RAP Uses a Histidine Switch to Regulate Its Interaction with LRP in the ER and Golgi

Molecular Cell

Volumn 22, Issue 3, 2006, Pages 423-430

  Lee, Donghan ^a   Walsh, Joseph D ^a   Mikhailenko, Irina ^c   Yu, Ping ^a   Migliorini, Molly ^c   Wu, Yibing ^a   Krueger, Susan ^d   Curtis, Joseph E ^d   Harris, Bradley ^b   Lockett, Stephen ^b   Blacklow, Steve C ^e   Strickland, Dudley K ^c   Wang, Yun Xing ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c Department of Physiology   (United States)

^d NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

PROTEINS

Indexed keywords

CHAPERONE; HISTIDINE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; RECEPTOR ASSOCIATED PROTEIN; UNCLASSIFIED DRUG; ALANINE; LOW DENSITY LIPOPROTEIN RECEPTOR; MEMBRANE PROTEIN;

ACIDITY; ANIMAL CELL; ARTICLE; CELL STRAIN COS1; DISSOCIATION; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; PH; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON TRANSPORT; ANIMAL; CERCOPITHECUS; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; REGULATOR GENE; SOLUBILITY; TITRIMETRY;

ALANINE; ANIMALS; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; COS CELLS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENES, SWITCH; GOLGI APPARATUS; HISTIDINE; HYDROGEN-ION CONCENTRATION; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, LDL; SOLUBILITY; TITRIMETRY;

EID: 33744802244     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.04.011     Document Type: Article

References (44)

1. Battey F.D., Gafvels M.E., FitzGerald D.J., Argraves W.S., Chappell D.A., Strauss III J.F., and Strickland D.K. The 39-kDa receptor-associated protein regulates ligand binding by the very low density lipoprotein receptor. J. Biol. Chem. 269 (1994) 23268-23273
2. Bu G., and Rennke S. Receptor-associated protein is a folding chaperone for low density lipoprotein receptor-related protein. J. Biol. Chem. 271 (1996) 22218-22224
3. Bu G., Geuze H.J., Strous G.J., and Schwartz A.L. 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J. 14 (1995) 2269-2280
4. Clore G.M., and Gronenborn A.M. Multidimensional heteronuclear nuclear-magnetic-resonance of proteins. Methods Enzymol. 239 (1994) 349-363
5. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
6. Demaurex N. pH Homeostasis of cellular organelles. News Physiol. Sci. 17 (2002) 1-5
7. Fisher C., Beglova N., and Blacklow S.C. Structure of an LDL-RAP complex reveals a general mode for ligand recognition by lipoprotein receptors. Mol. Cell 22 (2006) 277-283
8. Gardai S.J., McPhillips K.A., Frasch S.C., Janssen W.J., Starefeldt A., Murphy-Ullrich J.E., Bratton D.L., Oldenborg P.A., Michalak M., and Henson P.M. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123 (2005) 321-334
9. Grzesiek S., and Bax A. An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins. J. Magn. Reson. 99 (1992) 201-207
10. Grzesiek S., Anglister J., and Bax A. Correlation of backbone amide and aliphatic side-chain resonances in C-13/N-15-enriched proteins by isotropic mixing of C-13 magnetization. J. Magn. Reson. 101 (1993) 114-119
11. Guntert P., Mumenthaler C., and Wuthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273 (1997) 283-298
12. Herrmann T., Guntert P., and Wuthrich K. Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR 24 (2002) 171-189
13. Herrmann T., Guntert P., and Wuthrich K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319 (2002) 209-227
14. Herz J., and Strickland D.K. LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108 (2001) 779-784
15. Herz J., Goldstein J.L., Strickland D.K., Ho Y.K., and Brown M.S. 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J. Biol. Chem. 266 (1991) 21232-21238
16. Hsieh J.C., Lee L., Zhang L., Wefer S., Brown K., DeRossi C., Wines M.E., Rosenquist T., and Holdener B.C. Mesd encodes an LRP5/6 chaperone essential for specification of mouse embryonic polarity. Cell 112 (2003) 355-367
17. Kenworthy A.K. Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 24 (2001) 289-296
18. Koradi R., Billeter M., and Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1996) 51-55
19. Krieger M., and Herz J. Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu. Rev. Biochem. 63 (1994) 601-637
20. Laskowski R.A., Macarthur M.W., Moss D.S., and Thornton J.M. Procheck: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
21. Lazic A., Dolmer K., Strickland D.K., and Gettins P.G. Structural organization of the receptor associated protein. Biochemistry 42 (2003) 14913-14920
22. Lee, D. (2003). NMR studies on the structure and function of the Bombyx mori pheromone-binding protein, PhD thesis, Swiss Federal Institute of Technology, Zürich, Zürich.
23. Lee D., Pervushin K., Bischof D., Braun M., and Thony-Meyer L. Unusual heme-histidine bond in the active site of a chaperone. J. Am. Chem. Soc. 127 (2005) 3716-3717
24. Loukinova E., Ranganathan S., Kuznetsov S., Gorlatova N., Migliorini M.M., Loukinov D., Ulery P.G., Mikhailenko I., Lawrence D.A., and Strickland D.K. Platelet-derived growth factor (PDGF)-induced tyrosine phosphorylation of the low density lipoprotein receptor-related protein (LRP). Evidence for integrated co-receptor function betwenn LRP and the PDGF. J. Biol. Chem. 277 (2002) 15499-15506
25. Medved L.V., Migliorini M., Mikhailenko I., Barrientos L.G., Llinas M., and Strickland D.K. Domain organization of the 39-kDa receptor-associated protein. J. Biol. Chem. 274 (1999) 717-727
26. Meissner A., and Sorensen O.W. Optimization of three-dimensional TROSY-type HCCH NMR correlation of aromatic (1)H-(13)C groups in proteins. J. Magn. Reson. 139 (1999) 447-450
27. Meissner A., and Sorensen O.W. Suppression of diagonal peaks in three-dimensional protein NMR TROSY-type HCCH correlation experiments. J. Magn. Reson. 144 (2000) 171-174
28. Migliorini M.M., Behre E.H., Brew S., Ingham K.C., and Strickland D.K. Allosteric modulation of ligand binding to low density lipoprotein receptor-related protein by the receptor-associated protein requires critical lysine residues within its carboxyl-terminal domain. J. Biol. Chem. 278 (2003) 17986-17992
29. Nielsen P.R., Ellgaard L., Etzerodt M., Thogersen H.C., and Poulsen F.M. The solution structure of the N-terminal domain of alpha2- macroglobulin receptor-associated protein. Proc. Natl. Acad. Sci. USA 94 (1997) 7521-7525
30. Obermoeller L.M., Warshawsky I., Wardell M.R., and Bu G. Differential functions of triplicated repeats suggest two independent roles for the receptor-associated protein as a molecular chaperone. J. Biol. Chem. 272 (1997) 10761-10768
31. Pelton J.G., Torchia D.A., Meadow N.D., and Roseman S. Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci. 2 (1993) 543-558
32. Pervushin K., Riek R., Wider G., and Wuthrich K. Transverse relaxation-optimized spectroscopy (TROSY) for NMR studies of aromatic spin systems in C-13-labeled proteins. J. Am. Chem. Soc. 120 (1998) 6394-6400
33. Sarti M., Farquhar M.G., and Orlando R.A. The receptor-associated protein (RAP) interacts with several resident proteins of the endoplasmic reticulum including a glycoprotein related to actin. Exp. Cell Res. 260 (2000) 199-207
34. Strickland D.K., and Ranganathan S. Diverse role of LDL receptor-related protein in the clearance of proteases and in signaling. J. Thromb. Haemost. 1 (2003) 1663-1670
35. Strickland D.K., Ashcom J.D., Williams S., Battey F., Behre E., McTigue K., Battey J.F., and Argraves W.S. Primary structure of a 2 -macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J. Biol. Chem. 266 (1991) 13364-13369
36. Strickland D.K., Gonias S.L., and Argraves W.S. Diverse roles for the LDL receptor family. Trends Endocrinol. Metab. 13 (2002) 66-74
37. Vuister G.W., and Bax A. Measurement of four-bond HN-H-alpha J-couplings in staphylococcal nuclease. J. Biomol. NMR 4 (1994) 193-200
38. Wei W., Lu Q., Chaudry G.J., Leppla S.H., and Cohen S.N. The LDL receptor-related protein LRP6 mediates internalization and lethality of anthrax toxin. Cell 124 (2006) 1141-1154
39. Williams S.E., Ashcom J.D., Argraves W.S., and Strickland D.K. A novel mechanism for controlling the activity of a 2 -macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein. J. Biol. Chem. 267 (1992) 9035-9040
40. Willnow T.E., Armstrong S.A., Hammer R.E., and Herz J. Functional expression of low density lipoprotein receptor-related protein is controlled by receptor-associated protein in vivo. Proc. Natl. Acad. Sci. USA 92 (1995) 4537-4541
41. Willnow T.E., Rohlmann A., Horton J., Otani H., Braun J.R., Hammer R.E., and Herz J. RAP, a specialized chaperone, prevents ligand-induced ER retention and degradation of LDL receptor-related endocytic receptors. EMBO J. 15 (1996) 2632-2639
42. Wu Y., Migliorini M., Walsh J., Yu P., Strickland D.K., and Wang Y.X. NMR structural studies of domain 1 of receptor-associated protein. J. Biomol. NMR 29 (2004) 271-279
43. Yamazaki T., Formankay J.D., and Kay L.E. 2-dimensional NMR experiments for correlating C-13-beta and H- 1-delta/epsilon chemical-shifts of aromatic residues in C-13-labeled proteins via scalar couplings. J. Am. Chem. Soc. 115 (1993) 11054-11055
44. Yepes M., Sandkvist M., Moore E.G., Bugge T.H., Strickland D.K., and Lawrence D.A. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Invest. 112 (2003) 1533-1540