Elevation of Intracellular Cyclic AMP in Alloreactive CD4+ T Cells Induces Alloantigen-Specific Tolerance That Can Prevent GVHD Lethality In Vivo

Biology of Blood and Marrow Transplantation

Volumn 13, Issue 5, 2007, Pages 530-542

  O'Shaughnessy, Matthew J ^a   Chen, Zong Ming ^a   Gramaglia, Irene ^a   Taylor, Patricia A ^a   Panoskaltsis Mortari, Angela ^a   Vogtenhuber, Christine ^a   Palmer, Ed ^b   Grader Beck, Thomas ^c   Boussiotis, Vassiliki A ^c   Blazar, Bruce R ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

GVHD; Immune response; Mice; T cells; Tolerance; Transgenic

Indexed keywords

8 BROMO CYCLIC AMP; ALLOANTIGEN; BROMIDE; CYCLIC AMP; INTERLEUKIN 2; ISOBUTYLMETHYLXANTHINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGENIC AGENT; PHOSPHODIESTERASE;

ALLOIMMUNITY; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIVISION; CELL LABELING; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME INHIBITION; EX VIVO STUDY; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; LETHALITY; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; MOUSE; NONHUMAN; REGULATORY MECHANISM; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

1-METHYL-3-ISOBUTYLXANTHINE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL TRANSPLANTATION; CYCLIC AMP; GRAFT VS HOST DISEASE; IMMUNE TOLERANCE; ISOANTIBODIES; LYMPHOCYTE CULTURE TEST, MIXED; MICE; MICE, TRANSGENIC; PHOSPHODIESTERASE INHIBITORS; SURVIVAL ANALYSIS;

EID: 34247122701     PISSN: 10838791     EISSN: 15236536     Source Type: Journal    
DOI: 10.1016/j.bbmt.2007.01.071     Document Type: Article

References (39)

1. Dumont J.E., Jauniaux J.C., and Roger P.P. The cyclic AMP-mediated stimulation of cell proliferation. Trends Biochem Sci. 14 (1989) 67-71
2. Blomhoff H.K., Blomhoff R., Stokke T., et al. cAMP-mediated growth inhibition of a B-lymphoid precursor cell line Reh is associated with an early transient delay in G2/M, followed by an accumulation of cells in G1. J Cell Physiol. 137 (1988) 583-587
3. Dugan L.L., Kim J.S., Zhang Y., et al. Differential effects of cAMP in neurons and astrocytes. Role of B-raf. J Biol Chem. 274 (1999) 25842-25848
4. Bielekova B., Lincoln A., McFarland H., and Martin R. Therapeutic potential of phosphodiesterase-4 and -3 inhibitors in Th1-mediated autoimmune diseases. J Immunol. 164 (2000) 1117-1124
5. Chen D., and Rothenberg E.V. Interleukin 2 transcription factors as molecular targets of cAMP inhibition: delayed inhibition kinetics and combinatorial transcription roles. J Exp Med. 179 (1994) 931-942
6. Hofmann B., Nishanian P., Nguyen T., Insixiengmay P., and Fahey J.L. Human immunodeficiency virus proteins induce the inhibitory cAMP/protein kinase A pathway in normal lymphocytes. Proc Natl Acad Sci U S A 90 (1993) 6676-6680
7. Aandahl E.M., Aukrust P., Skalhegg B.S., et al. Protein kinase A type I antagonist restores immune responses of T cells from HIV-infected patients. FASEB J 12 (1998) 855-862
8. Boussiotis V.A., Freeman G.J., Taylor P.A., et al. p27kip1 functions as an anergy factor inhibiting interleukin 2 transcription and clonal expansion of alloreactive human and mouse helper T lymphocytes. Nat Med. 6 (2000) 290-297
9. Kammer G.M. The adenylate cyclase-cAMP-protein kinase A pathway and regulation of the immune response. Immunol Today 9 (1988) 222-229
10. Skalhegg B.S., Tasken K., Hansson V., Huitfeldt H.S., Jahnsen T., and Lea T. Location of cAMP-dependent protein kinase type I with the TCR-CD3 complex. Science 263 (1994) 84-87
11. Vang T., Torgersen K.M., Sundvold V., et al. Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T cell receptor. J Exp Med. 193 (2001) 497-507
12. Powell J.D., Lerner C.G., Ewoldt G.R., and Schwartz R.H. The -180 site of the IL-2 promoter is the target of CREB/CREM binding in T cell anergy. J Immunol. 163 (1999) 6631-6639
13. Ramstad C., Sundvold V., Johansen H.K., and Lea T. cAMP-dependent protein kinase (PKA) inhibits T cell activation by phosphorylating ser-43 of raf-1 in the MAPK/ERK pathway. Cell Signal 12 (2000) 557-563
14. Naderi S., Gutzkow K.B., Christoffersen J., Smeland E.B., and Blomhoff H.K. cAMP-mediated growth inhibition of lymphoid cells in G1: rapid down-regulation of cyclin D3 at the level of translation. Eur J Immunol. 30 (2000) 1757-1768
15. Kaminuma O., Mori A., Wada K., et al. A selective type 4 phosphodiesterase inhibitor, T-440, modulates intracellular cyclic AMP level and interleukin-2 production of Jurkat cells. Immunopharmacology 38 (1998) 247-252
16. Rascon A., Soderling S.H., Schaefer J.B., and Beavo J.A. Cloning and characterization of a cAMP-specific phosphodiesterase (TbPDE2B) from Trypanosoma brucei. Proc Natl Acad Sci U S A 99 (2002) 4714-4719
17. Spina D. Phosphodiesterase-4 inhibitors in the treatment of inflammatory lung disease. Drugs 63 (2003) 2575-2594
18. Rabe K.F., Bateman E.D., O'Donnell D., Witte S., Bredenbroker D., and Bethke T.D. Roflumilast-an oral anti-inflammatory treatment for chronic obstructive pulmonary disease: a randomised controlled trial. Lancet 366 (2005) 563-571
19. Mann S.C., Andrews P.A., and Howell S.B. Modulation of cis-diamminedichloroplatinum(II) accumulation and sensitivity by forskolin and 3-isobutyl-1-methylxanthine in sensitive and resistant human ovarian carcinoma cells. Int J Cancer 48 (1991) 866-872
20. Barnden M.J., Allison J., Heath W.R., and Carbone F.R. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol Cell Biol. 76 (1998) 34-40
21. Backstrom B.T., Muller U., Hausmann B., and Palmer E. Positive selection through a motif in the alphabeta T cell receptor. Science 281 (1998) 835-838
22. Chen Z.M., O'Shaughnessy M.J., Gramaglia I., et al. IL-10 and TGF-beta induce alloreactive CD4+CD25- T cells to acquire regulatory cell function. Blood 101 (2003) 5076-5083
23. Brice G.T., Riley J.L., Villinger F., et al. Development of an animal model for autotransfusion therapy: in vitro characterization and analysis of anti-CD3/CD28 expanded cells. J Acquir Immune Defic Syndr Hum Retrovirol. 19 (1998) 210-220
24. Gudmundsdottir H., Wells A.D., and Turka L.A. Dynamics and requirements of T cell clonal expansion in vivo at the single-cell level: effector function is linked to proliferative capacity. J Immunol. 162 (1999) 5212-5223
25. Boussiotis V.A., Barber D.L., Nakarai T., et al. Prevention of T cell anergy by signaling through the gamma c chain of the IL-2 receptor. Science 266 (1994) 1039-1042
26. Taube M., Svensson L., and Carlsten H. T lymphocytes are not the target for estradiol-mediated suppression of DTH in reconstituted female severe combined immunodeficient (SCID) mice. Clin Exp Immunol 114 (1998) 147-153
27. Boussiotis V.A., Barber D.L., Lee B.J., Gribben J.G., Freeman G.J., and Nadler L.M. Differential association of protein tyrosine kinases with the T cell receptor is linked to the induction of anergy and its prevention by B7 family-mediated costimulation. J Exp Med. 184 (1996) 365-376
28. Boussiotis V.A., Chen Z.M., Zeller J.C., et al. Altered T-cell receptor + CD28-mediated signaling and blocked cell cycle progression in interleukin 10 and transforming growth factor-beta-treated alloreactive T cells that do not induce graft-versus-host disease. Blood 97 (2001) 565-571
29. Cone R.E., Cochrane R., Lingenheld E.G., and Clark R.B. Elevation of intracellular cyclic AMP induces an anergic-like state in Th1 clones. Cell Immunol. 173 (1996) 246-251
30. Blazar B.R., Korngold R., and Vallera D.A. Recent advances in graft-versus-host disease (GVHD) prevention. Immunol Rev. 157 (1997) 79-109
31. Lanotte M., Riviere J.B., Hermouet S., et al. Programmed cell death (apoptosis) is induced rapidly and with positive cooperativity by activation of cyclic adenosine monophosphate-kinase I in a myeloid leukemia cell line. J Cell Physiol. 146 (1991) 73-80
32. Myklebust J.H., Josefsen D., Blomhoff H.K., et al. Activation of the cAMP signaling pathway increases apoptosis in human B-precursor cells and is associated with downregulation of Mcl-1 expression. J Cell Physiol. 180 (1999) 71-80
33. Powell J.D., Lerner C.G., and Schwartz R.H. Inhibition of cell cycle progression by rapamycin induces T cell clonal anergy even in the presence of costimulation. J Immunol. 162 (1999) 2775-2784
34. Grader-Beck T., van Puijenbroek A.A., Nadler L.M., and Boussiotis V.A. cAMP inhibits both Ras and Rap1 activation in primary human T lymphocytes, but only Ras inhibition correlates with blockade of cell cycle progression. Blood 101 (2003) 998-1006
35. Mohapatra S., Agrawal D., and Pledger W.J. p27Kip1 regulates T cell proliferation. J Biol Chem. 276 (2001) 21976-21983
36. Schwartz R.H. Models of T cell anergy: is there a common molecular mechanism?. J Exp Med. 184 (1996) 1-8
37. Blazar B.R., Taylor P.A., Noelle R.J., and Vallera D.A. CD4(+) T cells tolerized ex vivo to host alloantigen by anti-CD40 ligand (CD40L:CD154) antibody lose their graft-versus-host disease lethality capacity but retain nominal antigen responses. J Clin Invest. 102 (1998) 473-482
38. Taylor P.A., Panoskaltsis-Mortari A., Noelle R.J., and Blazar B.R. Analysis of the requirements for the induction of CD4+ T cell alloantigen hyporesponsiveness by ex vivo anti-CD40 ligand antibody. J Immunol. 164 (2000) 612-622
39. Wang L., Liu F., and Adamo M.L. Cyclic AMP inhibits extracellular signal-regulated kinase and phosphatidylinositol 3-kinase/Akt pathways by inhibiting Rap1. J Biol Chem. 276 (2001) 37242-37249