Fertility and Sterility
Volume 93, Issue 8 , Pages 2621-2626 , 15 May 2010

Selective insulin-like growth factor-I antagonist inhibits mouse embryo development in a dose-dependent manner

  • Jose Inzunza, Ph.D.

      Affiliations

    • Department of Biosciences and Nutrition, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Olle Danielsson, M.D., Ph.D.

      Affiliations

    • Department of Laboratory Medicine, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Parameswaran Grace Lalitkumar, Ph.D.

      Affiliations

    • Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Olle Larsson, M.D., Ph.D.

      Affiliations

    • Department of Laboratory Medicine, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Magnus Axelson, M.D., Ph.D.

      Affiliations

    • Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Virpi Töhönen, Ph.D.

      Affiliations

    • Department of Biosciences and Nutrition, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Kristina Gemzell Danielsson, M.D., Ph.D.

      Affiliations

    • Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Anneli Stavreus-Evers, Ph.D.

      Affiliations

    • Department of Women's and Children's Health, Uppsala University, Uppsala, Sweden
    • Corresponding Author InformationReprint requests: Anneli Stavreus-Evers, Ph.D., Department of Women's and Children's Health, Uppsala University, Uppsala University Hospital, SE-751 85 Uppsala, Sweden (FAX: 46-18-559-775).

Received 30 September 2009 ,Revised 14 December 2009 ,Accepted 16 December 2009.

References 

  1. Guzeloglu-Kayisli O, Basar M, Arici A. Basic aspects of implantation. Reprod Biomed Online. 2007;15:728–739
  2. Hess AP, Hamilton AE, Talbi S, Dosiou C, Nyegaard M, Nayak N, et al. Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod. 2007;76:102–117
  3. Lighten AD, Moore GE, Winston RM, Hardy K. Routine addition of human insulin-like growth factor-I ligand could benefit clinical in-vitro fertilization culture. Hum Reprod. 1998;13:3144–3150
  4. Hahnel A, Schultz GA. Insulin-like growth factor binding proteins are transcribed by preimplantation mouse embryos. Endocrinology. 1994;134:1956–1959
  5. Butler AA, LeRoith D. Minireview: tissue-specific versus generalized gene targeting of the igf1 and igf1r genes and their roles in insulin-like growth factor physiology. Endocrinology. 2001;142:1685–1688
  6. Baserga R, Porcu P, Sell C. Oncogenes, growth factors and control of the cell cycle. Cancer Surv. 1993;16:201–213
  7. Ullrich A, Gray A, Tam AW, Yang-Feng T, Tsubokawa M, Collins C, et al. Insulin-like growth factor I receptor primary structure: comparison with insulin receptor suggests structural determinants that define functional specificity. EMBO J. 1986;5:2503–2512
  8. Druckmann R, Rohr UD. IGF-1 in gynaecology and obstetrics: update 2002. Maturitas. 2002;41(Suppl. 1):S65–S83
  9. Huang YH, Chin CC, Ho HN, Chou CK, Shen CN, Kuo HC, et al. Pluripotency of mouse spermatogonial stem cells maintained by IGF-1–dependent pathway. FASEB J. 2009;23:2076–2087
  10. Baker J, Liu JP, Robertson EJ, Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell. 1993;75:73–82
  11. Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 1993;75:59–72
  12. Kim S, Lee GS, Lee SH, Kim HS, Jeong YW, Kim JH, et al. Embryotropic effect of insulin-like growth factor (IGF)-I and its receptor on development of porcine preimplantation embryos produced by in vitro fertilization and somatic cell nuclear transfer. Mol Reprod Dev. 2005;72:88–97
  13. Chi MM, Schlein AL, Moley KH. High insulin-like growth factor 1 (IGF-1) and insulin concentrations trigger apoptosis in the mouse blastocyst via down-regulation of the IGF-1 receptor. Endocrinology. 2000;141:4784–4792
  14. Markham KE, Kaye PL. Growth hormone, insulin-like growth factor I and cell proliferation in the mouse blastocyst. Reproduction. 2003;125:327–336
  15. Pfeifer TL, Chegini N. Immunohistochemical localization of insulin-like growth factor (IGF-I), IGF-I receptor, and IGF binding proteins 1-4 in human fallopian tube at various reproductive stages. Biol Reprod. 1994;50:281–289
  16. Carlsson B, Hillensjo T, Nilsson A, Tornell J, Billig H. Expression of insulin-like growth factor-I (IGF-I) in the rat fallopian tube: possible autocrine and paracrine action of fallopian tube-derived IGF-I on the fallopian tube and on the preimplantation embryo. Endocrinology. 1993;133:2031–2039
  17. Jin HY, Wang ZN. Insulin-like growth factors and their receptors in human fallopian tube in reproductive-age women. Fertil Steril. 2001;75:1037–1038
  18. Pushpakumara PG, Robinson RS, Demmers KJ, Mann GE, Sinclair KD, Webb R, et al. Expression of the insulin-like growth factor (IGF) system in the bovine oviduct at oestrus and during early pregnancy. Reproduction. 2002;123:859–868
  19. Zhang X, Kidder GM, Watson AJ, Schultz GA, Armstrong DT. Possible roles of insulin and insulin-like growth factors in rat preimplantation development: investigation of gene expression by reverse transcription–polymerase chain reaction. J Reprod Fertil. 1994;100:375–380
  20. Heyner S, Rao LV, Jarett L, Smith RM. Preimplantation mouse embryos internalize maternal insulin via receptor-mediated endocytosis: pattern of uptake and functional correlations. Dev Biol. 1989;134:48–58
  21. Tao Y, Pinzi V, Bourhis J, Deutsch E. Mechanisms of disease: signaling of the insulin-like growth factor 1 receptor pathway—therapeutic perspectives in cancer. Nat Clin Pract Oncol. 2007;4:591–602
  22. Girnita A, Girnita L, del Prete F, Bartolazzi A, Larsson O, Axelson M. Cyclolignans as inhibitors of the insulin-like growth factor-1 receptor and malignant cell growth. Cancer Res. 2004;64:236–242
  23. Vasilcanu R, Vasilcanu D, Rosengren L, Natalishvili N, Sehat B, Yin S, et al. Picropodophyllin induces downregulation of the insulin-like growth factor 1 receptor: potential mechanistic involvement of Mdm2 and beta-arrestin1. Oncogene. 2008;27:1629–1638
  24. Vasilcanu D, Girnita A, Girnita L, Vasilcanu R, Axelson M, Larsson O. The cyclolignan PPP induces activation loop-specific inhibition of tyrosine phosphorylation of the insulin-like growth factor-1 receptor. Link to the phosphatidyl inositol-3 kinase/Akt apoptotic pathway. Oncogene. 2004;23:7854–7862
  25. Nagy A, Gertsenstein M, Vintersten K, Behringer R. Manipulating the mouse embryo, a laboratory manual. 3rd ed. New York: Cold Spring Harbor Laboratory Press; 2003;
  26. Zhou J, Bondy C. Anatomy of the human ovarian insulin-like growth factor system. Biol Reprod. 1993;48:467–482
  27. Rappolee DA, Sturm KS, Behrendtsen O, Schultz GA, Pedersen RA, Werb Z. Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev. 1992;6:939–952
  28. Watson AJ, Hogan A, Hahnel A, Wiemer KE, Schultz GA. Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo. Mol Reprod Dev. 1992;31:87–95
  29. Watson AJ, Watson PH, Arcellana-Panlilio M, Warnes D, Walker SK, Schultz GA, et al. A growth factor phenotype map for ovine preimplantation development. Biol Reprod. 1994;50:725–733
  30. Jousan FD, Hansen PJ. Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling. Mol Reprod Dev. 2007;74:189–196
  31. Cui XS, Jeong YJ, Jun JH, Kim NH. Insulin-like growth factor-I alters apoptosis related genes and reduces apoptosis in porcine parthenotes developing in vitro. Theriogenology. 2005;63:1070–1080
  32. Kurzawa R, Glabowski W, Baczkowski T, Wiszniewska B, Marchlewicz M. Growth factors protect in vitro cultured embryos from the consequences of oxidative stress. Zygote. 2004;12:231–240
  33. Fabian D, Il'kova G, Rehak P, Czikkova S, Baran V, Koppel J. Inhibitory effect of IGF-I on induced apoptosis in mouse preimplantation embryos cultured in vitro. Theriogenology. 2004;61:745–755
  34. Harvey MB, Kaye PL. Insulin-like growth factor-1 stimulates growth of mouse preimplantation embryos in vitro. Mol Reprod Dev. 1992;31:195–199
  35. Loutradis D, Stefanidis K, Kousidis I, Bletsa R, Drakakis P, Milingos S, et al. Effect of human hydrosalpinx fluid on the development of mouse embryos and role of the concentration of growth factors in culture medium with and without hydrosalpinx fluid. Gynecol Endocrinol. 2005;20:26–29

 J.I. has nothing to disclose. O.D. has nothing to disclose. P.G.L. has nothing to disclose. O.L. has nothing to disclose. M.A. has nothing to disclose. V.T. has nothing to disclose. K.G.D. has nothing to disclose. A.S.-E. has nothing to disclose.

 Supported by grants from the Swedish Scientific Council (2005-7293), Karolinska Institutet, Stockholm County Council, Åke Wibergs foundation, and Goljes Foundation.

 Dr. Kristina Gemzell Danielsson and Dr. Anneli Stavreus-Evers contributed equally to this work.

PII: S0015-0282(09)04293-9

doi: 10.1016/j.fertnstert.2009.12.044

Fertility and Sterility
Volume 93, Issue 8 , Pages 2621-2626 , 15 May 2010