Assembly of collagen fibril meshes using gold nanoparticles functionalized with tris(hydroxymethyl)phosphine-alanine as multivalent cross-linking agents†
John S. Graham
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4
Department of Physics and Astronomy, University of Missouri, Columbia, MO 65211, USA
Both authors have equally contributed to the manuscript
Search for more papers by this authorYannick Miron
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4
Both authors have equally contributed to the manuscript
Search for more papers by this authorCorresponding Author
Michel Grandbois
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4.Search for more papers by this authorJohn S. Graham
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4
Department of Physics and Astronomy, University of Missouri, Columbia, MO 65211, USA
Both authors have equally contributed to the manuscript
Search for more papers by this authorYannick Miron
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4
Both authors have equally contributed to the manuscript
Search for more papers by this authorCorresponding Author
Michel Grandbois
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4
Département de Pharmacologie, Université de Sherbrooke, Sherbrooke, QC, Canada J1H-5N4.Search for more papers by this authorThis article is published in Journal of Molecular Recognition as a focus on AFM on Life Sciences and Medicine, edited by Jean-Luc Pellequer and Pierre Parot (CEA Marcoule, Life Science Division, Bagnols sur Cèze, France).
Abstract
We report on the use of tris(hydroxymethyl)phosphine-alanine (THPAL) functionalized gold nanoparticles as a multivalent cross-linking agent to assemble collagen fibrils into a mesh-like structure. Atomic force microscopy (AFM) was used for characterization of the structure after adsorption onto an atomically flat mica substrate, revealing a mesh-like construct in which the collagen fibrils and the gold nanoparticles interact to form interconnected nodes measuring from 100 to 500 nm. As expected, the density of the collagen mesh can be increased with a higher initial concentration of gold nanoparticles. The maximum thickness of the meshes (∼20 nm) obtained through cross-sectional height measurements confirms that the adsorbed structure consists of a single layer of collagen fibrils/gold nanoparticles assembled in two-dimensions. We propose that the capability of gold nanoparticles functionalized with the THPAL to bind to several collagen fibrils combined with the large persistence length of the fibrils, which was reported to be in the hundreds of nanometer range, are determinant factors for the preferential 2D growth of the mesh in solution. Copyright © 2011 John Wiley & Sons, Ltd.
REFERENCES
- Afrasiabi Z, Shukla R, Chanda N, Bhaskaran S, Upendran A, Zambre A, Katti KV, Kannan R. 2010. Nanoscale sensor design via in situ labeling of gold nanoparticles onto protein scaffolds. J. Nanosci. Nanotechnol. 10(2): 719–725.
- Birchall IE, Lee VW, Ketharanathan V. 2001. Retention of endothelium on ovine collagen biomatrix vascular conduits under physiological shear stress. Biomaterials 22(23): 3139–3144.
- Castaneda L, Valle J, Yang N, Pluskat S, Slowinska K. 2008. Collagen cross-linking with Au nanoparticles. Biomacromolecules 9(12): 3383–3388.
- Chanda N, Kan P, Watkinson LD, Shukla R, Zambre A, Carmack TL, Engelbrecht H, Lever JR, Katti K, Fent GM, Casteel SW, Smith CJ, Miller WH, Jurisson S, Boote E, Robertson JD, Cutler C, Dobrovolskaia M, Kannan R, Katti KV. 2010a. Radioactive gold nanoparticles in cancer therapy: Therapeutic efficacy studies of GA-198AuNP nanoconstruct in prostate tumor–bearing mice. Nanomed.: Nanotechnol. Biol. Med. 6(2): 201–209.
- Chanda N, Kattumuri V, Shukla R, Zambre A, Katti K, Upendran A, Kulkarni RR, Kan P, Fent GM, Casteel SW, Smith CJ, Boote E, Robertson JD, Cutler C, Lever JR, Katti KV, Kannan R. 2010b. Bombesin functionalized gold nanoparticles show in vitro and in vivo cancer receptor specificity. Proc. Natl. Acad. Sci. 107(19): 8760–8765.
- Courey MS. 2001. Homologous collagen substances for vocal fold augmentation. Laryngoscope 111(5): 747–758.
- Deng ZX, Mao CD. 2003. DNA-templated fabrication of 1D parallel and 2D crossed metallic nanowire arrays. Nano Lett. 3(11): 1545–1548.
- Fent GM, Casteel SW, Kim DY, Kannan R, Katti K, Chanda N, Katti K. 2009. Biodistribution of maltose and gum arabic hybrid gold nanoparticles after intravenous injection in juvenile swine. Nanomedicine 5(2): 128–135.
10.1016/j.nano.2009.01.007 Google Scholar
- Freyman TM, Yannas IV, Yokoo R, Gibson LJ. 2001. Fibroblast contraction of a collagen-GAG matrix. Biomaterials 22(21): 2883–2891.
- Friedrichs J, Helenius J, Muller DJ. 2010. Quantifying cellular adhesion to extracellular matrix components by single-cell force spectroscopy. Nat. Protoc. 5(7): 1353–1361.
- Griffith LG, Naughton G. 2002. Tissue engineering–current challenges and expanding opportunities. Science 295(5557): 1009–1014.
- Haidekker MA, Boettcher LW, Suter JD, Rone R, Grant SA. 2006. Influence of gold nanoparticles on collagen fibril morphology quantified using transmission electron microscopy and image analysis. BMC Med. Imaging 6: 4.
- Zhao H, Yuan B, Dou X. 2004. The effects of electrostatic interaction between biological molecules and nano-metal colloid on near-infrared surface-enhanced Raman scattering. J. Opt. A: Pure Appl. Opt. 6(9): 900–905.
- Howard J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates: USA, 367.
- Huynh T, Abraham G, Murray J, Brockbank K, Hagen PO, Sullivan S. 1999. Remodeling of an acellular collagen graft into a physiologically responsive neovessel. Nat. Biotechnol. 17(11): 1083–1086.
- Jiang F, Hörber H, Howard J, Müller DJ. 2004. Assembly of collagen into microribbons: Effects of pH and electrolytes. J. Struct. Biol. 148(3): 268–278.
- Kadler KE, Holmes DF, Trotter JA, Chapman JA. 1996. Collagen fibril formation. Biochem. J. 316: (Pt 1): 1–11.
- Kagan HM, Trackman PC. 1991. Properties and function of lysyl oxidase. Am. J. Resp. Cell Mol. Biol. 5(3): 206–210.
- Kannan R, Katti KK, Barbour LJ, Pillarsetty N, Barnes CL, Katti KV. 2003. Characterization of supramolecular (H2O)(18) water morphology and water-methanol (H2O)(15)(CH3OH)(3) clusters in a novel phosphorus functionalized trimeric amino acid host. J. Am. Chem. Soc. 125(23): 6955–6961.
- Kannan R, Rahing V, Cutler C, Pandrapragada R, Katti KK, Kattumuri V, Robertson JD, Casteel SJ, Jurisson S, Smith C, Boote E, Katti KV. 2006. Nanocompatible chemistry toward fabrication of target-specific gold nanoparticles. J. Am. Chem. Soc. 128(35): 11342–11343.
- Kannan R, Katti KK, Katti KK, White HW, Cutler CS. 2007. US patent 20070051202.
- Katti K, Kannan R, Katti K, Kattumori V, Pandrapraganda R, Rahing V, Cutler C, Boote E, Casteel S, Smith C, Robertson J, Jurrison S. 2006. Hybrid gold nanoparticles in molecular imaging and radiotherapy. Czech. J. Phys. 56(1): D23–D34.
- Katti KK, Kattumuri V, Bhaskaran S, Katti KV, Kannan R. 2009. Facile and general method for synthesis of sugar-coated gold nanoparticles. Int. J. Green Nanotechnol.: Biomed. 1(1): 53.
10.1080/19430850902983848 Google Scholar
- Kattumuri V, Katti K, Bhaskaran S, Boote EJ, Casteel SW, Fent GM, Robertson DJ, Chandrasekhar M, Kannan R, Katti KV. 2007. Gum arabic as a phytochemical construct for the stabilization of gold nanoparticles: In vivo pharmacokinetics and X-ray-contrast-imaging studies. Small 3(2): 333–341.
- Keilhoff G, Stang F, Wolf G, Fansa H. 2003. Bio-compatibility of type I/III collagen matrix for peripheral nerve reconstruction. Biomaterials 24(16): 2779–2787.
- Kikuchi M, Matsumoto HN, Yamada T, Koyama Y, Takakuda K, Tanaka J. 2004. Glutaraldehyde cross-linked hydroxyapatite/collagen self-organized nanocomposites. Biomaterials 25(1): 63–69.
- Kühner F, Erdmann M, Gaub HE. 2006. Scaling exponent and Kuhn length of pinned polymers by single molecule force spectroscopy. Phys. Rev. Lett. 97(21): 218301.
- Ma L, Gao CY, Mao ZW, Zhou J, Shen JC, Hu XQ, Han CM. 2003. Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials 24(26): 4833–4841.
- Mao C, Sun W, Shen Z, Seeman NC. 1999a. A nanomechanical device based on the B–Z transition of DNA. Nature 397(6715): 144–146.
- Mao CD, Sun WQ, Seeman NC. 1999b. Designed two-dimensional DNA Holliday junction arrays visualized by atomic force microscopy. J. Am. Chem. Soc. 121(23): 5437–5443.
- Marszalek PE, Oberhauser AF, Pang YP, Fernandez JM. 1998. Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature 396(6712): 661–664.
- Mertz EL, Leikin S. 2004. Interactions of inorganic phosphate and sulfate anions with collagen. Biochemistry (NY) 43(47): 14901–14912.
- Moores A, Goettmann F, Sanchez C, Le Floch P. 2004. Phosphinine stabilised gold nanoparticles; synthesis and immobilisation on mesoporous materials. Chem. Commun. (Cambridge) (24): 2842–2843.
- Nakao H, Shiigi H, Yamamoto Y, Tokonami S, Nagaoka T, Sugiyama S, Ohtani T. 2003. Highly ordered assemblies of Au nanoparticles organized on DNA. Nano Lett. 3(10): 1391–1394.
- Raspanti M, Viola M, Sonaggere M, Tira ME, Tenni R. 2007. Collagen fibril structure is affected by collagen concentration and decorin. Biomacromolecules 8(7): 2087–2091.
- Rief M, Oesterhelt F, Heymann B, Gaub HE. 1997. Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science 275(5304): 1295–1297.
- Rief M, Fernandez JM, Gaub HE. 1998. Elastically coupled two-level systems as a model for biopolymer extensibility. Phys. Rev. Lett. 81(21): 4764–4767.
- Sivakumar L, Agarwal G. 2010. The influence of discoidin domain receptor 2 on the persistence length of collagen type I fibers. Biomaterials 31(18): 4802–4808.
- Stevens MM, George JH. 2005. Exploring and engineering the cell surface interface. Science 310(5751): 1135–1138.
- Storhoff JJ, Lazarides AA, Mucic RC, Mirkin CA, Letsinger RL, Schatz GC. 2000. What controls the optical properties of DNA-linked gold nanoparticle assemblies? J. Am. Chem. Soc. 122(19): 4640–4650.
- Taton TA, Mucic RC, Mirkin CA, Letsinger RL. 2000. The DNA-mediated formation of supramolecular mono- and multilayered nanoparticle structures. J. Am. Chem. Soc. 122(26): 6305–6306.
- Turberfield AJ, Mitchell JC, Yurke B, Mills AP, Blakey MI, Simmel FC. 2003. DNA fuel for free-running nanomachines. Phys. Rev. Lett. 90(11): 118102.
- Van Der Aa BC, Michel RM, Asther M, Torrez Zamora, M, Rouxhet PG, Dufrêne, YF. 2001. Stretching cell surface macromolecules by atomic force microscopy. Langmuir 17(11): 3116–3119.
- Viator JA, Gupta S, Goldschmidt BS, Bhattacharyyal K, Kannan R, Shukla R, Dale PS, Boote E, Katti K. 2010. Gold nanoparticle mediated detection of prostate cancer cells using photoacoustic flowmetry with optical reflectance. J. Biomed. Nanotechnol 6(2): 187–191.
- Weare WW, Reed SM, Warner MG, Hutchison JE. 2000. Improved synthesis of small (d(CORE) approximate to 1.5 nm) phosphine-stabilized gold nanoparticles. J. Am. Chem. Soc. 122(51): 12890–12891.
- Wilson CG, Sisco PN, Gadala-Maria FA, Murphy CJ, Goldsmith EC. 2009. Polyelectrolyte-coated gold nanorods and their interactions with type I collagen. Biomaterials 30(29): 5639–5648.
- Wong GCL, Lin A, Tang JX, Li Y, Janmey PA, Safinya CR. 2003. Lamellar phase of stacked two-dimensional rafts of actin filaments. Phys. Rev. Lett. 91(1): 018103.
- Yan H, Park SH, Finkelstein G, Reif JH, LaBean TH. 2003. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 301(5641): 1882–1884.