Dynamics and non-canonical aspects of JAK/STAT signalling

European Journal of Cell Biology

Volumn 91, Issue 6-7, 2012, Pages 524-532

  Mohr, Anne ^a   Chatain, Nicolas ^a   Domoszlai, Tamás ^a   Rinis, Natalie ^a   Sommerauer, Michael ^a   Vogt, Michael ^a   Müller Newen, Gerhard ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Cytokines; JAK; Receptors; Signal transduction; STAT

Indexed keywords

CYTOKINE RECEPTOR; DIMER; GLYCOPROTEIN GP 130; JANUS KINASE; STAT PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR;

COMPLEX FORMATION; CYTOPLASM; GENE EXPRESSION; GENE TARGETING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SHORT SURVEY; SIGNAL TRANSDUCTION;

HUMANS; JANUS KINASES; RECEPTORS, CYTOKINE; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84860238507     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.09.005     Document Type: Short Survey

References (100)

1. Alexander W.S., Hilton D.J. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu. Rev. Immunol. 2004, 22:503-529.
2. Antunes F., Marg A., Vinkemeier U. STAT1 signaling is not regulated by a phosphorylation-acetylation switch. Mol. Cell. Biol. 2011, 31:3029-3037.
3. Autissier P., De Vos J., Liautard J., Tupitsyn N., Jacquet C., Chavdia N., Klein B., Brochier J., Gaillard J.P. Dimerization and activation of the common transducing chain (gp130) of the cytokines of the IL-6 family by mAb. Int. Immunol. 1998, 10:1881-1889.
4. Ballinger M.D., Wells J.A. Will any dimer do?. Nat. Struct. Biol. 1998, 5:938-940.
5. Bazan J.F. Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:6934-6938.
6. Becker S., Groner B., Müller C.W. Three-dimensional structure of the Stat3beta homodimer bound to DNA. Nature. 1998, 394:145-151.
7. Bhattacharya S., Schindler C. Regulation of Stat3 nuclear export. J. Clin. Invest. 2003, 111:553-559.
8. Bild A.H., Turkson J., Jove R. Cytoplasmic transport of Stat3 by receptor-mediated endocytosis. EMBO J. 2002, 21:3255-3263.
9. Boulanger M.J., Bankovich A.J., Kortemme T., Baker D., Garcia K.C. Convergent mechanisms for recognition of divergent cytokines by the shared signaling receptor gp130. Mol. Cell 2003, 12:577-589.
10. Boulanger M.J., Chow D., Brevnova E.E., Garcia K.C. Hexameric structure and assembly of the interleukin-6/IL-6α-receptor/gp130 complex. Science 2003, 300:2101-2104.
11. Braunstein J., Brutsaert S., Olson R., Schindler C. STATs dimerize in the absence of phosphorylation. J. Biol. Chem. 2003, 278:34133-34140.
12. Chatterjee-Kishore M., van den Akker F., Stark G.R. Association of STATs with relatives and friends. Trends Cell Biol. 2000, 10:106-111.
13. Chen H.C., Reich N.C. Live cell imaging reveals continuous STAT6 nuclear trafficking. J. Immunol. 2010, 185:64-70.
14. Constantinescu S.N., Huang L.J., Nam H., Lodish H.F. The erythropoietin receptor cytosolic juxtamembrane domain contains an essential, precisely oriented, hydrophobic motif. Mol. Cell 2001, 7:377-385.
15. Cunningham B.C., Ultsch M., De Vos A.M., Mulkerrin M.G., Clauser K.R., Wells J.A. Dimerization of the extracellular domain of the human growth hormone receptor by a single hormone molecule. Science 1991, 254:821-825.
16. Darnell J.E. Validating Stat3 in cancer therapy. Nat. Med. 2005, 11:595-596.
17. Darnell J.E. STAT3, HIF-1, glucose addiction and Warburg effect. Aging (Albany NY) 2010, 2:890-891.
18. Dawson M.A., Bannister A.J., Gottgens B., Foster S.D., Bartke T., Green A.R., Kouzarides T. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 2009, 461:819-822.
19. Demaria M., Giorgi C., Lebiedzinska M., Esposito G., D'Angeli L., Bartoli A., Gough D.J., Turkson J., Levy D.E., Watson C.J., Wieckowski M.R., Provero P., Pinton P., Poli V. A STAT3-mediated metabolic switch is involved in tumour transformation and STAT3 addiction. Aging (Albany, NY) 2010, 2:823-842.
20. Droescher M., Begitt A., Marg A., Zacharias M., Vinkemeier U. Cytokine-induced paracrystals prolong the activity of signal transducers and activators of transcription (STAT) and provide a model for the regulation of protein solubility by small ubiquitin-like modifier (SUMO). J. Biol. Chem. 2011, 286:18731-18746.
21. Frahm T., Hauser H., Köster M. IFN-type-I-mediated signaling is regulated by modulation of STAT2 nuclear export. J. Cell Sci. 2006, 119:1092-1104.
22. Gao S.P., Bromberg J.F. Touched and moved by STAT3. Sci. STKE 2006, e30.
23. Giese B., Roderburg C., Sommerauer M., Wortmann S.B., Metz S., Heinrich P.C., Müller-Newen G. Dimerization of the cytokine receptors gp130 and LIFR analysed in single cells. J. Cell Sci. 2005, 118:5129-5140.
24. Gough D.J., Corlett A., Schlessinger K., Wegrzyn J., Larner A.C., Levy D.E. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 2009, 324:1713-1716.
25. Greiser J.S., Stross C., Heinrich P.C., Behrmann I., Hermanns H.M. Orientational constraints of the gp130 intracellular juxtamembrane domain for signaling. J. Biol. Chem. 2002, 277:26959-26965.
26. Haan S., Kortylewski M., Behrmann I., Müller-Esterl W., Heinrich P.C., Schaper F. Cytoplasmic STAT proteins associate prior to activation. Biochem. J. 2000, 345:417-421.
27. Harir N., Pecquet C., Kerenyi M., Sonneck K., Kovacic B., Nyga R., Brevet M., Dhennin I., Gouilleux-Gruart V., Beug H., Valent P., Lassoued K., Moriggl R., Gouilleux F. Constitutive activation of Stat5 promotes its cytoplasmic localization and association with PI3-kinase in myeloid leukemias. Blood 2007, 109:1678-1686.
28. Hayes S., Chawla A., Corvera S. TGF beta receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J. Cell Biol. 2002, 158:1239-1249.
29. Hennighausen L., Robinson G.W. Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes Dev. 2008, 22:711-721.
30. Herrmann A., Sommer U., Pranada A.L., Giese B., Küster A., Haan S., Becker W., Heinrich P.C., Müller-Newen G. STAT3 is enriched in nuclear bodies. J. Cell Sci. 2004, 117:339-349.
31. Herrmann A., Vogt M., Mönnigmann M., Clahsen T., Sommer U., Haan S., Poli V., Heinrich P.C., Müller-Newen G. Nucleocytoplasmic shuttling of persistently activated STAT3. J. Cell Sci. 2007, 120:3249-3261.
32. Howe C.L., Mobley W.C. Signaling endosome hypothesis: a cellular mechanism for long distance communication. J. Neurobiol. 2004, 58:207-216.
33. Iyer J., Reich N.C. Constitutive nuclear import of latent and activated STAT5a by its coiled coil domain. FASEB J. 2008, 22:391-400.
34. Kawashima T., Bao Y.C., Minoshima Y., Nomura Y., Hatori T., Hori T., Fukagawa T., Fukada T., Takahashi N., Nosaka T., Inoue M., Sato T., Kukimoto-Niino M., Shirouzu M., Yokoyama S., Kitamura T. A Rac GTPase-activating protein, MgcRacGAP, is a nuclear localizing signal-containing nuclear chaperone in the activation of STAT transcription factors. Mol. Cell. Biol. 2009, 29:1796-1813.
35. Kermorgant S., Parker P.J. Receptor trafficking controls weak signal delivery: a strategy used by c-Met for STAT3 nuclear accumulation. J. Cell Biol. 2008, 182:855-863.
36. Krämer O.H., Knauer S.K., Greiner G., Jandt E., Reichardt S., Gührs K.H., Stauber R.H., Böhmer F.D., Heinzel T. A phosphorylation-acetylation switch regulates STAT1 signaling. Genes Dev. 2009, 23:223-235.
37. Kretzschmar A.K., Dinger M.C., Henze C., Brocke-Heidrich K., Horn F. Analysis of Stat3 dimerization by fluorescence resonance energy transfer in living cells. Biochem. J. 2004, 377:289-297.
38. Kurth I., Horsten U., Pflanz S., Dahmen H., Küster A., Grötzinger J., Heinrich P.C., Müller-Newen G. Activation of the signal transducer glycoprotein 130 by both IL-6 and IL-11 requires two distinct binding epitopes. J. Immunol. 1999, 162:1480-1487.
39. Kurth I., Horsten U., Pflanz S., Timmermann A., Küster A., Dahmen H., Tacken I., Heinrich P.C., Müller-Newen G. Importance of the membrane-proximal extracellular domains for activation of the signal transducer glycoprotein 130. J. Immunol. 2000, 164:273-282.
40. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
41. Leonard W.J., O'Shea J.J. Jaks and STATs: biological implications. Annu. Rev. Immunol. 1998, 16:293-322.
42. Levy D.E., Darnell J.E. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell. Biol. 2002, 3:651-662.
43. Levy D.E., Lee C.K. What does Stat3 do?. J. Clin. Invest. 2002, 109:1143-1148.
44. Li W.X. Canonical and non-canonical JAK-STAT signaling. Trends Cell Biol. 2008, 18:545-551.
45. Lillemeier B.F., Köster M., Kerr I.M. STAT1 from the cell membrane to the DNA. EMBO J. 2001, 20:2508-2517.
46. Lim C.P., Cao X. Structure, function, and regulation of STAT proteins. Mol. Biosyst. 2006, 2:536-550.
47. Liu L., McBride K.M., Reich N.C. STAT3 nuclear import is independent of tyrosine phosphorylation and mediated by importin-alpha3. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8150-8155.
48. Livnah O., Stura E.A., Middleton S.A., Johnson D.L., Jolliffe L.K., Wilson I.A. Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation. Science 1999, 283:987-990.
49. Lupardus P.J., Skiniotis G., Rice A.J., Thomas C., Fischer S., Walz T., Garcia K.C. Structural snapshots of full-length Jak1, a transmembrane gp130/IL-6/IL-6Ralpha cytokine receptor complex, and the receptor-Jak1 holocomplex. Structure 2011, 19:45-55.
50. Ma J., Cao X. Regulation of Stat3 nuclear import by importin alpha5 and importin alpha7 via two different functional sequence elements. Cell Signal. 2006, 18:1117-1126.
51. Marchetti M., Monier M.N., Fradagrada A., Mitchell K., Baychelier F., Eid P., Johannes L., Lamaze C. Stat-mediated signaling induced by type I and type II interferons (IFNs) is differentially controlled through lipid microdomain association and clathrin-dependent endocytosis of IFN receptors. Mol. Biol. Cell 2006, 17:2896-2909.
52. Marg A., Shan Y., Meyer T., Meissner T., Brandenburg M., Vinkemeier U. Nucleocytoplasmic shuttling by nucleoporins Nup153 and Nup214 and CRM1-dependent nuclear export control the subcellular distribution of latent Stat1. J. Cell Biol. 2004, 165:823-833.
53. Mertens C., Zhong M., Krishnaraj R., Zou W., Chen X., Darnell J.E. Dephosphorylation of phosphotyrosine on STAT1 dimers requires extensive spatial reorientation of the monomers facilitated by the N-terminal domain. Genes Dev. 2006, 20:3372-3381.
54. Metz S., Wiesinger M., Vogt M., Lauks H., Schmalzing G., Heinrich P.C., Müller-Newen G. Characterization of the interleukin (IL)-6 inhibitor IL-6-RFP: fused receptor domains act as high affinity cytokine-binding proteins. J. Biol. Chem. 2007, 282:1238-1248.
55. Meyer T., Marg A., Lemke P., Wiesner B., Vinkemeier U. DNA binding controls inactivation and nuclear accumulation of the transcription factor Stat1. Genes Dev. 2003, 17:1992-2005.
56. Müller-Newen G. The cytokine receptor gp130: faithfully promiscuous. Sci. STKE 2003, e40.
57. Müller-Newen G., Kuster A., Wijdenes J., Schaper F., Heinrich P.C. Studies on the interleukin-6-type cytokine signal transducer gp130 reveal a novel mechanism of receptor activation by monoclonal antibodies. J. Biol. Chem. 2000, 275:4579-4586.
58. Nardozzi J., Wenta N., Yasuhara N., Vinkemeier U., Cingolani G. Molecular basis for the recognition of phosphorylated STAT1 by importin alpha5. J. Mol. Biol. 2010, 402:83-100.
59. Neculai D., Neculai A.M., Verrier S., Straub K., Klumpp K., Pfitzner E., Becker S. Structure of the unphosphorylated STAT5a dimer. J. Biol. Chem. 2005, 280:40782-40787.
60. Ng D.C., Lin B.H., Lim C.P., Huang G., Zhang T., Poli V., Cao X. Stat3 regulates microtubules by antagonizing the depolymerization activity of stathmin. J. Cell Biol. 2006, 172:245-257.
61. Novak U., Ji H., Kanagasundaram V., Simpson R., Paradiso L. STAT3 forms stable homodimers in the presence of divalent cations prior to activation. Biochem. Biophys. Res. Commun. 1998, 247:558-563.
62. O'Shea J.J., Kanno Y., Chen X., Levy D.E. Cell signaling. Stat acetylation - a key facet of cytokine signaling?. Science 2005, 307:217-218.
63. O'Sullivan L.A., Liongue C., Lewis R.S., Stephenson S.E., Ward A.C. Cytokine receptor signaling through the Jak-Stat-Socs pathway in disease. Mol. Immunol. 2007, 44:2497-2506.
64. Ota N., Brett T.J., Murphy T.L., Fremont D.H., Murphy K.M. N-domain-dependent nonphosphorylated STAT4 dimers required for cytokine-driven activation. Nat. Immunol. 2004, 5:208-215.
65. Pestka S., Krause C.D., Sarkar D., Walter M.R., Shi Y., Fisher P.B. Interleukin-10 and related cytokines and receptors. Annu. Rev. Immunol. 2004, 22:929-979.
66. Phillips D., Reilley M.J., Aponte A.M., Wang G., Boja E., Gucek M., Balaban R.S. Stoichiometry of STAT3 and mitochondrial proteins: implications for the regulation of oxidative phosphorylation by protein-protein interactions. J. Biol. Chem. 2010, 285:23532-23536.
67. Poincloux R., Cougoule C., Daubon T., Maridonneau-Parini I., Le Cabec V. Tyrosine-phosphorylated STAT5 accumulates on podosomes in Hck-transformed fibroblasts and chronic myeloid leukemia cells. J. Cell Physiol. 2007, 213:212-220.
68. Pranada A.L., Metz S., Herrmann A., Heinrich P.C., Müller-Newen G. Real time analysis of STAT3 nucleocytoplasmic shuttling. J. Biol. Chem. 2004, 279:15114-15123.
69. Rebouissou S., Amessou M., Couchy G., Poussin K., Imbeaud S., Pilati C., Izard T., Balabaud C., Bioulac-Sage P., Zucman-Rossi J. Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumours. Nature 2009, 457:200-204.
70. Recker T., Haamann D., Schmitt A., Küster A., Klee D., Barth S., Müller-Newen G. Directed covalent immobilization of fluorescently labeled cytokines. Bioconjug. Chem. 2011, 22:1210-1220.
71. Ren Z., Mao X., Mertens C., Krishnaraj R., Qin J., Mandal P.K., Romanowski M.J., McMurray J.S., Chen X. Crystal structure of unphosphorylated STAT3 core fragment. Biochem. Biophys. Res. Commun. 2008, 374:1-5.
72. Schröder M., Kroeger K.M., Volk H.D., Eidne K.A., Grütz G. Preassociation of nonactivated STAT3 molecules demonstrated in living cells using bioluminescence resonance energy transfer: a new model of STAT activation?. J. Leukoc. Biol. 2004, 75:792-797.
73. Schütze S., Tchikov V., Schneider-Brachert W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat. Rev. Mol. Cell. Biol. 2008, 9:655-662.
74. Seubert N., Royer Y., Staerk J., Kubatzky K.F., Moucadel V., Krishnakumar S., Smith S.O., Constantinescu S.N. Active and inactive orientations of the transmembrane and cytosolic domains of the erythropoietin receptor dimer. Mol. Cell 2003, 12:1239-1250.
75. Shi S., Calhoun H.C., Xia F., Li J., Le L., Li W.X. JAK signaling globally counteracts heterochromatic gene silencing. Nat. Genet. 2006, 38:1071-1076.
76. Shi S., Larson K., Guo D., Lim S.J., Dutta P., Yan S.J., Li W.X. Drosophila STAT is required for directly maintaining HP1 localization and heterochromatin stability. Nat. Cell Biol. 2008, 10:489-496.
77. Skiniotis G., Lupardus P.J., Martick M., Walz T., Garcia K.C. Structural organization of a full-length gp130/LIF-R cytokine receptor transmembrane complex. Mol. Cell 2008, 31:737-748.
78. Stancato L.F., David M., Carter-Su C., Larner A.C., Pratt W.B. Preassociation of STAT1 with STAT2 and STAT3 in separate signalling complexes prior to cytokine stimulation. J. Biol. Chem. 1996, 271:4134-4137.
79. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Kontgen F., Abbondanzo S.J. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992, 359:76-79.
80. Syed R.S., Reid S.W., Li C., Cheetham J.C., Aoki K.H., Liu B., Zhan H., Osslund T.D., Chirino A.J., Zhang J., Finer-Moore J., Elliott S., Sitney K., Katz B.A., Matthews D.J., Wendoloski J.J., Egrie J., Stroud R.M. Efficiency of signalling through cytokine receptors depends critically on receptor orientation. Nature 1998, 395:511-516.
81. Takeda K., Noguchi K., Shi W., Tanaka T., Matsumoto M., Yoshida N., Kishimoto T., Akira S. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:3801-3804.
82. Tenhumberg S., Schuster B., Zhu L., Kovaleva M., Scheller J., Kallen K.J., Rose-John S. gp130 dimerization in the absence of ligand: preformed cytokine receptor complexes. Biochem. Biophys. Res. Commun. 2006, 346:649-657.
83. Verma N.K., Dourlat J., Davies A.M., Long A., Liu W.Q., Garbay C., Kelleher D., Volkov Y. STAT3-stathmin interactions control microtubule dynamics in migrating T-cells. J. Biol. Chem. 2009, 284:12349-12362.
84. Vinkemeier U., Moarefi I., Darnell J.E., Kuriyan J. Structure of the amino-terminal protein interaction domain of STAT-4. Science 1998, 279:1048-1052.
85. Vogt M., Domoszlai T., Kleshchanok D., Lehmann S., Schmitt A., Poli V., Richtering W., Müller-Newen G. The role of the N-terminal domain in dimerization and nucleocytoplasmic shuttling of latent STAT3. J. Cell Sci. 2011, 124:900-909.
86. Wang R., Cherukuri P., Luo J. Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREB-binding protein-mediated acetylation. J. Biol. Chem. 2005, 280:11528-11534.
87. Wang X., Lupardus P., Laporte S.L., Garcia K.C. Structural biology of shared cytokine receptors. Annu. Rev. Immunol. 2009, 27:29-60.
88. Ward L.D., Howlett G.J., Discolo G., Yasukawa K., Hammacher A., Moritz R.L., Simpson R.J. High affinity interleukin-6 receptor is a hexameric complex consisting of two molecules each of interleukin-6, interleukin-6 receptor, and gp-130. J. Biol. Chem. 1994, 269:23286-23289.
89. Watanabe K., Saito K., Kinjo M., Matsuda T., Tamura M., Kon S., Miyazaki T., Uede T. Molecular dynamics of STAT3 on IL-6 signaling pathway in living cells. Biochem. Biophys. Res. Commun. 2004, 324:1264-1273.
90. Wegrzyn J., Potla R., Chwae Y.J., Sepuri N.B., Zhang Q., Koeck T., Derecka M., Szczepanek K., Szelag M., Gornicka A., Moh A., Moghaddas S., Chen Q., Bobbili S., Cichy J., Dulak J., Baker D.P., Wolfman A., Stuehr D., Hassan M.O., Fu X.Y., Avadhani N., Drake J.I., Fawcett P., Lesnefsky E.J., Larner A.C. Function of mitochondrial Stat3 in cellular respiration. Science 2009, 323:793-797.
91. Wells J.A., de Vos A.M. Hematopoietic receptor complexes. Annu. Rev. Biochem. 1996, 65:609-634.
92. Wenta N., Strauss H., Meyer S., Vinkemeier U. Tyrosine phosphorylation regulates the partitioning of STAT1 between different dimer conformations. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9238-9243.
93. Wu C., Cui B., He L., Chen L., Mobley W.C. The coming of age of axonal neurotrophin signaling endosomes. J. Proteomics 2009, 72:46-55.
94. Xu F., Mukhopadhyay S., Sehgal P.B. Live cell imaging of interleukin-6-induced targeting of transcription factor STAT3 to sequestering endosomes in the cytoplasm. Am. J. Physiol. Cell Physiol. 2007, 293:C1374-C1382.
95. Yu H., Jove R. The STATs of cancer - new molecular targets come of age. Nat. Rev. Cancer 2004, 4:97-105.
96. Yuan Z.L., Guan Y.J., Chatterjee D., Chin Y.E. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 2005, 307:269-273.
97. Zeng R., Aoki Y., Yoshida M., Arai K., Watanabe S. Stat5B shuttles between cytoplasm and nucleus in a cytokine-dependent and -independent manner. J. Immunol. 2002, 168:4567-4575.
98. Zhang J.G., Owczarek C.M., Ward L.D., Howlett G.J., Fabri L.J., Roberts B.A., Nicola N.A. Evidence for the formation of a heterotrimeric complex of leukaemia inhibitory factor with its receptor subunits in solution. Biochem. J. 1997, 325(Pt 3):693-700.
99. Zhang L., Badgwell D.B., Bevers J.J., Schlessinger K., Murray P.J., Levy D.E., Watowich S.S. IL-6 signaling via the STAT3/SOCS3 pathway: functional analysis of the conserved STAT3 N-domain. Mol. Cell. Biochem. 2006, 288:179-189.
100. Zhang T., Seow K.T., Ong C.T., Cao X. Interdomain interaction of Stat3 regulates its Src homology 2 domain-mediated receptor binding activity. J. Biol. Chem. 2002, 277:17556-17563.