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.
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References
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
N. M. Dahms, P. Lobel, and S. Komfeld. Mannose 6-phosphate receptors and lysosomal enzyme targeting.J. Biol. Chem. 264: 12115 (1989).
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).
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).
Y. Yarden, and A. Ullrich. Growth factor receptor tyrosine kinases.Ann. Rev. Biochem. 57: 443 (1988).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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© 1991 Plenum Press, New York
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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
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DOI: https://doi.org/10.1007/978-1-4684-5949-4_28
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