Nanosomes carrying doxorubicin exhibit potent anticancer activity against human lung cancer cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Srivastava, Akhil ^a,b   Amreddy, Narsireddy ^a,b   Babu, Anish ^a,b   Panneerselvam, Janani ^a,b   Mehta, Meghna ^a,b   Muralidharan, Ranganayaki ^a,b   Chen, Allshine ^b   Zhao, Yan Daniel ^b   Razaq, Mohammad ^a,b   Riedinger, Natascha ^c   Kim, Hogyoung ^d   Liu, Shaorong ^b   Wu, Si ^b   Abdel Mageed, Asim B ^d   Munshi, Anupama ^a,b   Ramesh, Rajagopal ^a,b  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c OKLAHOMA STATE UNIVERSITY   (United States)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 9; DOXORUBICIN; METAL NANOPARTICLE; REACTIVE OXYGEN METABOLITE;

CELL DEATH; CHEMISTRY; CORONARY BLOOD VESSEL; DNA DAMAGE; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG RELEASE; ENZYME ACTIVATION; EXOSOME; FIBROBLAST; HUMAN; KINETICS; LUNG TUMOR; METABOLISM; MITOCHONDRION; MUSCLE CELL; PATHOLOGY; TUMOR CELL LINE; ULTRASTRUCTURE;

ANTINEOPLASTIC AGENTS; CASPASE 9; CELL DEATH; CELL LINE, TUMOR; CORONARY VESSELS; DNA DAMAGE; DOXORUBICIN; DRUG DELIVERY SYSTEMS; DRUG LIBERATION; ENZYME ACTIVATION; EXOSOMES; FIBROBLASTS; HUMANS; KINETICS; LUNG NEOPLASMS; METAL NANOPARTICLES; MITOCHONDRIA; MUSCLE CELLS; REACTIVE OXYGEN SPECIES;

EID: 85006043524     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep38541     Document Type: Article

References (52)

1. Urruticoechea, A. et al. Recent advances in cancer therapy: an overview. Curr. Pharm. Des. 16, 3-10 (2010).
2. Dy, G. K., Haluska, P., Adjei, A. A. Novel pharmacological agents in clinical development for solid tumors. Expert Opin. Investig. Drugs 10, 2059-2088 (2001).
3. Adjei, A. A., Rowinsky, E. K. Novel anticancer agents in clinical development. Cancer Biol. Ther. 4 Suppl 1, S5-15 (2003).
4. Jaracz, S., Chen, J., Kuznetsova, L. V., Ojima, I. Recent advances in tumor-targeting anticancer drug conjugates. Bioorg. Med. Chem. 13, 5043-5054 (2005).
5. Narvekar, M. H., Xue, J. Y., Eoh, Y., Lum, H. Nanocarrier for poorly water-soluble anticancer drugs-barriers of translation and solutions. AAPS Pharm. SciTech. 15, 822-833 (2014).
6. Mehrotra, N., Tripathi, R. M. Short interfering RNA therapeutics: nanocarriers, prospects and limitations. IET Nanobiotechnol. 9, 386-395 (2015).
7. Chen, Z. G. Small-molecule delivery by nanoparticles for anticancer therapy. Trends Mol. Med. 16, 594-602 (2010).
8. Babu, A., Templeton, A. K., Munshi, A., Ramesh, R. Nanodrug delivery systems: a promising technology for detection, diagnosis, and treatment of cancer. AAPS Pharm. SciTech. 15, 709-721 (2014).
9. Arias, J. L., Clares, B., Morales, M. E., Gallardo, V., Ruiz, M. A. Lipid-based drug delivery systems for cancer treatment. Curr. Drug Targets 12, 1151-1165 (2011).
10. Chen, S. et al. Inorganic nanomaterials as carriers for drug delivery. J. Biomed. Nanotechnol. 12, 1-27 (2016).
11. Wicki, A., Witzigmann, D., Balasubramanian, V., Huwyler, J. Nanomedicine in cancer therapy: challenges, opportunities, and clinical applications. J. Control. Release 200, 138-157 (2015).
12. Srivastava, A. et al. Exosomes: a role for naturally occurring nanovesicles in cancer growth, diagnosis and treatment. Curr. Gene Ther. 15, 182-189 (2015).
13. Théry, C., Zitvogel, L., Amigorena, S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579 (2002).
14. Thakur, B. K. et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 24, 766-769 (2014).
15. Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol. 9, 654-659 (2007).
16. Raiborg, C., Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452 (2009).
17. Raposo, G., Stoorvogel, W. Extracellular vesicles: Exosomes, microvesicles, and friends. J. Cell Biol. 200, 373-383 (2013).
18. Colombo, M., Raposo, G. A., Théry, C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Ann. Rev. Cell Dev. Biol. 30, 255-289 (2014).
19. Sun D. et al. A novel nanoparticle drug delivery system: The anti-inflammatory activity of Curcumin is enhanced when encapsulated in exosomes. Mol. Ther. 18, 1606-1614 (2010).
20. Alhasan, A. H., Patel, P. C., Choi, C. H., Mirkin, C. A. Exosome encased spherical nucleic acid gold nanoparticle conjugates as potent microRNA regulation agents. Small 10, 186-192 (2014).
21. Alvarez-Erviti, L. et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 29, 341-345 (2011).
22. Jain, S., Hirst, D. G., O'Sullivan, J. M. Gold nanoparticles as novel agents for cancer therapy. Br. J. Radiol. 85, 101-113 (2012).
23. Amreddy, N. et al. Tumor-targeted and pH-controlled delivery of doxorubicin using gold nanorods for lung cancer therapy. Int. J. Nanomedicine 10, 6773-6788 (2015).
24. Shah, M., Badwaik, V. D., Dakshinamurthy, R. Biological applications of gold nanoparticles. J. Nanosci. Nanotechnol. 14, 344-362 (2014).
25. Narsireddy, A., Anjaneyulu, K., Basak, P., Rao, N. M., Manorama, S. V. A simple approach to the design and functionalization of Fe3O4-Au nanoparticles for biomedical applications. ChemPlus Chem 77, 284-292 (2012).
26. Patra, C. R., Bhattacharya, R., Mukhopadhyay, D., Mukherjee, P. Fabrication of gold nanoparticles for targeted therapy in pancreatic cancer, Adv Drug Deliv Rev. 62, 346-361 (2010).
27. Heo, D. N. et al. Gold nanoparticles surface-functionalized with paclitaxel drug and biotin receptor as theranostic agents for cancer therapy. Biomaterials 3, 856-866 (2012).
28. Narsireddy, A., Vijayashree, K., Irudayaraj, J., Manorama, S. V., Rao, N. M. Targeted in vivo photodynamic therapy with epidermal growth factor receptor-specific peptide linked nanoparticles. Int. J. Pharm. 417, 421-429 (2014).
29. Théry, C., Amigorena, S., Raposo, G., Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3:Unit 3. 22 (2006).
30. Turkevich, J., Stevenson, P. C., Hillier, J. A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss Faraday Soc. 11, 55-75 (1951).
31. Muralidharan, R. et al. Folate receptor-targeted nanoparticle delivery of HuR-RNAi suppresses lung cancer cell proliferation and migration. J. Nanobiotechnology 1, doi: 10. 1186/s12951-016-0201-1 (2016).
32. Mehta, M. et al. Silencing of HuR radiosensitizes human TNBC cells by eliciting oxidative stress and DNA damage. Oncotarget., doi: 10. 18632/oncotarget. 11706 (2016).
33. Lötvall, J. et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J. Extracell. Vesicles 3, 26913 (2014).
34. Cruet-Hennequart, C. et al. Doxorubicin induces the DNA damage response in cultured human mesenchymal stem cells. Int. J. Hematol. 5, 649-656 (2012).
35. Wang, I. K., Lin-Shiau, S. Y., Lin, J. K. Induction of apoptosis by apigenin and related flavonoids through cytochrome c release and activation of Caspase-9 and Caspase-3 in Leukaemia HL-60 Cells. Eur. J. Cancer 35, 1517-1525 (2010).
36. Würstle, M. L., Laussmann, M. A., Rehm, M. The central role of initiator caspase-9 in apoptosis signal transduction and the regulation of its activation and activity on the apoptosome. Exp Cell Res. 11, 1213-1220 (2012).
37. Fragkos, M., Jurvansuu, J., Beard, P. H2AX is Required for cell cycle arrest via the p53/p21 pathway. Mol. Cell Biol. 10, 2828-2840 (2009).
38. Olive, P. L., Banáth, J. P. The comet assay: a method to measure DNA damage in individual cells. Nat. Protoc. 1 23-29 (2006).
39. Khiati, S. et al. Mitochondrial topoisomerase I (Top1mt) is a novel limiting factor of doxorubicin cardiotoxicity. Clin. Cancer Res. 18, 4873-4881 (2014).
40. Deavall, D. G. Martin, E. A., Horner, J. M., Roberts, R. Drug-induced oxidative stress and toxicity. J. of Toxicol. 2012, doi: 10.1155/2012/645460 (2012).
41. Takemura, G., Fujiwara, H. Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog. Cardiovasc. Dis. 49, 330-352 (2007).
42. Volkova, M., Russell, R. Anthracycline cardiotoxicity: prevalence, pathogenesis and treatment. Curr. Cardiol. Rev. 4, 214-220 (2011).
43. Kim, M. S. et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine 3, 655-664 (2016).
44. Tian, Y. et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials 35, 2383-2390 (2014).
45. Pascucci, L. et al. Paclitaxel is incorporated by mesenchymal stromal cells and released in exosomes that inhibit in vitro tumor growth: A new approach for drug delivery. J. Control. Release 192, 262-270 (2014).
46. Srivastava, A. et al. Exploitation of exosomes as nanocarriers for gene-, chemo-, and immune-therapy of cancer. J. Biomed. Nanotechnol. 6 1159-1173 (2016).
47. Clayton, A. et al. Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J. 9, 977-989 (2004).
48. Parolini, I. et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 49, 34211-34522 (2009).
49. Hood, J. L., Scott, M. J., Wickline, S. A. Maximizing exosome colloidal stability following electroporation. Anal. Biochem. 448, 41-49 (2014).
50. Hung, M. E., Leonard, J. N. Stabilization of exosome-targeting peptides via engineered glycosylation. J. Biol. Chem. 13, 8166-8172 (2015).
51. Toffoli, G. et al. Exosomal doxorubicin reduces the cardiac toxicity of doxorubicin, Nanomedicine 10, 2963-2971 (2015).
52. Saari, H. et al. Microvesicle-and exosome-mediated drug delivery enhances the cytotoxicity of Paclitaxel in autologous prostate cancer cells. J. Control. Release 220, 727-737 (2015).