Soluble amyloid-β precursor protein binds its cell surface receptor in a cooperative fashion with glypican and syndecan proteoglycans

Journal of Cell Science

Volumn 126, Issue 21, 2013, Pages 4856-4861

  Reinhard, Constanze ^a,b   Borgers, Marianne ^a,b   David, Guido ^a,b   De Strooper, Bart ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Alzheimer; Amyloid precursor protein (APP); APP receptor; Ectodomain of APP; Growth factor; Proteoglycan; sAPP

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CELL SURFACE RECEPTOR; FIBROBLAST GROWTH FACTOR; GLYPICAN; PROTEOHEPARAN SULFATE; SYNDECAN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RECEPTOR BINDING;

ALZHEIMER; AMYLOID PRECURSOR PROTEIN (APP); APP-RECEPTOR; ECTODOMAIN OF APP; GROWTH FACTOR; PROTEOGLYCAN; SAPP;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CHO CELLS; CRICETULUS; GLYPICANS; HUMANS; MICE; NEURONS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SYNDECAN-2;

EID: 84887574873     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.137919     Document Type: Article

References (29)

1. Anliker, B. and Müller, U. (2006). The functions of mammalian amyloid precursor protein and related amyloid precursor-like proteins. Neurodegener. Dis., 3, 239-246.
2. Clarris, H. J., Cappai, R., Heffernan, D., Beyreuther, K., Masters, C. L. and Small, D. H. (1997). Identification of heparin-binding domains in the amyloid precursor protein of Alzheimer's disease by deletion mutagenesis and peptide mapping. J. Neurochem., 68, 1164-1172.
3. David, G., Bai, X. M., Van der Schueren, B., Cassiman, J. J. and Van den Berghe, H. (1992). Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol., 119, 961-975.
4. Esko, J. D., Stewart, T. E. and Taylor, W. H. (1985). Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. USA, 82, 3197-3201.
5. Esko, J. D., Rostand, K. S. and Weinke, J. L. (1988). Tumor formation dependent on proteoglycan biosynthesis. Science, 241, 1092-1096.
6. Fotinopoulou, A., Tsachaki, M., Vlavaki, M., Poulopoulos, A., Rostagno, A., Frangione, B., Ghiso, J. and Efthimiopoulos, S. (2005). BRI2 interacts with amyloid precursor protein (APP) and regulates amyloid beta (Abeta) production. J. Biol. Chem., 280, 30768-30772.
7. Greenberg, S. M., Qiu, W. Q., Selkoe, D. J., Ben-Itzhak, A. and Kosik, K. S. (1995). Amino-terminal region of the beta-amyloid precursor protein activates mitogenactivated protein kinase. Neurosci. Lett., 198, 52-56.
8. Häcker, U., Nybakken, K. and Perrimon, N. (2005). Heparan sulphate proteoglycans:the sweet side of development. Nat. Rev. Mol. Cell Biol., 6, 530-541.
9. Hornsten, A., Lieberthal, J., Fadia, S., Malins, R., Ha, L., Xu, X., Daigle, I., Markowitz, M., O'Connor, G., Plasterk, R. et al. (2007). APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability. Proc. Natl. Acad. Sci. USA, 104, 1971-1976.
10. Iwamoto, R., and Mekada, E. (2000). Heparin-binding EGF-like growth factor: a juxtacrine growth factor. Cytokine Growth Factor Rev., 11, 335-344.
11. Jin, L. W., Ninomiya, H., Roch, J. M., Schubert, D., Masliah, E., Otero, D. A. and Saitoh, T. (1994). Peptides containing the RERMS sequence of amyloid beta/A4 protein precursor bind cell surface and promote neurite extension. J. Neurosci., 14, 5461-5470.
12. Kaden, D., Munter, L. M., Joshi, M., Treiber, C., Weise, C., Bethge, T., Voigt, P., Schaefer, M., Beyermann, M., Reif, B. et al. (2008). Homophilic interactions of the amyloid precursor protein (APP) ectodomain are regulated by the loop region and affect beta-secretase cleavage of APP. J. Biol. Chem., 283, 7271-7279.
13. Ma, Q. H., Futagawa, T., Yang, W. L., Jiang, X. D., Zeng, L., Takeda, Y., Xu, R. X., Bagnard, D., Schachner, M., Furley, A. J. et al. (2008). A TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat. Cell Biol., 10, 283-294.
14. Matsuda, S., Giliberto, L., Matsuda, Y., Davies, P., McGowan, E., Pickford, F., Ghiso, J., Frangione, B. and D'Adamio, L. (2005). The familial dementia BRI2 gene binds the Alzheimer gene amyloid-beta precursor protein and inhibits amyloidbeta production. J. Biol. Chem., 280, 28912-28916.
15. Morimoto, T., Ohsawa, I., Takamura, C., Ishiguro, M. and Kohsaka, S. (1998). Involvement of amyloid precursor protein in functional synapse formation in cultured hippocampal neurons. J. Neurosci. Res., 51, 185-195.
16. Ninomiya, H., Roch, J. M., Sundsmo, M. P., Otero, D. A. and Saitoh, T. (1993) Amino acid sequence RERMS represents the active domain of amyloid beta/A4 protein precursor that promotes fibroblast growth. J. Cell Biol. 121, 879-886.
17. Ninomiya, H., Roch, J. M., Jin, L. W. and Saitoh, T. (1994). Secreted form of amyloid beta/A4 protein precursor (APP) binds to two distinct APP binding sites on rat B103 neuron-like cells through two different domains, but only one site is involved in neuritotropic activity. J. Neurochem., 63, 495-500.
18. Osterfield, M., Egelund, R., Young, L. M. and Flanagan, J. G. (2008). Interaction of amyloid precursor protein with contactins and NgCAM in the retinotectal system. Development, 135, 1189-1199.
19. Park, P. W., Reizes, O. and Bernfield, M. (2000). Cell surface heparan sulfate proteoglycans: selective regulators of ligand-receptor encounters. J. Biol. Chem., 275, 29923-29926.
20. Reinhard, C., Hébert, S. S. and De Strooper, B. (2005). The amyloid-beta precursor protein: integrating structure with biological function. EMBO J., 24, 3996-4006.
21. Rice, H. C., Townsend, M., Bai, J., Suth, S., Cavanaugh, W., Selkoe, D. J. and Young-Pearse, T. L. (2012). Pancortins interact with amyloid precursor protein and modulate cortical cell migration. Development., 21, 3986-3996.
22. Rice, H. C., Young-Pearse, T. L. and Selkoe, D. J. (2013). Systematic Evaluation of Candidate Ligands Regulating Ectodomain Shedding of Amyloid Precursor Protein. Biochemistry,, 52, 3264-3277.
23. Ring, S., Weyer, S. W., Kilian, S. B., Waldron, E., Pietrzik, C. U., Filippov, M. A., Herms, J., Buchholz, C., Eckman, C. B., Korte, M. et al. (2007). The secreted betaamyloid precursor protein ectodomain APPs alpha is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice. J. Neurosci., 27, 7817-7826.
24. Roch, J. M., Jin, L. W., Ninomiya, H., Schubert, D. and Saitoh T. (1993). Biologically active domain of the secreted form of the amyloid beta/A4 protein precursor. Ann. N Y Acad. Sci., 695, 149-157.
25. Soba, P., Eggert, S., Wagner, K., Zentgraf, H., Siehl, K., Kreger, S., Löwer, A., Langer, A., Merdes, G., Paro, R. et al. (2005). Homo- and heterodimerization of APP family members promotes intercellular adhesion. EMBO J., 24, 3624-3634.
26. Turner, P. R., O'Connor, K., Tate, W. P. and Abraham, W. C. (2003). Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog. Neurobiol., 70, 1-32.
27. Uversky, V. N., Oldfield, C. J. and Dunker, A. K. (2005) Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J. Mol. Recognit. 18, 343-384.
28. Wang, Y. and Ha, Y. (2004). The X-ray structure of an antiparallel dimer of the human amyloid precursor protein E2 domain. Mol. Cell, 15, 343-353.
29. Wolfe, M. S. and Guénette, S. Y. (2007). APP at a glance. J. Cell Sci., 120, 3157-3161.