Downregulation of the growth hormone-induced Janus kinase 2/signal transducer and activator of transcription 5 signaling pathway requires an intact actin cytoskeleton

Experimental Cell Research

Volumn 294, Issue 1, 2004, Pages 269-280

  Rico Bautista, Elizabeth ^a   Negrín Martínez, Ciro ^b   Novoa Mogollón, Javier ^b   Fernández Perez, Leandro ^b   Flores Morales, Amilcar ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

Author keywords

Actin; Cytoskeleton; GHR; Internalization; JAK2; SOCS; STAT5; Ubiquitination

Indexed keywords

ACTIN; CYTOCHALASIN D; DNA; GROWTH HORMONE; JANUS KINASE 2; STAT5 PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BIOACCUMULATION; CONTROLLED STUDY; CYTOSKELETON; DNA BINDING; DOWN REGULATION; ELECTRIC POTENTIAL; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION;

JANUS;

EID: 1242339600     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.11.017     Document Type: Article

References (46)

1. Herrington J., Smit L.S., Schwartz J., Carter-Su C. The role of STAT proteins in growth hormone signaling. Oncogene. 19:2000;2585-2597.
2. Zhu T., Goh E.L.K., Graichen R., Ling L., Lobie P.E. Signal transduction via the growth hormone receptor. Cell. Signalling. 13:2001;599-616.
3. Fernandez L., Flores-Morales A., Lahuna O., Sliva D., Norstedt G., Haldosen L.A., Mode A., Gustafsson J.A. Desensitization of the growth hormone-induced Janus kinase 2 (Jak 2)/signal transducer and activator of transcription 5 (Stat5)-signaling pathway requires protein synthesis and phospholipase C. Endocrinology. 139:1998;1815-1824.
4. Stofega M.R., Wang H., Ullrich A., Carter-Su C. Growth hormone regulation of SIRP and SHP-2 tyrosyl phosphorylation and association. J. Biol. Chem. 273:1998;7112-7117.
5. Strous G.J., Gent J. Dimerization, ubiquitylation and endocytosis go together in growth hormone receptor function. FEBS Lett. 529:2002;102-109.
6. Krebs D.L., Hilton D.J. SOCS proteins: negative regulators of cytokine signaling. Stem Cells. 19:2001;378-387.
7. Metcalf D., Greenhalgh C.J., Viney E., Willson T.A., Starr R., Nicola N.A., Hilton D.J., Alexander W.S. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature. 405:2000;1069-1073.
8. Greenhalgh C.J., Bertolino P., Asa S.L., Metcalf D., Corbin J.E., Adams T.E., Davey H.W., Nicola N.A., Hilton D.J., Alexander W.S. Growth enhancement in suppressor of cytokine signaling 2 (SOCS-2)-deficient mice is dependent on signal transducer and activator of transcription 5b (STAT5b). Mol. Endocrinol. 16:2002;1394-1406.
9. Hansen J.A., Lindberg K., Hilton D.J., Nielsen J.H., Billestrup N. Mechanism of inhibition of growth hormone receptor signaling by suppressor of cytokine signaling proteins. Mol. Endocrinol. 13:1999;1832-1843.
10. Goh E.L., Pircher T.J., Wood T.J., Norstedt G., Graichen R., Lobie P.E. Growth hormone-induced reorganization of the actin cytoskeleton is not required for STAT5 (signal transducer and activator of transcription-5)-mediated transcription. Endocrinology. 138:1997;3207-3215.
11. Goh E.L.K., Pircher T.J., Lobie P.E. Growth hormone promotion of tubulin polymerization stabilizes the microtubule network and protects against colchicine-induced apoptosis. Endocrinology. 139:1998;4364-4372.
12. Kaulsay K.K., Mertani H.C., Lee K.O., Lobie P.E. Autocrine human growth hormone enhancement of human mammary carcinoma cell spreading is Jak2 dependent. Endocrinology. 141:2000;1571-1584.
13. Ryu H., Lee J.H., Kim K.S., Jeong S.M., Kim P.H., Chung H.T. Regulation of neutrophil adhesion by pituitary growth hormone accompanies tyrosine phosphorylation for Jak2, p125FAK, and paxillin. J. Immunol. 165:2000;2116-2123.
14. Diakonova M., Gunter D.R., Herrington J., Carter-Su C. SH2-Bβ is a Rac-binding protein that regulates cell motility. J. Biol. Chem. 277:2002;10669-10677.
15. Janmey P.A. The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol. Rev. 78:1998;763-781.
16. Pawlak G., Helfman D.M. Cytoskeletal changes in cell transformation and tumorigenesis. Curr. Opin. Genet. Dev. 11:2001;41-47.
17. Chintala S.K., Kyritsis A.P., Mohan P.M., Mohanam S., Sawaya R., Gokslan Z., Yung W.K., Steck P., Uhm J.H., Aggarwal B.B., Rao J.S. Altered actin cytoskeleton and inhibition of matrix metalloproteinase expression by vanadate and phenylarsine oxide, inhibitors of phosphotyrosine phosphatases: modulation of migration and invasion of human malignant glioma cells. Mol. Carcinog. 26:1999;274-285.
18. Schevzov G., Lloyd C., Hailstones D., Gunning P. Differential regulation of tropomyosin isoform organization and gene expression in response to altered actin gene expression. J. Cell Biol. 121:1993;811-821.
19. Providence K.M., Kutz S.M., Higgings P.J. Perturbation of the actin cytoskeleton induces PAI-1 gene expression in cultured epithelial cells independent of substrate anchorage. Cell Motil. Cytoskeleton. 42:1999;218-229.
20. Francis S.M., Enerbäck S., Möller C., Enberg B., Norstedt G. A novel in vitro model for studying signal transduction and gene regulation via the growth hormone receptor. Mol. Endocrinol. 7:1993;972-978.
21. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1983;1475-1489.
22. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
23. Sliva D., Wood T.J.J., Schindler C., Lobie P.E., Norstedt G. Growth hormone specifically regulates serine protease inhibitor gene transcription via gamma-activated sequence-like DNA elements. J. Biol. Chem. 269:1994;26208-26214.
24. Müller S., Sideras P., Smith C.I., Xanthopoulos K.G. Cell specific expression of human Bruton's agammaglobulinemia tyrosine kinase gene (Btk) is regulated by Sp1- and Sp1/PU.1 family members. Oncogene. 13:1996;1955-1964.
25. Mizushima S., Nagata S. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18:1990;5322.
26. Seed B., Sheen J.Y. A simple phase-extraction assay for chloramphenicol acyltransferase activity. Gene. 67:1988;271-277.
27. Govers R., van Kerkhof P., Schwartz A.L., Strous G.J. Linkage of the ubiquitin-conjugating system and the endocytic pathway in ligand-induced internalization of the growth hormone receptor. EMBO J. 16:1997;4851-4858.
28. Stapulionis R., Kolli S., Deutscher M.P. Efficient mammalian protein synthesis requires an intact F-actin system. J. Biol. Chem. 272:1997;24980- 24986.
29. Stofega M.R., Herrington J., Billestrup N., Carter-Su C. Mutation of the SHP-2 binding site in growth hormone (GH) receptor prolongs GH-promoted tyrosyl phosphorylation of GH receptor, JAK2, and STAT5B. Mol. Endocrinol. 14:2000;1338-1350.
30. Flores-Morales A., Fernandez L., Rico-Bautista E., Umana A., Negrin C., Zhang J.G., Norstedt G. Endoplasmic reticulum stress prolongs GH-induced Janus kinase (JAK2)/signal transducer and activator of transcription (STAT5) signaling pathway. Mol. Endocrinol. 15:2001;1471-1483.
31. Alves dos Santos C.M., van Kerkhof P., Strous G.J. The signal transduction of the growth hormone receptor is regulated by the ubiquitin/proteasome system and continues after endocytosis. J. Biol. Chem. 276:2001;10839-10846.
32. Gebert C.A., Park S.H., Waxman D.J. Down-regulation of liver Jak2-Stat5b signaling by the female plasma pattern of continuous growth hormone stimulation. Mol. Endocrinol. 13:1999;213-227.
33. Ram P.A., Waxman D.J. SOCS/CIS protein inhibition of growth hormone-stimulated STAT5 signaling by multiple mechanisms. J. Biol. Chem. 274:1999;35553-35561.
34. Fujimoto L.M., Roth R., Heuser J.E., Schmid S.L. Actin assembly plays a variable, but not obligatory role, in receptor-mediated endocytosis in mammalian cells. Traffic. 1:2000;161-171.
35. Wiley H.S., Burke P.M. Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic. 2:2001;12-18.
36. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67:1998;425-479.
37. Ungureanu D., Saharinen P., Junttila I., Hilton D.J., Silvennoinen O. Regulation of Jak2 through ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS1. Mol. Cell. Biol. 22:2002;3316-3326.
38. Tollet-Egnell P., Flores-Morales A., Stavreus-Evers A., Sahlin L., Norstedt G. Growth hormone regulation of SOCS-2, SOCS-3, and CIS messenger ribonucleic acid expression in the rat. Endocrinology. 140:1999;3693-3704.
39. Biener E., Maurice S., Sandowski Y., Cohen Y., Gusakowsky E.E., Hooghe R., Yoshimura A., Livnah O., Gertler A. Recombinant human CIS2 (SOCS2) protein: subcloning, expression, purification, and characterization. Protein Expression Purif. 25:2002;305-312.
40. Gottlieb T.A., Ivanov I.E., Adesnik M., Sabatini D.D. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120:1993;695-710.
41. Kubler E., Riezman H. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J. 12:1993;2855-2862.
42. Brown B.K., Song W. The actin cytoskeleton is required for the trafficking of the B cell antigen receptor to the late endosomes. Traffic. 2:2001;414-427.
43. Haj F.G., Verveer P.J., Squire A., Neel B.G., Bastiaens P.I. Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science. 295:2002;1708-1711.
44. Aoki N., Matsuda T. A nuclear protein tyrosine phosphatase TC-PTP is a potential negative regulator of the PRL-mediated signaling pathway: dephosphorylation and deactivation of signal transducer and activator of transcription 5a and 5b by TC-PTP in nucleus. Mol. Endocrinol. 16:2002;58-69.
45. Myers M.P., Andersen J.N., Cheng A., Tremblay M.L., Horvath C.M., Parisien J.P., Salmeen A., Barford D., Tonks N.K. TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J. Biol. Chem. 276:2001;47771-47774.
46. Gjorloff-Wingren A., Saxena M., Han S., Wang X., Alonso A., Renedo M., Oh P., Williams S., Schnitzer J., Mustelin T. Subcellular localization of intracellular protein tyrosine phosphatases in T cells. Eur. J. Immunol. 30:2000;2412-2421.