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Frontiers in neuroanatomy2016; 10; 97; doi: 10.3389/fnana.2016.00097

Intranasal Location and Immunohistochemical Characterization of the Equine Olfactory Epithelium.

Abstract: The olfactory epithelium (OE) is the only body site where neurons contact directly the environment and are therefore exposed to a broad variation of substances and insults. It can serve as portal of entry for neurotropic viruses which spread via the olfactory pathway to the central nervous system. For horses, it has been proposed and concluded mainly from rodent studies that different viruses, e.g., Borna disease virus, equine herpesvirus 1 (EHV-1), hendra virus, influenza virus, rabies virus, vesicular stomatitis virus can use this route. However, little is yet known about cytoarchitecture, protein expression and the intranasal location of the equine OE. Revealing differences in cytoarchitecture or protein expression pattern in comparison to rodents, canines, or humans might help to explain varying susceptibility to certain intranasal virus infections. On the other hand, disclosing similarities especially between rodents and other species, e.g., horses would help to underscore transferability of rodent models. Analysis of the complete noses of five adult horses revealed that in the equine OE two epithelial subtypes with distinct marker expression exist, designated as types a and b which resemble those previously described in dogs. Detailed statistical analysis was carried out to confirm the results obtained on the descriptive level. The equine OE was predominantly located in caudodorsal areas of the nasal turbinates with a significant decline in rostroventral direction, especially for type a. Immunohistochemically, olfactory marker protein and doublecortin (DCX) expression was found in more cells of OE type a, whereas expression of proliferating cell nuclear antigen and tropomyosin receptor kinase A was present in more cells of type b. Accordingly, type a resembles the mature epithelium, in contrast to the more juvenile type b. Protein expression profile was comparable to canine and rodent OE but equine types a and b were located differently within the nose and revealed differences in its cytoarchitecture when compared to canine OE. Equine OE type a closely resembles rat OE. Whether the observed differences contribute to species-specific susceptibility to intranasal insults such as virus infections has to be further investigated.
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Publication Date: 2016-10-13 PubMed ID: 27790096PubMed Central: PMC5061740DOI: 10.3389/fnana.2016.00097Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The researchers have examined the structures, protein expression, and nasal locations of the equine olfactory epithelium (OE), the tissue involved in the sense of smell. The study also focus on whether the OE could serve as an entry point for viruses that can affect the central nervous system. The work provides insight into how horse susceptibility to diseases may differ from other animals.

Understanding the Olfactory Epithelium (OE)

  • The olfactory epithelium (OE) is a specialized type of tissue found in animals’ noses responsible for detecting smells.
  • In horses, the OE provides a direct link between the surrounding environment and the neurons in their nervous system.
  • Due to this direct contact, it is possible for the OE to serve as a point of entry for neurotropic viruses, which are viruses that can spread to the central nervous system via the olfactory pathway.

Analysis Methodology and Key Findings

  • The study involved the analysis of the complete noses of five adult horses.
  • Two distinct subtypes of the OE, called and , were identified and found to express different markers.
  • The statistical analysis was performed to confirm the descriptive findings.
  • The subtype was mostly located in the caudodorsal areas of the nasal turbinates, showing a significant decline towards the rostroventral direction.
  • Through Immunohistochemical techniques, the researchers found that the protein expression varied between the two identified subtypes. was observed to have more expression of the olfactory marker protein and doublecortin (DCX), while had a higher expression of proliferating cell nuclear antigen and tropomyosin receptor kinase A.

Comparative Results and Conclusions

  • Comparison of protein expression profiles revealed that the equine OE corresponds with that of canines and rodents. However, the geographic localization and cytoarchitecture differed, particularly between equine and canine OE.
  • The subtype showed more relation to the mature OE while resembled a more juvenile form.
  • The study suggests that differences in OE might contribute to species-specific susceptibility to intranasal virus infections such as Borna disease virus, equine herpesvirus 1(EHV-1), hendra virus, influenza virus, rabies virus, and vesicular stomatitis virus.
  • To establish this possibility, further research is needed to understand how these differences could influence susceptibility to viral infections.

Cite This Article

APA
Kupke A, Wenisch S, Failing K, Herden C. (2016). Intranasal Location and Immunohistochemical Characterization of the Equine Olfactory Epithelium. Front Neuroanat, 10, 97. https://doi.org/10.3389/fnana.2016.00097

Publication

Frontiers in neuroanatomy
ISSN: 1662-5129
NlmUniqueID: 101477943
Country: Switzerland
Language: English
Volume: 10
Pages: 97

Researcher Affiliations

Kupke, Alexandra
  • Institute of Veterinary Pathology, Faculty of Veterinary Medicine, Justus Liebig University GiessenGiessen, Germany; Institute of Virology, Philipps University MarburgMarburg, Germany.
Wenisch, Sabine
  • Small Animal Clinic c/o Institute of Veterinary Anatomy, Histology and Embryology, Department of Veterinary Clinical Sciences, Justus Liebig University Giessen Giessen, Germany.
Failing, Klaus
  • Unit for Biomathematics and Data Processing, Faculty of Veterinary Medicine, Justus Liebig University Giessen Giessen, Germany.
Herden, Christiane
  • Institute of Veterinary Pathology, Faculty of Veterinary Medicine, Justus Liebig University Giessen Giessen, Germany.

References

This article includes 67 references
  1. Astic L, Saucier D. Anatomical mapping of the neuroepithelial projection to the olfactory bulb in the rat. Brain Res. Bull. 16 445–454.
    doi: 10.1016/0361-9230(86)90172-3pubmed: 3719376google scholar: lookup
  2. Barrios AW, Sanchez-Quinteiro P, Salazar I. Dog and mouse: toward a balanced view of the mammalian olfactory system. Front. Neuroanat. 8:106.
    doi: 10.3389/fnana.2014.00106pmc: PMC4174761pubmed: 25309347google scholar: lookup
  3. Barrios AW, Sanchez Quinteiro P, Salazar I. The nasal cavity of the sheep and its olfactory sensory epithelium. Microsc. Res. Tech. 77 1052–1059.
    doi: 10.1002/jemt.22436pubmed: 25213000google scholar: lookup
  4. Benarroch EE. Olfactory system: functional organization and involvement in neurodegenerative disease. Neurology 75 1104–1109.
    doi: 10.1212/WNL.0b013e3181f3db84pubmed: 20855854google scholar: lookup
  5. Bock P, Rohn K, Beineke A, Baumgartner W, Wewetzer K. Site-specific population dynamics and variable olfactory marker protein expression in the postnatal canine olfactory epithelium. J. Anat. 215 522–535.
    doi: 10.1111/j.1469-7580.2009.01147.xpmc: PMC2780570pubmed: 19788548google scholar: lookup
  6. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 1–10.
    doi: 10.1002/cne.10874pubmed: 14574675google scholar: lookup
  7. Buiakova OI, Baker H, Scott JW, Farbman A, Kream R, Grillo M. Olfactory marker protein (OMP) gene deletion causes altered physiological activity of olfactory sensory neurons. Proc. Natl. Acad. Sci. U.S.A. 93 9858–9863.
    doi: 10.1073/pnas.93.18.9858pmc: PMC38519pubmed: 8790421google scholar: lookup
  8. Buiakova OI, Krishna NS, Getchell TV, Margolis FL. Human and rodent OMP genes: conservation of structural and regulatory motifs and cellular localization. Genomics 20 452–462.
    doi: 10.1006/geno.1994.1200pubmed: 8034318google scholar: lookup
  9. Calof AL, Chikaraishi DM. Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3 115–127.
    doi: 10.1016/0896-6273(89)90120-7pubmed: 2482777google scholar: lookup
  10. Camara JA, Garrosa M, Gayoso MJ. Histological changes in rat nasal epithelia after unilateral neonatal naris occlusion. Microsc. Res. Tech. 69 585–594.
    doi: 10.1002/jemt.20314pubmed: 16718664google scholar: lookup
  11. Carr VM, Farbman AI, Colletti LM, Morgan JI. Identification of a new non-neuronal cell type in rat olfactory epithelium. Neuroscience 45 433–449.
    doi: 10.1016/0306-4522(91)90239-Kpubmed: 1762687google scholar: lookup
  12. Carson C, Murdoch B, Roskams AJ. Notch 2 and Notch 1/3 segregate to neuronal and glial lineages of the developing olfactory epithelium. Dev. Dyn. 235 1678–1688.
    doi: 10.1002/dvdy.20733pubmed: 16518823google scholar: lookup
  13. Carter LA, MacDonald JL, Roskams AJ. Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J. Neurosci. 24 5670–5683.
    doi: 10.1523/JNEUROSCI.0330-04.2004pmc: PMC6729216pubmed: 15215289google scholar: lookup
  14. Chen X, Fang H, Schwob JE. Multipotency of purified, transplanted globose basal cells in olfactory epithelium. J. Comp. Neurol. 469 457–474.
    doi: 10.1002/cne.11031pubmed: 14755529google scholar: lookup
  15. Choi JH, Lee CH, Yoo KY, Kwon SH, Her S, Shin HC. Immunoreactivity and protein levels of olfactory marker protein and tyrosine hydroxylase are not changed in the dog main olfactory bulb during normal ageing. J. Comp. Pathol. 142 147–156.
    doi: 10.1016/j.jcpa.2009.10.013pubmed: 19954797google scholar: lookup
  16. . Statistical Software for Exact Nonparametric Inference, User Manual. .
  17. Davis JA, Reed RR. Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J. Neurosci. 16 5082–5094.
    pmc: PMC6579294pubmed: 8756438
  18. Deckner ML, Frisen J, Verge VM, Hokfelt T, Risling M. Localization of neurotrophin receptors in olfactory epithelium and bulb. Neuroreport 5 301–304.
    doi: 10.1097/00001756-199312000-00030pubmed: 8298092google scholar: lookup
  19. . BMDP Statistical Software Manual Vol. 1 and 2. .
  20. Doty RL. The olfactory system and its disorders. Semin. Neurol. 29 74–81.
    doi: 10.1055/s-0028-1124025pubmed: 19214935google scholar: lookup
  21. Farbman AI. Olfactory neurogenesis: genetic or environmental controls?. Trends Neurosci. 13 362–365.
    doi: 10.1016/0166-2236(90)90017-5pubmed: 1699323google scholar: lookup
  22. Farbman AI, Margolis FL. Olfactory marker protein during ontogeny: immunohistochemical localization. Dev. Biol. 74 205–215.
    doi: 10.1016/0012-1606(80)90062-7pubmed: 7350009google scholar: lookup
  23. Feron F, Bianco J, Ferguson I, Mackay-Sim A. Neurotrophin expression in the adult olfactory epithelium. Brain Res. 1196 13–21.
    doi: 10.1016/j.brainres.2007.12.003pubmed: 18234155google scholar: lookup
  24. Garcia-Suarez O, Germana G, Naves FJ, Ciriaco E, Represa J, Vega JA. Sensory epithelium of the vomeronasal organ express TrkA-like and epidermal growth factor receptor in adulthood. An immunohistochemical study in the horse. Anat. Rec. 247 299–306.
    doi: 10.1002/(SICI)1097-0185(199703)247:3<299::AID-AR1>3.0.CO;2-Qpubmed: 9066907google scholar: lookup
  25. Goldstein BJ, Schwob JE. Analysis of the globose basal cell compartment in rat olfactory epithelium using GBC-1, a new monoclonal antibody against globose basal cells. J. Neurosci. 16 4005–4016.
    pmc: PMC6578610pubmed: 8656294
  26. Graziadei GA, Stanley RS, Graziadei PP. The olfactory marker protein in the olfactory system of the mouse during development. Neuroscience 5 1239–1252.
    doi: 10.1016/0306-4522(80)90197-9pubmed: 7402467google scholar: lookup
  27. Graziadei PP, Graziadei GA. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8 1–18.
    doi: 10.1007/BF01206454pubmed: 438867google scholar: lookup
  28. Graziadei PP, Monti Graziadei AG. Regeneration in the olfactory system of vertebrates. Am. J. Otolaryngol. 4 228–233.
    doi: 10.1016/S0196-0709(83)80063-5pubmed: 6353965google scholar: lookup
  29. Hartman BK, Margolis FL. Immunofluorescence localization of the olfactory marker protein. Brain Res. 96 176–180.
    doi: 10.1016/0006-8993(75)90593-4pubmed: 1100198google scholar: lookup
  30. Hempstead JL, Morgan JI. Monoclonal antibodies to the rat olfactory sustentacular cell. Brain Res. 288 289–295.
    doi: 10.1016/0006-8993(83)90105-1pubmed: 6362774google scholar: lookup
  31. Herden C, Briese T, Lipkin WI, Richt JA. Bornaviridae. Fields Virology 6th Edn 1124–1150.
  32. Hirschberger J. Herstellung und Charakterisierung monoklonaler Antikörper gegen T-Lymphozyten des Huhnes. .
  33. Holbrook EH, Szumowski KE, Schwob JE. An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium. J. Comp. Neurol. 363 129–146.
    doi: 10.1002/cne.903630111pubmed: 8682932google scholar: lookup
  34. Holbrook EH, Wu E, Curry WT, Lin DT, Schwob JE. Immunohistochemical characterization of human olfactory tissue. Laryngoscope 121 1687–1701.
    doi: 10.1002/lary.21856pmc: PMC3181071pubmed: 21792956google scholar: lookup
  35. Kalinke U, Bechmann I, Detje CN. Host strategies against virus entry via the olfactory system. Virulence 2 367–370.
    doi: 10.4161/viru.2.4.16138pubmed: 21758005google scholar: lookup
  36. Kavoi B, Makanya A, Hassanali J, Carlsson HE, Kiama S. Comparative functional structure of the olfactory mucosa in the domestic dog and sheep. Ann. Anat. 192 329–337.
    doi: 10.1016/j.aanat.2010.07.004pubmed: 20801626google scholar: lookup
  37. Keller A, Margolis FL. Immunological studies of the rat olfactory marker protein. J. Neurochem. 24 1101–1106.
    doi: 10.1111/j.1471-4159.1975.tb03883.xpubmed: 805214google scholar: lookup
  38. Kern RC. Chronic sinusitis and anosmia: pathologic changes in the olfactory mucosa. Laryngoscope 110 1071–1077.
    doi: 10.1097/00005537-200007000-00001pubmed: 10892672google scholar: lookup
  39. Koo JH, Gill S, Pannell LK, Menco BP, Margolis JW, Margolis FL. The interaction of Bex and OMP reveals a dimer of OMP with a short half-life. J. Neurochem. 90 102–116.
    doi: 10.1111/j.1471-4159.2004.02463.xpubmed: 15198671google scholar: lookup
  40. Krishna NS, Little SS, Getchell TV. Epidermal growth factor receptor mRNA and protein are expressed in progenitor cells of the olfactory epithelium. J. Comp. Neurol. 373 297–307.
    doi: 10.1002/(SICI)1096-9861(19960916)373:2<297::AID-CNE11>3.0.CO;2-Ipubmed: 8889929google scholar: lookup
  41. Kumar P, Timoney JF, Southgate HH, Sheoran AS. Light and scanning electron microscopic studies of the nasal turbinates of the horse. Anat. Histol. Embryol. 29 103–109.
    doi: 10.1046/j.1439-0264.2000.00244.xpubmed: 10932387google scholar: lookup
  42. Mackay-Sim A, Kittel P. Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J. Neurosci. 11 979–984.
    pmc: PMC6575367pubmed: 2010818
  43. McGavern DB, Kang SS. Illuminating viral infections in the nervous system. Nat. Rev. Immunol. 11 318–329.
    doi: 10.1038/nri2971pmc: PMC5001841pubmed: 21508982google scholar: lookup
  44. Miller MA, Kottler SJ, Ramos-Vara JA, Johnson PJ, Ganjam VK, Evans TJ. 3-methylindole induces transient olfactory mucosal injury in ponies. Vet. Pathol. 40 363–370.
    doi: 10.1354/vp.40-4-363pubmed: 12824507google scholar: lookup
  45. Morales JA, Herzog S, Kompter C, Frese K, Rott R. Axonal transport of Borna disease virus along olfactory pathways in spontaneously and experimentally infected rats. Med. Microbiol. Immunol. 177 51–68.
    doi: 10.1007/BF00189527pubmed: 2452338google scholar: lookup
  46. Mori I, Nishiyama Y, Yokochi T, Kimura Y. Olfactory transmission of neurotropic viruses. J. Neurovirol. 11 129–137.
    doi: 10.1080/13550280590922793pubmed: 16036791google scholar: lookup
  47. Morrison EE, Costanzo RM. Morphology of olfactory epithelium in humans and other vertebrates. Microsc. Res. Tech. 23 49–61.
    doi: 10.1002/jemt.1070230105pubmed: 1392071google scholar: lookup
  48. Murdoch B, Roskams AJ. Olfactory epithelium progenitors: insights from transgenic mice and in vitro biology. J. Mol. Histol. 38 581–599.
    doi: 10.1007/s10735-007-9141-2pubmed: 17851769google scholar: lookup
  49. Nickel R, Schummer A, Seiferle E. Lehrbuch der anatomie der haustiere. .
  50. Patel RM, Pinto JM. Olfaction: anatomy, physiology, and disease. Clin. Anat. 27 54–60.
    doi: 10.1002/ca.22338pubmed: 24272785google scholar: lookup
  51. Reinacher M, Bonin J, Narayan O, Scholtissek C. Pathogenesis of neurovirulent influenza A virus infection in mice. Route of entry of virus into brain determines infection of different populations of cells. Lab. Invest. 49 686–692.
    pubmed: 6656200
  52. Reisert J, Yau KW, Margolis FL. Olfactory marker protein modulates the cAMP kinetics of the odour-induced response in cilia of mouse olfactory receptor neurons. J. Physiol. 585 731–740.
    doi: 10.1113/jphysiol.2007.142471pmc: PMC2375515pubmed: 17932148google scholar: lookup
  53. Roskams AJ, Bethel MA, Hurt KJ, Ronnett GV. Sequential expression of Trks A, B, and C in the regenerating olfactory neuroepithelium. J. Neurosci. 16 1294–1307.
    pmc: PMC6578567pubmed: 8778281
  54. Rossler P, Mezler M, Breer H. Two olfactory marker proteins in Xenopus laevis. J. Comp. Neurol. 395 273–280.
    doi: 10.1002/(SICI)1096-9861(19980808)395:3<273::AID-CNE1>3.0.CO;2-#pubmed: 9596523google scholar: lookup
  55. Salazar I, Sanchez-Quinteiro P. A detailed morphological study of the vomeronasal organ and the accessory olfactory bulb of cats. Microsc. Res. Tech. 74 1109–1120.
    doi: 10.1002/jemt.21002pubmed: 21484946google scholar: lookup
  56. Salinas S, Schiavo G, Kremer EJ. A hitchhiker’s guide to the nervous system: the complex journey of viruses and toxins. Nat. Rev. Microbiol. 8 645–655.
    doi: 10.1038/nrmicro2395pubmed: 20706281google scholar: lookup
  57. Schwartz Levey M, Chikaraishi DM, Kauer JS. Characterization of potential precursor populations in the mouse olfactory epithelium using immunocytochemistry and autoradiography. J. Neurosci. 11 3556–3564.
    pmc: PMC6575532pubmed: 1719164
  58. Schwob JE. Neural regeneration and the peripheral olfactory system. Anat. Rec. 269 33–49.
    doi: 10.1002/ar.10047pubmed: 11891623google scholar: lookup
  59. Schwob JE, Huard JM, Luskin MB, Youngentob SL. Retroviral lineage studies of the rat olfactory epithelium. Chem. Senses 19 671–682.
    doi: 10.1093/chemse/19.6.671pubmed: 7735846google scholar: lookup
  60. Schwob JE, Youngentob SL, Mezza RC. Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. Comp. Neurol. 359 15–37.
    doi: 10.1002/cne.903590103pubmed: 8557844google scholar: lookup
  61. Shankar V, Kao M, Hamir AN, Sheng H, Koprowski H, Dietzschold B. Kinetics of virus spread and changes in levels of several cytokine mRNAs in the brain after intranasal infection of rats with Borna disease virus. J. Virol. 66 992–998.
    pmc: PMC240801pubmed: 1731117
  62. Strotmann J, Wanner I, Helfrich T, Beck A, Breer H. Rostro-caudal patterning of receptor-expressing olfactory neurones in the rat nasal cavity. Cell Tissue Res. 278 11–20.
    doi: 10.1007/BF00305773pubmed: 7954694google scholar: lookup
  63. Strotmann J, Wanner I, Helfrich T, Beck A, Meinken C, Kubick S. Olfactory neurones expressing distinct odorant receptor subtypes are spatially segregated in the nasal neuroepithelium. Cell Tissue Res. 276 429–438.
    doi: 10.1007/BF00343941pubmed: 8062338google scholar: lookup
  64. van Riel D, Verdijk R, Kuiken T. The olfactory nerve: a shortcut for influenza and other viral diseases into the central nervous system. J. Pathol. 235 277–287.
    doi: 10.1002/path.4461pubmed: 25294743google scholar: lookup
  65. Verhaagen J, Greer CA, Margolis FL. B-50/GAP43 gene expression in the rat olfactory system during postnatal development and aging. Eur. J. Neurosci. 2 397–407.
    doi: 10.1111/j.1460-9568.1990.tb00432.xpubmed: 12106027google scholar: lookup
  66. Weiler E, Benali A. Olfactory epithelia differentially express neuronal markers. J. Neurocytol. 34 217–240.
    doi: 10.1007/s11068-005-8355-zpubmed: 16841165google scholar: lookup
  67. Weiler E, Farbman AI. Supporting cell proliferation in the olfactory epithelium decreases postnatally. Glia 22 315–328.
    doi: 10.1002/(SICI)1098-1136(199804)22:4<315::AID-GLIA1>3.0.CO;2-2pubmed: 9517564google scholar: lookup

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