Startseite Lebenswissenschaften Morphological view on the evolution of the immunity and lymphoid organs of vertebrates, focused on thymus
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Morphological view on the evolution of the immunity and lymphoid organs of vertebrates, focused on thymus

  • Veronika Mešťanová und Ivan Varga EMAIL logo
Veröffentlicht/Copyright: 23. November 2016
Veröffentlichen auch Sie bei De Gruyter Brill
Biologia
Aus der Zeitschrift Biologia Band 71 Heft 10

Abstract

To understand fundamental defense mechanisms of an individual and to perceive organization and functioning of the human immune system, it is inevitable to sum up its phylogenic development. Lymphoid organs are crucial in regulation of physiological lymphocytes development and subsequently play a significant role in appropriate immunological responses to foreign pathogens. Throughout the evolutionary tree, the primary lymphoid organs have emerged earlier than the secondary lymphoid organs. Considering the sites for cell populations’ development responsible for adaptive immunity, B lymphocytes differentiation and maturation have considerably differed during phylogeny as well as ontogeny. On the contrary, T lymphocytes development is defined exclusively in the thymus. From the evolutionary point of view, location of primary lymphoid organs must have been sophistically pre-programmed in terms of their function. Need for thymus evolving from the foregut supports the fact of emerging diverse repertoire of antigen receptors. The thymus represents the very first lymphoid organ evolved in Vertebrata to deal with potentially autoreactive, somatically heterogeneous T lymphocyte receptors. The necessity of maintaining an immunological integrity was the most crucial stimulus for evolution. Thymus as a primary lymphoid organ constitutes an eminent structure that markedly differentiates the higher Vertebrata from the rest of the animal phyla. The present paper is meant to provide a profound evolutionary insight into the lymphoid organs with the emphasis on the thymus morphology through the phylogenesis.

References

Adamkov M., Furjelová M., Horáček J., Benčat M. & Kružliak P. 2014. Relationship of mismatch repair proteins and survivin in colon polyps and carcinomas. Acta Histochem. 116 (6): 1007–1014. 10.1016/j.acthis.2014.04.00510.1016/j.acthis.2014.04.005Suche in Google Scholar

Adamkov M., Halasova E., Rajcani J., Bencat M., Vybohova D., Rybarova S. & Galbavy S. 2011. Relation between expression pattern of p53 and survivin in cutaneous basal cell carcinomas. Med. Sci. Monit. 17 (3): BR74–80. 10.12659/MSM.88144210.12659/MSM.881442Suche in Google Scholar

Agius C. & Roberts R. J. 2003. Melano-macrophage centres and their role in fish pathology. J. Fish Dis. 26 (9): 499–509. 10.1046/j.1365-2761.2003.00485.x10.1046/j.1365-2761.2003.00485.xSuche in Google Scholar

Aifantis I., Mandal M., Sawai K., Ferrando A. & Vilimas T. 2006. Regulation of T-cell progenitor survival and cell-cycle entry by the pre-T-cell receptor. Immunol. Rev. 209 (1): 159–169. 10.1111/j.0105-2896.2006.00343.x10.1111/j.0105-2896.2006.00343.xSuche in Google Scholar

Alitheen N.B., McClure S. & McCullagh P. 2010. B-cell development: one problem, multiple solutions. Immunol. Cell. Biol. 88 (4): 445–450. 10.1038/icb.2009.11910.1038/icb.2009.119Suche in Google Scholar

Amemiya C.T., Saha N.R. & Zapata A. 2007. Evolution and development of immunological structures in the lamprey. Curr. Opin. Immunol. 19 (5): 535–541. 10.1016/j.coi.2007.08.00310.1016/j.coi.2007.08.003Suche in Google Scholar

Ardavin C.F., Gomariz R.P., Barrutia M.G., Fonfriat J. & Zapata A. 1984. The lympho-hemopoietic organs of the anadromous sea lamprey, Petromyzon marinus. A comparative study throughout its life span. Acta Zool. (Stockh.) 65 (1): 1–15. 10.1111/j.1463-6395.1984.tb00805.x10.1111/j.1463-6395.1984.tb00805.xSuche in Google Scholar

Ardavín C.F. & Zapata A. 1987. Ultrastructure and changes during metamorphosis of the lympho-hemopoietic tissue of the larval anadromous sea lamprey Petromyzon marinus. Dev. Comp. Immunol. 11 (1): 79–93.10.1016/0145-305X(87)90010-3Suche in Google Scholar

Arstilla T.P., Vainio O. & Lassila O. 1994. Central role of CD4+ T cells in avian immune response. Poultry Sci. 73 (7): 1019– 1026. 10.3382/ps.073101910.3382/ps.0731019Suche in Google Scholar PubMed

Austbø L., Aas I.B., König M., Weli S.C., Syed M., Falk K. & Koppang E.O. 2014 Transcriptional response of immune genes in gills and the interbranchial lymphoid tissue of Atlantic salmon challenged with infectious salmon anaemia virus. Dev. Comp. Immunol. 45 (1): 107–114. 10.1016/j.dci.2014.02.00710.1016/j.dci.2014.02.007Suche in Google Scholar PubMed

Aw D. & Palmer D.B. 2011. The origin and implication of thymic involution. Aging Dis. 2 (5): 437–443. PMID: 22396892Suche in Google Scholar

Azzali G. 2003. Structure, lymphatic vascularization and lymphocyte migration in mucosa-associated lymphoid tissue. Immunol. Rev. 195 (1): 178–193. 10.1034/j.1600065X.2003.00072.x10.1034/j.1600-065X.2003.00072.xSuche in Google Scholar

Bai M., Doukas M., Papoudou-Bai A., Barbouti A., Stefanaki K., Galani V. & Kanavaros P. 2013. Immunohistological analysis of cell cycle and apoptosis regulators in thymus. Ann. Anat. 195 (2): 159–165. 10.1016/j.aanat.2012.07.01210.1016/j.aanat.2012.07.012Suche in Google Scholar PubMed

Bajoghli B., Guo P., Aghaallaei N., Hirano M., Strohmeier C., McCurley N., Bockman D.E., Schorpp M., Cooper M.D. & Boehm T. 2011. A thymus candidate in lampreys. Nature 470 (7332): 90–94. 10.1038/nature09655.10.1038/nature09655Suche in Google Scholar PubMed

Balogh P. 2011. Introduction: Evolution of peripheral lymphoid organs, Chapter 1, pp. 1–3, 10.1007/978-3-642-144295 1 Balogh P. (ed.), Developmental Biology of Peripheral Lymphoid Organs, Springer-Verlag, Berlin, Heidelberg, 177 pp. ISBN: 978-3-642-14428-810.1007/978-3-642-14429-5_1Suche in Google Scholar

Balogh P. & Lábadi, A. 2011. Structural evolution of the spleen in man and mouse, Chapter 11, 121–141. 10.1007/9783-642-14429-5 11 In: Balogh P. (ed.), Developmental Biology of Peripheral Lymphoid Organs, Springer-Verlag, Berlin, Heidelberg, 177 pp. ISBN: 978-3-642-14428-810.1007/978-3-642-14429-5_11Suche in Google Scholar

Bao H.J., Li M.Y., Wang J., Qin J.H., Xu C.S., Hei N.N., Yang P., Gandahi J.A. & Chen Q.S. 2009. Architecture of the blood-spleen barrier in the soft-shelles turtle, Pelodiseus sinensis. Anat. Rec. (Hoboken) 292 (8): 1079–1087. 10.1002/ar.20917.10.1002/ar.20917Suche in Google Scholar PubMed

Beard J. 1894. The development and probable function of the thymus. Anat. Anz. 9: 476–486.Suche in Google Scholar

Berens von Rautenfeld D. & Budras K.D. 1983. Topography, ultrastructure and phagocytic capacity of avian lymph nodes. Cell Tissue Res. 228 (2): 389–403. 10.1007/BF002048 8710.1007/BF00204887Suche in Google Scholar PubMed

Biggs P.M. 1957. The association of lymphoid tissue with the lymph vessels in the domestic chicken (Gallus domesticus). Acta Anat. 29 (1-2): 36–47. 10.1159/00014115910.1159/000141159Suche in Google Scholar PubMed

Bockman D.G. 1970. The thymus, Chapter 4, pp. 111–130. In: Gans C. & Parsons T.S. (eds), Biology of the Reptilia, Vol. 3, Part C Morphology, Academic Press, New York, 385 pp.Suche in Google Scholar

Bockman D.E. & Cooper M.D. 1973. Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix and Peyer’s patches. An electron microscopic study. Am. J. Anat. 136 (4): 455–477. 10.1002/aja.100136040610.1002/aja.1001360406Suche in Google Scholar PubMed

Bodey B., Bodey B.Jr., Siegel S.E. & Kaiser H.E. 2000. Novel insights into the function of the thymic Hassall’s bodies. In Vivo (Athens, Greece) 14 (3): 407–418. PMID: 10904874Suche in Google Scholar

Boehm T. 2011. Design principles of adaptive immune system. Nat. Rev. Immunol. 11 (5): 307–317. 10.1038/nri2944.10.1038/nri2944Suche in Google Scholar PubMed

Boehm T. & Bleul C.C. 2007. The evolutionary history of lymphoid organs. Nat. Immunol. 8 (2): 131–135. 10.1038/ni143510.1038/ni1435Suche in Google Scholar PubMed

Boehm T., Hess I. & Swann J.B. 2012a. Evolution of lymphoid tissues. Trends Immunol. 33 (6): 315–321. 10.1016/j.it.2012.02.005.10.1016/j.it.2012.02.005Suche in Google Scholar PubMed

Boehm T., McCurley N., Sutoh Y., Schorpp M., Kasahara M. & Cooper M.D. 2012b. VLR-based adaptive immunity. Annu. Rev. Immunol. 30: 203–220. 10.1146/annurev-immunol020711-07503810.1146/annurev-immunol-020711-075038Suche in Google Scholar PubMed PubMed Central

Borysenko M. 1976. Phylogeny of immunity: An overview. Immunogenetics 3 (1): 305–326. 10.1007/BF0157696410.1007/BF01576964Suche in Google Scholar

Borysenko M. & Cooper E.L. 1972. Lymphoid tissue in the snapping turtle, Chelydra serpentine. J. Morphol. 138 (4): 487– 497. 10.1002/jmor.105138040810.1002/jmor.1051380408Suche in Google Scholar PubMed

Bowden T.J, Cook P. & Rombout J.H. 2005. Development and function of the thymus in teleosts. Fish Shellfish Immunol. 19 (5): 413–427. 10.1016/j.fsi.2005.02.00310.1016/j.fsi.2005.02.003Suche in Google Scholar PubMed

Brendolan A., Rosado M.M., Carsetti R., Selleri L. & Dear T.N. 2007. Development and function of the mammalian spleen. Bioessays 29 (2): 166–177. 10.1002/bies.2052810.1002/bies.20528Suche in Google Scholar PubMed

Bringworth J.F. & Thorn M. 2013. Vertebrate immune system evolution and comparative primate immunity, pp. 17– 64. 10.1007/978-1-4614-7181-3 2. In: Bringworth J.F. & Pechenkina K. (eds), Primates, Pathogens, and Evolution, Part I., series Developments in Primatology: Progress and Prospects, Springer, New York, Heidelberg, Dordrecht, London. 428 pp. ISBN: 978-1-4614-7180-610.1007/978-1-4614-7181-3_2Suche in Google Scholar

Budras K.-D., Hullinger R.L. & Rautenfeld D.B.V. 1987. Lymph heart musculature in birds. J. Morphol. 191 (1): 77–87. 10.1002/jmor.105191010810.1002/jmor.1051910108Suche in Google Scholar PubMed

Burne R.H. 1926. Anatomy of the ductless glands and lymphatic system of the angler fish (Lophius piscatorius). Philos. Trans. R. Soc. London 215 (421–430): 1–56. 10.1098/rstb.1927.000110.1098/rstb.1927.0001Suche in Google Scholar

Butler J.E. & Sinkora M. 2013. The enigma of the lower gut-associated lymphoid tissue (GALT). J. Leukoc. Biol. 94 (2): 259–270. 10.1189/jlb.031312010.1189/jlb.0313120Suche in Google Scholar

Butler J.E., Sinkora M., Wertz N., Holtmeier W. & Lemke C.D. 2006. Development of the neonatal B and T cell repertoire in swine: implications for comparative and veterinary immunology. Vet. Res. 37 (3): 417–441. 10.1051/vetres:200600910.1051/vetres:2006009Suche in Google Scholar

Castenholz A. & Castenholz H.E. 1996. Casting methods of scanning electron microscopy applied to hemal lymph nodes in rats. Lymphology 29 (3): 95–105.Suche in Google Scholar

Cerutti P. & Guerrero F. 2008. Erythropoiesis and erythrophagocytosis in bovine haemal nodes. Int. J. Morphol. 26 (3): 557– 562. 10.4067/S0717-9502200800030000810.4067/S0717-95022008000300008Suche in Google Scholar

Cesta M.F. 2006. Normal structure, function and histology of the spleen. Toxicol. Pathol. 34 (5): 455–465. 10.1080/0192623060086774310.1080/01926230600867743Suche in Google Scholar

Chantanachookhin C., Seikai T. & Tanaka M. 1991. Comparative study of the ontogeny of the lymphoid organs in three species of marine fish. Aquaculture 99 (1-2): 143–155. 10.1016/0044-8486(91)90294-H10.1016/0044-8486(91)90294-HSuche in Google Scholar

Chieffi G., Chieffi Bacari G., Di Matteo L., d’Istria M., Minucci S. & Varriale B. 1996. Cell biology of the Harderian gland. Int. Rev. Cytol. 168: 1–80. 10.1016/S0074-7696(08)60882-710.1016/S0074-7696(08)60882-7Suche in Google Scholar

Chilmonczyk K. 1992. The thymus in fish: Development and possible function in the immune response. Annu. Rev. Fish Disease 2: 181–200. 10.1016/0959-8030(92)90063-410.1016/0959-8030(92)90063-4Suche in Google Scholar

Chung C.Y., Ysebaert D., Berneman Z.N. & Cools N. 2013. Dendritic cells: cellular mediators for immunological tolerance. Clin. Dev. Immunol. 2013: 8 pp. 10.1155/2013/972865.10.1155/2013/972865Suche in Google Scholar PubMed PubMed Central

Ciriaco E., Pinera P.P., Diaz-Esnal B. & Laura R. 2003. Age-related changes in the avian primary lymphoid organs (thymus and bursa of Fabricius). Microsc. Res. Tech. 62 (6): 482–487. 10.1002/jemt.1041610.1002/jemt.10416Suche in Google Scholar PubMed

Cooper E.L. 1982. General Immunology. A Wheaton & Co. Ltd., Exeter, 343 pp. ISBN: 0080263682, 9780080263687Suche in Google Scholar

Cooper M.D. & Alder, M.N. 2006. The evolution of adaptive immune systems. Cell 124 (4): 815–822. 10.1016/j. cell.2006.02.00110.1016/j.cell.2006.02.001Suche in Google Scholar PubMed

Cooper E.L., Brown B.A. & Wright R.K. 1975. New ideas on amphibian immunity: the lymph gland: a generator of both T and B cells. Am. Zool. 15 (1): 85–92. 10.1093/icb/15.1.8510.1093/icb/15.1.85Suche in Google Scholar

Curtis S.K., Volpe E.P. & Cowden R.R. 1972. Ultrastructure of the developing thymus of the leopard frog. Rana pipiens. Z. Zellforsch. Mikrosk. Anat. 127 (3): 323–346. 10.1007/BF0030687710.1007/BF00306877Suche in Google Scholar PubMed

Dalum A.S., Austbø L., Bjørgen H., Skjødt K., Hordvik I., Hansen T., Fjelldal P.G., Press C.M., Griffiths D.J. & Koppang E.O. 2015. The interbranchial lymphoid tissue of Atlantic Salmon (Salmo salar L) extends as a diffuse mucosal lymphoid tissue throughout the trailing edge of the gill filament. J. Morphol. 276 (9): 1075–1088. 10.1002/jmor.2040310.1002/jmor.20403Suche in Google Scholar PubMed

Danilova N. 2006. The evolution of immune mechanisms. J. Exp. Zool. B. Mol. Dev. Evol. 306B (6): 496–520. 10.1002/jez.b.2110210.1002/jez.b.21102Suche in Google Scholar PubMed

Danilova N., Hohman V.S., Sacher F., Ota T., Willett C.E. & Steiner L.A. 2004. T cells and the thymus in developing zebrafish. Dev. Comp. Immunol. 28 (7-8): 755–767. 10.1016/j.dci.2003.12.00310.1016/j.dci.2003.12.003Suche in Google Scholar PubMed

Dooley J., Erickson M., Gillard G.O. & Farr A.G. 2006. Cervical thymus in the mouse. J. Immunol. 176 (11): 6484–6490. 10.4049/?jimmunol.176.11.648410.4049/jimmunol.176.11.6484Suche in Google Scholar PubMed

Dorko F., Danko J., Flešárová S., Boroš E. & Sobeková A. 2011a. Effect of pesticide bendiocarbamate on distribution of acetylcholine- and butyrylcholine-positive nerves in rabbit’s thymus. Eur. J. Histochem. 55 (4): e37. 10.4081/ejh.2011.e3710.4081/ejh.2011.e37Suche in Google Scholar PubMed PubMed Central

Dorko F., Horáček J., Tokarčík J. & Miko M. 2013. Cholinesterase activity in quail primary lymphoid organs. Biologia 68 (6): 1238–1242. 10.2478/s11756-013-0269-010.2478/s11756-013-0269-0Suche in Google Scholar

Dorko F., Kluchová D., Boleková A., Špakovská T., Borošová T. & Lovasová K. 2011b. Influence of surgical and chemical orchidectomy on weight and distribution of AChE-nerve fibers in thymuses of adult rats. Eur. J. Histochem. 55 (3): e22. 10.4081/ejh.2011.e2210.4081/ejh.2011.e22Suche in Google Scholar PubMed PubMed Central

Du Pasquier L. 1982. Ontogeny of immunological functions in amphibians, Chapter 18, pp. 633–657. 10.1007/978-14684-4166-6 18. In: Cohen N. & Sigel M.M. (eds), Phylogeny and Ontogeny, Springer US, 757 pp. ISBN: 978-1-4684-4168-010.1007/978-1-4684-4166-6_18Suche in Google Scholar

Du Pasquier L., Schwager J. & Flajnik M.F. 1989. The immune system of Xenopus. Annu. Rev. Immunol. 7: 251–275. 10.1146/annurev.iy.07.040189.00134310.1146/annurev.iy.07.040189.001343Suche in Google Scholar PubMed

Duellman W.E. & Trueb L. 1986. Biology of Amphibians. The Johns Hopkins University Press, Maryland, 670 pp. ISBN: 080184780X10.2307/1445022Suche in Google Scholar

Ekman A., Pessa-Morikawa T., Liljavirta J., Niku M. & Iivanainen A. 2010. B-cell development in bovine fetuses proceeds via a pre-B like cell in bone marrow and lymph nodes. Dev. Comp. Immunol. 34 (8): 896–903. 10.1016/j.dci.2010.03.01210.1016/j.dci.2010.03.012Suche in Google Scholar PubMed

Elmore S. 2007. Apoptosis. A review of programmed cell death. Toxicol. Pathol. 35 (4): 495–516. 10.1080/0192623070 132033710.1080/01926230701320337Suche in Google Scholar PubMed PubMed Central

Ezeasor D.N. & Singh A. 1988. Histology of the caprine hemal node. Acta Anat. 133 (1): 16–23. 10.1159/00014660710.1159/000146607Suche in Google Scholar PubMed

Fänge R. 1977. Size relations of lymphomyeloid organs in some cartilaginous fish. Acta Zool. 58 (3): 125–128. 10.1111/j.1463-6395.1977.tb00246.x10.1111/j.1463-6395.1977.tb00246.xSuche in Google Scholar

Fänge R. & Mattisson A. 1981. The lymphomyeloid (hemopoietic) system of the atlantic nurse shark, Gynglymostoma cirratum. Biol. Bull. 160 (2): 240–249.10.2307/1540884Suche in Google Scholar

Fänge R. & Pulsford A. 1983. Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L. Cell Tissue Res. 230 (2): 337–351. 10.1007/BF002138 0810.1007/BF00213808Suche in Google Scholar PubMed

Fänge R. & Sundell G. 1969. Lymphomyeloid tissues, blood cells and plasma proteins in Chimaera monstrosa (Pisces, Holocephali). Acta Zool. 50 (1-2): 155–168. 10.1111/j.14636395.1969.tb00537.x10.1111/j.1463-6395.1969.tb00537.xSuche in Google Scholar

Flajnik M.F. & Du Pasquier, L. 2004. Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol. 25 (12): 640–644. 10.1016/j.it.2004.10.00110.1016/j.it.2004.10.001Suche in Google Scholar PubMed

Fujii T. 1982. Electron microscopy of the leucocytes of the typhlosole in ammocoetes, with special attention to the antibody producing cells. J. Morphol. 173 (1): 87–100. 10.1002/jmor.105173010810.1002/jmor.1051730108Suche in Google Scholar PubMed

Geenen V. 2012a. The appearance of the thymus and the integrated evolution of adaptive immune and neuroendocrine systems. Acta Clin. Belg. 67 (3): 209–213. 10.1179/ACB.67.3.2062657 –Suche in Google Scholar

Geenen V. 2012b. Presentation of neuroendocrine self in the thymus: a necessity for integrated evolution of the immune and neuroendocrine systems. Ann. N. Y. Acad. Sci. 1261 (1): 42–48. 10.1111/j.1749-6632.2012.06624.x10.1111/j.1749-6632.2012.06624.xSuche in Google Scholar PubMed

Glick B. 1979. The avian immune system. Avian Dis. 23 (2): 282–289. 10.2307/158955710.2307/1589557Suche in Google Scholar

Glick B., Chang T.S. & Jaap R.G. 1956. The bursa of Fabricius and antibody production. Poultry Sci. 35 (1): 224–225. 10.3382/ps.035022410.3382/ps.0350224Suche in Google Scholar

Goldstine S.N., Manickavel V. & Cohen N. 1975. Phylogeny of gut-associated lymphoid tissue. Amer. Zool. 15: 107–118. 10.1093/icb/15.1.10710.1093/icb/15.1.107Suche in Google Scholar

Gorgollon P. 1983. Fine structure of the thymus in the adult cling fish Sicyases sanguineus (Pisces, Gobiesocidae). J. Morphol. 177 (1): 25–40. 10.1002/jmor.105177010310.1002/jmor.1051770103Suche in Google Scholar PubMed

Grapin-Botton A. & Constam D. 2007. Evolution of the mechanisms and molecular control of endoderm formation. Mech. Dev. 124 (4): 253–278. 10.1016/j.mod.2007.01.00110.1016/j.mod.2007.01.001Suche in Google Scholar PubMed

Guo P., Hirano M., Herrin B.R., Li J., Yu C., Sadlonova A. & Cooper M.D. 2009. Dual nature of the adaptive immune system in lampreys. Nature 459 (7248): 796–801. 10.1038/nature08068Suche in Google Scholar

Hadeiba H. & Butcher E.C. 2013. Thymus-homing dendritic cells in central tolerance. Eur. J. Immunol. 43 (6): 1425–1429. 10.1002/eji.20124319210.1002/eji.201243192Suche in Google Scholar PubMed PubMed Central

Halašová E., Adamkov M., Matáková T., Kavcová E., Poliaček I. & Šingliar A. 2010. Lung cancer incidence and survival in chromium exposed individuals with respect to expression of anti-apoptotic protein survivin and tumor suppresor p53 protein. Eur. J. Med. Res. 15 (Suppl. 2): 55–59. PMID: 2114762110.1186/2047-783X-15-S2-55Suche in Google Scholar

Hale L.P. & Markert M.L. 2004. Corticosteroids regulate epithelial cell differentiation and Hassall body formation in the human thymus. J. Immunol. 172 (1): 617–624. 10.4049/jimmunol.172.1.61710.4049/jimmunol.172.1.617Suche in Google Scholar PubMed

Hansen J.D. & Zapata A.G. 1998. Lymphocyte development in fish and amphibians. Immunol. Rev. 166: 199–220. 10.1111/j.1600-065X.1998.tb01264.x10.1111/j.1600-065X.1998.tb01264.xSuche in Google Scholar

Hart S., Wrathmell A.B. & Harris J.E. 1986. Ontogeny of gut-associated lymphoid tissue (GALT) in the dogfish Scyliorhinus canicula L. Vet. Immunol. Immunopathol. 12 (1-4): 107– 116. 10.1016/0165-2427(86)90115-710.1016/0165-2427(86)90115-7Suche in Google Scholar

Hedrick M.S., Hansen K., Wang T., Lauridsen H., Thygesen J. & Pedersen, M. 2014. Visualising lymph movement in anuran amphibians with computed tomography. J. Exp. Biol. 217 (17): 2990–2993 10.1242/jeb.10690610.1242/jeb.106906Suche in Google Scholar PubMed

Henry M. & Charlemagne J. 1980. Development of amphibian thymus. Morphological differentiation, multiplication, migration and lysis of thymocytes in the urodele Pleurodeles waltlii. J. Embryol. Exp. Morph. 57: 219–232. PMID: 743093110.1242/dev.57.1.219Suche in Google Scholar

Herrin B.R. & Cooper M.D. 2010. Alternative adaptive immunity in jawless vertebrates. J. Immunol. 185 (3): 1367–1374. 10.4049/jimmunol.090312810.4049/jimmunol.0903128Suche in Google Scholar PubMed

Honma Y., Okabe K. & Chiba A. 1984. Comparative histology of the Leydig and epigonal organs in some elasmobranches. Jap. J. Ichtyol. 31 (1): 47–54.Suche in Google Scholar

Ishizuya-Oka A., Hasebe T. & Shi Y.-B. 2010. Apoptosis in amphibian organs during metamorphosis. Apoptosis 15 (3): 350–364. 10.1007/s10495-009-0422-y.10.1007/s10495-009-0422-ySuche in Google Scholar PubMed PubMed Central

Jablonska-Mestanova V., Sisovsky V., Danisovic L., Polak S. & Varga I. 2013. The normal human newborns thymus. Bratisl. Lek. Listy 114 (7): 402–408.10.4149/BLL 2013 08610.4149/BLL_2013_086Suche in Google Scholar PubMed

John J.L. 1994. The avian spleen: A neglected organ. Q. Rev. Biol. 69 (3): 327–351. 10.1086/41864910.1086/418649Suche in Google Scholar PubMed

Johnston M.R.L. 1973. Perivascular lymphoid tissue associated with the axillary lymph sinus and lateral vein of the Gehyra variegate. J. Morphol. 139 (4): 431–438. 10.1002/jmor.105139040510.1002/jmor.1051390405Suche in Google Scholar PubMed

Jolly J. 1913. Sur les organs lympho-epitheliaux. Comp. Rend. Hebdom. Seanc. Mem. Soc. Biol. A65, 74 (T1): 540–543.Suche in Google Scholar

Jordan R.K. 1976. Development of sheep thymus in relation to utero thymectomy experiments. Eur. J. Immunol. 6 (10): 693–698. 10.1002/eji.183006100710.1002/eji.1830061007Suche in Google Scholar PubMed

Joss J.M.P. 1998. Are lungfish neotenic? Clin. Exp. Pharmacol. Physiol. 25 (9): 733–735. 10.1111/j.14401681.1998.tb02286.x10.1111/j.1440-1681.1998.tb02286.xSuche in Google Scholar

Junt T., Scandella E. & Ludewig B. 2008. Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat. Rev. Immunol. 8 (10): 764–775. 10.1038/nri241410.1038/nri2414Suche in Google Scholar

Kachlik D., Baca V., Bozdechova I., Cech P. & Musil V. 2008. Anatomical terminology and nomenclature: past, present and highlights. Surg. Radiol. Anat. 30 (6): 459–466. 10.1007/s00276-008-0357-y10.1007/s00276-008-0357-ySuche in Google Scholar

Kannan T.A., Ramesh G., Ushakumary S., Dhinakarraj G. & Vairamuthu S. 2015. Thymic Hassall’s corpuscles in Nandanam chicken – light and electronmicroscopic perspective (Gallus domesticus). J. Anim. Sci. Technol. 57: 30. 10.1186/s40781-015-0064-210.1186/s40781-015-0064-2Suche in Google Scholar

Katagiri Ch. 1978. Xenopus laevis as a model for the study of immunology. Dev. Comp. Immunol. 2 (1): 5–13. 10.1016/S0145-305X(78)80020-210.1016/S0145-305X(78)80020-2Suche in Google Scholar

Kendall M.D. 1980. Avian thymus glands: a review. Dev. Comp. Immunol. 4: 191–209. 10.1016/S0145-305X(80)80023-110.1016/S0145-305X(80)80023-1Suche in Google Scholar

Kihara T. & Naito E. 1933. Beiträge zur Anatomie des Lymphgefässsystems der Wirbeltiere und des Menschen (Japaner). Nr. 19. Uber den Einlagerungs- und Verbreitungsmodus des lympha tischen Gewebes im Lymphgefasssystem der Ente. Folia Anat. Jap. 11 (5): 405–413.10.2535/ofaj1922.11.5_405Suche in Google Scholar

Koch G. 1991. The immune system in poultry. Tijdschr. Diergeneeskde. 116 (14): 728–734.Suche in Google Scholar

Kondo M. 1937. Beiträge zur Anatomie des Lymphgefässsystems der Wirbeltiere und des Menschen (Japaner). Nr. 24. Die lymphatischen gebilde im lymphgefasssystem der Huhnes. Folia Anat. Jap. 15: 309–325.10.2535/ofaj1936.15.3_309Suche in Google Scholar

Konkel J.E., Jin W., Abbatiello B., Grainger J.R. & Chen W. 2014. Thymocyte apoptosis drives the intrathymic generation of regulatory T cells. Proc. Natl. Acad. Sci. USA. 111 (4): E465–473. 10.1073/pnas.1320319111.10.1073/pnas.1320319111Suche in Google Scholar PubMed PubMed Central

Koppang E.O., Fischer U., Moore L., Tranulis M.A., Dijkstra J.M., Köllner B., Aune L., Jirillo E. & Hordvik I. 2010. Salmonid T cells assemble in the thymus, spleen and in novel interbranchial lymphoid tissue. J. Anat. 217 (6): 728–739. 10.1111/j.1469-7580.2010.01305.x10.1111/j.1469-7580.2010.01305.xSuche in Google Scholar PubMed PubMed Central

Kovalska M., Kovalska L., Pavlikova M., Janickova M., Mikuskova M., Adamkov M., Kaplan P., Tatarkova Z. & Lehotsky J. 2012. Intracellular signaling MAPK pathway after cerebral ischemia-reperfusion injury. Neurochem. Res. 37 (7): 1568– 1577. 10.1007/s11064-012-0752-y10.1007/s11064-012-0752-ySuche in Google Scholar PubMed

Lillehoj H.S. & Trout J.M. 1996. Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clin. Microbiol. Rev. 9 (3): 349–360. PMID: 880946510.1128/CMR.9.3.349Suche in Google Scholar PubMed PubMed Central

Liu Z. & Casley-Smith J.R. 1989. The fine structure of the amphibian lymph heart. Lymphology 22 (1): 25–30. PMID:2725054Suche in Google Scholar

Lofts B. 2012. Physiology of the Amphibian. Vol. 3. Academic Press, INC, New York, 658 pp. ISBN: 0-12-455403-2Suche in Google Scholar

Luer C.A., Walsh C.J., Bodine A.B., Wyffels J.T. & Scott T.R. 1995. The elasmobranch thymus: Anatomical, histological, and preliminary functional characterization. J. Exp. Zool. 273 (4): 342–354. 10.1002/jez.140273040810.1002/jez.1402730408Suche in Google Scholar

Lutton B.V. & Callard I.P. 2008. Influence of reproductive activity, sex steroids, and seasonality on epigonal organ cellular proliferation in the skate (Leucoraja erinacea). Gen. Comp. Endocrinol. 155 (1): 116–125. 10.1016/j.ygcen. 2007.03.01110.1016/j.ygcen.2007.03.011Suche in Google Scholar PubMed

Manley N.R., Richie E.R., Blackburn C.C., Condie B.G. & Sage J. 2011. Structure and function of the thymic microenvironment. Front. Biosci. 16 (7): 2461–2477. 10.2741/386610.2741/3866Suche in Google Scholar PubMed

Manning M. J. 1979. Evolution of the vertebrate immune system. J. R. Soc. Med 72 (9): 683–688. 10.1177/01410768790 720091110.1177/014107687907200911Suche in Google Scholar PubMed

Manning M.J. & Horton J.D. 1969. Histogenesis of lymphoid organs in larvae of the South African clawed toad, Xenopus laevis (Daudin). J. Embryol. Exp. Morph. 22 (2): 265–277. PMID: 536155710.1242/dev.22.2.265Suche in Google Scholar

Manning M.J. & Horton J.D. 1982. RES Structure and Function of the Amphibia, pp. 423–459. In: Cohen N. & Sigel N.N. (eds), The Reticuloepithelial System 3. A Comprehensive Treatise. Plenum Press, New York.10.1007/978-1-4684-4166-6_11Suche in Google Scholar

Mattisson A. & Fänge R. 1982. The cellular structure of the Leydig organ in the shark, Etmopterus spinax (L.). Biol. Bull. 162 (2): 182–194. 10.2307/154081310.2307/1540813Suche in Google Scholar

Mattisson A., Fänge R. & Zapata A. 1990. Histology and ultrastructure of the cranial lymphohaemopoietic tissue in Chimaera monstrosa (Pisces, Holocephali). Acta Zool. 71 (2): 97–106. 10.1111/j.1463-6395.1990.tb01074.x10.1111/j.1463-6395.1990.tb01074.xSuche in Google Scholar

Mayer S. 1888. Zur lehre von der Schilddröuse und thymus bei Amphibien. Anat. Anz. 3: 97–103.Suche in Google Scholar

Mohammad M.G., Chilmonczyk S., Birch D., Aladaileh S., Raftos D. & Joss J. 2007. Anatomy and cytology of the thymus in juvenile Australian lungfish, Neoceratodus forsteri. J. Anat. 211 (6): 784–797. 10.1111/j.1469-7580.2007.00814.x10.1111/j.1469-7580.2007.00814.xSuche in Google Scholar

Mravec B., Ondicova K., Valaskova Z., Gidron Y. & Hulin I. 2009. Neurobiological principles in the etiopathogenesis of disease: when diseases have a head. Med. Sci. Monit. 15 (1): RA6–16. PMID: 19114982Suche in Google Scholar

Mueller S.N. & Germain R.N. 2009. Stromal cell contributions to the homeostasis and functionalityof the immune system. Nat. Rev. Immunol. 9 (9): 618–629. 10.1038/nri258810.1038/nri2588Suche in Google Scholar

Muthukkaruppan V.R., Borysenko M. & El Ridi R. 1982. RES Structure and function of the Reptilia, Chapter 12, pp. 461– 508. 10.1007/978-1-4684-4166-6 12 In: Cohen N. & Sigel N.N. (eds), The Reticuloeptelial System. A Comprehensive Treatise, Plenum Press, New York, 757 pp. ISBN: 978-1-4684-4168-010.1007/978-1-4684-4166-6_12Suche in Google Scholar

Nakagawa Y., Ohigashi I., Nitta T., Sakata M., Tanaka K., Murata S., Kanagawa O. & Takahama Y. 2012. Thymic nurse cells provide microenvironment for secondary T cell receptor α rearrangement in cortical thymocytes. Proc. Natl. Acad. Sci. USA. 109 (50): 20572–20577. 10.1073/pnas.12130 6910910.1073/pnas.1213069109Suche in Google Scholar

Nakamura H. & Ayer-Le Ličvre C. 1986. Neural crest and thymic myoid cells. Curr. Top. Dev. Biol. 20: 111–115. 10.1016/S0070-2153(08)60658-410.1016/S0070-2153(08)60658-4Suche in Google Scholar

Nelsen O.E. 1953. Comparative embryology of the vertebrates. McGraw-Hill Book Company, INC. New York, 982 pp. 10.5962/bhl.title.6451Suche in Google Scholar

Nishio H., Matsui K., Tsuji H., Tamura A. & Suzuki K. 2001. Immunolocalization of the mitogen-activated protein kinase signaling pathway in Hassall’s corpuscles of the human thymus. Acta Histochem. 103 (1): 89–98. 10.1078/00651281-0058110.1078/0065-1281-00581Suche in Google Scholar PubMed

Nishino M., Ashiku S.K., Kocher O.N., Thurer R.L., Boiselle P.M. & Hatabu H. 2006. The thymus: a comprehensive review. Radiographics 26 (2): 335–348. 10.1148/rg.2620 4521310.1148/rg.262045213Suche in Google Scholar PubMed

Oguri M. 1983. On the Leydig organ in the esophagus of some elasmobranchs. Bull. Jap. Soc. Sci. Fish. 49 (7): 989–991. http://doi.org/10.2331/suisan.49.98910.2331/suisan.49.989Suche in Google Scholar

Ohno H. 2016. Intestinal M cells. J. Biochem. 159 (2): 151–160. 10.1093/jb/mvv12110.1093/jb/mvv121Suche in Google Scholar PubMed PubMed Central

Oláh I., Glick B. & Taylor R.L. Jr. 1984. Meckel’s diverticulum. II. A novel lymphoepithelial organ in the chicken. Anat. Rec. 208 (2): 253–263. 10.1002/ar.109208021210.1002/ar.1092080212Suche in Google Scholar PubMed

Osório J. & Rétaux S. 2008. The lamprey in evolutionary studies. Dev. Genes Evol. 218 (5): 221–235. 10.1007/s00427008-0208-110.1007/s00427-008-0208-1Suche in Google Scholar

Ottaviani E., Franchini A. & Franceschi C. 1997. Evolution of neuroendocrine thymus: studies on POMC-derived peptides, cytokines and apoptosis in higher and lower vertebrates. J. Neuroimmunol. 72 (1): 67–74. 10.1016/S01655728(96)00146-410.1016/S0165-5728(96)00146-4Suche in Google Scholar

Øvergård A.C., Fiksdal I.U., Nerland A.H. & Patel S. 2011. Expression of T-cell markers during Atlantic halibut (Hippoglossus hippoglossus L.) ontogenesis. Dev. Comp. Immunol. 35 (2): 203–213. 10.1016/j.dci.2010.09.00910.1016/j.dci.2010.09.009Suche in Google Scholar

Paganelli R., Giovannetti A., Pierdominici M., Di Iorio A., Cianci R., Murdaca G., Puppo F. & Pandolfi P. 2008. Apoptosis in the homeostasis of the immune system and in human immune mediated disease. Curr. Pharm. Des. 14 (3): 253–268. 10.2174/13816120878341331010.2174/138161208783413310Suche in Google Scholar

Page M. & Rowley A.F. 1982. A morphological study of pharyngeal lymphoid accumulations in larval lampreys. Dev. Comp. Immunol. Suppl 2: 35–40.Suche in Google Scholar

Panse Le R. & Berrih-Aknin S. 2005. Thymic myoid cells protect thymocytes from apoptosis and modulate their differentiation: implication of the ERK and Akt signaling pathways. Cell Death Differ. 12 (5): 463–472. 10.1038/sj.cdd.440161110.1038/sj.cdd.4401611Suche in Google Scholar

Patel S., Sørhus E., Fiksdal I.U., Espedal P.G., BerghO., Rødseth O.M., Morton H.C. & Nerland A.H. 2009. Ontogeny of lymphoid organs and development of IgM-bearing cells in Atlantic halibut (Hippoglossus hippoglossus L.). Fish Shellfish Immunol. 26 (3): 385–395. 10.1016/j.fsi.2008.11.01810.1016/j.fsi.2008.11.018Suche in Google Scholar

Payne A.P. 1994. The Harderian gland: a tercentennial review. J. Anat. 185 (Pt 1): 1–49. PMID: 7559104Suche in Google Scholar

Picchietti S., Guerra L., Buonocore F., Randelli E., Fausto A.M. & Abelli L. 2009. Lymphocyte differentiation in sea bass thymus: CD4 and CD8-alpha gene expression studies. Fish Shellfish Immunol. 27 (1): 50–56. 10.1016/j.fsi.2009.04.00310.1016/j.fsi.2009.04.003Suche in Google Scholar

Pospíšilová V., Slípka J. & Černý R. 2003. The relation of the germ layers to the ecto-mesenchyme of the neural placodes during thymus development. Trends and Perspectives of Contemporary Morphology. 40th Congress of the Czech Anatomical Society, Plzeň, 10.-12.9.2002. Plzeň Lék. Sbor. 78 (Suppl 1): 23–28.Suche in Google Scholar

Prymak T. 1902. Beiträge zur Kenntniss des feinen Baues und der Involution der Thymusdrüse bei den Teleostieren. Anat. Anz. 21: 164.Suche in Google Scholar

Raica M., Cîmpean A.M., Encicăa S. & Cornea R. 2007. Involution of the thymus: a possible diagnostic pitfall. Rom. J. Morphol. Embryol. 48 (2): 101–106.Suche in Google Scholar

Raica M., Encicăa S., Motoc A., Cîmpean A.M., Scridon T. & Bârsan M. 2006. Structural heterogeneity and immunohistochemical profile of Hassall corpuscles in normal human thymus. Ann. Anat. 188 (4): 345–352. 10.1016/j.aanat. 2006.01.01210.1016/j.aanat.2006.01.012Suche in Google Scholar

Ratcliffe M.J. 2002. B cell development in gut associated lymphoid tissues. Vet. Immunol. Immunopathol. 87 (3-4): 337– 440. PMID: 1207225510.1016/S0165-2427(02)00061-2Suche in Google Scholar

Ratcliffe M.J. 2006. Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev. Comp. Immunol. 30 (1-2): 101–118. 10.1016/j.dci.2005.06.01810.1016/j.dci.2005.06.018Suche in Google Scholar PubMed

Reboldi A. & Cyster J.G. 2016. Peyer’s patches: organizing B-cell responses at the intestinal frontier. Immunol. Rev. 271(1): 230–245 10.1111/imr.12400.10.1111/imr.12400Suche in Google Scholar

Reyes García M.G. & García Tamayo F. 2013. The importance of the nurse cells and regulatory cells in the control of T lymphocyte responses. BioMed. Res. Int. 2013: 15 pp. 10.1155/2013/35241410.1155/2013/352414Suche in Google Scholar

Rezzani R., Bonomini F. & Rodella L.F. 2008. Histochemical and molecular overview of the thymus as site for T-cells development. Prog. Histochem. Cytochem. 43 (2): 73–120. 10.1016/j.proghi.2008.03.00110.1016/j.proghi.2008.03.001Suche in Google Scholar

Rezzani R., Nardo L., Favero G., Peroni M. & Rodella L.F. 2014. Thymus and aging: morphological, radiological, and functional overview. Age (Dordr.). 36 (1): 313–351. 10.1007/s11357-013-9564-510.1007/s11357-013-9564-5Suche in Google Scholar

Rodewald H. R. 2008. Thymus organogenesis. Annu. Rev. Immunol. 26: 355–388. 10.1146/annurev.immunol.26. 021607.09040810.1146/annurev.immunol.26.021607.090408Suche in Google Scholar

Rodríguez R.M., López-Vázquez A. & López-Larrea C. 2012. Immune systems evolution. Adv. Exp. Med. Biol. 739: 237–251. 10.1007/978-1-4614-1704-0 15.10.1007/978-1-4614-1704-0_15Suche in Google Scholar

Rollins-Smith L.A., Blair P.J. & Davis A.T. 1992. Thymus ontogeny in frogs: T-cell renewal at metamorphosis. Dev. Immunol. 2 (3): 207–213. 10.1155/1992/2625110.1155/1992/26251Suche in Google Scholar

Romano N., Fanelli M., Maria Del Papa G., Scapigliati G. & Mastrolia L. 1999a. Histological and cytological studies on the developing thymus of sharpsnout seabream, Diplodus puntazzo. J. Anat. 194 (Pt 1): 39–50. 10.1046/j.14697580.1999.19410039.x10.1046/j.1469-7580.1999.19410039.xSuche in Google Scholar

Romano N., Taverne-Thiele A.J., Fanelli M., Baldassini M.R., Abelli L., Mastrolia L., Van Muiswinkel W.B. & Rombout, J.H. 1999b. Ontogeny of the thymus in a teleost fish, Cyprinus carpio L.: developing thymocytes in the epithelial microenvironment. Dev. Comp. Immunol. 23 (2): 123–137. 10.1016/S0145-305X(98)00053-610.1016/S0145-305X(98)00053-6Suche in Google Scholar

Rosenstiel P., Philipp E.E., Schreiber S. & Bosch T.C. 2009. Evolution and function of innate immune receptors – insights from marine invertebrates. J. Innate. Immun. 1 (4): 291–300. 10.1159/000211193.10.1159/000211193Suche in Google Scholar PubMed

Rumfelt L.L., McKinney E.C., Taylor E. & Flajnik M.F. 2002. The development of primary and secondary lymphoid tissues in the nurse shark Ginglymostoma cirratum: B-cell zones precede dendritic cell immigration and T-cell zone formation during ontogeny of the spleen. Scand. J. Immunol. 56 (2): 130–148. 10.1046/j.1365-3083.2002.01116.x10.1046/j.1365-3083.2002.01116.xSuche in Google Scholar

Saha N.R., Smith J. & Amemiya C.T. 2010. Evolution of adaptive immune recognition in jawless vertebrates. Semin. Immunol. 22 (1): 25–33. 10.1016/j.smim.2009.12.00210.1016/j.smim.2009.12.002Suche in Google Scholar

Sarang Z., Garabuczi É., Joós G., Kiss B., Tóth K., Rühl R. & Szondy Z. 2013. Macrophages engulfing apoptotic thymocytes produce retinoids to promote selection, differentiation, removal and replacement of double positive thymocytes. Immunobiol. 218 (11): 1354–1360. 10.1016/j.imbio. 2013.06.00910.1016/j.imbio.2013.06.009Suche in Google Scholar

Scott T.R. 2004. Our current understanding of humoral immunity of poultry. Poultry Sci.83 (4): 574–579. 10.1093/ps/83.4.57410.1093/ps/83.4.574Suche in Google Scholar

Schrøder M.B., Villena A.J. & Jørgensen T.O. 1998. Ontogeny of lymphoid organs and immunoglobulin producing cells in Atlantic cod (Gadus morhua L.). Dev. Comp. Immunol. 22 (5-6): 507–517. 10.1016/S0145-305X(98)00030-510.1016/S0145-305X(98)00030-5Suche in Google Scholar

Seto F. 1981. Early development of the avian immune system. Poultry Sci. 60 (9): 1981–1995. 10.3382/ps.060198110.3382/ps.0601981Suche in Google Scholar PubMed

Sharma J.M. 1997. The structure and function of the avian immune system. Acta Vet. Hung. 45 (3): 229–238. PMID: 9276985Suche in Google Scholar

Síma P. 1997. The development of the defence system during evolution, pp. 6–20. In: Heidt P.J., Rusch V. & der Waaij D. (eds), Old Herborn University Seminar Monograph, 10. New Antimicrobial Strategies, Herborn Litterae, Herborn-Dill, 137 pp. ISBN: 3-923022-20-4Suche in Google Scholar

Sima P. & Vetvicka V. 1993. Evolution of immune reactions. Crit. Rev. Immunol. 13 (2): 83–114. PMID: 8352910Suche in Google Scholar

Slípka J. 1986. Evolutionary morphology of the branchial region as the reflection of environmental changes, pp. 203–211. In: Novák V.J.A., Vančata V. & Vančatová M.A. (eds), Behaviour, Adaptation and Evolution, Czechoslovak Academy of Sciences, Praha.Suche in Google Scholar

Slipka J. & Slipka J.Jr. 1996. The palatine tonsil as an evolutionary novelty. Acta Otolaryngol. Suppl. 523: 8–11. PMID: 9082817Suche in Google Scholar

Smith K.G. & Hunt J.L. 2004. On the use of spleen mass as a measure of avian immune system strength. Oecologia 138 (1): 28–31. 10.1007/s00442-003-1409-y10.1007/s00442-003-1409-ySuche in Google Scholar PubMed

Spalding H. & Heath T. 1987. Pathways of lymph flow through superficial inguinal lymph nodes in the pig. Anat. Rec. 217 (2): 188–195. 10.1002/ar.109217021110.1002/ar.1092170211Suche in Google Scholar PubMed

Sypek J. & Borysenko M. 1988. Reptiles. In: Rowley A.F. & Ratcliffe N.A. (eds), Vertebrate Blood Cells, Press Sindicate in the University of Cambridge, 432 pp. ISBN: 0-521-26032-9Suche in Google Scholar

Štěrba G. 1953. Die Physiologie und Histogenese der Schilddrüuse und des Thymus beim Bachneunauge (Lampetra planeri Bloch = Petromyzon planeri Bloch) als Grundlagen phylogenetischer Studien über die Evolution der innersekretorischen Kiemendarmderivate nebenst eingehenden Mitteilungen über die Bionomie der Bachneunaugen und morphologisch-physiologischen Untersuchungen über die Kiemendarm. Wissenschaftliche Zeitschrift. Mathematisch-Naturwissenschaftliche Reihe 3 (2): 239–298.Suche in Google Scholar

Terszowski G., Muller S.M., Bleul C.C., Blum C., Schirmback R., Reimann J., Pasquier L. D., Amagai T., Boehm T. & Rodewald H.R. 2006. Evidence for a functional second thymus in mice. Science 312 (5771): 284–287. 10.1126/science.1123497Suche in Google Scholar

Tischendorf F. 1985. On the evolution of the spleen. Experientia 41 (2): 145–152. PMID: 397206210.1007/BF02002606Suche in Google Scholar PubMed

Tochinai S. 1976. Lymphoid changes in Xenopus laevis following thymectomy at the initial stage of its histogenesis. J. Fac. Sci. Hokkaido Univ. Ser. Zool. 20 (2): 175–184.Suche in Google Scholar

Valančiūtė A., Mozuraitė R., Balnytė I., Didžiapetrienė J., Matusevičius P. & Stakišaitis D. 2015. Sodium valproate effect on the structure of rat glandule thymus: Gender-related differences. Exp. Toxicol. Pathol. 67 (7-8): 399–406. 10.1016/j.etp.2015.04.00510.1016/j.etp.2015.04.005Suche in Google Scholar PubMed

Valasek P., Macharia R., Neuhuber W.L., Wilting J., Becker D.L. & Patel K. 2007. Lymph heart in chick–somitic origin, development and embryonic oedema. Development. 134(24): 4427–4436. 10.1242/dev.00469710.1242/dev.004697Suche in Google Scholar

Van de Pavert S.A. & Mebius R.E. 2010. New insights into the development of the lymphoid tissue. Nat. Rev. Immunol. 10 (9): 664–674. 10.1038/nri283210.1038/nri2832Suche in Google Scholar

Varas A., Sacedón R., Hernandez-López C., Jiménez E., Garcia-Ceca J., Arias-Díaz J., Zapata A.G. & Vicente A. 2003. Age-dependent changes in thymic macrophages and dendritic cells. Microsc. Res. Techn. 62 (6): 501–507. 10.1002/jemt.1041110.1002/jemt.10411Suche in Google Scholar

Varga I., Galfiova P., Jablonska-Mestanova V., Polak S. & Adamkov M. 2011a. Some aspects of early development of the thymus: Embryological basis for ectopic thymus and thymopharyngeal duct cyst. Rev. Arg. Anat. Clin. 3 (1): 22–31.10.31051/1852.8023.v3.n1.13909Suche in Google Scholar

Varga I., Mikusova R., Pospisilova V., Galfiova P., Adamkov M., Polak S. & Galbavy S. 2009. Morphologic heterogeneity of human thymic nonlymphocytic cells. Neuro Endocrinol. Lett. 30 (3): 275–283. PMID: 19855349Suche in Google Scholar

Varga I., Nescakova E., Toth F., Uhrinova A. & Adamkov M. 2011b. Nutrition and immune system: the size of the thymus as an indicator of the newborn‘s nutrition status. Anthropol. Anz. 68(3): 265-274. PMID: 2190541610.1127/0003-5548/2011/0105Suche in Google Scholar

Varga I., Pospisilova V., Gmitterova K., Galfiova P., Polak S. & Galbavy S. 2008. The phylogenesis and ontogenesis of the human pharyngeal region focused on the thymus, parathyroid, and thyroid glands. Neuroendocrinol. Lett. 29 (6): 837–845. PMID: 19112385Suche in Google Scholar

Varga I., Pospisilova V., Jablonska V., Sisovsky V., Galfiova P., Polak S. & Adamkov M. 2010. Thymic Hassall’s bodies of children with congenital heart defects. Bratisl. Lek. Listy 111 (10): 552–557. PMID: 21125801Suche in Google Scholar

Varga I., Pospisilova V., Jablonska-Mestanova V., Galfiova P. & Polak S. 2011c. The thymus: picture review of human thymus prenatal development. Bratisl. Lek. Listy 112 (7): 368–376. PMID: 21744730Suche in Google Scholar

Vasse J. 1983. Transplantation of turtle embryonic thymus into quail embryo: colonization by quail cells. J. Embryol. Exp. Morph. 77: 309–322. PMID: 660669810.1242/dev.77.1.309Suche in Google Scholar

Vigliano F.A., Losada A.P., Castello M., Bermúdez R. & Quiroga M.I. 2011. Morphological and immunohistochemical characterisation of the thymus in juvenile turbot (Psetta maxima L.). Cell Tissue Res. 346 (3): 407–416. 10.1007/s00441011-1282-710.1007/s00441-011-1282-7Suche in Google Scholar

Wakimoto T., Tomisaka R., Nishikawa Y., Sato H., Yoshino T. & Takahashi K. 2008. Identification and characterization of human thymic cortical dendritic macrophages that may act as professional scavengers of apoptotic thymocytes. Immunobiol. 213 (9-10): 837–847. 10.1016/j.imbio.2008.07. 03210.1016/j.imbio.2008.07.032Suche in Google Scholar

Wetherall J. D. & Turner K. J., 1972. Immune response of the lizard, Tiliqua rugose. Aust. J. Exp. Biol. Med. Sci. 50: 79– 95. 10.1038/icb.1972.710.1038/icb.1972.7Suche in Google Scholar

White R.G. 1976. Organization of the lymphoid tissue of Gallus domesticus, pp. 15–29. In: Payne L.N. (ed.), Differential Diagnosis of Avian Lymphoid Leucosis and Marek’s Disease, Commission of the European Communities. Coordination of Agricultural research. Proceedings of a Seminar in the EEC Programme for Coordination of Research on Avian Leukosis held at the Royal Veterinary and Agricultural University of Copenhagen, Copenhagen, Denmark, Directorate-General, Scientific and Technical Information and Information Management, Luxembourg 99 pp.Suche in Google Scholar

Wolke R.E. 1992. Piscine macrophage aggregates: A review. Annu. Rev. Fish Dis. 2: 91–108. 10.1016/0959-8030(92) 90058-610.1016/0959-8030(92)90058-6Suche in Google Scholar

Wong E.S., Papenfuss A.T., Heger A., Hsu A.L., Ponting C.P., Miller R.D., Fenelon J.C., Renfree M.B., Gibbs R.A. & Belov K. 2011. Transcriptomic analysis supports similar functional roles for the two thymuses of the tammar wallaby. BMC Genomics 12: 420. 10.1186/1471-2164-12-42010.1186/1471-2164-12-420Suche in Google Scholar

Yasuda M., Jenne C.N., Kennedy L.J. & Reynolds J.D. 2006. The sheep and cattle Peyer’s patch as a site of B-cell development. Vet. Res. 37 (3): 401–415. 10.1051/vetres:200600810.1051/vetres:2006008Suche in Google Scholar

Zaitseva M., Kawamura T., Loomis R., Goldstein H., Blauvelt A. & Golding H. 2002. Stromal-derived factor 1 expression in the human thymus. J. Immunol. 168 (6): 2609–2617. 10.4049/jimmunol.168.6.260910.4049/jimmunol.168.6.2609Suche in Google Scholar

Zapata A. & Amemiya C.T. 2000. Phylogeny of lower vertebrates and their immunological structures. Curr. Top. Microbial. Immunol. 248: 67–107. 10.1007/978-3-642-59674-2 510.1007/978-3-642-59674-2_5Suche in Google Scholar

Zapata A., Diez B., Cejalvo T., Gutiérrez-de Frías C. & Cortés A. 2006. Ontogeny of the immune system of fish. Fish Shellfish Immunol. 20 (2): 126–136. 10.1016/j.fsi.2004.09.00510.1016/j.fsi.2004.09.005Suche in Google Scholar

Zapata A.G., Torroba M., Vicente A., Varas A., Sacedón R. & Jiménez E. 1995. The relevance of cell microenvironments for the appearance of lympho-haemopoietic tissues in primitive vertebrates. Histol. Histopathol. 10 (3): 761–778. PMID:7579826Suche in Google Scholar

Zapata A., Villena A. & Cooper E.L. 1981a. Ultrastructure of the jugular body of Rana pipiens. Cell Tissue Res. 221 (1): 193–202. 10.1007/BF0021658110.1007/BF00216581Suche in Google Scholar

Zapata A., Villena A., Razquin B. & Cooper E.L. 1981b. The jugular body in anuran amphibians: role in immunity. Dev. Comp. Immunol. 5 (Suppl. 1): 129–135.10.1016/0145-305X(81)90018-5Suche in Google Scholar

Zidan M. & Pabst R. 2010. Histology of hemal nodes of the water buffalo (Bos bubalus). Cell Tissue Res. 340 (3): 491–496. 10.1007/s00441-010-0962-z10.1007/s00441-010-0962-zSuche in Google Scholar PubMed

Received: 2015-9-11
Accepted: 2016-9-19
Published Online: 2016-11-23
Published in Print: 2016-10-1

© 2016 Institute of Zoology, Slovak Academy of Sciences

Artikel in diesem Heft

  1. Section Cellular and Molecular Biology
  2. Pigments from fungi, an opportunity of production for diverse applications
  3. Section Zoology
  4. Morphological view on the evolution of the immunity and lymphoid organs of vertebrates, focused on thymus
  5. Section Cellular and Molecular Biology
  6. p53-Fibrinolytic system and acute lung injury
  7. Section Cellular and Molecular Biology
  8. The multipotent action of electromagnetic field
  9. Section Cellular and Molecular Biology
  10. Prescreening, identification and harvesting of microalgae with antibacterial activity
  11. Section Botany
  12. Cloning and molecular characterization of Myb transcription factors from Leymus (Poaceae: Trticeae)
  13. Section Botany
  14. Hydrological soil behavior in areas with semi-arid vegetation (Beni Chougrane Mountains, Algeria)
  15. Section Botany
  16. Extent and persistence of water repellency in two Iranian soils
  17. Section Botany
  18. The impact of the permanent grass cover or conventional tillage on hydraulic properties of Haplic Cambisol developed on paragneiss substrate
  19. Section Zoology
  20. Species composition of tetranychoid mites (Acari: Trombidiformes: Prostigmata: Tetranychoidea) in main landscapes of Tehran and modelling ecological niche of Tetranychoidea in main climates of Tehran Province, Iran
  21. Section Zoology
  22. Abiotic factors affect the occurrence of different morphological characteristics in Erebia medusa (Lepidoptera: Nymphalidae)
  23. Section Zoology
  24. Comparison of molecular and morphometric analysis in species discrimination of larvae among five cyprinids from the subfamily Leuciscinae: A tool for sustainable conservation of riverine ichthyofauna
  25. Section Zoology
  26. Values of three branched plasma amino acids of farmed rainbow trout, Oncorhynchus mykiss
Heruntergeladen am 8.12.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biolog-2016-0137/html
Button zum nach oben scrollen