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.
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Adamkov M., Furjelová M., Horácek J., Bencat M. & Kružliak P. 2014. Relationship of mismatch repair proteins and survivin in colon polyps and carcinomas. Acta Histochem. 116 (6): 1007–1014. DOI: 10.1016/j.acthis.2014.04.005
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 DOI: 10.12659/MSM.881442
Agius C. & Roberts R. J. 2003. Melano-macrophage centres and their role in fish pathology. J. Fish Dis. 26 (9): 499–509. DOI: 10.1046/j.1365-2761.2003.00485.x
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. DOI: 10.1111/j.0105-2896.2006.00343.x
Alitheen N.B., McClure S. & McCullagh P. 2010. B-cell development: one problem, multiple solutions. Immunol. Cell. Biol. 88 (4): 445–450. DOI: 10.1038/icb.2009.119
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. DOI: 10.1016/j.coi.2007.08. 003
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. DOI: 10.1111/j.1463-6395.1984.tb00805.x
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.
Arstilla T.P., Vainio O. & Lassila O. 1994. Central role of CD4+ T cells in avian immune response. Poultry Sci. 73 (7): 1019–1026. DOI: 10.3382/ps.0731019
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. DOI: 10.1016/j.dci.2014.02.007
Aw D. & Palmer D.B. 2011. The origin and implication of thymic involution. Aging Dis. 2 (5): 437–443. PMID: 22396892
Azzali G. 2003. Structure, lymphatic vascularization and lymphocyte migration in mucosa-associated lymphoid tissue. Immunol. Rev. 195 (1): 178–193. DOI: 10.1034/j.1600-065X.2003.00072.x
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. DOI: 10.1016/j.aanat.2012.07.012
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. DOI: 10.1038/nature09655.
Balogh P. 2011. Introduction: Evolution of peripheral lymphoid organs, Chapter 1, pp. 1-3, DOI: 10.1007/978-3-642-14429-51 In: Balogh P. (ed.), Developmental Biology of Peripheral Lymphoid Organs, Springer-Verlag, Berlin, Heidelberg, 177 pp. ISBN: 978-3-642-14428-8
Balogh P. & Lábadi, A. 2011. Structural evolution of the spleen in man and mouse, Chapter 11, pp. 121–141. DOI: 10.1007/978-3-642-14429-511 In: Balogh P. (ed.), Developmental Biology of Peripheral Lymphoid Organs, Springer-Verlag, Berlin, Heidelberg, 177 pp. ISBN: 978-3-642-14428-8
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. DOI: 10.1002/ar.20917.
Beard J. 1894. The development and probable function of the thymus. Anat. Anz. 9: 476–486.
Berens von Rautenfeld D. & Budras K.D. 1983. Topography, ultrastructure and phagocytic capacity of avian lymph nodes. Cell Tissue Res. 228 (2): 389–403. DOI: 10.1007/BF002048
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. DOI: 10.1159/000141159
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.
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. DOI: 10.1002/aja.1001360406
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: 10904874
Boehm T. 2011. Design principles of adaptive immune system. Nat. Rev. Immunol. 11 (5): 307–317. DOI: 10.1038/nri2944.
Boehm T. & Bleul C.C. 2007. The evolutionary history of lymphoid organs. Nat. Immunol. 8 (2): 131–135. DOI: 10.1038/ni1435
Boehm T., Hess I. & Swann J.B. 2012a. Evolution of lymphoid tissues. Trends Immunol. 33 (6): 315–321. DOI: 10.1016/j.it.2012.02.005.
Boehm T., McCurley N., Sutoh Y., Schorpp M., Kasahara M. & Cooper M.D. 2012b. VLR-based adaptive immunity. Annu. Rev. Immunol. 30: 203–220. DOI: 10.1146/annurev-immunol-020711-075038
Borysenko M. 1976. Phylogeny of immunity: An overview. Immunogenetics 3 (1): 305–326. DOI: 10.1007/BF01576964
Borysenko M. & Cooper E.L. 1972. Lymphoid tissue in the snapping turtle, Chelydra serpentine. J. Morphol. 138 (4): 487–497. DOI: 10.1002/jmor.1051380408
Bowden T.J., Cook P. & Rombout J.H. 2005. Development and function of the thymus in teleosts. Fish Shellfish Immunol. 19 (5): 413–427. DOI: 10.1016/j.fsi.2005.02.003
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. DOI: 10.1002/bies.20528
Bringworth J.F. & Thorn M. 2013. Vertebrate immune system evolution and comparative primate immunity, pp. 17–64. DOI: 10.1007/978-1-4614-7181-32. 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: 978-1-4614-7180-6
Budras K.-D., Hullinger R.L. & Rautenfeld D.B.V. 1987. Lymph heart musculature in birds. J. Morphol. 191 (1): 77–87. DOI: 10.1002/jmor.1051910108
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. DOI: 10.1098/rstb.1927.0001
Butler J.E. & Sinkora M. 2013. The enigma of the lower gutassociated lymphoid tissue (GALT). J. Leukoc. Biol. 94 (2): 259–270. DOI: 10.1189/jlb.0313120
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. DOI: 10.1051/vetres:2006009
Castenholz A. & Castenholz H.E. 1996. Casting methods of scanning electron microscopy applied to hemal lymph nodes in rats. Lymphology 29 (3): 95–105.
Cerutti P. & Guerrero F. 2008. Erythropoiesis and erythrophagocytosis in bovine haemal nodes. Int. J. Morphol. 26 (3): 557–562. DOI: 10.4067/S0717-95022008000300008
Cesta M.F. 2006. Normal structure, function and histology of the spleen. Toxicol. Pathol. 34 (5): 455–465. DOI: 10.1080/01926230600867743
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. DOI: 10.1016/0044-8486(91)90294-H
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. DOI: 10.1016/S0074-7696(08)60882-7
Chilmonczyk K. 1992. The thymus in fish: Development and possible function in the immune response. Annu. Rev. Fish Disease 2: 181–200. DOI: 10.1016/0959-8030(92)90063-4
Chung C.Y., Ysebaert D., Berneman Z.N. & Cools N. 2013. Dendritic cells: cellular mediators for immunological tolerance. Clin. Dev. Immunol. 2013: 8 pp. DOI: 10.1155/2013/972865.
Ciriaco E., Pinera P.P., Diaz-Esnal B. & Laura R. 2003. Agerelated changes in the avian primary lymphoid organs (thymus and bursa of Fabricius). Microsc. Res. Tech. 62 (6): 482–487. DOI: 10.1002/jemt.10416
Cooper E.L. 1982. General Immunology. A Wheaton & Co. Ltd., Exeter, 343 pp. ISBN: 0080263682, 9780080263687
Cooper M.D. & Alder, M.N. 2006. The evolution of adaptive immune systems. Cell 124 (4): 815–822. DOI: 10.1016/j. cell.2006.02.001
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. DOI: 10.1093/icb/15.1.85
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. DOI: 10.1007/BF00306877
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. DOI: 10.1002/jmor.20403
Danilova N. 2006. The evolution of immune mechanisms. J. Exp. Zool. B. Mol. Dev. Evol. 306B (6): 496–520. DOI: 10.1002/jez.b.21102
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. DOI: 10.1016/j.dci.2003.12.003
Dooley J., Erickson M., Gillard G.O. & Farr A.G. 2006. Cervical thymus in the mouse. J. Immunol. 176 (11): 6484–6490. DOI: 10.4049/?jimmunol.176.11.6484
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. DOI: 10.4081/ejh.2011.e37
Dorko F., Horácek J., Tokarcík J. & Miko M. 2013. Cholinesterase activity in quail primary lymphoid organs. Biologia 68 (6): 1238–1242. DOI: 10.2478/s11756-013-0269-0
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. DOI: 10.4081/ejh.2011.e22
Du Pasquier L. 1982. Ontogeny of immunological functions in amphibians, Chapter 18, pp. 633–657. DOI: 10.1007/978-1-4684-4166-618. In: Cohen N. & Sigel M.M. (eds), Phylogeny and Ontogeny, Springer US, 757 pp. ISBN: 978-1-4684-4168-0
Du Pasquier L., Schwager J. & Flajnik M.F. 1989. The immune system of Xenopus. Annu. Rev. Immunol. 7: 251–275. DOI: 10.1146/annurev.iy.07.040189.001343
Duellman W.E. & Trueb L. 1986. Biology of Amphibians. The Johns Hopkins University Press, Maryland, 670 pp. ISBN: 080184780X
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. DOI: 10.1016/j.dci.2010.03.012
Elmore S. 2007. Apoptosis. A review of programmed cell death. Toxicol. Pathol. 35 (4): 495–516. DOI: 10.1080/0192623070 1320337
Ezeasor D.N. & Singh A. 1988. Histology of the caprine hemal node. Acta Anat. 133 (1): 16–23. DOI: 10.1159/000146607
Fänge R. 1977. Size relations of lymphomyeloid organs in some cartilaginous fish. Acta Zool. 58 (3): 125–128. DOI: 10.1111/j.1463-6395.1977.tb00246.x
Fänge R. & Mattisson A. 1981. The lymphomyeloid (hemopoietic) system of the atlantic nurse shark, Gynglymostoma cirratum. Biol. Bull. 160 (2): 240–249.
Fänge R. & Pulsford A. 1983. Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L. Cell Tissue Res. 230 (2): 337–351. DOI: 10.1007/BF002138 08
Fänge R. & Sundell G. 1969. Lymphomyeloid tissues, blood cells and plasma proteins in Chimaera monstrosa (Pisces, Holocephali). Acta Zool. 50 (1-2): 155–168. DOI: 10.1111/j.1463-6395.1969.tb00537.x
Flajnik M.F. & Du Pasquier, L. 2004. Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol. 25 (12): 640–644. DOI: 10.1016/j.it.2004.10.001
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. DOI: 10.1002/jmor.1051730108
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. DOI: 10.1179/ACB.67.3.2062657-
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. DOI: 10.1111/j.1749-6632.2012.06624.x
Glick B. 1979. The avian immune system. Avian Dis. 23 (2): 282–289. DOI: 10.2307/1589557
Glick B., Chang T.S. & Jaap R.G. 1956. The bursa of Fabricius and antibody production. Poultry Sci. 35 (1): 224–225. DOI: 10.3382/ps.0350224
Goldstine S.N., Manickavel V. & Cohen N. 1975. Phylogeny of gut-associated lymphoid tissue. Amer. Zool. 15: 107–118. DOI: 10.1093/icb/15.1.107
Gorgollon P. 1983. Fine structure of the thymus in the adult cling fish Sicyases sanguineus (Pisces, Gobiesocidae). J. Morphol. 177 (1): 25–40. DOI: 10.1002/jmor.1051770103
Grapin-Botton A. & Constam D. 2007. Evolution of the mechanisms and molecular control of endoderm formation. Mech. Dev. 124 (4): 253–278. DOI: 10.1016/j.mod.2007.01.001
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. DOI: 10.1038/nature08068
Hadeiba H. & Butcher E.C. 2013. Thymus-homing dendritic cells in central tolerance. Eur. J. Immunol. 43 (6): 1425–1429. DOI: 10.1002/eji.201243192
Halašová E., Adamkov M., Matáková T., Kavcová E., Poliacek 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: 21147621
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. DOI: 10.4049/jimmunol.172.1.617
Hansen J.D. & Zapata A.G. 1998. Lymphocyte development in fish and amphibians. Immunol. Rev. 166: 199–220. DOI: 10.1111/j.1600-065X.1998.tb01264.x
Hart S., Wrathmell A.B. & Harris J.E. 1986. Ontogeny of gutassociated lymphoid tissue (GALT) in the dogfish Scyliorhinus canicula L. Vet. Immunol. Immunopathol. 12 (1-4): 107–116. DOI: 10.1016/0165-2427(86)90115-7
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 DOI: 10.1242/jeb.106906
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: 7430931
Herrin B.R. & Cooper M.D. 2010. Alternative adaptive immunity in jawless vertebrates. J. Immunol. 185 (3): 1367–1374. DOI: 10.4049/jimmunol.0903128
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.
Ishizuya-Oka A., Hasebe T. & Shi Y.-B. 2010. Apoptosis in amphibian organs during metamorphosis. Apoptosis 15 (3): 350–364. DOI: 10.1007/s10495-009-0422-y.
Jablonska-Mestanova V., Sisovsky V., Danisovic L., Polak S. & Varga I. 2013. The normal human newborns thymus. Bratisl. Lek. Listy 114 (7): 402–408. DOI: 10.4149/BLL 2013 086
John J.L. 1994. The avian spleen: A neglected organ. Q. Rev. Biol. 69 (3): 327–351. DOI: 10.1086/418649
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. DOI: 10.1002/jmor.1051390405
Jolly J. 1913. Sur les organs lympho-epitheliaux. Comp. Rend. Hebdom. Seanc. Mem. Soc. Biol. A65, 74 (T1): 540–543.
Jordan R.K. 1976. Development of sheep thymus in relation to utero thymectomy experiments. Eur. J. Immunol. 6 (10): 693–698. DOI: 10.1002/eji.1830061007
Joss J.M.P. 1998. Are lungfish neotenic? Clin. Exp. Pharmacol. Physiol. 25 (9): 733–735. DOI: 10.1111/j.1440-1681.1998.tb02286.x
Junt T., Scandella E. & Ludewig B. 2008. Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat. Rev. Immunol. 8 (10): 764–775. DOI: 10.1038/nri2414
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. DOI: 10.1007/s00276-008-0357-y
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. DOI: 10.1186/s40781-015-0064-2
Katagiri Ch. 1978. Xenopus laevis as a model for the study of immunology. Dev. Comp. Immunol. 2 (1): 5–13. DOI: 10.1016/S0145-305X(78)80020-2
Kendall M.D. 1980. Avian thymus glands: a review. Dev. Comp. Immunol. 4: 191–209. DOI: 10.1016/S0145-305X(80)80023-1
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 Lymph-gefasssystem der Ente. Folia Anat. Jap. 11 (5): 405–413.
Koch G. 1991. The immune system in poultry. Tijdschr. Diergeneeskde. 116 (14): 728–734.
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.
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. DOI: 10.1073/pnas.1320319111.
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. DOI: 10.1111/j.1469-7580.2010.01305.x
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. DOI 10.1007/s11064-012-0752-y
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: 8809465
Liu Z. & Casley-Smith J.R. 1989. The fine structure of the amphibian lymph heart. Lymphology 22 (1): 25–30. PMID:2725054
Lofts B. 2012. Physiology of the Amphibian. Vol. 3. Academic Press, INC, New York, 658 pp. ISBN: 0-12-455403-2
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. DOI: 10.1002/jez.1402730408
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. DOI: 10.1016/j.ygcen. 2007.03.011
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. DOI: 10.2741/3866
Manning M. J. 1979. Evolution of the vertebrate immune system. J. R. Soc. Med 72 (9): 683–688. DOI: 10.1177/014107687907200911
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: 5361557
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.
Mattisson A. & Fänge R. 1982. The cellular structure of the Leydig organ in the shark, Etmopterus spinax (L.). Biol. Bull. 162 (2): 182–194. DOI: 10.2307/1540813
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. DOI: 10.1111/j.1463-6395.1990.tb01074.x
Mayer S. 1888. Zur lehre von der Schilddrüse und thymus bei Amphibien. Anat. Anz. 3: 97–103.
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. DOI: 10.1111/j.1469-7580.2007.00814.x
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: 19114982
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. DOI: 10.1038/nri2588
Muthukkaruppan V.R., Borysenko M. & El Ridi R. 1982. RES Structure and function of thse Reptilia, Chapter 12, pp. 461–508. DOI: 10.1007/978-1-4684-4166-612. In: Cohen N. & Sigel N.N. (eds), The Reticuloeptelial System. A Comprehensive Treatise, Plenum Press, New York, 757 pp. ISBN: 978-1-4684-4168-0
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 a rearrangement in cortical thymocytes. Proc. Natl. Acad. Sci. USA. 109 (50): 20572–20577. DOI: 10.1073/pnas.1213069109
Nakamura H. & Ayer-Le Licvre C. 1986. Neural crest and thymic myoid cells. Curr. Top. Dev. Biol. 20: 111–115. DOI: 10.1016/S0070-2153(08)60658-4
Nelsen O.E. 1953. Comparative embryology of the vertebrates. McGraw-Hill Book Company, INC. New York, 982 pp. DOI: 10.5962/bhl.title.6451
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. DOI: 10.1078/0065-1281-00581
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. DOI: 10.1148/rg.2620 45213
Oguri M. 1983. On the Leydig organ in the esophagus of some elasmobranchs. Bull. Jap. Soc. Sci. Fish. 49 (7): 989–991. DOI: http://doi.org/10.2331/suisan.49.989
Ohno H. 2016. Intestinal M cells. J. Biochem. 159 (2): 151–160. DOI: 10.1093/jb/mvv121
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. DOI: 10.1002/ar.1092080212
Osório J. & Rétaux S. 2008. The lamprey in evolutionary studies. Dev. Genes Evol. 218 (5): 221–235. DOI: 10.1007/s00427-008-0208-1
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. DOI: 10.1016/S0165-5728(96)00146-4
Øverg°ard 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. DOI: 10.1016/j.dci.2010.09.009
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. DOI: 10.2174/138161208783413310
Page M. & Rowley A.F. 1982. A morphological study of pharyngeal lymphoid accumulations in larval lampreys. Dev. Comp. Immunol. Suppl 2: 35–40.
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. DOI: 10.1038/sj.cdd.4401611
Patel S., Sørhus E., Fiksdal I.U., Espedal P.G., Bergh O., 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. DOI: 10.1016/j.fsi.2008.11.018
Payne A.P. 1994. The Harderian gland: a tercentennial review. J. Anat. 185 (Pt 1): 1–49. PMID: 7559104
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. DOI: 10.1016/j.fsi.2009.04.003
Pospíšilová V., Slípka J. & Cerný 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, Plzen, 10.-12.9.2002. Plzen Lék. Sbor. 78 (Suppl 1): 23–28.
Prymak T. 1902. Beiträge zur Kenntniss des feinen Baues und der Involution der Thymusdrüse bei den Teleostieren. Anat. Anz. 21: 164.
Raica M., Cîmpean A.M., Encică S. & Cornea R. 2007. Involution of the thymus: a possible diagnostic pitfall. Rom. J. Morphol. Embryol. 48 (2): 101–106.
Raica M., Encică 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. DOI: 10.1016/j.aanat. 2006.01.012
Ratcliffe M.J. 2002. B cell development in gut associated lymphoid tissues. Vet. Immunol. Immunopathol. 87 (3-4): 337–440. PMID: 12072255
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. DOI: 10.1016/j.dci.2005.06.018
Reboldi A. & Cyster J.G. 2016. Peyer’s patches: organizing B-cell responses at the intestinal frontier. Immunol. Rev. 271 (1): 230–245 DOI: 10.1111/imr.12400.
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. DOI: 10.1155/2013/352414
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. DOI: 10.1016/j.proghi.2008.03.001
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. DOI: 10.1007/s11357-013-9564-5
Rodewald H. R. 2008. Thymus organogenesis. Annu. Rev. Immunol. 26: 355–388. DOI: 10.1146/annurev.immunol.26. 021607.090408
Rodríguez R.M., López-Vázquez A. & López-Larrea C. 2012. Immune systems evolution. Adv. Exp. Med. Biol. 739: 237–251. DOI: 10.1007/978-1-4614-1704-0 15.
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. DOI: 10.1155/1992/26251
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. DOI: 10.1046/j.1469-7580.1999.19410039.x
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. DOI: 10.1016/S0145-305X(98)00053-6
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. DOI: 10.1159/000211193.
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. DOI: 10.1046/j.1365-3083.2002.01116.x
Saha N.R., Smith J. & Amemiya C.T. 2010. Evolution of adaptive immune recognition in jawless vertebrates. Semin. Immunol. 22 (1): 25–33. DOI: 10.1016/j.smim.2009.12.002
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. DOI: 10.1016/j.imbio. 2013.06.009
Scott T.R. 2004. Our current understanding of humoral immunity of poultry. Poultry Sci. 83 (4): 574–579. DOI: 10.1093/ps/83.4.574
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. DOI: 10.1016/S0145-305X(98)00030-5
Seto F. 1981. Early development of the avian immune system. Poultry Sci. 60 (9): 1981–1995. DOI: 10.3382/ps.0601981
Sharma J.M. 1997. The structure and function of the avian immune system. Acta Vet. Hung. 45 (3): 229–238. PMID: 9276985
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: 3-923022-20-4
Sima P. & Vetvicka V. 1993. Evolution of immune reactions. Crit. Rev. Immunol. 13 (2): 83–114. PMID: 8352910
Slípka J. 1986. Evolutionary morphology of the branchial region as the reflection of environmental changes, pp. 203–211. In: Novák V.J.A., Vancata V. & Vancatová M.A. (eds), Behaviour, Adaptation and Evolution, Czechoslovak Academy of Sciences, Praha.
Slipka J. & Slipka J.Jr. 1996. The palatine tonsil as an evolutionary novelty. Acta Otolaryngol. Suppl. 523: 8–11. PMID: 9082817
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. DOI: 10.1007/s00442-003-1409-y
Spalding H. & Heath T. 1987. Pathways of lymph flow through superficial inguinal lymph nodes in the pig. Anat. Rec. 217 (2): 188–195. DOI: 10.1002/ar.1092170211
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: 0-521-26032-9
Štěrba G. 1953. Die Physiologie und Histogenese der Schilddrüse 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.
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. DOI: 10.1126/science. 1123497
Tischendorf F. 1985. On the evolution of the spleen. Experientia 41 (2): 145–152. PMID: 3972062
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.
Valančiūtė A., Mozuraitė R., Balnytė I., Didžiapetrienė J., Matusevicius 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. DOI: 10.1016/j.etp.2015.04.005
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. DOI: 10.1242/dev.004697
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. DOI: 10.1038/nri2832
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. DOI: 10.1002/jemt.10411
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.
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: 19855349
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: 21905416
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: 19112385
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: 21125801
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: 21744730
Vasse J. 1983. Transplantation of turtle embryonic thymus into quail embryo: colonization by quail cells. J. Embryol. Exp. Morph. 77: 309–322. PMID: 6606698
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. DOI: 10.1007/s00441-011-1282-7
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. DOI: 10.1016/j.imbio.2008.07. 032
Wetherall J. D. & Turner K. J., 1972. Immune response of the lizard, Tiliqua rugose. Aust. J. Exp. Biol. Med. Sci. 50: 79–95. DOI: 10.1038/icb.1972.7
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.
Wolke R.E. 1992. Piscine macrophage aggregates: A review. Annu. Rev. Fish Dis. 2: 91–108. DOI: 10.1016/0959-8030(92) 90058-6
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. DOI: 10.1186/1471-2164-12-420
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. DOI: 10.1051/vetres:2006008
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. DOI: 10.4049/jimmunol.168.6.2609
Zapata A. & Amemiya C.T. 2000. Phylogeny of lower vertebrates and their immunological structures. Curr. Top. Microbial. Immunol. 248: 67–107. DOI: 10.1007/978-3-642-59674-25
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. DOI: 10.1016/j.fsi.2004.09.005
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:7579826
Zapata A., Villena A. & Cooper E.L. 1981a. Ultrastructure of the jugular body of Rana pipiens. Cell Tissue Res. 221 (1): 193–202. DOI: 10.1007/BF00216581
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.
Zidan M. & Pabst R. 2010. Histology of hemal nodes of the water buffalo (Bos bubalus). Cell Tissue Res. 340 (3): 491–496. DOI: 10.1007/s00441-010-0962-z
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Mešťanová, V., Varga, I. Morphological view on the evolution of the immunity and lymphoid organs of vertebrates, focused on thymus. Biologia 71, 1080–1097 (2016). https://doi.org/10.1515/biolog-2016-0137
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DOI: https://doi.org/10.1515/biolog-2016-0137