Microbiota-Immune System Interactions in Human Neurological Disorders

Author(s): Qin Huang, Fang Yu, Di Liao, Jian Xia*

Journal Name: CNS & Neurological Disorders - Drug Targets
Formerly Current Drug Targets - CNS & Neurological Disorders

Volume 19 , Issue 7 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Recent studies implicate microbiota-brain communication as an essential factor for physiology and pathophysiology in brain function and neurodevelopment. One of the pivotal mechanisms about gut to brain communication is through the regulation and interaction of gut microbiota on the host immune system. In this review, we will discuss the role of microbiota-immune systeminteractions in human neurological disorders. The characteristic features in the development of neurological diseases include gut dysbiosis, the disturbed intestinal/Blood-Brain Barrier (BBB) permeability, the activated inflammatory response, and the changed microbial metabolites. Neurological disorders contribute to gut dysbiosis and some relevant metabolites in a top-down way. In turn, the activated immune system induced by the change of gut microbiota may deteriorate the development of neurological diseases through the disturbed gut/BBB barrier in a down-top way. Understanding the characterization and identification of microbiome-immune- brain signaling pathways will help us to yield novel therapeutic strategies by targeting the gut microbiome in neurological disease.

Keywords: Gut microbiota, neurological disorders, immune system, inflammation, intestinal barrier, blood-brain barrier, microbiota-immune system.

[1]
Kamada N, Seo SU, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013; 13(5): 321-35.
[http://dx.doi.org/10.1038/nri3430] [PMID: 23618829]
[2]
Rooks MG, Garrett WS. Gut microbiota, metabolites and host immunity. Nat Rev Immunol 2016; 16(6): 341-52.
[http://dx.doi.org/10.1038/nri.2016.42] [PMID: 27231050]
[3]
Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature 2016; 535(7610): 75-84.
[http://dx.doi.org/10.1038/nature18848] [PMID: 27383982]
[4]
Rea K, Dinan TG, Cryan JF. The microbiome: a key regulator of stress and neuroinflammation. Neurobiol Stress 2016; 4: 23-33.
[http://dx.doi.org/10.1016/j.ynstr.2016.03.001] [PMID: 27981187]
[5]
Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell 2014; 157(1): 121-41.
[http://dx.doi.org/10.1016/j.cell.2014.03.011] [PMID: 24679531]
[6]
Erny D, Hrabě de Angelis AL, Jaitin D, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 2015; 18(7): 965-77.
[http://dx.doi.org/10.1038/nn.4030] [PMID: 26030851]
[7]
Rothhammer V, Mascanfroni ID, Bunse L, et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat Med 2016; 22(6): 586-97.
[http://dx.doi.org/10.1038/nm.4106] [PMID: 27158906]
[8]
Forsythe P. Microbes taming mast cells: implications for allergic inflammation and beyond. Eur J Pharmacol 2016; 778: 169-75.
[http://dx.doi.org/10.1016/j.ejphar.2015.06.034] [PMID: 26130124]
[9]
Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2011; 108(Suppl. 1): 4615-22.
[http://dx.doi.org/10.1073/pnas.1000082107] [PMID: 20660719]
[10]
Gaboriau-Routhiau V, Rakotobe S, Lécuyer E, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009; 31(4): 677-89.
[http://dx.doi.org/10.1016/j.immuni.2009.08.020] [PMID: 19833089]
[11]
Fung TC, Olson CA, Hsiao EY. Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 2017; 20(2): 145-55.
[http://dx.doi.org/10.1038/nn.4476] [PMID: 28092661]
[12]
Cryan JF, O’Riordan KJ, Sandhu K, Peterson V, Dinan TG. The gut microbiome in neurological disorders. Lancet Neurol 2020; 19(2): 179-94.
[http://dx.doi.org/10.1016/S1474-4422(19)30356-4] [PMID: 31753762]
[13]
Zhu S, Jiang Y, Xu K, et al. The progress of gut microbiome research related to brain disorders. J Neuroinflammation 2020; 17(1): 25.
[http://dx.doi.org/10.1186/s12974-020-1705-z] [PMID: 31952509]
[14]
El Aidy S, Dinan TG, Cryan JF. Immune modulation of the brain-gut-microbe axis. Front Microbiol 2014; 5: 146.
[http://dx.doi.org/10.3389/fmicb.2014.00146] [PMID: 24778631]
[15]
Matcovitch-Natan O, Winter DR, Giladi A, et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science 2016; 353(6301)aad8670
[http://dx.doi.org/10.1126/science.aad8670] [PMID: 27338705]
[16]
Huuskonen J, Suuronen T, Nuutinen T, Kyrylenko S, Salminen A. Regulation of microglial inflammatory response by sodium butyrate and short-chain fatty acids. Br J Pharmacol 2004; 141(5): 874-80.
[http://dx.doi.org/10.1038/sj.bjp.0705682] [PMID: 14744800]
[17]
Liddelow S, Hoyer D. Astrocytes: adhesion molecules and immunomodulation. Curr Drug Targets 2016; 17(16): 1871-81.
[http://dx.doi.org/10.2174/1389450117666160101120703] [PMID: 26721411]
[18]
Rothhammer V, Borucki DM, Tjon EC, et al. Microglial control of astrocytes in response to microbial metabolites. Nature 2018; 557(7707): 724-8.
[http://dx.doi.org/10.1038/s41586-018-0119-x] [PMID: 29769726]
[19]
Maier SF. Bi-directional immune-brain communication: implications for understanding stress, pain, and cognition. Brain Behav Immun 2003; 17(2): 69-85.
[http://dx.doi.org/10.1016/S0889-1591(03)00032-1] [PMID: 12676570]
[20]
Banks WA, Farr SA, Morley JE. Entry of blood-borne cytokines into the central nervous system: effects on cognitive processes. Neuroimmunomodulation 2002-2003; 10(6): 319-27.
[http://dx.doi.org/10.1159/000071472] [PMID: 12907838]
[21]
Yamagata K, Matsumura K, Inoue W, et al. Coexpression of microsomal-type prostaglandin E synthase with cyclooxygenase-2 in brain endothelial cells of rats during endotoxin-induced fever. J Neurosci 2001; 21(8): 2669-77.
[http://dx.doi.org/10.1523/JNEUROSCI.21-08-02669.2001] [PMID: 11306620]
[22]
Rivest S. How circulating cytokines trigger the neural circuits that control the hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology 2001; 26(8): 761-88.
[http://dx.doi.org/10.1016/S0306-4530(01)00064-6] [PMID: 11585678]
[23]
Romeo HETD, Tio DL, Rahman SU, Chiappelli F, Taylor AN. The glossopharyngeal nerve as a novel pathway in immune-to-brain communication: relevance to neuroimmune surveillance of the oral cavity. J Neuroimmunol 2001; 115(1-2): 91-100.
[http://dx.doi.org/10.1016/S0165-5728(01)00270-3] [PMID: 11282158]
[24]
Agace WW, McCoy KD. Regionalized development and maintenance of the intestinal adaptive immune landscape. Immunity 2017; 46(4): 532-48.
[http://dx.doi.org/10.1016/j.immuni.2017.04.004] [PMID: 28423335]
[25]
Yoo BB, Mazmanian SK. The enteric network: interactions between the immune and nervous systems of the gut. Immunity 2017; 46(6): 910-26.
[http://dx.doi.org/10.1016/j.immuni.2017.05.011] [PMID: 28636959]
[26]
Ashwood P, Anthony A, Torrente F, Wakefield AJ. Spontaneous mucosal lymphocyte cytokine profiles in children with autism and gastrointestinal symptoms: mucosal immune activation and reduced counter regulatory interleukin-10. J Clin Immunol 2004; 24(6): 664-73.
[http://dx.doi.org/10.1007/s10875-004-6241-6] [PMID: 15622451]
[27]
Furlano RI, Anthony A, Day R, et al. Colonic CD8 and gamma delta T-cell infiltration with epithelial damage in children with autism. J Pediatr 2001; 138(3): 366-72.
[http://dx.doi.org/10.1067/mpd.2001.111323] [PMID: 11241044]
[28]
Villumsen M, Aznar S, Pakkenberg B, Jess T, Brudek T. Inflammatory bowel disease increases the risk of Parkinson’s disease: a Danish nationwide cohort study 1977-2014. Gut 2019; 68(1): 18-24.
[http://dx.doi.org/10.1136/gutjnl-2017-315666] [PMID: 29785965]
[29]
Villarán RF, Espinosa-Oliva AM, Sarmiento M, et al. Ulcerative colitis exacerbates lipopolysaccharide-induced damage to the nigral dopaminergic system: potential risk factor in Parkinson’s disease. J Neurochem 2010; 114(6): 1687-700.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06879.x] [PMID: 20584104]
[30]
Khosravi A, Yáñez A, Price JG, et al. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe 2014; 15(3): 374-81.
[http://dx.doi.org/10.1016/j.chom.2014.02.006] [PMID: 24629343]
[31]
Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature 2016; 535(7610): 65-74.
[http://dx.doi.org/10.1038/nature18847] [PMID: 27383981]
[32]
Zhang D, Chen G, Manwani D, et al. Neutrophil ageing is regulated by the microbiome. Nature 2015; 525(7570): 528-32.
[http://dx.doi.org/10.1038/nature15367] [PMID: 26374999]
[33]
Nguyen MD, D’Aigle T, Gowing G, Julien JP, Rivest S. Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis. J Neurosci 2004; 24(6): 1340-9.
[http://dx.doi.org/10.1523/JNEUROSCI.4786-03.2004] [PMID: 14960605]
[34]
Rescigno M. The intestinal epithelial barrier in the control of homeostasis and immunity. Trends Immunol 2011; 32(6): 256-64.
[http://dx.doi.org/10.1016/j.it.2011.04.003] [PMID: 21565554]
[35]
Willing BP, Van Kessel AG. Enterocyte proliferation and apoptosis in the caudal small intestine is influenced by the composition of colonizing commensal bacteria in the neonatal gnotobiotic pig. J Anim Sci 2007; 85(12): 3256-66.
[http://dx.doi.org/10.2527/jas.2007-0320] [PMID: 17785595]
[36]
Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008; 453(7195): 620-5.
[http://dx.doi.org/10.1038/nature07008] [PMID: 18509436]
[37]
Erny D, Hrabě de Angelis AL, Prinz M. Communicating systems in the body: how microbiota and microglia cooperate. Immunology 2017; 150(1): 7-15.
[http://dx.doi.org/10.1111/imm.12645] [PMID: 27392533]
[38]
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005; 122(1): 107-18.
[http://dx.doi.org/10.1016/j.cell.2005.05.007] [PMID: 16009137]
[39]
Bouskra D, Brézillon C, Bérard M, et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008; 456(7221): 507-10.
[http://dx.doi.org/10.1038/nature07450] [PMID: 18987631]
[40]
Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9(5): 313-23.
[http://dx.doi.org/10.1038/nri2515] [PMID: 19343057]
[41]
Niess JHLF, Leithäuser F, Adler G, Reimann J. Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions. J Immunol 2008; 180(1): 559-68.
[http://dx.doi.org/10.4049/jimmunol.180.1.559] [PMID: 18097058]
[42]
Umesaki Y, Okada Y, Matsumoto S, Imaoka A, Setoyama H. Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol Immunol 1995; 39(8): 555-62.
[http://dx.doi.org/10.1111/j.1348-0421.1995.tb02242.x] [PMID: 7494493]
[43]
Wlodarska M, Willing B, Keeney KM, et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect Immun 2011; 79(4): 1536-45.
[http://dx.doi.org/10.1128/IAI.01104-10] [PMID: 21321077]
[44]
Ferreira RB, Gill N, Willing BP, et al. The intestinal microbiota plays a role in Salmonella-induced colitis independent of pathogen colonization. PLoS One 2011; 6(5)e20338
[http://dx.doi.org/10.1371/journal.pone.0020338] [PMID: 21633507]
[45]
Ochoa-Repáraz J, Mielcarz DW, Wang Y, et al. A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol 2010; 3(5): 487-95.
[http://dx.doi.org/10.1038/mi.2010.29] [PMID: 20531465]
[46]
Lathrop SK, Bloom SM, Rao SM, et al. Peripheral education of the immune system by colonic commensal microbiota. Nature 2011; 478(7368): 250-4.
[http://dx.doi.org/10.1038/nature10434] [PMID: 21937990]
[47]
Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013; 341(6145): 569-73.
[http://dx.doi.org/10.1126/science.1241165] [PMID: 23828891]
[48]
Horai R, Zárate-Bladés CR, Dillenburg-Pilla P, et al. Microbiota-dependent activation of an autoreactive T cell receptor provokes autoimmunity in an immunologically privileged site. Immunity 2015; 43(2): 343-53.
[http://dx.doi.org/10.1016/j.immuni.2015.07.014] [PMID: 26287682]
[49]
Berer K, Mues M, Koutrolos M, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011; 479(7374): 538-41.
[http://dx.doi.org/10.1038/nature10554] [PMID: 22031325]
[50]
Borre YE, O’Keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JF. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med 2014; 20(9): 509-18.
[http://dx.doi.org/10.1016/j.molmed.2014.05.002] [PMID: 24956966]
[51]
Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16(1): 1-13.
[http://dx.doi.org/10.1016/j.nbd.2003.12.016] [PMID: 15207256]
[52]
Braniste V, Al-Asmakh M, Kowal C, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med 2014; 6(263)263ra158
[http://dx.doi.org/10.1126/scitranslmed.3009759] [PMID: 25411471]
[53]
Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011; 476(7361): 458-61.
[http://dx.doi.org/10.1038/nature10287] [PMID: 21814201]
[54]
Marín-Burgin A, Schinder AF. Requirement of adult-born neurons for hippocampus-dependent learning. Behav Brain Res 2012; 227(2): 391-9.
[http://dx.doi.org/10.1016/j.bbr.2011.07.001] [PMID: 21763727]
[55]
Möhle L, Mattei D, Heimesaat MM, et al. Ly6C(hi) monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Rep 2016; 15(9): 1945-56.
[http://dx.doi.org/10.1016/j.celrep.2016.04.074] [PMID: 27210745]
[56]
Park H, Poo MM. Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 2013; 14(1): 7-23.
[http://dx.doi.org/10.1038/nrn3379] [PMID: 23254191]
[57]
Diaz Heijtz R, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 2011; 108(7): 3047-52.
[http://dx.doi.org/10.1073/pnas.1010529108] [PMID: 21282636]
[58]
Fernandez-Real JM, Serino M, Blasco G, et al. Gut microbiota interacts with brain microstructure and function. J Clin Endocrinol Metab 2015; 100(12): 4505-13.
[http://dx.doi.org/10.1210/jc.2015-3076] [PMID: 26445114]
[59]
Hintz SR, Kendrick DE, Stoll BJ, et al. NICHD neonatal research network. Neurodevelopmental and growth outcomes of extremely low birth weight infants after necrotizing enterocolitis. Pediatrics 2005; 115(3): 696-703.
[http://dx.doi.org/10.1542/peds.2004-0569] [PMID: 15741374]
[60]
O’Shea TM, Shah B, Allred EN, et al. ELGAN Study Investigators. Inflammation-initiating illnesses, inflammation-related proteins, and cognitive impairment in extremely preterm infants. Brain Behav Immun 2013; 29: 104-12.
[http://dx.doi.org/10.1016/j.bbi.2012.12.012] [PMID: 23295265]
[61]
Tomlinson MS, Lu K, Stewart JR, Marsit CJ, O’Shea TM, Fry RC. Microorganisms in the placenta. Clin Microbiol Rev 2019; 32(3): e00103-18.
[http://dx.doi.org/10.1128/CMR.00103-18] [PMID: 31043389]
[62]
Shatrov JG, Birch SC, Lam LT, Quinlivan JA, McIntyre S, Mendz GL. Chorioamnionitis and cerebral palsy: a meta-analysis. Obstet Gynecol 2010; 116(2 Pt 1): 387-92.
[http://dx.doi.org/10.1097/AOG.0b013e3181e90046] [PMID: 20664400]
[63]
Dammann O, Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 1997; 42(1): 1-8.
[http://dx.doi.org/10.1203/00006450-199707000-00001] [PMID: 9212029]
[64]
Yahfoufi N, Matar C, Ismail N. Adolescence and aging: impact of adolescence inflammatory stress and microbiota alterations on brain development, aging and neurodegeneration. J Gerontol A Biol Sci Med Sci 2020; 75(7): 1251-7.
[http://dx.doi.org/10.1093/gerona/glaa006] [PMID: 31917834]
[65]
Golubeva AV, Crampton S, Desbonnet L, et al. Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood. Psychoneuroendocrinology 2015; 60: 58-74.
[http://dx.doi.org/10.1016/j.psyneuen.2015.06.002] [PMID: 26135201]
[66]
Prenderville JA, Kennedy PJ, Dinan TG, Cryan JF. Adding fuel to the fire: the impact of stress on the ageing brain. Trends Neurosci 2015; 38(1): 13-25.
[http://dx.doi.org/10.1016/j.tins.2014.11.001] [PMID: 25705750]
[67]
Norden DM, Godbout JP. Review: microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathol Appl Neurobiol 2013; 39(1): 19-34.
[http://dx.doi.org/10.1111/j.1365-2990.2012.01306.x] [PMID: 23039106]
[68]
Shoji H, Takao K, Hattori S, Miyakawa T. Age-related changes in behavior in C57BL/6J mice from young adulthood to middle age. Mol Brain 2016; 9(1): 11.
[http://dx.doi.org/10.1186/s13041-016-0191-9] [PMID: 26822304]
[69]
Francia N, Cirulli F, Chiarotti F, Antonelli A, Aloe L, Alleva E. Spatial memory deficits in middle-aged mice correlate with lower exploratory activity and a subordinate status: role of hippocampal neurotrophins. Eur J Neurosci 2006; 23(3): 711-28.
[http://dx.doi.org/10.1111/j.1460-9568.2006.04585.x] [PMID: 16487153]
[70]
Ennaceur A, Michalikova S, van Rensburg R, Chazot PL. Detailed analysis of the behavior and memory performance of middle-aged male and female CD-1 mice in a 3D maze. Behav Brain Res 2008; 187(2): 312-26.
[http://dx.doi.org/10.1016/j.bbr.2007.09.025] [PMID: 17983672]
[71]
Franceschi C, Salvioli S, Garagnani P, de Eguileor M, Monti D, Capri M. Immunobiography and the heterogeneity of immune responses in the elderly: a focus on inflammaging and trained immunity. Front Immunol 2017; 8: 982.
[http://dx.doi.org/10.3389/fimmu.2017.00982] [PMID: 28861086]
[72]
Sparkman NL, Johnson RW. Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. Neuroimmunomodulation 2008; 15(4-6): 323-30.
[http://dx.doi.org/10.1159/000156474] [PMID: 19047808]
[73]
Claesson MJ, Cusack S, O’Sullivan O, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 2011; 108(Suppl. 1): 4586-91.
[http://dx.doi.org/10.1073/pnas.1000097107] [PMID: 20571116]
[74]
Fransen F, van Beek AA, Borghuis T, et al. Aged gut microbiota contributes to systemical inflammaging after transfer to germ-free mice. Front Immunol 2017; 8: 1385.
[http://dx.doi.org/10.3389/fimmu.2017.01385] [PMID: 29163474]
[75]
Thevaranjan N, Puchta A, Schulz C, et al. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host Microbe 2018; 23(4): 570.
[http://dx.doi.org/10.1016/j.chom.2018.03.006] [PMID: 29649447]
[76]
Scott KA, Ida M, Peterson VL, et al. Revisiting Metchnikoff: age-related alterations in microbiota-gut-brain axis in the mouse. Brain Behav Immun 2017; 65: 20-32.
[http://dx.doi.org/10.1016/j.bbi.2017.02.004] [PMID: 28179108]
[77]
Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr 2008; 88(5): 1438-46.
[PMID: 18996881]
[78]
Burokas A, Arboleya S, Moloney RD, et al. Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry 2017; 82(7): 472-87.
[http://dx.doi.org/10.1016/j.biopsych.2016.12.031] [PMID: 28242013]
[79]
Matt SM, Allen JM, Lawson MA, Mailing LJ, Woods JA, Johnson RW. Butyrate and dietary soluble fiber improve neuroinflammation associated with aging in mice. Front Immunol 2018; 9: 1832.
[http://dx.doi.org/10.3389/fimmu.2018.01832] [PMID: 30154787]
[80]
Boehme M, van de Wouw M, Bastiaanssen TFS, et al. Mid-life microbiota crises: middle age is associated with pervasive neuroimmune alterations that are reversed by targeting the gut microbiome. Mol Psychiatry 2019; 25: 2567-83.
[http://dx.doi.org/10.1038/s41380-019-0425-1] [PMID: 31092898]
[81]
He R, Yan X, Guo J, Xu Q, Tang B, Sun Q. Recent advances in biomarkers for Parkinson’s disease. Front Aging Neurosci 2018; 10: 305.
[http://dx.doi.org/10.3389/fnagi.2018.00305] [PMID: 30364199]
[82]
Wahner ADSJ, Sinsheimer JS, Bronstein JM, Ritz B. Inflammatory cytokine gene polymorphisms and increased risk of Parkinson disease. Arch Neurol 2007; 64(6): 836-40.
[http://dx.doi.org/10.1001/archneur.64.6.836] [PMID: 17562931]
[83]
Holmqvist S, Chutna O, Bousset L, et al. Direct evidence of Parkinson pathology spread from the gastrointestinal tract to the brain in rats. Acta Neuropathol 2014; 128(6): 805-20.
[http://dx.doi.org/10.1007/s00401-014-1343-6] [PMID: 25296989]
[84]
Keshavarzian A, Green SJ, Engen PA, et al. Colonic bacterial composition in Parkinson’s disease. Mov Disord 2015; 30(10): 1351-60.
[http://dx.doi.org/10.1002/mds.26307] [PMID: 26179554]
[85]
Sampson TR, Debelius JW, Thron T, Janssen S, Shastri GG, Ilhan ZE, et al. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease. Cell 2016; 165(6): 1469-1480.E12..
[http://dx.doi.org/10.1016/j.cell.2016.11.018]
[86]
Forsyth CB, Shannon KM, Kordower JH, et al. Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson’s disease. PLoS One 2011; 6(12)e28032
[http://dx.doi.org/10.1371/journal.pone.0028032] [PMID: 22145021]
[87]
Guan J, Pavlovic D, Dalkie N, et al. Vascular degeneration in Parkinson’s disease. Brain Pathol 2013; 23(2): 154-64.
[http://dx.doi.org/10.1111/j.1750-3639.2012.00628.x] [PMID: 22897695]
[88]
Feng L, Long H-Y, Liu R-K, et al. A quantum dot probe conjugated with aβ antibody for molecular imaging of Alzheimer’s disease in a mouse model. Cell Mol Neurobiol 2013; 33(6): 759-65.
[http://dx.doi.org/10.1007/s10571-013-9943-6] [PMID: 23695800]
[89]
Song IU, Chung SW, Kim YD, Maeng LS. Relationship between the hs-CRP as non-specific biomarker and Alzheimer’s disease according to aging process. Int J Med Sci 2015; 12(8): 613-7.
[http://dx.doi.org/10.7150/ijms.12742] [PMID: 26283879]
[90]
Rao JS, Rapoport SI, Kim HW. Altered neuroinflammatory, arachidonic acid cascade and synaptic markers in postmortem Alzheimer’s disease brain. Transl Psychiatry 2011; 1(8): e31-e.
[http://dx.doi.org/10.1038/tp.2011.27]
[91]
Asti A, Gioglio L. Can a bacterial endotoxin be a key factor in the kinetics of amyloid fibril formation? J Alzheimers Dis 2014; 39(1): 169-79.
[http://dx.doi.org/10.3233/JAD-131394] [PMID: 24150108]
[92]
Hu X, Wang T, Jin F. Alzheimer’s disease and gut microbiota. Sci China Life Sci 2016; 59(10): 1006-23.
[http://dx.doi.org/10.1007/s11427-016-5083-9] [PMID: 27566465]
[93]
Kim MS, Kim Y, Choi H, et al. Transfer of a healthy microbiota reduces amyloid and tau pathology in an Alzheimer’s disease animal model. Gut 2020; 69(2): 283-94.
[http://dx.doi.org/10.1136/gutjnl-2018-317431] [PMID: 31471351]
[94]
Sun J, Xu J, Ling Y, et al. Fecal microbiota transplantation alleviated Alzheimer’s disease-like pathogenesis in APP/PS1 transgenic mice. Transl Psychiatry 2019; 9(1): 189.
[http://dx.doi.org/10.1038/s41398-019-0525-3] [PMID: 31383855]
[95]
Cosorich I, Dalla-Costa G, Sorini C, et al. High frequency of intestinal TH17 cells correlates with microbiota alterations and disease activity in multiple sclerosis. Sci Adv 2017; 3(7)e1700492
[http://dx.doi.org/10.1126/sciadv.1700492] [PMID: 28706993]
[96]
Xu R, Wang Q. Towards understanding brain-gut-microbiome connections in Alzheimer’s disease. BMC Syst Biol 2016; 10(Suppl. 3): 63.
[http://dx.doi.org/10.1186/s12918-016-0307-y] [PMID: 27585440]
[97]
Pistollato F, Sumalla Cano S, Elio I, Masias Vergara M, Giampieri F, Battino M. Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr Rev 2016; 74(10): 624-34.
[http://dx.doi.org/10.1093/nutrit/nuw023] [PMID: 27634977]
[98]
Bonfili L, Cecarini V, Berardi S, et al. Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels. Sci Rep 2017; 7(1): 2426.
[http://dx.doi.org/10.1038/s41598-017-02587-2] [PMID: 28546539]
[99]
Liu XF, Luo YB, Luo ZH, Yang H. Biomarker studies in multiple sclerosis: from proteins to noncoding RNAs. Neurochem Res 2014; 39(9): 1661-74.
[http://dx.doi.org/10.1007/s11064-014-1386-z] [PMID: 25069641]
[100]
Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nat Rev Immunol 2015; 15(9): 545-58.
[http://dx.doi.org/10.1038/nri3871] [PMID: 26250739]
[101]
Ortiz GG, Pacheco-Moisés FP, Macías-Islas MA, et al. Role of the blood-brain barrier in multiple sclerosis. Arch Med Res 2014; 45(8): 687-97.
[http://dx.doi.org/10.1016/j.arcmed.2014.11.013] [PMID: 25431839]
[102]
Chen J, Chia N, Kalari KR, et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep 2016; 6: 28484.
[http://dx.doi.org/10.1038/srep28484] [PMID: 27346372]
[103]
Cekanaviciute E, Yoo BB, Runia TF, et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc Natl Acad Sci USA 2017; 114(40): 10713-8.
[http://dx.doi.org/10.1073/pnas.1711235114] [PMID: 28893978]
[104]
Ochoa-Repáraz J, Mielcarz DW, Ditrio LE, et al. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J Immunol 2009; 183(10): 6041-50.
[http://dx.doi.org/10.4049/jimmunol.0900747] [PMID: 19841183]
[105]
Chu F, Shi M, Lang Y, et al. Gut microbiota in multiple sclerosis and experimental autoimmune encephalomyelitis: current applications and future perspectives. Mediators Inflamm 2018; •••20188168717
[http://dx.doi.org/10.1155/2018/8168717] [PMID: 29805314]
[106]
Zhang YG, Wu S, Yi J, et al. Target intestinal microbiota to alleviate disease progression in amyotrophic lateral sclerosis. Clin Ther 2017; 39(2): 322-36.
[http://dx.doi.org/10.1016/j.clinthera.2016.12.014] [PMID: 28129947]
[107]
Jiao B, Tang B, Liu X, et al. Identification of C9orf72 repeat expansions in patients with amyotrophic lateral sclerosis and frontotemporal dementia in mainland China. Neurobiol Aging 2014; 35(4): 936.e19-22.
[http://dx.doi.org/10.1016/j.neurobiolaging.2013.10.001]
[108]
Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol Neurodegener 2009; 4: 47.
[http://dx.doi.org/10.1186/1750-1326-4-47] [PMID: 19917131]
[109]
Graves MC, Fiala M, Dinglasan LA, et al. Inflammation in amyotrophic lateral sclerosis spinal cord and brain is mediated by activated macrophages, mast cells and T cells. Amyotroph Lateral Scler Other Motor Neuron Disord 2004; 5(4): 213-9.
[http://dx.doi.org/10.1080/14660820410020286] [PMID: 15799549]
[110]
Rowin J, Xia Y, Jung B, Sun J. Gut inflammation and dysbiosis in human motor neuron disease. Physiol Rep 2017; 5(18)e13443
[http://dx.doi.org/10.14814/phy2.13443] [PMID: 28947596]
[111]
Fang X, Wang X, Yang S, et al. Evaluation of the microbial diversity in amyotrophic lateral sclerosis using high-throughput sequencing. Front Microbiol 2016; 7: 1479.
[http://dx.doi.org/10.3389/fmicb.2016.01479] [PMID: 27703453]
[112]
Brenner D, Hiergeist A, Adis C, et al. The fecal microbiome of ALS patients. Neurobiol Aging 2018; 61: 132-7.
[http://dx.doi.org/10.1016/j.neurobiolaging.2017.09.023] [PMID: 29065369]
[113]
Wu S, Yi J, Zhang YG, Zhou J, Sun J. Leaky intestine and impaired microbiome in an amyotrophic lateral sclerosis mouse model. Physiol Rep 2015; 3(4)e12356
[http://dx.doi.org/10.14814/phy2.12356] [PMID: 25847918]
[114]
Blacher E, Bashiardes S, Shapiro H, et al. Potential roles of gut microbiome and metabolites in modulating ALS in mice. Nature 2019; 572(7770): 474-80.
[http://dx.doi.org/10.1038/s41586-019-1443-5] [PMID: 31330533]
[115]
Zhang R, Miller RG, Gascon R, et al. Circulating endotoxin and systemic immune activation in sporadic amyotrophic lateral sclerosis (sALS). J Neuroimmunol 2009; 206(1-2): 121-4.
[http://dx.doi.org/10.1016/j.jneuroim.2008.09.017] [PMID: 19013651]
[116]
Forsythe P, Sudo N, Dinan T, Taylor VH, Bienenstock J. Mood and gut feelings. Brain Behav Immun 2010; 24(1): 9-16.
[http://dx.doi.org/10.1016/j.bbi.2009.05.058] [PMID: 19481599]
[117]
Horvath K, Perman JA. Autistic disorder and gastrointestinal disease. Curr Opin Pediatr 2002; 14(5): 583-7.
[http://dx.doi.org/10.1097/00008480-200210000-00004] [PMID: 12352252]
[118]
Li Q, Han Y, Dy ABC, Hagerman RJ. The Gut microbiota and autism spectrum disorders. Front Cell Neurosci 2017; 11: 120.
[http://dx.doi.org/10.3389/fncel.2017.00120] [PMID: 28503135]
[119]
Abdallah MWLN, Larsen N, Grove J, et al. Amniotic fluid inflammatory cytokines: potential markers of immunologic dysfunction in autism spectrum disorders. World J Biol Psychiatry 2013; 14(7): 528-38.
[http://dx.doi.org/10.3109/15622975.2011.639803] [PMID: 22175527]
[120]
Brown AS, Sourander A, Hinkka-Yli-Salomäki S, McKeague IW, Sundvall J, Surcel HM. Elevated maternal C-reactive protein and autism in a national birth cohort. Mol Psychiatry 2014; 19(2): 259-64.
[http://dx.doi.org/10.1038/mp.2012.197] [PMID: 23337946]
[121]
Adams JB, Johansen LJ, Powell LD, Quig D, Rubin RA. Gastrointestinal flora and gastrointestinal status in children with autism--comparisons to typical children and correlation with autism severity. BMC Gastroenterol 2011; 11(1): 22.
[http://dx.doi.org/10.1186/1471-230X-11-22] [PMID: 21410934]
[122]
De Angelis M, Piccolo M, Vannini L, et al. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS One 2013; 8(10)e76993
[http://dx.doi.org/10.1371/journal.pone.0076993] [PMID: 24130822]
[123]
Williams BL, Hornig M, Buie T, et al. Impaired carbohydrate digestion and transport and mucosal dysbiosis in the intestines of children with autism and gastrointestinal disturbances. PLoS One 2011; 6(9)e24585
[http://dx.doi.org/10.1371/journal.pone.0024585] [PMID: 21949732]
[124]
Hsiao EY, McBride SW, Hsien S, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013; 155(7): 1451-63.
[http://dx.doi.org/10.1016/j.cell.2013.11.024] [PMID: 24315484]
[125]
Choi GBYY, Yim YS, Wong H, et al. The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science 2016; 351(6276): 933-9.
[http://dx.doi.org/10.1126/science.aad0314] [PMID: 26822608]
[126]
Fiorentino M, Sapone A, Senger S, et al. Blood-brain barrier and intestinal epithelial barrier alterations in autism spectrum disorders. Mol Autism 2016; 7: 49.
[http://dx.doi.org/10.1186/s13229-016-0110-z] [PMID: 27957319]
[127]
Coretti L, Cristiano C, Florio E, et al. Sex-related alterations of gut microbiota composition in the BTBR mouse model of autism spectrum disorder. Sci Rep 2017; 7(1): 45356.
[http://dx.doi.org/10.1038/srep45356] [PMID: 28349974]
[128]
Abdelli LS, Samsam A, Naser SA. Propionic acid induces gliosis and neuro-inflammation through modulation of PTEN/AKT Pathway in Autism Spectrum Disorder. Sci Rep 2019; 9(1): 8824.
[http://dx.doi.org/10.1038/s41598-019-45348-z] [PMID: 31217543]
[129]
Mirza R, Sharma B. A selective peroxisome proliferator-activated receptor-γ agonist benefited propionic acid induced autism-like behavioral phenotypes in rats by attenuation of neuroinflammation and oxidative stress. Chem Biol Interact 2019; 311108758
[http://dx.doi.org/10.1016/j.cbi.2019.108758] [PMID: 31348919]
[130]
Kang D-W, Adams JB, Coleman DM, et al. Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota. Sci Rep 2019; 9(1): 5821.
[http://dx.doi.org/10.1038/s41598-019-42183-0] [PMID: 30967657]
[131]
Russo AJ. Decreased plasma myeloperoxidase associated with probiotic therapy in autistic children. Clin Med Insights Pediatr 2015; 9: 13-7.
[http://dx.doi.org/10.4137/CMPed.S17901] [PMID: 25674031]
[132]
Saurman V, Margolis KG, Luna RA. Autism spectrum disorder as a brain-gut-microbiome axis disorder. Dig Dis Sci 2020; 65(3): 818-28.
[http://dx.doi.org/10.1007/s10620-020-06133-5] [PMID: 32056091]
[133]
Preidis GA, Versalovic J. Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 2009; 136(6): 2015-31.
[http://dx.doi.org/10.1053/j.gastro.2009.01.072] [PMID: 19462507]
[134]
Aarts E, Ederveen THA, Naaijen J, et al. Gut microbiome in ADHD and its relation to neural reward anticipation. PLoS One 2017; 12(9)e0183509
[http://dx.doi.org/10.1371/journal.pone.0183509] [PMID: 28863139]
[135]
Cheng S, Han B, Ding M, et al. Identifying psychiatric disorder-associated gut microbiota using microbiota-related gene set enrichment analysis. Brief Bioinform 2020; 21(3): 1016-22.
[http://dx.doi.org/10.1093/bib/bbz034] [PMID: 30953055]
[136]
Dam SA, Mostert JC, Szopinska-Tokov JW, Bloemendaal M, Amato M, Arias-Vasquez A. The role of the gut-brain axis in attention-deficit/hyperactivity disorder. Gastroenterol Clin North Am 2019; 48(3): 407-31.
[http://dx.doi.org/10.1016/j.gtc.2019.05.001] [PMID: 31383279]
[137]
Szopinska-Tokov J, Dam S, Naaijen J, et al. Investigating the gut microbiota composition of individuals with attention-deficit/hyperactivity disorder and association with symptoms. Microorganisms 2020; 8(3)E406
[http://dx.doi.org/10.3390/microorganisms8030406] [PMID: 32183143]
[138]
Wan L, Ge WR, Zhang S, Sun YL, Wang B, Yang G. Case-control study of the effects of gut microbiota composition on neurotransmitter metabolic pathways in children with attention deficit hyperactivity disorder. Front Neurosci 2020; 14: 127.
[http://dx.doi.org/10.3389/fnins.2020.00127] [PMID: 32132899]
[139]
Tengeler AC, Dam SA, Wiesmann M, et al. Gut microbiota from persons with attention-deficit/hyperactivity disorder affects the brain in mice. Microbiome 2020; 8(1): 44.
[http://dx.doi.org/10.1186/s40168-020-00816-x] [PMID: 32238191]
[140]
Hamad AF, Alessi-Severini S, Mahmud SM, Brownell M, Kuo IF. antibiotic exposure in the first year of life and the risk of attention-deficit/hyperactivity disorder: a population-based cohort study. Am J Epidemiol 2019; 188(11): 1923-31.
[http://dx.doi.org/10.1093/aje/kwz178] [PMID: 31497848]
[141]
Slykerman RF, Coomarasamy C, Wickens K, et al. Exposure to antibiotics in the first 24 months of life and neurocognitive outcomes at 11 years of age. Psychopharmacology (Berl) 2019; 236(5): 1573-82.
[http://dx.doi.org/10.1007/s00213-019-05216-0] [PMID: 31041458]
[142]
Rianda D, Agustina R, Setiawan EA, Manikam NRM. Effect of probiotic supplementation on cognitive function in children and adolescents: a systematic review of randomised trials. Benef Microbes 2019; 10(8): 873-82.
[http://dx.doi.org/10.3920/BM2019.0068] [PMID: 31965841]
[143]
Cruz-Pereira JS, Rea K, Nolan YM, O’Leary OF, Dinan TG, Cryan JF. Depression’s unholy trinity: dysregulated stress, immunity, and the microbiome. Annu Rev Psychol 2020; 71(1): 49-78.
[http://dx.doi.org/10.1146/annurev-psych-122216-011613] [PMID: 31567042]
[144]
Dinan TG, Quigley EMM, Ahmed SMM, et al. Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology 2006; 130(2): 304-11.
[http://dx.doi.org/10.1053/j.gastro.2005.11.033] [PMID: 16472586]
[145]
O’Mahony SM, Marchesi JR, Scully P, et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009; 65(3): 263-7.
[http://dx.doi.org/10.1016/j.biopsych.2008.06.026] [PMID: 18723164]
[146]
Jang HM, Lee KE, Lee HJ, Kim DH. Immobilization stress-induced Escherichia coli causes anxiety by inducing NF-κB activation through gut microbiota disturbance. Sci Rep 2018; 8(1): 13897.
[http://dx.doi.org/10.1038/s41598-018-31764-0] [PMID: 30224732]
[147]
Bangsgaard Bendtsen KM, Krych L, Sørensen DB, et al. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS One 2012; 7(10)e46231
[http://dx.doi.org/10.1371/journal.pone.0046231] [PMID: 23056268]
[148]
Dudek KA, Dion-Albert L, Lebel M, et al. Molecular adaptations of the blood-brain barrier promote stress resilience vs. depression. Proc Natl Acad Sci USA 2020; 117(6): 3326-36.
[http://dx.doi.org/10.1073/pnas.1914655117] [PMID: 31974313]
[149]
Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558(Pt 1): 263-75.
[http://dx.doi.org/10.1113/jphysiol.2004.063388] [PMID: 15133062]
[150]
Goehler LE, Gaykema RP, Opitz N, Reddaway R, Badr N, Lyte M. Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 2005; 19(4): 334-44.
[http://dx.doi.org/10.1016/j.bbi.2004.09.002] [PMID: 15944073]
[151]
Severance EG, Gressitt KL, Stallings CR, et al. Discordant patterns of bacterial translocation markers and implications for innate immune imbalances in schizophrenia. Schizophr Res 2013; 148(1-3): 130-7.
[http://dx.doi.org/10.1016/j.schres.2013.05.018] [PMID: 23746484]
[152]
Silk DB, Davis A, Vulevic J, Tzortzis G, Gibson GR. Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome. Aliment Pharmacol Ther 2009; 29(5): 508-18.
[http://dx.doi.org/10.1111/j.1365-2036.2008.03911.x] [PMID: 19053980]
[153]
Rao AV, Bested AC, Beaulne TM, et al. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog 2009; 1(1): 6.
[http://dx.doi.org/10.1186/1757-4749-1-6] [PMID: 19338686]
[154]
Li N, Wang Q, Wang Y, et al. Oral probiotics ameliorate the behavioral deficits induced by chronic mild stress in mice via the gut microbiota-inflammation axis. Front Behav Neurosci 2018; 12: 266.
[http://dx.doi.org/10.3389/fnbeh.2018.00266] [PMID: 30459574]
[155]
Dickerson F, Severance E, Yolken R. The microbiome, immunity, and schizophrenia and bipolar disorder. Brain Behav Immun 2017; 62: 46-52.
[http://dx.doi.org/10.1016/j.bbi.2016.12.010] [PMID: 28003152]
[156]
Castro-Nallar E, Bendall ML, Pérez-Losada M, et al. Composition, taxonomy and functional diversity of the oropharynx microbiome in individuals with schizophrenia and controls. PeerJ 2015; 3e1140
[http://dx.doi.org/10.7717/peerj.1140] [PMID: 26336637]
[157]
Zheng P, Zeng B, Liu M, et al. The gut microbiome from patients with schizophrenia modulates the glutamate-glutamine-GABA cycle and schizophrenia-relevant behaviors in mice. Sci Adv 2019; 5(2)eaau8317
[http://dx.doi.org/10.1126/sciadv.aau8317] [PMID: 30775438]
[158]
Ghaderi A, Banafshe HR, Mirhosseini N, et al. Clinical and metabolic response to vitamin D plus probiotic in schizophrenia patients. BMC Psychiatry 2019; 19(1): 77.
[http://dx.doi.org/10.1186/s12888-019-2059-x] [PMID: 30791895]
[159]
Maes M, Kanchanatawan B, Sirivichayakul S, Carvalho AF. In schizophrenia, increased plasma IgM/IgA responses to gut commensal bacteria are associated with negative symptoms, neurocognitive impairments, and the deficit phenotype. Neurotox Res 2019; 35(3): 684-98.
[http://dx.doi.org/10.1007/s12640-018-9987-y] [PMID: 30552634]
[160]
Maes M, Sirivichayakul S, Kanchanatawan B, Vodjani A. Breakdown of the paracellular tight and adherens junctions in the gut and blood brain barrier and damage to the vascular barrier in patients with deficit schizophrenia. Neurotox Res 2019; 36(2): 306-22.
[http://dx.doi.org/10.1007/s12640-019-00054-6] [PMID: 31077000]
[161]
Maes M, Vojdani A, Geffard M, et al. Schizophrenia phenomenology comprises a bifactorial general severity and a single-group factor, which are differently associated with neurotoxic immune and immune-regulatory pathways. Biomol Concepts 2019; 10(1): 209-25.
[http://dx.doi.org/10.1515/bmc-2019-0023] [PMID: 31734647]
[162]
He Y, Kosciolek T, Tang J, et al. Gut microbiome and magnetic resonance spectroscopy study of subjects at ultra-high risk for psychosis may support the membrane hypothesis. Eur Psychiatry 2018; 53: 37-45.
[http://dx.doi.org/10.1016/j.eurpsy.2018.05.011] [PMID: 29870894]
[163]
Dickerson FB SC, Origoni A, Katsafanas E, et al. Effect of probiotic supplementation on schizophrenia symptoms and association with gastrointestinal functioning: a randomized, placebo-controlled trial. Prim Care Companion CNS Disord 2014; 16(1)PCC.13m01579.
[http://dx.doi.org/10.4088/PCC.13m01579]
[164]
Patel JP, Frey BN. Disruption in the blood-brain barrier: the missing link between brain and body inflammation in bipolar disorder? Neural Plast 2015; 2015708306
[http://dx.doi.org/10.1155/2015/708306] [PMID: 26075104]
[165]
Kılıç F, Işık Ü, Demirdaş A, Doğuç DK, Bozkurt M. Serum zonulin and claudin-5 levels in patients with bipolar disorder. J Affect Disord 2020; 266: 37-42.
[http://dx.doi.org/10.1016/j.jad.2020.01.117] [PMID: 32056901]
[166]
Rosenblat JD, Cha DS, Mansur RB, McIntyre RS. Inflamed moods: a review of the interactions between inflammation and mood disorders. Prog Neuropsychopharmacol Biol Psychiatry 2014; 53: 23-34.
[http://dx.doi.org/10.1016/j.pnpbp.2014.01.013] [PMID: 24468642]
[167]
Anderson G, Maes M. Bipolar disorder: role of immune-inflammatory cytokines, oxidative and nitrosative stress and tryptophan catabolites. Curr Psychiatry Rep 2015; 17(2): 8.
[http://dx.doi.org/10.1007/s11920-014-0541-1] [PMID: 25620790]
[168]
Hu S, Li A, Huang T, et al. Gut microbiota changes in patients with bipolar depression. Adv Sci (Weinh) 2019; 6(14)1900752
[http://dx.doi.org/10.1002/advs.201900752] [PMID: 31380217]
[169]
Evans SJ, Bassis CM, Hein R, et al. The gut microbiome composition associates with bipolar disorder and illness severity. J Psychiatr Res 2017; 87: 23-9.
[http://dx.doi.org/10.1016/j.jpsychires.2016.12.007] [PMID: 27988330]
[170]
Lu Q, Lai J, Lu H, et al. Gut microbiota in bipolar depression and its relationship to brain function: an advanced exploration. Front Psychiatry 2019; 10: 784.
[http://dx.doi.org/10.3389/fpsyt.2019.00784] [PMID: 31736803]
[171]
Reininghaus EZ, Wetzlmair LC, Fellendorf FT, et al. The impact of probiotic supplements on cognitive parameters in euthymic individuals with bipolar disorder: a pilot study. Neuropsychobiology 2018; 1-8.
[PMID: 30227422]
[172]
Wallace CJK, Milev R. The effects of probiotics on depressive symptoms in humans: a systematic review. Ann Gen Psychiatry 2017; 16: 14.
[http://dx.doi.org/10.1186/s12991-017-0138-2] [PMID: 28239408]
[173]
Yolken R, Adamos M, Katsafanas E, et al. Individuals hospitalized with acute mania have increased exposure to antimicrobial medications. Bipolar Disord 2016; 18(5): 404-9.
[http://dx.doi.org/10.1111/bdi.12416] [PMID: 27425597]
[174]
Benros ME, Waltoft BL, Nordentoft M, et al. Autoimmune diseases and severe infections as risk factors for mood disorders: a nationwide study. JAMA Psychiatry 2013; 70(8): 812-20.
[http://dx.doi.org/10.1001/jamapsychiatry.2013.1111] [PMID: 23760347]
[175]
Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat Med 2011; 17(7): 796-808.
[http://dx.doi.org/10.1038/nm.2399] [PMID: 21738161]
[176]
Benakis C, Brea D, Caballero S, et al. Commensal microbiota affects ischemic stroke outcome by regulating intestinal γδ T cells. Nat Med 2016; 22(5): 516-23.
[http://dx.doi.org/10.1038/nm.4068] [PMID: 27019327]
[177]
Singh V, Roth S, Llovera G, et al. Microbiota dysbiosis controls the neuroinflammatory response after stroke. J Neurosci 2016; 36(28): 7428-40.
[http://dx.doi.org/10.1523/JNEUROSCI.1114-16.2016] [PMID: 27413153]
[178]
Spychala MS, Venna VR, Jandzinski M, et al. Age-related changes in the gut microbiota influence systemic inflammation and stroke outcome. Ann Neurol 2018; 84(1): 23-36.
[http://dx.doi.org/10.1002/ana.25250] [PMID: 29733457]
[179]
Chen R, Xu Y, Wu P, et al. Transplantation of fecal microbiota rich in short chain fatty acids and butyric acid treat cerebral ischemic stroke by regulating gut microbiota. Pharmacol Res 2019; •••148104403
[http://dx.doi.org/10.1016/j.phrs.2019.104403] [PMID: 31425750]
[180]
Wanchao S, Chen M, Zhiguo S, Futang X, Mengmeng S. Protective effect and mechanism of Lactobacillus on cerebral ischemia reperfusion injury in rats. Braz J Med Biol Res 2018; 51(7)e7172
[http://dx.doi.org/10.1590/1414-431x20187172] [PMID: 29791585]
[181]
Peng J, Luo F, Ruan G, Peng R, Li X. Hypertriglyceridemia and atherosclerosis. Lipids Health Dis 2017; 16(1): 233.
[http://dx.doi.org/10.1186/s12944-017-0625-0] [PMID: 29212549]
[182]
Karlsson FH, Fåk F, Nookaew I, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun 2012; 3(1): 1245.
[http://dx.doi.org/10.1038/ncomms2266] [PMID: 23212374]
[183]
Fernandes CP, Oliveira FA, Silva PG, et al. Molecular analysis of oral bacteria in dental biofilm and atherosclerotic plaques of patients with vascular disease. Int J Cardiol 2014; 174(3): 710-2.
[http://dx.doi.org/10.1016/j.ijcard.2014.04.201] [PMID: 24820755]
[184]
Wang Z, Klipfell E, Bennett BJ, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011; 472(7341): 57-63.
[http://dx.doi.org/10.1038/nature09922] [PMID: 21475195]
[185]
Chen Ml, Zhu Xh, Ran L. Lang Hd, Yi L, Mi Mt. Trimethylamine‐N‐oxide induces vascular inflammation by activating the NLRP3 inflammasome through the SIRT3‐SOD2‐mtROS signaling pathway. J Am Heart Assoc 2017; 6(9)e006347
[http://dx.doi.org/10.1161/JAHA.117.006347]
[186]
Yin J, Liao SX, He Y, et al. Dysbiosis of gut microbiota with reduced trimethylamine-N-oxide level in patients with large-artery atherosclerotic stroke or transient ischemic attack. J Am Heart Assoc 2015; 4(11)e002699
[http://dx.doi.org/10.1161/JAHA.115.002699] [PMID: 26597155]
[187]
Fatkhullina ARPI, Peshkova IO, Dzutsev A, et al. An Interleukin-23-interleukin-22 axis regulates intestinal microbial homeostasis to protect from diet-induced atherosclerosis. Immunity 2018; 49(5): 943-957.e9.
[http://dx.doi.org/10.1016/j.immuni.2018.09.011] [PMID: 30389414]
[188]
Jonsson AL, Bäckhed F. Role of gut microbiota in atherosclerosis. Nat Rev Cardiol 2017; 14(2): 79-87.
[http://dx.doi.org/10.1038/nrcardio.2016.183] [PMID: 27905479]
[189]
Carnevale R, Nocella C, Petrozza V, et al. Localization of lipopolysaccharide from Escherichia coli into human atherosclerotic plaque. Sci Rep 2018; 8(1): 3598.
[http://dx.doi.org/10.1038/s41598-018-22076-4] [PMID: 29483584]
[190]
Ohira H, Tsutsui W, Fujioka Y. Are short chain fatty acids in gut microbiota defensive players for inflammation and atherosclerosis? J Atheroscler Thromb 2017; 24(7): 660-72.
[http://dx.doi.org/10.5551/jat.RV17006] [PMID: 28552897]
[191]
Du Y, Li X, Su C, et al. Butyrate protects against high-fat diet-induced atherosclerosis via up-regulating ABCA1 expression in apolipoprotein E-deficiency mice. Br J Pharmacol 2019; 177(8): 1754-72.
[PMID: 31769014]
[192]
Texakalidis P, Sweid A, Mouchtouris N, et al. Aneurysm formation, growth, and rupture: the biology and physics of cerebral aneurysms. World Neurosurg 2019; 130: 277-84.
[http://dx.doi.org/10.1016/j.wneu.2019.07.093] [PMID: 31323409]
[193]
Xie J, Lu W, Zhong L, et al. Alterations in gut microbiota of abdominal aortic aneurysm mice. BMC Cardiovasc Disord 2020; 20(1): 32.
[http://dx.doi.org/10.1186/s12872-020-01334-2] [PMID: 31992206]
[194]
Pyysalo MJ, Pyysalo LM, Pessi T, Karhunen PJ, Öhman JE. The connection between ruptured cerebral aneurysms and odontogenic bacteria. J Neurol Neurosurg Psychiatry 2013; 84(11): 1214-8.
[http://dx.doi.org/10.1136/jnnp-2012-304635] [PMID: 23761916]
[195]
Pyysalo MJ, Pyysalo LM, Pessi T, et al. Bacterial DNA findings in ruptured and unruptured intracranial aneurysms. Acta Odontol Scand 2016; 74(4): 315-20.
[http://dx.doi.org/10.3109/00016357.2015.1130854] [PMID: 26777430]
[196]
Shikata F, Shimada K, Sato H, et al. Potential influences of gut microbiota on the formation of intracranial aneurysm. Hypertension 2019; 73(2): 491-6.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.118.11804] [PMID: 30624992]
[197]
Fischer A, Zalvide J, Faurobert E, Albiges-Rizo C, Tournier-Lasserve E. Cerebral cavernous malformations: from CCM genes to endothelial cell homeostasis. Trends Mol Med 2013; 19(5): 302-8.
[http://dx.doi.org/10.1016/j.molmed.2013.02.004] [PMID: 23506982]
[198]
Shenkar R, Shi C, Check IJ, Lipton HL, Awad IA. Concepts and hypotheses: inflammatory hypothesis in the pathogenesis of cerebral cavernous malformations. Neurosurgery 2007; 61(4): 693-702.
[http://dx.doi.org/10.1227/01.NEU.0000298897.38979.07] [PMID: 17986930]
[199]
Tang AT, Choi JP, Kotzin JJ, et al. Endothelial TLR4 and the microbiome drive cerebral cavernous malformations. Nature 2017; 545(7654): 305-10.
[http://dx.doi.org/10.1038/nature22075] [PMID: 28489816]
[200]
Tang ATSK, Sullivan KR, Hong CC, et al. Distinct cellular roles for PDCD10 define a gut-brain axis in cerebral cavernous malformation. Sci Transl Med 2019; 11(520): eaaw352.
[http://dx.doi.org/10.1126/scitranslmed.aaw3521] [PMID: 31776290]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 7
Year: 2020
Page: [509 - 526]
Pages: 18
DOI: 10.2174/1871527319666200726222138
Price: $65

Article Metrics

PDF: 22
HTML: 3