // Инфекционные болезни, 2004. № 2. C. 53-58. [Gracheva N.M., Bondarenko V.M. Probiotics in therapy and prevention of intestinal dysbiosis. Infectsionnye bolezni = Infectious Diseases, 2004, no. 2, pp. 53-58. [In Russ.]

4. Ермоленко Е.И. Иммуномодулирующее действие пробиотических бактерий при заболеваниях желудочно-кишечного тракта // Вестник Санкт-Петербургского университета, Серия 11: Медицина, 2014. Вып. 4. С. 5-18. [Ermolenko E.I. Immunomodulatory effect of probiotic bacteria in case of the diseases of gastrointestinal tract. Bulletin of St. Petersburg State University, 2014, Vol. 4, pp. 5-18. (In Russ.)]

5. Ермоленко Е.И., Донец В.Н., Дмитриева Ю.В., Ильясов Ю.Ю., Суворова М.А., Громова Л.В. Влияние пробиотических энтерококков на функциональные характеристики кишечника крыс при дисбиозе, индуцированном антибиотиками // Вестник Санкт-Петербургского университета, Серия 11: Медицина, 2009. Вып. 1. C. 157-167. [Ermolenko E.I., Donets V.N., Dmitrieva Y.V., Ilyasov Yu.Yu., Suvorov M.A., Gromova L.V. Influence of probiotic enterococci on functional characteristics of rat bowel under disbiosis induced by antibiotics. Bulletin of St. Petersburg State University, 2009, Vol. 1, pp. 157-167. (In Russ.)]

6. Федорова И.А., Даниленко В.Н. Иммуногенные свойства пробиотического компонента микробиоты желудочно-кишечного тракта человека // Успехи современной биологии, 2014. Т. 134, № 2. С. 99-110. [Fedorova I.A., Danilenko V.N. Immunogenic Properties of a Probiotic Component of the Human Gastroenteric Tract Microbiota. Uspekhi sovremennoy biologii = Biology Bulletin Reviews, 2014, Vol. 134, no. 2, pp. 99-100. (In Russ.)]

7. Auwerx J. The human leukemia cell line, THP-1: a multifacetted model for the study of monocytemacrophage differentiation. Experientia, 1991, Vol. 47, рр. 22-31.

8. Baken K.A., Ezendam J., Gremmer E.R., de Klerk A., Pennings J.L.A., Matthee B., Peijnenburg A.A.C.M., van Loveren H. Evaluation of immunomodulation by Lactobacillus casei Shirota: Immune function, autoimmunity and gene expression. Int. J. Food Microbiol., 2006, Vol. 112, no. 1, рр. 8-18.

9. Bassaganya-Riera J., Viladomiu M., Pedragosa M., De Simone C., Carbo A., Shaykhutdinov R., Jobin C., Arthur J.C., Corl B.A., Vogel H., Storr M., Hontecillas R. Immunoregulatory mechanisms underlying prevention of colitis-associated colorectal cancer by probiotic bacteria. PLoS One, 2012, Vol. 7, no. 4, e34676.

10. Bengmark S. Gut microbiota, immune development and function. Pharmacological Research, 2013, Vol. 69, pp. 87-113.

11. Caselli M., Vaira D., Cassol F., Calò G., Vaira G., Papini F., Holton J. Recombinant probiotics and their potential in human health. Int. J. Probiotics Prebiotics, 2012, Vol. 7, pp. 53-58.

12. Collado M.C., Gueimonde M., Hernández M.S., Salminen S. Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. Journal of Food Protection, 2005, Vol. 12, pp. 2502-2720.

13. Cronin, M., Ventura M., Fitzgerald G.F. and van Sinderen D. Progress in genomics, metabolism and biotechnology of bifidobacteria. Int. J. Food Microbiol., 2011, Vol. 149, pp. 4-18.

14. de Moreno de LeBlanc, A., LeBlanc J. G., Perdigon, G., Miyoshi, A., Langella P., Azevedo V., Sesma, F. Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice. J. Med. Microbiol., 2008, Vol. 57, pp. 100-105.

15. Eeckhaut V., Machiels K., Perrier C., Romero C., Maes S., Flahou B., Steppe M., Haesebrouck F., Sas B., Ducatelle R., Vermeire S., Van Immerseel F. Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut, 2013, Vol. 62, no. 12, pp. 1745-1752.

16. Ermolenko E., Gromova L., Borschev Y., Voeikova A., Ermolenko K., Gruzdkov A., Suvorov A. Influence of different probiotic lactic acid bacteria on microbiota and metabolism of rats with dysbiosis. Bioscience of Microbiota, Food and Health, 2013, Vol. 32, no. 2, pp. 41-49.

17. Fanning S., Hall L.J., Cronin M., Zomer A., MacSharry J., Goulding D., Motherway M.O., Shanahan F., Nally K., Dougan G., van Sinderen D. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc. Natl. Acad. Sci. USA, 2012, Vol. 109, no. 6, pp. 2108-2113.

18. Foligne B. A Key Role of Dendritic Cells in Probiotic Functionality. PLoS One, 2007, Vol. 2, no. 3, e313.

19. Foroni E., Serafini F., Amidani D., Turroni F., He F., Bottacini F., O’Connell M.M., Viappiani A., Zhang Z., Rivetti C., van Sinderen D., Ventura M. Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium. Microbiol. Cell Factories, 2011, Vol. 10, pp. 1-13.

20. Galdeano C.M., de Moreno de Blance A., Vinderola G., Bonet M.E., Perdigon G. Proposed model: mechanisms of immunomodulation induced by probiotic bacteria. Clinical and Vaccine Immunology, 2007, Vol. 14, no. 5, pp. 484-492.

21. Hardy H., Harris J., Lyon E., Beal J., Foey A.D. Probiotics, Prebiotics and Immunomodulation of Gut Mucosal Defences: Homeostasis and immunopathology. Nutrients, 2013, Vol. 5, pp. 1869-1912.

22. Huibregtse I.L., Zaat S.A., Kapsenberg M.L., Maria A. Sartori da Silva M.A.S., Peppelenbosch M.P., Sander J.H., van Deventer S.J.H., Braat H. Genetically modified Lactococcus lactis for delivery of human interleukin-10 to dendritic cells. Gastroenterology Research and Practice, 2012, Article ID 639291, 7 p.

23. Jones S. and Versalovic J. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and antiinflammatory factors. BMC Microbiology, 2009, Vol. 9, p. 35.

24. Khokhlova E.V., Smeianov V.V, Efimov B.A., Kafarskaia L.I., Pavlova S.I. Anti-inflammatory properties of intestinal Bifidobacterium strains isolated from healthy infants. Microbiol. Immunol., 2012, Vol. 56, no. 1, pp. 27-39.

25. Kole A., Maloy K.J. Control of intestinal inflammation by interleukin-10. Curr Top Microbiol Immunol., 2014, Vol. 380, pp. 19-38.

26. Lan J.-G., Cruicshank S.M., Singh J.C.I., Farrar M., Lodge J.P.A., Felsburg P.J., Carding S.R. Different cytokine response of primary colonic epithelial cells to commensal bacteria. World Gastroenterol., 2005, Vol. 11, no. 22, pp. 3375-3384.

27. Maassen C., Claassen E. Strain-dependent effects of probiotic lactobacilli on EAE autoimmunity. Vaccine, 2008, Vol. 26, no. 17, pp. 2056-2057.

28. Medina M.,Izquierdo E., Ennahar S., Sanz Y. Differential immunomodulatory properties of Bifidobacterium longum strains: relevance to probiotic selection and clinical applications. Clin. Exp. Immunol., 2007, Vol. 150, no 3, pp. 531-538.

29. Miquel S., Martín R., Rossi O., Bermúdez-Humarán L., Chatel J., Sokol H., Thomas M., Wells J., Langella P. Faecalibacterium prausnitzii and human intestinal health. Curr. Opin. Microbiol., 2013, Vol. 16, no. 3, pp. 255-261.

30. Ouwehand A.C., Salminen S., Isolauri E. Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek, 2002, Vol. 82, pp. 279-289.

31. Pagnini C., Saeed R., Bamias G., Arseneau K.O., Pizarro T.T., Cominelli F. Probiotics promote gut health through stimulation of epithelial innate immunity. Proc. Natl. Acad. Sci. U. S. A., 2010, Vol. 107, no. 1, pp. 454-459.

32. Qiu X., Zhang M., Yang X., Hong N., Yu C. Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. J. Crohns. Colitis., 2013, Vol. 7, pp. 558-568.

33. Saleh M., Elson C.O. Experimental inflammatory bowel disease: insights into the host-microbiota dialog. Immunity, 2011, Vol. 34, no. 3, pp. 293-302.

34. Sartor R.B. Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol., 2006, Vol. 3, pp. 390-407.

35. Silva V. de O., Foureaux R.C., Araujo T.S., Peconick A.P., Zangeronimo M.G., Pereira L.J. Effect of Probiotic Administration on the Immune Response. A Systematic Review of Experimental Models in Rats. Braz. Arch. Biol. Technol., 2012, Vol. 55, no. 5, pp. 685-694.

36. Suvorov A. Gut Microbiota, Probiotics, and Human Health. Bioscience of Microbiota, Food and Health, 2013, Vol. 32, no. 3, pp. 81-91.

37. Wang S., Mei Ng L.H., Chow W.L., Lee Y.K. Infant intestinal Enterococcus faecalis down-regulates inflammatory responses in human intestinal al cell lines. World J. Gastroenterology, 2008, Vol. 14, no. 7. pp. 1067-1076.

38. Xu X.R., Liu C.Q., Feng B.S., Liu Z.J. Dysregulation of mucosal immune response in pathogenesis of inflammatory bowel disease. World J. Gastroenterol., 2014, Vol. 20, no. 12, pp. 3255-3264.

39. Young V.B. The intestinal microbiota in health and disease. Opin. Gastroenterol, 2012, Vol. 28, pp. 63-69.

40. Zhi-bing Q., Liang Z., Chen J., Lan R., Jian C. Construction of a recombinant Lactobacillus strain expressing IL-10. Infect. Immun., 2004, Vol. 72, no. 9, pp. 5308-5314.

41. Zhipeng L., Guangyu L., Hanlu L., Jiaping Z., Yi J., Fuhe Y. The analysis of the impacting factors of probiotics on immune responses. African Journal of Microbiology Research, 2012, Vol. 6, no. 11, pp. 2735-2743.

42. Zughaier S.M., Zimmer S.M., Datta, A., Carlson, R.W., Stephens D.S. Differential induction of the toll-like receptor 4-MyD88-dependent and -independent signaling pathways by endotoxins. Infect. Immun, 2005, Vol. 73, pp. 2940-2950.


Review

For citations:


Averina O.V., Ermolenko E.I., Ratushniy A.Yu., Tarasova E.A., Borschev Yu.Yu., Leontieva G.F., Kramskaya T.A., Kotyleva M.P., Danilenko V.N., Suvorov A.N. INFLUENCE OF PROBIOTICS ON CYTOKINE PRODUCTION IN THE IN VITRO AND IN VIVO SYSTEMS. Medical Immunology (Russia). 2015;17(5):443-454. (In Russ.) https://doi.org/10.15789/1563-0625-2015-5-443-454

Views: 2987


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


ISSN 1563-0625 (Print)
ISSN 2313-741X (Online)