Abstract
The plant lectin, IB4, binds to the surfaces of primary afferent neurons of the dorsal root and trigeminal ganglia and is documented to be selective for nociceptive neurons. Physiological data suggest that the intrinsic primary afferent neurons within the intestine are also nociceptors. In this study, we have compared IB4 binding to each of these neuron types in the guinea-pig. The only neurons in the intestine to be readily revealed by IB4 binding have Dogiel-type-II morphology; these neurons have been previously identified as intrinsic primary afferent neurons. Most of the neurons that are IB4-positive in the myenteric plexus are calbindin-immunoreactive, whereas those in the submucosal ganglia are immunoreactive for NeuN. The neurons that bind IB4 strongly have a similar appearance in enteric, dorsal root and trigeminal ganglia. Binding is to the cell surface, to the first part of axons and to cytoplasmic organelles. A low level of binding was found in the extracellular matrix. A few other neurons in all ganglia exhibit faint staining with IB4. Strongly reactive neurons are absent from the gastric corpus. Thus, IB4 binding reveals primary afferent neurons with similar morphologies, patterns of binding and physiological roles in enteric, dorsal root and trigeminal ganglia.
Similar content being viewed by others
References
Ambalavanar R, Morris R (1992) The distribution of binding by isolectin I-B4 from Griffonia simplicifolia in the trigeminal ganglion and brainstem trigeminal nuclei in the rat. Neuroscience 47:421–429
Ambalavanar R, Moritani M, Haines A, Hilton T, Dessem D (2003) Chemical phenotypes of muscle and cutaneous afferent neurons in the rat trigeminal ganglion. J Comp Neurol 460:167–179
Anderson CR, Furness JB, Woodman HL, Edwards SL, Crack PJ, Smith AI (1995) Characterisation of neurons with nitric oxide synthase immunoreactivity that project to prevertebral ganglia. J Auton Nerv Syst 52:107–116
Chiocchetti R, Poole DP, Kimura H, Aimi Y, Robbins HL, Castelucci P, Furness JB (2003) Evidence that two forms of choline acetyltransferase are differentially expressed in subclasses of enteric neurons. Cell Tissue Res 311:11–22
Collins SM (1996) The immunomodulation of enteric neuromuscular function: implications for motility and inflammatory disorders. Gastroenterology 111:1683–1699
Djouhri L, Bleazard L, Lawson SN (1998) Association of somatic action potential shape with sensory receptive properties in guinea-pig dorsal root ganglion neurones. J Physiol (Lond) 513:857–872
Furness JB, Bornstein JC, Trussell DC (1988) Shapes of nerve cells in the myenteric plexus of the guinea-pig small intestine revealed by the intracellular injection of dye. Cell Tissue Res 254:561–571
Furness JB, Jones C, Nurgali K, Clerc N (2004) Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol 72:143–164
Gerke MB, Plenderleith MB (2001) Binding sites for the plant lectin Bandeiraea simplicifolia I-isolectin B4 are expressed by nociceptive primary sensory neurones. Brain Res 911:101–104
Hirst GDS, Johnson SM, Helden DF van (1985) The slow calcium-dependent potassium current in a myenteric neurone of the guinea-pig ileum. J Physiol (Lond) 361:315–337
Iyer V, Bornstein JC, Costa M, Furness JB, Takahashi Y, Iwanaga T (1988) Electrophysiology of guinea-pig myenteric neurons correlated with immunoreactivity for calcium binding proteins. J Auton Nerv Syst 22:141–150
Kirchgessner AL, Dodd J, Gershon MD (1988) Markers shared between dorsal root and enteric ganglia. J Comp Neurol 276:607–621
Kitchener PD, Wilson P, Snow PJ (1993) Selective labelling of primary sensory afferent terminals in lamina II of the dorsal horn by injection of Bandeiraea simplicifolia isolectin B4 into peripheral nerves. Neuroscience 54:545–551
Laitinen L (1987) Griffonia simplicifolia lectins bind specifically to endothelial cells and some epithelial cells in mouse tissues. Histochem J 19:225–234
Lawrentjew BJ (1931) Zur Lehre von der Cytoarchitektonik des peripheren autonomen Nervensystems. 1. Die Cytoarchitektonik der Ganglien des Verdauungskanals beim Hunde. Z Mikrosk Anat Forsch 23:527–551
Lomax AEG, Furness JB (2000) Neurochemical classification of enteric neurons in the guinea-pig distal colon. Cell Tissue Res 302:59–73
Lu J, Zhou XF, Rush RA (2001) Small primary sensory neurons innervating epidermis and viscera display differential phenotype in the adult rat. Neurosci Res 41:355–363
Lundgren O (2002) Enteric nerves and diarrhoea. Pharmacol Toxicol 90:109–120
Lundgren O, Peregrin AT, Persson K, Kordasti S, Uhnoo I, Svensson L (2000) Role of the enteric nervous system in the fluid and electrolyte secretion of rotavirus diarrhea. Science 287:491–495
Maddox DE, Shibata S, Goldstein IJ (1982) Stimulated macrophages express a new glycoprotein receptor reactive with Griffonia simplicifolia I-B4 isolectin. Proc Natl Acad Sci USA 79:166–170
Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201–211
Pan H, Gershon MD (2000) Activation of intrinsic afferent pathways in submucosal ganglia of the guinea pig small intestine. J Neurosci 20:3295–3309
Quinson N, Robbins HL, Clark MJ, Furness JB (2001) Calbindin immunoreactivity of enteric neurons in the guinea-pig small intestine. Cell Tissue Res 305:3–9
Rugiero F, Gola M, Kunze WAA, Reynaud J-C, Furness JB, Clerc N (2002) Analysis of whole cell currents by patch clamp of guinea-pig myenteric neurones in intact ganglia. J Physiol (Lond) 538:447–463
Rugiero F, Mistry M, Sage D, Black JA, Waxman SG, Crest M, Clerc N, Delmas P, Gola M (2003) Selective expression of a persistent TTX-resistant Na+ current and Nav1.9 subunit in myenteric sensory neurons. J Neurosci 23:2715–2725
Schemann M, Wood JD (1989) Electrical behaviour of myenteric neurones in the gastric corpus of the guinea-pig. J Physiol (Lond) 417:501–518
Silverman JD, Kruger L (1990) Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J Neurocytol 19:789–801
Song ZM, Brookes SJH, Costa M (1991) Identification of myenteric neurons which project to the mucosa of the guinea-pig small intestine. Neurosci Lett 129:294–298
Streit WJ, Schulte BA, Balentine JD, Spicer SS (1985) Histochemical localization of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat. J Histochem Cytochem 33:1042–1052
Stucky CL, Lewin GR (1999) Isolectin B4-positive and -negative nociceptors are functionally distinct. J Neurosci 19:6497–6505
Tack JF, Wood JD (1992) Electrical behaviour of myenteric neurones in the gastric antrum of the guinea-pig. J Physiol (Lond) 447:49–66
Vallance BA, Blennerhassett PA, Collins SM (1997) Increased intestinal muscle contractility and worm expulsion in nematode-infected mice. Am J Physiol 272:G321–G327
Yoshida S, Matsuda Y, Samejima A (1978) Tetrodotoxin-resistant sodium and calcium components of action potentials in dorsal root ganglion cells of the adult mouse. J Neurophysiol 41:1096–1106
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by a grant from the National Health and Medical Council of Australia.
Rights and permissions
About this article
Cite this article
Hind, A., Migliori, M., Thacker, M. et al. Primary afferent neurons intrinsic to the guinea-pig intestine, like primary afferent neurons of spinal and cranial sensory ganglia, bind the lectin, IB4. Cell Tissue Res 321, 151–157 (2005). https://doi.org/10.1007/s00441-005-1129-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-005-1129-1