Skip to main content

Advertisement

Log in

Placental vascularity and growth factor expression in singleton, twin, and triplet pregnancies in the sheep

  • Original Paper
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

For singleton, twin, and triplet pregnancies, uteri were collected on day 140 of pregnancy. For each ewe (n = 18), placentomes were fixed by arterial perfusion supplying the fetal (cotyledon) and maternal placenta (caruncle). Tissue sections were stained for determination of vascularity by image analysis. Further, protein expression for factor VIII, vascular endothelial growth factor (VEGF) and its receptor, VEGFR1, as well as basic fibroblast growth factor (FGF2) and its receptor, FGFR, in tissue sections was determined by immunohistochemistry and image analyses. Cotyledonary and caruncular samples were analyzed for expression of mRNA for Vegf and its two receptors, Vegfr1 and Vegfr2, as well as Fgf2 and Fgfr. Fetal number did not affect placental capillary density or factor VIII expression, whereas increased fetal number reduced total cotyledon and caruncle capillary volume. While expression of Vegf, Vegfr1, Vegfr2, and Fgfr mRNA in cotyledonary but not caruncular tissue was greater in twin pregnancies compared to singleton and triplet pregnancies, protein expression of VEGF in the placentome decreased with increasing numbers of fetuses, VEGFR1 did not change, and FGFR was greater in twin versus singleton and triplet pregnancies. Fetal number did not affect the expression of Fgf2 mRNA in placental tissues, whereas FGF2 protein expression was less in triplet compared to singleton and twin pregnancies. Reduced fetal and placental weights in twins and/or triplet pregnancies are associated with an overall decrease in total placental vascularity, VEGF and FGF2 and/or FGFR protein expression, but not in angiogenic factor mRNA expression or VEGFR1 protein expression in sheep.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. CDC Reproductive Health, Assisted Reproductive Technology Report (2003). http://www.cdc.gov/ART/ART2003/PDF/ART2003.pdf

  2. R.K. Christenson, R.L. Prior, J. Anim. Sci. 46, 189–200 (1978)

    CAS  PubMed  Google Scholar 

  3. C.R. Rosenfeld, Semin. Perinatol. 8, 42–51 (1984)

    CAS  PubMed  Google Scholar 

  4. P.L. Greenwood, R.M. Slepetis, A.W. Bell, Reprod. Fertil. Dev. 12, 149–156 (2000)

    Article  CAS  PubMed  Google Scholar 

  5. K.A. Vonnahme, B.W. Hess, T.R. Hansen, R.J. McCormick, D.C. Rule, G.E. Moss, W.J. Murdoch, M.J. Nijland, D.C. Skinner, P.W. Nathanielsz, S.P. Ford, Biol. Reprod. 69, 133–140 (2003)

    Article  CAS  PubMed  Google Scholar 

  6. A.T. Grazul-Bilska, D. Pant, J.S. Luther, P.P. Borowicz, C. Navanukraw, J.S. Caton, M.A. Ward, D.A. Redmer, L.P. Reynolds, Anim. Reprod. Sci. 92, 268–283 (2006)

    Article  CAS  PubMed  Google Scholar 

  7. C.M. Dwyer, S.K. Calvert, M. Farish, J. Donbavand, H.E. Pickup, Theriogenology 63, 1092–1110 (2005)

    Article  CAS  PubMed  Google Scholar 

  8. D.S. Gardner, K. Tingey, B.W. Van Bon, S.E. Ozanne, V. Wilson, J. Dandrea, D.H. Keisler, T. Stephenson, M.E. Symonds, Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R947–R954 (2005)

    CAS  PubMed  Google Scholar 

  9. E. Gootwine, Anim. Sci. 81, 393–398 (2005)

    Article  Google Scholar 

  10. J.S. Luther, D.A. Redmer, L.P. Reynolds, J.M. Wallace, Hum. Fertil. 8, 179–187 (2005) (Cambridge, England)

    Article  Google Scholar 

  11. M.G. Ross, M. Desai, C. Guerra, S. Wang, Am. J. Obstet. Gynecol. 192, 1196–1204 (2005)

    Article  PubMed  Google Scholar 

  12. J.M. Wallace, D.A. Bourke, R.P. Aitken, N. Leitch, W.W. Hay Jr., Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1027–R1036 (2002)

    CAS  PubMed  Google Scholar 

  13. G. Alexander, D. Williams, J. Physiol. 198, 251–276 (1968)

    CAS  PubMed  Google Scholar 

  14. G. Alexander, Symposium on Size at Birth, vol. 27 (Elsevier, NY, 1974) pp. 215–245

  15. M.E. Symonds, M.J. Bryant, D.A. Shepherd, M.A. Lomax, Br. J. Nutr. 60, 249–263 (1988)

    Article  CAS  PubMed  Google Scholar 

  16. P.L. Greenwood, A.S. Hunt, J.W. Hermanson, A.W. Bell, J. Anim. Sci. 76, 2354–2367 (1998)

    CAS  PubMed  Google Scholar 

  17. K.M. Godfrey, D.J.P. Barker, Am. J. Clin. Nutr. 7, 1344S–1352S (2000)

    Google Scholar 

  18. L.P. Reynolds, D.A. Redmer, J. Anim. Sci. 73, 1839–1851 (1995)

    CAS  PubMed  Google Scholar 

  19. L.P. Reynolds, D.A. Redmer, Biol. Reprod. 64, 1033–1040 (2001)

    Article  CAS  PubMed  Google Scholar 

  20. L.P. Reynolds, C.L. Ferrell, S.P. Ford, Am. J. Physiol. 249, R539–R543 (1985)

    CAS  PubMed  Google Scholar 

  21. L.P. Reynolds, P.P. Borowicz, K.A. Vonnahme, M.L. Johnson, A.T. Grazul-Bilska, D.A. Redmer, J.S. Caton, J. Physiol. 565, 43–58 (2005a)

    Article  CAS  PubMed  Google Scholar 

  22. L.P. Reynolds, P. Borowicz, K.A. Vonnahme, M.L. Johnson, A.T. Grazul-Bilska, J.M. Wallace, J.S. Caton, D.A. Redmer, Placenta 26, 689–708 (2005b)

    Article  CAS  PubMed  Google Scholar 

  23. L.P. Reynolds, J.S. Caton, D.A. Redmer, A.T. Grazul-Bilska, K.A. Vonnahme, P.P. Borowicz, J.S. Luther, J.M. Wallace, G. Wu, T.E. Spencer, J. Physiol. 572, 51–58 (2006)

    CAS  PubMed  Google Scholar 

  24. K.A. Vonnahme, M.E. Wilson, S.P. Ford, Biol. Reprod. 64, 1821–1825 (2001)

    Article  CAS  PubMed  Google Scholar 

  25. K.A. Vonnahme, S.P. Ford, J. Physiol. 554, 194–201 (2004)

    Article  CAS  PubMed  Google Scholar 

  26. K.A. Vonnahme, S.P. Ford, Biol. Reprod. 71, 163–169 (2004)

    Article  CAS  PubMed  Google Scholar 

  27. J. Zheng, K.E. Vagnoni, I.M. Bird, R.R. Magness, Biol. Reprod. 56, 1189–1197 (1997)

    Article  CAS  PubMed  Google Scholar 

  28. C.Y. Cheung, R.A. Brace, J. Soc. Gynecol. Investig. 6, 179–185 (1999)

    Article  CAS  PubMed  Google Scholar 

  29. L.V. Bogic, R.A. Brace, C.Y. Cheung, Placenta 22, 265–275 (2001)

    Article  CAS  PubMed  Google Scholar 

  30. P.P. Borowicz, D.R. Arnold, M.L. Johnson, A.T. Grazul-Bilska, D.A. Redmer, L.P. Reynolds, Biol. Reprod. 76, 259–267 (2007)

    Article  CAS  PubMed  Google Scholar 

  31. A. Ahmed, C. Dunk, D. Kniss, M. Wilkes, Lab. Investig. 76, 779–791 (1997)

    CAS  PubMed  Google Scholar 

  32. T. Asahara, T. Murohara, A. Sullivan, M. Silver, R. van der Zee, T. Li, B. Witzenbichler, G. Schatteman, J.M. Isner, Science 275, 964–967 (1997)

    Article  CAS  PubMed  Google Scholar 

  33. R. van der Zee, T. Murohara, Z. Luo, F. Zollmann, J. Passeri, C. Lekutat, J.M. Isner, Circulation 95, 1030–1037 (1997)

    PubMed  Google Scholar 

  34. A. Parenti, L. Morbidelli, X.L. Cui, J.G. Douglas, J.D. Hood, H.J. Granger, F. Ledda, M. Ziche, J. Biol. Chem. 273, 4220–4226 (1998)

    Article  CAS  PubMed  Google Scholar 

  35. G.-H. Fong, J. Rossant, M. Gertsenstein, M.L. Breltman, Nature 376, 66–70 (1995)

    Article  CAS  PubMed  Google Scholar 

  36. F. Shalaby, J. Rossant, T.P. Yamaguchi, M. Gertsenstein, X.-F. Wu, M.L. Breltman, A.C. Schuh, Nature 376, 62–66 (1995)

    Article  CAS  PubMed  Google Scholar 

  37. D.M. Ornitz, J. Xu, J.S. Colvin, D.G. McEwen, C.A. MacArthur, F. Coulier, G. Gao, M. Goldfarb, J. Biol. Chem. 271, 15292–15297 (1996)

    Article  CAS  PubMed  Google Scholar 

  38. M. Okada-Ban, J.P. Thiery, J. Jouanneau, Int. J. Biochem. Cell Biol. 32, 263–267 (2000)

    Article  CAS  PubMed  Google Scholar 

  39. E. Gootwine, T.E. Spencer, F.W. Bazer, Animal 1, 547–564 (2007)

    Article  Google Scholar 

  40. T. Murohara, J.R. Horowitz, M. Silver, Y. Tsurumi, D. Chen, A. Sullivan, J.M. Isner, Circulation 97, 99–107 (1998)

    CAS  PubMed  Google Scholar 

  41. I. Vatnik, P.A. Schoknecht, R. Darrigrand, A.W. Bell, J. Dev. Physiol. 15, 351–356 (1991)

    Google Scholar 

  42. R.R. Magness, J.A. Sullivan, Y. Li, T.M. Phernetton, I.M. Bird, Am. J. Physiol. 280, H1692–H1698 (2001)

    CAS  Google Scholar 

  43. K.A. Vonnahme, M.E. Wilson, Y. Li, H.L. Rupnow, T.M. Phernetton, S.P. Ford, R.R. Magness, J. Physiol. 565, 101–109 (2005)

    Article  CAS  PubMed  Google Scholar 

  44. E.Y. Anteby, C. Greenfield, S. Natanson-Yaron, D. Goldman-Wohl, Y. Hamani, V. Khudyak, I. Ariel, S. Yagel, Mol. Hum. Reprod. 10, 229–235 (2004)

    Article  CAS  PubMed  Google Scholar 

  45. P. Pladys, F. Sennlaub, S. Brault, D. Checchin, I. Lahaie, N.L. Le, K. Bibeau, G. Cambonie, D. Abran, M. Brochu, G. Thibault, P. Hardy, S. Chemtob, A.M. Nuyt, Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1580–R1588 (2005)

    CAS  PubMed  Google Scholar 

  46. L.P. Reynolds, D.A. Redmer, Biol. Reprod. 47, 698–708 (1992)

    Article  CAS  PubMed  Google Scholar 

  47. D.A. Redmer, R.P. Aitken, J.S. Milne, L.P. Reynolds, J.M. Wallace, Biol. Reprod. 72, 1004–1009 (2005)

    Article  CAS  PubMed  Google Scholar 

  48. K.A. Vonnahme, D.A. Redmer, E. Borowczyk, J.J. Bilski, M.L. Johnson, L.P. Reynolds, A.T. Grazul-Bilska, Reproduction 131, 1115–1126 (2006)

    Article  CAS  PubMed  Google Scholar 

  49. A. Jablonka-Shariff, A.T. Grazul-Bilska, D.A. Redmer, L.P. Reynolds, Growth Factors 14, 15–23 (1997)

    Article  CAS  PubMed  Google Scholar 

  50. V. Doraiswamy, D.L. Knutson, A.T. Grazul-Bilska, D.A. Redmer, L.P. Reynolds, Growth Factors 16, 125–135 (1998)

    Article  CAS  PubMed  Google Scholar 

  51. D.A. Redmer, V. Doraiswamy, B.J. Bortnem, K. Fisher, A. Jablonka-Shariff, A.T. Grazul-Bilska, L.P. Reynolds, Biol. Reprod. 65, 879–889 (2001)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Jerzy J. Bilski, Mr. James D. Kirsch, Mr. Kim C. Kraft, Dr. Chainarong Navanukraw, and Mr. Robert Weigl for their assistance in animal handling and data collection. This work was supported, in part, by NIH grant HL64141 to LPR and DAR, and ND SBARE grant to ATG-B, LPR and DAR and by NIH grant number P20 RR016741 from the INBRE program of the National Center for Research Resources.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna T. Grazul-Bilska.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vonnahme, K.A., Evoniuk, J., Johnson, M.L. et al. Placental vascularity and growth factor expression in singleton, twin, and triplet pregnancies in the sheep. Endocr 33, 53–61 (2008). https://doi.org/10.1007/s12020-008-9052-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-008-9052-3

Keywords

Navigation