Modulation of trophoblast stem cell and giant cell phenotypes: Analyses using the Rcho-1 cell model

Differentiation

Volumn 73, Issue 9-10, 2005, Pages 452-462

  Sahgal, Namita ^a   Canham, Lindsey N ^a   Konno, Toshihiro ^a   Wolfe, Michael W ^a   Soares, Michael J ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Dimethyl sulfoxide; Eomesodermin; Placenta; Prolactin; Trophoblast differentiation; Trophoblast stem cells

Indexed keywords

DIMETHYL SULFOXIDE; EOMESODERMIN; GENE PRODUCT; HELIX LOOP HELIX PROTEIN; PROLACTIN; PROTEIN HAND1; UNCLASSIFIED DRUG; EOMES PROTEIN, HUMAN; T BOX TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELLULAR DISTRIBUTION; GENE EXPRESSION; GIANT CELL; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLACENTA; PRIORITY JOURNAL; RAT; STEM CELL; TROPHOBLAST; ANIMAL; CELL LINE; CELL LINEAGE; CYTOLOGY; DRUG EFFECT; FEMALE; METABOLISM; PREGNANCY; SPRAGUE DAWLEY RAT;

RODENTIA;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CELL PROLIFERATION; DIMETHYL SULFOXIDE; FEMALE; GIANT CELLS; PHENOTYPE; PREGNANCY; PROLACTIN; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS; T-BOX DOMAIN PROTEINS; TROPHOBLASTS;

EID: 33644878528     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2005.00044.x     Document Type: Article

References (77)

1. Ain R. Canham L.N. Soares M.J. ( 2003) Gestational stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev Biol 260 : 176 190.
2. Altschul S.F. Gish W. Miller W. Myers E.W. Lipman D.J. ( 1990) Basic local alignment search tool. J Mol Biol 215 : 403 410.
3. Angello J.C. Stern H.M. Hauschka S.D. ( 1997) P19 embryonal carcinoma cells: a model system for studying neural tube induction of skeletal myogenesis. Dev Biol 192 : 93 98.
4. Anson-Cartwright L. Dawson K. Holmyard D. Fisher S.J. Lazzarini R.A. Cross J.C. ( 2000) The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 25 : 311 314.
5. Arman E. Haffner-Krausz R. Chen Y. Heath J.K. Lonai P. ( 1998) Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci USA 95 : 5082 5087.
6. Auman H.J. Nottoli T. Lakiza O. Winger Q. Donaldson S. Williams T. ( 2002) Transcription factor AP-2γ is essential in the extra-embryonic lineages for early postimplantation development. Development 129 : 2733 2747.
7. Beck F. Erler T. Russell A. James R. ( 1995) Expression of Cdx-2 in the mouse embryo and placenta: possible role in the patterning of the extra-embryonic membranes. Dev Dyn 204 : 219 227.
8. Buehr M. Nichols J. Stenhouse F. Mountford P. Greenhalgh C.J. Kantachuvesiri S. Brooker G. Mullins J. Smith A.G. ( 2003) Rapid loss of Oct-4 and pluripotency in cultured rodent blastocysts and derivative cell lines. Biol Reprod 68 : 222 229.
9. Campbell W.J. Deb S. Kwok S.C.M. Joslin J. Soares M.J. ( 1989) Differential expression of placental lactogen-II and prolactin-like protein - A in the rat chorioallantoic placenta. Endocrinology 125 : 1565 1574.
10. Chawengsaksophak K. de Graaff W. Rossant J. Deschamps J. Beck F. ( 2004) Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci USA 101 : 7641 7645.
11. Chawengsaksophak K. James R. Hammond V.E. Köntgen F. Beck F. ( 1997) Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386 : 84 87.
12. Chomczynski P. Sacchi N. ( 1987) Single-step method of RNA isolation by acid guanididium thiocyanate-phenol-chloroform extraction. Anal Biochem 162 : 156 159.
13. Cohick C.B. Xu L. Soares M.J. ( 1997) Placental prolactin-like protein-B: heterologous expression and characterization of placental and decidual species. J Endocrinol 152 : 291 302.
14. Collins S.J. Ruscetti F.W. Gallagher R.E. Gallo R.C. ( 1978) Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc Natl Acad Sci USA 75 : 2458 2462.
15. Cross J.C. Flannery M.L. Blanar M.A. Steingrimsson E. Jenkins N.A. Copeland N.G. Rutter W.J. Werb Z. ( 1995) Hxt encodes a basic helix-loop-helix transcriptin factor that regulates trophoblast cell development. Development 121 : 2513 2523.
16. Dai G. Liu B. Levan G. Szpirer C. Kwok S.C.M. Soares M.J. ( 1996) Prolactin-like protein-C variant: complementary DNA, unique six exon gene structure, and trophoblast cell-specific expression. Endocrinology 137 : 5009 5019.
17. Dai G. Lu L. Tang S. Pea l.M.J. Soares M.J. ( 2002) Prolactin family miniarray: a tool for evaluating uteroplacental-trophoblast endocrine cell phenotypes. Reproduction 124 : 755 765.
18. Dai G. Wang D. Liu B. Kasik J.W. Müller H. White R.A. Hummel G.S. Soares M.J. ( 2000) Three novel paralogs of the rodent prolactin gene family. J Endocrinol 166 : 63 75.
19. Deb S. Faria T.N. Roby K.F. Larsen D. Kwok S.C.M. Talamantes F. Soares M.J. ( 1991a) Identification and characterization of a new member of the placental prolactin family: placental lactogen-I variant. J Biol Chem 266 : 1605 1610.
20. Deb S. Hamlin G.P. Roby K.F. Kwok S.C.M. Soares M.J. ( 1993) Heterologous expression and characterization of prolactin-like protein A. J Biol Chem 268 : 3298 3305.
21. Deb S. Hashizume K. Boone K. Southard J.N. Talamantes F. Rawitch A. Soares M.J. ( 1989) Antipeptide antibodies reveal structural and functional characteristics of rat placental lactogen-II. Mol Cell Endocrinol 63 : 45 56.
22. Deb S. Roby K.F. Faria T.N. Szpirer C. Levan G. Kwok S.C.M. Moares M.J. ( 1991b) Molecular cloning and characterization of prolactin-like protein-C complementary deoxyribonucleic acid. J Biol Chem 266 : 23027 23032.
23. Duckworth M.L. Schroedter I.C. Friesen H.G. ( 1990) Cellular localization of rat placental lactogen II and rat prolactin-like proteins A and B by in situ hybridization. Placenta 11 : 143 155.
24. Faria T.N. Deb S.C.M. Talamantes F. Soares M.J. ( 1990) Ontogeny of placental lactogen-I and placental lactogen-II expression in the developing rat placenta. Dev Biol 141 : 279 291.
25. Faria T.N. Soares M.J. ( 1991) Trophoblast cell differentiation: establishment, characterization, and modulation of a rat trophoblast cell line expressing members of the placental prolactin family. Endocrinology 129 : 2895 2906.
26. Feldman B. Poueymirou W. Papaioannou V.E. DeChiara T.M. Goldfarb M. ( 1995) Requirement of FGF-4 for postimplantation mouse development. Science 267 : 246 249.
27. Firulli A.B. McFadden D.G. Lin Q. Srivastava D. Olson E.N. ( 1998) Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nat Genet 18 : 266 270.
28. Firulli B.A. Howard M.J. McDaid J.R. McIlreaveym L. Dionne K.M. Centonze V.E. Cserjesi P. Virshup D.M. Firulli A.B. ( 2003) PKA, PKC, and the protein phosphatase 2A influence HAND factor function: a mechanism for tissue-specific transcriptional regulation. Mol Cell 12 : 1225 1237.
29. Freeman M.E. Kanyicska B. Lerant A. Nagy G. ( 2000) Prolactin: structure, function, and regulation of secretion. Physiol Rev 80 : 1523 1631.
30. Gardner R.L. Beddington R.S. ( 1988) Multi-lineage 'stem' cells in the mammalian embryo. J Cell Sci 10 (suppl.) : 11 27.
31. Geng Y.u.Q. Sicinska E. Das M. Schneider J.E. Bhattacharya S. Rideout W.M. Bronson R.T. Gardner H. Sicinski P. ( 2003) Cyclin E ablation in the mouse. Cell 114 : 31 443.
32. Georgiades P. Ferguson-Smith A.C. Burton G.J. ( 2002) Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23 : 3 19.
33. Guillemot F. Nagy A. Auerbach A. Rossant J. Joyner A.L. ( 1994) Essential role of Mash-2 in extraembryonic development. Nature 371 : 333 336.
34. Hamlin G.P. Lu X-J. Roby K.F. Soares M.J. ( 1994) Recapitulation of the pathway for trophoblast giant cell differentiation in vitro: stage-specific expression of members of the prolactin gene family. Endocrinology 134 : 2391 2396.
35. Hamlin G.P. Soares M.J. ( 1995) Regulation of deoxyribonucleic acid synthesis in proliferating and differentiating trophoblast cells: involvement of transferrin, transforming growth factor-β, and tyrosine kinases. Endocrinology 136 : 322 331.
36. Iwatsuki K. Oda M. Sun W. Tanaka S. Ogawa T. Shiota K. ( 1998) Molecular cloning and characterization of a new member of the rat placental prolactin (PRL) family, PRL-like protein H. Endocrinology 139 : 4976 4983.
37. Iwatsuki K. Shinozaki M. Hattori N. Hirasawa K. Itagaki S. Shiota K. Ogawa T. ( 1996) Molecular cloning and characterization of a new member of the rat placental prolactin (PRL) family, PRL-like protein D (PLP-D). Endocrinology 137 : 3849 3855.
38. Iwatsuki K. Shinozaki M. Sun W. Yagi S. Tanaka S. Shiota K. ( 2000) A novel secretory protein produced by rat spongiotrophoblast. Biol Reprod 62 : 1352 1359.
39. Kamei T. Hamlin G.P. Chapman B.M. Burkhardt A.L. Bolen J.B. Soares M.J. ( 1997) Signaling pathways controlling trophoblast cell differentiation: src-family protein tyrosine kinases. Biol Reprod 57 : 1302 1311.
40. Kamei T. Jones S.R. Chapman B.M. McGonigle K.L. Dai G. Soares M.J. ( 2002) The phosphatidylinositol 3-kinase/Akt signaling pathway modulates the endocrine differentiation of trophoblast cells. Mol Endocrinol 16 : 1469 1481.
41. Keppel G. ( 1973) Design and analysis. Prentice-Hall, Englewood Cliffs, NJ.
42. Kim J. Jones B.W. Zock C. Chen Z. Wang H. Goodman C.S. Anderson D.J. ( 1998) Isolation and characterization of mammalian homologs of the Drosophila gene glial cells missing. Proc Natl Acad Sci USA 95 : 12364 12369.
43. Kraut N. Snider. L. Chen C.-M.A. Tapscott S.J. Groudine M. ( 1998) Requirement of the mouse I-mfa gene for placental development and skeletal patterning. EMBO J 17 : 6276 6288.
44. Lever J.E. ( 1979) Inducers of mammalian cell differentiation stimulate dome formation in a differentiated kidney epithelial cell line (MDCK). Proc Natl Acad Sci USA 76 : 1323 1327.
45. Luo J. Sladek R. Bader J.A. Matthyssen A. Rossant J. Giguere V. ( 1997) Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERRβ. Nature 388 : 778 782.
46. McBurney M.W. Jones-Villeneuve E.M. Edwards M.K. Anderson P.J. ( 1982) Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature 299 : 165 167.
47. Nichols J. Zevnik B. Anastassiadis K. Niwa H. Kiewe-Nebenius D. Chambers I. Scholer H. Smith A. ( 1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95 : 379 391.
48. Omary M.B. de Grandpre L. McCaffrey M. Kagnoff M.F. ( 1992) Biochemical and morphological differentiation of the human colonic epithelial cell line SW620 in the presence of dimethylsulfoxide. J Cell Biochem 48 : 316 323.
49. Orr-Urtreger A. Bedford M.T. Burakova T. Arman E. Zimmer Y. Yayon A. Givol D. Lonai P. ( 1993) Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev Biol 158 : 475 486.
50. Papaioannou V.E. ( 2001) T-box genes in development: from hydra to humans. Int Rev Cytol 207 : 1 70.
51. Parisi T. Beck A.R. Rougier N. McNeil T. Lucian L. Werb Z. Amati B. ( 2003) Cyclins E1 and E2 are required for endoreduplication in placental trophoblast giant cells. EMBO J 22 : 4794 4803.
52. Peters T.J. Chapman B.M. Soares M.J. ( 2000) Trophoblast differentiation: an in vitro model for trophoblast giant cell development. In : Tuan R.S. Lo C.W. (eds.) Methods in molecular biology, Vol. 137. Developmental biology protocols. Vol. III, Humana Press Inc., Totowa, NJ, pp. 301 311.
53. Preisler H.D. Giladi M. ( 1975) Differentiation of erythroleukemic cells in vitro: irreversible induction by dimethyl sulfoxide (DMSO). J Cell Physiol 85 : 537 546.
54. Riley P. Anson-Cartwright L. Cross J.C. ( 1998) The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat Genet 18 : 271 275.
55. Roberts A.W. Robb L. Rakar S. Hartley L. Cluse L. Nicola N.A. Metcalf D. Hilton D.J. Alexander W.S. ( 2001) Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc Natl Acad Sci USA 98 : 9324 9329.
56. Roby K.F. Deb S. Gibori G. Szpirer C. Levan G. Kwok S.C.M. Soares M.J. ( 1993) Decidual prolactin related protein: identification, molecular cloning and characterization. J Biol Chem 268 : 3136 3142.
57. Rossant J. Cross J.C. ( 2002) Extraembryonic lineages. In : Rossant J. Tam P.P.L. (eds.) Mouse development. Academic Press, New York, pp. 155 180.
58. Russ A.P. Wattlers S. Colledge W.H. Aparicio S.A.J.R. Carlton M.B.L. Pearce J.J. Barton S.C. Surani M.A. Ryan K. Nehis M.C. Wilson V. Evans M.J. ( 2000) Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404 : 95 99.
59. Sahgal N. Knipp G.T. Liu B. Chapman B.M. Dai G. Soares M.J. ( 2000) Identification of two new nonclassical members of the rat prolactin family. J Mol Endocrinol 24 : 95 108.
60. Schreiber J. Riethmacher-Sonnenberg E. Riethmacher D. Tuerk E.E. Enderich J. Bosl M.R. Wegner M. ( 2000) Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol Cell Biol 20 : 2466 2474.
61. Scott I.C. Anson-Cartwright L. Riley P. Reda D. Cross J.C. ( 2000) The Hand1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol Cell Biol 20 : 530 541.
62. Skerjanc I.S. ( 1999) Cardiac and skeletal muscle development in P19 embryonal carcinoma cells. Trends Cardiovasc Med 9 : 139 143.
63. Soares M.J. ( 2004) The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol 2 : 51.
64. Soares M.J. Chapman B.M. Rasmussen C.A. Dai G. Kamei T. Orwig K.E. ( 1996) Differentiation of trophoblast endocrine cells. Placenta 17 : 277 289.
65. Soares M.J. Linzer D.I.H. ( 2001) Rodent prolactin family and pregnancy. In : Horseman N.D. (ed.) Prolactin. Kluwer Academic, Norwell, pp. 139 167.
66. Strumpf D. Mao C.-A. Yamanaka Y. Ralston A. Chawengsaksophak K. Beck F. Rossant J. ( 2005) Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132 : 2093 2102.
67. Takahashi Y. Carpino N. Cross J.C. Torres M. Parganas E. Ihle J.N. ( 2003) Socs3: an essential regulator of LIF receptor signaling in trophoblast giant cell differentiation. EMBO J 22 : 372 384.
68. Tanaka M. Gertsenstein M. Rossant J. Nagy A. ( 1997) Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev Biol 190 : 55 65.
69. Tanaka S. Kunath T. Hadjantonakis A.-K. Nagy A. Rossant J. ( 1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282 : 2072 2075.
70. Teshima S. Shimosato Y. Koide T. Kuroki M. Kiruchi M. Aizawa M. ( 1983) Transplantable choriocarcinoma of rats induced by fetectomy and its biological activities. Gann 74 : 205 212.
71. Thirkill T.L. Douglas G.C. ( 1997) Differentiation of human trophoblast cells in vitro is inhibited by dimethyl sulfoxide. J Cell Biochem 15 : 460 468.
72. Tremblay G.B. Kunath T. Bergeron D. Lapointe L. Champigny C. Bader J.-A. Rossant J. Giguere V. ( 2001) Diethylstilbesterol regulates trophoblast stem cell differentiation as a ligand of orphan nuclear receptor ERRβ. Genes Dev 15 : 833 838.
73. Wang H. Scott R.E. ( 1993) Inhibition of distinct steps in the adipocyte differentiation pathway in 3T3T mesenchymal stem cells by dimethyl suphoxide (DMSO). Cell Prolif 26 : 55 66.
74. Wiemers D.O. Ain R. Ohboshi S. Soares M.J. ( 2003a) Migratory trophoblast cells express a newly identified member of the prolactin gene family. J Endocrinol 179 : 335 346.
75. Wiemers D.O. Shao L.-J. Ain R. Dai G. Soares M.J. ( 2003b) The mouse prolactin gene family locus. Endocrinology 144 : 313 325.
76. Werling U. Schorle H. ( 2002) Transcription factor gene AP-2γ essential for early murine development. Mol Cell Biol 22 : 3149 3156.
77. Yu Z.W. Quinn P.J. ( 1994) Dimethyl sulphoxide: a review of its applications in cell biology. Biosci Rep 14 : 259 281.