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Glial cells revealed by GFAP immunoreactivity in fish gut

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Abstract

Glial fibrillary acidic protein (GFAP) is a commonly used marker to identify enteric glia in the mammalian gut. Little is however known about enteric glia in other vertebrates. The aim of the present study was to examine the distribution of GFAP immunoreactivity in adult and developing fish. In adult shorthorn sculpin (Myoxocephalus scorpius) and zebrafish (Danio rerio), GFAP immunoreactivity was seen in the myenteric plexus in all regions of the gut. Co-staining for the neuronal markers Hu C/D and acetylated tubulin showed that GFAP immunoreactivity was not associated with nerves. GFAP immunoreactivity was predominantly seen in processes with few glial cell bodies being demonstrated in adult fish. GFAP immunoreactivity was also found in the gut in larval zebrafish from 3 days post-fertilisation, i.e. at approximately the same time that differentiated enteric nerve cells first occur. Immunoreactivity was most prominent in areas with no or a low density of Hu-immunoreactive nerve cell bodies, indicating that the developing glia follows a different pattern from that of enteric neurons. The results suggest that GFAP can be used as a marker for enteric glia in fish, as in birds and mammals. The distribution of GFAP immunoreactivity implies that enteric glia are widespread in the fish gastrointestinal tract. Glia and neurons diverge early during development of the gastrointestinal tract.

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References

  • Aube AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, Doulay F, Liblau R, Galmiche JP, Neunlist M (2006) Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55:630–637

    Article  CAS  PubMed  Google Scholar 

  • Balaskas C, Gabella G (1998) Glial fibrillary acidic protein (GFAP) immunoreactivity in enteric ganglia of the chick embryo. Brain Res 804:275–283

    Article  CAS  PubMed  Google Scholar 

  • Barres BA (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60:430–440

    Article  CAS  PubMed  Google Scholar 

  • Bassotti G, Villanacci V, Antonelli E, Morelli A, Salerni B (2007a) Enteric glial cells: new players in gastrointestinal motility? Lab Invest 87:628–632

    Article  CAS  PubMed  Google Scholar 

  • Bassotti G, Villanacci V, Fisogni S, Rossi E, Baronio P, Clerici C, Maurer CA, Cathomas G, Antonelli E (2007b) Enteric glial cells and their role in gastrointestinal motor abnormalities: introducing the neuro-gliopathies. World J Gastroenterol 13:4035–4041

    CAS  PubMed  Google Scholar 

  • Bernardos RL, Raymond PA (2006) GFAP transgenic zebrafish. Gene Expr Patterns 6:1007–1013

    Article  CAS  PubMed  Google Scholar 

  • Bisgrove BW, Raible DW, Walter V, Eisen JS, Grunwald DJ (1997) Expression of c-ret in the zebrafish embryo: potential roles in motoneuronal development. J Neurobiol 33:749–768

    Article  CAS  PubMed  Google Scholar 

  • Björklund H, Dahl D, Seiger A (1984) Neurofilament and glial fibrillary acid protein-related immunoreactivity in rodent enteric nervous system. Neuroscience 12:277–287

    Article  PubMed  Google Scholar 

  • Boyen GB von, Steinkamp M, Reinshagen M, Schafer KH, Adler G, Kirsch J (2004) Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 53:222–228

    Article  Google Scholar 

  • Boyen GB von, Steinkamp M, Adler G, Kirsch J (2006) Glutamate receptor subunit expression in primary enteric glia cultures. J Recept Signal Transduct Res 26:329–336

    Article  Google Scholar 

  • Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH, Sofroniew MV (1998) Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93:189–201

    Article  CAS  PubMed  Google Scholar 

  • Conner PJ, Focke PJ, Noden DM, Epstein ML (2003) Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells. Dev Dyn 226:91–98

    Article  CAS  PubMed  Google Scholar 

  • Cook RD, Burnstock G (1976) The ultrastructure of Auerbach's plexus in the guinea-pig. II. Non-neuronal elements. J Neurocytol 5:195–206

    Article  CAS  PubMed  Google Scholar 

  • 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 1899:130–158

    Google Scholar 

  • Dulac C, Le Douarin NM (1991) Phenotypic plasticity of Schwann cells and enteric glial cells in response to the microenvironment. Proc Natl Acad Sci USA 88:6358–6362

    Article  CAS  PubMed  Google Scholar 

  • Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, Rauch J, Geisler R, Haffter P, Kelsh RN (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128:4113–4125

    CAS  PubMed  Google Scholar 

  • Gabella G (1981) Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience 6:425–436

    Article  CAS  PubMed  Google Scholar 

  • Gabella G (1984) Size of neurons and glial cells in the intramural ganglia of the hypertrophic intestine of the guinea-pig. J Neurocytol 13:73–84

    Article  CAS  PubMed  Google Scholar 

  • Gershon MD, Rothman TP (1991) Enteric glia. Glia 4:195–204

    Article  CAS  PubMed  Google Scholar 

  • Hanani M, Reichenbach A (1994) Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res 278:153–160

    Article  CAS  PubMed  Google Scholar 

  • Holmberg A, Schwerte T, Fritsche R, Pelster B, Holmgren S (2003) Ontogeny of intestinal motility in correlation to neuronal development in zebrafish embryos and larvae. J Fish Biol 63:318–331

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Holmberg A, Olsson C, Holmgren S (2006) The effects of endogenous and exogenous nitric oxide on gut motility in zebrafish Danio rerio embryos and larvae. J Exp Biol 209:2472–2479

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Holmberg A, Holmgren S, Olsson C (2008) Enteric control. In: Finn R (ed) Fish larval physiology. Science Publishers, Enfield, pp 553–572

    Google Scholar 

  • Jessen KR (2004) Glial cells. Int J Biochem Cell Biol 36:1861–1867

    Article  CAS  PubMed  Google Scholar 

  • Jessen KR, Mirsky R (1980) Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 286:736–737

    Article  CAS  PubMed  Google Scholar 

  • Jessen KR, Mirsky R (1983) Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3:2206–2218

    CAS  PubMed  Google Scholar 

  • Jutfelt F, Olsen RE, Glette J, Ringo E, Sundell K (2006) Translocation of viable Aeromonas salmonicida across the intestine of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 29:255–262

    Article  CAS  PubMed  Google Scholar 

  • Kelsh RN, Eisen JS (2000) The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development 127:515–525

    CAS  PubMed  Google Scholar 

  • Kimball BC, Mulholland MW (1996) Enteric glia exhibit P2U receptors that increase cytosolic calcium by a phospholipase C-dependent mechanism. J Neurochem 66:604–612

    CAS  PubMed  Google Scholar 

  • Le Douarin N, Dulac C, Dupin E, Cameron-Curry P (1991) Glial cell lineages in the neural crest. Glia 4:175–184

    Article  PubMed  Google Scholar 

  • Miampamba M, Yang H, Sharkey KA, Tache Y (2001) Intracisternal TRH analog induces Fos expression in gastric myenteric neurons and glia in conscious rats. Am J Physiol Gastrointest Liver Physiol 280:G979–G991

    CAS  PubMed  Google Scholar 

  • Nasser Y, Fernandez E, Keenan CM, Ho W, Oland LD, Tibbles LA, Schemann M, MacNaughton WK, Ruhl A, Sharkey KA (2006) Role of enteric glia in intestinal physiology: effects of the gliotoxin fluorocitrate on motor and secretory function. Am J Physiol Gastrointest Liver Physiol 291:G912–G927

    Article  CAS  PubMed  Google Scholar 

  • Nasser Y, Keenan CM, Ma AC, McCafferty DM, Sharkey KA (2007) Expression of a functional metabotropic glutamate receptor 5 on enteric glia is altered in states of inflammation. Glia 55:859–872

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Paratore C, Goerich DE, Suter U, Wegner M, Sommer L (2001) Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128:3949–3961

    CAS  PubMed  Google Scholar 

  • Ruhl A (2005) Glial cells in the gut. Neurogastroenterol Motil 17:777–790

    Article  CAS  PubMed  Google Scholar 

  • Ruhl A, Nasser Y, Sharkey KA (2004) Enteric glia. Neurogastroenterol Motil 16 (Suppl 1):44–49

    Article  PubMed  Google Scholar 

  • Shepherd IT, Beattie CE, Raible DW (2001) Functional analysis of zebrafish GDNF. Dev Biol 231:420–435

    Article  CAS  PubMed  Google Scholar 

  • Shepherd IT, Pietsch J, Elworthy S, Kelsh RN, Raible DW (2004) Roles for GFRα1 receptors in zebrafish enteric nervous system development. Development 131:241–249

    Article  CAS  PubMed  Google Scholar 

  • Ungos JM, Karlstrom RO, Raible DW (2003) Hedgehog signaling is directly required for the development of zebrafish dorsal root ganglia neurons. Development 130:5351–5362

    Article  CAS  PubMed  Google Scholar 

  • Van Nassauw L, Costagliola A, Op V, Bosch J den, Cecio A, Vanderwinden JM, Burnstock G, Timmermans JP (2006) Region-specific distribution of the P2Y4 receptor in enteric glial cells and interstitial cells of Cajal within the guinea-pig gastrointestinal tract. Auton Neurosci 126–127:299–306

    Article  PubMed  Google Scholar 

  • Young HM, Jones BR, McKeown SJ (2002) The projections of early enteric neurons are influenced by the direction of neural crest cell migration. J Neurosci 22:6005–6018

    CAS  PubMed  Google Scholar 

  • Young HM, Bergner AJ, Muller T (2003) Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1–11

    Article  PubMed  Google Scholar 

  • Zhang W, Sarosi G Jr, Barnhart D, Yule DI, Mulholland MW (1997) Endothelin-activated calcium signaling in enteric glia derived from neonatal guinea pig. Am J Physiol 272:G1175–G1185

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. Susanne Holmgren for critical reading of the manuscript.

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Authors and Affiliations

  1. Department of Zoology/Zoophysiology, University of Gothenburg, Box 463, SE-405 30, Gothenburg, Sweden

    Christina Hagström & Catharina Olsson

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  1. Christina Hagström
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  2. Catharina Olsson
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Correspondence to Catharina Olsson.

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This study was financed by a grant from the Swedish Research Council.

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Hagström, C., Olsson, C. Glial cells revealed by GFAP immunoreactivity in fish gut. Cell Tissue Res 341, 73–81 (2010). https://doi.org/10.1007/s00441-010-0979-3

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  • DOI: https://doi.org/10.1007/s00441-010-0979-3

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