cAMP inhibits both Ras and Rap1 activation in primary human T lymphocytes, but only Ras inhibition correlates with blockade of cell cycle progression

Blood

Volumn 101, Issue 3, 2003, Pages 998-1006

  Grader Beck, Thomas ^a   Van Puijenbroek, Andre A F L ^a   Nadler, Lee M ^a   Boussiotis, Vassiliki A ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CARRIER PROTEINS AND BINDING PROTEINS; CD28 ANTIGEN; CD3 ANTIGEN; CYCLIC AMP; CYTOKINE; FORSKOLIN; ISOBUTYLMETHYLXANTHINE; LAT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PHORBOL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE ZAP 70; RAP PROTEIN; RAS PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

EID: 0037306635     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2002-06-1665     Document Type: Article

References (56)

1. 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. 1998;38:247-252.
2. Soderling SH, Bayuga SJ, Beavo JA. Cloning and characterization of a cAMP-specific cyclic nucleotide phosphodiesterase. Proc Natl Acad Sci U S A. 1998;95:8991-8996.
3. Dumont JE, Jauniaux JC, Roger PP. The cyclic AMP-mediated stimulation of cell proliferation. Trends Biochem Sci. 1989;14:67-71.
4. Blomhoff HK, 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. 1988;137:583-587.
5. Dugan LL, Kim JS, Zhang Y, et al. Differential effects of cAMP in neurons and astrocytes. Role of B-raf. J Biol Chem. 1999;274:25842-25848.
6. Anastasiou ED, Paliogianni F, Balow JP, Yamada H, Boumpas DT. Prostaglandin E2 and other cyclic AMP-elevated agents modulate IL-2 and IL-2R alpha gene expression at multiple levels. J Immunol. 1992;148:2845-2852.
7. Chen D, Rothenberg EV. Interleukin 2 transcription factors as molecular targets of cAMP inhibition: delayed inhibition kinetics and combinatorial transcription roles. J Exp Med. 1994;179:931-942.
8. Bielekova B, Lincoln A, McFarland H, Martin R. Therapeutic potential of phosphodiesterase-4 and -3 inhibitors in Th1-mediated autoimmune diseases. J. Immunol. 2000;164:1117-1124.
9. Kammer GM. The adenylate cyclase-cAMP-protein kinase A pathway and regulation of the immune response. Immunol Today. 1988;9:222-229.
10. Skalhegg BS, Tasken K, Hansson V, Huitfeldt HS, Jahnsen T, Lea T. Location of cAMP-dependent protein kinase type I with the TCR-CD3 complex. Science. 1994;263:84-87.
11. Hofmann B, Nishanian P, Nguyen T, Insixiengmay P, Fahey JL. Human immunodeficiency virus proteins induce the inhibitory cAMP/protein kinase A pathway in normal lymphocytes. Proc Natl Acad Sci U S A. 1993;90:6676-6680.
12. Aandahl EM, Aukrust P, Skalhegg BS, et al. Protein kinase A type I antagonist restores immune responses of T cells from HIV-infected patients. FASEB J. 1998;12:855-862.
13. Aukrust P, Aandahl EM, Skalhegg BS, et al. Increased activation of protein kinase A type I contributes to the T cell deficiency in common variable immunodeficiency. J Immunol. 1999;162:1178-1185.
14. Boussiotis VA, Freeman GF, Taylor PA, et al. p27kip1 functions as an anergy factor inhibiting IL-2 transcription and clonal expansion of allo-reactive human and murine helper T lymphocytes. Nat Med. 2000;6:290-297.
15. Barton K, Muthusamy N, Chanyangam M, Fischer C, Clendenin C, Leiden JM. Defective thymocyte proliferation and IL-2 production in transgenic mice expressing a dominant-negative form of CREB. Nature. 1996;379:81-85.
16. Powell JD, Lerner CG, Ewoldt GR, Schwartz RH. The -180 site of the IL-2 promoter is the target of CREB/CREM binding in T cell anergy. J Immunol. 1999;163:6631-6639.
17. Li L, Yee C, Beavo JA. CD3- and CD28-dependent induction of PDE7 required for T cell activation. Science. 1999;263:646-651.
18. Appleman LJ, van Puijenbroek AA, Shu KM, Nadler LM, Boussiotis VA. CD28 costimulation mediates down-regulation of p27(kip1) and cell cycle progression by activation of the PI3K/PKB signaling pathway in primary human T cells. J Immunol. 2002;168:2729-2736.
19. Reedquist KA, Bos JL. Costimulation through CD28 suppresses T cell receptor-dependent activation of the Ras-like small GTPase Rap1 in human T lymphocytes. J Bio. Chem. 1998;273:4944-4949.
20. Tzachanis D, Freeman GJ, Hirano N, et al. Tob is a negative regulator of activation that is expressed in anergic and quiescent T cells. Nat Immunol. 2001;2:1174-1182.
21. Ebinu JO, Bottorff DA, Chan EY, Stang SL, Dunn RJ, Stone JC. RasGRP, a Ras guanyl nucleotide-releasing protein with calcium- and diacylglycerol binding motifs. Science. 1998;280:1082-1086.
22. Yamashita S, Mochizuki N, Ohba Y, et al. CalDAG-GEFIII activation of Ras, R-ras, and Rap1. J Biol Chem. 2000;275:25488-25493.
23. Appleman LJ, Berezovskaya A, Grass I, Boussiotis VA. CD28 costimulation mediates T cell expansion via IL-2 independent and IL-2 dependenl regulation of cell cycle progression. J Immunol. 2000;164:144-151.
24. Chen C-H, Zhang D-H, LaPorte JM, Ray A. Cyclic AMP activates p38 mitogen-activated protein kinase in Th2 cells: phosphorylation of GATA-3 and stimulation of Th2 cytokine gene expression. J Immunol. 2000;165:5597-5605.
25. Kang SM, Beverly B, Tran AC, Brorson K, Schwartz RH, Lenardo MJ. Transactivation by AP-1 is a molecular target of T cell clonal energy. Science. 1992;257:1134-1138.
26. Mondino A, Whaley CD, DeSilva DR, Li W, Jenkins MK, Mueller D. Defective transcription of the IL-2 gene is associated with impaired expression of c-Fos, FosB and JunB in anergic T helper 1 cells. J Immunol. 1996;157:2048-2057.
27. Wang L, Liu F, Adamo ML. Cyclic AMP inhibits extracellular signal-regulated kinase and phosphatidylinositol 3-kinase/Akt pathways by inhibiting Rap1. J. Cell. Biol. 2001;40:37242-37249
28. Marshall CJ. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr Opin Genet Dev. 1994;4:82-89.
29. Cook SJ, Rubinfeld B, Albert I, McCormic F. RapV12 antagonizes Ras-dependent activation of ERK1 and ERK2 by LPA and EGF in Rat-1 fibroblasts. EMBO J. 1993;12:3475-3485.
30. Ramstad C, Sundvold V, Johansen HK, 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. 2000;12:557-563.
31. Altschuler D, Lapentina EG. Mutational analysis of the cAMP-dependent protein kinase-mediated phosphorylation site of Rap1b. J Biol Chem. 1993;268:7527-7531.
32. Altschuler DL, Peterson SN, Ostrowski MC, Lapentina EG. Cyclic AMP-dependent activation of Rap1b. J Biol Chem. 1995;270:10373-10376.
33. de Rooij J, Zwartkruis FJ, Verheijen MH, et al. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature. 1998;396:416-417.
34. Kawasaki H, Springett GM, Toki S, et al. A Rap guanine nucleotide exchange factor enriched highly in the basal ganglia, Proc Natl Acad Sci U S A. 1998;95:13278-13283.
35. Jin TG, Satoh T, Liao Y, et al. Role of the CDC25 homology domain of phospholipase Cepsilon in amplification of Rap1-dependent signaling. J Biol Chem. 2001;276:30301-30307.
36. Downward J, Graves JD, Warne S, Rayter S, Cantrell DA. Stimulation of p21 ras upon T-cell activation. Nature. 1990;346:719-723.
37. Wittinghofer A. Signal transduction via Ras. Biol Chem. 1998;379:933-937.
38. Sieh M, Batzar A, Schlessinger J, Weiss A. GRB2 and phospholipase C-gamma 1 associate with a 36- to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol Cell Biol. 1994;14:4435-4442.
39. Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell. 1998;92:83-92.
40. Leevers SJ, Paterson HF, Marshall CJ. Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature. 1994;369:411-414.
41. Stokoe D, Macdonald SG, Cadwallader K, Symonsa M, Hancock JF. Activation of Ras as a result of recruitment to the plasma membrane. Science. 1994;264:1463-1467.
42. de Vries-Smits AM, Burgering BM, Leevers SJ, Marshall CJ, Bos JL. Involvement of p21 ras in activation of extracellular signal-regulated kinase 2. Nature. 1992;357:602-604.
43. Vang T, Torgersen KM, 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. 2001;193:497-507.
44. Cass LA, Summers SA, Prendergast GV, Backer JM, Birnbaum MJ, Meinkoth JL. Protein kinase A-dependent and -independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol Cell Biol. 1999;19:5882-5891.
45. Gotoh T, Hattori S, Nakamura S, et al. Identification of Rap1 as a Target for the crk SH3 domain binding guanine nucleotide-releasing factor C3G. Mol Cell Biol. 1995;15:6746-6753.
46. Kawasaki H, Springett GM, Mochizuki N, et al. A family of cAMP-binding proteins that directly activate Rap1. Science. 1998;282:2275-2279.
47. Nassar N, Horn G, Herrmann C, Scherer A, McCormick F, Wittinghofer A. The 2.2 A crystal structure of the Ras-binding domain of the serine/threonine kinase c-Rafl in complex with Rap1 A and a GTP analogue. Nature. 1995;375:554-560.
48. Boussiotis VA, Freeman GJ, Berezovskaya A, Barber DL, Nadler LM. Maintenance of human T cell anergy: blocking of IL-2 gene transcription by activated Rap1. Science. 1997;278:124-128.
49. Cook SJ, McCormick F. Inhibition by cAMP of Ras-dependent activation of Raf. Science. 1993;262:1069-1072.
50. Vossler MR, Yao H, York RD, Pan M, Rim CS, Stork PJ. cAMP activates MAP kinase and Elk-1 through a B-Raf-and Rap1-dependent pathway. Cell. 1997;89:73-82.
51. Schmitt JM, Stork PJS. Cyclic AMP-mediated inhibition of cell growth requires the small protein Rap1. Mol Cell Biol. 2001;21:3671-3663.
52. Cass LA, Meinkoth JL. Differential effects of cyclic adenosine 3′,5′-monophosphate on p70 ribosomal S6 kinase. Endocrinology. 1998;139:1991-1998.
53. Gonzalez-Robayna IJ, Alliston TN, Buse P, Firestone GL, Richards JS. Functional and subcellular changes in the A-kinase-signaling pathway: relation to aromatase and Sgk expression during the transition of granulosa cells to luteal cells. Mol Endocrinol. 1999;13:1318-1337.
54. Mei FC, Qiao J, Tsygankova OM, Meinkoth JL, Quilliam LA, Cheng X. Differential signaling of cyclic AMP: opposing effects of exchange protein directly activated by cyclic AMP and cAMP-dependent protein kinase on protein kinase B activation. J Biol Chem. 2002;277:11497-11504.
55. Tsygankova OM, Saavedra A, Rebhun JF, Quilliam LA, Meinkoth JL. Coordinated regulation of Rap1 and thyroid differentiation by cyclic AMP and protein kinase A. Mol Cell Biol. 2001;21:1921-1929.
56. Kim S, Jee K, Kim D, Koh H, Chung J. Cyclic AMP inhibits Akt activity by blocking the membrane localization of PDK1. J Biol Chem. 2001;276:12864-12870.