Dominant-negative inhibitors of soluble TNF attenuate experimental arthritis without suppressing innate immunity to infection

Journal of Immunology

Volumn 179, Issue 3, 2007, Pages 1872-1883

  Zalevsky, Jonathan ^a   Secher, Thomas ^b   Ezhevsky, Sergei A ^a   Janot, Laure ^b   Steed, Paul M ^a   O'Brien, Christopher ^a   Eivazi, Araz ^a   Kung, James ^a   Nguyen, Duc Hanh T ^a   Doberstein, Stephen K ^a   Erard, François ^b   Ryffel, Bernhard ^b   Szymkowski, David E ^a  

^a Xencor Inc   (United States)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; AUTACOID; CASPASE; INTERLEUKIN 8; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTHRITIS; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BLOOD; CELL STRAIN U937; COMPARATIVE STUDY; DBA MOUSE; DRUG ANTAGONISM; GENETICS; IMMUNOLOGY; LISTERIOSIS; METABOLISM; PARACRINE SIGNALING; PATHOLOGY; PHYSIOLOGY; SECRETION; SOLUBILITY; TUMOR CELL LINE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CASPASES; CELL LINE, TUMOR; FEMALE; HUMANS; IMMUNITY, NATURAL; INFLAMMATION MEDIATORS; INTERLEUKIN-8; LISTERIA INFECTIONS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED DBA; PARACRINE COMMUNICATION; RECOMBINANT PROTEINS; SOLUBILITY; TUMOR NECROSIS FACTOR-ALPHA; U937 CELLS;

EID: 34548657310     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.3.1872     Document Type: Article

References (62)

1. Aggarwal, B. B., A. Samanta, and M. Feldmann. 2000. TNF-α. In Cytokine Reference. J. J. Oppenheim, and M. Feldmann, eds. Academic Press, London, pp. 413-434.
2. Kollias, G., and D. Kontoyiannis. 2002. Role of TNF/TNFR in autoimmunity: specific TNF receptor blockade may be advantageous to anti-TNF treatments. Cytokine Growth Factor Rev. 13: 315-321.
3. Botha, T., and B. Ryffel. 2003. Reactivation of latent tuberculosis infection in TNF-deficient mice. J. Immunol. 171: 3110-3118.
4. Arnett, H. A., Y. Wang, G. K. Matsushima, K. Suzuki, and J. P. Ting. 2003. Functional genomic analysis of remyelination reveals importance of inflammation in oligodendrocyte regeneration. J. Neurosci. 23: 9824-9832.
5. Pikarsky, E., R. M. Porat, I. Stein, R. Abramovitch, S. Amit, S. Kasem, E. Gutkovich-Pyest, S. Urieli-Shoval, E. Galun, and Y. Ben-Neriah. 2004. NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature 431: 461-466.
6. Holtmann, M. H., and M. F. Neurath. 2004. Differential TNF-signaling in chronic inflammatory disorders. Curr. Mol. Med. 4: 439-444.
7. Ruuls, S. R., R. M. Hoek, V. N. Ngo, T. McNeil, L. A. Lucian, M. J. Janatpour, H. Korner, H. Scheerens, E. M. Hessel, J. G. Cyster, et al. 2001. Membrane-bound TNF supports secondary lymphoid organ structure but is subservient to secreted TNF in driving autoimmune inflammation. Immunity 15: 533-543.
8. Canault, M., F. Peiretti, C. Mueller, F. Kopp, P. Morange, S. Rihs, H. Portugal, I. Juhan-Vague, and G. Nalbone. 2004. Exclusive expression of transmembrane TNF-α in mice reduces the inflammatory response in early lipid lesions of aortic sinus. Atherosclerosis 172: 211-218.
9. Mueller, C., N. Corazza, S. Trachsel-Loseth, H. P. Eugster, M. Buhler-Jungo, T. Brunner, and M. A. Imboden. 1999. Noncleavable transmembrane mouse tumor necrosis factor-α (TNFα) mediates effects distinct from those of wild-type TNFα in vitro and in vivo. J. Biol. Chem. 274: 38112-38118.
10. Alexopoulou, L., K. Kranidioti, S. Xanthoulea, M. Denis, A. Kotanidou, E. Douni, P. J. Blackshear, D. L. Kontoyiannis, and G. Kollias. 2006. Transmembrane TNF protects mutant mice against intracellular bacterial infections, chronic inflammation and autoimmunity. Eur. J. Immunol. 36: 2768-2780.
11. Pasparakis, M., L. Alexopoulou, V. Episkopou, and G. Kollias. 1996. Immune and inflammatory responses in TNFα-deficient mice: a critical requirement for TNFα in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 184: 1397-1411.
12. Torres, D., L. Janot, V. F. Quesniaux, S. I. Grivennikov, I. Maillet, J. D. Sedgwick, B. Ryffel, and F. Erard. 2005. Membrane tumor necrosis factor confers partial protection to Listeria infection. Am. J. Pathol. 167: 1677-1687.
13. Olleros, M. L., R. Guler, D. Vesin, R. Parapanov, G. Marchal, E. Martinez-Soria, N. Corazza, J. C. Pache, C. Mueller, and I. Garcia. 2005. Contribution of transmembrane tumor necrosis factor to host defense against Mycobacterium bovis bacillus Calmette-guerin and Mycobacterium tuberculosis infections. Am. J. Pathol. 166: 1109-1120.
14. Saunders, B. M., S. Tran, S. Ruuls, J. D. Sedgwick, H. Briscoe, and W. J. Britton. 2005. Transmembrane TNF is sufficient to initiate cell migration and granuloma formation and provide acute, but not long-term, control of Mycobacterium tuberculosis infection. J. Immunol. 174: 4852-4859.
15. Fremond, C., N. Allie, I. Dambuza, S. I. Grivennikov, V. Yeremeev, V. F. Quesniaux, M. Jacobs, and B. Ryffel. 2005. Membrane TNF confers protection to acute mycobacterial infection. Respir. Res. 6: 136.
16. Jacobs, M., A. Samarina, S. Grivennikov, T. Botha, N. Allie, C. Fremond, D. Togbe, V. Vasseur, S. Rose, F. Erard, et al. 2007. Review: reactivation of tuberculosis by tumor necrosis factor neutralization. Eur. Cytokine Network 18: 1-9.
17. Jacob, C. O. 1992. Tumor necrosis factor α in autoimmunity: pretty girl or old witch? Immunol. Today 13: 122-125.
18. Saha, R. N., and K. Pahan. 2003. Tumor necrosis factor-α at the crossroads of neuronal life and death during HIV-associated dementia. J. Neurochem. 86: 1057-1071.
19. Grivennikov, S. I., A. V. Tumanov, D. J. Liepinsh, A. A. Kruglov, B. I. Marakusha, A. N. Shakhov, T. Murakami, L. N. Drutskaya, I. Forster, B. E. Clausen, et al. 2005. Distinct and nonredundant in vivo functions of TNF produced by T cells and macrophages/neutrophils; protective and deleterious effects. Immunity 22: 93-104.
20. Scheinfeld, N. 2004. A comprehensive review and evaluation of the side effects of the tumor necrosis factor α blockers etanercept, infliximab and adalimumab. J. Dermatolog. Treat. 15: 280-294.
21. Slifman, N. R., S. K. Gershon, J. H. Lee, E. T. Edwards, and M. M. Braun. 2003. Listeria monocytogenes infection as a complication of treatment with tumor necrosis factor α-neutralizing agents. Arthritis Rheum. 48: 319-324.
22. Wallis, R. S., M. S. Broder, J. Y. Wong, M. E. Hanson, and D. O. Beenhouwer. 2004. Granulomatous infectious diseases associated with tumor necrosis factor antagonists. Clin. Infect. Dis. 38: 1261-1265.
23. Wallis, R. S., M. Broder, J. Wong, and D. Beenhouwer. 2004. Granulomatous infections due to tumor necrosis factor blockade: correction. Clin. Infect. Dis. 39: 1254-1255.
24. Bongartz, T., A. J. Sutton, M. J. Sweeting, I. Buchan, E. L. Matteson, and V. Montori. 2006. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. J. Am. Med. Assoc. 295: 2275-2285.
25. Agnholt, J., J. F. Dahlerup, and K. Kaltoft. 2003. The effect of etanercept and infliximab on the production of tumour necrosis factor α, interferon-γ and GMCSF in in vivo activated intestinal T lymphocyte cultures. Cytokine 23: 76-85.
26. Scallon, B., A. Cai, N. Solowski, A. Rosenberg, X. Y. Song, D. Shealy, and C. Wagner. 2002. Binding and functional comparisons of two types of tumor necrosis factor antagonists. J. Pharmacol. Exp. Ther. 301: 418-426.
27. Shen, C., G. V. Assche, S. Colpaert, P. Maerten, K. Geboes, P. Rutgeerts, and J. L. Ceuppens. 2005. Adalimumab induces apoptosis of human monocytes: a comparative study with infliximab and etanercept. Aliment Pharmacol. Ther. 21: 251-258.
28. Mitoma, H., T. Horiuchi, N. Hatta, H. Tsukamoto, S. Harashima, Y. Kikuchi, J. Otsuka, S. Okamura, S. Fujita, and M. Harada. 2005. Infliximab induces potent anti-inflammatory responses by outside-to-inside signals through transmembrane TNF-α. Gastroenterology 128: 376-392.
29. Steed, P. M., M. G. Tansey, J. Zalevsky, E. A. Zhukovsky, J. R. Desjarlais, D. E. Szymkowski, C. Abbott, D. Carmichael, C. Chan, L. Cherry, et al. 2003. Inactivation of TNF signaling by rationally designed dominant-negative TNF variants. Science 301: 1895-1898.
30. McCoy, M. K., T. N. Martinez, K. A. Ruhn, D. E. Szymkowski, C. G. Smith, B. R. Botterman, K. E. Tansey, and M. G. Tansey. 2006. Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J. Neurosci. 26: 9365-9375.
31. Hug, H., M. Los, W. Hirt, and K. M. Debatin. 1999. Rhodamine 110-linked amino acids and peptides as substrates to measure caspase activity upon apoptosis induction in intact cells. Biochemistry 38: 13906-13911.
32. Perez, C., I. Albert, K. DeFay, N. Zachariades, L. Gooding, and M. Kriegler. 1990. A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact. Cell 63: 251-258.
33. Torres, D., M. Barrier, F. Bihl, V. J. Quesniaux, I. Maillet, S. Akira, B. Ryffel, and F. Erard. 2004. Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect. Immun. 72: 2131-2139.
34. Loetscher, H., D. Stueber, D. Banner, F. Mackay, and W. Lesslauer. 1993. Human tumor necrosis factor α (TNFα) mutants with exclusive specificity for the 55-kDa or 75-kDa TNF receptors. J. Biol. Chem. 268: 26350-26357.
35. Fujita, E., T. Mukasa, T. Tsukahara, K. Arahata, S. Omura, and T. Momoi. 1996. Enhancement of CPP32-like activity in the TNF-treated U937 cells by the proteasome inhibitors. Biochem. Biophys. Res. Commun. 224: 74-79.
36. Varghese, J., S. Chattopadhaya, and A. Sarin. 2001. Inhibition of p38 kinase reveals a TNF-α-mediated, caspase-dependent, apoptotic death pathway in a human myelomonocyte cell line. J. Immunol. 166: 6570-6577.
37. Hohmann, H. P., R. Remy, M. Brockhaus, and A. P. van Loon. 1989. Two different cell types have different major receptors for human tumor necrosis factor (TNF α). J. Biol. Chem. 264: 14927-14934.
38. Wright, S. C., P. Kumar, A. W. Tam, N. Shen, M. Varma, and J. W. Larrick. 1992. Apoptosis and DNA fragmentation precede TNF-induced cytolysis in U937 cells. J. Cell. Biochem. 48: 344-355.
39. Faraco, P. R., E. C. Ledgerwood, P. Vandenabeele, J. B. Prins, and J. R. Bradley. 1999. Tumor necrosis factor induces distinct patterns of caspase activation in WEHI-164 cells associated with apoptosis or necrosis depending on cell cycle stage. Biochem. Biophys. Res. Commun. 261: 385-392.
40. Khabar, K. S., S. Siddiqui, and J. A. Armstrong. 1995. WEHI-13VAR: a stable and sensitive variant of WEHI 164 clone 13 fibrosarcoma for tumor necrosis factor bioassay. Immunol. Lett. 46: 107-110.
41. Ameloot, P., W. Declercq, W. Fiers, P. Vandenabeele, and P. Brouckaert. 2001. Heterotrimers formed by tumor necrosis factors of different species or muteins. J. Biol. Chem. 276: 27098-27103.
42. Decoster, E., B. Vanhaesebroeck, P. Vandenabeele, J. Grooten, and W. Fiers. 1995. Generation and biological characterization of membrane-bound, uncleavable murine tumor necrosis factor. J. Biol. Chem. 270: 18473-18478.
43. Fiorucci, S., E. Antonelli, G. Migliorati, L. Santucci, O. Morelli, B. Federici, and A. Morelli. 1998. TNFα processing enzyme inhibitors prevent aspirin-induced TNFα release and protect against gastric mucosal injury in rats. Aliment Pharmacol. Ther. 12: 1139-1153.
44. Frishman, J. I., C. K. Edwards III, M. G. Sonnenberg, T. Kohno, A. M. Cohen, and C. A. Dinarello. 2000. Tumor necrosis factor (TNF)-α-induced interleukin-8 in human blood cultures discriminates neutralization by the p55 and p75 TNF soluble receptors. J. Infect. Dis. 182: 1722-1730.
45. DeForge, L. E., J. S. Kenney, M. L. Jones, J. S. Warren, and D. G. Remick. 1992. Biphasic production of IL-8 in lipopolysaccharide (LPS)-stimulated human whole blood: separation of LPS- and cytokine-stimulated components using antitumor necrosis factor and anti-IL-1 antibodies. J. Immunol. 148: 2133-2141.
46. Terato, K., K. A. Hasty, R. A. Reife, M. A. Cremer, A. H. Kang, and J. M. Stuart. 1992. Induction of arthritis with monoclonal antibodies to collagen. J. Immunol. 148: 2103-2108.
47. Nandakumar, K. S., and R. Holmdahl. 2005. Efficient promotion of collagen antibody induced arthritis (CAIA) using four monoclonal antibodies specific for the major epitopes recognized in both collagen induced arthritis and rheumatoid arthritis. J. Immunol. Methods 304: 126-136.
48. Kagari, T., H. Doi, and T. Shimozato. 2002. The importance of IL-1β and TNF-α, and the noninvolvement of IL-6, in the development of monoclonal antibody-induced arthritis. J. Immunol. 169: 1459-1466.
49. Joosten, L. A., M. M. Helsen, F. A. van de Loo, and W. B. van den Berg. 1996. Anticytokine treatment of established type II collagen-induced arthritis in DBA/1 mice. A comparative study using anti-TNFα, anti-IL-1α/ β, and IL-1Ra. Arthritis Rheum. 39: 797-809.
50. Wooley, P. H., J. Dutcher, M. B. Widmer, and S. Gillis. 1993. Influence of a recombinant human soluble tumor necrosis factor receptor FC fusion protein on type II collagen-induced arthritis in mice. J. Immunol. 151: 6602-6607.
51. Coppieters, K., T. Dreier, K. Silence, H. de Haard, M. Lauwereys, P. Casteels, E. Beirnaert, H. Jonckheere, C. Van de Wiele, L. Staelens, et al. 2006. Formatted anti-tumor necrosis factor α VHH proteins derived from camelids show superior potency and targeting to inflamed joints in a murine model of collagen-induced arthritis. Arthritis Rheum. 54: 1856-1866.
52. Jacobs, M., D. Togbe, C. Fremond, A. Samarina, N. Allie, T. Botha, D. Carlos, S. K. Parida, S. Grivennikov, S. Nedospasov, et al. 2007. Tumor necrosis factor is critical to control tuberculosis infection. Microbes Infect. 9: 623-628.
53. Pennica, D., G. E. Nedwin, J. S. Hayflick, P. H. Seeburg, R. Derynck, M. A. Palladino, W. J. Kohr, B. B. Aggarwal, and D. V. Goeddel. 1984. Human tumour necrosis factor: precursor structure, expression and homology to lymphotoxin. Nature 312: 724-729.
54. Utsumi, T., T. Takeshige, K. Tanaka, K. Takami, Y. Kira, J. Klostergaard, and R. Ishisaka. 2001. Transmembrane TNF (pro-TNF) is palmitoylated. FEBS Lett. 500: 1-6.
55. Rutschmann, S., K. Hoebe, J. Zalevsky, X. Du, N. Mann, B. I. Dahiyat, P. Steed, and B. Beutler. 2006. PanR1, a dominant negative missense allele of the gene encoding TNF-α (Tnf), does not impair lymphoid development. J. Immunol. 176: 7525-7532.
56. Wajant, H., K. Pfizenmaier, and P. Scheurich. 2003. Tumor necrosis factor signaling. Cell Death Differ. 10: 45-65.
57. Grell, M. 1995. Tumor necrosis factor (TNF) receptors in cellular signaling of soluble and membrane-expressed TNF. J. Inflamm. 47: 8-17.
58. Grell, M., H. Wajant, G. Zimmermann, and P. Scheurich. 1998. The type 1 receptor (CD120a) is the high-affinity receptor for soluble tumor necrosis factor. Proc. Natl. Acad. Sci. USA 95: 570-575.
59. Grell, M., E. Douni, H. Wajant, M. Lohden, M. Clauss, B. Maxeiner, S. Georgopoulos, W. Lesslauer, G. Kollias, K. Pfizenmaier, and P. Scheurich. 1995. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 83: 793-802.
60. Eissner, G., W. Kolch, and P. Scheurich. 2004. Ligands working as receptors: reverse signaling by members of the TNF superfamily enhance the plasticity of the immune system. Cytokine Growth Factor Rev. 15: 353-366.
61. Edwards, C. K., III, A. M. Bendele, L. I. Reznikov, G. Fantuzzi, E. S. Chlipala, L. Li, L. L. Moldawer, J. D. Mountz, Y. Y. Li, and C. A. Dinarello. 2006. Soluble human p55 and p75 tumor necrosis factor receptors reverse spontaneous arthritis in transgenic mice expressing transmembrane tumor necrosis factor α. Arthritis Rheum. 54: 2872-2885.
62. Alexopoulou, L., M. Pasparakis, and G. Kollias. 1997. A murine transmembrane tumor necrosis factor (TNF) transgene induces arthritis by cooperative p55/p75 TNF receptor signaling. Eur. J. Immunol. 27: 2588-2592.