Gut Microbiota as a Modulator of Post-Stress Neuroinflammation: Methodological Limitations of Existing Research Practices

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Abstract

According to the current hypothesis, gut microbiota has a significant impact on the central nervous system and behavior through various mechanisms, including modulation of the immune system and the hypothalamic-pituitary-adrenal axis (HPA axis), epigenetic regulation of gene expression, and production of metabolites. The gut-brain axis is one of the key targets for research into the mechanisms of Alzheimer’s disease, pathological anxiety, mood disorders, and autism. It is suggested that post-stress neuroinflammation, which may be related to changes in the microbiota, plays a role in the development of these pathologies. However, the discovered “dysbiotic patterns” in the microbiomes of animal models under different stress models and in patients suffering from psychopathologies are not specific and may be secondary to the disease. The lack of understanding of the mechanisms by which gut microbiota is involved in the pathogenesis of neuro- and psychopathologies hinders the translation of results obtained from animal models. The review discusses the main methodological problems of research on the “gut-brain axis” and explores ways to address them.

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About the authors

I. G. Shalaginova

Immanuel Kant Baltic Federal University

Author for correspondence.
Email: shalaginova_i@mail.ru
Russian Federation, Kaliningrad

S. P. Luzikova

Immanuel Kant Baltic Federal University

Email: shalaginova_i@mail.ru
Russian Federation, Kaliningrad

A. E. Vylegzhanina

Immanuel Kant Baltic Federal University; Pavlov Institute of Physiology of the Russian Academy of Sciences

Email: shalaginova_i@mail.ru
Russian Federation, Kaliningrad; Saint Petersburg

D. S. Katserov

Immanuel Kant Baltic Federal University

Email: shalaginova_i@mail.ru
Russian Federation, Kaliningrad

References

  1. Williams Z.A., Lang L., Nicolas S., Clarke G., Cryan J., Vauzour D., Nolan Y.M. // Microb. Biotechnol. 2024. Т. 17. № 4. e14462.
  2. Sherwin E., Bordenstein S.R., Quinn J.L., Dinan T.G., Cryan J.F. // Sci. 2019. T. 366. № 6465. eaar2016.
  3. Parashar A., Udayabanu M. // Europ. Neuropsychopharmacol. 2016. Т. 26. № 1. P. 78–91.
  4. Lachmansingh D.A., Lavelle A., Cryan J.F., Clarke G. // Curr. Top. in Behav. Neurosci. 2023. T. 66. P. 175–216.
  5. Sender R., Fuchs S., Milo R. // PLoS Biol. 2016. Т. 14. № 8. e1002533.
  6. Li X., Liu Y., Yang X., Li C., Song Z. // Front. Microbiol. 2022. Т. 13. 895537.
  7. Cryan J.F., O’Riordan K.J., Cowan C.S.M., Sandhu K.V., Bastiaanssen T.F.S., Boehme M., Codagnone M.G., Cussotto S., Fulling C., Golubeva A.V., Guzzetta K.E., Jaggar M., Long-Smith C.M., Lyte J.M., Martin J.A., Molinero-Perez A., Moloney G., Morelli E., Morillas E., O’Connor R., Cruz-Pereira J.S., Peterson V.L., Rea K., Ritz N.L., Sherwin E., Spichak S., Teichman E.M., van de Wouw M., Ventura-Silva A.P., Wallace-Fitzsimons S.E., Niall Hyland, Clarke G., Dinan T.G. // Physiol. Rev. 2019. Т. 99. № 4. P. 1877–2013.
  8. Шалагинова И.Г., Мацкова Л.В., Гуницева Н.М., Ваколюк И.А. // Экологич. генет. 2019. Т. 17. № 4. С. 91–102.
  9. Duvallet C., Gibbons S.M., Gurry T., Irizarry R.A., Alm E.J. // Nat. Comm. 2017. Т. 8. № 1. 1784.
  10. Foster J.A., Rinaman L., Cryan J.F. // Neurobiol. of Str. 2017. Т. 7. P. 124–136.
  11. Lozupone C.A., Stombaugh J.I., Gordon J.I., Jansson J.K., Knight R. // Nat. 2012. Т. 489. № 7415. P. 220–230.
  12. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E., Turnbaugh P.J. // Nat. 2014. Т. 505. № 7484. P. 559–563.
  13. Goodrich J.K., Waters J.L., Poole A.C., Sutter J.L., Koren O., Blekhman R., Ley R.E. // Cell. 2014. Т. 159. № 4. P. 789–799.
  14. Walter J., Armet A.M., Finlay B.B., Shanahan F. // Cell. 2020. Т. 180. № 2. P. 221–232.
  15. Wang Y., Ullah H., Deng T., Ren X., Zhao Z., Xin Y., Qiu J. // Neurosci. Lett. 2024. Т. 826. 137714.
  16. Agranyoni O., Sur D., Amidror S., Shidlovsky N., Bagaev A., Yissachar N., Navon-Venezia S. // BMC Med. 2024. Т. 22. № 1. 182.
  17. Bairachnaya M., Agranyoni O., Antoch M., Michaelevski I., Pinhasov A. // Aging. 2019. Т. 11. № 21. P. 9901–9911.
  18. Sudo N., Chida Y., Aiba Y., Sonoda J., Oyama N., Yu X.N., Kubo C., Koga Y. // J. Physiol. 2004. Т. 558. P. 263–275.
  19. Alam R., Abdolmaleky H.M., Zhou J. // Am. J. Med. Genet. Part B Neuropsychiatr. Genet. 2017. Т. 174. № 6. P. 651–660.
  20. Gur T.L., Shay L., Palkar A.V., Fisher S., Varaljay V.A., Dowd S., Bailey M.T. // Brain. Behav. Immun. 2017. Т. 64. P. 50–58.
  21. Qu Q., Li H., Bai L., Zhang S., Sun J., Lv W., Ye C., Liu S., Shi D. // Indian J. Microbiol. 2021. Т. 61. P. 338–347.
  22. Gao X., Cao Q., Cheng Y., Zhao D., Wang Z., Yang H., Wu Q., You L., Wang Y., Lin Y., Li X., Wang Y., Bian J. S., Sun D., Kong L., Birnbaumer L., Yang Y. // Proc. Natl. Acad. Sci. USA. 2018. Т. 115. № 13. P. 2960–2969.
  23. O’Mahony S.M., Hyland N.P., Dinan T.G., Cryan J.F. // Psychopharmacol. (Berl). 2011. Т. 214. № 1. P. 71–88.
  24. Tannock G.W., Savage D.C. // Infect. Immun. 1974. Т. 9. № 3. P. 591–598.
  25. Bailey M.T., Coe C.L. // Dev. Psychobiol. 1999. Т. 35. P. 146–155.
  26. Nikolova V.L., Smith M.R.B., Hall L.J., Cleare A.J., Stone J.M., Young A.H. // JAMA Psychiat. 2021. Т. 78. № 12. С. 1343–1354.
  27. Hasler G. // Wor. Psychiat. 2010. Т. 9. № 3. P. 155–161.
  28. Barandouzi Z.A., Starkweather A.R., Henderson W.A., Gyamfi A., Cong X.S. // Front. Psychiat. 2020. Т. 11. 541.
  29. Aizawa E., Tsuji H., Asahara T., Takahashi T., Teraishi T., Yoshida S., Ota M., Koga N., Hattori K., Kunugi H. // J. Aff. Disord. 2016. Т. 202. P. 254–257.
  30. Jiang H., Ling Z., Zhang Y., Mao H., Ma Z., Yin Y., Wang W., Tang W., Tan Z., Shi J., Li L., Ruan B. // Brain Behav. Immun. 2015. Т. 48. P. 186–194.
  31. Kelly J.R., Borre Y., O’Brien C., Patterson E., El Aidy S., Deane J., Kennedy P.J., Beers S., Scott K., Moloney G., Hoban A.E., Scott L., Fitzgerald P., Ross P., Stanton C., Clarke G., Cryan J.F., Dinan T.G. // J. Psychiat. Res. 2016. Т. 82. P. 109–118.
  32. McBurney M.I., Davis C., Fraser C.M., Schneeman B.O., Huttenhower C., Verbeke K., Walter J., Latulippe M.E. // J. Nutr. 2019. Т. 149. № 11. P. 1882–1895.
  33. Bastiaanssen T.F.S., Quinn T.P., Loughman A. // Nat. Ment. Health. 2023. Т. 1. P. 930–938.
  34. Zhang Y., Zhang J., Wu J., Zhu Q., Chen C., Li Y. // Front. Microbiol. 2023. Т. 14. 1124454.
  35. Knight R., Vrbanac A., Taylor B.C., Aksenov A., Callewaert C., Debelius J., Gonzalez A., Kosciolek T., McCall L.-I., McDonald D., Melnik A.V., Morton J.T., Navas J., Quinn R.A., Sanders J.G., Swafford A.D., Thompson L.R., Tripathi A., Xu Z.Z., Zaneveld J.R., Qiyun Zhu, Caporaso J.G., Dorrestein P.C. // Nat Rev Microbiol. 2018. Т. 16. P. 410–422.
  36. Geng S., Yang L., Cheng F., Zhang Z., Li J., Liu W., Li Y., Chen Y., Bao Y., Chen L., Fei Z., Li X., Hou J., Lin Y., Liu Z., Zhang S., Wang H., Zhang Q., Wang H., Wang X., Zhang J. // Front. Microbiol. 2020. T. 10. 3067.
  37. Meng C., Feng S., Hao Z., Dong C., Liu H. // PLoS One. 2020. Т. 17. № 3. e0265430.
  38. Shevchenko A., Shalaginova I., Katserov D., Matskova L., Shiryaeva N., Dyuzhikova N. // PloS One. 2023. T. 18. № 12. e0295709.
  39. Long-Smith C., O’Riordan K.J., Clarke G., Stanton C., Dinan T.G., Cryan J.F. // Annu. Rev. Pharmacol. Toxicol. 2020 Т. 6. № 60. P. 477–502.
  40. Olavarría-Ramírez L., Cooney-Quane J., Murphy G., McCafferty C.P., Cryan J.F., Dockray S. // Neurosci. & Biobehav. Rev. 2023. Т. 145. 105013.
  41. Voikar V., Gaburro S, Meyer N. // Front. Behav. Neurosci. 2020. Т. 14. 575434.
  42. Vandeputte D., Kathagen G., D’hoe K., Vieira-Silva S., Valles-Colomer M., Sabino J., Wang J., Tito R.Y., De Commer L., Darzi Y., Vermeire S., Falony G., Raes J. // Nat. 2017. Т. 551. P. 507–511.
  43. Louca S., Doebeli M., Parfrey L.W. // Microb. 2018. Т. 6. № 1. 41.
  44. Zemb O., Achard C.S., Hamelin J., De Almeida M.L., Gabinaud B., Cauquil L., Verschuren L.M.G., Godon J.J. // Microbiol-open. 2020. Т. 9. № 3. e977.

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