Structural model for the spider silk protein spidroin-1

Journal of Proteome Research

Volumn 14, Issue 9, 2015, Pages 3859-3870

  Dos Santos Pinto, José Roberto Aparecido ^a,b   Arcuri, Helen Andrade ^a   Priewalder, Helga ^c   Salles, Heliana Clara ^a   Palma, Mario Sergio ^a   Lubec, Gert ^b  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c ZAMG Zentralanstalt fuer Meteorologie und Geodynamik   (Austria)

Author keywords

mass spectrometry; molecular dynamics; Nephila clavipes; post translational modification; silk proteins

Indexed keywords

PEPTIDES AND PROTEINS; SPIDROIN 1A; SPIDROIN 1B; UNCLASSIFIED DRUG; FIBROIN; SILK; SPIDROIN 1;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COLLISIONALLY ACTIVATED DISSOCIATION; CONTROLLED STUDY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NEPHILA CLAVIPES; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; MOLECULAR GENETICS; SCANNING ELECTRON MICROSCOPY; SEQUENCE HOMOLOGY; SPIDER;

AMINO ACID SEQUENCE; ANIMALS; FIBROINS; MICROSCOPY, ELECTRON, SCANNING; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; SILK; SPIDERS;

EID: 84941079269     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00243     Document Type: Article

References (74)

1. Römer, L.; Scheibel, T. The elaborate structure of spider silk: structure and function of a natural high performance fiber Prion 2008, 2, 154-61 10.4161/pri.2.4.7490
2. Heim, M.; Keerl, D.; Scheibel, T. Spider silk: From soluble protein to extraordinary fiber Angew. Chem., Int. Ed. 2009, 48, 3584-3596 10.1002/anie.200803341
3. Rising, A.; Johansson, J.; Larson, G.; Bongcam-Rudloff, E.; Engström, W.; Hjälm, G. Major ampullate spidroins from euprosthenops australis: multiplicity at protein, mRNA and gene levels Insect Mol. Biol. 2007, 16, 551-561 10.1111/j.1365-2583.2007.00749.x
4. Hardy, J. G.; Scheibel, T. R. Composite materials based on silk proteins. Progr Prog. Polym. Sci. 2010, 35, 1093-1115 10.1016/j.progpolymsci.2010.04.005
5. Motriuk-Smith, D.; Smith, A.; Hayashi, C. Y.; Lewis, R. V. Analysis of conserved N-terminal domains in major ampullate spider silk proteins Biomacromolecules 2005, 6, 3152-3259 10.1021/bm050472b
6. Askarieh, G.; Hedhammar, M.; Nordling, K.; Saenz, A.; Casals, C.; Rising, A.; Johansson, J.; Knight, S. D. Self-assembly of spider silk proteins is controlled by a pH-sensitive relay Nature 2010, 465, 236-238 10.1038/nature08962
7. Humenik, M.; Smith, A. M.; Scheibel, T. R. Recombinant spider silks-Biopolymers with potential for future applications Polymers 2011, 3, 640-661 10.3390/polym3010640
8. Eisoldt, L.; Hardy, J. G.; Heim, M.; Scheibel, T. R. The role of salt and shear on the storage and assembly of spider silk proteins J. Struct. Biol. 2010, 170, 413-419 10.1016/j.jsb.2009.12.027
9. Liu, Y.; Shao, Z.; Vollrath, F. Relationships between supercontraction and mechanical properties of spider silk Nat. Mater. 2005, 4, 901-905 10.1038/nmat1534
10. Lefévre, T.; Paquet-Mercier, F.; Rioux-Dubé, J. F.; Pézolet, M. Structure of Silk by Raman Spectromicroscopy: From the Spinning Glands to the Fibers Biopolymers 2012, 97, 322-336 10.1002/bip.21712
11. Rising, A.; Widhe, M.; Johansson, J.; Hedhammar, M. Spider silk proteins: recent advances in recombinant production, structure-function relationships and biomedical applications Cell. Mol. Life Sci. 2011, 68, 169-184 10.1007/s00018-010-0462-z
12. Cranford, S. W.; Tarakanova, A.; Pugno, N. M.; Buehler, M. J. Nonlinear Material Behavior of Spider Silk Yields Robust Webs Nature 2012, 482, 72-76 10.1038/nature10739
13. Slotta, U.; Mougin, N.; Römer, L.; Leimer, A. H. Synthetic spider silk proteins and threads Soc. Biol. Eng. 2012, 43-49
14. Koski, K. J.; Akhenblit, P.; McKiernan, K.; Yarger, J. L. Non-invasive determination of the complete elastic moduli of spider silks Nat. Mater. 2013, 12, 262-267 10.1038/nmat3549
15. Ayoub, N. A.; Garb, J. E.; Tinghitella, R. M.; Collin, M. A.; Hayashi, C. Y. Blueprint for a High-Performance Biomaterial: Full-Length Spider Dragline Silk Genes PLoS One 2007, 2 (6) e514 10.1371/journal.pone.0000514
16. Sanggaard, K. W. et al. Spider genomes provide insight into composition and evolution of venom and silk Nat. Commun. 2014, 5, 3765 10.1038/ncomms4765
17. dos Santos-Pinto, J. R. A. et al. Structure and post-translational modifications of the web silk protein spidroin-1 from Nephila spiders J. Proteomics 2014, 105, 174-185 10.1016/j.jprot.2014.01.002
18. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye biding Anal. Biochem. 1976, 72, 248-254 10.1016/0003-2697(76)90527-3
19. Bae, N.; Li, L.; Lödl, M.; Lubec, G. Peptide toxin glacontryphan-M is present in the wings of the butterfly Hebomoia glaucippe (Linnaeus, 1758) (Lepidoptera: Pieridae) Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (44) 17920-4 10.1073/pnas.1209632109
20. Creasy, D. M.; Cottrell, J. S. Error tolerant searching of uninterpreted tandem mass spectrometry data Proteomics 2002, 2, 1426-1434 10.1002/1615-9861(200210)2:10<1426::AID-PROT1426>3.0.CO;2-5
21. Nuwal, T.; Heo, S.; Lubec, G.; Buchner, E. Mass spectrometric analysis of synapsins in Drosophila melanogaster and identification of novel phosphorylation sites J. Proteome Research 2011, 10, 541-550 10.1021/pr100746s
22. A-receptor subunit containing four transmembrane domains Nat. Protoc. 2009, 4, 1093-1102 10.1038/nprot.2009.92
23. Cuff, J. A.; Barton, G. J. Application of multiple sequence alignment profiles to improve protein secondary structure prediction Proteins: Struct., Funct., Genet. 2000, 40, 502-511 10.1002/1097-0134(20000815)40:3<502::AID-PROT170>3.0.CO;2-Q
24. Clamp, M.; Cuff, J.; Searle, S. M.; Barton, G. J. The Jalview Java Alignment Editor Bioinformatics 2004, 20, 426-427 10.1093/bioinformatics/btg430
25. Klose, D.; Janes, R. W. 2Struc-The Protein Secondary Structure Analysis Server Biophys. J. 2010, 98, 454-455 10.1016/j.bpj.2009.12.2470
26. Jones, D. T.; Taylort, W. R.; Thornton, J. M. A new approach to protein fold recognition Nature 1992, 358, 86-89 10.1038/358086a0
27. Lipman, D. J.; Pearson, W. R. Rapid and sensitive protein similarity searches Science 1985, 227, 1435-1441 10.1126/science.2983426
28. Hagn, F. et al. A conserved spider silk domain acts as a molecular switch that controls fibre assembly Nature 2010, 465, 239-242 10.1038/nature08936
29. Meng, G.; Spahich, N.; Kenjale, R.; Waksman, G.; St Geme, J. W. Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation EMBO J. 2011, 30, 3864-3874 10.1038/emboj.2011.279
30. Delano, W. L. The PyMOL Molecular Graphics System; DeLano Scientific: Palo Alto, CA, 2002.
31. Laskowski, R. A.; Macarthur, M. W.; Moss, D. S.; Thornton, J. M. PROCHECK-A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 1993, 26, 283-29 10.1107/S0021889892009944
32. Thompson, J. D.; Higgins, D. G.; Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions specific gap penalties and weight matrix choice Nucleic Acids Res. 1994, 22, 4673-4680 10.1093/nar/22.22.4673
33. Van Der Spoel, D. et al. GROMACS: fast, flexible, and free J. Comput. Chem. 2005, 26, 1701-1718 10.1002/jcc.20291
34. Scott, W. R. P. et al. The GROMOS biomolecular simulation program package J. Phys. Chem. A 1999, A103, 3596-3607 10.1021/jp984217f
35. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; Hermans, J. Interaction models for water in relation to protein hydration. In Intermolecular Forces; Reidel Publishing Co: Dordrecht, 1981; pp 331-342.
36. Salles, H. C.; Volsi, E. C. F. R.; Marques, M. R.; Santos, L. D.; Palma, M. S. et al. The Venomous Secrets of the Web Droplets from the Viscid Spiral of the Orb-Weaver Spider Nephila clavipes (Araneae, Tetragnatidae) Chem. Biodiversity 2006, 3, 727-741 10.1002/cbdv.200690075
37. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: a linear constraint solver for molecular simulations J. Comput. Chem. 1997, 18, 1463-1472 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L
38. Miyamoto, S.; Kollman, P. A. SETTLE: An analytical version of the SHAKE and RATTLE algorithm for rigid water models J. Comput. Chem. 1992, 13, 952-962 10.1002/jcc.540130805
39. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690 10.1063/1.448118
40. Chowdhuri, S.; Tan, M. L.; Ichiye, T. Dynamical properties of the soft sticky dipole-quadrupole-octupole water model: a molecular dynamics study J. Chem. Phys. 2006, 125, 144513 10.1063/1.2357117
41. Essmann, U. et al. A smooth particle mesh Ewald method J. Chem. Phys. 1995, 103, 8577-8593 10.1063/1.470117
42. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38 10.1016/0263-7855(96)00018-5
43. Frishman, D.; Argos, P. Knowledge-based protein secondary structure assignment Proteins: Struct., Funct., Genet. 1995, 23, 566-579 10.1002/prot.340230412
44. Joosten, R. P. et al. A series of PDB related databases for everyday needs Nucleic Acids Res. 2011, 39, 1-9 10.1093/nar/gkq1105
45. Chen, G. et al. Full-length minor ampullate spidroin gene sequence PLoS One 2012, 7 (12) e52293 10.1371/journal.pone.0052293
46. Thiel, B. L.; Kunkel, D. D.; Viney, C. Physical and Chemical Microstructure of Spider Dragline: A Study by Analytical Transmission Electron Microscopy Biopolymers 1994, 34, 1089-1097 10.1002/bip.360340812
47. Augsten, K.; Muhlig, P.; Herrmann, C. Glycoproteins and skin-core structure in Nephila clavipes spider silk observed by light and electron microscopy Scanning 2000, 22, 12-15 10.1002/sca.4950220103
48. Lubec, B.; Hermon, M.; Hoeger, H.; Lubec, G. Aromatic hydroxylation in animal models of diabetes mellitus FASEB J. 1998, 12, 1581-1587
49. Stadtman, E. R.; Levine, R. L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins Amino Acids 2003, 25, 207-218 10.1007/s00726-003-0011-2
50. Peluffo, G.; Radi, R. Biochemistry of protein tyrosine nitration in cardiovascular pathology Cardiovasc. Res. 2007, 75 (2) 291-302 10.1016/j.cardiores.2007.04.024
51. Tillinghast, E. K. Selective removal of glycoproteins from the adhesive spiral of the spiders orb web Naturwissenschaften 1981, 68, 526-527 10.1007/BF00365384
52. Vollrath, F. et al. Compounds in the droplets of the orb spider's viscid spiral Nature 1990, 345, 526-527 10.1038/345526a0
53. Vollrath, F.; Tillinghast, E. K. Glicoprotein glue beneath a spider web's aqueous coat Naturwissenschaften 1991, 78, 557-559 10.1007/BF01134447
54. Eyers, C. E.; Gaskell, S. J. Mass spectrometry to identify post-translational modifications Wiley Encyclopedia Chem. Biol. 2008, 10.1002/9780470048672.wecb469
55. Zhang, P. et al. Proteomic studies of isoforms of the P25 component of Bombyx mori fibroin Biosci., Biotechnol., Biochem. 2005, 69, 2086-2093 10.1271/bbb.69.2086
56. Chen, W. Q.; Priewalder, H.; Pradeep John, J. P.; Lubec, G. Silk cocoon of Bombix mori: Proteins and posttranslational modifications-heavy phosphorylation and evidence for lysine-mediated cross links Proteomics 2010, 10, 369-379 10.1002/pmic.200900624
57. Michal, C. A.; Simmons, A. H.; Chew, B. G.; Zax, D. B.; Jelinski, L. W. Presence of phosphorus in Nephila clavipes dragline silk Biophys. J. 1996, 70, 489-493 10.1016/S0006-3495(96)79594-2
58. Knight, D. P.; Vollrath, F. Changes in element composition along the spinning duct in a Nephila spider Naturwissenschaften 2001, 88, 179-182 10.1007/s001140100220
59. Huemmerich, D. et al. Primary structure elements of spider dragline silks and their contribution to protein solubility Biochemistry 2004, 43, 13604-13612 10.1021/bi048983q
60. Winkler, S.; Wilson, D.; Kaplan, D. L. Controlling beta-sheet assembly in genetically engineered silk by enzymatic phosphorylation/dephosphorylation Biochemistry 2000, 39, 12739-12746 10.1021/bi001335w
61. Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. Molecular Biology of the Cell, 4 th ed.; Garland Science: New York, 2002.
62. Schwarze, S.; Zwettler, F. U.; Johnson, M. J.; Neuweiler, H. The N-terminal domains of spider silk proteins assemble ultrafast and protected from charge screening Nat. Commun. 2013, 4, 2815 10.1038/ncomms3815
63. Kronqvist, N. et al. Sequential pH-driven dimerization and stabilization of the N-terminal domain enables rapid spider silk formation Nat. Commun. 2014, 5, 3254 10.1038/ncomms4254
64. l3C NMR of Nephila clavipes Dragline Silk Establishes Structure and Identity of Crystalline Regions Macromolecules 1994, 27, 5235-5237 10.1021/ma00096a060
65. Shao, Z.; Vollrath, F.; Sirichaisit, J.; Young, R. J. Analysis of spider silk in native and supercontracted states using Raman spectroscopy Polymer 1999, 40, 2493-2500 10.1016/S0032-3861(98)00475-3
66. Riekel, C.; Vollrath, F. Spider silk fibre extrusion: combined wide- and small-angle X-ray microdiffraction experiments Int. J. Biol. Macromol. 2001, 29, 203-210 10.1016/S0141-8130(01)00166-0
67. Knight, D. P.; Knight, M. M.; Vollrath, F. Beta transition and stress-induced phase separation in the spinning of spider dragline silk Int. J. Biol. Macromol. 2000, 27, 205-210 10.1016/S0141-8130(00)00124-0
68. Parkhe, A. J.; Seeley, S. K.; Gardner, K.; Thompson, L.; Lewis, R. V. Structural Studies of Spider Silk Proteins in the Fiber J. Mol. Recognit. 1997, 10, 1-6 10.1002/(SICI)1099-1352(199701/02)10:1<1::AID-JMR338>3.0.CO;2-7
69. Holland, G. P.; Jenkins, J. E.; Creager, M. S.; Lewis, R. V.; Yarger, J. L. Quantifying the fraction of glycine and alanine in b-sheet and helical conformations in spider dragline silk using solid-state Chem. Commun. 2008, 5568-5570 10.1039/b812928b
70. Holland, G. P.; Creager, M. S.; Jenkins, J. E.; Randolph, V.; Lewis, R. V.; Yarger, J. L. Determining Secondary Structure in Spider Dragline Silk by Carbon-Carbon Correlation Solid-State NMR Spectroscopy J. Am. Chem. Soc. 2008, 130, 9871-9877 10.1021/ja8021208
71. Jenkins, J. E.; Sampath, S.; Butler, E.; Kim, J.; Henning, R. W.; Holland, G. P.; Yarger, J. L. Characterizing the Secondary Protein Structure of Black Widow Dragline Silk Using Solid-State NMR and X-ray Diffraction Biomacromolecules 2013, 14, 3472-3483 10.1021/bm400791u
72. Lefévre, T.; Rousseau, M. E.; Pézolet, M. Protein Secondary Structure and Orientation in Silk as Revealed by Raman Spectromicroscopy Biophys. J. 2007, 92, 2885-2895 10.1529/biophysj.106.100339
73. Hedhammar, M. et al. Structural Properties of Recombinant Nonrepetitive and Repetitive Parts of Major Ampullate Spidroin 1 from Euprosthenops australis: Implications for Fiber Formation Biochemistry 2008, 47, 3407-3417 10.1021/bi702432y
74. Dicko, C.; Knight, D.; Kenney, J. M.; Vollrath, F. Secondary structures and conformational changes in flagelliform, cylindrical, major, and minor ampullate silk proteins. Temperature and concentration effects Biomacromolecules 2004, 5 (6) 2105-2115 10.1021/bm034486y