Engineered antigen-specific human regulatory T cells: Immunosuppression of FVIII-specific T- and B-cell responses

Blood

Volumn 125, Issue 7, 2015, Pages 1107-1115

  Kim, Yong Chan ^a   Zhang, Ai Hong ^a   Su, Yan ^a   Rieder, Sadiye Amcaoglu ^b   Rossi, Robert J ^a   Ettinger, Ruth A ^c   Pratt, Kathleen P ^a   Shevach, Ethan M ^b   Scott, David W ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c PUGET SOUND BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; RECOMBINANT BLOOD CLOTTING FACTOR 8; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; BLOOD CLOTTING FACTOR 8; F8 PROTEIN, HUMAN;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIGEN SPECIFICITY; ARTICLE; CELL EXPANSION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENETIC TRANSDUCTION; HEMOPHILIA A; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; LYMPHOCYTE CLONE; MALE; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; ANIMAL; B LYMPHOCYTE; CELL CULTURE; CELL ENGINEERING; GENE THERAPY; GENETIC ENGINEERING; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PROCEDURES; YOUNG ADULT;

ADULT; AGED; ANIMALS; B-LYMPHOCYTES, REGULATORY; CELL ENGINEERING; CELLS, CULTURED; FACTOR VIII; GENETIC ENGINEERING; GENETIC THERAPY; HEMOPHILIA A; HUMANS; IMMUNE TOLERANCE; MALE; MICE; MIDDLE AGED; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT;

EID: 84923313146     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-04-566786     Document Type: Article

References (51)

1. Hoyer LW. Factor VIII inhibitors. Curr Opin Hematol. 1995;2(5):365-371.
2. Aledort LM, Evatt BL, Lusher JM, Brownstein AP. HIV and hemophilia. J Thromb Haemost. 2007; 5(3):607-610.
3. Qian J, Burkly LC, Smith EP, et al. Role of CD154 in the secondary immune response: the reduction of pre-existing splenic germinal centers and antifactor VIII inhibitor titer. Eur J Immunol. 2000; 30(9):2548-2554.
4. Scott DW, Pratt KP, Miao CH. Progress toward inducing immunologic tolerance to factor VIII. Blood. 2013;121(22):4449-4456.
5. Bluestone JA. Regulatory T-cell therapy: is it ready for the clinic? Nat Rev Immunol. 2005;5(4): 343-349.
6. Miyara M, Wing K, Sakaguchi S. Therapeutic approaches to allergy and autoimmunity based on FoxP3+ regulatory T-cell activation and expansion. J Allergy Clin Immunol. 2009;123(4): 749-755.
7. Ohkura N, Kitagawa Y, Sakaguchi S. Development and maintenance of regulatory T cells. Immunity. 2013;38(3):414-423.
8. Tang Q, Bluestone JA, Kang SM. CD4(+)Foxp3(+) regulatory T cell therapy in transplantation. J Mol Cell Biol. 2012;4(1):11-21.
9. Brusko TM, Koya RC, Zhu S, et al. Human antigen-specific regulatory T cells generated by T cell receptor gene transfer. PLoS ONE. 2010; 5(7):e11726.
10. Tsang JY, Tanriver Y, Jiang S, et al. Conferring indirect allospecificity on CD41CD251 Tregs by TCR gene transfer favors transplantation tolerance in mice. J Clin Invest. 2008;118(11):3619-3628.
11. Wan Q, Kozhaya L, Imberg K, et al. Probing the effector and suppressive functions of human T cell subsets using antigen-specific engineered T cell receptors. PLoS ONE. 2013;8(2):e56302.
12. Blat D, Zigmond E, Alteber Z, Waks T, Eshhar Z. Suppression of murine colitis and its associated cancer by carcinoembryonic antigen-specific regulatory T cells. Mol Ther. 2014;22(5): 1018-1028.
13. Vonderheide RH, June CH. Engineering T cells for cancer: our synthetic future. Immunol Rev. 2014;257(1):7-13.
14. Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368(16): 1509-1518.
15. Kalos M, June CH. Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. Immunity. 2013;39(1):49-60.
16. Fransson M, Piras E, Burman J, et al. CAR/FoxP3-engineered T regulatory cells target the CNS and suppress EAE upon intranasal delivery. J Neuroinflammation. 2012;9:112.
17. Jethwa H, Adami AA, Maher J. Use of genemodified regulatory T-cells to control autoimmune and alloimmune pathology: is now the right time? Clin Immunol. 2014;150(1):51-63.
18. Plesa G, Zheng L, Medvec A, et al. TCR affinity and specificity requirements for human regulatory T-cell function. Blood. 2012;119(15):3420-3430.
19. James EA, Kwok WW, Ettinger RA, Thompson AR, Pratt KP. T-cell responses over time in a mild hemophilia A inhibitor subject: epitope identification and transient immunogenicity of the corresponding self-peptide. J Thromb Haemost. 2007;5(12):2399-2407.
20. Ettinger RA, James EA, Kwok WW, Thompson AR, Pratt KP. Lineages of human T-cell clones, including T helper 17/T helper 1 cells, isolated at different stages of anti-factor VIII immune responses. Blood. 2009;114(7):1423-1428.
21. Wä S, Kumari S, Fallang LE, et al. Invariant chain as a vehicle to load antigenic peptides on human MHC class I for cytotoxic T-cell activation. Eur J Immunol. 2013;44(3):774-784.
22. Yang S, Cohen CJ, Peng PD, et al. Development of optimal bicistronic lentiviral vectors facilitates high-level TCR gene expression and robust tumor cell recognition. Gene Ther. 2008;15(21): 1411-1423.
23. Thornton AM, Piccirillo CA, Shevach EM. Activation requirements for the induction of CD41CD251 T cell suppressor function. Eur J Immunol. 2004;34(2):366-376.
24. Thornton AM, Donovan EE, Piccirillo CA, Shevach EM. Cutting edge: IL-2 is critically required for the in vitro activation of CD41CD251 T cell suppressor function. J Immunol. 2004; 172(11):6519-6523.
25. Bi L, Lawler AM, Antonarakis SE, High KA, Gearhart JD, Kazazian HH Jr. Targeted disruption of the mouse factor VIII gene produces a model of haemophilia A. Nat Genet. 1995;10(1):119-121.
26. Moise L, Song C, Martin WD, Tassone R, De Groot AS, Scott DW. Effect of HLA DR epitope de-immunization of Factor VIII in vitro and in vivo. Clin Immunol. 2012;142(3):320-331.
27. Pratt KP, Qian J, Ellaban E, et al. Immunodominant T-cell epitopes in the factor VIII C2 domain are located within an inhibitory antibody binding site. Thromb Haemost. 2004; 92(3):522-528.
28. Hausl C, Ahmad RU, Schwarz HP, et al. Preventing restimulation of memory B cells in hemophilia A: a potential new strategy for the treatment of antibody-dependent immune disorders. Blood. 2004;104(1):115-122.
29. Hausl C, Ahmad RU, Sasgary M, et al. High-dose factor VIII inhibits factor VIII-specific memory B cells in hemophilia A with factor VIII inhibitors. Blood. 2005;106(10):3415-3422.
30. Tunnacliffe A, Kefford R, Milstein C, Forster A, Rabbitts TH. Sequence and evolution of the human T-cell antigen receptor beta-chain genes. Proc Natl Acad Sci USA. 1985;82(15):5068-5072.
31. Rabbitts TH, Lefranc MP, Stinson MA, et al. The chromosomal location of T-cell receptor genes and a T cell rearranging gene: possible correlation with specific translocations in human T cell leukaemia. EMBO J. 1985;4(6):1461-1465.
32. Miller DG, Edwards RH, Miller AD. Cloning of the cellular receptor for amphotropic murine retroviruses reveals homology to that for gibbon ape leukemia virus. Proc Natl Acad Sci USA. 1994;91(1):78-82.
33. Stockis J, Colau D, Coulie PG, Lucas S. Membrane protein GARP is a receptor for latent TGF-beta on the surface of activated human Treg. Eur J Immunol. 2009;39(12):3315-3322.
34. Tran DQ, Andersson J, Wang R, Ramsey H, Unutmaz D, Shevach EM. GARP (LRRC32) is essential for the surface expression of latent TGF-beta on platelets and activated FOXP3+ regulatory T cells. Proc Natl Acad Sci USA. 2009; 106(32):13445-13450.
35. Tran DQ, Andersson J, Hardwick D, Bebris L, Illei GG, Shevach EM. Selective expression of latency-associated peptide (LAP) and IL-1 receptor type I/II (CD121a/CD121b) on activated human FOXP3+ regulatory T cells allows for their purification from expansion cultures. Blood. 2009;113(21):5125-5133.
36. Kim YC, Bhairavabhotla R, Yoon J, et al. Oligodeoxynucleotides stabilize Heliosexpressing Foxp3+ human T regulatory cellsduring in vitro expansion. Blood. 2012;119(12): 2810-2818.
37. Polansky JK, Kretschmer K, Freyer J, et al. DNA methylation controls Foxp3 gene expression. Eur J Immunol. 2008;38(6):1654-1663.
38. Floess S, Freyer J, Siewert C, et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 2007;5(2):e38.
39. Jenabian MA, Seddiki N, Yatim A, et al. Regulatory T cells negatively affect IL-2 production of effector T cells through CD39/adenosine pathway in HIV infection. PLoS Pathog. 2013;9(4):e1003319.
40. Sojka DK, Fowell DJ. Regulatory T cells inhibit acute IFN-g synthesis without blocking T-helper cell type 1 (Th1) differentiation via a compartmentalized requirement for IL-10. Proc Natl Acad Sci USA. 2011;108(45):18336-18341.
41. Ettinger RA, James EA, Kwok WW, Thompson AR, Pratt KP. HLA-DR-restricted T-cell responses to factor VIII epitopes in a mild haemophilia A family with missense substitution A2201P. Haemophilia. 2010;16(102):44-55.
42. Picca CC, Larkin J III, Boesteanu A, Lerman MA, Rankin AL, Caton AJ. Role of TCR specificity in CD41 CD251 regulatory T-cell selection. Immunol Rev. 2006;212:74-85.
43. Larkin J III, Picca CC, Caton AJ. Activation of CD41 CD251 regulatory T cell suppressor function by analogs of the selecting peptide. Eur J Immunol. 2007;37(1):139-146.
44. Larkin J III, Rankin AL, Picca CC, et al. CD41 CD251 regulatory T cell repertoire formationshaped by differential presentation of peptides from a self-antigen. J Immunol. 2008;180(4): 2149-2157.
45. Deal watch: Boosting TRegs to target autoimmune disease. Nat Rev Drug Discov. 2011; 10(8):566.
46. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331(6015): 337-341.
47. Stewart CA, Metheny H, Iida N, et al. Interferondependent IL-10 production by Tregs limits tumor Th17 inflammation. J Clin Invest. 2013;123(11): 4859-4874.
48. Dieckmann D, Plottner H, Berchtold S, Berger T, Schuler G. Ex vivo isolation and characterization of CD4(1)CD25(1) T cells with regulatory properties from human blood. J Exp Med. 2001; 193(11):1303-1310.
49. Maynard CL, Harrington LE, Janowski KM, et al. Regulatory T cells expressing interleukin 10 develop from Foxp31 and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol. 2007;8(9):931-941.
50. Hoffman BE, Martino AT, Sack BK, et al. Nonredundant roles of IL-10 and TGF-b in suppression of immune responses to hepatic AAV-factor IX gene transfer. Mol Ther. 2011; 19(7):1263-1272.
51. MacDonald K, Orban P, Bramson, J., Levings M. Engineering antigen specific T regulatory cells for transplant tolerance. J Immunol. 2013;190(69):12.