Prenatal morphogenesis of compartments of the parenchyma of the lymph nodes of domestic cattle (Bos taurus)

Keywords: lymphoid tissue; deep cortex units; interfollicular cortex; lymphatic nodules; lymphatic sinuses; paracortical and medullaru cords

Abstract

The article analyzes the regularities of the formation and development of the lymphoid lobules of the parenchyma of the somatic (Limphonodi cervicales superficiales) and visceral (L. jejunales) lymph nodes in domestic cattle in the fetal period of ontogenesis. We used routine histological techniques and author's modification of the impregnation of total median sections with silver nitrate. Visualization of various zones of lymphoid lobules was carried out taking into account the specific for different cell zones architectonics of reticular fibers. It has been established that signs of morphological heterogeneity of parenchyma of lymph nodes are first found in three month-old fetuses, which is associated with the concentration of lymphoid tissue along the marginal sinus. Separation of lymphoid lobules and their structural and functional differentiation are first detected in five month fetuses. In the lymphoid lobules of five month-old fetuses all structural and functional cell zones are observable, among which the regions of clonal proliferation of T and B lymphocytes are the least developed, and regions of the transit corridors for lymphocytes migrating medullary and the cords (zone of potential accumulation of plasmocytes and antibody formation) are the most developed. Structural and functional transformations of compartments in the prenatal period of ontogenesis are accompanied by a predominantly moderate increase of the relative volume of specialized T- and B-dependent zones of lobules, against a background of a gradual decrease of the volume of transit corridors for lymphocytes migrating and zone of potential accumulation of plasmocytes and antibody formation. Due to the small volume and relatively low rates of development of the lymphocytes clonal proliferation zones, the quantitative ratios of the cellular zones in lymphoid lobules of the lymph nodes of domestic cattle in prenatal ontogenesis remain relatively stable, while maintaining the maximum indices of the development of transit corridors for lymphocytes migration and medullary cords. Among the zones of lymphocytes clonal proliferation throughout the fetal period, T-dependent zones predominate, the relative volume of which is 5.0–7.5 times greater than the volume of B-dependent zones. Lymphoid lobules in the lymph nodes of the domestic cattle fetuses of all age groups are arranged along the marginal sinus in one row and have a polar structure due to the formation of lymph nodes at one pole of the lobules in the interfollicular zone. In the visceral lymph nodes (L. jejunum) of 8–9 month-old fetuses, individual lymph nodes can form in paracortical strands, on the border with the interfollicular zone.

References

Ager, A. (2017). High endothelial venules and other blood vessels: Critical regulators of lymphoid organ development and function. Frontiers in Immunology, 8(3), 1–16.


Avtandilov, G. G. (1990). Meditsinskaya morfometrya [Medical morphometry]. Medicine, Moscow (in Russian).


Bélisle, C., & Sainte-Marie, G. (1981). Tridimensional study of the deep cortex of the rat lymph node. III. Morphology of the deep cortex units. The Anatomical Record, 199(2), 213–226.


Benezech, C., White, A., Mader, E., Serre, K., Parnell, S., Pfeffer, K., Ware, C. F., Anderson, G., & Caamano, J. H. (2010). Ontogeny of stromal organizer cells during lymph node development. The Journal of Immunology, 184(8), 4521–4530.


Butler, J., Sawtell, A., Jarrett, S., Cosgrove, J., Leigh, R., Timmis, J., & Coles, M. (2016). Imaging immunity in lymph nodes: Past, present and future. Advances in Experimental Medicine and Biology, 915, 329–346.


Capece, T., & Kim, M. (2016). The role of lymphatic niches in T cell differentiation. Molecules and Cells, 39(7), 515–523.


Chuchkova, N. N., Smetanina, M. V., Kormilina, N. V., & Komissarov, V. B. (2016). Morfogenez limfaticheskih uzlov v uslovijah hronicheskogo systemnogo vospalenija [The morphogenesis of lymph nodes in conditions of chronic systemic inflammation]. Morfologija, 149(3), 230–231 (in Russian).


De Bruyn, P. P. H., & Cho, Y. (1990). Structure and function of high endothelial postcapillary venules in lymphocyte circulation. In: Grundmann, E., & Vollmer, E. (Eds.). Reaction patterns of the lymph node. Current Topics in Pathology, 84(1). Springer, Berlin, Heidelberg. pp. 85–101.


Ekman, A., & Iivanainen, A. (2009). Generation of B cells in bovine fetuses. Veterinary Immunology and Immunopathology, 128(1–3), 268.


Emelyanenko, P. A. (1987). Immunologia zhivotnych v period vnytriutrobnogo razvitia [Immunology of animals in the period of intrauterine development]. Agropromizdat, Moscow (in Russian).


Gavrilin, P. N. (1999). Modificatsiya sposoba impregnatsii serebrom po Futy gistotopogramm organov krovetvoreniya, izgotovlennyih na microtome-kriostate [Modification of the silver impregnation method according to Fut histotopograms of hemopoietic organs made on a microtome cryostat]. Vestnik Morphologii, 5(1), 106–108 (in Russian).


Gavrilin, P. N., Gavrilina, О. G., & Kravtsovа, M. V. (2017a). The compartments of the parenchyma of the lymph nodes in the newborn bull calves of domestic cattle (Bos taurus). Regulatory Mechanisms in Biosystems, 8(2), 169–178.


Gavrilin, P. N., Gavrilina, O. G., Brygadyrenko, V. V., & Rahmoun, D. E. (2017b). Structural and functional units of parenchyma of lymph nodes of dromedaries (Camelus dromedarius). Regulatory Mechanisms in Biosystems, 8(3), 323–332.


Gavrilin, P., Gavrilina, E., & Evert, V. (2017c). Histoarchitectonics of the parenchyma of lymph nodes of mammals with different structure of intranodal lymphatic channel. Ukrainian Journal of Ecology, 7(3), 96–107.


Gavrilin, P. N., Masjuk, M. O., & Tishkina, N. N. (2014). Osoblivosti makrosko pichnoi strukturi limfatichnih vuzliv svini sviyskoi [Features of macroscopic structure of lymph nodes of the domestic pig]. Science and Technology Bulletin of SRC for Biosafety and Environmental Control of AIC, 2(1), 32–37 (in Ukrainian).


Gretz, J. E., Anderson, C. C., & Shaw, S. (1997). Cords, channels, corridors and conduits, critical architectural facilitating cell interactions in the lymph node cortex. Immunological Reviews, 156, 11–24.


Grigor'ev, V. S., & Moljanova, G. V. (2009). Organogenez central'nyh i perifericheskih organov immunnoj sistemy u sel'skohozjajstvennyh zhivotnyh [Organogenesis of central and peripheral bodies of the immune system in agricultural animals]. RIC SGSHA, Samara (in Russian).


Hlystova, Z. S. (1987). Stanovlenie sistemy immunogeneza ploda cheloveka [Formation of the system of human fetal immunogenesis]. Medicine, Moscow (in Russian).


Houston, S. A., Cerovic, V., Thomson, C., Brewer, J., Mowat, A. M., & Milling, S. (2016). The lymph nodes draining the small intestine and colon are anatomically separate and immunologically distinct. Mucosal Immunology. 9(2), 468–478.


Hoshi, N., Hashimoto, Y., Kitagawa, H., Kon, Y., & Kudo, N. (1986). Histological and immunohistochemical studies on the architecture of lymph nodes in pig. Japan Journal Veterinary Science, 48(6), 1097–1107.


Ikomi, F., Kawai, Y., & Ohhashi, T. (2012). Recent advance in lymph dynamic analysis in lymphatics and lymph nodes. Annals of Vascular Diseases, 5(3), 258–268.


Iwasaki, R., Mori, T., Ito, Y., Kawabe, M., Murakmi, M., & Maruo, K. (2016). Computed tomographic evaluation of presumptively normal canine sternal lymph nodes. Journal of the American Animal Hospital Association, 52(6), 371–377.


Jeklova, E., Leva, L., & Faldyna, M. (2007). Lymphoid organ development in rabbits: Major lymphocyte subsets. Developmental and Comparative Immunology, 31(6), 632–644.


Jia, L., Xie, Z., Zheng, J., Liu, L., He, Y., Liu, F., & He, Y. (2012). Morphological studies of lymphatic labyrinths in the rat mesenteric lymph node. The Anatomical Record, 295, 1291–1301.


Kaldjian, E. P., Gretz, J. E., Anderson, A. O., Shi, Y., & Shaw, S. (2001). Spatial and molecular organization of lymph node T cell cortex: A labyrinthine cavity bounded by an epithelium-like monolayer of fibroblastic reticular cells anchored to basement membrane-like extracellular matrix. International Immunology, 13(10), 1243–1253.


Katakai, T. (2004). A novel reticular stromal structure in lymph node cortex: An immuno-platform for interactions among dendritic cells, T cells and B cells. International Immunology, 16(8), 1133–1142.


Katakai, T., Hara, T., Sugai, M., Gonda, H., & Shimizu, A. (2004). Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. The Journal of Experimental Medicine, 200(6), 783–795.


Kelly, R. H. (1975). Functional anatomy of lymph nodes. International Archives of Allergy and Immunology, 48(6), 836–849.


Konenkov, V. I., Shkyrat, G. A., & Kolesnikov, A. P. (2008). Limfaticheksij uzel: Morfofunkcional’naja harakteristika i mezhkletochnaja kooperacija [Lymph node: Morphofunctional characteristic and intercellular cooperation]. Vestnik Limfologii, 4, 35–43 (in Russian).


Kowala, M. C., & Schoefi, G. I. (1986). The popliteal lymph node of the mouse: Internal architecture, vascular distribution and lymphatic supply. Journal of Anatomy, 148(1), 25–46.


Lipscomb, M. F., & Masten, B. J. (2002). Dendritic cells: Immune regulators in health and disease. Physiological Reviews, 82(1), 97–130.


Margaris, K. N., & Black, R. A. (2012). Modelling the lymphatic system: Challenges and opportunities. Journal of the Royal Society Interface, 9(69), 601–612.


Mebius, R. E. (2003). Erratum: Organogenesis of lymphoid tissues. Nature Reviews Immunology, 3(4), 292–303.


Nicander, L., Nafstad, P., Landsverk, T., & Engebretsen, R. H. (1991). A study of modified lymphatics in the deep cortex of ruminant lymph nodes. Journal of Anatomy, 178, 203–212.


Nishikawa, S.-I., Honda, K., Vieira, P., & Yoshida, H. (2003). Organogenesis of peripheral lymphoid organs. Immunological Reviews, 195(1), 72–80.


Nurken, M., & Marzhan, M. (2016). The movement of lymph in the system of lymph node-lymph vessel and its regulation. Australasian Medical Journal, 9(10).


Ohtani, O., & Ohtani, Y. (2008). Structure and function of rat lymph nodes. Archives of Histology and Cytology, 71(2), 69–76.


Olson, M. R., McDermott, D. S., & Varga, S. M. (2012). The initial draining lymph node primes the bulk of the CD8 T cell response and influences memory T cell trafficking after a systemic viral infection. PLOS Pathogens, 8(12), 1–15.


Palm, A.-K. E., Friedrich, H. C., & Kleinau, S. (2016). Nodal marginal zone B cells in mice: A novel subset with dormant self-reactivity. Scientific Reports, 6(1).


Parker, G. A., & Makori, N. (2017). Development of immune system organs. Reference Module in Biomedical Sciences, 11, 49–73.


Platt, A. M., & Randolph, G. J. (2013). Dendritic cell migration through the lymphatic vasculature to lymph nodes. Advances in Immunology, 120, 51–68.


Randall, T. D., Carragher, D. M., & Rangel-Moreno, J. (2008). Development of secondary lymphoid organs. Annual Review of Immunology, 26(1), 627–650.


Rjabchikov, O. P., Kalinina, I. I., Shmeleva, S. P., Hlystova, Z. S., Minina, T. A., & Rabotnikova, E. L. (2002). Karta zaselenija organov immunnoj sistemy jembriona i ploda cheloveka T- i B-limfocitami i nachalo jendokrinnoj funkcii timusa [Map of the population of the organs of the immune system of the embryo and fetus of human T- and B-lymphocytes and the beginning of the endocrine function of the thymus]. Immunologija, 2, 80–82 (in Russian).


Ruddle, N. H. (2016). High endothelial venules and lymphatic vessels in tertiary lymphoid organs: Characteristics, functions, and regulation. Frontiers in Immunology, 9(7), 1–7.


Rouse, R. V., Reichert, R. A., Gallatin, W. M., Weissman, I. L., & Bucher, E. C. (1984). Localization of lymphocyte subpopulation in peripheral lymphoid organs: Directed lymphocyte migration and segregation into specific microenvironments. American Journal of Anatomy, 170, 391–405.


Sainte-Marie, G. (2010). The lymph node revisited: Development, morphology, functioning, and role in triggering primary immune responses. The Anatomical Record, 293(2), 32–37.


Sapin, M. R., Jurina, N. A., & Etingen, L. (1978). Limfaticheskij uzel [Lymph node]. Medicine, Moscow (in Russian).


Sapin, M. R. (2006). Osobennosti imunnogo otveta pri razlichnych vnechnich vozdeistviyah [Features of the immune response under various external influences]. Morphology, 129(4), 109–110 (in Russian).


Sinkora, J., Rehakova, Z., Sinkora, M., Cukrowska, B., & Tlaskalova-Hogenova, H. (2002). Early development of immune system in pigs. Veterinary Immunology and Immunopathology, 87(3–4), 301–306.


Šinkora, M., & Butler, J. E. (2009). The ontogeny of the porcine immune system. Developmental and Comparative Immunology, 33(3), 273–283.


Sixt, M., Kanazawa, N., Selg, M., Samson, T., Roos, G., Reinhardt, D. P., Pabst, R., Lutz, M. B., & Sorokin, L. (2005). The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity, 22(1), 19–29.


Sminia, T., Van Rees, E. P., Döpp, E. A., & Dijkstra, C. D. (1986). Ontogeny of the popliteal lymph node in the rat. Developmental and Comparative Immunology, 10(1), 119.


Studencov, A. P., Shipilov, V. S., Nikitin, V. J., Miroljubov, M. G., Subbotina, L. G., Preobrazhenskij, O. N., & Hromcov, V. V. (1999). Veterinarnoe akusherstvo, ginekologija i biotehnika razmnozhenija [Veterinary obstetrics, gynecology and biotechnics of reproduction]. Kolos, Moscow (in Russian).


Von Andrian, U. H., & Mempel, T. R. (2003). Homing and cellular traffic in lymph nodes. Nature Reviews Immunology, 3(11), 867–878.


Vyrenkov, Y. E., Shishlo, V. K., Antropova, J. G., & Ryzhova, A. V. (1995). Sovremennye dannye o strukturno-funkcional'noj organizacii limfaticheskogo uzla [Modern data on the structural and functional organization of the lymph node]. Morphology, 103(3), 34–40 (in Russian).


Willard-Mack, C. L. (2006). Normal structure, function, and histology of lymph nodes. Toxicologic Pathology, 34(5), 409–424.


Zelenevsky, N. V. (2013). Mezhdunarodnaja veterinarnaja anatomicheskaja nomenklatura na latinskom i russkom jazykah. Nomina Anatomica Veterinaria [International veterinary anatomical nomenclature in Latin and Russian. Nomina Anatomica Veterinaria]. Mir, Sankt-Peterburg (in Russian).

Published
2018-02-15
How to Cite
Gavrilin, P. N., Lieshchova, M. A., Gavrilina, O. G., & Boldyreva, T. F. (2018). Prenatal morphogenesis of compartments of the parenchyma of the lymph nodes of domestic cattle (Bos taurus). Regulatory Mechanisms in Biosystems, 9(1), 95-104. https://doi.org/10.15421/021814

Most read articles by the same author(s)

> >>