Growth hormone signaling in human T47D breast cancer cells: Potential role for a growth hormone Receptor-Prolactin receptor complex

Molecular Endocrinology

Volumn 25, Issue 4, 2011, Pages 597-610

  Xu, Jie ^a   Zhang, Yue ^a   Berry, Philip A ^a   Jiang, Jing ^a   Lobie, Peter E ^b   Langenheim, John F ^c   Chen, Wen Y ^c   Frank, Stuart J ^d,e  

^a University of Alabama at Birmingham   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c CLEMSON UNIVERSITY   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; DIMER; ESTROGEN RECEPTOR; GROWTH HORMONE; GROWTH HORMONE ANTIBODY; GROWTH HORMONE RECEPTOR; JANUS KINASE 2; PEGVISOMANT; PROGESTERONE RECEPTOR; PROLACTIN RECEPTOR; STAT5 PROTEIN;

ARTICLE; BREAST CANCER; CANCER CELL; HORMONE ACTION; HUMAN; HUMAN CELL; LACTATION; PRIORITY JOURNAL; RECEPTOR INTRINSIC ACTIVITY; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GROWTH HORMONE; HUMANS; IMMUNOPRECIPITATION; JANUS KINASE 2; PHOSPHORYLATION; PROLACTIN; RECEPTORS, PROLACTIN; RECEPTORS, SOMATOTROPIN; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

MAMMALIA; VERTEBRATA;

EID: 79953754929     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0255     Document Type: Article

References (63)

1. Isaksson OG, Edén S, Jansson JO 1985 Mode of action of pituitary growth hormone on target cells. Annu Rev Physiol 47:483-499
2. Kaplan S 1999 Hormonal regulation of growth and metabolic effects of growth hormone. In: Kostyo JL, Goodman HM, eds. Handbook of physiology. Chap 5, New York: Oxford University Press; 129-143
3. Bazan JF 1990 Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sci USA 87:6934-6938
4. Frank SJ, Messina JL 2002 Growth hormone receptor. In: Oppenheim JJ, Feldman M, eds. Cytokine reference on-line. London: Academic Press, Harcourt; 1-21
5. Mertani HC, Garcia-Caballero T, Lambert A, Gérard F, Palayer C, Boutin JM, Vonderhaar BK, Waters MJ, Lobie PE, Morel G 1998 Cellular expression of growth hormone and prolactin receptors in human breast disorders. Int J Cancer 79:202-211
6. Gallego MI, Binart N, Robinson GW, Okagaki R, Coschigano KT, Perry J, Kopchick JJ, Oka T, Kelly PA, Hennighausen L 2001 Pro-lactin, growth hormone, and epidermal growth factor activate Stat5 in different compartments of mammary tissue and exert different and overlapping developmental effects. Dev Biol 229:163-175
7. Perry JK, Mohankumar KM, Emerald BS, Mertani HC, Lobie PE 2008 The contribution of growth hormone to mammary neoplasia. J Mammary Gland Biol 13:131-145
8. Mol JA, van Garderen E, Selman PJ, Wolfswinkel J, Rijinberk A, Rutteman GR 1995 Growth hormone mRNA in mammary gland tumors of dogs and cats. J Clin Invest 95:2028-2034
9. Raccurt M, Lobie PE, Moudilou E, Garcia-Caballero T, Frappart L, Morel G, Mertani HC 2002 High stromal and epithelial human gh gene expression is associated with proliferative disorders of the mammary gland. J Endocrinol 175:307-318
10. Pandey V, Perry JK, Mohankumar KM, Kong XJ, Liu SM, Wu ZS, Mitchell MD, Zhu T, Lobie PE 2008 Autocrine human growth hormone stimulates oncogenicity of endometrial carcinoma cells. Endocrinology 149:3909-3919
11. Swanson SM, Unterman TG 2002 The growth hormone-deficient spontaneous dwarf rat is resistant to chemically induced mammary carcinogenesis. Carcinogenesis 23:977-982
12. Shen Q, Lantvit DD, Lin Q, Li Y, Christov K, Wang Z, Unterman TG, Mehta RG, Swanson SM 2007 Advanced rat mammary cancers are growth hormone dependent. Endocrinology 148:4536-4544
13. Wang Z, Prins GS, Coschigano KT, Kopchick JJ, Green JE, Ray VH, Hedayat S, Christov KT, Unterman TG, Swanson SM 2005 Disruption of growth hormone signaling retards early stages of prostate carcinogenesis in the C3(1)/T antigen mouse. Endocrinology 146:5188-5196
14. Wang Z, Luque RM, Kineman RD, Ray VH, Christov KT, Lantvit DD, Shirai T, Hedayat S, Unterman TG, Bosland MC, Prins GS, Swanson SM 2008 Disruption of growth hormone signaling retards prostate carcinogenesis in the probasin/TAg rat. Endocrinology 149:1366-1376
15. Carter Su C, Schwartz J, Smit LS 1996 Molecular mechanism of growth hormone action. Annu Rev Physiol 58:187-207
16. Gent J, van Kerkhof P, Roza M, Bu G, Strous GJ 2002 Ligandindependent growth hormone receptor dimerization occurs in the endoplasmic reticulum and is required for ubiquitin system-dependent endocytosis. Proc Natl Acad Sci USA 99:9858-9863
17. Frank SJ 2002 Receptor dimerization in GH and erythropoietin action-it takes two to tango, but how? Endocrinology 143:2-10
18. Brown RJ, Adams JJ, Pelekanos RA, Wan Y, McKinstry WJ, Palethorpe K, Seeber RM, Monks TA, Eidne KA, Parker MW, Waters MJ 2005 Model for growth hormone receptor activation based on subunit rotation within a receptor dimer. Nat Struct Mol Biol 12:814-821
19. Yang N, Wang X, Jiang J, Frank SJ 2007 Role of the growth hormone (GH) receptor transmembrane domain in receptor predimerization and GH-induced activation. Mol Endocrinol 21: 1642-1655
20. Frank SJ, Gilliland G, Van Epps C 1994 Treatment of IM-9 cells with human growth hormone (GH) promotes rapid disulfide linkage of the GH receptor. Endocrinology 135:148-156
21. Zhang Y, Jiang J, Kopchick JJ, Frank SJ 1999 Disulfide linkage of growth hormone (GH) receptors (GHR) reflects GH-induced GHR dimerization. Association of JAK2 with the GHR is enhanced by receptor dimerization. J Biol Chem 274:33072-33084
22. Yang N, Langenheim JF, Wang X, Jiang J, Chen WY, Frank SJ 2008 Activation of growth hormone receptors by growth hormone and growth hormone antagonist dimers: insights into receptor triggering. Mol Endocrinol 22:978-988
23. Jiang J, Wang X, He K, Li X, Chen C, Sayeski PP, Waters MJ, Frank SJ 2004 A conformationally-sensitiveGHR(growth hormone (GH) receptor) antibody: impact on GH signaling and GHR proteolysis. Mol Endocrinol 18:2981-2996
24. Reynolds C, Montone KT, Powell CM, Tomaszewski JE, Clevenger CV 1997 Expression of prolactin and its receptor in human breast carcinoma. Endocrinology 138:5555-5560
25. Ginsburg E, Vonderhaar BK 1995 Prolactin synthesis and secretion by human breast cancer cells. Cancer Res 55:2591-2595
26. Boutin JM, Edery M, Shirota M, Jolicoeur C, Lesueur L, Ali S, Gould D, Djiane J, Kelly PA 1989 Identification of a cDNA encoding a long form of prolactin receptor in human hepatoma and breast cancer cells. Mol Endocrinol 3:1455-1461
27. Goffin V, Binart N, Touraine P, Kelly PA 2002 Prolactin: the new biology of an old hormone. Annu Rev Physiol 64:47-67
28. Rui H 2000 Prolactin. In: Oppenheim JJ, Feldman M, eds. Cytokine reference on-line. London: Academic Press, Harcourt; 267-283
29. Clevenger CV, Furth PA, Hankinson SE, Schuler LA 2003 The role of prolactin in mammary carcinoma. Endocr Rev 24:1-27
30. Goffin V, Touraine P, Pichard C, Bernichtein S, Kelly PA 1999 Should prolactin be reconsidered as a therapeutic target in human breast cancer? Mol Cell Endocrinol 151:79-87
31. Vonderhaar BK 1999 Prolactin involvement in breast cancer. Endocr Relat Cancer 6:389-404
32. Campbell GS, Argetsinger LS, Ihle JN, Kelly PA, Rillema JA, Carter- Su C 1994 Activation of JAK2 tyrosine kinase by prolactin receptors in Nb2 cells and mouse mammary gland explants. Proc Natl Acad Sci USA 91:5232-5236
33. Rui H, Kirken RA, Farrar WL 1994 Activation of receptor-associated tyrosine kinase JAK2 by prolactin. J Biol Chem 269:5364-5368
34. Clevenger CV, Kline JB 2001 Prolactin receptor signal transduction. Lupus 10:706-718
35. Huang Y, Li X, Jiang J, Frank SJ 2006 Prolactin modulates phosphorylation, signaling and trafficking of epidermal growth factor receptor in human T47D breast cancer cells. Oncogene 25:7565-7576
36. Hughes JP, Friesen HG 1985 The nature and regulation of the receptors for pituitary growth hormone. Annu Rev Physiol 47:469-482
37. Cunningham BC, Bass S, Fuh G, Wells JA 1990 Zinc mediation of the binding of human growth hormone to the human prolactin receptor. Science 250:1709-1712
38. Somers W, Ultsch M, De Vos AM, Kossiakoff AA 1994 The x-ray structure of a growth hormone-prolactin receptor complex. Nature 372:478-481
39. Fu YK, Arkins S, Fuh G, Cunningham BC, Wells JA, Fong S, Cronin MJ, Dantzer R, Kelley KW 1992 Growth hormone augments superoxide anion secretion of human neutrophils by binding to the prolactin receptor. J Clin Invest 89:451-457
40. Gadd SL, Clevenger CV 2006 Ligand-independent dimerization of the human prolactin receptor isoforms: functional implications. Mol Endocrinol 20:2734-2746
41. Qazi AM, Tsai-Morris CH, Dufau ML 2006 Ligand-independent homo- and heterodimerization of human prolactin receptor variants: inhibitory action of the short forms by heterodimerization. Mol Endocrinol 20:1912-1923
42. Langenheim JF, Chen W Y 2009 Development of a novel ligand that activates JAK2/STAT5 signaling through a heterodimer of prolactin receptor and growth hormone receptor. J Recept Signal Transduct Res 29:107-112
43. Biener E, Martin C, Daniel N, Frank SJ, Centonze VE, Herman B, Djiane J, Gertler A 2003 Ovine placental lactogen-induced heterodimerization of ovine growth hormone and prolactin receptors in living cells is demonstrated by fluorescence resonance energy transfer microscopy and leads to prolonged phosphorylation of signal transducer and activator of transcription (STAT)1 and STAT3. Endocrinology 144:3532-3540
44. Herman A, Bignon C, Daniel N, Grosclaude J, Gertler A, Djiane J 2000 Functional heterodimerization of prolactin and growth hormone receptors by ovine placental lactogen. J Biol Chem 275:6295-6301
45. Zhang Y, Guan R, Jiang J, Kopchick JJ, Black RA, Baumann G, Frank SJ 2001 Growth hormone (GH)-induced dimerization inhibits phorbol ester-stimulated GH receptor proteolysis. J Biol Chem 276:24565-24573
46. Goldsmith JF, Lee SJ, Jiang J, Frank SJ 1997 Growth hormone induces detergent insolubility of GH receptors in IM-9 cells. The American journal of physiology 273:E932-E941
47. Loesch K, Deng L, Cowan JW, Wang X, He K, Jiang J, Black RA, Frank SJ 2006 JAK2 influences growth hormone receptor metalloproteolysis. Endocrinology 147:2839-2849
48. Cunningham BC, Wells JA 1991 Rational design of receptor-specific variants of human growth hormone. Proc Natl Acad Sci USA 88:3407-3411
49. Goffin V, Bernichtein S, Carrière O, Bennett WF, Kopchick JJ, Kelly PA 1999 The human growth hormone antagonist B2036 does not interact with the prolactin receptor. Endocrinology 140:3853-3856
50. Peirce SK, Chen WY 2001 Quantification of prolactin receptor mRNA in multiple human tissues and cancer cell lines by real time RT-PCR. J Endocrinol 171:R1-R4
51. Goffin V, Bernichtein S, Touraine P, Kelly PA 2005 Development and potential clinical uses of human prolactin receptor antagonists. Endocr Rev 26:400-422
52. de Vos AM, Ultsch M, Kossiakoff AA 1992 Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science 255:306-312
53. Cunningham BC, Ultsch M, De Vos AM, Mulkerrin MG, Clauser KR, Wells JA 1991 Dimerization of the extracellular domain of the human growth hormone receptor by a single hormone molecule. Science 254:821-825
54. Fuh G, Cunningham BC, Fukunaga R, Nagata S, Goeddel DV, Wells JA 1992 Rational design of potent antagonists to the human growth hormone receptor. Science 256:1677-1680
55. Livnah O, Stura EA, Middleton SA, Johnson DL, Jolliffe LK, Wilson IA 1999 Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation. Science 283:987-990
56. Remy I, Wilson IA, Michnick SW 1999 Erythropoietin receptor activation by a ligand-induced conformation change. Science 283: 990-993
57. Tallet E, Rouet V, Jomain JB, Kelly PA, Bernichtein S, Goffin V 2008 Rational design of competitive prolactin/growth hormone receptor antagonists. J Mammary Gland Biol 13:105-117
58. Kleinberg DL, Wood TL, Furth PA, Lee AV 2009 Growth hormone and insulin-like growth factor-I in the transition from normal mammary development to preneoplastic mammary lesions. Endocr Rev 30:51-74
59. Gan Y, Zhang Y, Digirolamo DJ, Jiang J, Wang X, Cao X, Zinn KR, Carbone DP, Clemens TL, Frank SJ 2010 Deletion of IGF-I receptor (IGF-IR) in primary osteoblasts reduces GH-induced STAT5 signaling. Mol Endocrinol 24:644-656
60. Huang Y, Kim SO, Yang N, Jiang J, Frank SJ 2004 Physical and functional interaction of GH and IGF-1 signaling elements. Mol Endocrinol 18:1471-1485
61. Yamauchi T, Ueki K, Tobe K, Tamemoto H, Sekine N, Wada M, Honjo M, Takahashi M, Takahashi T, Hirai H, Tushima T, Akanuma Y, Fujita T, Komuro I, Yazaki Y, Kadowaki T 1997 Tyrosine phosphorylation of the EGF receptor by the kinase Jak2 is induced by growth hormone. Nature 390:91-96
62. Muller AF, Kopchick JJ, Flyvbjerg A, van der Lely AJ 2004 Clinical review 166: growth hormone receptor antagonists. J Clin Endocrinol Metab 89:1503-1511
63. Jiang J, Liang L, Kim SO, Zhang Y, Mandler R, Frank SJ 1998 Growth hormone-dependent tyrosine phosphorylation of a GH receptor-associated high molecular weight protein immunologically related to JAK2. Biochem Biophys Res Commun 253:774-779