Journal Home > Volume 3 , Issue 11
Nano Research 2010, 3(11): 779-793 https://doi.org/10.1007/s12274-010-0045-1
Research Article | Open Access | Issue | Published: 12 October 2010

High Performance In Vivo Near-IR (> 1μm) Imaging and Photothermal Cancer Therapy with Carbon Nanotubes

Show Author's Information Joshua T. Robinson1,  Kevin Welsher1,  Scott M. Tabakman1,  Sarah P. Sherlock1,  Hailiang Wang1,  Richard Luong2,  Hongjie Dai1( )
Department of Chemistry Stanford UniversityStanfordCA 94305 USA
Department of Comparative Medicine Stanford University School of MedicineStanfordCA 94305 USA
Keywords:
treatment, imaging, cancer, Photothermal, SWNT
Cite this article:
Robinson JT, Welsher K, Tabakman SM, et al. High Performance In Vivo Near-IR (> 1μm) Imaging and Photothermal Cancer Therapy with Carbon Nanotubes. Nano Research, 2010, 3(11): 779-793. https://doi.org/10.1007/s12274-010-0045-1
Download citation
EndNote(RIS)
BibTeX

656

Views

23

Downloads

Citations

431

Crossref

N/A

WoS

466

Scopus

0

CSCD

Abstract Full text Electronic supplementary material About this article

Short single-walled carbon nanotubes (SWNTs) functionalized by PEGylated phospholipids are biologically non-toxic and long-circulating nanomaterials with intrinsic near infrared photoluminescence (NIR PL), characteristic Raman spectra, and strong optical absorbance in the near infrared (NIR). This work demonstrates the first dual application of intravenously injected SWNTs as photoluminescent agents for in vivo tumor imaging in the 1.0-1.4 μm emission region and as NIR absorbers and heaters at 808 nm for photothermal tumor elimination at the lowest injected dose (70 μg of SWNT/mouse, equivalent to 3.6 mg/kg) and laser irradiation power (0.6 W/cm2) reported to date. Ex vivo resonance Raman imaging revealed the SWNT distribution within tumors at a high spatial resolution. Complete tumor elimination was achieved for large numbers of photothermally treated mice without any toxic side effects after more than six months post-treatment. Further, side-by-side experiments were carried out to compare the performance of SWNTs and gold nanorods (AuNRs) at an injected dose of 700 μg of AuNR/mouse (equivalent to 35 mg/kg) in NIR photothermal ablation of tumors in vivo. Highly effective tumor elimination with SWNTs was achieved at 10 times lower injected doses and lower irradiation powers than for AuNRs. These results suggest there are significant benefits of utilizing the intrinsic properties of biocompatible SWNTs for combined cancer imaging and therapy.


menu
Abstract
Full text
Outline
Electronic supplementary material
About this article

High Performance In Vivo Near-IR (> 1μm) Imaging and Photothermal Cancer Therapy with Carbon Nanotubes

Show Author's information Joshua T. Robinson1, Kevin Welsher1, Scott M. Tabakman1, Sarah P. Sherlock1, Hailiang Wang1, Richard Luong2, Hongjie Dai1( )
Department of Chemistry Stanford UniversityStanfordCA 94305 USA
Department of Comparative Medicine Stanford University School of MedicineStanfordCA 94305 USA

Abstract

Short single-walled carbon nanotubes (SWNTs) functionalized by PEGylated phospholipids are biologically non-toxic and long-circulating nanomaterials with intrinsic near infrared photoluminescence (NIR PL), characteristic Raman spectra, and strong optical absorbance in the near infrared (NIR). This work demonstrates the first dual application of intravenously injected SWNTs as photoluminescent agents for in vivo tumor imaging in the 1.0-1.4 μm emission region and as NIR absorbers and heaters at 808 nm for photothermal tumor elimination at the lowest injected dose (70 μg of SWNT/mouse, equivalent to 3.6 mg/kg) and laser irradiation power (0.6 W/cm2) reported to date. Ex vivo resonance Raman imaging revealed the SWNT distribution within tumors at a high spatial resolution. Complete tumor elimination was achieved for large numbers of photothermally treated mice without any toxic side effects after more than six months post-treatment. Further, side-by-side experiments were carried out to compare the performance of SWNTs and gold nanorods (AuNRs) at an injected dose of 700 μg of AuNR/mouse (equivalent to 35 mg/kg) in NIR photothermal ablation of tumors in vivo. Highly effective tumor elimination with SWNTs was achieved at 10 times lower injected doses and lower irradiation powers than for AuNRs. These results suggest there are significant benefits of utilizing the intrinsic properties of biocompatible SWNTs for combined cancer imaging and therapy.

Keywords: treatment, imaging, cancer, Photothermal, SWNT

References(44)

1

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.
DOI Google Scholar
2

Liu, Z.; Cai, W.; He, L.; Nakayama, N.; Chen, K.; Sun, X.; Chen, X.; Dai, H. In vivo biodistribution and highly efficient tumor targeting of carbon nanotubes in mice. Nat. Nanotechnol. 2007, 2, 47-52.
DOI Google Scholar
3

Liu, Z.; Chen, K.; Davis, C.; Sherlock, S.; Cao, Q.; Chen, X.; Dai, H. Drug delivery with carbon nanotubes for in vivo cancer treatment. Cancer Res. 2008, 68, 6652-6660.
DOI Google Scholar
4

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. Edit. 2009, 48, 7668-7672.
DOI Google Scholar
5

Kam, N. W.; 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. Sci. USA 2005, 102, 11600-11605.
DOI Google Scholar
6

Moon, H. K.; Lee, S. H.; Choi, H. C. In vivo near-infrared mediated tumor destruction by photothermal effect of carbon nanotubes. ACS Nano 2009, 3, 3707-3713.
DOI Google Scholar
7

Chen, Z.; Tabakman, S. M.; Goodwin, A. P.; Kattah, M. G.; Daranciang, D.; Wang, X.; Zhang, G.; Li, X.; Liu, Z.; Utz, P. J., et al. Protein microarrays with carbon nanotubes as multicolor raman labels. Nat. Biotechnol. 2008, 26, 1285-1292.
DOI Google Scholar
8

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.
DOI Google Scholar
9

Cherukuri, P.; Gannon, C. J.; Leeuw, T. K.; Schmidt, H. K.; Smalley, R. E.; Curley, S. A.; Weisman, R. B. Mammalian pharmacokinetics of carbon nanotubes using intrinsic near-infrared fluorescence. Proc. Natl. Acad. Sci. USA 2006, 103, 18882-18886.
DOI Google Scholar
10

Leeuw, T. K.; Reith, R. M.; Simonette, R. A.; Harden, M. E.; Cherukuri, P.; Tsyboulski, D. A.; Beckingham, K. M.; Weisman, R. B. Single-walled carbon nanotubes in the intact organism: Near-ir imaging and biocompatibility studies in drosophila. Nano Lett. 2007, 7, 2650-2654.
DOI Google Scholar
11

Liu, Z.; Li, X.; Tabakman, S. M.; Jiang, K.; Fan, S.; Dai, H. Multiplexed multicolor raman imaging of live cells with isotopically modified single walled carbon nanotubes. J. Am. Chem. Soc. 2008, 130, 13540-13541.
DOI Google Scholar
12

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.
DOI Google Scholar
13

Keren, S.; Zavaleta, C.; Cheng, Z.; de la Zerda, A.; Gheysens, O.; Gambhir, S. S. Noninvasive molecular imaging of small living subjects using raman spectroscopy. Proc. Natl. Acad. Sci. USA 2008, 105, 5844-5849.
DOI Google Scholar
14

Smith, A. M.; Mancini, M. C.; Nie, S. Bioimaging: Second window for in vivo imaging. Nat. Nanotechnol. 2009, 4, 710-711.
DOI Google Scholar
15

Welsher, K.; Liu, Z.; Sherlock, S. P.; Robinson, J. T.; Chen, Z.; Daranciang, D.; Dai, H. A route to brightly fluorescent carbon nanotubes for near-infrared imaging in mice. Nat. Nanotechnol. 2009, 4, 773-780.
DOI Google Scholar
16

Perrault, S. D.; Walkey, C.; Jennings, T.; Fischer, H. C.; Chan, W. C. W. Mediating tumor targeting efficiency of nanoparticles through design. Nano Lett. 2009, 9, 1909-1915.
DOI Google Scholar
17

Eghtedari, M.; Oraevsky, A.; Copland, J. A.; Kotov, N. A.; Conjusteau, A.; Motamedi, M. High sensitivity of in vivo detection of gold nanorods using a laser optoacoustic imaging system. Nano Lett. 2007, 7, 1914-1918.
DOI Google Scholar
18

Kim, J. -W.; Galanzha, E. I.; Shashkov, E. V.; Moon, H. -M.; Zharov, V. P. Golden carbon nanotubes as multimodal photoacoustic and photothermal high-contrast molecular agents. Nat. Nanotechnol. 2009, 4, 688-694.
DOI Google Scholar
19

De La Zerda, A.; Zavaleta, C.; Keren, S.; Vaithilingam, S.; Bodapati, S.; Liu, Z.; Levi, J.; Smith, B. R.; Ma, T. -J.; Oralkan, O., et al. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat. Nanotechnol. 2008, 3, 557-562.
DOI Google Scholar
20

Aubin, J. E. Autofluorescence of viable cultured mammalian cells. J. Histochem. Cytochem. 1979, 27, 36-43.
DOI Google Scholar
21

O'Neal, D. P.; Hirsch, L. R.; Halas, N. J.; Payne, J. D.; West, J. L. Photo-thermal tumor ablation in mice using near infrared-absorbing nanoparticles. Cancer Lett. 2004, 209, 171-176.
DOI Google Scholar
22

Sassaroli, E.; Li, K. C. P.; O'Neill, B. E. Numerical investigation of heating of a gold nanoparticle and the surrounding microenvironment by nanosecond laser pulses for nanomedicine applications. Phys. Med. Biol. 2009, 54, 5541-5560.
DOI Google Scholar
23

Stern, J. M.; Stanfield, J.; Kabbani, W.; Hsieh, J. -T.; Cadeddu, J. A. Selective prostate cancer thermal ablation with laser activated gold nanoshells. J. Urology 2008, 179, 748-753.
DOI Google Scholar
24

Terentyuk, G. S.; Maslyakova, G. N.; Suleymanova, L. V.; Khlebtsov, N. G.; Khlebtsov, B. N.; Akchurin, G. G.; Maksimova, I. L.; Tuchin, V. V. Laser-induced tissue hyperthermia mediated by gold nanoparticles: Toward cancer phototherapy. J. Biomed. Opt. 2009, 14, 021016.
DOI Google Scholar
25

Huang, X.; Jain, P.; El-Sayed, I.; El-Sayed, M. Plasmonic photothermal therapy (pptt) using gold nanoparticles. Laser Med. Sci. 2008, 23, 217-228.
DOI Google Scholar
26

von Maltzahn, G.; Park, J. -H.; Agrawal, A.; Bandaru, N. K.; Das, S. K.; Sailor, M. J.; Bhatia, S. N. Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas. Cancer Res. 2009, 69, 3892-3900.
DOI Google Scholar
27

Huff, T. B.; Tong, L.; Zhao, Y.; Hansen, M. N.; Cheng, J. -X.; Wei, A. Hyperthermic effects of gold nanorods on tumor cells. Nanomedicine-UK 2007, 2, 125-132.
DOI Google Scholar
28

Dickerson, E. B.; Dreaden, E. C.; Huang, X.; El-Sayed, I. H.; Chu, H.; Pushpanketh, S.; McDonald, J. F.; El-Sayed, M. A. Gold nanorod assisted near-infrared plasmonic photothermal therapy (pptt) of squamous cell carcinoma in mice. Cancer Lett. 2008, 269, 57-66.
DOI Google Scholar
29

Hasan, W.; Stender, C. L.; Lee, M. H.; Nehl, C. L.; Lee, J.; Odom, T. W. Tailoring the structure of nanopyramids for optimal heat generation. Nano Lett. 2009, 9, 1555-1558.
DOI Google Scholar
30

Ghosh, S.; Dutta, S.; Gomes, E.; Carroll, D.; D'Agostino, R.; Olson, J.; Guthold, M.; Gmeiner, W. H. Increased heating efficiency and selective thermal ablation of malignant tissue with DNA-encased multiwalled carbon nanotubes. ACS Nano 2009, 3, 2667-2673.
DOI Google Scholar
31

Gannon, C. J.; Cherukuri, P.; Yakobsen, 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.
DOI Google Scholar
32

Xiao, Y.; Gao, X.; Taratula, O.; Treado, S.; Urbas, A.; Holbrook, R. D.; Cavicchi, R.; Avedisian, C. T.; Mitra, S.; Savla, R., et al. Anti-her2 igy antibody-functionalized single-walled carbon nanotubes for detection and selective destruction of breast cancer cells. BMC Cancer 2009, 9, 351.
DOI Google Scholar
33

Zhou, F.; Xing, D.; Ou, Z.; Wu, B.; Resasco, D. E.; Chen, W. R. Cancer photothermal therapy in the near-infrared region by using single-walled carbon nanotubes. J. Biomed. Opt. 2009, 14, 021009.
DOI Google Scholar
34

Prencipe, G.; Tabakman, S. M.; Welsher, K.; Liu, Z.; Goodwin, A. P.; Zhang, L.; Henry, J.; Dai, H. PEG branched polymer for functionalization of nanomaterials with ultralong blood circulation. J. Am. Chem. Soc. 2009, 131, 4783-4787.
DOI Google Scholar
35

Liu, Z.; Tabakman, S. M.; Chen, Z.; Dai, H. Preparation of carbon nanotube bioconjugates for biomedical applications. Nat. Protoc, 2009, 4, 1372-1381.
DOI Google Scholar
36

O'Connell, M. J.; Bachilo, S. M.; Huffman, C. B.; Moore, V. C.; Strano, M. S.; Haroz, E. H.; Rialon, K. L.; Boul, P. J.; Noon, W. H.; Kittrell, C., et al. Band gap fluorescence from individual single-walled carbon nanotubes. Science 2002, 297, 593-596.
DOI Google Scholar
37

Nikoobakht, B.; El-Sayed, M. A. Preparation and growth mechanism of gold nanorods (NRs) using seed-mediated growth method. Chem. Mater. 2003, 15, 1957-1962.
DOI Google Scholar
38

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.
DOI Google Scholar
39

Lee, J. H.; Sherlock, S. P.; Masahiro, T.; Hisanori, K.; Suzuki, Y.; Goodwin, A.; Robinson, J.; Seo, W.S.; Liu, Z.; Luong, R., et al. High-contrast in vivo visualization of microvessels using novel feco/gc magnetic nanocrystals. Magn. Reson. Med. 2009, 62, 1497-1509.
DOI Google Scholar
40

Schwartz, J. A.; Shetty, A. M.; Price, R. E.; Stafford, R. J.; Wang, J. C.; Uthamanthil, R. K.; Pham, K.; McNichols, R. J.; Coleman, C. L.; Payne, J. D. Feasibility study of particle-assisted laser ablation of brain tumors in orthotopic canine model. Cancer Res. 2009, 69, 1659-1667.
DOI Google Scholar
41

Jain, P. K.; Lee, K. S.; El-Sayed, I. H.; El-Sayed, M. A. Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: Applications in biological imaging and biomedicine. J. Phys. Chem. B 2006, 110, 7238-7248.
DOI Google Scholar
42

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. Nat. Nanotechnol. 2008, 3, 216-221.
DOI Google Scholar
43

Day, E. S.; Morton, J. G.; West, J. L. Nanoparticles for thermal cancer therapy. J. Biomech. Eng. -T ASME 2009, 131, 074001.
DOI Google Scholar
44

Wang, S.; Lu, W.; Tovmachenko, O.; Rai, U. S.; Yu, H.; Ray, P. C. Challenge in understanding size and shape dependent toxicity of gold nanomaterials in human skin keratinocytes. Chem. Phys. Lett. 2008, 463, 145-149.
DOI Google Scholar
File
12274_2010_45_MOESM1_ESM.pdf (441.8 KB)
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 23 August 2010
Accepted: 13 September 2010
Published: 12 October 2010
Issue date: November 2010

Copyright

© The Author(s) 2010

Acknowledgements

Acknowledgements

This work was supported by Ensysce Biosciences, CCNE-TR at Stanford University and NIH-NCI RO1 CA135109-02.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Return