Crystal structure of the conserved domain of the DC lysosomal associated membrane protein: implications for the lysosomal glycocalyx
详细信息 查看全文
- 作者：Sonja Wilke (1)
Joern Krausze (1)
Konrad Büssow (1) - 刊名：BMC Biology
- 出版年：2012
- 出版时间：December 2012
- 年：2012
- 卷：10
- 期：1
- 全文大小：1148KB
- 参考文献：1. Braulke T, Bonifacino JS: Sorting of lysosomal proteins. / Biochim Biophys Acta 2009, 1793:605-14. CrossRef
2. Huotari J, Helenius A: Endosome maturation. / Embo J 2011, 30:3481-500. CrossRef
3. Pillay CS, Elliott E, Dennison C: Endolysosomal proteolysis and its regulation. / Biochem J 2002, 363:417-29. CrossRef
4. Luzio JP, Pryor PR, Bright NA: Lysosomes: fusion and function. / Nat Rev Mol Cell Biol 2007, 8:622-32. CrossRef
5. Bright NA, Gratian MJ, Luzio JP: Endocytic delivery to lysosomes mediated by concurrent fusion and kissing events in living cells. / Curr Biol 2005, 15:360-65. CrossRef
6. Pryor PR, Mullock BM, Bright NA, Gray SR, Luzio JP: The role of intraorganellar Ca 2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. / J Cell Biol 2000, 149:1053-062. CrossRef
7. Henell F, Ericsson JL, Glaumann H: Degradation of phagocytosed lysosomes by Kupffer cell lysosomes. / Lab Invest 1983, 48:556-64.
8. Neiss WF: A coat of glycoconjugates on the inner surface of the lysosomal membrane in the rat kidney. / Histochemistry 1984, 80:603-08.
9. Neiss WF: / Ultrachemistry of Intracellular Membrane Glycoconjugates. Berlin, Heidelberg: Springer-Verlag; 1986. CrossRef
10. Ebong EE, Macaluso FP, Spray DC, Tarbell JM: Imaging the endothelial glycocalyx in vitro by rapid freezing/freeze substitution transmission electron microscopy. / Arterioscler Thromb Vasc Biol 2011, 31:1908-915. CrossRef
11. Saftig P: Lysosomal membrane proteins. In / Lysosomes. Edited by: Saftig P. New York: Springer; 2005:37-9. CrossRef
12. Carlsson SR, Fukuda M: The polylactosaminoglycans of human lysosomal membrane glycoproteins lamp-1 and lamp-2. Localization on the peptide backbones. / J Biol Chem 1990, 265:20488-0495.
13. Carlsson SR, Fukuda M: Structure of human lysosomal membrane glycoprotein 1. Assignment of disulfide bonds and visualization of its domain arrangement. / J Biol Chem 1989, 264:20526-0531.
14. Chen JW, Pan W, D'Souza MP, August JT: Lysosome-associated membrane proteins: Characterization of LAMP-1 of macrophage P388 and mouse embryo 3T3 cultured cells. / Arch Biochem Biophys 1985, 239:574-86. CrossRef
15. Furuta K, Yang X-L, Chen J-S, Hamilton SR, August JT: Differential expression of the lysosome-associated membrane proteins in normal human tissues. / Arch Biochem Biophys 1999, 365:75-2. CrossRef
16. Andrejewski N, Punnonen EL, Guhde G, Tanaka Y, Lullmann-Rauch R, Hartmann D, von Figura K, Saftig P: Normal lysosomal morphology and function in LAMP-1-deficient mice. / J Biol Chem 1999, 274:12692-2701. CrossRef
17. Tanaka Y, Guhde G, Suter A, Eskelinen EL, Hartmann D, Lullmann-Rauch R, Janssen PM, Blanz J, von Figura K, Saftig P: Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. / Nature 2000, 406:902-06. CrossRef
18. Eskelinen EL, Schmidt CK, Neu S, Willenborg M, Fuertes G, Salvador N, Tanaka Y, Lullmann-Rauch R, Hartmann D, Heeren J, von Figura K, Knecht E, Saftig P: Disturbed cholesterol traffic but normal proteolytic function in LAMP-1/LAMP-2 double-deficient fibroblasts. / Mol Biol Cell 2004, 15:3132-145. CrossRef
19. Nishino I, Fu J, Tanji K, Yamada T, Shimojo S, Koori T, Mora M, Riggs JE, Oh SJ, Koga Y, Sue CM, Yamamoto A, Murakami N, Shanske S, Byrne E, Bonilla E, Nonaka I, DiMauro S, Hirano M: Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). / Nature 2000, 406:906-10. CrossRef
20. Saftig P, Beertsen W, Eskelinen EL: LAMP-2: a control step for phagosome and autophagosome maturation. / Autophagy 2008, 4:510-12.
21. Huynh KK, Eskelinen EL, Scott CC, Malevanets A, Saftig P, Grinstein S: LAMP proteins are required for fusion of lysosomes with phagosomes. / Embo J 2007, 26:313-24. CrossRef
22. Binker MG, Cosen-Binker LI, Terebiznik MR, Mallo GV, McCaw SE, Eskelinen EL, Willenborg M, Brumell JH, Saftig P, Grinstein S, Gray-Owen SD: Arrested maturation of Neisseria-containing phagosomes in the absence of the lysosome-associated membrane proteins, LAMP-1 and LAMP-2. / Cell Microbiol 2007, 9:2153-166. CrossRef
23. Beertsen W, Willenborg M, Everts V, Zirogianni A, Podschun R, Schroder B, Eskelinen EL, Saftig P: Impaired phagosomal maturation in neutrophils leads to periodontitis in lysosomal-associated membrane protein-2 knockout mice. / J Immunol 2008, 180:475-82.
24. Schneede A, Schmidt CK, Holtta-Vuori M, Heeren J, Willenborg M, Blanz J, Domanskyy M, Breiden B, Brodesser S, Landgrebe J, Sandhoff K, Ikonen E, Saftig P, Eskelinen EL: Role for LAMP-2 in endosomal cholesterol transport. / J Cell Mol Med 2011, 15:280-95. CrossRef
25. Granger BL, Green SA, Gabel CA, Howe CL, Mellman I, Helenius A: Characterization and cloning of lgp110, a lysosomal membrane glycoprotein from mouse and rat cells. / J Biol Chem 1990, 265:12036-2043.
26. Kundra R, Kornfeld S: Asparagine-linked oligosaccharides protect Lamp-1 and Lamp-2 from intracellular proteolysis. / J Biol Chem 1999, 274:31039-1046. CrossRef
27. Kon M, Cuervo AM: Chaperone-mediated autophagy in health and disease. / Febs lett 2010, 584:1399-404. CrossRef
28. Bandyopadhyay U, Kaushik S, Varticovski L, Cuervo AM: The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. / Mol Cell Biol 2008, 28:5747-763. CrossRef
29. Zhang C, Cuervo AM: Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. / Nat Med 2008, 14:959-65. CrossRef
30. de Saint-Vis B, Vincent J, Vandenabeele S, Vanbervliet B, Pin JJ, Ait-Yahia S, Patel S, Mattei MG, Banchereau J, Zurawski S, Davoust J, Caux C, Lebecque S: A novel lysosome-associated membrane glycoprotein, DC-LAMP, induced upon DC maturation, is transiently expressed in MHC class II compartment. / Immunity 1998, 9:325-36. CrossRef
31. Defays A, David A, de Gassart A, De Angelis Rigotti F, Wenger T, Camossetto V, Brousset P, Petrella T, Dalod M, Gatti E, Pierre P: BAD-LAMP is a novel biomarker of nonactivated human plasmacytoid dendritic cells. / Blood 2011, 118:609-17. CrossRef
32. Rabinowitz SS, Gordon S: Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli. / J Exp Med 1991, 174:827-36. CrossRef
33. Salaun B, de Saint-Vis B, Clair-Moninot V, Pin J-J, Barthélemy-Dubois C, Kissenpfennig A, Peronne C, Bates E, Mattei M-G, Lebecque S: Cloning and characterization of the mouse homologue of the human dendritic cell maturation marker CD208/DC-LAMP. / Eur JImmunol 2003, 33:2619-629. CrossRef
34. Salaun B, de Saint-Vis B, Pacheco N, Pacheco Y, Riesler A, Isaac S, Leroux C, Clair-Moninot V, Pin JJ, Griffith J, Treilleux I, Goddard S, Davoust J, Kleijmeer M, Lebecque S: CD208/dendritic cell-lysosomal associated membrane protein is a marker of normal and transformed type II pneumocytes. / Am J Pathol 2004, 164:861-71. CrossRef
35. Debbabi H, Ghosh S, Kamath AB, Alt J, Demello DE, Dunsmore S, Behar SM: Primary type II alveolar epithelial cells present microbial antigens to antigen-specific CD4 + T cells. / Am J Physiol Lung Cell Mol Physiol 2005, 289:L274-79. CrossRef
36. Gereke M, Jung S, Buer J, Bruder D: Alveolar type II epithelial cells present antigen to CD4(+) T cells and induce Foxp3(+) regulatory T cells. / Am J Respir Crit Care Med 2009, 179:344-55. CrossRef
37. Wu Z, Hu T, Butter C, Kaiser P: Cloning and characterization of the chicken orthologue of dendritic cell-lysosomal associated membrane protein (DC-LAMP). / Dev Comp Immunol 2010, 34:183-88. CrossRef
38. Wilke S, Groebe L, Maffenbeier V, J?ger V, Gossen M, Josewski J, Duda A, Polle L, Owens RJ, Wirth D, Heinz DW, van den Heuvel J, Büssow K: Streamlining homogeneous glycoprotein production for biophysical and structural applications by targeted cell line development. / Plos One 2011, 6:e27829. CrossRef
39. Wilke S, Krausze J, Gossen M, Groebe L, J?ger V, Gherardi E, van den Heuvel J, Büssow K: Glycoprotein production for structure analysis with stable, glycosylation mutant CHO cell lines established by fluorescence-activated cell sorting. / Protein Sci 2010, 19:1264-271. CrossRef
40. Krissinel E, Henrick K: Inference of macromolecular assemblies from crystalline state. / J Mol Biol 2007, 372:774-97. CrossRef
41. Murzin AG, Brenner SE, Hubbard T, Chothia C: SCOP: a structural classification of proteins database for the investigation of sequences and structures. / J Mol Biol 1995, 247:536-40.
42. Chan AW, Hutchinson EG, Harris D, Thornton JM: Identification, classification, and analysis of beta-bulges in proteins. / Protein Sci 1993, 2:1574-590. CrossRef
43. Tremblay DM, Tegoni M, Spinelli S, Campanacci V, Blangy S, Huyghe C, Desmyter A, Labrie S, Moineau S, Cambillau C: Receptor-binding protein of Lactococcus lactis phages: identification and characterization of the saccharide receptor-binding site. / J Bacteriol 2006, 188:2400-410. CrossRef
44. McMahon SA, Miller JL, Lawton JA, Kerkow DE, Hodes A, Marti-Renom MA, Doulatov S, Narayanan E, Sali A, Miller JF, Ghosh P: The C-type lectin fold as an evolutionary solution for massive sequence variation. / Nat Struct Mol Biol 2005, 12:886-92. CrossRef
45. Jentoft N: Why are proteins O-glycosylated? / Trends Biochem Sci 1990, 15:291-94. CrossRef
46. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A: Comparative protein structure modeling using MODELLER. / Curr Protoc Bioinformatics 2006.,Chapter 5(Unit 5 6):
47. Bohne-Lang A, von der Lieth CW: GlyProt: in silico glycosylation of proteins. / Nucleic Acids Res 2005, 33:W214-19. CrossRef
48. GLYCAM Web [http://www.glycam.com]
49. Javadpour MM, Eilers M, Groesbeek M, Smith SO: Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. / Biophys J 1999, 77:1609-618. CrossRef
50. Demirel ?, Jan I, Wolters D, Blanz J, Saftig P, Tampé R, Abele R: The lysosomal polypeptide transporter TAPL is stabilized by the interaction with LAMP-1 and LAMP-2. / J Cell Sci 2012, in press.
51. Schuske K, Palfreyman MT, Watanabe S, Jorgensen EM: UNC-46 is required for trafficking of the vesicular GABA transporter. / Nat Neurosci 2007, 10:846-53. CrossRef
52. Griffiths G, Back R, Marsh M: A quantitative analysis of the endocytic pathway in baby hamster kidney cells. / J Cell Biol 1989, 109:2703-720. CrossRef
53. Griffiths G, Fuller SD, Back R, Hollinshead M, Pfeiffer S, Simons K: The dynamic nature of the Golgi complex. / J Cell Biol 1989, 108:277-97. CrossRef
54. Schr?der BA, Wrocklage C, Hasilik A, Saftig P: The proteome of lysosomes. / Proteomics 2010, 10:4053-076. CrossRef
55. Reitsma S, Slaaf D, Vink H, van Zandvoort M, oude Egbrink M: The endothelial glycocalyx: composition, functions, and visualization. / Pflügers Arch 2007, 454:345-59. CrossRef
56. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ: Jalview Version 2--a multiple sequence alignment editor and analysis workbench. / Bioinformatics 2009, 25:1189-191. CrossRef
57. Katoh K, Asimenos G, Toh H: Multiple alignment of DNA sequences with MAFFT. / Methods Mol Biol 2009, 537:39-4. CrossRef
58. Guex N, Peitsch MC: SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling. / Electrophoresis 1997, 18:2714-723. CrossRef
59. Carlsson SR, Lycksell PO, Fukuda M: Assignment of O-glycan attachment sites to the hinge-like regions of human lysosomal membrane glycoproteins lamp-1 and lamp-2. / Arch Biochem Biophys 1993, 304:65-3. CrossRef
60. Case DA, Darden TA, Cheatham TE III, Simmerling CL, Wang J, Duke RE, Luo R, Walker RC, Zhang W, Merz KM, Roberts B, Wang B, Hayik S, Roitberg A, Seabra G, Kolossvary I, Wong FK, Paesani F, Vanicek J, Liu J, Wu X, Brozell SR, Steinbrecher T, Gohlke H, Cai Q, Ye X, Wang J, Hsieh M-J, Cui G, Roe DR, / et al.: / AMBER11. San Francisco: University of California; 2010.
61. Kirschner KN, Yongye AB, Tschampel SM, Gonzalez-Outeirino J, Daniels CR, Foley BL, Woods RJ: GLYCAM06: a generalizable biomolecular force field. Carbohydrates. / J Comput Chem 2008, 29:622-55. CrossRef
62. Kabsch W: XDS. / Acta Crystallogr D 2010, 66:125-32. CrossRef
63. Matthews BW: Solvent content of protein crystals. / J Mol Biol 1968, 33:491-97. CrossRef
64. Vagin A, Teplyakov A: MOLREP: An automated programm for molecular replacement. / J Appl Crystallogr 1997, 30:1022-025. CrossRef
65. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH: PHENIX: a comprehensive Python-based system for macromolecular structure solution. / Acta Crystallogr D 2010, 66:213-21. CrossRef
66. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ: Phaser crystallographic software. / J Appl Crystallogr 2007, 40:658-74. CrossRef
67. Emsley P, Cowtan K: Coot: model-building tools for molecular graphics. / Acta Crystallogr D 2004, 60:2126-132. CrossRef
68. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE: UCSF Chimera--a visualization system for exploratory research and analysis. / J Comput Chem 2004, 25:1605-612. CrossRef
69. Kabsch W, Sander C: Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. / Biopolymers 1983, 22:2577-637. CrossRef
70. Ho BK, Gruswitz F: HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. / BMC Struct Biol 2008, 8:49. CrossRef - 作者单位：Sonja Wilke (1)
Joern Krausze (1)
Konrad Büssow (1)
1. Department of Molecular Structural Biology, Helmholtz Centre for Infection Research, Inhoffenstr. 7, 38124, Braunschweig, Germany
文摘
Background The family of lysosome-associated membrane proteins (LAMP) comprises the multifunctional, ubiquitous LAMP-1 and LAMP-2, and the cell type-specific proteins DC-LAMP (LAMP-3), BAD-LAMP (UNC-46, C20orf103) and macrosialin (CD68). LAMPs have been implicated in a multitude of cellular processes, including phagocytosis, autophagy, lipid transport and aging. LAMP-2 isoform A acts as a receptor in chaperone-mediated autophagy. LAMP-2 deficiency causes the fatal Danon disease. The abundant proteins LAMP-1 and LAMP-2 are major constituents of the glycoconjugate coat present on the inside of the lysosomal membrane, the 'lysosomal glycocalyx'. The LAMP family is characterized by a conserved domain of 150 to 200 amino acids with two disulfide bonds. Results The crystal structure of the conserved domain of human DC-LAMP was solved. It is the first high-resolution structure of a heavily glycosylated lysosomal membrane protein. The structure represents a novel β-prism fold formed by two β-sheets bent by β-bulges and connected by a disulfide bond. Flexible loops and a hydrophobic pocket represent possible sites of molecular interaction. Computational models of the glycosylated luminal regions of LAMP-1 and LAMP-2 indicate that the proteins adopt a compact conformation in close proximity to the lysosomal membrane. The models correspond to the thickness of the lysosomal glycoprotein coat of only 5 to 12 nm, according to electron microscopy. Conclusion The conserved luminal domain of lysosome-associated membrane proteins forms a previously unknown β-prism fold. Insights into the structure of the lysosomal glycoprotein coat were obtained by computational models of the LAMP-1 and LAMP-2 luminal regions.