In vivo therapeutic silencing of hypoxia-inducible factor 1 alpha (HIF-1α) using single-walled carbon nanotubes noncovalently coated with siRNA

Nano Research

Volumn 2, Issue 4, 2009, Pages 279-291

  Bartholomeusz, Geoffrey ^a   Cherukuri, Paul ^a,b   Kingston, John ^a   Cognet, Laurent ^b,c   Lemos Jr , Robert ^a   Leeuw, Tonya K ^b   Gumbiner Russo, Laura ^a   Weisman, R Bruce ^b   Powis, Garth ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b RICE UNIVERSITY   (United States)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Anti cancer therapy; In vivo delivery agent; Single walled carbon nanotubes; SiRNA

Indexed keywords

EID: 65349083822     PISSN: 19980124     EISSN: 19980000     Source Type: Journal    
DOI: 10.1007/s12274-009-9026-7     Document Type: Article

References (45)

1. Hoeckel, M.; Schlenger, K.; Hoeckel, S.; Vaupel, P. Hypoxic cervical cancers with low apoptotic index are highly aggressive. Cancer Res. 1999, 59, 4525-4528. (Pubitemid 29428951)
2. Brown, J. M. Exploiting the hypoxic cancer cell: Mechanisms and therapeutic strategies. Mol. Med. Today 2000, 6, 157-162. (Pubitemid 30171366)
3. Brown, J. M. & Giaccia, A. J. The unique physiology of solid tumors: Opportunities (and problems) for cancer therapy. Cancer Res. 1998, 58, 1408-1416. (Pubitemid 28193601)
4. Unruh, A.; Ressel, A.; Mohamed, H. G.; Johnson, R. S.; Nadrowitz, R.; Richter, E.; Katschinski, D. M.; Wenger, R. H. The hypoxia-inducible factor-1α is a negative factor for tumor therapy. Oncogene 2003, 22, 3213-3220. (Pubitemid 36712933)
5. Aebersold, D. M.; Burri, P.; Beer, K. T.; Laissue, J.; Djonov, V.; Greiner, R. H.; Semenza, G. L. Expression of hypoxia-inducible factor-1α: A novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res. 2001, 61, 2911-2916. (Pubitemid 32691934)
6. Zhang, X. W.; Kon, T.; Wang, H.; Li, F.; Huang, Q.; Rabbani, Z. N.; Kirkpatrick, J. P.; Vujaskovic, Z.; Dewhirst, M. W.; Li, C. Y. Enhancement of hypoxia-induced tumor cell death in vitro and radiation therapy in vivo by use of small interfering RNA targeted to hypoxia-inducible factor-1α. Cancer Res. 2004, 64, 8139-8142. (Pubitemid 39491746)
7. Talks, K. L.; Turley, H.; Gatter, K. C.; Maxwell, P. H.; Pugh, C. W.; Ratcliffe, P. J.; Harris, A. L. The expression and distribution of the hypoxia-inducible factors HIF-1α and HIF-2α in normal human tissues, cancers, and tumor-associated macrophages. Am. J. Path. 2000, 157, 411-421. (Pubitemid 30626905)
8. Zhong, H.; De Marzo, A. M.; Laughner, E.; Lim, M.; Hilton, D. A.; Zagzag, D.; Buechler, P.; Isaacs, W. B.; Semenza, G. L.; Simons, J. W. Overexpression of hypoxia-inducible factor 1α in common human cancers and their metastases. Cancer Res. 1999, 59, 5830-5835.
9. Semenza, G. L. Targeting HIF-1α for cancer therapy. Nat. Rev. Cancer 2003, 3, 721-732. (Pubitemid 37328811)
10. Liao, D.; Corle, C.; Seagroves, T. N.; Johnson, R. S. Hypoxia-inducible factor-1α is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res. 2007, 67, 563-572. (Pubitemid 46192193)
11. Stoeltzing, O.; McCarty, M. F.; Wey, J. S.; Fan, F.; Liu, W. B.; Belcheva, A.; Bucana, C. D.; Semenza, G. L.; Ellis, L. M. Role of hypoxia-inducible factor 1α in gastric cancer cell growth, angiogenesis, and vessel maturation. J. Natl. Cancer Inst. 2004, 96, 946-956. (Pubitemid 38868141)
12. Maxwell, P. H.; Dachs, G. U.; Gleadle, J. M.; Nicholls, L. G.; Harris, A. L.; Stratford, I. J.; Hankinson, O.; Pugh, C. W.; Ratcliffe, P. J. Hypoxia-inducible factor-1α modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc. Natl. Acad. Sci. USA 1997, 94, 8104-8109. (Pubitemid 27343784)
13. Ryan, H. E.; Poloni, M.; McNulty, W.; Elson, D.; Gassmann, M.; Arbeit, J. M.; Johnson, R. S. Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res. 2000, 60, 4010-4015. (Pubitemid 30636574)
14. Kung, A. L.; Wang, S.; Klco, J. M.; Kaelin, W. G.; Livingston, D. M. Suppresion of tumor growth through disruption of hypoxia-inducible transcription. Nat. Med. 2000, 6, 1335-1340. (Pubitemid 32001016)
15. Dykxhoorn, D. M.; Lieberman, J. Knocking down diseases with siRNA. Cell 2006, 126, 231-235.
16. Kam, N. W. S.; Dai, H. Carbon nanotubes as intracellular protein transporters: Generality and biological functionality. J. Am. Chem. Soc. 2005, 127, 6021-6026. (Pubitemid 40577658)
17. Kam, N. W. S.; Liu, Z.; Dai, H. Functionalization of carbon nanotubes via cleavable disulfide bonds for efficient intracellular delivery of siRNA and potent gene silencing. J. Am. Chem. Soc. 2005, 127, 12492-12493. (Pubitemid 41292159)
18. Kam, N. W. S.; Jessop, T. C.; Wender, P. A; Dai, H. Nanotube molecular transporters: Internalization of carbon nanotubes-protein conjugates into mammalian cells. J. Am. Chem. Soc. 2004, 126, 6850-6851. (Pubitemid 38855367)
19. Zhang, Z. H.; Yang, X. Y.; Zhang, Y.; Zeng, B.; Wang, Z. J.; Zhu, T. H.; Roden, R. B. S.; Chen, Y. S.; Yang, R. C. Delivery of telomerase reverse transcriptase small interfering RNA in complex with positively charged single-walled carbon nanotubes suppresses tumor growth. Clin. Cancer Res. 2006, 12, 4933-4939. (Pubitemid 44338581)
20. Cherukuri, P.; Bachilo, S. M.; Litovsky, S. H.; Weisman, R. B. Near-infrared flourescence microscopy of sinngled-walled carbon nanotubes in phagocytic cells. J. Am. Chem. Soc. 2004, 126, 15638-15639. (Pubitemid 39602412)
21. Tasis, D.; Tagmatarchis, N.; Georgakilas, V.; Prato, M. Soluble carbon nanotubes. Chem. Eur. J. 2003, 9, 4000-4008.
22. Bianco, A.; Kostarelos, K.; Prato, M. Application of carbon nanotubes in drug discovery. Curr. Opin. Chem. Biol. 2005, 9, 674-679. (Pubitemid 41612196)
23. Pantarotto, D.; Singh, R.; McCarthy, D.; Erhardt, M.; Briand, J. P.; Prato, M.; Kostarelos, K.; Bianco, A. Functionalized carbon nanotubes for plasmid DNA gene delivery. Angew. Chem. Int. Ed. 2004, 43, 5242-5246. (Pubitemid 39382552)
24. Tasis, D.; Tagmatarchis, N.; Bianco, A.; Prato, M. Chemistry of carbon nanotubes. Chem. Rev. 2006, 106, 1105-1136.
25. Zhao, W.; Song, C.; Pehrsson, P. E. Water-soluble and optically pH-sensitive single-walled carbon nanotubes from surface modification. J. Am. Chem. Soc. 2002, 124, 12418-12419. (Pubitemid 35204560)
26. He, P.; Urban, M. W. Controlled phospholipid functionalization of single-walled carbon nanotubes. Biomacromolecules 2005, 6, 2455-2457. (Pubitemid 41388253)
27. Liu, Z.; Winters, M.; Holodniy, M.; Dai, H. siRNA delivery into human T cells and primary cells with carbonnanotube transporters. Angew. Chem. Int. Ed. 2007, 46, 1-6. (Pubitemid 46973660)
28. Magrez, A.; Kasas, S.; Salicio, V.; Pasquier, N.; Seo, J. W.; Celio, M.; Catsicas, S.; Schwaller, B.; Forro, L. Cellular toxicity of carbon-based nanometrials. Nano Lett. 2006, 6, 1121-1125.
29. Zheng, M.; Jagota, A.; Semke, E. D.; Diner, B. A.; Mclean, R. S.; Lustig, S. R.; Richardson, R. E.; Tassi, N. G. DNA-assisted dispersion and separation of carbon nanotubes. Nat. Mater. 2003, 2, 338-342.
30. Dwyer, C.; Guthold, M.; Falvo, M.; Washburn, S.; Superfine, R.; Erie, D. DNA-functionalized single-walled carbon nanotubes. Nanotechnology 2002, 13, 601-604. (Pubitemid 35263787)
31. Nepal, D.; Sohn, J. I.; Aicher, W. K.; Lee, S. J.; Geckeler, K. E. Supramolecular conjugates of carbon nanotubes and dna by a solid-state reaction. Biomacromolecules 2005, 6, 2919-2922. (Pubitemid 41764043)
32. Zheng, M.; Jagota, A.; Strano, M. S.; Santos, A. P.; Barone, P.; Chou, S. G.; Diner, B. A.; Dresselhaus, M. S.; McLean, R. S.; Onoa, G. B.; Samsonidze, G. G.; Semke, E. D.; Usrey, M.; Walls, D. J. Structure-based carbon nanotubes sorting by sequence-dependent dna assembly. Science 2003, 302, 1545-1548. (Pubitemid 37475693)
33. Nikolaev, P.; Bronikowski, M. J.; Bradley, R. K.; Rohmund, F.; Colbert, D. T.; Smith, K. A.; Smalley, R. E. Gas-phase catalytic growth of single-walled carbon nanotubes from carbon monoxide. Chem. Phys. Lett. 1999, 313, 91-97. (Pubitemid 129556626)
34. Tsyboulski, D. A.; Bachilo, S. M.; Weisman, R. B. Versatile visualization of individual single-walled carbon nanotubes with near-infrared fluorescence microscopy. Nano Lett. 2005, 5, 975-979.
35. PaineMurrieta, G. D.; Taylor, C. W.; Curtis, R. A.; Lopez, M. H. A.; Dorr, R. T.; Johnson, C. S.; Funk, C. Y.; Thompson, F.; Hersh, E. M. Human tumor models in the severe combined immune deficient (scid) mouse. Cancer Chemother Pharmacol. 1997, 40, 209-214. (Pubitemid 27257733)
36. Svensson, R. U.; Barnes, J. M.; Rokhlin, O. W.; Cohen, M. B.; Henry, M. D. Chemotherapeutic agents up-regulate the cytomegalovirus promoter: implications for bioluminescence imaging of tumor response to therapy. Cancer Res. 2007, 67, 10445-10454. (Pubitemid 350070820)
37. 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. (Pubitemid 350002796)
38. 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. (Pubitemid 43346474)
39. Liu, Z.; Davis, C.; Cai, W. B.; He, L.; Chen, X. Y.; Dai, H. J. 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.
40. Liu, Z.; Cai, W. B.; He, L. N.; Nakayama, N.; Chen, K.; Sun, X. M.; Chen, X. Y.; Dai, H. J. In vivo biodistribution and highly efficient tumour targeting of carbon nanotubes in mice. Nat. Nanotechnol. 2007, 2, 47-52. (Pubitemid 46210038)
41. Schipper, M. L.; Nakayama-Ratchford, N.; Davis, C. R.; Kam, N. W. S.; Chu, P.; Liu, Z.; Sun, X. M.; Dai, H. J.; Gambhir, S. S. A pilot toxicology study of single-walled carbon nanotubes in a small sample of mice. Nat. Nanotechnol. 2008, 3, 216-221.
42. Yang, S. T.; Guo, W.; Lin, Y.; Deng, X. Y.; Wang, H. F.; Sun, H. F.; Liu, Y. F.; Wang, X.; Wang, W.; Chen, M.; Huang, Y. P.; Sun, Y. P. Biodistribution of pristine single-walled carbon nanotubes in vivo. J. Phys. Chem. 2007, 111, 17761-17764. (Pubitemid 350279908)
43. Thomas, C. E.; Ehrhardt, A.; Kay, M. A. Progress and problems with the use of viral vectors for gene therapy. Nat. Rev. Genet. 2003, 4, 346-358. (Pubitemid 36538359)
44. Fu, K.; Huang, W.; Lin, Y.; Zhang, D.; Hanks, T. W.; Rao, A. M.; Sun, Y. P. Functionalization of carbon nanotubes with bovine serum albumin in homogeneous aqueous soultions. J. Nanosci. Nanotech. 2002, 2, 457-461. (Pubitemid 135713073)
45. Meng, J.; Song, L.; Xu, H.; Kong, H.; Wang, C.; Guo, X.; Xie, S. Effect of single-walled carbon nanotubes on the functions of plasma proteins and potentials in vascular prostheses. Nanomed. Nanotechnol. Biol. and Med. 2005, 1, 136-142. (Pubitemid 43963617)