Intracellular signaling prevents effective blockade of oncogenic gp130 mutants by neutralizing antibodies

Cell Communication and Signaling

Volumn 12, Issue 1, 2014, Pages

  Rinis, Natalie ^a   Küster, Andrea ^a   Schmitz Van De Leur, Hildegard ^a   Mohr, Anne ^a   Müller Newen, Gerhard ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Constitutively active gp130; Endocytosis; IHCAs; Intracellular signaling; Neutralizing antibodies; Stat3

Indexed keywords

GLYCOPROTEIN GP 130; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MUTANT PROTEIN; NEUTRALIZING ANTIBODY; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; YELLOW FLUORESCENT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; CD135 ANTIGEN; DYNAMIN; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR ALPHA; PROTEIN TYROSINE PHOSPHATASE SHP 2; STAT1 PROTEIN;

ARTICLE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GENE OVEREXPRESSION; GLYCOSYLATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; INFLAMMATORY HEPATOCELLULAR ADENOMA; INTRACELLULAR SIGNALING; LIVER ADENOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSCRIPTION INITIATION; WILD TYPE; CELL MEMBRANE; ENDOCYTOSIS; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; CONFOCAL MICROSCOPY; CONSENSUS SEQUENCE; FEEDBACK SYSTEM; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; HEPATOCELLULAR CARCINOMA CELL LINE; IMMUNOPRECIPITATION; INTERNAL RIBOSOME ENTRY SITE; LIVER CELL CARCINOMA; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; WESTERN BLOTTING;

ANTIBODIES, NEUTRALIZING; CELL MEMBRANE; CYTOKINE RECEPTOR GP130; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GOLGI APPARATUS; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84899407021     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-12-14     Document Type: Article

References (33)

1. Hexameric structure and assembly of the interleukin-6/IL-6a-receptor/ gp130 complex. Boulanger MJ, Chow D, Brevnova EE, Garcia KC, Science 2003 300 2101 2104 10.1126/science.1083901 12829785
2. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, Schaper F, Biochem J 2003 374 1 20 10.1042/BJ20030407 12773095
3. Genetics and imaging of hepatocellular adenomas: 2011 update. Katabathina VS, Menias CO, Shanbhogue AK, Jagirdar J, Paspulati RM, Prasad SR, Radiographics 2011 31 1529 1543 10.1148/rg.316115527 21997980
4. Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumours. Rebouissou S, Amessou M, Couchy G, Poussin K, Imbeaud S, Pilati C, Izard T, Balabaud C, Bioulac-Sage P, Zucman-Rossi J, Nature 2009 457 200 204 10.1038/nature07475 19020503
5. Somatic mutations activating STAT3 in human inflammatory hepatocellular adenomas. Pilati C, Amessou M, Bihl MP, Balabaud C, Nhieu JT, Paradis V, Nault JC, Izard T, Bioulac-Sage P, Couchy G, Poussin K, Zucman-Rossi J, J Exp Med 2011 208 1359 1366 10.1084/jem.20110283 21690253
6. Endocytosis and signalling: intertwining molecular networks. Sorkin A, von Zastrow M, Nat Rev Mol Cell Biol 2009 10 609 622 10.1038/nrm2748 19696798
7. Ligand-independent thrombopoietin mutant receptor requires cell surface localization for endogenous activity. Marty C, Chaligne R, Lacout C, Constantinescu SN, Vainchenker W, Villeval JL, J Biol Chem 2009 284 11781 11791 10.1074/jbc.M808703200 19261614
8. Anchoring of FLT3 in the endoplasmic reticulum alters signaling quality. Schmidt-Arras D, Böhmer SA, Koch S, Müller JP, Blei L, Cornils H, Bauer R, Korasikha S, Thiede C, Böhmer FD, Blood 2009 113 3568 3576 10.1182/blood-2007-10-121426 19204327
9. Model-driven experimental analysis of the function of SHP-2 in IL-6-induced Jak/STAT signaling. Dittrich A, Quaiser T, Khouri C, Görtz D, Mönnigmann M, Schaper F, Mol Biosyst 2012 8 2119 2134 10.1039/c2mb05488d 22711165
10. Biosynthesis and half-life of the interleukin-6 receptor and its signal transducer gp130. Gerhartz C, Dittrich E, Stoyan T, Rose-John S, Yasukawa K, Heinrich PC, Graeve L, Eur J Biochem 1994 223 265 274 10.1111/j.1432-1033.1994. tb18991.x 8033901
11. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Stahl N, Farrugella TJ, Boulton TG, Zhong Z, Darnell JE Jr, Yancopoulos GD, Science 1995 267 1349 1353 10.1126/science. 7871433 7871433
12. Differential activation of acute phase response factor/STAT3 and STAT1 via the cytoplasmic domain of the interleukin-6 signal transducer gp130. 1. Definition of a novel phosphotyrosine motif mediating STAT1 activation. Gerhartz C, Heesel B, Sasse J, Hemmann U, Landgraf C, Schneider-Mergener J, Horn F, Heinrich PC, Graeve L, J Biol Chem 1996 271 12991 12998 10.1074/jbc.271.22.12991 8662591
13. The cytoplasmic tyrosine motifs in full-length gp130 have different roles in IL-6 signal transduction. Schmitz J, Dahmen H, Grimm C, Gendo C, Müller-Newen G, Heinrich PC, Schaper F, J Immunol 2000 164 848 854 10623831
14. Biochemical and functional analyses of gp130 mutants unveil JAK1 as a novel therapeutic target in human inflammatory hepatocellular adenoma. Poussin K, Pilati C, Couchy G, Calderaro J, Bioulac-Sage P, Bacq Y, Paradis V, Leteurtre E, Sturm N, Ramos J, Guettier C, Bardier-Dupas A, Boulai A, Wendum D, Selves J, Izard T, Nault JC, Zucman-Rossi J, Oncoimmunology 2013 2 27090 10.4161/onci.27090 24501689
15. Constitutive internalization and association with adaptor protein-2 of the interleukin-6 signal transducer gp130. Thiel S, Dahmen H, Martens A, Müller-Newen G, Schaper F, Heinrich PC, Graeve L, FEBS lett 1998 441 231 234 10.1016/S0014-5793(98)01559-2 9883890
16. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. Damke H, Baba T, Warnock DE, Schmid SL, J Cell Biol 1994 127 915 934 10.1083/jcb.127.4.915 7962076
17. Interleukin-6 signal transducer gp130 has specific binding sites for different cytokines as determined by antagonistic and agonistic anti-gp130 monoclonal antibodies. Wijdenes J, Heinrich PC, Müller-Newen G, Roche C, Zong-Jiang G, Clement C, Klein B, Eur J Immunol 1995 25 3474 3481 10.1002/eji.1830251240 8566040
18. Constitutively active mutant gp130 receptor protein from inflammatory hepatocellular adenoma is inhibited by an anti-gp130 antibody that specifically neutralizes interleukin 11 signaling. Sommer J, Effenberger T, Volpi E, Waetzig GH, Bernhardt M, Suthaus J, Garbers C, Rose-John S, Floss DM, Scheller J, J Biol Chem 2012 287 13743 13751 10.1074/jbc.M111.349167 22523320
19. Dominant-negative activity of the STAT3-Y705F mutant depends on the N-terminal domain. Mohr A, Fahrenkamp D, Rinis N, Müller-Newen G, Cell Commun Signal 2013 11 83 10.1186/1478-811X-11-83 24192293
20. Tyrosine phosphorylation regulates maturation of receptor tyrosine kinases. Schmidt-Arras DE, Böhmer A, Markova B, Choudhary C, Serve H, Böhmer FD, Mol Cell Biol 2005 25 3690 3703 10.1128/MCB.25.9.3690-3703.2005 15831474
21. Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. Reith AD, Ellis C, Lyman SD, Anderson DM, Williams DE, Bernstein A, Pawson T, EMBO J 1991 10 2451 2459 1714377
22. Quality control in the endoplasmic reticulum. Ellgaard L, Helenius A, Nat Rev Mol Cell Biol 2003 4 181 191 10.1038/nrm1052 12612637
23. Oncogenic deletion mutants of gp130 signal from intracellular compartments. Schmidt-Arras D, Muller M, Stevanovic M, Horn S, Schutt A, Bergmann J, Wilkens R, Lickert A, Rose-John S, J Cell Sci 2014 127 341 353 10.1242/jcs.130294 24213527
24. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Hetz C, Nat Rev Mol Cell Biol 2012 13 89 102 22251901
25. A new mechanism for the regulation of Gab1 recruitment to the plasma membrane. Eulenfeld R, Schaper F, J Cell Sci 2009 122 55 64 10.1242/jcs.037226 19050043
26. Janus kinases affect thrombopoietin receptor cell surface localization and stability. Royer Y, Staerk J, Costuleanu M, Courtoy PJ, Constantinescu SN, J Biol Chem 2005 280 27251 27261 10.1074/jbc.M501376200 15899890
27. The N-terminal domain of Janus kinase 2 is required for Golgi processing and cell surface expression of erythropoietin receptor. Huang LJ, Constantinescu SN, Lodish HF, Mol Cell 2001 8 1327 1338 10.1016/S1097-2765(01)00401-4 11779507
28. Novel role of Janus kinase 1 in the regulation of oncostatin M receptor surface expression. Radtke S, Hermanns HM, Haan C, Schmitz-Van De Leur H, Gascan H, Heinrich PC, Behrmann I, J Biol Chem 2002 277 11297 11305 10.1074/jbc.M100822200 11786531
29. Forced dimerization of gp130 leads to constitutive STAT3 activation, cytokine-independent growth, and blockade of differentiation of embryonic stem cells. Stuhlmann-Laeisz C, Lang S, Chalaris A, Krzysztof P, Enge S, Eichler J, Klingmuller U, Samuel M, Ernst M, Rose-John S, Scheller J, Mol Biol Cell 2006 17 2986 2995 10.1091/mbc.E05-12-1129 16624864
30. EGF receptor trafficking: consequences for signaling and cancer. Tomas A, Futter CE, Eden ER, Trends Cell Biol 2014 24 26 34 10.1016/j.tcb.2013.11.002 24295852
31. Single-step purification and structural characterization of human interleukin-6 produced in Escherichia coli from a T7 RNA polymerase expression vector. Arcone R, Pucci P, Zappacosta F, Fontaine V, Malorni A, Marino G, Ciliberto G, Eur J Biochem 1991 198 541 547 10.1111/j.1432-1033.1991.tb16048.x 2050135
32. Soluble human interleukin-6 receptor: expression in insect cells, purification and characterization. Weiergräber O, Hemmann U, Küster A, Müller-Newen G, Schneider J, Rose-John S, Kurschat P, Brakenhoff JP, Hart MH, Stabel S, Heinrich PC, Eur J Biochem 1995 234 661 669 10.1111/j.1432-1033. 1995.661-b.x 8536717
33. Long-term association of the cytokine receptor gp130 and the Janus kinase Jak1 revealed by FRAP analysis. Giese B, Au-Yeung C-K, Herrmann A, Diefenbach S, Haan C, Küster A, Wortmann SB, Roderburg C, Heinrich PC, Behrmann I, Müller-Newen G, J Biol Chem 2003 278 39205 39213 10.1074/jbc.M303347200 12878601