Placenta
Volume 29 , Pages 10-16 , March 2008

Human Embryonic Stem Cells as Models for Trophoblast Differentiation

  • L.C. Schulz

      Affiliations

    • Division of Animal Sciences, University of Missouri-Columbia, Columbia, MO 65211, USA
    • ,
  • T. Ezashi

      Affiliations

    • Division of Animal Sciences, University of Missouri-Columbia, Columbia, MO 65211, USA
    • ,
  • P. Das

      Affiliations

    • Division of Animal Sciences, University of Missouri-Columbia, Columbia, MO 65211, USA
    • ,
  • S.D. Westfall

      Affiliations

    • Division of Animal Sciences, University of Missouri-Columbia, Columbia, MO 65211, USA
    • ,
  • K.A. Livingston

      Affiliations

    • Division of Animal Sciences, University of Missouri-Columbia, Columbia, MO 65211, USA
    • ,
  • R.M. Roberts

      Affiliations

    • Division of Animal Sciences, University of Missouri-Columbia, Columbia, MO 65211, USA
    • Division of Biochemistry, University of Missouri-Columbia, Columbia, MO 65211, USA
    • Corresponding Author InformationCorresponding author. Division of Animal Sciences, University of Missouri-Columbia, 240b Bond Life Sciences Center, 1201 E. Rollins Street, Columbia, MO 65211, USA. Tel.: +1 573 882 0908; fax: +1 573 884 9676.

,Accepted 24 October 2007.

References 

  1. Fleming TP. A quantitative analysis of cell allocation to trophectoderm and inner cell mass in the mouse blastocyst. Dev Biol. 1987;119:520–531
  2. Gardner RL. Specification of embryonic axes begins before cleavage in normal mouse development. Development. 2001;128:839–847
  3. Hiiragi T, Solter D. Mechanism of first cleavage specification in the mouse egg: is our body plan set at day 0?. Cell Cycle. 2005;4:661–664
  4. Johnson MH, McConnell JM. Lineage allocation and cell polarity during mouse embryogenesis. Semin Cell Dev Biol. 2004;15:583–597
  5. Zernicka-Goetz M. Developmental cell biology: cleavage pattern and emerging asymmetry of the mouse embryo. Nat Rev Mol Cell Biol. 2005;6:919–928
  6. Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta. 2002;23:3–19
  7. Malassine A, Cronier L. Hormones and human trophoblast differentiation: a review. Endocrine. 2002;19:3–11
  8. Benirschke K. Anatomical relationship between fetus and mother. Ann N Y Acad Sci. 1994;731:9–20
  9. Bischof P, Campana A. Molecular mediators of implantation. Best Pract Res Clin Obstet Gynaecol. 2000;14:801–814
  10. Pijnenborg R. Implantation and immunology: maternal inflammatory and immune cellular responses to implantation and trophoblast invasion. Reprod Biomed Online. 2002;4(Suppl. 3):14–17
  11. Carter AM. Animal models of human placentation – a review. Placenta. 2007;28(Suppl. A):S41–S47
  12. Enders AC. Trophoblast–uterine interactions in the first days of implantation: models for the study of implantation events in the human. Semin Reprod Med. 2000;18:255–263
  13. Ringler GE, Strauss JF. In vitro systems for the study of human placental endocrine function. Endocr Rev. 1990;11:105–123
  14. King A, Thomas L, Bischof P. Cell culture models of trophoblast II: trophoblast cell lines–a workshop report. Placenta. 2000;21(Suppl. A):S113–S119
  15. Shiverick KT, King A, Frank H, Whitley GS, Cartwright JE, Schneider H. Cell culture models of human trophoblast II: trophoblast cell lines–a workshop report. Placenta. 2001;22(Suppl. A):S104–S106
  16. Graham CH, Connelly I, MacDougall JR, Kerbel RS, Stetler-Stevenson WG, Lala PK. Resistance of malignant trophoblast cells to both the anti-proliferative and anti-invasive effects of transforming growth factor-beta. Exp Cell Res. 1994;214:93–99
  17. Hohn HP, Linke M, Ugele B, Denker HW. Differentiation markers and invasiveness: discordant regulation in normal trophoblast and choriocarcinoma cells. Exp Cell Res. 1998;244:249–258
  18. Zhang J, Cao YJ, Zhao YG, Sang QX, Duan EK. Expression of matrix metalloproteinase-26 and tissue inhibitor of metalloproteinase-4 in human normal cytotrophoblast cells and a choriocarcinoma cell line, JEG-3. Mol Hum Reprod. 2002;8:659–666
  19. Khoo NK, Bechberger JF, Shepherd T, Bond SL, McCrae KR, Hamilton GS, et al. SV40 Tag transformation of the normal invasive trophoblast results in a premalignant phenotype. I. Mechanisms responsible for hyperinvasiveness and resistance to anti-invasive action of TGFbeta. Int J Cancer. 1998;77:429–439
  20. Khoo NK, Zhang Y, Bechberger JF, Bond SL, Hum K, Lala PK. SV40 Tag transformation of the normal invasive trophoblast results in a premalignant phenotype. II. Changes in gap junctional intercellular communication. Int J Cancer. 1998;77:440–448
  21. Lala PK, Lee BP, Xu G, Chakraborty C. Human placental trophoblast as an in vitro model for tumor progression. Can J Physiol Pharmacol. 2002;80:142–149
  22. Lee BP, Rushlow WJ, Chakraborty C, Lala PK. Differential gene expression in premalignant human trophoblast: role of IGFBP-5. Int J Cancer. 2001;94:674–684
  23. Frank HG, Morrish DW, Potgens A, Genbacev O, Kumpel B, Caniggia I. Cell culture models of human trophoblast: primary culture of trophoblast – a workshop report. Placenta. 2001;22(Suppl. A):S107–S109
  24. Aplin JD, Straszewski-Chavez SL, Kalionis B, Dunk C, Morrish D, Forbes K, et al. Trophoblast differentiation: progenitor cells, fusion and migration – a workshop report. Placenta. 2006;27(Suppl. A):S141–S143
  25. Genbacev O, Miller RK. Post-implantation differentiation and proliferation of cytotrophoblast cells: in vitro models – a review. Placenta. 2000;21(Suppl. A):S45–S49
  26. Draper JS, Pigott C, Thomson JA, Andrews PW. Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat. 2002;200:249–258
  27. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–1147
  28. Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA, et al. Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci U S A. 1995;92:7844–7848
  29. Iles RK. Ectopic hCGbeta expression by epithelial cancer: malignant behaviour, metastasis and inhibition of tumor cell apoptosis. Mol Cell Endocrinol. 2007;260–262:264–270
  30. Ezashi T, Das P, Roberts RM. Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A. 2005;102:4783–4788
  31. Velkey JM, O'Shea KS. Oct4 RNA interference induces trophectoderm differentiation in mouse embryonic stem cells. Genesis. 2003;37:18–24
  32. Hay DC, Sutherland L, Clark J, Burdon T. Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells. 2004;22:225–235
  33. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000;24:372–376
  34. Hough SR, Clements I, Welch PJ, Wiederholt KA. Differentiation of mouse embryonic stem cells after RNA interference-mediated silencing of OCT4 and Nanog. Stem Cells. 2006;24:1467–1475
  35. Ivanova N, Dobrin R, Lu R, Kotenko I, Levorse J, DeCoste C, et al. Dissecting self-renewal in stem cells with RNA interference. Nature. 2006;442:533–538
  36. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet. 2006;38:431–440
  37. Babaie Y, Herwig R, Greber B, Brink TC, Wruck W, Groth D, et al. Analysis of Oct4-dependent transcriptional networks regulating self-renewal and pluripotency in human embryonic stem cells. Stem Cells. 2007;25:500–510
  38. Matin MM, Walsh JR, Gokhale PJ, Draper JS, Bahrami AR, Morton I, et al. Specific knockdown of Oct4 and beta2-microglobulin expression by RNA interference in human embryonic stem cells and embryonic carcinoma cells. Stem Cells. 2004;22:659–668
  39. Hyslop L, Stojkovic M, Armstrong L, Walter T, Stojkovic P, Przyborski S, et al. Downregulation of NANOG induces differentiation of human embryonic stem cells to extraembryonic lineages. Stem Cells. 2005;23:1035–1043
  40. Hubner K, Kehler J, Scholer HR. Oocytes. Methods Enzymol. 2006;418:284–307
  41. Schenke-Layland K, Angelis E, Rhodes KE, Heydarkhan-Hagvall S, Mikkola HK, Maclellan WR. Collagen IV induces trophoectoderm differentiation of mouse embryonic stem cells. Stem Cells. 2007;25:1529–1538
  42. Rossant J. Stem cells and lineage development in the mammalian blastocyst. Reprod Fertil Dev. 2007;19:111–118
  43. Gerami-Naini B, Dovzhenko OV, Durning M, Wegner FH, Thomson JA, Golos TG. Trophoblast differentiation in embryoid bodies derived from human embryonic stem cells. Endocrinology. 2004;145:1517–1524
  44. Golos TG, Pollastrini LM, Gerami-Naini B. Human embryonic stem cells as a model for trophoblast differentiation. Semin Reprod Med. 2006;24:314–321
  45. Harun R, Ruban L, Matin M, Draper J, Jenkins NM, Liew GC, et al. Cytotrophoblast stem cell lines derived from human embryonic stem cells and their capacity to mimic invasive implantation events. Hum Reprod. 2006;21:1349–1358
  46. Peiffer I, Belhomme D, Barbet R, Haydont V, Zhou YP, Fortunel NO, et al. Simultaneous differentiation of endothelial and trophoblastic cells derived from human embryonic stem cells. Stem Cells Dev. 2007;16:393–402
  47. Xu RH, Chen X, Li DS, Li R, Addicks GC, Glennon C, et al. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol. 2002;20:1261–1264
  48. Liu YP, Dovzhenko OV, Garthwaite MA, Dambaeva SV, Durning M, Pollastrini LM, et al. Maintenance of pluripotency in human embryonic stem cells stably over-expressing enhanced green fluorescent protein. Stem Cells Dev. 2004;13:636–645
  49. Xu RH, Peck RM, Li DS, Feng X, Ludwig T, Thomson JA. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods. 2005;2:185–190
  50. Bendall SC, Stewart MH, Menendez P, George D, Vijayaragavan K, Werbowetski-Ogilvie T, et al. IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature. 2007;448:1015–1021
  51. Das P, Ezashi T, Schulz LC, Westfall SD, Livingston KA, Roberts RM. Effects of FGF2 and oxygen in the BMP4-driven differentiation of trophoblast from human embryonic stem cells. Stem Cell Res 2007; in press.
  52. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest. 1996;97:540–550
  53. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science. 1997;277:1669–1672
  54. James JL, Stone PR, Chamley LW. The effects of oxygen concentration and gestational age on extravillous trophoblast outgrowth in a human first trimester villous explant model. Hum Reprod. 2006;21:2699–2705
  55. Shapiro JA. Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol. 1998;52:81–104
  56. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev. 2001;25:365–404

PII: S0143-4004(07)00258-5

doi: 10.1016/j.placenta.2007.10.009

Placenta
Volume 29 , Pages 10-16 , March 2008

Article Tools

* Image Usage & Resolution