Refined Crystal Structure of Samia cynthia ricini Silk Fibroin Revealed by Solid-State NMR Investigations.

Samia cynthia ricini is one of the wild silkworms and its silk fibroin (SF) consists of alternatively repeating poly-l-alanine (PLA) sequences as crystalline domain and glycine-rich sequences as noncrystalline domain; the structure is similar to those of spider silk and other wild silkworm silks. In this paper, we proposed a new staggered model for the packing arrangement of the PLA sequence through the use of the Cambridge Serial Total Energy Package program and a comparison of the observed and calculated chemical shifts of the PLA sequence with the Gauge Including Projector Augmented Wave method. The new model was supported by the interatomic distance information from the cross peaks of Ala Cβ dipolar-assisted rotational resonance (DARR) spectrum of the PLA sequences in S. c. ricini SF fiber. In addition, three 13C NMR peaks observed in the β-sheet region were assigned to the carbons with different environments in the same model, but not assigned to different β-sheet structures.

[1]  A. Naito,et al.  Packing arrangement of 13C selectively labeled sequence model peptides of Samia cynthia ricini silk fibroin fibers studied by solid-state NMR. , 2017, Physical chemistry chemical physics : PCCP.

[2]  B. Mandal,et al.  Relationships between physical properties and sequence in silkworm silks , 2016, Scientific Reports.

[3]  R. Reis,et al.  Fabrication and characterization of Eri silk fibers-based sponges for biomedical application. , 2016, Acta biomaterialia.

[4]  Verónica de Zea Bermudez,et al.  Bombyx mori Silk Fibers: An outstanding family of materials , 2015 .

[5]  K. Numata,et al.  Crystal structure and physical properties of Antheraea yamamai silk fibers: Long poly(alanine) sequences are partially in the crystalline region , 2015 .

[6]  C. Holland,et al.  Identification and classification of silks using infrared spectroscopy , 2015, Journal of Experimental Biology.

[7]  Yuan Cheng,et al.  Structures, mechanical properties and applications of silk fibroin materials , 2015 .

[8]  M. Williamson,et al.  Analysis of the Structure of Bombyx mori Silk Fibroin by NMR , 2015 .

[9]  K. Nishimura,et al.  Intermolecular Packing in B. mori Silk Fibroin: Multinuclear NMR Study of the Model Peptide (Ala-Gly)15 Defines a Heterogeneous Antiparallel Antipolar Mode of Assembly in the Silk II Form , 2015 .

[10]  H. Sezutsu,et al.  The complete nucleotide sequence of the Eri-silkworm (Samia cynthia ricini) fibroin gene , 2014 .

[11]  A. Percot,et al.  Water dependent structural changes of silk from Bombyx mori gland to fibre as evidenced by Raman and IR spectroscopies , 2014 .

[12]  M. Williamson,et al.  Local Structure and Dynamics of Serine in the Heterogeneous Structure of the Crystalline Domain of Bombyx mori Silk Fibroin in Silk II Form Studied by 2D 13C–13C Homonuclear Correlation NMR and Relaxation Time Observation , 2014 .

[13]  S. Kundu,et al.  Silk proteins for biomedical applications: Bioengineering perspectives , 2014 .

[14]  Tetsuo Asakura,et al.  Elucidating silk structure using solid-state NMR , 2013 .

[15]  Janelle E. Jenkins,et al.  Characterizing the secondary protein structure of black widow dragline silk using solid-state NMR and X-ray diffraction. , 2013, Biomacromolecules.

[16]  K. Nishimura,et al.  Determination of Accurate 1H Positions of (Ala-Gly)n as a Sequential Peptide Model of Bombyx mori Silk Fibroin before Spinning (Silk I) , 2013 .

[17]  David L Kaplan,et al.  Structure-function-property-design interplay in biopolymers: spider silk. , 2013, Acta biomaterialia.

[18]  Joydip Kundu,et al.  An emerging functional natural silk biomaterial from the only domesticated non-mulberry silkworm Samia ricini. , 2013, Macromolecular bioscience.

[19]  T. Asakura,et al.  Silk structure studied with nuclear magnetic resonance. , 2013, Progress in nuclear magnetic resonance spectroscopy.

[20]  K. Nishimura,et al.  Determination of accurate 1H positions of an alanine tripeptide with anti-parallel and parallel β-sheet structures by high resolution 1H solid state NMR and GIPAW chemical shift calculation. , 2012, Chemical communications.

[21]  M. Williamson,et al.  Two different packing arrangements of antiparallel polyalanine. , 2012, Angewandte Chemie.

[22]  Thomas Scheibel,et al.  Recombinant Spider Silks—Biopolymers with Potential for Future Applications , 2011 .

[23]  T. Asakura,et al.  Microscopic structural analysis of fractured silk fibers from Bombyx mori and Samia cynthia ricini using 13C CP/MAS NMR with a 1mm microcoil MAS NMR probehead. , 2010, Solid state nuclear magnetic resonance.

[24]  Janelle E. Jenkins,et al.  Structure and dynamics of aromatic residues in spider silk: 2D carbon correlation NMR of dragline fibers. , 2010, Biomacromolecules.

[25]  Janelle E. Jenkins,et al.  Quantitative Correlation between the protein primary sequences and secondary structures in spider dragline silks. , 2010, Biomacromolecules.

[26]  Fritz Vollrath,et al.  Silks as ancient models for modern polymers , 2009 .

[27]  Z. Shao,et al.  Animal silks: their structures, properties and artificial production. , 2009, Chemical communications.

[28]  T. Lefèvre,et al.  Study by Raman spectromicroscopy of the effect of tensile deformation on the molecular structure of Bombyx mori silk , 2009 .

[29]  B. Meier,et al.  Dipolar truncation in magic-angle spinning NMR recoupling experiments. , 2009, The Journal of chemical physics.

[30]  P. Schmieder,et al.  High-resolution double-quantum deuterium magic angle spinning solid-state NMR spectroscopy of perdeuterated proteins. , 2009, Journal of the American Chemical Society.

[31]  Janelle E. Jenkins,et al.  Determining secondary structure in spider dragline silk by carbon-carbon correlation solid-state NMR spectroscopy. , 2008, Journal of the American Chemical Society.

[32]  Janelle E. Jenkins,et al.  Solid-state NMR investigation of major and minor ampullate spider silk in the native and hydrated states. , 2008, Biomacromolecules.

[33]  David L Kaplan,et al.  Silk as a Biomaterial. , 2007, Progress in polymer science.

[34]  F. Vollrath,et al.  Spider and mulberry silkworm silks as compatible biomaterials , 2007 .

[35]  A. I. Kishore,et al.  Orientational order of Australian spider silks as determined by solid‐state NMR , 2006, Biopolymers.

[36]  T. Asakura,et al.  Structural analysis of alanine tripeptide with antiparallel and parallel beta-sheet structures in relation to the analysis of mixed beta-sheet structures in Samia cynthia ricini silk protein fiber using solid-state NMR spectroscopy. , 2006, Journal of the American Chemical Society.

[37]  T. Asakura,et al.  Development of MicroMAS NMR Probehead for Mass-limited Solid-state Samples , 2006 .

[38]  T. Asakura,et al.  Use of microcoil probehead for determination of the structure of oriented silk fibers by solid-state NMR. , 2005, The journal of physical chemistry. B.

[39]  T. Asakura,et al.  Spectroscopic Characterization of Heterogeneous Structure of Samia cynthia ricini Silk Fibroin Induced by Stretching and Molecular Dynamics Simulation , 2004 .

[40]  T. Asakura,et al.  Structure determination of a peptide model of the repeated helical domain in Samia cynthia ricini silk fibroin before spinning by a combination of advanced solid-state NMR methods. , 2003, Journal of the American Chemical Society.

[41]  Kiyonori Takegoshi,et al.  13C–1H dipolar-driven 13C–13C recoupling without 13C rf irradiation in nuclear magnetic resonance of rotating solids , 2003 .

[42]  T. Yamane,et al.  Heterogeneous structure of silk fibers from Bombyx mori resolved by 13C solid-state NMR spectroscopy. , 2002, Journal of the American Chemical Society.

[43]  Matt Probert,et al.  First-principles simulation: ideas, illustrations and the CASTEP code , 2002 .

[44]  T. Asakura,et al.  High-Resolution 13C CP/MAS NMR Study on Structure and Structural Transition of Antheraea pernyi Silk Fibroin Containing Poly(l-alanine) and Gly-Rich Regions , 2002 .

[45]  A. Ghosh,et al.  Purification and characterization of fibroin from the tropical Saturniid silkworm, Antheraea mylitta. , 2001, Insect biochemistry and molecular biology.

[46]  Kiyonori Takegoshi,et al.  13C–1H dipolar-assisted rotational resonance in magic-angle spinning NMR , 2001 .

[47]  M. Jacquet,et al.  Silk fibroin: Structural implications of a remarkable amino acid sequence , 2001, Proteins.

[48]  F. Mauri,et al.  All-electron magnetic response with pseudopotentials: NMR chemical shifts , 2001, cond-mat/0101257.

[49]  Hideki Sezutsu,et al.  Dynamic Rearrangement Within the Antheraea pernyi Silk Fibroin Gene Is Associated with Four Types of Repetitive Units , 2000, Journal of Molecular Evolution.

[50]  B. Meier,et al.  Solid-state NMR determination of the secondary structure of Samia cynthia ricini silk , 2000, Nature.

[51]  M. Jacquet,et al.  Fine organization of Bombyx mori fibroin heavy chain gene. , 2000, Nucleic acids research.

[52]  J. Gosline,et al.  The mechanical design of spider silks: from fibroin sequence to mechanical function. , 1999, The Journal of experimental biology.

[53]  Takuro Ito,et al.  Structure of Alanine and Glycine Residues of Samia cynthia ricini Silk Fibers Studied with Solid-State 15N and 13C NMR , 1999 .

[54]  R. Lewis,et al.  Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. , 1999, International journal of biological macromolecules.

[55]  Y. Takahashi,et al.  Structure refinement and diffuse streak scattering of silk (Bombyx mori). , 1999, International journal of biological macromolecules.

[56]  H. Limbach,et al.  Temperature gradients and sample heating in variable temperature high speed MAS NMR spectroscopy , 1990 .

[57]  T. Asakura,et al.  NMR of silk fibroin. 8. Carbon-13 NMR analysis of the conformation and the conformational transition of Philosamia cynthia ricini silk fibroin protein on the basis of Bixon-Scheraga-Lifson theory , 1988 .

[58]  Tetsuo Asakura,et al.  Conformational characterization of Bombyx mori silk fibroin in the solid state by high-frequency carbon-13 cross polarization-magic angle spinning NMR, x-ray diffraction, and infrared spectroscopy , 1985 .

[59]  A Elliott,et al.  Structure of beta-poly-L-alanine: refined atomic co-ordinates for an anti-parallel beta-pleated sheet. , 1967, Journal of molecular biology.

[60]  S. Arnott,et al.  Atomic co-ordinates for an alpha-helix: refinement of the crystal structure of alpha-poly-l-alanine. , 1966, Journal of molecular biology.

[61]  K. Nishimura,et al.  Difference in the structures of alanine tri- and tetra-peptides with antiparallel β-sheet assessed by X-ray diffraction, solid-state NMR and chemical shift calculations by GIPAW. , 2014, Biopolymers.

[62]  R. E. Marsh,et al.  An investigation of the structure of silk fibroin. , 1955, Biochimica et biophysica acta.