Drosophila SOCS36E negatively regulates JAK/STAT pathway signaling via two separable mechanisms

Molecular Biology of the Cell

Volumn 24, Issue 18, 2013, Pages 3000-3009

  Stec, Wojciech ^a   Vidal, Oscar ^a,b   Zeidler, Martin P ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CULLIN 5; ELONGIN B; ELONGIN C; JANUS KINASE; PROTEIN; PROTEIN DOME; PROTEIN SOCS36E; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; JANUS KINASES; LYSOSOMES; MUTANT PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STABILITY; PROTEOLYSIS; RECEPTORS, INTERLEUKIN; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; STAT TRANSCRIPTION FACTORS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84884482526     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-05-0275     Document Type: Article

References (67)

1. Alicea-Velázquez NL, Jakoncic J, Boggon TJ (2013). Structure-guided studies of the SHP-1/JAK1 interaction provide new insights into phosphatase catalytic domain substrate recognition. J Struct Biol 181, 243-251.
2. Almudi I, Stocker H, Hafen E, Corominas M, Serras F (2009). SOCS36E specifically interferes with Sevenless signaling during Drosophila eye development. Dev Biol 326, 212-223.
3. Arbouzova NI, Zeidler MP (2006). JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development 133, 2605-2616. (Pubitemid 44177882)
4. Aso T, Conrad MN (1997). Molecular cloning of DNAs encoding the regulatory subunits of elongin from Saccharomyces cerevisiae and Drosophila melanogaster. Biochem Biophys Res Commun 241, 334-340. (Pubitemid 28020102)
5. Babon JJ et al. (2006). The structure of SOCS3 reveals the basis of the extended SH2 domain function and identifies an unstructured insertion that regulates stability. Mol Cell 22, 205-216. (Pubitemid 44316440)
6. Babon JJ, Sabo JK, Zhang JG, Nicola NA, Norton RS (2009). The SOCS box encodes a hierarchy of affinities for Cullin5: implications for ubiquitin ligase formation and cytokine signalling suppression. J Mol Biol 387, 162-174.
7. Binari R, Perrimon N (1994). Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. Genes Dev 8, 300-312. (Pubitemid 24065972)
8. Brown S, Hu N, Hombría JC (2001). Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol 11, 1700-1705. (Pubitemid 33037783)
9. Bullock AN, Rodriguez MC, Debreczeni JE, Songyang Z, Knapp S (2007). Structure of the SOCS4-ElonginB/C complex reveals a distinct SOCS box interface and the molecular basis for SOCS-dependent EGFR degradation. Structure 15, 1493-1504. (Pubitemid 350051927)
10. Callus BA, Mathey-Prevot B (2002). SOCS36E, a novel Drosophila SOCS protein, suppresses JAK/STAT and EGF-R signalling in the imaginal wing disc. Oncogene 21, 4812-4821. (Pubitemid 34879456)
11. Chomczynski P, Mackey K (1995). Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. Biotechniques 19, 942-945. (Pubitemid 3021405)
12. Croker BA, Kiu H, Nicholson SE (2008). SOCS regulation of the JAK/STAT signalling pathway. Semin Cell Dev Biol 19, 414-422.
13. Delgado-Ortega M, Marc D, Dupont J, Trapp S, Berri M, Meurens F (2013). SOCS proteins in infectious diseases of mammals. Vet Immunol Immunopathol 151, 1-19.
14. Devergne O, Ghiglione C, Noselli S (2007). The endocytic control of JAK/STAT signalling in Drosophila. J Cell Sci 120, 3457-3464. (Pubitemid 350028353)
15. Dittrich A, Quaiser T, Khouri C, Görtz D, Mönnigmann M, Schaper F (2012). Model-driven experimental analysis of the function of SHP-2 in IL-6-induced Jak/STAT signaling. Mol Biosyst 8, 2119-2134.
16. Doti N, Scognamiglio PL, Madonna S, Scarponi C, Ruvo M, Perretta G, Albanesi C, Marasco D (2012). New mimetic peptides of the kinase-inhibitory region (KIR) of SOCS1 through focused peptide libraries. Biochem J 443, 231-240.
17. Feng Z, Chandrashekaran I, Low A, Speed T, Nicholson SE, Norton RS (2011). The N-terminal domains of SOCS proteins: a conserved region in the disordered N-termini of SOCS4 and 5. Proteins 80, 946-957.
18. Funakoshi-Tago M, Pelletier S, Matsuda T, Parganas E, Ihle JN (2006). Receptor specific downregulation of cytokine signaling by autophosphorylation in the FERM domain of Jak2. EMBO J 25, 4763-4772. (Pubitemid 44607022)
19. Grant B, Donaldson J (2009). Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10, 597-608.
20. Haan C, Kreis S, Margue C, Behrmann I (2006). Jaks and cytokine receptors-an intimate relationship. Biochem Pharmacol 72, 1538-1546. (Pubitemid 44666728)
21. Herranz H, Hong X, Hung NT, Voorhoeve PM, Cohen SM (2012). Oncogenic cooperation between SOCS family proteins and EGFR identified using a Drosophila epithelial transformation model. Genes Dev 26, 1602-1611.
22. Hörtner M, Nielsch U, Mayr LM, Johnston JA, Heinrich PC, Haan S (2002). Suppressor of cytokine signaling-3 is recruited to the activated granulocyte-colony stimulating factor receptor and modulates its signal transduction. J Immunol 169, 1219-1227. (Pubitemid 34809162)
23. Hou XS, Melnick MB, Perrimon N (1996). Marelle acts downstream of the Drosophila HOP/JAK kinase and encodes a protein similar to the mammalian STATs. Cell 84, 411-419. (Pubitemid 26058566)
24. James C, Ugo V, Casadevall N, Constantinescu SN, Vainchenker W (2005). A JAK2 mutation in myeloproliferative disorders: pathogenesis and therapeutic and scientific prospects. Trends Mol Med 11, 546-554. (Pubitemid 41713996)
25. Jatiani SS, Baker SJ, Silverman LR, Reddy EP (2010). JAK/STAT pathways in cytokine signaling and myeloproliferative disorders: approaches for targeted therapies. Genes Cancer 1, 979-993.
26. Kamura T, Sato S, Haque D, Liu L, Kaelin WG, Conaway RC, Conaway JW (1998). The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev 12, 3872-3881. (Pubitemid 29024849)
27. Kaneko T, Joshi R, Feller SM, Li SS (2012). Phosphotyrosine recognition domains: the typical, the atypical and the versatile. Cell Commun Signal 10, 32.
28. Kario E, Marmor MD, Adamsky K, Citri A, Amit I, Amariglio N, Rechavi G, Yarden Y (2005). Suppressors of cytokine signaling 4 and 5 regulate epidermal growth factor receptor signaling. J Biol Chem 280, 7038-7048. (Pubitemid 40341260)
29. Karsten P, Häder S, Zeidler MP (2002). Cloning and expression of Drosophila SOCS36E and its potential regulation by the JAK/STAT pathway. Mech Dev 117, 343-346. (Pubitemid 36158745)
30. Kershaw NJ, Murphy JM, Liau NP, Varghese LN, Laktyushin A, Whitlock EL, Lucet IS, Nicola NA, Babon JJ (2013). SOCS3 binds specific receptor-JAK complexes to control cytokine signaling by direct kinase inhibition. Nat Struct Mol Biol 20, 469-476.
31. Kugler JM, Lem C, Lasko P (2010). Reduced cul-5 activity causes aberrant follicular morphogenesis and germ cell loss in Drosophila oogenesis. PLoS One 5, e9048.
32. Lachance C, Goupil S, Leclerc P (2012). StatticV, a STAT3 inhibitor, affects human spermatozoa through regulation of mitochondrial activity. J Cell Physiol 228, 704-713.
33. Lauwers E, Jacob C, André B (2009). K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway. J Cell Biol 185, 493-502.
34. Levine RL, Wernig G (2006). Role of JAK-STAT signaling in the pathogenesis of myeloproliferative disorders. Hematology Am Soc Hematol Educ Program 2006, 233-239, 510.
35. Linossi EM, Nicholson SE (2012). The SOCS box-adapting proteins for ubiquitination and proteasomal degradation. IUBMB Life 64, 316-323.
36. Liu BA, Engelmann BW, Nash PD (2012). The language of SH2 domain interactions defines phosphotyrosine-mediated signal transduction. FEBS Lett 586, 2597-2605.
37. Marengere LE, Pawson T (1992). Identification of residues in GTPase-activating protein Src homology 2 domains that control binding to tyrosine phosphorylated growth factor receptors and p62. J Biol Chem 267, 22779-22786.
38. Matsuda T, Feng J, Witthuhn BA, Sekine Y, Ihle JN (2004). Determination of the transphosphorylation sites of Jak2 kinase. Biochem Biophys Res Commun 325, 586-594. (Pubitemid 39458035)
39. Müller P, Kuttenkeuler D, Gesellchen V, Zeidler MP, Boutros M (2005). Identification of JAK/STAT signalling components by genome-wide RNA interference. Nature 436, 871-875. (Pubitemid 41160648)
40. Nicholson SE et al. (2005). Suppressor of cytokine signaling (SOCS)-5 is a potential negative regulator of epidermal growth factor signaling. Proc Natl Acad Sci USA 102, 2328-2333. (Pubitemid 40279375)
41. Nicholson SE, Willson TA, Farley A, Starr R, Zhang JG, Baca M, Alexander WS, Metcalf D, Hilton DJ, Nicola NA (1999). Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J 18, 375-385. (Pubitemid 29041946)
42. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D, Gygi SP (2003). A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21, 921-926. (Pubitemid 36936199)
43. Pfeffer SR (2009). Multiple routes of protein transport from endosomes to the trans Golgi network. FEBS Lett 583, 3811-3816.
44. Pickart CM, Fushman D (2004). Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 8, 610-616. (Pubitemid 39535722)
45. Piessevaux J, Lavens D, Peelman F, Tavernier J (2008). The many faces of the SOCS box. Cytokine Growth Factor Rev 19, 371-381.
46. Piganis RA, De Weerd NA, Gould JA, Schindler CW, Mansell A, Nicholson SE, Hertzog PJ (2011). Suppressor of cytokine signaling (SOCS) 1 inhibits type I interferon (IFN) signaling via the interferon ? receptor (IFNAR1)-associated tyrosine kinase Tyk2. J Biol Chem 286, 33811-33818.
47. Platta HW, Stenmark H (2011). Endocytosis and signaling. Curr Opin Cell Biol 23, 393-403.
48. Raiborg C, Stenmark H (2009). The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452.
49. Rawlings JS, Rennebeck G, Harrison SM, Xi R, Harrison DA (2004a). Two Drosophila suppressors of cytokine signaling (SOCS) differentially regulate JAK and EGFR pathway activities. BMC Cell Biol 5, 38.
50. Rawlings JS, Rosler KM, Harrison DA (2004b). The JAK/STAT signaling pathway. J Cell Sci 117, 1281-1283. (Pubitemid 38559804)
51. Saharinen P, Takaluoma K, Silvennoinen O (2000). Regulation of the Jak2 tyrosine kinase by its pseudokinase domain. Mol Cell Biol 20, 3387-3395. (Pubitemid 30243884)
52. Sasaki A, Yasukawa H, Suzuki A, Kamizono S, Syoda T, Kinjyo I, Sasaki M, Johnston JA, Yoshimura A (1999). Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells 4, 339-351. (Pubitemid 29359449)
53. Seki Y, Hayashi K, Matsumoto A, Seki N, Tsukada J, Ransom J, Naka T, Kishimoto T, Yoshimura A, Kubo M (2002). Expression of the suppressor of cytokine signaling-5 (SOCS5) negatively regulates IL-4-dependent STAT6 activation and Th2 differentiation. Proc Natl Acad Sci USA 99, 13003-13008.
54. Silver DL, Geisbrecht ER, Montell DJ (2005). Requirement for JAK/STAT signaling throughout border cell migration in Drosophila. Development 132, 3483-3492. (Pubitemid 41246122)
55. Staerk J, Kallin A, Royer Y, Diaconu CC, Dusa A, Demoulin JB, Vainchenker W, Constantinescu SN (2007). JAK2, the JAK2 V617F mutant and cytokine receptors. Pathol Biol 55, 88-91. (Pubitemid 46412669)
56. Starr R, Hilton DJ (1998). SOCS: suppressors of cytokine signalling. Int J Biochem Cell Biol 30, 1081-1085. (Pubitemid 28484830)
57. Stec WJ, Zeidler MP (2011). Drosophila SOCS proteins. J Signal Transduct 894510.
58. Tamiya T, Kashiwagi I, Takahashi R, Yasukawa H, Yoshimura A (2011). Suppressors of cytokine signaling (SOCS) proteins and JAK/STAT pathways: regulation of T-cell inflammation by SOCS1 and SOCS3. Arterioscler Thromb Vasc Biol 31, 980-985.
59. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000). Recognition of the polyubiquitin proteolytic signal. EMBO J 19, 94-102. (Pubitemid 30009229)
60. Tinti M et al. (2013). The SH2 domain interaction landscape. Cell Rep 3, 1293-1305.
61. Valentino L, Pierre J (2006). JAK/STAT signal transduction: regulators and implication in hematological malignancies. Biochem Pharmacol 71, 713-721. (Pubitemid 43208827)
62. Vidal OM, Stec W, Bausek N, Smythe E, Zeidler MP (2010). Negative regulation of Drosophila JAK-STAT signalling by endocytic trafficking. J Cell Sci 123, 3457-3466.
63. Wölfler A, Irandoust M, Meenhuis A, Gits J, Roovers O, Touw IP (2009). Site-specific ubiquitination determines lysosomal sorting and signal attenuation of the granulocyte colony-stimulating factor receptor. Traffic 10, 1168-1179.
64. Yan R, Small S, Desplan C, Dearolf CR, Darnell JE (1996). Identification of a Stat gene that functions in Drosophila development. Cell 84, 421-430. (Pubitemid 26058567)
65. Yasukawa H et al. (1999). The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 18, 1309-1320. (Pubitemid 29110315)
66. Yoshimura A (2009). Regulation of cytokine signaling by the SOCS and Spred family proteins. Keio J Med 58, 73-83.
67. Zhuang D, Qiu Y, Haque SJ, Dong F (2005). Tyrosine 729 of the G-CSF receptor controls the duration of receptor signaling: involvement of SOCS3 and SOCS1. J Leukoc Biol 78, 1008-1015. (Pubitemid 41384418)