Splenic marginal zone antigen-presenting cells are critical for the primary allo-immune response to therapeutic factor VIII in hemophilia A

Journal of Thrombosis and Haemostasis

Volumn 7, Issue 11, 2009, Pages 1816-1823

  Navarrete, A ^a,b,c   Dasgupta, S ^a,b,c   Delignat, S ^a,b,c   Caligiuri, G ^a,b,c   Christophe, O D ^d   Bayry, J ^a,b,c   Nicoletti, A ^a,b,c   Kaveri, S V ^a,b,c   Lacroix Desmazes, S ^a,b,c  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSERM   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Allo immunization; Factor VIII; FVIII inhibitors; Hemophilia A; Protein therapeutics; Spleen

Indexed keywords

BLOOD CLOTTING FACTOR 8; CD8ALPHA ANTIGEN; CLODRONIC ACID; GLYCOPROTEIN P 15095; RECOMBINANT BLOOD CLOTTING FACTOR 8;

ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CELL FUNCTION; DENDRITIC CELL; HEMOPHILIA A; HISTOPATHOLOGY; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; IN VIVO STUDY; LIPOSOMAL DELIVERY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; SPLEEN; SPLENECTOMY; SPLENIC MARGINAL ZONE ANTIGEN PRESENTING CELL;

ANIMALS; ANTIGEN-PRESENTING CELLS; FACTOR VIII; HEMOPHILIA A; IMMUNITY; ISOANTIBODIES; MACROPHAGES; MICE; SPLEEN; SPLENECTOMY; TISSUE DISTRIBUTION;

EID: 70449431508     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2009.03571.x     Document Type: Article

References (33)

1. De Groot AS, Moise L. Prediction of immunogenicity for therapeutic proteins: state of the art. Curr Opin Drug Discov Devel 2007, 10:332-40.
2. Ehrenforth S, Kreuz W, Scharrer I, Linde R, Funk M, Güngör T, Krackhardt B, Kornhuber B. Incidence of development of factor VIII and factor IX inhibitors in haemophiliacs. Lancet 1992, 339:594-8.
3. Mebius RE, Kraal G. Structure and function of the spleen. Nat Rev Immunol 2005, 5:606-16.
4. Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol 2000, 164:2978-86.
5. Nolte MA, Hoen EN, van Stijn A, Kraal G, Mebius RE. Isolation of the intact white pulp. Quantitative and qualitative analysis of the cellular composition of the splenic compartments. Eur J Immunol 2000, 30:626-34.
6. Nolte MA, Belien JA, Schadee-Eestermans I, Jansen W, Unger WW, van Rooijen N, Kraal G, Mebius RE. A conduit system distributes chemokines and small blood-borne molecules through the splenic white pulp. J Exp Med 2003, 198:505-12.
7. Cinamon G, Zachariah MA, Lam OM, Foss FW, Cyster JG. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat Immunol 2008, 9:54-62.
8. Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C, Yamazaki S, Cheong C, Liu K, Lee HW, Park CG, Steinman RM, Nussenzweig MC. Differential antigen processing by dendritic cell subsets in vivo. Science 2007, 315:107-11.
9. Breukels MA, Zandvoort A, van Den Dobbelsteen GP, van Den Muijsenberg A, Lodewijk ME, Beurret M, Klok PA, Timens W, Rijkers GT. Pneumococcal conjugate vaccines overcome splenic dependency of antibody response to pneumococcal polysaccharides. Infect Immun 2001, 69:7583-7.
10. Delignat S, Dasgupta S, André S, Navarrete A, Kaveri S, Bayry J, André M, Chtourou S, Tellier Z, Lacroix-Desmazes S. Comparison of the immunogenicity of different therapeutic preparations of human factor VIII in the murine model of hemophilia A. Haematologica 2007, 92:1423-6.
11. van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 1994, 174:83-93.
12. Kraal G, Rodrigues H, Hoeben K, van Rooijen N. Lymphocyte migration in the spleen: the effect of macrophage elimination. Immunology 1989, 68:227-32.
13. Morfini M, Longo G, Messori A, Lee M, White G, Mannucci P. Pharmacokinetic properties of recombinant factor VIII compared with a monoclonally purified concentrate (Hemofil M). The Recombinate Study Group. Thromb Haemost 1992, 68:433-5.
14. Mordenti J, Osaka G, Garcia K, Thomsen K, Licko V, Meng G. Pharmacokinetics and interspecies scaling of recombinant human factor VIII. Toxicol Appl Pharmacol 1996, 136:75-8.
15. Jacquemin M, Neyrinck A, Hermanns MI, Lavend'homme R, Rega F, Saint-Remy JM, Peerlinck K, van Raemdonck D, Kirkpatrick CJ. FVIII production by human lung microvascular endothelial cells. Blood 2006, 108:515-7.
16. Stel HV, van der Kwast TH, Veerman EC. Detection of factor VIII/coagulant antigen in human liver tissue. Nature 1983, 303:530-2.
17. Bovenschen N, Rijken DC, Havekes LM, Vlijmen BJ, Mertens K. The B domain of coagulation factor VIII interacts with the asialoglycoprotein receptor. J Thromb Haemost 2005, 3:1257-65.
18. van Schooten CJ, Shahbazi S, Groot E, Oortwijn BD, van den Berg HM, Denis CV, Lenting PJ. Macrophages contribute to the cellular uptake of von Willebrand factor and factor VIII in vivo. Blood 2008, 112:1704-12.
19. Saenko E, Yakhyaev A, Mikhailenko I, Strickland D, Sarafanov A. Role of the low density lipoprotein-related protein receptor in mediation of factor VIII catabolism. J Biol Chem 1999, 274:37685-92.
20. Burgdorf S, Lukacs-Kornek V, Kurts C. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J Immunol 2006, 176:6770-6.
21. Qian J, Burkly L, Smith E, Ferrant J, Hoyer L, Scott D, Haudenschild C. Role of CD154 in the secondary immune response: the reduction of pre-existing splenic germinal centers and anti-factor VIII inhibitor titer. Eur J Immunol 2000, 30:2548-54.
22. Feuerer M, Beckhove P, Garbi N, Mahnke Y, Limmer A, Hommel M, Hammerling GJ, Kyewski B, Hamann A, Umansky V, Schirrmacher V. Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat Med 2003, 9:1151-7.
23. Kraal G, Janse M, Claassen E. Marginal metallophilic macrophages in the mouse spleen: effects of neonatal injections of MOMA-1 antibody on the humoral immune response. Immunol Lett 1988, 17:139-44.
24. Eloranta ML, Alm GV. Splenic marginal metallophilic macrophages and marginal zone macrophages are the major interferon-alpha/beta producers in mice upon intravenous challenge with herpes simplex virus. Scand J Immunol 1999, 49:391-4.
25. Taylor PR, Zamze S, Stillion RJ, Wong SY, Gordon S, Martinez-Pomares L. Development of a specific system for targeting protein to metallophilic macrophages. Proc Natl Acad Sci U S A 2004, 101:1963-8.
26. Ciavarra RP, Taylor L, Greene AR, Yousefieh N, Horeth D, van Rooijen N, Steel C, Gregory B, Birkenbach M, Sekellick M. Impact of macrophage and dendritic cell subset elimination on antiviral immunity, viral clearance and production of type 1 interferon. Virol 2005, 342:177-89.
27. Pooley JL, Heath WR, Shortman K. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J Immunol 2001, 166:5327-30.
28. Bovenschen N, Mertens K, Hu L, Havekes L, van Vlijmen B. LDL receptor cooperates with LDL receptor-related protein in regulating plasma levels of coagulation factor VIII in vivo. Blood 2005, 106:906-12.
29. Lenting P, Neels J, van den Berg B, Clijsters P, Meijerman D, Pannekoek H, van Mourik J, Mertens K, van Zonneveld A. The light chain of factor VIII comprises a binding site for low density lipoprotein receptor-related protein. J Biol Chem 1999, 274:23734-9.
30. Dasgupta S, Navarrete AM, Bayry J, Delignat S, Wootla B, Andre S, Christophe O, Nascimbeni M, Jacquemin M, Martinez-Pomares L, Geijtenbeek TB, Moris A, Saint-Remy JM, Kazatchkine MD, Kaveri SV, Lacroix-Desmazes S. A role for exposed mannosylations in presentation of human therapeutic self-proteins to CD4+ T lymphocytes. Proc Natl Acad Sci U S A 2007, 104:8965-70.
31. van der Laan LJ, Kangas M, Dopp EA, Broug-Holub E, Elomaa O, Tryggvason K, Kraal G. Macrophage scavenger receptor MARCO: in vitro and in vivo regulation and involvement in the anti-bacterial host defense. Immunol Lett 1997, 57:203-8.
32. Jones C, Virji M, Crocker PR. Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol Microbiol 2003, 49:1213-25.
33. Delputte PL, Nauwynck HJ. Porcine arterivirus infection of alveolar macrophages is mediated by sialic acid on the virus. J Virol 2004, 78:8094-101.