Calretinin and Somatostatin Immunoreactivities Label Different Human Submucosal Neuron Populations

Anatomical Record

Volumn 294, Issue 5, 2011, Pages 858-869

  Kustermann, Andreas ^a   Neuhuber, Winfried ^a   Brehmer, Axel ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Chemical coding; Enteric nervous system; Gut; Innervation; Neuron type; Submucosal plexus

Indexed keywords

CALRETININ; HU PROTEIN; PERIPHERIN; SOMATOSTATIN;

AGED; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CELL STRUCTURE; CLINICAL ARTICLE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADULT; AGED; AGED, 80 AND OVER; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CHILD; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; INTERMEDIATE FILAMENT PROTEINS; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; NERVE TISSUE PROTEINS; NEURONS; SOMATOSTATIN; SUBMUCOUS PLEXUS; YOUNG ADULT;

CAVIA;

EID: 79954494796     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21365     Document Type: Article

References (65)

1. Accili EA, Dhatt N, Buchan AM. 1995. Neural somatostatin, vasoactive intestinal polypeptide and substance P in canine and human jejunum. Neurosci Lett 185: 37-40.
2. Barshack I, Fridman E, Goldberg I, Chowers Y, Kopolovic J. 2004. The loss of calretinin expression indicates aganglionosis in Hirschsprung's disease. J Clin Pathol 57: 712-716.
3. Beck M, Schlabrakowski A, Schrödl F, Neuhuber W, Brehmer A. 2009. ChAT and NOS in human myenteric neurons: co-existence and co-absence. Cell Tissue Res 338: 37-51.
4. Brehmer A. 2006. Structure of enteric neurons. Adv Anat Embryol Cell Biol 186: 1-94.
5. Brehmer A. 2007. The value of neurofilament-immunohistochemistry for identifying enteric neuron types-special reference to intrinsic primary afferent (sensory) neurons. In: Arlen RK, editor. New research on neurofilament proteins. New York: Nova Science Publishers. p 99-114.
6. Brehmer A, Blaser B, Seitz G, Schrödl F, Neuhuber W. 2004a. Pattern of lipofuscin pigmentation in nitrergic and non-nitrergic, neurofilament immunoreactive myenteric neuron types of human small intestine. Histochem Cell Biol 121: 13-20.
7. Brehmer A, Croner R, Dimmler A, Papadopoulos T, Schrödl F, Neuhuber W. 2004b. Immunohistochemical characterization of putative primary afferent (sensory) myenteric neurons in human small intestine. Auton Neurosci 112: 49-59.
8. Brehmer A, Rupprecht H, Neuhuber W. 2010. Two submucosal nerve plexus in human intestines. Histochem Cell Biol 133: 149-161.
9. Chiocchetti R, Bombardi C, Mongardi-Fantaguzzi C, Venturelli E, Russo D, Spadari A, Montoneri C, Romagnoli N, Grandis A. 2009. Intrinsic innervation of the horse ileum. Res Vet Sci 87: 177-185.
10. Chiocchetti R, Grandis A, Bombardi C, Lucchi ML, Dal Lago DT, Bortolami R, Furness JB. 2006. Extrinsic and intrinsic sources of calcitonin gene-related peptide immunoreactivity in the lamb ileum: a morphometric and neurochemical investigation. Cell Tissue Res 323: 183-196.
11. Crowe R, Kamm MA, Burnstock G, Lennard-Jones JE. 1992. Peptide-containing neurons in different regions of the submucous plexus of human sigmoid colon. Gastroenterology 102: 461-467.
12. De Fontgalland D, Wattchow DA, Costa M, Brookes SJ. 2008. Immunohistochemical characterization of the innervation of human colonic mesenteric and submucosal blood vessels. Neurogastroenterol Motil 20: 1212-1226.
13. Dhatt N, Buchan AM. 1994. Colocalization of neuropeptides with calbindin D28k and NADPH diaphorase in the enteric nerve plexuses of normal human ileum. Gastroenterology 107: 680-690.
14. Dogiel AS. 1899. Ueber den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugethiere. Arch Anat Physiol Anat Abt (Leipzig) 130-158.
15. Domoto T, Bishop AE, Oki M, Polak JM. 1990. An in vitro study of the projections of enteric vasoactive intestinal polypeptide-immunoreactive neurons in the human colon. Gastroenterology 98: 819-827.
16. Evans RJ, Jiang MM, Surprenant A. 1994. Morphological properties and projections of electrophysiologically characterized neurons in the guinea-pig submucosal plexus. Neuroscience 59: 1093-1110.
17. Furness JB. 2006. The enteric nervous system. Oxford: Blackwell.
18. Furness JB, Alex G, Clark MJ, Lal VV. 2003. Morphologies and projections of defined classes of neurons in the submucosa of the guinea-pig small intestine. Anat Rec A Discov Mol Cell Evol Biol 272: 475-483.
19. Furness JB, Robbins HL, Xiao J, Stebbing MJ, Nurgali K. 2004. Projections and chemistry of Dogiel type II neurons in the mouse colon. Cell Tissue Res 317: 1-12.
20. Ganns D, Schrödl F, Neuhuber W, Brehmer A. 2006. Investigation of general and cytoskeletal markers to estimate numbers and proportions of neurons in the human intestine. Histol Histopathol 21: 41-51.
21. Gershon MD, Kirchgessner AL, Wade PR. 1994. Functional anatomy of the enteric nervous system. In: Johnson LR, editor. Physiology of the gastrointestinal tract. 3rd ed. New York: Raven Press. p 381-422.
22. Guinard-Samuel V, Bonnard A, De Lagausie P, Philippe-Chomette P, Alberti C, El Ghoneimi A, Peuchmaur M, Berrebi-Binczak D. 2009. Calretinin immunohistochemistry: a simple and efficient tool to diagnose Hirschsprung disease. Mod Pathol 22: 1379-1384.
23. Hendriks R, Bornstein JC, Furness JB. 1990. An electrophysiological study of the projections of putative sensory neurons within the myenteric plexus of the guinea-pig ileum. Neurosci Lett 110: 286-290.
24. Hens J, Vanderwinden JM, De Laet MH, Scheuermann DW, Timmermans JP. 2001. Morphological and neurochemical identification of enteric neurones with mucosal projections in the human small intestine. J Neurochem 76: 464-471.
25. Hoyle CH, Burnstock G. 1989. Galanin-like immunoreactivity in enteric neurons of the human colon. J Anat 166: 23-33.
26. Kapur RP, Reed RC, Finn LS, Patterson K, Johanson J, Rutledge JC. 2009. Calretinin immunohistochemistry versus acetylcholinesterase histochemistry in the evaluation of suction rectal biopsies for Hirschsprung Disease. Pediatr Dev Pathol 12: 6-15.
27. Knowles CH, De Giorgio R, Kapur RP, Bruder E, Farrugia G, Geboes K, Gershon MD, Hutson J, Lindberg G, Martin JE, Meier-Ruge WA, Milla PJ, Smith VV, Vandervinden JM, Veress B, Wedel T. 2009. Gastrointestinal neuromuscular pathology: guidelines for histological techniques and reporting on behalf of the Gastro 2009 International Working Group. Acta Neuropathol 118: 271-301.
28. Koelliker A. 1896. Handbuch der Gewebelehre des Menschen. II. Bd.: Nervensystem des Menschen und der Thiere. Leipzig: Engelmann.
29. Michel K, Zeller F, Langer R, Nekarda H, Kruger D, Dover TJ, Brady CA, Barnes NM, Schemann M. 2005. Serotonin excites neurons in the human submucous plexus via 5-HT3 receptors. Gastroenterology 128: 1317-1326.
30. Mitsui R. 2009. Characterisation of calcitonin gene-related peptide-immunoreactive neurons in the myenteric plexus of rat colon. Cell Tissue Res 337: 37-43.
31. Mitsui R. 2010. Immunohistochemical characteristics of submucosal Dogiel type II neurons in rat colon. Cell Tissue Res 340: 257-265.
32. Mongardi Fantaguzzi C, Thacker M, Chiocchetti R, Furness JB. 2009. Identification of neuron types in the submucosal ganglia of the mouse ileum. Cell Tissue Res 336: 179-189.
33. Murphy EM, Defontgalland D, Costa M, Brookes SJ, Wattchow DA. 2007. Quantification of subclasses of human colonic myenteric neurons by immunoreactivity to Hu, choline acetyltransferase and nitric oxide synthase. Neurogastroenterol Motil 19: 126-134.
34. Phillips RJ, Hargrave SL, Rhodes BS, Zopf DA, Powley TL. 2004. Quantification of neurons in the myenteric plexus: an evaluation of putative pan-neuronal markers. J Neurosci Methods 133: 99-107.
35. Pimont S, Bruley Des Varannes S, Le Neel JC, Aubert P, Galmiche JP, Neunlist M. 2003. Neurochemical coding of myenteric neurones in the human gastric fundus. Neurogastroenterol Motil 15: 655-662.
36. Porter AJ, Wattchow DA, Brookes SJ, Costa M. 1997. The neurochemical coding and projections of circular muscle motor neurons in the human colon. Gastroenterology 113: 1916-1923.
37. Porter AJ, Wattchow DA, Brookes SJ, Costa M. 1999. Projections of nitric oxide synthase and vasoactive intestinal polypeptide-reactive submucosal neurons in the human colon. J Gastroenterol Hepatol 14: 1180-1187.
38. Porter AJ, Wattchow DA, Brookes SJ, Costa M. 2002. Cholinergic and nitrergic interneurones in the myenteric plexus of the human colon. Gut 51: 70-75.
39. Porter AJ, Wattchow DA, Brookes SJ, Schemann M, Costa M. 1996. Choline acetyltransferase immunoreactivity in the human small and large intestine. Gastroenterology 111: 401-408.
40. Quartu M, Polak JM, Del Fiacco M. 1993. Neuropeptides in the human celiac/superior mesenteric ganglionic complex: an immunohistochemical study. J Chem Neuroanat 6: 79-99.
41. Ramón y Cajal S. 1911. Histologie du système nerveux de l'homme et des vertébrés. Paris: Maloine.
42. Rossi O. 1929. Contributo alla conoscenza degli apparati nervosi intramurali dell' intestino tenue. Arch Ital Anat 26: 632-644.
43. Schabadasch A. 1930. Intramurale Nervengeflechte des Darmrohrs. Z Zellforsch Mikrosk Anat 10: 320-385.
44. Schemann M, Mazzuoli G. 2010. Multifunctional mechanosensitive neurons in the enteric nervous system. Auton Neurosci 153: 21-25.
45. Scheuermann DW, Stach W, De Groodt-Lasseel MH, Timmermans JP. 1987. Calcitonin gene-related peptide in morphologically well-defined type II neurons of the enteric nervous system in the porcine small intestine. Acta Anat 129: 325-328.
46. Schnell SA, Staines WA, Wessendorf MW. 1999. Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47: 719-730.
47. Smith TK, Spencer NJ, Hennig GW, Dickson EJ. 2007. Recent advances in enteric neurobiology: mechanosensitive interneurons. Neurogastroenterol Motil 19: 869-878.
48. Sokolova ML. 1931. Zur Lehre von der Cytoarchitektonik des peripherischen autonomen Nervensystems. II. Die Architektur der intramuralen Ganglien des Verdauungstrakts des Rindes. Z Mikrosk Anat Forsch 23: 552-570.
49. Spencer NJ, Smith TK. 2004. Mechanosensory S-neurons rather than AH-neurons appear to generate a rhythmic motor pattern in guinea-pig distal colon. J Physiol 558.2: 577-596.
50. Stach W. 1977. Der Plexus submucosus externus (Schabadasch) im Dünndarm des Schweins. I. Form, Struktur und Verbindungen der Ganglien und Nervenzellen. Z Mikrosk Anat Forsch 91: 737-755.
51. Stach W. 1980. Zur neuronalen Organisation des Plexus myentericus (Auerbach) im Schweinedünndarm. I. Typ I-Neurone. Z Mikrosk Anat Forsch 94: 833-849.
52. Stach W. 1981. Zur neuronalen Organisation des Plexus myentericus (Auerbach) im Schweinedünndarm. II. Typ II-Neurone. Z Mikrosk Anat Forsch 95: 161-182.
53. Stach W. 1982. Zur neuronalen Organisation des Plexus myentericus (Auerbach) im Schweinedünndarm. III. Typ III-Neurone. Z Mikrosk Anat Forsch 96: 497-516.
54. Stach W. 1989. A revised morphological classification of neurons in the enteric nervous system. In: Singer MV, Goebell H, editors. Nerves and the gastrointestinal tract. Lancaster: Kluwer. p 29-45.
55. Stach W, Krammer HJ, Brehmer A. 2000. Structural organization of enteric nerve cells in large mammals including man. In: Krammer HJ, Singer MV, editors. Neurogastroenterology from the basics to the clinics. Dordrecht: Kluwer. p 3-20.
56. Stöhr P. 1949. Mikroskopische Studien zur Innervation des Magen-Darmkanales V. Z Zellforsch Mikrosk Anat 34: 1-54.
57. Timmermans JP, Hens J, Adriaensen D. 2001. Outer submucous plexus: an intrinsic nerve network involved in both secretory and motility processes in the intestine of large mammals and humans. Anat Rec 262: 71-78.
58. Timmermans JP, Scheuermann DW, Barbiers M, Adriaensen D, Stach W, Van Hee R, De Groodt-Lasseel MH. 1992. Calcitonin gene-related peptide-like immunoreactivity in the human small intestine. Acta Anat (Basel) 143: 48-53.
59. Van Nassauw L, Wu M, De Jonge F, Adriaensen D, Timmermans JP. 2005. Cytoplasmic, but not nuclear, expression of the neuronal nuclei (NeuN) antibody is an exclusive feature of Dogiel type II neurons in the guinea-pig gastrointestinal tract. Histochem Cell Biol 124: 369-377.
60. Wattchow DA, Brookes SJ, Costa M. 1995. The morphology and projections of retrogradely labeled myenteric neurons in the human intestine. Gastroenterology 109: 866-875.
61. Wattchow DA, Porter AJ, Brookes SJ, Costa M. 1997. The polarity of neurochemically defined myenteric neurons in the human colon. Gastroenterology 113: 497-506.
62. Weidmann S, Schrödl F, Neuhuber W, Brehmer A. 2007. Quantitative estimation of putative primary afferent neurons in the myenteric plexus of human small intestine. Histochem Cell Biol 128: 399-407.
63. Wolf M, Schrödl F, Neuhuber W, Brehmer A. 2007. Calcitonin gene-related peptide: a marker for putative primary afferent neurons in the pig small intestinal plexus? Anat Rec 290: 1273-1279.
64. Wong V, Blennerhassett M, Vanner S. 2008. Electrophysiological and morphological properties of submucosal neurons in the mouse distal colon. Neurogastroenterol Motil 20: 725-734.
65. Wood JD. 1994. Physiology of the enteric nervous system. In: Johnson LR, editor. Physiology of the gastrointestinal tract. New York: Paven Press. p 423-482.