Expression of neuropeptides and anoctamin 1 in the embryonic and adult zebrafish intestine, revealing neuronal subpopulations and ICC-like cells

Cell and Tissue Research

Volumn 354, Issue 2, 2013, Pages 355-370

  Uyttebroek, Leen ^a   Shepherd, Iain T ^b   Hubens, Guy ^a   Timmermans, Jean Pierre ^a   Van Nassauw, Luc ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b EMORY UNIVERSITY   (United States)

Author keywords

Anoctamin 1; Enteric nervous system; Interstitial cells of Cajal; Neuropeptides; Zebrafish

Indexed keywords

ANOCTAMIN 1; BIOLOGICAL MARKER; CALBINDIN; CALCITONIN GENE RELATED PEPTIDE; CALRETININ; CHOLINE ACETYLTRANSFERASE; GALANIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; NEURONAL NITRIC OXIDE SYNTHASE; NEUROPEPTIDE; SEROTONIN; SUBSTANCE P; TACHYKININ; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; EMBRYO; IMMUNOCOMPETENT CELL; INTERSTITIAL CELL OF CAJAL; INTESTINE INNERVATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ZEBRA FISH;

DANIO RERIO; MAMMALIA;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM CHANNELS; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELLS OF CAJAL; INTESTINES; NEURONS; NEUROPEPTIDES; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; VASOACTIVE INTESTINAL PEPTIDE; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84888293911     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1685-8     Document Type: Article

References (94)

1. Badawy G, Reinecke M (2003) Ontogeny of the VIP system in the gastro-intestinal tract of the axolotl, Ambystoma mexicanum: successive appearance of co-existing PACAP and NOS. Anat Embryol 206:319-325
2. Ball ER, Matsuda MM, Dye L, Hoffmann V, Zerfas PM, Szarek E, Rich A, Chitnis AB, Stratakis CA (2012) Ultra-structural identification of interstitial cells of Cajal in the zebrafish Danio rerio. Cell Tissue Res 349:483-491
3. Bermudez R, Vigliano F, Quiroga MI, Nieto JM, Bosi G, Domeneghini C (2007) Immunohistochemical study on the neuroendocrine system of the digestive tract of turbot, Scophthalmus maximus (L.), infected by Enteromyxum scophthalmi (Myxozoa). Fish Shellfish Immunol 22:252-263
4. Bjenning C, Holmgren S (1988) Neuropeptides in the fish gut. An immunohistochemical study of evolutionary patterns. Histochemistry 88:155-163
5. Bosi G, Di Giancamillo A, Arrighi S, Domeneghini C (2004) An immunohistochemical study on the neuroendocrine system in the alimentary canal of the brown trout, Salmo trutta, L., 1758. Gen Comp Endocrinol 138:166-181
6. Bosi G, Domeneghini C, Arrighi S, Giari L, Simoni E, Dezfuli BS (2005) Response of the gut neuroendocrine system of Leuciscus cephalus (L.) to the presence of Pomphorhynchus laevis Müller, 1776 (Acanthocephala). Histol Histopathol 20:509-518
7. Bosi G, Shinn AP, Simoni E, Arrighi S, Domeneghini C (2006) A comparative immunohistochemical study on a galanin-like peptide in the neuroendocrine system of the alimentary canal of three species of siluriform catfishes. J Fish Biol 68:86-100
8. Bosi G, Bermudez R, Domeneghini C (2007) The galaninergic enteric nervous system of pleuronectiformes (Pisces, Osteichthyes): an immunohistochemical and confocal laser scanning immunofluorescence study. Gen Comp Endocrinol 152:22-29
9. Brookes SJ (2001) Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 262:58-70
10. Burns AJ, Roberts RR, Bornstein JC, Young HM (2009) Development of the enteric nervous system and its role in intestinal motility during fetal and early postnatal stages. Semin Pediatr Surg 18:196-205
11. Castro A, Becerra M, Manso MJ, Anadon R (2006) Calretinin immunoreactivity in the brain of the zebrafish, Danio rerio: distribution and comparison with some neuropeptides and neurotransmitter-synthesizing enzymes. II. Midbrain, hindbrain, and rostral spinal cord. J Comp Neurol 494:792-814
12. Chino Y, Fujimura M, Kitahama K, Fujimiya M (2002) Colocalization of NO and VIP in neurons of the submucous plexus in the rat intestine. Peptides 23:2245-2250
13. Collins SM, Van Assche G, Hogaboam C (1997) Alterations in enteric nerve and smooth-muscle function in inflammatory bowel diseases. Inflam Bowel Dis 3:38-48
14. Dezfuli BS, Pironi F, Giari L, Domeneghini C, Bosi G (2002) Effect of Pomphorhynchus laevis (Acanthocephala) on putative neuromodulators in the intestine of naturally infected Salmo trutta. Dis Aquat Org 51:27-35
15. Dezfuli BS, Pironi F, Shinn AP, Manera M, Giari L (2007) Histopathology and ultrastructure of Platichthys flesus naturally infected with Anisakis simplex s.l. larvae (Nematoda: Anisakidae). J Parasitol 93:1416-1423
16. Domeneghini C, Radaelli G, Arrighi S, Mascarello F, Veggetti A (2000) Neurotransmitters and putative neuromodulators in the gut of Anguilla anguilla (L.). Localizations in the enteric nervous and endocrine systems. Eur J Histochem 44:295-306
17. Ekblad E, Mulder H, Sundler F (1996) Vasoactive intestinal peptide expression in enteric neurons is upregulated by both colchicine and axotomy. Regul Pept 63:113-121
18. Freytag C, Seeger J, Siegemund T, Grosche J, Grosche A, Freeman DE, Schusser GF, Hartig W (2008) Immunohistochemical characterization and quantitative analysis of neurons in the myenteric plexus of the equine intestine. Brain Res 1244:53-64
19. Furness JB (2006) The enteric nervous system. Blackwell, Oxford
20. Furness JB (2012) The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 9:286-294
21. Furness JB, Pompolo S, Murphy R, Giraud A (1989) Projections of neurons with neuromedin U-like immunoreactivity in the small intestine of the guinea-pig. Cell Tissue Res 257:415-422
22. Garcia-Lopez P, Garcia-Marin V, Martinez-Murillo R, Freire M (2009) Updating old ideas and recent advances regarding the interstitial cells of Cajal. Brain Res Rev 61:154-169
23. Gomez-Pinilla PJ, Gibbons SJ, Bardsley MR, Lorincz A, Pozo MJ, Pasricha PJ, Van de Rijn M, West RB, Sarr MG, Kendrick ML, Cima RR, Dozois EJ, Larson DW, Ordog T, Farrugia G (2009) Ano1 is a selective marker of interstitial cells of Cajal in the human and mouse gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 296:G1370-G1381
24. Grider JR (1994) CGRP as a transmitter in the sensory pathway mediating peristaltic reflex. Am J Physiol Gastrointest Liver Physiol 266:G1139-G1145
25. Grider JR (2003) Neurotransmitters mediating the intestinal peristaltic reflex in the mouse. J Pharmacol Exp Ther 307:460-467
26. Grunwald DJ, Eisen JS (2002) Headwaters of the zebrafish - emergence of a new model vertebrate. Nat Rev Genet 3:717-724
27. Hannibal J, Ekblad E, Mulder H, Sundler F, Fahrenkrug J (1998) Pituitary adenylate cyclase activating polypeptide (PACAP) in the gastrointestinal tract of the rat: distribution and effects of capsaicin or denervation. Cell Tissue Res 291:65-79
28. Holmberg A, Hägg U, Fritsche R, Holmgren S (2001) Occurrence of neurotrophin receptors and transmitters in the developing Xenopus gut. Cell Tissue Res 306:35-47
29. Holmberg A, Schwerte T, Fritsche R, Pelster B, Holmgren S (2003) Ontogeny of intestinal motility in correlation to neuronal development in zebrafish embryo and larvae. J Fish Biol 63:318-331
30. Holmberg A, Schwerte T, Pelster B, Holmgren S (2004) Ontogeny of the gut motility control system in zebrafish Danio rerio embryos and larvae. J Exp Biol 207:4085-4094
31. Holmberg A, Olsson C, Hennig GW (2007) TTX-sensitive and TTX-insensitive control of spontaneous gut motility in the developing zebrafish (Danio rerio) larvae. J Exp Biol 210:1084-1091
32. Holmgren S, Jensen J (2001) Evolution of vertebrate neuropeptides. Brain Res Bull 55:723-735
33. Holmgren S, Vaillant C, Dimaline R (1982) VIP-, substance P-, gastrin/CCK-, bombesin-, somatostatin- and glucagon-like immunoreactivities in the gut of the rainbow trout, Salmo gairdneri. Cell Tissue Res 223:141-153
34. Holzer P, Schicho R, Holzer-Petsche U, Lippe IT (2001) The gut as a neurological organ. Wien Klin Wochenschr 113:647-660
35. Hwang SJ, Blair PJ, Britton FC, O'Driscoll KE, Hennig G, Bayguinov YR, Rock JR, Harfe BD, Sanders KM, Ward SM (2009) Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol 587:4887-4904
36. Jensen J, Conlon JM (1992) Substance-P-related and neurokinin-A-related peptides from the brain of the cod and trout. Eur J Biochem 206:659-664
37. Jensen J, Holmgren S (1985) Neurotransmitters in the intestine of the Atlantic cod, Gadus morhua. Comp Biochem Physiol C 82:81-89
38. Jensen J, Holmgren S, Jonsson AC (1987) Substance P-like immunoreactivity and the effects of tachykinins in the intestine of the Atlantic cod, Gadus morhua. J Auton Nerv Syst 20:25-33
39. Jensen J, Karila P, Jönsson A-C, Aldman G, Holmgren S (1993a) Effects of substance P and distribution of substance P-like immunoreactivity in nerves supplying the stomach of the cod, Gadus morhua. Fish Physiol Biochem 12:237-247
40. Jensen J, Olson KR, Conlon JM (1993b) Primary structures and effects on gastrointestinal motility of tachykinins from the rainbow trout. Am J Physiol Regul Integr Comp Physiol 265:R804-R810
41. 2+-recruitment in tachykinin-induced contractions of gut smooth muscle from African clawed frog, Xenopus laevis and rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 131:185-191
42. Johnson RJR, Schemann M, Santer RM, Cowen T (1998) The effects of age on the overall population and on subpopulations of myenteric neurons in the rat small intestine. J Anat 192:479-488
43. Kågström J, Holmgren S (1998) Calcitonin gene-related peptide (CGRP), but not tachykinins, causes relaxation of small arteries from the rainbow trout gut. Peptides 19:577-584
44. Kapp S, Schrodl F, Neuhuber W, Brehmer A (2006) Chemical coding of submucosal type V neurons in porcine ileum. Cells Tissues Organs 184:31-41
45. Karila P, Holmgren S (1997) Anally projecting neurons exhibiting immunoreactivity to galanin, nitric oxide synthase and vasoactive intestinal peptide, detected by confocal laser scanning microscopy, in the intestine of the Atlantic cod, Gadus morhua. Cell Tissue Res 287:525-533
46. Karila P, Jonsson AC, Jensen J, Holmgren S (1993) Galanin-like immunoreactivity in extrinsic and intrinsic nerves to the gut of the Atlantic cod, Gadus morhua, and the effect of galanin on the smooth muscle of the gut. Cell Tissue Res 271:537-544
47. Karila P, Shahbazi F, Jensen J, Holmgren S (1998) Projections and actions of tachykininergic, cholinergic, and serotonergic neurones in the intestine of the atlantic cod. Cell Tissue Res 291:403-413
48. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310
49. Kitazawa T, Itoh K, Yaosaka N, Maruyama K, Matsuda K, Teraoka H, Kaiya H (2012) Ghrelin does not affect gastrointestinal contractility in rainbow trout and goldfish in vitro. Gen Comp Endocrinol 178:539-545
50. Klüppel M, Huizinga JD, Malysz J, Bernstein A (1998) Developmental origin and Kit-dependent development of the interstitial cells of Cajal in the mammalian intestine. Dev Dyn 211:60-71
51. Komuro T (2006) Structure and organization of interstitial cells of Cajal in the gastrointestinal tract. J Physiol 576:653-658
52. Kuhlman J, Eisen JS (2007) Genetic screen for mutations affecting development and function of the enteric nervous system. Dev Dyn 236:118-127
53. Li ZS, Murphy S, Furness JB, Young HM, Campbell G (1993) Relationships between nitric oxide synthase, vasoactive intestinal peptide and substance P immunoreactivities in neurons of the amphibian intestine. J Auton Nerv Syst 44:197-206
54. Lu B, Fu WM, Greengard P, Poo MM (1993) Calcitonin gene-related peptide potentiates synaptic responses at developing neuromuscular juntion. Nature 363:76-79
55. Martinez-Alvarez RM, Volkoff H, Munoz Cueto JA, Delgado MJ (2008) Molecular characterization of calcitonin gene-related peptide (CGRP) related peptides (CGRP, amylin, adrenomedullin and adrenomedullin-2/intermedin) in goldfish (Carassius auratus): cloning and distribution. Peptides 29:1534-1543
56. Matthews M, Trevarrow B, Matthews J (2002) A virtual tour of the Guide for zebrafish users. Lab Anim 31:34-40
57. Mazzone A, Eisenman ST, Yao Z, Ordog T, Gibbons SJ, Farrugia G (2012) Smooth muscle interstitial cells of Cajal pacing/electrical stimulation electrogastrography. Gastroenterology 142(Suppl 1):S29
58. McConalogue K, Furness JB, Vremec MA, Holst JJ, Tornøe K, Marley PD (1995) Histochemical, pharmacological, biochemical and chromatographic evidence that pituitary adenyl cyclase activating peptide is involved in inhibitory neurotransmission in the taenia of the guinea-pig caecum. J Auton Nerv Syst 50:311-322
59. Mirabella N, Lamanna C, Assisi L, Botte V, Cecio A (2000) The relationships of nicotinamide adenine dinucleotide phosphate-d to nitric oxide synthase, vasoactive intestinal polypeptide, galanin and pituitary adenylate activating peptide (PACAP) in pigeon gut neurons. Neurosci Lett 293:147-151
60. Mirabella N, Squillacioti C, Colitti M, Germano G, Pelagalli A, Paino G (2002) Pituitary adenylate cyclase activating peptide (PACAP) immunoreactivity and mRNA expression in the duck gastrointestinal tract. Cell Tissue Res 308:347-359
61. Mitsui R (2010) Immunohistochemical characteristics of submucosal Dogiel type II neurons in rat colon. Cell Tissue Res 340:257-265
62. Negoescu A, Labat-Moleur F, Lorimier P, Lamarcq L, Guillermet C, Chambaz E, Brambilla E (1994) F(ab) secondary antibodies: a general method for double immunolabeling with primary antisera from the same species. Efficiency control by chemiluminescence. J Histochem Cytochem 42:433-437
63. Ng ANY, de Jong-Curtain TA, Mawdsley DJ, White SJ, Shin J, Appel B, Dong PD, Stainier DY, Heatj JK (2005) Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis. Dev Biol 286:114-135
64. Ohtani R, Kaneko T, Kline LW, Labedz T, Tang Y, Pang PKT (1989) Localization of calcitonin gene-related peptide in the small intestine of various vertebrate species. Cell Tissue Res 258:35-42
65. Olsson C (2002) Distribution and effects of PACAP, VIP, nitric oxide and GABA in the gut of the African clawed frog Xenopus laevis. J Exp Biol 205:1123-1134
66. Olsson C (2009) Autonomic innervation of the fish gut. Acta Histochem 111:185-195
67. Olsson C, Holmgren S (1994) Distribution of PACAP (pituitary adenylate cyclase-activating polypeptide)-like and helospectin-like peptides in the teleost gut. Cell Tissue Res 277:539-547
68. Olsson C, Holmgren S (2001) The control of gut motility. Comp Biochem Physiol A 128:481-503
69. Olsson C, Karila P (1995) Coexistence of NAPDPH-diaphorase and vasoactive intestinal polypeptide in the enteric nervous system of the Atlantic cod (Gadus morhua) and the spiny dogfish (Squalus acanthias). Cell Tissue Res 280:297-305
70. Olsson C, Holmberg A, Holmgren S (2008) Development of enteric and vagal innervation of the zebrafish (Danio rerio) gut. J Comp Neurol 508:756-770
71. Pederzoli A, Bertacchi I, Gambarelli A, Mola L (2004) Immunolocalisation of vasoactive intestinal peptide and substance P in the developing gut of Dicentrarchus labrax (L.). Eur J Histochem 48:179-184
72. Portbury AL, Pompolo S, Furness JB, Stebbing MJ, Kunze WA, Bornstein JC, Hughes S (1995) Cholinergic, somatostatin-immunoreactive interneurons in the guinea pig intestine: morphology, ultrastructure, connections and projections. J Anat 187:303-321
73. Qu ZD, Thacker M, Castelucci P, Bagyanszki M, Epstein ML, Furness JB (2008) Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res 334:147-161
74. Rich A, Leddon SA, Hess SL, Gibbons SJ, Miller S, Xu X, Farrugia G (2007) Kit-like immunoreactivity in the zebrafish gastrointestinal tract reveals putative ICC. Dev Dyn 236:903-911
75. Roch GJ, Wu S, Sherwood NM (2009) Hormones and receptors in fish: do duplicates matter? Gen Comp Endocrinol 161:3-12
76. Salvi E, Vaccaro R, Rendag TG (1999) Ontogeny of galanin-immunoreactive elements in the intrinsic nervous system of the chicken gut. Anat Rec 254:28-38
77. Salvi EP, Vaccaro R, Renda TG (2000) Ontogeny of PACAP immunoreactivity in extrinsic and intrinsic innervation of chicken gut. Peptides 21:1703-1709
78. Sanders KM, Zhu MH, Britton F, Koh SD, Ward SM (2011) Anoctamins and gastrointestinal smooth muscle excitability. Exp Physiol 97:200-206
79. Shahbazi F, Karila P, Olsson C, Holmgren S, Conlon JM, Jensen J (1998) Primary structure, distribution, and effects on motility of CGRP in the intestine of the cod, Gadus morhua. Am J Physiol Regul Integr Comp Physiol 275:R19-R28
80. Shen Z, Larsson LT, Malmfors G, Absood A, Håkanson R, Sundler F (1992) A novel neuropeptide, pituitary adenylate cyclase-activating polypeptide (PACAP), in human intestine: evidence for reduced content in Hirschsprung's disease. Cell Tissue Res 269:369-374
81. Shepherd I, Eisen J (2011) Development of the zebrafish enteric nervous system. Methods Cell Biol 101:143-160
82. Stanich JE, Gibbons SJ, Eisenman ST, Bardsley MR, Rock JR, Harfe BD, Ordog T, Farugia G (2011) Ano1 as a regulator of proliferation. Am J Physiol Gastrointest Liver Physiol 301:G1044-G1051
83. Sundler F, Ekblad E, Absood A, Håkanson R, Köves K, Arimura A (1992) Pituitary adenylate cyclase activating peptide: a novel vasoactive intestinal peptide-like neuropeptide in the gut. Neuroscience 46:439-454
84. Terkeltaub RA (2009) Colchicine update: 2008. Semin Arthritis Rheum 38:411-419
85. Timmermans JP, Adriaensen D, Cornelissen W, Scheuermann DW (1997) Structural organization and neuropeptide distribution in the mammalian enteric nervous system, with special attention to those components involved in mucosal reflexes. Comp Biochem Physiol A 118:331-340
86. Torihashi S, Ward SM, Sanders KM (1997) Development of c-Kit-positive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology 112:144-155
87. Uyttebroek L, Shepherd IT, Harrisson F, Hubens G, Blust R, Timmermans JP, Van Nassauw L (2010) Neurochemical coding of enteric neurons in adult and embryonic zebrafish (Danio rerio). J Comp Neurol 518:4419-4438
88. Vigliano FA, Munoz L, Hernandez D, Cerutti P, Bermudez R, Quiroga MI (2011) An immunohistochemical study of the gut neuroendocrine system in juvenile pejerrey Odontesthes bonariensis (Valenciennes). J Fish Biol 78:901-911
89. Wallace AS, Burns AJ (2005) Development of the enteric nervous system, smooth muscle and interstitial cells of Cajal in the human gastrointestinal tract. Cell Tissue Res 319:367-382
90. Wallace KN, Akhter S, Smith EM, Lorent K, Pack M (2005) Intestinal growth and differentiation in zebrafish. Mech Dev 122:157-173
91. Wang Y, Wong AO, Ge W (2003) Cloning, regulation of messenger ribonucleic acid expression, and function of a new isoform of pituitary adenylate cyclase-activating polypeptide in the zebrafish ovary. Endocrinology 144:4799-4810
92. Ward SM, Sanders KM, Hirst GD (2004) Role of interstitial cells of Cajal in neural control of gastrointestinal smooth muscles. Neurogastroenterol Motil 16(Suppl 1):112-117
93. Wattchow DA, Porter AJ, Brookes SJH, Costa M (1997) The polarity of neurochemically defined myenteric neurons in the human colon. Gastroenterology 113:497-506
94. Westerfield M (2007) The zebrafish book a guide for the laboratory use of zebrafish Danio Rerio. Univiversity of Oregon Press, Eugene