Original Scientific Article
Morphometric and histochemical features of the Harderian gland in rabbits with different types of autonomous regulation
Аndrii Tybinka
*
,
Marta Zakrevska
,
Olga Shchebentovska
Received: 28 January 2022
Received in revised form: 11 May 2022
Accepted: 05 August 2022
Available Online First: 31 August 2022
Published on: 15 October 2022
Correspondence: Аndrii Tybinka, a.m.tybinka@gmail.com
Abstract
The tonus of autonomous centers reflected in the morpho-functional features of the organs in mammals. The study aimed to establish the influence of the autonomous regulation and its’ typological peculiarities on the structural features of the rabbits’ Harderian gland. Clinically healthy male rabbits, four months old, weighing 3.6-3.9 kg, were selected for the research. Based on the study of heart rate variability, three types of autonomous regulation were outlined, according to which three groups of rabbits were formed: ST rabbits (sympathetic dominant regulation), PS rabbits (parasympathetic dominant regulation), and NT rabbits (combined sympathetic and parasympathetic regulation). After euthanasia, the Harderian gland was dissected in all animals. Histological specimens were prepared and a morphometric examination was performed. ST rabbits corresponded to the minimal indicators in the tubular alveoli in both parts of the gland, as well as the maximum indicators of capsule thickness. NT rabbits corresponded to the maximum values of the acini area in the pink lobe, and in the white lobe - the maximal values of the cross-sectional area of the tubular alveoli, its wall area, and the epithelium height. The maximum acini area corresponded to PS rabbits in the white lobe, and in the pink lobe - the maximum indicators of the tubular alveoli cross-sectional area, and epithelial height. The pink and white lobes’ structure of the rabbit’s Harderian gland was affected by the combined tonus of the sympathetic and parasympathetic centers. The findings elucidate the regulatory and trophic effects on the Harderian gland in rabbits.
Keywords: Harderian gland, rabbits, tubular alveoli, morphometry, autonomous regulation
References
- Dunn, D.G., Baker, J., Sorden, S.D. (2018). Eye and associated glands. In A.W. Suttie (Ed.) Boorman’s Pathology of the Rat. (Second Edition). Reference and Atlas (pp. 251-278). Academic Press https://doi.org/10.1016/B978-0-12-391448-4.00016-2 PMCid:PMC7148627
- Santillo, A., Chieffi Baccari, G., Minucci, S., Falvo, S., Venditti, M., Di Matteo, L. (2020). The Harderian gland: endocrine function and hormonal control. Gen Comp Endocrinol. 297, 113548. https://doi.org/10.1016/j.ygcen.2020.113548 PMid:32679156
- Bejdic, P., Avdic, R., Amidzic, L., Cutahija, V., Tandir, F., Hadziomerovic, N. (2014). Developmental changes of lymphoid tissue in the harderian gland of laying hens. Mac Vet Rev. 37(1): 83-88. https://doi.org/10.14432/j.macvetrev.2014.02.009
- Deist, M.S., Lamont, S.J. (2018). What makes the Harderian gland transcriptome different from other chicken immune tissues? A gene expression comparative analysis. Front Physiol. 9, 492. https://doi.org/10.3389/fphys.2018.00492 PMid:29867543 PMCid:PMC5952037
- Khayoon, E.S., Reshag, A.F., Almayahi, M.S., Al-Saffar, F.J. (2019). Age related changes in the cellular population and lymphoid tissue in the harderian gland of turkey. EAJBS 11(2): 23-32. https://doi.org/10.21608/eajbsd.2019.56517
- Hanniche, N., Saadi-Brenkia, O., Maciejewski-Duval, A., Lounis, S., Bougrid, A., Bendjelloul, M. (2019). Structural study and expression of the androgen receptors during the reproductive cycle in the harderian gland of the male Meriones libycus. C R Biol. 342(1-2): 27-34. https://doi.org/10.1016/j.crvi.2018.11.002 PMid:30792115
- Rodriguez, C., Kotler, M., Antolin, I., Sainz, R.M., Menendez-Pelaez, A. (1996). Regulation of the aminolevulinate synthase gene in the Syrian hamster Harderian gland: changes during development and circadian rhythm and role of some hormones. Microsc Res Tech. 34(1): 65-70. https://doi.org/10.1002/(SICI)1097-0029(19960501) 34:1<65::AID-JEMT9>3.0.CO;2-V
- EL-Leithy, E., El-Sakhawy, M.A., Al-Sabaa, A., El-Habak, H., Shaheen, Y. (2015). Seasonal immunohistochemical expression of androgen receptor (AR) in the harderian gland (HG) of male rabbit. IJAR. 3(8): 479-489.
- Tatsuo, S. (1992). Comparative anatomy of mammalian Harderian glands. In S.M. Webb, R.A. Hoffman, M.L. Puig-Domingo, R.J. Reiter (Eds.), Harderian glands: porphyrin metabolism, behavioral, and endocrine effects (pp. 7-23). Berlin: Springer Verlag https://doi.org/10.1007/978-3-642-76685-5_2
- Hittmair, K.M., Tichy, A., Nell, B. (2014). Ultrasonography of the Harderian gland in the rabbit, guinea pig, and chinchilla. Vet Ophthalmol. 17(3): 175-183. https://doi.org/10.1111/vop.12063 PMid:23738702 PMCid:PMC7169276
- Eltony, S.A.M. (2009). A comparative study of the Harderian gland in the female rat and female rabbit (a histological, histochemical, scanning electron microscopic and morphometric study). Egypt J Histol. 32(1): 46-65.
- Elgayar, S.A.M., Abou-Elghait, A.T., Sayed, A.A. (2015). Morphology of female guinea pig Harderian gland during postnatal development – secretory endpieces. Eur J Anat. 19(1): 15-26.
- Lopez, J.M., Carbajo-Perez, E., Fernandez-Suarez, A., Alvarez-Uria, M. (1996). Postnatal development of cell types in the hamster harderian gland. Microsc Res Tech. 34(1): 48-54. https://doi.org/10.1002/(SICI)1097-0029(19960501) 34:1<48::AID-JEMT7>3.0.CO;2-S
- Bayraktaroglu, A.G., Ergun, E. (2010). Histomorphology of the Harderian gland in the Angora rabbit. Anat Histol Embryol. 39(6): 494-502. https://doi.org/10.1111/j.1439-0264.2010.01020.x PMid:20624156
- Shirama, K., Ozawa, S., Seyama, Y., Kobayashi, M., Sawamura, S., Yamada, J. (1997). Postnatal development of the harderian gland in the rabbit: light and electron microscopic observations. Microsc Res Tech. 37(5-6): 572-582. https://doi.org/10.1002/(SICI)1097-0029(19970601) 37:5/6<572::AID-JEMT17>3.0.CO;2-N
- Butler, J.M., Ruskell, G.L., Cole, D.F., Unger, W.G., Zhang, S.Q., Blank, M.A., McGregor, G.P., Bloom, S.R. (1984). Effects of VIIth (facial) nerve degeneration on vasoactive intestinal polypeptide and substance P levels in ocular and orbital tissues of the rabbit. Exp Eye Res. 39(4): 523-532. https://doi.org/10.1016/0014-4835(84)90052-6
- Pangerl, A., Pangerl, B., Buzzell, G.R., Jones, D.J., Reiter, R.J. (1989). Characterization of β-adrenoceptors in the syrian hamster harderian gland: Sexual differences and effects of either castration of superior cervical ganglionectomy. J Neurosci Res. 22(4): 456-460. https://doi.org/10.1002/jnr.490220411 PMid:2547980
- Zakrevska, M.V., Tybinka, A.M. (2019). Peculiarities of microstructure of the suprarenal glands of rabbits with different types of autonomic tone. Regul Mech Biosyst. 10(4): 415-421. https://doi.org/10.15421/021962
- Shaffer, F., Ginsberg, J.P. (2017). An overview of heart rate variability metrics and norms. Front Public Health 5, 258. https://doi.org/10.3389/fpubh.2017.00258 PMid:29034226 PMCid:PMC5624990
- Baevsky, R.М., Chernikova, A.G. (2017). Heart rate variability analysis: physiological foundations and main methods. Cardiometry 10, 66-76. https://doi.org/10.12710/cardiometry.2017.10.6676
- Directive 2010/63/EU of the European parliament and of the council of 22 September 2010 on the protection of animals used for scientific purposes (Text with EEA relevance), Official Journal of the European Union, L 276, 33-79.
- Mulisch, M., Welsch, U. (2015). Romeis - Microscopic Technique. Berlin: Springer Spektrum [In German] https://doi.org/10.1007/978-3-642-55190-1
- Pearse, A.G.E. (1960). Histochemistry, theoretical and applied (ed. 2). Boston: Little, Brown & Company
- Di Matteo, L., Baccari, G.C., Minucci, S. (1995). Effect of cholinergic secretagogue substances on the morphology of the harderian gland in the frog, Rana esculenta. Comp Biochem Physiol A Physiol. 112(1): 29-34. https://doi.org/10.1016/0300-9629(95)00095-O
- Coto-Montes, A., García-Macía, M., Caballero, B., Sierra, V., Rodríguez-Colunga, M.J., Reiter, R.J., Vega-Naredo, I. (2013). Analysis of constant tissue remodeling in Syrian hamster Harderian gland: intra-tubular and inter-tubular syncytial masses. J Anat. 222(5): 558-569. https://doi.org/10.1111/joa.12040 PMid:23496762 PMCid:PMC3633345
- Hussein, O.A., Elgamal, D.A., Elgayar, S.A.M. (2015). Structure of the secretory cells of male and female adult guinea pigs Harderian gland. Tissue Cell 47(3): 323-335. https://doi.org/10.1016/j.tice.2015.04.006 PMid:25960413
- Chieffi, G., Baccari, G.C., Di Matteo, L., d’Istria, M., Minucci, S., Varriale, B. (1996). Cell biology of the Harderian gland. Int Rev Cytol 168, 1-80. https://doi.org/10.1016/S0074-7696(08)60882-7
- Pradidarcheep, W., Asavapongpatana, S., Mingsakul, T., Poonkhum R., Nilbu-nga, S., Somana, R. (2003). Microscopic anatomy of the orbital harderian gland in the common tree shrew (Tupaia glis). J Morphol. 255(3): 328-336. https://doi.org/10.1002/jmor.10066 PMid:12520550
- Saadi-Brenkia, O., Haniche, N., Bendjelloul, M. (2013). Light and electron microscopic studies of the Gerbillus tarabuli (Thomas, 1902) Harderian gland. Zoolog Sci. 30(1): 53-59. https://doi.org/10.2108/zsj.30.53 PMid:23317366
- Rehorek, S.J., Hillenius, W.J., Sanjur, J., Chapman, N.G. (2007). One gland, two lobes: organogenesis of the “Harderian” and “nictitans” glands of the Chinese muntjac (Muntiacus reevesi) and fallow deer (Dama dama). Ann Anat. 189(5): 434-446. https://doi.org/10.1016/j.aanat.2006.10.007 PMid:17910397
- Maini, S., Hartley, C. (2019). Guide to ophthalmology in rabbits. In Practice. 41(7): 310-320. https://doi.org/10.1136/inp.l4775
- Kleckowska-Nawrot, J., Nowaczyk, R Gozdziewska-Harfajczuk, K., Szara, T., Olbrych, K. (2015). Histology, histochemistry and fine structure of the Harderian gland, lacrimal gland and superficial gland of the third eyelid of the European bison, Bison bonasus bonasus (Artiodactyla: Bovidae). oologia 32(5): 380-394. https://doi.org/10.1590/S1984-46702015000500007
- Kleckowska-Nawrot, J., Gozdziewska-Harłajczuk, K., Barszcz, K., Kowalczyk, A. (2015). Morphological studies on the harderian gland in the ostrich (Struthio camelus domesticus) on the embryonic and post-natal period. Anat Histol Embryol. 44(2): 146-156. https://doi.org/10.1111/ahe.12124 PMid:24995381
- Rajathi, S. Ramesh, G., Raja, K., Kannan, T.A, Sriram, P., Hemalatha, S. (2019). Microscopic anatomy of Harderian gland in goats. JEZS 7(1): 1413-1418.
- Djeridane, Y. (1996). Comparative histological and ultrastructural studies of the Harderian gland of rodents. Microsc Res Tech. 34(1): 28-38. https://doi.org/10.1002/(SICI)1097-0029(19960501) 34:1<28::AID-JEMT5>3.0.CO;2-S
- Marcos, H.J.A., Affanni, J.M. (2005). Anatomy, histology, histochemistry and fine structure of the Harderian gland in the South American armadillo Chaetophractus villosus (Xenarthra, Mammalia). Anat Embryol. 209, 409-424. https://doi.org/10.1007/s00429-005-0457-y PMid:15883851
- Kozlu, T., Bozkurt, Y.A., Altunay, H., Sari, E.K. (2010). Histological and histochemical studies on the Harderian gland of the osprey (Pandion haliaetus). J Anim Vet Adv. 9(13): 1875-1879. https://doi.org/10.3923/javaa.2010.1875.1879
- Beheiry, R.R., Ali, S.A., Aref, M., Emam H. (2020). Harderian gland of flying and non-flying birds: morphological, histological, and histochemical studies. JOBAZ 81, 35. https://doi.org/10.1186/s41936-020-00175-x
- Chieffi, G., Chieffi Baccari, G., Di Matteo, L., d’Istria, M., Minucci, S., Varriale, B. (1996). Cell biology of the harderian gland. Int Rev Cytol. 168, 1-80. https://doi.org/10.1016/S0074-7696(08)60882-7
- Coto-Montes, A., Tomás-Zapico, C., Escames, G., León, J., Tolivia, D., JosefaRodríguez-Colunga, M., Acuña-Castroviejo, D. (2003). Characterization of melatonin high-affinity binding sites in purified cell nuclei of the hamster (Mesocricetus auratus) Harderian gland. JPR 34(3): 202-207. https://doi.org/10.1034/j.1600-079X.2003.00029.x PMid:12614480
- Garcia-Macia, M., Rubio-Gonzalez, A., de Luxán-Delgado, B., Potes, Y., Rodríguez-González, S., de Gonzalo-Calvo, D., Boga, J.A., Coto-Montes, A. (2014). Autophagic and proteolytic processes in the Harderian gland are modulated during the estrous cycle. Histochem Cell Biol. 141(5): 519-529. https://doi.org/10.1007/s00418-013-1170-1
- Monteforte, R., Santillo, A., Lanni, A., D’Aniello, S., Chieffi Baccari, G. (2008). Morphological and biochemical changes in the Harderian gland of hypothyroid rats. J Exp Biol. 211(4): 606-612. https://doi.org/10.1242/jeb.015115 PMid:18245638
Copyright
© 2022 Tybinka A. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Conflict of Interest Statement
The authors have declared that no competing interests exist.
Citation Information
Macedonian Veterinary Review. Volume 45, Issue 2, Pages 157-168, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2022-0024, 2022