A clinical conundrum: the detrimental effect of TNF antagonists in multiple sclerosis

Pharmacogenomics

Volumn 14, Issue 12, 2013, Pages 1397-1404

  Dendrou, Calliope A ^a   Bell, John I ^b   Fugger, Lars ^a,c,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

anti TNF therapy; demyelination; genome wide association; multiple sclerosis; TNF; TNF antagonist; tumor necrosis factor

Indexed keywords

INFLIXIMAB; LENERCEPT; PLACEBO; TUMOR NECROSIS FACTOR INHIBITOR; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

ANKYLOSING SPONDYLITIS; ARTICLE; AUTOIMMUNE DISEASE; DISEASE EXACERBATION; DRUG EFFECT; GENE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC CODE; GENETIC RISK; GENETIC VARIABILITY; HUMAN; IMMUNOREGULATION; MULTIPLE SCLEROSIS; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PSORIASIS; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TNFR1 GENE; TNFR2 GENE; TNFRSF1A GENE;

GENOME-WIDE ASSOCIATION STUDY; HUMANS; INFLAMMATION; MOLECULAR TARGETED THERAPY; MULTIPLE SCLEROSIS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84883882190     PISSN: 14622416     EISSN: 17448042     Source Type: Journal    
DOI: 10.2217/pgs.13.140     Document Type: Article

References (53)

1. Wallach D, Engelmann H, Nophar Y et al. Soluble and cell-surface receptors for tumor-necrosis-factor. Agents Act.Suppl. 35, 51-57 (1991
2. Grell M. Tumor necrosis factor (TNF) receptors in cellular signaling of soluble and membrane-expressed TNF. J. Inflamm. 47(1-2), 8-17 (1996
3. Grell M, Wajant H, Zimmermann G et al. The type 1 receptor (CD120a) is the high-affinity receptor for soluble tumor necrosis factor. Proc. Natl Acad. Sci. USA 95(2), 570-575 (1998
4. Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: Integrating mammalian biology. Cell 104(4), 487-501 (2001
5. Cabal-Hierro L, Lazo PS. Signal transduction by tumor necrosis factor receptors. Cell Signal. 24(6), 1297-1305 (2012
6. Kang TB, Yang SH, Toth B et al. Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38(1), 27-40 (2013
7. van Herreweghe F, Festjens N, Declercq W et al. Tumor necrosis factor-mediated cell death: To break or to burst, that's the question. Cell. Mol. Life Sci. 67(10), 1567-1579 (2010
8. Grell M, Douni E, Wajant H et al The transmembrane form of tumor-necrosis-factor is the prime activating ligand of the 80 kDa tumor-necrosis-factor-receptor Cell 83(5), 793-802 (1995
9. Faustman D, Davis M. TNF receptor 2 pathway: Drug target for autoimmune diseases. Nat. Rev. Drug Dis. 9(6), 482-493 (2010
10. Eissner G, Kirchner S, Lindner H et al. Reverse signaling through transmembrane TNF confers resistance to lipopolysaccharide in human monocytes and macrophages. J. Immunol. 164(12), 6193-6198 (2000
11. Bradley Jr. TNF-mediated inflammatory disease. J. Pathol. 214(2), 149-160 (2008
12. Tristano AG. Neurological adverse events associated with anti-tumor necrosis factor a treatment. J. Neurol. 257(9), 1421-1431 (2010
13. Caminero A, Comabella M, Montalban X. Tumor necrosis factor a (TNF-a), anti-TNF-a and demyelination revisited: An ongoing story. J. Neuroimmunol. 234(1-2), 1-6 (2011
14. Hofman FM, Hinton DR, Johnson K et al. Tumor necrosis factor identified in multiple sclerosis brain. J. Exp. Med. 170(2), 607-612 (1989
15. Maimone D, Gregory S, Arnason BGW et al. Cytokine levels in the cerebrospinal-fluid and serum of patients with multiple-sclerosis. J. Neuroimmunol. 32(1), 67-74 (1991
16. Rieckmann P, Albrecht M, Kitze B et al. Tumor-necrosis-factor-a messenger-RNA expression in patients with relapsing-remitting multiple-sclerosis is associated with disease-activity. Ann. Neurol. 37(1), 82-88 (1995
17. Selmaj KW, Raine CS. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23(4), 339-346 (1988
18. Kuroda Y, Shimamoto Y. Human tumor-necrosis-factor-a augments experimental allergic encephalomyelitis in rats. J. Neuroimmunol. 34(2), 159-164 (1991
19. Ruddle NH, Bergman CM, McGrath KM et al. An antibody to lymphotoxin and tumor-necrosis-factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med. 172(4), 1193-1200 (1990
20. Selmaj K, Raine CS, Cross AH. Antitumor necrosis factor therapy abrogates autoimmune demyelination. Ann. Neurol. 30(5), 694-700 (1991
21. Baker D, Butler D, Scallon BJ et al. Control of established experimental allergic encephalomyelitis by inhibition of tumor-necrosis-factor (TNF) activity within the central nervous system using monoclonal antibodies and TNF receptor immunoglobulin fusion proteins. Eur. J. Immunol. 24(9), 2040-2048 (1994
22. Klinkert WEF, Kojima K, Lesslauer W et al. TNF-a receptor fusion protein prevents experimental auto-immune encephalomyelitis and demyelination in Lewis rats: An overview. J. Neuroimmunol. 72(2), 163-168 (1997
23. The Lenercept Multiple Sclerosis Study Group and The University of British Columbia MS/MRI Analysis Group. TNF neutralization in MS: Results of a randomized, placebo-controlled multicenter study. Neurology 53(3), 457-465 (1999
24. van Oosten BW, Barkhof F, Truyen L et al. Increased MRI activity and immune activation in two multiple sclerosis patients treated with the monoclonal anti-tumor necrosis factor antibody cA2. Neurology 47(6), 1531-1534 (1996
25. Bosch X, Saiz A, Ramos-Casals M et al. Monoclonal antibody therapy-associated neurological disorders. Nat. Rev. Neurol. 7(3), 165-172 (2011
26. Perez-Alvarez R, Perez-de-Lis M, Ramos-Casals M et al. Biologics-induced autoimmune diseases. Curr. Opin. Rheumatol. 25(1), 56-64 (2013
27. Titelbaum DS, Degenhardt A, Kinkel RP. Anti-tumor necrosis factor a-associated multiple sclerosis. Am. J. Neuroradiol. 26(6), 1548-1550 (2005
28. Weisman MH. What are the risks of biologic therapy in rheumatoid arthritis? An update on safety. J. Rheumatol. 2933-2938 (2002
29. Cope A, Ettinger R, McDevitt H. The role of TNF a and related cytokines in the development and function of the autoreactive T-cell repertoire. Res. Immunol. 148(5), 307-312 (1997
30. Robinson WH, Genovese MC, Moreland LW. Demyelinating and neurologic events reported in association with tumor necrosis factor a antagonism: By what mechanisms could tumor necrosis factor a antagonists improve rheumatoid arthritis but exacerbate multiple sclerosis? Arthritis Rheum. 44(9), 1977-1983 (2001
31. Sawcer S, Hellenthal G, Pirinen M et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476(7359), 214-219 (2011
32. Gregory AP, Dendrou CA, Attfield KE et al. TNF receptor 1 genetic risk mirrors outcome of anti-TNF therapy in multiple sclerosis. Nature 488(7412), 508-511 (2012
33. International Genetics of Ankylosing Spondylitis Consortium (IGAS), Cortes A, Hadler J et al. Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci. Nat. Genet. 45(7), 730-738 (2013
34. Braun J, Brandt J, Listing J et al. Treatment of active ankylosing spondylitis with infliximab: A randomised controlled multicentre trial. Lancet 359(9313), 1187-1193 (2002
35. Methner A, Zipp F. Novel therapeutic options and drug targets in MS. Nat. Rev. Neurol. 9(2), 72-73 (2013
36. Korner H, Riminton DS, Strickland DH et al. Critical points of tumor necrosis factor action in central nervous system autoimmune inflammation defined by gene targeting. J. Exp. Med. 186(9), 1585-1590 (1997
37. Kassiotis G, Pasparakis M, Kollias G et al. TNF accelerates the onset but does not alter the incidence and severity of myelin basic protein-induced experimental autoimmune encephalomyelitis. Eur. J. Immunol. 29(3), 774-780 (1999
38. Liu JL, Marino MW, Wong G et al. TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 4(1), 78-83 (1998
39. Attfield KE, Dendrou CA, Fugger L. Bridging the gap from genetic association to functional understanding: The next generation of mouse models of multiple sclerosis. Immunol. Rev. 24810-24822 (2012
40. Evangelidou M, Tseveleki V, Vamvakas SS et al. TNFRI is a positive T-cell costimulatory molecule important for the timing of cytokine responses. Immunol. Cell Biol. 88(5), 586-595 (2010
41. Prinz JC. Autoimmune-like syndromes during TNF blockade: Does infection have a role? Nat. Rev. Rheumatol. 7(7), 429-434 (2011
42. Elicabe RJ, Cargnelutti E, Serer MI et al. Lack of TNFR p55 results in heightened expression of IFN-g and IL-17 during the development of reactive arthritis. J. Immunol. 185(7), 4485-4495 (2010
43. Compston A, Coles A. Multiple sclerosis. Lancet 372(9648), 1502-1517 (2008
44. Fugger L, Friese MA, Bell JI. From genes to function: The next challenge to understanding multiple sclerosis. Nat. Rev. Immunol. 9(6), 408-417 (2009
45. Kodama S, Davis M, Faustman DL. The therapeutic potential of tumor necrosis factor for autoimmune disease: A mechanistically based hypothesis. Cell. Mol. Life Sci. 62(16), 1850-1862 (2005
46. Kassiotis G, Kollias G. Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: Implications for pathogenesis and therapy of autoimmune demyelination. J. Exp. Med. 193(4), 427-434 (2001
47. Alexopoulou L, Kranidioti K, Xanthoulea S et al. Transmembrane TNF protects mutant mice against intracellular bacterial infections, chronic inflammation and autoimmunity. Eur. J. Immunol. 36(10), 2768-2780 (2006
48. Taoufik E, Tseveleki V, Chu SY et al. Transmembrane tumour necrosis factor is neuroprotective and regulates experimental autoimmune encephalomyelitis via neuronal nuclear factor-kB. Brain 134, 2722-2735 (2011
49. Brambilla R, Ashbaugh JJ, Magliozzi R et al. Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain 134, 2736-2754 (2011
50. Suvannavejh GC, Lee HO, Padilla J et al. Divergent roles for p55 and p75 tumor necrosis factor receptors in the pathogenesis of MOG(35-55)-induced experimental autoimmune encephalomyelitis. Cell. Immunol. 205(1), 24-33 (2000
51. Arnett HA, Mason J, Marino M et al. TNF a promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 4(11), 1116-1122 (2001
52. Figiel I. Pro-inflammatory cytokine TNF-a as a neuroprotective agent in the brain. Acta Neurobiol. Exp. 68(4), 526-534 (2008
53. Lambertsen KL, Clausen BH, Babcock AA et al. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J. Neurosci. 29(5), 1319-1330 (2009