Current role of nanoparticles in the treatment of lung cancer

Background. Worldwide, lung cancer is one of the leading causes of cancer death. Nevertheless, new therapeutic agents have been developed to treat lung cancer that could change this mortality-rate. Interestingly, incredible advances have occurred in recent years in the development and application of nanotechnology in the detection, diagnosis, and treatment of lung cancer.
Aim. Nanoparticles have the ability to incorporate multiple drugs and targeting agents and therefore lead to an improved bioavailability, sustained delivery, solubility, and intestinal absorption.
Relevance for patients. This review briefly summarizes the latest innovations in therapeutic nanomedicine in lung cancer with examples on magnetic, lipid and polymer nanoparticles. Emphasis will be placed on future studies and ongoing clinical trials in this field.
[1] Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 2018;68:394-424.
[2] Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2018. CA Cancer J Clin 2018;68:7-30.
[3] Rivera MP, Mehta AC, Wahidi MM. Establishing the Diagnosis of Lung Cancer: Diagnosis and Management of Lung Cancer: American College of Chest Physicians Evidence-based Clinical Practice Guidelines. Chest J 2013;143:e142S-65.
[4] Hochhegger B, Alves GR, Irion KL, Fritscher CC, Fritscher LG, Concatto NH, et al. PET/CT Imaging in Lung Cancer: Indications and Findings. J Bras Pneumol 2015;41:264-74.
[5] Kozower BD, Larner JM, Detterbeck FC, Jones DR. Special Treatment Issues in Non-Small Cell Lung Cancer: Diagnosis and Management of Lung Cancer: American College of Chest Physicians Evidence-based Clinical Practice Guidelines. Chest 2013;143:e369S-99.
[6] Ko EC, Raben D, Formenti SC. The Integration of Radiotherapy with Immunotherapy for the Treatment of Non-Small Cell Lung Cancer. Clin Cancer Res 2018;24:5792-806.
[7] Horikoshi S, Serpone N. Introduction to nanoparticles. In: Horikoshi S, Serpone N, editors. Microwaves in Nanoparticle Synthesis: Fundamentals and Applications. Weinheim, Germany: Wiley-VCH Verlag GmbH and Co. KGaA; 2013. p. 1-24.
[8] Almeida JP, Lin AY, Langsner RJ, Eckels P, Foster AE, Drezek RA. In Vivo Immune Cell Distribution of Gold Nanoparticles in Naive and Tumor Bearing Mice. Small 2014;10:812-9.
[9] Chow EK, Ho D. Cancer Nanomedicine: From Drug Delivery to Imaging. Sci Transl Med 2013;5:216rv4.
[10] Baetke SC, Lammers T, Kiessling F. Applications of Nanoparticles for Diagnosis and Therapy of Cancer. Br J Radiol 2015;88:20150207.
[11] Thanh NT, Green LA. Functionalisation of Nanoparticles for Biomedical Applications. Nano Today 2010;5:213-30.
[12] Avval ZM, Malekpour L, Raeisi F, Babapoor A, Mousavi SM, Hashemi SA, et al. Introduction of Magnetic and Supermagnetic Nanoparticles in New Approach of Targeting Drug Delivery and Cancer Therapy Application. Drug Metab Rev 2020;52:157-84.
[13] Wu K, Su D, Liu J, Saha R, Wang JP. Magnetic Nanoparticles in Nanomedicine: A Review of Recent Advances. Nanotechnology 2019;30:502003.
[14] Woodman C, Vundu G, George A, Wilson CM. Applications and Strategies in Nanodiagnosis and nanotherapy in Lung Cancer. Semin Cancer Biol 2021;69:349-64.
[15] Saadat M, Manshadi MK, Mohammadi M, Zare MJ, Zarei M, Kamali R, et al. Magnetic Particle Targeting for Diagnosis and Therapy of Lung Cancers. J Control Release 2020;328:776-91.
[16] Singh N, Jenkins GJ, Asadi R, Doak SH. Potential Toxicity of Superparamagnetic Iron Oxide Nanoparticles (SPION). Nano Rev 2010;1:5358.
[17] Ankamwar B, Lai TC, Huang JH, Liu RS, Hsiao M, Chen CH, et al. Biocompatibility of Fe3 O4 Nanoparticles Evaluated Byin Vitrocytotoxicity Assays Using Normal, Glia and Breast Cancer Cells. Nanotechnology 2010;21:075102.
[18] Kandasamy G, Maity D. Recent Advances in Superparamagnetic Iron Oxide Nanoparticles (SPIONs) for In Vitro and In Vivo Cancer Nanotheranostics. Int J Pharm 2015;496:191-218.
[19] Aggarwal P, Hall JB, Mcleland CB, Dobrovolskaia MA, Mcneil SE. Nanoparticle Interaction with Plasma Proteins as it Relates to Particle Biodistribution, Biocompatibility and Therapeutic Efficacy. Adv Drug Deliv Rev 2009;61:428-37.
[20] Lu AH, Salabas EL, Schüth F. Magnetic Nanoparticles: Synthesis, Protection, Functionalization, and Application. Angew Chem Int Ed Engl 2007;46:1222-44.
[21] Li X, Wei J, Aifantis KE, Fan Y, Feng Q, Cui FZ, et al. Current Investigations into Magnetic Nanoparticles for Biomedical Applications. J Biomed Mater Res Part A 2016;104:1285-96.
[22] Muthiah M, Park IK, Cho CS. Surface Modification of Iron Oxide Nanoparticles by Biocompatible Polymers for Tissue Imaging and Targeting. Biotechnol Adv 2013;31:1224-36.
[23] Malvindi MA, De Matteis V, Galeone A, Brunetti V, Anyfantis GC, Athanassiou A, et al. Toxicity Assessment of Silica Coated Iron Oxide Nanoparticles and Biocompatibility Improvement by Surface Engineering. PLoS One 2014;9:e85835.
[24] Dwivedi S, Siddiqui MA, Farshori NN, Ahamed M, Musarrat J, Al Khedhairy AA. Synthesis, Characterization and Toxicological Evaluation of Iron Oxide Nanoparticles in Human Lung Alveolar Epithelial Cells. Colloids Surf B Biointerfaces 2014;122:209-15.
[25] Soenen SJH, De Cuyper M. Assessing Cytotoxicity of (Iron Oxide Based) Nanoparticles: An Overview of Different Methods Exemplified with Cationic Magnetoliposomes. Contrast Media Mol Imaging 2009;4:207-19.
[26] Kunzmann A, Andersson B, Vogt C, Feliu N, Ye F, Gabrielsson S, et al. Efficient Internalization of SilicaCoated Iron Oxide Nanoparticles of Different Sizes by Primary Human Macrophages and Dendritic Cells. Toxicol Appl Pharmacol 2011;253:81-93.
[27] Eaton JW, Qian M. Molecular Bases of Cellular Iron Toxicity. Free Radic Biol Med 2002;32:833-40.
[28] Wu J, Sun J. Investigation on Mechanism of Growth Arrest Induced by Iron Oxide Nanoparticles in PC12 Cells. J Nanosci Nanotechnol 2011;11:11079-83.
[29] Wu W, Chen B, Cheng J, Wang J, Xu W, Liu L, et al. Biocompatibility of Fe3 O4 /DNR Magnetic Nanoparticles in the Treatment of Hematologic Malignancies. Int J Nanomed 2010;5:1079-84.
[30] Zhu MT, Wang Y, Feng WY, Wang B, Wang M, Ouyang H, et al. Oxidative Stress and Apoptosis Induced by Iron Oxide Nanoparticles in Cultured Human Umbilical Endothelial Cells. J Nanosci Nanotechnol 2010;10:8584-90.
[31] Wang D, Wang LH, Zhao Y, Lu YP, Zhu L. Hypoxia Regulates the Ferrous Iron Uptake and Reactive Oxygen Species Level Via Divalent Metal Transporter 1 (DMT1) Exon1B by Hypoxia Inducible Factor-1. IUBMB Life 2010;62:629-36.
[32] Wan X, Song Y, Song N, Li J, Yang L, Li Y, et al. The Preliminary Study of Immune Superparamagnetic Iron Oxide Nanoparticles for the Detection of Lung Cancer in Magnetic Resonance Imaging. Carbohydr Res 2016;419:33-40.
[33] Pfaff A, Schallon A, Ruhland TM, Majewski AP, SchmalzH, Freitag R, Müller AH. Magnetic and Fluorescent Glycopolymer Hybrid Nanoparticles for Intranuclear Optical Imaging. Biomacromolecules 2011;12:3805-11.
[34] Huang G, Zhang C, Li S, Khemtong C, Yang SG, Tian R, et al. A Novel Strategy for Surface Modification of Superparamagnetic Iron Oxide Nanoparticles for Lung Cancer Imaging. J Mater Chem 2009;19:6367-72.
[35] Nishimoto K, Mimura A, Aoki M, Banura N, Murase K. Application of Magnetic Particle Imaging to Pulmonary Imaging Using Nebulized Magnetic Nanoparticles. Open J Med Imag 2015;5:49.
[36] Chatterjee DK, Diagaradjane P, Krishnan S. Nanoparticlemediated Hyperthermia in Cancer Therapy. Ther Deliv 2011;2:1001-14.
[37] Gupta R, Sharma D. Evolution of Magnetic Hyperthermia for Glioblastoma Multiforme Therapy. ACS Chem Neurosci 2019;10:1157-72.
[38] Legge CJ, Colley HE, Lawson MA, Rawlings AE. Targeted Magnetic Nanoparticle Hyperthermia for the Treatment of Oral Cancer. J Oral Pathol Med 2019;48:803-9.
[39] Liang B, Zuo D, Yu K, Cai X, Qiao B, Deng R, et al. Multifunctional Bone Cement for Synergistic Magnetic Hyperthermia Ablation and Chemotherapy of Osteosarcoma. Mater Sci Eng C Mater Biol Appl 2020;108:110460.
[40] Brero F, Albino M, Antoccia A, Arosio P, Avolio M, Berardinelli F, et al. Hadron Therapy, Magnetic Nanoparticles and Hyperthermia: A Promising Combined Tool for Pancreatic Cancer Treatment. Nanomaterials (Basel) 2020;10:1919.
[41] Cędrowska E, Pruszyński M, Gawęda W, Żuk M, Krysiński P, Bruchertseifer F, et al. Trastuzumab Conjugated Superparamagnetic Iron Oxide Nanoparticles Labeled with 225Ac as a Perspective Tool for Combined α-Radioimmunotherapy and Magnetic Hyperthermia of HER2-Positive Breast Cancer. Molecules 2020;25:1025.
[42] Duval KE, Vernice NA, Wagner RJ, Fiering SN, Petryk JD, Lowry GJ, et al. Immunogenetic Effects of Low Dose (CEM43 30) Magnetic Nanoparticle Hyperthermia and Radiation in Melanoma Cells. Int J Hyperthermia 2019;36:37-46.
[43] Attaluri A, Kandala SK, Wabler M, Zhou H, Cornejo C, Armour M, et al. Magnetic Nanoparticle Hyperthermia Enhances Radiation Therapy: A Study in Mouse Models of Human Prostate Cancer. Int J Hyperthermia 2015;31:359-74.
[44] Stocke NA, Meenach SA, Arnold SM, Mansour HM, Hilt JZ. Formulation and Characterization of Inhalable Magnetic Nanocomposite Microparticles (MnMs) for Targeted Pulmonary Delivery Via Spray Drying. Int J Pharm 2015;479:320-8.
[45] Tseng CL, Chang KC, Yeh MC, Yang KC, Tang TP, Lin FH. Development of a Dual-functional PtFeHAP Magnetic Nanoparticles Application for Chemo-hyperthermia Treatment of Cancer. Ceram Int 2014;40:511727.
[46] Ma J, Zhang Z, Zhang Z, Huang J, Qin Y, Li X, et al. Magnetic Nanoparticle Clusters Radiosensitise Human Nasopharyngeal and Lung Cancer Cells after Alternating Magnetic Field Treatment. Int J Hyperthermia 2015;31:800-12.
[47] Baskar G, Ravi M, Panda JJ, Khatri A, Dev B, Santosham R, et al. Efficacy of Dipeptide-Coated Magnetic Nanoparticles in Lung Cancer Models Under Pulsed Electromagnetic Field. Cancer Invest 2017;35:431-42.
[48] Araya T, Kasahara K, Nishikawa S, Kimura H, Sone T, Nagae H, et al. Antitumor Effects of Inductive Hyperthermia Using Magnetic Ferucarbotran Nanoparticles on Human Lung Cancer Xenografts in Nude Mice. Onco Targets Ther 2013;6:237-42.
[49] Dabbagh A, Hedayatnasab Z, Karimian H, Sarraf M, Yeong CH, Hosseini HR, et al. Polyethylene Glycol-coated Porous Magnetic Nanoparticles for Targeted Delivery of Chemotherapeutics Under Magnetic Hyperthermia Condition. Int J Hyperthermia 2019;36:104-14.
[50] Torchilin VP. Targeted Pharmaceutical Nanocarriers for Cancer Therapy and Imaging. AAPS J 2007;9:E128-47.
[51] Barenholz Y. Doxil®--the first FDA-approved nano-drug: Lessons Learned. J Control Release 2012;160:117-34.
[52] Adrianzen Herrera D, Ashai N, Perez-Soler R, Cheng H. Nanoparticle Albumin Bound-paclitaxel for Treatment of Advanced Non-small Cell Lung Cancer: An Evaluation of the Clinical Evidence. Expert Opin Pharmacother 2019;20:95-102.
[53] Zhang H. Onivyde for the Therapy of Multiple Solid Tumors. Onco Targets Ther 2016;9:3001-7.
[54] Kang MK, Mao W, Lee JB, Yoo HS. Epidermal Growth Factor (EGF) Fragment-guided Anticancer Theranostic Particles for pH-responsive Release of Doxorubicin. Int J Pharm 2017;519:104-12.
[55] Ramasamy S, Enoch IV, Rajkumar SR. Polymeric Cyclodextrin-dextran Spooled Nickel Ferrite Nanoparticles: Expanded Anticancer Efficacy of Loaded Camptothecin. Mater Lett 2020;261:127114.
[56] Taratula O, Garbuzenko O, Savla R, Wang YA, He H, Minko T. Multifunctional Nanomedicine Platform for Cancer Specific Delivery of siRNA by Superparamagnetic Iron Oxide Nanoparticles-Dendrimer Complexes. Curr Drug Deliv 2011;8:59-69.
[57] Taylor A, Krupskaya Y, Krämer K, Fssel S, Klingeler R, Bchner B, et al. Cisplatin-loaded Carbon-encapsulated Iron Nanoparticles and their In Vitro Effects in Magnetic Fluid Hyperthermia. Carbon 2010;48:2327-34.
[58] Ak G, Aksu D, Çapkın E, Sarı Ö, Geboloğlu IK, Şanlıer ŞH. Delivery of Pemetrexed by Magnetic Nanoparticles: Design, Characterization, In Vitro and In Vivo Assessment. Prep Biochem Biotechnol 2020;50:215-25.
[59] Zeng F, Xu B, Zhu H, Wu S, Liao G, Xie D, et al. A Cascade Dual-targeted Nanocarrier for Enhanced Alectinib Delivery to ALK-Positive Lung Cancer. Biomater Sci 2020;8:6404-13.
[60] Zhao J, Li X, Wang X, Wang X. Fabrication of Hybrid Nanostructures Based on Fe3 O4 Nanoclusters as Theranostic Agents for Magnetic Resonance Imaging and Drug Delivery. Nanoscale Res Lett 2019;14:200.
[61] Domac BH, AlKhatib S, Zirhli O, Akdogan NG, Dirican SC, Bulut G, et al. Effects of PEGylated Fe-Fe3 O4 Core-Shell Nanoparticles on NIH3T3 and A549 Cell Lines. Heliyon 2019;6:e03124.
[62] Guthi JS, Yang SG, Huang G, L Si, Khemtong C, Kessinger CW, et al. MRI-Visible Micellar Nanomedicine for Targeted Drug Delivery to Lung Cancer Cells. Mol Pharm 2010;7:32-40.
[63] Hoffman A. The Origins and Evolution of “Controlled” Drug Delivery Systems. J Control Release 2008;132:153-63.
[64] Kong W, Sung D, Shim YH, Bae KH, Dubois P, Park TG, et al. Efficient Intracellular siRNA Delivery Strategy through Rapid and Simple Two Steps Mixing Involving Noncovalent Post-PEGylation. J Control Release 2009;138:141-7.
[65] Chan JM, Valencia PM, Zhang L, Langer R, Farokhzad OC. Polymeric Nanoparticles for Drug Delivery. Methods Mol Biol 2010;624:163-75.
[66] Liu J, Liu J, Chu L, Wang Y, Duan Y, Feng L, et al. Novel Peptide-dendrimer Conjugates as Drug Carriers for Targeting Nonsmall Cell Lung Cancer. Int J Nanomedicine 2010;6:59-69.
[67] Singh S, Nalwa HS. Nanotechnology and Health Safetytoxicity and Risk Assessment of Nanostructured Material Son Human Health. J Nanosci Nanotechnol 2007;7:3048-70.
[68] Allouche J. Synthesis of Organic and Bioorganic Nanoparticles: An Overview of the Preparation Methos. In: Nanomaterials: A Danger or a Promise. 2013. p. 27-74.
[69] Ma P, Mumper RJ. Paclitaxel Nano-delivery Systems: A Comprehensive Review. J Nanomed Nanotechnol 2013;4:100164.
[70] Jung J, Park SJ, Chung HK, Kang HW, Lee SW, Seo MH, et al. Polymeric Nanoparticles Containing Taxanes Enhance Chemoradiotherapeutic Efficacy in Non-small Cell Lung Cancer. Int J Radiat Oncol Biol Phys 2012;84:e77-83.
[71] Hu J, Fu S, Peng Q, Han YW, Xie J, Zan N, et al. PaclitaxelLoaded Polymeric Nanoparticles Combined with Chronomodulated Chemotherapy on Lung Cancer: In Vitro and In Vivo Evaluation. Int J Pharm 2017;516:313-22.
[72] Wang X, Chen H, Zeng X, Guo W, Jin Y, Wang S, et al. Efficient Lung Cancer-targeted Drug Delivery Via a Nanoparticle/MSC System. Acta Pharm Sin B 2019;9: 167-76.
[73] Zhang Z, Wang J, Nie X, Wen T, Ji Y, Wu X, et al. Near Infrared Laser-induced Targeted Cancer Therapy Using Thermoresponsive Polymer Encapsulated Gold Nanorods. J Am Chem Soc 2014;136:7317-26.
[74] Tseng CL, Su WY, Yen KC, Yang KC, Lin FH. The Use of Biotinylated-EGF-Modified Gelatin Nanoparticle Carrier to Enhance Cisplatin Accumulation in Cancerous Lung Via Inhalation. Biomaterials 2009;30:3476-85.
[75] Jiang ZM, Dai SP, Xu YQ, Li T, Xie J, Li C, et al. Crizotinib-loaded Polymeric Nanoparticles in Lung Cancer Chemotherapy. Med Oncol 2015;32:193.
[76] Vaidya B, Parvathaneni V, Kulkarni NS, Shukla SK, Damon JK, Sarode A, et al. Cyclodextrin Modified Erlotinib Loaded PLGA Nanoparticles for Improved Therapeutic Efficacy against Non-small Cell Lung Cancer. Int J Biol Macromol 2019;122:338-47.
[77] Yang Y, Huang Z, Li J, Mo Z, Huang Y, Ma C, et al. PLGA Porous Microspheres Dry Powders for Codelivery of Afatinib-Loaded Solid Lipid Nanoparticles and Paclitaxel: Novel Therapy for EGFR Tyrosine Kinase Inhibitors Resistant Nonsmall Cell Lung Cancer. Adv Healthc Mater 2019;8;1900965.
[78] Murakami M, Cabral H, Matsumoto Y, Wu S, Kano MR, Yamori T, et al. Improving Drug Potency and Efficacy by Nanocarrier-Mediated Subcellular Targeting. Sci Transl Med 2011;3:64ra2.
[79] Kim DW, Kim SY, Kim HK, Kim SW, Shin SW, Kim JS, et al. Multicenter Phase II Trial of Genexol-PM, a Novel Cremophor-free, Polymeric Micelle Formulation of Paclitaxel, with Cisplatin in Patients with Advanced Nonsmall-cell lung Cancer. Ann Oncol 2007;18:2009-14.
[80] Ahn HK, Jung M, Sym SJ, Shin DB, Kang SM, Kyung SY, et al. A phase II trial of Cremorphor EL-free paclitaxel (Genexol-PM) and gemcitabine in patients with advanced non-small cell lung cancer. Cancer Chemother Pharmacol 2014;74:277-82.
[81] Li LP. Cisplatin-loaded Polymeric Micelles with Aggregation-Induced Emission Feature for Cellular Imaging and Chemotherapy. Chem Eur 2018;3:13541-781.
[82] Zhang L, Liu Z, Kong C, Liu C, Yang K, Chen H, et al. Improving Drug Delivery of Micellar Paclitaxel against Non-Small Cell Lung Cancer by Co-Loading Itraconazole as a Micelle Stabilizer and a Tumor Vascular Manipulator. Small 2018;14:e1802112.
[83] Mei D, Zhao L, Chen B, Zhang X, Wang X, Yu Z, et al. α-Conotoxin Imi-modified Polymeric Micelles as Potential Nanocarriers for Targeted Docetaxel Delivery to α7-nAChR Overexpressed Non-small Cell Lung Cancer. Drug Deliv 2018;25:493-503.
[84] Ding M, Zeng X, He X, Li J, Tan H, Fu Q, et al. Cell Internalizable and Intracellularly Degradable Cationic Polyurethane Micelles as a Potential Platform for Efficient Imaging and Drug Delivery. Biomacromolecules 2014;15:2896-906.
[85] Reshma P, Unnikrishnan B, Preethi GU, Syama HP, Archana MG, Remya K, et al. Overcoming Drug-resistance in Lung Cancer Cell by Paclitaxel Loaded Galactoxyloglucan Nanoparticles. Int J Biol Macromol 2019;136:266-74.
[86] Abdelaziz H, Gaber M, Abd-Elwakil MM, Mabrouk MT, Elgohary MM, Kamel NM, et al. Inhalable Particulate Drug Delivery Systems for Lung Cancer Therapy: Nanoparticles, Microparticles, Nanocomposites and Nanoaggregates. J Control Release 2018;269:374-92.
[87] Elzoghby AO. Gelatin-based Nanoparticles as Drug and Gene Delivery Systems: Reviewing Three Decades of Research. J Control Release 2013;172:1075-91.
[88] Al-Hallak KM, Azarmi S, Anwar-Mohamed A, Roa WH, Löbenberg R. Secondary Cytotoxicity Mediated by Alveolar Macrophages: A Contribution to the Total Efficacy of Nanoparticles in Lung Cancer Therapy? Eur J Pharm Biopharm 2010;76:112-9.
[89] Xie Y, Aillon KL, Cai S, Christian JM, Davies NM, Berkland CJ, et al. Pulmonary Delivery of Cisplatinhyaluronan Conjugates Via Endotracheal Instillation for the Treatment of Lung Cancer. Int J Pharm 2010;392:156-63.
[90] Lyu Z, Ding L, Huang AY, Kao CL, Peng L. Poly(amidoamine) dendrimers: Covalent and supramolecular synthesis. Mater Today Chem 2019;13:34-48.
[91] Sohail I, Bhatti IA, Ashar A, Sarim FM, Mohsin M, Naveed R, et al. Polyamidoamine (PAMAM) Dendrimers Synthesis, Characterization and Adsorptive Removal of Nickel Ions from Aqueous Solution. J Mater Res Technol 2020;9:498-506.
[92] Pandita D, Poonia N, Kumar S, Lather V, Madaan K. Dendrimers in Drug Delivery and Targeting: Drugdendrimer Interactions and Toxicity Issues. J Pharm Bioallied Sci 2014;6:139-50.
[93] Cojocaru FD, Botezat D, Gardikiotis I, Uritu CM, Dodi G, Trandafir L, et al. Nanomaterials Designed for Antiviral Drug Delivery Transport Across Biological Barriers. Pharmaceutics 2020;12:171.
[94] Sherje AP, Jadhav M, Dravyakar BR, Kadam D. Dendrimers: A Versatile Nanocarrier for Drug Delivery and Targeting. Int J Pharm 2018;548:707-20.
[95] Gerber DE. Targeted Therapies: A New Generation of Cancer Treatments. Am Fam Physician 2008;77:311-9.
[96] Castro RI, Forero-Doria O, Guzmán L. Perspectives of Dendrimer-based Nanoparticles in Cancer Therapy. An Acad Bras Cienc 2018;90:2331-46.
[97] Zhong Q, Da Rocha SR. Poly(Amidoamine) Dendrimerdoxorubicin Conjugates: In Vitro Characteristics and Pseudosolution Formulation in Pressurized Metered-Dose Inhalers. Mol Pharm 2016;13:1058-72.
[98] Kale AA, Torchilin VP. Design, Synthesis, and Characterization of pH-Sensitive PEG-PE Conjugates for Stimuli-sensitive Pharmaceutical Nanocarriers: The Effect of Substitutes at the Hydrazone Linkage on the pH Stability of PEG-PE Conjugates. Bioconjug Chem 2007;18:363-70.
[99] Markowicz M, Szymánski P, Ciszewski M, Klys A, Mikiciuk-Olasik E. Evaluation of Poly(Amidoamine) Dendrimers as Potential Carriers of Iminodiacetic Derivatives Using Solubility Studies and 2D-NOESY NMR Spectroscopy. J Biol Phys 2012;38:637-56.
[100] Karthikeyan R, Vijayarajkumar P. PEGylated Nanoarchitechture Mediated Solubility Enhancement of Tyrosine-kinase Inhibitor. Inventi Rapid 2015;2:1-4.
[101] Amreddy N, Babu A, Panneerselvam J, Srivastava A, Muralidharan R, Chen A, et al. Chemo-biologic Combinatorial Drug Delivery Using Folate Receptortargeted Dendrimer Nanoparticles for Lung Cancer Treatment. Nanomedicine 2018;14:373-84.
[102] Abu Lila AS, Ishida T. Liposomal Delivery Systems: Design Optimization and Current Applications. Biol Pharm Bul Biol Pharm Bull 2017;40:1-10.
[103] Haluska CK, Riske KA, Marchi-Artzner V, Lehn JM, Lipowsky R, Dimova R. Time Scales of Membrane Fusion Revealed by Direct Imaging of Vesicle Fusion with High Temporal Resolution. Proc Natl Acad Sci 2006;103:15841-6.
[104] Torchilin VP. Recent Advances with Liposomes as Pharmaceutical Carriers. Nat Rev Drug Discov 2005;4: 145-60.
[105] Wagner U, Marth C, Largillier R, Kaern J, Brown C, Heywood M, et al. Final Overall Survival Results of Phase III GCIG CALYPSO Trial of Pegylated Liposomal Doxorubicin and Carboplatin vs Paclitaxel and Carboplatin in Platinum-sensitive Ovarian Cancer Patients. Br J Cancer 2012;107:588-91.
[106] Paliwal R, Paliwal SR, Kenwat R, Kurmi BD, Sahu MK. Solid Lipid Nanoparticles: A Review on Recent Perspectives and Patents. Expert Opin Ther Pat 2020;30:179-94.
[107] Aupérin A, Péchoux CL, Rolland E, Curran WJ, Furuse K, Fournel P, et al. Meta-Analysis of Concomitant Versus Sequential Radiochemotherapy in Locally Advanced NonSmall-Cell Lung Cancer. J Clin Oncol 2010;28:2181-90.
[108] Hamroun A, Lenain R, Bigna JJ, Speyer E, Bui L, Chamley P, et al. Prevention of Cisplatin-induced Acute Kidney Injury: A Systematic Review and Meta-analysis. Drugs 2019;79:1567-82.
[109] Boulikas T. Clinical Overview on Lipoplatin™: A Successful Liposomal Formulation of Cisplatin. Expert Opin Investig Drugs 2009;18:1197-218.
[110] Giuberti CD, Reis EC, Rocha TG, Leite EA, Lacerda RG, Ramaldes GA, et al. Study of the Pilot Production Process of Long-Circulating and pH-sensitive Liposomes Containing Cisplatin. J Liposome Res 2010;21:60-9.
[111] Stathopoulos GP, Antoniou D, Dimitroulis J, Stathopoulos J, Marosis K, Michalopoulou P. Comparison of Liposomal Cisplatin Versus Cisplatin in Non-squamous Cell Non-small-cell Lung Cancer. Cancer Chemother Pharmacol 2011;68:945-50.
[112] Khan MM, Madni A, Torchilin V, Filipczak N, Pan J, Tahir N, et al. Lipid-Chitosan Hybrid Nanoparticles for Controlled Delivery of Cisplatin. Drug Deliv 2019;26:765-72.
[113] Paraskar AS, Soni S, Chin KT, Chaudhuri P, Muto KW, Berkowitz J, et al. Harnessing Structure-activity Relationship to Engineer a Cisplatin Nanoparticle for Enhanced Antitumor Efficacy. Proc Natl Acad Sci 2010;107:12435-40.
[114] Khurana RK, Mahajan M, Teenu, Kapoor S, Jain S, Singh B. The Sojourn from Parenteral to Oral Taxanes using Nanocarrier Systems: A Patent Review. Recent Pat Drug Deliv Formul 2016;10:44-58.
[115] Koudelka Š, Turánek J. Liposomal Paclitaxel Formulations. J Controlled Release 2012;163:322-34.
[116] Wang X, Zhou J, Wang Y, Zhu Z, Lu Y, Wei Y, et al. A Phase I Clinical and Pharmacokinetic Study of Paclitaxel Liposome Infused in Non-small Cell Lung Cancer Patients with Malignant Pleural Effusions. Eur J Cancer 2010;46:1474-80.
[117] Paclitaxel Liposome for Squamous Non-Smallcell Lung Cancer Study (LIPUSU) Full Text View. Paclitaxel Liposome for Squamous Non-Smallcell Lung Cancer Study (LIPUSU) Full Text View. Available from: https://clinicaltrials.gov/ct2/show/ NCT02996214?term=NCT02996214&draw=2&rank=1. [Last accessed on 2020 Aug 14].
[118] Matsumura Y, Hamaguchi T, Ura T, Muro K, Yamada Y, Shimada Y, et al. Phase I Clinical Trial and Pharmacokinetic Evaluation of NK911, a MicelleEncapsulated Doxorubicin. Br J Cancer 2004;91:1775-81.
[119] Hamaguchi T, Doi T, Eguchi-Nakajima T, Kato K, Yamada Y, Shimada Y, et al. Phase I Study of NK012, a Novel SN38-Incorporating Micellar Nanoparticle, in Adult Patients with Solid Tumors. Clin Cancer Res 2010;16:5058-66.
[120] Paclitaxel Micelles for Injection / Paclitaxel Injection in Combination with Cisplatin for Firstline Therapy of Advanced NSCLC Full Text View. Full Text View ClinicalTrials. Shanghai Yizhong Biotechnology Co., Ltd.; 2020. Available from: https://www.clinicaltrials.gov/ct2/show/ NCT02667743?term=NCT02667743&draw=2&rank=1. [Last accessed on 2020 Aug 14].
[121] Selvan ST, Tan TT, Yi DK, Jana NR. Functional and Multifunctional Nanoparticles for Bioimaging and Biosensing. Langmuir 2010;26:11631-41.
[122] Hainfeld JF, Dilmanian FA, Slatkin DN, Smilowitz HM. Radiotherapy Enhancement with Gold Nanoparticles. J Pharm Pharmacol 2008;60:977-85.
[123] Yavuz MS, Cheng Y, Chen J, Cobley CM, Zhang Q, Rycenga M, et al. Gold Nanocages Covered by Smart Polymers for Controlled Release with Near-infrared Light. Nat Mater 2009;8:935-939.
[124] Xie J, Lee S, Chen X. Nanoparticle-based Theranostic Agents. Adv Drug Deliv Rev 2010;62:1064-79.
[125] Sperling RA, Parak W. Surface Modification, Functionalization and Bioconjugation of Colloidal Inorganic Nanoparticles. Philos Trans R Soc Lond A Math Phys Eng Sci 2010;368:1333-83.
[126] Sau TK, Rogach AL, Jckel F, Klar TA, Feldmann J. Properties and Applications of Colloidal Nonspherical Noble Metal Nanoparticles. Adv Mater 2010;22:1805-25.
[127] Sperling RA, Gil PR, Zhang F, Zanella M, Parak WJ. Biological Applications of Gold Nanoparticles. Chem Soc Rev 2008;37:1896-908.
[128] Porcel E, Liehn S, Remita H, Usami N, Kobayashi K, Furusawa Y, et al. Platinum Nanoparticles: A Promising Material for Future Cancer Therapy? Nanotechnology 2010;21:85103.
[129] Danhier F, Feron O, Préat V. To Exploit the Tumor Microenvironment: Passive and Active Tumor Targeting of Nanocarriers for Anti-cancer Drug Delivery. J Control Release 2010;148:135-46.
[130] Silva AC, Oliveira TR, Mamani JB, Malheiros SM, Malavolta L, Pavon LF, et al. Application of Hyperthermia Induced by Superparamagnetic Iron Oxide Nanoparticles in Glioma Treatment. Int J Nanomed 2011;6:591-603.
[131] Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B, et al. Efficacy and Safety of Intratumoral Thermotherapy Using Magnetic Iron-oxide Nanoparticles Combined with External Beam Radiotherapy on Patients with Recurrent Glioblastoma Multiforme. J Neurooncol 2011;103:317-24.
[132] Hou Z, Zhang Y, Deng K, Chen Y, Li X, Deng X, et al. UV-emitting Upconversionbased TiO2 Photosensitizing Nanoplatform: Near-infrared Light Mediated In Vivo Photodynamic Therapy Via Mitochondria Involved Apoptosis Pathway. ACS Nano 2015;9: 2584-99.
[133] Baskar G, Chandhuru J, Fahad KS, Praveen AS, Chamundeeswari M, Muthukumar T. Anticancer Activity of Fungal l-Asparaginase Conjugated with Zinc Oxide Nanoparticles. J Mater Sci Mater Med 2015;26:5380.
[134] Ali D, Alarifi S, Alkahtani S, AlKahtane AA, Almalik A. Cerium Oxide Nanoparticles Induce Oxidative Stress and Genotoxicity in Human Skin Melanoma Cells. Cell Biochem Biophys 2015;71:1643-51.
[135] Zhang XF, Liu ZG, Shen W, Gurunathan S. Silver Nanoparticles: Synthesis, Characterization, Properties, Applications, and Therapeutic Approaches. Int J Mol Sci 2016;17:1534.
[136] Haume K, Rosa S, Grellet S, ´Smiałek MA, ButterworthKT, Solov’yov AV, et al. Gold Nanoparticles for Cancer Radiotherapy: A Review. Cancer Nano 2016;7:8.
[137] Lopez-Campos F, Candini D, Carrasco E, Francés MA. Nanoparticles Applied to Cancer Immunoregulation. Rep Pract Oncol Radiother 2019;24:47-55.
[138] Zhao N, Pan Y, Cheng Z, Liu H. Gold Nanoparticles for Cancer Theranostics a Brief Update. J Innov Opt Health Sci 2016;9:1630004.
[139] Zhao P, Li N, Astruc D. State of the Art in Gold Nanoparticle Synthesis. Coord Chem Rev 2013;257:638-65.
[140] Singh P, Pandit S, Mokkapati VR, Garg A, Ravikumar V, Mijakovic I. Gold Nanoparticles in Diagnostics and Therapeutics for Human Cancer. Int J Mol Sci 2018;19:1979.
[141] Mioc A, Mioc M, Ghiulai R, Voicu M, Racoviceanu R, Trandafirescu C, et al. Gold Nanoparticles as Targeted Delivery Systems and Theranostic Agents in Cancer Therapy. Curr Med Chem 2019;26:6493-513.
[142] Coelho SC, Almeida GM, Santos-Silva F, Pereira MC, Coelho MA. Enhancing the Efficiency of Bortezomib Conjugated to Pegylated Gold Nanoparticles: An In Vitro Study on Human Pancreatic Cancer Cells and Adenocarcinoma Human Lung Alveolar Basal Epithelial Cells. Expert Opin Drug Deliv 2016;13:1075-81.
[143] Ramalingam V, Varunkumar K, Ravikumar V, Rajaram R. Target Delivery of Doxorubicin Tethered with PVP Stabilized Gold Nanoparticles for Effective Treatment of Lung Cancer. Sci Rep 2018;8:3815.
[144] Cryer AM, Chan C, Eftychidou A, Maksoudian C, Mahesh M, Tetley TD, et al. Tyrosine Kinase Inhibitor Gold Nanoconjugates for the Treatment of Non-Small Cell Lung Cancer. ACS Appl Mater Interfaces 2019;11:16336-46.
[145] Gadoue SM, Toomeh D. Radio-sensitization Efficacy of Gold Nanoparticles in Inhalational Nanomedicine and the Adverse Effect of Nano-Detachment due to Coating Inactivation. Phys Med 2019;60:7-13.
[146] Ngwa W, Kumar R, Sridhar S, Korideck H, Zygmanski P, Cormack RA, et al. Targeted Radiotherapy with Gold Nanoparticles: Current Status and Future Perspectives. Nanomedicine (Lond) 2014;9:1063-82.
[147] Taratula O, Garbuzenko OB, Chen AM, Minko T. Innovative Strategy for Treatment of Lung Cancer: Targeted Nanotechnology-based Inhalation Co-delivery of Anticancer Drugs and siRNA. J Drug Target 2011;19:900-14.
[148] Rousseau J, Barth RF, Fernandez M, Adam JF, Balosso J, Esteve F, et al. Efficacy of Intracerebral Delivery of Cisplatin in Combination with Photon Irradiation for Treatment of Brain Tumors. J Neurooncol 2010;98:287-95.
[149] Taratula O, Kuzmov A, Shah M, Garbuzenko OB, Minko T. Nanostructured Lipid Carriers as Multifunctional Nanomedicine Platform for Pulmonary Co-delivery of Anticancer Drugs and siRNA. J Control Release 2013;171:349-57.
[150] Hao Y, Altundal Y, Moreau M, Sajo E, Kumar R, Ngwa W. Potential for Enhancing External Beam Radiotherapy for Lung Cancer Using High-Z Nanoparticles Administered Via Inhalation. Phys Med Biol 2015;60:7035-43.
[151] Wang C, Beiss V, Steinmetz NF. Cowpea Mosaic Virus Nanoparticles and Empty Virus-Like Particles Show Distinct but Overlapping Immunostimulatory Properties. J Virol 2019;93:e00129-19.
[152] Johnstone TC, Suntharalingam K, Lippard SJ. The Next Generation of Platinum Drugs: Targeted Pt(II) Agents, Nanoparticle Delivery, and Pt(IV) Prodrugs. Chem Rev 2016;116:3436-86.
[153] Chung YH, Cai H, Steinmetz NF. Viral Nanoparticles for Drug Delivery, Imaging, Immunotherapy, and Theranostic Applications. Adv Drug Deliv Rev 2020;156:214-35.
[154] Ren Y, Wong SM, Lim LY. Folic Acid-conjugated Protein Cages of a Plant Virus: A Novel Delivery Platform for Doxorubicin. Bioconjug Chem 2007;18:836-43.
[155] Zeng Q, Wen H, Wen Q, Chen X, Wang Y, Xuan W, et al. Cucumber Mosaic Virus as Drug Delivery Vehicle for Doxorubicin. Biomaterials 2013;34:4632-42.
[156] Aljabali AA, Shukla S, Lomonossoff GP, Steinmetz NF, Evans DJ. CPMV-DOX Delivers. Mol Pharm 2013;10:3-10.
[157] Cao J, Guenther RH, Sit TL, Opperman CH, Lommel SA, Willoughby JA. Loading and Release Mechanism of Red Clover Necrotic Mosaic Virus Derived Plant Viral Nanoparticles for Drug Delivery of Doxorubicin. Small 2014;10:5126-36.
[158] Le DH, Lee KL, Shukla S, Commandeur U, Steinmetz NF. Potato Virus X, a Filamentous Plant Viral Nanoparticle for Doxorubicin Delivery in Cancer Therapy. Nanoscale 2017;9:2348-57.
[159] Shan W, Zhang D, Wu Y, Lv X, Hu B, Zhou X, et al. Modularized Peptides Modified HBc Virus-like Particles for Encapsulation and Tumor-targeted Delivery of Doxorubicin. Nanomedicine 2018;14:725-34.
[160] Hu H, Steinmetz NF. Doxorubicin-Loaded Physalis Mottle Virus Particles as a pH-Responsive Prodrug for Cancer Therapy. Biotechnol J 2020;12:e2000077.
[161] Robertson KL, Soto CM, Archer MJ, Odoemene O, Liu JL. Engineered T4 Viral Nanoparticles for Cellular Imaging and Flow Cytometry. Bioconjug Chem 2011;22:595-604.
[162] Destito G, Yeh R, Rae CS, Finn MG, Manchester M. Folic Acid-mediated Targeting of Cowpea Mosaic Virus Particles to Tumor Cells. Chem Biol 2007;14:1152-62.
[163] Beatty PH, Lewis JD. Cowpea Mosaic Virus Nanoparticles for Cancer Imaging and Therapy. Adv Drug Deliv Rev 2019;145:130-44.
[164] Franke CE, Czapar AE, Patel RB, Steinmetz NF. Tobacco Mosaic Virus-Delivered Cisplatin Restores Efficacy in Platinum-Resistant Ovarian Cancer Cells. Mol Pharm 2018;15:2922-31.
[165] Gao S, Liu X, Wang Z, Jiang S, Wu M, Tian Y, et al. Fluorous Interaction Induced Self-assembly of Tobacco Mosaic Virus Coat Protein for Cisplatin Delivery. Nanoscale 2018;10:11732-36.
[166] Lizotte PH, Wen AM, Sheen MR, Fields J, Rojanasopondist P, Steinmetz NF, et al. In Situ Vaccination with Cowpea Mosaic Virus Nanoparticles Suppresses Metastatic Cancer. Nat Nanotechnol 2016;11:295-303.
[167] Xi W, Ke D, Min L, Lin W, Jiahui Z, Fang L, et al. Incorporation of CD40 Ligand Enhances the Immunogenicity of Tumor-Associated Calcium Signal Transducer 2 Virus-Like Particles Against Lung Cancer. Int J Mol Med 2018;41:3671-9.
[168] Lin MC, Shen CH, Chang D, Wang M. Inhibition of Human Lung Adenocarcinoma Growth and Metastasis by JC Polyomavirus-like Particles Packaged with an SP-B Promoter-Driven CD59-Specific shRNA. Clin Sci 2019;133:2159-69.
[169] Feldmann DP, Cheng Y, Kandil R, Xie Y, Mohammadi M, Harz H, et al. In Vitro and In Vivo Delivery of siRNA via VIPER Polymer System to Lung Cells. J Control Release 2018;276:50-8.
[170] Sainsbury F. Virus-like Nanoparticles: Emerging Tools for Targeted Cancer Diagnostics and Therapeutics. Ther Deliv 2017;8:1019-21.
[171] Lewinski N, Colvin V, Drezek R. Cytotoxicity of Nanoparticles. Small 2008;4:26-49.
[172] de Mello Donegá C. Synthesis and Properties of Colloidal Heteronanocrystals. Chem Soc Rev 2011;40:1512-46.
[173] Ghasemi Y, Peymani P, Afifi S. Quantum Dot: Magic Nanoparticle for Imaging, Detection and Targeting. Acta Biomed 2009;80:156-65.
[174] Jin S, Hu YX, Gu ZJ, Liu L, Wu HC. Application of Quantum Dots in Biological Imaging. J Nanomater 2011;2011:834139.
[175] Hardman R. A Toxicologic Review of Quantum Dots: Toxicity Depends on Physicochemical and Environmental Factors. Environ Health Perspect 2006;114:165-72.
[176] Smith AM, Nie S. Next-generation Quantum Dots. Nat Biotechnol 2009;27:732-3.
[177] Singh RD, Shandilya R, Bhargava A, Kumar R, Tiwari R, Chaudhury K, et al. Quantum Dot Based Nano-Biosensors for Detection of Circulating Cell Free miRNAs in Lung Carcinogenesis: From Biology to Clinical Translation. Front Genet 2018;9:616.
[178] Mashinchian O, Johari-Ahar M, Ghaemi B, Rashidi M, Barar J, Omidi Y. Impacts of Quantum Dots in Molecular Detection and Bioimaging of Cancer. Bioimpacts 2014;4:149-66.
[179] Ranjbar-Navazi Z, Eskandani M, Johari-Ahar M, Nemati A, Akbari H, Davaran S, et al. Doxorubicinconjugated D-glucosamine-and Folate- bi-functionalised InP/ZnS Quantum Dots for Cancer Cells Imaging and Therapy. J Drug Target 2018;26:267-77.
[180] Cai X, Luo Y, Zhang W, Du D, Lin Y. pH-Sensitive ZnO Quantum Dots-Doxorubicin Nanoparticles for Lung Cancer Targeted Drug Delivery. ACS Appl Mater Interfaces 2016;8:22442-50.
[181] Kulkarni NS, Parvathaneni V, Shukla SK, Barasa L, Perron JC, Yoganathan S, et al. Tyrosine Kinase Inhibitor Conjugated Quantum Dots for Non-small Cell Lung Cancer (NSCLC) Treatment. Eur J Pharm Sci 2019;133:145-59.
[182] Socinski MA, Bondarenko I, Karaseva NA, Makhson AM, Vynnychenko I, Okamoto I, et al. Weekly Nab-paclitaxel in Combination with Carboplatin Versus Solvent-based Paclitaxel Plus Carboplatin as First-line Therapy in Patients with Advanced Non-small Cell Lung Cancer: Final Results of a Phase III Trial. J Clin Oncol 2012;30:2055-62.
[183] Yang JJ, Huang C, Chen GY, Song Y, Cheng Y, Yan HH, et al. A Randomized Phase II Clinical Trial of Nabpaclitaxel and Carboplatin Compared with Gemcitabine and Carboplatin as First-line Therapy in Locally Advanced or Metastatic Squamous Cell Carcinoma of Lung. BMC Cancer 2014;14:684.
[184] Langer CJ, Hirsh V, Ko A, Renschler MF, Socinski MA. Weekly Nab-paclitaxel in Combination with Carboplatin as First-line Therapy in Patients with Advanced Nonsmall Cell Lung Cancer: Analysis of Safety and Efficacy in Patients with Renal Impairment. Clin Lung Cancer 2015;16:112-20.
[185] Autio KA, Dreicer R, Anderson J, Garcia JA, Alva A, Hart LL, et al. Safety and Efficacy of BIND-014, a Docetaxel Nanoparticle Targeting Prostate-Specific Membrane Antigen for Patients With Metastatic Castration-Resistant Prostate Cancer: A Phase 2 Clinical Trial. JAMA Oncol 2018;4:1344-51.
[186] Von Hoff DD, Mita MM, Ramanathan RK, Weiss GJ, Mita AC, LoRusso PM, et al. Phase I Study of PSMATargeted Docetaxel-Containing Nanoparticle BIND-014 in Patients with Advanced Solid Tumors. Clin Cancer Res 2016;22:3157-63.
[187] Chen YF, Wang YH, Lei CS, Changou CA, Davis ME, Yen Y. Host Immune Response to Anti-cancer Camptothecin Conjugated Cyclodextrin-based Polymers. J Biomed Sci 2019;26:85.