Functionalized carbon nanotubes as emerging nanovectors for the delivery of therapeutics

Biochimica et Biophysica Acta - Biomembranes

Volumn 1758, Issue 3, 2006, Pages 404-412

  Klumpp, Cédric ^a,b   Kostarelos, Kostas ^c   Prato, Maurizio ^b   Bianco, Alberto ^a  

^a INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITY OF TRIESTE   (Italy)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Carbon nanotube; Drug delivery; Gene; Peptide; Vaccine; Vector

Indexed keywords

ADENOVIRUS VECTOR; AMPHOTERICIN B; ANTIBIOTIC AGENT; BIOPOLYMER; CARBON NANOTUBE; DRUG CARRIER; FOLIC ACID; LENTIVIRUS VECTOR; LIPOFECTAMINE; MACROGOL; NUCLEIC ACID; OLIGODEOXYNUCLEOTIDE; PHOSPHOLIPID; PLASMID DNA; POLY(METAPHENYLENEVINYLENE); POLYETHYLENEIMINE; POLYMER; POLYOXYETHYLENE; POVIDONE; PROTEIN VP1; RETROVIRUS VECTOR; SINGLE STRANDED DNA; SURFACTANT; UNCLASSIFIED DRUG; VACCINE; VIRUS VECTOR;

COVALENT BOND; CPG ISLAND; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; GENE DELIVERY SYSTEM; HUMAN; MOLECULAR INTERACTION; MOLECULAR STABILITY; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SUPRAMOLECULAR CHEMISTRY;

DNA; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; NANOTUBES, CARBON; RNA;

EID: 33646534455     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2005.10.008     Document Type: Review

References (84)

1. Baughman R.H., Zakhidov A.A., and De Heer W.A. Carbon nanotubes-The route toward applications. Science 297 (2002) 787-792
2. Special issue on carbon nanotubes. Acc. Chem. Res. 35 (2002) 997-1113
3. Balavoine F., Richard C., Mioskowski C., Schultz P., Mallouh V., and Ebbesen T.W. Helical crystallization of proteins on carbon nanotubes: a first step towards the development of new biosensors. Angew. Chem., Int. Ed. 38 (1999) 1912-1915
4. Bekyarova E., Ni Y., Malarkey E.B., Montana V., McWilliams J.L., Haddon R.C., and Parpura V. Applications of carbon nanotubes in biotechnology and biomedicine. J. Biomed. Nanotechnol. 1 (2005) 3-17
5. Lin Y., Taylor S., Li H., Fernando K.A.S., Qu L., Wang W., Gu L., Zhou B., and Sun Y.-P. Advances toward bioapplications of carbon nanotubes. J. Mater. Chem. 14 (2004) 527-541
6. Richard C., Balavoine F., Mioskowski C., Schultz P., and Ebbesen T.W. Supramolecutar self-assembly of lipid derivatives on carbon nanotubes. Science 300 (2003) 775-778
7. Wang J., Musameh M., and Lin Y. Solubilization of carbon nanotubes by nafion toward the preparation of amperometric biosensors. J. Am. Chem. Soc. 125 (2003) 2408-2409
8. Wang S., Delduco D.F., Lustig S.R., Wang H., Parker K.N., Rizzo N.W., Subramoney S., Jagota A., Humphreys E.S., Chung S.-Y., and Chiang Y.-M. Peptides with selective affinity for carbon nanotubes. Nat. Mater. 2 (2003) 196-200
9. Lovat V., Pantarotto D., Lagostena L., Spalluto G., Prato M., Ballerini L., Cacciari B., Grandolfo M., and Righi M. Carbon nanotube substrates boost neuronal electrical signaling. Nano Lett. 5 (2005) 1107-1110
10. Hu H., Haddon R.C., Ni Y., Montana V., and Parpura V. Chemically functionalized carbon nanotubes as substrates for neuronal growth. Nano Lett. 4 (2004) 507-511
11. Mattson M.P., Haddon R.C., and Rao A.M. Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J. Mol. Neurosci. 14 (2000) 175-182
12. Chen X., Lee G.S., Zettl A., and Bertozzi C.R. Biomimetic engineering of carbon nanotubes by using cell surface mucin mimics. Angew. Chem., Int. Ed. 43 (2004) 6112-6116
13. Park K.H., Chhowalla M., Iqbal Z., and Sesti F. Single-walled carbon nanotubes are a new class of ion channel blockers. J. Biol. Chem. 278 (2003) 50212-50216
14. Bianco A., Kostarelos K., Partidos C.D., and Prato M. Biomedical applications of functionalised carbon nanotubes. Chem. Commun. (2005) 571-577
15. Bianco A., and Prato M. Can carbon nanotubes be considered useful tools for biological applications?. Adv. Mater. 15 (2003) 1765-1768
16. Bacon R. Growth, structure, and properties of graphite whiskers. J. Appl. Phys. 31 (1960) 284
17. Iijima S. Helical microtubules of graphitic carbon. Nature 354 (1991) 56-58
18. Popov V.N. Carbon nanotubes: properties and application. Mater. Sci. Eng. R43 (2004) 61-102
19. Baddour C.E., and Briens C. Carbon nanotube synthesis: a review. Int. J. Chem. React. Eng. 3 (2005) R3
20. Nikolaev P., Bronikowski M.J., Bradley R.K., Rohmund F., Colbert D.T., Smith K.A., and Smalley R.E. Gas-phase catalytic growth of single-walled carbon nanotubes from carbon monoxide. Chem. Phys. Lett. 313 (1999) 91-97
21. Arnold M.S., Stupp S.I., and Hersam M.C. Enrichment of single-walled carbon nanotubes by diameter in density gradients. Nano Lett. 5 (2005) 713-718
22. Dyke C.A., Stewart M.P., and Tour J.M. Separation of single-walled carbon nanotubes on silica gel. Materials morphology and raman excitation wavelength affect data interpretation. J. Am. Chem. Soc. 127 (2005) 4497-4509
23. Georgakilas V., Voulgaris D., Vázquez E., Prato M., Guldi D.M., Kukovecz A., and Kuzmany H. Purification of hipco carbon nanotubes via organic functionalization. J. Am. Chem. Soc. 124 (2002) 14318-14319
24. Zhao B., Hu H., Niyogi S., Itkis M.E., Hamon M.A., Bhowmik P., Meier M.S., and Haddon R.C. Chromatographic purification and properties of soluble single-walled carbon nanotubes. J. Am. Chem. Soc. 123 (2001) 11673-11677
25. Niyogi S., Hu H., Hamon M.A., Bhowmik P., Zhao B., Rozenzhak S.M., Chen J., Itkis M.E., Meier M.S., and Haddon R.C. Chromatographic purification of soluble single-walled carbon nanotubes (s-SWNTs). J. Am. Chem. Soc. 123 (2001) 733-734
26. Tang B.Z., and Xu H. Preparation, alignment, and optical properties of soluble poly(phenylacetylene)-wrapped carbon nanotubes. Macromolecules 32 (1999) 2569-2576
27. Islam M.F., Rojas E., Bergey D.M., Johnson A.T., and Yodh A.G. High weight fraction surfactant solubilization of single-wall carbon nanotubes in water. Nano Lett. 3 (2003) 269-273
28. Moore V.C., Strano M.S., Haroz E.H., Hauge R.H., Smalley R.E., Schmidt J., and Talmon Y. Individually suspended single-walled carbon nanotubes in various surfactants. Nano Lett. 3 (2003) 1379-1382
29. Petrov P., Stassin F., Pagnoulle C., and Jérôme R. Noncovalent functionalization of multi-walled carbon nanotubes by pyrene containing polymers. Chem. Commun. 9 (2003) 2904-2905
30. Shvartzman-Cohen R., Nativ-Roth E., Yerushalmi-Rozen R., Baskaran E., Szleifer I., and Levi-Kalisman Y. Selective dispersion of single-walled carbon nanotubes in the presence of polymers: the role of molecular and colloidal length scales. J. Am. Chem. Soc. 126 (2004) 14850-14857
31. Sinani V.A., Kotov N.A., Yaroslavov A.A., Rakhnyanskaya A.A., Gheith M.K., Wicksted J.P., Sun K., and Mamedov A.A. Aqueous dispersions of single-wall and multiwall carbon nanotubes with designed amphiphilic polycations. J. Am. Chem. Soc. 127 (2005) 3463-3472
32. Nakashima N., Okuzono S., Murakami H., Nakai T., and Yoshikawa K. DNA dissolves single-walled carbon nanotubes in water. Chem. Lett. 32 (2003) 456-457
33. Zheng M., Jagota A., Semke E.D., Diner B.A., McLean R.S., Lustig S.R., Richardson R.E., and Tassi N.G. DNA-assisted dispersion and separation of carbon nanotubes. Nat. Mater. 2 (2003) 338-342
34. Tagmatarchis N., and Prato M. Functionalization of carbon nanotubes via 1,3-dipolar cycloadditions. J. Mater. Chem. 14 (2004) 437-439
35. Hirsch A. Functionalization of single-walled carbon nanotubes. Angew. Chem., Int. Ed. 41 (2002) 1853-1859
36. Dyke C.A., and Tour J.M. Overcoming the insolubility of carbon nanotubes through high degrees of sidewall functionalization. Chem. Eur. J. 10 (2004) 812-817
37. Stevens J.L., Huang A.Y., Peng H., Chiang I.W., Khabashesku V.N., and Margrave J.L. Sidewall amino-functionalization of single-walled carbon nanotubes through fluorination and subsequent reactions with terminal diamines. Nano Lett. 3 (2003) 331-336
38. Hudson J.L., Casavant M.J., and Tour J.M. Water-soluble, exfoliated, nonroping single-wall carbon nanotubes. J. Am. Chem. Soc. 126 (2004) 11158-11159
39. Chen R.J., Zhang Y., Wang D., and Dai H. Noncovalent sidewall functionalization of single-walled carbon nanotubes for protein immobilization. J. Am. Chem. Soc. 123 (2001) 3838-3839
40. Minko T. Soluble polymer conjugates for drug delivery. Curr. Drug Discov. Technol. 2 (2005) 15-20
41. Star A., Stoddart J.F., Steuerman D., Diehl M., Boukai A., Wong E.W., Yang X., Chung S.-W., Choi H., and Heath J.R. Preparation and properties of polymer- wrapped single-walled carbon nanotubes. Angew. Chem., Int. Ed. 40 (2001) 1721-1725
42. Didenko V.V., Moore V.C., Baskin D.S., and Smalley R.E. Visualization of individual single-walled carbon nanotubes by fluorescent polymer wrapping. Nano Lett. 5 (2005) 1563-1567
43. Zheng M., Jagota A., Diner B.A., McLean R.S., Onoa G.B., Semke E.D., Watts D.J., Strano M.S., Barone P., Usrey M., Santos A.P., Chou S.G., Dresselhaus M.S., and Samsonidze G.G. Structure-based carbon nanotube sorting by sequence-dependent DNA assembly. Science 302 (2003) 1545-1548
44. Dieckmann G.R., Razal J., Giordano G.M., Musselman I.H., Baughman R.H., Dalton A.B., Muñoz E., Johnson P.A., Draper R.K., and Chen J. Controlled assembly of carbon nanotubes by designed amphiphilic peptide helices. J. Am. Chem. Soc. 125 (2003) 1770-1777
45. Zorbas V., Ortiz-Acevedo A., Dieckmann G.R., Draper R.K., Baughman R.H., Musselman I.H., Dalton A.B., Yoshida M.M., and Jose-Yacaman M. Preparation and characterization of individual peptide-wrapped single-walled carbon nanotubes. J. Am. Chem. Soc. 126 (2004) 7222-7227
46. Dalton A.B., Razal J.M., Baughman R.H., Draper R.K., Musselman I.H., Dieckmann G.R., Ortiz-Acevedo A., Zorbas V., Brunner E., Sampson W.M., Collins S., Yoshida M.M., and Jose-Yacaman M. Hierarchical self-assembly of peptide-coated carbon nanotubes. Adv. Funct. Mater. 14 (2004) 1147-1151
47. Ortiz-Acevedo A., Xie H., Zorbas V., Sampson W.M., Dalton A.B., Baughman R.H., Draper R.K., Musselman I.H., and Dieckmann G.R. Diameter-selective solubilization of single-walled carbon nanotubes by reversible cyclic peptides. J. Am. Chem. Soc. 127 (2005) 9512-9517
48. Balasubramanian K., and Burghard M. Chemically functionalized carbon nanotubes. Small 1 (2005) 180-192
49. Ziegler K.J., Gu Z., Peng H., Flor E.L., Hauge R.H., and Smalley R.E. Controlled oxidative cutting of single-walled carbon nanotubes. J. Am. Chem. Soc. 127 (2005) 1541-1547
50. Chen J., Rao A.M., Lyuksyutov S., Itkis M.E., Hamon M.A., Hu H., Cohn R.W., Eklund P.C., Colbert D.T., Smalley R.E., and Haddon R.C. Dissolution of full-length single-walled carbon nanotubes. J. Phys. Chem., B 105 (2001) 2525-2528
51. Lin Y., Rao A.M., Sadanadan B., Kenik E.A., and Sun Y.-P. Functionalizing multiple-walled carbon nanotubes with aminopolymers. J. Phys. Chem., B 106 (2002) 1294-1298
52. Heald C.G.R., Wildgoose G.G., Compton R.G., Jiang L., and Jones T.G.J. Chemical derivatisation of multiwalled carbon nanotubes using diazonium salts. Chem. Phys. Chem. 5 (2004) 1794-1799
53. Liang F., Sadana A.K., Peera A., Chattopadhyay J., Gu Z., Hauge R.H., and Billups W.E. A convenient route to functionalized carbon nanotubes. Nano Lett. 4 (2004) 1257-1260
54. Lee K.M., Li L., and Dai L. Asymmetric end-functionalization of multi-walled carbon nanotubes. J. Am. Chem. Soc. 127 (2005) 4122-4123
55. Allen T.M., and Cullis P.R. Drug delivery systems: entering the mainstream. Science 303 (2004) 1818-1822
56. Pouton C.W., and Seymour L.W. Key issues in non-viral gene delivery. Adv. Drug. Deliv. Rev. 46 (2000) 187-203
57. Pantarotto D., Briand J.-P., Prato M., and Bianco A. Translocation of bioactive peptides across cell membranes by carbon nanotubes. Chem. Commun. (2004) 16-17
58. Kam N.W.S., Jessop T.C., Wender P.A., and Dai H. Nanotube molecular transporters: internalization of carbon nanotube-protein conjugates into mammalian cells. J. Am. Chem. Soc. 126 (2004) 6850-6851
59. Pantarotto D., Singh R., McCarthy D., Erhardt M., Briand J.-P., Prato M., Kostarelos K., and Bianco A. Functionalized carbon nanotubes for plasmid DNA gene delivery. Angew. Chem., Int. Ed. 43 (2004) 5242-5246
60. Cai D., Huang Z., Carnahan D., Mataraza J.M., Chiles T.C., Qin Z.-H., Huang J., Kempa K., and Ren Z. Highly efficient molecular delivery into mammalian cells using carbon nanotube spearing. Nat. Methods 2 (2005) 449-454
61. Kam N.W.S., and Dai H. Carbon nanotubes as intracellular protein transporters: generality and biological functionality. J. Am. Chem. Soc. 127 (2005) 6021-6026
62. Wu W., Wieckowski S., Pastorin G., Benincasa M., Klumpp C., Briand J.-P., Gennaro R., Prato M., and Bianco A. Targeted delivery of amphotericin B to cells by using functionalized carbon nanotubes. Angew. Chem., Int. Ed. 44 (2005) 6358-6362
63. Yinghuai Z., Peng A.T., Carpenter K., Maguire J.A., Hosmane N.S., and Takagaki M. Substituted carborane-appended water-soluble single-wall carbon nanotubes: new approach to boron neutron capture therapy drug delivery. J. Am. Chem. Soc. 127 (2005) 9875-9880
64. Kam N.W.S., O'Connell M., Wisdom J.A., and Dai H. Carbon nanotubes as multifunctional biological transporters and near-infrared agents for selective cancer cell destruction. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11600-11605
65. Pantarotto D., Partidos C.D., Graff R., Hoebeke J., Briand J.-P., Prato M., and Bianco A. Synthesis, structural characterization, and immunological properties of carbon nanotubes functionalized with peptides. J. Am. Chem. Soc. 125 (2003) 6160-6164
66. Pantarotto D., Partidos C.D., Hoebeke J., Brown F., Kramer E., Briand J.-P., Muller S., Prato M., and Bianco A. Immunization with peptide-functionalized carbon nanotubes enhances virus-specific neutralizing antibody responses. Chem. Biol. 10 (2003) 961-966
67. Carter P.J., and Samulski R.J. Adeno-associated viral vectors as gene delivery vehicles. Int. J. Mol. Med. 6 (2000) 17-27
68. Singh R., Pantarotto D., McCarthy D., Chaloin O., Hoebeke J., Partidos C.D., Briand J.-P., Prato M., Bianco A., and Kostarelos K. Binding and condensation of plasmid DNA onto functionalized carbon nanotubes: toward the construction of nanotube-based gene delivery vectors. J. Am. Chem. Soc. 127 (2005) 4388-4396
69. Liu Y., Wu D.-C., Zhang W.-D., He C.-B., Goh S.H., Jiang X., Chung T.S., and Leong K.W. Polyethylenimine-grafted multiwalled carbon nanotubes for secure noncovalent immobilization and efficient delivery of DNA. Angew. Chem., Int. Ed. 44 (2005) 4782-4785
70. Bianco A., Hoebeke J., Godefroy S., Chaloin O., Pantarotto D., Briand J.-P., Muller S., Prato M., and Partidos C.D. Cationic carbon nanotubes bind to cpg oligodeoxynucleotides and enhance their immunostimulatory properties. J. Am. Chem. Soc. 127 (2005) 58-59
71. Lu Q., Moore J.M., Rao A.M., Larcom L.L., Ke P.C., Huang G., and Mount A.S. RNA polymer translocation with single-walled carbon nanotubes. Nano Lett. 4 (2004) 2473-2477
72. Kam N.W.S., Liu Z., and Dai H. Functionalization of carbon nanotubes via cleavable disulfide bonds for efficient intracellular delivery of sirna and potent gene silencing. J. Am. Chem. Soc. 127 (2005) 12492-12493
73. Cui D., Tian F., Wang M., Gao H., and Ozkan C.S. Effect of single wall carbon nanotubes on human HEK293 cells. Toxicol. Lett. 155 (2005) 73-85
74. Bottini M., Bruckner S., Nika K., Bottini N., Bellucci S., Magrini A., Bergamaschi A., and Mustelin T. Multi-walled carbon nanotubes induce T lymphocyte apoptosis. Toxicol. Lett. 160 (2006) 121-126
75. Sato Y., Yokoyama A., Shibata K., Akimoto Y., Ogino S., Nodasaka Y., Kohgo T., Tamura K., Akasaka T., Uo M., Motomiya K., Jeyadevan B., Ishiguro M., Hatakeyama R., Watarib F., and Tohji K. Influence of length on cytotoxicity of multi-walled carbon nanotubes against human acute monocytic leukemia cell THP-1 in vitro and subcutaneous tissue of rats in vivo. Mol. BioSyst. 1 (2005) 176-183
76. Jia G., Wang H., Yan L., Wang X., Pei R., Yan T., Zhao Y., and Guo X. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ. Sci. Technol. 39 (2005) 1378-1383
77. Manna S.K., Sarkar S., Barr J., Wise K., Barrera E.V., Jejelowo O., Rice-Ficht A.C., and Ramesh G.T. Single-walled carbon nanotube induces oxidative stress and activates nuclear transcription factor-κB in human keratinocytes. Nano Lett. 5 (2005) 1676-1684
78. Monteiro-Riviere N.A., Nemanich R.J., Inman A.O., Wang Y.Y., and Riviere J.E. Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicol. Lett. 155 (2005) 377-384
79. Shvedova A.A., Castranova V., Kisin E.R., Schwegler-Berry D., Murray A.R., Gandelsman V.Z., Maynard A., and Baron P. Exposure to carbon nanotube material: assessment of nanotube cytotoxicity using human keratinocyte cells. J. Toxicol. Environ. Health, Part A 66 (2003) 1909-1926
80. Salvador-Morales C., Flahaut E., Sim E., Sloan J., Green M.L.H., and Sim R.B. Complement activation and protein adsorption by carbon nanotubes. Mol. Immunol. 43 (2006) 193-201
81. Sayes C.M., Fortner J.D., Guo W., Lyon D., Boyd A.M., Ausman K.D., Tao Y.J., Sitharaman B., Wilson L.J., Hughes J.B., West J.L., and Colvin V.L. The differential cytotoxicity of water-soluble fullerenes. Nano Lett. 4 (2004) 1881-1887
82. Lam C.-W., James J.T., McCluskey R., and Hunter R.L. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intractracheal instillation. Toxicol. Sci. 77 (2004) 126-134
83. Warheit D.B., Laurence B.R., Reed K.L., Roach D.H., Reynolds G.A.M., and Webb T.R. Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats. Toxicol. Sci. 77 (2004) 117-125
84. Wang H., Wang J., Deng X., Sun H., Shi Z., Gu Z., Liu Y., and Zhao Y. Biodistribution of carbon single-wall carbon nanotubes in mice. J. Nanosci. Nanotech. 4 (2004) 1019-1024