Skip to main content

Reciprocal Modulation of Binding of Lysosomal Enzymes and Insulin-Like Growth Factor-II (IGF-II) to the Mannose 6- Phosphate/IGF-II Receptor

  • Chapter
Molecular Biology and Physiology of Insulin and Insulin-Like Growth Factors

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 293))

Abstract

The discovery by Morgan et al.1 that the human IGF-II receptor is 80% homologous to the bovine cation-independent mannose 6-phosphate (Man-6-P) receptor led them to propose that the receptor is bifunctional, binding both a large number of lysosomal enzymes through the Man-6-P recognition site, and the growth factor, IGF-II. Later, Komfeld’s and Czech’s laboratories reported that the avian and amphibian Man-6-P receptors did not bind IGF-II, suggesting that the bifunctional property of the receptor may be confined to mammals.2,3 Did the mammalian receptor gene simply pick up a nucleotide sequence encoding an IGF-II binding site, enabling the receptor to provide a degradative pathway for IGF-II, or are there important interactions of the two disparate classes of ligands for binding to the receptor? These interactions could result in reciprocal modulation of the targeting of lysosomal enzymes by IGF-II, on the one hand, and the modulation of IGF-II degradation and IGF-II stimulated biologic responses by lysosomal enzymes, on the other. We will briefly summarize our experimental results which provide evidence for reciprocal inhibition of binding of the two classes of ligands for the mammalian Man-6-P/ IGF-II receptor.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. D. O. Morgan, J. C. Edman, D. N. Standring, V. A. Fried, M. C. Smith, R. A. Roth, and W. J. Rutter. Insulin-like growth factor II receptor as a multifunctional binding protein.Nature 329: 301 (1987).

    Article  PubMed  CAS  Google Scholar 

  2. W. M. Canfleld and S. Kornfeld. The chicken liver cation-independent mannose 6-phosphate receptor lacks the high affinity binding site for insulin-like growth factor II.J. Biol. Chem. 264: 7100 (1989).

    Google Scholar 

  3. K. B. Clairmont and M. P. Czech. Chicken andXenopus mannose 6-phosphate receptors fail to bind insulin-like growth factor II.J. Biol. Chem. 264: 16390 (1989).

    PubMed  CAS  Google Scholar 

  4. W. Kiess, C. L. Thomas, M. M. Sklar, and S. P. Nissley. Betagalactosidase decreases the binding affinity of the insulin-like growth factor-ll/mannose 6-phosphate receptor for the insulin-like growth factor-ll.Eur. J. Biochem. 190: 71 (1990).

    Article  PubMed  CAS  Google Scholar 

  5. A. R. Robbins, R. Myerowitz, R. J. Youle, G. J. Murray, and D. M. Neville. The mannose 6-phosphate receptor of Chinese hamster ovary cells. Isolation of mutants with altered receptors.J. Biol. Chem. 256: 10618 (1981).

    PubMed  CAS  Google Scholar 

  6. G. G. Sahagian, J. Distler, and G. W. Jourdian. Characterization of a membrane-associated receptor from bovine liver that binds phosphomannosyl residues of bovine testicular β-galactosidase.Proc. Natl. Acad. Sci. USA. 78: 4289 (1981).

    Article  PubMed  CAS  Google Scholar 

  7. P. Y. Tong, W. Gregory, and S. Kornfeld. Ligand interactions of the cationindependent mannose 6-phosphate receptor. The stoichiometry of mannose 6-phosphate binding.J. Biol. Chem. 264: 7962 (1989).

    PubMed  CAS  Google Scholar 

  8. W. Kiess, G. D. Blickenstaff, M. M. Sklar, C. L. Thomas, S. P. Nissley, and G. G. Sahagian. Biochemical evidence that the type II insulin-like growth factor receptor is identical to the cation-independent mannose 6-phosphate receptor.J. Biol. Chem. 263: 9339 (1988).

    PubMed  CAS  Google Scholar 

  9. M. Mathieu, H. Rochefort, B. Barenton, C. Prebois, and F. Vignon. Interactions of cathepsin-D and insulin-like growth factor-ll (IGF-II) on the IGF-ll/mannose-6-phosphate receptor in human breast cancer cells and possible consequences on mitogenic activity of IGF-II.Mol. Endocrinol. 4: 1327 (1990).

    Article  PubMed  CAS  Google Scholar 

  10. C. M. Nolan, J. W. Kyle, H. Watanabe, and W. S. Sly. Binding of insulinlike growth factor II (IGF-II) by human cation-independent mannose 6-phosphate receptor/IGF-ll receptor expressed in receptor-deficient mouse L cells.Cell Regulation 1: 197 (1990).

    PubMed  CAS  Google Scholar 

  11. T. Braulke, C. Causin, A. Waheed, U. Junghans, A. Hasilik, P. Maly, R. E. Humbel, and K. von Figura. Mannose 6-phosphate/insulin-like growth factor II receptor: distinct binding sites for mannose 6-phosphate and insulin-like growth factor II.Biochem. Biophys. Res. Comm. 150: 1287 (1988).

    Article  PubMed  CAS  Google Scholar 

  12. R. A. Roth, C. Stover, J. Hari, D. O. Morgan, M. C. Smith, V. Sara, and V. A. Fried. Interactions of the receptor for insulin-like growth factor II with mannose 6-phosphate and antibodies to the mannose 6-phosphate receptor.Biochem. Biophys. Res. Comm. 149: 600 (1987).

    Article  PubMed  CAS  Google Scholar 

  13. R. G. MacDonald, S. R. Pfeffer, L. Coussens, M. A. Tepper, C. M. Brocklebank, J. E. Mole, J. K. Anderson, E. Chen, M. P. Czech, and A. Ullrich. A single receptor binds both insulin-like growth factor II and mannose 6-phosphate.Science 239: 1134 (1988).

    Article  PubMed  CAS  Google Scholar 

  14. C. Polychronakos, H. J. Guyda, and B. I. Posner. Mannnose 6-phosphate increases the affinity of its cation-independent receptor for insulin-like growth factor II by displacing inhibitory endogenous ligands.Biochem. Biophys. Res. Commun. 157: 632 (1988).

    Article  PubMed  CAS  Google Scholar 

  15. N. M. Dahms, P. Lobel, and S. Komfeld. Mannose 6-phosphate receptors and lysosomal enzyme targeting.J. Biol. Chem. 264: 12115 (1989).

    PubMed  CAS  Google Scholar 

  16. Y. Oka, L. M. Rozek, and M. P. Czech. Direct demonstration of rapid insulin-like growth factor II receptor internalization and recycling in rat adipocytes. Insulin stimulates 125l-insulin-like growth factor II degradation by modulating the IGF-II receptor recycling process.J. Biol. Chem. 260: 9435 (1985).

    PubMed  CAS  Google Scholar 

  17. W. Kiess, J. F. Haskell, L Lee, L A. Greenstein, B. E. Miller, A. L Aarons, M. M. Rechler, and S. P. Nissley. An antibody that blocks insulin-like growth factor (IGF) binding to the type II IGF receptor is neither an agonist nor an inhibitor of IGF-stimulated biologic responses in L6 myoblasts.J. Biol. Chem. 262: 12745 (1987).

    PubMed  CAS  Google Scholar 

  18. Y. Yarden, and A. Ullrich. Growth factor receptor tyrosine kinases.Ann. Rev. Biochem. 57: 443 (1988).

    Article  PubMed  CAS  Google Scholar 

  19. R. W. Furlanetto, J. N. DiCarlo, and C. Wisehart. The type II insulin-like growth factor receptor does not mediate deoxyribonucleic acid synthesis in human fibroblasts.J. Clin. Endocrinol. Metab. 64: 1142 (1987).

    Article  PubMed  CAS  Google Scholar 

  20. C. A. Conover, P. Misra, R. L. Hintz, and R. G. Rosenfeld. Effect of an anti-insulin-like growth factor I receptor antibody on insulin-like growth factor II stimulation of DNA synthesis in human fibroblasts.Biochem. Biophys. Res. Commun. 139: 501 (1986).

    Article  PubMed  CAS  Google Scholar 

  21. S. A. Rogers and M. R. Hammerman. Insulin-like growth factor II stimulates production of inositol trisphosphate in proximal tubular basolateral membranes from canine kidney.Proc. Natl. Acad. Sci. USA. 85: 4037 (1988).

    Article  PubMed  CAS  Google Scholar 

  22. M. Tally, C. H. Li, and K. Hall. IGF-2 stimulated growth mediated by the somatomedin type 2 receptor.Biochem. Biophys. Res. Commun. 148: 811 (1987).

    Article  PubMed  CAS  Google Scholar 

  23. B. Bhaumick and R. M. Bala. Parallel effects of insulin-like growth factorII and insulin on glucose metabolism of developing mouse embryonic limb buds in culture.Biochem. Biophys. Res. Commun. 152: 359 (1988).

    Article  CAS  Google Scholar 

  24. J. Hari, S. B. Pierce, D. O. Morgan, V. Sara, M. C. Smith, and R. A. Roth. The receptor for insulin-like growth factor II mediates an insulin-like response.EMBO J. 6: 3367 (1987).

    PubMed  CAS  Google Scholar 

  25. I. Kojima, I. Nishimoto, T. liri, E. Ogata, and R. Rosenfeld. Evidence that type II insulin-like growth factor receptor is coupled to calcium gating system.Biochem. Biophys. Res. Commun. 154: 9 (1988).

    Article  PubMed  CAS  Google Scholar 

  26. I. Nishimoto, Y. Murayama, Y. Katada, M. Ui, and E. Ogata. Possible direct linkage of insulin-like growth factor-ll receptor with guanine nucleotide-binding proteins.J. Biol. Chem. 264: 14029 (1989).

    PubMed  CAS  Google Scholar 

  27. W. Kiess, C. L. Thomas, L. A. Greenstein, L. Lee, M. M. Sklar, M. M. Rechler, G. G. Sahagian, and S. P. Nissley. Insulin-like growth factor-ll (IGF-II) inhibits both the cellular uptake of /3-galactosidase and the binding of β-galactosidase to purified IGF-ll/mannose 6-phosphate receptor.J. Biol. Chem. 264: 4710 (1989).

    PubMed  CAS  Google Scholar 

  28. P. Y. Tong, S. E. Tollefsen, and S. Komfeld. The cation-independent mannose 6-phosphate receptor binds insulin-like growth factor II.J. Biol. Chem. 263: 2585 (1988).

    PubMed  CAS  Google Scholar 

  29. W. Kiess, L. A. Greenstein, L. Lee, C. Thomas, and S. P. Nissley. Biosynthesis of the insulin-like growth factor-ll (IGF-ll)/mannose 6-phosphate receptor in rat C6 glial cells. The role of N-linked glycosylation in binding of IGF-II to the receptor.Mol. Endocrinol. ,in press (1991).

    Google Scholar 

  30. G. G. Sahagian and E. F. Neufeld. Biosynthesis and turnover of the mannose 6-phosphate receptor in cultured Chinese hamster ovary cells.J. Biol. Chem. 258: 7121 (1983).

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Plenum Press, New York

About this chapter

Cite this chapter

Nissley, P., Kiess, W. (1991). Reciprocal Modulation of Binding of Lysosomal Enzymes and Insulin-Like Growth Factor-II (IGF-II) to the Mannose 6- Phosphate/IGF-II Receptor. In: Raizada, M.K., LeRoith, D. (eds) Molecular Biology and Physiology of Insulin and Insulin-Like Growth Factors. Advances in Experimental Medicine and Biology, vol 293. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5949-4_28

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-5949-4_28

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-5951-7

  • Online ISBN: 978-1-4684-5949-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics