Differential intracellular signalling properties of the growth hormone receptor induced by the activation of an anti-GHR antibody

Molecular and Cellular Endocrinology

Volumn 390, Issue 1-2, 2014, Pages 54-64

  Lan, Hainan ^a   Li, Wei ^b   Fu, Zhiling ^a   Yang, Yanhong ^a   Wu, Tiancheng ^a   Liu, Yu ^a   Zhang, Hui ^a   Cui, Huanzhong ^a   Li, Yumeng ^a   Hong, Pan ^a   Liu, Jingsheng ^a   Zheng, Xin ^a  

^a JILIN AGRICULTURAL UNIVERSITY   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Anti GHR antibody; Growth hormone receptor; Signal transduction pathway

Indexed keywords

GROWTH HORMONE RECEPTOR; HORMONE ANTIBODY; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CG 172; PROTEIN KINASE B; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; UNCLASSIFIED DRUG; HUMAN GROWTH HORMONE; STAT PROTEIN;

ANIMAL CELL; ANTIBODY COMBINING SITE; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN ANTIBODY REACTION; ARTICLE; CELL PROLIFERATION; CELL STRAIN; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG RECEPTOR BINDING; DRUG RESPONSE; DRUG TARGETING; ENZYME ACTIVATION; ENZYME KINETICS; EPITOPE MAPPING; HORMONE RECEPTOR INTERACTION; IMMUNOPRECIPITATION; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WESTERN BLOTTING; AGONISTS; ANIMAL; BAGG ALBINO MOUSE; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; FEMALE; HAMSTER; HUMAN; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; CELL PROLIFERATION; CHO CELLS; CRICETINAE; CRICETULUS; EPITOPE MAPPING; FEMALE; HEPATOCYTES; HUMAN GROWTH HORMONE; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE, INBRED BALB C; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTORS, SOMATOTROPIN; STAT TRANSCRIPTION FACTORS;

EID: 84899881975     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.04.004     Document Type: Article

References (47)

1. Abdel-Meguid S.S., Shieh H.S., Smith W.W., Dayriner H.E., Violand B.N., Bentle L.A. Three dimensional structure of a genetically engineered variant of porcine growth hormone. Proc. Natl. Acad. Sci. 1987, 84:6434-6437.
2. Allevato G., Billestrup N., Goujon L., Galsgaard E.D., Norstedt G., Postel-Vinay M.C., Kelly P.A., Nielsen J.H. Identification of phenylalanine 346 in the rat growth hormone receptor as being critical for ligand-mediated internalization and down-regulation. J. Biol. Chem. 1995, 270:17210-17214.
3. Alzari P.M., Lascombe M.B., Poljak R.J. Three-dimensional structure of antibodies. Annu. Rev. Immunol. 1988, 6:555-580.
4. Argetsinger L.S., Norstedt G., Billestrup N., White M.F., Carter-Su C. Growth hormone, interferon-γ, and leukemia inhibitory factor utilize insulin receptor substrate-2 in intracellular signaling. J. Biol. Chem. 1996, 271:29415-29421.
5. Barclay J.L., Kerr L.M., Arthur L., Rowland J.E., Nelson C.N., Ishikawa M., d'Aniello E.M., White M., Noakes P.G., Waters M.J. In vivo targeting ofthe growth hormone receptor (GHR) Box1 sequence demonstrates that the GHR does not signal exclusively through JAK2. Mol. Endocrinol. 2010, 24:204-217.
6. Barnard R., Bundesen P.G., Rylatt D.B., Waters M.J. Evidence from the use of monoclonal antibody probes for structural heterogeneity of the growth hormone receptor. Biochem. J. 1985, 231:459-468.
7. Behncken S.N., Billestrup N., Brown R., Amstrup J., Conway-Campbell B., Waters M.J. Growth hormone (GH)-independent dimerization of GH receptor by a leucine zipper results in constitutive activation. J. Biol. Chem. 2000, 275:17000-17007.
8. Brooks A.J., Waters M.J. The growth hormone receptor: mechanism of activation and clinical implications. Nat. Rev. Endocrinol. 2010, 6:515-525.
9. Brooks A.J., Wooh J.W., Tunny K.A., Waters M.J. Growth hormone receptor; mechanism of action. Int. J. Biochem. Cell. Biol. 2008, 40:1984-1989.
10. Brown R.J., Adams J.J., Pelekanos R.A., Wan Y., McKinstry W.J., Palethorpe K., Seeber R.M., Monks T.A., Eidne K.A., Parker M.W., Waters M.J. Model forgrowth hormone receptor activation based on subunit rotation within a receptordimer. Nat. Struct. Mol. Biol. 2005, 12:814-821.
11. Carlsson, L.M.S., Mortensen, D.L., Cunnungham, B.C., Clark, R.G., 1994. A monoclonal antibody against the GH receptor stimulates growth in hypophysectomized rats. In: Program of the 76th Annual Meeting of the Endocrine, Society, 434p.
12. Costoya J.A., Finidori J., Moutoussamy S., Señaris R., Devesa J., Arce V.M. Activation of growth hormone receptor delivers an antiapoptotic signal: evidence for a role of Akt in this pathway. Endocrinology 1999, 140:5937-5943.
13. 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.
14. De Vos A.M., Mark U., Anthony A.K. Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science 1992, 255:306-312.
15. Elliott S., Lorenzini T., Yanagihara D., Chang D., Elliott G. Activation of the erythropoietin (EPO) receptor by bivalent anti-EPO receptor antibodies. J. Biol. Chem. 1996, 271:24691-24697.
16. Fuh G., Cunningham B.C., Fukunaga R., Nagata S., Goeddel D.V., Wells J.A. Rational design of potent antagonists to the human growth hormone receptor. Science 1992, 256:1677-1680.
17. Gurney A.L., Wong S.C., Henzel W.J., de Sauvage F.J. Distinct regions of c-Mpl cytoplasmic domain are coupled to the JAK-STAT signal transduction pathway and Shc phosphorylation. Proc. Natl. Acad. Sci. 1995, 92:5292-5296.
18. Herrington J., Smit L.S., Schwartz J., Carter-Su C. The role of STATproteins in growth hormone signaling. Oncogene 2000, 19:2585-2597.
19. Jin H., Lanning N.J., Carter-Su C. JAK2, but not Src family kinases, is required for STAT, ERK, and Akt signaling in response to growth hormone in preadipocytes and hepatoma cells. Mol. Endocrinol. 2008, 22:1825-1841.
20. Li W., Lan H., Liu H., Fu Z., Yang Y., Han W.W., Zheng X. The activation and differential signalling of the growth hormone receptor induced by pGH or anti-idiotypic monoclonal antibodies in primary rat hepatocytes. Mol. Cell Endocrinol. 2013, 376:51-59.
21. Ling L., Zhu T., Lobie P.E. Src-CrkII-C3G-dependent activation of Rap1 switches growth hormone-stimulated p44/42 MAP kinase and JNK/SAPK activities. J. Biol. Chem. 2003, 278:27301-27311.
22. Liu Z.H., Stoll V.S., Devries P.J., Jakob C.G., Xie N., Simmer R.L. A potent erythropoietin-mimicking human antibody interacts through a novel binding site. Blood 2007, 110:2408-2413.
23. Mathews L.S., Enberg B., Norstedt G. Regulation of rat growth hormone receptor gene expression. J. Biol. Chem. 1989, 264:9905-9910.
24. Mellado M., Rodriguez-Frade J.M., Kremer L., Von Kobbe C., De Ana A.M., Merida I., Martinez-A C. Conformational changes required in the human growth Hormone receptor for growth hormone signaling. J. Biol. Chem. 1997, 272:9189-9196.
25. Milward A., Metherell L., Maamra M., Barahona M.J., Wilkinson I.R., Camacho-Hübner C., Savage M.O., Bildlingmaier C.M., Clark A.J.L., Ross R.J.M., Webb S.M. Growth hormone (GH) insensitivity syndrome due to a GH receptor truncated after Box1, resulting in isolated failure of STAT 5 signal transduction. J. Clin. Endocrinol. Metab. 2004, 89:1259-1266.
26. Møller N., Jens O.L.J. Effects of growth hormone on glucose, lipid, and protein metabolism in human subjects. Endocr. Rev. 2009, 30:152-177.
27. Moutoussamy S., Renaudie F., Lago F., Kelly P.A., Finidori J. Grb10 identified as a potential regulator of growth hormone (GH) signaling by cloning of GH receptor target proteins. J. Biol. Chem. 1998, 273:15906-15912.
28. Murray R.D., Kim K., Ren S.G., Chelly M., Umehara Y., Melmed S. Central and peripheral actions of somatostatin on the growth hormone-IGF-I axis. J. Clin. Invest. 2004, 114:349-356.
29. Pang X., Zhou H.X. A common model for cytokine receptor activation: combined scissor-like rotation and self-rotation of receptor dimer induced by class I cytokine. PloS Comput. Biol. 2012, 8:e1002427.
30. Ram P.A., Park S.H., Choi H.K., Waxman D.J. Growth hormone activation of Stat 1, Stat 3, and Stat 5 in rat liver. J. Biol. Chem. 1996, 271:5929-5940.
31. Ribaux P., Gjinovci A., Sadowski H.B., Iynedjian P.B. Discrimination between signaling pathways in regulation of specific gene expression by insulinand growth hormone in hepatocytes. Endocrinology 2002, 143:3766-3772.
32. Ridderstråle M., Degerman E., Tornqvist H. Growth hormone stimulates the tyrosine phosphorylation of the insulin receptor substrate-1 and its association with phosphatidylinositol 3-kinase in primary adipocytes. J. Biol. Chem. 1995, 270:3471-3474.
33. Rowlinson S.W., Behncken S.N., Rowland J.E., Clarkson R.W., Strasburger C.J., Wu Z., Baumbach W., Waters M.J. Activation of chimeric and full-length growth hormone receptors by growth hormone receptor monoclonal antibodies. A specific conformational change may be required for full-length receptor signaling. J. Biol. Chem. 1998, 273:5307-5314.
34. Rowlinson S.W., Yoshizato H., Barclay J.L., Brooks A.J., Behncken S.N., Kerr L.M., Millard K., Palethorpe K., Nielsen K., Clyde-Smith J., Hancock J.F., Waters M.J. An agonist-induced conformational change in the GH receptor determines choice of signaling pathway. Nat. Cell Biol. 2008, 10:740-747.
35. Ryazantsev S., Tischenko V., Nguyen C., Abramov V., Zav'yalov V. Three-dimensional structure of the human myeloma IgG2. PloS one 2013, 8:e64076.
36. Smit L.S., Meyer D.J., Billestrup N., Norstedt G., Schwartz J., Carter-Su C. The role of the growth hormone (GH) receptor and JAK1 and JAK2 kinases in the activation of Stats 1, 3, and 5 by GH. Mol. Endocrinol. 1996, 10:519-533.
37. Sotiropoulos A., Moutoussamy S., Renaudie F., Clauss M., Kayser C., Gouilleux F., Kelly P.A., Finidori J. Differential activation of Stat3 and Stat5by distinct regions of the growth hormone receptor. Mol. Endocrinol. 1996, 10:998-1009.
38. Tiulpakov A., Rubtsov P., Dedov I., Peterkova V., Bezlepkina O., Chrousos G.P., Hochberg Z.E. A novel C-terminal growth hormone receptor (GHR) mutation results in impaired GHR-STAT5 but normal STAT-3 signaling. J. Clin. Endocrinol. Metab. 2005, 90:542-547.
39. VanderKuur J., Allevato G., Billestrup N., Norstedt G., Carter-Su C. Growth hormone-promoted tyrosyl phosphorylation of SHC proteins and SHC association with Grb2. J. Biol. Chem. 1995, 270:7587-7593.
40. VanderKuur J.A., Butch E.R., Waters S.B., Pessin J.E., Guan K.L., Carter-Su C. Signaling molecules involved in coupling growth hormone receptor tomitogen-activated protein kinase activation. Endocrinology 1997, 138:4301-4307.
41. Wan Y., Zheng Y.Z., Harris J.M., Brown R., Waters M.J. Epitope map for a GH receptor agonist monoclonal antibody Mab 263. Mol. Endocrinol. 2003, 17:2240-2250.
42. Wang B.S., Lumanglas A.A., Bona C.A., Moran T.M. Promotion of animal growth with a monoclonal antibody specific to growth hormone receptor. Mol. Cell. Endocrinol. 1996, 116:223-226.
43. Wang B.S., Lumanglas A.L., Bona C.A., Moran T.M. Functional characterization of monoclonal antibodies specific to growth hormone receptor. Mol. Immunol. 1996, 33:1197-1202.
44. Winston L.A., Hunter T. JAK2, Ras, and Raf are required for activationof extracellular signal-regulated kinase/mitogen-activated protein kinase by growth hormone. J. Biol. Chem. 1995, 270:30837-30840.
45. Wu Z., Lima G., Strasburger C.J. Explore the mechanism of growth hormone signaling with growth hormone receptor monoclonal antibodies. Growth Horm. IGF Res. 2010, 20:S32-S33.
46. Zhu T., Goh E.L., Graichen R., Ling L., Lobie P.E. Signal transduction via the growth hormone receptor. Cell. Signal. 2001, 13:599-616.
47. Zhu T., Ling L., Lobie P.E. Identification of a JAK2-independent pathway regulating growth hormone (GH)-stimulated p44/42 mitogen-activated protein kinase activity GH activation of Ral and phospholipase D ISSrc-dependent. J. Biol. Chem. 2002, 277:45592-45603.