Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor

Development

Volumn 122, Issue 2, 1996, Pages 637-645

  Raab, Gerhard ^a   Kover, Karen ^b   Paria, Bibhash C ^b   Dey, Sudhansu K ^b   Ezzell, Robert M ^c   Klagsbrun, Michael ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

EGF receptor; Heparan sulfate proteoglycan; Juxtacrine growth factor; Mouse; TGF

Indexed keywords

CELL ADHESION MOLECULE; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR; HEPARIN BINDING PROTEIN; HEPARIN LYASE; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL ADHESION; CONTROLLED STUDY; FEMALE; MOUSE; NIDATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BASE SEQUENCE; BLASTOCYST; CELL ADHESION; CELL COMMUNICATION; CELL LINE; COCULTURE TECHNIQUES; DNA PRIMERS; EPIDERMAL GROWTH FACTOR; FEMALE; GENE EXPRESSION; GESTATIONAL AGE; HEPARIN; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PREGNANCY; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; RNA, MESSENGER; TRANSFECTION; UTERUS;

EID: 0030058026     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Adamson, E. D. (1993). Activities of growth factors in preimplantation embryos. J. Cell. Biochem. 53, 280-287.
2. Anklesaria, P., Teixido, J., Laiho, M., Pierce, J. H., Greenberger, J. S., and Massague, J. (1990). Cell-cell adhesion mediated by binding of membrane-anchored transforming growth factor-a to epidermal growth factor receptors promotes cell proliferation. Proc. Natl. Acad. Sci. USA 87, 3289-3293.
3. Baird, A. and Klagsbrun, M. (1991). A dual receptor system is required for basic fibroblast growth factor activity. Cell 67, 229-231.
4. Besner, G., Higashiyama, S. and Klagsbrun, M. (1990). Isolation and characterization of a macrophage-derived heparin-binding growth factor. Cell Reg. 1, 811-819.
5. Bhatt, H., Brunet, L. J. and Stewart, C. L. (1991). Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc. Natl. Acad. Sci. USA 88, 11408-11412.
6. Blotnick, S., Peoples, G. E., Freeman, M. R., Eberlein, T. J. and Klagsbrun, M. (1994). T lymphocytes synthesize and export heparin-binding epidermal growth factor-like growth factor and basic fibroblast growth factor, mitogens for vascular cells and fibroblasts: differential production and release by CD4+ and CD8+ T cells. Proc. Natl. Acad. Sci USA 91, 2890-2894.
7. Brachmann, R., Lindquist, P. B., Nagashima, M., Kohr, W., Lipari, T., Napier, M. and Derynck, R. (1989). Transmembrane TGF-α precursors activate EGF/TGF-α receptors. Cell 56, 691-700
8. Carpenter, G. and Wahl, M. I. (1990). The epidermal growth factor family. In Peptide Growth Factors and Their Receptors 1, (ed. M B Sporn and A.B. Roberts), pp. 69-171. New York: Springer-Verlag
9. Carson, D. D., Tang, J. P. and Julian, J. (1993). Heparan sulfate proteoglycan (perlecan) expression by mouse embryos during acquisition of attachment competence. Dev. Biol. 155, 97-106.
10. Carson, D. D., Rohde, L. H. and Surveyor, G. (1994). Cell surface glycoconjugates as modulators of embryo attachment to uterine epithelial cells. Int. J. Biochem. 26, 1269-1277.
11. Chavez, D. J. (1986). Cell surface of mouse blastocysts at the trophectodermuterine interface during the adhesive stage of implantation. Am. J. Anat. 176, 153-158.
12. Chen, X., Raab, G., Deutsch, U., Zhang, J., Ezzel, R. and Klagsbrun, M. (1995). Induction of heparin-binding EGF-like growth factor expression during myogenesis: Activation of the gene by MyoD and localization of the transmembrane form of the protein on the myotube surface J. Biol. Chem. 270, 18285-18294.
13. Cohen, T., Gitay-Goren, H., Sharon, R., Shibuya, M., Halaban, R., Levi, B. Z. and Neufeld, G. (1995). VEGF121, a vascular endothelial growth factor (VEGF) isoform lacking heparin binding ability, requires cell-surface heparan sulfates for efficient binding to the VEGF receptors of human melanoma cells. J. Biol. Chem. 270, 11322-11326.
14. Cross, J. C., Werb, Z. and Fisher, S. J. (1994). Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508-1518.
15. Dardik, A., Smith, R. M. and Schultz, R. M. (1992). Colocalization of transforming growth factor-α and a functional epidermal growth factor receptor (EGFR) to the inner cell mass and preferential localization of the EGFR on the basolateral surface of the trophectoderm in the mouse blastocyst. Dev. Biol. 154, 396-409.
16. Das, S. K., Wang, X. N., Paria, B. C., Damm, D., Abraham, J. A., Klagsbrun, M., Andrews, G. K. and Dey, S. K. (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. Denker, H. W. (1993). Implantation: a cell biological paradox. J. Exp. Zoo. 266, 541-58.
18. Enders, A. C., Schlafke, S., Hubbard, N. E. and Mead, R. A. (1986). Morphological changes in the blastocyst of the western spotted skunk during activation from delayed implantation. Biol. Reprod. 34, 423-437.
19. Farach, M. C., Tang, J. P., Decker, G. L. and Carson, D. D. (1987). Heparin/heparan sulfate is involved in attachment and spreading of mouse embryos in vitro. Dev. Biol. 123, 407-410.
20. Flanagan, J. G. and Leder, P. (1990). The kit ligand: a cell surface molecule altered in steel mutant fibroblasts. Cell 63, 185-194.
21. Goishi, K., Higashiyama, S., Klagsbrun, M., Nakano, N., Umata, T., Ishikawa, M., Mekada, E. and 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
22. Graham, C. H. and Lala, P. K. (1988). Mechanisms of placental invasion of the uterus and their control. J. Cell Biol. 107, 867-874.
23. Haimovici, F. and Anderson, D. J. (1993). Effects of growth factors and growth factor-extracellular matrix interactions on mouse trophoblast outgrowth in vitro. Biol. Reprod. 49, 124-130
24. Higashiyama, S., Abraham, J. A., Miller, J., Fiddes, J. C. and Klagsbrun, M. (1991). A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 251, 936-939.
25. Higashiyama, S., Lau, K., Besner, G. E., Abraham, J. A. and 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.
26. Higashiyama, S., Abraham, J. A. and Klagsbrun, M. (1993). Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate. J. Cell Biol. 122, 933-940.
27. Higashiyama, S., Iwamoto, R., Goishi, K., Raab, G., Taniguchi, N., Klagsbrun, M. and Mekada, E. (1995). The membrane protein CD9/DRAP 27 potentiates the juxtacrine growth factor activity of the membrane-anchored heparin-binding EGF-like growth factor. J. Cell Biol 128, 929-938.
28. Hou, Q. and Gorski, J. (1993). Estrogen receptor and progesterone receptor genes are expressed differentially in mouse embryos during preimplantation development. Proc. Natl. Acad. Sci. USA 90, 9460-9464.
29. Huet-Hudson, Y. M., Andrews, G. K. and Dey, S. K. (1990) Epidermal growth factor and pregnancy in the mouse. In Early Embryo Development and Paracrine Relationships Vol. 117. (ed. S. Heyner and L. M. Wiley). pp. 125-136. New York: Wiley-Liss
30. Huet-Hudson, Y. M. and Dey, S. K. (1990). Requirement for progesterone priming and its long-term effects on implantation in the mouse. Proc Soc. Exp. Biol. Med. 193, 259-263.
31. Hynes, N.E. and Stern, D.F. (1994). The biology of erbB-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta 1198, 165-184
32. Jacobs, A. L. and Carson, D. D. (1991). Proteoglycan synthesis and metabolism by mouse uterine stroma cultured in vitro. J. Biol. Chem. 266, 15464-15473.
33. Kimber, S. J., Bentley, J., Ciemerych, M., Moller, C. J. and Bock, E. (1994). Expression of N-CAM in fertilized pre- and periimplantation and parthenogenetically activated mouse embryos. Eur. J. Cell Biol 63, 102-113.
34. Kraus, M. H., Issing, W., Miki, T., Popescu, N. C. and Aaronson, S. A. (1989) Isolation and characterization of ERBB3, a third member of the ERBB/epidermal growth factor receptor family: evidence for overexpression in a subset of human mammary tumors. Proc. Natl. Acad. Sci. USA 86, 9193-9197
35. Lee, D.C., Rose, T.M., Webb, N.R. and Todaro G.J. (1985). Cloning and sequence analysis of a cDNA for rat transforming growth factor-α. Nature 313. 489-491
36. Luetteke, N. C., Qiu, T. H., Peiffer, R. L., Oliver, P., Smithies, O. and Lee, D. C. (1993). TGF-α deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell 73, 263-278.
37. Mann, G. B., Fowler, K. J., Gabriel, A., Nice, E. C., Williams, R. L. and Dunn, A. R. (1993). Mice with a null mutation of the TGF-α gene have abnormal skin architecture, wavy hair, and curly whiskers and often develop corneal inflammation. Cell 73, 249-261.
38. Marikovsky, M., Breuing, K., Liu, P. Y., Eriksson, E., Higashiyama, S., Farber, P., Abraham, J. and Klagsbrun, M. (1993). Appearance of heparin-binding EGF-like growth factor in wound fluid as a response to injury. Proc. Natl. Acad. Sci. USA 90, 3889-3893.
39. McCormack, J. T. and Greenwald, G. S. (1974). Evidence for a preimplantation rise in oestradiol-17β levels on day 4 of pregnancy in the mouse. J Reprad Fertil. 41, 297-301.
40. Miettinen, P. J., Berger, J. E., Meneses, J., Phung, Y., Pedersen, R. A., Werb, Z. and Derynck, R. (1995). Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376, 337-341
41. Naglich, J. G., Metherall, J. E., Russell, D. W. and Eidels, L. (1992). Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor. Cell 69, 1051-1061.
42. Ono, M., Raab, G., Lau, K., Abraham, J. and Klagsbrun, M. (1994). Purification and characterization of transmembrane forms of heparin-binding epidermal growth factor-like growth factor. J. Biol. Chem 269 31315-31321.
43. Paria, B. C. and Dey, S. K. (1990). Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc. Natl. Acad. Sci. USA 87, 4756-4760.
44. Paria, B. C., Das, S. K., Andrews, G. K. and Dey, S. K. (1993a). Expression of the epidermal growth factor receptor gene is regulated in mouse blasiocysts during delayed implantation. Proc. Natl. Acad. Sci. USA 90, 55-59.
45. Paria, B. C., Huet-Hudson, Y. M. and Dey, S. K. (1993b). Blastocyst's state of activity determines the 'window' of implantation in the receptive mouse uterus Proc Natl. Acad. Sci. USA 90, 10159-10162.
46. Paria, B. C., Das, S. K., Huet-Hudson, Y. M. and Dey, S. K. (1994). Distribution of transforming growth factor-α precursors in the mouse uterus during the periimplantation period and after steroid hormone treatments. Biol Reprod. 50, 481-491.
47. Pierce, J. H., Ruggiero, M., Fleming, T. P., DI Fiore, P. P., Greenberger, J. S., Varticovsky, L., Schlessinger, J., Rovera, G. and Aaronson, S. A. (1988). Signal transduction through the EGF receptor transfected in IL-3-dependent hematopoetic cells. Science 239, 628-631.
48. Plowman, G. D., Culouscou, J. M., Whitney, G. S., Green, J. M., Carlton, G. W., Foy, L., Neubauer, M. G. and Shoyab, M. (1993). Ligand-specific activation of HER4/p 180erbB4. a fourth member of the epidermal growth factor receptor family Proc. Natl. Acad. Sci. USA 90, 1746-1750.
49. Raab, G., Higashiyama, S., Hetelekidis, S., Abraham, J., Damm, D., Onu, M. and Klagsbrun, M. (1994). Biosynthesis and processing by phorbol ester of the cell surface-associated precursor form of heparin-binding EGF-like growth factor Biochem. Biophys. Res. Commun. 204, 592-597.
50. Raboudi, N., Julian, J., Ronde, L. H. and Carson, D. D. (1992). Identification of cell-surface heparin/heparan sulfate-binding proteins of a human uterine epithelial cell line (RL95). J. Biol Chem 267, 11930-11939.
51. Schlafke, S. and Enders, A. C. (1975). Cellular basis of interactions between trophoblast and uterus at implantation. Biol. Reprod. 12, 41-65.
52. Sibilia, M. and Wagner, E. F. (1995). Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269, 234-238.
53. Smith, S. E., French, M., Julian, J., Paria, B. C., Dey, S. K. and Carson, D. D. (1995). Gene expression of a heparan sulfate proteoglycan (perlecan) in mouse embryos at the time of attachment competence. Biol. Reprod. 52 (suppl. 1), Abst. 148.
54. Stewart, C. L., Kaspar, P., Brunet, L. J., Bhatt, H., Gadi, I., Kontgen, F. and Abbondanzo, S. J. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76-79.
55. Sutherland, A. E., Calarco, P. G. and Damsky, C. H. (1988). Expression and function of cell surface extracellular matrix receptors in mouse blastocyst attachment and outgrowth. J. Cell Biol. 106, 1331-1348.
56. Sutherland, A. E., Sanderson, R. D., Mayes, M., Seibert, M., Calarco, P. G., Bernfield, M. and Damsky, C. H. (1991). Expression of syndecan, a putative low affinity fibroblast growth factor receptor, in the early mouse embryo Development 113, 339-351.
57. Sutherland, A. E., Calarco, P. G. and Damsky, C. H. (1993). Developmental regulation of integrin expression at the time of implantation in the mouse embryo Development 119, 1175-1186.
58. Tamada, H., McMaster, M. T., Flanders, K. C., Andrews, G. K. and Dey, S. K. (1990) Cell type-specific expression of transforming growth factor-β1 in the mouse uterus durins the implantation period. Mol. Endocrinol. 4, 965-972
59. Tamada, H., Das, S. K., Andrews, G. K. and Dey, S. K. (1991). Cell type-specific expression of transforming growth factor-α in the mouse uterus during the pen-implantation period. Biol. Reprod. 45, 365-372.
60. Thompson, S. A., Higashiyama, S., Wood, K., Pollitt, N. S., Damm, D., McEnroe, G., Garrick, B., Ashton, N., Lau, K., Hancock, N., Klagsbrun, M. and Abraham, J. A. (1994). Characterization of sequences within heparin-binding factor that mediate interaction with heparin. J. Biol. Chem. 269, 2541-2549
61. Threadgill, D. W., Dlugosz, A. A., Hansen, I., A., Tennenbaum, T., Lichti, U., Yee, D., LaMantia, C., Mourton, T., Herrup, K., Harris, R. C., A., B. J., Yuspa, S. H., J., C. R. and Magnuson, T. (1995). Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269, 230-234
62. Whitten, W. K. (1971) Nutritional requirements for the culture of preimplantation embryos in vitro. Adv. Biol. Sci. 6, 129-139.
63. Wiley, L. M., Wu, J. X., Harari, I. and Adamson, E. D. (1992). Epidermal growth factor receptor mRNA and protein increase after the four-cell preimplantation stage in murine development. Dev. Biol. 149, 247-260.
64. Wong, S. T., Winchell, L. F., McCune, B. K., Earp, H. S., Teixido, J., Massague, J., Herman, B. and Lee, D. C. (1989). The TGF-α precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction Cell 56, 495-506.
65. Wu, T. C., Wang, L. and Wan, Y. J. (1992). Expression of estrogen receptor gene in mouse oocyte and during embryogenesis. Mol Reprod. Dev. 33, 407-412.
66. Yayon, A., Ktagsbrun, M., Esko, J. D., Leder, P. and Ornitz, D. M. (1991). Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848.
67. Yoshinaga, K. and Adams, C. E. (1966). Delayed implantation in the spayed, progesterone treated adult mouse. J. Reprod Fertil. 12, 593-595.