Two Drosophila suppressors of cytokine signaling (SOCS) differentially regulate JAK and EGFR pathway activities

BMC Cell Biology

Volumn 5, Issue , 2004, Pages

  Rawlings, Jason S ^a   Rennebeck, Gabriela ^a   Harrison, Susan M W ^a   Xi, Rongwen ^a   Harrison, Douglas A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; SUPPRESSOR OF CYTOKINE SIGNALING; EGFR PROTEIN, DROSOPHILA; JANUS KINASE 1; JANUS KINASE 2; JANUS KINASE 3; ONCOPROTEIN; PROTEIN KINASE; PROTEIN TYROSINE KINASE; RECEPTOR; REPRESSOR PROTEIN; SIGNAL PEPTIDE; SOCS36E PROTEIN, DROSOPHILA; SOCS44A PROTEIN, DROSOPHILA;

ANIMAL CELL; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; ENZYME REPRESSION; GENOME ANALYSIS; MAMMAL; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VERTEBRATE; ANIMAL; ARTICLE; CHEMISTRY; DROSOPHILA MELANOGASTER; ENZYMOLOGY; FEMALE; FORELIMB; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; MOLECULAR GENETICS; OOCYTE DEVELOPMENT; OVARY; PHYSIOLOGY; PRENATAL DEVELOPMENT; UPREGULATION;

INVERTEBRATA; JANUS; MAMMALIA; VERTEBRATA;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JANUS KINASE 1; JANUS KINASE 2; JANUS KINASE 3; MOLECULAR SEQUENCE DATA; OOGENESIS; OVARY; PROTEIN KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; UP-REGULATION; WING;

EID: 10444257919     PISSN: 14712121     EISSN: None     Source Type: Journal    
DOI: 10.1186/1471-2121-5-38     Document Type: Review

References (67)

1. O'Shea JJ, Gadina M, Schreiber RD: Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 2002, 109 Suppl:S121-31.
2. Igaz P, Toth S, Falus A: Biological and clinical significance of the JAK-STAT pathway; lessons from knockout mice. Inflamm Res 2001, 50:435-441.
3. Rawlings JS, Rosler KM, Harrison DA: The JAK/STAT signaling pathway. J Cell Sci 2004, 117:1281-1283.
4. Lacronique V, Boureux A, Valle VD, Poirel H, Quang CT, Mauchauffe M, Berthou C, Lessard M, Berger R, Ghysdael J, Bernard OA: A TELJAK2 fusion protein with constitutive kinase activity in human leukemia. Science 1997, 278:1309-1312.
5. Peeters P, Raynaud SD, Cools J, Wlodarska I, Grosgeorge J, Philip P, Monpoux F, Van Rompaey L, Baens M, Van den Berghe H, Marynen P: Fusion of TEL, the ETS-variant gene 6 (ETV6), to the receptor-associated kinase JAK2 as a result of t(9;12) in a lymphoid and t(9;15;12) in a myeloid leukemia. Blood 1997, 90: 535-2540.
6. Ho JM, Beattie BK, Squire JA, Frank DA, Barber DL: Fusion of the ets transcription factor TEL to Jak2 results in constitutive Jak-Stat signaling. Blood 1999, 93:4354-4364.
7. Bowman T, Garcia R, Turkson J, Jove R: STATs in oncogenesis. Oncogene 2000, 19:2474-2488.
8. Coffer PJ, Koenderman L, de Groot RP: The role of STATs in myeloid differentiation and leukemia. Oncogene 2000, 19: 511-2522.
9. Alexander WS: Suppressors of cytokine signalling (SOCS) in the immune system. Nat Rev Immunol 2002, 2:410-416.
10. Zong C, Yan R, August A, Darnell JE, Hanafusa H: Unique signal transduction of Eyk: constitutive stimulation of the JAKSTAT pathway by an oncogenic receptor-type tyrosine kinase. EMBO J 1996, 15:4515-4525.
11. Cao X, Tay A, Guy GR, Tan YH: Activation and association of Stat3 with Src in v-Src-transformed cell lines. Mol Cell Biol 1996, 16:1595-1603.
12. Danial NN, Pernis A, Rothman PB: Jak-STAT signaling induced by the v-abl oncogene. Science 1995, 269: 875-1877.
13. Yu CL, Meyer DJ, Campbell GS, Larner AC, Carter-Su C, Schwartz J, Jove R: Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 1995, 269:81-83.
14. Kile BT, Nicola NA, Alexander WS: Negative regulators of cytokine signaling. Int J Hematol 2001, 73:292-298.
15. Greenhalgh CJ, Hilton DJ: Negative regulation of cytokine signaling. J Leukoc Biol 2001, 70:348-356.
16. Alexander Warren S., Hilton Douglas J.: The Role of Suppressors of Cytokine Signaling (SOCS) Proteins in Regulation of the Immune Response. Annual Review of Immunology 2004, 22: 03-529.
17. Kamura T, Sato S, Haque D, Liu L, Kaelin W. G., Jr., Conaway RC, Conaway JW: 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 1998, 12:3872-3881.
18. Zhang JG, Farley A, Nicholson SE, Willson TA, Zugaro LM, Simpson RJ, Moritz RL, Cary D, Richardson R, Hausmann G, Kile BJ, Kent SB, Alexander WS, Metcalf D, Hilton DJ, Nicola NA, Baca M: The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc Natl Acad Sci U S A 1999, 96:2071-2076.
19. Zeidler MP, Bach EA, Perrimon N: The roles of the Drosophila JAK/STAT pathway. Oncogene 2000, 19:2598-2606.
20. Barillas-Mury C, Han YS, Seeley D, Kafatos FC: Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. Embo J 1999, 18:959-967.
21. Hombria JC, Brown S: The fertile field of Drosophila Jak/STAT signalling. Curr Biol 2002, 12:R569-75.
22. Harrison DA, Binari R, Nahreini TS, Gilman M, Perrimon N: Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J 1995, 14: 857-2865.
23. Luo H, Hanratty WP, Dearolf CR: An amino acid substitution in the Drosophila hopTum-1 Jak kinase causes leukemia-like hematopoietic defects. EMBO J 1995, 14:1412-1420.
24. Luo H, Rose P, Barber D, Hanratty WP, Lee S, Roberts TM, D'Andrea AD, Dearolf CR: Mutation in the Jak kinase JH2 domain hyperactivates Drosophila and mammalian Jak-Stat pathways. Mol Cell Biol 1997, 17:1562-1571.
25. Zeidler MP, Perrimon N, Strutt DI: Polarity determination in the Drosophila eye: a novel role for unpaired and JAK/STAT signaling. Genes Dev 1999, 13:1342-1353.
26. McGregor Jennifer R., Xi Rongwen, Harrison Douglas A.: JAK signaling is somatically required for follicle cell differentiation in Drosophila. Development 2002, 129:705-717.
27. Bach EA, Vincent S, Zeidler MP, Perrimon N: A sensitized genetic screen to identify novel regulators and components of the Drosophila janus kinase/signal transducer and activator of transcription pathway. Genetics 2003, 165:1149-1166.
28. Callus BA, Mathey-Prevot B: SOCS36E, a novel Drosophila SOCS protein, suppresses JAK/STAT and EGF-R signalling in the imaginal wing disc. Oncogene 2002, 21:4812-4821.
29. Karsten P, Hader S, Zeidler M: Cloning and expression of Drosophila SOCS36E and its potential regulation by the JAK/STAT pathway. Mech Dev 2002, 117:343.
30. Hilton DJ, Richardson RT, Alexander WS, Viney EM, Willson TA, Sprigg NS, Starr R, Nicholson SE, Metcalf D, Nicola NA: Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc Natl Acad Sci U S A 1998, 95:114-119.
31. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor Miklos GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, et al.: The genome sequence of Drosophila melanogaster. Science 2000, 287:2185-2195.
32. Harrison DA, McCoon PE, Binari R, Gilman M, Perrimon N: Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev 1998, 12:3252-3263.
33. Xi R, McGregor JR, Harrison DA: A gradient of JAK pathway activity patterns the anterior-posterior axis of the follicular epithelium. Dev Cell 2003, 4:167-177.
34. Chou TB, Perrimon N: Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 1992, 131:643-653.
35. Brown S, Hu N, Hombria JC: Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless. Curr Biol 2001, 11:1700-1705.
36. Chen HW, Chen X, Oh SW, Marinissen MJ, Gutkind JS, Hou SX: mom identifies a receptor for the Drosophila JAK/STAT signal transduction pathway and encodes a protein distantly related to the mammalian cytokine receptor family. Genes Dev 2002, 16:388-398.
37. Yan R, Luo H, Darnell J E, Jr, Dearolf CR: A JAK-STAT pathway regulates wing vein formation in Drosophila. Proc Natl Acad Sci USA 1996, 93:5842-5847.
38. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F: Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003, 374:1-20.
39. Rane SG, Reddy EP: Janus kinases: components of multiple signaling pathways. Oncogene 2000, 19:5662-5679.
40. Shuai K: Modulation of STAT signaling by STAT-interacting proteins. Oncogene 2000, 19:2638-2644.
41. Shilo BZ: Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp Cell Res 2003, 284:140-149.
42. de Celis JF: Pattern formation in the Drosophila wing: The development of the veins. Bioessays 2003, 25:443-451.
43. Johnston JA, O'Shea JJ: Matching SOCS with function. Nat Immunol 2003, 4:507-509.
44. Beccari S, Teixeira L, Rorth P: The JAK/STAT pathway is required for border cell migration during Drosophila oogenesis. Mech Dev 2002, 111:115-123.
45. Silver DL, Montell DJ: Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell 2001, 107:831-841.
46. Gonzalez-Reyes A, Elliott H, St Johnston D: Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 1995, 375:654-658.
47. Roth S, Neuman-Silberberg FS, Barcelo G, Schupbach T: cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 1995, 81:967-978.
48. Morimoto AM, Jordan KC, Tietze K, Britton JS, O'Neill EM, Ruohola-Baker H: Pointed, an ETS domain transcription factor, negatively regulates the EGF receptor pathway in Drosophila oogenesis. Development 1996, 122:3745-3754.
49. Gonzalez-Reyes A, St Johnston D: Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila oogenesis. Development 1998, 125:2837-2846.
50. Nicholson SE, Willson TA, Farley A, Starr R, Zhang JG, Baca M, Alexander WS, Metcalf D, Hilton DJ, Nicola NA: 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 1999, 18:375-385.
51. Krebs DL, Uren RT, Metcalf D, Rakar S, Zhang JG, Starr R, De Souza DP, Hanzinikolas K, Eyles J, Connolly LM, Simpson RJ, Nicola NA, Nicholson SE, Baca M, Hilton DJ, Alexander WS: SOCS-6 binds to insulin receptor substrate 4, and mice lacking the SOCS-6 gene exhibit mild growth retardation. Mol Cell Biol 2002, 22:4567-4578.
52. Mooney RA, Senn J, Cameron S, Inamdar N, Boivin LM, Shang Y, Furlanetto RW: Suppressors of cytokine signaling-1 and -6 associate with and inhibit the insulin receptor. A potential mechanism for cytokine-mediated insulin resistance. J Biol Chem 2001, 276: 5889-25893.
53. Matuoka K, Miki H, Takahashi K, Takenawa T: A novel ligand for an SH3 domain of the adaptor protein Nck bears an SH2 domain and nuclear signaling motifs. Biochem Biophys Res Commun 1997, 239:488-492.
54. Mohr SE, Boswell RE: Zimp encodes a homologue of mouse Miz1 and PIAS3 and is an essential gene in Drosophila melanogaster. Gene 1999, 229:109-116.
55. Betz A, Lampen N, Martinek S, Young MW, Darnell JE, Jr.: A Drosophila PIAS homologue negatively regulates stat92E. Proc Natl Acad Sci U S A 2001, 98:9563-9568.
56. De Sepulveda P, Ilangumaran S, Rottapel R: Suppressor of cytokine signaling-1 inhibits VAV function through protein degradation. J Biol Chem 2000, 275:14005-14008.
57. Ohya K, Kajigaya S, Yamashita Y, Miyazato A, Hatake K, Miura Y, Ikeda U, Shimada K, Ozawa K, Mano H: SOCS-1/JAB/SSI-1 can bind to and suppress Tec protein-tyrosine kinase. J Biol Chem 1997, 272:27178-27182.
58. Pircher TJ, Geiger JN, Zhang D, Miller CP, Gaines P, Wojchowski DM: Integrative signaling by minimal erythropoietin receptor forms and c-Kit. J Biol Chem 2001, 276:8995-9002.
59. Liu E, Cote JF, Vuori K: Negative regulation of FAK signaling by SOCS proteins. Embo J 2003, 22:5036-5046.
60. Li S, Chen S, Xu X, Sundstedt A, Paulsson KM, Anderson P, Karlsson S, Sjogren HO, Wang P: Cytokine-induced Src homology 2 protein (CIS) promotes T cell receptor-mediated proliferation and prolongs survival of activated T cells. J Exp Med 2000, 191: 85-994.
61. Cacalano NA, Sanden D, Johnston JA: Tyrosine-phosphorylated SOCS-3 inhibits STAT activation but binds to p120 RasGAP and activates Ras. Nat Cell Biol 2001, 3:460-465.
62. Brown NH, Kafatos FC: Functional cDNA libraries from Drosophila embryos. J Mol Biol 1988, 203:425-437.
63. Isaac DD, Andrew DJ: Tubulogenesis in Drosophila: a requirement for the trachealess gene product. Genes Dev 1996, 10:103-117.
64. Brand AH, Perrimon N: Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
65. Spradling A: P element-mediated transformation. Drosophila: A practical approach Edited by: D Roberts. Oxford, IRL Press; 1986:175-197.
66. Ashburner M: Drosophila: A Laboratory Manual. Cold Spring Harbor, Cold Spring Harbor Laboratory Press; 1989:434.
67. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D: The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 1997, 124:761-771.