Structural profiling and biological performance of phospholipid-hyaluronan functionalized single-walled carbon nanotubes

Journal of Controlled Release

Volumn 170, Issue 2, 2013, Pages 295-305

  Dvash, Ram ^a   Khatchatouriants, Artium ^a   Solmesky, Leonardo J ^b   Wibroe, Peter P ^c   Weil, Miguel ^b   Moghimi, S Moein ^c   Peer, Dan ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b Tel Aviv University ^*  (Israel)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Carbon nanotubes; Cytotoxicity; High content analysis; Hyaluronan; Immune response

Indexed keywords

BIOCOMPATIBILITY; CARBON; CARBON NANOTUBES; CYTOTOXICITY; HYALURONIC ACID; IMMUNE SYSTEM; MACROPHAGES; MEDICAL NANOTECHNOLOGY; NANOTUBES; PHOSPHOLIPIDS; TOXICITY; YARN;

BIOLOGICAL PERFORMANCE; BIOMEDICAL RESEARCH; HIGH CONTENT ANALYSIS; HYALURONAN; IMMUNE RESPONSE; INFLAMMATORY RESPONSE; SYSTEMIC ADMINISTRATION; THERAPEUTIC BENEFITS;

SINGLE-WALLED CARBON NANOTUBES (SWCN);

HYALURONIC ACID; INTERLEUKIN 10; LIVER ENZYME; PHOSPHOLIPID; SINGLE WALLED NANOTUBE; TUMOR NECROSIS FACTOR ALPHA; CARBON NANOTUBE; PHOSPHATIDYLETHANOLAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; CANCER CELL; CELL DEATH; CELL PROLIFERATION; CELL STRESS; CHEMICAL STRUCTURE; COMPARATIVE STUDY; COMPLEMENT ACTIVATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; ELECTROPHORETIC MOBILITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNE EVASION; IMMUNOCOMPETENT CELL; IMMUNOTOXICITY; INTERNALIZATION; LEUKOCYTE; MACROPHAGE; MITOCHONDRIAL TOXICITY; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SOLUBILIZATION; SUSPENSION; TRANSMISSION ELECTRON MICROSCOPY; ZETA POTENTIAL; ANIMAL; C57BL MOUSE; CELL LINE; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; HCT116 CELL LINE; METABOLISM;

ANIMALS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; COMPLEMENT ACTIVATION; HCT116 CELLS; HUMANS; HYALURONIC ACID; INTERLEUKIN-10; MACROPHAGES; MICE; MICE, INBRED C57BL; NANOTUBES, CARBON; PHOSPHATIDYLETHANOLAMINES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84879487807     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.05.042     Document Type: Article

References (48)

1. F. Lu, L. Gu, M.J. Meziani, X. Wang, P.G. Luo, L.M. Veca, L. Cao, Y.-P. Sun, Advances in bioapplications of carbon nanotubes, Adv. Mater. 21 (2) (2009) 139-152.
2. R. Sirdeshmukh, K. Teker, B. Panchapakesan (Eds.), Functionalization of Carbon Nanotubes with Antibodies for Breast Cancer Detection Applications. MEMS, NANO and Smart Systems, 2004 ICMENS 2004 Proceedings 2004 International Conference on, Aug. 25-27 2004.
3. M. Prato, K. Kostarelos, A. Bianco, Functionalized carbon nanotubes in drug design and discovery, Acc. Chem. Res. 41 (1) (Jan 2008) 60-68, (PubMed PMID: 17867649).
4. T.K. Leeuw, R.M. Reith, R.A. Simonette, M.E. Harden, P. Cherukuri, D.A. Tsyboulski, et al, Single-walled carbon nanotubes in the intact organism: near-IR imaging and biocompatibility studies in Drosophila, Nano Lett. 7 (9) (Sep 2007) 2650-2654, (PubMed PMID: 17696559). (Pubitemid 47522416)
5. Y. Zhang, Y. Bai, B. Yan, Functionalized carbon nanotubes for potential medicinal applications, Drug Discov. Today 15 (11-12) (Jun 2010) 428-435, (PubMed PMID: 20451656).
6. D.A. Heller, S. Baik, T.E. Eurell, M.S. Strano, Single-walled carbon nanotube spec-troscopy in live cells: towards long-term labels and optical sensors, Adv. Mater. 17 (23) (2005) 2793-2799. (Pubitemid 41797798)
7. Z. Liu, S.M. Tabakman, Z. Chen, H. Dai, Preparation of carbon nanotube bioconjugates for biomedical applications, Nat. Protoc. 4 (9) (2009) 1372-1382, (PubMed PMID: 19730421. Pubmed Central PMCID: 2853228).
8. Z. Liu, X. Sun, N. Nakayama-Ratchford, H. Dai, Supramolecular chemistry on water-soluble carbon nanotubes for drug loading and delivery, ACS Nano 1 (1) (Aug 2007) 50-56, (PubMed PMID: 19203129).
9. N.W. Kam, H. Dai, Carbon nanotubes as intracellular protein transporters: generality and biological functionality, J. Am. Chem. Soc. 127 (16) (Apr 27 2005) 6021-6026, (PubMed PMID: 15839702). (Pubitemid 40577658)
10. J. Cheng, K.A. Fernando, L.M. Veca, Y.P. Sun, A.I. Lamond, Y.W. Lam, et al, Reversible accumulation of PEGylated single-walled carbon nanotubes in the mammalian nucleus, ACS Nano 2 (10) (Oct 28 2008) 2085-2094, (PubMed PMID: 19206455).
11. Z. Liu, M. Winters, M. Holodniy, H. Dai, siRNA delivery into human T cells and primary cells with carbon-nanotube transporters, Angew. Chem. Int. Ed. Engl. 46 (12) (2007) 2023-2027, (PubMed PMID: 17290476). (Pubitemid 46973660)
12. M.S. Ladeira, V.A. Andrade, E.R. Gomes, C.J. Aguiar, E.R. Moraes, J.S. Soares, et al, Highly efficient siRNA delivery system into human and murine cells using single-wall carbon nanotubes, Nanotechnology 21 (38) (Sep 24 2010) 385101, (PubMed PMID: 20798464).
13. Z. Liu, K. Chen, C. Davis, S. Sherlock, Q. Cao, X. Chen, et al, Drug delivery with carbon nanotubes for in vivo cancer treatment, Cancer Res. 68 (16) (Aug 15 2008) 6652-6660, (PubMed PMID: 18701489. Pubmed Central PMCID: 2562710).
14. R. Crinelli, E. Carloni, M. Menotta, E. Giacomini, M. Bianchi, G. Ambrosi, et al, Oxidized ultrashort nanotubes as carbon scaffolds for the construction of cell-penetrating NF-kappaB decoy molecules, ACS Nano 4 (5) (May 25 2010) 2791-2803, (PubMed PMID: 20411956).
15. M.R. McDevitt, D. Chattopadhyay, B.J. Kappel, J.S. Jaggi, S.R. Schiffman, C. Antczak, et al, Tumor targeting with antibody-functionalized, radiolabeled carbon nanotubes, J. Nucl. Med. 48 (7) (Jul 2007) 1180-1189, (PubMed PMID: 17607040). (Pubitemid 47052659)
16. S.Y. Hong, G. Tobias, K.T. Al-Jamal, B. Ballesteros, H. Ali-Boucetta, S. Lozano-Perez, et al, Filled and glycosylated carbon nanotubes for in vivo radioemitter localization and imaging, Nat. Mater. 9 (6) (Jun 2010) 485-490, (PubMed PMID: 20473287).
17. Z. Liu, S. Tabakman, K. Welsher, H. Dai, Carbon nanotubes in biology and medicine: in vitro and in vivo detection, imaging and drug delivery, Nano Res. 2 (2) (Feb 1 2009) 85-120, (PubMed PMID: 20174481. Pubmed Central PMCID: 2824900).
18. M.S. Strano, Probing chiral selective reactions using a revised Kataura plot for the interpretation of single-walled carbon nanotube spectroscopy, J. Am. Chem. Soc. 125 (51) (2003) 16148-16153. (Pubitemid 37553733)
19. D. Peer, J.M. Karp, S. Hong, O.C. Farokhzad, R. Margalit, R. Langer, Nanocarriers as an emerging platform for cancer therapy, Nat. Nanotechnol. 2 (12) (Dec 2007) 751-760, (PubMed PMID: 18654426). (Pubitemid 350223348)
20. S. Mizrahy, D. Peer, Polysaccharides as building blocks for nanotherapeutics, Chem. Soc. Rev. 41 (7) (Apr 7 2012) 2623-2640, (PubMed PMID: 22085917).
21. D. Peer, E.J. Park, Y. Morishita, C.V. Carman, M. Shimaoka, Systemic leukocyte-directed siRNA delivery revealing cyclin D1 as an anti-inflammatory target, Science 319 (5863) (Feb 1 2008) 627-630, (PubMed PMID: 18239128. Pubmed Central PMCID: 2490797). (Pubitemid 351197066)
22. R. Kedmi, N. Ben-Arie, D. Peer, The systemic toxicity of positively charged lipid nanoparticles and the role of Toll-like receptor 4 in immune activation, Biomaterials 31 (26) (Sep 2010) 6867-6875, (PubMed PMID: 20541799).
23. S.S. Kim, D. Peer, P. Kumar, S. Subramanya, H. Wu, D. Asthana, et al, RNAi-mediated CCR5 silencing by LFA-1-targeted nanoparticles prevents HIV infection in BLT mice, Mol. Ther. 18 (2) (Feb 2010) 370-376, (PubMed PMID: 19997090).
24. X. Li, Y. Peng, J. Ren, X. Qu, Carboxyl-modified single-walled carbon nanotubes selectively induce human telomeric i-motif formation, Proc. Natl. Acad. Sci. U. S. A. 103 (52) (Dec 26 2006) 19658-19663, (PubMed PMID: 17167055. Pubmed Central PMCID: 1750900). (Pubitemid 46037487)
25. A.J. Andersen, J.T. Robinson, H. Dai, A.C. Hunter, T.L. Andresen, S.M. Moghimi, Single-walled carbon nanotube surface control of complement recognition and activation, ACS Nano 7 (2) (Jan 16 2013) 1108-1119, (PubMed PMID: 23301860).
26. S. Mizrahy, S.R. Raz, M. Hasgaard, H. Liu, N. Soffer-Tsur, K. Cohen, et al, Hyaluronan-coated nanoparticles: the influence of the molecular weight on CD44-hyaluronan interactions and on the immune response, J. Control. Release 156 (2) (Dec 10 2011) 231-238, (PubMed PMID: 21745506).
27. L.A. Mitchell, F.T. Lauer, S.W. Burchiel, J.D. McDonald, Mechanisms for how inhaled multiwalled carbon nanotubes suppress systemic immune function in mice, Nat. Nanotechnol. 4 (7) (Jul 2009) 451-456, (PubMed PMID: 19581899).
28. Z. Liu, S. Tabakman, K. Welsher, H.J. Dai, Carbon nanotubes in biology and medicine: in vitro and in vivo detection, imaging and drug delivery, Nano Res. 2 (2) (Feb 2009) 85-120, (PubMed PMID: ISI:000273939000001. English).
29. D.F. Williams, On the nature of biomaterials, Biomaterials 30 (30) (Oct 2009) 5897-5909, (PubMed PMID: 19651435).
30. I. Rivkin, K. Cohen, J. Koffler, D. Melikhov, D. Peer, R. Margalit, Paclitaxel-clusters coated with hyaluronan as selective tumor-targeted nanovectors, Biomaterials 31 (27) (Sep 2010) 7106-7114, (PubMed PMID: 20619792).
31. M. Cohen, Z. Kam, L. Addadi, B. Geiger, Dynamic study of the transition from hyaluronan- to integrin-mediated adhesion in chondrocytes, EMBO J. 25 (2) (Jan 25 2006) 302-311, (PubMed PMID: 16407968. Pubmed Central PMCID: 1383524). (Pubitemid 43152851)
32. D. Joester, E. Klein, B. Geiger, L. Addadi, Temperature-sensitive micrometer-thick layers of hyaluronan grafted on microspheres, J. Am. Chem. Soc. 128 (4) (Feb 1 2006) 1119-1124, (PubMed PMID: 16433527). (Pubitemid 43190622)
33. L.J. Solmesky, M. Shuman, M. Goldsmith, M. Weil, D. Peer, Assessing cellular tox-icities in fibroblasts upon exposure to lipid-based nanoparticles: a high content analysis approach, Nanotechnology 22 (49) (Nov 21 2011) 494016, (PubMed PMID: 22101838).
34. D. Landesman-Milo, D. Peer, Altering the immune response with lipid-based nanoparticles, J. Control. Release 161 (2) (Jul 20 2012) 600-608, (PubMed PMID: 22230342).
35. D.F. Moyano, M. Goldsmith, D.J. Solfiell, D. Landesman-Milo, O.R. Miranda, D. Peer, et al, Nanoparticle hydrophobicity dictates immune response, J. Am. Chem. Soc. 134 (9) (Mar 7 2012) 3965-3967, (PubMed PMID: 22339432. Pubmed Central PMCID: 3296893).
36. R. Ulevitch, Molecular mechanisms of innate immunity, Immunol. Res. 21 (2) (2000) 49-54.
37. B. Beutler, Inferences, questions and possibilities in Toll-like receptor signalling, Nature 430 (6996) (Jul 8 2004) 257-263, (PubMed PMID: 15241424). (Pubitemid 38902439)
38. C. Platzer, C. Meisel, K. Vogt, M. Platzer, H.D. Volk, Up-regulation of monocytic IL-10 by tumor necrosis factor-alpha and cAMP elevating drugs, Int. Immunol. 7 (4) (Apr 1995) 517-523, (PubMed PMID: 7547677).
39. S.M. Moghimi, P.P. Wibroe, S.Y. Helvig, Z.S. Farhangrazi, A.C. Hunter, Genomic perspectives in inter-individual adverse responses following nanomedicine administration: the way forward, Adv. Drug Deliv. Rev. 64 (13) (May 23 2012) 1385-1393, (PubMed PMID: 22634158).
40. A.J. Andersen, P.P. Wibroe, S.M. Moghimi, Perspectives on carbon nanotube-mediated adverse immune effects, Adv. Drug Deliv. Rev. 64 (15) (May 23 2012) 1700-1705, (PubMed PMID: 22634159).
41. S.M. Moghimi, A.J. Andersen, S.H. Hashemi, B. Lettiero, D. Ahmadvand, A.C. Hunter, et al, Complement activation cascade triggered by PEG-PL engineered nanomedicines and carbon nanotubes: the challenges ahead, J. Control. Release 146 (2) (Sep 1 2010) 175-181, (PubMed PMID: 20388529).
42. S.M. Moghimi, A.C. Hunter, Complement monitoring of carbon nanotubes, Nat. Nanotechnol. 5 (6) (Jun 2010) 382, (author reply-3. PubMed PMID: 20523330).
43. D. Peer, R. Margalit, Tumor-targeted hyaluronan nanoliposomes increase the antitumor activity of liposomal Doxorubicin in syngeneic and human xenograft mouse tumor models, Neoplasia 6 (4) (Jul-Aug 2004) 343-353, (PubMed PMID: 15256056. Pubmed Central PMCID: 1502115). (Pubitemid 38924849)
44. G. Bachar, K. Cohen, R. Hod, R. Feinmesser, A. Mizrachi, T. Shpitzer, et al, Hyaluronan-grafted particle clusters loaded with Mitomycin C as selective nanovectors for primary head and neck cancers, Biomaterials 32 (21) (Jul 2011) 4840-4848, (PubMed PMID: 21482433).
45. D. Peer, Immunotoxicity derived from manipulating leukocytes with lipid-based nanoparticles, Adv. Drug Deliv. Rev. 64 (15) (2012 Dec) 1738-1748, (PubMed PMID: 22820531).
46. D. Landesman-Milo, M. Goldsmith, S. Leviatan Ben-Arye, B. Witenberg, E. Brown, S. Leibovitch, et al., Hyaluronan grafted lipid-based nanoparticles as RNAi carriers for cancer cells, Cancer Lett. 334 (2) (Aug 27 2012) 221-227, (PubMed PMID: 22935680).
47. D. Peer, R. Margalit, Loading mitomycin C inside long circulating hyaluronan targeted nano-liposomes increases its antitumor activity in three mice tumor models, Int. J. Cancer 108 (5) (Feb 20 2004) 780-789, (PubMed PMID: 14696107). (Pubitemid 38076412)
48. R.E. Eliaz, F.C. Szoka Jr., Liposome-encapsulated doxorubicin targeted to CD44: a strategy to kill CD44-overexpressing tumor cells, Cancer Res. 61 (6) (Mar 15 2001) 2592-2601, (PubMed PMID: 11289136). (Pubitemid 32685844)