Analysis of nidogen-1/laminin γ1 interaction by cross-linking, mass spectrometry, and computational modeling reveals multiple binding modes

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Lössl, Philip ^a,d   Kölbel, Knut ^a   Tänzler, Dirk ^a   Nannemann, David ^b   Ihling, Christian H ^a   Keller, Manuel V ^c   Schneider, Marian ^a   Zaucke, Frank ^c   Meiler, Jens ^b   Sinz, Andrea ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; BIS(SULFOSUCCINIMIDYL)GLUTARATE; ENTACTIN; GLUTARIC ACID; LAMININ GAMMA1; LEUCINE; METHIONINE; MULTIPROTEIN COMPLEX; NIDOGEN 1; PROTEIN VARIANT; UNCLASSIFIED DRUG; CROSS LINKING REAGENT; LAMININ; MEMBRANE PROTEIN;

AB INITIO CALCULATION; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; ENZYME LINKED IMMUNOSORBENT ASSAY; KINETICS; MASS SPECTROMETRY; MATHEMATICAL MODEL; PHOTOREACTIVITY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; ULTRAVIOLET RADIATION; ANIMAL; CHEMISTRY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR MODEL; MOUSE; PROTEIN TERTIARY STRUCTURE; TANDEM MASS SPECTROMETRY;

ANIMALS; CROSS-LINKING REAGENTS; HEK293 CELLS; HUMANS; KINETICS; LAMININ; MEMBRANE GLYCOPROTEINS; MICE; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; SURFACE PLASMON RESONANCE; TANDEM MASS SPECTROMETRY;

EID: 84915819201     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112886     Document Type: Article

References (70)

1. Yurchenco PD, O'Rear JJ (1994) Basal lamina assembly. Curr Opin Cell Biol 6 (5): 674-681.
2. Yurchenco PD (2011) Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb Perspect Biol 3 (2): a004911.
3. Timpl R, Rohde H, Robey PG, Rennard SI, Foidart JM, et al. (1979) Laminin-a glycoprotein from basement membranes. J Biol Chem 254 (19): 9933-9937.
4. Tunggal P, Smyth N, Paulsson M, Ott MC (2000) Laminins: structure and genetic regulation. Microsc Res Techniq 51 (3): 214-227.
5. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, et al. (2005) A simplified laminin nomenclature. Matrix Biol 24 (5): 326-332.
6. Beck K, Hunter I, Engel J (1990) Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J 4 (2): 148-160.
7. Kalkhof S, Haehn S, Paulsson M, Smyth N, Meiler J, et al. (2010) Computational modeling of laminin N-terminal domains using sparse distance constraints from disulfide bonds and chemical cross-linking. Proteins 78 (16): 3409-3427.
8. Carlin B, Jaffe R, Bender B, Chung AE (1981) Entactin, a novel basal lamina-associated sulfated glycoprotein. J Biol Chem 256 (10): 5209-5214.
9. Kohfeldt E, Sasaki T, Göhring W, Timpl R (1998) Nidogen-2: a new basement membrane protein with diverse binding properties. J Mol Biol 282 (1): 99-109.
10. Timpl R, Dziadek M, Fujiwara S, Nowack H, Wick G (1983) Nidogen: a new, self-aggregating basement membrane protein. Eur J Biochem 137 (3): 455-465.
11. Salmivirta K (2002) Binding of mouse nidogen-2 to basement membrane components and cells and its expression in embryonic and adult tissues suggest complementary functions of the two nidogens. Exp Cell Res 279 (2): 188-201.
12. Miosge N, Sasaki T, Timpl R (2002) Evidence of nidogen-2 compensation for nidogen-1 deficiency in transgenic mice. Matrix Biol 21 (7): 611-621.
13. Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, et al. (1991) Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10 (11): 3137-3146.
14. Ho MSP, Boese K, Mokkapati S, Nischt R, Smyth N (2008) Nidogens-extracellular matrix linker molecules. Microsc Res Techniq 71 (5): 387-395.
15. Dziadek M, Paulsson M, Timpl R (1985) Identification and interaction repertoire of large forms of the basement membrane protein nidogen. EMBO J 4 (10): 2513-2518.
16. Paulsson M, Aumailley M, Deutzmann R, Timpl R, Beck K, et al. (1987) Laminin-nidogen complex. Extraction with chelating agents and structural characterization. Eur J Biochem 166 (1): 11-19.
17. Mann K, Deutzmann R, Timpl R (1988) Characterization of proteolytic fragments of the laminin-nidogen complex and their activity in ligand-binding assays. Eur J Biochem 178 (1): 71-80.
18. Mayer U, Nischt R, Pöschl E, Mann K, Fukuda K, et al. (1993) A single EGF-like motif of laminin is responsible for high affinity nidogen binding. EMBO J 12 (5): 1879-1885.
19. Gerl M, Mann K, Aumailley M, Timpl R (1991) Localization of a major nidogen-binding site to domain III of laminin B2 chain. Eur J Biochem 202 (1): 167-174.
20. Baumgartner R, Czisch M, Mayer U, Pöschl E, Huber R, et al. (1996) Structure of the nidogen binding LE module of the laminin gamma 1 chain in solution. J Mol Biol 257 (3): 658-668.
21. Stetefeld J, Mayer U, Timpl R, Huber R (1996) Crystal structure of three consecutive laminin-type epidermal growth factor-like (LE) modules of laminin gamma 1 chain harboring the nidogen binding site. J Mol Biol 257 (3): 644-657.
22. Pöschl E, Mayer U, Stetefeld J, Baumgartner R, Holak TA, et al. (1996) Site-directed mutagenesis and structural interpretation of the nidogen binding site of the laminin gamma 1 chain. EMBO J 15 (19): 5154-5159.
23. Sasaki M, Yamada Y (1987) The laminin B2 chain has a multidomain structure homologous to the B1 chain. J Biol Chem 262 (35): 17111-17117.
24. Takagi J, Yang YT, Liu JH, Wang JH, Springer TA (2003) Complex between nidogen and laminin fragments reveals a paradigmatic beta-propeller interface. Nature 424 (6951): 969-974.
25. Patel TR, Bernards C, Meier M, McEleney K, Winzor DJ, et al. (2014) Structural elucidation of full-length nidogen and the laminin-nidogen complex in solution. Matrix Biol 33: 60-67.
26. Sinz A (2014) The advancement of chemical cross-linking and mass spectrometry for structural proteomics: from single proteins to protein interaction networks. Expert Rev Proteomics Sept. 16: 1-11, online available.
27. Sinz A (2006) Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions. Mass Spectrom Rev 25 (4): 663-682.
28. Kalisman N, Adams CM, Levitt M (2012) Subunit order of eukaryotic TRiC/CCT chaperonin by cross-linking, mass spectrometry, and combinatorial homology modeling. Proc Natl Acad Sci USA 109 (8): 2884-2889.
29. Leitner A, Joachimiak LA, Bracher A, Mönkemeyer L, Walzthoeni T, et al. (2012) The molecular architecture of the eukaryotic chaperonin TRiC/CCT. Structure 20 (5): 814-825.
30. Rappsilber J (2011) The beginning of a beautiful friendship: cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. J Struct Biol 173 (3): 530-540.
31. Rinner O, Seebacher J, Walzthoeni T, Mueller LN, Beck M, et al. (2008) Identification of cross-linked peptides from large sequence databases. Nat Meth 5 (4): 315-318.
32. Müller MQ, Dreiocker F, Ihling CH, Schäfer M, Sinz A (2010) Cleavable cross-linker for protein structure analysis: reliable identification of cross-linking products by tandem MS. Anal Chem 82 (16): 6958-6968.
33. Hussain S, Carafoli F, Hohenester E (2011) Determinants of laminin polymerization revealed by the structure of the a5 chain amino-terminal region. EMBO Rep 12 (3): 276-282.
34. Carafoli F, Hussain S, Hohenester E (2012) Crystal structures of the network-forming short-arm tips of the laminin b1 and c1 chains. PLoS ONE 7 (7): e42473.
35. Kölbel K, Ihling CH, Sinz A (2012) Analysis of peptide secondary structures by photoactivatable amino acid analogues. Angew Chem Int Ed Engl 51 (50): 12602-12605.
36. Karlsson R, Katsamba PS, Nordin H, Pol E, Myszka DG (2006) Analyzing a kinetic titration series using affinity biosensors. Anal Biochem 349 (1): 136-147.
37. Schaks S, Maucher D, Ihling CH, Sinz A (2012) Investigation of a calmodulin/peptide complex by chemical cross-linking and high-resolution mass spectrom-etry. In: König S, editor. Biomacromolecular mass spectrometry. Tips from the bench. Hauppauge: Nova Science Publishers. 1-18.
38. Götze M, Pettelkau J, Schaks S, Bosse K, Ihling CH, et al. (2012) StavroX-a software for analyzing crosslinked products in protein interaction studies. J Am Soc Mass Spectrom 23 (1): 76-87.
39. Boratyn GM, Schäffer AA, Agarwala R, Altschul SF, Lipman DJ, et al. (2012) Domain enhanced lookup time accelerated BLAST. Biol Direct 7: 12.
40. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4 (3): 363-371.
41. Söding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33 (Web Server issue): W244-8.
42. Buchan DWA, Minneci F, Nugent TCO, Bryson K, Jones DT (2013) Scalable web services for the PSIPRED Protein Analysis Workbench. Nucleic Acids Res 41 (Web Server issue): W349-57.
43. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40.
44. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23 (21): 2947-2948.
45. Combs SA, DeLuca SL, DeLuca SH, Lemmon GH, Nannemann DP, et al. (2013) Small-molecule ligand docking into comparative models with Rosetta. Nat Protoc 8 (7): 1277-1298.
46. Konagurthu AS, Whisstock JC, Stuckey PJ, Lesk AM (2006) MUSTANG: a multiple structural alignment algorithm. Proteins 64 (3): 559-574.
47. Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292 (2): 195-202.
48. Leman JK, Mueller R, Karakas M, Woetzel N, Meiler J (2013) Simultaneous prediction of protein secondary structure and transmembrane spans. Proteins 81 (7): 1127-1140.
49. Joosten RP, te Beek TAH, Krieger E, Hekkelman ML, Hooft RWW, et al. (2010) A series of PDB related databases for everyday needs. Nucleic Acids Res 39 (Database): D411.
50. Lange OF, Baker D (2012) Resolution-adapted recombination of structural features significantly improves sampling in restraint-guided structure calculation. Proteins 80 (3): 884-895.
51. Gront D, Kulp DW, Vernon RM, Strauss CEM, Baker D, et al. (2011) Generalized Fragment Picking in Rosetta: Design, Protocols and Applications. PLoS ONE 6 (8): e23294.
52. Wang G, Dunbrack RL (2003) PISCES: a protein sequence culling server. Bioinformatics 19 (12): 1589-1591.
53. Ortiz AR, Strauss CE, Olmea O (2002) MAMMOTH (matching molecular models obtained from theory): An automated method for model comparison. Protein Sci 11 (11): 2606-2621.
54. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 (9): 1189-1191.
55. Green NS, Reisler E, Houk KN (2001) Quantitative evaluation of the lengths of homobifunctional protein cross-linking reagents used as molecular rulers. Protein Sci 10 (7): 1293-1304.
56. Herzog F, Kahraman A, Boehringer D, Mak R, Bracher A, et al. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 337 (6100): 1348-1352.
57. Kahraman A, Herzog F, Leitner A, Rosenberger G, Aebersold R, et al. (2013) Cross-link guided molecular modeling with ROSETTA. PLoS ONE 8 (9): e73411.
58. Suchanek M, Radzikowska A, Thiele C (2005) Photo-leucine and photo-methionine allow identification of protein-protein interactions in living cells. Nat Meth 2 (4): 261-267.
59. Borek F (1961) A new two-stage method for cross-linking proteins. Nature 191 (4795): 1293-1294.
60. Merkley ED, Rysavy S, Kahraman A, Hafen RP, Daggett V, et al. (2014) Distance restraints from crosslinking mass spectrometry: mining a molecular dynamics simulation database to evaluate lysine-lysine distances. Protein Sci. 23 (6): 747-759.
61. Leitner A, Walzthoeni T, Kahraman A, Herzog F, Rinner O, et al. (2010) Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics. Mol Cell Proteomics 9 (8): 1634-1649.
62. Allen FH (2002) The Cambridge Structural Database: a quarter of a million crystal structures and rising. Acta Crystallogr., B 58 (Pt 3 Pt 1): 380-388.
63. Ries A, Göhring W, Fox JW, Timpl R, Sasaki T (2001) Recombinant domains of mouse nidogen-1 and their binding to basement membrane proteins and monoclonal antibodies. Eur J Biochem 268 (19): 5119-5128.
64. Butler JE (2000) Solid supports in enzyme-linked immunosorbent assay and other solid-phase immunoassays. Methods 22 (1): 4-23.
65. Aumailley M, Wiedemann H, Mann K, Timpl R (1989) Binding of nidogen and the laminin-nidogen complex to basement membrane collagen type IV. Eur J Biochem 184 (1): 241-248.
66. Guo X, Bandyopadhyay P, Schilling B, Young MM, Fujii N, et al. (2008) Partial acetylation of lysine residues improves intraprotein cross-linking. Anal Chem 80 (4): 951-960.
67. Bechtel M, Keller MV, Bloch W, Sasaki T, Boukamp P, et al. (2012) Different domains in nidogen-1 and nidogen-2 drive basement membrane formation in skin organotypic cocultures. FASEB J 26 (9): 3637-3648.
68. Sasaki T (2004) Laminin: the crux of basement membrane assembly. J Cell Biol 164 (7): 959-963.
69. Hohenester E, Yurchenco PD (2013) Laminins in basement membrane assembly. Cell Adh Migr 7 (1): 56-63.
70. Lössl P, Sinz A (2014) Combining amine-reactive cross-linkers and photo-reactive amino acids for 3D-structure analysis of proteins and protein complexes. Meth Mol Biol (submitted).