Red blood cells as innovative antigen carrier to induce specific immune tolerance

International Journal of Pharmaceutics

Volumn 443, Issue 1-2, 2013, Pages 39-49

  Cremel, Magali ^a   Guérin, Nathalie ^a   Horand, Françoise ^a   Banz, Alice ^a   Godfrin, Yann ^a  

^a ERYTECH PHARMA   (France)

Author keywords

Antibodies; Cellular immunology; Immunotherapy; Red blood cell carrier; Tolerance induction

Indexed keywords

OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; CELL ENCAPSULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; ERYTHROCYTE; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOLOGICAL TOLERANCE; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TARGET ORGAN;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS; CALCIUM IONOPHORES; CELL AGING; CELLS, CULTURED; CROSS-LINKING REAGENTS; DRUG CARRIERS; ERYTHROCYTES; HUMANS; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; MACROPHAGES; MICE; MICE, INBRED C57BL; OVALBUMIN; PHAGOCYTOSIS; SUCCINIMIDES;

EID: 84873924157     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2012.12.044     Document Type: Article

References (41)

1. M.L. Alegre, H. Shiels, C.B. Thompson, and T.F. Gajewski Expression and function of CTLA-4 in Th1 and Th2 cells J. Immunol. 161 1998 3347 3356
2. J. Astermark Immune tolerance induction in patients with hemophilia A Thromb. Res. 127 Suppl. 1 2010 S6 S9
3. A. Banz, M. Cremel, A. Rembert, and Y. Godfrin In situ targeting of dendritic cells by antigen-loaded red blood cells: a novel approach to cancer immunotherapy Vaccine 28 2010 2965 2972
4. D. Bratosin, J. Mazurier, J.P. Tissier, C. Slomianny, J. Estaquier, F. Russo-Marie, J.J. Huart, J.M. Freyssinet, D. Aminoff, J.C. Ameisen, and J. Montreuil Molecular mechanisms of erythrophagocytosis. Characterization of the senescent erythrocytes that are phagocytized by macrophages C. R. Acad. Sci. III 320 1997 811 818
5. P. Chappert, M. Leboeuf, P. Rameau, D. Stockholm, R. Liblau, O. Danos, J.M. Davoust, and D.A. Gross Antigen-driven interactions with dendritic cells and expansion of Foxp3+ regulatory T cells occur in the absence of inflammatory signals J. Immunol. 180 2008 327 334
6. L. Chiarantini, L. Rossi, A. Fraternale, and M. Magnani Modulated red blood cell survival by membrane protein clustering Mol. Cell. Biochem. 144 1995 53 59
7. C. Delaby, N. Pilard, G. Hetet, F. Driss, B. Grandchamp, C. Beaumont, and F. Canonne-Hergaux A physiological model to study iron recycling in macrophages Exp. Cell Res. 310 2005 43 53
8. D.C. Fitzgerald, G.X. Zhang, S. Yu, M.L. Cullimore, Z. Zhao, and A. Rostami Intravenous tolerance effectively overcomes enhanced pro-inflammatory responses and experimental autoimmune encephalomyelitis severity in the absence of IL-12 receptor signaling J. Neuroimmunol. 247 2012 32 37
9. T. Fukaya, H. Takagi, Y. Sato, K. Sato, K. Eizumi, H. Taya, T. Shin, L. Chen, C. Dong, M. Azuma, H. Yagita, B. Malissen, and K. Sato Crucial roles of B7-H1 and B7-DC expressed on mesenteric lymph node dendritic cells in the generation of antigen-specific CD4+Foxp3+ regulatory T cells in the establishment of oral tolerance Blood 116 2010 2266 2276
10. Y. Godfrin, F. Horand, R. Franco, E. Dufour, E. Kosenko, B.E. Bax, A. Banz, O.A. Skorokhod, J.M. Lanao, V. Vitvitsky, E. Sinauridze, V. Bourgeaux, and K.C. Gunter Meeting highlights: international seminar on the red blood cells as vehicles for drugs Expert Opin. Biol. Ther. 12 2012 127 133
11. M.L. Gumanovskaya, L.K. Myers, E.F. Rosloniec, J.M. Stuart, and A.H. Kang Intravenous tolerization with type II collagen induces interleukin-4-and interleukin-10-producing CD4+ T cells Immunology 97 1999 466 473
12. W.R. Heath, G.T. Belz, G.M. Behrens, C.M. Smith, S.P. Forehan, I.A. Parish, G.M. Davey, N.S. Wilson, F.R. Carbone, and J.A. Villadangos Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens Immunol. Rev. 199 2004 9 26
13. B.A. Hilliard, M. Kamoun, E. Ventura, and A. Rostami Mechanisms of suppression of experimental autoimmune encephalomyelitis by intravenous administration of myelin basic protein: role of regulatory spleen cells Exp. Mol. Pathol. 68 2000 29 37
14. R. Ing, M. Segura, N. Thawani, M. Tam, and M.M. Stevenson Interaction of mouse dendritic cells and malaria-infected erythrocytes: uptake, maturation, and antigen presentation J. Immunol. 176 2006 441 450
15. J.A. Jordan, F.J. Alvarez, L.A. Lotero, A. Herraez, J.C. Diez, and M.C. Tejedor In vitro phagocytosis of carrier mouse red blood cells is increased by Band 3 cross-linking or diamide treatment Biotechnol. Appl. Biochem. 34 2001 143 149
16. J.A. Jordan, J.R. DeLoach, J. Luque, and J.C. Diez Targeting of mouse erythrocytes by band 3 crosslinkers Biochim. Biophys. Acta 1291 1996 27 34
17. J.A. Jordan, J.C. Murciano, A. Lotero, A. Herraez, and J.C. Diez In vitro properties and organ uptake of rat band 3 cross-linked erythrocytes Biochimie 79 1997 53 61
18. M.M. Kay Mechanism of removal of senescent cells by human macrophages in situ Proc. Natl. Acad. Sci. U.S.A. 72 1975 3521 3525
19. S. Khandelwal, R.N. van, and R.K. Saxena Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation Transfusion (Paris) 47 2007 1725 1732
20. R. Kushwah, and J. Hu Complexity of dendritic cell subsets and their function in the host immune system Immunology 133 2011 409 419
21. S.J. Lee, S.Y. Park, M.Y. Jung, S.M. Bae, and I.S. Kim Mechanism for phosphatidylserine-dependent erythrophagocytosis in mouse liver Blood 117 2011 5215 5223
22. H. Li, G.X. Zhang, Y. Chen, H. Xu, D.C. Fitzgerald, Z. Zhao, and A. Rostami CD11c+CD11b+ dendritic cells play an important role in intravenous tolerance and the suppression of experimental autoimmune encephalomyelitis J. Immunol. 181 2008 2483 2493
23. R.S. Liblau, R. Tisch, K. Shokat, X. Yang, N. Dumont, C.C. Goodnow, and H.O. McDevitt Intravenous injection of soluble antigen induces thymic and peripheral T-cells apoptosis Proc. Natl. Acad. Sci. U.S.A. 93 1996 3031 3036
24. K. Mahnke, E. Schmitt, L. Bonifaz, A.H. Enk, and H. Jonuleit Immature, but not inactive: the tolerogenic function of immature dendritic cells Immunol. Cell Biol. 80 2002 477 483
25. G.P. Morris, N.K. Brown, and Y.C. Kong Naturally-existing CD4(+)CD25(+)Foxp3(+) regulatory T cells are required for tolerance to experimental autoimmune thyroiditis induced by either exogenous or endogenous autoantigen J. Autoimmun. 33 2009 68 76
26. A.M. Murray, I.F. Pearson, L.D. Fairbanks, R.A. Chalmers, M.D. Bain, and B.E. Bax The mouse immune response to carrier erythrocyte entrapped antigens Vaccine 24 2006 6129 6139
27. D.M. Sansom, and L.S. Walker The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology Immunol. Rev. 212 2006 131 148
28. Y. Sasamoto, Y.I. Kawano, R. Bouligny, B. Wiggert, G.J. Chader, and I. Gery Immunomodulation of experimental autoimmune uveoretinitis by intravenous injection of uveitogenic peptides Invest. Ophthalmol. Vis. Sci. 33 1992 2641 2649
29. H. Schellekens The immunogenicity of therapeutic proteins Discov. Med. 9 2010 560 564
30. A. Schildknecht, S. Brauer, C. Brenner, K. Lahl, H. Schild, T. Sparwasser, H.C. Probst, and M. van den Broek FoxP3+ regulatory T cells essentially contribute to peripheral CD8+ T-cell tolerance induced by steady-state dendritic cells Proc. Natl. Acad. Sci. U.S.A. 107 2010 199 203
31. A.J. Schroit, J.W. Madsen, and Y. Tanaka In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes J. Biol. Chem. 260 1985 5131 5138
32. J.A. Singer, L.K. Jennings, C.W. Jackson, M.E. Dockter, M. Morrison, and W.S. Walker Erythrocyte homeostasis: antibody-mediated recognition of the senescent state by macrophages Proc. Natl. Acad. Sci. U.S.A. 83 1986 5498 5501
33. S.K. Switzer, B.P. Wallner, T.J. Briner, G.H. Sunshine, C.R. Bourque, and M. Luqman Bolus injection of aqueous antigen leads to a high density of T-cell-receptor ligand in the spleen, transient T-cell activation and anergy induction Immunology 94 1998 513 522
34. F. Turrini, P. Arese, J. Yuan, and P.S. Low Clustering of integral membrane proteins of the human erythrocyte membrane stimulates autologous IgG binding, complement deposition, and phagocytosis J. Biol. Chem. 266 1991 23611 23617
35. X. Valencia, C. Yarboro, G. Illei, and P.E. Lipsky Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus J. Immunol. 178 2007 2579 2588
36. R. Verbeek, K. van der Mark, E.F. Wawrousek, A.C. Plomp, and J.M. van Noort Tolerization of an established alphaB-crystallin-reactive T-cell response by intravenous antigen Immunology 121 2007 416 426
37. A. Wakabayashi, M. Utsuyama, T. Hosoda, K. Sato, H. Takahashi, and K. Hirokawa Induction of immunological tolerance by oral, but not intravenous and intraportal,administration of ovalbumin and the difference between young and old mice J. Nutr. Health Aging 10 2006 183 191
38. K. Wing, Y. Onishi, P. Prieto-Martin, T. Yamaguchi, M. Miyara, Z. Fehervari, T. Nomura, and S. Sakaguchi CTLA-4 control over Foxp3+ regulatory T cell function Science 322 2008 271 275
39. S. Yamazaki, D. Dudziak, G.F. Heidkamp, C. Fiorese, A.J. Bonito, K. Inaba, M.C. Nussenzweig, and R.M. Steinman CD8+ CD205+ splenic dendritic cells are specialized to induce Foxp3+ regulatory T cells J. Immunol. 181 2008 6923 6933
40. Q. You, L. Cheng, R.M. Kedl, and C. Ju Mechanism of T cell tolerance induction by murine hepatic Kupffer cells Hepatology 48 2008 978 990
41. E. Zocchi, M. Tonetti, C. Polvani, L. Guida, U. Benatti, and F.A. De Encapsulation of doxorubicin in liver-targeted erythrocytes increases the therapeutic index of the drug in a murine metastatic model Proc. Natl. Acad. Sci. U.S.A. 86 1989 2040 2044