Histamine modulation of peripheral CRH receptor type 1α expression is dependent on Ca2+ signalling and NF-κB/p65 transcriptional activity

Molecular Immunology

Volumn 47, Issue 7-8, 2010, Pages 1426-1437

  Zocco, Davide ^a   McMorrow, Jason P ^a   Murphy, Evelyn P ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Calcium; Corticotropin releasing hormone receptor 1; Gene expression; Histamine; Inflammatory arthritis; NF B; Promoter activity

Indexed keywords

CALCIUM IONOPHORE; CHELATING AGENT; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1ALPHA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HISTAMINE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEAR RECEPTOR NR4A2; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ARTHRITIS; ARTICLE; BINDING SITE; BIOINFORMATICS; CALCIUM SIGNALING; CONCENTRATION RESPONSE; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE DELETION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SYNOVIOCYTE; TRANSCRIPTION INITIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; CALCIUM SIGNALING; CELL LINE; CREB-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOTHELIAL CELLS; HISTAMINE; HUMANS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; SYNOVIAL MEMBRANE; TRANSCRIPTION FACTOR RELA; TRANSCRIPTIONAL ACTIVATION;

EID: 77950628592     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.02.012     Document Type: Article

References (68)

1. Ades E.W., Candal F.J., Swerlick R.A., George V.G., Summers S., Bosse D.C., Lawley T.J. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 1992, 99:683-690.
2. Adlesic M., Verdrengh M., Bokarewa M., Dahlberg L., Foster S.J., Tarkowski A. Histamine in rheumatoid arthritis. Scand. J. Immunol. 2007, 65:530-537.
3. Aherne C.M., McMorrow J., Kane D., FitzGerald O., Mix K.S., Murphy E.P. Identification of NR4A2 as a transcriptional activator of IL-8 expression in human inflammatory arthritis. Mol. Immunol. 2009, 46:3345-3357.
4. Anwar K.N., Fazal F., Malik A.B., Rahman A. RhoA/Rho-associated kinase pathway selectively regulates thrombin-induced intercellular adhesion molecule-1 expression in endothelial cells via activation of I kappa B kinase beta and phosphorylation of RelA/p65. J. Immunol. 2004, 173:6965-6972.
5. Arkenbout E.K., de Waard V., van Bragt M., van Achterberg T.A., Grimbergen J.M., Pichon B., Pannekoek H., de Vries C.J. Protective function of transcription factor TR3 orphan receptor in atherogenesis: decreased lesion formation in carotid artery ligation model in TR3 transgenic mice. Circulation 2002, 106:1530-1535.
6. Arts J., Grimbergen J., Bosma P.J., Rahmsdorf H.J., Kooistra T. Role of c-Jun and proximal phorbol 12-myristate-13-acetate-(PMA)-responsive elements in the regulation of basal and PMA-stimulated plasminogen-activator inhibitor-1 gene expression in HepG2. Eur. J. Biochem. 1996, 241:393-402.
7. Bakker A.C., van de Loo F.A., van Beuningen H.M., Sime P., van Lent P.L., van der Kraan P.M., Richards C.D., van den Berg W.B. Overexpression of active TGF-beta-1 in the murine knee joint: evidence for synovial-layer-dependent chondro-osteophyte formation. Osteoarthr. Cartilage 2001, 9:128-136.
8. Bakker R.A., Schoonus S.B., Smit M.J., Timmerman H., Leurs R. Histamine H(1)-receptor activation of nuclear factor-kappa B: roles for G beta gamma- and G alpha(q/11)-subunits in constitutive and agonist-mediated signaling. Mol. Pharmacol. 2001, 60:1133-1142.
9. Binstadt B.A., Patel P.R., Alencar H., Nigrovic P.A., Lee D.M., Mahmood U., Weissleder R., Mathis D., Benoist C. Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat. Immunol. 2006, 7:284-292.
10. Bonta P.I., van Tiel C.M., Vos M., Pols T.W., van Thienen J.V., Ferreira V., Arkenbout E.K., Seppen J., Spek C.A., van der Poll T., Pannekoek H., de Vries C.J. Nuclear receptors Nur77, Nurr1, and NOR-1 expressed in atherosclerotic lesion macrophages reduce lipid loading and inflammatory responses. Arterioscler. Thromb. Vasc. Biol. 2006, 26:2288.
11. Cummins E.P., Berra E., Comerford K.M., Ginouves A., Fitzgerald K.T., Seeballuck F., Godson C., Nielsen J.E., Moynagh P., Pouyssegur J., Taylor C.T. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18154-18159.
12. Davies M.R., Harding C.J., Raines S., Tolley K., Parker A.E., Downey-Jones M., Needham M.R. Nurr1 dependent regulation of pro-inflammatory mediators in immortalised synovial fibroblasts. J. Inflamm. (Lond.) 2005, 2:15.
13. Davis I.J., Hazel T.G., Lau L.F. Transcriptional activation by Nur77, a growth factor-inducible member of the steroid hormone receptor superfamily. Mol. Endocrinol. 1991, 5:854-859.
14. Deak M., Clifton A.D., Lucocq L.M., Alessi D.R. 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, 17:4426-4441.
15. Denk A., Goebeler M., Schmid S., Berberich I., Ritz O., Lindemann D., Ludwig S., Wirth T. Activation of NF-kappa B via the Ikappa B kinase complex is both essential and sufficient for proinflammatory gene expression in primary endothelial cells. J. Biol. Chem. 2001, 276:28451-28458.
16. Ditzel H.J. The K/BxN mouse: a model of human inflammatory arthritis. Trends Mol. Med. 2004, 10:40-45.
17. Enslen H., Soderling T.R. Roles of calmodulin-dependent protein kinases and phosphatase in calcium-dependent transcription of immediate early genes. J. Biol. Chem. 1994, 269:20872-20877.
18. Fife M.S., Fisher S.A., John S., Worthington J., Shah C.J., Ollier W.E., Panayi G.S., Lewis C.M., Lanchbury J.S. Multipoint linkage analysis of a candidate gene locus in rheumatoid arthritis demonstrates significant evidence of linkage and association with the corticotropin-releasing hormone genomic region. Arthritis Rheum. 2000, 43:1673-1678.
19. Gonzalez G.A., Yamamoto K.K., Fischer W.H., Karr D., Menzel P., Biggs W., Vale W.W., Montminy M.R. A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature 1989, 337:749-752.
20. Grzybowska-Kowalczyk A., Wojtecka-Lukasik E., Maslinska D., Gujski M., Maslinski S. Distribution pattern of histamine H4 receptor in human synovial tissue from patients with rheumatoid arthritis. Inflamm. Res. 2007, 56(Suppl. 1):S59-60.
21. Haas C., Aicher W.K., Dinkel A., Peter H.H., Eibel H. Characterization of SV40T antigen immortalized human synovial fibroblasts: maintained expression patterns of EGR-1, HLA-DR and some surface receptors. Rheumatol. Int. 1997, 16:241-247.
22. Hagiwara M., Alberts A., Brindle P., Meinkoth J., Feramisco J., Deng T., Karin M., Shenolikar S., Montminy M. Transcriptional attenuation following cAMP induction requires PP-1-mediated dephosphorylation of CREB. Cell 1992, 70:105-113.
23. Kageyama K., Hanada K., Moriyama T., Nigawara T., Sakihara S., Suda T. G protein-coupled receptor kinase 2 involvement in desensitization of corticotropin-releasing factor (CRF) receptor type 1 by CRF in murine corticotrophs. Endocrinology 2006, 147:441-450.
24. Karalis K.P., Kontopoulos E., Muglia L.J., Majzoub J.A. Corticotropin-releasing hormone deficiency unmasks the proinflammatory effect of epinephrine. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:7093-7097. (published erratum appears in Proc. Natl. Acad. Sci. U.S.A. 2000 March 28, 97(7), 3782).
25. Kopicky-Burd J.A., Kagey-Sobotka A., Peters S.P., Dvorak A.M., Lennox D.W., Lichtenstein L.M., Wigley F.M. Characterization of human synovial mast cells. J. Rheumatol. 1988, 15:1326-1333.
26. Lammi J., Huppunen J., Aarnisalo P. Regulation of the osteopontin gene by the orphan nuclear receptor Nurr1 in osteoblasts. Mol. Endocrinol. 2004.
27. Lee D.M., Friend D.S., Gurish M.F., Benoist C., Mathis D., Brenner M.B. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 2002, 297:1689-1692.
28. Lombardi M.S., Kavelaars A., Cobelens P.M., Schmidt R.E., Schedlowski M., Heijnen C.J. Adjuvant arthritis induces down-regulation of G protein-coupled receptor kinases in the immune system. J. Immunol. 2001, 166:1635-1640.
29. Lombardi M.S., Kavelaars A., Schedlowski M., Bijlsma J.W., Okihara K.L., Van de Pol M., Ochsmann S., Pawlak C., Schmidt R.E., Heijnen C.J. Decreased expression and activity of G-protein-coupled receptor kinases in peripheral blood mononuclear cells of patients with rheumatoid arthritis. FASEB J. 1999, 13:715-725.
30. Maeng Y.S., Min J.K., Kim J.H., Yamagishi A., Mochizuki N., Kwon J.Y., Park Y.W., Kim Y.M., Kwon Y.G. ERK is an anti-inflammatory signal that suppresses expression of NF-kappaB-dependent inflammatory genes by inhibiting IKK activity in endothelial cells. Cell Signal. 2006, 18:994-1005.
31. Marok R., Winyard P.G., Coumbe A., Kus M.L., Gaffney K., Blades S., Mapp P.I., Morris C.J., Blake D.R., Kaltschmidt C., Baeuerle P.A. Activation of the transcription factor nuclear factor-kappaB in human inflamed synovial tissue. Arthritis Rheum. 1996, 39:583-591.
32. 2+-dependent protein kinase C, Raf/MEK/ERK and IKK/I kappa B/NF-kappa B signal cascades. Biochem. Pharmacol. 2005, 69:433-449.
33. Maxwell M.A., Muscat G.E. The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl. Recept. Signal. 2006, 4:e002.
34. Mayr B., Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2001, 2:599-609.
35. McEvoy A.N., Bresnihan B., FitzGerald O., Murphy E.P. Corticotropin-releasing hormone signaling in synovial tissue from patients with early inflammatory arthritis is mediated by the type 1 alpha corticotropin-releasing hormone receptor. Arthritis Rheum. 2001, 44:1761-1767.
36. McEvoy A.N., Bresnihan B., Fitzgerald O., Murphy E.P. Corticotropin-releasing hormone signaling in synovial tissue vascular endothelium is mediated through the cAMP/CREB pathway. Ann. N. Y. Acad. Sci. 2002, 966:119-130.
37. McEvoy A.N., Bresnihan B., FitzGerald O., Murphy E.P. Cyclooxygenase 2-derived prostaglandin E2 production by corticotropin-releasing hormone contributes to the activated cAMP response element binding protein content in rheumatoid arthritis synovial tissue. Arthritis Rheum. 2004, 50:1132-1145.
38. McEvoy A.N., Murphy E.A., Ponnio T., Conneely O.M., Bresnihan B., FitzGerald O., Murphy E.P. Activation of nuclear orphan receptor NURR1 transcription by NF-kappa B and cyclic adenosine 5′-monophosphate response element-binding protein in rheumatoid arthritis synovial tissue. J. Immunol. 2002, 168:2979-2987.
39. Minami T., Abid M.R., Zhang J., King G., Kodama T., Aird W.C. Thrombin stimulation of vascular adhesion molecule-1 in endothelial cells is mediated by protein kinase C (PKC)-delta-NF-kappa B and PKC-zeta-GATA signaling pathways. J. Biol. Chem. 2003, 278:6976-6984.
40. Montminy M.R.B.L. Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature 1987, 328:175-178.
41. Murphy E.P., Dobson A.D., Keller C., Conneely O.M. Differential regulation of transcription by the NURR1/NUR77 subfamily of nuclear transcription factors. Gene Exp. 1996, 5:169-179.
42. Murphy E.P., McEvoy A., Conneely O.M., Bresnihan B., FitzGerald O. Involvement of the nuclear orphan receptor NURR1 in the regulation of corticotropin-releasing hormone expression and actions in human inflammatory arthritis. Arthritis Rheum. 2001, 44:782-793.
43. Nigrovic P.A., Lee D.M. Synovial mast cells: role in acute and chronic arthritis. Immunol. Rev. 2007, 217:19-37.
44. Ohki E., Suzuki M., Aoe T., Ikawa Y., Negishi E., Ueno K. Expression of histamine H4 receptor in synovial cells from rheumatoid arthritic patients. Biol. Pharm. Bull. 2007, 30:2217-2220.
45. Parham K.L., Zervou S., Karteris E., Catalano R.D., Old R.W., Hillhouse E.W. Promoter analysis of human corticotropin-releasing factor (CRF) type 1 receptor and regulation by CRF and urocortin. Endocrinology 2004, 145:3971-3983.
46. 2+ influx induced by protease-activated receptor-1 activates a feed-forward mechanism of TRPC1 expression via nuclear factor-kappaB activation in endothelial cells. J. Biol. Chem. 2006, 281:20715-20727.
47. Paulsen R.E., Weaver C.A., Fahrner T.J., Milbrandt J. Domains regulating transcriptional activity of the inducible orphan receptor NGFI-B. J. Biol. Chem. 1992, 267:16491-16496.
48. Paulsen R.F., Granas K., Johnsen H., Rolseth V., Sterri S. Three related brain nuclear receptors, NGFI-B, Nurr1, and NOR-1, as transcriptional activators. J. Mol. Neurosci. 1995, 6:249-255.
49. Perkins N.D. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell Biol. 2007, 8:49-62.
50. Rahman A., Anwar K.N., True A.L., Malik A.B. Thrombin-induced p65 homodimer binding to downstream NF-kappa B site of the promoter mediates endothelial ICAM-1 expression and neutrophil adhesion. J. Immunol. 1999, 162:5466-5476.
51. Rajasekaran N., Solomon S., Watanabe T., Ohtsu H., Gajda M., Brauer R., Illges H. Histidine decarboxylase but not histamine receptor 1 or 2 deficiency protects from K/BxN serum-induced arthritis. Int. Immunol. 2009, 21:1263-1268.
52. Ralph J.A., McEvoy A.N., Kane D., Bresnihan B., FitzGerald O., Murphy E.P. Modulation of orphan nuclear receptor NURR1 expression by methotrexate in human inflammatory joint disease involves adenosine A2A receptor-mediated responses. J. Immunol. 2005, 175:555-565.
53. Ralph J.A., Zocco D., Bresnihan B., Fitzgerald O., McEvoy A.N., Murphy E.P. A role for type 1alpha corticotropin-releasing hormone receptors in mediating local changes in chronically inflamed tissue. Am. J. Pathol. 2007, 170:1121-1133.
54. Reber L., Da Silva C.A., Frossard N. Stem cell factor and its receptor c-Kit as targets for inflammatory diseases. Eur. J. Pharmacol. 2006, 533:327-340.
55. Sandoval R., Malik A.B., Minshall R.D., Kouklis P., Ellis C.A., Tiruppathi C. Ca(2+) signalling and PKCalpha activate increased endothelial permeability by disassembly of VE-cadherin junctions. J. Physiol. 2001, 533:433-445.
56. Sands W.A., Palmer T.M. Regulating gene transcription in response to cyclic AMP elevation. Cell Signal. 2008, 20:460-466.
57. Sen R., Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 1986, 46:705-716.
58. Takeba Y., Suzuki N., Wakisaka S., Takeno M., Kaneko A., Asai T., Sakane T. Involvement of cAMP responsive element binding protein (CREB) in the synovial cell hyperfunction in patients with rheumatoid arthritis. Clin. Exp. Rheumatol. 2000, 18:47-55.
59. Tanimoto A., Wang K.Y., Murata Y., Kimura S., Nomaguchi M., Nakata S., Tsutsui M., Sasaguri Y. Histamine upregulates the expression of inducible nitric oxide synthase in human intimal smooth muscle cells via histamine H1 receptor and NF-kappaB signaling pathway. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1556-1561.
60. Tebib J., Mariette X., Bourgeois P., Flipo R.M., Gaudin P., Le Loet X., Gineste P., Guy L., Mansfield C.D., Moussy A., Dubreuil P., Hermine O., Sibilia J. Masitinib in the treatment of active rheumatoid arthritis: results of a multicentre, open-label, dose-ranging, phase 2a study. Arthritis Res. Ther. 2009, 11:R95.
61. 2+ signaling in the regulation of endothelial permeability. Vascul. Pharmacol. 2002, 39:173-185.
62. Wadzinski B.E., Wheat W.H., Jaspers S., Peruski L.F., Lickteig R.L., Johnson G.L., Klemm D.J. Nuclear protein phosphatase 2A dephosphorylates protein kinase A-phosphorylated CREB and regulates CREB transcriptional stimulation. Mol. Cell Biol. 1993, 13:2822-2834.
63. Webster E., Barrientos R.M., Contoreggi C., Isaac M.G., Ligier S., Gabry K.E., Chrousos G.P., McCarthy E.F., Rice K.C., Gold P.W., Sternberg E.M. Corticotropin releasing hormone (CRH) antagonist attenuates adjuvant induced arthritis: role of CRH in peripheral inflammation. J. Rheumatol. 2002, 29:1252-1261.
64. Winn R.A., Van Scoyk M., Hammond M., Rodriguez K., Crossno J.T., Heasley L.E., Nemenoff R.A. Antitumorigenic effect of Wnt 7a and Fzd 9 in non-small cell lung cancer cells is mediated through ERK-5-dependent activation of peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 2006, 281:26943-26950.
65. Woiciechowsky C., Asadullah K., Nestler D., Eberhardt B., Platzer C., Schoning B., Glockner F., Lanksch W.R., Volk H.D., Docke W.D. Sympathetic activation triggers systemic interleukin-10 release in immunodepression induced by brain injury. Nat. Med. 1998, 4:808-813.
66. Xu D., Jiang H.R., Kewin P., Li Y., Mu R., Fraser A.R., Pitman N., Kurowska-Stolarska M., McKenzie A.N., McInnes I.B., Liew F.Y. IL-33 exacerbates antigen-induced arthritis by activating mast cells. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10913-10918.
67. Xu G., Rabadan-Diehl C., Nikodemova M., Wynn P., Spiess J., Aguilera G. Inhibition of corticotropin releasing hormone type-1 receptor translation by an upstream AUG triplet in the 5′ untranslated region. Mol. Pharmacol. 2001, 59:485-492.
68. Zeng H., Qin L., Zhao D., Tan X., Manseau E.J., Van Hoang M., Senger D.R., Brown L.F., Nagy J.A., Dvorak H.F. Orphan nuclear receptor TR3/Nur77 regulates VEGF-A-induced angiogenesis through its transcriptional activity. J. Exp. Med. 2006, 203:719-729.