The soluble interleukin-6 receptor and related proteins

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 29, Issue 5, 2015, Pages 787-797

  Rose John, Stefan ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

ADAM protease; cancer; cytokine; inflammation; receptor; shedding; trans signaling

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR RECEPTOR; GAMMA INTERFERON RECEPTOR; GLYCOPROTEIN GP 130; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 6 RECEPTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; ANTINEOPLASTIC AGENT; INTERLEUKIN 6;

ANTIINFLAMMATORY ACTIVITY; HUMAN; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ALTERNATIVE RNA SPLICING; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; GENETICS; METABOLISM;

ALTERNATIVE SPLICING; ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; INTERLEUKIN-6; RECEPTORS, INTERLEUKIN-6; SIGNAL TRANSDUCTION;

EID: 84945930543     PISSN: 1521690X     EISSN: 15321908     Source Type: Journal    
DOI: 10.1016/j.beem.2015.07.001     Document Type: Review

References (98)

1. T. Kishimoto IL-6: from its discovery to clinical applications Int Immunol 22 2010 347 352
2. H. Baumann, and J. Gauldie Regulation of hepatic acute phase plasma protein genes by hepatocyte stimulating factors and other mediators of inflammation Mol Biol Med 7 1990 147 159
3. E. Bettelli, Y. Carrier, W. Gao, and et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells Nature 441 2006 235 238
4. P. Marz, U. Otten, and S. Rose-John Neural activities of IL-6-type cytokines often depend on soluble cytokine receptors Eur J Neurosci 11 1999 2995 3004
5. T. Taga IL6 signalling through IL6 receptor and receptor-associated signal transducer, gp130 Res Immunol 143 1992 737 739
6. J. Scheller, J. Grötzinger, and S. Rose-John Updating IL-6 classic- and trans-signaling Signal Transduct 6 2006 240 259
7. J. Scheller, N. Ohnesorge, and S. Rose-John Interleukin-6 trans-signaling in chronic inflammation and cancer Scand J Immunol 63 2006 321 329
8. C. Garbers, H.M. Hermanns, F. Schaper, and et al. Plasticity and cross-talk of interleukin 6-type cytokines Cytokine Growth Factor Rev 23 2012 85 97
9. D. Novick, H. Engelmann, D. Wallach, and et al. Soluble cytokine receptors are present in normal human urine J Exerimental Med 170 1989 1409 1414
10. J.A. Lust, K.A. Donovan, M.P. Kline, and et al. Isolation of an mRNA encoding a soluble form of the human interleukin-6 receptor Cytokine 4 1992 96 100
11. S. Rose-John, and P.C. Heinrich Soluble receptors for cytokines and growth factors: generation and biological function Biochem J 300 Pt 2 1994 281 290
12. S. Horiuchi, Y. Koyanagi, Y. Zhou, and et al. Soluble interleukin-6 receptors released from T cell or granulocyte/macrophage cell lines and human peripheral blood mononuclear cells are generated through an alternative splicing mechanism Eur J Immunol 24 1994 1945 1948
13. J. Mullberg, H. Schooltink, T. Stoyan, and et al. The soluble interleukin-6 receptor is generated by shedding Eur J Immunol 23 1993 473 480
14. J. Mullberg, H. Schooltink, T. Stoyan, and et al. Protein kinase C activity is rate limiting for shedding of the interleukin-6 receptor Biochem Biophys Res Commun 189 1992 794 800
15. J. Mullberg, W. Oberthur, F. Lottspeich, and et al. The soluble human IL-6 receptor. Mutational characterization of the proteolytic cleavage site J Immunol 152 1994 4958 4968
16. S. Dimitrov, T. Lange, C. Benedict, and et al. Sleep enhances IL-6 trans-signaling in humans FASEB J Official Publ Fed Am Soc Exp Biol 20 2006 2174 2176
17. S. Horiuchi, W. Ampofo, Y. Koyanagi, and et al. High-level production of alternatively spliced soluble interleukin-6 receptor in serum of patients with adult T-cell leukaemia/HTLV-1-associated myelopathy Immunology 95 1998 360 369
18. C. Garbers, N. Janner, A. Chalaris, and et al. Species specificity of ADAM10 and ADAM17 proteins in interleukin-6 (IL-6) trans-signaling and novel role of ADAM10 in inducible IL-6 receptor shedding J Biol Chem 286 2011 14804 14811
19. K.M. Mohler, P.R. Sleath, J.N. Fitzner, and et al. Protection against a lethal dose of endotoxin by an inhibitor of tumour necrosis factor processing Nature 370 1994 218 220
20. R.A. Black, C.T. Rauch, C.J. Kozlosky, and et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells Nature 385 1997 729 733
21. V. Matthews, B. Schuster, S. Schutze, and et al. Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE) J Biol Chem 278 2003 38829 38839
22. A. Chalaris, C. Garbers, B. Rabe, and et al. The soluble interleukin 6 receptor: generation and role in inflammation and cancer Eur J Cell Biol 90 2011 484 494
23. J.J. Peschon, J.L. Slack, P. Reddy, and et al. An essential role for ectodomain shedding in mammalian development Science 282 1998 1281 1284
24. J. Scheller, A. Chalaris, C. Garbers, and et al. a molecular switch to control inflammation and tissue regeneration Trends Immunol 32 2011 380 387
25. T. Taga, M. Hibi, Y. Hirata, and et al. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130 Cell 58 1989 573 581
26. M. Peters, S. Jacobs, M. Ehlers, and et al. The function of the soluble interleukin 6 (IL-6) receptor in vivo: sensitization of human soluble IL-6 receptor transgenic mice towards IL-6 and prolongation of the plasma half-life of IL-6 J Exp Med 183 1996 1399 1406
27. E. Fattori, C. Della Rocca, P. Costa, and et al. Development of progressive kidney damage and myeloma kidney in interleukin-6 transgenic mice Blood 83 1994 2570 2579
28. M. Peters, P. Schirmacher, J. Goldschmitt, and et al. Extramedullary expansion of hematopoietic progenitor cells in interleukin (IL)-6-sIL-6R double transgenic mice J Exp Med 185 1997 755 766
29. D. Maione, E. Di Carlo, W. Li, and et al. Coexpression of IL-6 and soluble IL-6R causes nodular regenerative hyperplasia and adenomas of the liver EMBO J 17 1998 5588 5597
30. P. Schirmacher, M. Peters, G. Ciliberto, and et al. Hepatocellular hyperplasia, plasmacytoma formation, and extramedullary hematopoiesis in interleukin (IL)-6/soluble IL-6 receptor double-transgenic mice Am J Pathol 153 1998 639 648
31. M. Peters, A.M. Muller, and S. Rose-John Interleukin-6 and soluble interleukin-6 receptor: direct stimulation of gp130 and hematopoiesis Blood 92 1998 3495 3504
32. M. Fischer, J. Goldschmitt, C. Peschel, and et al. I. A bioactive designer cytokine for human hematopoietic progenitor cell expansion Nat Biotechnol 15 1997 142 145
33. M. Peters, G. Blinn, T. Jostock, and et al. Combined interleukin 6 and soluble interleukin 6 receptor accelerates murine liver regeneration Gastroenterology 119 2000 1663 1671
34. E. Galun, E. Zeira, O. Pappo, and et al. Liver regeneration induced by a designer human IL-6/sIL-6R fusion protein reverses severe hepatocellular injury FASEB J Official Publ Fed Am Soc Exp Biol 14 2000 1979 1987
35. N. Hecht, O. Pappo, D. Shouval, and et al. Hyper-IL-6 gene therapy reverses fulminant hepatic failure Mol Ther J Am Soc Gene Ther 3 2001 683 687
36. P. Marz, J.G. Cheng, R.A. Gadient, and et al. Sympathetic neurons can produce and respond to interleukin 6 Proc Natl Acad Sci U S A 95 1998 3251 3256
37. P. Marz, K. Heese, B. Dimitriades-Schmutz, and et al. Role of interleukin-6 and soluble IL-6 receptor in region-specific induction of astrocytic differentiation and neurotrophin expression Glia 26 1999 191 200
38. O. Islam, X. Gong, S. Rose-John, and et al. Interleukin-6 and neural stem cells: more than gliogenesis Mol Biol Cell 20 2009 188 199
39. J. Audet, C.L. Miller, S. Rose-John, and et al. Distinct role of gp130 activation in promoting self-renewal divisions by mitogenically stimulated murine hematopoietic stem cells Proc Natl Acad Sci U S A 98 2001 1757 1762
40. C. Hacker, R.D. Kirsch, X.S. Ju, and et al. Transcriptional profiling identifies Id2 function in dendritic cell development Nat Immunol 4 2003 380 386
41. T. Hieronymus, T.C. Gust, R.D. Kirsch, and et al. Progressive and controlled development of mouse dendritic cells from Flt3+CD11b+ progenitors in vitro J Immunol 174 2005 2552 2562
42. I.L. Campbell, C.R. Abraham, E. Masliah, and et al. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6 Proc Natl Acad Sci U. S. A 90 1993 10061 10065
43. I.L. Campbell, M. Erta, S.L. Lim, and et al. Trans-signaling is a dominant mechanism for the pathogenic actions of interleukin-6 in the brain J Neurosci Official J Soc Neurosci 34 2014 2503 2513
44. F. Garcia-Oscos, D. Pena, M. Housini, and et al. Vagal nerve stimulation blocks interleukin 6-dependent synaptic hyperexcitability induced by lipopolysaccharide-induced acute stress in the rodent prefrontal cortex Brain Behav Immun 43 2015 149 158
45. A.G. Smith, J.K. Heath, D.D. Donaldson, and et al. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides Nature 336 1988 688 690
46. S. Viswanathan, T. Benatar, S. Rose-John, and et al. Ligand/receptor signaling threshold (LIST) model accounts for gp130-mediated embryonic stem cell self-renewal responses to LIF and HIL-6 Stem Cells 20 2002 119 138
47. R.K. Humphrey, G.M. Beattie, A.D. Lopez, and et al. Maintenance of pluripotency in human embryonic stem cells is STAT3 independent Stem Cells 22 2004 522 530
48. M. Diamant, K. Rieneck, N. Mechti, and et al. Cloning and expression of an alternatively spliced mRNA encoding a soluble form of the human interleukin-6 signal transducer gp130 FEBS Lett 412 1993 379 384
49. M. Tanaka, M. Kishimura, S. Ozaki, and et al. Cloning of novel soluble gp130 and detection of its neutralising autoantibodies in rheumatoid arthritis J Clin Invest 106 2000 137 144
50. P.J. Richards, M.A. Nowell, S. Horiuchi, and et al. Functional characterization of a soluble gp130 isoform and its therapeutic capacity in an experimental model of inflammatory arthritis Arthritis Rheum 54 2006 1662 1672
51. J. Sommer, C. Garbers, J. Wolf, and et al. Alternative intronic polyadenylation generates the interleukin-6 trans-signaling inhibitor sgp130-E10 J Biol Chem 289 2014 22140 22150
52. M.J. Layton, B.A. Cross, D. Metcalf, and et al. A major binding protein for leukemia inhibitory factor in normal mouse serum: identification as a soluble form of the cellular receptor Proc Natl Acad Sci U. S. A 89 1992 8616 8620
53. P. Martin, G. Palmer, S. Vigne, and et al. Mouse neutrophils express the decoy type 2 interleukin-1 receptor (IL-1R2) constitutively and in acute inflammatory conditions J Leukoc Biol 94 2013 791 802
54. J. Schwarz, S. Schmidt, O. Will, and et al. Polo-like kinase 2, a novel ADAM17 signaling component, regulates tumor necrosis factor alpha ectodomain shedding J Biol Chem 289 2014 3080 3093
55. S.A. Jones, J. Scheller, and S. Rose-John Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling J Clin Invest 121 2011 3375 3383
56. S. Davis, T.H. Aldrich, D.M. Valenzuela, and et al. The receptor for ciliary neurotrophic factor Science 253 1991 59 63
57. S. Davis, T.H. Aldrich, N.Y. Ip, and et al. Released form of CNTF receptor alpha component as a soluble mediator of CNTF responses Science 259 1993 1736 1739
58. I. Walev, P. Vollmer, M. Palmer, and et al. Pore-forming toxins trigger shedding of receptors for interleukin 6 and lipopolysaccharide Proc Natl Acad Sci U S A 93 1996 7882 7887
59. S. Pflanz, I. Tacken, J. Grotzinger, and et al. A fusion protein of interleukin-11 and soluble interleukin-11 receptor acts as a superagonist on cells expressing gp130 FEBS Lett 450 1999 117 122
60. T. Jostock, J. Mullberg, S. Ozbek, and et al. Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses Eur J Biochem/FEBS J 268 2001 160 167
61. S. Rose-John IL-6 trans-signaling via the soluble IL-6 receptor: importance for the pro-inflammatory activities of IL-6 Int J Biol Sci 8 2012 1237 1247
62. J. Scheller, A. Chalaris, D. Schmidt-Arras, and et al. The pro- and anti-inflammatory properties of the cytokine interleukin-6 Biochim Biophys Acta 1813 2011 878 888
63. J. Hoge, I. Yan, N. Janner, and et al. IL-6 controls the innate immune response against Listeria monocytogenes via classical IL-6 signaling J Immunol 190 2013 703 711
64. J. Sodenkamp, G.H. Waetzig, J. Scheller, and et al. Therapeutic targeting of interleukin-6 trans-signaling does not affect the outcome of experimental tuberculosis Immunobiology 217 2012 996 1004
65. A. Stallmach, S. Hagel, and T. Bruns Adverse effects of biologics used for treating IBD Best Pract Res Clin Gastroenterol 24 2010 167 182
66. V.R. Lang, M. Englbrecht, J. Rech, and et al. Risk of infections in rheumatoid arthritis patients treated with tocilizumab Rheumatology (Oxford) 51 2012 852 857
67. G.H. Waetzig, and S. Rose-John Hitting a complex target: an update on interleukin-6 trans-signalling Expert Opin Ther Targets 16 2012 225 236
68. R. Lissilaa, V. Buatois, G. Magistrelli, and et al. Although IL-6 trans-signaling is sufficient to drive local immune responses, classical IL-6 signaling is obligate for the induction of T cell-mediated autoimmunity J Immunol 185 2010 5512 5521
69. C. Garbers, W. Thaiss, G.W. Jones, and et al. 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 2011 42959 42970
70. G. Scambia, U. Testa, P.B. Panici, and et al. Interleukin-6 serum levels in patients with gynecological tumors Int J Cancer 57 1994 318 323
71. A. Waage, P. Brandtzaeg, A. Halstensen, and et al. The complex pattern of cytokines in serum from patients with meningococcal septic shock J Exp Med 169 1989 333 338
72. M. Honda, S. Yamamoto, M. Cheng, and et al. Human soluble IL-6 receptor: its detection and enhanced release by HIV infection J Immunol 148 1992 2175 2180
73. M. Narazaki, K. Yasukawa, T. Saito, and et al. Soluble forms of the interleukin-6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130 Blood 82 1993 1120 1126
74. F. Padberg, W. Feneberg, S. Schmidt, and et al. CSF and serum levels of soluble interleukin-6 receptors (sIL-6R and sgp130), but not of interleukin-6 are altered in multiple sclerosis J Neuroimmunol 99 1999 218 223
75. S. Rose-John, H. Schooltink, D. Lenz, and et al. Studies on the structure and regulation of the human hepatic interleukin-6 receptor Eur J Biochem/FEBS J 190 1990 79 83
76. IL6R Genetics Consortium Emerging Risk Factors Collaboration Interleukin-6 receptorpathways in coronary heart disease: a collaborative meta-analysis of 82 studies Lancet 379 2012 1205 1213
77. The Interleukin-6 Receptor Mendelian Randomisation Analysis (IL6R MR) Consortium The interleukin-6 receptor as atarget for prevention of coronary heartdisease: a mendelian randomisation analysis Lancet 379 2012 1214 1224
78. C. Garbers, N. Monhasery, S. Aparicio-Siegmund, and et al. The interleukin-6 receptor Asp358Ala single nucleotide polymorphism rs2228145 confers increased proteolytic conversion rates by ADAM proteases Biochim Biophys Acta 1842 2014 1485 1494
79. R.C. Ferreira, D.F. Freitag, A.J. Cutler, and et al. Functional IL6R 358Ala allele impairs classical IL-6 receptor signaling and influences risk of diverse inflammatory diseases PLoS Genet 9 2013 e1003444
80. J. Scheller, and S. Rose-John The interleukin 6 pathway and atherosclerosis Lancet 380 2012 338
81. L.H. Calabrese, and S. Rose-John IL-6 biology: implications for clinical targeting in rheumatic disease Nat Rev Rheumatol 10 2014 720 727
82. R. Atreya, J. Mudter, S. Finotto, and et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo Nat Med 6 2000 583 588
83. K. Mitsuyama, S. Matsumoto, S. Rose-John, and et al. STAT3 activation via interleukin 6 trans-signalling contributes to ileitis in SAMP1/Yit mice Gut 55 2006 1263 1269
84. M.A. Nowell, P.J. Richards, S. Horiuchi, and et al. Soluble IL-6 receptor governs IL-6 activity in experimental arthritis: blockade of arthritis severity by soluble glycoprotein 130 J Immunol 171 2003 3202 3209
85. M.A. Nowell, A.S. Williams, S.A. Carty, and et al. Therapeutic targeting of IL-6 trans signaling counteracts STAT3 control of experimental inflammatory arthritis J Immunol 182 2009 613 622
86. A. Chalaris, B. Rabe, K. Paliga, and et al. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils Blood 110 2007 1748 1755
87. B. Rabe, A. Chalaris, U. May, and et al. Transgenic blockade of interleukin 6 transsignaling abrogates inflammation Blood 111 2008 1021 1028
88. T. Barkhausen, T. Tschernig, P. Rosenstiel, and et al. Selective blockade of interleukin-6 trans-signaling improves survival in a murine polymicrobial sepsis model Crit Care Med 39 2011 1407 1413
89. C.J. Greenhill, S. Rose-John, R. Lissilaa, and et al. IL-6 trans-signaling modulates TLR4-dependent inflammatory responses via STAT3 J Immunol 186 2011 1199 1208
90. H. Schuett, R. Oestreich, G.H. Waetzig, and et al. Transsignaling of interleukin-6 crucially contributes to atherosclerosis in mice Arterioscler Thromb Vasc Biol 32 2012 281 290
91. A. Doganci, T. Eigenbrod, N. Krug, and et al. The IL-6R alpha chain controls lung CD4+CD25+ Treg development and function during allergic airway inflammation in vivo J Clin Invest 115 2005 313 325
92. S. Finotto, T. Eigenbrod, R. Karwot, and et al. Local blockade of IL-6R signaling induces lung CD4+ T cell apoptosis in a murine model of asthma via regulatory T cells Int Immunol 19 2007 685 693
93. M. Luig, M.A. Kluger, B. Goerke, and et al. Inflammation-induced IL-6 functions as a natural brake on macrophages and limits GN J Am Soc Nephrol 26 2015 Jul 1597 1607
94. E. Tsantikos, M.J. Maxwell, T. Putoczki, and et al. Interleukin-6 trans-signaling exacerbates inflammation and renal pathology in lupus-prone mice Arthritis Rheum 65 2013 2691 2702
95. C. Becker, M.C. Fantini, C. Schramm, and et al. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling Immunity 21 2004 491 501
96. S. Matsumoto, T. Hara, K. Mitsuyama, and et al. Essential roles of IL-6 trans-signaling in colonic epithelial cells, induced by the IL-6/soluble-IL-6 receptor derived from lamina propria macrophages, on the development of colitis-associated premalignant cancer in a murine model J Immunol 184 2010 1543 1551
97. C.W. Lo, M.W. Chen, M. Hsiao, and et al. IL-6 trans-signaling in formation and progression of malignant ascites in ovarian cancer Cancer Res 71 2011 424 434
98. M. Lesina, M.U. Kurkowski, K. Ludes, and et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer Cancer Cell 19 2011 456 469