Limosilactobacillus reuteri normalizes blood–brain barrier dysfunction and neurodevelopment deficits associated with prenatal exposure to lipopolysaccharide

References

• Han VX, Patel S, Jones HF, Nielsen TC, Mohammad SS, Hofer MJ, Gold W, Brilot F, Lain SJ, Nassar N, et al. Maternal acute and chronic inflammation in pregnancy is associated with common neurodevelopmental disorders: a systematic review. Transl Psychiatry. 2021;11(71). doi:10.1038/s41398-021-01198-w
   Google Scholar
• Furman D, Campisi J, Verdin E, Carrera-Bastos P, Targ S, Franceschi C, Ferrucci L, Gilroy DW, Fasano A, Miller GW, et al. Chronic inflammation in the etiology of disease across the life span. Nat Med. 2019;25(1822–1832). doi:10.1038/s41591-019-0675-0
   Google Scholar
• Ginsberg Y, Khatib N, Weiner Z, Beloosesky R. Maternal inflammation, fetal brain implications and suggested neuroprotection: a summary of 10 years of research in animal models. Rambam Maimonides Med J. 2017;8. doi:10.5041/RMMJ.10305.
   Google Scholar
• Meyer U, Feldon J, Schedlowski M, Yee BK. Immunological stress at the maternal-foetal interface: a link between neurodevelopment and adult psychopathology. Brain Behav Immun. 2006;20(378–388). doi:10.1016/j.bbi.2005.11.003.
   PubMedGoogle Scholar
• Burd I, Bentz AI, Chai J, Gonzalez J, Monnerie H, Le Roux PD, Cohen AS, Yudkoff M, Elovitz MA. Inflammation-induced preterm birth alters neuronal morphology in the mouse fetal brain. J Neurosci Res. 2010;88(1872–1881). doi:10.1002/jnr.22368.
   PubMedGoogle Scholar
• Beloosesky R, Khatib N, Ginsberg Y, Anabosy S, Shalom-Paz E, Dahis M, Ross MG, Weiner Z. Maternal magnesium sulfate fetal neuroprotective effects to the fetus: inhibition of neuronal nitric oxide synthase and nuclear factor kappa-light-chain-enhancer of activated B cells activation in a rodent model. Am J Obstet Gynecol. 2016;215:382 e381–21. doi:10.1016/j.ajog.2016.03.032.
   Web of Science ®Google Scholar
• Wu YW, Colford J. M. Jr. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA. 2000;284:1417–1424. doi:10.1001/jama.284.11.1417.
   PubMed Web of Science ®Google Scholar
• Shatrov JG, Birch SCM, Lam LT, Quinlivan JA, McIntyre S, Mendz GL. Chorioamnionitis and cerebral palsy: a meta-analysis. Obstet Gynecol. 2010;116(387–392). doi:10.1097/AOG.0b013e3181e90046.
   PubMedGoogle Scholar
• Kuypers E, Ophelders D, Jellema RK, Kunzmann S, Gavilanes AW, Kramer BW. White matter injury following fetal inflammatory response syndrome induced by chorioamnionitis and fetal sepsis: lessons from experimental ovine models. Early Hum Dev. 2012;88(931–936). doi:10.1016/j.earlhumdev.2012.09.011.
   PubMedGoogle Scholar
• Paton MCB, McDonald CA, Allison BJ, Fahey MC, Jenkin G, Miller SL. Perinatal brain injury as a consequence of preterm birth and intrauterine inflammation: designing targeted stem cell therapies. Front Neurosci. 2017;11(200). doi:10.3389/fnins.2017.00200.
   PubMedGoogle Scholar
• Bell MJ, Hallenbeck JM. Effects of intrauterine inflammation on developing rat brain. J Neurosci Res. 2002;70(570–579). doi:10.1002/jnr.10423.
   PubMedGoogle Scholar
• Larouche A, Roy M, Kadhim H, Tsanaclis AM, Fortin D, Sébire G. Neuronal injuries induced by perinatal hypoxic-ischemic insults are potentiated by prenatal exposure to lipopolysaccharide: animal model for perinatally acquired encephalopathy. Dev Neurosci. 2005;27(134–142). doi:10.1159/000085985.
   PubMedGoogle Scholar
• Paintlia MK, Paintlia AS, Barbosa E, Singh I, Singh AK. N-acetylcysteine prevents endotoxin-induced degeneration of oligodendrocyte progenitors and hypomyelination in developing rat brain. J Neurosci Res. 2004;78(347–361). doi:10.1002/jnr.20261.
   PubMedGoogle Scholar
• Rousset CI, Chalon S, Cantagrel S, Bodard S, Andres C, Gressens P, Saliba E. Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res. 2006;59(428–433). doi:10.1203/01.pdr.0000199905.08848.55.
   PubMedGoogle Scholar
• Rousset CI, Kassem J, Aubert A, Planchenault D, Gressens P, Chalon S, Belzung C, Saliba E. Maternal exposure to lipopolysaccharide leads to transient motor dysfunction in neonatal rats. Dev Neurosci. 2013;35(172–181). doi:10.1159/000346579
   PubMedGoogle Scholar
• Girard S, Tremblay L, Lepage M, Sebire GIL-1. receptor antagonist protects against placental and neurodevelopmental defects induced by maternal inflammation. J Immunol. 2010;184(3997–4005). doi:10.4049/jimmunol.0903349.
   PubMedGoogle Scholar
• Bao M, Hofsink N, Plosch T. LPS versus Poly I:C model: comparison of long-term effects of bacterial and viral maternal immune activation on the offspring. Am J Physiol Regul Integr Comp Physiol. 2022;322:R99–R111. doi:10.1152/ajpregu.00087.2021.
   PubMed Web of Science ®Google Scholar
• Diaz Heijtz R, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011;108(3047–3052). doi:10.1073/pnas.1010529108.
   PubMedGoogle Scholar
• 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(509–518). doi:10.1016/j.molmed.2014.05.002.
   PubMedGoogle Scholar
• Borre YE, Moloney RD, Clarke G, Dinan TG, Cryan JF. The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Adv Exp Med Biol. 2014;817(373–403). doi:10.1007/978-1-4939-0897-4_17.
   PubMedGoogle Scholar
• Lu J, Lu L, Yu Y, Oliphant K, Drobyshevsky A, Claud EC. Early preterm infant microbiome impacts adult learning. Sci Rep. 2022;12(3310). doi:10.1038/s41598-022-07245-w
   Google Scholar
• Lu J, Lu L, Yu Y, Cluette-Brown J, Martin CR, Claud EC. Effects of intestinal microbiota on brain development in humanized gnotobiotic mice. Sci Rep. 2018;8(5443). doi:10.1038/s41598-018-23692-w
   Google Scholar
• Lu J, Synowiec S, Lu L, Yu Y, Bretherick T, Takada S, Yarnykh V, Caplan J, Caplan M, Claud EC, et al. Microbiota influence the development of the brain and behaviors in C57BL/6J mice. PLoS One. 2018;13(e0201829). doi:10.1371/journal.pone.0201829
   Google Scholar
• Mayer EA, Knight R, Mazmanian SK, Cryan JF, Tillisch K. Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci. 2014;34(15490–15496). doi:10.1523/JNEUROSCI.3299-14.2014.
   Google Scholar
• Burokas A, Moloney RD, Dinan TG, Cryan JF. Microbiota regulation of the Mammalian gut-brain axis. Adv Appl Microbiol. 2015;91(1–62). doi:10.1016/bs.aambs.2015.02.001.
   PubMedGoogle Scholar
• Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, et al. Expert consensus document. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11:506–514. doi:10.1038/nrgastro.2014.66.
   PubMed Web of Science ®Google Scholar
• Deshpande G, Rao S, Patole S. Probiotics for prevention of necrotising enterocolitis in preterm neonates with very low birthweight: a systematic review of randomised controlled trials. Lancet. 2007;369(1614–1620). doi:10.1016/S0140-6736(07)60748-X.
   Google Scholar
• Martin CR, Walker WA. Probiotics: role in pathophysiology and prevention in necrotizing enterocolitis. Semin Perinatol. 2008;32(127–137). doi:10.1053/j.semperi.2008.01.006.
   Google Scholar
• Gutierrez-Castrellon P, Indrio F, Bolio-Galvis A, Jiménez-Gutiérrez C, Jimenez-Escobar I, López-Velázquez G. Efficacy of Lactobacillus reuteri DSM 17938 for infantile colic: systematic review with network meta-analysis. Medicine (Baltimore). 2017;96(e9375). doi:10.1097/MD.0000000000009375.
   PubMedGoogle Scholar
• Sung V, D’Amico F, Cabana MD, Chau K, Koren G, Savino F, Szajewska H, Deshpande G, Dupont C, Indrio F, et al. Lactobacillus reuteri to Treat Infant Colic: a Meta-analysis. Pediatrics. 2018;141. doi:10.1542/peds.2017-1811.
   PubMed Web of Science ®Google Scholar
• Indrio F, Di Mauro A, Riezzo G, Civardi E, Intini C, Corvaglia L, Ballardini E, Bisceglia M, Cinquetti M, Brazzoduro E, Del Vecchio A, Tafuri S, Francavilla R. Prophylactic use of a probiotic in the prevention of colic, regurgitation, and functional constipation: a randomized clinical trial. JAMA Pediatr. 2014;168(228–233). doi:10.1001/jamapediatrics.2013.4367
   Google Scholar
• Buffington SA, Di Prisco GV, Auchtung TA, Ajami NJ, Petrosino JF, Costa-Mattioli M. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell. 2016;165(1762–1775). doi:10.1016/j.cell.2016.06.001.
   PubMedGoogle Scholar
• Soll RF. Probiotics: are we ready for routine use? Pediatrics. 2010;125:1071–1072. doi:10.1542/peds.2010-0643.
   PubMed Web of Science ®Google Scholar
• Caplan MS. Probiotic and prebiotic supplementation for the prevention of neonatal necrotizing enterocolitis. J Perinatol. 2009;29(Suppl 2):S2–6. doi:10.1038/jp.2009.21.
   PubMedGoogle Scholar
• Yu JC, Khodadadi H, Malik A, Davidson B, Salles ÉDSL, Bhatia J, Hale VL, Baban B. Innate immunity of neonates and infants. Front Immunol. 2018;9(1759). doi:10.3389/fimmu.2018.01759.
   Google Scholar
• Dani C, Coviello C C, Corsini I I, Arena F, Antonelli A, Rossolini GM. Lactobacillus sepsis and probiotic therapy in newborns: two new cases and literature review. AJP Rep. 2016;6(e25–29). doi:10.1055/s-0035-1566312.
   PubMedGoogle Scholar
• Esaiassen E, Cavanagh P, Hjerde E, Simonsen GS, Støen R, Klingenberg C. Bifidobacterium longum subspecies infantis bacteremia in 3 extremely preterm infants receiving probiotics. Emerg Infect Dis. 2016;22(1664–1666). doi:10.3201/eid2209.160033.
   PubMedGoogle Scholar
• Hartel C, Pagel J, Rupp J, Bendiks M, Guthmann F, Rieger-Fackeldey E, Heckmann M, Franz A, Schiffmann J-H, Zimmermann B, et al. Prophylactic use of Lactobacillus acidophilus/Bifidobacterium infantis probiotics and outcome in very low birth weight infants. J Pediatr. 2014;165:285–289 e281. doi:10.1016/j.jpeds.2014.04.029.
   PubMed Web of Science ®Google Scholar
• Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. The central nervous system and the gut microbiome. Cell. 2016;167(915–932). doi:10.1016/j.cell.2016.10.027.
   PubMedGoogle Scholar
• Lu J, Lu L, Yu Y, Baranowski J, Claud EC. Maternal administration of probiotics promotes brain development and protects offspring’s brain from postnatal inflammatory insults in C57/BL6J mice. Sci Rep. 2020;10(8178). doi:10.1038/s41598-020-65180-0.
   Google Scholar
• Liang S, Wu X, Jin F. Gut-brain psychology: rethinking psychology from the microbiota-gut-brain axis. Front Integr Neurosci. 2018;12(33). doi:10.3389/fnint.2018.00033.
   Google Scholar
• Moretti R, Pansiot J, Bettati D, Strazielle N, Ghersi-Egea J-F, Damante G, Fleiss B, Titomanlio L, Gressens P. Blood-brain barrier dysfunction in disorders of the developing brain. Front Neurosci. 2015;9(40). doi:10.3389/fnins.2015.00040.
   PubMedGoogle Scholar
• Bell RD, Zlokovic BV. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer’s disease. Acta Neuropathol. 2009;118(103–113). doi:10.1007/s00401-009-0522-3.
   PubMedGoogle Scholar
• Tarlungeanu DC, Deliu E, Dotter CP, Kara M, Janiesch PC, Scalise M, Galluccio M, Tesulov M, Morelli E, Sonmez FM, et al. Impaired amino acid transport at the blood brain barrier is a cause of autism spectrum disorder. Cell. 2016;167:1481–1494 e1418. doi:10.1016/j.cell.2016.11.013.
   PubMed Web of Science ®Google Scholar
• Charriaut-Marlangue C, Bonnin P, Leger PL, Renolleau S. Brief update on hemodynamic responses in animal models of neonatal stroke and hypoxia-ischemia. Exp Neurol. 2013;248(316–320). doi:10.1016/j.expneurol.2013.06.022.
   PubMedGoogle Scholar
• Banks WA. Blood-brain barrier transport of cytokines: a mechanism for neuropathology. Curr Pharm Des. 2005;11(973–984). doi:10.2174/1381612053381684.
   PubMedGoogle Scholar
• Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, Korecka A, Bakocevic N, Ng LG, Kundu P, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6(263ra158). doi:10.1126/scitranslmed.3009759
   PubMedGoogle Scholar
• Saunders NR, Liddelow SA, Dziegielewska KM. Barrier mechanisms in the developing brain. Front Pharmacol. 2012;3(46). doi:10.3389/fphar.2012.00046.
   PubMedGoogle Scholar
• Stolp HB, Dziegielewska KM, Ek CJ, Potter AM, Saunders NR. Long-term changes in blood-brain barrier permeability and white matter following prolonged systemic inflammation in early development in the rat. Eur J Neurosci. 2005;22(2805–2816). doi:10.1111/j.1460-9568.2005.04483.x.
   PubMedGoogle Scholar
• Stolp HB, Dziegielewska KM. Review: role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathol Appl Neurobiol. 2009;35(132–146). doi:10.1111/j.1365-2990.2008.01005.x.
   PubMedGoogle Scholar
• Cabezas R, à vila M, Gonzalez J, El-Bachá RS, Bã¡ez E, GarcÃ-a-Segura LM, Jurado Coronel JC, Capani F, Cardona-Gomez GP, Barreto GE, et al. Astrocytic modulation of blood brain barrier: perspectives on Parkinson’s disease. Front Cell Neurosci. 2014;8(211). doi:10.3389/fncel.2014.00211
   PubMedGoogle Scholar
• Meyer K, Lulla A, Debroy K, Shikany JM, Yaffe K, Meirelles O, Launer LJ. Association of the gut microbiota with cognitive function in midlife. JAMA Netw Open. 2022;5(e2143941). doi:10.1001/jamanetworkopen.2021.43941.
   Google Scholar
• Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, et al. Synaptic pruning by microglia is necessary for normal brain development. Science. 2011;333(1456–1458). doi:10.1126/science.1202529
   PubMedGoogle Scholar
• Zhao Q, Dai W, Chen HY, Jacobs RE, Zlokovic BV, Lund BT, Montagne A, Bonnin A. Prenatal disruption of blood-brain barrier formation via cyclooxygenase activation leads to lifelong brain inflammation. Proc Natl Acad Sci U S A. 2022;119(e2113310119). doi:10.1073/pnas.2113310119
   Google Scholar
• Kim EA, Ae Kim J, Park MH, Jung SC, Suh SH, Pang M-G, Kim YJ. Lysophosphatidylcholine induces endothelial cell injury by nitric oxide production through oxidative stress. J Matern Fetal Neonatal Med. 2009;22(325–331). doi:10.1080/14767050802556075.
   Google Scholar
• Wahlstrom A, Sayin SI, Marschall HU, Backhed F. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 2016;24(41–50). doi:10.1016/j.cmet.2016.05.005.
   PubMedGoogle Scholar
• Bile MA. Acids as key modulators of the brain-gut-microbiota axis in Alzheimer’s disease. J Alzheimers Dis. 2021;84(461–477). doi:10.3233/JAD-210608.
   Google Scholar
• Mertens KL, Kalsbeek A, Soeters MR, Eggink HM. Bile acid signaling pathways from the enterohepatic circulation to the central nervous system. Front Neurosci. 2017;11(617). doi:10.3389/fnins.2017.00617.
   Google Scholar
• Monteiro-Cardoso VF, Corliano M, Singaraja RR. Bile acids: a communication channel in the gut-brain axis. Neuromolecular Med. 2021;23(99–117). doi:10.1007/s12017-020-08625-z.
   PubMedGoogle Scholar
• Quinn M, McMillin M, Galindo C, Frampton G, Pae HY, DeMorrow S. Bile acids permeabilize the blood brain barrier after bile duct ligation in rats via Rac1-dependent mechanisms. Dig Liver Dis. 2014;46(527–534). doi:10.1016/j.dld.2014.01.159.
   PubMedGoogle Scholar
• Palmela I, Correia L, Silva RFM, Sasaki H, Kim KS, Brites D, Brito MA. Hydrophilic bile acids protect human blood-brain barrier endothelial cells from disruption by unconjugated bilirubin: an in vitro study. Front Neurosci. 2015;9(80). doi:10.3389/fnins.2015.00080.
   PubMedGoogle Scholar
• Yanguas-Casas N, Barreda-Manso MA, Nieto-Sampedro M, Romero-Ramirez L. TUDCA: an agonist of the bile acid receptor GPBAR1/TGR5 with anti-inflammatory effects in microglial cells. J Cell Physiol. 2017;232(2231–2245). doi:10.1002/jcp.25742.
   Google Scholar
• Varian BJ, Poutahidis T, DiBenedictis BT, Levkovich T, Ibrahim Y, Didyk E, Shikhman L, Cheung HK, Hardas A, Ricciardi CE, et al. Microbial lysate upregulates host oxytocin. Brain Behav Immun. 2017;61(36–49). doi:10.1016/j.bbi.2016.11.002
   PubMedGoogle Scholar
• Sgritta M, Dooling SW, Buffington SA, Momin EN, Francis MB, Britton RA, Costa-Mattioli M. Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron. 2019;101:246–259 e246. doi:10.1016/j.neuron.2018.11.018.
   PubMed Web of Science ®Google Scholar
• Yamamoto Y, Higashida H. RAGE regulates oxytocin transport into the brain. Commun Biol. 2020;3(70). doi:10.1038/s42003-020-0799-2.
   Google Scholar
• Frick KM, Burlingame LA, Arters JA, Berger-Sweeney J. Reference memory, anxiety and estrous cyclicity in C57BL/6NIA mice are affected by age and sex. Neuroscience. 2000;95(293–307). doi:10.1016/s0306-4522(99)00418-2.
   PubMedGoogle Scholar
• Voikar V, Koks S, Vasar E, Rauvala H. Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol Behav. 2001;72(271–281). doi:10.1016/s0031-9384(00)00405-4.
   PubMedGoogle Scholar
• Tucker LB, Fu AH, McCabe JT. Performance of male and female C57BL/6J mice on motor and cognitive tasks commonly used in pre-clinical traumatic brain injury research. J Neurotrauma. 2016;33(880–894). doi:10.1089/neu.2015.3977.
   PubMedGoogle Scholar
• Jonasson Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci Biobehav Rev. 2005;28(811–825). doi:10.1016/j.neubiorev.2004.10.006.
   PubMedGoogle Scholar
• Baldan Ramsey LC, Pittenger C. Cued and spatial learning in the water maze: equivalent learning in male and female mice. Neurosci Lett. 2010;483(148–151). doi:10.1016/j.neulet.2010.07.082.
   PubMedGoogle Scholar
• An XL, Zou J-X, WU R-Y, YANG Y, TAI F-D, Zeng S-Y, Jia R, Zhang X, LIU E-Q, Broders H, et al. Strain and sex differences in anxiety-like and social behaviors in C57BL/6J and BALB/cJ mice. Exp Anim. 2011;60(111–123). doi:10.1538/expanim.60.111.
   PubMedGoogle Scholar
• Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, Piven J, Crawley JN. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 2004;3(287–302). doi:10.1111/j.1601-1848.2004.00076.x.
   Google Scholar
• Krishna M, Engevik M, Queliza K, Britto S, Shah R, Ruan W, Wang H, Versalovic J, Kellermayer R. Maternal Lactobacillus reuteri supplementation shifts the intestinal microbiome in mice and provides protection from experimental colitis in female offspring. FASEB Bioadv. 2022;4(109–120). doi:10.1096/fba.2021-00078
   PubMedGoogle Scholar
• Pluskal T, Castillo S, Villar-Briones A, Oresic M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinform. 2010;11(395). doi:10.1186/1471-2105-11-395.
   PubMedGoogle Scholar
• Nothias LF, Petras D, Schmid R, Duhrkop K, Rainer J, Sarvepalli A, Protsyuk I, Ernst M, Tsugawa H, Fleischauer M, Aicheler F et al. Feature-based molecular networking in the GNPS analysis environment. Nat Methods. 2020;17(905–908). doi:10.1038/s41592-020-0933-6
   Google Scholar
• Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, Nguyen DD, Watrous J, Kapono CA, Luzzatto-Knaan T et al. Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat Biotechnol. 2016;34(828–837). doi:10.1038/nbt.3597
   Google Scholar
• Pang Z, Chong J, Zhou G, de Lima Morais DA, Chang L, Barrette M, Gauthier C, Jacques PE, Li S, Xia J. MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 2021;49:W388–W396. doi:10.1093/nar/gkab382.
   PubMed Web of Science ®Google Scholar