Nano Research

, Volume 3, Issue 11, pp 764–778 | Cite as

Improved non-covalent biofunctionalization of multi-walled carbon nanotubes using carbohydrate amphiphiles with a butterfly-like polyaromatic tail

  • Mohyeddin Assali
  • Manuel Pernía Leal
  • Inmaculada Fernández
  • Pablo Romero-Gomez
  • Rachid Baati
  • Noureddine Khiar
Open Access
Research Article

Abstract

We have developed an efficient strategy for the non-covalent functionalization of multi-walled carbon nanotubes (MWCNTs) which allows a biomimetic presentation of carbohydrates on their surface by π-π stacking interactions. The strategy is based on the use of sugar-based amphiphiles functionalized with tetrabenzo[a,c,g,i]fluorene (Tbf), a polyaromatic compound with a topology that resembles a butterfly with open wings. The new carbohydrate-tethered Tbf amphiphiles have been synthesized in a straightforward manner using click chemistry. The reported method has been developed in order to improve the rather low ability of pyrene-based systems to exfoliate MWCNTs in water. By means of thermogravimetric analysis (TGA), ultraviolet (UV), infrared (IR), and fluorescence spectroscopies the interaction between MWCNTs and the Tbf group has been found to be stronger than those involving pyrene-based amphiphilic carbohydrates. The resulting aggregates with a multivalent sugar exposition on their surface are able to engage in specific ligand-lectin interactions similar to glycoconjugates on a cell membrane.

Keywords

Carbon nanotubes non-covalent functionalization tetrabenzo[a,c,g,i]fluorene carbohydrates click chemistry biocompatible system 

Supplementary material

12274_2010_44_MOESM1_ESM.pdf (777 kb)
Supplementary material, approximately 605 KB.

References

  1. [1]
    Ijima, S. Helical microtubules of graphitic carbon. Nature 1991, 354, 56–58.CrossRefADSGoogle Scholar
  2. [2]
    Tanaka, K.; Yamabe, T.; Fukui, K. The Science and Technology of Carbon Nanotubes; Elsevier: Oxford U.K., 1999.Google Scholar
  3. [3]
    Dresselhaus, M. S.; Dresselhaus, G.; Avouris, P. Carbon Nanotubes: Synthesis, Structure, Properties and Applications; Springer-Verlag: Berlin, 2000.Google Scholar
  4. [4]
    Lu, F.; Gu, L.; Meziani, M. J.; Wang, X.; Luo, P. G.; Veca, L. M.; Cao, L.; Sun, Y. P. Advances in bioapplications of carbon nanotubes. Adv. Mater. 2009, 21, 139–152.CrossRefGoogle Scholar
  5. [5]
    Liu, Z.; Tabakman, S.; Welsher, K.; Dai, H. Carbon nanotubes in biology and medicine: In vitro and in vivo detection, imaging and drug delivery. Nano Res. 2009, 2, 85–120.CrossRefPubMedGoogle Scholar
  6. [6]
    Byon, H. R.; Choi, H. C. Network single-walled carbon nanotube-field effect transistors (SWNT-FETs) with increased schottky contact area for highly sensitive biosensor applications. J. Am. Chem. Soc. 2006, 128, 2188–2189.CrossRefPubMedGoogle Scholar
  7. [7]
    Cherukuri, P.; Bachilo, S. M.; Litovsky. S. H.; Weisman, R. B. Near-infrared fluorescence microscopy of single-walled carbon nanotubes in phagocytic cells. J. Am. Chem. Soc. 2004, 126, 15638–15639.CrossRefPubMedGoogle Scholar
  8. [8]
    Porter, A. E.; Gass, M.; Muller, K.; Skepper, J. N.; Midgley, P. A.; Welland, M. Direct imaging of single-walled carbon nanotubes in cells. Nat. Nanotechnol. 2007, 2, 713–717.CrossRefADSPubMedGoogle Scholar
  9. [9]
    Welsher, K.; Liu, Z.; Daranciang, D.; Dai, H. Selective probing and imaging of cells with single walled carbon nanotubes as near-infrared fluorescent molecules. Nano Lett. 2008, 8, 586–590.CrossRefADSPubMedGoogle Scholar
  10. [10]
    Bianco, A.; Kostarelos, K.; Prato, M. Applications of carbon nanotubes in drug delivery. Curr. Opin. Chem. Biol. 2005, 9, 674–679.CrossRefPubMedGoogle Scholar
  11. [11]
    Bhirde, A. A.; Patel, V.; Gavard, J.; Zhang, G.; Sousa, A. A.; Masedunskas, A.; Leapman, R. D.; Weigert, R.; Gutkind, J. S.; Rusling, J. F. Targeted killing of cancer cells in vivo and in vitro with EGF-directed carbon nanotube-based drug delivery. ACS Nano 2009, 3, 307–316.CrossRefPubMedGoogle Scholar
  12. [12]
    Kam, N. W. S.; Dai, H. Carbon nanotubes as intracellular protein transporters generality and biological functionality. J. Am. Chem. Soc. 2005, 127, 6021–6026.CrossRefPubMedGoogle Scholar
  13. [13]
    Pantarotto, D.; Briand, J. P.; Prato, M.; Bianco, A. Translocation of bioactive peptides across cell membranes by carbon nanotubes. Chem. Commun. 2004, 16–17.Google Scholar
  14. [14]
    Liu, Y.; Wu, D. C.; Zhang, W. D.; Jiang, X.; He, C. B.; Chung, T. S.; Goh, S. H.; Leong, K. W. Polyethylenimine-grafted multiwalled carbon nanotubes for secure noncovalent immobilization and efficient delivery of DNA. Angew. Chem. Int. Ed. 2005, 44, 4782–4785.CrossRefGoogle Scholar
  15. [15]
    Liu, Z.; Winters, M.; Holodniy, M.; Dai, H. siRNA delivery into human T cells and primary cells with carbon nanotube transporters. Angew. Chem. Int. Ed. 2007, 46, 2023–2027.CrossRefGoogle Scholar
  16. [16]
    Yang, R.; Yang, X.; Zhang, Z.; Zhang, Y.; Wang, S.; Cai, Z.; Jia, Y.; Ma, Y.; Zheng, C.; Lu, Y.; Roden, R.; Chen, Y. Single walled carbon nanotubes-mediated in vivo and in vitro delivery of siRNA into antigen-presenting cells. Gene Ther. 2006, 13, 1714–1723.CrossRefPubMedGoogle Scholar
  17. [17]
    Kam, N. W. S.; O’Connell, M.; Wisdom, J. A.; Dai, H. Carbon nanotubes as multifunctional biological transporters and near-infrared agents for selective cancer cell destruction. Proc. Natl. Acad. Sc. USA. 2005, 102, 11600–11605.CrossRefADSGoogle Scholar
  18. [18]
    Chakravarty, P.; Marches, R.; Zimmerman, N. S.; Swafford, A. D. E.; Bajaj, P.; Musselman, I. H.; Pantano, P.; Draper, R. K.; Vitetta. E. S. Thermal ablation of tumor cells with antibody-functionalized single-walled carbon nanotubes. Proc. Nat. Acad. Sci. USA 2008, 105, 8697–8702.CrossRefADSPubMedGoogle Scholar
  19. [19]
    Gannon, C. J.; Cherukuri, P.; Yakobson, B. I.; Cognet, L.; Kanzius, J. S.; Kittrell, C.; Weisman, R. B.; Pasquali, M.; Schmidt, H. K.; Smalley, R. E.; Curley, S. A. Carbon nanotube-enhanced thermal destruction of cancer cells in a noninvasive radiofrequency field. Cancer 2007, 110, 2654–2665.CrossRefPubMedGoogle Scholar
  20. [20]
    Singh, R.; Pantarotto, D.; Lacerda, L.; Pastorin, G.; Klumpp, C.; Prato, M.; Bianco, A.; Kostarelos, K. Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. Proc. Natl. Acad. Sci. USA 2006, 103, 3357–3362.CrossRefADSPubMedGoogle Scholar
  21. [21]
    Liu, Z.; Davis, C.; Cai, W.; He, L.; Chen, X.; Dai, H. Circulation and long-term fate of functionalized, biocompatible single-walled carbon nanotubes in mice probed by Raman spectroscopy. Proc. Natl. Acad. Sci. USA 2008, 105, 1410–1415.CrossRefADSPubMedGoogle Scholar
  22. [22]
    Schipper, M. L.; Nakayama-Ratchford, N.; Davis, C. R.; Kam, N. W. S.; Chu, P.; Liu, Z.; Sun, X.; Dai, H.; Gambhir, S. S. A pilot toxicology study of single-walled carbon nanotubes in a small sample of mice. Nature Nanotech. 2008, 3, 216–221.CrossRefGoogle Scholar
  23. [23]
    Sudibya, H. G.; Ma, J.; Dong, X.; Ng, S.; Li, L. J.; Liu, X. W.; Chen, P. Interfacing glycosylated carbon-nanotube-network devices with living cells to detect dynamic secretion of biomolecules. Angew. Chem. Int. Ed. 2009, 48, 2723–2726.CrossRefGoogle Scholar
  24. [24]
    Tasis, D.; Tagmatarchis, N.; Bianco, A.; Prato, M. Chemistry of carbon nanotubes. Chem. Rev. 2006, 106, 1105–1136.CrossRefPubMedGoogle Scholar
  25. [25]
    Britz, D. A.; Khlobystov, A. N. Noncovalent interactions of molecules with single walled carbon nanotubes. Chem. Soc. Rev. 2006, 35, 637–659.CrossRefPubMedGoogle Scholar
  26. [26]
    Hahn, U.; Engmann, S.; Oelsner, C.; Ehli, C.; Guldi, D. M.; Torres, T. Immobilizing water-soluble dendritic electron donors and electron acceptors-phtalocyanines and perylendiimide-onto single Wall carbon nanotubes. J. Am. Chem. Soc. 2010, 132, 6392–6401.CrossRefPubMedGoogle Scholar
  27. [27]
    Chen, R. J.; Zhang, Y.; Wang, D.; Dai, H. Noncovalent sidwall functionalization of single-walled carbon nanotubes for protein immobilization. J. Am. Chem. Soc. 2001, 123, 3838–3839.CrossRefPubMedGoogle Scholar
  28. [28]
    Nakashima, N.; Tomonari, Y.; Murakami, H. Water-soluble single-walled carbon nanotubes via non-covalent sidewall-functionalization with a pyrene-carrying ammonium ion. Chem. Lett. 2002, 638–639.Google Scholar
  29. [29]
    Georgakilas, V.; Tzitzios, V.; Gournis, D.; Petridis, D. Attachement of magnetic nanoparticles on carbon nanotubes and their soluble derivatives. Chem Mater. 2005, 17, 1613–1617.CrossRefGoogle Scholar
  30. [30]
    Liu, Z.; Sun, X.; Nakayama-Ratchford, N.; Dai, H. Supramolecular chemistry on water-soluble carbon nanotubes for drug loading and delivery. ACS Nano 2007, 1, 50–56.CrossRefPubMedGoogle Scholar
  31. [31]
    Richard, C.; Balavoine, F.; Schultz, P.; Moreau, N.; Mioskowski, C. Immobilization of histidine-tagged proteins on functionalized carbon nanotubes. J. Bionanosci. 2007, 1, 106–113.CrossRefGoogle Scholar
  32. [32]
    Ali-Boucetta, H.; Al-Jamal, K. T.; McCarthy, D.; Prato, M.; Bianco, A.; Kostarelos, K. Multiwalled carbon nanotube-doxorubicin supramolecular complexes for cancer therapeutics. Chem Commun. 2008, 459–461.Google Scholar
  33. [33]
    Liu, Z.; Fan, A. C.; Rakhra, K.; Sherlock, S.; Goodwin, A.; Chen, X.; Yang, Q.; Felsher, D. W.; Dai, H. Supramolecular stacking of doxorubicin on carbon nanotubes for in vivo cancer therapy. Angew. Chem. Int. Ed. 2009, 48, 7668–7672.CrossRefGoogle Scholar
  34. [34]
    Simmons, T. J.; Bult, J.; Hashim, D. P.; Linhardt, R. J.; Ajayan, P. M. Noncovalent functionalization as an alternative to oxidative acid treatment of single wall carbon nanotubes with applications for polymer composites. ACS Nano 2009, 3, 865–870.CrossRefPubMedGoogle Scholar
  35. [35]
    Peigney, A.; Laurent, C.; Flahaut, E.; Bacsa, R. R.; Rousset, A. Specific surface area of carbon nanotubes and bundles of carbon nanotubes. Carbon 2001, 39, 507–514.CrossRefGoogle Scholar
  36. [36]
    Astronomo, R. A.; Burton, D. R. Carbohydrate vaccines: Developing sweet solutions to sticky situations? Nature Rev. Drug Discover. 2010, 9, 308–324.CrossRefGoogle Scholar
  37. [37]
    Dube, D. H.; Bertozzi, C. R; Glycans in cancer and inflammation—potential for therapeutics and diagnostics. Nature Rev. Drug Discover. 2005, 4, 477–488.CrossRefGoogle Scholar
  38. [38]
    Seeberger, P. H.; Werz, D. B. Synthesis and medical applications of oligosaccharides. Nautre 2007, 446, 1046–1051.Google Scholar
  39. [39]
    Lundquist, J. J.; Toone, E. J. The cluster glycoside effect. Chem. Rev. 2002, 102, 555–578.CrossRefPubMedGoogle Scholar
  40. [40]
    Mammen, M.; Choi, S. K.; Whitesides, G. M. Polyvalent interactions in biological systems: Implications for design and use of multivalent ligands and inhibitors Angew. Chem. Int. Ed. 1998, 37, 2754–2794.CrossRefGoogle Scholar
  41. [41]
    Chen, X.; Tam, U. C.; Czlapinski, J. L.; Lee, G. S.; Rabuka, D.; Zettl, A.; Bertozzi, C. R. Interfacing carbon nanotubes with living cells. J. Am. Chem. Soc. 2006, 128, 6292–6293.CrossRefPubMedGoogle Scholar
  42. [42]
    Wang, H.; Gu, L.; Lin, Y.; Lu, F.; Meziani, M. J.; Luo, P. G.; Wang, W.; Cao, L.; Sun, Y. P. Unique aggregation of anthrax (bacillus anthracis) spores by sugar-coated single-walled carbon nanotubes. J. Am. Chem. Soc. 2006, 128, 13364–13365.CrossRefPubMedGoogle Scholar
  43. [43]
    Khiar, N.; Pernia Leal, M.; Baati, R.; Ruhlmann, C.; Mioskowski, C.; Schultz, P.; Fernandez, I. Tailoring carbon nanotube surfaces with glyconanorings: New bionanomaterials with specific lectin affinity. Chem. Commun. 2009, 27, 4121–4123.CrossRefGoogle Scholar
  44. [44]
    Assali, M.; Pernia Leal, M.; Fernandez, I.; Baati, R.; Mioskowski, C.; Khiar, N. Non-covalent functionalization of carbon nanotubes with glycolipids: Glyconanomaterials with specific lectin-affinity. Soft Matter 2009, 5, 948–950.CrossRefGoogle Scholar
  45. [45]
    Andersson, C. H.; Lahmann, M.; Oscarson, S.; Grennberg, H. Reversible non-covalent derivatisation of carbon nanotubes with glycosides. Soft Matter 2009, 5, 2713–2716.CrossRefGoogle Scholar
  46. [46]
    Zhang, J.; Lee, J. K.; Wu, Y.; Murray, R. W. Photoluminescence and electronic interaction of anthracene derivatives adsorbed on sidewalls of single-walled carbon nanotubes. Nano Lett. 2003, 3, 403–407.CrossRefADSGoogle Scholar
  47. [47]
    Paloniemi, H.; Ääritalo, T.; Laiho, T.; Liuke, H.; Kocharova, N.; Haapkka, K.; Terzi, F.; Seeber, R.; Lukkari, J. Water-soluble full-lenght single-wall carbon nanotube polyelectrolytes: Preparation and characterization. J. Phys. Chem. B. 2005, 109, 8634–8642.CrossRefPubMedGoogle Scholar
  48. [48]
    Kar, T.; Bettinger, H. F.; Scheiner, S.; Roy, A. K. Noncovalent π-π stacking and CH—π interactions of aromatics on the surface of single-wall carbon nanotubes: An MP2 study. J. Phys. Chem. C. 2008, 112, 20070–20075.CrossRefGoogle Scholar
  49. [49]
    Brown, A. P.; Anson, F. C. Molecular anchors for the attachment of metal complexes to graphite electrode surfaces. J. Electroanal. Chem. 1977, 83, 203–206.Google Scholar
  50. [50]
    Pérez, E. M.; Martin, N. Curves ahead: Molecular receptors for fullerenes based on concave-convex complementarity. Chem. Soc. Rev. 2008, 37, 1512–1519.CrossRefPubMedGoogle Scholar
  51. [51]
    Brown, A. R.; Irving, S. L.; Ramage, R. Affinity purification of synthetic peptides and proteins on porous graphitised carbon. Tetrahedron Letters. 1993, 34, 7129–7132.CrossRefGoogle Scholar
  52. [52]
    Brown, A. R.; Irving, S. L.; Ramage, R.; Raphy, G. (17-Tetrabenzo [a,c,g,i] fluorenyl) methyl chloroformate (TbfmocCl) a reagent for the rapid and efficient purification of synthetic peptides and proteins. Tetrahedron 1995, 51, 11815–11830.CrossRefGoogle Scholar
  53. [53]
    Ramage, R.; Wahl, F. O. 4-(17-Tetrabenzo [a,c,g,i] fluorenyl-methyl)-4’, 4“-dimethoxytrityl chloride: A hydrophobic 5’-protecting group for the separation of synthetic oligonucleotides. Tetrahedron Letters 1993, 34, 7133–7136.CrossRefGoogle Scholar
  54. [54]
    Kolb, H. C.; Finn, M. G.; Sharpless, K. B. Click chemistry: Diverse chemical function from a few good reactions. Angew. Chem. Int. Ed. 2001, 40, 2004–2021.CrossRefGoogle Scholar
  55. [55]
    Tornøe, C. W.; Christensen, C.; Meldal, M. Peptidotriazoles on solid phase: [1,2,3]-Triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 2002, 67, 3057–3064.CrossRefPubMedGoogle Scholar
  56. [56]
    Hay, A. M.; Hobbs-Dewitt, S.; MacDonald, A. A.; Ramage, R. Use of tetrabenzo [a,c,g,i] fluorene as an anchor group for the solid/solution phase synthesis of the quinolone antibacterial, ciprofloxacin. Synthesis 1999, 11, 1979–1985.CrossRefGoogle Scholar
  57. [57]
    Yang, Z.; Chen, X.; Chen, C.; Li, W.; Zhang, H.; Xu, L.; Yi, B. Noncovalent-wrapped sidewall functionalization of multiwalled carbon nanotubes with polyimide. Polymer Composites, 2007, 28, 36–41.CrossRefGoogle Scholar
  58. [58]
    Brown, S. D. M.; Jorio, A.; Dresselhaus, M. S.; Dresselhaus, G. Observations of the D-band feature in the raman spectra of carbon nanotubes. Phys. Rev. B. 2001, 64, 073403.CrossRefADSGoogle Scholar
  59. [59]
    Yang, Q.; Shuai, Li.; Zhou, J.; Lu, F.; Pan, X. Functionalization of multiwalled carbon nanotubes by pyrene-labeled hydroxypropyl cellulose. J. Phys. Chem. B 2008, 112, 12934–12939.CrossRefPubMedGoogle Scholar
  60. [60]
    D’souza, F.; Ito, O. Supramolecular donor-acceptor hybrids of porphyrins/phthalocyanines with fullerenes/carbon nanotubes: Electron transfer, sensing, switching, and catalytic applications. Chem. Commun. 2009, 4913–4928.Google Scholar
  61. [61]
    Banerjee, R.; Das, K.; Ravishankar, R.; Suguna, K.; Surolia, A.; Vijayan, A. M. Conformation, protein-carbohydrate interactions and a novel subunit association in the refined structure of peanut lectin-lactose complex. J. Mol. Biol. 1996, 259, 281–296.CrossRefPubMedGoogle Scholar
  62. [62]
    Balavoine, F.; Schultz, P.; Richard, C.; Mallouh, M.; Ebbesen, T. W.; Mioskowski, C. Helical crystallization of proteins on carbon nanotubes: A first step towards the development of new biosensors. Angew. Chem. Int. Ed. 1999, 38, 1912–1915.CrossRefGoogle Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Mohyeddin Assali
    • 1
  • Manuel Pernía Leal
  • Inmaculada Fernández
    • 2
  • Pablo Romero-Gomez
    • 3
  • Rachid Baati
    • 4
  • Noureddine Khiar
    • 1
  1. 1.Instituto de Investigaciones QuímicasC.S.I.C-Universidad de SevillaSevillaSpain
  2. 2.Departamento de Química Orgánica y Farmacéutica, Facultad de FarmaciaUniversidad de SevillaSevillaSpain
  3. 3.Instituto de Ciencias de Materiales de SevillaC.S.I.C-Universidad de SevillaSevillaSpain
  4. 4.Laboratoire des Systèmes Chimiques Fonctionnels BP 60024Université de Strasbourg Faculté de Pharmacie CNRS/UMR 7199IllkirchFrance

Personalised recommendations