B cells "transduced" with TAT-fusion proteins can induce tolerance and protect mice from diabetes and EAE

Clinical Immunology

Volumn 140, Issue 3, 2011, Pages 260-267

  Su, Yan ^a,c   Zhang, Ai Hong ^a   Li, Xin ^a   Owusu Boaitey, Nana ^b   Skupsky, Jonathan ^a   Scott, David W ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^c Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

Author keywords

B cells; EAE; Protein therapy; T1D; TAT fusion; Tolerance

Indexed keywords

HYBRID PROTEIN; INSULIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; OVALBUMIN; TRANSACTIVATOR PROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; FEMALE; GENETIC TRANSDUCTION; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADOPTIVE TRANSFER; ANIMALS; B-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE PRODUCTS, TAT; IMMUNE TOLERANCE; INSULIN; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, TRANSGENIC; MYELIN-ASSOCIATED GLYCOPROTEIN; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS;

EID: 80051787580     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2011.04.009     Document Type: Article

References (32)

1. Gilbert K.M., Weigle W.O. Tolerogenicity of resting and activated B cells. J. Exp. Med. 1994, 179:249-258.
2. Fuchs E.J., Matzinger P. B cells turn off virgin but not memory T cells. Science 1992, 258:1156-1159.
3. Eynon E.E., Parker D.C. Small B cells as antigen-presenting cells in the induction of tolerance to soluble protein antigens. J. Exp. Med. 1992, 175:131-138.
4. Chen C., Rivera A., Ron N., Dougherty J.P., Ron Y. A gene therapy approach for treating T-cell-mediated autoimmune diseases. Blood 2001, 97:886-894.
5. Chen C.C., Rivera A., Dougherty J.P., Ron Y. Complete protection from relapsing experimental autoimmune encephalomyelitis induced by syngeneic B cells expressing the autoantigen. Blood 2004, 103:4616-4618.
6. Zambidis E.T., Barth R.K., Scott D.W. Both resting and activated B lymphocytes expressing engineered peptide-Ig molecules serve as highly efficient tolerogenic vehicles in immunocompetent adult recipients. J. Immunol. 1997, 158:2174-2182.
7. Zambidis E.T., Scott D.W. Epitope-specific tolerance induction with an engineered immunoglobulin. Proc Natl Acad Sci USA 1996, 93:5019-5024.
8. Agarwal R.K., Kang Y., Zambidis E., Scott D.W., Chan C.C., Caspi R.R. Retroviral gene therapy with an immunoglobulin-antigen fusion construct protects from experimental autoimmune uveitis. J. Clin. Invest. 2000, 106:245-252.
9. Melo M.E., Qian J., El-Amine M., Agarwal R.K., Soukhareva N., Kang Y., Scott D.W. Gene transfer of Ig-fusion proteins into B cells prevents and treats autoimmune diseases. J. Immunol. 2002, 168:4788-4795.
10. Soukhareva N., Jiang Y., Scott D.W. Treatment of diabetes in NOD mice by gene transfer of Ig-fusion proteins into B cells: role of T regulatory cells. Cell. Immunol. 2006, 240:41-46.
11. Xu B., Scott D.W. A novel retroviral gene therapy approach to inhibit specific antibody production and suppress experimental autoimmune encephalomyelitis induced by MOG and MBP. Clin. Immunol. 2004, 111:47-52.
12. Ahangarani R.R., Janssens W., VanderElst L., Carlier V., VandenDriessche T., Chuah M., Weynand B., Vanoirbeek J.A., Jacquemin M., Saint-Remy J.M. In vivo induction of type 1-like regulatory T cells using genetically modified B cells confers long-term IL-10-dependent antigen-specific unresponsiveness. J. Immunol. 2009, 183:8232-8243.
13. Lei T.C., Scott D.W. Induction of tolerance to factor VIII inhibitors by gene therapy with immunodominant A2 and C2 domains presented by B cells as Ig fusion proteins. Blood 2005, 105:4865-4870.
14. Liang W., Karabekian Z., Mattapallil M., Xu Q., Viley A.M., Caspi R., Scott D.W. B-cell delivered gene transfer of human S-Ag-Ig fusion protein protects from experimental autoimmune uveitis. Clin. Immunol. 2006, 118:35-41.
15. Satpute S.R., Soukhareva N., Scott D.W., Moudgil K.D. Mycobacterial Hsp65-IgG-expressing tolerogenic B cells confer protection against adjuvant-induced arthritis in Lewis rats. Arthritis Rheum. 2007, 56:1490-1496.
16. Aldo-Benson M., Borel Y. Loss of carrier-determined tolerance in vitro with loss of receptor blockade. J. Immunol. 1976, 116:223-226.
17. Borel Y., Kilham L., Hyslop N., Borel H. Isologous IgG-induced tolerance to benzyl penicilloyl. Nature 1976, 261:49-50.
18. Venkataraman M., Scott D.W. Cellular events in tolerance, VI. Neonatal vs adult B cell tolerance: differences in antigen-binding cell patterns and lipopolysaccharide stimulation. J. Immunol. 1977, 119:1879-1881.
19. Su Y., Carey G., Maric M., Scott D.W. B cells induce tolerance by presenting endogenous peptide-IgG on MHC class II molecules via an IFN-gamma-inducible lysosomal thiol reductase-dependent pathway. J. Immunol. 2008, 181:1153-1160.
20. Litzinger M.T., Su Y., Lei T.C., Soukhareva N., Scott D.W. Mechanisms of gene therapy for tolerance: B7 signaling is required for peptide-IgG gene-transferred tolerance induction. J. Immunol. 2005, 175:780-787.
21. Skupsky J., Zhang A.H., Su Y., Scott D.W. B-cell-delivered gene therapy induces functional T regulatory cells and leads to a loss of antigen-specific effector cells. Mol. Ther. 2010, 18:1527-1535.
22. Frankel A.D., Young J.A. HIV-1: fifteen proteins and an RNA. Annu. Rev. Biochem. 1998, 67:1-25.
23. Becker-Hapak M., McAllister S.S., Dowdy S.F. TAT-mediated protein transduction into mammalian cells. Methods 2001, 24:247-256.
24. Schwarze S.R., Ho A., Vocero-Akbani A., Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 1999, 285:1569-1572.
25. Nagahara H., Vocero-Akbani A.M., Snyder E.L., Ho A., Latham D.G., Lissy N.A., Becker-Hapak M., Ezhevsky S.A., Dowdy S.F. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med. 1998, 4:1449-1452.
26. Stromnes I.M., Goverman J.M. Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 2006, 1:1810-1819.
27. El-Amine M., Melo M., Kang Y., Nguyen H., Qian J., Scott D.W. Mechanisms of tolerance induction by a gene-transferred peptide-IgG fusion protein expressed in B lineage cells. J. Immunol. 2000, 165:5631-5636.
28. Lei T.C., Su Y., Scott D.W. Tolerance induction via a B-cell delivered gene therapy-based protocol: optimization and role of the Ig scaffold. Cell. Immunol. 2005, 235:12-20.
29. Wadia J.S., Dowdy S.F. Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer. Adv. Drug Deliv. Rev. 2005, 57:579-596.
30. Vives E., Brodin P., Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 1997, 272:16010-16017.
31. Kang Y., Melo M., Deng E., Tisch R., El-Amine M., Scott D.W. Induction of hyporesponsiveness to intact foreign protein via retroviral-mediated gene expression: the IgG scaffold is important for induction and maintenance of immune hyporesponsiveness. Proc Natl Acad Sci USA 1999, 96:8609-8614.
32. Wadia J.S., Stan R.V., Dowdy S.F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 2004, 10:310-315.