Carbon nanotubes enhance CpG uptake and potentiate antiglioma immunity

Clinical Cancer Research

Volumn 17, Issue 4, 2011, Pages 771-782

  Zhao, Dongchang ^a   Alizadeh, Darya ^a   Zhang, Leying ^a   Liu, Wei ^b   Farrukh, Omar ^a   Manuel, Edwin ^a   Diamond, Don J ^a   Badie, Behnam ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; CYTOKINE; SINGLE WALLED NANOTUBE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER REGRESSION; CANCER SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG POTENCY; DRUG UPTAKE; FEMALE; FLOW CYTOMETRY; GLIOMA; IMMUNE RESPONSE; IMMUNOPOTENTIATION; IMMUNOSTIMULATION; IN VITRO STUDY; INTERNALIZATION; INTRACRANIAL TUMOR; LOW DRUG DOSE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR IMMUNITY; TUMOR REGRESSION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BRAIN NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHEMOKINES; CPG ISLANDS; CYTOKINES; FEMALE; GLIOMA; HUMANS; KILLER CELLS, NATURAL; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROGLIA; MONOCYTES; NANOCONJUGATES; NANOTUBES, CARBON; NEOPLASM TRANSPLANTATION; POLYNUCLEOTIDES; TOLL-LIKE RECEPTOR 9; TRANSPLANTATION, HETEROLOGOUS; TUMOR MICROENVIRONMENT;

EID: 79951842455     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-2444     Document Type: Article

References (51)

1. Gomez GG, Kruse CA. Mechanisms of malignant glioma immune resistance and sources of immunosuppression. Gene Ther Mol Biol 2006;10:133-46. (Pubitemid 351976185)
2. Carpentier A, Laigle-Donadey F, Zohar S, Capelle L, Behin A, Tibi A, et al. Phase 1 trial of a CpG oligodeoxynucleotide for patients with recurrent glioblastoma. Neuro Oncol 2006;8:60-6. (Pubitemid 43154452)
3. Dalpke AH, Schafer MK, Frey M, Zimmermann S, Tebbe J, Weihe E, et al. Immunostimulatory CpG-DNA activates murine microglia. J Immunol 2002;168:4854-63. (Pubitemid 34495946)
4. El Andaloussi A, Sonabend AM, Han Y, Lesniak MS. Stimulation of TLR9 with CpG ODN enhances apoptosis of glioma and prolongs the survival of mice with experimental brain tumors. Glia 2006;54:526-35. (Pubitemid 44449333)
5. Vollmer J, Krieg AM. Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv Drug Deliv Rev 2009;61:195-204.
6. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004;173:3916-24. (Pubitemid 39280755)
7. Carpentier AF, Auf G, Delattre JY. CpG-oligonucleotides for cancer immunotherapy: review of the literature and potential applications in malignant glioma. Front Biosci 2003;8:e115-27.
8. Carpentier A, Metellus P, Ursu R, Zohar S, Lafitte F, Barrié M, et al. Intracerebral administration of CpG oligonucleotide for patients with recurrent glioblastoma: a phase II study. Neuro Oncol 2010;12:401-8.
9. Bianco A, Hoebeke J, Kostarelos K, Prato M, Partidos CD. Carbon nanotubes: on the road to deliver. Curr Drug Deliv 2005;2:253-9. (Pubitemid 40943997)
10. Pulskamp K, Diabate S, Krug HF. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol Lett 2007;168:58-74. (Pubitemid 44909723)
11. Schipper ML, Nakayama-Ratchford N, Davis CR, Kam NW, Chu P, Liu Z, et al. A pilot toxicology study of single-walled carbon nanotubes in a small sample of mice. Nat Nano 2008;3:216-21. (Pubitemid 351506336)
12. VanHandel M, Alizadeh D, Zhang L, et al. Selective uptake of multiwalled carbon nanotubes by tumor macrophages in a murine glioma model. J Neuroimmunol 2009;208:3-9.
13. McDevitt MR, Chattopadhyay D, Kappel BJ, et al. Tumor targeting with antibody-functionalized, radiolabeled carbon nanotubes. J Nucl Med 2007;48:1180-9. (Pubitemid 47052659)
14. Singh R, Pantarotto D, Lacerda L, et al. Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. Proc Natl Acad Sci U S A 2006;103:3357-62. (Pubitemid 43346474)
15. Wang H, Wang J, Deng X, Sun H, Shi Z, Gu Z, et al. Biodistribution of carbon single-wall carbon nanotubes in mice. J Nanosci Nanotechnol 2004;4:1019-24. (Pubitemid 40056461)
16. Liu Z, Cai W, He L, Nakayama N, Chen K, Sun X, et al. In vivo biodistribution and highly efficient tumour targeting of carbon nanotubes in mice. Nat Nanotechnol 2007;2:47-52.
17. Villa CH, McDevitt MR, Escorcia FE, Rey DA, Bergkvist M, Batt CA, et al. Synthesis and biodistribution of oligonucleotide-functionalized, tumor-targetable carbon nanotubes. Nano Lett 2008;8:4221-8.
18. Kateb B, Van Handel M, Zhang L, Bronikowski MJ, Manohara H, Badie B. Internalization of MWCNTs by microglia: possible application in immunotherapy of brain tumors. Neuroimage 2007;37 Suppl 1:S9-17.
19. Rosi NL, Giljohann DA, Thaxton CS, Lytton-Jean AK, Han MS, Mirkin CA. Oligonucleotide-modified gold nanoparticles for intracellular gene regulation. Science 2006;312:1027-30.
20. Daftarian P, Song GY, Ali S, Faynsod M, Longmate J, Diamond DJ, et al. Two distinct pathways of immuno-modulation improve potency of p53 immunization in rejecting established tumors. Cancer Res 2004;64:5407-14. (Pubitemid 39006563)
21. Alizadeh D, Zhang L, Brown CE, Farrukh O, Jensen MC, Badie B. Induction of anti-glioma NK cell response following multiple low-dose intracerebral CpG therapy. Clin Cancer Res 2010;16:3399-408.
22. Alizadeh D, Zhang L, Hwang J, Schluep T, Badie B. Tumor-associated macrophages are predominant carriers of cyclodextrin-based nanoparticles into gliomas. Nanomedicine 2010;6:382-90.
23. Manohara HM, Wong EW, Schlecht E, Hunt BD, Siegel PH. Carbon nanotube Schottky diodes using Ti-Schottky and Pt-Ohmic contacts for high frequency applications. Nano Lett 2005;5:1469-74. (Pubitemid 41084437)
24. Liu Z, Tabakman SM, Chen Z, Dai H. Preparation of carbon nanotube bioconjugates for biomedical applications. Nat Protoc 2009;4:1372-82.
25. Zhang L, Alizadeh D, Van Handel M, Kortylewski M, Yu H, Badie B. Stat3 inhibition activates tumor macrophages and abrogates glioma growth in mice. Glia 2009;57:1458-67.
26. Badie B, Schartner JM. Flow cytometric characterization of tumor-associated macrophages in experimental gliomas. Neurosurgery 2000;46:957-61; discussion 61-2.
27. Carpentier AF, Chen L, Maltonti F, Delattre JY. Oligodeoxynucleotides containing CpG motifs can induce rejection of a neuroblastoma in mice. Cancer Res 1999;59:5429-32. (Pubitemid 29526450)
28. Carpentier AF, Xie J, Mokhtari K, Delattre JY. Successful treatment of intracranial gliomas in rat by oligodeoxynucleotides containing CpG motifs. Clin Cancer Res 2000;6:2469-73. (Pubitemid 30399217)
29. Wu A, Oh S, Gharagozlou S, Vedi RN, Ericson K, Low WC, et al. In vivo vaccination with tumor cell lysate plus CpG oligodeoxynucleotides eradicates murine glioblastoma. J Immunother 2007;30:789-97.
30. Grauer OM, Molling JW, Bennink E, Toonen LW, Sutmuller RP, Nierkens S, et al. TLR ligands in the local treatment of established intracerebral murine gliomas. J Immunol 2008;181:6720-9.
31. Sanjuan MA, Rao N, Lai KT, Gu Y, Sun S, Fuchs A, et al. CpG-induced tyrosine phosphorylation occurs via a TLR9-independent mechanism and is required for cytokine secretion. J Cell Biol 2006;172:1057-68.
32. Wilson KD, de Jong SD, Tam YK. Lipid-based delivery of CpG oligonucleotides enhances immunotherapeutic efficacy. Adv Drug Deliv Rev 2009;61:233-42.
33. Bourquin C, Anz D, Zwiorek K, Lanz AL, Fuchs S, Weigel S, et al. Targeting CpG oligonucleotides to the lymph node by nanoparticles elicits efficient antitumoral immunity. J Immunol 2008;181:2990-8.
34. Chikh G, de Jong SD, Sekirov L, Raney SG, Kazem M, Wilson KD, et al. Synthetic methylated CpG ODNs are potent in vivo adjuvants when delivered in liposomal nanoparticles. Int Immunol 2009;21:757-67.
35. de Jong SD, Basha G, Wilson KD, Kazem M, Cullis P, Jefferies W, et al. The immunostimulatory activity of unmethylated and methylated CpG oligodeoxynucleotide is dependent on their ability to colocalize with TLR9 in late endosomes. J Immunol 2010;184:6092-102.
36. Malyala P, O'Hagan DT, Singh M. Enhancing the therapeutic efficacy of CpG oligonucleotides using biodegradable microparticles. Adv Drug Deliv Rev 2009;61:218-25.
37. Schreiber HA, Prechl J, Jiang H, Zozulya A, Fabry Z, Denes F, et al. Using carbon magnetic nanoparticles to target, track, and manipulate dendritic cells. J Immunol Methods 2010;356:47-59.
38. Krishnamachari Y, Salem AK. Innovative strategies for co-delivering antigens and CpG oligonucleotides. Adv Drug Deliv Rev 2009; 61:205-17.
39. Partidos CD, Hoebeke J, Wieckowski S, Chaloin O, Bianco A, Moreau E, et al. Immunomodulatory consequences of ODN CpG-polycation complexes. Methods 2009;49:328-33.
40. Wagner H. The sweetness of the DNA backbone drives Toll-like receptor 9. Curr Opin Immunol 2008;20:396-400.
41. Haas T, Metzger J, Schmitz F, Heit A, Müller T, Latz E, et al. The DNA sugar backbone 2' deoxyribose determines toll-like receptor 9 activation. Immunity 2008;28:315-23. (Pubitemid 351335308)
42. Yasuda K, Rutz M, Schlatter B, Metzger J, Luppa PB, Schmitz F, et al. CpG motif-independent activation of TLR9 upon endosomal translocation of "natural" phosphodiester DNA. Eur J Immunol 2006;36:431-6.
43. Raffa V, Ciofani G, Vittorio O, Riggio C, Cuschieri A. Physicochemical properties affecting cellular uptake of carbon nanotubes. Nanomedicine (Lond) 2010;5:89-97.
44. Allen BL, Kichambare PD, Gou P, Vlasova II, Kapralov AA, Konduru N, et al. Biodegradation of single-walled carbon nanotubes through enzymatic catalysis. Nano Lett 2008;8:3899-903.
45. Chou C-C, Hsiao H-Y, Hong Q-S, Chen CH, Peng YW, Chen HW, et al. Single-Walled Carbon Nanotubes Can Induce Pulmonary Injury in Mouse Model. Nano Lett 2008;8:437-45. (Pubitemid 351345996)
46. De La Zerda A, Zavaleta C, Keren S, Vaithilingam S, Bodapati S, Liu Z, et al. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat Nano 2008;3:557-62.
47. 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 U S A 2008;105:1410-5. (Pubitemid 351346531)
48. 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 Engl 2007;46:2023-7. (Pubitemid 46973660)
49. Zavaleta C, de la Zerda A, Liu Z, Keren S, Cheng Z, Schipper M, et al. Noninvasive Raman spectroscopy in living mice for evaluation of tumor targeting with carbon nanotubes. Nano Lett 2008; 8:2800-5.
50. Chakravarty P, Marches R, Zimmerman NS, Swafford AD, Bajaj P, Musselman IH, et al. Thermal ablation of tumor cells with antibody-functionalized single-walled carbon nanotubes. Proc Natl Acad Sci USA 2008;105:8697-702. (Pubitemid 351987743)
51. Al-Jamal KT, Toma FM, Yilmazer A, Ali-Boucetta H, Nunes A, Herrero MA, et al. Enhanced cellular internalization and gene silencing with a series of cationic dendron-multiwalled carbon nanotube:siRNA complexes. FASEB J 2010;24:4354-65.