Rosmarinic acid inhibits Ca2+-dependent pathways of T-cell antigen receptor-mediated signaling by inhibiting the PLC-γ1 and Itk activity

Blood

Volumn 101, Issue 9, 2003, Pages 3534-3542

  Kang, Mi Ae ^b   Yun, Su Young ^b   Won, Jonghwa ^a  

^a Mogam Biotechnology Research Institute   (South Korea)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; INDUCIBLE T CELL KINASE; INOSITOL 1,4,5 TRISPHOSPHATE; INTERLEUKIN 2; ISOENZYME; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C GAMMA1; PROTEIN TYROSINE KINASE; ROSMARINIC ACID; SERINE; T LYMPHOCYTE RECEPTOR; THREONINE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT; TYROSINE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CINNAMIC ACID DERIVATIVE; DEPSIDE; DNA BINDING PROTEIN; EMT PROTEIN TYROSINE KINASE; EMT PROTEIN-TYROSINE KINASE; ENZYME INHIBITOR; GRB2 PROTEIN, HUMAN; GRB2 PROTEIN, MOUSE; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; LAT PROTEIN, HUMAN; LAT PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NONSTEROID ANTIINFLAMMATORY AGENT; NUCLEAR PROTEIN; OKT 3; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEIN; PROTEIN; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SLP 76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; SLP-76 SIGNAL TRANSDUCING ADAPTOR PROTEINS; TRANSCRIPTION FACTOR; ZAP70 PROTEIN, HUMAN; ZAP70 PROTEIN, MOUSE;

ARTICLE; CALCIUM MOBILIZATION; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CALCIUM SIGNALING; DRUG ANTAGONISM; ENZYME ACTIVATION; ENZYMOLOGY; IMMUNOLOGY; LEUKEMIA CELL LINE; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CALCIUM SIGNALING; CARRIER PROTEINS; CINNAMATES; DEPSIDES; DNA-BINDING PROTEINS; ENZYME ACTIVATION; ENZYME INHIBITORS; GRB2 ADAPTOR PROTEIN; HUMANS; JURKAT CELLS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MUROMONAB-CD3; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE KINASES; PROTEINS; RECEPTORS, ANTIGEN, T-CELL; TRANSCRIPTION FACTORS; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 0038204157     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2002-07-1992     Document Type: Article

References (64)

1. al-Sereiti MR, Abu-Amer KM, Sen P. Pharmacology of rosemary (Rosmarinus officinalis Linn.) and its therapeutic potentials. Indian J Exp Biol. 1999;37:124-130.
2. Zheng W, Wang SY. Antioxidant activity and phenolic compounds in selected herbs. J Agric Food Chem. 2001;49:5165-5170.
3. van Kessel KP, Kalter ES, Verhoef J. Rosmarinic acid inhibits external oxidative effects of human polymorphonuclear granulocytes. Agents Actions. 1986;17:375-376.
4. Sahu A, Rawal N, Pangburn MK. Inhibition of complement by covalent attachment of rosmarinic acid to activated C3b. Biochem Pharmacol. 1999;57:1439-1446.
5. Kimura Y, Okuda H, Okuda T, Hatano T, Arichi S. Studies on the activities of tannins and related compounds, X: effects of caffeetannins and related compounds on arachidonate metabolism in human polymorphonuclear leukocytes. J Nat Prod. 1987;50:392-399.
6. Kelm MA, Nair MG, Strasburg GM, DeWitt DL. Antioxidant and cyclooxygenase inhibitory phenolic compounds from Ocimum sanctum Linn. Phytomedicine. 2000;7:7-13.
7. Englberger W, Hadding U, Etschenberg E, et al. Rosmarinic acid: a new inhibitor of complement C3-convertase with anti-inflammatory activity. Int J Immunopharmacol. 1988;10:729-737.
8. Goldman FD, Gilman AL, Hollenback C, Kato RM, Premack BA, Rawlings DJ. Hydroxychloroquine inhibits calcium signals in T cells: a new mechanism to explain its immunomodulatory properties. Blood. 2000;95:3460-3466.
9. Paccani SR, Boncristiano M, Ulivieri C, D'Elios MM, Del Prete G, Baldari CT. Nonsteroidal anti-inflammatory drugs suppress T-cell activation by inhibiting p38 MAPK induction. J Biol Chem. 2002;277:1509-1513.
10. Ho LJ, Chang DM, Chang ML, Kuo SY, Lai JH. Mechanism of immunosuppression of the anti-rheumatic herb TWHf in human T cells. J Rheumatol. 1999;26:14-24.
11. Xu X, Williams JW, Bremer EG, Finnegan A, Chong AS. Inhibition of protein tyrosine phosphorylation in T cells by a novel immunosuppressive agent, leflunomide. J Biol Chem. 1995;270:12398-12403.
12. Alberola-Ila J, Takaki S, Kerner JD, Perlmutter RM. Differential signaling by lymphocyte antigen receptors. Annu Rev Immunol. 1997;15:125-154.
13. Irving BA, Chan AC, Weiss A. Functional characterization of a signal transducing motif present in the T cell antigen receptor zeta chain. J Exp Med. 1993;177:1093-1103.
14. Irving BA, Weiss A. The cytoplasmic domain of the T cell receptor zeta chain is sufficient to couple to receptor-associated signal transduction pathways. Cell. 1991;64:891-901.
15. Iwashima M, Irving BA, van Oers NS, Chan AC, Weiss A. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science. 1994;263:1136-1139.
16. Letourneur F, Klausner RD. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3 epsilon. Science. 1992;255:79-82.
17. Chan AC, Iwashima M, Turck CW, Weiss A. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain. Cell. 1992;71:649-662.
18. Wardenburg JB, Fu C, Jackman JK, et al. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J Biol Chem. 1996;271:19641-19644.
19. Yablonski D, Kuhne MR, Kadlecek T, Weiss A. Uncoupling of nonreceptor tyrosine kinases from PLC-gamma1 in an SLP-76-deficient T cell. Science. 1998;281:413-416.
20. 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.
21. Clements JL, Yang B, Ross-Barta SE, et al. Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science. 1998;281:416-419.
22. Dewulf L, Hendrickx B, Lesaffre E. Epidemiological data of patients treated with fluvoxamine: results from a 12 week non-comparative multicentre study. Int Clin Psychopharmacol. 1995;9(Suppl 4):67-72.
23. Sieh M, Batzer 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.
24. Gilliland LK, Schieven GL, Norris NA, Kanner SB, Aruffo A, Ledbetter JA. Lymphocyte lineage-restricted tyrosine-phosphorylated proteins that bind PLC gamma 1 SH2 domains. J Biol Chem. 1992;267:13610-13616.
25. Buday L, Egan SE, Rodriguez Viciana P, Cantrell DA, Downward J. A complex of Grb2 adaptor protein, Sos exchange factor, and a 36-kDa membrane-bound tyrosine phosphoprotein is implicated in ras activation in T cells. J Biol Chem. 1994;269:9019-9023.
26. Perez-Villar JJ, Kanner SB. Regulated association between the tyrosine kinase Emt/Itk/Tsk and phospholipase-C gamma 1 in human T lymphocytes. J Immunol. 1999;163:6435-6441.
27. Bunnell SC, Diehn M, Yaffe MB, Findell PR, Cantley LC, Berg LJ. Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J Biol Chem. 2000;275:2219-2230.
28. Wange RL. LAT, the linker for activation of T cells: a bridge between T cell-specific and general signaling pathways. Sci STKE. 2000(63):RE1.
29. Zhang W, Samelson LE. The role of membrane-associated adaptors in T cell receptor signalling. Semin Immunol. 2000;12:35-41.
30. Myung PS, Boerthe NJ, Koretzky GA. Adapter proteins in lymphocyte antigen-receptor signaling. Curr Opin Immunol. 2000;12:256-266.
31. Hughes AR, Putney JW Jr. Metabolism and functions of inositol phosphates. Biofactors. 1988;1:117-121.
32. Nishibe S, Wahl MI, Hernandez-Sotomayor SM, Tonks NK, Rhee SG, Carpenter G. Increase of the catalytic activity of phospholipase C-gamma 1 by tyrosine phosphorylation. Science. 1990;250:1253-1256.
33. Kazanietz MG. Eyes wide shut: protein kinase C isozymes are not the only receptors for the phorbol ester tumor promoters. Mol Carcinog. 2000;28:5-11.
34. Scharenberg AM, Kinet JP. Ptdins-3,4,5-P3: a regulatory nexus between tyrosine kinases and sustained calcium signals. Cell. 1998;94:5-8.
35. Crabtree GR. Contingent genetic regulatory events in T lymphocyte activation. Science. 1989;243:355-361.
36. Cantrell D. T cell antigen receptor signal transduction pathways. Annu Rev Immunol. 1996;14:259-274.
37. Kolch W, Heidecker G, Kochs G, et al. Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature. 1993;364:249-252.
38. Marais R, Light Y, Mason C, Paterson H, Olson MF, Marshall CJ. Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science. 1998;280:109-112.
39. Ueda Y, Hirai S, Osada S, Suzuki A, Mizuno K, Ohno S. Protein kinase C activates the MEK-ERK pathway in a manner independent of Ras and dependent on Raf. J Biol Chem. 1996;271:23512-23519.
40. Carroll MP, May WS. Protein kinase C-mediated serine phosphorylation directly activates Raf-1 in murine hematopoietic cells. J Biol Chem. 1994;269:1249-1256.
41. 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.
42. Lorenzo PS, Beheshti M, Pettit GR, Stone JC, Blumberg PM. The guanine nucleotide exchange factor RasGRP is a high-affinity target for diacylglycerol and phorbol esters. Mol Pharmacol. 2000;57:840-846.
43. Tognon CE, Kirk HE, Passmore LA, Whitehead IP, Der CJ, Kay RJ. Regulation of RasGRP via a phorbol ester-responsive C1 domain. Mol Cell Biol. 1998;18:6995-7008.
44. Clements JL, Boerth NJ, Lee JR, Koretzky GA. Integration of T cell receptor-dependent signaling pathways by adapter proteins. Annu Rev Immunol. 1999;17:89-108.
45. Pawson T, Saxton TM. Signaling networks - do all roads lead to the same genes? Cell. 1999;97:675-678.
46. Dong Y, Zeng CQ, Ball JM, Estes MK, Morris AP. The rotavirus enterotoxin NSP4 mobilizes intracellular calcium in human intestinal cells by stimulating phospholipase C-mediated inositol 1,4,5-triphosphate production. Proc Natl Acad Sci U S A. 1997;94:3960-3965.
47. Won J, Hur Y-G, Hur EM, et al. Rosmarinic acid inhibits TCR-induced T cell activation and proliferation in an Lck-dependent manner. Eur J Immunol. In press.
48. Carpenter G, Ji Q. Phospholipase C-gamma as a signal-transducing element. Exp Cell Res. 1999;253:15-24.
49. Heyeck SD, Wilcox HM, Bunnell SC, Berg LJ. Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J Biol Chem. 1997;272:25401-25408.
50. Veillette A, Fournel M. The CD4 associated tyrosine protein kinase p561ck is positively regulated through its site of autophosphorylation. Oncogene. 1990;5:1455-1462.
51. Schroder AJ, Quehl P, Muller J, Samstag Y. Conversion of p56(lck) to p60(lck) in human peripheral blood T lymphocytes is dependent on co-stimulation through accessory receptors: involvement of phospholipase C, protein kinase C and MAP-kinases in vivo. Eur J Immunol. 2000;30:635-643.
52. Finco TS, Kadlecek T, Zhang W, Samelson LE, Weiss A. LAT is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity. 1998;9:617-626.
53. Zhang W, Irvin BJ, Trible RP, Abraham RT, Samelson LE. Functional analysis of LAT in TCR-mediated signaling pathways using a LAT-deficient Jurkat cell line. Int Immunol. 1999;11:943-950.
54. Shan X, Wange RL. Itk/Emt/Tsk activation in response to CD3 cross-linking in Jurkat T cells requires ZAP-70 and Lat and is independent of membrane recruitment. J Biol Chem. 1999;274:29323-29330.
55. Schaeffer EM, Debnath J, Yap G, et al. Requirement for Tec kinases Rlk and Itk in T cell receptor signaling and immunity. Science. 1999;284:638-641.
56. Liu KQ, Bunnell SC, Gurniak CB, Berg LJ. T cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itk-deficient T cells. J Exp Med. 1998;187:1721-1727.
57. Fraser JD, Straus D, Weiss A. Signal transduction events leading to T-cell lymphokine gene expression. Immunol Today. 1993;14:357-362.
58. Rayter SI, Woodrow M, Lucas SC, Cantrell DA, Downward J. p21 ras mediates control of IL-2 gene promoter function in T cell activation. EMBO J. 1992;11:4549-4556.
59. Woodrow MA, Rayter S, Downward J, Cantrell DA. p21 ras function is important for T cell antigen receptor and protein kinase C regulation of nuclear factor of activated T cells. J Immunol. 1993;150:3853-3861.
60. Lin J, Weiss A. Identification of the minimal tyrosine residues required for linker for activation of T cell function. J Biol Chem. 2001;276:29588-29595.
61. Koretzky GA. The role of Grb2-associated proteins in T-cell activation. Immunol Today. 1997;18:401-406.
62. Chau LA, Madrenas J. Phospho-LAT-independent activation of the ras-mitogen-activated protein kinase pathway: a differential recruitment model of TCR partial agonist signaling. J Immunol. 1999;163:1853-1858.
63. August A, Dupont B. Association between mitogen-activated protein kinase and the zeta chain of the T cell receptor (TcR) with the SH2,3 domain of p56lck: differential regulation by TcR cross-linking. J Biol Chem. 1996;271:10054-10059.
64. Blanco-Aparicio C, Torres J, Pulido R. A novel regulatory mechanism of MAP kinases activation and nuclear translocation mediated by PKA and the PTP-SLtyrosine phosphatase. J Cell Biol. 1999;147:1129-1136.