Ontogeny of hemopoietic and immune organs in the Chinese soft2shelled turtle ( Trionyx sinensis) 3
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1 49 (2) : , 2003 A cta Zoologica S inica 3 (, ),,,, ( ),,,,,, [ 49 (2) : , 2003 ] Ontogeny of hemopoietic and immune organs in the Chinese soft2shelled turtle ( Trionyx sinensis) 3 GUO Qiong2Lin J IA Wei2Zhang ( Instit ute of Hydrobiology, Chi nese Academy of Science, W uhan , Chi na) Abstract The ontogeny of hemopoietic and immune organs in the Chinese soft2shelled turtle, T rionyx sinensis, was studied and the morphological characteristics of two to three embryos from each embryonic stage described with histological examination. The first hemopoietic organ in embryos was the yolk sac. Later in development, hemopoietic stem cells in the yolk sac migrate via blood vessels and yolk sac hemopoietic activity is succeeded by development of the fetal thymus, liver, spleen and bone marrow (possibly kidney). Hemopoiesis was detected in the yolk sac at stage 6 after incubation. Hemopoietic stem cells were small, with an oval nucleus surrounded by a thin rim of basophilic cytoplasm. In addition, different developmental stages of erythrocytes were observed. The primordial thymus appeared at stage 14 as a detectable thickening of the posterioventral wall of the pharyngeal pouch. The dorsal portion of the thickening gave rise to the thymic primordium, whereas the ventral part became the parathyroid rudiment. By stage 16, the thymus rudiments were more defined, were closely situated near the internal jugular vein in which there were a large number of stem2like cells and appeared as a condensation of epithelial cells surrounded by mesenchyme. By stage 19, the thymus lobes were distinctly encapsulated and contained numerous small basophilic cells as well as lymphocytes among the epithelial cells. Until stage 25, complete demarcation of cortex and medulla was apparent. During the course of embryonic development, the thymus and parathyroid rudiments migrated ventrocaudally. The parathyroid glands were surrounded by thymus tissue because the thymus didnπt enter into the chest cavity. The thymus is the first lymphoid organ in embryonic development. Within the thymus, stem cells from the yolk sac differentiate into small lymphocytes which subsequently migrate to the spleen. The histogenesis of the spleen commenced with a thickening of the dorsal mesogastrium. By stage 15-16, the splenic rudi2 ment had budded into the body cavity ; later, blood sinuses developed as separate cavities in the mesenchyme. In the ves2 sels of the dorsal mesogastrium between the liver and kidney there were many hemopoietic stem cells, and near mesogastri , (No ) [ This research was funded by National Natural Science Foun2 dation of China and Institute Directorπs Priority Programmes of Chinese Academy Sciences],, 45,, : ν 2003 Acta Zoologica Sinica
2 2 : 239 um there were a lot of acidophilic cells. At stage 21-23, erythroblastic islands, a lot of acidophilic cells and a few granu2 locytes were seen in the spleen, and by stage 24, lymphopoiesis began. Until stage 25, white pulp and red pulp were clearly discernable. No splenic corpuscle was found in any developmental stage. In the embryonic liver, the hemopoietic stem cells were observed in the vitelline vein and other blood vessels near the liver diverticulum and also in the hepatic si2 nusoids of peripheral parts of the hepatic diverticulum. There were also some erythrocytes of different developmental stages and some acidophilic cells. Acidophilic cells and head kidney2like tissue were found during the development of the embry2 onic kidney. Hemopoiesis in bone marrow was observed until the end of embryonic development [ Acta Zoologica Sinica 49 (2) : , 2003 ]. Key words Chinese soft2shelled turtle ( T rionyx sinensis ), Immune organ, Ontogeny, Comparative immunology, Parathyroid gland ) 70 % ( 1 % ) 24, h, (Le Douarin et al., 1984 ; Romano et al., 1999 ; Kanakambika et al., 1973 ; Pitchappan et al., 1977 ; El Deeb et al., 1985, 1990 ; J urd, 1994 ;, 1995) El Deeb et al. (1990), 3 ( ) :,,, 6 ( 36 h) :,,,,, ; 10 ( 3 d) : 11 ( 4 d) :,, 13 :, ( Chalci des ocella2 16 : C, t us) ( Calotes versicolor) ( T rionyx sinensis Viegmann) ( ) ( ), 18 : ( ) ( ),,,, 19 :, 5 ( ) 4 ( ) ( ) ; 17 :, 20 :, 21 :, 22 :,, 23 :, ( ) 24 :, (1984) 2 3 Bouin 25 :,, 27 : m, H1E (
3 :, ; 212,,, 6, 26,, (: 9),,,, ;, ;, ;, (: 10) 15 16,,, (: 11),, (: 1, 2) (:, 12), (: 3),, ; 14, 3,, (: (: 4) 14 15, 13, 14) 19 20,, ;,,,,, 21 23,, (: 15) 16, (: 16),,, (: 3), 24, (:, 5) 17,,, 25,,, (, ), ( ) (: 6 ; : 7), 13, 19,, ( ),, ;,,, ;,, ( 14 15, ),,,,,,,, 16, 22 (: 8), 25 27, 22, (: 1, 2),
4 2 : 241 (: 1, 2 ; : 17),,, ( Xenopus,, laevis) ( ) (: 17) ( Kau et al., 1983 ; Maeno et al.,, 1985) ; ( Turpen et al., 1976 ; El Deeb et al., 1985),, (: 11) 20, ( ),,,,,, 25, (: 18) 27 Pitchappan et al. (1977) 28,,, ( ) 29, ( ) 14,,, (Bockman, 1970), 4 5, 3 ( Cooper, 1982 ; Bockman, 1970), Cooper, Bockman ( A nguis f ragilis) 3 2 : 3 ( Hightower et al., ; 1971 ; El Deeb et al., 1985, 1990) El Deeb et al1 (1985), (Undifferentiated blast), (, 1999) 3, ( El Deeb et al., 1985) ( L acerta vi ridis) ( L ac2 erta agil us),,, m, ( El Deeb,,, 1990), Jordan et al. ( Hemoblast),,,,, ( ),, (, 1999),,
5 ,,,, (Le Douarin, 1984) El Deeb et al. (1985), (, 1998) 35, Kanakambika et al. (1973) 35 ( Pitchappan et al., 1977) 36, 35 ( 38 El Deeb et al. (1985) ), 27, ; ( ) ,,,,, ( El Deeb et,, al., ) ( ),, 21 22,,?,,, ( Romano et al., 1999 ; El Deeb et al., 1985, 1990 ; Le Douarin et al., 1984) Turpen et al ; ( Kanakambika et al., 1973 ; Pitchappan et al., 1977 ; El Deeb et al., 1985) ( El Deeb et al., 1985),, (Le Douarin et al., 1984), 15 16,,,, : ; 21,, (An2, 24, drews et al., 1978 ; Lassila, 1981 ; El Deeb et, al., 1985, 1990), B, ( Kanakambika et al., 1973 ;, (1977), El Deeb et al., 1985) 40,, 38 ( Turpen, 1977 ; Romano et al.,
6 2 : ), ( El Deeb et al., 1985), Press., Sauria, Scincidae). J ,, ( El Deeb et al., 1985, 1990), 11 : (Urodeles) ( Ellis, 1977 ; Hightower et al., 1971 ; Goldstine et al., 1975) ol. Si n. 22 (Suppl) : [ 1998, ( Hor2. 22 ( ) : ton, 1971), ],, : Cooper et al. (1980),, :, (4) : [, 70. ] ( ),,, ( References) Andrews, T. A and J. J. T. Owen 1978 Studies on the earliest site of B cell differentiation in the mouse embryo. Dev. Comp. Im2 m unol. 2 : Bockman, D. E The thymus. In : Gans, C. and T. S. Par2 son ed. Biology of the Reptilia. London : Academic Press, Cooper, E. L General Immunology. New York : Pergamon Cooper, E. L., A. E. Klempau, J. A. Ramirez and A. G. Zapata 1980 Sources of stem cells in evolution. In : Horton, J. D. ed. Development and Differentiation of Vertebrate Lymphocytes. Ams2 terdam : Elsevier, El Deeb, S., S. Zada and R. El Ridi 1985 Ontogeny of hemopoietic and lymphopoietic tissues in the lizard, Chacides ocellatus (Reptilia, Morphol. 185 : El Deeb, S and A2H. Saad 1990 Ontogeny muturation of the im2 mune system in reptiles. Dev. Com p. Im m unol. 14 : Ellis, A. E The leucocytes of fish : a review. J. Fish Biol. Goldstine, S. N., V. Manickavel and N. Cohen 1975 Phylogeny of gut2associated lymphoid tissue. A m. Zool. 15 : Guo, Q. L The microstructure, ultrastructure and the func2 tional significance of the spleen in Trionyx sinensis. Acta Hydrobi2 Guo, Q. L The microstructure, ultrastructure of thymus in Trionyx sinensis and its significance in evolution. Acta Zoologica Si nica 45 (2) : [ (2) : ] Hightower, J. A and S. T. Pierre 1971 Hemopoietic tissue in the adult newt, Notopthalam us viridescens. J. Morphol. 135 : Horton, J. D Ontogeny of the immune system in amphibians. A m. Zool. 11 : Hou, L Studies on the embryonic development of the turtle, Trionyx sinensis. Acta sci. Nat. U niv. Norm. Hunan ( Trionyx si nensis). ( ) 3 (4) : 59 J urd, R. D Reptile and birds. In : Turner, R. J. ed. Im2 munology: A Comparative Approach. England : John Wiley & Sons ltd, Kanakambika, P. and V. R. Muthukkaruppan 1973 Lymphoid differentiation and organization of the spleen in the lizard Calotes versicolor. Proc. Indian Acad. Sci. 78 : Kau, C. L. and J. B. Turpen 1983 Dual contribution of embryonic ventral blood island dorsal central plate mesoderm during ontogeny of hemopoietic cells in Xenopus laevis. J. Im m unol. 131 : Lassila, O Embryonic differentiation of lymphoid stem cell : a
7 review. Dev. Com p. I m m unol. 5 : Le Douarin, N., F. Dieterlen2Lievre and P. D. Oliver 1984 On2 togeny of primary lymphoid organs and lymphoid stem cells. A m. J. A nat. 170 : Maeno, M., S. Tochinai and C. Katagiri 1985 Differential partici2 pation of ventral and dorsolateral mesoderm in the hemopoiesis of Xenopus, as revealed in dipioid2triploid or interspecific chimeras. Dev. Biol. 110 : Pitchappan, R. M. and V. R. Muthukkaruppan 1977 Analysis of the development of the lizard, Calotes versicolor. of the thymus. Dev. Com p. I m m unol. 1 : Histogenesis Romano, N., J. J. Taverne2Thiele, M. Fanelli, M. R. Baldassini, L. Abelli, L. Mastrolia, W. B. Van Muiswinkel and J. H. M. W. Rombout 1999 Ontogeny of the thymus in a teleost fish, Cyprinus carpio L. : developing thymocytes in the epithelial mi2 croenvironment. Dev. Com p. Im m unol. 23 : Turpen, J. B., L. Claire and K. L. Carpenter 1977 Lymphoid differentiation in the liver of larval Rana pipens. In : Solomon, J. B. and J. D. Horton ed. Developmental Immunobiology. Amater2 dam : Elsevier, Turpen, J. B and N. Cohen 1976 Localization of thymocytes stem cell precursors in the pharyngeal endoderm of early amphibian em2 bryos. Cell Im m unol. 24 : Zhong, M. C. and Z. Huang 1995 Ontogeny of lymphomyeloid or2 gans in catfish ( Silurus asot us L. ). J. Fisheries. China. 19 (3) : [, (3) : ] ( Explanation of Plates) ( Plate ) 11 ( ) [ Hemopoietic stem cells in the embryonic liver (black arrow) ] ( ) [ Hemopoietic stem cells near embryonic liver (black arrow) ] ( ) [ Hemopoietic stem cells in blood vessel near thymic primordium (black arrow) ] ( ) [ The thymic primordium (black arrow) ] ( ) [ Two thymic primodia consisting of mesenchyme cells (black arrows) ] ( ) ( ) [ Two thymuses containing a large number of hemopoietic stem cells (prothymocytes) and the parathyroid gland (black arrows) ] 200 ( Plate ) 71 ( ) ( ) [ Thymus containing a large number of hemopoietic stem cells (prothymo2 cytes) and the parathyroid gland (black arrows) ] ( ) [ Thymus containing a large number of thymocytes and the parathyroid gland embedded in the thymus (black arrows) ] ( ) [ The thymus containing complete thymus lobes and the parathyroid gland embedded in the thymus (black arrows) ] ( ) [ The splenic primordium (black arrow) ] ( ) [ The splenic primordium, embryonic liver and the head kidney2like tissue in embryonic kidney (black arrows) ] ( ) [ The splenic primordium and the hemopoietic stem cells near splenic primordium (black arrows) ] 200 ( Plate ) 131 ( ) [ Acidophilic cells in the dorsal mesogastrium (black arrows) ] ( ) [ Acidophilic cells in dorsal mesogastrium near the splenic primordium (black arrows) ] ( ) [ Acidophilic cells in the spleen (black arrows) ] ( ) [ Hemopoietic stem cells and lymphocytes in the spleen (black arrow) ] ( ) [ Erythrocytes at different developmental stages in the embryonic liver (black arrow) ] ( ) [ Acidophilic cells in kidney (black arrows) ] 400
8 : GUO Qiong2Lin et al. : Ontogeny of hempopoietic and immune organs in the Chinese soft2shelled turtle ( T rionyx sinensis) Plate ( Explanation at the end of the text)
9 : GUO Qiong2Lin et al. : Ontogeny of hempopoietic and immune organs in the Chinese soft2shelled turtle ( T rionyx sinensis) Plate ( Explanation at the end of the text)
10 : GUO Qiong2Lin et al. : Ontogeny of hempopoietic and immune organs in the Chinese soft2shelled turtle ( T rionyx sinensis) Plate ( Explanation at the end of the text)
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