Skip to main content
SpringerLink
Log in

Crypt cell markers in the olfactory organ of Poecilia reticulata: analysis and comparison with the fish model Danio rerio

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Olfactory crypt neurons have been observed in several bony fishes and chondrichtyans. Although their morphology is uniform in all fish, very few is known about their antigenic properties, usually studied in zebrafish, but quite overlooked in other species. We tested in Poecilia reticulata (guppy) the two antibodies recognized to mark zebrafish crypt cells: while anti-S100 showed an immunohistochemical pattern comparable to what reported in zebrafish, anti-TrkA gave no signal. Western blot analysis revealed that S100-antiserum bound an antigen of expected weight, probably belonging to the S100 family. On the contrary, anti-TrkA detected more bands, but the protein/s might be too much diffused and/or diluted in the tissue to be detected with immunohistochemistry. Because of the high level of conservation in the Trk family proteins of the kinase domain, on which anti-TrkA was produced, we also tested anti-TrkB to exclude cross reactivity. Immunohistochemistry and Western blot confirmed that anti-TrkB displayed high specificity to its target and a different staining pattern compared to anti-TrkA, but, as anti-TrkA, it did not label crypt neurons. Finally, we documented that calretinin, a known marker of zebrafish ciliated and microvillous olfactory cells, in the guppy is expressed also by a subpopulation of S100-positive crypt neurons. These results reveal differences in antigen expression between zebrafish and guppy crypt cells. Together with the already known species-specific projections to the olfactory bulb and a heterogeneous panel of odorants, our findings support the possibility that crypt cells are functionally less uniform as supposed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahuja G, Ivandic I, Saltürk M, Oka Y, Nadler W, Korsching SI (2013) Zebrafish crypt neurons project to a single, identified mediodorsal glomerulus. Sci Rep 3:2063–2071

    Article  PubMed  PubMed Central  Google Scholar 

  • Ahuja G, Bozorg Nia S, Zapilko V, Shiriagin V, Kowatschew D, Oka Y, Korsching SI (2014) Kappe neurons, a novel population of olfactory sensory neurons. Sci Rep 4:4037–4044

    Article  PubMed  PubMed Central  Google Scholar 

  • Arvedlund M, Munday PL, Takemura A (2007) The morphology and ultrastructure of the peripheral olfactory organ in newly metamorphosed coral-dwelling gobies, Paragobiodon xanthosomus Bleeker (Gobiidae, Teleostei). Tissue Cell 39(5):335–342

    Article  CAS  PubMed  Google Scholar 

  • Bazáes A, Schmachtenberg O (2012) Odorant tuning of olfactory crypt cells from juvenile and adult rainbow trout. J Exp Biol 215:1740–1748

    Article  PubMed  Google Scholar 

  • Bettini S, Lazzari M, Ciani F, Franceschini V (2009) Immunohistochemical and histochemical characteristics of the olfactory system of the guppy, Poecilia reticulata (Teleostei, Poecilidae). Anat Rec (Hoboken) 292(10):1569–1576

    Article  Google Scholar 

  • Bettini S, Lazzari M, Franceschini V (2012) Quantitative analysis of crypt cell population during postnatal development of the olfactory organ of the guppy, Poecilia reticulata (Teleostei, Poecilidae), from birth to sexual maturity. J Exp Biol 215(15):2711–2715

    Article  PubMed  Google Scholar 

  • Bettini S, Lazzari M, Ferrando S, Gallus L, Franceschini V (2016) Histopathological analysis of the olfactory epithelium of zebrafish (Danio rerio) exposed to sublethal doses of urea. J Anat 228(1):59–69

    Article  CAS  PubMed  Google Scholar 

  • Braubach OR, Fine A, Croll RP (2012) Distribution and functional organization of glomeruli in the olfactory bulbs of zebrafish (Danio rerio). J Comp Neurol 520(11):2317–2339

    Article  PubMed  Google Scholar 

  • Castro A, Becerra M, Manso MJ, Anadón R (2006a) Calretinin immunoreactivity in the brain of the zebrafish, Danio rerio: distribution and comparison with some neuropeptides and neurotransmitter-synthesizing enzymes. I. Olfactory organ and forebrain. J Comp Neurol 494(3):435–459

    Article  CAS  PubMed  Google Scholar 

  • Castro A, Becerra M, Manso MJ, Anadón R (2006b) 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(5):792–814

    Article  PubMed  Google Scholar 

  • Castro A, Becerra M, Anadón R, Manso MJ (2008) Distribution of calretinin during development of the olfactory system in the brown trout, Salmo trutta fario: Comparison with other immunohistochemical markers. J Chem Neuroanat 35(4):306–316

    Article  CAS  PubMed  Google Scholar 

  • Catania S, Germanà A, Laurà R, Gonzalez-Martinez T, Ciriaco E, Vega JA (2003) The crypt neurons in the olfactory epithelium of the adult zebrafish express TrkA-like immunoreactivity. Neurosci Lett 350(1):5–8

    Article  CAS  PubMed  Google Scholar 

  • Catania S, Germanà A, Cabo R, Ochoa-Erena FJ, Guerrera MC, Hannestad J, Represa J, Vega JA (2007) Neurotrophin and Trk neurotrophin receptors in the inner ear of Salmo salar and Salmo trutta. J Anat 210(1):78–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakrabarti P, Ghosh SK (2011) Histological and ultrastructural studies of the olfactory epithelium of spotted butter fish Scatophagus argus (Linnaeus). Folia Morphol (Warsz) 70(2):74–79

    CAS  Google Scholar 

  • D’Angelo L, de Girolamo P, Cellerino A, Tozzini ET, Castaldo L, Lucini C (2012) Neurotrophin Trk receptors in the brain of a teleost fish, Nothobranchius furzeri. Microsc Res Tech 75(1):81–88

    Article  PubMed  Google Scholar 

  • Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL (2013) Functions of S100 proteins. Curr Mol Med 13(1):24–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farbman AI (2000) Cell biology of olfactory epithelium. In: Finger TE, Silver WL, Restrepo D (eds) The neurobiology of taste and smell. Wiley, New York, pp 131–158

    Google Scholar 

  • Ferrando S, Bottaro M, Gallus L, Girosi L, Vacchi M, Tagliafierro G (2006) Observations of crypt neuron-like cells in the olfactory epithelium of a cartilaginous fish. Neurosci Lett 403(3):280–282

    Article  CAS  PubMed  Google Scholar 

  • Gatta C, Altamura G, Avallone L, Castaldo L, Corteggio A, D’Angelo L, de Girolamo P, Lucini C (2016) Neurotrophins and their Trk-receptors in the cerebellum of zebrafish. J Morphol 277(6):725–736

    Article  CAS  PubMed  Google Scholar 

  • Gayoso JÁ, Castro A, Anadón R, Manso MJ (2011) Differential bulbar and extrabulbar projections of diverse olfactory receptor neuron populations in the adult zebrafish (Danio rerio). J Comp Neurol 519(2):247–276

    Article  PubMed  Google Scholar 

  • Gayoso JÁ, Castro A, Anadón R, Manso MJ (2012) Crypt cells of the zebrafish Danio rerio mainly project to the dorsomedial glomerular field of the olfactory bulb. Chem Senses 37(4):357–369

    Article  CAS  PubMed  Google Scholar 

  • Germanà A, Montalbano G, Laurà R, Ciriaco E, del Valle ME, Vega JA (2004a) S100 protein-like immunoreactivity in the crypt olfactory neurons of the adult zebrafish. Neurosci Lett 371(2–3):196–198

    Article  PubMed  Google Scholar 

  • Germanà A, González-Martínez T, Catania S, Laura R, Cobo J, Ciriaco E, Vega JA (2004b) Neurotrophin receptors in taste buds of adult zebrafish (Danio rerio). Neurosci Lett 354(3):189–192

    Article  PubMed  Google Scholar 

  • Germanà A, Marino F, Guerrera MC, Campo S, De Girolamo P, Montalbano G, Germanà GP, Ochoa-Erena FJ, Ciriaco E, Vega JA (2008) Expression and distribution of S100 protein in the nervous system of the adult zebrafish (Danio rerio). Microsc Res Tech 71:248–255

    Article  PubMed  Google Scholar 

  • Hamdani el H, Døving KB (2006) Specific projection of the sensory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chem Senses 31(1):63–67

    Article  PubMed  Google Scholar 

  • Hansen A, Finger TE (2000) Phyletic distribution of crypt-type olfactory receptor neurons in fishes. Brain Behav Evol 55(2):100–110

    Article  CAS  PubMed  Google Scholar 

  • Hansen A, Zeiske E (1998) The peripheral olfactory organ of the zebrafish, Danio rerio: an ultrastructural study. Chem Senses 23(1):39–48

    Article  CAS  PubMed  Google Scholar 

  • Hansen A, Zippel HP, Sorensen PW, Caprio J (1999) Ultrastructure of the olfactory epithelium in intact, axotomized, and bulbectomized goldfish, Carassius auratus. Microsc Res Tech 45(4–5):325–338

    Article  CAS  PubMed  Google Scholar 

  • Hansen A, Rolen SH, Anderson K, Morita Y, Caprio J, Finger TE (2003) Correlation between olfactory receptor cell type and function in the channel catfish. J Neurosci 23(28):9328–9339

    CAS  PubMed  Google Scholar 

  • Hansen A, Rolen SH, Anderson K, Morita Y, Caprio J, Finger TE (2005) Olfactory receptor neurons in fish: structural, molecular and functional correlates. Chem Senses 30(Suppl 1):i311

    Article  PubMed  Google Scholar 

  • Jullien J, Guili V, Reichardt LF, Rudkin BB (2002) Molecular kinetics of nerve growth factor receptor trafficking and activation. J Biol Chem 277(41):38700–38708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kress S, Biechl D, Wullimann MF (2015) Combinatorial analysis of calcium-binding proteins in larval and adult zebrafish primary olfactory system identifies differential olfactory bulb glomerular projection fields. Brain Struct Funct 220(4):1951–1970

    Article  CAS  PubMed  Google Scholar 

  • Lazzari M, Bettini S, Ciani F, Franceschini V (2007) Light and transmission electron microscopy study of the peripheral olfactory organ of the guppy, Poecilia reticulata (Teleostei, Poecilidae). Microsc Res Tech 9:782–789

    Article  Google Scholar 

  • Lazzari M, Bettini S, Franceschini V (2013) Immunocytochemical characterization of olfactory ensheathing cells in fish. Brain Struct Funct 218(2):539–549

    Article  CAS  PubMed  Google Scholar 

  • Lazzari M, Bettini S, Franceschini V (2014) Immunocytochemical characterisation of olfactory ensheathing cells of zebrafish. J Anat 224(2):192–206

    Article  CAS  PubMed  Google Scholar 

  • Llovera M, de Pablo Y, Egea J, Encinas M, Peiró S, Martín-Zanca D, Rocamora N, Comella JX (2004) Trk is a calmodulin-binding protein: implications for receptor processing. J Neurochem 88(2):422–433

    Article  CAS  PubMed  Google Scholar 

  • Milani L, Maurizii MG (2015) Vasa expression in spermatogenic cells during the reproductive-cycle phases of Podarcis sicula (Reptilia, Lacertidae). J Exp Zool B Mol Dev Evol 324(5):424–434

    Article  CAS  PubMed  Google Scholar 

  • Mitchell A, Chang H-Y, Daugherty L et al (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43:D213–D221

    Article  PubMed  Google Scholar 

  • Oka Y, Saraiva LR, Korsching SI (2012) Crypt neurons express a single V1R-related ora gene. Chem Senses 37(3):219–227

    Article  CAS  PubMed  Google Scholar 

  • Parisi V, Guerrera MC, Abbate F, Garcia-Suarez O, Viña E, Vega JA, Germanà A (2014) Immunohistochemical characterization of the crypt neurons in the olfactory epithelium of adult zebrafish. Ann Anat 196(4):178–182

    Article  PubMed  Google Scholar 

  • Schmachtenberg O (2006) Histological and electrophysiological properties of crypt cells from the olfactory epithelium of the marine teleost Trachurus symmetricus. J Comp Neurol 495:113–121

  • Schwaller B (2014) Calretinin: from a “simple” Ca(2+) buffer to a multifunctional protein implicated in many biological processes. Front Neuroanat 8:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Skaper SD (2008) The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS Neurol Disord Drug Targets 7(1):46–62

    Article  CAS  PubMed  Google Scholar 

  • van der Loos CM (2008) Multiple immunoenzyme staining: methods and visualizations for the observation with spectral imaging. J Histochem Cytochem 56(4):313–328

    Article  PubMed  PubMed Central  Google Scholar 

  • Vielma A, Ardiles A, Delgado L, Schmachtenberg O (2008) The elusive crypt olfactory receptor neuron: evidence for its stimulation by amino acids and cAMP pathway agonists. J Exp Biol 211(Pt 15):2417–2422

    Article  CAS  PubMed  Google Scholar 

  • Zeiske E, Kasumyan A, Bartsch P, Hansen A (2003) Early development of the olfactory organ in sturgeons of the genus Acipenser: a comparative and electron microscopic study. Anat Embryol (Berl) 206(5):357–372

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological, Geological and Environmental Sciences, University of Bologna, Via Selmi 3, 40126, Bologna, Italy

    Simone Bettini, Liliana Milani, Maurizio Lazzari, Maria Gabriella Maurizii & Valeria Franceschini

Authors
  1. Simone Bettini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liliana Milani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maurizio Lazzari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Gabriella Maurizii
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Valeria Franceschini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Simone Bettini or Valeria Franceschini.

Additional information

S. Bettini and L. Milani contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bettini, S., Milani, L., Lazzari, M. et al. Crypt cell markers in the olfactory organ of Poecilia reticulata: analysis and comparison with the fish model Danio rerio . Brain Struct Funct 222, 3063–3074 (2017). https://doi.org/10.1007/s00429-017-1386-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-017-1386-2

Keywords

Search

Navigation