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Localisation and activation of the neurokinin 1 receptor in the enteric nervous system of the mouse distal colon

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Abstract

The substance P neurokinin 1 receptor (NK1R) regulates motility, secretion, inflammation and pain in the intestine. The distribution of the NK1R is a key determinant of the functional effects of substance P in the gut. Information regarding the distribution of NK1R in subtypes of mouse enteric neurons is lacking and is the focus of the present study. NK1R immunoreactivity (NK1R-IR) is examined in whole-mount preparations of the mouse distal colon by indirect immunofluorescence and confocal microscopy. The distribution of NK1R-IR within key functional neuronal subclasses was determined by using established neurochemical markers. NK1R-IR was expressed by a subpopulation of myenteric and submucosal neurons; it was mainly detected in large multipolar myenteric neurons and was colocalized with calcitonin gene-related peptide, neurofilament M, choline acetyltransferase and calretinin. The remaining NK1R-immunoreactive neurons were positive for nitric oxide synthase. NK1R was expressed by most of the submucosal neurons and was exclusively co-expressed with vasoactive intestinal peptide, with no overlap with choline acetyltransferase. Treatment with substance P resulted in the concentration-dependent internalisation of NK1R from the cell surface into endosome-like structures. Myenteric NK1R was mainly expressed by intrinsic primary afferent neurons, with minor expression by descending interneurons and inhibitory motor neurons. Submucosal NK1R was restricted to non-cholinergic secretomotor neurons. These findings highlight key differences in the neuronal distribution of NK1R-IR between the mouse, rat and guinea-pig, with important implications for the functional role of NK1R in regulating intestinal motility and secretion.

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Acknowledgement

We thank Professors J.B. Furness and G.W. Aponte for providing antibodies used in this study.

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Authors and Affiliations

  1. Department of Pediatric Surgery, The University of Chicago, Chicago, IL, 60637, USA

    Juan-Carlos Pelayo

  2. Monash Institute of Pharmaceutical Sciences, 381 Royal Parade, Parkville, VIC, 3052, Australia

    Nicholas A. Veldhuis, Nigel W. Bunnett & Daniel P. Poole

  3. Division of Infection and Immunity, Walter and Eliza Hall Institute of Medical Research, Parkville, VIC, 3052, Australia

    Emily M. Eriksson

  4. Department of Medical Biology, The University of Melbourne, Parkville, VIC, 3010, Australia

    Emily M. Eriksson

  5. Department of Pharmacology, The University of Melbourne, Parkville, VIC, 3010, Australia

    Nigel W. Bunnett

  6. Department of Anatomy and Neuroscience, The University of Melbourne, Parkville, VIC, 3010, Australia

    Daniel P. Poole

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  1. Juan-Carlos Pelayo
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  2. Nicholas A. Veldhuis
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  3. Emily M. Eriksson
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  4. Nigel W. Bunnett
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  5. Daniel P. Poole
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Correspondence to Nigel W. Bunnett or Daniel P. Poole.

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This work was supported by NIH/NIDDK grants DK07573 (J.-C.P.), DK39957, DK43207 and DK57840 (N.W.B.), NHMRC grants 63303, 103188 (N.W.B.) and 454858 (D.P.P.) and Monash University (N.W.B.).

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Pelayo, JC., Veldhuis, N.A., Eriksson, E.M. et al. Localisation and activation of the neurokinin 1 receptor in the enteric nervous system of the mouse distal colon. Cell Tissue Res 356, 319–332 (2014). https://doi.org/10.1007/s00441-014-1822-z

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