Inhibition of interferon-beta responses in multiple sclerosis immune cells associated with high-dose statins

Archives of Neurology

Volumn 69, Issue 10, 2012, Pages 1303-1309

  Feng, Xuan ^a   Han, Diana ^a   Kilaru, Bharat K ^a   Franek, Beverly S ^a   Niewold, Timothy B ^a   Reder, Anthony T ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ATORVASTATIN; BETA INTERFERON; BETA1A INTERFERON; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INTERFERON REGULATORY FACTOR 1; MYXOVIRUS RESISTANCE 1 PROTEIN; MYXOVIRUS RESISTANCE PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; UNCLASSIFIED DRUG;

ADD ON THERAPY; ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE EXACERBATION; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; DRUG MEGADOSE; DRUG POTENTIATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LEUKEMIA CELL LINE; MALE; MONONUCLEAR CELL; MULTIPLE SCLEROSIS; PATIENT ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ADULT; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; IMMUNOLOGIC FACTORS; INTERFERON REGULATORY FACTOR-1; INTERFERON-BETA; JURKAT CELLS; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TIME FACTORS;

EID: 84867352003     PISSN: 00039942     EISSN: 15383687     Source Type: Journal    
DOI: 10.1001/archneurol.2012.465     Document Type: Article

References (53)

1. Lassmann H, Brück W, Lucchinetti CF. The immunopathology of multiple sclerosis: an overview. Brain Pathol. 2007;17(2):210-218. (Pubitemid 46466140)
2. Feng X, Petraglia AL, Chen M, Byskosh PV, Boos MD, Reder AT. Low expression of interferon-stimulated genes in active multiple sclerosis is linked to subnormal phosphorylation of STAT1. J Neuroimmunol. 2002;129(1-2):205-215. (Pubitemid 34874925)
3. Yamaguchi KD, Ruderman DL, Croze E, et al. IFN-β-regulated genes are abnormally expressed in therapy-naive MS mononuclear cells: unbiased gene expression analysis parallels literature on signaling pathways. J Neuroimmunol. 2008;195:116-120.
4. Youssef S, Stüve O, Patarroyo JC, et al. The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature. 2002;420(6911):78-84.
5. Greenwood J, Steinman L, Zamvil SS. Statin therapy and autoimmune disease: from protein prenylation to immunomodulation. Nat Rev Immunol. 2006;6(5):358-370.
6. Stüve O, Youssef S, Weber MS, et al. Immunomodulatory synergy by combination of atorvastatin and glatiramer acetate in treatment of CNS autoimmunity. J Clin Invest. 2006;116(4):1037-1044.
7. Rudick RA, Pace A, Rani MR, et al. Effect of statins on clinical and molecular responses to intramuscular interferon beta-1a. Neurology. 2009;72(23):1989-1993.
8. Sorensen PS, Lycke J, Erälinna JP, et al; SIMCOMBIN study investigators. Simvastatin as add-on therapy to interferon β-1a for relapsing-remitting multiple sclerosis (SIMCOMBIN study): a placebo-controlled randomised phase 4 trial. Lancet Neurol. 2011;10(8):691-701.
9. Sellner J, Weber MS, Vollmar P, Mattle HP, Hemmer B, Stüve O. The combination of interferon-beta and HMG-CoA reductase inhibition in multiple sclerosis: enthusiasm lost too soon? CNS Neurosci Ther. 2010;16(6):362-373.
10. Birnbaum G, Cree B, Altafullah I, Zinser M, Reder AT. Combining beta interferon and atorvastatin may increase disease activity in multiple sclerosis. Neurology. 2008;71(18):1390-1395.
11. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem. 1998;67:227-264. (Pubitemid 28411130)
12. Takaoka A, Yanai H. Interferon signalling network in innate defence. Cell Microbiol. 2006;8(6):907-922. (Pubitemid 43670834)
13. Ghislain JJ, Fish EN. Application of genomic DNA affinity chromatography identifies multiple interferon-α-regulated Stat2 complexes. J Biol Chem . 1996;271(21):12408-12413. (Pubitemid 26160909)
14. Li X, Leung S, Qureshi S, Darnell JE Jr, Stark GR. Formation of STAT1-STAT2 heterodimers and their role in the activation of IRF-1 gene transcription by interferon-α. J Biol Chem. 1996;271(10):5790-5794. (Pubitemid 26083918)
15. Reder AT. MxA: a biomarker for predicting multiple sclerosis disease activity. Neurology. 2010;75(14):1222-1223.
16. Hinson ER, Joshi NS, Chen JH, et al. Viperin is highly induced in neutrophils and macrophages during acute and chronic lymphocytic choriomeningitis virus infection. J Immunol. 2010;184(10):5723-5731.
17. Vosslamber S, van Baarsen LG, Verweij CL. Pharmacogenomics of IFN-β in multiple sclerosis: towards a personalized medicine approach. Pharmacogenomics. 2009;10(1):97-108.
18. Ghittoni R, Patrussi L, Pirozzi K, et al. Simvastatin inhibits T-cell activation by selectively impairing the function of Ras superfamily GTPases. FASEB J. 2005;19(6):605-607. (Pubitemid 40471259)
19. Jabs WJ, Hennig, Zawatzky R, Kirchner H. Failure to detect antiviral activity in serum and plasma of healthy individuals displaying high activity in ELISA for IFN-alpha and IFN-beta. J Interferon Cytokine Res. 1999;19(5):463-469. (Pubitemid 29269936)
20. Niewold TB, Kelly JA, Flesch MH, Espinoza LR, Harley JB, Crow MK. Association of the IRF5 risk haplotype with high serum interferon-α activity in systemic lupus erythematosus patients. Arthritis Rheum. 2008;58(8):2481-2487.
21. Hua J, Kirou K, Lee C, Crow MK. Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies. Arthritis Rheum. 2006;54(6):1906-1916. (Pubitemid 43877940)
22. Niewold TB, Hua J, Lehman TJ, Harley JB, Crow MK. High serum IFN-α activity is a heritable risk factor for systemic lupus erythematosus. Genes Immun. 2007;8(6):492-502. (Pubitemid 47365615)
23. Niewold TB, Kariuki SN, Morgan GA, Shrestha S, Pachman LM. Elevated serum interferon-α activity in juvenile dermatomyositis: associations with disease activity at diagnosis and after thirty-six months of therapy. Arthritis Rheum. 2009;60(6):1815-1824.
24. Feng X, Reder NP, Yanamandala M, et al. Type I interferon signature is high in lupus and neuromyelitis optica but low in multiple sclerosis. J Neurol Sci. 2012;313(1-2):48-53.
25. van der Voort LF, Vennegoor A, Visser A, et al. Spontaneous MxA mRNA level predicts relapses in patients with recently diagnosed MS. Neurology. 2010;75(14):1228-1233.
26. Kwak B, Mulhaupt F, Myit S, Mach F. Statins as a newly recognized type of immunomodulator. Nat Med. 2000;6(12):1399-1402. (Pubitemid 32001026)
27. Reder AT, Velichko S, Yamaguchi KD, et al. IFN-β1b induces transient and variable gene expression in relapsing-remitting multiple sclerosis patients independent of neutralizing antibodies or changes in IFN receptor RNA expression. J Interferon Cytokine Res. 2008;28(5):317-331. (Pubitemid 351725305)
28. Youssef S, Stüve O, Patarroyo JC, et al. The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature. 2002;420(6911):78-84.
29. Zamvil SS, Steinman L. Cholesterol-lowering statins possess anti-inflammatory activity that might be useful for treatment of MS. Neurology. 2002;59(7):970-971.
30. Stüve O, Prod'homme T, Slavin A, et al. Statins and their potential targets in multiple sclerosis therapy. Expert Opin Ther Targets. 2003;7(5):613-622.
31. Neuhaus O, Stüve O, Archelos JJ, Hartung HP. Putative mechanisms of action of statins in multiple sclerosis: comparison to interferon-β and glatiramer acetate. J Neurol Sci. 2005;233(1-2):173-177. (Pubitemid 40804833)
32. Peng X, Jin J, Giri S, et al. Immunomodulatory effects of 3-hydroxy-3-methylglutaryl coenzyme-A reductase inhibitors, potential therapy for relapsing remitting multiple sclerosis. J Neuroimmunol. 2006;178(1-2):130- 139. (Pubitemid 44307344)
33. Aktas O, Waiczies S, Smorodchenko A, et al. Treatment of relapsing paralysis in experimental encephalomyelitis by targeting Th1 cells through atorvastatin. J Exp Med. 2003;197(6):725-733. (Pubitemid 36350867)
34. Zhang X, Jin J, Peng X, Ramgolam VS, Markovic-Plese S. Simvastatin inhibits IL-17 secretion by targeting multiple IL-17-regulatory cytokines and by inhibiting the expression of IL-17 transcription factor RORC in CD4+ lymphocytes. J Immunol. 2008;180(10):6988-6996.
35. + T cells derived from patients with multiple sclerosis. J Immunol. 2011;187(6):3431-3437.
36. Vollmer T, Key L, Durkalski V, et al. Oral simvastatin treatment in relapsingremitting multiple sclerosis. Lancet. 2004;363(9421):1607-1608. (Pubitemid 38625664)
37. Paul F, Waiczies S, Wuerfel J, et al. Oral high-dose atorvastatin treatment in re-lapsing- remitting multiple sclerosis. PLoS One. 2008;3(4):e1928.
38. Zhao Y, Traboulsee A, Petkau AJ, Li D. Regression of new gadolinium enhancing lesion activity in relapsing-remitting multiple sclerosis. Neurology. 2008;70(13, pt 2):1092-1097. (Pubitemid 351464765)
39. Dunn SE, Youssef S, Goldstein MJ, et al. Isoprenoids determine Th1/Th2 fate in pathogenic T cells, providing a mechanism of modulation of autoimmunity by atorvastatin. J Exp Med. 2006;203(2):401-412. (Pubitemid 43290849)
40. Ghittoni R, Napolitani G, Benati D, et al. Simvastatin inhibits the MHC class II pathway of antigen presentation by impairing Ras superfamily GTPases [published correction appears in Eur J Immunol. 2006;36(12):3381]. Eur J Immunol. 2006;36(11):2885-2893. (Pubitemid 44782562)
41. Feng X, Heyden NV, Ratner L. Alpha interferon inhibits human T-cell leukemia virus type 1 assembly by preventing Gag interaction with rafts. J Virol. 2003;77(24):13389-13395. (Pubitemid 37494332)
42. Kuipers HF, Biesta PJ, Groothuis TA, Neefjes JJ, Mommaas AM, van den Elsen PJ. Statins affect cell-surface expression of major histocompatibility complex class II molecules by disrupting cholesterol-containing microdomains. Hum Immunol. 2005;66(6):653-665. (Pubitemid 40922554)
43. Ehrenstein MR, Jury EC, Mauri C. Statins for atherosclerosis: as good as it gets? N Engl J Med. 2005;352(1):73-75.
44. Fessler MB, Parks JS. Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling. J Immunol. 2011;187(4):1529-1535.
45. Miron VE, Zehntner SP, Kuhlmann T, et al. Statin therapy inhibits remyelination in the central nervous system. Am J Pathol. 2009;174(5):1880-1890.
46. Sellner J, Greeve I, Findling O, et al. Effect of interferon-beta and atorvastatin on Th1/Th2 cytokines in multiple sclerosis. Neurochem Int. 2008;53(1-2):17-21.
47. Togha M, Karvigh SA, Nabavi M, et al. Simvastatin treatment in patients with relapsing-remitting multiple sclerosis receiving interferon beta 1a: a double-blind randomized controlled trial. Mult Scler. 2010;16(7):848-854.
48. Lanzillo R, Orefice G, Quarantelli M, et al. Atorvastatin Combined to Interferon to Verify the Efficacy (ACTIVE) in relapsing-remitting active multiple sclerosis patients: a longitudinal controlled trial of combination therapy. Mult Scler. 2010;16(4):450-454.
49. Corsini A, Bellosta S, Baetta R, Fumagalli R, Paoletti R, Bernini F. New insights into the pharmacodynamic and pharmacokinetic properties of statins. Pharmacol Ther. 1999;84(3):413-428.
50. Butterfield DA, Barone E, Mancuso C. Cholesterol-independent neuroprotective and neurotoxic activities of statins: perspectives for statin use in Alzheimer disease and other age-related neurodegenerative disorders. Pharmacol Res. 2011;64(3):180-186.
51. Neuvonen PJ, Niemi M, Backman JT. Drug interactions with lipid-lowering drugs: mechanisms and clinical relevance. Clin Pharmacol Ther . 2006;80(6):565-581. (Pubitemid 44908269)
52. Kajinami K, Akao H, Polisecki E, Schaefer EJ. Pharmacogenomics of statin responsiveness. Am J Cardiol. 2005;96(9A):65K-70K. (Pubitemid 41598115)
53. Germain RN. The art of the probable: system control in the adaptive immune system. Science. 2001;293(5528):240-245. (Pubitemid 32694729)