NMR study of ligand release from asialoglycoprotein receptor under solution conditions in early endosomes

FEBS Journal

Volumn 279, Issue 15, 2012, Pages 2645-2656

  Onizuka, Takuo ^a,b   Shimizu, Hiroyuki ^a   Moriwaki, Yuka ^a   Nakano, Takayuki ^a   Kanai, Shozo ^a   Shimada, Ichio ^b,c   Takahashi, Hideo ^b,d  

^a Japan Biological Informatics Consortium   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

asialoglycoprotein receptor; Ca2+; cooperativity; ligand release; NMR

Indexed keywords

ASIALOGLYCOPROTEIN RECEPTOR; C TYPE LECTIN RECEPTOR; CALCIUM ION; LECTIN RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CONCENTRATION (PARAMETERS); ENDOCYTOSIS; ENDOSOME; LIGAND BINDING; LIGAND RELEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; SECRETION (PROCESS); SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ASIALOGLYCOPROTEIN RECEPTOR; CALCIUM; CIRCULAR DICHROISM; ENDOSOMES; GALACTOSE; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SOLUTIONS; SURFACE PLASMON RESONANCE;

EID: 84863845301     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08643.x     Document Type: Article

References (39)

1. Weigel PH, &, Yik JHN, (2002) Glycans as endocytosis signals: the cases of the asialoglycoprotein and hyaluronan/chondroitin sulfate receptors. Biochim Biophys Acta 1572, 341-363.
2. Zelensky AN, &, Gready JE, (2005) The C-type lectin-like domain superfamily. FEBS J 272, 6179-6217.
3. Rumjantseva V, Grewal PK, Wandall HH, Josefsson EC, Sorensen AL, Larson G, Marth JD, Hartwig JH, &, Hoffmeister KM, (2009) Dual roles for hepatic receptors in the clearance of chilled platelets. Nat Med 15, 1273-1280.
4. Spiess M, (1990) The asialoglycoprotein receptor: a model for endocytic transport receptors. Biochemistry 29, 10009-10018.
5. Steirer LM, Park EI, Townsend RR, &, Baenziger JU, (2009) The asialoglycoprotein receptor regulates levels of plasma glycoproteins terminating with sialic acid α2,6-galactose. J Biol Chem 284, 3777-3783.
6. Grewal PK, Uchiyama S, Ditto D, Varki N, Le DT, Nizet V, &, Marth JD, (2008) The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med 14, 648-655.
7. Bareford LM, &, Swaan PW, (2007) Endocytic mechanisms for targeted drug delivery. Adv Drug Deliv Rev 59, 748-758.
8. Kolatkar AR, &, Weis WI, (1996) Structural basis of galactose recognition by C-type animal lectins. J Biol Chem 271, 6679-6685.
9. Kolatkar AR, Leung AK, Isecke R, Brossmer R, Drickamer K, &, Weis WI, (1998) Mechanism of N-acetylgalactosamine binding to a C-type animal lectin carbohydrate-recognition domain. J Biol Chem 273, 19502-19508.
10. Feinberg H, Torgersen D, Drickamer K, &, Weis WI, (2000) Mechanism of pH-dependent N-acetylgalactosamine binding by a functional mimic of the hepatocyte asialoglycoprotein receptor. J Biol Chem 275, 35176-35184.
11. Meier M, Bider MD, Malashkevich VN, Spiess M, &, Burkhard P, (2000) Crystal structure of the carbohydrate recognition domain of the H1 subunit of the asialoglycoprotein receptor. J Mol Biol 300, 857-865.
12. Oka JA, &, Weigel PH, (1983) Recycling of the asialoglycoprotein receptor in isolated rat hepatocytes. Dissociation of internalized ligand from receptor occurs in two kinetically and thermally distinguishable compartments. J Biol Chem 258, 10253-10262.
13. Yamashiro DJ, &, Maxfield FR, (1988) Regulation of endocytic processes by pH. Trends Pharmacol Sci 9, 190-193.
14. Wragg S, &, Drickamer K, (1999) Identification of amino acid residues that determine pH dependence of ligand binding to the asialoglycoprotein receptor during endocytosis. J Biol Chem 274, 35400-35406.
15. Gerasimenko JV, Tepikin AV, Petersen OH, &, Gerasimenko OV, (1998) Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr Biol 8, 1335-1338.
16. 2+-binding helix-loop-helix EF-hand motifs. Biochem J 405, 199-221.
17. Saito M, Hanson PI, &, Schlesinger P, (2007) Luminal chloride-dependent activation of endosome calcium channels. J Biol Chem 282, 27327-27333.
18. Lelouvier B, &, Puertollano R, (2011) Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway. J Biol Chem 286, 9826-9832.
19. 2+ and N-ethylmaleimide-sensitive factor differentially regulate disassembly of SNARE complexes on early endosomes. J Biol Chem 279, 18270-18276.
20. Stokmaier D, Khorev O, Cutting B, Born R, Ricklin D, Ernst TOG, Boni F, Schwingruber K, Gentner M, Wittwer M, et al. (2009) Design, synthesis and evaluation of monovalent ligands for the asialoglycoprotein receptor (ASGP-R). Bioorg Med Chem 17, 7254-7264.
21. Mullin NP, Hall KT, &, Taylor ME, (1994) Characterization of ligand binding to a carbohydrate-recognition domain of the macrophage mannose receptor. J Biol Chem 269, 28405-28413.
22. Weis WI, Crichlow GV, Murthy HM, Hendrickson WA, &, Drickamer K, (1991) Physical characterization and crystallization of the carbohydrate- recognition domain of a mannose-binding protein from rat. J Biol Chem 266, 20678-20686.
23. Nielbo S, Thomsen JK, Graversen JH, Jensen PH, Etzerodt M, Poulsen FM, &, Thogersen HC, (2004) Structure of the plasminogen kringle 4 binding calcium-free form of the C-type lectin-like domain of tetranectin. Biochemistry 43, 8636-8643.
24. 2+-dependent structural changes in C-type mannose-binding proteins. Biochemistry 37, 17965-17976.
25. Posget SF, Freund SM, Howard MJ, &, Bycroft M, (2001) The ligand-binding loops in the tunicate C-type lectin TC14 are rigid. Biochemistry 40, 10966-10972.
26. Feinberg H, Mitchell DA, Drickamer K, &, Weis WI, (2001) Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294, 2163-2166.
27. Hakansson K, Lim NK, Hoppe HJ, &, Reid KB, (1999) Crystal structure of the trimeric alpha-herical coiled-coil and the three lectin domains of human lung surfactant protein D. Structure 7, 255-264.
28. Lundell A, Olin AI, Morgelin M, al-Karadaghi S, Aspberg A, &, Logan DT, (2004) Structural basis for interactions between tenacins and lectican C-type lectin domains: evidence for a crosslinking role for tenascins. Structure (Camb) 12, 1495-1506.
29. Blomhoff R, Tolleshaug H, &, Berg T, (1982) Binding of calcium ions to the isolated asialo-glycoprotein receptor. Implications for receptor function in suspended hepatocytes. J Biol Chem 257, 7456-7459.
30. 2+ and phosphatidylinositol 4,5-bisphosphate binding by the C2A domain of rabphilin-3A. J Biol Chem 283, 35918-35928.
31. Mizuno H, Fujimoto Z, Koizumi M, Kano H, Atoda H, &, Morita T, (1997) Structure of coagulation factors IX/X-binding protein, a heterodimer of C-type lectin domains. Nat Struct Biol 4, 438-441.
32. Biekofsky RR, &, Feeney J, (1998) Co-operative cyclic interactions involved in metal binding to pairs of sites in EF-hand proteins. FEBS Lett 439, 101-106.
33. Thompson JD, Higgins DG, &, Gibson TJ, (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
34. Endo S, Tomimoto Y, Shimizu H, Taniguchi Y, &, Onizuka T, (2006) Effects of E. coli chaperones on the solubility of human receptors in an in vitro expression system. Mol Biotechnol 33, 199-209.
35. Pace CN, Vajdos L, Fee L, Grimsley G, &, Gray T, (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4, 2411-2423.
36. Cavanagh J, Fairbrother WJ, Palmer AGIII, Rance M, &, Skelton NL, (1996) Protein NMR Spectroscopy: Principles and Practice. Academic Press, San Diego, CA.
37. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, &, Bax A, (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277-293.
38. Keller R, (2004) The Computer-aided Resonance Assignment Tutorial. Cantina Verlag, Goldau, Switzerland.
39. Garrett DS, Seok YJ, Peterkofsky A, Clore GM, &, Gronenborn AM, (1997) Identification by NMR of the binding surface for the histidine-containing phosphocarrier protein HPr on the N-terminal domain of enzyme I of the Escherichia coli phosphotransferase system. Biochemistry 36, 4393-4398.