Sea star tenacity mediated by a protein that fragments, then aggregates

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 17, 2014, Pages 6317-6322

  Hennebert, Elise ^a   Wattiez, Ruddy ^a   Demeuldre, Mélanie ^a   Ladurner, Peter ^b   Hwang, Dong Soo ^c   Waite, J Herbert ^d   Flammang, Patrick ^a  

^a UNIVERSITY OF MONS   (Belgium)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c Pohang University of Science and Technology (POSTECH)   (South Korea)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Asterias rubens; Echinoderms; Marine adhesion

Indexed keywords

CARBOHYDRATE; STRUCTURAL PROTEIN; SYNAPSIN I; TRANSCRIPTOME;

AMBIGUITY; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; FRAGMENTATION REACTION; IMMUNOHISTOCHEMISTRY; METAL BINDING; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOOTPRINTING; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; STARFISH; WESTERN BLOTTING;

ASTERIAS RUBENS; ECHINODERMS; MARINE ADHESION;

ADHESIVENESS; ANIMAL STRUCTURES; ANIMALS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEINS; STARFISH;

EID: 84899650086     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400089111     Document Type: Article

References (45)

1. Gorb SN (2008) Biological attachment devices: Exploring nature's diversity for biomimetics. Phil Trans R Soc A 366(1870):1557-1574.
2. Walker G (1987) Synthetic Adhesives and Sealants, ed Wake WC (Wiley, Chichester, UK), pp 112-135.
3. Smith AM, Callow JA (2006) Biological Adhesives (Springer-Verlag, Berlin).
4. von Byern J, Grunwald I (2010) Biological Adhesive Systems-From Nature to Technical and Medical Application (Springer-Verlag, Berlin).
5. Flammang P (1996) Echinoderm Studies, eds Jangoux M, Lawrence JM (Balkema, Rotterdam).
6. Silverman HG, Roberto FF (2007) Understanding marine mussel adhesion. Mar Biotechnol (NY) 9(6):661-681.
7. Kamino K (2010) Molecular design of barnacle cement in comparison with those of mussel and tubeworm. J Adhes 86(1):96-110.
8. Whittington ID, Cribb BW (2001) Adhesive secretions in the Platyhelminthes. Adv Parasitol 48:101-224.
9. Flammang P, Santos R, Haesaerts D (2005) Marine Molecular Biotechnology: Echinodermata, ed Matranga V (Springer-Verlag, Berlin).
10. Aldred N, Clare AS (2008) The adhesive strategies of cyprids and development of barnacle-resistant marine coatings. Biofouling 24(5):351-363.
11. Lee BP, Messersmith PB, Israelachvili JN, Waite JH (2011) Mussel-inspired adhesives and coatings. Annu Rev Mater Res 41:99-132.
12. Wang CS, Stewart RJ (2012) Localization of the bioadhesive precursors of the sandcastle worm, Phragmatopoma californica (Fewkes). J Exp Biol 215(2):351-361.
13. Smith AM, Quick TJ, St Peter RLS (1999) Differences in the composition of adhesive and non-adhesive mucus from the limpet Lottia limatula. Biol Bull 196(1):34-44.
14. Hennebert E, Wattiez R, Waite JH, Flammang P (2012) Characterization of the protein fraction of the temporary adhesive secreted by the tube feet of the sea star Asterias rubens. Biofouling 28(3):289-303.
15. Hennebert E (2010) Biological Adhesive Systems, eds von Byern J, Grunwald I (Springer-Verlag, Berlin).
16. Flammang P, Michel A, Van Cauwenberge A, Alexandre H, Jangoux M (1998) A study of the temporary adhesion of the podia in the sea star Asterias rubens (Echinodermata, Asteroidea) through their footprints. J Exp Biol 201(16):2383-2395.
17. Hennebert E, Viville P, Lazzaroni R, Flammang P (2008) Micro-and nanostructure of the adhesive material secreted by the tube feet of the sea star Asterias rubens. J Struct Biol 164(1):108-118.
18. Thomas LA, Hermans CO (1985) Adhesive interactions between the tube feet of a starfish, Leptasterias hexactis, and substrata. Biol Bull 169:675-688.
19. Hennebert E, Wattiez R, Flammang P (2011) Characterization of the carbohydrate fraction of the temporary adhesive secreted by the tube feet of the sea star Asterias rubens. Mar Biotechnol (NY) 13(3):484-495.
20. Ishihama Y, et al. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4(9):1265-1272.
21. Marchler-Bauer A, et al. (2011) CDD: A Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:D225-D229.
22. Meyer D, Girma J-P (1993) von Willebrand factor: Structure and function. Thromb Haemost 70:99-104.
23. Rao Z, et al. (1995) The structure of a Ca2+-binding epidermal growth factor-like domain: Its role in protein-protein interactions. Cell 82(1):131-141.
24. Baumgartner S, Hofmann K, Chiquet-Ehrismann R, Bucher P (1998) The discoidin domain family revisited: New members from prokaryotes and a homology-based fold prediction. Protein Sci 7(7):1626-1631.
25. Tateno H (2010) SUEL-Related Lectins, a lectin family widely distributed throughout organisms. Biosci Biotechnol Biochem 74(6):1141-1144.
26. Inoue K, Takeuchi Y, Miki D, Odo S (1995) Mussel adhesive plaque protein gene is a novel member of epidermal growth factor-like gene family. J Biol Chem 270(12): 6698-6701.
27. Hwang DS, et al. (2010) Protein-and metal-dependent interactions of a prominent protein in mussel adhesive plaques. J Biol Chem 285(33):25850-25858.
28. Sun C, Lucas JM, Waite JH (2002) Collagen-binding matrix proteins from elastomeric extraorganismic byssal fibers. Biomacromolecules 3(6):1240-1248.
29. Miseta A, Csutora P (2000) Relationship between the occurrence of cysteine in proteins and the complexity of organisms. Mol Biol Evol 17(8):1232-1239.
30. He L-S, Zhang G, Qian P-Y (2013) Characterization of two 20kDa-cement protein (cp20k) homologues in Amphibalanus Amphitrite. PLoS ONE 8:e64130, 10.1371/journal.pone.0064130.
31. Lidell ME, Johansson MEV, Hansson GC (2003) An autocatalytic cleavage in the C Terminus of the human MUC2 mucin occurs at the low pH of the late secretory pathway. J Biol Chem 278(16):13944-13951.
32. Lidell ME, Hansson GC (2006) Cleavage in the GDPH sequence of the C-terminal cysteine-rich part of the human MUC5AC mucin. Biochem J 399(1):121-129.
33. Thuveson M, Fries E (2000) The low pH in trans-Golgi triggers autocatalytic cleavage of pre-α-inhibitor heavy chain precursor. J Biol Chem 275(40):30996-31000.
34. Monnier PP, et al. (2002) RGM is a repulsive guidance molecule for retinal axons. Nature 419(6905):392-395.
35. Zhang A-S, West AP, Wyman AE, Bjorkman PJ, Enns CA (2005) Interaction of hemojuvelin with neogenin results in iron accumulation in human embryonic kidney 293 cells. J Biol Chem 280(40):33885-33894.
36. Bi M, Hickox JR, Winfrey VP, Olson GE, Hardy DM (2003) Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. Biochem J 375(2):477-488.
37. Flammang P, Demeulenaere S, Jangoux M (1994) The role of podial secretions in adhesion in two species of sea stars (Echinodermata). Biol Bull 187(1):35-47.
38. Ameye L, Hermann R, Dubois P, Flammang P (2000) Ultrastructure of the echinoderm cuticle after fast-freezing/freeze substitution and conventional chemical fixations. Microsc Res Tech 48(6):385-393.
39. Mayadas TN, Wagner DD (1992) Vicinal cysteines in the prosequence play a role in von Willebrand factor multimer assembly. Proc Natl Acad Sci USA 89:3531-3535.
40. Enghild JJ, et al. (1991) Chondroitin 4-sulfate covalently cross-links the chains of the human blood protein pre-α-inhibitor. J Biol Chem 266(2):747-751.
41. Santos R, Haesaerts D, Jangoux M, Flammang P (2005) Comparative histological and immunohistochemical study of sea star tube feet (Echinodermata, Asteroidea). J Morphol 263(3):259-269.
42. Waite JH, Andersen NH, Jewhurst S, Sun C (2005) Mussel adhesion: Finding the tricks worth mimicking. J Adhes 81(3):297-317.
43. Lee H, Lee BP, Messersmith PB (2007) A reversible wet/dry adhesive inspired by mussels and geckos. Nature 448(7151):338-341.
44. Taylor SW (2002) Chemoenzymatic synthesis of peptidyl 3,4-dihydroxyphenylalanine for structure-activity relationships in marine invertebrate polypeptides. Anal Biochem 302(1):70-74.
45. Nakano M, Shen J-R, Kamino K (2007) Self-assembling peptide inspired by a barnacle underwater adhesive protein. Biomacromolecules 8(6):1830-1835.