DOI QR코드

DOI QR Code

Lectin histochemistry of the olfactory mucosa of Korean native cattle, Bos taurus coreanae

  • Sungwoong, Jang (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University) ;
  • Bohye, Kim (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University) ;
  • Jeongmin, Lee (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University) ;
  • Sohi, Kang (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University) ;
  • Joong-Sun, Kim (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University) ;
  • Jong-Choon, Kim (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University) ;
  • Sung-Ho, Kim (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University) ;
  • Taekyun, Shin (Department of Veterinary Anatomy, College of Veterinary Medicine, Jeju National University) ;
  • Changjong, Moon (Department of Veterinary Anatomy and Animal Behavior, College of Veterinary Medicine and BK21 FOUR Program, Chonnam National University)
  • Received : 2022.07.01
  • Accepted : 2022.09.13
  • Published : 2022.11.30

Abstract

Background: The olfactory mucosa (OM) is crucial for odorant perception in the main olfactory system. The terminal carbohydrates of glycoconjugates influence chemoreception in the olfactory epithelium (OE). Objectives: The histological characteristics and glycoconjugate composition of the OM of Korean native cattle (Hanwoo, Bos taurus coreae) were examined to characterize their morphology and possible functions during postnatal development. Methods: The OM of neonate and adult Korean native cattle was evaluated using histological, immunohistochemical, and lectin histochemical methods. Results: Histologically, the OM in both neonates and adults consists of the olfactory epithelium and the lamina propria. Additionally, using periodic acid Schiff and Alcian blue (pH 2.5), the mucus specificity of the Bowman's gland duct and acini in the lamina propria was determined. Immunohistochemistry demonstrated that mature and immature olfactory sensory neurons of OEs express the olfactory marker protein and growth associated protein-43, respectively. Lectin histochemistry indicated that numerous glycoconjugates, including as N-acetylglucosamine, mannose, galactose, N-acetylgalactosamine, complex type N-glycan, and fucose groups, were expressed at varied levels in the different cell types in the OMs of neonates and adults at varying levels. According to our observations, the cattle possessed a well-developed olfactory system, and the expression patterns of glycoconjugates in neonatal and adult OMs varied considerably. Conclusions: This is the first study to describe the morphological assessment of the OM of Korean native cattle with a focus on lectin histochemistry. The findings suggest that glycoconjugates may play a role in olfactory chemoreception, and that their labeling properties may be closely related to OM development and maturity.

Keywords

Acknowledgement

This research was supported by the National Research Foundation (NRF) of Korea grant funded by the Korean Government (NRF-2022R1A2C1004022).

References

  1. Ache BW, Young JM. Olfaction: diverse species, conserved principles. Neuron. 2005;48(3):417-430. https://doi.org/10.1016/j.neuron.2005.10.022
  2. Mendoza AS. Morphological studies on the rodent main and accessory olfactory systems: the regio olfactoria and vomeronasal organ. Ann Anat. 1993;175(5):425-446. https://doi.org/10.1016/S0940-9602(11)80110-X
  3. Meredith M. Human vomeronasal organ function: a critical review of best and worst cases. Chem Senses. 2001;26(4):433-445. https://doi.org/10.1093/chemse/26.4.433
  4. Xu F, Greer CA, Shepherd GM. Odor maps in the olfactory bulb. J Comp Neurol. 2000;422(4):489-495. https://doi.org/10.1002/1096-9861(20000710)422:4<489::AID-CNE1>3.0.CO;2-#
  5. Tirindelli R, Dibattista M, Pifferi S, Menini A. From pheromones to behavior. Physiol Rev. 2009;89(3):921-956. https://doi.org/10.1152/physrev.00037.2008
  6. Halpern M, Martinez-Marcos A. Structure and function of the vomeronasal system: an update. Prog Neurobiol. 2003;70(3):245-318.
  7. Buck LB. The molecular architecture of odor and pheromone sensing in mammals. Cell. 2000;100(6):611-618. https://doi.org/10.1016/S0092-8674(00)80698-4
  8. Dulac C, Torello AT. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci. 2003;4(7):551-562.   https://doi.org/10.1038/nrn1140
  9. Mucignat-Caretta C, Redaelli M, Caretta A. One nose, one brain: contribution of the main and accessory olfactory system to chemosensation. Front Neuroanat. 2012;6:46.
  10. Morrison EE, Costanzo RM. Morphology of olfactory epithelium in humans and other vertebrates. Microsc Res Tech. 1992;23(1):49-61. https://doi.org/10.1002/jemt.1070230105
  11. Sharma A, Kumar R, Aier I, Semwal R, Tyagi P, Varadwaj P. Sense of smell: structural, functional, mechanistic advancements and challenges in human olfactory research. Curr Neuropharmacol. 2019;17(9):891-911. https://doi.org/10.2174/1570159X17666181206095626
  12. Eisthen HL. Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates. Microsc Res Tech. 1992;23(1):1-21. https://doi.org/10.1002/jemt.1070230102
  13. Plendl J, Sinowatz F. Glycobiology of the olfactory system. Acta Anat (Basel). 1998;161(1-4):234-253. https://doi.org/10.1159/000046461
  14. Cook GM. Cell surface carbohydrates: molecules in search of a function? J Cell Sci Suppl. 1986;4:45-70. https://doi.org/10.1242/jcs.1986.Supplement_4.4
  15. Ibrahim D, Nakamuta N, Taniguchi K, Yamamoto Y, Taniguchi K. Histological and lectin histochemical studies on the olfactory and respiratory mucosae of the sheep. J Vet Med Sci. 2014;76(3):339-346. https://doi.org/10.1292/jvms.13-0436
  16. Foster JD, Getchell ML, Getchell TV. Identification of sugar residues in secretory glycoconjugates of olfactory mucosae using lectin histochemistry. Anat Rec. 1991;229(4):525-544. https://doi.org/10.1002/ar.1092290414
  17. Takami S, Getchell ML, Getchell TV. Resolution of sensory and mucoid glycoconjugates with terminal alpha-galactose residues in the mucomicrovillar complex of the vomeronasal sensory epithelium by dual confocal laser scanning microscopy. Cell Tissue Res. 1995;280(2):211-216. https://doi.org/10.1007/BF00307791
  18. Franceschini V, Lazzari M, Revoltella RP, Ciani F. Histochemical study by lectin binding of surface glycoconjugates in the developing olfactory system of rat. Int J Dev Neurosci. 1994;12(3):197-206. https://doi.org/10.1016/0736-5748(94)90041-8
  19. Mendoza AS, Borish-Che'piuz B, Kiune'l V. Lectin-binding properties of the neuroepithelium of the vomeronasal organ, olfactory epithelium proper and the septal organ of Masera in mice (semithin section study). Arkh Anat Gistol Embriol 1989;97(9):76-81.
  20. Smuts MS. Concanavalin A binding to the epithelial surface of the developing mouse olfactory placode. Anat Rec. 1977;188(1):29-37. https://doi.org/10.1002/ar.1091880104
  21. Nakajima T, Shiratori K, Ogawa K, Tanioka Y, Taniguchi K. Lectin-binding patterns in the olfactory epithelium and vomeronasal organ of the common marmoset. J Vet Med Sci. 1998;60(9):1005-1011. https://doi.org/10.1292/jvms.60.1005
  22. Ibrahim D, Nakamuta N. Comparative histochemical analysis of glycoconjugates in the nasal vestibule of camel and sheep. Microsc Res Tech. 2018;81(6):681-689. https://doi.org/10.1002/jemt.23024
  23. Lee KH, Park C, Bang H, Ahn M, Moon C, Kim S, et al. Histochemical study of the olfactory mucosae of the horse. Acta Histochem. 2016;118(4):361-368. https://doi.org/10.1016/j.acthis.2016.03.006
  24. Gheri G, Gheri Bryk S, Balboni GC. Sugar residues of glycoconjugates in the olfactory epithelium of the human fetus: histochemical study using peroxidase-conjugated lectins. Boll Soc Ital Biol Sper 1991;67(8):781-788.
  25. Menco BP, Leunissen JL, Bannister LH, Dodd GH. Bovine olfactory and nasal respiratory epithelium surfaces. High-voltage and scanning electron microscopy, and cryo-ultramicrotomy. Cell Tissue Res. 1978;193(3):503-524. https://doi.org/10.1007/BF00225347
  26. Nomura T, Takahashi S, Ushiki T. Cytoarchitecture of the normal rat olfactory epithelium: light and scanning electron microscopic studies. Arch Histol Cytol. 2004;67(2):159-170. https://doi.org/10.1679/aohc.67.159
  27. 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. 2010;192(5):329-337.   https://doi.org/10.1016/j.aanat.2010.07.004
  28. Solbu TT, Holen T. Aquaporin pathways and mucin secretion of Bowman's glands might protect the olfactory mucosa. Chem Senses. 2012;37(1):35-46.   https://doi.org/10.1093/chemse/bjr063
  29. Buiakova OI, Baker H, Scott JW, Farbman A, Kream R, Grillo M, et al. Olfactory marker protein (OMP) gene deletion causes altered physiological activity of olfactory sensory neurons. Proc Natl Acad Sci U S A. 1996;93(18):9858-9863.   https://doi.org/10.1073/pnas.93.18.9858
  30. Farbman AI, Margolis FL. Olfactory marker protein during ontogeny: immunohistochemical localization. Dev Biol. 1980;74(1):205-215.   https://doi.org/10.1016/0012-1606(80)90062-7
  31. Kuhlmann K, Tschapek A, Wiese H, Eisenacher M, Meyer HE, Hatt HH, et al. The membrane proteome of sensory cilia to the depth of olfactory receptors. Mol Cell Proteomics. 2014;13(7):1828-1843.   https://doi.org/10.1074/mcp.M113.035378
  32. McClintock TS, Khan N, Xie C, Martens JR. Maturation of the olfactory sensory neuron and its cilia. Chem Senses. 2020;45(9):805-822.   https://doi.org/10.1093/chemse/bjaa070
  33. 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. 2009;215(5):522-535.   https://doi.org/10.1111/j.1469-7580.2009.01147.x
  34. Key B, Giorgi PP. Soybean agglutinin binding to the olfactory systems of the rat and mouse. Neurosci Lett. 1986;69(2):131-136.  
  35. Key B, Giorgi PP. Selective binding of soybean agglutinin to the olfactory system of Xenopus. Neuroscience. 1986;18(2):507-515.   https://doi.org/10.1016/0306-4522(86)90171-5
  36. Plendl J, Schmahl W. Dolichos biflorus agglutinin: a marker of the developing olfactory system in the NMRI-mouse strain. Anat Embryol (Berl). 1988;177(5):459-464.   https://doi.org/10.1007/BF00304744
  37. Barber PC. Ulex europeus agglutinin I binds exclusively to primary olfactory neurons in the rat nervous system. Neuroscience. 1989;30(1):1-9.   https://doi.org/10.1016/0306-4522(89)90348-5
  38. Ibrahim D, Abdel-Maksoud F, Taniguchi K, Yamamoto Y, Taniguchi K, Nakamuta N. Immunohistochemical studies for the neuronal elements in the vomeronasal organ of the one-humped camel. J Vet Med Sci. 2015;77(2):241-245.   https://doi.org/10.1292/jvms.14-0424
  39. Ichikawa M, Takami S, Osada T, Graziadei PP. Differential development of binding sites of two lectins in the vomeronasal axons of the rat accessory olfactory bulb. Brain Res Dev Brain Res. 1994;78(1):1-9.   https://doi.org/10.1016/0165-3806(94)90002-7
  40. Gong Q, Shipley MT. Expression of extracellular matrix molecules and cell surface molecules in the olfactory nerve pathway during early development. J Comp Neurol. 1996;366(1):1-14.   https://doi.org/10.1002/(SICI)1096-9861(19960226)366:1<1::AID-CNE1>3.0.CO;2-7
  41. Lee SH, Park BH, Sharma A, Dang CG, Lee SS, Choi TJ, et al. Hanwoo cattle: origin, domestication, breeding strategies and genomic selection. J Anim Sci Technol. 2014;56(1):2.  
  42. Joo YH, Jeong SM, Paradhipta DH, Lee HJ, Lee SS, Choi JS, et al. Improvement of conception rate on Hanwoo; the key hormones and novel estrus detector. J Anim Sci Technol. 2021;63(6):1265-1274.   https://doi.org/10.5187/jast.2021.e122
  43. Du G, Prestwich GD. Protein structure encodes the ligand binding specificity in pheromone binding proteins. Biochemistry. 1995;34(27):8726-8732.   https://doi.org/10.1021/bi00027a023
  44. Senger PL. The estrus detection problem: new concepts, technologies, and possibilities. J Dairy Sci. 1994;77(9):2745-2753.   https://doi.org/10.3168/jds.s0022-0302(94)77217-9
  45. Shin DH, Lee HJ, Cho S, Kim HJ, Hwang JY, Lee CK, et al. Deleted copy number variation of Hanwoo and Holstein using next generation sequencing at the population level. BMC Genomics. 2014;15(1):240.