Accumulated polymer degradation products as effector molecules in cytotoxicity of polymeric nanoparticles

Toxicological Sciences

Volumn 136, Issue 1, 2013, Pages 131-143

  Singh, Raman Preet ^a,b   Ramarao, Poduri ^a,c  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

^b Evalueserve SEZ (Gurgaon) Pvt Ltd   (India)

^c CENTRAL UNIVERSITY OF PUNJAB   (India)

Author keywords

Dye release; In vitro toxicity; Intracellular degradation; Nanoparticle degradation; Osmotic pressure; Poly(DL lactic acid); Poly(lactide co glycide); Poly(lactide cocaprolactone); Poly caprolactone; Polymeric nanoparticles

Indexed keywords

INTERLEUKIN 6; NANOPARTICLE; POLY(LACTIDE CO GLYCIDE); POLY(LACTIDE COCAPROLACTONE); POLYCAPROLACTONE; POLYLACTIC ACID; POLYLACTIDE; POLYMER; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BIODEGRADATION; BRAIN CELL; CELL DEATH; CELL LINE; CELL STIMULATION; CELL STRAIN HEPG2; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE PRODUCTION; CYTOTOXICITY; EPITHELIUM CELL; FLUORESCENCE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; INTERNALIZATION; KIDNEY CELL; KIDNEY EPITHELIUM; LIVER CELL; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; LYSOSOME; MACROPHAGE; MITOCHONDRIAL DYNAMICS; MOLECULE; MOUSE; NANOTOXICOLOGY; NONHUMAN; OSMOLALITY; POLYMERIZATION; TOXICOLOGICAL PARAMETERS;

DYE RELEASE; IN VITRO TOXICITY; INTRACELLULAR DEGRADATION; NANOPARTICLE DEGRADATION; OSMOTIC PRESSURE; POLY(DL-LACTIC ACID); POLY(LACTIDE-CO-GLYCIDE); POLY(LACTIDE-COCAPROLACTONE); POLY-Ε-CAPROLACTONE; POLYMERIC NANOPARTICLES;

ANIMALS; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HEP G2 CELLS; HEPATOCYTES; HUMANS; KIDNEY; LUNG; MACROPHAGES; NANOPARTICLES; NEURONS; OSMOLAR CONCENTRATION; POLYESTERS; POLYGLACTIN 910; POLYMERS; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84887962535     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft179     Document Type: Article

References (63)

1. Adair, J. H., Parette, M. P., Altinoglu, E. I., and Kester, M. (2010). Nanoparticulate alternatives for drug delivery. ACS Nano 4, 4967-4970.
2. Allen, T. M., Mumbengegwi, D. R., and Charrois, G. J. (2005). Anti-CD19-targeted liposomal doxorubicin improves the therapeutic efficacy in murine B-cell lymphoma and ameliorates the toxicity of liposomes with varying drug release rates. Clin. Cancer Res. 11, 3567-3573.
3. Antunes, F., Cadenas, E., and Brunk, U. T. (2001). Apoptosis induced by exposure to a low steady-state concentration of H2O2 is a consequence of lysosomal rupture. Biochem. J. 356(Pt 2), 549-555.
4. Barbosa, M. E. M., Cammas, S., Appel, M., and Ponchel, G. (2003). Investigation of the degradation mechanisms of poly(malic acid) esters in vitro and their related cytotoxicities on J774 macrophages. Biomacromolecules 5, 137-143.
5. Bayles, A. R., Chahal, H. S., Chahal, D. S., Goldbeck, C. P., Cohen, B. E., and Helms, B. A. (2010). Rapid cytosolic delivery of luminescent nanocrystals in live cells with endosome-disrupting polymer colloids. Nano Lett. 10, 4086-4092.
6. Brocker, C., Thompson, D. C., and Vasiliou, V. (2012). The role of hyperosmotic stress in inflammation and disease. Biomol. Concepts 3, 345-364.
7. Bussolaro, D., Filipak Neto, F., Gargioni, R., Fernandes, L. C., Randi, M. A., Pelletier, E., and Oliveira Ribeiro, C. A. (2008). The immune response of peritoneal macrophages due to exposure to inorganic lead in the house mouse Mus musculus. Toxicol. In Vitro 22, 254-260.
8. Cao, H., McHugh, K., Chew, S. Y., and Anderson, J. M. (2010). The topographical effect of electrospun nanofibrous scaffolds on the in vivo and in vitro foreign body reaction. J. Biomed. Mater. Res. A 93, 1151-1159.
9. Cartiera, M. S., Johnson, K. M., Rajendran, V., Caplan, M. J., and Saltzman, W. M. (2009). The uptake and intracellular fate of PLGA nanoparticles in epithelial cells. Biomaterials 30, 2790-2798.
10. Castino, R., Bellio, N., Nicotra, G., Follo, C., Trincheri, N. F., and Isidoro, C. (2007). Cathepsin D-Bax death pathway in oxidative stressed neuroblastoma cells. Free Radic. Biol. Med. 42, 1305-1316.
11. Chang, J., Jallouli, Y., Kroubi, M., Yuan, X. B., Feng, W., Kang, C. S., Pu, P. Y., and Betbeder, D. (2009). Characterization of endocytosis of transferrincoated PLGA nanoparticles by the blood-brain barrier. Int. J. Pharm. 379, 285-292.
12. Charrois, G. J., and Allen, T. M. (2004). Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer. Biochim. Biophys. Acta 1663, 167-177.
13. Chavanpatil, M. D., Patil, Y., and Panyam, J. (2006). Susceptibility of nanoparticle-encapsulated paclitaxel to P-glycoprotein-mediated drug efflux. Int. J. Pharm. 320, 150-156.
14. Chawla, J. S., and Amiji, M. M. (2002). Biodegradable poly(epsilon -caprolactone) nanoparticles for tumor-targeted delivery of tamoxifen. Int. J. Pharm. 249, 127-138.
15. Chernenko, T., Matthäus, C., Milane, L., Quintero, L., Amiji, M., and Diem, M. (2009). Label-free Raman spectral imaging of intracellular delivery and degradation of polymeric nanoparticle systems. ACS Nano 3, 3552-3559.
16. Clouzeau, C., Godefroy, D., Riancho, L., Rostène, W., Baudouin, C., and Brignole-Baudouin, F. (2012). Hyperosmolarity potentiates toxic effects of benzalkonium chloride on conjunctival epithelial cells in vitro. Mol. Vis. 18, 851-863.
17. Cordewener, F. W., van Geffen, M. F., Joziasse, C. A. P., Schmitz, J. P., Bos, R. R. M., Rozema, F. R., and Pennings, A. J. (2000). Cytotoxicity of poly(96L/4D-lactide): The influence of degradation and sterilization. Biomaterials 21, 2433-2442.
18. Daiber, A. (2010). Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta 1797, 897-906.
19. Das, M., Singh, R. P., Datir, S. R., and Jain, S. (2013). Surface chemistry dependent "switch" regulates the trafficking and therapeutic performance of drug-loaded carbon nanotubes. Bioconjug. Chem. 24, 626-639.
20. Deryabina, Y. I., Bazhenova, E. N., Saris, N. E., and Zvyagilskaya, R. A. (2001). Ca(2+) efflux in mitochondria from the yeast Endomyces magnusii. J. Biol. Chem. 276, 47801-47806.
21. Dinarvand, R., Sepehri, N., Manoochehri, S., Rouhani, H., and Atyabi, F. (2011). Polylactide-co-glycolide nanoparticles for controlled delivery of anticancer agents. Int. J. Nanomedicine 6, 877-895.
22. Forrest, M. L., and Kwon, G. S. (2008). Clinical developments in drug delivery nanotechnology. Adv. Drug Deliv. Rev. 60, 861-862.
23. Geys, J., Nemmar, A., Verbeken, E., Smolders, E., Ratoi, M., Hoylaerts, M. F., Nemery, B., and Hoet, P. H. (2008). Acute toxicity and prothrombotic effects of quantum dots: Impact of surface charge. Environ. Health Perspect. 116, 1607-1613.
24. Gil, P. R., Oberdörster, G., Elder, A., Puntes, V., and Parak, W. J. (2010). Correlating physico-chemical with toxicological properties of nanoparticles: The present and the future. ACS Nano 4, 5527-5531.
25. Green, J. J., Zhou, B. Y., Mitalipova, M. M., Beard, C., Langer, R., Jaenisch, R., and Anderson, D. G. (2008). Nanoparticles for gene transfer to human embryonic stem cell colonies. Nano Lett. 8, 3126-3130.
26. Harde, H., Singh, R. P., Agrawal, A. K., and Jain, S. (2013). Disease-based selection of nanocarriers in drug delivery based on hydrophobicity and surface charge. J. Nanogenomics Nanomedicine (forthcoming).
27. Jain, A. K., Swarnakar, N. K., Godugu, C., Singh, R. P., and Jain, S. (2011a). The effect of the oral administration of polymeric nanoparticles on the efficacy and toxicity of tamoxifen. Biomaterials 32, 503-515.
28. Jain, A. K., Swarnakar, N. K., Godugu, C., Singh, R. P., Ramarao, P., and Jain, S. (2011b). Augmented anticancer efficacy of doxorubicin-loaded polymeric nanoparticles after oral administration in a breast cancer induced animal model. Mol. Pharm. 8, 1140-1151.
29. Johnson, L. V., Walsh, M. L., Bockus, B. J., and Chen, L. B. (1981). Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J. Cell Biol. 88, 526-535.
30. Kamel, A. O., Awad, G. A., Geneidi, A. S., and Mortada, N. D. (2009). Preparation of intravenous stealthy acyclovir nanoparticles with increased mean residence time. AAPS PharmSciTech 10, 1427-1436.
31. Kang, S. W., Cho, E. R., Jeon, O., and Kim, B. S. (2007). The effect of microsphere degradation rate on the efficacy of polymeric microspheres as bulking agents: An 18-month follow-up study. J. Biomed. Mater. Res. B Appl. Biomater. 80, 253-259.
32. Kedar, U., Phutane, P., Shidhaye, S., and Kadam, V. (2010). Advances in polymeric micelles for drug delivery and tumor targeting. Nanomedicine 6, 714-729.
33. Kim, M. S., Ahn, H. H., Shin, Y. N., Cho, M. H., Khang, G., and Lee, H. B. (2007). An in vivo study of the host tissue response to subcutaneous implantation of PLGA-and/or porcine small intestinal submucosa-based scaffolds. Biomaterials 28, 5137-5143.
34. Kultz, D. (2004). Hyperosmolality triggers oxidative damage in kidney cells. Proc. Natl. Acad. Sci. U.S.A. 101, 9177-9178.
35. Lee, J. H., Kim, M., Im, Y. S., Choi, W., Byeon, S. H., and Lee, H. K. (2008). NFAT5 induction and its role in hyperosmolar stressed human limbal epithelial cells. Invest. Ophthalmol. Vis. Sci. 49, 1827-1835.
36. Lickorish, D., Chan, J., Song, J., and Davies, J. E. (2004). An in-vivo model to interrogate the transition from acute to chronic inflammation. Eur. Cell. Mater. 8, 12-19.
37. Lim, H. J., Masin, D., Madden, T. D., and Bally, M. B. (1997). Influence of drug release characteristics on the therapeutic activity of liposomal mitoxantrone. J. Pharmacol. Exp. Ther. 281, 566-573.
38. Lim, H. J., Masin, D., McIntosh, N. L., Madden, T. D., and Bally, M. B. (2000). Role of drug release and liposome-mediated drug delivery in governing the therapeutic activity of liposomal mitoxantrone used to treat human A431 and LS180 solid tumors. J. Pharmacol. Exp. Ther. 292, 337-345.
39. Luo, L., Li, D. Q., and Pflugfelder, S. C. (2007). Hyperosmolarity-induced apoptosis in human corneal epithelial cells is mediated by cytochrome c and MAPK pathways. Cornea 26, 452-460.
40. Mittal, G., Sahana, D. K., Bhardwaj, V., and Kumar, M. N. V. R. (2007). Estradiol loaded PLGA nanoparticles for oral administration: Effect of polymer molecular weight and copolymer composition on release behavior in vitro and in vivo. J. Control. Release 119, 77-85.
41. Mundargi, R. C., Babu, V. R., Rangaswamy, V., Patel, P., and Aminabhavi, T. M. (2008). Nano/micro technologies for delivering macromolecular therapeutics using poly(D,L-lactide-co-glycolide) and its derivatives. J. Control. Release 125, 193-209.
42. Panyam, J., Sahoo, S. K., Prabha, S., Bargar, T., and Labhasetwar, V. (2003). Fluorescence and electron microscopy probes for cellular and tissue uptake of poly(D,L-lactide-co-glycolide) nanoparticles. Int. J. Pharm. 262, 1-11.
43. Panyam, J., Zhou, W. Z., Prabha, S., Sahoo, S. K., and Labhasetwar, V. (2002). Rapid endo-lysosomal escape of poly(DL-lactide-co-glycolide) nanoparticles: Implications for drug and gene delivery. FASEB J. 16, 1217-1226.
44. Prencipe, G., Tabakman, S. M., Welsher, K., Liu, Z., Goodwin, A. P., Zhang, L., Henry, J., and Dai, H. (2009). PEG branched polymer for functionalization of nanomaterials with ultralong blood circulation. J. Am. Chem. Soc. 131, 4783-4787.
45. Ren, T., Xu, N., Cao, C., Yuan, W., Yu, X., Chen, J., and Ren, J. (2009). Preparation and therapeutic efficacy of polysorbate-80-coated amphotericin B/PLA-b-PEG nanoparticles. J. Biomater. Sci. Polym. Ed. 20, 1369-1380.
46. Ryman-Rasmussen, J. P., Riviere, J. E., and Monteiro-Riviere, N. A. (2007). Variables influencing interactions of untargeted quantum dot nanoparticles with skin cells and identification of biochemical modulators. Nano Lett. 7, 1344-1348.
47. Schwartz, L., Guais, A., Pooya, M., and Abolhassani, M. (2009). Is inflammation a consequence of extracellular hyperosmolarity? J. Inflamm. (Lond). 6, 21.
48. Severin, F. F., Severina, I. I., Antonenko, Y. N., Rokitskaya, T. I., Cherepanov, D. A., Mokhova, E. N., Vyssokikh, M. Y., Pustovidko, A. V., Markova, O. V., Yaguzhinsky, L. S., et al. (2010). Penetrating cation/fatty acid anion pair as a mitochondria-targeted protonophore. Proc. Natl. Acad. Sci. U.S.A. 107, 663-668.
49. Seyednejad, H., Ghassemi, A. H., van Nostrum, C. F., Vermonden, T., and Hennink, W. E. (2011). Functional aliphatic polyesters for biomedical and pharmaceutical applications. J. Control. Release 152, 168-176.
50. Shi, J., Votruba, A. R., Farokhzad, O. C., and Langer, R. (2010). Nanotechnology in drug delivery and tissue engineering: From discovery to applications. Nano Lett. 10, 3223-3230.
51. Singh, R. P., Das, M., Thakare, V., and Jain, S. (2012). Functionalization density dependent toxicity of oxidized multiwalled carbon nanotubes in a murine macrophage cell line. Chem. Res. Toxicol. 25, 2127-2137.
52. Singh, R. P., and Ramarao, P. (2012). Cellular uptake, intracellular trafficking and cytotoxicity of silver nanoparticles. Toxicol. Lett. 213, 249-259.
53. Sivadas, N., O'Rourke, D., Tobin, A., Buckley, V., Ramtoola, Z., Kelly, J. G., Hickey, A. J., and Cryan, S. A. (2008). A comparative study of a range of polymeric microspheres as potential carriers for the inhalation of proteins. Int. J. Pharm. 358, 159-167.
54. Sohaebuddin, S. K., Thevenot, P. T., Baker, D., Eaton, J. W., and Tang, L. (2010). Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part. Fibre Toxicol. 7, 22.
55. Swarnakar, N. K., Jain, A. K., Singh, R. P., Godugu, C., Das, M., and Jain, S. (2011). Oral bioavailability, therapeutic efficacy and reactive oxygen species scavenging properties of coenzyme Q10-loaded polymeric nanoparticles. Biomaterials 32, 6860-6874.
56. Teodoro, J. S., Simões, A. M., Duarte, F. V., Rolo, A. P., Murdoch, R. C., Hussain, S. M., and Palmeira, C. M. (2011). Assessment of the toxicity of silver nanoparticles in vitro: A mitochondrial perspective. Toxicol. In Vitro 25, 664-670.
57. Terman, A., Kurz, T., Navratil, M., Arriaga, E. A., and Brunk, U. T. (2010). Mitochondrial turnover and aging of long-lived postmitotic cells: The mitochondrial-lysosomal axis theory of aging. Antioxid. Redox Signal. 12, 503-535.
58. Tsikas, D. (2005). Methods of quantitative analysis of the nitric oxide metabolites nitrite and nitrate in human biological fluids. Free Radic. Res. 39, 797-815.
59. Uskokovic, D., and Stevanovic, M. (2009). Poly(lactide-co-glycolide)-based micro and nanoparticles for the controlled drug delivery of vitamins. Cur. Nanosc. 5, 1-14.
60. Wang, L., Liu, Y., Li, W., Jiang, X., Ji, Y., Wu, X., Xu, L., Qiu, Y., Zhao, K., Wei, T., et al. (2011). Selective targeting of gold nanorods at the mitochondria of cancer cells: Implications for cancer therapy. Nano Lett. 11, 772-780.
61. Weber, T. A., and Reichert, A. S. (2010). Impaired quality control of mitochondria: Aging from a new perspective. Exp. Gerontol. 45, 503-511.
62. Xiong, S., Li, H., Yu, B., Wu, J., and Lee, R. J. (2010). Triggering liposomal drug release with a lysosomotropic agent. J. Pharm. Sci. 99, 5011-5018.
63. Zhong, Y., Yingge, Z., Yanlian, Y., Lan, S., Dong, H., Hong, L., and Chen, W. (2010). Pharmacological and toxicological target organelles and safe use of single-walled carbon nanotubes as drug carriers in treating Alzheimer disease. Nanomedicine 6, 427-441.