Advertisement

BioMetals

, Volume 22, Issue 4, pp 595–604 | Cite as

Surface modifications based on the cyanobacterial siderophore anachelin: from structure to functional biomaterials design

  • Karl Gademann
  • Joanna Kobylinska
  • Jean-Yves Wach
  • Tom M. Woods
Article

Abstract

This review describes the design, synthesis and evaluation of novel catechol based anchors for surface modification. The anachelin chromophore, the catecholate fragment of the siderophore anachelin from the cyanobacterium Anabaena cylindrica, allows for the immobilization of polyethylene glycol (PEG) on titania and glass surfaces thus rendering them protein resistant and antifouling. It is proposed that catecholate siderophores constitute a class of natural products useful for surface modification similar to dihydroxyphenylalanine and dopamine derived compounds found in mussel adhesive proteins. Second-generation dopamine derivatives featuring a quaternary ammonium group were found to be equally efficient in generating antifouling surfaces. The anachelin chromophore, merged via a PEG linker to the glycopeptide antibiotic vancomycin, allowed for the generation of antimicrobial surfaces through an operationally simple dip-and-rinse procedure. This approach offers an option for the prevention of nosocomial infections through antimicrobial implants, catheters and stents. Consequences for the mild generation of functional biomaterials are discussed and novel strategies for the immobilization of complex natural products, proteins and DNA on surfaces are presented.

Keywords

Natural products Siderophores Surface chemistry Biomaterials Organic synthesis 

Notes

Acknowledgments

K.G. is a European Young Investigator (EURYI). Support of this work by the SNF is gratefully acknowledged (PE002-117136/1 and 200021-115918/1). We thank Prof. Dr. Marcus Textor, Barbora Malisova and Sina Saxer (ETH Zürich) and Dr. Stefan Zürcher and Dr. Samuele Tosatti (SurfaceSolutionS, Dübendorf) for the excellent collaboration.

References

  1. Antoci V Jr, Adams CS, Hickok NJ, Shapiro IM, Parvizi J (2007a) Vancomycin bound to Ti rods reduces periprosthetic infection: Preliminary study. Clin Orthop Relat Res 461:88–95PubMedGoogle Scholar
  2. Antoci V Jr, King SB, Jose B, Parvizi J, Zeiger AR, Wickstrom E, Freeman TA, Composto RJ, Ducheyne P, Shapiro IM, Hickok NJ, Adams CS (2007b) Vancomycin covalently bonded to titanium alloy prevents bacterial colonization. J Orthop Res 25:858–866. doi: 10.1002/jor.20348 PubMedCrossRefGoogle Scholar
  3. Barbaras D, Gademann K (2008) Stable beta turns of tripeptides in water through cation-pi interactions. Chembiochem 9:2398–2401. doi: 10.1002/cbic.200800344 PubMedCrossRefGoogle Scholar
  4. Barbaras D, Kaiser M, Brun R, Gademann K (2008) Potent and selective antiplasmodial activity of the cyanobacterial alkaloid nostocarboline and its dimers. Bioorg Med Chem Lett 18:4413–4415. doi: 10.1016/j.bmcl.2008.06.049 PubMedCrossRefGoogle Scholar
  5. Becher PG, Beuchat J, Gademann K, Jüttner F (2005) Nostocarboline: Isolation and synthesis of a new cholinesterase inhibitor from Nostoc 78–12A. J Nat Prod 68:1793–1795. doi: 10.1021/np050312l PubMedCrossRefGoogle Scholar
  6. Becher PG, Baumann HI, Gademann K, Jüttner F (2009) The cyanobacterial alkaloid nostocarboline: an inhibitor of acetylcholinesterase and trypsin. J Appl Phycol 21:103–110. doi: 10.1007/s10811-008-9335-3 CrossRefGoogle Scholar
  7. Beiderbeck H, Taraz K, Budzikiewicz H, Walsby AE (2000) Anachelin, the siderophore of the cyanobacterium Anabaena cylindrica CCAP 1403/2A. Z Naturforsch C Biosci 55:681–687Google Scholar
  8. Bethuel Y, Gademann K (2005) Synthesis and evaluation of the bis-nor-anachelin chromophore as potential cyanobacterial ligand. J Org Chem 70:6258–6264. doi: 10.1021/jo050674y PubMedCrossRefGoogle Scholar
  9. Blom JF, Brutsch T, Barbaras D, Bethuel Y, Locher HH, Hubschwerlen C, Gademann K (2006) Potent algicides based on the cyanobacterial alkaloid nostocarboline. Org Lett 8:737–740. doi: 10.1021/ol052968b PubMedCrossRefGoogle Scholar
  10. Bonazzi S, Güttinger S, Zemp I, Kutay U, Gademann K (2007) Total synthesis, configuration, and biological evaluation of anguinomycin C. Angew Chem Int Ed 46:8707–8710. doi: 10.1002/anie.200703134 CrossRefGoogle Scholar
  11. Burja AM, Banaigs B, Abou-Mansour E, Burgess JG, Wright PC (2001) Marine cyanobacteria–a prolific source of natural products. Tetrahedron 57:9347–9377. doi: 10.1016/S0040-4020(01)00931-0 CrossRefGoogle Scholar
  12. Burke JP (2003) Infection control–a problem for patient safety. N Engl J Med 348:651–656. doi: 10.1056/NEJMhpr020557 PubMedCrossRefGoogle Scholar
  13. Cardo D, Horan T, Andrus M, Dembinski M, Edwards J, Peavy G, Tolson J, Wagner D (2004) National nosocomial infections surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 32:470–485. doi: 10.1016/j.ajic.2004.10.001 CrossRefGoogle Scholar
  14. Carmichael WW (1992) Cyanobacteria secondary metabolites–the cyanotoxins. J Appl Bacteriol 72:445–459PubMedGoogle Scholar
  15. Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 270:78–86PubMedCrossRefGoogle Scholar
  16. Chen Q, Jia Y, Liu S, Mogilevsky G, Kleinhammes A, Wu Y (2008) Molecules immobilization in titania nanotubes: a solid-state NMR and computational chemistry study. J Phys Chem C 112:17331–17335. doi: 10.1021/jp8050593 CrossRefGoogle Scholar
  17. Christiansen G, Yoshida WY, Blom JF, Portmann C, Gademann K, Hemscheidt T, Kurmayer R (2008) Isolation and structure determination of two microcystins and sequence comparison of the McyABC adenylation domains in planktothrix species. J Nat Prod 71:1881–1886. doi: 10.1021/np800397u CrossRefGoogle Scholar
  18. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745. doi: 10.1146/annurev.mi.49.100195.003431 PubMedCrossRefGoogle Scholar
  19. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322. doi: 10.1126/science.284.5418.1318 PubMedCrossRefGoogle Scholar
  20. Crichton R (2001) Inorganic biochemistry of iron metabolism: from molecular mechanism to clinical consequences, 2nd edn. Wiley, New YorkGoogle Scholar
  21. Cunnion KM, Lee JC, Frank MM (2001) Capsule production and growth phase influence binding of complement to staphylococcus aureus. Infect Immun 69:6796–6803. doi: 10.1128/IAI.69.11.6796-6803.2001 PubMedCrossRefGoogle Scholar
  22. Dalsin JL, Hu B-H, Lee BP, Messersmith PB (2003) Mussel adhesive protein mimetic polymers for the preparation of nonfouling surfaces. J Am Chem Soc 125:4253–4258. doi: 10.1021/ja0284963 PubMedCrossRefGoogle Scholar
  23. Dalsin JL, Lin LJ, Tosatti S, Voros J, Textor M, Messersmith PB (2005) Protein resistance of titanium oxide surfaces modified by biologically inspired mPEG-DOPA. Langmuir 21:640–646. doi: 10.1021/la048626g PubMedCrossRefGoogle Scholar
  24. Dawes IW, Mandelstam J (1970) Sporulation of bacillus-subtilis in continuous culture. J Bacteriol 103:529–535PubMedGoogle Scholar
  25. Deming TJ (1999) Mussel byssus and biomolecular materials. Curr Opin Chem Biol 3:100–105. doi: 10.1016/S1367-5931(99)80018-0 PubMedCrossRefGoogle Scholar
  26. Desai NP, Hubbell JA (1991) Solution technique to incorporate polyethylene oxide and other water-soluble polymers into surfaces of polymeric biomaterials. Biomaterials 12:144–153. doi: 10.1016/0142-9612(91)90193-E PubMedCrossRefGoogle Scholar
  27. Drechsel H, Jung G (1998) Peptide siderophores. J Pept Sci 4:147–181. doi: 10.1002/(SICI)1099-1387(199805)4:3<147::AID-PSC136>3.0.CO;2-C PubMedCrossRefGoogle Scholar
  28. Edupuganti OP, Antoci V, King SB, Jose B, Adams CS, Parvizi J, Shapiro IM, Zeiger AR, Hickok NJ, Wickstrom E (2007) Covalent bonding of vancomycin to Ti6Al4 V alloy pins provides long-term inhibition of Staphylococcus aureus colonization. Bioorg Med Chem Lett 17:2692–2696. doi: 10.1016/j.bmcl.2007.03.005 PubMedCrossRefGoogle Scholar
  29. Gademann K (2005) Mechanistic studies on the tyrosinase-catalyzed formation of the anachelin chromophore. Chembiochem 6:913–919. doi: 10.1002/cbic.200400343 PubMedCrossRefGoogle Scholar
  30. Gademann K (2006) Natural product hybrids. Chimia (Aarau) 60:841–845. doi: 10.2533/chimia.2006.841 CrossRefGoogle Scholar
  31. Gademann K (2007) Cyanobacterial natural products for the inhibition of biofilm formation and biofouling. Chimia (Aarau) 61:373–377. doi: 10.2533/chimia.2007.373 CrossRefGoogle Scholar
  32. Gademann K, Bethuel Y (2004a) A biomimetic route to the peptide alkaloid anachelin. Angew Chem Int Ed 43:3327–3329. doi: 10.1002/anie.200453909 CrossRefGoogle Scholar
  33. Gademann K, Bethuel Y (2004b) Total synthesis of anachelin H. Org Lett 6:4707–4710. doi: 10.1021/ol048068x PubMedCrossRefGoogle Scholar
  34. Gademann K, Portmann C (2008) Secondary metabolites from cyanobacteria: complex structures and powerful bioactivities. Curr Org Chem 12:326–341. doi: 10.2174/138527208783743750 CrossRefGoogle Scholar
  35. Gademann K, Bethuel Y, Locher HH, Hubschwerlen C (2007) Biomimetic total synthesis and antimicrobial evaluation of anachelin H. J Org Chem 72:8361–8370. doi: 10.1021/jo701402b PubMedCrossRefGoogle Scholar
  36. Gold HS, Moellering RC (1996) Drug therapy–antimicrobial-drug resistance. N Engl J Med 335:1445–1453. doi: 10.1056/NEJM199611073351907 PubMedCrossRefGoogle Scholar
  37. Goldman SJ, Lammers PJ, Berman MS, Sanders-Loehr J (1983) Siderophore-mediated iron uptake in different strains of Anabaena sp. J Bacteriol 156:1144–1150PubMedGoogle Scholar
  38. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108. doi: 10.1038/nrmicro821 PubMedCrossRefGoogle Scholar
  39. Harada K (2004) Production of secondary metabolites by freshwater cyanobacteria. Chem Pharm Bull (Tokyo) 52:889–899. doi: 10.1248/cpb.52.889 CrossRefGoogle Scholar
  40. Herrero A, Flores E (eds) (2008) The cyanobacteria: molecular biology, genomics and evolution. Caister Academic Press, SevillaGoogle Scholar
  41. Higashi JM, Wang IW, Shlaes DM, Anderson JM, Marchant RE (1998) Adhesion of Staphylococcus epidermidis and transposon mutant strains to hydrophobic polyethylene. J Biomed Mater Res 39:341–350. doi: 10.1002/(SICI)1097-4636(19980305)39:3<341::AID-JBM1>3.0.CO;2-J PubMedCrossRefGoogle Scholar
  42. Ito Y, Butler A (2005) Structure of synechobactins, new siderophores of the marine cyanobacterium Synechococcus sp PCC 7002. Limnol Oceanogr 50:1918–1923Google Scholar
  43. Ito Y, Ishida K, Okada S, Murakami M (2004) The absolute stereochemistry of anachelins, siderophores from the cyanobacterium Anabaena cylindrica. Tetrahedron 60:9075–9080. doi: 10.1016/j.tet.2004.07.105 CrossRefGoogle Scholar
  44. Itou Y, Okada S, Murakami M (2001) Two structural isomeric siderophores from the freshwater cyanobacterium Anabaena cylindrica (NIES-19). Tetrahedron 57:9093–9099. doi: 10.1016/S0040-4020(01)00934-6 CrossRefGoogle Scholar
  45. Jose B, Antoci V, Zeiger AR, Wickstrom E, Hickok NJ (2005) Vancomycin covalently bonded to titanium beads kills Staphylococcus aureus. Chem Biol 12:1041–1048. doi: 10.1016/j.chembiol.2005.06.013 PubMedCrossRefGoogle Scholar
  46. Kahne D, Leimkuhler C, Lu W, Walsh C (2005) Glycopeptide and lipoglycopeptide antibiotics. Chem Rev 105:425–448. doi: 10.1021/cr030103a PubMedCrossRefGoogle Scholar
  47. Keller-Schierlein W, Prelog V, Zähner H (1964) Siderochrome. (Natürliche Eisen(III)-trihydroxamat-Komplexe). Fortschr Chem Org Naturst 22:279–322Google Scholar
  48. Klibanov AM (2007) Permanently microbicidal materials coatings. J Mat Chem 17:2479–2482. doi:  10.1039/b702079a CrossRefGoogle Scholar
  49. Kolasa T, Miller MJ (1990) Synthesis of the chromophore of pseudobactin, a fluorescent siderophore from Pseudomonas. J Org Chem 55:4246–4255. doi: 10.1021/jo00301a008 CrossRefGoogle Scholar
  50. Konradi R, Pidhatika B, Mühlebach A, Textor M (2008) Poly-2-methyl-2-oxazoline: A peptide-like polymer for protein-repellent surfaces. Langmuir 24:613–616. doi: 10.1021/la702917z PubMedCrossRefGoogle Scholar
  51. Lammers PJ, Sanders-Loehr J (1982) Active transport of ferric schizokinen in anabaena sp. J Bacteriol 151:288–294PubMedGoogle Scholar
  52. Lawrence AK, Gademann K (2008) Aza-annulation strategies in alkaloid total synthesis. Synthesis 331–351. doi: 10.1055/s-2008-1032134
  53. Leape LL, Brennan TA, Laird N, Lawthers AG, Localio AR, Barnes BA, Hebert L, Newhouse JP, Weiler PC, Hiatt H (1991) The nature of adverse events in hospitalized-patients–results of the harvard medical-practice study. N Engl J Med 324:377–384PubMedGoogle Scholar
  54. Lee JH, Kopecek J, Andrade JD (1989) Protein-resistant surfaces prepared by PEO-containing block copolymer surfactants. J Biomed Mater Res 23:351–368. doi: 10.1002/jbm.820230306 PubMedCrossRefGoogle Scholar
  55. Lee JH, Ju YM, Kim DM (2000) Platelet adhesion onto segmented polyurethane film surfaces modified by addition and crosslinking of PEO-containing block copolymers. Biomaterials 21:683–691. doi: 10.1016/S0142-9612(99)00197-0 PubMedCrossRefGoogle Scholar
  56. Lee H, Dellatore SM, Miller WM, Messersmith PB (2007) Mussel-inspired surface chemistry for multifunctional coatings. Science 318:426–430. doi: 10.1126/science.1147241 PubMedCrossRefGoogle Scholar
  57. Love JC, Estroff LA, Kriebel JK, Nuzzo RG, Whitesides GM (2005) Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chem Rev 105:1103–1169. doi: 10.1021/cr0300789 PubMedCrossRefGoogle Scholar
  58. Luesch H, Harrigan GG, Goetz G, Horgen FD (2002) The cyanobacterial origin of potent anticancer agents originally isolated from sea hares. Curr Med Chem 9:1791–1806PubMedGoogle Scholar
  59. Mah TFC, O’toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39. doi: 10.1016/S0966-842X(00)01913-2 PubMedCrossRefGoogle Scholar
  60. Marsh LH, Coke M, Dettmar PW, Ewen RJ, Havler M, Nevell TG, Smart JD, Smith JR, Timmins B, Tsibouklis J, Alexander C (2002) Adsorbed poly(ethyleneoxide)-poly(propyleneoxide) copolymers on synthetic surfaces: Spectroscopy and microscopy of polymer structures and effects on adhesion of skin-borne bacteria. J Biomed Mater Res 61:641–652. doi: 10.1002/jbm.10174 PubMedCrossRefGoogle Scholar
  61. Mason HS (1965) Oxidases. Annu Rev Biochem 34:595–634. doi: 10.1146/annurev.bi.34.070165.003115 PubMedCrossRefGoogle Scholar
  62. McWhirter MJ, Bremer PJ, Lamont L, McQuillan A (2003) Siderophore-mediated covalent bonding to metal (oxide) surfaces during biofilm initiation by pseudomonas aeruginosa bacteria. Langmuir 19:3575–3577. doi: 10.1021/la020918z CrossRefGoogle Scholar
  63. Mizutani H, Takayama J, Soeda Y, Honda T (2004) A formal synthesis of a muscarinic M1 receptor antagonist, (-)-TAN1251A. Heterocycles 62:343–355. doi: 10.3987/COM-03-S(P)14 CrossRefGoogle Scholar
  64. Moser J, Punchihewa S, Infelta PP, Grätzel M (1991) Surface complexation of colloidal semiconductors strongly enhances interfacial electron-transfer rates. Langmuir 7:3012–3018. doi: 10.1021/la00060a018 CrossRefGoogle Scholar
  65. Namikoshi M, Rinehart KL (1996) Bioactive compounds produced by cyanobacteria. J Ind Microbiol Biotechnol 17:373–384. doi: 10.1007/BF01574768 CrossRefGoogle Scholar
  66. Pasche S, De Paul SM, Vörös J, Spencer ND, Textor M (2003) Poly(l-lysine)-graft-poly(ethylene glycol) assembled monolayers on niobium oxide surfaces: a quantitative study of the influence of polymer interfacial architecture on resistance to protein adsorption by ToF-SIMS and in situ OWLS. Langmuir 19:9216–9225. doi: 10.1021/la034111y CrossRefGoogle Scholar
  67. Portmann C, Blom JF, Gademann K, Jüttner F (2008a) Aerucyclamides A and B: isolation and synthesis of toxic ribosomal heterocyclic peptides from the cyanobacterium microcystis aeruginosa PCC 7806. J Nat Prod 71:1193–1196. doi: 10.1021/np800118g PubMedCrossRefGoogle Scholar
  68. Portmann C, Blom JF, Kaiser M, Brun R, Jüttner F, Gademann K (2008b) Isolation of aerucyclamides C and D and structure revision of microcyclamide 7806A: heterocyclic ribosomal peptides from microcystis aeruginosa PCC 7806 and their antiparasite evaluation. J Nat Prod 71:1891–1896. doi: 10.1021/np800409z CrossRefGoogle Scholar
  69. Portmann C, Prestinari C, Myers T, Scharte J, Gademann K (2009) Directed biosynthesis of phytotoxic alkaloids in the cyanobacterium nostoc 78–12A. Chembiochem 10:889–895. doi: 10.1002/cbic.200800837 PubMedCrossRefGoogle Scholar
  70. Prime KL, Whitesides GM (1991) Self-assembled organic monolayers: model systems for studying adsorption of proteins at surfaces. Science 252:1164–1167. doi: 10.1126/science.252.5009.1164 CrossRefGoogle Scholar
  71. Raymond KN, Müller G, Matzanke BF (1984) Complexation of iron by siderophores: a review of their solution and structural chemistry and biological function. Top Curr Chem 123:49–102Google Scholar
  72. Rice CR, Ward MD, Nazeeruddin MK, Grätzel M (2000) Catechol as an efficient anchoring group for attachment of ruthenium-polypyridine photosensitisers to solar cells based on nanocrystalline TiO2 films. New J Chem 24:651–652. doi: 10.1039/b003823g CrossRefGoogle Scholar
  73. Rodriguez-Martinez JM, Pascual A (2006) Antimicrobial resistance in bacterial biofilms. Rev Med Microbiol 17:65–75Google Scholar
  74. Roosenberg JM 2nd, Lin YM, Lu Y, Miller MJ (2000) Studies and syntheses of siderophores, microbial iron chelators, and analogs as potential drug delivery agents. Curr Med Chem 7:159–197PubMedGoogle Scholar
  75. Roth BL, Poot M, Yue ST, Millard PJ (1997) Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain. Appl Environ Microbiol 63:2421–2431PubMedGoogle Scholar
  76. Sever MJ, Weisser JT, Monahan J, Srinivasan S, Wilker JJ (2004) Metal-mediated cross-linking in the generation of a marine-mussel adhesive. Angew Chem Int Ed 43:448–450. doi: 10.1002/anie.200352759 CrossRefGoogle Scholar
  77. Siegers C, Biesalski M, Haag R (2004) Self-assembled monolayers of dendritic polyglycerol derivatives on gold that resist the adsorption of proteins. Chem Eur J 10:2831–2838. doi: 10.1002/chem.200306073 CrossRefGoogle Scholar
  78. Singh S, Kate BN, Banerjee UC (2005) Bioactive compounds from cyanobacteria and microalgae–an overview. Crit Rev Biotechnol 25:73–95. doi: 10.1080/07388550500248498 PubMedCrossRefGoogle Scholar
  79. Starfield B (2000) Is US health really the best in the world? JAMA 284:483–485. doi: 10.1001/jama.284.4.483 PubMedCrossRefGoogle Scholar
  80. Statz AR, Messersmith PB, Meagher RJ, Barron AE (2005) New peptidomimetic polymers for antifouling surfaces. J Am Chem Soc 127:7972–7973. doi: 10.1021/ja0522534 PubMedCrossRefGoogle Scholar
  81. Statz AR, Park JP, Chongsiriwatana NP, Barron AE, Messersmith PB (2008) Surface-immobilised antimicrobial peptoids. Biofouling 24:439–448. doi: 10.1080/08927010802331829 PubMedCrossRefGoogle Scholar
  82. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138. doi: 10.1016/S0140-6736(01)05321-1 PubMedCrossRefGoogle Scholar
  83. Stone PW, Braccia D, Larson E (2005) Systematic review of economic analyses of health care-associated infections. Am J Infect Control 33:501–509. doi: 10.1016/j.ajic.2005.04.246 PubMedCrossRefGoogle Scholar
  84. Upritchard HG, Yang J, Bremer PJ, Lamont IL, McQuillan AJ (2007) Adsorption to metal oxides of the Pseudomonas aeruginosa siderophore pyoverdine and implications for bacterial biofilm formation on metals. Langmuir 23:7189–7195. doi: 10.1021/la7004024 PubMedCrossRefGoogle Scholar
  85. Wach JY, Bonazzi S, Gademann K (2008a) Antimicrobial surfaces through natural product hybrids. Angew Chem Int Ed 47:7123–7126. doi: 10.1002/anie.200801570 CrossRefGoogle Scholar
  86. Wach JY, Malisova B, Bonazzi S, Tosatti S, Textor M, Zürcher S, Gademann K (2008b) Protein-resistant surfaces through mild dopamine surface functionalization. Chem Eur J 14:10579–10584. doi: 10.1002/chem.200801134 CrossRefGoogle Scholar
  87. Waite JH, Tanzer ML (1981) Polyphenolic substance of mytilus edulis: novel adhesive containing L-dopa and hydroxyproline. Science 212:1038–1040. doi: 10.1126/science.212.4498.1038 PubMedCrossRefGoogle Scholar
  88. Walsby AE (1974a) The extracellular products of anabaena cylindrica lemm. I. Isolation of a macromolecular pigment-peptide complex. Br Phycol J 9:371–381. doi: 10.1080/00071617400650441 CrossRefGoogle Scholar
  89. Walsby AE (1974b) The extracellular products of Anabaena cylindrica Lemm. II. Fluorescent substances containing serine and threonine and their role in extracellular pigment formation. Br Phycol J 9:383–391. doi: 10.1080/00071617400650451 CrossRefGoogle Scholar
  90. Walsh C (2000) Molecular mechanisms that confer antibacterial drug resistance. Nature 406:775–781. doi: 10.1038/35021219 PubMedCrossRefGoogle Scholar
  91. Xing B, Yu C-W, Chow K-H, Ho P-L, Fu D, Xu B (2002) Hydrophobic interaction and hydrogen bonding cooperatively confer a vancomycin hydrogel: a potential candidate for biomaterials. J Am Chem Soc 124:14846–14847. doi: 10.1021/ja028539f PubMedCrossRefGoogle Scholar
  92. Xu C, Xu K, Gu H, Guo Z, Xu B, Zheng R, Liu H, Zhang X (2004) Dopamine as a robust anchor to immobilize functional molecules on the iron oxide shell of magnetic nanoparticles. J Am Chem Soc 126:9938–9939. doi: 10.1021/ja0464802 PubMedCrossRefGoogle Scholar
  93. Yang Z, Galloway JA, Yu H (1999) Protein interactions with poly(ethylene glycol) self-assembled monolayers on glass substrates: diffusion and adsorption. Langmuir 15:8405–8411. doi: 10.1021/la990260y CrossRefGoogle Scholar
  94. Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology–past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104. doi: 10.1016/j.porgcoat.2003.06.001 CrossRefGoogle Scholar
  95. Zürcher S, Wäckerlin D, Bethuel Y, Malisova B, Textor M, Tosatti S, Gademann K (2006) Biomimetic surface modifications based on the cyanobacterial iron chelator anachelin. J Am Chem Soc 128:1064–1065. doi: 10.1021/ja056256s PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2009

Authors and Affiliations

  • Karl Gademann
    • 1
  • Joanna Kobylinska
    • 1
  • Jean-Yves Wach
    • 1
  • Tom M. Woods
    • 1
  1. 1.Chemical Synthesis Laboratory (SB-ISIC-LSYNC), Swiss Federal Institute of Technology (EPFL)LausanneSwitzerland

Personalised recommendations