Activated fluid transport regulates bacterial-epithelial interactions and significantly shifts the murine colonic microbiome

Gut Microbes

Volumn 3, Issue 3, 2012, Pages 1-11

  Keely, Simon ^a,b   Kelly, Caleb J ^a   Weissmueller, Thomas ^a,c   Burgess, Adrianne ^a   Wagner, Brandie D ^d   Robertson, Charles E ^a   Harris, Kirk ^e   Colgan, Sean P ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d Food Science and Human Nutrition   (United States)

^e CHILDREN S HOSPITAL COLORADO   (United States)

Author keywords

Commensal bacteria; Epithelial transport; Infection; Innate immunity; Lactobacillus; Microbiota; Ribosomal RNA

Indexed keywords

BUMETANIDE; CHLORIDE; CHLORIDE CHANNEL; CHLORINE; DRUG ADMINISTRATION; DRUG DERIVATIVE; ELECTROLYTE; LUBIPROSTONE; PROSTAGLANDIN E1; WATER;

ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL TRANSLOCATION; BACTERIUM; BACTEROIDETES; BIODIVERSITY; BODY FLUID; C57BL MOUSE; CELL INTERACTION; CELL LINE; CLASSIFICATION; COLON FLORA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENTIATION; ELECTROLYTE TRANSPORT; FEMALE; FIRMICUTES; FLUID TRANSPORT; GASTROINTESTINAL TRACT; HYDRATION; IN VITRO STUDY; INNATE IMMUNITY; INTERNALIZATION; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; LAMINA PROPRIA; METABOLISM; MICROBIOLOGY; MICROBIOME; MOUSE; NONHUMAN; ORAL DRUG ADMINISTRATION; PASSIVE TRANSPORT; PHYLUM; REGULATORY MECHANISM; SALMONELLA TYPHIMURIUM; WATER TRANSPORT;

ADMINISTRATION AND DOSAGE; ADMINISTRATION, ORAL; AGONISTS; ALPROSTADIL; ANALOGS AND DERIVATIVES; ANIMALS; BACTERIA; BACTERIAL TRANSLOCATION; BIODIVERSITY; BODY FLUIDS; CELL LINE; CHLORIDE CHANNELS; CHLORINE; CLASSIFICATION; ELECTROLYTES; FEMALE; GASTROINTESTINAL TRACT; INTESTINAL MUCOSA; ISOLATION AND PURIFICATION; METABOLISM; MICE; MICE, INBRED C57BL; MICROBIOLOGY; WATER;

BACTERIA (MICROORGANISMS); BACTEROIDETES PHYLUM; FIRMICUTES; LACTOBACILLUS; MURINAE; MUS;

EID: 84930484871     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gutmic.20529     Document Type: Article

References (33)

1. Gamba G. Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol Rev 2005; 85:423-493; PMID:15788703; http://dx.doi.org/10.1152/physrev.00011.2004.
2. Barrett KE, Keely SJ. Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects. Annu Rev Physiol 2000; 62:535-572; PMID:10845102; http://dx.doi.org/10.1146/annurev.physiol.62.1.535.
3. Campbell EL, Serhan CN, Colgan SP. Antimicrobial aspects of inflammatory resolution in the mucosa: a role for proresolving mediators. J Immunol 2011; 187:3475-3481; PMID:21934099; http://dx.doi.org/10.4049/jimmunol.1100150.
4. Ivanov AI, Parkos CA, Nusrat A. Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol 2010; 177:512-524; PMID:20581053; http://dx.doi.org/10.2353/ajpath.2010.100168.
5. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009; 9:799-809; PMID:19855405; http://dx.doi.org/10.1038/nri2653.
6. Clunes MT, Boucher RC. Introduction to section I: overview of approaches to study cystic fibrosis pathophysiology. Methods Mol Biol 2011; 742:3-14; PMID:21547723; http://dx.doi.org/10.1007/978-1-61779-120-8_1.
7. Glenn GM, Francis DH, Danielsen EM. Toxinmediated effects on the innate mucosal defenses: implications for enteric vaccines. Infect Immun 2009; 77:5206-5215; PMID:19737904; http://dx.doi.org/10.1128/IAI.00712-09.
8. Hallstrom K, McCormick BA. Salmonella Interaction with and Passage through the Intestinal Mucosa: Through the Lens of the Organism. Front Microbiol 2011; 2:88; PMID:21747800; http://dx.doi.org/10.3389/fmicb.2011.00088.
9. McCole DF, Barrett KE. Varied role of the gut epithelium in mucosal homeostasis. Curr Opin Gastroenterol 2007; 23:647-654; PMID:17906442; http://dx.doi.org/10.1097/MOG.0b013e3282f0153b.
10. Dharmsathaphorn K, Madara JL. Established intestinal cell lines as model systems for electrolyte transport studies. Methods Enzymol 1990; 192:354-389; PMID:2074798; http://dx.doi.org/10.1016/0076-6879(90)92082-O.
11. Asfaha S, MacNaughton WK, Appleyard CB, Chadee K, Wallace JL. Persistent epithelial dysfunction and bacterial translocation after resolution of intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 2001; 281:635-644; PMID:11518675.
12. Zamuner SR, Warrier N, Buret AG, MacNaughton WK, Wallace JL. Cyclooxygenase 2 mediates postinflammatory colonic secretory and barrier dysfunction. Gut 2003; 52:1714-1720; PMID:14633948; http://dx.doi.org/10.1136/gut.52.12.1714.
13. Bijvelds MJ, Bot AG, Escher JC, De Jonge HR. Activation of intestinal Cl- secretion by lubiprostone requires the cystic fibrosis transmembrane conductance regulator. Gastroenterology 2009; 137:976-985; PMID:19454284; http://dx.doi.org/10.1053/j.gastro.2009.05.037.
14. De Lisle RC, Mueller R, Roach E. Lubiprostone ameliorates the cystic fibrosis mouse intestinal phenotype. BMC Gastroenterol 2010; 10:107; PMID:20843337; http://dx.doi.org/10.1186/1471-230X-10-107.
15. Kageyama A, Benno Y. Coprobacillus catenaformis gen. nov., sp. nov., a new genus and species isolated from human feces. Microbiol Immunol 2000; 44:23-28; PMID:10711596.
16. Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 2007; 133:24-33; PMID:17631127; http://dx.doi.org/10.1053/j.gastro.2007.04.005.
17. Lyra A, Rinttilä T, Nikkilä J, Krogius-Kurikka L, Kajander K, Malinen E, et al. Diarrhoea-predominant irritable bowel syndrome distinguishable by 16S rRNA gene phylotype quantification. World J Gastroenterol 2009; 15:5936-5945; PMID:20014457; http://dx.doi.org/10.3748/wjg.15.5936.
18. Fukudo S, Hongo M, Kaneko H, Ueno R. Efficacy and safety of oral lubiprostone in constipated patients with or without irritable bowel syndrome: a randomized, placebo-controlled and dose-finding study. Neurogastroenterol Motil 2011; 23:544; PMID:21303430; http://dx.doi.org/10.1111/j.1365-2982.2011.01668.x.
19. Saad RJ. Peripherally acting therapies for the treatment of irritable bowel syndrome. Gastroenterol Clin North Am 2011; 40:163-182; PMID:21333906; http://dx.doi.org/10.1016/j.gtc.2010.12.008.
20. Boesten RJ, de Vos WM. Interactomics in the human intestine: Lactobacilli and Bifidobacteria make a difference. J Clin Gastroenterol 2008; 42:163-167; PMID:18685514; http://dx.doi.org/10.1097/MCG.0b013e31817dbd62.
21. Reading NC, Kasper DL. The starting lineup: key microbial players in intestinal immunity and homeostasis. Front Microbiol 2011; 2:148; PMID:21779278; http://dx.doi.org/10.3389/fmicb.2011.00148.
22. Sánchez B, Urdaci MC, Margolles A. Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions. Microbiology 2010; 156:3232-3242; PMID:20864471; http://dx.doi.org/10.1099/mic.0.044057-0.
23. Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 1999; 116:1107-1114; PMID:10220502; http://dx.doi.org/10.1016/S0016-5085(99)70013-2.
24. Walker J, Jijon HB, Churchill T, Kulka M, Madsen KL. Activation of AMP-activated protein kinase reduces cAMP-mediated epithelial chloride secretion. Am J Physiol Gastrointest Liver Physiol 2003; 285:850-860; PMID:12869384.
25. Madara JL, Parkos CA, Colgan SP, MacLeod RJ, Nash S, Matthews J, et al. Cl- secretion in a model intestinal epithelium induced by a neutrophilderived secretagogue. J Clin Invest 1992; 89:1938-1944; PMID:1602001; http://dx.doi.org/10.1172/JCI115800.
26. Blume ED, Taylor CT, Lennon PF, Stahl GL, Colgan SP. Activated endothelial cells elicit paracrine induction of epithelial chloride secretion. 6-Keto-PGF1α is an epithelial secretagogue. J Clin Invest 1998; 102:1161-1172; PMID:9739050; http://dx.doi.org/10.1172/JCI3465.
27. Keely S, Rawlinson LA, Haddleton DM, Brayden DJ. A tertiary amino-containing polymethacrylate polymer protects mucus-covered intestinal epithelial monolayers against pathogenic challenge. Pharm Res 2008; 25:1193-1201; PMID:18046631; http://dx.doi.org/10.1007/s11095-007-9501-3.
28. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 2008; 5:235-237; PMID:18264105; http://dx.doi.org/10.1038/nmeth.1184.
29. Harris JK, Sahl JW, Castoe TA, Wagner BD, Pollock DD, Spear JR. Comparison of normalization methods for construction of large, multiplex amplicon pools for next-generation sequencing. Appl Environ Microbiol 2010; 76:3863-3868; PMID:20418443; http://dx.doi.org/10.1128/AEM.02585-09.
30. Frank DN. BARCRAWL and BARTAB: software tools for the design and implementation of barcoded primers for highly multiplexed DNA sequencing. BMC Bioinformatics 2009; 10:362; PMID:19874596; http://dx.doi.org/10.1186/1471-2105-10-362.
31. Nawrocki EP, Kolbe DL, Eddy SR. Infernal 1.0: inference of RNA alignments. Bioinformatics 2009; 25:1335-1337; PMID:19307242; http://dx.doi.org/10.1093/bioinformatics/btp157.
32. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, et al.; Human Microbiome Consortium. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 2011; 21:494-504; PMID:21212162; http://dx.doi.org/10.1101/gr.112730.110.
33. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73:5261-5267; PMID:17586664; http://dx.doi.org/10.1128/AEM.00062-07.