Abstract
The ellipsoid-associated cell (EAC) is a blood-borne phagocytic cell, residing in the antigen trapping zone of the chicken spleen. Binding and endocytosis of βGalactosidase (βGal) are independent from the Fc and complement receptors, because sulfated polysaccharides, in a concentration manner, inhibit the bacterial antigen uptake. The βGal-positive cells migrate to the periarterial lymphatic sheath (PALS), the preexisting germinal centers (GC), and form clusters with B- and T-cells. βGal, E5G12 double positive cells on the surface of the ellipsoid and in the PALS, GC and clusters prove that the EACs carry the enzyme. The EAC and the follicular dendritic cell (FDC) express, 68.2 and E5G12 and, 74.3 and E5G12, antigens, respectively. During migration the cessation of 68.2 and expression of 74.3 indicate the differentiation of EAC to FDC. By day 14 the clusters had disappeared, and in several GC the presence of double positive cells (74.3 and βGal; E5G12 and βGal) showed that the clusters had developed to GC. The presence of βGal+ cells in the PALS, where interdigitating dendritic cells (IDC) cooperate with the T-cells, suggests that in the spleen alternate routes exist for the EAC differentiation to FDC: EAC to FDC: βGal-loaded cells in the preexisting GC; and EAC through IDC to FDC: βGal+ EAC in the PALS and clusters. The EAC-FDC axis works exclusively inside the spleen; therefore; this system may be operated in pneumococcus infection.
Similar content being viewed by others
Abbreviations
- EAC:
-
Ellipsoid-associated cell
- PALS:
-
Periarterial lymphatic sheath
- PWP:
-
Periellipsoidal white pulp
- GC:
-
Germinal center
- FDC:
-
Follicular dendritic cell
- IDC:
-
Interdigitating dendritic cell
- βGal:
-
βGalactosidase
References
Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392:245–252
Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811
Bofill M, Akbar AN, Amlot PL (2000) Follicular dendritic cells share a membrane-bound protein with fibroblasts. J Pathol 191:217–226
Brown JC, De Jesus DG, Holborow EJ, Harris G (1970) Lymphocyte-mediated transport of aggregated human gamma-globulin into germinal centre areas of normal mouse spleen. Nature 228:367–369
Cavaillon JM, Marie C, Caroff M, Ledur A, Godard I, Poulain D, Fitting C, Hareffner-Cavaillon N (1996) CD14/LPS receptor exhibits lectin-like properties. J Endotoxin Res 3:471–478
del Cacho E, Gallego M, Arnal C, Bascuas JA (1995) Localization of splenic cells with antigen-transporting capability in the chicken. Anat Rec 241:105–112
Denzer K, van Eijk M, Kleijmeer MJ, Jakobson E, de Groot C, Geuze HJ (2000) Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol 165:1259–1265
Ferguson AR, Youd ME, Corley RB (2004) Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells. Int Immunol 16:1411–1422
Gallego M, del Cacho E, Lopez-Bernad F, Bascuas JA (1997) Identification of avian dendritic cells in the spleen using a monoclonal antibody specific for chicken follicular dendritic cells. Anat Rec 249:81–85
Gray D, Kumararatne DS, Lortan J, Khan M, MacLennan IC (1984) Relation of intra-splenic migration of marginal zone B cells to antigen localization on follicular dendritic cells. Immunology 52:659–669
Groeneveld PH, Eikelenboom P, van Rooijen N (1983) Mechanism of follicular trapping: similarities and differences in trapping of antibody-complexed antigens and carbon particles in the follicles of the spleen. J Reticuloendothel Soc 33:109–117
Haberman AM, Shlomchik MJ (2003) Reassessing the function of immune-complex retention by follicular dendritic cells. Nat Rev Immunol 3:757–764
Hannum LG, Haberman AM, Anderson SM, Shlomchik MJ (2000) Germinal center initiation, variable gene region hypermutation, and mutant B cell selection without detectable immune complexes on follicular dendritic cells. J Exp Med 192:931–942
Heinen E, Braun M, Coulie PG, Van Snick J, Moeremans M, Cormann N, Kinet-Denoel C, Simar LJ (1986) Transfer of immune complexes from lymphocytes to follicular dendritic cells. Eur J Immunol 16:167–172
Heinzelmann M, Bosshart H (2005) Heparin binds to lipopolysaccharide (LPS)-binding protein, facilitates the transfer of LPS to CD14, and enhances LPS-induced activation of peripheral blood monocytes. J Immunol 174:2280–2287
Hogasen AK, Abrahamsen TG (1995) Heparin suppresses lipopolysaccharide-induced monocyte production of several cytokines, but simultaneously stimulates C3 production. Thromb Res 80:179–184
Humphrey JH, Grennan D, Sundaram V (1984) The origin of follicular dendritic cells in the mouse and the mechanism of trapping of immune complexes on them. Eur J Immunol 14:859–864
Jeurissen SH, Claassen HE, Janse EM (1992) Histological and functional differentiation of non-lymphoid cells in the chicken spleen. Immunology 77:75–80
Jeurissen SH, Vervelde L, Marga Janse E (1994) Structure and function of lymphoid tissue of the chicken. Poultry Science Rev 5:183–207
Kang YS, Do Y, Lee HK, Park SH, Cheong C, Lynch RM, Loeffler JM, Steinman RM, Park CG (2006) A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell 125:47–58
Kapasi ZF, Qin D, Kerr WG, Kosco-Vilbois MH, Shultz LD, Tew JG, Szakal AK (1998) Follicular dendritic cell (FDC) precursors in primary lymphoid tissue. J Immunol 160:1078–1084
Kroese FGM, Wubbena AS, Nieuwenhuis P (1986) Germinal center formation and follicular antigen trapping in the spleen of lethally X-irradiated and reconstituted rats. Immunology 57:99–104
Laman JD, Kors N, Van Rooijen N, Claassen E (1990) Mechanism of follicular trapping: localization of immune complexes and cell remnants after elimination and repopulation of different spleen cell populations. Immunology 71:57–62
Lanoue A, Clatworthy MR, Smith P, Green S, Townsend MJ, Jolin HE, Smith KG, Fallon PG, McKenzie AN (2004) SIGN-R1 contributes to protection against lethal pneumococcal infection in mice. J Exp Med. 200:1383–93
Liu YJ, Grouard G, de Bouteiller O, Banchereau J (1996) Follicular dendritic cells and germinal centers. Int Rev Cytol 166:139–179
Lutz MB, Rovere P, Kleijmeer MJ, Rescigno M, Assmann CU, Oorschot VM, Geuze HJ, Trucy J, Demandolx D, Davoust J, Ricciardi-Castagnoli P (1997) Intracellular routes and selective retention of antigens in mildly acidic cathepsin D/lysosome-associated membrane protein-1/MHC class II-positive vesicles in immature dendritic cells. J Immunol 159:3707–3716
Nagy N, Bíró E, Takács Á, Pólos M, Magyar A, Olah I (2005) Peripheral blood fibrocytes contribute to the formation of the avian spleen. Dev Dyn 232:55–66
Nagy ZA, Horváth E, Urbán Zs (1973) Antigen capture in chicken spleen during the primary immune response and relationship to phagocytic activity. Nature New Biol 242:241–244
Nieuwenhuis P, Opstelten D (1984) Functional anatomy of germinal centers. Am J Anat 170:421–435
Nossal GJV, Abbot A, Mitchell J, Lummus Z (1968) Antigens in immunity. XV. Ultrastructural features of antigen capture in primary and secondary lymphoid follicles. J Exp Med 127:277–290
Olah I, Glick B (1982) Splenic white pulp and associated vascular channels in chicken spleen. Am J Anat 165:445–480
Olah I, Glick B, Taylor Jr RL (1984) Effect of soluble antigen on the ellipsoid-associated cells of the chicken’ spleen. J Leukoc Biol 35:501–510
Oldfield S, Lortan JE, Hyatt MA, MacLennan IC (1988) Marginal zone B cells and the localisation of antigen on follicular dendritic cells. Adv Exp Med Biol 237:99–104
Steinman RM, Cohn ZA (1973) Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med 137:1142–1162
Szakal AK, Holmes KL, Tew JG (1983) Transport of immune complexes from the subcapsular sinus to lymph node follicles on the surface of nonphagocytic cells, including cells with dendritic morphology. J Immunol 131:1714–1727
Szakal AK, Kapasi ZF, Haley ST, Tew JG (1999) Multiple lines of evidence favoring a bone marrow derivation of follicular dendritic cells. In: Banchereau J (ed) Dendritic cells in Fundamental and Clinical Immunology. Plenum Press, New York, pp 267–272
Tew JG, Kosco-Vilbois MH, Burton GH, Szakal AK (1990) Follicular dendritic cells as accessory cells. Immunol Rev 117:185–211
Veerman AJ, van Rooijen N (1975) Lymphocyte capping and lymphocyte migration as associated events in the in vivo antigen trapping process. An electron-microscopic autoradiographic study in the spleen of mice. Cell Tissue Res 161:211–217
Veromaa T, Vainio O, Eerola E, Toivanen P (1988) Monoclonal antibodies against chicken Bu-1a and Bu-1b alloantigens. Hybridoma 7:41–48
White RG (1963) In: Wotstenholme GW, Knight J The Immunologically competent cell. CIBA Foundation Study Group, vol 16. Churchill, London, p6
White RG, French VI, Starck JM (1969) A study of the localization of a protein antigen in the chicken spleen and its relation to the formation of germinal centres. J Med Microbiol 3:65–83
White RG, Henderson DC, Eslami MB, Nielsen KH (1975) Localization of a protein antigen in the chicken spleen. Immunology 28:1–21
Wykes M, Pombo A, Jenkins C, MacPherson GG (1998) Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J Immunol 161:1313–1319
Yoshida K, Van Den Berg TK, Dijkstra CD (1993) Two functionally different follicular dendritic cells in secondary lymphoid follicles of mouse spleen, as revealed by CR1/2 and FcR II-mediated immune-complex trapping. Immunology 80:34–39
Yoshida K, Kaji M, Takahashi T, Van den Bergh TK, Dijkstra CD (1995) Host origin of follicular dendritic cells induced in the spleen of SCID mice after transfer of allogeneic lymphocytes. Immunology 84:117–126
Zahner D, Hakenbeck R (2000) The Streptococcus pneumoniae beta-galactosidase is a surface protein. J Bacteriol 182:5919–5921
Acknowledgements
The authors wish to thank to Zsuzsanna Vidra and Beáta Urák for the laboratory and photographical assistance, and appreciate the editing done by Scott D. Everett.
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by OTKA Grant number: T-042558.
Rights and permissions
About this article
Cite this article
Igyártó, BZ., Magyar, A. & Oláh, I. Origin of follicular dendritic cell in the chicken spleen. Cell Tissue Res 327, 83–92 (2007). https://doi.org/10.1007/s00441-006-0250-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-006-0250-0