Visceral sensitivity modulation by faecal microbiota transplantation: the active role of gut bacteria in pain persistence.


Journal

Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686

Informations de publication

Date de publication:
01 05 2022
Historique:
received: 15 03 2021
accepted: 02 08 2021
pubmed: 17 8 2021
medline: 20 4 2022
entrez: 16 8 2021
Statut: ppublish

Résumé

Recent findings linked gastrointestinal disorders characterized by abdominal pain to gut microbiota composition. The present work aimed to evaluate the power of gut microbiota as a visceral pain modulator and, consequently, the relevance of its manipulation as a therapeutic option in reversing postinflammatory visceral pain persistence. Colitis was induced in mice by intrarectally injecting 2,4-dinitrobenzenesulfonic acid (DNBS). The effect of faecal microbiota transplantation from viscerally hypersensitive DNBS-treated and naive donors was evaluated in control rats after an antibiotic-mediated microbiota depletion. Faecal microbiota transplantation from DNBS donors induced a long-lasting visceral hypersensitivity in control rats. Pain threshold trend correlated with major modifications in the composition of gut microbiota and short chain fatty acids. By contrast, no significant alterations of colon histology, permeability, and monoamines levels were detected. Finally, by manipulating the gut microbiota of DNBS-treated animals, a counteraction of persistent visceral pain was achieved. The present results provide novel insights into the relationship between intestinal microbiota and visceral hypersensitivity, highlighting the therapeutic potential of microbiota-targeted interventions.

Identifiants

pubmed: 34393197
doi: 10.1097/j.pain.0000000000002438
pii: 00006396-202205000-00010
pmc: PMC9009324
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

861-877

Informations de copyright

Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the International Association for the Study of Pain.

Références

Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe 2018;23:716–24.
Antonioli L, Fornai M, Colucci R, Awwad O, Ghisu N, Tuccori M, Del Tacca M, Blandizzi C. Differential recruitment of high affinity A1 and A2A adenosine receptors in the control of colonic neuromuscular function in experimental colitis. Eur J Pharmacol 2011;650:639–49.
Antonioli L, Fornai M, Colucci R, Ghisu N, Da Settimo F, Natale G, Kastsiuchenka O, Duranti E, Virdis A, Vassalle C, La Motta C, Mugnaini L, Breschi MC, Blandizzi C, Del Taca M. Inhibition of adenosine deaminase attenuates inflammation in experimental colitis. J Pharmacol Exp Ther 2007;322:435–42.
Banasiewicz T, Krokowicz L, Stojcev Z, Kaczmarek BF, Kaczmarek E, Maik J, Marciniak R, Krokowicz P, Walkowiak J, Drews M. Microencapsulated sodium butyrate reduces the frequency of abdominal pain in patients with irritable bowel syndrome. Colorectal Dis 2013;15:204–9.
Bandyopadhyaya A, Rajagopalan DR, Rath NP, Herrold A, Rajagopalan R, Napier TC, Tedford CE, Rajagopalan P. The synthesis and receptor binding affinities of DDD-016, a novel, potential, atypical antipsychotic. Medchemcomm 2012;3:580–3.
Bannister K, Dickenson AH. What do monoamines do in pain modulation? Curr Opin Support Palliat Care 2016;10:143–8.
Basso L, Benamar M, Mas-Orea X, Deraison C, Blanpied C, Cenac N, Saoudi A, Dietrich G. Endogenous control of inflammatory visceral pain by T cell-derived opioids in IL-10-deficient mice. Neurogastroenterol Motil 2020;32:e13743.
Bennet SM, Polster A, Törnblom H, Isaksson S, Capronnier S, Tessier A, Le Nevé B, Simrén M, Öhman L. Global cytokine profiles and association with clinical characteristics in patients with irritable bowel syndrome. Am J Gastroenterol 2016;111:1165–76.
Blumberg RS, Saubermann LJ, Strober W. Animal models of mucosal inflammation and their relation to human inflammatory bowel disease. Curr Opin Immunol 1999;11:648–56.
Boccella S, Guida F, De Logu F, De Gregorio D, Mazzitelli M, Belardo C, Iannotta M, Serra N, Nassini R, de Novellis V, Geppetti P, Maione S, Luongo L. Ketones and pain: unexplored role of hydroxyl carboxylic acid receptor type 2 in the pathophysiology of neuropathic pain. FASEB J 2019;33:1062–73.
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodriguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS II, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vazquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019;37:852–7.
Bravo L, Llorca-Torralba M, Berrocoso E, Micó JA. Monoamines as drug targets in chronic pain: focusing on neuropathic pain. Front Neurosci 2019;13:1268.
Buhner S, Li Q, Vignali S, Barbara G, De Giorgio R, Stanghellini V, Cremon C, Zeller F, Langer R, Daniel H, Michel K, Schemann M. Activation of human enteric neurons by supernatants of colonic biopsy specimens from patients with irritable bowel syndrome. Gastroenterology 2009;137:1425–34.
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 2016;13:581–3.
Camilleri M, Boeckxstaens G. Dietary and pharmacological treatment of abdominal pain in IBS. Gut 2017;66:966–74.
Cammarota G, Ianiro G, Tilg H, Rajilic-Stojanovic M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart A, Segal J, Aloi M, Masucci L, Molinaro A, Scaldaferri F, Gasbarrini G, Lopez-Sanroman A, Link A, de Groot P, de Vos WM, Hogenauer C, Malfertheiner P, Mattila E, Milosavljevic T, Nieuwdorp M, Sanguinetti M, Simren M, Gasbarrini A. European consensus conference on faecal microbiota transplantation in clinical practice. Gut 2017;66:569–80.
Cani PD. Human gut microbiome: hopes, threats and promises. Gut 2018;67:1716–25.
Chen H, Assmann JC, Krenz A, Rahman M, Grimm M, Karsten CM, Köhl J, Offermanns S, Wettschureck N, Schwaninger M. Hydroxycarboxylic acid receptor 2 mediates dimethyl fumarate's protective effect in EAE. J Clin Invest 2014;124:2188–92.
Chen Y, Lin C, Tang Y, Chen A-Q, Liu C-Y, Lu D-L. ZD 7288, an HCN channel blocker, attenuates chronic visceral pain in irritable bowel syndrome-like rats. World J Gastroenterol 2014;20:2091–7.
Chen Y, Xiao S, Gong Z, Zhu X, Yang Q, Li Y, Gao S, Dong Y, Shi Z, Wang Y, Weng X, Li Q, Cai W, Qiang W. Wuji Wan formula ameliorates diarrhea and disordered colonic motility in post-inflammation irritable bowel syndrome rats by modulating the gut microbiota. Front Microbiol 2017;8:2307–.
Choghakhori R, Abbasnezhad A, Hasanvand A, Amani R. Inflammatory cytokines and oxidative stress biomarkers in irritable bowel syndrome: association with digestive symptoms and quality of life. Cytokine 2017;93:34–43.
Christianson JA, Gebhart GF. Assessment of colon sensitivity by luminal distension in mice. Nat Protoc 2007;2:2624–31.
Contijoch EJ, Britton GJ, Yang C, Mogno I, Li Z, Ng R, Llewellyn SR, Hira S, Johnson C, Rabinowitz KM, Barkan R, Dotan I, Hirten RP, Fu SC, Luo Y, Yang N, Luong T, Labrias PR, Lira S, Peter I, Grinspan A, Clemente JC, Kosoy R, Kim-Schulze S, Qin X, Castillo A, Hurley A, Atreja A, Rogers J, Fasihuddin F, Saliaj M, Nolan A, Reyes-Mercedes P, Rodriguez C, Aly S, Santa-Cruz K, Peters L, Suarez-Farinas M, Huang R, Hao K, Zhu J, Zhang B, Losic B, Irizar H, Song WM, Di Narzo A, Wang W, Cohen BL, DiMaio C, Greenwald D, Itzkowitz S, Lucas A, Marion J, Maser E, Ungaro R, Naymagon S, Novak J, Shah B, Ullman T, Rubin P, George J, Legnani P, Telesco SE, Friedman JR, Brodmerkel C, Plevy S, Cho JH, Colombel JF, Schadt EE, Argmann C, Dubinsky M, Kasarskis A, Sands B, Faith JJ. Gut microbiota density influences host physiology and is shaped by host and microbial factors. Elife 2019;8:e40553.
Crouzet L, Gaultier E, Del'Homme C, Cartier C, Delmas E, Dapoigny M, Fioramonti J, Bernalier-Donadille A. The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota. Neurogastroenterol Motil 2013;25:e272–82.
Cruz-Aguliar RM, Wantia N, Clavel T, Vehreschild MJ, Buch T, Bajbouj M, Haller D, Busch D, Schmid RM, Stein-Thoeringer CK. An open-labeled study on fecal microbiota transfer in irritable bowel syndrome patients reveals improvement in abdominal pain associated with the relative abundance of Akkermansia muciniphila. Digestion 2019;100:127–38.
Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012;13:701–12.
Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, Kayser BD, Levenez F, Chilloux J, Hoyles L, Dumas ME, Rizkalla SW, Dore J, Cani PD, Clement K. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 2016;65:426–36.
Derrien M, Belzer C, de Vos WM. Akkermansia muciniphila and its role in regulating host functions. Microb Pathog 2017;106:171–81.
El-Salhy M, Hausken T, Hatlebakk JG. Increasing the dose and/or repeating faecal microbiota transplantation (FMT) increases the response in patients with irritable bowel syndrome (IBS). Nutrients 2019;11:1415.
Esquerre N, Basso L, Defaye M, Vicentini FA, Cluny N, Bihan D, Hirota SA, Schick A, Jijon HB, Lewis IA, Geuking MB, Sharkey KA, Altier C, Nasser Y. Colitis-induced microbial perturbation promotes postinflammatory visceral hypersensitivity. Cell Mol Gastroenterol Hepatol 2020;10:225–44.
Fasano A. Intestinal permeability and its regulation by zonulin: diagnostic and therapeutic implications. Clin Gastroenterol Hepatol 2012;10:1096–100.
Foster JA, Rinaman L, Cryan JF. Stress & the gut-brain axis: regulation by the microbiome. Neurobiol Stress 2017;7:124–36.
Franzosa EA, Sirota-Madi A, Avila-Pacheco J, Fornelos N, Haiser HJ, Reinker S, Vatanen T, Hall AB, Mallick H, McIver LJ, Sauk JS, Wilson RG, Stevens BW, Scott JM, Pierce K, Deik AA, Bullock K, Imhann F, Porter JA, Zhernakova A, Fu J, Weersma RK, Wijmenga C, Clish CB, Vlamakis H, Huttenhower C, Xavier RJ. Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nat Microbiol 2019;4:293–305.
Fung TC. The microbiota-immune axis as a central mediator of gut-brain communication. Neurobiol Dis 2020;136:104714.
Fung TC, Vuong HE, Luna CDG, Pronovost GN, Aleksandrova AA, Riley NG, Vavilina A, McGinn J, Rendon T, Forrest LR, Hsiao EY. Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut. Nat Microbiol 2019;4:2064–73.
Gonçalves dos Santos G, Delay L, Yaksh TL, Corr M. Neuraxial cytokines in pain states. Front Immunol 2020;10:3061.
Goyal N, Rana A, Ahlawat A, Bijjem KRV, Kumar P. Animal models of inflammatory bowel disease: a review. Inflammopharmacology 2014;22:219–33.
Greenwood-Van Meerveld B, Prusator DK, Johnson AC. Animal models of gastrointestinal and liver diseases. Animal models of visceral pain: pathophysiology, translational relevance, and challenges. Am J Physiol Gastrointest Liver Physiol 2015;308:G885–903.
Gu L, Ding C, Tian H, Yang B, Zhang X, Hua Y, Zhu Y, Gong J, Zhu W, Li J, Li N. Serial frozen fecal microbiota transplantation in the treatment of chronic intestinal pseudo-obstruction: a preliminary study. J Neurogastroenterol Motil 2017;23:289–97.
Guida F, Boccella S, Belardo C, Iannotta M, Piscitelli F, De Filippis F, Paino S, Ricciardi F, Siniscalco D, Marabese I, Luongo L, Ercolini D, Di Marzo V, Maione S. Altered gut microbiota and endocannabinoid system tone in vitamin D deficiency-mediated chronic pain. Brain Behav Immun 2020;85:128–41.
Guida F, Turco F, Iannotta M, De Gregorio D, Palumbo I, Sarnelli G, Furiano A, Napolitano F, Boccella S, Luongo L, Mazzitelli M, Usiello A, De Filippis F, Iannotti FA, Piscitelli F, Ercolini D, de Novellis V, Di Marzo V, Cuomo R, Maione S. Antibiotic-induced microbiota perturbation causes gut endocannabinoidome changes, hippocampal neuroglial reorganization and depression in mice. Brain Behav Immun 2018;67:230–45.
Hadizadeh F, Bonfiglio F, Belheouane M, Vallier M, Sauer S, Bang C, Bujanda L, Andreasson A, Agreus L, Engstrand L, Talley NJ, Rafter J, Baines JF, Walter S, Franke A, D'Amato M. Faecal microbiota composition associates with abdominal pain in the general population. Gut 2018;67:778–9.
Hernández-Chirlaque C, Aranda CJ, Ocón B, Capitán-Cañadas F, Ortega-González M, Carrero JJ, Suárez MD, Zarzuelo A, Sánchez de Medina F, Martínez-Augustin O. Germ-free and antibiotic-treated mice are highly susceptible to epithelial injury in DSS colitis. J Crohns Colitis 2016;10:1324–35.
Hevia A, Bernardo D, Montalvillo E, Al-Hassi HO, Fernandez-Salazar L, Garrote JA, Milani C, Ventura M, Arranz E, Knight SC, Margolles A, Sanchez B. Human colon-derived soluble factors modulate gut microbiota composition. Front Oncol 2015;5:86.
Hoban AE, Moloney RD, Golubeva AV, McVey Neufeld KA, O'Sullivan O, Patterson E, Stanton C, Dinan TG, Clarke G, Cryan JF. Behavioural and neurochemical consequences of chronic gut microbiota depletion during adulthood in the rat. Neuroscience 2016;339:463–77.
Huda-Faujan N, Abdulamir AS, Fatimah AB, Anas OM, Shuhaimi M, Yazid AM, Loong YY. The impact of the level of the intestinal short chain fatty acids in inflammatory bowel disease patients versus healthy subjects. Open Biochem J 2010;4:53–8.
Hyland NP, Quigley EMM, Brint E. Microbiota-host interactions in irritable bowel syndrome: epithelial barrier, immune regulation and brain-gut interactions. World J Gastroenterol 2014;20:8859–66.
Iversen L. Biochemistry of biogenic amines. Vol. 3. New York and Philadelphia: Springer Science & Business Media, 2013.
Kamada N, Chen GY, Inohara N, Nunez G. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol 2013;14:685–90.
Kannampalli P, Shaker R, Sengupta JN. Colonic butyrate- algesic or analgesic? Neurogastroenterol Motil 2011;23:975–9.
Kavelaars A, Heijnen CJ. T cells as guardians of pain resolution. Trends Mol Med 2021;27:302–13.
Khan KJ, Ullman TA, Ford AC, Abreu MT, Abadir A, Marshall JK, Talley NJ, Moayyedi P. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol 2011;106:661–73.
Kiesler P, Fuss IJ, Strober W. Experimental models of inflammatory bowel diseases. Cell Mol Gastroenterol Hepatol 2015;1:154–70.
Klem F, Wadhwa A, Prokop LJ, Sundt WJ, Farrugia G, Camilleri M, Singh S, Grover M. Prevalence, risk factors, and outcomes of irritable bowel syndrome after infectious enteritis: a systematic review and meta-analysis. Gastroenterology 2017;152:1042–54.e1.
Laumet G, Bavencoffe A, Edralin JD, Huo XJ, Walters ET, Dantzer R, Heijnen CJ, Kavelaars A. Interleukin-10 resolves pain hypersensitivity induced by cisplatin by reversing sensory neuron hyperexcitability. PAIN 2020;161:2344–52.
Li M, van Esch BCAM, Wagenaar GTM, Garssen J, Folkerts G, Henricks PAJ. Pro- and anti-inflammatory effects of short chain fatty acids on immune and endothelial cells. Eur J Pharmacol 2018;831:52–9.
Li S, Hua D, Wang Q, Yang L, Wang X, Luo A, Yang C. The role of bacteria and its derived metabolites in chronic pain and depression: recent findings and research progress. Int J Neuropsychopharmacol 2020;23:26–41.
Li ZS, Schmauss C, Cuenca A, Ratcliffe E, Gershon MD. Physiological modulation of intestinal motility by enteric dopaminergic neurons and the D 2 receptor: analysis of dopamine receptor expression, location, development, and function in wild-type and knock-out mice. J Neurosci 2006;26:2798.
Lucarini E, Parisio C, Branca JJV, Segnani C, Ippolito C, Pellegrini C, Antonioli L, Fornai M, Micheli L, Pacini A, Bernardini N, Blandizzi C, Ghelardini C, Di Cesare Mannelli L. Deepening the mechanisms of visceral pain persistence: an evaluation of the gut-spinal cord relationship. Cells 2020;9:1772.
Luczynski P, Tramullas M, Viola M, Shanahan F, Clarke G, O'Mahony S, Dinan TG, Cryan JF. Microbiota regulates visceral pain in the mouse. Elife 2017;6:e25887.
Macchione IG, Lopetuso LR, Ianiro G, Napoli M, Gibiino G, Rizzatti G, Petito V, Gasbarrini A, Scaldaferri F. Akkermansia muciniphila: key player in metabolic and gastrointestinal disorders. Eur Rev Med Pharmacol Sci 2019;23:8075–83.
Macia L, Tan J, Vieira AT, Leach K, Stanley D, Luong S, Maruya M, Ian McKenzie C, Hijikata A, Wong C, Binge L, Thorburn AN, Chevalier N, Ang C, Marino E, Robert R, Offermanns S, Teixeira MM, Moore RJ, Flavell RA, Fagarasan S, Mackay CR. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat Commun 2015;6:6734.
Martinucci I, Blandizzi C, de Bortoli N, Bellini M, Antonioli L, Tuccori M, Fornai M, Marchi S, Colucci R. Genetics and pharmacogenetics of aminergic transmitter pathways in functional gastrointestinal disorders. Pharmacogenomics 2015;16:523–39.
Mawe GM, Hoffman JM. Serotonin signalling in the gut—functions, dysfunctions and therapeutic targets. Nat Rev Gastroenterol Hepatol 2013;10:473–86.
Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest 2015;125:926–38.
McGrath JC, Lilley E. Implementing guidelines on reporting research using animals (ARRIVE etc.): new requirements for publication in BJP. Br J Pharmacol 2015;172:3189–93.
Mittal R, Debs LH, Patel AP, Nguyen D, Patel K, O'Connor G, Grati M, Mittal J, Yan D, Eshraghi AA, Deo SK, Daunert S, Liu XZ. Neurotransmitters: the critical modulators regulating gut-brain Axis. J Cell Physiol 2017;232:2359–72.
Niccolai E, Baldi S, Ricci F, Russo E, Nannini G, Menicatti M, Poli G, Taddei A, Bartolucci G, Calabrò AS, Stingo FC, Amedei A. Evaluation and comparison of short chain fatty acids composition in gut diseases. World J Gastroenterol 2019;25:5543–58.
Nikolaus S, Schulte B, Al-Massad N, Thieme F, Schulte DM, Bethge J, Rehman A, Tran F, Aden K, Hasler R, Moll N, Schutze G, Schwarz MJ, Waetzig GH, Rosenstiel P, Krawczak M, Szymczak S, Schreiber S. Increased tryptophan metabolism is associated with activity of inflammatory bowel diseases. Gastroenterology 2017;153:1504–16.e2.
O'Mahony SM, Clarke G, Dinan TG, Cryan JF. Early-life adversity and brain development: is the microbiome a missing piece of the puzzle? Neuroscience 2017;342:37–54.
O'Mahony SM, Felice VD, Nally K, Savignac HM, Claesson MJ, Scully P, Woznicki J, Hyland NP, Shanahan F, Quigley EM, Marchesi JR, O'Toole PW, Dinan TG, Cryan JF. Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats. Neuroscience 2014;277:885–901.
Offermanns S, Schwaninger M. Nutritional or pharmacological activation of HCA(2) ameliorates neuroinflammation. Trends Mol Med 2015;21:245–55.
Ouyang J, Lin J, Isnard S, Fombuena B, Peng X, Marette A, Routy B, Messaoudene M, Chen Y, Routy JP. The bacterium Akkermansia muciniphila : a sentinel for gut permeability and its relevance to HIV-related inflammation. Front Immunol 2020;11:645.
Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, Leong RWL, Connor S, Ng W, Paramsothy R, Xuan W, Lin E, Mitchell HM, Borody TJ. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet 2017;389:1218–28.
Parisio C, Lucarini E, Micheli L, Toti A, Di Cesare Mannelli L, Antonini G, Panizzi E, Maidecchi A, Giovagnoni E, Lucci J. Researching new therapeutic approaches for abdominal visceral pain treatment: preclinical effects of an assembled system of molecules of vegetal origin. Nutrients 2020;12:22.
Pfeiffer N, Desmarchelier C, Blaut M, Daniel H, Haller D, Clavel T. Acetatifactor muris gen. nov., sp. nov., a novel bacterium isolated from the intestine of an obese mouse. Arch Microbiol 2012;194:901–7.
Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain–gut–enteric microbiota axis. Nat Rev Gastroenterol Hepatol 2009;6:306.
Rigsbee L, Agans R, Shankar V, Kenche H, Khamis HJ, Michail S, Paliy O. Quantitative profiling of gut microbiota of children with diarrhea-predominant irritable bowel syndrome. Am J Gastroenterol 2012;107:1740–51.
Sartor RB. Genetics and environmental interactions shape the intestinal microbiome to promote inflammatory bowel disease versus mucosal homeostasis. Gastroenterology 2010;139:1816–19.
Skolnick SD, Greig NH. Microbes and monoamines: potential neuropsychiatric consequences of dysbiosis. Trends Neurosci 2019;42:151–63.
Stern EK, Brenner DM. Gut microbiota-based therapies for irritable bowel syndrome. Clin Transl Gastroenterol 2018;9:e134.
Stevens BR, Goel R, Seungbum K, Richards EM, Holbert RC, Pepine CJ, Raizada MK. Increased human intestinal barrier permeability plasma biomarkers zonulin and FABP2 correlated with plasma LPS and altered gut microbiome in anxiety or depression. Gut 2018;67:1555–7.
Strandwitz P. Neurotransmitter modulation by the gut microbiota. Brain Res 2018;1693:128–33.
Vanderwall AG, Milligan ED. Cytokines in pain: harnessing endogenous anti-inflammatory signaling for improved pain management. Front Immunol 2019;10:3009.
Vanhoutvin SA, Troost FJ, Kilkens TO, Lindsey PJ, Hamer HM, Jonkers DM, Venema K, Brummer RJ. The effects of butyrate enemas on visceral perception in healthy volunteers. Neurogastroenterol Motil 2009;21:952-e976.
Verdú EF, Bercik P, Verma-Gandhu M, Huang XX, Blennerhassett P, Jackson W, Mao Y, Wang L, Rochat F, Collins SM. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 2006;55:182–90.
Vieira-Coelho MA, Soares-da-Silva P. Dopamine formation, from its immediate precursor 3,4-dihydroxyphenylalanine, along the rat digestive tract. Fundam Clin Pharmacol 1993;7:235–43.
Vinolo MA, Rodrigues HG, Nachbar RT, Curi R. Regulation of inflammation by short chain fatty acids. Nutrients 2011;3:858–76.
Walker JK, Gainetdinov RR, Mangel AW, Caron MG, Shetzline MA. Mice lacking the dopamine transporter display altered regulation of distal colonic motility. Am J Physiol Gastrointest Liver Physiol 2000;279:G311–8.
Wang P, Du C, Chen F-X, Li C-Q, Yu Y-B, Han T, Akhtar S, Zuo X-L, Tan X-D, Li Y-Q. BDNF contributes to IBS-like colonic hypersensitivity via activating the enteroglia-nerve unit. Sci Rep 2016;6:20320.
Wilson BC, Vatanen T, Cutfield WS, O'Sullivan JM. The super-donor phenomenon in fecal microbiota transplantation. Front Cell Infect Microbiol 2019;9:2.
Wirtz S, Popp V, Kindermann M, Gerlach K, Weigmann B, Fichtner-Feigl S, Neurath MF. Chemically induced mouse models of acute and chronic intestinal inflammation. Nat Protoc 2017;12:1295–309.
Xu D, Chen VL, Steiner CA, Berinstein JA, Eswaran S, Waljee AK, Higgins PDR, Owyang C. Efficacy of fecal microbiota transplantation in irritable bowel syndrome: a systematic review and meta-analysis. Am J Gastroenterol 2019;114:1043–50.
Xue R, Zhang H, Pan J, Du Z, Zhou W, Zhang Z, Tian Z, Zhou R, Bai L. Peripheral dopamine controlled by gut microbes inhibits invariant natural killer T cell-mediated hepatitis. Front Immunol 2018;9:2398.

Auteurs

Elena Lucarini (E)

Department of Neuroscience, Psychology, Drug Research and Child Health, Neurofarba, Pharmacology and Toxicology Section, University of Florence, Florence, Italy.

Vincenzo Di Pilato (V)

Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.
Clinical Microbiology and Virology Unit, Florence Careggi University Hospital, Florence, Italy.
Department of Surgical Sciences and Integrated Diagnostics, University of Genoa, Genoa, Italy.

Carmen Parisio (C)

Department of Neuroscience, Psychology, Drug Research and Child Health, Neurofarba, Pharmacology and Toxicology Section, University of Florence, Florence, Italy.

Laura Micheli (L)

Department of Neuroscience, Psychology, Drug Research and Child Health, Neurofarba, Pharmacology and Toxicology Section, University of Florence, Florence, Italy.

Alessandra Toti (A)

Department of Neuroscience, Psychology, Drug Research and Child Health, Neurofarba, Pharmacology and Toxicology Section, University of Florence, Florence, Italy.

Alessandra Pacini (A)

Department of Experimental and Clinical Medicine, Anatomy and Histology Section, University of Florence, Florence, Italy.

Gianluca Bartolucci (G)

Department of Neurosciences, Psychology, Drug Research and Child Health Section of Pharmaceutical and Nutraceutical Sciences University of Florence, Florence, Italy.

Simone Baldi (S)

Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.

Elena Niccolai (E)

Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.

Amedeo Amedei (A)

Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.

Gian Maria Rossolini (GM)

Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.
Clinical Microbiology and Virology Unit, Florence Careggi University Hospital, Florence, Italy.

Claudio Nicoletti (C)

Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.

John F Cryan (JF)

APC Microbiome Ireland, University College Cork, Cork, Ireland.
Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland.

Siobhain M O'Mahony (SM)

APC Microbiome Ireland, University College Cork, Cork, Ireland.
Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland.

Carla Ghelardini (C)

Department of Neuroscience, Psychology, Drug Research and Child Health, Neurofarba, Pharmacology and Toxicology Section, University of Florence, Florence, Italy.

Lorenzo Di Cesare Mannelli (L)

Department of Neuroscience, Psychology, Drug Research and Child Health, Neurofarba, Pharmacology and Toxicology Section, University of Florence, Florence, Italy.

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