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Origin of follicular dendritic cell in the chicken spleen

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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.

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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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bofill M, Akbar AN, Amlot PL (2000) Follicular dendritic cells share a membrane-bound protein with fibroblasts. J Pathol 191:217–226

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Haberman AM, Shlomchik MJ (2003) Reassessing the function of immune-complex retention by follicular dendritic cells. Nat Rev Immunol 3:757–764

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hogasen AK, Abrahamsen TG (1995) Heparin suppresses lipopolysaccharide-induced monocyte production of several cytokines, but simultaneously stimulates C3 production. Thromb Res 80:179–184

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Jeurissen SH, Claassen HE, Janse EM (1992) Histological and functional differentiation of non-lymphoid cells in the chicken spleen. Immunology 77:75–80

    PubMed  CAS  Google Scholar 

  • Jeurissen SH, Vervelde L, Marga Janse E (1994) Structure and function of lymphoid tissue of the chicken. Poultry Science Rev 5:183–207

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Liu YJ, Grouard G, de Bouteiller O, Banchereau J (1996) Follicular dendritic cells and germinal centers. Int Rev Cytol 166:139–179

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Nieuwenhuis P, Opstelten D (1984) Functional anatomy of germinal centers. Am J Anat 170:421–435

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Olah I, Glick B (1982) Splenic white pulp and associated vascular channels in chicken spleen. Am J Anat 165:445–480

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Tew JG, Kosco-Vilbois MH, Burton GH, Szakal AK (1990) Follicular dendritic cells as accessory cells. Immunol Rev 117:185–211

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Veromaa T, Vainio O, Eerola E, Toivanen P (1988) Monoclonal antibodies against chicken Bu-1a and Bu-1b alloantigens. Hybridoma 7:41–48

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • White RG, Henderson DC, Eslami MB, Nielsen KH (1975) Localization of a protein antigen in the chicken spleen. Immunology 28:1–21

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Zahner D, Hakenbeck R (2000) The Streptococcus pneumoniae beta-galactosidase is a surface protein. J Bacteriol 182:5919–5921

    Article  PubMed  CAS  Google Scholar 

Download references

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.

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Correspondence to Imre Oláh.

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This work was supported by OTKA Grant number: T-042558.

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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

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