Glucocorticoids regulate innate immunity in a model of multiple sclerosis: Reciprocal interactions between the A1 adenosine receptor and β-arrestin-1 in monocytoid cells

FASEB Journal

Volumn 22, Issue 3, 2008, Pages 786-796

  Tsutsui, Shigeki ^a   Vergote, David ^a,b   Shariat, Neda ^a   Warren, Kenneth ^b   Ferguson, Stephen S G ^c   Power, Christopher ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Central nervous system; Cytokines; Experimental autoimmune encephalomyelitis; G protein coupled receptor

Indexed keywords

ADENOSINE A1 RECEPTOR; BETA ARRESTIN 1; CYTOKINE; DEXAMETHASONE; PREDNISONE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; COGNITION; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; INNATE IMMUNITY; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SPINAL CORD;

ANIMALS; ARRESTINS; BRAIN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GLUCOCORTICOIDS; HUMANS; IMMUNITY, NATURAL; MICE; MONOCYTES; MULTIPLE SCLEROSIS; RECEPTOR, ADENOSINE A1;

MURINAE;

EID: 40449126433     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-9002com     Document Type: Article

References (65)

1. Nguyen, M. D., Julien, J. P., and Rivest, S. (2002) Innate immunity: the missing link in neuroprotection and neurodegeneration? Nature Rev. Neurosci. 3, 216-227
2. Gehrmann, J., Matsumoto, Y., and Kreutzberg, G. W. (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res. Brain Res. Rev. 20, 269-287
3. Ulvestad, E., Williams, K., Mork, S., Antel, J., and Nyland, H. (1994) Phenotypic differences between human monocytes/ macrophages and microglial cells studied in situ and in vitro. J. Neuropathol. Exp. Neurol. 53, 492-501
4. Gonzalez-Scarano, F., and Baltuch, G. (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu. Rev. Neurosci. 22, 219-240
5. Meda, L. M. A. Cassatella, G. I., Szendrei Otvos, L., Jr., Baron, P., Villalba, M., Ferrari, D., and Rossi, F. (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374, 647-650
6. Jones, G., and Power, C. (2006) Regulation of neural cell survival by HIV-1 infection. Neurobiol. Dis. 21, 1-17
7. Mayne, M., Ni, W., Yan, H. J., Xue, M., Johnston, J. B., Del Bigio, M. R. Peeling, J., and Power, C. (2001) Antisense oligodeoxynucleotide inhibition of tumor necrosis factor-alpha expression is neuroprotective after intracerebral hemorrhage. Stroke 32, 240-248
8. Johnston, J. B., Silva, C., Gonzalez, G., Holden, J. K. G. Warren, L., Metz, M., and Power, C. (2001) Diminished adenosine A1 receptor expression on macrophages in brain and blood of patients with multiple sclerosis. Ann. Neurol. 49, 650-658
9. Hasko, G., Szabo, C., Nemeth, Z. H., Kvetan, V., Pastores, S. M., and Vizi, E. S. (1996) Adenosine receptor agonists differentially regulate IL-10, TNF-alpha, and nitric oxide production in RAW 264.7 macrophages and in endotoxemic mice. J. Immunol. 157, 4634-4640
10. Wardas, J. (2002) Neuroprotective role of adenosine in the CNS. Pol. J. Pharmacol. 54, 313-326
11. Lassmann, H. (2001) Classification of demyelinating diseases at the interface between etiology and pathogenesis. Curr. Opin. Neurol. 14, 253-258
12. Burgoon, M. P., Gilden, D. H., and Owens, G. P. (2004) B cells in multiple sclerosis. Front. Biosci. 9, 786-796
13. Noseworthy, J. H., Lucchinetti, C., Rodriguez, M., and Weinshenker, B. G. (2000) Multiple sclerosis. N. Engl. J. Med. 343, 938-952
14. Navikas, V., and Link, H. (1996) Review: cytokines and the pathogenesis of multiple sclerosis. J. Neurosci. Res. 45, 322-333
15. Bar-Or, A., Oliveira, E. M., Anderson, D. E., and Hafler, D. A. (1999) Molecular pathogenesis of multiple sclerosis. J. Neuroimmunol. 100, 252-259
16. Sorensen, T. L., Tani, M., Jensen, J., Pierce, V., Lucchinetti, C. Folcik, V. A., Qin, S., Rottman, J., Sellebjerg, F., Strieter, R. M., Frederiksen, J. L., and Ransohoff, R. M. (1999) Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J. Clin. Invest. 103, 807-815
17. Yong, V. W., Power, C., Forsyth, P., and Edwards, D. R. (2001) Metalloproteinases in biology and pathology of the nervous system. Nature Rev. Neurosci. 2, 502-511
18. Barnett, M. H., and Prineas, J. W. (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 55, 458-468
19. Mayne, M., Shepel, P. N., Jiang, Y., Geiger, J. D., and Power, C. (1999) Dysregulation of adenosine A1 receptor-mediated cytokine expression in peripheral blood mononuclear cells from multiple sclerosis patients. Ann. Neurol. 45, 633-639
20. Tsutsui, S., Schnermann, J., Noorbakhsh, F., Henry, S., Yong, V. W., Winston, B. W., Warren, K., and Power, C. (2004) A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J. Neurosci. 24, 1521-1529
21. Ohguro, H., Chiba, S., Igarashi, Y., Matsumoto, H., Akino, T., and Palczewski, K. (1993) Beta-arrestin and arrestin are recognized by autoantibodies in sera from multiple sclerosis patients. Proc. Natl. Acad. Sci. U. S. A. 90, 3241-3245
22. Forooghian, F., Cheung, R. K., Smith, W. C., O'Connor, P., and Dosch, H. M. (2007) Enolase and arrestin are novel nonmyelin autoantigens in multiple sclerosis. J. Clin. Immunol. 27, 388-396
23. Vroon, A., Lombardi, M. S., Kavelaars, A., and Heijnen, C. J. (2003) Changes in the G-protein-coupled receptor desensitization machinery during relapsing-progressive experimental allergic encephalomyelitis. J. Neuroimmunol. 137, 79-86
24. Kohno, H., Sakai, T., Saito, S., Okano, K., and Kitahara, K. (2007) Treatment of experimental autoimmune uveoretinitis with atorvastatin and lovastatin. Exp. Eye. Res. 84, 569-576
25. Nie, Z., Mei, Y., and Ramkumar, V. (1997) Short term desensitization of the A1 adenosine receptors in DDT1MF-2 cells. Mol. Pharmacol. 52, 456-464
26. Brusaferri, F., and Candelise, L. (2000) Steroids for multiple sclerosis and optic neuritis: a meta-analysis of randomized controlled clinical trials. J. Neurol. 247, 435-442
27. Wandinger, K. P., Wessel, K., Trillenberg, P., Heindl, N., and Kirchner, H. (1998) Effect of high-dose methylprednisolone administration on immune functions in multiple sclerosis patients. Acta Neurol. Scand. 97, 359-365
28. Gelati, M., Corsini, E., De Rossi, M., Masini, L., Bernardi, G., Massa, G., Boiardi, A., and Salmaggi, A. (2002) Methylprednisolone acts on peripheral blood mononuclear cells and endothelium in inhibiting migration phenomena in patients with multiple sclerosis. Arch. Neurol. 59, 774-780
29. Leussink, V. I., Jung, S., Merschdorf, U., Toyka, K. V., and Gold, R. (2001) High-dose methylprednisolone therapy in multiple sclerosis induces apoptosis in peripheral blood leukocytes. Arch. Neurol. 58, 91-97
30. Gerwins, P., and Fredholm, B. B. (1991) Glucocorticoid receptor activation leads to up-regulation of adenosine A1 receptors and down-regulation of adenosine A2 responses in DDT1 MF-2 smooth muscle cells. Mol. Pharmacol. 40, 149-155
31. Vecil, G. G., Larsen, P. H., Corley, S. M., Herx, L. M., Besson, A. Goodyer, C. G., and Yong, V. W. (2000) Interleukin-1 is a key regulator of matrix metalloproteinase-9 expression in human neurons in culture and following mouse brain trauma in vivo. J. Neurosci. Res. 61, 212-224
32. Song, X., Raman, D., Gurevich, E. V., Vishnivetskiy, S. A., and Gurevich, V. V. (2006) Visual and both non-visual arrestins in their "inactive" conformation bind JNK3 and Mdm2 and relocalize them from the nucleus to the cytoplasm. J. Biol. Chem. 281, 21491-21499
33. Boven, L. A., Vergnolle, N., Henry, S. D., Silva, C., Imai, Y., Holden, J., Warren, K. Hollenberg, M. D., and Power, C. (2003) Up-regulation of proteinase-activated receptor 1 expression in astrocytes during HIV encephalitis. J. Immunol. 170, 2638-2646
34. Tsutsui, S., Noorbakhsh, F., Sullivan, A., Henderson, A. J., Warren, K., Toney-Earley, K., Waltz, S. E., and Power, C. (2005) RON-regulated innate immunity is protective in an animal model of multiple sclerosis. Ann. Neurol. 57, 883-895
35. Liu, J., Marino, M. W., Wong, G., Grail, D., Dunn, A., Bettadapura, J., Slavin, A. J., Old, L., and Bernard, C. C. (1998) TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 4, 78-83
36. Morrow, S. A., Stoian, C. A., Dmitrovic, J., Chan, S. C., and Metz, L. M. (2004) The bioavailability of IV methylprednisolone and oral prednisone in multiple sclerosis. Neurology 63, 1079-1080
37. Brundula, V., Rewcastle, N. B., Metz, L. M., Bernard, C. C., and Yong, V. W. (2002) Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 125, 1297-1308
38. Pless, I. B., Power, C., and Peckham, C. S. (1993) Long-term psychosocial sequelae of chronic physical disorders in childhood. Pediatrics 91, 1131-1136
39. Power, C., Henry, S., Del Bigio, M. R., Larsen, P. H., Corbett, D., Imai, Y., Yong, V. W., and Peeling, J. (2003) Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann. Neurol. 53, 731-742
40. Lefkowitz, R. J., and Shenoy, S. K. (2005) Transduction of receptor signals by beta-arrestins. Science 308, 512-517
41. Cato, A. C., and Wade, E. (1996) Molecular mechanisms of anti-inflammatory action of glucocorticoids. Bioessays 18, 371-378
42. De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., and Joels, M. (1998) Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19, 269-301
43. Yong, V. W. (2004) Prospects for neuroprotection in multiple sclerosis. Front Biosci. 9, 864-872
44. Vassilatis, D. K., Hohmann, J. G., Zeng, H., Li, F., Ranchalis, J. E., Mortrud, M. T., Brown, A., Rodriguez, S. S., Weller, J. R., Wright, A. C., Bergmann, J. E., and Gaitanaris, G. A. (2003) The G protein-coupled receptor repertoires of human and mouse. Proc. Natl. Acad. Sci. U. S. A. 100, 4903-4908
45. Wise, A., Jupe, S. C., and Rees, S. (2004) The identification of ligands at orphan G-protein coupled receptors. Annu. Rev. Pharmacol. Toxicol. 44, 43-66
46. Hausdorff, W. P., Campbell, P. T., Ostrowski, J., Yu, S. S., Caron, M. G., and Lefkowitz, R. J. (1991) A small region of the beta-adrenergic receptor is selectively involved in its rapid regulation. Proc. Natl. Acad. Sci. U. S. A. 88, 2979-2983
47. Lefkowitz, R. J., and Whalen, E. J. (2004) Beta-arrestins: traffic cops of cell signaling. Curr. Opin. Cell Biol. 16, 162-168
48. Gainetdinov, R. R., Premont, R. T., Bohn, L. M., Lefkowitz, R. J., and Caron, M. G. (2004) Desensitization of G protein-coupled receptors and neuronal functions. Annu. Rev. Neurosci. 27, 107-144
49. Ferguson, S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24
50. Claing, A., Laporte, S. A., Caron, M. G., and Lefkowitz, R. J. (2002) Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and beta-arrestin proteins. Prog. Neurobiol. 66, 61-79
51. Linden, J. (2001) Molecular approach to adenosine receptors: receptor-mediated mechanisms of tissue protection. Annu. Rev. Pharmacol. Toxicol. 41, 775-787
52. Ren, H., and Stiles, G. L. (1999) Dexamethasone stimulates human A1 adenosine receptor (A1AR) gene expression through multiple regulatory sites in promoter B. Mol. Pharmacol. 55, 309-316
53. Rivkees, S. A., Chen, M., Kulkarni, J., Browne, J., and Zhao, Z. (1999) Characterization of the murine A1 adenosine receptor promoter, potent regulation by GATA-4 and Nkx2.5. J. Biol. Chem. 274, 14204-14209
54. Parruti, G., Peracchia, F., Sallese, M., Ambrosini, G., Masini, M., Rotilio, D., and De Blasi, A. (1993) Molecular analysis of human beta-arrestin-1: cloning, tissue distribution, and regulation of expression. Identification of two isoforms generated by alternative splicing. J. Biol. Chem. 268, 9753-9761
55. Wang, J., Guan, E., Roderiquez, G., Calvert, V., Alvarez, R., and Norcross, M. A. (2001) Role of tyrosine phosphorylation in ligand-independent sequestration of CXCR4 in human primary monocytes-macrophages. J. Biol. Chem. 276, 49236-49243
56. McQualter, J. L., Darwiche, R., Ewing, C., Onuki, M., Kay, T. W., Hamilton, J. A., Reid, H. H., and Bernard, C. C. (2001) Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis. J. Exp. Med. 194, 873-882
57. Ponomarev, E. D., Shriver, L. P., Maresz, K., Pedras-Vasconcelos, J., Verthelyi, D., and Dittel, B. N. (2007) GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis. J. Immunol. 178, 39-48
58. Giorelli, M., Livrea, P., Defazio, G., Iacovelli, L., Capobianco, L., Picascia, A., Sallese, M., Martino, D., Aniello, M. S., Trojano, M., and De Blasi, A. (2002) Interferon beta-1a counteracts effects of activation on the expression of G-protein-coupled receptor kinases 2 and 3, beta-arrestin-1, and regulators of G-protein signalling 2 and 16 in human mononuclear leukocytes. Cell. Signal. 14, 673-678
59. Pitzalis, C., Pipitone, N., and Perretti, M. (2002) Regulation of leukocyte-endothelial interactions by glucocorticoids. Ann. N. Y. Acad. Sci. 966, 108-118
60. McEwan, I. J., Wright, A. P., and Gustafsson, J. A. (1997) Mechanism of gene expression by the glucocorticoid receptor: role of protein-protein interactions. Bioessays 19, 153-160
61. Garlow, S. J., and Ciaranello, R. D. (1995) Transcriptional control of the rat serotonin-2 receptor gene. Brain Res. Mol. Brain Res. 31, 201-209
62. Jonat, C., Rahmsdorf, H. J., Park, K. K., Cato, A. C. Gebel, S., Ponta, H., and Herrlich, P. (1990) Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell 62, 1189-1204
63. Teurich, S., and Angel, P. (1995) The glucocorticoid receptor synergizes with Jun homodimers to activate AP-1-regulated promoters lacking GR binding sites. Chem. Senses 20, 251-255
64. Svenningsson, P., and Fredholm, B. B. (1997) Glucocorticoids regulate the expression of adenosine A1 but not A(2A) receptors in rat brain. J. Pharmacol. Exp. Ther. 280, 1094-1101
65. Pender, M. P., and Wolfe, N. P. (2002) Prevention of autoimmune attack and disease progression in multiple sclerosis: current therapies and future prospects. Intern. Med. J. 32, 554-563