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Published in: Langenbeck's Archives of Surgery 2/2008

01-03-2008 | Original Article

Donor B cells in splenic follicles of experimental pulmonary allograft recipients

Published in: Langenbeck's Archives of Surgery | Issue 2/2008

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Abstract

Background

After transplantation, passenger leukocytes move to lymphoid organs of the recipient. These cells appear to initiate allograft rejection, but they also might be involved in tolerance induction.

Materials and methods

Orthotopic left lung transplantation was performed in the Dark Agouti to Lewis rat strain combination with no immunosuppression. Recipient spleens were removed at intervals of 24 h until day 6 after transplantation. For comparison, spleens from renal allograft recipients were analysed. Donor-derived major histocompatibility complex (MHC) class II antigens were detected by monoclonal antibody OX76. In double-staining experiments with antibodies specific for leukocyte subpopulations, their localisation and identity was analysed.

Results

OX76-positive leukocytes were already detected in recipient spleens on day 1 post-transplantation. They increased in number until day 3 and decreased in number thereafter. Most of them were localised in splenic follicles and expressed the B cell variant of CD45R and IgG. Cell surface antigens typical for other leukocyte subpopulations were not detected. In the spleens of renal allograft recipients, only few donor-derived cells were seen.

Conclusion

After lung transplantation, numerous MHC class II-positive B cells migrate to the splenic follicles of the recipient. These cells might, in part, be responsible for immunologic differences observed between renal and pulmonary allografts.
Literature
1.
go back to reference Wood KJ (2003) Passenger leukocytes and microchimerism: what role in tolerance induction? Transplantation 75:17S–20SPubMedCrossRef Wood KJ (2003) Passenger leukocytes and microchimerism: what role in tolerance induction? Transplantation 75:17S–20SPubMedCrossRef
2.
go back to reference Starzl TE (2004) Chimerism and tolerance in transplantation. Proc Natl Acad Sci USA 101(Suppl):14607–14614CrossRef Starzl TE (2004) Chimerism and tolerance in transplantation. Proc Natl Acad Sci USA 101(Suppl):14607–14614CrossRef
3.
go back to reference Steiniger B, Klempnauer J (1986) Donor-type MHC-positive cells in the host spleen after rat organ transplantation—differences between pancreas and heart allograft recipients. Transplantation 41:787–789PubMedCrossRef Steiniger B, Klempnauer J (1986) Donor-type MHC-positive cells in the host spleen after rat organ transplantation—differences between pancreas and heart allograft recipients. Transplantation 41:787–789PubMedCrossRef
4.
go back to reference Larsen CP, Morris PJ, Austyn JM (1990) Migration of dendritic leukocytes from cardiac allografts into host spleens—a novel pathway for initiation of rejection. J Exp Med 171:307–314PubMedCrossRef Larsen CP, Morris PJ, Austyn JM (1990) Migration of dendritic leukocytes from cardiac allografts into host spleens—a novel pathway for initiation of rejection. J Exp Med 171:307–314PubMedCrossRef
5.
go back to reference Okuda T, Ishikawa T, Azhipa O, Ichikawa N, Demeris AJ, Starzl TE, Murase N (2002) Early passenger leukocyte migration and acute immune reactions in the rat recipient spleen during liver engraftment: with particular emphasis on donor major histocompatibility complex class II+ cells. Transplantation 74:103–111PubMedCrossRef Okuda T, Ishikawa T, Azhipa O, Ichikawa N, Demeris AJ, Starzl TE, Murase N (2002) Early passenger leukocyte migration and acute immune reactions in the rat recipient spleen during liver engraftment: with particular emphasis on donor major histocompatibility complex class II+ cells. Transplantation 74:103–111PubMedCrossRef
6.
go back to reference Lechler RI, Batchelor JR (1982a) Immunogenicity of retransplanted rat kidney allografts. Effect of inducing chimerism in the first recipient and quantitative studies on immunosuppression of the second recipient. J Exp Med 156:1835–1841PubMedCrossRef Lechler RI, Batchelor JR (1982a) Immunogenicity of retransplanted rat kidney allografts. Effect of inducing chimerism in the first recipient and quantitative studies on immunosuppression of the second recipient. J Exp Med 156:1835–1841PubMedCrossRef
7.
go back to reference Lechler RI, Batchelor JR (1982b) Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donor strain dendritic cells. J Exp Med 155:31–41PubMedCrossRef Lechler RI, Batchelor JR (1982b) Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donor strain dendritic cells. J Exp Med 155:31–41PubMedCrossRef
8.
go back to reference Sriwatanawongsa V, Davis HS, Calne RY (1995) The essential roles of parenchymal tissues and passenger leukocytes in the tolerance induced by liver grafting in rats. Nat Med 1:428–432PubMedCrossRef Sriwatanawongsa V, Davis HS, Calne RY (1995) The essential roles of parenchymal tissues and passenger leukocytes in the tolerance induced by liver grafting in rats. Nat Med 1:428–432PubMedCrossRef
9.
go back to reference Tschernig T, Boeke K, Steinhoff G, Wonigeit K, Pabst R, Westermann J (1997) The lung as a source and a target organ for T- and B-lymphocytes. Am J Respir Cell Mol Biol 17:411–421 Tschernig T, Boeke K, Steinhoff G, Wonigeit K, Pabst R, Westermann J (1997) The lung as a source and a target organ for T- and B-lymphocytes. Am J Respir Cell Mol Biol 17:411–421
10.
go back to reference Vriens PW, Nisco SJ, Hoyt G, Lyu SC, Pierre P, Reitz BA, Clayberger C (1994) Tissue-specific differences in the establishment of tolerance. Transplantation 57:1795–1798PubMed Vriens PW, Nisco SJ, Hoyt G, Lyu SC, Pierre P, Reitz BA, Clayberger C (1994) Tissue-specific differences in the establishment of tolerance. Transplantation 57:1795–1798PubMed
11.
go back to reference Moller F, Hoyt G, Farfan F, Starnes VA, Clayberger C (1993) Cellular mechanisms underlying differential rejection of sequential heart and lung allografts in rats. Transplantation 55:650–655PubMedCrossRef Moller F, Hoyt G, Farfan F, Starnes VA, Clayberger C (1993) Cellular mechanisms underlying differential rejection of sequential heart and lung allografts in rats. Transplantation 55:650–655PubMedCrossRef
12.
go back to reference Wilkes DS, Egan TM, Reynolds HY (2005) Lung transplantation—opportunities for research and clinical advancement. Am J Respir Crit Care Med 172:944–955PubMedCrossRef Wilkes DS, Egan TM, Reynolds HY (2005) Lung transplantation—opportunities for research and clinical advancement. Am J Respir Crit Care Med 172:944–955PubMedCrossRef
13.
go back to reference Mizuta T, Kawaguchi A, Nakahara K, Kawashima Y (1989) Simplified rat lung transplantation using a cuff technique. J Thorac Cardiovasc Surg 97:578–581PubMed Mizuta T, Kawaguchi A, Nakahara K, Kawashima Y (1989) Simplified rat lung transplantation using a cuff technique. J Thorac Cardiovasc Surg 97:578–581PubMed
14.
go back to reference Schmidt A, Sucke J, Fuchs-Moll G, Freitag P, Hirschburger M, Kaufmann A, Padberg W, Grau V (2007) Macrophages in experimental lung isografts and allografts: infiltration and proliferation in situ. J Leukoc Biol 81:186–194PubMedCrossRef Schmidt A, Sucke J, Fuchs-Moll G, Freitag P, Hirschburger M, Kaufmann A, Padberg W, Grau V (2007) Macrophages in experimental lung isografts and allografts: infiltration and proliferation in situ. J Leukoc Biol 81:186–194PubMedCrossRef
15.
go back to reference Fabre J, Lim SH, Morris PJ (1971) Renal transplantation in the rat: details of a technique. Aust N Z J Surg 41:69–75PubMed Fabre J, Lim SH, Morris PJ (1971) Renal transplantation in the rat: details of a technique. Aust N Z J Surg 41:69–75PubMed
16.
go back to reference Grau V, Herbst B, Steiniger B (1998) Dynamics of monocytes/macrophages and T lymphocytes in acutely rejecting rat renal allografts. Cell Tissue Res 291:117–126PubMedCrossRef Grau V, Herbst B, Steiniger B (1998) Dynamics of monocytes/macrophages and T lymphocytes in acutely rejecting rat renal allografts. Cell Tissue Res 291:117–126PubMedCrossRef
17.
go back to reference Turnbull EL, Yrlid U, Jenkins CD, MacPherson GG (2005) Intestinal dendritic cell subsets: differential effects of systemic TLR4 stimulation on migratory fate and activation in vivo. J Immunol 174:1374–1384PubMed Turnbull EL, Yrlid U, Jenkins CD, MacPherson GG (2005) Intestinal dendritic cell subsets: differential effects of systemic TLR4 stimulation on migratory fate and activation in vivo. J Immunol 174:1374–1384PubMed
18.
go back to reference van den Berg T, Puklavec MJ, Barclay AN, Dijkstra CD (2001) Monoclonal antibodies against rat leukocyte surface antigens. Immunol Rev 183:109–116CrossRef van den Berg T, Puklavec MJ, Barclay AN, Dijkstra CD (2001) Monoclonal antibodies against rat leukocyte surface antigens. Immunol Rev 183:109–116CrossRef
19.
go back to reference Dijkstra CD, Döpp EA, Joling P, Kraal G (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54:589–599PubMed Dijkstra CD, Döpp EA, Joling P, Kraal G (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54:589–599PubMed
20.
go back to reference Barbé E, Damoiseaux JGMC, Döpp EA, Dijkstra CD (1990) Characterization and expression of the antigen present on resident rat macrophages recognized by monoclonal antibody ED2. Immunobiology 182:88–99PubMed Barbé E, Damoiseaux JGMC, Döpp EA, Dijkstra CD (1990) Characterization and expression of the antigen present on resident rat macrophages recognized by monoclonal antibody ED2. Immunobiology 182:88–99PubMed
21.
go back to reference Jeurissen SHM, Dijkstra CD (1986) Characteristics and functional aspects of non lymphoid cells in rat germinal centres, recognised by two monoclonal antibodies ED5 and ED6. Eur J Immunol 16:562–568PubMedCrossRef Jeurissen SHM, Dijkstra CD (1986) Characteristics and functional aspects of non lymphoid cells in rat germinal centres, recognised by two monoclonal antibodies ED5 and ED6. Eur J Immunol 16:562–568PubMedCrossRef
22.
go back to reference Damoiseaux JG, Döpp EA, Beelen RH, Dijkstra CD (1989) Rat bone marrow and monocyte cultures: influence of culture time and lymphokines on the expression of macrophage differentiation antigens. J Leukoc Biol 46:246–253PubMed Damoiseaux JG, Döpp EA, Beelen RH, Dijkstra CD (1989) Rat bone marrow and monocyte cultures: influence of culture time and lymphokines on the expression of macrophage differentiation antigens. J Leukoc Biol 46:246–253PubMed
23.
go back to reference Adams S, van der Laan LJW, Vernon-Wilson E, Renardel de Lavalette C, Döpp EA, Dijkstra CD, Simmons DL, van den Berg T (1998) Signal-regulatory protein is selectively expressed by myeloid and neuronal cells. J Immunol 161:1853–1859PubMed Adams S, van der Laan LJW, Vernon-Wilson E, Renardel de Lavalette C, Döpp EA, Dijkstra CD, Simmons DL, van den Berg T (1998) Signal-regulatory protein is selectively expressed by myeloid and neuronal cells. J Immunol 161:1853–1859PubMed
24.
go back to reference Bazin H, Beckers A, Querinjean P (1974) Three classes and four (sub)classes of rat immunoglobulins: IgM, IgA, IgE, and IgG1, IgG2a, IgG2b, IgG2c. Eur J Immunol 4:44–48PubMedCrossRef Bazin H, Beckers A, Querinjean P (1974) Three classes and four (sub)classes of rat immunoglobulins: IgM, IgA, IgE, and IgG1, IgG2a, IgG2b, IgG2c. Eur J Immunol 4:44–48PubMedCrossRef
25.
go back to reference Pockley AG, Reid SD, Bowles MJ (1995) An enzyme immunoassay for rat soluble MHC class I molecules (RT1a) and the release of soluble class I from mitogenically stimulated mononuclear cells. Immunol Invest 24:679–687PubMedCrossRef Pockley AG, Reid SD, Bowles MJ (1995) An enzyme immunoassay for rat soluble MHC class I molecules (RT1a) and the release of soluble class I from mitogenically stimulated mononuclear cells. Immunol Invest 24:679–687PubMedCrossRef
26.
go back to reference McMaster WR, Williams AF (1979) Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol 9:426–433PubMedCrossRef McMaster WR, Williams AF (1979) Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol 9:426–433PubMedCrossRef
27.
go back to reference Fukumoto T, McMaster WR, Williams AF (1982) Mouse monoclonal antibodies against rat major histocompatibility antigens. Two Ia antigens and expression of Ia and class I antigens in rat thymus. Eur J Immunol 12:237–243PubMedCrossRef Fukumoto T, McMaster WR, Williams AF (1982) Mouse monoclonal antibodies against rat major histocompatibility antigens. Two Ia antigens and expression of Ia and class I antigens in rat thymus. Eur J Immunol 12:237–243PubMedCrossRef
28.
go back to reference Dallman MJ, Thomas ML, Green JR (1984) MRC OX-19, a monoclonal antibody that labels rat T lymphocytes and augments in vitro proliferative responses. Eur J Immunol 14:260–267PubMedCrossRef Dallman MJ, Thomas ML, Green JR (1984) MRC OX-19, a monoclonal antibody that labels rat T lymphocytes and augments in vitro proliferative responses. Eur J Immunol 14:260–267PubMedCrossRef
29.
go back to reference Woollett GR, Barclay AN, Puklavec M, Williams AF (1985) Molecular and antigenic heterogeneity of the rat leukocyte-common antigen from thymocytes and T and B lymphocytes. Eur J Immunol 15:168–173PubMedCrossRef Woollett GR, Barclay AN, Puklavec M, Williams AF (1985) Molecular and antigenic heterogeneity of the rat leukocyte-common antigen from thymocytes and T and B lymphocytes. Eur J Immunol 15:168–173PubMedCrossRef
30.
go back to reference Brenan M, Puklavec M (1992) The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J Exp Med 27:3070–3079 Brenan M, Puklavec M (1992) The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J Exp Med 27:3070–3079
31.
go back to reference Hünig T, Wallny HJ, Hartley JK, Lawetzky A, Tiefenthaler G (1989) A monoclonal antibody to a constant determinant of the rat T cell antigen receptor that induces T cell activation. Differential reactivity with subsets of immature and mature T lymphocytes. J Exp Med 169:73–86PubMedCrossRef Hünig T, Wallny HJ, Hartley JK, Lawetzky A, Tiefenthaler G (1989) A monoclonal antibody to a constant determinant of the rat T cell antigen receptor that induces T cell activation. Differential reactivity with subsets of immature and mature T lymphocytes. J Exp Med 169:73–86PubMedCrossRef
32.
go back to reference Kuhnlein P, Park JH, Herrmann T, Elbe A, Hünig T (1994) Identification and characterization of rat γδ T lymphocytes in peripheral lymphoid organs, small intestine, and skin with a monoclonal antibody to a constant determinant of the γ/δ T cell receptor. J Immunol 153:979–986PubMed Kuhnlein P, Park JH, Herrmann T, Elbe A, Hünig T (1994) Identification and characterization of rat γδ T lymphocytes in peripheral lymphoid organs, small intestine, and skin with a monoclonal antibody to a constant determinant of the γ/δ T cell receptor. J Immunol 153:979–986PubMed
Metadata
Title
Donor B cells in splenic follicles of experimental pulmonary allograft recipients
Publication date
01-03-2008
Published in
Langenbeck's Archives of Surgery / Issue 2/2008
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-007-0195-0

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