Soluble gp130 prevents interleukin-6 and interleukin-11 cluster signaling but not intracellular autocrine responses

Science Signaling

Volumn 11, Issue 550, 2018, Pages

  Lamertz, Larissa ^a   Rummel, Franziska ^a   Polz, Robin ^a   Baran, Paul ^a   Hansen, Selina ^a   Waetzig, Georg H ^b   Moll, Jens M ^a   Floss, Doreen M ^a   Scheller, Jürgen ^a  

^a Department of Orthopedic Surgery   (Germany)

^b CONARIS Research Institute AG ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 130; INTERLEUKIN 11; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; PROTEIN BINDING;

ANIMAL; AUTOCRINE EFFECT; CELL LINE; CHO CELL LINE; CRICETULUS; HAMSTER; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; SIGNAL TRANSDUCTION; SOLUBILITY;

ANIMALS; AUTOCRINE COMMUNICATION; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOKINE RECEPTOR GP130; HEK293 CELLS; HUMANS; INTERLEUKIN-11; INTERLEUKIN-6; MICE; PROTEIN BINDING; RECEPTORS, INTERLEUKIN-6; SIGNAL TRANSDUCTION; SOLUBILITY;

EID: 85054348552     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aar7388     Document Type: Article

References (37)

1. J. Scheller, A. Chalaris, D. Schmidt-Arras, S. Rose-John, The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 1813, 878–888 (2011).
2. S. Rose-John, K. Winthrop, L. Calabrese, The role of IL-6 in host defence against infections: Immunobiology and clinical implications. Nat. Rev. Rheumatol. 13, 399–409 (2017).
3. C. Garbers, H. M. Hermanns, F. Schaper, G. Müller-Newen, J. Grötzinger, S. Rose-John, J. Scheller, Plasticity and cross-talk of interleukin 6-type cytokines. Cytokine Growth Factor Rev. 23, 85–97 (2012).
4. T. Jostock, J. Mullberg, S. Özbek, R. Atreya, G. Blinn, N. Voltz, M. Fischer, M. F. Neurath, S. Rose-John, Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur. J. Biochem. 268, 160–167 (2001).
5. J. Scheller, A. Chalaris, C. Garbers, S. Rose-John, ADAM17: A molecular switch to control inflammatory and regenerative responses. Trends Immunol. 32, 380–387 (2011).
6. S. A. Jones, J. Scheller, S. Rose-John, Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J. Clin. Invest. 121, 3375–3383 (2011).
7. S. Rose-John, The soluble interleukin 6 receptor: Advanced therapeutic options in inflammation. Clin. Pharmacol. Ther. 102, 591–598 (2017).
8. C. Garbers, W. Thaiss, G. W. Jones, G. H. Waetzig, I. Lorenzen, F. Guilhot, R. Lissilaa, W. G. Ferlin, J. Grötzinger, S. A. Jones, S. Rose-John, J. Scheller, Inhibition of classic signaling is a novel function of soluble glycoprotein 130 (sgp130), which is controlled by the ratio of interleukin 6 and soluble interleukin 6 receptor. J. Biol. Chem. 286, 42959–42970 (2011).
9. S. Heink, N. Yogev, C. Garbers, M. Herwerth, L. Aly, C. Gasperi, V. Husterer, A. L. Croxford, K. Möller-Hackbarth, H. Bartsch, K. Sotlar, S. Krebs, T. Regen, H. Blum, B. Hemmer, T. Misgeld, T. F. Wunderlich, J. Hidalgo, M. Oukka, S. Rose-John, M. Schmidt-Supprian, A. Waisman, T. Korn, Trans-presentation of IL-6 by dendritic cells is required for the priming of pathogenic TH17 cells. Nat. Immunol. 18, 74–85 (2017).
10. + T cell function. Cell Rep. 8, 1318–1327 (2014).
11. C. Garbers, J. Scheller, Interleukin-6 and interleukin-11: Same same but different. Biol. Chem. 394, 1145–1161 (2013).
12. M. Mihara, K. Kasutani, M. Okazaki, A. Nakamura, S. Kawai, M. Sugimoto, Y. Matsumoto, Y. Ohsugi, Tocilizumab inhibits signal transduction mediated by both mIL-6R and sIL-6R, but not by the receptors of other members of IL-6 cytokine family. Int. Immunopharmacol. 5, 1731–1740 (2005).
13. J.-P. Gaillard, M. Pugnière, J.-P. Tresca, J.-C. Mani, B. Klein, J. Brochier, Interleukin-6 receptor signaling. II. Bio-availability of interleukin-6 in serum. Eur. Cytokine Netw. 10, 337–344 (1999).
14. M. Fischer, J. Goldschmitt, C. Peschel, J. P. G. Brakenhoff, K.-J. Kallen, A. Wollmer, J. Grötzinger, S. Rose-John, A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat. Biotechnol. 15, 145–145 (1997).
15. H. Yawata, K. Yasukawa, S. Natsuka, M. Murakami, K. Yamasaki, M. Hibi, T. Taga, T. Kishimoto, Structure-function analysis of human IL-6 receptor: Dissociation of amino acid residues required for IL-6-binding and for IL-6 signal transduction through gp130. EMBO J. 12, 1705–1712 (1993).
16. A. Chalaris, B. Rabe, K. Paliga, H. Lange, T. Laskay, C. A. Fielding, S. A. Jones, S. Rose-John, J. Scheller, Apoptosis is a natural stimulus of IL6R shedding and contributes to the pro-inflammatory trans-signaling function of neutrophils. Blood 110, 1748–1755 (2007).
17. R. Adams, R. J. Burnley, C. R. Valenzano, O. Qureshi, C. Doyle, S. Lumb, M. del Carmen Lopez, R. Griffin, D. McMillan, R. D. Taylor, C. Meier, P. Mori, L. M. Griffin, U. Wernery, J. Kinne, S. Rapecki, T. Baker, A. Lawson, M. Wright, A. Ettorre, Discovery of a junctional epitope antibody that stabilizes IL-6 and gp80 protein:protein interaction and modulates its downstream signaling. Sci. Rep. 7, 37716 (2017).
18. A. L. Mui, H. Wakao, A. M. O’Farrell, N. Harada, A. Miyajima, Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two STAT5 homologs. EMBO J. 14, 1166–1175 (1995).
19. 2 protein-ligation generates active IL-6-type hyper-cytokines from inactive precursors. ACS Synth. Biol. 6, 2260–2272 (2017).
20. H. Dams-Kozlowska, K. Gryska, E. Kwiatkowska-Borowczyk, D. Izycki, S. Rose-John, A. Mackiewicz, A designer hyper interleukin 11 (H11) is a biologically active cytokine. BMC Biotechnol. 12, 8 (2012).
21. J. Lokau, R. Nitz, M. Agthe, N. Monhasery, S. Aparicio-Siegmund, N. Schumacher, J. Wolf, K. Möller-Hackbarth, G. H. Waetzig, J. Grötzinger, G. Müller-Newen, S. Rose-John, J. Scheller, C. Garbers, Proteolytic cleavage governs interleukin-11 trans-signaling. Cell Rep. 14, 1761–1773 (2016).
22. J. E. Thompson, R. M. Cubbon, R. T. Cummings, L. S. Wicker, R. Frankshun, B. R. Cunningham, P. M. Cameron, P. T. Meinke, N. Liverton, Y. Weng, J. A. DeMartino, Photochemical preparation of a pyridone containing tetracycle: A Jak protein kinase inhibitor. Bioorg. Med. Chem. Lett. 12, 1219–1223 (2002).
23. J. Wijdenes, P. C. Heinrich, G. Müller-Newen, C. Roche, Z.-J. Gu, C. Clément, B. Klein, Interleukin-6 signal transducer gp130 has specific binding sites for different cytokines as determined by antagonistic and agonistic anti-gp130 monoclonal antibodies. Eur. J. Immunol. 25, 3474–3481 (1995).
24. M. Kovaleva, I. Bussmeyer, B. Rabe, J. Grötzinger, E. Sudarman, J. Eichler, U. Conrad, S. Rose-John, J. Scheller, Abrogation of viral interleukin-6 (vIL-6)-induced signaling by intracellular retention and neutralization of vIL-6 with an anti-vIL-6 single-chain antibody selected by phage display. J. Virol. 80, 8510–8520 (2006).
25. M. B. Meads, P. G. Medveczky, Kaposi’s sarcoma-associated herpesvirus-encoded viral interleukin-6 is secreted and modified differently than human interleukin-6: Evidence for a unique autocrine signaling mechanism. J. Biol. Chem. 279, 51793–51803 (2004).
26. N. Rinis, A. Küster, H. Schmitz-Van de Leur, A. Mohr, G. Müller-Newen, Intracellular signaling prevents effective blockade of oncogenic gp130 mutants by neutralizing antibodies. Cell Commun. Signal 12, 14 (2014).
27. D. Schmidt-Arras, M. Müller, M. Stevanovic, S. Horn, A. Schütt, J. Bergmann, R. Wilkens, A. Lickert, S. Rose-John, Oncogenic deletion mutants of gp130 signal from intracellular compartments. J. Cell Sci. 127, 341–353 (2014).
28. S. Tenhumberg, B. Schuster, L. Zhu, M. Kovaleva, J. Scheller, K.-J. Kallen, S. Rose-John, gp130 dimerization in the absence of ligand: Preformed cytokine receptor complexes. Biochem. Biophys. Res. Commun. 346, 649–657 (2006).
29. B. Giese, C. Roderburg, M. Sommerauer, S. B. Wortmann, S. Metz, P. C. Heinrich, G. Müller-Newen, Dimerization of the cytokine receptors gp130 and LIFR analysed in single cells. J. Cell Sci. 118, 5129–5140 (2005).
30. D. Zohlnhöfer, L. Graeve, S. Rose-John, H. Schooltink, E. Dittrich, P. C. Heinrich, The hepatic interleukin-6 receptor. Down-regulation of the interleukin-6 binding subunit (gp80) by its ligand. FEBS Lett. 306, 219–222 (1992).
31. J. Fritsch, P. Zingler, V. Särchen, A. L. Heck, S. Schütze, Role of ubiquitination and proteolysis in the regulation of pro- and anti-apoptotic TNF-R1 signaling. Biochim. Biophys. Acta 1864, 2138–2146 (2017).
32. C. L. German, B. M. Sauer, C. L. Howe, The STAT3 beacon: IL-6 recurrently activates STAT 3 from endosomal structures. Exp. Cell Res. 317, 1955–1969 (2011).
33. A. J. H. Gearing, P. Beckett, M. Christodoulou, M. Churchill, J. Clements, A. H. Davidson, A. H. Drummond, W. A. Galloway, R. Gilbert, J. L. Gordon, T. M. Leber, M. Mangan, K. Miller, P. Nayee, K. Owen, S. Patel, W. Thomas, G. Wells, L. M. Wood, K. Woolley, Processing of tumour necrosis factor- precursor by metalloproteinases. Nature 370, 555–557 (1994).
34. A. Schroers, O. Hecht, K.-J. Kallen, M. Pachta, S. Rose-John, J. Grötzinger, Dynamics of the gp130 cytokine complex: A model for assembly on the cellular membrane. Protein Sci. 14, 783–790 (2005).
35. A. Ludwig, C. Hundhausen, M. H. Lambert, N. Broadway, R. C. Andrews, D. M. Bickett, M. A. Leesnitzer, J. D. Becherer, Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Comb. Chem. High Throughput Screen. 8, 161–171 (2005).
36. J. Suthaus, A. Tillmann, I. Lorenzen, E. Bulanova, S. Rose-John, J. Scheller, Forced homo- and heterodimerization of all gp130-type receptor complexes leads to constitutive ligand-independent signaling and cytokine-independent growth. Mol. Biol. Cell 21, 2797–2807 (2010).
37. D. M. Floss, S. Mrotzek, T. Klöcker, J. Schröder, J. Grözinger, S. Rose-John, J. Scheller, Identification of canonical tyrosine-dependent and non-canonical tyrosine-independent STAT3 activation sites in the intracellular domain of the interleukin 23 receptor. J. Biol. Chem. 288, 19386–19400 (2013).