Cancer active targeting by nanoparticles: a comprehensive review of literature

  • Remon Bazak
  • Mohamad Houri
  • Samar El Achy
  • Serag Kamel
  • Tamer Refaat
Review – Cancer Research

Abstract

Purpose

Cancer is one of the leading causes of death, and thus, the scientific community has but great efforts to improve cancer management. Among the major challenges in cancer management is development of agents that can be used for early diagnosis and effective therapy. Conventional cancer management frequently lacks accurate tools for detection of early tumors and has an associated risk of serious side effects of chemotherapeutics. The need to optimize therapeutic ratio as the difference with which a treatment affects cancer cells versus healthy tissues lead to idea that it is needful to have a treatment that could act a the “magic bullet”—recognize cancer cells only. Nanoparticle platforms offer a variety of potentially efficient solutions for development of targeted agents that can be exploited for cancer diagnosis and treatment. There are two ways by which targeting of nanoparticles can be achieved, namely passive and active targeting. Passive targeting allows for the efficient localization of nanoparticles within the tumor microenvironment. Active targeting facilitates the active uptake of nanoparticles by the tumor cells themselves.

Methods

Relevant English electronic databases and scientifically published original articles and reviews were systematically searched for the purpose of this review.

Results

In this report, we present a comprehensive review of literatures focusing on the active targeting of nanoparticles to cancer cells, including antibody and antibody fragment-based targeting, antigen-based targeting, aptamer-based targeting, as well as ligand-based targeting.

Conclusion

To date, the optimum targeting strategy has not yet been announced, each has its own advantages and disadvantages even though a number of them have found their way for clinical application. Perhaps, a combination of strategies can be employed to improve the precision of drug delivery, paving the way for a more effective personalized therapy.

Keywords

Cancer Active targeting Nanoparticles  

References

  1. Adolphi NL, Butler KS, Lovato DM, Tessier TE, Trujillo JE, Hathaway HJ et al (2012) Imaging of Her2-targeted magnetic nanoparticles for breast cancer detection: comparison of SQUID-detected magnetic relaxometry and MRI. Contrast Media Mol Imaging 7(3):308–319PubMedGoogle Scholar
  2. Anabousi S, Bakowsky U, Schneider M, Huwer H, Lehr CM, Ehrhardt C (2006) In vitro assessment of transferrin-conjugated liposomes as drug delivery systems for inhalation therapy of lung cancer. Eur J Pharm Sci Off J Eur Fed Pharm Sci 29(5):367–374Google Scholar
  3. Asadishad B, Vossoughi M, Alamzadeh I (2010) In vitro release behavior and cytotoxicity of doxorubicin-loaded gold nanoparticles in cancerous cells. Biotechnol Lett 32(5):649–654PubMedGoogle Scholar
  4. Bagalkot V, Zhang L, Levy-Nissenbaum E, Jon S, Kantoff PW, Langer R et al (2007) Quantum dot-aptamer conjugates for synchronous cancer imaging, therapy, and sensing of drug delivery based on bi-fluorescence resonance energy transfer. Nano Lett 7(10):3065–3070PubMedGoogle Scholar
  5. Beduneau A, Saulnier P, Benoit JP (2007) Active targeting of brain tumors using nanocarriers. Biomaterials 28(33):4947–4967PubMedGoogle Scholar
  6. Bisker G, Yeheskely-Hayon D, Minai L, Yelin D (2012) Controlled release of Rituximab from gold nanoparticles for phototherapy of malignant cells. J Control Release 162(2):303–309PubMedGoogle Scholar
  7. Bouras A, Kaluzova M, Hadjipanayis CG (2012) 192 Epidermal growth factor receptor antibody-conjugated iron-oxide nanoparticles: therapeutic targeting and radiosensitivity enhancement of glioblastoma. Neurosurgery 71(2):E574–E575Google Scholar
  8. Brignole C, Marimpietri D, Gambini C, Allen TM, Ponzoni M, Pastorino F (2003) Development of Fab’ fragments of anti-GD(2) immunoliposomes entrapping doxorubicin for experimental therapy of human neuroblastoma. Cancer Lett 197(1–2):199–204PubMedGoogle Scholar
  9. Byrne JD, Betancourt T, Brannon-Peppas L (2008) Active targeting schemes for nanoparticle systems in cancer therapeutics. Adv Drug Deliv Rev 60(15):1615–1626PubMedGoogle Scholar
  10. Chattopadhyay N, Fonge H, Cai Z, Scollard D, Lechtman E, Done SJ et al (2012) Role of antibody-mediated tumor targeting and route of administration in nanoparticle tumor accumulation in vivo. Mol Pharm 9(8):2168–2179Google Scholar
  11. Chen H, Gao J, Lu Y, Kou G, Zhang H, Fan L et al (2008a) Preparation and characterization of PE38KDEL-loaded anti-HER2 nanoparticles for targeted cancer therapy. J Control Release 128(3):209–216PubMedGoogle Scholar
  12. Chen HW, Medley CD, Sefah K, Shangguan D, Tang Z, Meng L et al (2008b) Molecular recognition of small-cell lung cancer cells using aptamers. ChemMedChem 3(6):991–1001PubMedCentralPubMedGoogle Scholar
  13. Chen TJ, Cheng TH, Hung YC, Lin KT, Liu GC, Wang YM (2008c) Targeted folic acid-PEG nanoparticles for noninvasive imaging of folate receptor by MRI. J Biomed Mater Res A 87(1):165–175PubMedGoogle Scholar
  14. Chen T, Shukoor MI, Wang R, Zhao Z, Yuan Q, Bamrungsap S et al (2011) Smart multifunctional nanostructure for targeted cancer chemotherapy and magnetic resonance imaging. ACS Nano 5(10):7866–7873PubMedCentralPubMedGoogle Scholar
  15. Cherukuri P, Curley SA (2010) Use of nanoparticles for targeted, noninvasive thermal destruction of malignant cells. Methods Mol Biol 624:359–373PubMedGoogle Scholar
  16. Chiu TC, Huang CC (2009) Aptamer-functionalized nano-biosensors. Sensors (Basel) 9(12):10356–10388Google Scholar
  17. Cho YS, Yoon TJ, Jang ES, Soo Hong K, Young Lee S, Ran Kim O et al (2010) Cetuximab-conjugated magneto-fluorescent silica nanoparticles for in vivo colon cancer targeting and imaging. Cancer Lett 299(1):63–71PubMedGoogle Scholar
  18. Choi H, Choi SR, Zhou R, Kung HF, Chen IW (2004) Iron oxide nanoparticles as magnetic resonance contrast agent for tumor imaging via folate receptor-targeted delivery. Acad Radiol 11(9):996–1004PubMedGoogle Scholar
  19. Choi CH, Alabi CA, Webster P, Davis ME (2010) Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles. Proc Natl Acad Sci U S A 107(3):1235–1240PubMedCentralPubMedGoogle Scholar
  20. Choi J, Yang J, Bang D, Park J, Suh JS, Huh YM et al (2012) Targetable gold nanorods for epithelial cancer therapy guided by near-IR absorption imaging. Small 8(5):746–753PubMedGoogle Scholar
  21. Cirstoiu-Hapca A, Bossy-Nobs L, Buchegger F, Gurny R, Delie F (2007) Differential tumor cell targeting of anti-HER2 (Herceptin) and anti-CD20 (Mabthera) coupled nanoparticles. Int J Pharm 331(2):190–196PubMedGoogle Scholar
  22. Corbin IR, Ng KK, Ding L, Jurisicova A, Zheng G (2012) Near-infrared fluorescent imaging of metastatic ovarian cancer using folate receptor-targeted high-density lipoprotein nanocarriers. Nanomedicine (Lond) 8(6):875–890Google Scholar
  23. Corsi F, Fiandra L, De Palma C, Colombo M, Mazzucchelli S, Verderio P et al (2011) HER2 expression in breast cancer cells is downregulated upon active targeting by antibody-engineered multifunctional nanoparticles in mice. ACS Nano 5(8):6383–6393PubMedGoogle Scholar
  24. Danhier F, Feron O, Preat V (2010) To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J Control Release 148(2):135–146PubMedGoogle Scholar
  25. Daniels TR, Bernabeu E, Rodriguez JA, Patel S, Kozman M, Chiappetta DA et al (2012) The transferrin receptor and the targeted delivery of therapeutic agents against cancer. Biochim Biophys Acta 1820(3):291–317PubMedCentralPubMedGoogle Scholar
  26. Day ES, Bickford LR, Slater JH, Riggall NS, Drezek RA, West JL (2010) Antibody-conjugated gold–gold sulfide nanoparticles as multifunctional agents for imaging and therapy of breast cancer. Int J Nanomed 5:445–454Google Scholar
  27. Debbage P (2009) Targeted drugs and nanomedicine: present and future. Curr Pharm Des 15(2):153–172PubMedGoogle Scholar
  28. Deepagan VG, Sarmento B, Menon D, Nascimento A, Jayasree A, Sreeranganathan M et al (2012) In vitro targeted imaging and delivery of camptothecin using cetuximab-conjugated multifunctional PLGA-ZnS nanoparticles. Nanomedicine (Lond) 7(4):507–519Google Scholar
  29. Derycke AS, De Witte PA (2002) Transferrin-mediated targeting of hypericin embedded in sterically stabilized PEG-liposomes. Int J Oncol 20(1):181–187PubMedGoogle Scholar
  30. Destounis SV, DiNitto P, Logan-Young W, Bonaccio E, Zuley ML, Willison KM (2004) Can computer-aided detection with double reading of screening mammograms help decrease the false-negative rate? Initial experience. Radiology 232(2):578–584PubMedGoogle Scholar
  31. Dhar S, Gu FX, Langer R, Farokhzad OC, Lippard SJ (2008) Targeted delivery of cisplatin to prostate cancer cells by aptamer functionalized Pt(IV) prodrug-PLGA-PEG nanoparticles. Proc Natl Acad Sci U S A 105(45):17356–17361PubMedCentralPubMedGoogle Scholar
  32. Dilnawaz F, Singh A, Mohanty C, Sahoo SK (2010) Dual drug loaded superparamagnetic iron oxide nanoparticles for targeted cancer therapy. Biomaterials 31(13):3694–3706PubMedGoogle Scholar
  33. Eavarone DA, Yu X, Bellamkonda RV (2000) Targeted drug delivery to C6 glioma by transferrin-coupled liposomes. J Biomed Mater Res 51(1):10–14PubMedGoogle Scholar
  34. Elnakat H, Ratnam M (2004) Distribution, functionality and gene regulation of folate receptor isoforms: implications in targeted therapy. Adv Drug Deliv Rev 56(8):1067–1084PubMedGoogle Scholar
  35. Estevez MC, Huang YF, Kang H, O’Donoghue MB, Bamrungsap S, Yan J et al (2010) Nanoparticle-aptamer conjugates for cancer cell targeting and detection. Methods Mol Biol 624:235–248PubMedGoogle Scholar
  36. Fan K, Cao C, Pan Y, Lu D, Yang D, Feng J et al (2012) Magnetoferritin nanoparticles for targeting and visualizing tumour tissues. Nat Nanotechnol 7(7):459–464PubMedGoogle Scholar
  37. Fang X, Tan W (2010) Aptamers generated from cell-SELEX for molecular medicine: a chemical biology approach. Acc Chem Res 43(1):48–57PubMedCentralPubMedGoogle Scholar
  38. Farokhzad OC, Jon S, Khademhosseini A, Tran TN, Lavan DA, Langer R (2004) Nanoparticle-aptamer bioconjugates: a new approach for targeting prostate cancer cells. Cancer Res 64(21):7668–7672PubMedGoogle Scholar
  39. Farokhzad OC, Cheng J, Teply BA, Sherifi I, Jon S, Kantoff PW et al (2006) Targeted nanoparticle-aptamer bioconjugates for cancer chemotherapy in vivo. Proc Natl Acad Sci U S A 103:6315–6320PubMedCentralPubMedGoogle Scholar
  40. Fonseca C, Moreira JN, Ciudad CJ (2005) Pedroso de Lima MC, Simoes S. Targeting of sterically stabilised pH-sensitive liposomes to human T-leukaemia cells. Eur J Pharm Biopharm 59(2):359–366PubMedGoogle Scholar
  41. Gabizon A, Horowitz AT, Goren D, Tzemach D, Shmeeda H, Zalipsky S (2003) In vivo fate of folate-targeted polyethylene-glycol liposomes in tumor-bearing mice. Clin Cancer Res 9(17):6551–6559PubMedGoogle Scholar
  42. Gabizon A, Tzemach D, Gorin J, Mak L, Amitay Y, Shmeeda H et al (2010) Improved therapeutic activity of folate-targeted liposomal doxorubicin in folate receptor-expressing tumor models. Cancer Chemother Pharmacol 66(1):43–52PubMedGoogle Scholar
  43. Gan CW, Feng SS (2010) Transferrin-conjugated nanoparticles of poly(lactide)-D-alpha-tocopheryl polyethylene glycol succinate diblock copolymer for targeted drug delivery across the blood–brain barrier. Biomaterials 31(30):7748–7757PubMedGoogle Scholar
  44. Gao X, Luo Y, Wang Y, Pang J, Liao C, Lu H et al (2012) Prostate stem cell antigen-targeted nanoparticles with dual functional properties: in vivo imaging and cancer chemotherapy. Int J Nanomed 7:4037–4051Google Scholar
  45. Glazer ES, Massey KL, Zhu C, Curley SA (2010a) Pancreatic carcinoma cells are susceptible to noninvasive radio frequency fields after treatment with targeted gold nanoparticles. Surgery 148(2):319–324PubMedCentralPubMedGoogle Scholar
  46. Glazer ES, Zhu C, Massey KL, Thompson CS, Kaluarachchi WD, Hamir AN et al (2010b) Noninvasive radiofrequency field destruction of pancreatic adenocarcinoma xenografts treated with targeted gold nanoparticles. Clin Cancer Res 16(23):5712–5721PubMedCentralPubMedGoogle Scholar
  47. Gosk S, Vermehren C, Storm G, Moos T (2004) Targeting anti-transferrin receptor antibody (OX26) and OX26-conjugated liposomes to brain capillary endothelial cells using in situ perfusion. J Cereb Blood Flow Metab 24(11):1193–1204PubMedGoogle Scholar
  48. Greish K (2007) Enhanced permeability and retention of macromolecular drugs in solid tumors: a royal gate for targeted anticancer nanomedicines. J Drug Target 15(7–8):457–464PubMedGoogle Scholar
  49. Greish K (2010) Enhanced permeability and retention (EPR) effect for anticancer nanomedicine drug targeting. Methods Mol Biol 624:25–37PubMedGoogle Scholar
  50. Groothuis DR (2000) The blood–brain and blood–tumor barriers: a review of strategies for increasing drug delivery. Neuro Oncol 2(1):45–59PubMedCentralPubMedGoogle Scholar
  51. Harding J, Burtness B (2005) Cetuximab: an epidermal growth factor receptor chemeric human-murine monoclonal antibody. Drugs Today (Barc) 41(2):107–127Google Scholar
  52. Hathaway HJ, Butler KS, Adolphi NL, Lovato DM, Belfon R, Fegan D et al (2011) Detection of breast cancer cells using targeted magnetic nanoparticles and ultra-sensitive magnetic field sensors. Breast Cancer Res 13(5):R108PubMedCentralPubMedGoogle Scholar
  53. Herr JK, Smith JE, Medley CD, Shangguan D, Tan W (2006) Aptamer-conjugated nanoparticles for selective collection and detection of cancer cells. Anal Chem 78(9):2918–2924PubMedGoogle Scholar
  54. Hilgenbrink AR, Low PS (2005) Folate receptor-mediated drug targeting: from therapeutics to diagnostics. J Pharm Sci 94(10):2135–2146PubMedGoogle Scholar
  55. Hong M, Zhu S, Jiang Y, Tang G, Sun C, Fang C et al (2010) Novel anti-tumor strategy: pEG-hydroxycamptothecin conjugate loaded transferrin-PEG-nanoparticles. J Control Release 141(1):22–29PubMedGoogle Scholar
  56. Hrkach J, Von Hoff D, Mukkaram Ali M, Andrianova E, Auer J, Campbell T et al (2012) Preclinical development and clinical translation of a PSMA-targeted docetaxel nanoparticle with a differentiated pharmacological profile. Sci Transl Med 4(128):128ra39PubMedGoogle Scholar
  57. Huang YF, Chang HT, Tan W (2008) Cancer cell targeting using multiple aptamers conjugated on nanorods. Anal Chem 80(3):567–572PubMedGoogle Scholar
  58. Huang YF, Lin YW, Lin ZH, Chang HT (2009) Aptamer-modified gold nanoparticles for targeting breast cancer cells through light scattering. J Nanopart Res 11:775–783Google Scholar
  59. Huh YM, Jun YW, Song HT, Kim S, Choi JS, Lee JH et al (2005) In vivo magnetic resonance detection of cancer by using multifunctional magnetic nanocrystals. J Am Chem Soc 127(35):12387–12391PubMedGoogle Scholar
  60. Huwyler J, Wu D, Pardridge WM (1996) Brain drug delivery of small molecules using immunoliposomes. Proc Natl Acad Sci U S A 93(24):14164–14169PubMedCentralPubMedGoogle Scholar
  61. Hwang do W, Ko HY, Lee JH, Kang H, Ryu SH, Song IC et al (2010) A nucleolin-targeted multimodal nanoparticle imaging probe for tracking cancer cells using an aptamer. J Nucl Med 51(1):98–105PubMedGoogle Scholar
  62. Iinuma H, Maruyama K, Okinaga K, Sasaki K, Sekine T, Ishida O et al (2002) Intracellular targeting therapy of cisplatin-encapsulated transferrin-polyethylene glycol liposome on peritoneal dissemination of gastric cancer. Int J Cancer 99(1):130–137PubMedGoogle Scholar
  63. Ishida O, Maruyama K, Tanahashi H, Iwatsuru M, Sasaki K, Eriguchi M et al (2001) Liposomes bearing polyethyleneglycol-coupled transferrin with intracellular targeting property to the solid tumors in vivo. Pharm Res 18(7):1042–1048PubMedGoogle Scholar
  64. Javier DJ, Nitin N, Levy M, Ellington A, Richards-Kortum R (2008) Aptamer-targeted gold nanoparticles as molecular-specific contrast agents for reflectance imaging. Bioconjug Chem 19(6):1309–1312PubMedCentralPubMedGoogle Scholar
  65. Jefferies WA, Brandon MR, Hunt SV, Williams AF, Gatter KC, Mason DY (1984) Transferrin receptor on endothelium of brain capillaries. Nature 312(5990):162–163PubMedGoogle Scholar
  66. Jiang W, Xie H, Ghoorah D, Shang Y, Shi H, Liu F et al (2012) Conjugation of functionalized SPIONs with transferrin for targeting and imaging brain glial tumors in rat model. PLoS ONE 7(5):e37376PubMedCentralPubMedGoogle Scholar
  67. Kim D, Jeong YY, Jon S (2010) A drug-loaded aptamer-gold nanoparticle bioconjugate for combined CT imaging and therapy of prostate cancer. ACS Nano 4(7):3689–3696PubMedGoogle Scholar
  68. Kobayashi T, Ishida T, Okada Y, Ise S, Harashima H, Kiwada H (2007) Effect of transferrin receptor-targeted liposomal doxorubicin in P-glycoprotein-mediated drug resistant tumor cells. Int J Pharm 329(1–2):94–102PubMedGoogle Scholar
  69. Kohler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256(5517):495–497PubMedGoogle Scholar
  70. Kolishetti N, Dhar S, Valencia PM, Lin LQ, Karnik R, Lippard SJ et al (2010) Engineering of self-assembled nanoparticle platform for precisely controlled combination drug therapy. Proc Natl Acad Sci U S A 107(42):17939–17944PubMedCentralPubMedGoogle Scholar
  71. Kreuter J (2007) Nanoparticles—a historical perspective. Int J Pharm 331(1):1–10PubMedGoogle Scholar
  72. LaRocque J, Bharali DJ, Mousa SA (2009) Cancer detection and treatment: the role of nanomedicines. Mol Biotechnol 42(3):358–366PubMedGoogle Scholar
  73. Lee JH, Yigit MV, Mazumdar D, Lu Y (2010) Molecular diagnostic and drug delivery agents based on aptamer-nanomaterial conjugates. Adv Drug Deliv Rev 62(6):592–605PubMedCentralPubMedGoogle Scholar
  74. Li X, Ding L, Xu Y, Wang Y, Ping Q (2009a) Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int J Pharm 373(1–2):116–123PubMedGoogle Scholar
  75. Li G, Li D, Zhang L, Zhai J, Wang E (2009b) One-step synthesis of folic acid protected gold nanoparticles and their receptor-mediated intracellular uptake. Chemistry 15(38):9868–9873PubMedGoogle Scholar
  76. Li N, Larson T, Nguyen HH, Sokolov KV, Ellington AD (2010) Directed evolution of gold nanoparticle delivery to cells. Chem Commun (Camb) 46(3):392–394Google Scholar
  77. Liao C, Sun Q, Liang B, Shen J, Shuai X (2011) Targeting EGFR-overexpressing tumor cells using cetuximab-immunomicelles loaded with doxorubicin and superparamagnetic iron oxide. Eur J Radiol 80(3):699–705PubMedGoogle Scholar
  78. Ling Y, Wei K, Luo Y, Gao X, Zhong S (2011) Dual docetaxel/superparamagnetic iron oxide loaded nanoparticles for both targeting magnetic resonance imaging and cancer therapy. Biomaterials 32(29):7139–7150PubMedGoogle Scholar
  79. Liss M, Petersen B, Wolf H, Prohaska E (2002) An aptamer-based quartz crystal protein biosensor. Anal Chem 74(17):4488–4495PubMedGoogle Scholar
  80. Liu G, Mao X, Phillips JA, Xu H, Tan W, Zeng L (2009) Aptamer-nanoparticle strip biosensor for sensitive detection of cancer cells. Anal Chem 81(24):10013–10018PubMedCentralPubMedGoogle Scholar
  81. Liu D, Chen C, Hu G, Mei Q, Qiu H, Long G (2011) Specific targeting of nasopharyngeal carcinoma cell line CNE1 by C225-conjugated ultrasmall superparamagnetic iron oxide particles with magnetic resonance imaging. Acta Biochim Biophys Sin (Shanghai) 43(4):301–306Google Scholar
  82. Low PS, Kularatne SA (2009) Folate-targeted therapeutic and imaging agents for cancer. Current Opin Chem Biol 13(3):256–262Google Scholar
  83. Lu Y, Yang J, Sega E (2006) Issues related to targeted delivery of proteins and peptides. AAPS J 8(3):E466–E478PubMedCentralPubMedGoogle Scholar
  84. Lu RM, Chang YL, Chen MS, Wu HC (2011) Single chain anti-c-Met antibody conjugated nanoparticles for in vivo tumor-targeted imaging and drug delivery. Biomaterials 32(12):3265–3274PubMedGoogle Scholar
  85. Manju S, Sreenivasan K (2012) Gold nanoparticles generated and stabilized by water soluble curcumin-polymer conjugate: blood compatibility evaluation and targeted drug delivery onto cancer cells. J Colloid Interface Sci 368(1):144–151PubMedGoogle Scholar
  86. Marty C, Schwendener RA (2005) Cytotoxic tumor targeting with scFv antibody-modified liposomes. Methods Mol Med 109:389–402PubMedGoogle Scholar
  87. Marty C, Odermatt B, Schott H, Neri D, Ballmer-Hofer K, Klemenz R et al (2002) Cytotoxic targeting of F9 teratocarcinoma tumours with anti-ED-B fibronectin scFv antibody modified liposomes. Br J Cancer 87(1):106–112PubMedCentralPubMedGoogle Scholar
  88. Marty C, Langer-Machova Z, Sigrist S, Schott H, Schwendener RA, Ballmer-Hofer K (2006) Isolation and characterization of a scFv antibody specific for tumor endothelial marker 1 (TEM1), a new reagent for targeted tumor therapy. Cancer Lett 235(2):298–308PubMedGoogle Scholar
  89. Matherly LH, Goldman DI (2003) Membrane transport of folates. Vitam Horm 66:403–456PubMedGoogle Scholar
  90. Medley CD, Smith JE, Tang Z, Wu Y, Bamrungsap S, Tan W (2008) Gold nanoparticle-based colorimetric assay for the direct detection of cancerous cells. Anal Chem 80(4):1067–1072PubMedGoogle Scholar
  91. Nahta R, Yu D, Hung MC, Hortobagyi GN, Esteva FJ (2006) Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer. Nat Clin Pract Oncol 3(5):269–280PubMedGoogle Scholar
  92. Nakase M, Inui M, Okumura K, Kamei T, Nakamura S, Tagawa T (2005) p53 gene therapy of human osteosarcoma using a transferrin-modified cationic liposome. Mol Cancer Ther 4(4):625–631PubMedGoogle Scholar
  93. Ni S, Stephenson SM, Lee RJ (2002) Folate receptor targeted delivery of liposomal daunorubicin into tumor cells. Anticancer Res 22(4):2131–2135PubMedGoogle Scholar
  94. Ni X, Castanares M, Mukherjee A, Lupold SE (2011) Nucleic acid aptamers: clinical applications and promising new horizons. Curr Med Chem 18(27):4206–4214PubMedCentralPubMedGoogle Scholar
  95. Nobs L, Buchegger F, Gurny R, Allemann E (2006) Biodegradable nanoparticles for direct or two-step tumor immunotargeting. Bioconjug Chem 17(1):139–145PubMedGoogle Scholar
  96. Oghabian MA, Jeddi-Tehrani M, Zolfaghari A, Shamsipour F, Khoei S, Amanpour S (2011) Detectability of Her2 positive tumors using monoclonal antibody conjugated iron oxide nanoparticles in MRI. J Nanosci Nanotechnol 11(6):5340–5344PubMedGoogle Scholar
  97. Pan XQ, Zheng X, Shi G, Wang H, Ratnam M, Lee RJ (2002) Strategy for the treatment of acute myelogenous leukemia based on folate receptor beta-targeted liposomal doxorubicin combined with receptor induction using all-trans retinoic acid. Blood 100(2):594–602PubMedGoogle Scholar
  98. Pan X, Wu G, Yang W, Barth RF, Tjarks W, Lee RJ (2007) Synthesis of cetuximab-immunoliposomes via a cholesterol-based membrane anchor for targeting of EGFR. Bioconjug Chem 18(1):101–108PubMedCentralPubMedGoogle Scholar
  99. Parab HJ, Huang JH, Lai TC, Jan YH, Liu RS, Wang JL et al (2011) Biocompatible transferrin-conjugated sodium hexametaphosphate-stabilized gold nanoparticles: synthesis, characterization, cytotoxicity and cellular uptake. Nanotechnology 22(39):395706PubMedGoogle Scholar
  100. Patra CR, Bhattacharya R, Wang E, Katarya A, Lau JS, Dutta S et al (2008) Targeted delivery of gemcitabine to pancreatic adenocarcinoma using cetuximab as a targeting agent. Cancer Res 68(6):1970–1978PubMedGoogle Scholar
  101. Patra CR, Bhattacharya R, Mukherjee P (2010) Fabrication and functional characterization of goldnanoconjugates for potential application in ovarian cancer. J Mater Chem 20(3):547–554PubMedCentralPubMedGoogle Scholar
  102. Prabaharan M, Grailer JJ, Pilla S, Steeber DA, Gong S (2009) Gold nanoparticles with a monolayer of doxorubicin-conjugated amphiphilic block copolymer for tumor-targeted drug delivery. Biomaterials 30(30):6065–6075PubMedGoogle Scholar
  103. Press MF, Cordon-Cardo C, Slamon DJ (1990) Expression of the HER-2/neu proto-oncogene in normal human adult and fetal tissues. Oncogene 5(7):953–962PubMedGoogle Scholar
  104. Pulkkinen M, Pikkarainen J, Wirth T, Tarvainen T, Haapa-aho V, Korhonen H et al (2008) Three-step tumor targeting of paclitaxel using biotinylated PLA-PEG nanoparticles and avidin-biotin technology: formulation development and in vitro anticancer activity. Eur J Pharm Biopharm 70(1):66–74PubMedGoogle Scholar
  105. Puvanakrishnan P, Diagaradjane P, Kazmi SM, Dunn AK, Krishnan S, Tunnell JW (2012) Narrow band imaging of squamous cell carcinoma tumors using topically delivered anti-EGFR antibody conjugated gold nanorods. Lasers Surg Med 44(4):310–317PubMedGoogle Scholar
  106. Qian ZM, Tang PL (1995) Mechanisms of iron uptake by mammalian cells. Biochim Biophys Acta 1269(3):205–214PubMedGoogle Scholar
  107. Riviere K, Huang Z, Jerger K, Macaraeg N, Szoka FC Jr (2011) Antitumor effect of folate-targeted liposomal doxorubicin in KB tumor-bearing mice after intravenous administration. J Drug Target 19(1):14–24PubMedCentralPubMedGoogle Scholar
  108. Ruan J, Song H, Qian Q, Li C, Wang K, Bao C et al (2012) HER2 monoclonal antibody conjugated RNase-A-associated CdTe quantum dots for targeted imaging and therapy of gastric cancer. Biomaterials 33(29):7093–7102PubMedGoogle Scholar
  109. Rudolph C, Schillinger U, Plank C, Gessner A, Nicklaus P, Muller R et al (2002) Nonviral gene delivery to the lung with copolymer-protected and transferrin-modified polyethylenimine. Biochim Biophys Acta 1573(1):75–83PubMedGoogle Scholar
  110. Sahoo SK, Labhasetwar V (2005) Enhanced antiproliferative activity of transferrin-conjugated paclitaxel-loaded nanoparticles is mediated via sustained intracellular drug retention. Mol Pharm 2(5):373–383PubMedGoogle Scholar
  111. Sahoo SK, Ma W, Labhasetwar V (2004) Efficacy of transferrin-conjugated paclitaxel-loaded nanoparticles in a murine model of prostate cancer. Int J Cancer 112(2):335–340PubMedGoogle Scholar
  112. Sapra P, Moase EH, Ma J, Allen TM (2004) Improved therapeutic responses in a xenograft model of human B lymphoma (Namalwa) for liposomal vincristine versus liposomal doxorubicin targeted via anti-CD19 IgG2a or Fab’ fragments. Clin Cancer Res 10(3):1100–1111PubMedGoogle Scholar
  113. Schroeder JE, Shweky I, Shmeeda H, Banin U, Gabizon A (2007) Folate-mediated tumor cell uptake of quantum dots entrapped in lipid nanoparticles. J Control Release 124(1–2):28–34PubMedGoogle Scholar
  114. Serda RE, Adolphi NL, Bisoffi M, Sillerud LO (2007) Targeting and cellular trafficking of magnetic nanoparticles for prostate cancer imaging. Mol Imaging 6(4):277–288PubMedGoogle Scholar
  115. Shah N, Chaudhari K, Dantuluri P, Murthy RS, Das S (2009) Paclitaxel-loaded PLGA nanoparticles surface modified with transferrin and Pluronic((R))P85, an in vitro cell line and in vivo biodistribution studies on rat model. J Drug Target 17(7):533–542PubMedGoogle Scholar
  116. Shangguan D, Li Y, Tang Z, Cao ZC, Chen HW, Mallikaratchy P et al (2006) Aptamers evolved from live cells as effective molecular probes for cancer study. Proc Natl Acad Sci U S A 103(32):11838–11843PubMedCentralPubMedGoogle Scholar
  117. Shi X, Wang S, Meshinchi S, Van Antwerp ME, Bi X, Lee I et al (2007) Dendrimer-entrapped gold nanoparticles as a platform for cancer-cell targeting and imaging. Small 3(7):1245–1252PubMedGoogle Scholar
  118. Shi X, Wang SH, Van Antwerp ME, Chen X, Baker JR Jr (2009a) Targeting and detecting cancer cells using spontaneously formed multifunctional dendrimer-stabilized gold nanoparticles. Analyst 134(7):1373–1379PubMedCentralPubMedGoogle Scholar
  119. Shi X, Wang SH, Lee I, Shen M, Baker JR Jr (2009b) Comparison of the internalization of targeted dendrimers and dendrimer-entrapped gold nanoparticles into cancer cells. Biopolymers 91(11):936–942PubMedCentralPubMedGoogle Scholar
  120. Shmeeda H, Mak L, Tzemach D, Astrahan P, Tarshish M, Gabizon A (2006) Intracellular uptake and intracavitary targeting of folate-conjugated liposomes in a mouse lymphoma model with up-regulated folate receptors. Mol Cancer Ther 5(4):818–824PubMedGoogle Scholar
  121. Song EQ, Zhang ZL, Luo QY, Lu W, Shi YB, Pang DW (2009) Tumor cell targeting using folate-conjugated fluorescent quantum dots and receptor-mediated endocytosis. Clin Chem 55(5):955–963PubMedCentralPubMedGoogle Scholar
  122. Spector NL, Blackwell KL (2009) Understanding the mechanisms behind trastuzumab therapy for human epidermal growth factor receptor 2-positive breast cancer. J Clin Oncol 27(34):5838–5847PubMedGoogle Scholar
  123. Steinhauser I, Spankuch B, Strebhardt K, Langer K (2006) Trastuzumab-modified nanoparticles: optimisation of preparation and uptake in cancer cells. Biomaterials 27(28):4975–4983PubMedGoogle Scholar
  124. Sugano M, Egilmez NK, Yokota SJ, Chen FA, Harding J, Huang SK et al (2000) Antibody targeting of doxorubicin-loaded liposomes suppresses the growth and metastatic spread of established human lung tumor xenografts in severe combined immunodeficient mice. Cancer Res 60(24):6942–6949PubMedGoogle Scholar
  125. Suzuki R, Takizawa T, Kuwata Y, Mutoh M, Ishiguro N, Utoguchi N et al (2008) Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome. Int J Pharm 346(1–2):143–150PubMedGoogle Scholar
  126. Taghdisi SM, Lavaee P, Ramezani M, Abnous K (2011) Reversible targeting and controlled release delivery of daunorubicin to cancer cells by aptamer-wrapped carbon nanotubes. Eur J Pharm Biopharm 77(2):200–206PubMedGoogle Scholar
  127. Talekar M, Kendall J, Denny W, Garg S (2011) Targeting of nanoparticles in cancer: drug delivery and diagnostics. Anticancer Drugs 22(10):949–962PubMedGoogle Scholar
  128. Taylor RM, Sillerud LO (2012) Paclitaxel-loaded iron platinum stealth immunomicelles are potent MRI imaging agents that prevent prostate cancer growth in a PSMA-dependent manner. Int J Nanomed 7:4341–4352Google Scholar
  129. Taylor RM, Huber DL, Monson TC, Ali AM, Bisoffi M, Sillerud LO (2011) Multifunctional iron platinum stealth immunomicelles: targeted detection of human prostate cancer cells using both fluorescence and magnetic resonance imaging. J Nanopart Res 13(10):4717–4729PubMedCentralPubMedGoogle Scholar
  130. Thistlethwaite JR Jr, Cosimi AB, Delmonico FL, Rubin RH, Talkoff-Rubin N, Nelson PW et al (1984) Evolving use of OKT3 monoclonal antibody for treatment of renal allograft rejection. Transplantation 38(6):695–701PubMedGoogle Scholar
  131. Thomas TP, Patri AK, Myc A, Myaing MT, Ye JY, Norris TB et al (2004) In vitro targeting of synthesized antibody-conjugated dendrimer nanoparticles. Biomacromolecules 5(6):2269–2274PubMedGoogle Scholar
  132. Torchilin VP (2010) Passive and active drug targeting: drug delivery to tumors as an example. Handb Exp Pharmacol 197:3–53PubMedGoogle Scholar
  133. Ulbrich K, Hekmatara T, Herbert E, Kreuter J (2009) Transferrin- and transferrin-receptor-antibody-modified nanoparticles enable drug delivery across the blood–brain barrier (BBB). Eur J Pharm Biopharm 71(2):251–256PubMedGoogle Scholar
  134. Waldmann TA (2003) Immunotherapy: past, present and future. Nat Med 9(3):269–277PubMedGoogle Scholar
  135. Wang AZ, Gu F, Zhang L, Chan JM, Radovic-Moreno A, Shaikh MR et al (2008a) Biofunctionalized targeted nanoparticles for therapeutic applications. Expert Opin Biol Ther 8(8):1063–1070PubMedCentralPubMedGoogle Scholar
  136. Wang X, Yang L, Chen ZG, Shin DM (2008b) Application of nanotechnology in cancer therapy and imaging. CA Cancer J Clin 58(2):97–110PubMedGoogle Scholar
  137. Wang AZ, Bagalkot V, Vasilliou CC, Gu F, Alexis F, Zhang L et al (2008c) Superparamagnetic iron oxide nanoparticle-aptamer bioconjugates for combined prostate cancer imaging and therapy. ChemMedChem 3(9):1311–1315PubMedCentralPubMedGoogle Scholar
  138. Wang X, Wang Y, Chen ZG, Shin DM (2009) Advances of cancer therapy by nanotechnology. Cancer Res Treat 41(1):1–11PubMedCentralPubMedGoogle Scholar
  139. Wang H, Wang S, Liao Z, Zhao P, Su W, Niu R et al (2012) Folate-targeting magnetic core-shell nanocarriers for selective drug release and imaging. Int J Pharm 430(1–2):342–349PubMedGoogle Scholar
  140. Wang H, Zheng L, Peng C, Shen M, Shi X, Zhang G (2013) Folic acid-modified dendrimer-entrapped gold nanoparticles as nanoprobes for targeted CT imaging of human lung adenocarcinoma. Biomaterials 34(2):470–480Google Scholar
  141. Wartlick H, Michaelis K, Balthasar S, Strebhardt K, Kreuter J, Langer K (2004) Highly specific HER2-mediated cellular uptake of antibody-modified nanoparticles in tumour cells. J Drug Target 12(7):461–471PubMedGoogle Scholar
  142. Wu J, Lu Y, Lee A, Pan X, Yang X, Zhao X et al (2007) Reversal of multidrug resistance by transferrin-conjugated liposomes co-encapsulating doxorubicin and verapamil. J Pharm Pharm Sci Publ Can Soc Pharm Sci (Societe canadienne des sciences pharmaceutiques) 10(3):350–357Google Scholar
  143. Xu L, Pirollo KF, Tang WH, Rait A, Chang EH (1999) Transferrin-liposome-mediated systemic p53 gene therapy in combination with radiation results in regression of human head and neck cancer xenografts. Hum Gene Ther 10(18):2941–2952PubMedGoogle Scholar
  144. Xu Z, Gu W, Huang J, Sui H, Zhou Z, Yang Y et al (2005) In vitro and in vivo evaluation of actively targetable nanoparticles for paclitaxel delivery. Int J Pharm 288(2):361–368PubMedGoogle Scholar
  145. Yang J, Eom K, Lim EK, Park J, Kang Y, Yoon DS et al (2008) In situ detection of live cancer cells by using bioprobes based on Au nanoparticles. Langmuir 24(21):12112–12115PubMedGoogle Scholar
  146. Yang L, Mao H, Wang YA, Cao Z, Peng X, Wang X et al (2009) Single chain epidermal growth factor receptor antibody conjugated nanoparticles for in vivo tumor targeting and imaging. Small 5(2):235–243PubMedCentralPubMedGoogle Scholar
  147. Yang HM, Park CW, Woo MA, Kim MI, Jo YM, Park HG et al (2010) HER2/neu antibody conjugated poly(amino acid)-coated iron oxide nanoparticles for breast cancer MR imaging. Biomacromolecules 11(11):2866–2872Google Scholar
  148. Yu B, Tai HC, Xue W, Lee LJ, Lee RJ (2010) Receptor-targeted nanocarriers for therapeutic delivery to cancer. Mol Membr Biol 27(7):286–298PubMedCentralPubMedGoogle Scholar
  149. Yu MK, Kim D, Lee IH, So JS, Jeong YY, Jon S (2011a) Image-guided prostate cancer therapy using aptamer-functionalized thermally cross-linked superparamagnetic iron oxide nanoparticles. Small 7(15):2241–2249PubMedGoogle Scholar
  150. Yu C, Hu Y, Duan J, Yuan W, Wang C, Xu H et al (2011b) Novel aptamer-nanoparticle bioconjugates enhances delivery of anticancer drug to MUC1-positive cancer cells in vitro. PLoS ONE 6(9):e24077PubMedCentralPubMedGoogle Scholar
  151. Yu MK, Park J, Jon S (2012) Targeting strategies for multifunctional nanoparticles in cancer imaging and therapy. Theranostics 2(1):3–44PubMedCentralPubMedGoogle Scholar
  152. Zhang Y, Kohler N, Zhang M (2002) Surface modification of superparamagnetic magnetite nanoparticles and their intracellular uptake. Biomaterials 23(7):1553–1561PubMedGoogle Scholar
  153. Zhang L, Radovic-Moreno AF, Alexis F, Gu FX, Basto PA, Bagalkot V et al (2007) Co-delivery of hydrophobic and hydrophilic drugs from nanoparticle-aptamer bioconjugates. ChemMedChem 2(9):1268–1271PubMedGoogle Scholar
  154. Zhang Y, Hong H, Cai W (2011) Tumor-targeted drug delivery with aptamers. Curr Med Chem 18(27):4185–4194PubMedCentralPubMedGoogle Scholar
  155. Zhao N, Bagaria HG, Wong MS, Zu Y (2011) A nanocomplex that is both tumor cell-selective and cancer gene-specific for anaplastic large cell lymphoma. J Nanobiotechnol 9:2Google Scholar
  156. Zheng Y, Yu B, Weecharangsan W, Piao L, Darby M, Mao Y et al (2010) Transferrin-conjugated lipid-coated PLGA nanoparticles for targeted delivery of aromatase inhibitor 7alpha-APTADD to breast cancer cells. Int J Pharm 390(2):234–241PubMedGoogle Scholar
  157. Zhou Y, Drummond DC, Zou H, Hayes ME, Adams GP, Kirpotin DB et al (2007) Impact of single-chain Fv antibody fragment affinity on nanoparticle targeting of epidermal growth factor receptor-expressing tumor cells. J Mol Biol 371(4):934–947PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Remon Bazak
    • 1
  • Mohamad Houri
    • 5
  • Samar El Achy
    • 2
  • Serag Kamel
    • 3
  • Tamer Refaat
    • 4
    • 6
  1. 1.Department of Otorhinolaryngology, Faculty of MedicineAlexandria UniversityAlexandriaEgypt
  2. 2.Department of Pathology, Faculty of MedicineAlexandria UniversityAlexandriaEgypt
  3. 3.House Officer, Faculty of MedicineAlexandria UniversityAlexandriaEgypt
  4. 4.Department of Clinical Oncology and Nuclear Medicine, Faculty of MedicineAlexandria UniversityAlexandriaEgypt
  5. 5.Department of Ophthalmology, Faculty of MedicineBeirut Arab UniversityBeirutLebanon
  6. 6.Department of Radiation Oncology, Robert H. Lurie Comprehensive Cancer CenterNorthwestern UniversityChicagoUSA

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