Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-26T05:19:04.609Z Has data issue: false hasContentIssue false

Histological and Ultrastructural Studies of the Unique Hemopoietic-Endocrine Organ of the Grass Carp, Ctenopharyngodon idella (Valenciennes, 1844)

Published online by Cambridge University Press:  13 October 2020

Doaa M. Mokhtar*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut 71526, Egypt
*
Author for correspondence: Doaa M. Mokhtar, E-mail: [email protected]
Get access

Abstract

Specific features of the immunohistochemical and ultrastructural organization of the hemopoietic head-kidney (HK) in adult Ctenopharyngodon idella (Valenciennes, 1844) were investigated using light and transmission electron microscopy. The HK of grass carp possessed all developmental stages of leucocytes and erythrocytes, as well as dendritic cells and epithelial reticular cells. The rodlet cells were expressed α-smooth muscle actin (SMA). In addition, macrophages were the most numerous cells in the HK, which aggregated into structures called melanomacrophage centers (MMCs). On contrary, the chromaffin and interrenal cells (ICs) were mixed and organized into large anastomosing cords, which lined the posterior cardinal veins of the HK, and associated with many blood capillaries. The ICs displayed the characteristic features of steroid-producing cells. Three types of chromaffin cells: adrenaline, noradrenaline, and small granule-containing cells were observed in the HK. Glial fibrillary acidic protein (GFAP)-positive sustentacular cells were marked among the chromaffin cells. Hemopoietic cells, immune cells, MMCs, rodlet cells, in addition to three types of chromaffin cells and one type of interrenal cells in the HK were correlated with the functional significance of the fish concerned.

Type
Micrographia
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Aziz, E-S, El-Sayed, AT, Abdu, SBS & Fouad, HF (2010). Chromaffin cells and interregnal tissue in the head kidney of the grouper, Epinephelus tauvina (Teleostei, Serranidae): A morphological (optical and ultrastructural) study. J Appl Ichthyol 26, 522527.CrossRefGoogle Scholar
Agius, C & Roberts, RJ (2003). Melano-macrophage centers and their role in fish pathology. J Fish Dis 26(9), 499509.CrossRefGoogle ScholarPubMed
Chakrabarti, P & Ghosh, SK (2014). Cyclical changes in interrenal and chromaffin cells in relation to testicular activity of olive barb, Puntius sarana (Hamilton). Arch Pol Fish 22, 151158.CrossRefGoogle Scholar
Dezfuli, B, Capuano, S & Manera, M (1998). A description of rodlet cells from the alimentary canal of Anguilla anguilla and their relationship with parasitic helminths. J Fish Biol 53, 10841095.Google Scholar
Dezfuli, BS, Simoni, E, Rossi, R & Manera, M (2000). Rodlet cells and other inflammatory cells of Phoxinus phoxinus infected with Raphidascaris acus (Nematoda). Dis Aquat Org 43, 6169.CrossRefGoogle ScholarPubMed
Díaz-Flores, L, Gutiérrez, R, Varela, H, Valladares, F, Alvarez-Argüelles, H & Borges, R (2008). Histogenesis and morphofunctional characteristics of chromaffin cells. Acta Physiol (Oxford) 192(2), 145163.CrossRefGoogle ScholarPubMed
Fijan, N (2002). Morphogenesis of blood cell lineages in channel catfish. J Fish Biol 60, 9991014.CrossRefGoogle Scholar
Finkenbine, SS, Gettys, TW & Burnett, G (1997). Direct effects of catecholamines on T and B cell lines of the channel catfish, Ictalurus punctatus. Develop Comparative Immunol 21, 155.CrossRefGoogle Scholar
Gaber, W & Abdel-maksoud, FM (2019). Interrenal tissue, chromaffin cells and corpuscles of Stannius of Nile tilapia (Oreochromis niloticus). Microscopy 68(3), 195206.CrossRefGoogle ScholarPubMed
Geven, EJW & Klaren, PHM (2017). The teleost head kidney: Integrating thyroid and immune signaling. Develop Comparative Immunol 66, 7383.CrossRefGoogle Scholar
Gfell, B, Kloas, W & Hanke, W (1997). Neuroendocrine effects on adrenal hormone secretion in carp (Cyprinus carpio). Gen Comp Endocrinol 116, 310319.CrossRefGoogle Scholar
Herraez, MP & Zapata, AG (1991). Structural characterization of the melanomacrophage centres (MMC) of goldfish Carassius auratus. European J Morphol 29, 89102.Google ScholarPubMed
Hsu, SM, Raine, L & Fanger, H (1981). Use of avidin-biotin-peroxidase complex (ABC) in immznoperoxidase techniques. J Histochem Cytochem 29, 577580.CrossRefGoogle ScholarPubMed
Iger, Y & Abraham, M (1997). Rodlet cells in the epidermis of fish exposed to stressors. Tissue Cell 29, 431438.CrossRefGoogle ScholarPubMed
Karnovsky, MJ (1965). A formaldehyde glutaraldehyde fixative of high osmolality for use in electron microscopy. Cell Biol 27, 137138.Google Scholar
Köllner, B, Blohm, U, Kotterba, G & Fischer, U (2001). A monoclonal antibody recognizing a surface marker on rainbow trout (Oncorhynchus mykiss) monocytes. Fish Shellfish Immunol 11, 127142.CrossRefGoogle ScholarPubMed
Köllner, B, Fischer, U, Rombout, JH, Taverne-Thiele, JJ & Hansen, JD (2004). Potential involvement of rainbow trout thrombocytes in immune functions: A study using a panel of monoclonal antibodies and RT-PCR. Develop Comparative Immunol 28, 10491062.CrossRefGoogle ScholarPubMed
Kum, C & Sekkin, S (2011). The Immune System Drugs in Fish: Immune Function, Immunoassay, Drugs. Recent Advances in Fish Farm, 1st ed. London, UK: Faruk Aral and Zafer, IntechOpen.Google Scholar
Lin, HT, Lin, HY & Yang, HL (2005). Histology and histochemical enzyme-staining patterns of major immune organs in Epinephelus malabaricus. J Fish Biology 66, 729740.CrossRefGoogle Scholar
Magro, G & Grasso, S (1997). Immunohistochemical identification and comparison of glial cell lineage in fetal, neonatal, adult and neoplastic human adrenal medulla. Histochem J 29(4), 293299.CrossRefGoogle ScholarPubMed
Meseguer, J, Esteban, MA & Agulleiro, B (1991). Stromal cells, macrophages and lymphoid cells in the head-kidney of sea bass (Dicentrarchus labrax L.). An ultrastructural study. Arch Histol Cytol 54, 299309.CrossRefGoogle ScholarPubMed
Meseguer, J, Esteban, MA, Garcia Ayala, A, Lopez Ruiz, A & Agulleiro, B (1990). Granulopoiesis in the head kidney of the sea bass Dicentrarchus labrax L. An ultrastructural study. Arch Histol Cytol 53, 287296.CrossRefGoogle ScholarPubMed
Meseguer, J, Lopez-Ruiz, A & Garcia-Ayala, A (1995). Reticulo-endothelial stroma of the head-kidney form the seawater teleost gilthead seabream (Sparus aurata L.): An ultrastructural and cytochemical study. Anat Rec 241, 303309.CrossRefGoogle Scholar
Mokhtar, DM (2019). Characterization of the fish ovarian stroma during the spawning season: Cytochemical, immunohistochemical and ultrastructural studies. Fish Shellfish Immunol 94, 566579.CrossRefGoogle ScholarPubMed
Mokhtar, DM (2020). Fish Histology From Cells to Organs. 2nd ed. Canada: Apple Academic Press.Google Scholar
Nandi, J (1962). The structure of the interrenal gland in teleost fishes. Univ Calif Publ Zool 65, 129212.Google Scholar
Petrie-Hanson, L & Ainsworth, AJ (2001). Ontogeny of channel catfish lymphoid organs. Vet Immunol Immunopathol 81, 113127.CrossRefGoogle ScholarPubMed
Press, CML & Evensen, O (1999). The morphology of the immune system in teleost fish. Fish Shellfish Immunol 9, 309318.CrossRefGoogle Scholar
Reynolds, ES (1963). Use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17, 208213.Google ScholarPubMed
Rideout, RM, Smith, SA & Morgan, MJ (2015). High-density aggregations of rodlet cells in the gonads of Greenland halibut Reinhardtius hippoglossoides, a deep-water marine flatfish. Fish Biol 86, 16301637.CrossRefGoogle ScholarPubMed
Rocha, RM, Santos, LS, Vicentini, CA & Da Cruz, C (2001). Structural and ultrastructural characteristics of interrenal gland and chromaffin cell of Matrinxã, Brycon cephalus Gunther 1869 (Teleostei-Characidae). Anat Histol Embryol 30, 351355.CrossRefGoogle ScholarPubMed
Rodriguez, H, Filippa, V, Mohamed, F, Dominquez, S & Scardapane, L (2007). Interaction between chromaffin and sustentacular cells in adrenal medulla of viscacha (Lagostomus maximus maximus). Anat Histol Embryol 36(3), 182185.CrossRefGoogle ScholarPubMed
Romano, N, Ceccariglia, S, Mastroliad, L & Mazzini, M (2002). Cytology of lymphomyeloid head kidney of antarctic fishes Trematomus bernacchii (Nototheniidae) and Chionodraco hamatus (Channicthyidae). Tissue Cell 34, 6372.CrossRefGoogle ScholarPubMed
Sampour, M (2008). The study of adrenal chromaffin of fish, Carassius auratus (Teleostei). Pak J Biol Sci 11, 10321036.CrossRefGoogle Scholar
Santos, AA, Gutierre, RC, Antoniazzi, MM, Ranzani-Paiva, MJT, Silva, MRR, Oshima, CTF & Egami, MI (2011). Morphocytochemical, immunohistochemical and ultrastructural characterization of the head kidney of fat snook Centropomus parallelus. J Fish Biol 79, 16851707.CrossRefGoogle ScholarPubMed
Secombes, CJ & Wang, T (2012). The innate and adaptive immune system of fish. In Infectious Disease in Aquaculture, Austin, B (Ed.), pp. 368. Sawston, UK: Woodhead Publishing.CrossRefGoogle Scholar
Weyts, FAA, Cohen, N, Flik, G & Kemenade, BML (1999). Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish Shellfish Immunol 9(1), 120.CrossRefGoogle Scholar
Zuasti, A & Ferrer, C (1989). Haematopoiesis in the head kidney of Sparus auratus. Arch Histol Cytol 52, 249255.CrossRefGoogle ScholarPubMed