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The Intrinsic Reflex Circuitry of the Inflamed Colon

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Part of the book series: Advances in Experimental Medicine and Biology ((ANS,volume 891))

Abstract

In 1899, Bayliss and Starling determined that the innervation of the intestines differs from that of other organs. They found that local neuronal networks are capable of generating reflex responses without the involvement of the central nervous system (Bayliss and Starling 1899). Once this unique feature of the enteric nervous system (ENS) was identified, it took roughly a century for enteric neurobiologists to accomplish the task of being able to identify the components of this “intrinsic neural mechanism”, including intrinsic primary afferent neuron, ascending and descending interneuron, and excitatory and inhibitory motor neurons (Bayliss and Starling 1899). Once this was possible, we and others began to investigate the intrinsic circuitry of the colon and ileum to systematically determine the cellular mechanisms that explain the changes in motility and secretion that occur in intestinal inflammation. We wanted to establish what changes occur in the enteric neural circuitry, where they occur, the mechanisms responsible for these changes, and how these changes in the neural circuitry impact intestinal function.

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References

  • Bayliss WM, Starling EH (1899) The movements and innervation of the small intestine. J Physiol 24:99–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Suntres Z, Palmer J, Guzman J, Javed A, Xue J, Yu JG, Cooke H, Awad H, Hassanain HH, Cardounel AJ, Christofi FL (2007) Cyclic AMP signaling contributes to neural plasticity and hyperexcitability in AH sensory neurons following intestinal Trichinella spiralis-induced inflammation. Int J Parasitol 37:743–761

    Article  CAS  PubMed  Google Scholar 

  • Costedio MM, Hyman N, Mawe GM (2007) Serotonin and its role in colonic function and in gastrointestinal disorders. Dis Colon Rectum 50:376–388

    Article  PubMed  Google Scholar 

  • Frieling T, Cooke HJ, Wood JD (1994) Neuroimmune communication in the submucous plexus of guinea pig colon after sensitization to milk antigen. Am J Physiol 267:G1087–G1093

    CAS  PubMed  Google Scholar 

  • Gulbransen BD, Bashashati M, Hirota SA, Gui X, Roberts JA, MacDonald JA, Muruve DA, McKay DM, Beck PL, Mawe GM, Thompson RJ, Sharkey KA (2012) Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med 18:600–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffman JM, Brooks EM, Mawe GM (2010) Gastrointestinal Motility Monitor (GIMM). J Vis Exp (46). doi:10.3791/2435

  • Hoffman JM, McKnight ND, Sharkey KA, Mawe GM (2011) The relationship between inflammation-induced neuronal excitability and disrupted motor activity in the guinea pig distal colon. Neurogastroenterol Motil 23:673-e279

    Article  PubMed  Google Scholar 

  • Krauter EM, Linden DR, Sharkey KA, Mawe GM (2007a) Synaptic plasticity in myenteric neurons of the guinea-pig distal colon: presynaptic mechanisms of inflammation-induced synaptic facilitation. J Physiol 581:787–800

    Article  PubMed  PubMed Central  Google Scholar 

  • Krauter EM, Strong DS, Brooks EM, Linden DR, Sharkey KA, Mawe GM (2007b) Changes in colonic motility and the electrophysiological properties of myenteric neurons persist following recovery from trinitrobenzene sulfonic acid colitis in the guinea pig. Neurogastroenterol Motil 19:990–1000

    CAS  PubMed  Google Scholar 

  • Linden DR, Sharkey KA, Mawe GM (2003) Enhanced excitability of myenteric AH neurones in the inflamed guinea-pig distal colon. J Physiol 547:589–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linden DR, Sharkey KA, Ho W, Mawe GM (2004) Cyclooxygenase-2 contributes to dysmotility and enhanced excitability of myenteric AH neurones in the inflamed guinea pig distal colon. J Physiol 557:191–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linden DR, Couvrette JM, Ciolino A, McQuoid C, Blaszyk H, Sharkey KA, Mawe GM (2005) Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol Motil 17:751–760

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Hu HZ, Gao N, Gao C, Wang G, Wang X, Peck OC, Kim G, Gao X, Xia Y, Wood JD (2003) Neuroimmune interactions in guinea pig stomach and small intestine. Am J Physiol Gastrointest Liver Physiol 284:G154–G164

    Article  CAS  PubMed  Google Scholar 

  • Lomax AE, Mawe GM, Sharkey KA (2005) Synaptic facilitation and enhanced neuronal excitability in the submucosal plexus during experimental colitis in guinea-pig. J Physiol 564:863–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lomax AE, O’Hara JR, Hyland NP, Mawe GM, Sharkey KA (2007) Persistent alterations to enteric neural signaling in the guinea pig colon following the resolution of colitis. Am J Physiol Gastrointest Liver Physiol 292:G482–G491

    Article  CAS  PubMed  Google Scholar 

  • Manning BP, Sharkey KA, Mawe GM (2002) Effects of PGE2 in guinea pig colonic myenteric ganglia. Am J Physiol Gastrointest Liver Physiol 283:G1388–G1397

    Article  CAS  PubMed  Google Scholar 

  • Mawe GM, Hoffman JM (2013) Serotonin signalling in the gut—functions, dysfunctions and therapeutic targets. Nat Rev Gastroenterol Hepatol 10:473–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer JM, Wong-Riley M, Sharkey KA (1998) Functional alterations in jejunal myenteric neurons during inflammation in nematode-infected guinea pigs. Am J Physiol 275:G922–G935

    CAS  PubMed  Google Scholar 

  • Roberts JA, Durnin L, Sharkey KA, Mutafova-Yambolieva VN, Mawe GM (2013) Oxidative stress disrupts purinergic neuromuscular transmission in the inflamed colon. J Physiol 591:3725–3737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strong DS, Cornbrooks CF, Roberts JA, Hoffman JM, Sharkey KA, Mawe GM (2010) Purinergic neuromuscular transmission is selectively attenuated in ulcerated regions of inflamed guinea pig distal colon. J Physiol 588:847–859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work has been supported by NIH-NIDDK grant DK62267 and by the Crohn’s and Colitis Foundation of Canada. KAS is a Killam Annual Professor and holds the Crohn’s and Colitis Foundation of Canada Chair in Inflammatory Bowel Disease Research.

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Correspondence to Gary M. Mawe Ph.D. .

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Mawe, G.M., Sharkey, K.A. (2016). The Intrinsic Reflex Circuitry of the Inflamed Colon. In: Brierley, S., Costa, M. (eds) The Enteric Nervous System. Advances in Experimental Medicine and Biology(), vol 891. Springer, Cham. https://doi.org/10.1007/978-3-319-27592-5_15

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