Activation of p38 mitogen-activated protein kinase by norepinephrine in T-lineage cells

Immunology

Volumn 132, Issue 2, 2011, Pages 197-208

  LaJevic, Melissa D ^a   Suleiman, Samia ^b   Cohen, Rhonna L ^b   Chambers, Donald A ^b  

^a University of Illinois at Chicago   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Catecholamine; P38 mitogen activated protein kinase (p38 MAPK); Protein kinase A (PKA); Signal transduction; T cell

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; ADENYLATE CYCLASE; BETA ADRENERGIC RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FAS LIGAND; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NORADRENALIN; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; CATALYSIS; CELL CYCLE REGULATION; CELL DEATH; CELL LINEAGE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; THYMOMA; TRANSCRIPTION REGULATION;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; FAS LIGAND PROTEIN; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; NOREPINEPHRINE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, ADRENERGIC, BETA; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; THYMOMA; THYMUS GLAND; TUMOR CELLS, CULTURED;

EID: 78650930018     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2010.03354.x     Document Type: Article

References (68)

1. Chambers DA, Cohen RL, Perlman RL. Neuroimmune modulation: signal transduction and catecholamines. Neurochem Int 1993; 22:95-110.
2. Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve- an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000; 52:595-638.
3. Leposavic G, Pilipovic I, Radojevic K, Pesic V, Perisic M, Kosec D. Catecholamines as immunomodulators: a role for adrenoceptor-mediated mechanisms in fine tuning of T-cell development. Auton Neurosci 2008; 144:1-12.
4. Gharami K, Das S. Delayed but sustained induction of mitogen-activated protein kinase activity is associated with β-adrenergic receptor-mediated morphological differentiation of astrocytes. J Neurochem 2004; 88:12-22.
5. Pullar CE, Isseroff RR. The β2-adrenergic receptor activates pro-migratory and pro-proliferative pathways in dermal fibroblasts via divergent mechanisms. J Cell Sci 2006; 119:592-602.
6. Yan L, Herrmann V, Hofer JK, Insel PA. β-Adrenergic receptor/cAMP-mediated signaling and apoptosis of S49 lymphoma cells. Am J Physiol Cell Physiol 2000; 279:C1665-74.
7. Barnes PJ. Effect of β-agonists on inflammatory cells. J Allergy Clin Immunol 1999; 104:S10-7.
8. Chambers DA, Martin DW Jr, Weinstein Y. The effect of cyclic nucleotides on purine biosynthesis and the induction of PRPP synthetase during lymphocyte activation. Cell 1974; 3:375-80.
9. Cook-Mills JM, Munshi HG, Perlman RL, Chambers DA. Mouse hepatitis virus infection suppresses modulation of mouse spleen T-cell activation. Immunology 1992; 75:542-5.
10. Cook-Mills JM, Cohen RL, Perlman RL, Chambers DA. Inhibition of lymphocyte activation by catecholamines: evidence for a non-classical mechanism of catecholamine action. Immunology 1995; 85:544-9.
11. Wajeman-Chao SA, Lancaster SA, Graf LH Jr, Chambers DA. Mechanism of catecholamine-mediated destabilization of messenger RNA encoding Thy-1 protein in T-lineage cells. J Immunol 1998; 161:4825-33.
12. Gu C, Ma YC, Benjamin J, Littman D, Chao MV, Huang XY. Apoptotic signaling through the β-adrenergic receptor. A new Gs effector pathway. J Biol Chem 2000; 275:20726-33.
13. Zambon AC, Zhang L, Minovitsky S et al. Gene expression patterns define key transcriptional events in cell-cycle regulation by cAMP and protein kinase A. Proc Natl Acad Sci USA 2005; 102:8561-6.
14. Zhang L, Zambon AC, Vranizan K, Pothula K, Conklin BR, Insel PA. Gene expression signatures of cAMP/protein kinase A (PKA)-promoted, mitochondrial-dependent apoptosis. Comparative analysis of wild-type and cAMP-deathless S49 lymphoma cells. J Biol Chem 2008; 283:4304-13.
15. Krishna M, Narang H. The complexity of mitogen-activated protein kinases (MAPKs) made simple. Cell Mol Life Sci 2008; 65:3525-44.
16. Thornton TM, Rincon M. Non-classical p38 map kinase functions: cell cycle checkpoints and survival. Int J Biol Sci 2009; 5:44-52.
17. Wada T, Penninger JM. Mitogen-activated protein kinases in apoptosis regulation. Oncogene 2004; 23:2838-49.
18. Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res 2005; 15:11-8.
19. Szelenyi J, Selmeczy Z, Brozik A, Medgyesi D, Magocsi M. Dual β-adrenergic modulation in the immune system: stimulus-dependent effect of isoproterenol on MAPK activation and inflammatory mediator production in macrophages. Neurochem Int 2006; 49:94-103.
20. Dobreva ZG, Miteva LD, Stanilova SA. The inhibition of JNK and p38 MAPKs downregulates IL-10 and differentially affects c-Jun gene expression in human monocytes. Immunopharmacol Immunotoxicol 2009; 31:195-201.
21. Hitti E, Iakovleva T, Brook M et al. Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenine/uridine-rich element. Mol Cell Biol 2006; 26:2399-407.
22. Thalhamer T, McGrath MA, Harnett MM. MAPKs and their relevance to arthritis and inflammation. Rheumatology 2008; 47:409-14.
23. Adler HS, Steinbrink K. MAP kinase p38 and its relation to T cell anergy and suppressor function of regulatory T cells. Cell Cycle 2008; 7:169-75.
24. Gong Q, Cheng AM, Akk AM, Alberola-Ila J, Gong G, Pawson T, Chan AC. Disruption of T cell signaling networks and development by Grb2 haploid insufficiency. Nat Immunol 2001; 2:29-36.
25. Hsu SC, Wu CC, Han J, Lai MZ. Involvement of p38 mitogen-activated protein kinase in different stages of thymocyte development. Blood 2003; 101:970-6.
26. Rincon M, Conze D, Weiss L et al. Conference highlight: do T cells care about the mitogen-activated protein kinase signalling pathways? Immunol Cell Biol 2000; 78:166-75.
27. Rincon M, Flavell RA, Davis RJ. The JNK and P38 MAP kinase signaling pathways in T cell-mediated immune responses. Free Radic Biol Med 2000; 28:1328-37.
28. Sohn SJ, Lewis GM, Winoto A. Non-redundant function of the MEK5-ERK5 pathway in thymocyte apoptosis. EMBO J 2008; 27:1896-906.
29. Sugawara T, Moriguchi T, Nishida E, Takahama Y. Differential roles of ERK and p38 MAP kinase pathways in positive and negative selection of T lymphocytes. Immunity 1998; 9:565-74.
30. Deak M, Clifton AD, Lucocq LM, Alessi DR. Mitogen- and stress-activated protein kinase-1(MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J 1998; 17:4426-41.
31. Lemaire M, Froment C, Boutros R, Mondesert O, Nebreda AR, Monsarrat B, Ducommun B. CDC25B phosphorylation by p38 and MK-2. Cell Cycle 2006; 5:1649-53.
32. McLaughlin MM, Kumar S, McDonnell PC, Van Horn S, Lee JC, Livi GP, Young PR. Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase. J Biol Chem 1996; 271:8488-92.
33. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, Nebreda AR. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 1994; 78:1027-37.
34. Tan Y, Rouse J, Zhang A, Cariati S, Cohen P, Comb MJ. FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. EMBO J 1996; 15:4629-42.
35. Pongratz G, McAlees JW, Conrad DH, Erbe RS, Haas KM, Sanders VM. The level of IgE produced by a B cell is regulated by norepinephrine in a p38 MAPK- and CD23-dependent manner. J Immunol 2006; 177:2926-38.
36. Loza MJ, Foster S, Peters SP, Penn RB. Beta-agonists modulate T-cell functions via direct actions on type 1 and type 2 cells. Blood 2006; 107:2052-60.
37. Tan X, Sanders P, Bolado J Jr, Whitney M. Integration of G-protein coupled receptor signaling pathways for activation of a transcription factor (EGR-3). Genomics Proteomics Bioinformatics 2003; 1:173-9.
38. Magocsi M, Vizi ES, Selmeczy Z, Brozik A, Szelenyi J. Multiple G-protein-coupling specificity of β-adrenoceptor in macrophages. Immunology 2007; 122:503-13.
39. 2-adrenergic receptor-induced p38 MAPK activation is mediated by protein kinase A rather than by Gi or Gβγ in adult mouse cardiomyocytes. J Biol Chem 2000; 275:40635-40.
40. Insel PA, Koachman AM. Cytochalasin B enhances hormone and cholera toxin-stimulated cyclic AMP accumulation in S49 lymphoma cells. J Biol Chem 1982; 257:9717-23.
41. Jakobs KH, Aktories K, Schultz G. Mechanism of pertussis toxin action on the adenylate cyclase system. Inhibition of the turn-on reaction of the inhibitory regulatory site. Eur J Biochem 1984; 140:177-81.
42. 2-adrenergic receptors. J Biol Chem 2008; 283:29028-36.
43. Mittelstadt PR, Salvador JM, Fornace AJ Jr, Ashwell JD. Activating p38 MAPK: new tricks for an old kinase. Cell Cycle 2005; 4:1189-92.
44. Salvador JM, Mittelstadt PR, Guszczynski T, Copeland TD, Yamaguchi H, Appella E, Fornace AJ Jr, Ashwell JD. Alternative p38 activation pathway mediated by T cell receptor-proximal tyrosine kinases. Nat Immunol 2005; 6:390-5.
45. Hazzalin CA, Cano E, Cuenda A, Barratt MJ, Cohen P, Mahadevan LC. p38/RK is essential for stress-induced nuclear responses: JNK/SAPKs and c-Jun/ATF-2 phosphorylation are insufficient. Curr Biol 1996; 6:1028-31.
46. Young PR, McLaughlin MM, Kumar S et al. Pyridinyl imidazole inhibitors of p38 mitogen-activated protein kinase bind in the ATP site. J Biol Chem 1997; 272:12116-21.
47. Miller AL, Webb MS, Copik AJ, Wang Y, Johnson BH, Kumar R, Thompson EB. p38 Mitogen-activated protein kinase (MAPK) is a key mediator in glucocorticoid-induced apoptosis of lymphoid cells: correlation between p38 MAPK activation and site-specific phosphorylation of the human glucocorticoid receptor at serine 211. Mol Endocrinol 2005; 19:1569-83.
48. Mahan LC, Insel PA. Use of superoxide dismutase and catalase to protect catecholamines from oxidation in tissue culture studies. Anal Biochem 1984; 136:208-16.
49. Zimmermann KC, Bonzon C, Green DR. The machinery of programmed cell death. Pharmacol Ther 2001; 92:57-70.
50. + T cells. Mol Cell Biol 2006; 26:2118-29.
51. Hsu SC, Gavrilin MA, Tsai MH, Han J, Lai MZ. p38 mitogen-activated protein kinase is involved in Fas ligand expression. J Biol Chem 1999; 274:25769-76.
52. Zhang L, Insel PA. The pro-apoptotic protein Bim is a convergence point for cAMP/protein kinase A- and glucocorticoid-promoted apoptosis of lymphoid cells. J Biol Chem 2004; 279:20858-65.
53. Faris M, Latinis KM, Kempiak SJ, Koretzky GA, Nel A. Stress-induced Fas ligand expression in T cells is mediated through a MEK kinase 1-regulated response element in the Fas ligand promoter. Mol Cell Biol 1998; 18:5414-24.
54. 2-adrenergic receptor-induced regulation of p38 mitogen-activated protein kinase in B lymphocytes. Mol Cell Biol 2009; 29:675-86.
55. Morioka N, Tanabe H, Inoue A, Dohi T, Nakata Y. Noradrenaline reduces the ATP-stimulated phosphorylation of p38 MAP kinase via β-adrenergic receptors-cAMP-protein kinase A-dependent mechanism in cultured rat spinal microglia. Neurochem Int 2009; 55:226-34.
56. Schraml E, Fuchs R, Kotzbeck P, Grillari J, Schauenstein K. Acute adrenergic stress inhibits proliferation of murine hematopoietic progenitor cells via p38/MAPK signaling. Stem Cells Dev 2009; 18:215-27.
57. 2-, and β-adrenergic receptors to mitogen-activated protein kinase pathways and differentiation in transfected PC12 cells. J Biol Chem 1998; 273:24624-32.
58. Tsang MY, Rabkin SW. p38 mitogen-activated protein kinase (MAPK) is activated by noradrenaline and serves a cardioprotective role, whereas adrenaline induces p38 MAPK dephosphorylation. Clin Exp Pharmacol Physiol 2009; 36:e12-29.
59. Yin F, Wang YY, Du JH, Li C, Lu ZZ, Han C, Zhang YY. Noncanonical cAMP pathway and p38 MAPK mediate beta2-adrenergic receptor-induced IL-6 production in neonatal mouse cardiac fibroblasts. J Mol Cell Cardiol 2006; 40:384-93.
60. Krupnick JG, Benovic JL. The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu Rev Pharmacol Toxicol 1998; 38:289-319.
61. Zhang J, Bui TN, Xiang J, Lin A. Cyclic AMP inhibits p38 activation via CREB-induced dynein light chain. Mol Cell Biol 2006; 26:1223-34.
62. 2 enhances osteoclastic differentiation of precursor cells through protein kinase A-dependent phosphorylation of TAK1. J Biol Chem 2005; 280:11395-403.
63. Nika K, Hyunh H, Williams S, Paul S, Bottini N, Tasken K, Lombroso PJ, Mustelin T. Haematopoietic protein tyrosine phosphatase (HePTP) phosphorylation by cAMP-dependent protein kinase in T-cells: dynamics and subcellular location. Biochem J 2004; 378:335-42.
64. Lu G, Kang YJ, Han J, Herschman HR, Stefani E, Wang Y. TAB-1 modulates intracellular localization of p38 MAP kinase and downstream signaling. J Biol Chem 2006; 281:6087-95.
65. Mittelstadt PR, Yamaguchi H, Appella E, Ashwell JD. T cell receptor-mediated activation of p38α by mono-phosphorylation of the activation loop results in altered substrate specificity. J Biol Chem 2009; 284:15469-74.
66. Mansouri A, Ridgway LD, Korapati AL et al. Sustained activation of JNK/p38 MAPK pathways in response to cisplatin leads to Fas ligand induction and cell death in ovarian carcinoma cells. J Biol Chem 2003; 278:19245-56.
67. Dominguez-Gerpe L, Rey-Mendez M. Alterations induced by chronic stress in lymphocyte subsets of blood and primary and secondary immune organs of mice. BMC Immunol 2001; 2:7.
68. Zivkovic IP, Rakin AK, Petrovic-Djergovic DM, Kosec DJ, Micic MV. Exposure to forced swim stress alters morphofunctional characteristics of the rat thymus. J Neuroimmunol 2005; 160:77-86.