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Development of Drugs and Technology for Radiation Theragnosis

  • Jeong, Hwan-Jeong (Department of Nuclear Medicine, Biomedical Research Institute, Chonbuk National University Medical School and Hospital) ;
  • Lee, Byung Chul (Department of Nuclear Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital) ;
  • Ahn, Byeong-Cheol (Department of Nuclear Medicine, Kyungpook National University School of Medicine and Hospital) ;
  • Kang, Keon Wook (Department of Nuclear Medicine and Cancer Research Institute, Seoul National University)
  • Received : 2016.04.10
  • Accepted : 2016.04.13
  • Published : 2016.06.25

Abstract

Personalized medicine is tailored medical treatment that targets the individual characteristics of each patient. Theragnosis, combining diagnosis and therapy, plays an important role in selecting appropriate patients. Noninvasive in vivo imaging can trace small molecules, antibodies, peptides, nanoparticles, and cells in the body. Recently, imaging methods have been able to reveal molecular events in cells and tissues. Molecular imaging is useful not only for clinical studies but also for developing new drugs and new treatment modalities. Preclinical and early clinical molecular imaging shows biodistribution, pharmacokinetics, mechanisms of action, and efficacy. When therapeutic materials are labeled using radioisotopes, nuclear imaging with positron emission tomography or gamma camera can be used to treat diseases and monitor therapy simultaneously. Such nuclear medicine technology is defined as radiation theragnosis. We review the current development of drugs and technology for radiation theragnosis using peptides, albumin, nanoparticles, and cells.

Keywords

References

  1. E.P. Krenning, W.H. Bakker, W.A. Breeman, J.W. Koper, P.P. Kooij, L. Ausema, J.S. Lameris, J.C. Reubi, S.W. Lamberts, Localisation of endocrine-related tumours with radioiodinated analogue of somatostatin, Lancet 1 (1989) 242-244.
  2. V. Rufini, M.L. Calcagni, R.P. Baum, Imaging of neuroendocrine tumors, Semin. Nucl. Med. 36 (2006) 228-247. https://doi.org/10.1053/j.semnuclmed.2006.03.007
  3. C. Decristoforo, S.J. Mather, Preparation, 99mTc-labeling, and in vitro characterization of HYNIC and N3S modified RC-160 and [Tyr3]octreotide, Bioconjug. Chem. 10 (1999) 431-438. https://doi.org/10.1021/bc980121c
  4. S. Angeletti, V.D. Corleto, O. Schillaci, M. Marignani, B. Annibale, A. Moretti, G. Silecchia, F. Scopinaro, N. Basso, C. Bordi, G. Delle Fave, Use of the somatostatin analogue octreotide to localise and manage somatostatin-producing tumours, Gut 42 (1998) 792-794. https://doi.org/10.1136/gut.42.6.792
  5. N. Leners, F. Jamar, R. Fiasse, A. Ferrant, S. Pauwels, Indium-111-pentetreotide uptake in endocrine tumors and lymphoma, J. Nucl. Med. 37 (1996) 916-922.
  6. V. Prasad, R.P. Baum, Biodistribution of the Ga-68 labeled somatostatin analogue DOTA-NOC in patients with neuroendocrine tumors: characterization of uptake in normal organs and tumor lesions, Q. J. Nucl. Med. Mol. Imaging 54 (2010) 61-67.
  7. D.J. Kwekkeboom, J.J. Teunissen, W.H. Bakker, P.P. Kooij, W.W. de Herder, R.A. Feelders, C.H. van Eijck, J.P. Esser, B.L. Kam, E.P. Krenning, Radiolabeled somatostatin analog [177Lu-DOTA0,Tyr3]octreotate in patients with endocrine gastroenteropancreatic tumors, J. Clin. Oncol. 23 (2005) 2754-2762. https://doi.org/10.1200/JCO.2005.08.066
  8. G.A. Kaltsas, D. Papadogias, P. Makras, A.B. Grossman, Treatment of advanced neuroendocrine tumours with radiolabelled somatostatin analogues, Endocr. Relat. Cancer 12 (2005) 683-699. https://doi.org/10.1677/erc.1.01116
  9. S.M. Bison, M.W. Konijnenberg, M. Melis, S.E. Pool, M.R. Bernsen, J.J. Teunissen, D.J. Kwekkeboom, M. de Jong, Peptide receptor radionuclide therapy using radiolabeled somatostatin analogs: focus on future developments, Clin. Transl. Imaging 2 (2014) 55-66. https://doi.org/10.1007/s40336-014-0054-2
  10. F. Graf, J. Fahrer, S. Maus, A. Morgenstern, F. Bruchertseifer, S. Venkatachalam, C. Fottner, M.M. Weber, J. Huelsenbeck, M. Schreckenberger, B. Kaina, M. Miederer, DNA double strand breaks as predictor of efficacy of the alpha-particle emitter Ac-225 and the electron emitter Lu-177 for somatostatin receptor targeted radiotherapy, PLoS One 9 (2014) e88239. https://doi.org/10.1371/journal.pone.0088239
  11. J.C. Reubi, Peptide receptors as molecular targets for cancer diagnosis and therapy, Endocr. Rev. 24 (2003) 389-427. https://doi.org/10.1210/er.2002-0007
  12. A. Dimitrakopoulou-Strauss, P. Hohenberger, U. Haberkorn, H.R. Macke, M. Eisenhut, L.G. Strauss, 68Ga-labeled bombesin studies in patients with gastrointestinal stromal tumors: comparison with 18F-FDG, J. Nucl. Med. 48 (2007) 1245-1250. https://doi.org/10.2967/jnumed.106.038091
  13. A. Dimitrakopoulou-Strauss, M. Seiz, J. Tuettenberg, K. Schmieder, M. Eisenhut, U. Haberkorn, L.G. Strauss, Pharmacokinetic studies of (6)(8)Ga-labeled Bombesin ((6)(8) Ga-BZH(3)) and F-18 FDG PET in patients with recurrent gliomas and comparison to grading: preliminary results, Clin. Nucl. Med. 36 (2011) 101-108. https://doi.org/10.1097/RLU.0b013e318203bb24
  14. E. Kahkonen, I. Jambor, J. Kemppainen, K. Lehtio, T.J. Gronroos, A. Kuisma, P. Luoto, H.J. Sipila, T. Tolvanen, K. Alanen, J. Silen, M. Kallajoki, A. Roivainen, N. Schafer, R. Schibli, M. Dragic, A. Johayem, R. Valencia, S. Borkowski, H. Minn, In vivo imaging of prostate cancer using [68Ga]- labeled bombesin analog BAY86-7548, Clin. Cancer Res. 19(2013) 5434-5443. https://doi.org/10.1158/1078-0432.CCR-12-3490
  15. B.R. Sah, I.A. Burger, R. Schibli, M. Friebe, L. Dinkelborg, K. Graham, S. Borkowski, C. Bacher-Stier, R. Valencia, A. Srinivasan, T.F. Hany, L. Mu, P.J. Wild, N.G. Schaefer, Dosimetry and first clinical evaluation of the new 18Fradiolabeled bombesin analogue BAY 864367 in patients with prostate cancer, J. Nucl. Med. 56 (2015) 372-378. https://doi.org/10.2967/jnumed.114.147116
  16. K.L. Chatalic, G.M. Franssen, W.M. van Weerden, W.J. McBride, P. Laverman, E. de Blois, B. Hajjaj, L. Brunel, D.M. Goldenberg, J.A. Fehrentz, J. Martinez, O.C. Boerman, M. de Jong, Preclinical comparison of Al18F- and 68Ga-labeled gastrin-releasing peptide receptor antagonists for PET imaging of prostate cancer, J. Nucl. Med. 55 (2014) 2050-2056. https://doi.org/10.2967/jnumed.114.141143
  17. J.C. Lim, S.H. Dho, E.H. Cho, S.Y. Lee, S.Y. Kim, S.H. Jung, J.C. Kim, Development of a $^{68}Ga$-labeled bombesin analog for gastrin-releasing peptide receptor-expressing prostate tumor imaging, Adv. Tech. Biol. Med. 3 (2015) 135.
  18. P.A. Schubiger, L. Allemann-Tannahill, A. Egli, R. Schibli, R. Alberto, N. Carrel-Remy, M. Willmann, P. Blauenstein, D. Tourwe, Catabolism of neurotensins. Implications for the design of radiolabeling strategies of peptides, Q. J. Nucl. Med. 43 (1999) 155-158.
  19. F. Buchegger, F. Bonvin, M. Kosinski, A.O. Schaffland, J. Prior, J.C. Reubi, P. Blauenstein, D. Tourwe, E. Garcia Garayoa, A. Bischof Delaloye, Radiolabeled neurotensin analog, 99mTc-NT-XI, evaluated in ductal pancreatic adenocarcinoma patients, J. Nucl. Med. 44 (2003) 1649-1654.
  20. E. Garcia-Garayoa, P. Blauenstein, A. Blanc, V. Maes, D. Tourwe, P.A. Schubiger, A stable neurotensin-based radiopharmaceutical for targeted imaging and therapy of neurotensin receptor-positive tumours, Eur. J. Nucl. Med. Mol. Imaging 36 (2009) 37-47. https://doi.org/10.1007/s00259-008-0894-y
  21. B. Brans, O. Linden, F. Giammarile, J. Tennvall, C. Punt, Clinical applications of newer radionuclide therapies, Eur. J. Cancer 42 (2006) 994-1003. https://doi.org/10.1016/j.ejca.2005.12.020
  22. A.C. Froberg, M. de Jong, B.A. Nock, W.A. Breeman, J.L. Erion, T. Maina, M. Verdijsseldonck, W.W. de Herder, A. van der Lugt, P.P. Kooij, E.P. Krenning, Comparison of three radiolabelled peptide analogues for CCK-2 receptor scintigraphy in medullary thyroid carcinoma, Eur, J. Nucl. Med. Mol. Imaging 36 (2009) 1265-1272. https://doi.org/10.1007/s00259-009-1098-9
  23. D. Wild, M. Behe, A. Wicki, D. Storch, B. Waser, M. Gotthardt, B. Keil, G. Christofori, J.C. Reubi, H.R. Macke, [Lys40(Ahx-DTPA-111In)NH2]exendin-4, a very promising ligand for glucagon-like peptide-1 (GLP-1) receptor targeting, J. Nucl. Med. 47 (2006) 2025-2033.
  24. D. Wild, H. Macke, E. Christ, B. Gloor, J.C. Reubi, Glucagonlike peptide 1-receptor scans to localize occult insulinomas, N. Engl. J. Med. 359 (2008) 766-768. https://doi.org/10.1056/NEJMc0802045
  25. E. Christ, D. Wild, F. Forrer, M. Brandle, R. Sahli, T. Clerici, B. Gloor, F. Martius, H. Maecke, J.C. Reubi, Glucagon-like peptide-1 receptor imaging for localization of insulinomas, J. Clin. Endocrinol. Metab. 94 (2009) 4398-4405. https://doi.org/10.1210/jc.2009-1082
  26. R. Haubner, W.A. Weber, A.J. Beer, E. Vabuliene, D. Reim, M. Sarbia, K.F. Becker, M. Goebel, R. Hein, H.J. Wester, H. Kessler, M. Schwaiger, Noninvasive visualization of the activated alphavbeta3 integrin in cancer patients by positron emission tomography and [18F]Galacto-RGD, PLoS Med. 2 (2005) e70. https://doi.org/10.1371/journal.pmed.0020070
  27. M. Janssen, C. Frielink, I. Dijkgraaf, W. Oyen, D.S. Edwards, S. Liu, M. Rajopadhye, L. Massuger, F. Corstens, O. Boerman, Improved tumor targeting of radiolabeled RGD peptides using rapid dose fractionation, Cancer Biother. Radiopharm. 19 (2004) 399-404. https://doi.org/10.1089/cbr.2004.19.399
  28. B.C. Lee, B.S. Moon, J.S. Kim, J.H. Jung, H.S. Park, J.A. Katzenellenbogen, S.E. Kim, Synthesis and biological evaluation of RGD peptides with the $^{99m}Tc/^{188}Re$ chelated iminodiacetate core: highly enhanced uptake and excretion kinetics of theragnosiss against tumor angiogenesis, RSC Adv. 3 (2013) 782-792. https://doi.org/10.1039/C2RA22460G
  29. J.S. Yoo, J. Lee, J.H. Jung, B.S. Moon, S. Kim, B.C. Lee, S.E. Kim, SPECT/CT imaging of high-risk atherosclerotic plaques using integrin-binding RGD dimer peptides, Sci. Rep. 5 (2015) 11752. https://doi.org/10.1038/srep11752
  30. A. Capello, E.P. Krenning, B.F. Bernard, W.A. Breeman, J.L. Erion, M. de Jong, Anticancer activity of targeted proapoptotic peptides, J. Nucl. Med. 47 (2006) 122-129.
  31. Z.B. Li, Z. Wu, K. Chen, E.K. Ryu, X. Chen, 18F-labeled BBNRGD heterodimer for prostate cancer imaging, J. Nucl. Med. 49 (2008) 453-461. https://doi.org/10.2967/jnumed.107.048009
  32. P.M. van Hagen, W.A. Breeman, J.C. Reubi, P.T. Postema, P.J. van den Anker-Lugtenburg, D.J. Kwekkeboom, J. Laissue, B. Waser, S.W. Lamberts, T.J. Visser, E.P. Krenning, Visualization of the thymus by substance P receptor scintigraphy in man, Eur. J. Nucl. Med. 23 (1996) 1508-1513. https://doi.org/10.1007/BF01254476
  33. S. Kneifel, D. Cordier, S. Good, M.C. Ionescu, A. Ghaffari, S. Hofer, M. Kretzschmar, M. Tolnay, C. Apostolidis, B. Waser, M. Arnold, J. Mueller-Brand, H.R. Maecke, J.C. Reubi, A. Merlo, Local targeting of malignant gliomas by the diffusible peptidic vector 1,4,7,10-tetraazacyclododecane-1-glutaric acid-4,7,10-triacetic acidesubstance P, Clin. Cancer Res. 12 (2006) 3843-3850. https://doi.org/10.1158/1078-0432.CCR-05-2820
  34. D. Cordier, F. Forrer, S. Kneifel, M. Sailer, L. Mariani, H. Macke, J. Muller-Brand, A. Merlo, Neoadjuvant targeting of glioblastoma multiforme with radiolabeled DOTAGAsubstance Pdresults from a phase I study, J. Neurooncol. 100 (2010) 129-136. https://doi.org/10.1007/s11060-010-0153-5
  35. P. Theodore Jr., All about Albumin, Elsevier, Amsterdam, 1995.
  36. K.M. Sand, M. Bern, J. Nilsen, H.T. Noordzij, I. Sandlie, J.T. Andersen, Unraveling the interaction between FcRn and albumin: opportunities for design of albumin-based therapeutics, Front. Immunol. 5 (2014) 682.
  37. M.E. Baker, Albumin, steroid hormones and the origin of vertebrates, J. Endocrinol. 175 (2002) 121-127. https://doi.org/10.1677/joe.0.1750121
  38. Y. Matsumura, H. Maeda, A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs, Cancer Res. 46 (1986) 6387-6392.
  39. T.A. Waldmann, Gastrointestinal protein loss demonstrated by Cr-51-labelled albumin, Lancet 2 (1961) 121-123.
  40. C.R. Divgi, N.M. Lisann, S.D. Yeh, R.S. Benua, Technetium-99m albumin scintigraphy in the diagnosis of protein-losing enteropathy, J. Nucl. Med. 27 (1986) 1710-1712.
  41. D.W. Nyman, K.J. Campbell, E. Hersh, K. Long, K. Richardson, V. Trieu, N. Desai, M.J. Hawkins, D.D. Von Hoff, Phase I and pharmacokinetics trial of ABI-007, a novel nanoparticle formulation of paclitaxel in patients with advanced nonhematologic malignancies, J. Clin. Oncol. 23 (2005) 7785-7793. https://doi.org/10.1200/JCO.2004.00.6148
  42. A.M. Merlot, D.S. Kalinowski, D.R. Richardson, Unraveling the mysteries of serum albumin-more than just a serum protein, Front. Physiol. 5 (2014) 299.
  43. F. Kratz, Albumin as a drug carrier: design of prodrugs, drug conjugates and nanoparticles, J. Control. Rel. 132 (2008) 171-183. https://doi.org/10.1016/j.jconrel.2008.05.010
  44. C. Boyer, M.R. Whittaker, V. Bulmus, J. Liu, T.P. Davis, The design and utility of polymer-stabilized iron-oxide nanoparticles for nanomedicine applications, NPG Asia Mater. 2 (2010) 23-30. https://doi.org/10.1038/asiamat.2010.6
  45. M. Di Marco, C. Sadun, M. Port, I. Guilbert, P. Couvreur, C. Dubernet, Physicochemical characterization of ultrasmall superparamagnetic iron oxide particles (USPIO) for biomedical application as MRI contrast agents, Int. J. Nanomed. 2 (2007) 609-622.
  46. J.D. Bronzino, D.R. Peterson, Biomedical signals, imaging, and informatics, in: C. Yuan, W.S. Kerwin, G. Canton, J. Wang, H. Chen, N. Balu (Eds.), Magnetic Resonance Imaging of Atherosclerosis, fourth ed., CRC Press, Boca Raton (FL), 2015, pp. 16-33.
  47. K.J. Widder, R.M. Morris, G. Poore, D.P. Howard Jr., A.E. Senyei, Tumor remission in Yoshida sarcoma-bearing rats by selective targeting of magnetic albumin microspheres containing doxorubicin, Proc. Natl. Acad. Sci. U. S. A. 78 (1981) 579-581. https://doi.org/10.1073/pnas.78.1.579
  48. X. Yang, J.J. Grailer, I.J. Rowland, A. Javadi, S.A. Hurley, V.Z. Matson, D.A. Steeber, S. Gong, Multifunctional stable and pH-responsive polymer vesicles formed by heterofunctional triblock copolymer for targeted anticancer drug delivery and ultrasensitive MR imaging, ACS Nano 4 (2010) 6805-6817. https://doi.org/10.1021/nn101670k
  49. J.R. Hwu, Y.S. Lin, T. Josephrajan, M.H. Hsu, F.Y. Cheng, C.S. Yeh, W.C. Su, D.B. Shieh, Targeted Paclitaxel by conjugation to iron oxide and gold nanoparticles, J. Am. Chem. Soc. 131 (2009) 66-68. https://doi.org/10.1021/ja804947u
  50. T. Lammers, F. Kiessling, W.E. Hennink, G. Storm, Nanotheranostics and image-guided drug delivery: current concepts and future directions, Mol. Pharm. 7 (2010) 1899-1912. https://doi.org/10.1021/mp100228v
  51. C.H. Fan, C.Y. Ting, H.J. Lin, C.H. Wang, H.L. Liu, T.C. Yen, C.K. Yeh, SPIO-conjugated, doxorubicin-loaded microbubbles for concurrent MRI and focused-ultrasound enhanced brain-tumor drug delivery, Biomaterials 34 (2013) 3706-3715. https://doi.org/10.1016/j.biomaterials.2013.01.099
  52. C.M. Lee, S.J. Cheong, E.M. Kim, S.T. Lim, Y.Y. Jeong, M.H. Sohn, H.J. Jeong, Nonpolymeric surface-coated iron oxide nanoparticles for in vivo molecular imaging: biodegradation, biocompatibility, and multiplatform, J. Nucl. Med. 54 (2013) 1974-1980. https://doi.org/10.2967/jnumed.113.122267
  53. H. Zhou, X. Hou, Y. Liu, T. Zhao, Q. Shang, J. Tang, J. Liu, Y. Wang, Q. Wu, Z. Luo, H. Wang, C. Chen, Superstable magnetic nanoparticles in conjugation with near-infrared dye as a multimodal theranostic platform, ACS Appl. Mater. Interfaces 8 (2016) 4424-4433. https://doi.org/10.1021/acsami.5b11308
  54. C.M. Lee, D. Jang, J. Kim, S.J. Cheong, E.M. Kim, M.H. Jeong, S.H. Kim, D.W. Kim, S.T. Lim, M.H. Sohn, Y.Y. Jeong, H.J. Jeong, Oleyl-chitosan nanoparticles based on a dual probe for optical/MR imaging in vivo, Bioconjug. Chem. 22 (2011) 186-192. https://doi.org/10.1021/bc100241a
  55. G. Frens, Controlled nucleation for the regulation of particle size in monodisperse gold suspensions, Nat. Phys. Sci. 241 (1972) 20-22.
  56. S. Hwang, J. Nam, S. Jung, J. Song, H. Doh, S. Kim, Gold nanoparticle-mediated photothermal therapy: current status and future perspective, Nanomedicine (Lond) 9 (2014) 2003-2022. https://doi.org/10.2217/nnm.14.147
  57. X. Huang, M.A. El-Sayeda, Plasmonic photo-thermal therapy (PPTT), Alexandria J. Med. 47 (2011) 1-9. https://doi.org/10.1016/j.ajme.2011.01.001
  58. Z. Li, H. Huang, S. Tang, Y. Li, X.F. Yu, H. Wang, P. Li, Z. Sun, H. Zhang, C. Liu, P.K. Chu, Small gold nanorods laden macrophages for enhanced tumor coverage in photothermal therapy, Biomaterials 74 (2016) 144-154. https://doi.org/10.1016/j.biomaterials.2015.09.038
  59. J.G. Piao, L. Wang, F. Gao, Y.Z. You, Y. Xiong, L. Yang, Erythrocyte membrane is an alternative coating to polyethylene glycol for prolonging the circulation lifetime of gold nanocages for photothermal therapy, ACS Nano 8 (2014) 10414-10425. https://doi.org/10.1021/nn503779d
  60. A.K. Rengan, A.B. Bukhari, A. Pradhan, R. Malhotra, R. Banerjee, R. Srivastava, A. De, In vivo analysis of biodegradable liposome gold nanoparticles as efficient agents for photothermal therapy of cancer, Nano Lett. 15 (2015) 842-848. https://doi.org/10.1021/nl5045378
  61. Q.K. Ng, C.I. Olariu, M. Yaffee, V.F. Taelman, N. Marincek, T. Krause, L. Meier, M.A. Walter, Indium-111 labeled gold nanoparticles for in-vivo molecular targeting, Biomaterials 35 (2014) 7050-7057. https://doi.org/10.1016/j.biomaterials.2014.04.098
  62. J. Zhu, J. Chin, C. Wangler, B. Wangler, R.B. Lennox, R. Schirrmacher, Rapid (18)F-labeling and loading of PEGylated gold nanoparticles for in vivo applications, Bioconjug. Chem. 25 (2014) 1143-1150. https://doi.org/10.1021/bc5001593
  63. A. Vilchis-Juarez, G. Ferro-Flores, C. Santos-Cuevas, E. Morales-Avila, B. Ocampo-Garcia, L. Diaz-Nieto, M. Luna-Gutierrez, N. Jimenez-Mancilla, M. Pedraza-Lopez, L. Gomez-Olivan, Molecular targeting radiotherapy with cyclo- RGDFK(C) peptides conjugated to 177Lu-labeled gold nanoparticles in tumor-bearing mice, J. Biomed. Nanotechnol. 10 (2014) 393-404. https://doi.org/10.1166/jbn.2014.1721
  64. C.B. Murray, D.J. Norris, M.G. Bawendi, Synthesis and characterization of nearly monodisperse CdE (E = sulfur, selenium, tellurium) semiconductor nanocrystallites, J. Am. Chem. Soc. 115 (1993) 8706-8715. https://doi.org/10.1021/ja00072a025
  65. W.K. Chung Leland, W.B. Isaacs, J.W. Simons, Prostate cancer: biology, genetics, and the new therapeutics, in: X. Gao, Y. Xing, W.K. Chung Leland, S. Nie (Eds.), Quantum Dot Nanotechnology for Prostate cancer Research, Human Press, New Jersey, 2007, p. 231.
  66. R. Savla, O. Taratula, O. Garbuzenko, T. Minko, Tumor targeted quantum dot-mucin 1 aptamer-doxorubicin conjugate for imaging and treatment of cancer, J. Control. Rel. 153 (2011) 16-22. https://doi.org/10.1016/j.jconrel.2011.02.015
  67. H.S. Han, E. Niemeyer, Y. Huang, W.S. Kamoun, J.D. Martin, J. Bhaumik, Y. Chen, S. Roberge, J. Cui, M.R. Martin, D. Fukumura, R.K. Jain, M.G. Bawendi, D.G. Duda, Quantum dot/antibody conjugates for in vivo cytometric imaging in mice, Proc. Natl. Acad. Sci. U. S. A. 112 (2015) 1350-1355. https://doi.org/10.1073/pnas.1421632111
  68. S. Sonali, R.P. Singh, N. Singh, G. Sharma, M.R. Vijayakumar, B. Koch, S. Singh, U. Singh, D. Dash, B.L. Pandey, M.S. Muthu, Transferrin liposomes of docetaxel for brain-targeted cancer applications: formulation and brain theranostics, Drug Deliv. (2016) 1-11.
  69. H. Zhu, S. Zhang, Y. Ling, G. Meng, Y. Yang, W. Zhang, pHresponsive hybrid quantum dots for targeting hypoxic tumor siRNA delivery, J. Control. Rel. 220 (2015) 529-544. https://doi.org/10.1016/j.jconrel.2015.11.017
  70. X. Liang, B. Shi, K. Wang, M. Fan, D. Jiao, J. Ao, N. Song, C. Wang, J. Gu, Z. Li, Development of self-assembling peptide nanovesicle with bilayers for enhanced EGFR-targeted drug and gene delivery, Biomaterials 82 (2016) 194-207. https://doi.org/10.1016/j.biomaterials.2015.12.015
  71. W. Yin, C.W. Kimbrough, J.G. Gomez-Gutierrez, C.T. Burns, P. Chuong, W.E. Grizzle, L.R. McNally, Tumor specific liposomes improve detection of pancreatic adenocarcinoma in vivo using optoacoustic tomography, J. Nanobiotechnol. 13 (2015) 90. https://doi.org/10.1186/s12951-015-0139-8
  72. H.S. Jeong, C.M. Lee, S.J. Cheong, E.M. Kim, H. Hwang, K.S. Na, S.T. Lim, M.H. Sohn, H.J. Jeong, The effect of mannosylation of liposome-encapsulated indocyanine green on imaging of sentinel lymph node, J. Liposome Res. 23 (2013) 291-297. https://doi.org/10.3109/08982104.2013.801488
  73. H.S. Jeong, K.S. Na, H. Hwang, P.S. Oh, D.H. Kim, S.T. Lim, M.H. Sohn, H.J. Jeong, Effect of space length of mannose ligand on uptake of mannosylated liposome in RAW 264.7 cells: in vitro and in vivo studies, J. Biomed. Mater. Res. A 102 (2014) 4545-4553.
  74. M.A. Fischbach, J.A. Bluestone, W.A. Lim, Cell-based therapeutics: the next pillar of medicine, Sci. Transl. Med. 5 (2013) 179ps7.
  75. J.E. Kim, B.C. Ahn, H.W. Lee, M.H. Hwang, S.H. Shin, S.W. Lee, Y.K. Sung, J. Lee, In vivo monitoring of survival and proliferation of hair stem cells in a hair follicle generation animal model, Mol. Imaging 12 (2013) 310-317.
  76. S.S. Yaghoubi, M.C. Jensen, N. Satyamurthy, S. Budhiraja, D. Paik, J. Czernin, S.S. Gambhir, Noninvasive detection of therapeutic cytolytic T cells with 18F-FHBG PET in a patient with glioma, Nat. Clin. Pract. Oncol. 6 (2009) 53-58. https://doi.org/10.1038/ncponc1278
  77. B.C. Ahn, Applications of molecular imaging in drug discovery and development process, Curr. Pharm. Biotechnol. 12 (2011) 459-468. https://doi.org/10.2174/138920111795163904
  78. B.C. Ahn, N. Parashurama, M. Patel, K. Ziv, S. Bhaumik, S.S. Yaghoubi, R. Paulmurugan, S.S. Gambhir, Noninvasive reporter gene imaging of human Oct4 (pluripotency) dynamics during the differentiation of embryonic stem cells in living subjects, Mol. Imaging Biol. 16 (2014) 865-876. https://doi.org/10.1007/s11307-014-0744-1
  79. H.W. Lee, S.Y. Yoon, T.D. Singh, Y.J. Choi, H.J. Lee, J.Y. Park, S.Y. Jeong, S.W. Lee, J.H. Ha, B.C. Ahn, Y.H. Jeon, J. Lee, Tracking of dendritic cell migration into lymph nodes using molecular imaging with sodium iodide symporter and enhanced firefly luciferase genes, Sci. Rep. 14 (2015) 9865.
  80. R.J. Creusot, S.S. Yaghoubi, P. Chang, J. Chia, C.H. Contag, S.S. Gambhir, C.G. Fathman, Lymphoid-tissue-specific homing of bone-marrow-derived dendritic cells, Blood 113 (2009) 6638-6647. https://doi.org/10.1182/blood-2009-02-204321
  81. X. Yu, D. Chen, Y. Zhang, X. Wu, Z. Huang, H. Zhou, Y. Zhang, Z. Zhang, Overexpression of CXCR4 in mesenchymal stem cells promotes migration, neuroprotection and angiogenesis in a rat model of stroke, J. Neurol. Sci. 316 (2012) 141-149. https://doi.org/10.1016/j.jns.2012.01.001
  82. J. Zhao, J. Vykoukal, M. Abdelsalam, A. Recio-Boiles, Q. Huang, Y. Qiao, B. Singhana, M. Wallace, R. Avritscher, M.P. Melancon, Stem cell-mediated delivery of SPIO-loaded gold nanoparticles for the theranosis of liver injury and hepatocellular carcinoma, Nanotechnology 25 (2014) 405101. https://doi.org/10.1088/0957-4484/25/40/405101

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