A versatile, stimulus-responsive nanoparticle-based platform for use in both sonodynamic and photodynamic cancer therapy

N Nomikou, K Curtis, C McEwan, Barry O'Hagan, Bridgeen Callan, J Callan, AP McHale

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

A PLGA-based multifunctional biodegradable nanoparticle platform co-harboring hematoporporphyrin and indocyanine green has been developed. In vitro studies demonstrate ultrasound and light stimulated generation of cytotoxic reactive oxygen species. In vivo studies demonstrate that the ICG component facilitates nIR fluorescence imaging that demonstrates accumulation of IV- administered nanoparticles in tumours. In vivo studies also demonstrate ultrasound- and light-mediated inhibition of tumor growth in animals treated with the platform. Since the platform consists entirely of clinically-approved agents it could find use in sonodynamic- and photodynamic-based therapies for cancer.
LanguageEnglish
Pages414-421
Number of pages7
JournalActa Biomaterialia
Volume49
Early online date14 Nov 2016
DOIs
Publication statusPublished - Feb 2017

Fingerprint

Photochemotherapy
Nanoparticles
Tumors
Ultrasonics
Indocyanine Green
Light
Reactive Oxygen Species
Neoplasms
Animals
Fluorescence
Optical Imaging
Imaging techniques
Oxygen
Growth
polylactic acid-polyglycolic acid copolymer

Keywords

  • nanoparticle
  • sonodynamic
  • photodynamic
  • cancer
  • real-time
  • imaging
  • therapy

Cite this

@article{f50e8a68930d45699869831ffa6abce3,
title = "A versatile, stimulus-responsive nanoparticle-based platform for use in both sonodynamic and photodynamic cancer therapy",
abstract = "A PLGA-based multifunctional biodegradable nanoparticle platform co-harboring hematoporporphyrin and indocyanine green has been developed. In vitro studies demonstrate ultrasound and light stimulated generation of cytotoxic reactive oxygen species. In vivo studies demonstrate that the ICG component facilitates nIR fluorescence imaging that demonstrates accumulation of IV- administered nanoparticles in tumours. In vivo studies also demonstrate ultrasound- and light-mediated inhibition of tumor growth in animals treated with the platform. Since the platform consists entirely of clinically-approved agents it could find use in sonodynamic- and photodynamic-based therapies for cancer.",
keywords = "nanoparticle, sonodynamic, photodynamic, cancer, real-time, imaging, therapy",
author = "N Nomikou and K Curtis and C McEwan and Barry O'Hagan and Bridgeen Callan and J Callan and AP McHale",
note = "Reference text: 1. T.J Dougherty, G.B.Grindley, R. Fiel, K.R.Weishaupt and D.Boyle, Photodynamic therapy II. Cure of animal tumors with hematoporphyrin and light. J. Natl. Cancer Inst. 55 (1975) 115-121. 2. T.J.Dougherty, C.J. Gomer, B.W.Henderson, G.Jori,,D. Kessel, M.Korbelik, J.Moan and Q. Peng, Photodynamic Therapy, J. Natl. Cancer Inst., 90 (1998) 889-905. 3. J.R. Starkey, A.K. Rebane, M.A. Drobizhev, F. Meng, A.Gong, A. Elliott, K. McInnerney and C.W. Spangler, New two-photon activated photodynamic therapy sensitizers unduce xenograft tumor regressions after near-IR laser treatment through the body of the host mouse, Clin Cancer Res., 14 (2008) 6564-6573. 4. N. Yumita, R. Nishigaki, K. Umemura and S. Umemura, Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound. Jpn. J. Cancer Res., 80 (1989) 219-222. 5. D. Costley, C. McEwan, C. Fowley, A.P. McHale, J. Atchison, N. Nomikou and J.F. Callan, Treating cancer with sonodynamic therapy: a review, Int. J. Hyperthermia., 31 (2015) 107-117. 6. B. McCaughan, C. Rouanet, C. Fowley, N. Nomikou, A.P. McHale, P.A. McCarron and J.F. Callan, Enhanced ROS production and cell death through combined photo- and sono-activation of conventional photosensitizing drugs, Bioorg. Med. Chem. Lett., 21 (2011) 5750-5752. 7. N. Nomikou, C. Fowley, N.M. Byrne, B. McCaughan, A.P. McHale and J.F. Callan., Microbuble-sonosensitiser conjugates as therapeutics in sonodynamic therapy, Chem Commun (Camb)., 48 (2012) 8332-8334. 8. V. Torchilin, Tumor delivery of macromolecular drugs based on the EPR effect, Adv. Drug Deliv. Rev., 63 (2011) 131-135. 9. A. Master, M. Livingston and A. Sen Gupta, Photodynamic nanomedicine in the treatment of solid tumors: perspectives and challenges, J. Control. Release, 168, (2013) 88. 10. D.G. You, V.G. Deepagan, W. Um, S. Jeon, S. Son, H. Chang, H.I. Yoon, Y.W. Cho, M. Swierczewska, S. Lee, M.G. Pomper, I.C. Kwon, K. Kim and H.J.Park., ROS-generating TiO2 nanoparticles for non-invasive sonodynamic therapy of cancer, Sci. Rep., 6 (2016) DOI: 10.1038/srep23200. 11. Y.W. Chen, T.Y. Liu, P.H. Chang, P.H. Hsu, H.L. Liu, H.C. Lin and S.Y. Chen., A theranostic nrGO@MSN-ION nanocarrier developed to enhance the combination effect of sonodynamic therapy and ultrasound hyperthermia for treating tumor, 8 (2016) 12648-12657. 12. D. Mew, V. Lum, C-K Wat, G.H.N. Towers, C-H.C. Sun, R.J. Walter, W. Wright, M.W. Berns and J.G.Levy, Ability of specific monoclonal antibodies and conventional antisera conjugated to hematoporphyrin to label and kill selected cell lines subsequent to light activation. Cancer Res., 45 (1985) 4380-4386. 13. J. Moan and Q. Peng, An outline of the history of PDT in: T. Patrice (Ed), Photodynamic Therapy, Royal Society of Chemistry, Cambridge UK, (2003) 1-18. 14. Y. Zhou, X. Liang, Z. Dia. Porphyrin-loaded nanoparticles for cancer theranostics, Nanoscale, 8 (2016) 12394-12405. 15. M.S. Shive and J.M. Anderson, Biodegradation and biocompatibility of PLA and PLGA microspheres, Adv. Drug Deliv. Rev., 28 (1997) 5-24. 16. X. Zheng, D. Xing, F. Zhou, B. Wu and W.R. Chen, Indocyanine green-containing nanostructure as a near infrared dual-functional targeting probes for optical imaging and photothermal therapy, Mol Pharm., 8 (2011) 447-456. 17. N. Nomikou, C. Sterrett, C. Arthur, B. McCaughan, J.K. Callan and A.P. McHale, The effects of ultrasound and light on indocyanine-gree-treated tumour cells and tissues, ChemMedChem, 7 (2012) 1465-1471. 18. E. Ricci-Junior and J.M. Marchetti, Preparation, characterization, photocytotoxicity assay of PLGA nanoparticles containing zinc (II) phthalocyanine for photodynamic therapy use, J. Microencapsul., 23 (2006) 523-538. 19. V, Saxena and M. Sadoqi, J. Shao, Indocyanine green-loaded biodegradable nanoparticles: preparation, physicochemical characterization and in vitro release. Int. J. Pharm., 278 (2004) 293-301. 20. Y. Zheng, Y. Zhang, M. Ao, P. Zhang, H. Zhang, P. Li, L. Qing, Z. Wang and H. Ran, Hematoporphyrin encapsulated PLGA microbubbe for contrast enhanced ultrasound imaging and sonodynamic therapy. J. Microencapsul., 29 (2012) 437-444. 21. L. Chronopoulou, A. Amalfitano, C. Palocci, G. Nocca, C. Calla and A. Arcovito, Dexamethasone-loaded biopolymeric nanoparticles promote gingival fibroblasts differentiation. Biotechnol Prog., 31 (2015) 1381-1387. 22. K.Y. Win and S.S. Feng, Biomaterials, Effects of particle size and surface coating on cellular uptake of polymeric nanoparticles for oral delivery of anticancer drugs, 26 (2005) 2713-2722. 23. Y, Zhou, L. Zhai, R. Simmons and P. Zhong, Measurement of high intensity focused ultrasound fields by a fiber optic probe hydrophone. J. Acoust. Soc. Am. 120 (2006) 676-685. 24. M. Nui, Y.W. Naguib, A.M. Aldayel, Y.C. Shi, S.D. Hursting, M.A. Hersh and Z. Cui. Biodistribution and in vivo activities of tumor-associated macrophage-targeting nanoparticles incorporated with doxorubicin. Mol. Pharm. 11 (2014) 4425-4436 25. N. Alam, V. Khare, R. Dubey, A. Saneja, M. Kushwaha, G. Singh, N. Sharma, B. Chandan and P.N. Gupta, Biodegradable polymeric system for cisplatin delivery: development, in vitro characterization and investigation of toxicity profile, Mater. Sci. Eng. C. Mater. Biol. Appl., 38 (2014) 85-93. 26. Photofrin Prescribing information FDA (United States of America), http://www.accessdata.fda.gov/drugsatfda_docs/label/2011/020451s020lbl.pdf accessed June, 2016. 27. C.J. Gomer and T.J. Dougherty. Determination of [3H] and [14C] hematoporphyrin derivative distribution in malignant and normal tissue. Cancer Res., 39 (1979) 146-151. 28. B. Semete, L. Booysen, Y. Lemmer, L. Kalombo, L. Katata, J. Vershcoor and H.S. Swai, In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems, Nanomedicine, 6 (2010) 662-671 29. A.C. Souza, A.L. Nascimento, N.M. de Vasconcelos, M.S. Jeronimo, I.M. Siqueira, L. R-Santos, D.O. Cintra, L.L. Fuscaldi, O.R. Pires Junior, R. Titze-de-Almeida, M.F. Borin, S.N. Bao, O.P. Martins, V. N. Cardoso, S.O. Fernandes, M.R. Mortari, A. C. Tedesco, A.C. Amaral, M.S. Felipe and A.L. Bocca, Activity and in vivo tracking of amphotericin B loaded PLGA nanoparticles, Eur. J. Med. Chem. 95 (2015) 267-176. 30. P. Wang, C. Li, X. Wang, W. Xiong, X. Feng, Q. Liu, A.W. Leung and C. Xu, Anti-metastatic and pro-apoptotic effects elicited by combination photodynamic therapy with sonodynamic therapy on breast cancer both in vitro and in vivo, Ultrason. Sonochem. 23 (2015) 116-127. 31. C. McEwan, H. Nesbitt, D. Nicholas, O.N. Kavanagh, K. McKenna, P. Loan, I.G. Jack, A.P. McHale, J.F. Callan, Comparing the efficacy of photodynamic and sonodynamic therapy in non-melanoma and melanoma skin cancer. Bioorg. Med. Chem. 24 (2016) 3023-3028 32. H. Xu, X. Zhang, R. Han, P. Yang, H. Ma, Y. Song, Z. Lu, W. Yin, X. Wu and H. Wang, Nanoparticles in sonodynamic therapy: state of the art review, RCS Advances, 6 (2016) 50697-50705. 33. A. Sazgarnia, A. Shanei, N.T. Meibodi, H. Eshghi, H. Nassirli, Sonodynamic therapy. In vivo study on a colon tumor model. J. Ultrasound Med., 30 (2011) 1321-1329.",
year = "2017",
month = "2",
doi = "10.1016/j.actbio.2016.11.031",
language = "English",
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pages = "414--421",
journal = "Acta Biomaterialia",
issn = "1742-7061",
publisher = "Elsevier",

}

TY - JOUR

T1 - A versatile, stimulus-responsive nanoparticle-based platform for use in both sonodynamic and photodynamic cancer therapy

AU - Nomikou, N

AU - Curtis, K

AU - McEwan, C

AU - O'Hagan, Barry

AU - Callan, Bridgeen

AU - Callan, J

AU - McHale, AP

N1 - Reference text: 1. T.J Dougherty, G.B.Grindley, R. Fiel, K.R.Weishaupt and D.Boyle, Photodynamic therapy II. Cure of animal tumors with hematoporphyrin and light. J. Natl. Cancer Inst. 55 (1975) 115-121. 2. T.J.Dougherty, C.J. Gomer, B.W.Henderson, G.Jori,,D. Kessel, M.Korbelik, J.Moan and Q. Peng, Photodynamic Therapy, J. Natl. Cancer Inst., 90 (1998) 889-905. 3. J.R. Starkey, A.K. Rebane, M.A. Drobizhev, F. Meng, A.Gong, A. Elliott, K. McInnerney and C.W. Spangler, New two-photon activated photodynamic therapy sensitizers unduce xenograft tumor regressions after near-IR laser treatment through the body of the host mouse, Clin Cancer Res., 14 (2008) 6564-6573. 4. N. Yumita, R. Nishigaki, K. Umemura and S. Umemura, Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound. Jpn. J. Cancer Res., 80 (1989) 219-222. 5. D. Costley, C. McEwan, C. Fowley, A.P. McHale, J. Atchison, N. Nomikou and J.F. Callan, Treating cancer with sonodynamic therapy: a review, Int. J. Hyperthermia., 31 (2015) 107-117. 6. B. McCaughan, C. Rouanet, C. Fowley, N. Nomikou, A.P. McHale, P.A. McCarron and J.F. Callan, Enhanced ROS production and cell death through combined photo- and sono-activation of conventional photosensitizing drugs, Bioorg. Med. Chem. Lett., 21 (2011) 5750-5752. 7. N. Nomikou, C. Fowley, N.M. Byrne, B. McCaughan, A.P. McHale and J.F. Callan., Microbuble-sonosensitiser conjugates as therapeutics in sonodynamic therapy, Chem Commun (Camb)., 48 (2012) 8332-8334. 8. V. Torchilin, Tumor delivery of macromolecular drugs based on the EPR effect, Adv. Drug Deliv. Rev., 63 (2011) 131-135. 9. A. Master, M. Livingston and A. Sen Gupta, Photodynamic nanomedicine in the treatment of solid tumors: perspectives and challenges, J. Control. Release, 168, (2013) 88. 10. D.G. You, V.G. Deepagan, W. Um, S. Jeon, S. Son, H. Chang, H.I. Yoon, Y.W. Cho, M. Swierczewska, S. Lee, M.G. Pomper, I.C. Kwon, K. Kim and H.J.Park., ROS-generating TiO2 nanoparticles for non-invasive sonodynamic therapy of cancer, Sci. Rep., 6 (2016) DOI: 10.1038/srep23200. 11. Y.W. Chen, T.Y. Liu, P.H. Chang, P.H. Hsu, H.L. Liu, H.C. Lin and S.Y. Chen., A theranostic nrGO@MSN-ION nanocarrier developed to enhance the combination effect of sonodynamic therapy and ultrasound hyperthermia for treating tumor, 8 (2016) 12648-12657. 12. D. Mew, V. Lum, C-K Wat, G.H.N. Towers, C-H.C. Sun, R.J. Walter, W. Wright, M.W. Berns and J.G.Levy, Ability of specific monoclonal antibodies and conventional antisera conjugated to hematoporphyrin to label and kill selected cell lines subsequent to light activation. Cancer Res., 45 (1985) 4380-4386. 13. J. Moan and Q. Peng, An outline of the history of PDT in: T. Patrice (Ed), Photodynamic Therapy, Royal Society of Chemistry, Cambridge UK, (2003) 1-18. 14. Y. Zhou, X. Liang, Z. Dia. Porphyrin-loaded nanoparticles for cancer theranostics, Nanoscale, 8 (2016) 12394-12405. 15. M.S. Shive and J.M. Anderson, Biodegradation and biocompatibility of PLA and PLGA microspheres, Adv. Drug Deliv. Rev., 28 (1997) 5-24. 16. X. Zheng, D. Xing, F. Zhou, B. Wu and W.R. Chen, Indocyanine green-containing nanostructure as a near infrared dual-functional targeting probes for optical imaging and photothermal therapy, Mol Pharm., 8 (2011) 447-456. 17. N. Nomikou, C. Sterrett, C. Arthur, B. McCaughan, J.K. Callan and A.P. McHale, The effects of ultrasound and light on indocyanine-gree-treated tumour cells and tissues, ChemMedChem, 7 (2012) 1465-1471. 18. E. Ricci-Junior and J.M. Marchetti, Preparation, characterization, photocytotoxicity assay of PLGA nanoparticles containing zinc (II) phthalocyanine for photodynamic therapy use, J. Microencapsul., 23 (2006) 523-538. 19. V, Saxena and M. Sadoqi, J. Shao, Indocyanine green-loaded biodegradable nanoparticles: preparation, physicochemical characterization and in vitro release. Int. J. Pharm., 278 (2004) 293-301. 20. Y. Zheng, Y. Zhang, M. Ao, P. Zhang, H. Zhang, P. Li, L. Qing, Z. Wang and H. Ran, Hematoporphyrin encapsulated PLGA microbubbe for contrast enhanced ultrasound imaging and sonodynamic therapy. J. Microencapsul., 29 (2012) 437-444. 21. L. Chronopoulou, A. Amalfitano, C. Palocci, G. Nocca, C. Calla and A. Arcovito, Dexamethasone-loaded biopolymeric nanoparticles promote gingival fibroblasts differentiation. Biotechnol Prog., 31 (2015) 1381-1387. 22. K.Y. Win and S.S. Feng, Biomaterials, Effects of particle size and surface coating on cellular uptake of polymeric nanoparticles for oral delivery of anticancer drugs, 26 (2005) 2713-2722. 23. Y, Zhou, L. Zhai, R. Simmons and P. Zhong, Measurement of high intensity focused ultrasound fields by a fiber optic probe hydrophone. J. Acoust. Soc. Am. 120 (2006) 676-685. 24. M. Nui, Y.W. Naguib, A.M. Aldayel, Y.C. Shi, S.D. Hursting, M.A. Hersh and Z. Cui. Biodistribution and in vivo activities of tumor-associated macrophage-targeting nanoparticles incorporated with doxorubicin. Mol. Pharm. 11 (2014) 4425-4436 25. N. Alam, V. Khare, R. Dubey, A. Saneja, M. Kushwaha, G. Singh, N. Sharma, B. Chandan and P.N. Gupta, Biodegradable polymeric system for cisplatin delivery: development, in vitro characterization and investigation of toxicity profile, Mater. Sci. Eng. C. Mater. Biol. Appl., 38 (2014) 85-93. 26. Photofrin Prescribing information FDA (United States of America), http://www.accessdata.fda.gov/drugsatfda_docs/label/2011/020451s020lbl.pdf accessed June, 2016. 27. C.J. Gomer and T.J. Dougherty. Determination of [3H] and [14C] hematoporphyrin derivative distribution in malignant and normal tissue. Cancer Res., 39 (1979) 146-151. 28. B. Semete, L. Booysen, Y. Lemmer, L. Kalombo, L. Katata, J. Vershcoor and H.S. Swai, In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems, Nanomedicine, 6 (2010) 662-671 29. A.C. Souza, A.L. Nascimento, N.M. de Vasconcelos, M.S. Jeronimo, I.M. Siqueira, L. R-Santos, D.O. Cintra, L.L. Fuscaldi, O.R. Pires Junior, R. Titze-de-Almeida, M.F. Borin, S.N. Bao, O.P. Martins, V. N. Cardoso, S.O. Fernandes, M.R. Mortari, A. C. Tedesco, A.C. Amaral, M.S. Felipe and A.L. Bocca, Activity and in vivo tracking of amphotericin B loaded PLGA nanoparticles, Eur. J. Med. Chem. 95 (2015) 267-176. 30. P. Wang, C. Li, X. Wang, W. Xiong, X. Feng, Q. Liu, A.W. Leung and C. Xu, Anti-metastatic and pro-apoptotic effects elicited by combination photodynamic therapy with sonodynamic therapy on breast cancer both in vitro and in vivo, Ultrason. Sonochem. 23 (2015) 116-127. 31. C. McEwan, H. Nesbitt, D. Nicholas, O.N. Kavanagh, K. McKenna, P. Loan, I.G. Jack, A.P. McHale, J.F. Callan, Comparing the efficacy of photodynamic and sonodynamic therapy in non-melanoma and melanoma skin cancer. Bioorg. Med. Chem. 24 (2016) 3023-3028 32. H. Xu, X. Zhang, R. Han, P. Yang, H. Ma, Y. Song, Z. Lu, W. Yin, X. Wu and H. Wang, Nanoparticles in sonodynamic therapy: state of the art review, RCS Advances, 6 (2016) 50697-50705. 33. A. Sazgarnia, A. Shanei, N.T. Meibodi, H. Eshghi, H. Nassirli, Sonodynamic therapy. In vivo study on a colon tumor model. J. Ultrasound Med., 30 (2011) 1321-1329.

PY - 2017/2

Y1 - 2017/2

N2 - A PLGA-based multifunctional biodegradable nanoparticle platform co-harboring hematoporporphyrin and indocyanine green has been developed. In vitro studies demonstrate ultrasound and light stimulated generation of cytotoxic reactive oxygen species. In vivo studies demonstrate that the ICG component facilitates nIR fluorescence imaging that demonstrates accumulation of IV- administered nanoparticles in tumours. In vivo studies also demonstrate ultrasound- and light-mediated inhibition of tumor growth in animals treated with the platform. Since the platform consists entirely of clinically-approved agents it could find use in sonodynamic- and photodynamic-based therapies for cancer.

AB - A PLGA-based multifunctional biodegradable nanoparticle platform co-harboring hematoporporphyrin and indocyanine green has been developed. In vitro studies demonstrate ultrasound and light stimulated generation of cytotoxic reactive oxygen species. In vivo studies demonstrate that the ICG component facilitates nIR fluorescence imaging that demonstrates accumulation of IV- administered nanoparticles in tumours. In vivo studies also demonstrate ultrasound- and light-mediated inhibition of tumor growth in animals treated with the platform. Since the platform consists entirely of clinically-approved agents it could find use in sonodynamic- and photodynamic-based therapies for cancer.

KW - nanoparticle

KW - sonodynamic

KW - photodynamic

KW - cancer

KW - real-time

KW - imaging

KW - therapy

U2 - 10.1016/j.actbio.2016.11.031

DO - 10.1016/j.actbio.2016.11.031

M3 - Article

VL - 49

SP - 414

EP - 421

JO - Acta Biomaterialia

T2 - Acta Biomaterialia

JF - Acta Biomaterialia

SN - 1742-7061

ER -