Insulin-stimulated oocyte maturation requires insulin receptor substrate 1 and interaction with the SH2 domains of phosphatidylinositol 3-kinase - PubMed (original) (raw)

Insulin-stimulated oocyte maturation requires insulin receptor substrate 1 and interaction with the SH2 domains of phosphatidylinositol 3-kinase

L M Chuang et al. Mol Cell Biol. 1993 Nov.

Abstract

Xenopus oocytes from unprimed frogs possess insulin-like growth factor I (IGF-I) receptors but lack insulin and IGF-I receptor substrate 1 (IRS-1), the endogenous substrate of this kinase, and fail to show downstream responses to hormonal stimulation. Microinjection of recombinant IRS-1 protein enhances insulin-stimulated phosphatidylinositol (PtdIns) 3-kinase activity and restores the germinal vesicle breakdown response. Activation of PtdIns 3-kinase results from formation of a complex between phosphorylated IRS-1 and the p85 subunit of PtdIns 3-kinase. Microinjection of a phosphonopeptide containing a pYMXM motif with high affinity for the src homology 2 (SH2) domain of PtdIns 3-kinase p85 inhibits IRS-1 association with and activation of the PtdIns 3-kinase. Formation of the IRS-1-PtdIns 3-kinase complex and insulin-stimulated PtdIns 3-kinase activation are also inhibited by microinjection of a glutathione S-transferase fusion protein containing the SH2 domain of p85. This effect occurs in a concentration-dependent fashion and results in a parallel loss of hormone-stimulated oocyte maturation. These inhibitory effects are specific and are not mimicked by glutathione S-transferase fusion proteins expressing the SH2 domains of ras-GAP or phospholipase C gamma. Moreover, injection of the SH2 domains of p85, ras-GAP, and phospholipase C gamma do not interfere with progesterone-induced oocyte maturation. These data demonstrate that phosphorylation of IRS-1 plays an essential role in IGF-I and insulin signaling in oocyte maturation and that this effect occurs through interactions of the phosphorylated YMXM/YXXM motifs of IRS-1 with SH2 domains of PtdIns 3-kinase or some related molecules.

PubMed Disclaimer

Similar articles

• Interactive roles of Ras, insulin receptor substrate-1, and proteins with Src homology-2 domains in insulin signaling in Xenopus oocytes.
  Chuang LM, Hausdorff SF, Myers MG Jr, White MF, Birnbaum MJ, Kahn CR. Chuang LM, et al. J Biol Chem. 1994 Nov 4;269(44):27645-9. J Biol Chem. 1994. PMID: 7961682
• IRS-1 activates phosphatidylinositol 3'-kinase by associating with src homology 2 domains of p85.
  Myers MG Jr, Backer JM, Sun XJ, Shoelson S, Hu P, Schlessinger J, Yoakim M, Schaffhausen B, White MF. Myers MG Jr, et al. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10350-4. doi: 10.1073/pnas.89.21.10350. Proc Natl Acad Sci U S A. 1992. PMID: 1332046 Free PMC article.
• Potent activation of phosphatidylinositol 3'-kinase by simple phosphotyrosine peptides derived from insulin receptor substrate 1 containing two YMXM motifs for binding SH2 domains.
  Herbst JJ, Andrews G, Contillo L, Lamphere L, Gardner J, Lienhard GE, Gibbs EM. Herbst JJ, et al. Biochemistry. 1994 Aug 16;33(32):9376-81. doi: 10.1021/bi00198a002. Biochemistry. 1994. PMID: 7520748
• The new elements of insulin signaling. Insulin receptor substrate-1 and proteins with SH2 domains.
  Myers MG Jr, White MF. Myers MG Jr, et al. Diabetes. 1993 May;42(5):643-50. doi: 10.2337/diab.42.5.643. Diabetes. 1993. PMID: 8387037 Review.
• Insulin and IGF-I signaling through the insulin receptor substrate 1.
  Keller SR, Lamphere L, Lavan BE, Kuhné MR, Lienhard GE. Keller SR, et al. Mol Reprod Dev. 1993 Aug;35(4):346-51; discussion 351-2. doi: 10.1002/mrd.1080350405. Mol Reprod Dev. 1993. PMID: 8398112 Review.

Cited by

• Molecular cloning of an amphibian insulin receptor substrate 1-like cDNA and involvement of phosphatidylinositol 3-kinase in insulin-induced Xenopus oocyte maturation.
  Liu XJ, Sorisky A, Zhu L, Pawson T. Liu XJ, et al. Mol Cell Biol. 1995 Jul;15(7):3563-70. doi: 10.1128/MCB.15.7.3563. Mol Cell Biol. 1995. PMID: 7791763 Free PMC article.
• Managing the Oocyte Meiotic Arrest-Lessons from Frogs and Jellyfish.
  Jessus C, Munro C, Houliston E. Jessus C, et al. Cells. 2020 May 7;9(5):1150. doi: 10.3390/cells9051150. Cells. 2020. PMID: 32392797 Free PMC article. Review.
• SIP/SHIP inhibits Xenopus oocyte maturation induced by insulin and phosphatidylinositol 3-kinase.
  Deuter-Reinhard M, Apell G, Pot D, Klippel A, Williams LT, Kavanaugh WM. Deuter-Reinhard M, et al. Mol Cell Biol. 1997 May;17(5):2559-65. doi: 10.1128/MCB.17.5.2559. Mol Cell Biol. 1997. PMID: 9111325 Free PMC article.
• Participation of Phosphatidylinositol-3 Kinase Signalling in Human Chorionic Gonadotropin, Bovine Insulin (B-Insulin) and Human-Insulin-Like Growth Factor-I Induced Oocyte Maturation and Steroidogenesis in the Grey Mullet, Mugil Cephalus.
  Das P, Saha I, Chatterjee A, Pramanick K, Chakraborty SB, Maity A, Bhowal S, Pradhan D, Mukherjee D, Maiti BR. Das P, et al. Acta Endocrinol (Buchar). 2020 Oct-Dec;16(4):426-436. doi: 10.4183/aeb.2020.426. Acta Endocrinol (Buchar). 2020. PMID: 34084233 Free PMC article.
• Microinjection of the SH2 domain of the 85-kilodalton subunit of phosphatidylinositol 3-kinase inhibits insulin-induced DNA synthesis and c-fos expression.
  Jhun BH, Rose DW, Seely BL, Rameh L, Cantley L, Saltiel AR, Olefsky JM. Jhun BH, et al. Mol Cell Biol. 1994 Nov;14(11):7466-75. doi: 10.1128/mcb.14.11.7466-7475.1994. Mol Cell Biol. 1994. PMID: 7935461 Free PMC article.

References

1. 1. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1844-8 - PubMed
2. 1. Proc Natl Acad Sci U S A. 1987 Feb;84(3):704-8 - PubMed
3. 1. Science. 1987 May 15;236(4803):840-3 - PubMed
4. 1. Science. 1987 Sep 18;237(4821):1452-8 - PubMed
5. 1. Gene. 1988 Jul 15;67(1):31-40 - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources

• Full Text Sources

  • Atypon
  • Europe PubMed Central
  • PubMed Central
  • Taylor & Francis

• Medical

  • MedlinePlus Health Information

• Miscellaneous

  • NCI CPTAC Assay Portal