Snail is an immediate early target gene of parathyroid hormone related peptide signaling in parietal endoderm formation

International Journal of Developmental Biology

Volumn 44, Issue 3, 2000, Pages 297-307

  Veltmaat, Jacqueline M ^b   Orelio, Claudia C ^a,b   Ward Van Oostwaard, Dorien ^b   Van Rooijen, Marga A ^b   Mummery, Christine L ^b   Defize, Libert H K ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b HUBRECHT INSTITUTE   (Netherlands)

Author keywords

F9 cells; Mouse; Parietal endoderm; PTHrP; Sna

Indexed keywords

PARATHYROID HORMONE RELATED PROTEIN;

ANIMAL CELL; ARTICLE; BLASTOCYST; CARCINOMA CELL; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONAL CARCINOMA; ENDODERM; GASTRULATION; GENE EXPRESSION; GENE TARGETING; MOUSE; NEURAL CREST CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; BLASTOCYST; BLOTTING, NORTHERN; CELL LINE; CYCLIC AMP; DNA-BINDING PROTEINS; ENDODERM; EPITHELIAL CELLS; IN SITU HYBRIDIZATION; MESODERM; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; ORGAN CULTURE TECHNIQUES; PARATHYROID HORMONE; PARATHYROID HORMONE-RELATED PROTEIN; PHENOTYPE; PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; UP-REGULATION;

ANIMALIA; GASTROPODA; MAMMALIA;

EID: 0034123245     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. ABOU-SAMRA, A.B., JUPPNER, H., FORCE, T., FREEMAN, M.W., KONG, X.F., SCHIPANI, E., URENA, P., RICHARDS, J., BONVENTRE, J.V. and POTTS, J.T.J. (1992). Expression cloning of a common receptor for parathyroid hormone and parathyroid hormone-related peptide from rat osteoblast-like cells: a single receptor stimulates intracellular accumulation of both cAMP and inositol trisphosphates and increases intracellular free calcium. Proc. Natl. Acad. Sci. USA 89: 2732-2736.
2. AOKI, F., WORRAD, D.M. and SCHULTZ, R.M. (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181: 296-307.
3. ASHRAF, S.I., HU, X., ROOTE, J. and IP, Y.T. (1999). The mesoderm determinant Snail collaborates with related zinc-finger proteins to control Drosophila neurogenesis. EMBO J. 18: 6426-6438.
4. BATLLE, E., SANCHO, E., FRANCI, C., DOMINGUEZ, D., MONFAR, M., BAULIDA, J. and GARCIA, D.H. (2000). The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nature Cell Biol. 2: 84-89.
5. BEHRENDTSEN, O., ALEXANDER, C.M. and WERB, Z. (1995). Cooperative interactions between extracellular matrix, integrins and parathyroid hormone-related peptide regulate parietal endoderm differentiation in mouse embryos. Development 121: 4137-4148.
6. BOULAY, J.L., DENNEFELD, C. and ALBERGA, A. (1987). The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 330: 395-398.
7. BRINGHURST, F.R., JUPPNER, H., GUO, J., URENA, P., POTTS, J.T.J., KRONENBERG, H.M., ABOU-SAMRA, A.B. and SEGRE, G.V. (1993). Cloned, stably expressed parathyroid hormone (PTH)/PTH-related peptide receptors activate multiple messenger signals and biological responses in LLC-PK1 kidney cells. Endocrinology 132: 2090-2098.
8. BROWN, S.J. and DENELL, R.E. (1996). Segmentation and dorsoventral patterning in Tribolium. Cell Dev. Biol. 7: 553-560.
9. BUXTON, P.G., KOSTAKOPOULOU, K., BRICKELL, P., THOROGOOD, P. and FERRETTI, P. (1997). Expression of the transcription factor slug correlates with growth of the limb bud and is regulated by FGF-4 and retinoic acid. Int. J. Dev. Biol. 41: 559-568.
10. CANO, A., PEREZ-MORENO, M.A., RODRIGO, I., LOCASCIO, A., BLANCO, M.J., DEL BARRIO, M.G., PORTILLO, F. and NIETO, M.A. (2000). The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nature Cell Biol. 2: 76-83.
11. CARL, T.F., DUFTON, C., HANKEN, J. and KLYMKOWSKY, M.W. (1999). Inhibition of neural crest migration in Xenopus using antisense slug RNA. Dev. Biol. 213: 101-115.
12. CHAN, S.D., STREWLER, G.J., KING, K.L. and NISSENSON, R.A. (1990). Expression of a parathyroid hormone-like protein and its receptor during differentiation of embryonal carcinoma cells. Mol. Endocrinol. 4: 638-646.
13. COCKROFT, D.L. and GARDNER, R.L. (1987). Clonal analysis of the developmental potential of 6th and 7th day visceral endoderm cells in the mouse. Development 101: 143-155.
14. EMERY, J.F. and BIER, E. (1995). Specificity of CNS and PNS regulatory subelements comprising pan-neural enhancers of the deadpan and scratch genes is achieved by repression. Development 121: 3549-3560.
15. ENDERS, A.C. (1997). The role of hypoblast endoderm in early develoment of higher primates. In Microscopy of reproduction and develoment: a dynamic approach, (Ed. Motta P.M.) Antonio Delfino Editore, Rome, pp. 299-305.
16. ENDERS, A.C., GIVEN, R.L. and SCHLAFKE, S. (1978). Differentiation and migration of endoderm in the rat and mouse at implantation. Anat. Rec. 190: 65-77.
17. ERIVES, A., CORBO, J.C. and LEVINE, M. (1998). Lineage-specific regulation of the Ciona snail gene in the embryonic mesoderm and neuroectoderm. Dev. Biol. 194: 213-225.
18. ESSEX, L.J., MAYOR, R. and SARGENT, M.G. (1993). Expression of Xenopus snail in mesoderm and prospective neural fold ectoderm. Dev. Dyn. 198: 108-122.
19. FEIJEN, A., GOUMANS, M.J. and VAN DEN EIJNDEN-VAN RAAIJ, A.J. (1994). Expression of activin subunits, activin receptors and follistatin in postimplantation mouse embryos suggests specific developmental functions for different activins. Development 120: 3621-3637.
20. FREEMAN, W.M., WALKER, S.J. and VRANA, K.E. (1999). Quantitative RT-PCR: pitfalls and potential. Biotechniques 26: 112-115.
21. FUSE, N., HIROSE, S. and HAYASHI, S. (1994). Diploidy of Drosophila imaginal cells is maintained by a transcriptional repressor encoded by escargot. Genes Dev. 8: 2270-2281.
22. FUSE, N., HIROSE, S. and HAYASHI, S. (1996). Determination of wing cell fate by the escargot and snail genes in Drosophila. Development 122: 1059-1067.
23. GRABEL, L.B. and WATTS, T.D. (1987). The role of extracellular matrix in the migration and differentiation of parietal endoderm from teratocarcinoma embryoid bodies. J. Cell Biol. 105: 441-448.
24. GRAU, Y., CARTERET, C. and SIMPSON, P. (1984). Mutations and chromosomal rearangements affecting the expression of snail, a gene involved in embryonic patterning in Drosophila Melanogaster. Genetics 108: 347-360.
25. GROVER, A., ANDREWS, G. and ADAMSON, E.D. (1983). Role of laminin in epithelium formation by F9 aggregates. J. Cell Biol. 97: 137-144.
26. HAMMERSCHMIDT, M. and NUSSLEIN-VOLHARD, C. (1993). The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation. Development 119: 1107-1118.
27. HARDIN, J. (1995). Target recognition by mesenchyme cells during sea urchin gastrulation. Am. Zool. 35: 358-371.
28. HAY, E.D. (1995). An overview of epithelio-mesenchymal transformation. Acta Anat. (Basel.) 154: 8-20.
29. HAYASHI, S. (1996). A Cdc2 dependent checkpoint maintains diploidy in Drosophila. Development 122: 1051-1058.
30. HAYASHI, S., HIROSE, S., METCALFE, T. and SHIRRAS, A.D. (1993). Control of imaginal cell development by the escargot gene of Drosophila. Development 118: 105-115.
31. HOGAN, B.L. and TILLY, R. (1981). Cell interactions and endoderm differentiation in cultured mouse embryos. J. Embryol. Exp. Morphol. 62: 379-394.
32. HOGAN, B., BARLOW, D.P. and TILLY, R. (1983). F9 teratocarcinoma cells as a model for the differentiation of parietal and visceral endoderm in the mouse embryo. Cancer Surv. 2: 115-140.
33. HOGAN, B., BEDDINGTON, R., COSTANTINI, F. and LACY, E. (Eds.) (1994). Manipulating the mouse embryo, a laboratory manual. Cold Spring Harbor Laboratory Press, Plainview, NY.
34. HOGAN, B.L., COOPER, A.R. and KURKINEN, M. (1980). Incorporation into Reichert's membrane of laminin-like extracellular proteins synthesized by parietal endoderm cells of the mouse embryo. Dev. Biol. 80: 289-300.
35. HOGAN, B.L., TAYLOR, A. and COOPER, A.R. (1982). Murine parietal endoderm cells synthesise heparan sulphate and 170K and 145K sulphated glycoproteins as components of Reichert's membrane. Dev. Biol. 90: 210-214.
36. IMADA, S., YAMAGUCHI, H., NAGUMO, M., KATAYANAGI, S., IWASAKI, H. and IMADA, M. (1990). Identification of fetomodulin, a surface marker protein of fetal development, as thrombomodulin by gene cloning and functional assays. Dev. Biol. 140: 113-122.
37. INUKAI, T., INOUE, A., KUROSAWA, H., GOI, K., SHINJYO, T., OZAWA, K., MAO, M., INABA, T. and LOOK, A.T. (1999). SLUG, a ces-1-related zinc finger transcription factor gene with antiapoptotic activity, is a downstream target of the E2A-HLF oncoprotein. Mol. Cell 4: 343-352.
38. JIANG, R, LAN, Y, NORTON, C, and GRIDLEY, T (1998a). Defects in gastrulation and mesoderm migration in mice lacking the Sna gene. Dev. Biol. 198: 224 (Abstr.).
39. JIANG, R., LAN, Y., NORTON, C.R., SUNDBERG, J.P. and GRIDLEY, T. (1998b). The Slug gene is not essential for mesoderm or neural crest development in mice. Dev. Biol. 198: 277-285.
40. KARPERIEN, M., LANSER, P., DE LAAT, S.W., BOONSTRA, J. and DEFIZE, L.H. (1996). Parathyroid hormone related peptide mRNA expression during murine postimplantation development: evidence for involvement in multiple differentiation processes. Int. J. Dev. Biol. 40: 599-608.
41. KARPERIEN, M., VAN DIJK, T.B., HOEIJMAKERS, T., CREMERS, F., ABOUSAMRA, A.B., BOONSTRA, J., DE LAAT, S.W. and DEFIZE, L.H. (1994). Expression pattern of parathyroid hormone/parathyroid hormone related peptide receptor mRNA in mouse postimplantation embryos indicates involvement in multiple developmental processes. Mech. Dev. 47: 29-42.
42. KAUFMAN M.H. (Ed.) (1992). The atlas of mouse development. Academic Press Limited, London, UK.
43. KELLER, G., KENNEDY, M., PAPAYANNOPOULOU, T. and WILES, M.V. (1993). Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell Biol. 13: 473-486.
44. KESTER, H.A., VAN DER LEEDE, B.M., VAN DER SAAG, P.T. and VAN DER BURG, B. (1997). Novel progesterone target genes identified by an improved differential display technique suggest that progestin-induced growth inhibition of breast cancer cells coincides with enhancement of differentiation. J. Biol. Chem. 272: 16637-16643.
45. KOSMAN, D., IP, Y.T., LEVINE, M. and ARORA, K. (1991). Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo. Science 254: 118-122.
46. KURKINEN, M., BARLOW, D.P., JENKINS, J.R. and HOGAN, B.L. (1983). In vitro synthesis of laminin and entactin polypeptides. J. Biol. Chem. 258: 6543-6548.
47. LABONNE, C. and BRONNER-FRASER, M. (1998). Neural crest induction in Xenopus: evidence for a two-signal model. Development 125: 2403-2414.
48. LANGELAND, J.A., TOMSA, J.M., JACKMAN, W.R.J. and KIMMEL, C.B. (1998). An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev. Genes Evol. 208: 569-577.
49. MASON, I.J., TAYLOR, A., WILLIAMS, J.G., SAGE, H. and HOGAN, B.L. (1986). Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell 'culture shock' glycoprotein of Mr 43,000. EMBO J. 5: 1465-1472.
50. MAYOR, R., MORGAN, R. and SARGENT, M.G. (1995). Induction of the prospective neural crest of Xenopus. Development 121: 767-777.
51. METZSTEIN, M.M. and HORVITZ, H.R. (1999). The C. elegans cell death specification gene ces-1 encodes a snail family zinc finger protein. Mol. Cell 4: 309-319.
52. MUMMERY, C.L., FEYEN, A., FREUND, E. and SHEN, S. (1990). Characteristics of embryonic stem cell differentiation: a comparison with two embryonal carcinoma cell lines. Cell Differ. Dev. 30: 195-206.
53. NAKAYAMA, H., SCOTT, I.C. and CROSS, J.C. (1998). The transition to endoreduplication in trophoblast giant cells is regulated by the mSNA zinc finger transcription factor. Dev. Biol. 199: 150-163.
54. NIETO, M.A., BENNETT, M.F., SARGENT, M.G. and WILKINSON, D.G. (1992). Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 116: 227-237.
55. NIETO, M.A., SARGENT, M.G., WILKINSON, D.G. and COOKE, J. (1994). Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264: 835-839.
56. ROARK, M., STURTEVANT, M.A., EMERY, J., VAESSIN, H., GRELL, E. and BIER, E. (1995). scratch, a pan-neural gene encoding a zinc finger protein related to snail, promotes neuronal development. Genes Dev. 9: 2384-2398.
57. ROELEN, B.A., GOUMANS, M.J., ZWIJSEN, A. and MUMMERY, C.L. (1998). Identification of two distinct functions for TGF-beta in early mouse development. Differentiation. 64: 19-31.
58. ROMANO, L.A. and RUNYAN, R.B. (1999). Slug is a mediator of epithelial-mesenchymal cell transformation in the developing chicken heart. Dev. Biol. 212: 243-254.
59. ROS, M. A., SEFTON, M. and NIETO, M.A. (1997). Slug, a zinc finger gene previously implicated in the early patterning of the mesoderm and the neural crest, is also involved in chick limb development. Development 124: 1821-1829.
60. SAMBROOK J., FRITSCH E.F., and MANIATIS T. (Eds.) (1989). Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Plainview, NY.
61. SARGENT, M.G. and BENNETT, M.F. (1990). Identification in Xenopus of a structural homologue of the Drosophila gene snail. Development 109: 967-973.
62. SAVAGNER, P., KARAVANOVA, I., PERANTONI, A., THIERY, J.P and YAMADA, K.M. (1998). Slug mRNA is expressed by specific mesodermal derivatives during rodent organogenesis. Dev. Dyn. 213: 182-187.
63. SAVAGNER, P., YAMADA, K.M. and THIERY, J.P. (1997). The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J. Cell Biol. 137: 1403-1419.
64. SCHULTZ, R.M. (1993). Regulation of zygotic gene activation in the mouse. BioEssays 15: 531-538.
65. SEFTON, M., SANCHEZ, S. and NIETO, M.A. (1998). Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125: 3111-3121.
66. SIMPSON, P. (1983). Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics 105: 615-632.
67. SMITH, D.E., FRANCO, D.A. and GRIDLEY, T. (1992). Isolation of Sna, a mouse gene homologous to the Drosophila genes snail and escargot: its expression pattern suggests multiple roles during postimplantation development. Development 116: 1033-1039.
68. SMITH, K.K. and STRICKLAND, S. (1981). Structural components and characteristics of Reichert's membrane, an extra-embryonic basement membrane. J. Biol. Chem. 256: 4654-4661.
69. STRICKLAND, S., SMITH, K.K. and MAROTTI, K.R. (1980). Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell 21: 347-355.
70. THISSE, C. and THISSE, B. (1999). Antivin, a novel and divergent member of the TGFbeta superfamily, negatively regulates mesoderm induction. Development 126: 229-240.
71. THISSE, C., THISSE, B. and POSTLETHWAIT, J.H. (1995). Expression of snail2, a second member of the zebrafish snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos. Dev. Biol. 172: 86-99.
72. THISSE, C., THISSE, B., SCHILLING, T.F. and POSTLETHWAIT, J.H. (1993). Structure of the zebrafish snail 1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119: 1203-1215.
73. TWIGG, S.R. and WILKIE, A.O. (1999). Characterisation of the human snail (SNAI1) gene and exclusion as a major disease gene in craniosynostosis. Hum. Genet. 105: 320-326.
74. VAN DE STOLPE, A., KARPERIEN, M., LOWIK, C.W., JUPPNER, H, SEGRE, G.V., ABOU-SAMRA, A.B., DE LAAT, S.W. and DEFIZE, L.H. (1993). Parathyroid hormone-related peptide as an endogenous inducer of parietal endoderm differentiation. J. Cell Biol. 120: 235-243.
75. VERHEIJEN, M.H.G. and DEFIZE, L.H.K. (1999). Signals governing extraembryonic endoderm formation in the mouse: involvement of the type 1 parathyroid hormone-related peptide (PTHrP) receptor, p21 Ras and cell adhesion molecules. Int. J. Dev. Biol. 43: 711-721.
76. VERHEIJEN, M.H., KARPERIEN, M., CHUNG, U., VAN WIJUEN, M., HEYSTEK, H., HENDRIKS, J.A., VELTMAAT, J.M., LANSKE, B., LI, E., LOWIK, C.W., DE LAAT, S.W., KRONENBERG, H.M. and DEFIZE, L.H. (1999). Parathyroid hormone-related peptide (PTHrP) induces parietal endoderm formation exclusively via the type I PTH/PTHrP receptor. Mech. Dev. 81: 151-161.
77. WARTIOVAARA, J., LEIVO, I. and VAHERI, A. (1979). Expression of the cell surface-associated glycoprotein, fibronectin, in the early mouse embryo. Dev. Biol. 69: 247-257.
78. WHITELEY, M., NOGUCHI, P.D., SENSABAUGH, S.M., ODENWALD, W.F. and KASSIS, J.A. (1992). The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech. Dev. 36: 117-127.