Antibiotic-Induced Depletion of Murine Microbiota Induces Mild Inflammation and Changes in Toll-Like Receptor Patterns and Intestinal Motility (original) (raw)

References

  1. Guarner F (2011) The intestinal microbiota and inflammatory bowel disease. Gastroenterol Hepatol 34:147–154. doi:10.1016/j.gastrohep.2010.11.009
    Article PubMed Google Scholar
  2. Dupont HL (2014) Review article: evidence for the role of gut microbiota in irritable bowel syndrome and its potential influence on therapeutic targets. Aliment Pharmacol Ther 39:1033–1042. doi:10.1111/apt.12728
    Article CAS PubMed Google Scholar
  3. Cerf-Bensussan N, Gaboriau-Routhiau V (2010) The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 10:735–744. doi:10.1038/nri2850
    Article CAS PubMed Google Scholar
  4. Hawrelak JA, Myers SP (2004) The causes of intestinal dysbiosis: a review. Altern Med Rev 9:180–197
    PubMed Google Scholar
  5. Konig J, Brummer RJ (2014) Alteration of the intestinal microbiota as a cause of and a potential therapeutic option in irritable bowel syndrome. Benef Microbes 5:247–261. doi:10.3920/BM2013.0033
    Article CAS PubMed Google Scholar
  6. Uusijarvi A, Bergstrom A, Simren M, Ludvigsson JF, Kull I, Wickman M, Alm J, Olen O (2014) Use of antibiotics in infancy and childhood and risk of recurrent abdominal pain—a Swedish birth cohort study. Neurogastroenterol Motil 26:841–850. doi:10.1111/nmo.12340
    Article CAS PubMed Google Scholar
  7. Ubeda C, Pamer EG (2012) Antibiotics, microbiota, and immune defense. Trends Immunol 33:459–466. doi:10.1016/j.it.2012.05.003
    Article PubMed Central CAS PubMed Google Scholar
  8. Reikvam DH, Erofeev A, Sandvik A, Grcic V, Jahnsen FL, Gaustad P, McCoy KD, Macpherson AJ, Meza-Zepeda LA, Johansen FE (2011) Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PLoS One 6, e17996. doi:10.1371/journal.pone.0017996
    Article PubMed Central CAS PubMed Google Scholar
  9. Eutamene H, Lamine F, Chabo C, Theodorou V, Rochat F, Bergonzelli GE, Corthesy-Theulaz I, Fioramonti J, Bueno L (2007) Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats. J Nutr 137:1901–1907. doi: 137/8/1901
  10. Verdu EF, Bercik P, Verma-Gandhu M, Huang XX, Blennerhassett P, Jackson W, Mao Y, Wang L, Rochat F, Collins SM (2006) Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 55:182–190. doi:10.1136/gut.2005.066100
    Article PubMed Central CAS PubMed Google Scholar
  11. Collins SM, Bercik P (2009) The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 136:2003–2014. doi:10.1053/j.gastro.2009.01.075
    Article PubMed Google Scholar
  12. Lees GM, Percy WH (1981) Antibiotic-associated colitis: an in vitro investigation of the effects of antibiotics on intestinal motility. Br J Pharmacol 73:535–547
    Article PubMed Central CAS PubMed Google Scholar
  13. Anitha M, Vijay-Kumar M, Sitaraman SV, Gewirtz AT, Srinivasan S (2012) Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology 143(1006–1016), e1004. doi:10.1053/j.gastro.2012.06.034
    Google Scholar
  14. Cario E (2010) Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm Bowel Dis 16:1583–1597. doi:10.1002/ibd.21282
    Article PubMed Central PubMed Google Scholar
  15. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1–14. doi:17/1/1
  16. Abreu MT (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10:131–144. doi:10.1038/nri2707
    Article CAS PubMed Google Scholar
  17. Brun P, Giron MC, Qesari M, Porzionato A, Caputi V, Zoppellaro C, Banzato S, Grillo AR, Spagnol L, De Caro R, Pizzuti D, Barbieri V, Rosato A, Sturniolo GC, Martines D, Zaninotto G, Palu G, Castagliuolo I (2013) Toll-like receptor 2 regulates intestinal inflammation by controlling integrity of the enteric nervous system. Gastroenterology 145:1323–1333. doi:10.1053/j.gastro.2013.08.047
    Article CAS PubMed Google Scholar
  18. Filippova LV, Malyshev FS, Bykova AA, Nozdrachev AD (2012) Expression of toll-like receptors 4 in nerve plexuses of the rat duodenum, jejunum, and colon. Dokl Biol Sci 445:215–217. doi:10.1134/S0012496612040114
    Article CAS PubMed Google Scholar
  19. Barajon I, Serrao G, Arnaboldi F, Opizzi E, Ripamonti G, Balsari A, Rumio C (2009) Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J Histochem Cytochem 57:1013–1023. doi:10.1369/jhc.2009.953539
    Article PubMed Central CAS PubMed Google Scholar
  20. Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, Deng Y, Blennerhassett P, Macri J, McCoy KD, Verdu EF, Collins SM (2011) The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141:599–609, 609 e591–593. doi:10.1053/j.gastro.2011.04.052
  21. Marin-Manzano MC, Abecia L, Hernandez-Hernandez O, Sanz ML, Montilla A, Olano A, Rubio LA, Moreno FJ, Clemente A (2013) Galacto-oligosaccharides derived from lactulose exert a selective stimulation on the growth of Bifidobacterium animalis in the large intestine of growing rats. J Agric Food Chem 61:7560–7567. doi:10.1021/jf402218z
    Article CAS PubMed Google Scholar
  22. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
    PubMed Central CAS PubMed Google Scholar
  23. Abecia L, Rodriguez-Romero N, Yanez-Ruiz DR, Fondevila M (2012) Biodiversity and fermentative activity of caecal microbial communities in wild and farm rabbits from Spain. Anaerobe 18:344–349. doi:10.1016/j.anaerobe.2012.04.004
    Article CAS PubMed Google Scholar
  24. Cattaruzza F, Cenac N, Barocelli E, Impicciatore M, Hyun E, Vergnolle N, Sternini C (2006) Protective effect of proteinase-activated receptor 2 activation on motility impairment and tissue damage induced by intestinal ischemia/reperfusion in rodents. Am J Pathol 169:177–188. doi:S0002-9440(10)61441-1
  25. Appleyard CB, Wallace JL (1995) Reactivation of hapten-induced colitis and its prevention by anti-inflammatory drugs. Am J Physiol 269:G119–G125
    CAS PubMed Google Scholar
  26. Jiang X, McClellan SA, Barrett RP, Zhang Y, Hazlett LD (2012) Vasoactive intestinal peptide downregulates proinflammatory TLRs while upregulating anti-inflammatory TLRs in the infected cornea. J Immunol 189:269–278. doi:10.4049/jimmunol.1200365
    Article PubMed Central CAS PubMed Google Scholar
  27. Williams AS, Leung SY, Nath P, Khorasani NM, Bhavsar P, Issa R, Mitchell JA, Adcock IM, Chung KF (2007) Role of TLR2, TLR4, and MyD88 in murine ozone-induced airway hyperresponsiveness and neutrophilia. J Appl Physiol (1985) 103:1189–1195. doi:10.1152/japplphysiol.00172.2007
    Article CAS Google Scholar
  28. Lundin A, Bok CM, Aronsson L, Bjorkholm B, Gustafsson JA, Pott S, Arulampalam V, Hibberd M, Rafter J, Pettersson S (2008) Gut flora, Toll-like receptors and nuclear receptors: a tripartite communication that tunes innate immunity in large intestine. Cell Microbiol 10:1093–1103. doi:10.1111/j.1462-5822.2007.01108.x
    Article CAS PubMed Google Scholar
  29. Shin OS, Isberg RR, Akira S, Uematsu S, Behera AK, Hu LT (2008) Distinct roles for MyD88 and Toll-like receptors 2, 5, and 9 in phagocytosis of Borrelia burgdorferi and cytokine induction. Infect Immun 76:2341–2351. doi:10.1128/IAI.01600-07
    Article PubMed Central CAS PubMed Google Scholar
  30. Santiago-Raber ML, Dunand-Sauthier I, Wu T, Li QZ, Uematsu S, Akira S, Reith W, Mohan C, Kotzin BL, Izui S (2010) Critical role of TLR7 in the acceleration of systemic lupus erythematosus in TLR9-deficient mice. J Autoimmun 34:339–348. doi:10.1016/j.jaut.2009.11.001
    Article CAS PubMed Google Scholar
  31. Thatcher TH, Luzina I, Fishelevich R, Tomai MA, Miller RL, Gaspari AA (2006) Topical imiquimod treatment prevents UV-light induced loss of contact hypersensitivity and immune tolerance. J Invest Dermatol 126:821–831. doi:10.1038/sj.jid.5700167
    Article CAS PubMed Google Scholar
  32. Zhou M, Jia P, Chen J, Xiu A, Zhao Y, Zhan Y, Chen P, Zhang J (2013) Laxative effects of Salecan on normal and two models of experimental constipated mice. BMC Gastroenterol 13:52. doi:10.1186/1471-230X-13-52
    Article PubMed Central CAS PubMed Google Scholar
  33. De Palma G, Collins SM, Bercik P (2014) The microbiota-gut-brain axis in functional gastrointestinal disorders. Gut Microbes 5:419–429. doi: 10.4161/gmic.29417
  34. Aguilera M, Vergara P, Martinez V (2013) Stress and antibiotics alter luminal and wall-adhered microbiota and enhance the local expression of visceral sensory-related systems in mice. Neurogastroenterol Motil 25:e515–e529. doi:10.1111/nmo.12154
    Article CAS PubMed Google Scholar
  35. Barbara G, Stanghellini V, Brandi G, Cremon C, Di Nardo G, De Giorgio R, Corinaldesi R (2005) Interactions between commensal bacteria and gut sensorimotor function in health and disease. Am J Gastroenterol 100:2560–2568. doi:10.1111/j.1572-0241.2005.00230.x
    Article CAS PubMed Google Scholar
  36. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98:694–702. doi:S0016508590000725
  37. Muzio M, Bosisio D, Polentarutti N, D'Amico G, Stoppacciaro A, Mancinelli R, van't Veer C, Penton-Rol G, Ruco LP, Allavena P, Mantovani A (2000) Differential expression and regulation of toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol 164:5998–6004. doi:ji_v164n10p5998
  38. Zarember KA, Godowski PJ (2002) Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 168:554–561
    Article CAS PubMed Google Scholar
  39. Abreu MT (2003) Immunologic regulation of toll-like receptors in gut epithelium. Curr Opin Gastroenterol 19:559–564. doi:10.1097/00001574-200311000-00008
    Article CAS PubMed Google Scholar
  40. Furrie E, Macfarlane S, Thomson G, Macfarlane GT (2005) Toll-like receptors-2, -3 and -4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 115:565–574. doi:10.1111/j.1365-2567.2005.02200.x
    Article PubMed Central CAS PubMed Google Scholar
  41. Chen LW, Chang WJ, Chen PH, Liu WC, Hsu CM (2008) TLR ligand decreases mesenteric ischemia and reperfusion injury-induced gut damage through TNF-alpha signaling. Shock 30:563–570. doi:10.1097/SHK.0b013e31816a3458
    Article CAS PubMed Google Scholar
  42. Brint EK, MacSharry J, Fanning A, Shanahan F, Quigley EM (2011) Differential expression of toll-like receptors in patients with irritable bowel syndrome. Am J Gastroenterol 106:329–336. doi:10.1038/ajg.2010.438
    Article CAS PubMed Google Scholar
  43. Barona I, Fagundes DS, Gonzalo S, Grasa L, Arruebo MP, Plaza MA, Murillo MD (2011) Role of TLR4 and MAPK in the local effect of LPS on intestinal contractility. J Pharm Pharmacol 63:657–662. doi:10.1111/j.2042-7158.2011.01253.x
    Article CAS PubMed Google Scholar
  44. Grasa L, Arruebo MP, Plaza MA, Murillo MD (2008) A downregulation of nNOS is associated to dysmotility evoked by lipopolysaccharide in rabbit duodenum. J Physiol Pharmacol 59:511–524
    CAS PubMed Google Scholar
  45. Gonzalo S, Grasa L, Arruebo MP, Plaza MA, Murillo MD (2010) Inhibition of p38 MAPK improves intestinal disturbances and oxidative stress induced in a rabbit endotoxemia model. Neurogastroenterol Motil 22: 564-572, e123. doi:10.1111/j.1365-2982.2009.01439.x
  46. Hernandez LV, Gonzalo S, Castro M, Arruebo MP, Plaza MA, Murillo MD, Grasa L (2011) Nuclear factor kappaB is a key transcription factor in the duodenal contractility alterations induced by lipopolysaccharide. Exp Physiol 96:1151–1162. doi:10.1113/expphysiol.2011.060830
    Article CAS PubMed Google Scholar
  47. Rolli J, Rosenblatt-Velin N, Li J, Loukili N, Levrand S, Pacher P, Waeber B, Feihl F, Ruchat P, Liaudet L (2010) Bacterial flagellin triggers cardiac innate immune responses and acute contractile dysfunction. PLoS One 5, e12687. doi:10.1371/journal.pone.0012687
    Article PubMed Central PubMed Google Scholar
  48. Tattoli I, Petitta C, Scirocco A, Ammoscato F, Cicenia A, Severi C (2012) Microbiota, innate immune system, and gastrointestinal muscle: ongoing studies. J Clin Gastroenterol 46(Suppl):S6–S11. doi:10.1097/MCG.0b013e318265ea7d
    Article CAS PubMed Google Scholar

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