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Architecture and Cellular Composition of the Spleen in the Japanese Quail (Coturnix japonica)

Published online by Cambridge University Press:  12 May 2020

Fatma El-Zahraa A. Mustafa*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut 71526, Egypt
Sara M.M. El-Desoky
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut 71526, Egypt
*
*Author for correspondence: Fatma El-Zahraa A. Mustafa, E-mail: f.histology@aun.edu.eg
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Abstract

The spleen is considered a key player in birds’ immunity. The stroma and the parenchyma of the spleen of the adult quail were demonstrated histologically, histochemically, and ultrastructurally. A thin capsule and the absence of trabeculae were the most characteristics of spleen stroma. The demarcation between white pulp and red pulp was not observed in the quail. White pulp formed from the periarterial lymphatic sheath and the periellipsoidal lymphatic sheath, both of which were surrounded by arteriole and ellipsoid, respectively. Ellipsoids appeared more numerous and were characterized by cuboidal lining of the epithelium and supporting cells. Red pulp consisted of sinuses and cords. White pulp and red pulp of the quail spleen contained various cells, such as red blood cells, macrophages, heterophils with characteristic granules, lymphocytes of different sizes, dendritic cells, plasma cells, and telocytes. In addition, closed circulation and open circulation established the blood flow on the spleen.

Type
Micrographia
Copyright
Copyright © Microscopy Society of America 2020

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References

Abd-Elhafeez, HH & Soliman, SA (2017). New description of telocyte sheaths in the bovine uterine tube: An immunohistochemical and scanning microscopic study. Cells Tissues Organs 203, 295315.CrossRefGoogle ScholarPubMed
Abd-Elkareem, M (2017). Cell-specific immuno-localization of progesterone receptor alpha in the rabbit ovary during pregnancy and after parturition. Anim Reprod Sci 180, 100120.CrossRefGoogle ScholarPubMed
Abdel-Maksoud, FM, Abd-Elhafeez, HH & Soliman, SA (2019). Morphological changes of telocytes in camel efferent ductules in response to seasonal variations during the reproductive cycle. Sci Rep 9, 117.CrossRefGoogle ScholarPubMed
Andreasen, CB, Latimer, KS, Harmon, BG, Glisson, JR, Golden, JM & Brown, J (1991). Heterophil function in healthy chickens and in chickens with experimentally induced staphylococcal tenosynovitis. Vet Pathol 28, 419427.CrossRefGoogle ScholarPubMed
Baishya, G & Bhattacharyya, R (2012). Gross and micro-anatomy of the spleen of adult indigenous fowl of Assam. Indian J Vet Anat 24, 8486.Google Scholar
Bancroft, JD, Layton, C & Suvarna, SK (2013). Bancroft's Theory and Practice of Histological Techniques, 7th ed.London: Churchill Livingstone.Google Scholar
Bao, HJ, Li, MY, Wang, J, Qin, JH, Xu, CS, Hei, NN, Yang, P, Gandahi, JA & Chen, QS (2009). Architecture of the blood-spleen barrier in the soft-shelled turtle, Pelodiseus sinensis. Anat Rec 292(8), 10791087.CrossRefGoogle ScholarPubMed
Bingöl, S, Gülmez, NY, Deprem, T, Taşci, SK & Aslan, Ş (2014). Histologic and histometric examination of spleen in geese (Anser anser). Atatürk Üniv Vet Bilim Derg 9, 157162.Google Scholar
Biro, E, Kocsis, K, Nagy, N, Molnar, D, Kabell, S, Palya, V & Olah, I (2011). Origin of the chicken splenic reticular cells influences the effect of the infectious bursal disease virus on the extracellular matrix. Avian Pathol 40, 199206.CrossRefGoogle ScholarPubMed
Bonadiman, SF, Stratievsky, GC, Machado, JA, Albernaz, AP, Rabelo, GR & DaMatta, RA (2009). Leukocyte ultrastructure, hematological and serum biochemical profiles of ostriches (Struthio camelus). Poult Sci 88, 22982306.CrossRefGoogle Scholar
Brendolan, A, Rosado, MM, Carsetti, R, Selleri, L & Dear, TN (2007). Development and function of the mammalian spleen. BIOEEJ 29, 166177.Google ScholarPubMed
Burke, JS & Simon, GT (1970). Electron Microscopy of the Spleen 1. Anatomy and Microcirculation. Am J Clin Pathol 58, 127155.Google ScholarPubMed
Caxton-Martins, AE & Daimon, T (1976). Histochemical observations on chicken blood and bone marrow cells. J Anat 122, 553.Google ScholarPubMed
Ceafalan, L, Gherghiceanu, M, Popescu, LM & Simionescu, O (2012). Telocytes in human skin-are they involved in skin regeneration? J Cell Mol Med 16, 14051420.CrossRefGoogle ScholarPubMed
Chang, Y, Li, C, Gan, L, Li, H & Guo, Z (2015). Telocytes in the spleen. PLoS One 10, e0138851.CrossRefGoogle ScholarPubMed
Chen, LT & Weiss, L (1973). The role of the sinus wall in the passage of erythrocytes through the spleen. Blood 41, 529537.CrossRefGoogle ScholarPubMed
Ciriaco, E, Píñera, PP, Díaz-Esnal, B & Laurà, R (2003). Age-related changes in the avian primary lymphoid organs (Thymus and Bursa of Fabricius). Microsc Res Techniq 62, 482487.CrossRefGoogle Scholar
Cismasiu, VB & Popescu, LM (2015). Telocytes transfer extracellular vesicles loaded with micro RNA s to stem cells. J Cell Mol Med 19, 351358.CrossRefGoogle ScholarPubMed
Claver, JA & Quaglia, AI (2009). Comparative morphology, development, and function of blood cells in non-mammalian vertebrates. J Exot Pet Med 18, 8797.CrossRefGoogle Scholar
Daimon, T & Caxton-Martins, A (1977). Electron microscopic and enzyme cytochemical studies on granules of mature chicken granular leucocytes. J Anat 123, 553.Google ScholarPubMed
Den Haan, JM, Mebius, R & Kraal, G (2012). Stromal cells of the mouse spleen. Front Immunol 3, 201.Google ScholarPubMed
El-Dawi, EFA (2008). Comparative studies on the structure of spleen in representatives of three vertebrate classes with special reference to certain immune cells. A contribution to the evolution of lymphatic organs. African J Biol Sci 2, 47–36.Google Scholar
El-Desoky, SM & Mustafa, FEZA (2019). Histological and histochemical studies on the oviduct microcirculation of the laying Japanese quail (Coturnix japonica). Anat Histol Embryol 48, 346357.CrossRefGoogle Scholar
Evans, EW, Beach, GG, Wunderlich, J & Harmon, BG (1994). Isolation of antimicrobial peptides from avian heterophils. J Leukoc Biol 56, 661665.CrossRefGoogle ScholarPubMed
Fox, AJ & Solomon, JB (1981). Chicken non-lymphoid leukocytes. In Avian Immunology: Proceedings of the 16th Poultry Science Symposium, September 25–27, 1980, Rose ME, Payne LN and Freeman BM (Eds.). Edinburgh: British Poultry Science Ltd.Google Scholar
Gallego, M, Del Cacho, E, Lopez-Bernad, F & Bascuas, JA (1997). Identification of avian dendritic cells in the spleen using a monoclonal antibody specific for chicken follicular dendritic cells. Anat Rec 249, 8185.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Gumati, MK, Magyar, A, Nagy, N, Kurucz, É, Felföldi, B & Oláh, I (2003). Extracellular matrix of different composition supports the various splenic compartments of guinea fowl (Numida meleagris). Cell Tissue Res 312, 333343.CrossRefGoogle Scholar
Hamza, RA (2017). Anatomical and histological changes in the spleen of post hatching indigenous chicken in Iraq. IJVS 41, 174178.Google Scholar
Hartwig, H & Hartwig, HG (1985). Structural characteristics of the mammalian spleen indicating storage and release of red blood cells. Aspects of evolutionary and environmental demands. Experientia 41, 159163.CrossRefGoogle ScholarPubMed
Hashimoto, Y & Sugimura, M (1977). Histological and quantitative studies on the postnatal growth of the duck spleen. Jpn J Vet Res 25, 7182.Google ScholarPubMed
Igyártó, BZ, Magyar, A & Oláh, I (2007). Origin of follicular dendritic cell in the chicken spleen. Cell Tissue Res 327, 8392.CrossRefGoogle ScholarPubMed
Jeurissen, SH (1993). The role of various compartments in the chicken spleen during an antigen-specific humoral response. Immunology 80, 29.Google ScholarPubMed
Jiang, XJ, Cretoiu, D, Shen, ZJ & Yang, XJ (2018). An in vitro investigation of telocytes-educated macrophages: Morphology, heterocellular junctions, apoptosis and invasion analysis. J Transl Med 16, 85.CrossRefGoogle Scholar
John, JL (1994). The avian spleen: A neglected organ. Q Rev Biol 69, 327351.CrossRefGoogle ScholarPubMed
Juul-Madsen, HR, Viertlboeck, B, Smith, AL & Göbel, TW (2008). Avian innate immune responses. In Avian Immunology (ed. F. Davison, B. Kaspers and K. A. Schat), pp. 129158. Amsterdam: Academic Press.CrossRefGoogle Scholar
Kannan, TA & Ramesh, G (2015). Light and electron microscopic details of blood-spleen barrier in nandanam chicken (Gallus domesticus). Int J Sci Res 4, 22032208.Google Scholar
Kannan, TA, Ramesh, G, Venkatesan, S, Ushakumari, S & Basha, SH (2015). Cytoarchitecture of periarterial lymphatic sheath (PALS) in chicken spleen–light and transmission electronmicroscopic study. Int J Adv Res 3, 11671172.Google Scholar
Karnovsky, MJ (1965). A formaldehyde-glutraldehyde fixative of high osmolarity for use in electron microscopy. Cell Biol 27, 137A.Google Scholar
Kasai, K, Nakayama, A, Ohbayashi, M, Nakagawa, A, Ito, M, Saga, S & Asai, J (1995). Immunohistochemical characteristics of chicken spleen ellipsoids using newly established monoclonal antibodies. Cell Tissue Res 281, 135141.CrossRefGoogle ScholarPubMed
Kita, K (2014). The spleen accumulates advanced glycation end products in the chicken: Tissue comparison with rat. Poult Sci 93, 429433.CrossRefGoogle ScholarPubMed
Kogut, MH, Iqbal, M, He, H, Philbin, V, Kaiser, P & Smith, A (2005). Expression and function of toll-like receptors in chicken heterophils. Dev Comp Immunol 29, 791–780.CrossRefGoogle ScholarPubMed
Liman, N & Bayram, GK (2011). Structure of the quail (Coturnix coturnix japonica) spleen during pre-and post-hatching periods. Revue Méd Vét 162, 2533.Google Scholar
Lucas, AM & Jamroz, C (1961). Atlas of Avian Hematology. Agriculture Monograph 25. Washington, DC: United States Department of Agriculture.Google Scholar
Mast, J & Goddeeris, BM (1997). CD57, a marker for B-cell activation and splenic ellipsoid-associated reticular cells of the chicken. Cell Tissue Res 291, 107115.CrossRefGoogle Scholar
Maxwell, MH (1987). The avian eosinophil—a review. World Poultry Sci J 43, 190207.CrossRefGoogle Scholar
Maxwell, MH & Robertson, GW (1998). The avian heterophil leucocyte: A review. World Poultry Sci J 54, 155178.CrossRefGoogle Scholar
Mebius, RE & Kraal, G (2005). Structure and function of the spleen. Nat Rev Immunol 5, 606616.CrossRefGoogle ScholarPubMed
Mohd, KI, Mrigesh, M, Singh, B & Singh, I (2016). Ultrastructural study on the granulocytes of Uttara fowl (Gallus domesticus). Vet World 9, 320.CrossRefGoogle Scholar
Mokhtar, DM (2018). Cellular and stromal elements organization in the liver of grass carp, Ctenopharyngodon idella (Cypriniformes: Cyprinidae). Micron 112, 114.CrossRefGoogle Scholar
Nagy, N, Bíró, É, Takács, Á, Pólos, M, Magyar, A & Oláh, I (2005). Peripheral blood fibrocytes contribute to the formation of the avian spleen. Dev Dynam 232, 5566.CrossRefGoogle ScholarPubMed
Nasu, T, Shimizu, K & Nakai, M (1992). Morphological study of the dove spleen. Poult Sci 71, 15271530.CrossRefGoogle ScholarPubMed
Oláh, I & Glick, B (1982). Splenic white pulp and associated vascular channels in chicken spleen. Am J Anat 165, 445480.CrossRefGoogle ScholarPubMed
Olah, I, Glick, B & Taylor, RL Jr. (1985). Effect of surgical bursectomy on the ellipsoid, ellipsoid-associated cells, and periellipsoid region of the chicken's spleen. J Leukocyte Biol 38, 459469.CrossRefGoogle ScholarPubMed
Pharr, T, Olah, I, Bricker, J, Olson, WC, Ewert, D, Marsh, J & Glick, B (1995). Characterization of a novel monoclonal antibody, EIV-E12, raised against enriched splenic ellipsoid-associated cells. Hybridoma 14, 5157.CrossRefGoogle ScholarPubMed
Polák, Š, Gálfiová, P & Varga, I (2009). Ultrastructure of human spleen in transmission and scanning electron microscope. Biologia 64, 402408.CrossRefGoogle Scholar
Popescu, LM, Gherghiceanu, M, Suciu, LC, Manole, CG & Hinescu, ME (2011). Telocytes and putative stem cells in the lungs: Electron microscopy, electron tomography and laser scanning microscopy. Cell Tissue Res 345, 391.CrossRefGoogle ScholarPubMed
Reynolds, ES (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17, 208212.CrossRefGoogle ScholarPubMed
Roitt, I, Brostoff, J & Male, D (1989). Immunology, 2nd ed.London, New York: Churchill Livingstone, Gower Medical Publishing.Google Scholar
Salakij, C, Kasorndorkbua, C, Salakij, J, Suwannasaeng, P & Jakthong, P (2015). Quantitative and qualitative morphologic, cytochemical and ultrastructural characteristics of blood cells in the Crested Serpent eagle and Shikra. Jpn J Vet Res 63, 95105.Google ScholarPubMed
Simon, GT & Burke, JS (1970). Electron microscopy of the spleen III. Erythro-leukophagocytosis. Am J Clin Pathol 58, 451469.Google Scholar
Soliman, SA, Ahmed, YA & Abdelsabour-Khalaf, M (2016). Histogenesis of the stomach of the pre-hatching quail: A light microscopic study. Anat Sci Int 91, 407418.CrossRefGoogle ScholarPubMed
Soliman, SA, Kamal, BM & Abd-Elhafeez, HH (2019). Cellular invasion and matrix degradation, a different type of matrix-degrading cells in the cartilage of catfish (Clarias gariepinus) and Japanese quail embryos (Coturnix coturnix japonica). Microsc Microanal 25, 12831292.CrossRefGoogle Scholar
Song, H, Peng, KM, Li, SH, Wang, Y, Wei, L & Tang, L (2012). Morphological characterization of the immune organs in ostrich chicks. Turk J Vet Anim Sci 36, 89100.Google Scholar
Spazier, E, Storch, V & Braunbeck, T (1992). Cytopathology of spleen in eel Anguilla anguilla exposed to a chemical spill in the Rhine River. Dis Aquat Organ 14, 122.CrossRefGoogle Scholar
Tanaka, Y (1990). “Intermediate zone” of mammalian spleens: Light and electron microscopic study of three primitive mammalian species (platypus, shrew, and mole) with special reference to intrasplenic arteriovenous communication. Am J Anat 187, 313337.CrossRefGoogle ScholarPubMed
Verma, VK, Yadav, SK & Haldar, C (2017). Influence of environmental factors on avian immunity: An overview. J Immun Res 4, 1028.Google Scholar
Wols, HAM (2005). Plasma cells. Encyclopedia of Life Sciences, pp. 1–8. John Wiley & Sons, Ltd.Google Scholar
Yadav, GC (2011). Light and ultrastructural studies on the blood cells of Kadaknath fowl. MVSc, Doctoral Dissertation, Thesis, GBPUAT, Pantnagar.Google Scholar
Yousef, MS, Abd-Elhafeez, HH, Talukder, AK & Miyamoto, A (2019). Ovulatory follicular fluid induces sperm phagocytosis by neutrophils, but oviductal fluid around oestrus suppresses its inflammatory effect in the buffalo oviduct in vitro. Mol Reprod Dev 86, 835846.CrossRefGoogle ScholarPubMed
Zhang, Q, Chen, B, Yang, P, Zhang, L, Liu, Y, Ullah, S, Wu, L, Waqas, Y, Le, Y, Chen, W & Chen, Q (2015). Identification and structural composition of the blood–spleen barrier in chickens. Vet J 204, 110116.CrossRefGoogle ScholarPubMed
Zhang, Q, Ullah, S, Liu, Y, Yang, P, Chen, B, Waqas, Y, Waqas, Y, Bao, H, Hu, L, Li, Q & Chen, Q (2016). Lymphocyte migration in the micro-channel of splenic sheathed capillaries in Chinese soft-shelled turtles, Pelodiscus sinensis. Micron 80, 6672.CrossRefGoogle ScholarPubMed
Zhang, Q, Waqas, Y, Yang, P, Sun, X, Liu, Y, Ahmed, N, Chen, B, Li, Q, Hu, L, Huang, Y, Chen, H, Hu, B & Chen, Q (2017). Cytological study on the regulation of lymphocyte homing in the chicken spleen during LPS stimulation. Oncotarget 8, 7405.CrossRefGoogle Scholar