Histochemical and ultrastructural analyses of the lubrication systems in the olfactory organs of soft-shelled turtle

In general, the nasal cavity of turtles is divided into two chambers: the upper chamber, lined with the olfactory epithelium containing ciliated olfactory receptor cells, and the lower chamber, lined with the vomeronasal epithelium containing microvillous receptor cells. In the nasal cavity of soft-...

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Published inJournal of Veterinary Medical Science Vol. 78; no. 5; pp. 769 - 774
Main Authors NAKAMUTA, Shoko, YOKOSUKA, Makoto, TANIGUCHI, Kazumi, YAMAMOTO, Yoshio, NAKAMUTA, Nobuaki
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Published Japan JAPANESE SOCIETY OF VETERINARY SCIENCE 01.01.2016
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Abstract In general, the nasal cavity of turtles is divided into two chambers: the upper chamber, lined with the olfactory epithelium containing ciliated olfactory receptor cells, and the lower chamber, lined with the vomeronasal epithelium containing microvillous receptor cells. In the nasal cavity of soft-shelled turtles, however, differences between the upper and lower chamber epithelia are unclear due to the presence of ciliated receptor cells in both epithelia. In the olfactory organ of vertebrates, the surface of sensory epithelium is covered with secretory products of associated glands and supporting cells, playing important roles in the olfaction by dissolving odorants and transporting them to the olfactory receptors. Here, the associated glands and supporting cells in the olfactory organ of soft-shelled turtles were analyzed histochemically and ultrastructurally. The upper chamber epithelium possessed associated glands, constituted by cells containing serous secretory granules; whereas, the lower chamber epithelium did not. In the upper chamber epithelium, secretory granules filled the supranuclear region of supporting cells, while most of the granules were distributed near the free border of supporting cells in the lower chamber epithelium. The secretory granules in the supporting cells of both epithelia were seromucous, but alcian blue stained them differently from each other. In addition, distinct expression of carbohydrates was suggested by the differences in lectin binding. These data indicate the quantitative and qualitative differences in the secretory properties between the upper and lower chamber epithelia, suggesting their distinct roles in the olfaction.
AbstractList In general, the nasal cavity of turtles is divided into two chambers: the upper chamber, lined with the olfactory epithelium containing ciliated olfactory receptor cells, and the lower chamber, lined with the vomeronasal epithelium containing microvillous receptor cells. In the nasal cavity of soft-shelled turtles, however, differences between the upper and lower chamber epithelia are unclear due to the presence of ciliated receptor cells in both epithelia. In the olfactory organ of vertebrates, the surface of sensory epithelium is covered with secretory products of associated glands and supporting cells, playing important roles in the olfaction by dissolving odorants and transporting them to the olfactory receptors. Here, the associated glands and supporting cells in the olfactory organ of soft-shelled turtles were analyzed histochemically and ultrastructurally. The upper chamber epithelium possessed associated glands, constituted by cells containing serous secretory granules; whereas, the lower chamber epithelium did not. In the upper chamber epithelium, secretory granules filled the supranuclear region of supporting cells, while most of the granules were distributed near the free border of supporting cells in the lower chamber epithelium. The secretory granules in the supporting cells of both epithelia were seromucous, but alcian blue stained them differently from each other. In addition, distinct expression of carbohydrates was suggested by the differences in lectin binding. These data indicate the quantitative and qualitative differences in the secretory properties between the upper and lower chamber epithelia, suggesting their distinct roles in the olfaction.
In general, the nasal cavity of turtles is divided into two chambers: the upper chamber, lined with the olfactory epithelium containing ciliated olfactory receptor cells, and the lower chamber, lined with the vomeronasal epithelium containing microvillous receptor cells. In the nasal cavity of soft-shelled turtles, however, differences between the upper and lower chamber epithelia are unclear due to the presence of ciliated receptor cells in both epithelia. In the olfactory organ of vertebrates, the surface of sensory epithelium is covered with secretory products of associated glands and supporting cells, playing important roles in the olfaction by dissolving odorants and transporting them to the olfactory receptors. Here, the associated glands and supporting cells in the olfactory organ of soft-shelled turtles were analyzed histochemically and ultrastructurally. The upper chamber epithelium possessed associated glands, constituted by cells containing serous secretory granules; whereas, the lower chamber epithelium did not. In the upper chamber epithelium, secretory granules filled the supranuclear region of supporting cells, while most of the granules were distributed near the free border of supporting cells in the lower chamber epithelium. The secretory granules in the supporting cells of both epithelia were seromucous, but alcian blue stained them differently from each other. In addition, distinct expression of carbohydrates was suggested by the differences in lectin binding. These data indicate the quantitative and qualitative differences in the secretory properties between the upper and lower chamber epithelia, suggesting their distinct roles in the olfaction.
Author TANIGUCHI, Kazumi
NAKAMUTA, Shoko
YAMAMOTO, Yoshio
YOKOSUKA, Makoto
NAKAMUTA, Nobuaki
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Cites_doi 10.1242/jeb.204.24.4199
10.1292/jvms.13-0650
10.1016/0006-8993(96)00267-3
10.1159/000113838
10.1007/BF03404913
10.3389/fnana.2011.00003
10.1186/1471-2202-8-64
10.1002/aja.1001110104
10.1002/ar.21377
10.1523/JNEUROSCI.16-03-01239.1996
10.1016/0300-9629(89)90357-5
10.1002/(SICI)1096-9861(19980824)398:2<273::AID-CNE8>3.0.CO;2-Y
10.1525/california/9780520252783.003.0005
10.2108/zsj.25.178
10.1292/jvms.10-0574
10.1292/jvms.58.7
10.1016/S0092-8674(00)80536-X
10.1002/(SICI)1097-0185(199810)252:2<301::AID-AR16>3.0.CO;2-R
10.1007/BF00335424
10.1016/0896-6273(95)90016-0
10.1016/0092-8674(91)90418-X
10.1242/jeb.201.21.2913
10.1002/jemt.1070230203
10.1007/s003590050287
10.1016/B0-12-370878-8/00142-7
10.1007/BF00221807
10.1016/0092-8674(95)90161-2
10.1159/000113836
10.1085/jgp.98.5.909
10.1292/jvms.15-0359
10.1016/j.tice.2010.07.008
10.1292/jvms.12-0532
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References 28. Schwenk, K. 2008. Comparative anatomy and physiology of chemical senses in nonavian aquatic reptiles. pp. 65–81. In: Sensory Evolution on the Threshold. (Thewissen, J. G. M. and Nummels, S. eds.), Univ. of California Press, Berkley.
33. Taniguchi, K., Toshima, Y., Saito, T. R. and Taniguchi, K. 1996. Development of the olfactory epithelium and vomeronasal organ in the Japanese reddish frog, Rana japonica. J. Vet. Med. Sci. 58: 7–15.
5. Eisthen, H. L. and Polese, G. 2007. Evolution of vertebrate olfactory subsystems. pp. 355–406. In: Evolution of Nervous System Vol. 2 Non-mammalian Vertebrates. (Kaas J. H., ed.), Academic Press, Oxford.
25. Rehorek, S. J., Firth, B. T. and Hutchinson, M. N. 2000. The structure of the nasal chemosensory system in squamate reptiles. 1. The olfactory organ, with special reference to olfaction in geckos. J. Biosci. 25: 173–179.
11. Getchell, M. L. and Getchell, T. V. 1992. Fine structural aspects of secretion and extrinsic innervation in the olfactory mucosa. Microsc. Res. Tech. 23: 111–127.
21. Kratzing, J. E. 1975. The fine structure of the olfactory and vomeronasal organs of a lizard (Tiliqua scincoides scincoides). Cell Tissue Res. 156: 239–252.
6. Endo, D., Yamamoto, Y., Nakamuta, N. and Taniguchi, K. 2011. Developmental changes in lectin-binding patterns of three nasal sensory epithelia in Xenopus laevis. Anat. Rec. (Hoboken) 294: 839–846.
8. Franceschini, V., Lazzari, M. and Ciani, F. 1996. Identification of surface glycoconjugates in the olfactory system of turtle. Brain Res. 725: 81–87.
19. Ibrahim, D., Nakamuta, N., Taniguchi, K. and Taniguchi, K. 2013. Lectin histochemical studies on the vomeronasal organ of the sheep. J. Vet. Med. Sci. 75: 1131–1137.
32. Taniguchi, K. and Taniguchi, K. 2014. Phylogenic studies on the olfactory system in vertebrates. J. Vet. Med. Sci. 76: 781–788.
2. Damjanov, I. 1987. Lectin cytochemistry and histochemistry. Lab. Invest. 57: 5–20.
18. Herrada, G. and Dulac, C. 1997. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90: 763–773.
30. Shoji, T. and Kurihara, K. 1991. Sensitivity and transduction mechanisms of responses to general odorants in turtle vomeronasal system. J. Gen. Physiol. 98: 909–919.
20. Kondoh, D., Nashimoto, M., Kanayama, S., Nakamuta, N. and Taniguchi, K. 2011. Ultrastructural and histochemical properties of the olfactory system in the Japanese jungle crow, Corvus macrorhynchos. J. Vet. Med. Sci. 73: 1007–1014.
13. Hansen, A. 2007. Olfactory and solitary chemosensory cells: two different chemosensory systems in the nasal cavity of the American alligator, Alligator mississippiensis. BMC Neurosci. 8: 64.
34. Taniguchi, M., Kashiwayanagi, M. and Kurihara, K. 1996. Intracellular dialysis of cyclic nucleotides induces inward currents in turtle vomeronasal receptor neurons. J. Neurosci. 16: 1239–1246.
9. Freitag, J., Krieger, J., Strotmann, J. and Breer, H. 1995. Two classes of olfactory receptors in Xenopus laevis. Neuron 15: 1383–1392.
7. Fadool, D. A., Wachowiak, M. and Brann, J. H. 2001. Patch-clamp analysis of voltage-activated and chemically activated currents in the vomeronasal organ of Sternotherus odoratus (stinkpot/musk turtle). J. Exp. Biol. 204: 4199–4212.
16. Hatanaka, T. and Matsuzaki, O. 1993. Odor responses of the vomeronasal system in Reeve’s turtle, Geoclemys reevesii. Brain Behav. Evol. 41: 183–186.
26. Rehorek, S. J., Firth, B. T. and Hutchinson, M. N. 2000. The structure of the nasal chemosensory system in squamate reptiles. 2. Lubricatory capacity of the vomeronasal organ. J. Biosci. 25: 181–190.
4. Døving, K. B. and Trotier, D. 1998. Structure and function of the vomeronasal organ. J. Exp. Biol. 201: 2913–2925.
1. Buck, L. and Axel, R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65: 175–187.
3. Dulac, C. and Axel, R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83: 195–206.
29. Shackleford, J. M. and Klapper, E. C. 1962. Structure and carbohydrate histochemistry of mammalian salivary glands. Am. J. Anat. 111: 25–47.
15. Hatanaka, T. and Matsuzaki, O. 1989. Odor response patterns of single units in the accessory olfactory bulb of the turtle, Geoclemys reevesii. Comp. Biochem. Physiol. A 92: 505–512.
23. Nakamuta, S., Yokosuka, M., Taniguchi, K., Yamamoto, Y. and Nakamuta, N. 2016. Immunohistochemical analysis for G protein in the olfactory organs of soft-shelled turtle, Pelodiscus sinensis. J. Vet. Med. Sci. 78: 245–250.
24. Oikawa, T., Suzuki, K., Saito, T. R., Takahashi, K. W. and Taniguchi, K. 1998. Fine structure of three types of olfactory organs in Xenopus laevis. Anat. Rec. 252: 301–310.
12. Graziadei, P. P. and Tucker, D. 1970. Vomeronasal receptors in turtles. Z. Zellforsch. Mikrosk. Anat. 105: 498–514.
14. Hansen, A., Reiss, J. O., Gentry, C. L. and Burd, G. D. 1998. Ultrastructure of the olfactory organ in the clawed frog, Xenopus laevis, during larval development and metamorphosis. J. Comp. Neurol. 398: 273–288.
36. Wakabayashi, Y. and Ichikawa, M. 2008. Localization of G protein alpha subunits and morphology of receptor neurons in olfactory and vomeronasal epithelia in Reeve’s turtle, Geoclemys reevesii. Zoolog. Sci. 25: 178–187.
10. Freitag, J., Ludwig, G., Andreini, I., Rössler, P. and Breer, H. 1998. Olfactory receptors in aquatic and terrestrial vertebrates. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 183: 635–650.
27. Saito, S., Oikawa, T., Taniguchi, K. and Taniguchi, K. 2010. Fine structure of the vomeronasal organ in the grass lizard, Takydromus tachydromoides. Tissue Cell 42: 322–327.
31. Shoji, T., Enomoto, S., Taniguchi, M. and Kurihara, K. 1993. Transduction mechanisms in the olfactory and vomeronasal organs of turtles. Brain Behav. Evol. 41: 192–197.
17. Hatanaka, T., Matsuzaki, O. and Shibuya, T. 1982. Fine structure of vomeronasal receptor cells in the Reeve’s turtle, Geoclemys reevesii. Zool. Mag. 91: 190–193.
35. Ubeda-Bañon, I., Pro-Sistiaga, P., Mohedano-Moriano, A., Saiz-Sanchez, D., de la Rosa-Prieto, C., Gutierrez-Castellanos, N., Lanuza, E., Martinez-Garcia, F. and Martinez-Marcos, A. 2011. Cladistic analysis of olfactory and vomeronasal systems. Front Neuroanat. 5: 3.
22. Nakamuta, S., Nakamuta, N. and Taniguchi, K. 2010. Immunohistochemical study on G protein alpha subunits in the olfactory system of red-eared turtle. Kaibogaku Zasshi 85: 143 [in Japanese].
9776085 - Anat Rec. 1998 Oct;252(2):301-10
10878858 - J Biosci. 2000 Jun;25(2):173-9
3298849 - Lab Invest. 1987 Jul;57(1):5-20
17683564 - BMC Neurosci. 2007 Aug 03;8:64
1421551 - Microsc Res Tech. 1992 Oct 15;23(2):111-27
8645760 - J Vet Med Sci. 1996 Jan;58(1):7-15
18533749 - Zoolog Sci. 2008 Feb;25(2):178-87
1765762 - J Gen Physiol. 1991 Nov;98 (5):909-19
21478653 - J Vet Med Sci. 2011 Aug;73(8):1007-14
21290004 - Front Neuroanat. 2011 Jan 26;5:3
8558252 - J Neurosci. 1996 Feb 1;16(3):1239-46
8828589 - Brain Res. 1996 Jun 24;725(1):81-7
9839455 - J Comp Physiol A. 1998 Nov;183(5):635-50
8845161 - Neuron. 1995 Dec;15(6):1383-92
9700571 - J Comp Neurol. 1998 Aug 24;398(2):273-88
23595118 - J Vet Med Sci. 2013;75(9):1131-7
11815645 - J Exp Biol. 2001 Dec;204(Pt 24):4199-212
7682889 - Brain Behav Evol. 1993;41(3-5):192-7
8386587 - Brain Behav Evol. 1993;41(3-5):183-6
4919108 - Z Zellforsch Mikrosk Anat. 1970;105(4):498-514
7585937 - Cell. 1995 Oct 20;83(2):195-206
26440778 - J Vet Med Sci. 2016 Feb;78(2):245-50
13911094 - Am J Anat. 1962 Jul;111:25-47
10878859 - J Biosci. 2000 Jun;25(2):181-90
9288755 - Cell. 1997 Aug 22;90(4):763-73
21433307 - Anat Rec (Hoboken). 2011 May;294(5):839-46
24531771 - J Vet Med Sci. 2014 Jun;76(6):781-8
20817242 - Tissue Cell. 2010 Oct;42(5):322-7
9866877 - J Exp Biol. 1998 Nov;201(Pt 21):2913-25
1122519 - Cell Tissue Res. 1975;156(2):239-52
1840504 - Cell. 1991 Apr 5;65(1):175-87
22
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  doi: 10.1242/jeb.204.24.4199
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  doi: 10.1292/jvms.13-0650
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  doi: 10.1016/0006-8993(96)00267-3
– ident: 31
  doi: 10.1159/000113838
– ident: 26
  doi: 10.1007/BF03404913
– ident: 35
  doi: 10.3389/fnana.2011.00003
– ident: 13
  doi: 10.1186/1471-2202-8-64
– ident: 29
  doi: 10.1002/aja.1001110104
– ident: 6
  doi: 10.1002/ar.21377
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  doi: 10.1523/JNEUROSCI.16-03-01239.1996
– ident: 15
  doi: 10.1016/0300-9629(89)90357-5
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  doi: 10.1002/(SICI)1096-9861(19980824)398:2<273::AID-CNE8>3.0.CO;2-Y
– ident: 28
  doi: 10.1525/california/9780520252783.003.0005
– ident: 36
  doi: 10.2108/zsj.25.178
– ident: 22
– ident: 17
– ident: 20
  doi: 10.1292/jvms.10-0574
– ident: 33
  doi: 10.1292/jvms.58.7
– ident: 18
  doi: 10.1016/S0092-8674(00)80536-X
– ident: 24
  doi: 10.1002/(SICI)1097-0185(199810)252:2<301::AID-AR16>3.0.CO;2-R
– ident: 12
  doi: 10.1007/BF00335424
– ident: 9
  doi: 10.1016/0896-6273(95)90016-0
– ident: 1
  doi: 10.1016/0092-8674(91)90418-X
– ident: 4
  doi: 10.1242/jeb.201.21.2913
– ident: 11
  doi: 10.1002/jemt.1070230203
– ident: 10
  doi: 10.1007/s003590050287
– ident: 5
  doi: 10.1016/B0-12-370878-8/00142-7
– ident: 21
  doi: 10.1007/BF00221807
– ident: 3
  doi: 10.1016/0092-8674(95)90161-2
– ident: 16
  doi: 10.1159/000113836
– ident: 30
  doi: 10.1085/jgp.98.5.909
– ident: 23
  doi: 10.1292/jvms.15-0359
– ident: 27
  doi: 10.1016/j.tice.2010.07.008
– ident: 19
  doi: 10.1292/jvms.12-0532
– ident: 25
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Snippet In general, the nasal cavity of turtles is divided into two chambers: the upper chamber, lined with the olfactory epithelium containing ciliated olfactory...
In general, the nasal cavity of turtles is divided into two chambers: the upper chamber, lined with the olfactory epithelium containing ciliated olfactory...
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SubjectTerms Animals
associated glands
chemoreception
electron microscopy
Exocrine Glands - ultrastructure
Female
Male
Microscopy, Electron, Transmission - veterinary
Nasal Cavity - anatomy & histology
Nasal Cavity - ultrastructure
Nasal Mucosa - ultrastructure
Receptors, Odorant - ultrastructure
reptile
supporting cells
Turtles - anatomy & histology
Turtles - physiology
Wildlife Science
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Title Histochemical and ultrastructural analyses of the lubrication systems in the olfactory organs of soft-shelled turtle
URI https://www.jstage.jst.go.jp/article/jvms/78/5/78_15-0564/_article/-char/en
https://www.ncbi.nlm.nih.gov/pubmed/26782135
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https://search.proquest.com/docview/1811903217
https://pubmed.ncbi.nlm.nih.gov/PMC4905829
Volume 78
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ispartofPNX Journal of Veterinary Medical Science, 2016, Vol.78(5), pp.769-774
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