Infiltration of chitin by protein coacervates defines the squid beak mechanical gradient

Nature Chemical Biology

Volumn 11, Issue 7, 2015, Pages 488-495

  Tan, Yerpeng ^a   Hoon, Shawn ^b,c   Guerette, Paul A ^d,e   Wei, Wei ^a   Ghadban, Ali ^e   Hao, Cai ^e   Miserez, Ali ^c,e   Waite, J Herbert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Agency for Science   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; HISTIDINE; N ACETYLGLUCOSAMINE; TRANSCRIPTOME; 4-METHYLCATECHOL; CATECHOLS; CROSS-LINKING REAGENTS; HISTIDINE-RICH PROTEINS; METAPERIODATE; PERIODIC ACID; PROTEIN BINDING; PROTEINS; WATER;

AMINO ACID COMPOSITION; ARTICLE; COACERVATION; CONSENSUS SEQUENCE; CROSS LINKING; LIQUID CHROMATOGRAPHY; MOLECULAR LIBRARY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; RIGIDITY; SQUID; SQUID BEAK; TANDEM MASS SPECTROMETRY; TANDEM REPEAT; AMINO ACID SEQUENCE; ANIMALS; BEAK; BIOMECHANICAL PHENOMENA; CHEMISTRY; DECAPODIFORMES; HARDNESS; METABOLISM; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; SEQUENCE ANALYSIS, RNA; ULTRASTRUCTURE;

CEPHALOPODA; DOSIDICUS GIGAS;

AMINO ACID SEQUENCE; ANIMALS; BEAK; BIOMECHANICAL PHENOMENA; CATECHOLS; CHITIN; CROSS-LINKING REAGENTS; DECAPODIFORMES; HARDNESS; MOLECULAR SEQUENCE DATA; PERIODIC ACID; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; PROTEOMICS; SEQUENCE ANALYSIS, RNA; WATER;

EID: 84931566487     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1833     Document Type: Article

References (57)

1. Farren, L., Shayler, S. & Ennos, A.R. The fracture properties and mechanical design of human fingernails. J. Exp. Biol. 207, 735-741 (2004).
2. Benjamin, M. et al. Where tendons and ligaments meet bone: attachment sites ('entheses') in relation to exercise and/or mechanical load. J. Anat. 208, 471-490 (2006).
3. Lu, H.H. & Thomopoulos, S. Functional attachment of soft tissues to bone: development, healing, and tissue engineering. Annu. Rev. Biomed. Eng. 15, 201-226 (2013).
4. Zajac, F.E. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 17, 359-411 (1989).
5. Sun, C.J. & Waite, J.H. Mapping chemical gradients within and along a fibrous structural tissue, mussel byssal threads. J. Biol. Chem. 280, 39332-39336 (2005).
6. Miserez, A., Schneberk, T., Sun, C., Zok, F.W. & Waite, J.H. The transition from stiff to compliant materials in squid beaks. Science 319, 1816-1819 (2008).
7. Suresh, S. Graded materials for resistance to contact deformation and damage. Science 292, 2447-2451 (2001).
8. Waite, J.H., Lichtenegger, H.C., Stucky, G.D. & Hansma, P. Exploring molecular and mechanical gradients in structural bioscaffolds. Biochemistry 43, 7653-7662 (2004).
9. Mikos, A.G. et al. Engineering complex tissues. Tissue Eng. 12, 3307-3339 (2006).
10. Helton, K.L., Ratner, B.D. & Wisniewski, N.A. Biomechanics of the sensor-tissue interface-effects of motion, pressure, and design on sensor performance and the foreign body response-part I: theoretical framework. J. Diabetes Sci. Technol. 5, 632-646 (2011).
11. Fleckman, P. & Olerud, J.E. Models for the histologic study of the skin interface with percutaneous biomaterials. Biomed. Mater. 3, 034006 (2008).
12. Fox, J.D., Capadona, J.R., Marasco, P.D. & Rowan, S.J. Bioinspired water-enhanced mechanical gradient nanocomposite films that mimic the architecture and properties of the squid beak. J. Am. Chem. Soc. 135, 5167-5174 (2013).
13. Zvarec, O., Purushotham, S., Masic, A., Ramanujan, R.V. & Miserez, A. Catechol-functionalized chitosan/iron oxide nanoparticle composite inspired by mussel thread coating and squid beak interfacial chemistry. Langmuir 29, 10899-10906 (2013).
14. Miserez, A., Rubin, D. & Waite, J.H. Cross-linking chemistry of squid beak. J. Biol. Chem. 285, 38115-38124 (2010).
15. Rubin, D.J., Miserez, A. & Waite, J.H. Diverse strategies of protein sclerotization in marine invertebrates: structure-property relationships in natural biomaterials. Adv. Insect Physiol. 38, 75-133 (2010).
16. Dilly, P.N. & Nixon, M. The cells that secrete the beaks in octopods and squids (Mollusca, Cephalopoda). Cell Tissue Res. 167, 229-241 (1976).
17. Grabherr, M.G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644-652 (2011).
18. de Kruif, C.G., Weinbreck, F. & De Vries, R.K. Complex coacervation of proteins and anionic polysaccharides. Curr. Opin. Colloid Interface Sci. 9, 340-349 (2004).
19. Smith, B.J. in The Protein Protocols Handbook (ed. Walker, J.M.) 507-510 (Humana Press Inc., 2002).
20. Miserez, A., Li, Y., Waite, J.H. & Zok, F. Jumbo squid beaks: inspiration for design of robust organic composites. Acta Biomater. 3, 139-149 (2007).
21. Sahal, D. et al. Specific and instantaneous one-step chemodetection of histidine-rich proteins by Pauly's stain. Anal. Biochem. 308, 405-408 (2002).
22. de Castro, E. et al. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34, W362-W365 (2006).
23. Li, A.Q. et al. Chemical cleavage at aspartyl residues for protein identification. Anal. Chem. 73, 5395-5402 (2001).
24. Tan, Y., Yildiz, U.H., Wei, W., Waite, J.H. & Miserez, A. Layer-by-layer polyelectrolyte deposition: a mechanism for forming biocomposite materials. Biomacromolecules 14, 1715-1726 (2013).
25. Mithieux, S.M. & Weiss, A.S. in Fibrous Proteins: Coiled-Coils, Collagen and Elastomers (Advances in Protein Chemistry vol. 7) (eds. Parry, D.A.D. & Squire, J.M.) 437-461 (Elsevier Academic Press Inc., 2005).
26. Yeo, G.C., Keeley, F.W. & Weiss, A.S. Coacervation of tropoelastin. Adv. Colloid Interface Sci. 167, 94-103 (2011).
27. Wei, W. et al. A mussel-derived one component adhesive coacervate. Acta Biomater. 10, 1663-1670 (2014).
28. Ortony, J.H., Hwang, D.S., Franck, J.M., Waite, J.H. & Han, S. Asymmetric collapse in biomimetic complex coacervates revealed by local polymer and water dynamics. Biomacromolecules 14, 1395-1402 (2013).
29. Kizilay, E., Kayitmazer, A.B. & Dubin, P.L. Complexation and coacervation of polyelectrolytes with oppositely charged colloids. Adv. Colloid Interface Sci. 167, 24-37 (2011).
30. Betre, H., Setton, L.A., Meyer, D.E. & Chilkoti, A. Characterization of a genetically engineered elastin-like polypeptide for cartilaginous tissue repair. Biomacromolecules 3, 910-916 (2002).
31. Spruijt, E., Sprakel, J., Cohen-Stuart, M.A. & van der Gucht, J. Interfacial tension between a complex coacervate phase and its coexisting aqueous phase. Soft Matter 6, 172-178 (2010).
32. Weinbreck, F., de Vries, R., Schrooyen, P. & de Kruif, C.G. Complex coacervation of whey proteins and gum arabic. Biomacromolecules 4, 293-303 (2003).
33. Kaibara, K., Okazaki, T., Bohidar, H.B. & Dubin, P.L. pH-induced coacervation in complexes of bovine serum albumin and cationic polyelectrolytes. Biomacromolecules 1, 100-107 (2000).
34. Lin, J. & Brown, C.W. Spectroscopic measurement of NaCl and seawater salinity in the near-IR region of 680-1230 nm. Appl. Spectrosc. 47, 239-241 (1993).
35. Liu, B., Burdine, L. & Kodadek, T. Chemistry of periodate-mediated cross-linking of 3,4-dihydroxylphenylalanine-containing molecules to proteins. J. Am. Chem. Soc. 128, 15228-15235 (2006).
36. Kerwin, J.L. et al. Mass spectrometric analysis of catechol-histidine adducts from insect cuticle. Anal. Biochem. 268, 229-237 (1999).
37. Guerette, P.A. et al. Accelerating the design of biomimetic materials by integrating RNA-seq with proteomics and materials science. Nat. Biotechnol. 31, 908-915 (2013).
38. Zhao, H., Sun, C., Stewart, R.J. & Waite, J.H. Cement proteins of the tube-building polychaete Phragmatopoma californica. J. Biol. Chem. 280, 42938-42944 (2005).
39. Oparin, A.I. & Synge, A. The Origin of Life on the Earth 3rd edn. (Academic Press, 1957).
40. Hwang, D.S. et al. Viscosity and interfacial properties in a mussel-inspired adhesive coacervate. Soft Matter 6, 3232-3236 (2010).
41. Fournier, R.L. Basic Transport Phenomena in Biomedical Engineering 3rd edn. (CRC Press, Taylor & Francis Group, 2012).
42. Vrhovski, B. & Weiss, A.S. Biochemistry of tropoelastin. Eur. J. Biochem. 258, 1-18 (1998).
43. Giesa, T. & Buehler, M.J. Nanoconfinement and the strength of biopolymers. Annu. Rev. Biophys. 42, 651-673 (2013).
44. Gosline, J.M., Guerette, P.A., Ortlepp, C.S. & Savage, K.N. The mechanical design of spider silks: from fibroin sequence to mechanical function. J. Exp. Biol. 202, 3295-3303 (1999).
45. d'Orbigny, A.D. et al. Voyage dans l'Amérique méridionale: Tome Neuvième (Pitois-Levrault, Paris, 1847).
46. Schägger, H. Tricine-SDS-PAGE. Nat. Protoc. 1, 16-22 (2006).
47. Paz, M.A., Fluckiger, R., Boak, A., Kagan, H.M. & Gallop, P.M. Specific detection of quinoproteins by redox-cycling staining. J. Biol. Chem. 266, 689-692 (1991).
48. Stajich, J.E. et al. The Bioperl toolkit: Perl modules for the life sciences. Genome Res. 12, 1611-1618 (2002).
49. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J.V. & Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860 (2006).
50. Edgar, R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
51. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M. & Barton, G.J. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).
52. Larkin, M.A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
53. Newman, A.M. & Cooper, J.B. XSTREAM: A practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics 8, 382 (2007).
54. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
55. Rebers, J.E. & Willis, J.H. A conserved domain in arthropod cuticular proteins binds chitin. Insect Biochem. Mol. Biol. 31, 1083-1093 (2001).
56. Goodarzi, M.T., Fotinopoulou, A. & Turner, G.A.A. in The Protein Protocols Handbook Springer Protocols Handbooks (ed. Walker, J.M.) 1205-1214 (Humana Press, 2009).
57. Hwang, D.S., Waite, J.H. & Tirrell, M. Promotion of osteoblast proliferation on complex coacervation-based hyaluronic acid-recombinant mussel adhesive protein coatings on titanium. Biomaterials 31, 1080-1084 (2010).