Abstract
Little is known about lymphoid organ development in yaks. In this study, we characterize and evaluate the main markers of T cell, B cell, plasma cell and antigen-presenting cell in the mesenteric lymph nodes, spleen and hemal node in newborn, juvenile and adult yaks by immunohistochemistry, real-time quantitative polymerase chain reaction and western blotting. The structures of all organs were not fully developed in newborn. The CD3+ cells were mainly located in the paracortex area of the mesenteric lymph node and the T cell dependent area in the hemal node and spleen. CD79a+ cells were mainly detected in the lymphoid follicles. The expression of CD3 and CD79a increased from newborn to juvenile and then decreased in adults. The expression of CD3 was always higher in the spleen and CD79a was higher in the mesenteric lymph node. IgG+ and IgA+ cells were observed in all examined samples, except in newborn yak hemal node. IgG and IgA were up-regulated with age and the highest expression was observed in the mesenteric lymph node. The SIRPα and CD68 were widely expressed. A significant feature was that the SIRPα expression in the spleen was lowest in newborns but highest in juvenile and adult yaks. The expression of CD68 in the hemal node was highest in all groups and increased from newborn to adult yaks. This study sheds light on the relationship between the morphology and function of these organs and provides useful references for normal yak lymphoid organ development.
Similar content being viewed by others
References
Ackermann MR, Debey BM, Stabel TJ, Gold JH, Register KB, Meehan JT (1994) Distribution of anti-CD68 (EBM11) immunoreactivity in formalin-fixed, paraffin-embedded bovine tissues. Vet Pathol 31(3):340–348
Barclay AN, Van den Berg TK (2014) The interaction between signal regulatory protein alpha (SIRPα) and CD47: structure, function, and therapeutic target. Annu Rev Immunol 32(1):25–50
Bozkurt YA, Kuş S, Kozlu T, Başak F (2014) Histological and immunohistochemical studies of the structure of lymph nodes in Kilis goats. Biotech Histochem 89(6):440–445
Casteleyn CR, Breugelmans S, Simoens P, de Van BW (2008) Morphological and immunological characteristics of the bovine temporal lymph node and hemal node. Vet Immunol Immunopathol 126(3–4):339–350
Cerutti P, Guerrero F (2008) Erythropoiesis and erythrophagocytosis in bovine haemal nodes. Int J Morphol 26:557–562
Cesta M (2006) Normal structure, function, and histology of the spleen. Toxicol Pathol 34(5):455–465
Chattha KS, Firth MA, Hodgins DC, Shewen PE (2009) Age related variation in expression of CD21 and CD32 on bovine lymphocytes: a cross-sectional study. Vet Immunol Immunopathol 130(1–2):70–78
Chattha KS, Firth MA, Hodgins DC, Shewen PE (2010) Variation in expression of membrane IgM, CD21 (CR2) and CD32 (Fcgamma RIIB) on bovine lymphocytes with age: a longitudinal study. Dev Comp Immunol 34(5):510–517
Ezeasor DN, Singh A (1988) Histology of the caprine hemal node. Acta Anat (Basel) 133(1):16–23
Ezeasor DN, Singh A, Sims DE (1989) Erythrophagocytosis in the caprine hemal node. Acta Anat (Basel) 134(4):341–345
Faldyna M, Sinkora J, Knotigova P, Leva L, Toman M (2005) Lymphatic organ development in dogs: major lymphocyte subsets and activity. Vet Immunol Immunopathol 104(3–4):239–247
Galeotti M, Sarli G, Eleni C, Marcato PS (1993) Identification of cell types present in bovine hemolymph nodes and lymph nodes by immunostaining. Vet Immunol Immunopathol 36(4):319–331
Gao J, Liu M, Meng X, Han Z, Zhang D, Hou B, Zhang K, SIzhu S, Li J (2013) Seroprevalence of bovine viral diarrhea infection in yaks (Bos grunniens) on the Qinghai-Tibetan Plateau of China. Trop Anim Health Prod 45(3):791–793
Gough PJ, Gordon S, Greaves DR (2001) The use of human CD68 transcriptional regulatory sequences to direct high-level expression of class A scavenger receptor in macrophages in vitro and in vivo. Immunology. 103(3):351–361
Grossmann A, Maggio-Price L, Jinneman JC, Rabinovith PS (1991) Influence of aging on intracellular free calcium and proliferation of mouse T-cell subsets from various lymphoid organs. Cell Immunol 135(1):118–131
Huang Y, Cui Y, Yu S, He J, He Y, Zhang Q, Liu P, Sun J, Pu Y, Kang X (2019) Comparison of histological characteristics and expression of CD3 and CD79a among the hemal nodes, lymph nodes and spleens of yaks (Bos grunniens). Histol Histopathol 34:241–256
Jeklova E, Leva L, Faldyna M (2007) Lymphoid organ development in rabbits: major lymphocyte subsets. Dev Comp Immunol 31(6):632–644
Joling P, Bianchi AT, Kappe AL, Zwart RJ (1994) Distribution of lymphocyte subpopulations in thymus, spleen, and peripheral blood of specific pathogen free pigs from 1 to 40 weeks of age. Vet Immunol Immunopathol 40(2):105–117
Kampen AH, Olsen I, Tollersrud T, Storset AK, Lund A (2006) Lymphocyte subpopulations and neutrophil function in calves during the first 6 months of life. Vet Immunol Immunopathol 113(1–2):53–63
Kohyama M, Ise W, Edelson BT, Wilker PR, Hildner K, Mejia C, Frazier WA, Murphy TL, Murphy KM (2009) Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457(7227):318–321
Luscieti P, Hubschmid T, Cottier H, Hess MW, Sobin LH (1980) Human lymph node morphology as a function of age and site. J Clin Pathol 33(5):454–461
Mcwilliams M, Phillipsquagliata JM, Lamm ME (1977) Mesenteric lymph node B lymphoblasts which home to the small intestine are precommitted to IgA synthesis. J Exp Med 145(4):866–875
Miller RA (1997) Age-related changes in T cell surface markers: a longitudinal analysis in genetically heterogeneous mice. Mech Ageing Dev 96(1–3):181–196
Ogembo JG, Milner DA, Mansfield KG, Rodig SJ, Murphy GF, Kutok JL, Pinlus GS, Fingeroth JD (2012) SIRPα/CD172a and FHOD1 are unique markers of littoral cells, a recently evolved major cell population of red pulp of human spleen. J Immunol 188(9):4496–4505
Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP (2000) Role of CD47 as a marker of self on red blood cells. Science 288(5473):2051–2054
Oruc E, Kara A, Can I (2012) Caspase-3 and CD68 immunoreactivity in lymphoid tissues and haematology of rats exposed to cisplatin and L-carnitine. Kafkas Universitesi Veteriner Fakultesi Dergisi 18(5):871–878
Pawelec G, Barnett Y, Forsey R, Frasca D, Globerson A, McLeod J, Caruso C, Franceschi C, Fülöp T, Gupta S, Mariani E, Mocchegiani E, Solana R (2002) T cells and aging, January 2002 update. Front Biosci 7:d1056–d1083
Piguet PF, Irle C, Vassalli P (2010) Immunosuppressor cells from newborn mouse spleen are macrophages differentiating in vitro from monoblastic precursors. Eur J Immunol 11(1):56–61
Raj GD, Mathivanan B, Matheswaran K, Nachimuthu K, Davis WC (2007) Lymphocyte subset distribution in apparently normal and single intradermal test-positive water buffaloes analyzed by flow cytometry. Res Vet Sci 82(1):0–38
Ruddle NH, Akirav EM (2009) Secondary lymphoid organs: responding to genetic and environmental cues in ontogeny and the immune response. J Immunol 183(4):2205–2212
Sun J, Xu Y, Cui Y, Liu P, Yu S, He J, Zhang Q, Huang Y, Yang X (2018) Age-related changes in the morphology and the distribution of IgA and IgG in the palatine tonsils of yaks (Bos grunniens). Histol Histopathol 33(6):577–588
Tanaka T, Ichimura K, Sato Y, Takata K, Morito T, Tamura M, Kondo E, Ohara N, Yanai H, Sakai M, Takahashi S, Yoshino T (2009) Frequent downregulation or loss of CD79a expression in plasma cell myelomas: potential clue for diagnosis. Pathol Int 59:804–808
Taub DD, Longo DL (2010) Insights into thymic aging and regeneration. Immunol Rev 205:72–93
Thorp BH, Seneque S, Staute K, Kimpton WG (1991) Characterization and distribution of lymphocyte subsets in sheep hemal nodes. Dev Comp Immunol 15(4):393–400
Uhde AK, Lehmbecker A, Baumgärtner W, Spitzbarth I (2017) Evaluation of a panel of antibodies for the immunohistochemical identification of immune cells in paraffin-embedded lymphoid tissues of new- and old-world camelids. Vet Immunol Immunopathol 184:42–53
Van OA, Haaijman JJ, Benner R (1984) Frequencies of background cytoplasmic Ig-containing cells in various lymphoid organs of athymic and euthymic mice as a function of age and immune status. Immunology 51(4):735–742
Wilson RA, Zolnai A, Rudas P, Frenyo LV (1996) T-cell subsets in blood and lymphoid tissues obtained from fetal calves, maturing calves, and adult bovine. Vet Immunol Immunopathol 53(1–2):49–60
Xu Y, Sun J, Cui Y, Yu S, He J, Liu P, Zhang Q (2019) Age-related changes in the morphology and the distribution of IgA and IgG in the pharyngeal tonsils of yaks (Bos grunniens). J Morphol 280(2):214–222
Yasuda M, Jenne CN, Kennedy LJ, Reynolds JD (2006) The sheep and cattle Peyer’s patch as a site of B-cell development. Vet Res 37(3):401–415
Zhang W, Nasu T, Hosaka YZ, Yasuda M (2012) Comparative studies on the distribution and population of immunocompetent cells in bovine hemal node, lymph node and spleen. J Vet Med Sci 74(4):405–411
Zhang Q, Yang K, Huang Y, He J, Yu S, Cui Y (2017) Distribution of T-cell markers CD4 and CD8α in lymphoid organs of healthy newborn, juvenile, and adult highland-plateau yaks. Am J Vet Res 78(5):609–617
Zhou GY (2013) Principles of immunology. Science Press, Beijing
Zidan M, Pabst R (2004) Histological, histochemical and immunohistochemical study of the haemal nodes of the dromedary camel. Anat Histol Embryol 33(5):284–289
Funding
This study was supported by the National Natural Science Foundation of China (Grant No. 31572478).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All experimental animals were handled according to the Animal Ethics Procedures and Guidelines of the People’s Republic of China and the study was approved by the Institutional Animal Care and Use Committee (IACUC) (No. GSAUAEC-2016-007) of the College of Veterinary Medicine of Gansu Agricultural University.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Huang, Y., Cui, Y., Yu, S. et al. Expression characteristics of immune factors in secondary lymphoid organs of newborn, juvenile and adult yaks (Bos grunniens). Cell Tissue Res 381, 285–298 (2020). https://doi.org/10.1007/s00441-020-03219-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-020-03219-4