Cited by 207

Modulation of Intestinal Microbiota by the Probiotic VSL#3 Resets Brain Gene Expression and Ameliorates the Age-Related Deficit in LTP

Distrutti, Eleonora, O’Reilly, Julie-Ann, McDonald, Claire, Cipriani, Sabrina, Renga, Barbara, Lynch, Marina A., Fiorucci, Stefano·2014·PLoS ONE

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0106503

Cites

8 of 8 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • VSL#3 acts as an anti-inflammatory in the mouse gut, mirrored in the brain by a reduction in CD11b and CD68 mRNA expression in the hippocampus in VSL#3-treated aged rats.

    “This is consistent with the fact that VSL#3 acted as an anti-inflammatory in the mouse gut, which was mirrored in the brain, as noted by a reduction in CD11b and CD68 mRNA expression (two markers of microglial activation) in the hippocampus in VSL#3-treated aged rats (Distrutti et al., 2014).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Distrutti et al., 2014

  • VSL#3 increases hippocampal BDNF and synapsin expression, suggesting a neuro-synaptotrophic effect.

    “Here, they witnessed an increase in hippocampal BDNF and synapsin expression, suggesting that VSL#3 exerted a neuro-synaptotrophic effect.”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Distrutti et al., 2014

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 61

  1. [1]Lynch MA (2010) Age-related neuroinflammatory changes negatively impact on neuronal function. Front Aging Neurosci 1: 6. 20552057 PMC2874409
  2. [2]Lynch MA (2004) Long-term potentiation and memory. Physiological Reviews 84: 87– 136. 14715912
  3. [3]Kelly L, Grehan B, Chiesa AD, O′Mara SM, Downer E, et al (2011) The polyunsaturated fatty acids, EPA and DPA exert a protective effect in the hippocampus of the aged rat. Neurobiol Aging 32: 2318 e2311– 2315. 20570403
  4. [4]Clarke RM, Lyons A, O′Connell F, Deighan BF, Barry CE, et al (2008) A pivotal role for interleukin-4 in atorvastatin-associated neuroprotection in rat brain. J Biol Chem 283: 1808– 1817. 17981803
  5. [5]Moore M, Piazza A, Nolan Y, Lynch MA (2007) Treatment with dexamethasone and vitamin D3 attenuates neuroinflammatory age-related changes in rat hippocampus. Synapse 61: 851– 861. 17621647
  6. [6]Moore ME, Piazza A, McCartney Y, Lynch MA (2005) Evidence that vitamin D3 reverses age-related inflammatory changes in the rat hippocampus. Biochem Soc Trans 33: 573– 577. 16042547
  7. [7]Taliaz D, Stall N, Dar DE, Zangen A (2010) Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 15: 80– 92. 19621014 PMC2834321
  8. [8]O′Callaghan RM, Griffin EW, Kelly AM (2009) Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus 19: 1019– 1029. 19309034
  9. [9]Rex CS, Lauterborn JC, Lin CY, Kramar EA, Rogers GA, et al (2006) Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J Neurophysiol 96: 677– 685. 16707719 PMC1554892
  10. [10]Dantzer R, Kelley KW (2007) Twenty years of research on cytokine-induced sickness behavior. Brain Behav Immun 21: 153– 160. 17088043 PMC1850954
  11. [11]Godbout JP, Chen J, Abraham J, Richwine AF, Berg BM, et al (2005) Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. Faseb J 19: 1329– 1331. 15919760
  12. [12]Honjo K, van Reekum R, Verhoeff NP (2009) Alzheimer's disease and infection: do infectious agents contribute to progression of Alzheimer's disease? Alzheimers Dement 5: 348– 360. 19560105
  13. [13]Simpson S Jr, Taylor B, Dwyer DE, Taylor J, Blizzard L, et al (2012) Anti-HHV-6 IgG titer significantly predicts subsequent relapse risk in multiple sclerosis. Mult Scler 18: 799– 806. 22084489
  14. [14]Reber SO (2012) Stress and animal models of inflammatory bowel disease—an update on the role of the hypothalamo-pituitary-adrenal axis. Psychoneuroendocrinology 37: 1– 19. 21741177
  15. [15]Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nature Reviews Neuroscience 13: 701– 712. 22968153
  16. [16]O′Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, et al (2009) Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65: 263– 267. 18723164
  17. [17]Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ (2007) Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32: 256– 266. 17307298
  18. [19]Wang L, Jiao J, Dulawa SC (2011) Infant maternal separation impairs adult cognitive performance in BALB/cJ mice. Psychopharmacology 216: 207– 218. 21331521
  19. [21]Evrard B, Coudeyras S, Dosgilbert A, Charbonnel N, Alame J, et al (2011) Dose-dependent immunomodulation of human dendritic cells by the probiotic Lactobacillus rhamnosus Lcr35. PLoS One 6: e18735. 21533162 PMC3078917
  20. [22]Lin YP, Thibodeaux CH, Pena JA, Ferry GD, Versalovic J (2008) Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflammatory bowel diseases 14: 1068– 1083. 18425802
  21. [23]Mencarelli A, Distrutti E, Renga B, D′Amore C, Cipriani S, et al (2011) Probiotics modulate intestinal expression of nuclear receptor and provide counter-regulatory signals to inflammation-driven adipose tissue activation. PLoS One 6: e22978. 21829567 PMC3146529
  22. [24]Dai C, Zheng CQ, Meng FJ, Zhou Z, Sang LX, et al (2013) VSL#3 probiotics exerts the anti-inflammatory activity via PI3k/Akt and NF-kappaB pathway in rat model of DSS-induced colitis. Mol Cell Biochem 374: 1– 11. 23271629
  23. [25]Reiff C, Delday M, Rucklidge G, Reid M, Duncan G, et al (2009) Balancing inflammatory, lipid, and xenobiotic signaling pathways by VSL#3, a biotherapeutic agent, in the treatment of inflammatory bowel disease. Inflammatory Bowel Diseases 15: 1721– 1736. 19639558
  24. [27]Mimura T, Rizzello F, Helwig U, Poggioli G, Schreiber S, et al (2004) Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut 53: 108– 114. 14684584 PMC1773918
  25. [28]Kim HJ, Camilleri M, McKinzie S, Lempke MB, Burton DD, et al (2003) A randomized controlled trial of a probiotic, VSL#3, on gut transit and symptoms in diarrhoea-predominant irritable bowel syndrome. Alimentary Pharmacology &Therapeutics 17: 895– 904. 12656692
  26. [29]Dharmani P, De Simone C, Chadee K (2013) The probiotic mixture VSL#3 accelerates gastric ulcer healing by stimulating vascular endothelial growth factor. PLoS One 8: e58671. 23484048 PMC3590171
  27. [31]Costello DA, Watson MB, Cowley TR, Murphy N, Murphy Royal C, et al (2011) Interleukin-1alpha and HMGB1 mediate hippocampal dysfunction in SIGIRR-deficient mice. J Neurosci 31: 3871– 3879. 21389242 PMC6622806
  28. [32]Lyons A, Murphy KJ, Clarke R, Lynch MA (2011) Atorvastatin prevents age-related and amyloid-beta-induced microglial activation by blocking interferon-gamma release from natural killer cells in the brain. J Neuroinflammation 8: 27. 21453520 PMC3077319
  29. [33]Lyons A, Griffin RJ, Costelloe CE, Clarke RM, Lynch MA (2007) IL-4 attenuates the neuroinflammation induced by amyloid-betain vivo and in vitro. J Neurochem 101: 771– 781. 17250684
  30. [34]Benno Y, Nakao H, Uchida K, Mitsuoka T (1992) Impact of the advances in age on the gastrointestinal microflora of Beagle dogs. J Vet Med Sci 54: 703– 706. 1391181
  31. [35]Hopkins MJ, Sharp R, Macfarlane GT (2001) Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles. Gut 48: 198– 205. 11156640 PMC1728209
  32. [36]Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, et al (2012) Human gut microbiome viewed across age and geography. Nature 486: 222– 227. 22699611 PMC3376388
  33. [37]Ewaschuk J, Endersby R, Thiel D, Diaz H, Backer J, et al (2007) Probiotic bacteria prevent hepatic damage and maintain colonic barrier function in a mouse model of sepsis. Hepatology 46: 841– 850. 17659579
  34. [38]Jobin C (2010) Probiotics and ileitis: could augmentation of TNF/NFκB activity be the answer? Gut Microbes 1: 196– 9. 21327025 PMC3023599
  35. [39]Claes IJ, De Keersmaecker SC, Vanderleyden J, Lebeer S (2011) Lessons from probiotic-host interaction studies in murine models of experimental colitis. Mol Nutr Food Res 55: 1441– 53. 21796777
  36. [41]Viladomiu M, Hontecillas R, Yuan L, Lu P, Bassaganya-Riera J (2013) Nutritional protective mechanisms against gut inflammation. J Nutr Biochem 24: 929– 39. 23541470 PMC3730123
  37. [42]Qiu X, Zhang M, Yang X, Hong N, Yu C (2013) Faecali bacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. J Crohn Colitis 7: e558– 68. 23643066
  38. [43]Mamdani F, Berlim MT, Beaulieu MM, Labbe A, Merette C, et al (2011) Gene expression biomarkers of response to citalopram treatment in major depressive disorder. Transl Psychiatry 1: e13. 22832429 PMC3309465
  39. [44]Baba H, Nakahira K, Morita N, Tanaka F, Akita H, et al (1997) GFAP gene expression during development of astrocyte. Dev Neurosci 19: 49– 57. 9078433
  40. [45]Martínez-García A, Sastre I, Recuero M, Aldudo J, Vilella E, et al (2010) PLA2G3, a gene involved in oxidative stress induced death, is associated with Alzheimer's disease. J Alzheimers Dis 22: 1181– 1187. 20930276
  41. [46]Rosenthal SL, Wang X, Demirci FY, Barmada MM, Ganguli M, et al (2012) Beta-amyloid toxicity modifier genes and the risk of Alzheimer's disease. Am J Neurodegener Dis 1: 191– 198. 22984654 PMC3560458
  42. [47]Bhatia S, Knoch B, Wong J, Kim WS, Else PL, et al (2012) Selective reduction of hydroperoxyeicosatetraenoic acids to their hydroxy derivatives by apolipoprotein D: implications for lipid antioxidant activity and Alzheimer's disease. Biochem J 442: 713– 721. 22150111
  43. [48]Glezer I, Lapointe A, Rivest S (2006) Innate immunity triggers oligodendrocyte progenitor reactivity and confines damages to brain injuries. FASEB J 20: 750– 752. 16464958
  44. [49]Khorooshi R, Owens T (2010) Injury-induced type I IFN signaling regulates inflammatory responses in the central nervous system. Immunol 185: 1258– 1264. 20562259
  45. [50]Hawkes CA, Gatherer M, Sharp MM, Dorr A, Yuen HM, et al (2013) Regional differences in the morphological and functional effects of aging on cerebral basement membranes and perivascular drainage of amyloid-β from the mouse brain. Aging Cell 12: 224– 236. 23413811
  46. [51]Yamada K, Santo-Yamada Y, Wada K (2003) Stress-induced impairment of inhibitory avoidance learning in female neuromedin B receptor-deficient mice. Physiol Behav 78: 303– 309. 12576129
  47. [52]Zhao Y, Bhattacharjee S, Jones BM, Hill J, Dua P, et al (2013) Regulation of Neurotropic Signaling by the Inducible, NF-kB-Sensitive miRNA-125b in Alzheimer's Disease (AD) and in Primary Human Neuronal-Glial (HNG). Cells Mol Neurobiol: Nov 29 PMC4038663 24293102
  48. [54]BorovikovaLV, Ivanova S, Zhang M, Yang H, Botchkina GI, et al (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405: 458– 462. 10839541
  49. [55]Holmes E, Li JV, Marchesi JR, Nicholson JK (2012) Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab 16: 559– 64. 23140640
  50. [56]Kumar A (2011) Long-Term Potentiation at CA3-CA1 Hippocampal Synapses with Special Emphasis on Aging, Disease, and Stress. Front Aging Neurosci 3: 7. 21647396 PMC3102214
  51. [57]Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7: 30– 40. 16371948
  52. [58]Griffin R, Nally R, Nolan Y, McCartney Y, Linden J, et al (2006) The age-related attenuation in long-term potentiation is associated with microglial activation. J Neurochem 99: 1263– 1272. 16981890
  53. [59]Lynch AM, Loane DJ, Minogue AM, Clarke RM, Kilroy D, et al (2007) Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus. Neurobiol Aging 28: 845– 855. 16714069
  54. [60]Loane DJ, Deighan BF, Clarke RM, Griffin RJ, Lynch AM, et al (2009) Interleukin-4 mediates the neuroprotective effects of rosiglitazone in the aged brain. Neurobiol Aging 30: 920– 931. 17950491
  55. [61]Reiff C, Delday M, Rucklidge G, Reid M, Duncan G, et al (2009) Balancing inflammatory, lipid, and xenobiotic signaling pathways by VSL#3, a biotherapeutic agent, in the treatment of inflammatory bowel disease. Inflamm Bowel Dis 15: 1721– 36. 19639558
  56. [62]Dai C, Zheng CQ, Meng FJ, Zhou Z, Sang LX, et al (2013) VSL#3 probiotics exerts the anti-inflammatory activity via PI3k/Akt and NF-κB pathway in rat model of DSS-induced colitis. Mol Cell Biochem 374: 1– 11. 23271629
  57. [64]Bajaj JS, Hylemon PB, Ridlon JM, Heuman DM, Daita K, et al (2012) Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am J Physiol Gastrointest Liver Physiol 303: G675– 685. 22821944 PMC3468538
  58. [66]Taliaz D, Stall N, Dar DE, Zangen A (2010) Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 15: 80– 92. 19621014 PMC2834321
  59. [67]Cunha C, Brambilla R, Thomas KL (2010) A simple role for BDNF in learning and memory? Front Molecular Neurosci 3: 1. PMC2821174 20162032
  60. [68]O′Callaghan RM, Griffin EW, Kelly AM (2009) Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus 19: 1019– 1029. 19309034
  61. [69]Rex CS, Lauterborn JC, Lin CY, Kramar EA, Rogers GA, et al (2006) Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J Neurophysiol 96: 677– 685. 16707719 PMC1554892

Cited by

Sorted by citations

Authors
Distrutti, E., O’Reilly, J.-A., McDonald, C., Cipriani, S., Renga, B., Lynch, M. A., & Fiorucci, S.
Venue
PLoS ONE
Published
2014-09-09
Volume
9
Issue
9
Pages
e106503
ISSN
1932-6203
Cited by
207
References
8
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review