Structure and post-translational modifications of the web silk protein spidroin-1 from Nephila spiders

Journal of Proteomics

Volumn 105, Issue , 2014, Pages 174-185

  dos Santos Pinto, José Roberto Aparecido ^a,b   Lamprecht, Günther ^c   Chen, Wei Qiang ^b   Heo, Seok ^b   Hardy, John George ^d   Priewalder, Helga ^e   Scheibel, Thomas Rainer ^d   Palma, Mario Sergio ^a   Lubec, Gert ^b  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF BAYREUTH   (Germany)

^e ZAMG Zentralanstalt für Meteorologie und Geodynamik   (Austria)

Author keywords

Dityrosine; Mass spectrometry; Peptide sequencing; Phosphorylation; Proteomic analysis

Indexed keywords

INSECT PROTEIN; PEROXIDASE; SPIDROIN 1; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG; WEB SILK PROTEIN; DITYROSINE; DOPA; FIBROIN; TYROSINE;

AMINO ACID SEQUENCE; FRAGMENTATION REACTION; MASS SPECTROMETRY; MOLECULAR MECHANICS; NEPHILA; NEPHILA CLAVIPES; NEPHILA EDULIS; NEPHILA MADAGASCARIENSIS; NONHUMAN; OXIDATION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RADIATION EXPOSURE; REVIEW; ULTRAVIOLET RADIATION; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SPIDER;

ARANEAE; NEPHILA; NEPHILA CLAVIPES; NEPHILA EDULIS; NEPHILA INAURATA MADAGASCARIENSIS;

ANIMALS; DIHYDROXYPHENYLALANINE; FIBROINS; MASS SPECTROMETRY; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SPIDERS; TYROSINE;

EID: 84901841295     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.01.002     Document Type: Review

References (50)

1. Vollrath F. Strength and structure of spiders' silks. J Biotechnol 2000, 74:67-83.
2. Römer L., Scheibel T. The elaborate structure of spider silk: structure and function of a natural high performance fiber. Prion 2008, 2:154-161.
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.
4. Hardy J.G., Scheibel T.R. Composite materials based on silk proteins. Prog Polym Sci 2010, 35:1093-1115.
5. Xu M., Lewis R.V. Structure of a protein superfiber: spider dragline silk. Proc Natl Acad Sci U S A 1990, 87:7120-7124.
6. Ayoub N.A., Hayashi C.Y. Multiple recombining loci encode MaSp1, the primary constituent of dragline silk, in widow spiders (Latrodectus: Theridiidae). Mol Biol Evol 2008, 25:277-286.
7. Sponner A., Schlott B., Vollrath F., Unger E. Characterization of the protein components of Nephila clavipes dragline silk. Biochemistry 2005, 44:4727-4736.
8. Sponner A., Vater W., Monajembashi S., Unger E., Grosse F., Weisshart K. Composition and hierarchical organisation of a spider silk. PLoS One 2007, 2(10):e998.
9. 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. 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.
11. Askarieh G., Hedhammar M., Nordling K., Saenz A., Casals C., Rising A., et al. Self-assembly of spider silk proteins is controlled by a pH-sensitive relay. Nature 2010, 465:236-238.
12. Hagn F., Eisoldt L., Hardy J.G., Vendrely C., Coles M., Scheibel T., et al. A conserved spider silk domain acts as a molecular switch that controls fibre assembly. Nature 2010, 465:239-242.
13. 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.
14. Hagn F., Thamm C., Scheibel T., Kessler H. pH-dependent dimerization and salt-dependent stabilization of the N-terminal domain of spider dragline silk - implications for fiber formation. Angew Chem Int Ed 2011, 50:310-313.
15. Gatesy J., Hayashi C., Motriuk D., Woods J., Lewis L. Extreme diversity, conservation, and convergence of spider silk fibroin sequences. Science 2001, 291:2603-2605.
16. Van Beek J.D., Hess S., Vollrath F., Meier B.H. The molecular structure of spider dragline silk: folding and orientation of the protein backbone. Proc Natl Acad Sci U S A 2002, 99:10266-10271.
17. Savage K.N., Gosline J.M. The effect of proline on the network structure of major ampullate silks as inferred from their mechanical and optical properties. J Exp Biol 2008, 211:1937-1947.
18. Rauscher S., Baud S., Miao M., Keeley F.W., Pomes R. Proline and glycine control protein self-organization into elastomeric or amyloid fibrils. Structure 2006, 14:1667-1676.
19. Semmrich C., Bausch A.R. Proteins crystals: how the weak become strong. Nat Mater 2010, 9:293-295.
20. Lefèvre T., Boudreault S., Cloutier C., Pézolet M. Diversity of molecular transformations involved in the formation of spider silks. J Mol Biol 2011, 405:238-253.
21. Liu Y., Shao Z., Vollrath F. Relationships between supercontraction and mechanical properties of spider silk. Nat Mater 2005, 4:901-905.
22. Humenik M., Smith A.M., Scheibel T. Recombinant spider silks - biopolymers with potential for future applications. Polymers 2011, 3:640-661.
23. 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.
24. Chen W.-Q., Priewalder H., John J.P.P., Lubec G. Silk cocoon of Bombyx mori: proteins and posttranslational modifications - heavy phosphorylation and evidence for lysine-mediated cross links. Proteomics 2010, 10:369-379.
25. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
26. 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, 109:17920-17924.
27. A-receptor subunit containing four transmembrane domains. Nat Protoc 2009, 4:1093-1102.
28. Dong-Ik L., Sangpill H., Yun C.J., Ik-Sung A., Chang-Ha L. A convenient preparation of dityrosine via Mn(III)-mediated oxidation of tyrosine. Process Biochem 2008, 43:999-1003.
29. Tso I.M., Wu H.C., Hwang I.R. Giant wood spider Nephila clavipes alters silk protein in response to prey variation. J Exp Biol 2005, 208:1053-1061.
30. Blamires S.J., Chao I.C., Tso I.M. Prey type, vibrations and handling interactively influence spider silk expression. J Exp Biol 2010, 213:3906-3910.
31. 18O stable isotope labeling and mass spectrometry. Rapid Commun Mass Spectrom 2005, 19:683-688.
32. Gyorgy B., Toth E., Tarcsa E., Falus A., Buzas E.I. Citrullination: a posttranslational modification in health and disease. Int J Biochem Cell Biol 2006, 38:1662-1677.
33. Smith B.C., Denu J.M. Chemical mechanisms of histone lysine and arginine modifications. Biophys Acta 2009, 1789:45-57.
34. Loos T., Mortier A., Gouwy M., Ronsse I., Put W., Lenaerts J.P., et al. Citrullination of CXCL10 and CXCL11 by peptidylarginine deiminase: a naturally occurring posttranslational modification of chemokines and new dimension of immunoregulation. Blood 2012, 112:2648-2656.
35. Papov V.V., Diamond T.V., Biemann K., Waite J.H. Hydroxyarginine-containing polyphenolic proteins in the adhesive plaques of the marine mussel Mytilus edulis. J Biol Chem 1995, 270:20183-20192.
36. Taylor S.W., Graig A.G., Fischer W.H., Park M., Lehrer R.I. Styelin D, an extensively modified antimicrobial peptide from Ascidian hemocytes. J Biol Chem 2000, 275:38417-38426.
37. Lubec B., Hermon M., Hoeger H., Lubec G. Aromatic hydroxylation in animal models of diabetes mellitus. FASEB J 1998, 12:1581-1587.
38. 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.
39. Pouchkina N.N., Stanchev B.S., McQueen-Manson S.J. From EST sequence to spider silk spinning: identification and molecular characterisation of Nephila senegalensis major ampullate gland peroxidase NsPox. Insect Biochem Mol Biol 2003, 33:229-238.
40. Vollrath F., Knight D.P. Structure and function of the silk production pathway in the spider Nephila edulis. Int J Biol Macromol 1999, 24:243-249.
41. Eyers C.E., Gaskell S.J. Mass spectrometry to identify post-translational modifications. Wiley Encycl Chem Biol May 15, 2008, 10.1002/9780470048672.wecb469.
42. Zhang P., Aso Y., Yamamoto K., Banno Y., Wang Y., Tsuchida K., et al. Proteome analysis of silk gland proteins from the silkworm, Bombyx mori. Proteomics 2006, 6:2586-2599.
43. 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.
44. Heim M., Keerl D., Scheibel T. Spider silk: from soluble protein to extraordinary fiber. Angew Chem Int Ed 2009, 48:3584-3596.
45. Knight D.P., Vollrath F. Changes in element composition along the spinning duct in a Nephila spider. Naturwissenschaften 2001, 88:179-182.
46. Huemmerich D., Helsen C.W., Quedzuweit S., Oschmann J., Rudolph R., Sheibel T. Primary structure elements of spider dragline silks and their contribution to protein solubility. Biochemistry 2004, 43:13604-13612.
47. Stewart R.J., Wang C.S. Adaptation of caddisfly larval silks to aquatic habitats by phosphorylation of H-fibroin serines. Biomacromolecules 2010, 11:969-974.
48. Addison J.B., Ashton N.N., Weber W.S., Stewart R.J., Holland G.P., Yarger J.L. β-Sheet nanocrystalline domains formed from phosphorylated serine-rich motifs in caddisfly larval silk: a solid state NMR and XRD study. Biomacromolecules 2013, 14:1140-1148.
49. Winkler S., Wilson D., Kaplan D.L. Controlling beta-sheet assembly in genetically engineered silk by enzymatic phosphorylation/dephosphorylation. Biochemistry 2000, 39:12739-12746.
50. Keten S., Xu Z., Ihle B., Buehler M.J. Nanoconfinement controls stiffness, strength and mechanical toughness of β-sheet crystals in silk. Nat Mater 2010, 9:359-367.