The microscopic network structure of mussel (Mytilus) adhesive plaques

Journal of the Royal Society Interface

Volumn 12, Issue 113, 2015, Pages

  Filippidi, Emmanouela ^a   DeMartini, Daniel G ^b   De Molina, Paula Malo ^c   Danner, Eric W ^d   Kim, Juntae ^c   Helgeson, Matthew E ^c   Waite, J Herbert ^a,b,d   Valentine, Megan T ^a,e  

^a Materials Research Laboratory   (United States)

^b Cellular and Developmental Biology Laboratory   (United States)

^c Chemical Engineering Laboratory   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e University of California   (United States)

Author keywords

Electron microscopy; Mussels; Mytilus; Plaques; Small angle neutron scattering

Indexed keywords

ALKALINITY; BIOMIMETIC MATERIALS; BIOMIMETICS; COMPLEX NETWORKS; ELECTRON MICROSCOPES; ELECTRON MICROSCOPY; MOLLUSCS; NEUTRON SCATTERING; OCEAN CURRENTS; SELF ASSEMBLY;

CHARACTERISTIC LENGTH; KINETICALLY CONTROLLED; MOLECULAR COMPOSITIONS; MUSSELS; MYTILUS; MYTILUS CALIFORNIANUS; MYTILUS GALLOPROVINCIALIS; PLAQUES;

NETWORK ARCHITECTURE;

ARTICLE; CONTROLLED STUDY; CROSS LINKING; DENATURATION; MYTILUS; MYTILUS CALIFORNIANUS; MYTILUS GALLOPROVINCIALIS; NEUTRON SCATTERING; NONHUMAN; SCANNING ELECTRON MICROSCOPY; TEMPERATURE; ANIMAL; ANIMAL STRUCTURES; CHEMISTRY; ULTRASTRUCTURE;

ANIMAL STRUCTURES; ANIMALS; MYTILUS;

EID: 84954137983     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2015.0827     Document Type: Article

References (41)

1. Carrington E, Moeser GM, Dimond J, Mello JJ, Boller ML. 2009 Seasonal disturbance to mussel beds: Field test of a mechanistic model predicting wave dislodgment. Limnol. Oceanogr. 54, 978-986. (doi:10.4319/lo.2009.54. 3.0978)
2. Lee H, Lee BP, Messersmith PB. 2007 A reversible wet/dry adhesive inspired by mussels and geckos. Nature 448, 338-341. (doi:10.1038/nature05968)
3. Zhong C, Gurry T, Cheng AA, Downey J, Deng Z, Stultz CM, Lu TK. 2014 Strong underwater adhesives made by self-assembling multi-protein nanofibres. Nat. Nanotechnol. 9, 858-866. (doi:10.1038/nnano. 2014.199)
4. Meredith HJ, Jenkins CL, Wilker JJ. 2014 Strong underwater adhesives made by self-assembling multi-protein nanofibres. Adv. Funct. Mater. 24, 3259-3267. (doi:10.1002/adfm.201303536)
5. Brubaker CE, Kissler H, Wang L-J, Kaufman DB, Messersmith PB. 2010 Biological performance of mussel-inspired adhesive in extrahepatic islet transplantation. Biomaterials 31, 420-427. (doi:10. 1016/j.biomaterials.2009.09.062)
6. Mehdizadeh M, Weng H, Gyawali D, Tang L, Yang J. 2012 Injectable citrate-based mussel-inspired tissue bioadhesives with high wet strength for sutureless wound closure. Biomaterials 33, 7972-7983. (doi:10.1016/j.biomaterials.2012.07.055)
7. Qin Z, Buehler MJ. 2013 Impact tolerance in mussel thread networks by heterogeneous material distribution. Nat. Commun. 4, 1-8. (doi:10.1038/ncomms3187)
8. Desmond KW, Zacchia NA, Waite JH, Valentine MT. 2015 Dynamics of mussel plaque detachment. Soft Matter 11, 6832-6839. (doi:10.1039/C5SM01072A)
9. Meadows PS, Shand P. 1989 Experimental analysis of byssus thread production by Mytilus edulis and Modiolus modiolus in sediments. Mar. Biol. 101, 219-226. (doi:10.1007/BF00391461)
10. Danner EW, Kan Y, Hammer MU, Israelachvili JN, Waite JH. 2012 Adhesion of mussel foot protein mefp-5 to mica: An underwater superglue. Biochemistry 51, 6511-6518. (doi:10.1021/bi3002538)
11. Yu J, Wei W, Danner EW, Ashley RK, Israelachvili JN, Waite JH. 2011 Mussel protein adhesion depends on interprotein thiol-mediated redox modulation. Nat. Chem. Biol. 7, 588-590. (doi:10.1038/nchembio.630)
12. Lee BP, Messersmith PB, Israelachvili JN, Waite JH. 2011 Mussel-inspired adhesives and coatings. Annu. Rev. Mater. Res. 41, 99-132. (doi:10.1146/annurevmatsci-062910-100429)
13. McDowell LM, Burzio LA, Waite JH, Schaefer J. 1999 Rotational echo double resonance detection of cross-links formed in mussel byssus under highflow stress. J. Biol. Chem. 274, 20 293-20 295. (doi:10.1074/jbc.274.29.20293)
14. Hwang DS, Waite JH. 2012 Three intrinsically unstructured mussel adhesive proteins, mfp-1, mfp-2, and mfp-3: Analysis by circular dichroism. Protein Sci. 21, 1689-1695. (doi:10.1002/pro.2147)
15. Tamarin A, Lewis P, Askey J. 1976 The structure and formation of the byssus attachment plaque in Mytilus. J. Morphol. 149, 199-221. (doi:10.1002/jmor.1051490205)
16. Kline SR. 2006 Reduction and analysis of SANS and USANS data using IGOR Pro. J. Appl. Cryst. 39, 895-900. (doi:10.1107/S0021889806035059)
17. Bressler I, Kohlbrecher J, Thünemann AF. 2015 SASfit: A comprehensive tool for small-angle scattering data analysis. (http://arxiv.org/abs/1506.02958)
18. Nordestgaard BG, Rostgaard J. 1985 Critical-point drying versus freeze drying for scanning electron microscopy: A quantitative and qualitative study on isolated hepatocytes. J. Microsc. 137, 189-207. (doi:10.1111/j.1365-2818.1985.tb02577.x)
19. Bray DF, Bagu J, Koegler P. 1993 Comparison of hexamethyldisilazane (HMDS), Peldri II, and criticalpoint drying methods for scanning electron microscopy of biological specimens. Microsc. Res. Tech. 26, 489-495. (doi:10.1002/jemt. 1070260603)
20. Michailidis N, Stergioudi F, Omar H, Tsipas DN. 2008 Investigation of the mechanical behavior of opencell Ni foams by experimental and FEM procedures. Adv. Eng. Mater. 10, 1122-1126. (doi:10.1002/adem.200800152)
21. Wei W, Tan Y, Martinez Rodriguez NR, Yu J, Israelachvili JN, Waite JH. 2014 A mussel-derived one component adhesive coacervate. Acta Biomater. 10, 1663-1670. (doi:10.1016/j.actbio.2013.09.007)
22. Zheden V, von Byern J, Kerbl A, Leisch N, Staedler Y, Grunwald I, Power AM, Klepal W. 2012 Morphology of the cement apparatus and the cement of the buoy barnacle Dosima fascicularis (Crustacea, Cirripedia, Thoracica, Lepadidae). Biol. Bull. 223, 192-204.
23. Stewart RJ, Weaver JC, Morse DE, Waite JH. 2004 The tube cement of Phragmatopoma californica: A solid foam. J. Exp. Biol. 207, 4727-4734. (doi:10. 1242/jeb.01330)
24. Wang CS, Stewart RJ. 2013 Multipart copolyelectrolyte adhesive of the sandcastle worm, Phragmatopoma californica (Fewkes): Catechol oxidase catalyzed curing through peptidyl-DOPA. Biomacromolecules 14, 1607-1617. (doi:10.1021/bm400251k)
25. Foster T, Safran SA, Sottmann T, Strey R. 2007 Scattering form factors for self-assembled network junctions. J. Chem. Phys. 127, 204711. (doi:10. 1063/1.2748754)
26. Hammouda B. 2012 Small-angle scattering from branched polymers. Macromol. Theory Simul. 21, 372-381. (doi:10.1002/mats.201100111)
27. Shibayama M. 1998 Spatial inhomogeneity and dynamic fluctuations of polymer gels. Macrom. Chem. Phys. 199, 1-30. (doi:10.1002/(SICI)1521-3935(19980101)199:1,1::AID-MACP1.3.0. CO;2-M)
28. Nie J, Du B, Oppermann W. 2004 Influence of formation conditions on spatial inhomogeneities in poly(N-isopropylacrylamide) hydrogels. Macromolecules 37, 6558-6564. (doi:10.1021/ma049169d)
29. Kohn JE et al. 2004 Random-coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl Acad. Sci. USA 101, 12 491-12 496. (doi:10. 1073/pnas.0403643101)
30. Le Guillou JC, Zinn-Justin J. 1977 Critical exponents for the n-vector model in three dimensions from field theory. Phys. Rev. Lett. 39, 95-98. (doi:10. 1103/PhysRevLett.39.95)
31. Millett IS, Doniach S, Plaxco KW. 2002 Toward a taxonomy of the denatured state: Small angle scattering studies of unfolded proteins. Adv. Protein Chem. 62, 241-262. (doi:10.1016/S0065-3233 (02)62009-1)
32. National Center for Biotechnology Information protein database. 2014 See www.ncbi.nlm.nih.gov/protein/?term=foot+protein+mytilus.
33. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011 SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods. 8, 785-786. (doi:10.1038/nmeth.1701)
34. Kohn JE, Millett IS, Jacob J, Zagrovic B, Dillon TM, Cingel N et al. 2005 Correction for Kohn et al., Random-coil behavior and the dimensions of chemically unfolded proteins, PNAS 2004 101:12491-12496.
35. Proc. Natl Acad. Sci. USA 102, 14475. (doi:10.1073/pnas.0507472102)
36. Griffiths CL, King JA. 1979 Energy expended on growth and gonad output in the ribbed mussel Aulacomya ater. Mar. Biol. 53, 217-222. (doi:10. 1007/BF00952429)
37. O'Donnell MJ, George MN, Carrington E. 2013 Mussel byssus attachment weakened by ocean acidification. Nat. Clim. Change 3, 587-590. (doi:10.1038/nclimate1846)
38. Monera OD, Kay CM, Hodges RS. 1994 Protein denaturation with guanidine hydrochloride or urea provides. Protein Sci. 3, 1984-1991. (doi:10.1002/pro.5560031110)
39. Zhao H, Waite JH. 2006 Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus. J. Biol. Chem. 281, 26 150-26 158. (doi:10.1074/jbc.M604357200)
40. National Oceanic and Atmospheric Administration. 2015 Water temperature table of the South Pacific Coast. See www.nodc.noaa.gov/dsdt/cwtg/spac.html.
41. Martinez Rodriguez NR, Das S, Kaufman Y, Israelachvili JN, Waite JH. 2015 Interfacial pH during mussel adhesive plaque formation. Biofouling 31, 221-227. (doi:10.1080/08927014.2015.1026337)