The mitogenic potential of heparin-binding epidermal growth factor in the human endometrium is mediated by the epidermal growth factor receptor and is modulated by tumor necrosis factor-α

Journal of Clinical Endocrinology and Metabolism

Volumn 87, Issue 12, 2002, Pages 5769-5777

  Chobotova, Katya ^a   Muchmore, Mary Elizabeth ^a   Carver, Janet ^a   Yoo, Hyung J ^a   Manek, Sanjiv ^a   Gullick, William J ^b   Barlow, David H ^a   Mardon, Helen J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF KENT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETACELLULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; AUTOCRINE EFFECT; CELL MATURATION; CELL REGENERATION; DNA SYNTHESIS; ENDOMETRIUM CANCER; ENDOMETRIUM CELL; HUMAN; HUMAN TISSUE; MENSTRUAL CYCLE; MITOGENESIS; NIDATION; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADULT; CELLS, CULTURED; DNA; ENDOMETRIUM; EPIDERMAL GROWTH FACTOR; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MENSTRUAL CYCLE; MIDDLE AGED; MITOGENS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SOLUBILITY; STROMAL CELLS; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0036930148     PISSN: 0021972X     EISSN: None     Source Type: Journal    
DOI: 10.1210/jc.2002-020069     Document Type: Article

References (58)

1. Higashiyama S, Abraham JA, Miller J, Fiddes JC, Klagsbrun M 1991 A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 251:936-939
2. Raab G, Klagsbrun M 1997 Heparin-binding EGF-like growth factor. Biochim Biophys Acta 1333:F179-199
3. Arkonac BM, Foster LC, Sibinga NE, Patterson C, Lai K, Tsai JC, Lee ME, Perrella MA, Haber E 1998 Vascular endothelial growth factor induces heparin-binding epidermal growth factor-like growth factor in vascular endothelial cells [published erratum appears in J Biol Chem 1998 Apr 10;273(15): 9352]. J Biol Chem 273:4400-4405
4. Abraham JA, Damm D, Bajardi A, Miller J, Klagsbrun M, Ezekowitz RA 1993 Heparin-binding EGF-like growth factor: Characterization of rat and mouse cDNA clones, protein domain conservation across species, and transcript expression in tissues. Biochem Biophys Res Commun 190:125-133
5. Kennedy TG, Brown KD, Vaughan TJ 1994 Expression of the genes for the epidermal growth factor receptor and its ligands in porcine oviduct and endometrium. Biol Reprod 50:751-756
6. Vaughan TJ, Pascall JC, Brown KD 1992 Tissue distribution of mRNA for heparin-binding epidermal growth factor. Biochem J 287:681-684
7. Yoshizumi M, Kourembanas S, Temizer DH, Cambria RP, Quertermous T, Lee ME 1992 Tumor necrosis factor increases transcription of the heparin-binding epidermal growth factor-like growth factor gene in vascular endothelial cells. J Biol Chem 267:9467-9469
8. Yoo HJ, Barlow DH, Mardon HJ 1997 Temporal and spatial regulation of expression of heparin-binding epidermal growth factor-like growth factor in the human endometrium: A possible role in blastocyst implantation. Dev Genet 21:102-108
9. Higashiyama S, Lau K, Besner GE, Abraham JA, Klagsbrun M 1992 Structure of heparin-binding EGF-like growth factor. Multiple forms, primary structure, and glycosylation of the mature protein. J Biol Chem 267:6205-6212
10. Suzuki M, Raab G, Moses MA, Fernandez CA, Klagsbrun M 1997 Matrix metalloproteinase-3 releases active heparin-binding EGF-like growth factor by cleavage at a specific juxtamembrane site. J Biol Chem 272:31730-31737
11. Izumi Y, Hirata M, Hasuwa H, Iwamoto R, Umata T, Miyado K, Tamai Y, Kurisaki T, Sehara Fujisawa A, Ohno S, Mekada E 1998 A metalloprotease-disintegrin, MDC9/meltrin-γ/ADAM9 and PKCδ are involved in TPA-induced ectodomain shedding of membrane-anchored heparin-binding EGF-like growth factor. EMBO J 17:7260-7272
12. Goishi K, Higashiyama S, Klagsbrun M, Nakano N, Umata T, Ishikawa M, Mekada E, Taniguchi N 1995 Phorbol ester induces the rapid processing of cell surface heparin-binding EGF-like growth factor: Conversion from juxtacrine to paracrine growth factor activity. Mol Biol Cell 6:967-980
13. Aviezer D, Yayon A 1994 Heparin-dependent binding and autophosphorylation of epidermal growth factor (EGF) receptor by heparin-binding EGF-like growth factor but not by EGF. Proc Natl Acad Sci USA 91:12173-12177
14. Elenius K, Paul S, Allison G, Sun J, Klagsbrun M 1997 Activation of HER4 by heparin-binding EGE-like growth factor stimulates chemotaxis but not proliferation. EMBO J 16:1268-1278
15. Zhang Z, Funk C, Glasser SR, Mulholland J 1994 Progesterone regulation of heparin-binding epidermal growth factor-like growth factor gene expression during sensitization and decidualization in the rat uterus: Effects of the antiprogestin, ZK 98.299. Endocrinology 135:1256-1263
16. Das SK, Wang XN, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK 1994 Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: A possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 120:1071-1083
17. Raab G, Kover K, Paria BC, Dey SK, Ezzell RM, Klagsbrun M 1996 Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of hepartn-binding EGF-like growth factor. Development 122:637-645
18. Paria BC, Elenius K, Klagsbrun M, Dey SK 1999 Heparin-binding EGF-like growth factor interacts with mouse blastocysts independently of ErbB1: A possible role for heparan sulfate proteoglycans and ErbB4 in blastocyst implantation. Development 126:1997-2005
19. Leach RE, Khalifa R, Armant DR, Brudney A, Das SK, Dey SK, Fazleabas AT 2001 Heparin-binding EGF-like growth factor modulation by antiprogestin and CG in the baboon (Papio anubis). J Clin Endocrinol Metab 86:4520-4528
20. Birdsall MA, Hopkisson JF, Grant KE, Barlow DH, Mardon HJ 1996 Expression of heparin-binding epidermal growth factor messenger RNA in the human endometrium. Mol Hum Reprod 2:31-34
21. Leach RE, Khalifa R, Ramirez ND, Das SK, Wang J, Dey SK, Romero R, Armant DR 1999 Multiple roles for heparin-binding epidermal growth factor-like growth factor are suggested by its cell-specific expression during the human endometrial cycle and early placentation. J Clin Endocrinol Metab 84:3355-3363
22. Niikura H, Sasano H, Kaga K, Sato S, Yajima A 1996 Expression of epidermal growth factor family proteins and epidermal growth factor receptor in human endometrium. Hum Pathol 27:282-289
23. Moiler B, Rasmussen C, Lindbloom B, Olovsson M 2001 Expression of the angiogenic growth factors VEGF, FGF-2, EGF and their receptors in normal human endometrium during the menstrual cycle. Mol Hum Reproduction 7:65-72
24. Srinivasan R, Benton E, McCormick F, Thomas H, Gullick W 1999 Expression of the c-erbB-3/HER-3 and c-erbB-4/HER-4 growth factor receptors and their ligands, neuregulin-1α, neuregulin-1β, and betacellulin, in normal endometrium and endometrial cancer. Clin Cancer Res 5:2877-2883
25. Martin KL, Barlow DH, Sargent IL 1998 Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum Reprod 13:1645-1652
26. Hunt JS, Chen HL, Hu XL, Tabibzadeh S 1992 Tumor necrosis factor-α messenger ribonucleic acid and protein in human endometrium. Biol Reprod 47:141-147
27. Philippeaux MM, Piguet PF 1993 Expression of tumor necrosis factor-α and its mRNA in the endometrial mucose during the menstrual cycle. Am J Pathol 143:480-486
28. Tabibzadeh S, Zupi E, Babakina A, Liu R, Marconi D, Romanini C 1995 Site and menstrual cycle-dependent expression of proteins of the tumor necrosis factor (TNF) receptor family, and BCL-2 oncoprotein and phase-specific production of TNFα in human endometrium. Hum Reprod 10:277-286
29. Tabibzadeh S, Kong QF, Satyaswaroop PG, Zupi E, Marconi D, Romanini C, Kapur S 1994 Distinct regional and menstrual cycle dependent distribution of apoptosis in human endometrium. Potential regulatory role of T cells and TNFα Endocr J 2:87-95
30. Noyes RW, Hertig AT, Rock J 1950 Dating the endometrial biopsy. Fertil Steril 1:3-25
31. Biddolph S, Jones M 1999 Low temperature, heat-mediated antigen retrival (LTHMAR) on archival endometrial sections. Appl Immunohistochem Mol Morphol 7:289-293
32. Fernandez-Shaw S, Shorter SC, Naish CE, Barlow DH, Starkey PM 1992 Isolation and purification of human endometrial stromal and glandular cells using immuno-magnetic microspheres. Hum Reprod 7:156-161
33. 1 binding via stabilization of the ninth FIII domain. J Biol Chem 276:38885-38892
34. Srinivasan R, Poulsom R, Hurst HC, Gullick WJ 1998 Expression of the c-erbB-4/HER4 protein and mRNA in normal human fetal and adult tissues and in a survey of nine solid tumour types. J Pathol 185:236-245
35. Simmons DC 1993 Cloning cell surface molecules by transient expression in mammalian cells. In: Hartley DA, ed. Cellular Interaction in Development: A Practical Approach. Oxford: IRL Press; 93-127
36. Takemura T, Kondo S, Homma T, Sakai M, Harris RC 1997 The membrane-bound form of heparin-binding epidermal growth factor-like growth factor promotes survival of cultured renal epithelial cells. J Biol Chem 272:31036-33042
37. Gechtman Z, Alonso JL, Raab G, Ingber DE, Klagsbrun M 1999 The shedding of membrane-anchored heparin-binding epidermal-like growth factor is regulated by the Raf/mitogen-activated protein kinase cascade and by cell adhesion and spreading. J Biol Chem 274:28828-28835
38. Cross JC, Werb Z, Fisher S 1994 Implantation and the placenta: Key pieces of the development puzzle. Science 266:1508-1518
39. Kane MT, Morgan PM, Coonan C 1997 Peptide growth factors and preimplantation development. Hum Reprod Update 3:137-157
40. Hammond MG, Oh ST, Anners J, Surrey ES, Halme J 1993 The effect of growth factors on the proliferation of human endometrial stromal cells in culture. Am J Obstet Gynecol 168:1131-1138
41. Haining RE, Cameron IT, van Papendorp C, Davenport AP, Prentice A, Thomas EJ, Smith SK 1991 Epidermal growth factor in human endometrium: Proliferative effects in culture and immunocytochemical localization in normal and endometriotic tissues. Hum Reprod 6:1200-1205
42. Zhang Z, Funk C, Roy D, Glasser S, Mulholland J 1994 Heparin-binding epidermal growth factor-like growth factor is differentially regulated by progesterone and estradiol in rat uterine epithelial and stromal cells. Endocrinology 134:1089-1094
43. Iwamoto R, Higashiyama S, Mitamura T, Taniguchi N, Klagsbrun M, Mekada E 1994 Heparin-binding EGF-like growth factor, which acts as the diphtheria toxin receptor, forms a complex with membrane protein DRAP27/ CD9, which up-regulates functional receptors and diphtheria toxin sensitivity. EMBO J 13:2322-2330
44. 1 at cell-cell contact sites. J Cell Biol 129:1691-1705
45. Berchuck A, Soisson AP, Olt GJ, Soper JT, Clarke-Pearson DL, Bast RCJ, McCarty KSJ 1989 Epidermal growth factor receptor expression in normal and malignant endometrium. Am J Obstet Gynecol 161:1247-1252
46. Fry DW, Kraker AJ, McMichael A, Ambroso LA, Nelson JM, Leopold WR, Connors RW, Bridges AJ 1994 A specific inhibitor of epidermal growth factor receptor tyrosine kinase. Science 265:1093-1095
47. Schroeder JA, Lee DC 1998 Dynamic expression and activation of ErbB receptors in the developing mouse mammary gland. Cell Growth Differ 9:451-464
48. Russell KS, Stern DF, Polverini PJ, Bender JR 1999 Neuregulin activation of ErbB receptors in vascular endothelium leads to angiogenesis. Am J Physiol 277:H2205-H2211
49. Ni C-Y, Murphy MP, Glode TE, Carpenter G 2001 γ-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294:2179-2181
50. Tabibzadeh S 1995 Signals and molecular pathways involved in apoptosis, with special emphasis on human endometrium. Hum Reprod Update 1:303-323
51. Tabibzadeh S 1996 The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod 2:77-92
52. Aggarwal BB, Natarajan K 1996 Tumor necrosis factors: Developments during the last decade. Eur Cytokine Network 7:93-124
53. Perez M, Donato NJ 1996 Activation of epidermal growth factor receptor tyrosine phosphorylation by tumor necrosis factor correlates with loss of cytotoxic activity. J Interferon Cytokine Res 16:307-314
54. Donato NJ, Ince C, Rosenblum M, Gallick G 1989 Early events in the anti-proliferative action of tumor necrosis factor are similar to the early events in epidermal growth factor stimulation. J Cell Biochem 41:139-157
55. Bird TA, Saklatvala J 1990 Down-modulation of epidermal growth factor receptor affinity in fibroblasts treated with interleukin 1 or tumor necrosis factor is associated with phosphorylation at a site other than threonine 654. J Biol Chem 265:235-240
56. Imai T, Kurachi H, Adachi K, Adachi H, Yoshimoto Y, Homma H, Tadokoro C, Takeda S, Yamaguchi M, Sakata M, Sakoyama Y, Miyake A 1995 Changes in epidermal growth factor receptor and the levels of its ligands during menstrual cycle in human endometrium. Biol Reprod 52:928-938
57. Adachi K, Belser P, Bender H, Li D, Rodeck U, Benveniste EN, Woo D, Schmiegel WH, Herlyn D 1992 Enhancement of epidermal growth factor receptor expression on glioma cells by recombinant tumor necrosis factor α. Cancer Immunol Immunother 34:370-376
58. Kalthoff H, Roeder C, Gieseking J, Humburg I, Schmiegel W 1993 Inverse regulation of human ERBB2 and epidermal growth factor receptors by tumor necrosis factor α. Proc Natl Acad Sci USA 90:8972-8976