Exploring the microbiota-gut-brain axis: impact on brain structure and function.

Lidya K Yassin, Mohammed M Nakhal, Alreem Alderei, Afra Almehairbi, Ayishal B Mydeen, Amal Akour, Mohammad I K Hamad
Author Information
  1. Lidya K Yassin: Department of Anatomy, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
  2. Mohammed M Nakhal: Department of Anatomy, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
  3. Alreem Alderei: Department of Anatomy, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
  4. Afra Almehairbi: Department of Anatomy, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
  5. Ayishal B Mydeen: Department of Anatomy, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
  6. Amal Akour: Department of Pharmacology and Therapeutics, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
  7. Mohammad I K Hamad: Department of Anatomy, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.

Abstract

The microbiota-gut-brain axis (MGBA) plays a significant role in the maintenance of brain structure and function. The MGBA serves as a conduit between the CNS and the ENS, facilitating communication between the emotional and cognitive centers of the brain via diverse pathways. In the initial stages of this review, we will examine the way how MGBA affects neurogenesis, neuronal dendritic morphology, axonal myelination, microglia structure, brain blood barrier (BBB) structure and permeability, and synaptic structure. Furthermore, we will review the potential mechanistic pathways of neuroplasticity through MGBA influence. The short-chain fatty acids (SCFAs) play a pivotal role in the MGBA, where they can modify the BBB. We will therefore discuss how SCFAs can influence microglia, neuronal, and astrocyte function, as well as their role in brain disorders such as Alzheimer's disease (AD), and Parkinson's disease (PD). Subsequently, we will examine the technical strategies employed to study MGBA interactions, including using germ-free (GF) animals, probiotics, fecal microbiota transplantation (FMT), and antibiotics-induced dysbiosis. Finally, we will examine how particular bacterial strains can affect brain structure and function. By gaining a deeper understanding of the MGBA, it may be possible to facilitate research into microbial-based pharmacological interventions and therapeutic strategies for neurological diseases.

Keywords

References

  1. Curr Opin Clin Nutr Metab Care. 2003 Jan;6(1):49-54 [PMID: 12496680]
  2. Am J Physiol Gastrointest Liver Physiol. 2013 Jan 15;304(2):G211-20 [PMID: 23139216]
  3. Iran J Biotechnol. 2023 Jan 01;21(1):e2798 [PMID: 36811101]
  4. Psychopharmacology (Berl). 2024 May;241(5):925-945 [PMID: 38156998]
  5. Cereb Cortex. 2019 Jun 1;29(6):2424-2436 [PMID: 29771287]
  6. Microb Ecol Health Dis. 2015 Dec 15;26:29719 [PMID: 26679775]
  7. Mol Endocrinol. 2014 Aug;28(8):1221-38 [PMID: 24892638]
  8. Psychoneuroendocrinology. 2012 Nov;37(11):1885-95 [PMID: 22541937]
  9. Brain Behav Immun. 2014 Mar;37:197-206 [PMID: 24333160]
  10. Diabetes Care. 2015 Oct;38(10):1827-34 [PMID: 26084343]
  11. Psychoneuroendocrinology. 2019 Jun;104:132-142 [PMID: 30844607]
  12. Front Nutr. 2020 Jan 10;6:193 [PMID: 31998741]
  13. J Neurol Sci. 2017 Oct 15;381:176-181 [PMID: 28991675]
  14. Front Integr Neurosci. 2018 Sep 11;12:33 [PMID: 30271330]
  15. Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):16050-5 [PMID: 21876150]
  16. Expert Rev Neurother. 2018 Jan;18(1):83-90 [PMID: 29095058]
  17. N Engl J Med. 2009 Jul 16;361(3):302-3 [PMID: 19605837]
  18. Behav Brain Res. 2015 Sep 15;291:306-314 [PMID: 26048426]
  19. Clin Nutr. 2019 Apr;38(2):522-528 [PMID: 29731182]
  20. Nat Commun. 2016 Jun 24;7:11939 [PMID: 27340092]
  21. J Exp Med. 2019 Jan 7;216(1):41-59 [PMID: 30385457]
  22. Nutrients. 2023 May 06;15(9): [PMID: 37432351]
  23. Neuron. 2015 Jan 21;85(2):296-302 [PMID: 25611508]
  24. Cell. 2008 May 30;133(5):916-27 [PMID: 18510934]
  25. Dig Dis Sci. 2012 Aug;57(8):2096-102 [PMID: 22535281]
  26. Gastroenterol Clin North Am. 2017 Mar;46(1):77-89 [PMID: 28164854]
  27. J Neurosci. 2013 Jan 30;33(5):2156-65 [PMID: 23365251]
  28. J Lipid Res. 2016 Jun;57(6):943-54 [PMID: 27080715]
  29. Mol Neurodegener. 2023 Feb 1;18(1):9 [PMID: 36721148]
  30. Adv Immunol. 2014;121:91-119 [PMID: 24388214]
  31. Sci Transl Med. 2014 Nov 19;6(263):263ra158 [PMID: 25411471]
  32. Brain Behav Immun. 2018 May;70:48-60 [PMID: 29471030]
  33. Immune Netw. 2017 Feb;17(1):1-12 [PMID: 28261015]
  34. Mol Psychiatry. 2014 Feb;19(2):146-8 [PMID: 23689536]
  35. Steroids. 2017 Sep;125:1-13 [PMID: 28624548]
  36. Front Cell Neurosci. 2020 Mar 18;14:50 [PMID: 32256317]
  37. J Bacteriol. 2007 Mar;189(6):2566-70 [PMID: 17209019]
  38. Parkinsonism Relat Disord. 2016 Nov;32:66-72 [PMID: 27591074]
  39. Mucosal Immunol. 2018 Sep;11(5):1386-1397 [PMID: 29867078]
  40. J Pharmacol Exp Ther. 2002 Dec;303(3):1061-6 [PMID: 12438528]
  41. Prog Neurobiol. 2020 Apr;187:101770 [PMID: 32001310]
  42. J Neurochem. 2020 Sep;154(6):635-646 [PMID: 31784978]
  43. Brain Behav Immun. 2018 Oct;73:310-319 [PMID: 29787855]
  44. Microb Ecol Health Dis. 2016 Jul 05;27:30971 [PMID: 27389418]
  45. Oncotarget. 2017 May 10;8(32):53829-53838 [PMID: 28881854]
  46. Neurologia (Engl Ed). 2022 Jul-Aug;37(6):492-498 [PMID: 35779869]
  47. EBioMedicine. 2017 Oct;24:166-178 [PMID: 28965876]
  48. PLoS One. 2019 Aug 28;14(8):e0221828 [PMID: 31461505]
  49. Nat Commun. 2014 Apr 29;5:3611 [PMID: 24781306]
  50. Cells. 2022 Jan 23;11(3): [PMID: 35159192]
  51. Sci Rep. 2019 Apr 9;9(1):5821 [PMID: 30967657]
  52. Brain Behav Immun. 2017 Oct;65:20-32 [PMID: 28179108]
  53. Neurogastroenterol Motil. 2014 Aug;26(8):1155-62 [PMID: 24888394]
  54. Br J Pharmacol Chemother. 1962 Dec;19:385-93 [PMID: 13970018]
  55. J Psychiatr Res. 2017 Apr;87:23-29 [PMID: 27988330]
  56. Mol Psychiatry. 2019 Jan;24(1):67-87 [PMID: 29679070]
  57. Nat Rev Gastroenterol Hepatol. 2015 Sep;12(9):494-6 [PMID: 26215386]
  58. Curr Opin Microbiol. 2013 Jun;16(3):255-61 [PMID: 23831042]
  59. Trends Neurosci. 2015 Jul;38(7):439-47 [PMID: 26100142]
  60. Maturitas. 2013 May;75(1):44-50 [PMID: 23489554]
  61. Microbiome. 2020 Jun 8;8(1):88 [PMID: 32513301]
  62. Gut Microbes. 2018 Nov 2;9(6):486-496 [PMID: 29723105]
  63. Br J Nutr. 2011 Mar;105(5):755-64 [PMID: 20974015]
  64. Med Hypotheses. 2014 Dec;83(6):649-55 [PMID: 25288537]
  65. Am J Physiol Gastrointest Liver Physiol. 2012 Jan 1;302(1):G168-75 [PMID: 21940902]
  66. Brain Behav Immun. 2015 Aug;48:165-73 [PMID: 25866195]
  67. Front Cell Dev Biol. 2022 Jun 06;10:917575 [PMID: 35733853]
  68. Cell. 2019 May 30;177(6):1600-1618.e17 [PMID: 31150625]
  69. Front Immunol. 2022 Jul 07;13:934695 [PMID: 35874661]
  70. Neuropsychopharmacology. 2013 Sep;38(10):2027-34 [PMID: 23615664]
  71. Development. 2024 Jul 1;151(13): [PMID: 38856043]
  72. Behav Brain Res. 2015;287:59-72 [PMID: 25794930]
  73. Nat Rev Neurosci. 2004 Nov;5(11):844-52 [PMID: 15496862]
  74. Front Aging Neurosci. 2016 Nov 10;8:256 [PMID: 27891089]
  75. Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4615-22 [PMID: 20660719]
  76. J Nutr. 2009 Sep;139(9):1619-25 [PMID: 19625695]
  77. Int J Mol Sci. 2022 Jun 19;23(12): [PMID: 35743271]
  78. Biol Psychiatry. 2018 Jan 15;83(2):148-159 [PMID: 28793975]
  79. mBio. 2014 Apr 22;5(2):e00889 [PMID: 24757212]
  80. Eur Psychiatry. 2018 Sep;53:37-45 [PMID: 29870894]
  81. Gastroenterology. 2017 Aug;153(2):448-459.e8 [PMID: 28483500]
  82. Neurogastroenterol Motil. 2010 Sep;22(9):1029-35, e268 [PMID: 20518856]
  83. Age (Dordr). 2012 Aug;34(4):917-33 [PMID: 21861096]
  84. Neuroscience. 2015 Dec 3;310:561-77 [PMID: 26408987]
  85. Nat Rev Gastroenterol Hepatol. 2019 Aug;16(8):461-478 [PMID: 31123355]
  86. PLoS One. 2014 Sep 09;9(9):e106503 [PMID: 25202975]
  87. Microorganisms. 2021 Dec 10;9(12): [PMID: 34946159]
  88. Am J Physiol Gastrointest Liver Physiol. 2012 Dec 1;303(11):G1288-95 [PMID: 23064760]
  89. Cell. 2018 Jun 14;173(7):1728-1741.e13 [PMID: 29804833]
  90. Science. 2013 Aug 2;341(6145):569-73 [PMID: 23828891]
  91. Gut. 2011 Mar;60(3):307-17 [PMID: 20966022]
  92. Med Hypotheses. 2011 Aug;77(2):270-4 [PMID: 21592674]
  93. PLoS One. 2018 May 15;13(5):e0196510 [PMID: 29763437]
  94. Medicine (Baltimore). 2019 Jun;98(26):e16163 [PMID: 31261545]
  95. Front Cell Dev Biol. 2023 Dec 07;11:1254589 [PMID: 38155836]
  96. Front Endocrinol (Lausanne). 2020 Jan 31;11:25 [PMID: 32082260]
  97. Exp Neurol. 2021 Mar;337:113585 [PMID: 33370556]
  98. Int J Dev Neurosci. 2016 Dec;55:28-33 [PMID: 27603970]
  99. Annu Rev Neurosci. 2017 Jul 25;40:21-49 [PMID: 28301775]
  100. J Neuroinflammation. 2018 Jan 09;15(1):11 [PMID: 29316965]
  101. Neuropharmacology. 2016 Mar;102:136-45 [PMID: 26577018]
  102. Front Immunol. 2020 Dec 10;11:604179 [PMID: 33362788]
  103. Nat Rev Neurosci. 2012 Oct;13(10):701-12 [PMID: 22968153]
  104. Am J Physiol. 1973 Jun;224(6):1450-3 [PMID: 4712154]
  105. Brain Plast. 2022 Oct 21;8(1):97-119 [PMID: 36448039]
  106. J Cereb Blood Flow Metab. 2018 Aug;38(8):1293-1298 [PMID: 29846130]
  107. Proc Natl Acad Sci U S A. 2018 Jun 19;115(25):6458-6463 [PMID: 29866843]
  108. Nat Neurosci. 2017 Feb;20(2):145-155 [PMID: 28092661]
  109. J Appl Microbiol. 2012 Aug;113(2):411-7 [PMID: 22612585]
  110. Am J Physiol Gastrointest Liver Physiol. 2016 Jun 1;310(11):G989-98 [PMID: 27056723]
  111. Brain Res. 2018 Feb 1;1680:13-38 [PMID: 29229502]
  112. Eur J Neurosci. 2006 Dec;24(11):2978-86 [PMID: 17156359]
  113. J Cell Biol. 2013 Oct 28;203(2):175-86 [PMID: 24165934]
  114. Front Microbiol. 2023 Jan 25;14:1118529 [PMID: 36760508]
  115. Transl Psychiatry. 2016 Apr 05;6:e774 [PMID: 27045844]
  116. Mol Pharmacol. 2016 Mar;89(3):388-98 [PMID: 26719580]
  117. Signal Transduct Target Ther. 2024 Feb 16;9(1):37 [PMID: 38360862]
  118. Gastroenterology. 2013 Jun;144(7):1394-401, 1401.e1-4 [PMID: 23474283]
  119. World J Clin Cases. 2022 Feb 26;10(6):1754-1763 [PMID: 35317140]
  120. Nat Rev Microbiol. 2012 Nov;10(11):735-42 [PMID: 23000955]
  121. J Neuroimmune Pharmacol. 2013 Mar;8(1):287-300 [PMID: 23233245]
  122. Aliment Pharmacol Ther. 2008 Mar 15;27(6):504-13 [PMID: 18081736]
  123. Mol Psychiatry. 2013 Jun;18(6):666-73 [PMID: 22688187]
  124. Curr Biol. 2016 Jun 6;26(11):1480-5 [PMID: 27185560]
  125. Am J Physiol Gastrointest Liver Physiol. 2014 Oct 15;307(8):G793-802 [PMID: 25190473]
  126. Neuropsychopharmacology. 2008 Jan;33(1):18-41 [PMID: 17728696]
  127. Brain Behav Immun. 2021 Aug;96:227-238 [PMID: 34111528]
  128. Nature. 2013 Dec 19;504(7480):451-5 [PMID: 24226773]
  129. Appl Physiol Nutr Metab. 2018 Jul;43(7):718-726 [PMID: 29462572]
  130. J Neurochem. 2012 Nov;123(4):555-67 [PMID: 22924711]
  131. Neurogastroenterol Motil. 2014 Nov;26(11):1615-27 [PMID: 25251188]
  132. Front Immunol. 2022 Feb 14;13:785644 [PMID: 35237258]
  133. Nat Commun. 2013;4:1465 [PMID: 23403566]
  134. J Comp Neurol. 2008 Apr 10;507(5):1734-47 [PMID: 18253967]
  135. Eur J Clin Nutr. 2019 Jan;73(1):24-37 [PMID: 29581563]
  136. Eur J Nutr. 2018 May;57(Suppl 1):1-14 [PMID: 29748817]
  137. Sci Rep. 2017 May 25;7(1):2426 [PMID: 28546539]
  138. Curr Opin Support Palliat Care. 2024 Jun 1;18(2):71-72 [PMID: 38757684]
  139. Am J Physiol Gastrointest Liver Physiol. 2008 Oct;295(4):G664-70 [PMID: 18653723]
  140. World J Clin Cases. 2023 May 26;11(15):3385-3394 [PMID: 37383914]
  141. Nat Neurosci. 2019 Mar;22(3):374-385 [PMID: 30718903]
  142. Neurogastroenterol Motil. 2018 May;30(5):e13260 [PMID: 29193450]
  143. Calcif Tissue Int. 2018 Apr;102(4):406-414 [PMID: 29362822]
  144. Microbiome Res Rep. 2022 Aug 17;1(4):23 [PMID: 38046904]
  145. Microorganisms. 2018 Jul 23;6(3): [PMID: 30041463]
  146. Brain Behav Immun. 2017 May;62:41-45 [PMID: 27871802]
  147. Cell Host Microbe. 2017 Apr 12;21(4):455-466.e4 [PMID: 28407483]
  148. Brain Behav Immun. 2021 Jan;91:437-450 [PMID: 33157256]
  149. Behav Brain Res. 2015 Jan 15;277:32-48 [PMID: 25078296]
  150. Nat Immunol. 2012 Nov;13(11):1118-28 [PMID: 23023392]
  151. Int J Mol Sci. 2019 Dec 08;20(24): [PMID: 31817968]
  152. Curr Opin Neurobiol. 2016 Aug;39:93-100 [PMID: 27152449]
  153. Proc Natl Acad Sci U S A. 2009 Jan 27;106(4):1255-60 [PMID: 19171901]
  154. Psychopharmacology (Berl). 2024 Feb;241(2):327-340 [PMID: 37966492]
  155. Life (Basel). 2024 Sep 26;14(10): [PMID: 39459534]
  156. Nutrition. 2014 Jul-Aug;30(7-8):776-83.e1 [PMID: 24984992]
  157. Aging (Albany NY). 2020 May 1;12(9):7801-7817 [PMID: 32357144]
  158. ISME J. 2021 Sep;15(9):2574-2590 [PMID: 33723382]
  159. PLoS One. 2018 Feb 15;13(2):e0192925 [PMID: 29447237]
  160. Cell Rep Med. 2021 Sep 14;2(9):100398 [PMID: 34622235]
  161. Mol Psychiatry. 2006 Nov;11(11):992-1002 [PMID: 16801951]
  162. Biochem Biophys Res Commun. 2018 Apr 15;498(4):824-829 [PMID: 29530528]
  163. Development. 2014 Apr;141(8):1737-48 [PMID: 24667327]
  164. J Alzheimers Dis. 2011;26(1):187-97 [PMID: 21593570]
  165. Clinics (Sao Paulo). 2011;66 Suppl 1:3-17 [PMID: 21779718]
  166. mBio. 2017 Sep 19;8(5): [PMID: 28928206]
  167. Pharmaceuticals (Basel). 2023 May 19;16(5): [PMID: 37242552]
  168. Curr Opin Neurobiol. 2001 Feb;11(1):118-26 [PMID: 11179881]
  169. Sci Transl Med. 2019 Nov 13;11(518): [PMID: 31723038]
  170. J Appl Microbiol. 2018 Jul;125(1):257-269 [PMID: 29575441]
  171. Cell Metab. 2016 Jul 12;24(1):151-7 [PMID: 27411015]
  172. J Physiol. 2018 Oct;596(20):4923-4944 [PMID: 30066368]
  173. Neurochem Res. 1986 Feb;11(2):185-91 [PMID: 2422565]
  174. Mov Disord. 2015 Sep;30(10):1351-60 [PMID: 26179554]
  175. Trends Mol Med. 2019 Sep;25(9):750-759 [PMID: 31122805]
  176. Neurogastroenterol Motil. 2017 Jan;29(1): [PMID: 27458085]
  177. Microbiome. 2020 Oct 1;8(1):140 [PMID: 33004079]
  178. Neurosci Lett. 2016 Feb 2;613:30-5 [PMID: 26733300]
  179. Neurobiol Dis. 2019 Jul;127:65-75 [PMID: 30802499]
  180. Neurosci Bull. 2021 Oct;37(10):1510-1522 [PMID: 34216356]
  181. Front Microbiol. 2018 Mar 06;9:346 [PMID: 29559959]
  182. Front Neurosci. 2017 Sep 15;11:490 [PMID: 28966571]
  183. Development. 2021 Sep 1;148(17): [PMID: 34414407]
  184. Alzheimers Dement. 2012 May;8(3):196-203 [PMID: 22546352]
  185. Front Cell Neurosci. 2013 Apr 08;7:34 [PMID: 23596391]
  186. Pharmacotherapy. 2017 Mar;37(3):261-267 [PMID: 28035686]
  187. Front Microbiol. 2023 Jan 12;13:1103836 [PMID: 36713166]
  188. Cells. 2024 Jan 12;13(2): [PMID: 38247841]
  189. J Nutr. 1977 Sep;107(9):1707-14 [PMID: 894368]
  190. J Biol Chem. 2004 Sep 24;279(39):40545-59 [PMID: 15273246]
  191. EBioMedicine. 2017 Oct;24:159-165 [PMID: 28943228]
  192. Cell. 2018 Jan 25;172(3):500-516.e16 [PMID: 29275859]
  193. Biol Psychiatry. 2017 Oct 1;82(7):472-487 [PMID: 28242013]
  194. Trends Neurosci. 2020 Mar;43(3):144-154 [PMID: 32044129]
  195. J Dairy Sci. 2019 Mar;102(3):1901-1909 [PMID: 30639021]
  196. Nat Neurosci. 2015 Jul;18(7):965-77 [PMID: 26030851]
  197. Sci China Life Sci. 2017 Nov;60(11):1223-1233 [PMID: 28536926]
  198. Gut. 2022 Nov;71(11):2233-2252 [PMID: 35017199]
  199. Adv Exp Med Biol. 2017;1015:1-15 [PMID: 29080018]
  200. Cell. 2016 Dec 1;167(6):1469-1480.e12 [PMID: 27912057]
  201. Nat Rev Immunol. 2016 Jan;16(1):22-34 [PMID: 26711676]
  202. Infect Immun. 2016 Apr 22;84(5):1446-1456 [PMID: 26930710]
  203. Sci Rep. 2016 Oct 14;6:35405 [PMID: 27739530]
  204. J Adv Res. 2023 Aug;50:83-105 [PMID: 36332796]
  205. Brain Behav Immun. 2022 Jan;99:203-217 [PMID: 34673174]
  206. FASEB J. 2015 Apr;29(4):1395-403 [PMID: 25550456]
  207. Mol Neurobiol. 2017 Oct;54(8):6391-6411 [PMID: 27722928]
  208. PLoS One. 2015 Nov 05;10(11):e0142164 [PMID: 26539989]
  209. Front Cell Infect Microbiol. 2021 Jan 27;10:611014 [PMID: 33585279]
  210. Eur Neuropsychopharmacol. 2020 Dec;41:152-159 [PMID: 33191074]
  211. J Psychiatr Res. 2015 Feb;61:114-21 [PMID: 25467060]
  212. Transl Psychiatry. 2016 Nov 1;6(11):e939 [PMID: 27801892]
  213. PLoS One. 2014 Aug 29;9(8):e103740 [PMID: 25170769]
  214. J Affect Disord. 2016 Sep 15;202:254-7 [PMID: 27288567]
  215. Psychoneuroendocrinology. 2005 Apr;30(3):225-42 [PMID: 15511597]
  216. Neuroscience. 2014 Sep 26;277:885-901 [PMID: 25088912]
  217. Hum Genomics. 2013 Nov 27;7:24 [PMID: 24283712]
  218. Nature. 2000 May 11;405(6783):187-91 [PMID: 10821275]
  219. Pharmacol Res. 2019 Aug;146:104312 [PMID: 31207344]
  220. Sci Rep. 2017 Sep 5;7(1):10411 [PMID: 28874832]
  221. Neuropsychiatr Dis Treat. 2019 May 01;15:1077-1088 [PMID: 31118641]
  222. Front Neurol. 2014 Apr 04;5:43 [PMID: 24772103]
  223. Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8629-34 [PMID: 10900020]
  224. J Infect Dis. 1984 Apr;149(4):489-94 [PMID: 6725987]
  225. Trends Mol Med. 2014 Sep;20(9):509-18 [PMID: 24956966]
  226. Behav Pharmacol. 2013 Oct;24(7):569-79 [PMID: 23994816]
  227. Int J Neuropsychopharmacol. 2014 Oct 31;18(2): [PMID: 25618518]
  228. Curr Pharm Des. 2014;20(10):1487-98 [PMID: 23789956]
  229. Sci Rep. 2018 Apr 3;8(1):5443 [PMID: 29615691]
  230. Psychol Sci. 2016 Sep;27(9):1171-80 [PMID: 27422874]
  231. Nat Microbiol. 2019 Apr;4(4):623-632 [PMID: 30718848]
  232. Front Microbiol. 2016 Dec 02;7:1945 [PMID: 27994578]
  233. Neurogastroenterol Motil. 2013 Jun;25(6):521-8 [PMID: 23480302]
  234. J Am Heart Assoc. 2015 Nov 23;4(11): [PMID: 26597155]
  235. Gastroenterology. 2011 Aug;141(2):599-609, 609.e1-3 [PMID: 21683077]
  236. J Gen Virol. 2017 Jul;98(7):1943-1952 [PMID: 28708055]
  237. Brain Behav Immun. 2024 Feb;116:34-51 [PMID: 38030048]
  238. Proc Natl Acad Sci U S A. 2017 Oct 3;114(40):10713-10718 [PMID: 28893978]
  239. Mol Psychiatry. 2023 Apr;28(4):1611-1621 [PMID: 36914812]
  240. Physiol Rev. 2019 Oct 1;99(4):1877-2013 [PMID: 31460832]
  241. Front Cell Neurosci. 2018 Nov 16;12:428 [PMID: 30519159]
  242. Neurobiol Stress. 2016 Mar 04;4:23-33 [PMID: 27981187]
  243. Neuron. 2019 Jan 16;101(2):246-259.e6 [PMID: 30522820]
  244. Cell. 2015 Apr 9;161(2):264-76 [PMID: 25860609]
  245. Neurochem Int. 2016 Oct;99:110-132 [PMID: 27346602]
  246. Nutrients. 2017 Mar 15;9(3): [PMID: 28294985]
  247. J Lipid Res. 2013 Sep;54(9):2437-49 [PMID: 23772041]
  248. Anaerobe. 2010 Aug;16(4):444-53 [PMID: 20603222]
  249. Neuroscientist. 2014 Apr;20(2):160-72 [PMID: 24106265]
  250. Mediators Inflamm. 2014;2014:162021 [PMID: 25214711]
  251. Brain Res. 2016 Jul 1;1642:70-78 [PMID: 27017959]
  252. Nutr Neurosci. 2016 Sep;19(7):279-83 [PMID: 25710209]
  253. Phytomedicine. 2024 Nov;134:156012 [PMID: 39260135]
  254. Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):4037-42 [PMID: 11891290]
  255. Brain Behav Immun. 2017 Jan;59:21-37 [PMID: 27423492]
  256. J Int Neuropsychol Soc. 2017 Sep;23(8):700-705 [PMID: 28641593]
  257. J Physiol. 2017 Mar 15;595(6):1929-1945 [PMID: 27104646]
  258. Neurosci Lett. 2019 Nov 20;713:134532 [PMID: 31589903]
  259. J Neurochem. 2016 Oct;139 Suppl 2:115-125 [PMID: 26968531]
  260. Front Cell Neurosci. 2013 Sep 17;7:153 [PMID: 24062644]
  261. Neuroscience. 2013 Aug 29;246:281-90 [PMID: 23673277]
  262. Philos Trans R Soc Lond B Biol Sci. 2003 Apr 29;358(1432):617-20 [PMID: 12740104]
  263. Front Immunol. 2022 Nov 08;13:1011129 [PMID: 36426369]
  264. Neuron. 2003 Oct 9;40(2):229-42 [PMID: 14556706]
  265. Appl Environ Microbiol. 2005 Oct;71(10):6438-42 [PMID: 16204576]
  266. Am J Physiol. 1998 Dec;275(6):G1415-22 [PMID: 9843779]
  267. ISME J. 2014 Jun;8(6):1323-35 [PMID: 24553467]
  268. Nutrients. 2018 Dec 07;10(12): [PMID: 30544489]
  269. Cell Mol Life Sci. 2013 Jan;70(1):55-69 [PMID: 22638926]
  270. Psychiatry Res. 2016 Jan 30;235:154-9 [PMID: 26654753]
  271. J Alzheimers Dis. 2017;60(4):1241-1257 [PMID: 29036812]
  272. Neuroscience. 2013 Aug 29;246:382-90 [PMID: 23623990]
  273. Cells. 2021 Aug 13;10(8): [PMID: 34440854]
  274. Development. 2011 Oct;138(19):4301-13 [PMID: 21865324]
  275. Front Physiol. 2011 Mar 07;2:9 [PMID: 21483729]
  276. Chin Med J (Engl). 2019 Aug 5;132(15):1815-1822 [PMID: 31306225]
  277. Gut Microbes. 2024 Jan-Dec;16(1):2333483 [PMID: 38532703]
  278. J Clin Psychiatry. 2000;61 Suppl 6:7-11 [PMID: 10775018]
  279. Dig Dis Sci. 2013 Mar;58(3):660-7 [PMID: 23344966]
  280. Annu Rev Neurosci. 2019 Jul 8;42:107-127 [PMID: 31283900]
  281. Endocrine. 2018 Sep;61(3):357-371 [PMID: 29721802]
  282. Pharmacol Res. 2021 Oct;172:105840 [PMID: 34450312]
  283. Benef Microbes. 2015;6(5):707-17 [PMID: 25869281]
  284. Gut. 2020 Dec;69(12):2232-2243 [PMID: 32917747]
  285. Healthcare (Basel). 2015 Sep 29;3(4):898-916 [PMID: 27417803]
  286. Semin Immunopathol. 2023 May;45(3):377-387 [PMID: 37052711]
  287. Cell. 2013 Dec 19;155(7):1451-63 [PMID: 24315484]
  288. Transl Psychiatry. 2016 May 31;6(5):e823 [PMID: 27244232]
  289. Hum Mol Genet. 2017 Jun 15;26(12):2231-2246 [PMID: 28369321]
  290. Nutrients. 2021 Jul 30;13(8): [PMID: 34444820]
  291. Br J Nutr. 2009 Feb;101(4):541-50 [PMID: 18590586]
  292. Neurogastroenterol Motil. 2014 Apr;26(4):510-20 [PMID: 24372793]
  293. Brain Res Bull. 2017 Oct;135:113-119 [PMID: 28964773]
  294. Aging (Albany NY). 2018 May 16;10(5):930-950 [PMID: 29769431]
  295. Prog Mol Biol Transl Sci. 2020;176:111-122 [PMID: 33814112]
  296. Microb Ecol Health Dis. 2017 Jan 01;28(1):1353881 [PMID: 28959180]
  297. Neurogastroenterol Motil. 2011 Mar;23(3):255-64, e119 [PMID: 21054680]
  298. Front Neurosci. 2022 Dec 23;16:1065995 [PMID: 36620458]
  299. J Physiol. 2004 Jul 1;558(Pt 1):263-75 [PMID: 15133062]
  300. Exp Gerontol. 2018 Nov;113:209-217 [PMID: 30304709]
  301. Neuroscience. 2017 Sep 17;359:18-29 [PMID: 28694176]
  302. J Neurosci. 2002 Sep 15;22(18):8042-51 [PMID: 12223558]
  303. Biol Psychiatry. 2015 Aug 15;78(4):e7-9 [PMID: 25700599]
  304. Front Psychiatry. 2020 Aug 11;11:799 [PMID: 32903683]
  305. ISME J. 2014 Nov;8(11):2218-30 [PMID: 24763370]
  306. Appl Environ Microbiol. 2004 Jun;70(6):3575-81 [PMID: 15184159]
  307. Mol Neurobiol. 2015 Aug;52(1):734-40 [PMID: 25284351]
  308. Appl Environ Microbiol. 2002 Oct;68(10):5186-90 [PMID: 12324374]
  309. Front Microbiol. 2023 May 10;14:1174800 [PMID: 37234527]
  310. Immunity. 2015 Oct 20;43(4):817-29 [PMID: 26488817]
  311. Front Pharmacol. 2016 Aug 15;7:253 [PMID: 27574508]
  312. Eur J Neurosci. 2016 Nov;44(9):2654-2666 [PMID: 27256072]
  313. Genome Med. 2017 Jun 29;9(1):61 [PMID: 28662719]
  314. Neurochem Int. 2013 Dec;63(8):756-64 [PMID: 24140431]
  315. Dev Psychopathol. 2020 Feb;32(1):309-328 [PMID: 30919798]
  316. Science. 2005 Jun 10;308(5728):1635-8 [PMID: 15831718]
  317. Appl Environ Microbiol. 2012 Jan;78(2):511-8 [PMID: 22081579]
  318. Front Aging Neurosci. 2021 Jun 25;13:671142 [PMID: 34248602]
  319. Neurosci Res. 2021 Jul;168:64-75 [PMID: 32017965]
  320. PLoS One. 2013 May 28;8(5):e65465 [PMID: 23724144]
  321. J Neurochem. 2012 Apr;121(1):4-27 [PMID: 22251135]
  322. Exp Neurol. 2015 Jul;269:202-12 [PMID: 25917529]
  323. Am J Gastroenterol. 2010 Apr;105(4):933-9 [PMID: 20179687]
  324. Neuroscience. 2013 Jun 14;240:287-96 [PMID: 23500100]
  325. Microbiome. 2018 Aug 2;6(1):133 [PMID: 30071894]
  326. Neuropharmacology. 2023 Jun 15;231:109491 [PMID: 36924923]
  327. Alzheimers Dement. 2021 Dec;17(12):1966-1975 [PMID: 34043283]
  328. Proc Natl Acad Sci U S A. 2011 Feb 15;108(7):3047-52 [PMID: 21282636]
  329. Nat Neurosci. 2022 Mar;25(3):295-305 [PMID: 35241804]
  330. Brain Behav Immun. 2018 Jan;67:230-245 [PMID: 28890155]
  331. Cell Rep. 2016 May 31;15(9):1945-56 [PMID: 27210745]
  332. Rev Colomb Psiquiatr (Engl Ed). 2022 Jan-Mar;51(1):6-7 [PMID: 35210205]
  333. Int J Mol Sci. 2012;13(5):5482-5497 [PMID: 22754309]

Word Cloud

Created with Highcharts 10.0.0MGBAbrainstructurewillfunctionmicrobiota-gut-brainroleexaminecanaxispathwaysreviewneuronalmorphologymicrogliabarrierBBBneuroplasticityinfluenceshort-chainfattySCFAsdiseasestrategiesinterventionsplayssignificantmaintenanceservesconduitCNSENSfacilitatingcommunicationemotionalcognitivecentersviadiverseinitialstageswayaffectsneurogenesisdendriticaxonalmyelinationbloodpermeabilitysynapticFurthermorepotentialmechanisticacidsplaypivotalmodifythereforediscussastrocytewelldisordersAlzheimer'sADParkinson'sPDSubsequentlytechnicalemployedstudyinteractionsincludingusinggerm-freeGFanimalsprobioticsfecalmicrobiotatransplantationFMTantibiotics-induceddysbiosisFinallyparticularbacterialstrainsaffectgainingdeeperunderstandingmaypossiblefacilitateresearchmicrobial-basedpharmacologicaltherapeuticneurologicaldiseasesExploringaxis:impactblood–brainmicrobialacid

Similar Articles

Cited By