Abstract
Artemin is a member of the glial cell line-derived neurotrophic factor (GDNF) family. It is a neurotrophic factor that supports neurite migration and outgrowth and survival of the sympathetic and sensory nervous system. Artemin has been studied in human and murine tissues, but no study has been devoted to nonmammalian species. Zebrafish is a teleost fish belonging to the family Ciprinidae, which is becoming an important model species for genetic and developmental studies. Thus, the aim of the present investigation was to evaluate, by immunochemical and immunocytochemical analyses, the tissue distribution pattern of artemin in zebrafish. Different isoforms of artemin with corresponding different molecular weights were detected in the brain, muscle, testis, ovary, kidney, gut, and gills of zebrafish by Western blot analysis. Immunocytochemical analysis showed artemin-like immunoreactivity in different cell types: in glial cells and rare neurons of the central nervous system, taste buds, retina, neuromasts of the lateral line, dorsal root ganglia, sympathetic ganglia, gill epithelium, tubular kidney epithelium, gut epithelium and ganglia, pancreas, thyroid, hypothalamus, testis, and ovary. These results indicate a wide distribution of artemin-like immunoreactivity in adult zebrafish, related to the presence of different forms of artemin. These findings might suggest a complex maturation pattern of artemin, whose forms could also exert different roles in zebrafish tissues.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Airaksinen MS, Saarma M (2002) The GDNF family : signalling, biological functions and therapeutic value. Nature Rev 3:383–394
Andres R, Forgie A, Wyatt S, Chen Q, de Sauvage FJ, Davies AM (2001) Multiple effects of artemin on sympathetic neurone generation, survival and growth. Development 128:3685–3695
Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H, Simburger KS, Leitner ML, Araki T, Johnson EM Jr, Millbrandt J (1998) Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRα3-RET receptor complex. Neuron 21:1291–1302
De Girolamo P, Lucini C, Vega JA, Andreozzi G, Coppola L, Castaldo L (1999) Co-localization of Trk neurotrophin receptors and regulatory peptides in the endocrine cells of the teleostean stomach. Anat Rec 256:219–226
Gardell LR, Wang R, Ehrenfels C, Ossipov MH, Rossomando AJ, Miller S, Buckley C, Cai AK, Foley AT, Gong B, Walus L, Carmillo P, Worley D, Huang C, Engber T, Pepinsky B, Cate R L, Vanderach TW, Lai J, Sah DWS, Porreca F (2003) Multiple actions of systemic artemin in experimental neuropathy. Nat Med 9:1383–1389
HonmaY, Araki T, Gianino S, Bruce A, Heuckeroth RO, Johnson EM, Milbrandt J (2002) Artemin is a vascular-derived neurotrophic factor for developing sympathetic neurons. Neuron 35:267–282
Kotrschal K, Krautgartner WD, Hansen A (1997) Ontogeny of the solitary chemosensory cells in the zebrafish, Danio rerio. Chem Senses 22:111–118
Kotzbauer PT, Lampe PA, Heuckeroth RO, Golden JP, Creedon DJ, Johnson EM, Milbrandt J (1996) Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature 384:467–470
Lee R, Kermani P, Teng KK, Hempestead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294:1945–1948
Lin L-FH, Doherty DH, Lile JD, Bektesh S, Collins F (1993) GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260:1130–1132
Lipson AC, Widenfalk J, Lindqvist E, Ebendal T, Olson L (2003) Neurotrophic properties of olfactory ensheathing glia. Exp Neurol 180:167–171
Lucini C, De Girolamo P, Maruccio L, Lamanna C, Castaldo l, Vega JA (1999) Trk-neurotrophin receptor-like immunoreactivity in the gut of teleost species. Cell Tissue Res 296:323–330
Lucini C, Maruccio L, Arcamone N, Lamanna C, Castaldo L (2003) Neurotrophin-like immunoreactivity in the gut of teleost species. Neurosci Lett 345:33–36
Masure S, Geerts H, Cik M, Hoegnagel E, Van Den Kieboom G, Tutytelaars A, Harris S, Lesage ASJ, Leysen JE, VanDer Helm L, Verhasselt P, Yon J, Gordon RD (1999) Enovin, a member of the glial cell-line-derived neurotrophic factor (GDNF) family with growth promoting activity on neuronal cells. Eur J Biochem 266:892–902
Milbrandt J, de Sauvage FJ, Fahrner TJ, Baloh RH, Leitner ML, Tansey MG, Lamoe PA, Heuckeroth RO, Kotzbauer PT, Simburger KS, Golden JP, Davies JA, Vejsada R, Kato AC, Hynes M, Sherman D, Nishimura M, Wang LC, Vandlen R, Moffat B, Klein RD, Poulsen K, Gray C, Garces A, Henderson CE, Phillips HS, Johnson EM Jr (1998) Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 20:245–253
Neet KE, Campenot RB (2001) Receptor binding, internalization, and retrogade transport of neurotrophic factors. Cell Mol Life Sci 58:1021–1035
Nishino J, Mochida K, Ohfuji Y, Shimazaki T, Meno C, Ohishi S, Matsuda Y, Fujii H, Saijoh Y, Hamada H (1999) GFRα3, a component of the artemin receptor, is required for migration and survival of the superior cervical ganglion. Neuron 23:725–736
Poteryaev D, Titievsky A, Sun YF, Thomas-Crusells J, Lindahl M, Billaud N, Arumae U, Saarma M (1999) GDNF triggers a novel ret-independent Src kinase family-coupled signaling via a GPI-linked GDNF receptor alpha 1. FEBS Lett 463:63–66
Raisman G (2001) Olfactory ensheathing cells—another miracle cure for spinal cord injury? Nat Rev Neurosci 2:369–375
Reynolds GM, Young FI, Williams A, Rowlands DC (1994) Microwave-oven antigen retrieval applied to the immunostaining of cytopathology specimens. Cytopathology 5:345–358
Rosenblad C, Grønborg M, Hansen C, Blom N, Meyer M, Johansen J, Dagø L, Kirik D, Patel UA, Lundberg C, Trono D, Björklund A, Johansen TE (2000) In vivo protection of nigral dopamine neurons by lentiviral gene transfer of the novel GDNF-family member neublastin/artemin. Mol Cell Neurosci 15:199–214
Sariola H (2001) The neurotrophic factors in non-neuronal tissues. Cell Mol Life Sci 58:1061–1066
Sariola H, Saarma M (2003) Novel functions and signalling pathways for GDNF. J Cell Sci 116:3855–3862
Shepherd IT, Beattie CE, Raible DW (2002) Functional analysis of zebrafish GDNF. Dev Biol 231:420–435
Sternberger LA (1986) Immunocytochemistry, 3rd edn. Wiley & Sons, New York
Trupp M, Scott R, Whittemore SR, Ibañez CF (1999) Ret-independent mechanisms of glial cell line-derived neurotrophic factor signaling in neuronal cells. J Biol Chem 274:20885–20894
Yan H, Newgreen DF, Young HM (2003) Developmental changes in neurite outgrowth responses of dorsal root and sympathetic ganglia to GDNF, neurturin and artemin. Dev Dyn 227:395–401
Zaccone G, Fasulo SW, Ainis L (1994) Distribution patterns of the paraneuronal endocrine cells in the skin, gills and the airway of fishes as determined by immunohistochemical and histological methods. Histochem J 26:609–629
Zupanc GK, Clint SC (2003) Potential role of radial glia in adult neurogenesis of teleost fish. Glia 43:77–86
Acknowledgements
We thank Mrs. Annamaria Zollo for her skillful technical assistance. This study was supported by a grant from Università di Napoli Federico II, Polo delle Scienze e Tecnologie per la Vita, Napoli, Italy.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lucini, C., Maruccio, L., Tafuri, S. et al. Artemin-like immunoreactivity in the zebrafish, Danio rerio. Anat Embryol 208, 403–410 (2004). https://doi.org/10.1007/s00429-004-0409-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-004-0409-y