Detoxifying Antitumoral Drugs via Nanoconjugation: The Case of Gold Nanoparticles and Cisplatin

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Comenge, Joan ^a,b   Sotelo, Carmen ^c   Romero, Francisco ^d   Gallego, Oscar ^e   Barnadas, Agustí ^e   Parada, Tomás García Caballero ^c   Domínguez, Fernando ^c   Puntes, Víctor F ^a,f  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INTERNATIONAL IBERIAN NANOTECHNOLOGY LABORATORY   (Portugal)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

^e HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^f INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; GOLD NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD; BRAIN; CHEMICAL BOND; CONJUGATION; CONTROLLED STUDY; DRUG DETOXIFICATION; DRUG DISTRIBUTION; DRUG RELEASE; FEMALE; HEART; HUMAN; HUMAN CELL; INTERNALIZATION; KIDNEY; LIVER; LUNG; MALE; MOUSE; NANOCONJUGATION; NONHUMAN; OVARY; PH; PROTEIN MODIFICATION; SPLEEN;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CISPLATIN; DNA, NEOPLASM; DRUG CARRIERS; ENDOCYTOSIS; GOLD; HUMANS; HYDROGEN-ION CONCENTRATION; METABOLIC DETOXICATION, DRUG; METAL NANOPARTICLES; MICE; NANOTECHNOLOGY; ORGAN SIZE; TIME FACTORS; TISSUE DISTRIBUTION; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION;

EID: 84867651637     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047562     Document Type: Article

References (100)

1. Varmus H, (2006) The New Era in Cancer Research. Science 312: 1162-1165.
2. Jain PK, El-Sayed IH, El-Sayed MA, (2007) Au nanoparticles target cancer. Nano Today 2: 18-29.
3. Davis ME, Chen Z, Shin DM, (2008) Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 7: 771-782.
4. Farokhzad OC, Langer R, (2009) Impact of Nanotechnology on Drug Delivery. ACS Nano 3: 16-20.
5. Minelli C, Lowe SB, Stevens MM, (2010) Engineering Nanocomposite Materials for Cancer Therapy. Small 6: 2336-2357.
6. Dhar S, Kolishetti N, Lippard SJ, Farokhzad OC, (2011) Targeted delivery of a cisplatin prodrug for safer and more effective prostate cancer therapy in vivo. Proceedings of the National Academy of Sciences 108: 1850-1855.
7. Farokhzad OC, Cheng J, Teply BA, Sherifi I, Jon S, et al. (2006) Targeted nanoparticle-aptamer bioconjugates for cancer chemotherapy in vivo. Proceedings of the National Academy of Sciences 103: 6315-6320.
8. Paciotti GF, Kingston DGI, Tamarkin L, (2006) Colloidal gold nanoparticles: A novel nanoparticle platform for developing multifunctional tumor-targeted drug delivery vectors. Drug Development Research 67: 47-54.
9. El-Sayed IH, Huang X, El-Sayed MA, (2005) Surface Plasmon Resonance Scattering and Absorption of anti-EGFR Antibody Conjugated Gold Nanoparticles in Cancer Diagnostics: Applications in Oral Cancer. Nano Letters 5: 829-834.
10. Meng H, Xue M, Xia T, Ji Z, Tarn DY, et al. (2011) Use of Size and a Copolymer Design Feature To Improve the Biodistribution and the Enhanced Permeability and Retention Effect of Doxorubicin-Loaded Mesoporous Silica Nanoparticles in a Murine Xenograft Tumor Model. ACS Nano 5: 4131-4144.
11. Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V, (2010) Time Evolution of the Nanoparticle Protein Corona. ACS Nano 4: 3623-3632.
12. Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, et al. (2008) Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proceedings of the National Academy of Sciences 105: 14265-14270.
13. Ojea-Jiménez I, Puntes V, (2009) Instability of Cationic Gold Nanoparticle Bioconjugates: The Role of Citrate Ions. Journal of the American Chemical Society 131: 13320-13327.
14. Borm P, Klaessig FC, Landry TD, Moudgil B, Pauluhn J, et al. (2006) Research Strategies for Safety Evaluation of Nanomaterials, Part V: Role of Dissolution in Biological Fate and Effects of Nanoscale Particles. Toxicological Sciences 90: 23-32.
15. Bastús NG, Casals E, Vázquez-Campos S, Puntes V, (2008) Reactivity of engineered inorganic nanoparticles and carbon nanostructures in biological media. Nanotoxicology 2: 99-112.
16. Ruenraroengsak P, Cook JM, Florence AT, (2010) Nanosystem drug targeting: Facing up to complex realities. Journal of Controlled Release 141: 265-276.
17. Vasir JK, Reddy MK, Labhasetwar VD, (2005) Nanosystems in drug targeting: Opportunities and challenges. Current Nanoscience 1: 47-64.
18. Takakura Y, Hashida M, (1996) Macromolecular Carrier Systems for Targeted Drug Delivery: Pharmacokinetic Considerations on Biodistribution. Pharmaceutical Research 13: 820-831.
19. Soo Choi H, Liu W, Misra P, Tanaka E, Zimmer JP, et al. (2007) Renal clearance of quantum dots. Nat Biotech 25: 1165-1170.
20. Khlebtsov N, Dykman L (2011) Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies. Chemical Society Reviews 40.
21. Sperling RA, Casals E, Comenge J, Bastus NG, Puntes VF, (2009) Inorganic Engineered Nanoparticles and Their Impact on the Immune Response. Current Drug Metabolism 10: 895-904.
22. Michel CC, Curry FE, (1999) Microvascular Permeability. Physiological Reviews 79: 703-761.
23. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K, (2000) Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. Journal of Controlled Release 65: 271-284.
24. Dreher MR, Liu W, Michelich CR, Dewhirst MW, Yuan F, et al. (2006) Tumor Vascular Permeability, Accumulation, and Penetration of Macromolecular Drug Carriers. Journal of the National Cancer Institute 98: 335-344.
25. Dou H, Destache CJ, Morehead JR, Mosley RL, Boska MD, et al. (2006) Development of a macrophage-based nanoparticle platform for antiretroviral drug delivery. Blood 108: 2827-2835.
26. Bastús NG, Sánchez-Tilló E, Pujals S, Farrera C, López C, et al. (2009) Homogeneous Conjugation of Peptides onto Gold Nanoparticles Enhances Macrophage Response. ACS Nano 3: 1335-1344.
27. Owens Iii DE, Peppas NA, (2006) Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. International Journal of Pharmaceutics 307: 93-102.
28. Murphy CJ, Gole AM, Stone JW, Sisco PN, Alkilany AM, et al. (2008) Gold Nanoparticles in Biology: Beyond Toxicity to Cellular Imaging. Accounts of Chemical Research 41: 1721-1730.
29. Ghosh P, Han G, De M, Kim CK, Rotello VM, (2008) Gold nanoparticles in delivery applications. Advanced Drug Delivery Reviews 60: 1307-1315.
30. Han G, Ghosh P, Rotello VM, (2007) Functionalized gold nanoparticles for drug delivery. Nanomedicine 2: 113-123.
31. El-Sayed IH, Huang X, El-Sayed MA, (2006) Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles. Cancer Letters 239: 129-135.
32. Thakor AS, Jokerst J, Zavaleta C, Massoud TF, Gambhir SS, (2011) Gold Nanoparticles: A Revival in Precious Metal Administration to Patients. Nano Letters 11: 4029-4036.
33. Jose Ruben M, Jose Luis E, Alejandra C, Katherine H, Juan BK, et al. (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16: 2346.
34. Gupta AK, Naregalkar RR, Vaidya VD, Gupta M, (2007) Recent advances on surface engineering of magnetic iron oxide nanoparticles and their biomedical applications. Nanomedicine 2: 23-39.
35. Chen JP, Patil S, Seal S, McGinnis JF, (2006) Rare earth nanoparticles prevent retinal degeneration induced by intracellular peroxides. Nature Nanotechnology 1: 142-150.
36. Niu JL, Azfer A, Rogers LM, Wang XH, Kolattukudy PE, (2007) Cardioprotective effects of cerium oxide nanoparticles in a transgenic murine model of cardiomyopathy. Cardiovascular Research 73: 549-559.
37. Rosenberg B, Vancamp L, Trosko JE, Mansour VH, (1969) Platinum Compounds: a New Class of Potent Antitumour Agents. Nature 222: 385-386.
38. Wang D, Lippard SJ, (2005) Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 4: 307-320.
39. Jung Y, Lippard SJ, (2007) Direct Cellular Responses to Platinum-Induced DNA Damage. Chemical Reviews 107: 1387-1407.
40. Kelland L, (2007) The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 7: 573-584.
41. Reedijk J, (2003) New clues for platinum antitumor chemistry: Kinetically controlled metal binding to DNA. Proceedings of the National Academy of Sciences of the United States of America 100: 3611-3616.
42. Oliver TG, Mercer KL, Sayles LC, Burke JR, Mendus D,et al. Chronic cisplatin treatment promotes enhanced damage repair and tumor progression in a mouse model of lung cancer. Genes & Development 24: 837-852.
43. Graham MA, Lockwood GF, Greenslade D, Brienza S, Bayssas M, et al. (2000) Clinical Pharmacokinetics of Oxaliplatin: A Critical Review. Clinical Cancer Research 6: 1205-1218.
44. Perrault SD, Walkey C, Jennings T, Fischer HC, Chan WCW, (2009) Mediating Tumor Targeting Efficiency of Nanoparticles Through Design. Nano Letters 9: 1909-1915.
45. Zhang G, Yang Z, Lu W, Zhang R, Huang Q, et al. (2009) Influence of anchoring ligands and particle size on the colloidal stability and in vivo biodistribution of polyethylene glycol-coated gold nanoparticles in tumor-xenografted mice. Biomaterials 30: 1928-1936.
46. DeConti RC, Toftness BR, Lange RC, Creasey WA, (1973) Clinical and Pharmacological Studies with cis-Diamminedichloroplatinum(II). Cancer Research 33: 1310-1315.
47. Peleg-Shulman T, Najajreh Y, Gibson D, (2002) Interactions of cisplatin and transplatin with proteins: Comparison of binding kinetics, binding sites and reactivity of the Pt-protein adducts of cisplatin and transplatin towards biological nucleophiles. Journal of Inorganic Biochemistry 91: 306-311.
48. Moreno D, Zalba S, Navarro I, Tros de Ilarduya C, Garrido MJ, (2010) Pharmacodynamics of cisplatin-loaded PLGA nanoparticles administered to tumor-bearing mice. Eur J Pharm Biopharm 74: 265-274.
49. Cheng L, Jin C, Lv W, Ding Q, Han X, (2011) Developing a Highly Stable PLGA-mPEG Nanoparticle Loaded with Cisplatin for Chemotherapy of Ovarian Cancer. PLoS ONE 6: e25433.
50. Burger KNJ, Staffhorst RWHM, de Vijlder HC, Velinova MJ, Bomans PH, et al. (2002) Nanocapsules: lipid-coated aggregates of cisplatin with high cytotoxicity. Nat Med 8: 81-84.
51. Access Pharma website. Available: http://www.accesspharma.com/downloads/product-programs/ProLindac-Fact-Sheet.pdf. Accessed: 2012 Sep 20.
52. Feazell RP, Nakayama-Ratchford N, Dai H, Lippard SJ, (2007) Soluble Single-Walled Carbon Nanotubes as Longboat Delivery Systems for Platinum(IV) Anticancer Drug Design. Journal of the American Chemical Society 129: 8438-8439.
53. Ajima K, Murakami T, Mizoguchi Y, Tsuchida K, Ichihashi T, et al. (2008) Enhancement of In Vivo Anticancer Effects of Cisplatin by Incorporation Inside Single-Wall Carbon Nanohorns. ACS Nano 2: 2057-2064.
54. Cheng K, Peng S, Xu C, Sun S, (2009) Porous Hollow Fe3O4 Nanoparticles for Targeted Delivery and Controlled Release of Cisplatin. Journal of the American Chemical Society 131: 10637-10644.
55. Craig GE, Brown SD, Lamprou DA, Graham D, Wheate NJ, (2012) Cisplatin-Tethered Gold Nanoparticles That Exhibit Enhanced Reproducibility, Drug Loading, and Stability: a Step Closer to Pharmaceutical Approval? Inorganic Chemistry 51: 3490-3497.
56. Dhar S, Daniel WL, Giljohann DA, Mirkin CA, Lippard SJ, (2009) Polyvalent Oligonucleotide Gold Nanoparticle Conjugates as Delivery Vehicles for Platinum(IV) Warheads. Journal of the American Chemical Society 131: 14652-14653.
57. Huang X-L, Zhang B, Ren L, Ye S-F, Sun L-P, et al. (2008) In vivo toxic studies and biodistribution of near infrared sensitive Au-Au2S nanoparticles as potential drug delivery carriers. Journal of Materials Science-Materials in Medicine 19: 2581-2588.
58. Ren L, Chow GM, (2003) Synthesis of nir-sensitive Au-Au2S nanocolloids for drug delivery. Materials Science and Engineering: C 23: 113-116.
59. Ren L, Huang X-L, Zhang B, Sun L-P, Zhang Q-Q, et al. (2008) Cisplatin-loaded Au-Au2S nanoparticles for potential cancer therapy: Cytotoxicity, in vitro carcinogenicity, and cellular uptake. Journal of Biomedical Materials Research Part A 85A: 787-796.
60. Comenge J, Romero FM, Sotelo C, Dominguez F, Puntes V, (2010) Exploring the binding of Pt drugs to gold nanoparticles for controlled passive release of cisplatin. J Control Release 148: e31-32.
61. Bastu?s NG, Comenge J, Puntes Vc, (2011) Kinetically Controlled Seeded Growth Synthesis of Citrate-Stabilized Gold Nanoparticles of up to 200 nm: Size Focusing versus Ostwald Ripening. Langmuir 27: 11098-11105.
62. Nel AE, Madler L, Velegol D, Xia T, Hoek EMV, et al. (2009) Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 8: 543-557.
63. Griset AP, Walpole J, Liu R, Gaffey A, Colson YL, et al. (2009) Expansile Nanoparticles: Synthesis, Characterization, and in Vivo Efficacy of an Acid-Responsive Polymeric Drug Delivery System. Journal of the American Chemical Society 131: 2469-2471.
64. Mikhail AS, Allen C, (2009) Block copolymer micelles for delivery of cancer therapy: Transport at the whole body, tissue and cellular levels. Journal of Controlled Release 138: 214-223.
65. Bishop KJM, Grzybowski BA, (2007) "Nanoions": Fundamental Properties and Analytical Applications of Charged Nanoparticles. ChemPhysChem 8: 2171-2176.
66. Kelland LR, Farrell N (2000) Platinum-Based Drugs in Cancer Therapy: Humana Press Inc.
67. Sonavane G, Tomoda K, Makino K, (2008) Biodistribution of colloidal gold nanoparticles after intravenous administration: Effect of particle size. Colloids and Surfaces B: Biointerfaces 66: 274-280.
68. Amigo JM, Bastús NG, Hoen R, Vázquez-Campos S, Varón M, et al. (2011) Analysis of time-dependent conjugation of gold nanoparticles with an antiparkinsonian molecule by using curve resolution methods. Analytica Chimica Acta 683: 170-177.
69. Kim B, Han G, Toley BJ, Kim C-k, Rotello VM, et al. (2010) Tuning payload delivery in tumour cylindroids using gold nanoparticles. Nat Nano 5: 465-472.
70. Jabr-Milane LS, van Vlerken LE, Yadav S, Amiji MM, (2008) Multi-functional nanocarriers to overcome tumor drug resistance. Cancer Treatment Reviews 34: 592-602.
71. Sinha R, Kim GJ, Nie S, Shin DM, (2006) Nanotechnology in cancer therapeutics: bioconjugated nanoparticles for drug delivery. Molecular Cancer Therapeutics 5: 1909-1917.
72. Madaan A, Singh P, Awasthi A, Verma R, Singh A, et al. (2012) Efficiency and mechanism of intracellular paclitaxel delivery by novel nanopolymer-based tumor-targeted delivery system, NanoxelTM. Clinical and Translational Oncology: 1-7.
73. Moghimi SM, Hunter AC, Murray JC, (2001) Long-Circulating and Target-Specific Nanoparticles: Theory to Practice. Pharmacological Reviews 53: 283-318.
74. Rehemtulla A, Stegman LD, Cardozo SJ, Gupta S, Hall DE, et al. (2000) Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2: 491-495.
75. Dreher MR, Chilkoti A, (2007) Toward a systems engineering approach to cancer drug delivery. J Natl Cancer Inst 99: 983-985.
76. Ruenraroengsak P, Cook JM, Florence AT Nanosystem drug targeting: Facing up to complex realities. Journal of Controlled Release 141: 265-276.
77. Minchinton AI, Tannock IF, (2006) Drug penetration in solid tumours. Nat Rev Cancer 6: 583-592.
78. Nam J, Won N, Jin H, Chung H, Kim S, (2009) pH-Induced Aggregation of Gold Nanoparticles for Photothermal Cancer Therapy. Journal of the American Chemical Society 131: 13639-13645.
79. Chithrani DB, Jelveh S, Jalali F, van Prooijen M, Allen C,et al. Gold Nanoparticles as Radiation Sensitizers in Cancer Therapy. Radiation Research 173: 719-728.
80. McMahon SJ, Hyland WB, Muir MF, Coulter JA, Jain S, et al. (2011) Biological consequences of nanoscale energy deposition near irradiated heavy atom nanoparticles. Sci Rep 1: 18, 19 pp.
81. Arvizo RR, Miranda OR, Moyano DF, Walden CA, Giri K, et al. (2011) Modulating Pharmacokinetics, Tumor Uptake and Biodistribution by Engineered Nanoparticles. PLoS ONE 6: e24374.
82. Cho W-S, Cho M, Jeong J, Choi M, Cho H-Y, et al. (2009) Acute toxicity and pharmacokinetics of 13 nm-sized PEG-coated gold nanoparticles. Toxicology and Applied Pharmacology 236: 16-24.
83. Lipka J, Semmler-Behnke M, Sperling RA, Wenk A, Takenaka S, et al. (2010) Biodistribution of PEG-modified gold nanoparticles following intratracheal instillation and intravenous injection. Biomaterials 31: 6574-6581.
84. Lynch I, Salvati A, Dawson KA, (2009) Protein-nanoparticle interactions: What does the cell see? Nat Nano 4: 546-547.
85. Mehta D, Bhattacharya J, Matthay MA, Malik AB, (2004) Integrated control of lung fluid balance. American Journal of Physiology-Lung Cellular and Molecular Physiology 287: L1081-L1090.
86. Heckel K, Kiefmann R, Dorger M, Stoeckelhuber M, Goetz AE, (2004) Colloidal gold particles as a new in vivo marker of early acute lung injury. American Journal of Physiology-Lung Cellular and Molecular Physiology 287: L867-L878.
87. Kato T, Yashiro T, Murata Y, Herbert DC, Oshikawa K, et al. (2003) Evidence that exogenous substances can be phagocytized by alveolar epithelial cells and transported into blood capillaries. Cell and Tissue Research 311: 47-51.
88. Bajaj G, Yeo Y Drug Delivery Systems for Intraperitoneal Therapy. Pharmaceutical Research 27: 735-738.
89. Lu H, Li B, Kang Y, Jiang W, Huang Q, et al. (2007) Paclitaxel nanoparticle inhibits growth of ovarian cancer xenografts and enhances lymphatic targeting. Cancer Chemotherapy and Pharmacology 59: 175-181.
90. Vickers AEM, Rose K, Fisher R, Saulnier M, Sahota P, et al. (2004) Kidney Slices of Human and Rat to Characterize Cisplatin-Induced Injury on Cellular Pathways and Morphology. Toxicologic Pathology 32: 577-590.
91. Miller RP, Tadagavadi RK, Ramesh G, Reeves WB, (2010) Mechanisms of Cisplatin Nephrotoxicity. Toxins 2: 2490-2518.
92. Khlebtsov N, Dykman L, (2011) Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies. Chemical Society Reviews 40: 1647-1671.
93. Lasagna-Reeves C, Gonzalez-Romero D, Barria MA, Olmedo I, Clos A, et al. (2010) Bioaccumulation and toxicity of gold nanoparticles after repeated administration in mice. Biochemical and Biophysical Research Communications 393: 649-655.
94. (2011) Size-dependent in vivo toxicity of PEG-coated gold nanoparticles Journal: International Journal of Nanomedicine Volume: 6 Issue: 1 Pages: 2071-2081 Date: 20 September 2011 Short Title: Size-dependent in vivo toxicity of PEG coated gold nanoparticles.
95. Abdelhalim M, Jarrar B, (2011) Gold nanoparticles administration induced prominent inflammatory, central vein intima disruption, fatty change and Kupffer cells hyperplasia. Lipids in Health and Disease 10: 133.
96. Zhang X-D, Wu H-Y, Wu D, Wang Y-Y, Chang J-H, et al. (2010) Toxicologic effects of gold nanoparticles in vivo by different administration routes. International Journal of Nanomedicine 5: 771-781.
97. Chen Y-S, Hung Y-C, Liau I, Huang G, (2009) Assessment of the In Vivo Toxicity of Gold Nanoparticles. Nanoscale Research Letters 4: 858-864.
98. Simpson CA, Huffman BJ, Gerdon AE, Cliffel DE, (2010) Unexpected Toxicity of Monolayer Protected Gold Clusters Eliminated by PEG-Thiol Place Exchange Reactions. Chemical Research in Toxicology 23: 1608-1616.
99. Pujals S, Bastús NG, Pereiro E, López-Iglesias C, Puntes VF, et al. (2009) Shuttling Gold Nanoparticles into Tumoral Cells with an Amphipathic Proline-Rich Peptide. ChemBioChem 10: 1025-1031.
100. Tseng C-L, Su W-Y, Yen K-C, Yang K-C, Lin F-H, (2009) The use of biotinylated-EGF-modified gelatin nanoparticle carrier to enhance cisplatin accumulation in cancerous lungs via inhalation. Biomaterials 30: 3476-3485.