The gut microbiota keeps enteric glial cells on the move; prospective roles of the gut epithelium and immune system

Gut Microbes

Volumn 6, Issue 6, 2015, Pages 398-403

  Kabouridis, Panagiotis S ^a   Lasrado, Reena ^a   McCallum, Sarah ^a   Chng, Song Hui ^a,b,c   Snippert, Hugo J ^d   Clevers, Hans ^d   Pettersson, Sven ^b,c   Pachnis, Vassilis ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Enteric glial cells; Enteric nervous system; Germ free mice; Gut immune system; Gut microbiota; Inflammation; TLRs

Indexed keywords

GLIA CELL; IMMUNE SYSTEM; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE INNERVATION; LAMINA PROPRIA; ANIMAL; CELL MOTION; CYTOLOGY; GLIA; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INNERVATION; INTESTINE MUCOSA; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNE SYSTEM; INTESTINAL MUCOSA; MICE; NEUROGLIA; SIGNAL TRANSDUCTION;

EID: 84964262347     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.1080/19490976.2015.1109767     Document Type: Article

References (55)

1. Furness JB, The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 2012; 9:286-94; PMID:22392290; http://dx.doi.org/10.1038/nrgastro.2012.32
2. Heanue TA, Pachnis V. Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nat Rev Neurosci 2007; 8:466-79; PMID:17514199; http://dx.doi.org/10.1038/nrn2137
3. Boesmans W, Lasrado R, Vanden Berghe P, Pachnis V. Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia 2015; 63:229-41; PMID:25161129; http://dx.doi.org/10.1002/glia.22746
4. Gulbransen BD, Sharkey KA. Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 2012; 9:625-32; PMID:22890111; http://dx.doi.org/10.1038/nrgastro.2012.138
5. Neunlist M, Van Landeghem L, Mahe MM, Derkinderen P, des Varannes SB, Rolli-Derkinderen M. The digestive neuronal-glial-epithelial unit: a new actor in gut health and disease. Nat Rev Gastroenterol Hepatol 2013; 10:90-100; PMID:23165236; http://dx.doi.org/10.1038/nrgastro.2012.221
6. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH, Sofroniew MV. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 1998; 93:189-201; PMID:9568712; http://dx.doi.org/10.1016/S0092-8674(00)81571-8
7. Zhou Y, Yang J, Watkins DJ, Boomer LA, Matthews MA, Su Y, Besner GE. Enteric nervous system abnormalities are present in human necrotizing enterocolitis: potential neurotransplantation therapy. Stem Cell Res Ther 2013; 4:157; PMID:24423414; http://dx.doi.org/10.1186/scrt387
8. Fagbemi AO, Torrente F, Puleston J, Lakhoo K, James S, Murch SH. Enteric neural disruption in necrotizing enterocolitis occurs in association with myenteric glial cell CCL20 expression. J Pediatr Gastroenterol Nutr 2013; 57:788-93; PMID:24280992; http://dx.doi.org/10.1097/MPG.0b013e3182a86fd4
9. Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Vanden Berghe P, Pachnis V. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest 2011; 121:3412-24; PMID:21865647; http://dx.doi.org/10.1172/JCI58200
10. Roberts RR, Murphy JF, Young HM, Bornstein JC. Development of colonic motility in the neonatal mouse-studies using spatiotemporal maps. Am J Physiol Gastrointest Liver Physiol 2007; 292:G930-8; PMID:17158255; http://dx.doi.org/10.1152/ajpgi.00444.2006
11. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med 2014; 6:237ra65; PMID:24848255
12. Fardini Y, Chung P, Dumm R, Joshi N, Han YW. Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection. Infect Immun 2010; 78:1789-96; PMID:20123706; http://dx.doi.org/10.1128/IAI.01395-09
13. Stout MJ, Conlon B, Landeau M, Lee I, Bower C, Zhao Q, Roehl KA, Nelson DM, Macones GA, Mysorekar IU. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol 2013; 208:226 e1-7
14. Gosalbes MJ, Llop S, Valles Y, Moya A, Ballester F, Francino MP. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy 2013; 43:198-211; PMID:23331561; http://dx.doi.org/10.1111/cea.12063
15. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010; 107:11971-5; PMID:20566857; http://dx.doi.org/10.1073/pnas.1002601107
16. Ma J, Prince AL, Bader D, Hu M, Ganu R, Baquero K, Blundell P, Alan Harris R, Frias AE, Grove KL, et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun 2014; 5:3889; PMID:24846660
17. Del Chierico F, Vernocchi P, Petrucca A, Paci P, Fuentes S, Pratico G, Capuani G, Masotti A, Reddel S, Russo A, et al. Phylogenetic and metabolic tracking of gut microbiota during perinatal development. PloS One 2015; 10:e0137347; PMID:26332837; http://dx.doi.org/10.1371/journal.pone.0137347
18. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 2011; 108 Suppl 1:4578-85; PMID:20668239; http://dx.doi.org/10.1073/pnas.1000081107
19. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science 2012; 336:1262-7; PMID:22674330; http://dx.doi.org/10.1126/science.1223813
20. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol 2007; 5:e177; PMID:17594176; http://dx.doi.org/10.1371/journal. pbio.0050177
21. Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell 2014; 157:121-41; PMID:24679531; http://dx.doi.org/10.1016/j.cell.2014.03.011
22. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012; 489:231-41; PMID:22972296; http://dx.doi.org/10.1038/nature11551
23. Claesson MJ, Cusack S, O’Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A 2011; 108 Suppl 1:4586-91; PMID:20571116; http://dx.doi.org/10.1073/pnas.1000097107
24. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Dietinduced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008; 3:213-23; PMID:18407065; http://dx.doi.org/10.1016/j.chom.2008.02.015
25. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334:105-8; PMID:21885731; http://dx.doi.org/10.1126/science.1208344
26. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008; 6:e280; PMID:19018661; http://dx.doi.org/10.1371/journal.pbio.0060280
27. Kabouridis PS, Lasrado R, McCallum S, Chng SH, Snippert HJ, Clevers H, Pettersson S, Pachnis V. Microbiota controls the homeostasis of glial cells in the gut lamina propria. Neuron 2015; 85:289-95; PMID:25578362; http://dx.doi.org/10.1016/j.neuron.2014.12.037
28. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010; 143:134-44; PMID:20887898; http://dx.doi.org/10.1016/j.cell.2010.09.016
29. von Boyen GB, Steinkamp M, Reinshagen M, Schafer KH, Adler G, Kirsch J. Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 2004; 53:222-8; PMID:14724154; http://dx.doi.org/10.1136/gut.2003.012625
30. Dinan TG, Cryan JF. The impact of gut microbiota on brain and behaviour: implications for psychiatry. Curr Opin Clin Nutr Metab Care 2015; 18(6):552-8; PMID:26372511
31. Ruhl A. Glial cells in the gut. Neurogastroenterol Motil 2005; 17:777-90; PMID:16336493; http://dx.doi.org/10.1111/j.1365-2982.2005.00687.x
32. Cornet A, Savidge TC, Cabarrocas J, Deng WL, Colombel JF, Lassmann H, Desreumaux P, Liblau RS. Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn’s disease? Proc Natl Acad Sci U S A 2001; 98:13306-11; PMID:11687633; http://dx.doi.org/10.1073/pnas.231474098
33. Anitha M, Vijay-Kumar M, Sitaraman SV, Gewirtz AT, Srinivasan S. Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology 2012; 143:1006-16 e4; PMID:22732731; http://dx.doi.org/10.1053/j.gastro.2012.06.034
34. Brun P, Giron MC, Qesari M, Porzionato A, Caputi V, Zoppellaro C, Banzato S, Grillo AR, Spagnol L, De Caro R, et al. Toll-like receptor 2 regulates intestinal inflammation by controlling integrity of the enteric nervous system. Gastroenterology 2013; 145:1323-33; PMID:23994200; http://dx.doi.org/10.1053/j.gastro.2013.08.047
35. Barbara G, Zecchi L, Barbaro R, Cremon C, Bellacosa L, Marcellini M, De Giorgio R, Corinaldesi R, Stanghellini V. Mucosal permeability and immune activation as potential therapeutic targets of probiotics in irritable bowel syndrome. J Clin Gastroenterol 2012; 46 Suppl:S52-5; PMID:22955358; http://dx.doi.org/10.1097/MCG.0b013e318264e918
36. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013; 504:451-5; PMID:24226773; http://dx.doi.org/10.1038/nature12726
37. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013; 504:446-50; PMID:24226770; http://dx.doi.org/10.1038/nature12721
38. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013; 341:569-73; PMID:23828891; http://dx.doi.org/10.1126/science.1241165
39. Nohr MK, Pedersen MH, Gille A, Egerod KL, Engelstoft MS, Husted AS, Sichlau RM, Grunddal KV, Poulsen SS, Han S, et al. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology 2013; 154:3552-64; PMID:23885020; http://dx.doi.org/10.1210/en.2013-1142
40. Soret R, Chevalier J, De Coppet P, Poupeau G, Derkinderen P, Segain JP, Neunlist M. Short-chain fatty acids regulate the enteric neurons and control gastrointestinal motility in rats. Gastroenterology 2010; 138:1772-82; PMID:20152836; http://dx.doi.org/10.1053/j.gastro.2010.01.053
41. Mukherji A, Kobiita A, Ye T, Chambon P. Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 2013; 153:812-27; PMID:23663780; http://dx.doi.org/10.1016/j.cell.2013.04.020
42. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004; 118:229-41; PMID:15260992; http://dx.doi.org/10.1016/j.cell.2004.07.002
43. Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bayless AJ, Wilson KE, Glover LE, Kominsky DJ, Magnuson A, et al. Crosstalk between Microbiota-Derived Short-Chain Fatty Acids and Intestinal Epithelial HIF Augments Tissue Barrier Function. Cell Host Microbe 2015; 17:662-71; PMID:25865369; http://dx.doi.org/10.1016/j.chom.2015.03.005
44. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science 2012; 336:1268-73; PMID:22674334; http://dx.doi.org/10.1126/science.1223490
45. Muller PA, Koscso B, Rajani GM, Stevanovic K, Berres ML, Hashimoto D, Mortha A, Leboeuf M, Li XM, Mucida D, et al. Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 2014; 158:300-13; PMID:25036630; http://dx.doi.org/10.1016/j.cell.2014.04.050
46. Arthur-Farraj PJ, Latouche M, Wilton DK, Quintes S, Chabrol E, Banerjee A, Woodhoo A, Jenkins B, Rahman M, Turmaine M, et al. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 2012; 75:633-47; PMID:22920255; http://dx.doi.org/10.1016/j.neuron.2012.06.021
47. Bardehle S, Kruger M, Buggenthin F, Schwausch J, Ninkovic J, Clevers H, Snippert HJ, Theis FJ, Meyer-Luehmann M, Bechmann I, et al. Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nat Neurosci 2013; 16:580-6; PMID:23542688; http://dx.doi.org/10.1038/nn.3371
48. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R, Sofroniew MV. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 2007; 132:1344-58; PMID:17408650; http://dx.doi.org/10.1053/j.gastro.2007.01.051
49. Van Landeghem L, Chevalier J, Mahe MM, Wedel T, Urvil P, Derkinderen P, Savidge T, Neunlist M. Enteric glia promote intestinal mucosal healing via activation of focal adhesion kinase and release of proEGF. Am J Physiol Gastrointest Liver Physiol 2011; 300:G976-87; PMID:21350188; http://dx.doi.org/10.1152/ajpgi.00427.2010
50. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, Korecka A, Bakocevic N, Ng LG, Kundu P, et al. The gut microbiota influences bloodbrain barrier permeability in mice. Sci Transl Med 2014; 6:263ra158; PMID:25411471; http://dx.doi.org/10.1126/scitranslmed.3009759
51. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13:701-12; PMID:22968153; http://dx.doi.org/10.1038/nrn3346
52. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm 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; 108:3047-52; PMID:21282636; http://dx.doi.org/10.1073/pnas.1010529108
53. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, Bäckhed F, Mithieux G. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 2014; 156:84-96; PMID:24412651; http://dx.doi.org/10.1016/j.cell.2013.12.016
54. Chaidez V, Hansen RL, Hertz-Picciotto I. Gastrointestinal problems in children with autism, developmental delays or typical development. J Autism Dev Disord 2014; 44:1117-27; PMID:24193577; http://dx.doi.org/10.1007/s10803-013-1973-x
55. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013; 155:1451-63; PMID:24315484; http://dx.doi.org/10.1016/j.cell.2013.11.024