Olfactory and gustatory chemical sensor systems in the African turquoise killifish: Insights from morphology.
Fish
Olfactory epithelium
Taste buds
Journal
Cell and tissue research
ISSN: 1432-0878
Titre abrégé: Cell Tissue Res
Pays: Germany
ID NLM: 0417625
Informations de publication
Date de publication:
21 Oct 2024
21 Oct 2024
Historique:
received:
01
08
2024
accepted:
01
10
2024
medline:
21
10
2024
pubmed:
21
10
2024
entrez:
21
10
2024
Statut:
aheadofprint
Résumé
Smell and taste are extensively studied in fish species as essential for finding food and selecting mates while avoiding toxic substances and predators. Depending on the evolutionary position and adaptation, a discrete variation in the morphology of these sense organs has been reported in numerous teleost species. Here, for the first time, we approach the phenotypic characterization of the olfactory epithelium and taste buds in the African turquoise killifish (Nothobranchius furzeri), a model organism known for its short lifespan and use in ageing research. Our observations indicate that the olfactory epithelium of N. furzeri is organized as a simple patch, lacking the complex folding into a rosette, with an average size of approximately 600 µm in length, 300 µm in width, and 70 µm in thickness. Three main cytotypes, including olfactory receptor neurons (CalbindinD28K), supporting cells (β-tubulin IV), and basal cells (Ki67), were identified across the epithelium. Further, we determined the taste buds' distribution and quantification between anterior (skin, lips, oral cavity) and posterior (gills, pharynx, oesophagus) systems. We identified the key cytotypes by using immunohistochemical markers, i.e. CalbindinD28K, doublecortin, and neuropeptide Y (NPY) for gustatory receptor cells, glial fibrillary acidic protein (GFAP) for supporting cells, and Ki67, a marker of cellular proliferation for basal cells. Altogether, these results indicate that N. furzeri is a microsmatic species with unique taste and olfactory features and possesses a well-developed posterior taste system compared to the anterior. This study provides fundamental insights into the chemosensory biology of N. furzeri, facilitating future investigations into nutrient-sensing mechanisms and their roles in development, survival, and ageing.
Identifiants
pubmed: 39432108
doi: 10.1007/s00441-024-03923-5
pii: 10.1007/s00441-024-03923-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ministero dell'Università e della Ricerca
ID : Prin 2022 - 2022LYPBCT
Organisme : Ministero dell'Università e della Ricerca
ID : Prin 2022 - 2022LYPBCT
Organisme : Ministero dell'Università e della Ricerca
ID : Prin 2022 - 2022LYPBCT
Organisme : Ministero dell'Università e della Ricerca
ID : Prin 2022 - 2022LYPBCT
Informations de copyright
© 2024. The Author(s).
Références
Ahuja G, Korsching S (2014) Zebrafish olfactory receptor ORA1 recognizes a putative reproductive pheromone. Commun Integr Biol 7(5). https://doi.org/10.4161/19420889.2014.970501
Atema J (1971) Structures and functions of the sense of taste in the catfish (Ictalurus natalis). Brain Behav Evol 4(4):273–294. https://doi.org/10.1159/000125438
doi: 10.1159/000125438
pubmed: 5118142
Ayanlaja AA, Xiong Y, Gao Y, Ji G, Tang C, Abdikani Abdullah Z, Gao D (2017) Distinct features of doublecortin as a marker of neuronal migration and its implications in cancer cell mobility. Front Mol Neurosci 10:270229. https://doi.org/10.3389/fnmol.2017.00199
doi: 10.3389/fnmol.2017.00199
Barreiro-Iglesias A, Villar-Cerviño V, Villar-Cheda B, Anadón R, Rodicio MC (2008) Neurochemical characterization of sea lamprey taste buds and afferent gustatory fibers: presence of serotonin, calretinin, and CGRP immunoreactivity in taste bud bi-ciliated cells of the earliest vertebrates. J Comp Neurol 511(4):438–453. https://doi.org/10.1002/cne.21844
doi: 10.1002/cne.21844
pubmed: 18831528
Bastianelli E, Pochet R (1994) Distribution of calmodulin, calbindin-D28k and calretinin among rat olfactory nerve bundles. Neurosci Lett 169(1–2):223–226. https://doi.org/10.1016/0304-3940(94)90397-2
doi: 10.1016/0304-3940(94)90397-2
pubmed: 8047286
Bettini S, Lazzari M, Milani L, Maurizii MG, Franceschini V (2023) Immunohistochemical analysis of olfactory sensory neuron populations in the developing olfactory organ of the guppy, Poecilia reticulata (Cyprinodontiformes, Poecilidae). Microsc Microanal 29(5):1764–1773. https://doi.org/10.1093/micmic/ozad099
doi: 10.1093/micmic/ozad099
pubmed: 37639707
Cellerino A, Valenzano DR, Reichard M (2016) From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol Rev Camb Philos Soc 91(2):511–533. https://doi.org/10.1111/brv.12183
doi: 10.1111/brv.12183
pubmed: 25923786
D’Angelo L, Lossi L, Merighi A, de Girolamo P (2016) Anatomical features for the adequate choice of experimental animal models in biomedicine: I. Fishes Ann Anat 205:75–84. https://doi.org/10.1016/j.aanat.2016.02.001
doi: 10.1016/j.aanat.2016.02.001
pubmed: 26925824
D’Angelo L (2013) Brain atlas of an emerging teleostean model: Nothobranchius furzeri. Anat Rec 296(4):681–691. https://doi.org/10.1002/ar.22668
doi: 10.1002/ar.22668
De Felice E, Giaquinto D, Damiano S, Salzano A, Fabroni S, Ciarcia R, Scocco P, de Girolamo P, D’Angelo L (2021) Distinct pattern of NPY in gastro-entero-pancreatic system of goat kids fed with a new standardized red orange and lemon extract (RLE). Animals 11(2):449. https://doi.org/10.3390/ani11020449
doi: 10.3390/ani11020449
pubmed: 33572145
pmcid: 7914828
Devitsina GV (2005) Comparative morphology of intraoral taste apparatus in fishes. J Ichthyol 45(suppl. 2):S286–S306
Elsheikh EH, Nasr ES, Gamal AM (2012) Ultrastructure and distribution of the taste buds in the buccal cavity in relation to the food and feeding habit of a herbivorous fish: Oreochromis niloticus. Tissue Cell 44(3):164–169. https://doi.org/10.1016/j.tice.2012.02.002
doi: 10.1016/j.tice.2012.02.002
pubmed: 22440511
Fan D, Chettouh Z, Consalez GG, Brunet J-F (2019) Taste bud formation depends on taste nerves. eLife 8:e49226. https://doi.org/10.7554/eLife.49226
doi: 10.7554/eLife.49226
pubmed: 31570121
pmcid: 6785267
Finger TE, Morita Y (1985) Two gustatory systems: facial and vagal gustatory nuclei have different brainstem connections. Science 227(4688):776–778. https://doi.org/10.1126/science.3969566
doi: 10.1126/science.3969566
pubmed: 3969566
Fujiwara M, Nakamura H, Kawasaki M, Nakano Y, Kuwano R (1997) Expressions of a calcium-binding protein (spot35/calbindin-D28k) in mouse olfactory cells: possible relationship to neuronal differentiation. Eur Arch Otorhinolaryngol 254:105–109. https://doi.org/10.1007/BF01526190
doi: 10.1007/BF01526190
pubmed: 9065666
Giaquinto D, De Felice E, Attanasio C, Palladino A, Schiano V, Mollo E, Lucini C, de Girolamo P, D’Angelo L (2022) Central and peripheral NPY age-related regulation: a comparative analysis in fish translational models. Int J Mol Sci 23(7):3839. https://doi.org/10.3390/ijms23073839
doi: 10.3390/ijms23073839
pubmed: 35409198
pmcid: 8998975
Hansen A, Zeiske E (1998) The peripheral olfactory organ of the zebrafish, Danio rerio: an ultrastructural study. Chem Senses 23:39–48. https://doi.org/10.1093/chemse/23.1.39
doi: 10.1093/chemse/23.1.39
pubmed: 9530968
Hara TJ, Kitada Y, Evans RE (1994) Distribution patterns of palatal taste buds and their responses to amino acids in salmonids. J Fish Biol 45:453–465. https://doi.org/10.1111/j.1095-8649.1994.tb01328.x
doi: 10.1111/j.1095-8649.1994.tb01328.x
Herness S (2012) The neurobiology of gustation: taste buds and transduction processes. In: Johnson LR, Ghishan FK, Kaunitz JD, Merchant JL, Said HM, Wood JD (eds) Physiology of the gastrointestinal tract, 5th edn. Academic Press, pp 741–767. https://doi.org/10.1016/B978-0-12-382026-6.00026-9
Holbrook EH, Wu E, Curry WT, Lin DT, Schwob JE (2011) Immunohistochemical characterization of human olfactory tissue. Laryngoscope 121(8):1687–1701. https://doi.org/10.1002/lary.21856
doi: 10.1002/lary.21856
pubmed: 21792956
pmcid: 3181071
Hu Y, Majoris JE, Buston PM, Webb JF (2019) Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology. J Fish Biol 95(1):311–323. https://doi.org/10.1111/jfb.13793
doi: 10.1111/jfb.13793
pubmed: 30198213
Ikenaga T, Ogura T, Finger TE (2009) Vagal gustatory reflex circuits for intraoral food sorting behavior in the goldfish: cellular organization and neurotransmitters. J Comp Neurol 516(3):213–225. https://doi.org/10.1002/cne.22097
doi: 10.1002/cne.22097
pubmed: 19598285
pmcid: 2737690
Iqbal T, Byrd-Jacobs C (2010) Rapid degeneration and regeneration of the zebrafish olfactory epithelium after triton X-100 application. Chem Senses 35(5):351–361. https://doi.org/10.1093/chemse/bjq019
doi: 10.1093/chemse/bjq019
pubmed: 20228140
pmcid: 2871777
Ishimaru Y, Okada S, Naito H, Nagai T, Yasuoka A, Matsumoto I, Abe K (2005) Two families of candidate taste receptors in fishes. Mech Dev 122:1310–1321. https://doi.org/10.1016/j.mod.2005.07.005
doi: 10.1016/j.mod.2005.07.005
pubmed: 16274966
Jang W, Chen X, Flis D, Harris M, Schwob JE (2014) Label-retaining, quiescent globose basal cells are found in the olfactory epithelium. J Comp Neurol 522(4):731–749. https://doi.org/10.1002/cne.23470
doi: 10.1002/cne.23470
pubmed: 24122672
pmcid: 4240005
Jia C, Halpern M (2003) Calbindin D28K immunoreactive neurons in vomeronasal organ and their projections to the accessory olfactory bulb in the rat. Brain Res 977(2):261–269. https://doi.org/10.1016/S0006-8993(03)02693-3
doi: 10.1016/S0006-8993(03)02693-3
pubmed: 12834886
Kasumyan AO (2019) The taste system in fishes and the effects of environmental variables. J Fish Biol 95:155–178. https://doi.org/10.1111/jfb.13940
doi: 10.1111/jfb.13940
pubmed: 30793305
Kirchmaier S, Naruse K, Wittbrodt J, Loosli F (2015) The genomic and genetic toolbox of the teleost medaka (Oryzias latipes). Genetics 199(4):905–918. https://doi.org/10.1534/genetics.114.173849
doi: 10.1534/genetics.114.173849
pubmed: 25855651
pmcid: 4391551
Korsching SI (2020) Taste and smell in zebrafish. In: Fritzsch B (ed) The senses: a comprehensive reference, 2nd edn. Elsevier, pp 466–492. https://doi.org/10.1016/B978-0-12-809324-5.24155-2
Lauder GV, Liem KF (1983) The evolution and interrelationships of the actinopterygian fishes. In: Liem KF (ed) Bulletin of the Museum of Comparative Zoology at Harvard College, vol 150. Cambridge, Mass, The Museum, pp 95–197
Leggieri A, Attanasio C, Palladino A, de Girolamo P, Lucini C, D’Angelo L (2022) Neuronal phenotype of col4a1 and col25a1: an intriguing hypothesis in vertebrates brain aging. Int J Mol Sci 23(3):1778. https://doi.org/10.3390/ijms23031778
doi: 10.3390/ijms23031778
pubmed: 35163698
pmcid: 8836537
Lemons K, Fu Z, Ogura T, Lin W (2020) TRPM5-expressing microvillous cells regulate region-specific cell proliferation and apoptosis during chemical exposure. Neuroscience 434:171–190. https://doi.org/10.1016/j.neuroscience.2020.03.026
doi: 10.1016/j.neuroscience.2020.03.026
pubmed: 32224228
Mariën V, Piskin I, Zandecki C, Vanhoucke J, Arckens L (2024) Age-related alterations in the behavioral response to a novel environment in the African turquoise killifish (Nothobranchius furzeri). Front Behav Neurosci 17:1326674. https://doi.org/10.3389/fnbeh.2023.1326674
doi: 10.3389/fnbeh.2023.1326674
pubmed: 38259633
pmcid: 10800983
Mii S, Amoh Y, Katsuoka K, Hoffman RM (2014) Comparison of nestin-expressing multipotent stem cells in the tongue fungiform papilla and vibrissa hair follicle. J Cell Biochem 115(6):1070–1076. https://doi.org/10.1002/jcb.24696
doi: 10.1002/jcb.24696
pubmed: 24142339
Miyawaki Y, Morisaki I, Tabata M et al (1997) Calbindin D28k-like immunoreactivity in the developing and regenerating circumvallate papilla of the rat. Cell Tissue Res 291:81–90. https://doi.org/10.1007/s004410050981
doi: 10.1007/s004410050981
Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278. https://doi.org/10.1038/nrn1365
doi: 10.1038/nrn1365
pubmed: 15034552
Northcutt RG (2005) Taste bud development in the channel catfish. J Comp Neurol 482(1):1–16. https://doi.org/10.1002/cne.20425
doi: 10.1002/cne.20425
pubmed: 15612020
Okada S (2015) The taste system of small fish species. Biosci Biotechnol Biochem 79:1039–1043. https://doi.org/10.1080/09168451.2015.1023251
doi: 10.1080/09168451.2015.1023251
pubmed: 25776867
Reutter K, Breipohl W, Bijvank GJ (1974) Taste bud types in fishes. Cell Tissue Res 153:151–165. https://doi.org/10.1007/BF00226604
doi: 10.1007/BF00226604
pubmed: 4442083
Riddle MR, Hu CK (2021) Fish models for investigating nutritional regulation of embryonic development. Dev Biol 476:101–111. https://doi.org/10.1016/j.ydbio.2021.03.012
doi: 10.1016/j.ydbio.2021.03.012
pubmed: 33831748
Terzibasi ET, Baumgart M, Battistoni G, Cellerino A (2012) Adult neurogenesis in the short-lived teleost Nothobranchius furzeri: localization of neurogenic niches, molecular characterization and effects of aging. Aging Cell 11(2):241–251. https://doi.org/10.1111/j.1474-9726.2011.00781.x
doi: 10.1111/j.1474-9726.2011.00781.x
Thoré ESJ, Philippe C, Brendonck L, Pinceel T (2021) Towards improved fish tests in ecotoxicology - efficient chronic and multi-generational testing with the killifish Nothobranchius furzeri. Chemosphere 273. https://doi.org/10.1016/j.chemosphere.2021.129697
Villamayor PR, Arana ÁJ, Coppel C et al (2021) A comprehensive structural, lectin and immunohistochemical characterization of the zebrafish olfactory system. Sci Rep 11:8865. https://doi.org/10.1038/s41598-021-88317-1
doi: 10.1038/s41598-021-88317-1
pubmed: 33893372
pmcid: 8065131
Volff JN (2005) Genome evolution and biodiversity in teleost fish. Heredity 94(3):280–294. https://doi.org/10.1038/sj.hdy.6800635
doi: 10.1038/sj.hdy.6800635
pubmed: 15674378
Yamamoto M (1982) Comparative morphology of the peripheral olfactory organ in teleosts. In: Hara TJ (ed) Chemoreception in fishes. Elsevier, New York, pp 39–59
Yasuoka A, Endo K, Asano-Miyoshi M, Abe K, Emori Y (1999) Two subfamilies of olfactory receptor genes in medaka fish, Oryzias latipes: genomic organization and differential expression in olfactory epithelium. J Biochem 126:866–873. https://doi.org/10.1093/oxfordjournals.jbchem.a022528
doi: 10.1093/oxfordjournals.jbchem.a022528
pubmed: 10544279
Žák J, Šuhajová P (2024) The effect of water turbidity on prey consumption and female feeding patterns in African turquoise killifish. Ecol Freshw Fish 33(3):e12774. https://doi.org/10.1111/eff.12774
doi: 10.1111/eff.12774
Žák J, Dyková I, Reichard M (2020) Good performance of turquoise killifish (Nothobranchius furzeri) on pelleted diet as a step towards husbandry standardization. Sci Rep 10:8986. https://doi.org/10.1038/s41598-020-65930-0
doi: 10.1038/s41598-020-65930-0
pubmed: 32488062
pmcid: 7265286
Žák J, Roy K, Dyková I, Mráz J, Reichard M (2022) Starter feed for carnivorous species as a practical replacement of bloodworms for a vertebrate model organism in ageing, the turquoise killifish Nothobranchius furzeri. J Fish Biol 100:894–908. https://doi.org/10.1111/jfb.15021
doi: 10.1111/jfb.15021
pubmed: 35195903