Imaging of cells and nanoparticles: Implications for drug delivery to the brain

Pharmaceutical Research

Volumn 29, Issue 12, 2012, Pages 3213-3234

  Stojanov, Katica ^a   Zuhorn, Inge S ^a   Dierckx, Rudi A J O ^b   De Vries, Erik F J ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Brain; Drug delivery; Imaging; Nanocarriers; Stem cells

Indexed keywords

8 QUINOLINOL INDIUM IN 111; FLUORODEOXYGLUCOSE F 18; GADODIAMIDE; GADOLINIUM PENTETATE; GADOLINIUM PENTETATE MEGLUMINE; GADOTERIDOL; HEXAMETHYLPROPYLENE AMINE OXIME TECHNETIUM TC 99M; LIPOFECTAMINE; LIPOSOME; LUCIFERASE; MAGNETIC NANOPARTICLE; NANOCARRIER; NANOPARTICLE; PENTETATE INDIUM IN 111; POLYLYSINE; PROTAMINE SULFATE; QUANTUM DOT; SMALL INTERFERING RNA; SOLID LIPID NANOPARTICLE; SUPERPARAMAGNETIC IRON OXIDE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE;

ANTINEOPLASTIC ACTIVITY; AUTORADIOGRAPHY; BIOLUMINESCENCE; BLOOD BRAIN BARRIER; CELL LABELING; CONFOCAL MICROSCOPY; CONVECTION ENHANCED DELIVERY; DRUG DELIVERY SYSTEM; DRUG PENETRATION; EX VIVO STUDY; EXOSOME; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; GLIOMA; HUMAN; IMAGING; IN VIVO STUDY; ISOTOPE LABELING; NEURAL STEM CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REPORTER GENE; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; STEM CELL GENE THERAPY;

ANIMALS; BRAIN; CONTRAST MEDIA; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; FLUORESCENT DYES; GENES, REPORTER; HUMANS; MAGNETIC RESONANCE IMAGING; NANOPARTICLES; OPTICAL IMAGING; POSITRON-EMISSION TOMOGRAPHY; RADIOISOTOPES; STAINING AND LABELING; TISSUE DISTRIBUTION; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 84872066573     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-012-0826-1     Document Type: Review

References (178)

1. Misra A, Ganesh S, Shahiwala A, Shah SP. Drug delivery to the central nervous system: a review. J Pharm Pharm Sci. 2003;6(2):252-73. (Pubitemid 37207232)
2. Krauze MT, McKnight TR, Yamashita Y, Bringas J, Noble CO, Saito R, et al. Real-time visualization and characterization of liposomal delivery into the monkey brain by magnetic resonance imaging. Brain Res Brain Res Protoc. 2005;16(1-3):20-6. (Pubitemid 41774067)
3. Gogel S, Gubernator M, Minger SL. Progress and prospects: stem cells and neurological diseases. Gene Ther. 2011;18(1):1-6.
4. Pardridge WM. Blood-brain barrier drug targeting: the future of brain drug development. Mol Interv. 2003;3(2):90-105. 151.
5. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJA. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotech. 2011;29(4):341-5.
6. Tiwari SB, Amiji MM. A review of nanocarrier-based CNS delivery systems. Curr Drug Deliv. 2006;3(2):219-32. (Pubitemid 43738987)
7. Moos T, Morgan EH. Restricted transport of anti-transferrin receptor antibody (OX26) through the blood-brain barrier in the rat. J Neurochem. 2001;79(1):119-29. (Pubitemid 32946649)
8. Duffy KR, Pardridge WM. Blood-brain barrier transcytosis of insulin in developing rabbits. Brain Res. 1987;420(1):32-8. (Pubitemid 17151294)
9. Georgieva JV, Brinkhuis RP, Stojanov K, Weijers CAGM, Zuilhof H, Rutjes FPJT, et al. Peptide-mediated blood-brain barrier transport of polymersomes. Angew Chem Int Ed Engl. 2012. doi:10.1002/anie.201202001
10. Kanwar JR, Sun X, Punj V, Sriramoju B, Mohan RR, Zhou SF, et al. Nanoparticles in the treatment and diagnosis of neurological disorders: untamed dragon with fire power to heal. Nanomedicine. 2012;8(4):399-14.
11. Tang Y, Shah K, Messerli SM, Snyder E, Breakefield X, Weissleder R. In vivo tracking of neural progenitor cell migration to glioblastomas. Hum Gene Ther. 2003;14(13):1247-54. (Pubitemid 37034574)
12. Bjugstad KB, Redmond Jr DE, Teng YD, Elsworth JD, Roth RH, Blanchard BC, et al. Neural stem cells implanted into MPTP-treated monkeys increase the size of endogenous tyrosine hydroxylase-positive cells found in the striatum: a return to control measures. Cell Transplant. 2005;14(4):183-92. (Pubitemid 40677148)
13. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci U S A. 2004;101(32):11839-44. (Pubitemid 39095381)
14. Muller FJ, Snyder EY, Loring JF. Gene therapy: can neural stem cells deliver? Nat Rev Neurosci. 2006;7(1):75-84. (Pubitemid 41828933)
15. Fischer UM, Harting MT, Jimenez F, Monzon-Posadas WO, Xue H, Savitz SI, et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev. 2009;18(5):683-92.
16. Harting MT, Jimenez F, Xue H, Fischer UM, Baumgartner J, Dash PK, et al. Intravenous mesenchymal stem cell therapy for traumatic brain injury. J Neurosurg. 2009;110(6):1189-97.
17. Stojanov K, de Vries EF, Hoekstra D, van Waarde A, Dierckx RA, Zuhorn IS. [18F]FDG labeling of neural stem cells for in vivo cell tracking with positron emission tomography: inhibition of tracer release by phloretin. Mol Imaging. 2012;11(1):1-12
18. Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs. 2001;169(1):12-20. (Pubitemid 32437040)
19. Talbott JF, Cao Q, Bertram J, Nkansah M, Benton RL, Lavik E, et al. CNTF promotes the survival and differentiation of adult spinal cord-derived oligodendrocyte precursor cells in vitro but fails to promote remyelination in vivo. Exp Neurol. 2007;204(1):485-9. (Pubitemid 46330291)
20. Ozeki T, Kaneko D, Hashizawa K, Imai Y, Tagami T, Okada H. Improvement of survival in C6 rat glioma model by a sustained drug release from localized PLGA microspheres in a thermoreversible hydrogel. Int J Pharm. 2012;427(2):299-304.
21. Jones AR, Shusta EV. Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm Res. 2007;24(9):1759-71. (Pubitemid 47206625)
22. Charlton ST, Whetstone J, Fayinka ST, Read KD, Illum L, Davis SS. Evaluation of direct transport pathways of glycine receptor antagonists and an angiotensin antagonist from the nasal cavity to the central nervous system in the rat model. Pharm Res. 2008;25(7):1531-43.
23. Semete B, Booysen L, Lemmer Y, Kalombo L, Katata L, Verschoor J, et al. In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems. Nanomedicine. 2010;6(5):662-71.
24. Mendez I, Sanchez-Pernaute R, Cooper O, Vinuela A, Ferrari D, Bjorklund L, et al. Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinson's disease. Brain. 2005;128(Pt 7):1498-510. (Pubitemid 41373670)
25. Ding H, Inoue S, Ljubimov AV, Patil R, Portilla-Arias J, Hu J, et al. Inhibition of brain tumor growth by intravenous poly (beta-L-malic acid) nanobioconjugate with pH-dependent drug release [corrected]. Proc Natl Acad Sci U S A. 2010;107(42):18143-8.
26. Giesel FL, Stroick M, Griebe M, Troster H, von der Lieth CW, Requardt M, et al. Gadofluorine m uptake in stem cells as a new magnetic resonance imaging tracking method: an in vitro and in vivo study. Invest Radiol. 2006;41(12):868-73. (Pubitemid 44747114)
27. Allen TM, Mumbengegwi DR, Charrois GJ. Anti-CD19-targeted liposomal doxorubicin improves the therapeutic efficacy in murine B-cell lymphoma and ameliorates the toxicity of liposomes with varying drug release rates. Clin Cancer Res. 2005;11(9):3567-73. (Pubitemid 40627913)
28. Pirko I, Fricke ST, Johnson AJ, Rodriguez M, Macura SI. Magnetic resonance imaging, microscopy, and spectroscopy of the central nervous system in experimental animals. NeuroRx. 2005;2(2):250-64. (Pubitemid 40471436)
29. Delikatny EJ, Poptani H. MR techniques for in vivo molecular and cellular imaging. Radiol Clin North Am. 2005;43(1):205-20. (Pubitemid 40326569)
30. Choy G, Choyke P, Libutti SK. Current advances in molecular imaging: noninvasive in vivo bioluminescent and fluorescent optical imaging in cancer research. Mol Imaging. 2003;2(4):303-12.
31. Weissleder R and Ntziachristos V. Shedding light onto live molecular targets. Nat Med. 2003;9(1):123-8. (Pubitemid 36098273)
32. Rao J, Dragulescu-Andrasi A, Yao H. Fluorescence imaging in vivo: recent advances. Curr Opin Biotechnol. 2007;18(1):17-25. (Pubitemid 46237739)
33. Zacharakis G, Kambara H, Shih H, Ripoll J, Grimm J, Saeki Y, et al. Volumetric tomography of fluorescent proteins through small animals in vivo. Proc Natl Acad Sci U S A. 2005;102(51):18252-7. (Pubitemid 43011213)
34. Ntziachristos V, Ripoll J, Wang LV, Weissleder R. Looking and listening to light: the evolution of whole-body photonic imaging. Nat Biotechnol. 2005;23(3):313-20. (Pubitemid 41094419)
35. Doyle TC, Burns SM, Contag CH. In vivo bioluminescence imaging for integrated studies of infection. Cell Microbiol. 2004;6(4):303-17. (Pubitemid 38379814)
36. Michelini E, Cevenini L, Mezzanotte L, Roda A. Luminescent probes and visualization of bioluminescence. Methods Mol Biol. 2009;574:1-13.
37. Chatziioannou AF. Instrumentation for molecular imaging in preclinical research: micro-PET and Micro-SPECT. Proc Am Thorac Soc. 2005;2(6):533-6. 510-511. (Pubitemid 43128025)
38. Rahmim Aand Zaidi H. PET versus SPECT: strengths, limitations and challenges. Nucl Med Commun. 2008;29(3):193-207.
39. Franc BL, Acton PD, Mari C, Hasegawa BH. Small-animal SPECT and SPECT/CT: important tools for preclinical investigation. J Nucl Med. 2008;49(10):1651-63.
40. Shen J, Cheng LN, Zhong XM, Duan XH, Guo RM, Hong GB. Efficient in vitro labeling rabbit neural stem cell with paramagnetic Gd-DTPA and fluorescent substance. Eur J Radiol. 2010;75(3):397-405.
41. Cheng LN, Duan XH, Zhong XM, Guo RM, Zhang F, Zhou CP, et al. Transplanted neural stem cells promote nerve regeneration in acute peripheral nerve traction injury: assessment using MRI. AJR Am J Roentgenol. 2011;196(6):1381-7.
42. Modo M, Cash D, Mellodew K, Williams SC, Fraser SE, Meade TJ, et al. Tracking transplanted stem cell migration using bifunctional, contrast agent-enhanced, magnetic resonance imaging. Neuroimage. 2002;17(2):803-11. (Pubitemid 35317014)
43. Modo M, Mellodew K, Cash D, Fraser SE, Meade TJ, Price J, et al. Mapping transplanted stem cell migration after a stroke: a serial, in vivo magnetic resonance imaging study. Neuroimage. 2004;21(1):311-7. (Pubitemid 38115022)
44. Arbab AS, Yocum GT, Wilson LB, Parwana A, Jordan EK, Kalish H, et al. Comparison of transfection agents in forming complexes with ferumoxides, cell labeling efficiency, and cellular viability. Mol Imaging. 2004;3(1):24-32.
45. Modo M, Hoehn M, Bulte JW. Cellular MR imaging. Mol Imaging. 2005;4(3):143-64. (Pubitemid 43143788)
46. Montet-Abou K, Montet X, Weissleder R, Josephson L. Transfection agent induced nanoparticle cell loading. Mol Imaging. 2005;4(3):165-71. (Pubitemid 43143789)
47. Kustermann E, Himmelreich U, Kandal K, Geelen T, Ketkar A, Wiedermann D, et al. Efficient stem cell labeling for MRI studies. Contrast Media Mol Imaging. 2008;3(1):27-37. (Pubitemid 351493976)
48. Zhu J, Zhou L, XingWu F. Tracking neural stem cells in patients with brain trauma. N Engl J Med. 2006;355(22):2376-8. (Pubitemid 44837805)
49. Politi LS, Bacigaluppi M, Brambilla E, Cadioli M, Falini A, Comi G, et al. Magnetic-resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis. Stem Cells. 2007;25(10):2583-92. (Pubitemid 47582751)
50. Walczak P, Kedziorek DA, Gilad AA, Lin S, Bulte JW. Instant MR labeling of stem cells using magnetoelectroporation. Magn Reson Med. 2005;54(4):769-74. (Pubitemid 41457046)
51. Shapiro EM, Skrtic S, Sharer K, Hill JM, Dunbar CE, Koretsky AP. MRI detection of single particles for cellular imaging. Proc Natl Acad Sci U S A. 2004;101(30):10901-6. (Pubitemid 38989558)
52. Hinds KA, Hill JM, Shapiro EM, Laukkanen MO, Silva AC, Combs CA, et al. Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells. Blood. 2003;102(3):867-72. (Pubitemid 36917777)
53. Michalet X, Pinaud FF, Bentolila LA, Tsay JM, Doose S, Li JJ, et al. Quantum dots for live cells, in vivo imaging, and diagnostics. Science. 2005;307(5709):538-44. (Pubitemid 40165671)
54. Lin S, Xie X, Patel MR, Yang YH, Li Z, Cao F, et al. Quantum dot imaging for embryonic stem cells. BMC Biotechnol. 2007;7:67.
55. So MK, Xu C, Loening AM, Gambhir SS, Rao J. Selfilluminating quantum dot conjugates for in vivo imaging. Nat Biotechnol. 2006;24(3):339-43. (Pubitemid 43372158)
56. Pichler A, Prior JL, Piwnica-Worms D. Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine. Proc Natl Acad Sci U S A. 2004;101(6):1702-7. (Pubitemid 38234218)
57. Elhami E, Goertzen AL, Xiang B, Deng J, Stillwell C, Mzengeza S, et al. Viability and proliferation potential of adipose-derived stem cells following labeling with a positron-emitting radiotracer. Eur J Nucl Med Mol Imaging. 2011;38(7):1323-34.
58. Botti C, Negri DR, Seregni E, Ramakrishna V, Arienti F, Maffioli L, et al. Comparison of three different methods for radiolabelling human activated T lymphocytes. Eur J Nucl Med. 1997;24(5):497-504. (Pubitemid 27239207)
59. Adonai N, Nguyen KN, Walsh J, Iyer M, Toyokuni T, Phelps ME, et al. Ex vivo cell labeling with 64Cu-pyruvaldehyde-bis (N4-methylthiosemicarbazone) for imaging cell trafficking in mice with positron-emission tomography. Proc Natl Acad Sci U S A. 2002;99(5):3030-5. (Pubitemid 34240580)
60. Ma B, Hankenson KD, Dennis JE, Caplan AI, Goldstein SA, Kilbourn MR. A simple method for stem cell labeling with fluorine 18. Nucl Med Biol. 2005;32(7):701-5. (Pubitemid 41502975)
61. 64Cu-labeled PEGylated polyethylenimine for cell trafficking and tumor imaging. Mol Imaging Biol. 2009;11(6):415-23.
62. Chen K, Miao Z, Cheng Z. In vivo PET imaging to track mesenchymal stem cells labelled with copper-64-pyruvaldehyde-bis (N4-methylthiosemicarbazone). J Nucl Med Meeting Abstracts. 2011;52(1-MeetingAbstracts):521.
63. 18F-FDG. Nucl Med Biol. 2009;36(5):545-9.
64. Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A, et al. Systemic delivery of bone marrow-derived mesenchymal stem cells tothe infarcted myocardium: feasibility, cell migration, and body distribution. Circulation. 2003;108(7):863-8. (Pubitemid 37022130)
65. Nowak B, Weber C, Schober A, Zeiffer U, Liehn EA, von Hundelshausen P, et al. Indium-111 oxine labelling affects the cellular integrity of haematopoietic progenitor cells. Eur J Nucl Med Mol Imaging. 2007;34(5):715-21. (Pubitemid 46669358)
66. Jin Y, Kong H, Stodilka RZ, Wells RG, Zabel P, Merrifield PA, et al. Determining the minimum number of detectable cardiactransplanted 111In-tropolone-labelled bone-marrow-derived mesenchymal stem cells by SPECT. Phys Med Biol. 2005;50(19):4445-55. (Pubitemid 41361509)
67. Bindslev L, Haack-Sorensen M, Bisgaard K, Kragh L, Mortensen S, Hesse B, et al. Labelling of human mesenchymal stem cells with indium-111 for SPECT imaging: effect on cell proliferation and differentiation. Eur J Nucl Med Mol Imaging. 2006;33(10):1171-7. (Pubitemid 44484473)
68. Aicher A, Brenner W, Zuhayra M, Badorff C, Massoudi S, Assmus B, et al. Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling. Circulation. 2003;107(16):2134-9. (Pubitemid 36532196)
69. + hematopoietic progenitor cells in a rat myocardial infarction model. J Nucl Med. 2004;45(3):512-8. (Pubitemid 47618629)
70. Kuyama J, McCormack A, George AJ, Heelan BT, Osman S, Batchelor JR, et al. Indium-111 labelled lymphocytes: isotope distribution and cell division. Eur J Nucl Med. 1997;24(5):488-96. (Pubitemid 27239206)
71. Eggert AA, Schreurs MW, Boerman OC, Oyen WJ, de Boer AJ, Punt CJ, et al. Biodistribution and vaccine efficiency of murine dendritic cells are dependent on the route of administration. Cancer Res. 1999;59(14):3340-5. (Pubitemid 29334488)
72. Bestor TH. Gene silencing as a threat to the success of gene therapy. J Clin Invest. 2000;105(4):409-11. (Pubitemid 30127239)
73. Gilad AA, Ziv K, McMahon MT, van Zijl PC, Neeman M, Bulte JW. MRI reporter genes. J Nucl Med. 2008;49(12):1905-8.
74. Cohen B, Dafni H, Meir G, Harmelin A, Neeman M. Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia. 2005;7(2):109-17. (Pubitemid 40315988)
75. Genove G, DeMarco U, Xu H, Goins WF, Ahrens ET. A new transgene reporter for in vivo magnetic resonance imaging. Nat Med. 2005;11(4):450-4. (Pubitemid 40562338)
76. Nakamura C, Burgess JG, Sode K, Matsunaga T. An ironregulated gene, magA, encoding an iron transport protein of Magnetospirillum sp. strain AMB-1. J Biol Chem. 1995;270(47):28392-6.
77. Nakamura C, Kikuchi T, Burgess JG, Matsunaga T. Ironregulated expression and membrane localization of the magA protein in Magnetospirillum sp. strain AMB-1. J Biochem. 1995;118(1):23-7.
78. Zurkiya O, Chan AW, Hu X. MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magn Reson Med. 2008;59(6):1225-31. (Pubitemid 351813249)
79. Boulnois J-L. Photophysical processes in recent medical laser developments: a review. Lasers Med Sci. 1986;1(1):47-66. (Pubitemid 17145870)
80. Deliolanis NC, Wurdinger T, Pike L, Tannous BA, Breakefield XO, Weissleder R, et al. In vivo tomographic imaging of red-shifted fluorescent proteins. Biomed Opt Express. 2011;2(4):887-900.
81. Roda A, Guardigli M, Michelini E, Mirasoli M. Nanobioanalytical luminescence: forster-type energy transfer methods. Anal Bioanal Chem. 2009;393(1):109-23. (Pubitemid 50305067)
82. de Almeida PE, van Rappard JR, Wu JC. In vivo bioluminescence for tracking cell fate and function. Am J Physiol Heart Circ Physiol. 2011;301(3):H663-71.
83. Sher F, van Dam G, Boddeke E, Copray S. Bioluminescence imaging of Olig2-neural stem cells reveals improved engraftment in a demyelination mouse model. Stem Cells. 2009;27(7):1582-91.
84. Zhang Y, Bressler JP, Neal J, Lal B, Bhang HE, Laterra J, et al. ABCG2/BCRP expression modulates D-Luciferin based bioluminescence imaging. Cancer Res. 2007;67(19):9389-97. (Pubitemid 47535929)
85. Meighen EA. Molecular biology of bacterial bioluminescence. Microbiol Rev. 1991;55(1):123-42. (Pubitemid 21895148)
86. Close DM, Patterson SS, Ripp S, Baek SJ, Sanseverino J, Sayler GS. Autonomous bioluminescent expression of the bacterial luciferase gene cassette (lux) in a mammalian cell line. PLoS One. 2010;5(8):e12441.
87. Acton PD, Zhou R. Imaging reporter genes for cell tracking with PET and SPECT. QJ Nucl Med Mol Imaging. 2005;49(4):349-60. (Pubitemid 43246284)
88. Vandeputte C, Evens N, Toelen J, Deroose CM, Bosier B, Ibrahimi A, et al. A PET brain reporter gene system based on type 2 cannabinoid receptors. J Nucl Med. 2011;52(7):1102-9.
89. Maresz K, Carrier EJ, Ponomarev ED, Hillard CJ, Dittel BN. Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli. J Neurochem. 2005;95(2):437-45. (Pubitemid 41457512)
90. Unger EC, MacDougall P, Cullis P, Tilcock C. Liposomal Gd-DTPA: effect of encapsulation on enhancement of hepatoma model by MRI. Magn Reson Imaging. 1989;7(4):417-23. (Pubitemid 20021972)
91. Saito R, Bringas JR, McKnight TR, Wendland MF, Mamot C, Drummond DC, et al. Distribution of liposomes into brain and rat brain tumor models by convection-enhanced delivery monitored with magnetic resonance imaging. Cancer Res. 2004;64(7):2572-9. (Pubitemid 38523915)
92. Saito R, Krauze MT, Bringas JR, Noble C, McKnight TR, Jackson P, et al. Gadolinium-loaded liposomes allow for real-time magnetic resonance imaging of convection-enhanced delivery in the primate brain. Exp Neurol. 2005;196(2):381-9. (Pubitemid 41607827)
93. Kabalka G, Buonocore E, Hubner K, Moss T, Norley N, Huang L. Gadolinium-labeled liposomes: targeted MR contrast agents for the liver and spleen. Radiology. 1987;163(1):255-8. (Pubitemid 17043038)
94. Kozlowska D, Foran P, MacMahon P, Shelly MJ, Eustace S, O'Kennedy R. Molecular and magnetic resonance imaging: the value of immunoliposomes. Adv Drug Deliv Rev. 2009;61(15):1402-11.
95. Elmi MM, Sarbolouki MN. A simple method for preparation of immuno-magnetic liposomes. Int J Pharm. 2001;215(1-2):45-50. (Pubitemid 32206602)
96. Martina MS, Fortin JP, Menager C, Clement O, Barratt G, Grabielle-Madelmont C, et al. Generation of superparamagnetic liposomes revealed as highly efficient MRI contrast agents for in vivo imaging. J Am Chem Soc. 2005;127(30):10676-85. (Pubitemid 41061441)
97. Hickey RJ, Haynes AS, Kikkawa JM, Park SJ. Controlling the self-assembly structure of magnetic nanoparticles and amphiphilic block-copolymers: from micelles to vesicles. J Am Chem Soc. 2011;133(5):1517-25.
98. Sanson C, Diou O, Thevenot J, Ibarboure E, Soum A, Brulet A, et al. Doxorubicin loaded magnetic polymersomes: theranostic nanocarriers for MR imaging and magneto-chemotherapy. ACS Nano. 2011;5(2):1122-40.
99. Hadaczek P, Yamashita Y, Mirek H, Tamas L, Bohn MC, Noble C, et al. The "perivascular pump" driven by arterial pulsation is a powerful mechanism for the distribution of therapeutic molecules within the brain. Mol Ther. 2006;14(1):69-78. (Pubitemid 43922142)
100. Lu W, Zhang Y, Tan YZ, Hu KL, Jiang XG, Fu SK. Cationic albumin-conjugated pegylated nanoparticles as novel drug carrier for brain delivery. J Control Release. 2005;107(3):428-48. (Pubitemid 41393353)
101. Pang Z, Lu W, Gao H, Hu K, Chen J, Zhang C, et al. Preparation and brain delivery property of biodegradable polymersomes conjugated with OX26. J Control Release. 2008;128(2):120-7.
102. Deissler V, Ruger R, Frank W, Fahr A, Kaiser WA, Hilger I. Fluorescent liposomes as contrast agents for in vivo optical imaging of edemas in mice. Small. 2008;4(8):1240-6.
103. He X, Na MH, Kim JS, Lee GY, Park JY, Hoffman AS, et al. A novel peptide probe for imaging and targeted delivery of liposomal doxorubicin to lung tumor. Mol Pharm. 2011;8(2):430-8.
104. Nobs L, Buchegger F, Gurny R, Allemann E. Current methods for attaching targeting ligands to liposomes and nanoparticles. J Pharm Sci. 2004;93(8):1980-92. (Pubitemid 39045480)
105. Harrington KJ, Rowlinson-Busza G, Syrigos KN, Uster PS, Vile RG, Stewart JS. Pegylated liposomes have potential as vehicles for intratumoral and subcutaneous drug delivery. Clin Cancer Res. 2000;6(6):2528-37. (Pubitemid 30399225)
106. Levchenko TS, Rammohan R, Lukyanov AN, Whiteman KR, Torchilin VP. Liposome clearance in mice: the effect of a separate and combined presence of surface charge and polymer coating. Int J Pharm. 2002;240(1-2):95-102. (Pubitemid 34607706)
107. Phillips WT, Goins BA, Bao A. Radioactive liposomes. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2009;1(1):69-83.
108. Andreozzi E, Seo JW, Ferrara K, Louie A. Novel method to label solid lipid nanoparticles with 64cu for positron emission tomography imaging. Bioconjug Chem. 2011;22(4):808-18.
109. Harivardhan Reddy L, Sharma RK, Chuttani K, Mishra AK, Murthy RS. Influence of administration route on tumor uptake and biodistribution of etoposide loaded solid lipid nanoparticles in Dalton's lymphoma tumor bearing mice. J Control Release. 2005;105(3):185-98. (Pubitemid 40941985)
110. Upadhyay KK, Bhatt AN, Castro E, Mishra AK, Chuttani K, Dwarakanath BS, et al. In vitro and in vivo evaluation of docetaxel loaded biodegradable polymersomes. Macromol Biosci. 2010;10(5):503-12.
111. Brinkhuis RP, Stojanov K, Laverman P, Eilander J, Zuhorn IS, Rutjes FP, et al. Size dependent biodistribution and SPECT imaging of 111In-labeled polymersomes. Bioconjug Chem. 2012. doi:10.1021/bc200578s
112. Chertok B, Cole AJ, David AE, Yang VC. Comparison of electron spin resonance spectroscopy and inductively-coupled plasma optical emission spectroscopy for biodistribution analysis of iron-oxide nanoparticles. Mol Pharm. 2010;7(2):375-85.
113. Wenger Y, Schneider 2nd RJ, Reddy GR, Kopelman R, Jolliet O, Philbert MA. Tissue distribution and pharmacokinetics of stable polyacrylamide nanoparticles following intravenous injection in the rat. Toxicol Appl Pharmacol. 2011;251(3):181-90.
114. Calvo P, Gouritin B, Chacun H, Desmaele D, D'Angelo J, Noel JP, et al. Long-circulating PEGylated polycyanoacrylate nanoparticles as new drug carrier for brain delivery. Pharm Res. 2001;18(8):1157-66. (Pubitemid 32900402)
115. Vinogradov SV, Batrakova EV, Kabanov AV. Nanogels for oligonucleotide delivery to the brain. Bioconjug Chem. 2004;15(1):50-60. (Pubitemid 38165980)
116. Costantino L, Gandolfi F, Tosi G, Rivasi F, Vandelli MA, Forni F. Peptide-derivatized biodegradable nanoparticles able to cross the blood-brain barrier. J Control Release. 2005;108(1):84-96. (Pubitemid 41476677)
117. Weiss CK, Kohnle MV, Landfester K, Hauk T, Fischer D, Schmitz-Wienke J, et al. The first step into the brain: uptake of NIO-PBCA nanoparticles by endothelial cells in vitro and in vivo, and direct evidence for their blood-brain barrier permeation. ChemMedChem. 2008;3(9):1395-403.
118. Zensi A, Begley D, Pontikis C, Legros C, Mihoreanu L, Wagner S, et al. Albumin nanoparticles targeted with Apo E enter the CNS by transcytosis and are delivered to neurones. J Control Release. 2009;137(1):78-86.
119. Khor SP, Mayersohn M. Potential error in the measurement of tissue to blood distribution coefficients in physiological pharmacokinetic modeling. Residual tissue blood. I. Theoretical considerations. Drug Metab Dispos. 1991;19(2):478-85.
120. Khor SP, Bozigian H, Mayersohn M. Potential error in the measurement of tissue to blood distribution coefficients in physiological pharmacokinetic modeling. Residual tissue blood. II. Distribution of phencyclidine in the rat. Drug Metab Dispos. 1991;19(2):486-90.
121. Triguero D, Buciak J, Pardridge WM. Capillary depletion method for quantification of blood-brain barrier transport of circulating peptides and plasma proteins. J Neurochem. 1990;54(6):1882-8.
122. Gutierrez EG, Banks WA, Kastin AJ. Murine tumor necrosis factor alpha is transported from blood to brain in the mouse. J Neuroimmunol. 1993;47(2):169-76. (Pubitemid 23284281)
123. Gosk S, Vermehren C, Storm G, Moos T. Targeting antitransferrin receptor antibody (OX26) and OX26-conjugated liposomes to brain capillary endothelial cells using in situ perfusion. J Cereb Blood Flow Metab. 2004;24(11):1193-204. (Pubitemid 39482480)
124. Sakamoto Aand Ido T. Liposome targeting to rat brain: effect of osmotic opening of the blood-brain barrier. Brain Res. 1993;629(1):171-5.
125. Martinez-Serrano A and Bjorklund A. Ex vivo nerve growth factor gene transfer to the basal forebrain in presymptomatic middleaged rats prevents the development of cholinergic neuron atrophy and cognitive impairment during aging. Proc Natl Acad Sci U S A. 1998;95(4):1858-63. (Pubitemid 28103484)
126. Sugiyama T, Kuroda S, Osanai T, Shichinohe H, Kuge Y, Ito M, et al. Near-infrared fluorescence labeling allows noninvasive tracking of bone marrow stromal cells transplanted into rat infarct brain. Neurosurgery. 2011;68(4):1036-47. discussion 1047.
127. Miletic H, Fischer Y, Litwak S, Giroglou T, Waerzeggers Y, Winkeler A, et al. Bystander killing of malignant glioma by bone marrow-derived tumor-infiltrating progenitor cells expressing a suicide gene. Mol Ther. 2007;15(7):1373-81. (Pubitemid 46965333)
128. Zhao D, Najbauer J, Garcia E, Metz MZ, Gutova M, Glackin CA, et al. Neural stem cell tropism to glioma: critical role of tumor hypoxia. Mol Cancer Res. 2008;6(12):1819-29.
129. Rao KS, Reddy MK, Horning JL, Labhasetwar V. TAT-conjugated nanoparticles for the CNS delivery of anti-HIV drugs. Biomaterials. 2008;29(33):4429-38.
130. Sousa F, Mandal S, Garrovo C, Astolfo A, Bonifacio A, Latawiec D, et al. Functionalized gold nanoparticles: a detailed in vivo multimodal microscopic brain distribution study. Nanoscale. 2010;2(12):2826-34.
131. Deroose CM, Reumers V, Gijsbers R, Bormans G, Debyser Z, Mortelmans L, et al. Noninvasive monitoring of long-term lentiviral vector-mediated gene expression in rodent brain with bioluminescence imaging. Mol Ther. 2006;14(3):423-31. (Pubitemid 44184969)
132. Massoud TF, Gambhir SS. Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev. 2003;17(5):545-80. (Pubitemid 36307540)
133. Fand Callera, de Melo CM. Magnetic resonance tracking of magnetically labeled autologous bone marrow CD34+ cells transplanted into the spinal cord via lumbar puncture technique in patients with chronic spinal cord injury: CD34+ cells' migration into the injured site. Stem Cells Dev. 2007;16(3):461-6. (Pubitemid 47016231)
134. Walczak P, Kedziorek DA, Gilad AA, Barnett BP, Bulte JW. Applicability and limitations of MR tracking of neural stem cells with asymmetric cell division and rapid turnover: the case of the shiverer dysmyelinated mouse brain. Magn Reson Med. 2007;58(2):261-9. (Pubitemid 47267643)
135. Burgess A, Ayala-Grosso CA, Ganguly M, Jordao JF, Aubert I, Hynynen K. Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier. PLoS One. 2011;6(11):e27877.
136. Alexiou C, Arnold W, Klein RJ, Parak FG, Hulin P, Bergemann C, et al. Locoregional cancer treatment with magnetic drug targeting. Cancer Res. 2000;60(23):6641-8.
137. Lubbe AS, Alexiou C, Bergemann C. Clinical applications of magnetic drug targeting. J Surg Res. 2001;95(2):200-6. (Pubitemid 34953556)
138. Cole AJ, David AE, Wang J, Galban CJ, Hill HL, Yang VC. Polyethylene glycol modified, cross-linked starch-coated iron oxide nanoparticles for enhanced magnetic tumor targeting. Biomaterials. 2011;32(8):2183-93.
139. Cole AJ, David AE, Wang J, Galban CJ, Yang VC. Magnetic brain tumor targeting and biodistribution of long-circulating PEG-modified, cross-linked starch-coated iron oxide nanoparticles. Biomaterials. 2011;32(26):6291-301.
140. Raghavan R, Brady ML, Rodriguez-Ponce MI, Hartlep A, Pedain C, Sampson JH. Convection-enhanced delivery of therapeutics for brain disease, and its optimization. Neurosurg Focus. 2006;20(4):E12.
141. Shah K, Bureau E, Kim DE, Yang K, Tang Y, Weissleder R, et al. Glioma therapy and real-time imaging of neural precursor cell migration and tumor regression. Ann Neurol. 2005;57(1):34-41. (Pubitemid 40053313)
142. Billinton N and Knight AW. Seeing the wood through the trees: a review of techniques for distinguishing green fluorescent protein from endogenous autofluorescence. Anal Biochem. 2001;291(2):175-97. (Pubitemid 32373153)
143. Ntziachristos V. Fluorescence molecular imaging. Annu Rev Biomed Eng. 2006;8:1-33. (Pubitemid 44314811)
144. McCann CM, Waterman P, Figueiredo JL, Aikawa E, Weissleder R, Chen JW. Combined magnetic resonance and fluorescence imaging of the living mouse brain reveals glioma response to chemotherapy. Neuroimage. 2009;45(2):360-9.
145. Hyde D, de Kleine R, MacLaurin SA, Miller E, Brooks DH, Krucker T, et al. Hybrid FMT-CT imaging of amyloid-beta plaques in a murine Alzheimer's disease model. Neuroimage. 2009;44(4):1304-11.
146. Levasseur JE, Wei EP, Raper AJ, Kontos AA, Patterson JL. Detailed description of a cranial window technique for acute and chronic experiments. Stroke. 1975;6(3):308-17.
147. Grutzendler J, Kasthuri N, Gan WB. Long-term dendritic spine stability in the adult cortex. Nature. 2002;420(6917):812-6. (Pubitemid 36019628)
148. Drew PJ, Shih AY, Driscoll JD, Knutsen PM, Blinder P, Davalos D, et al. Chronic optical access through a polished and reinforced thinned skull. Nat Methods. 2010;7(12):981-4.
149. Campbell RB, Fukumura D, Brown EB, Mazzola LM, Izumi Y, Jain RK, et al. Cationic charge determines the distribution of liposomes between the vascular and extravascular compartments of tumors. Cancer Res. 2002;62(23):6831-6. (Pubitemid 35424069)
150. Dreher MR, Liu W, Michelich CR, Dewhirst MW, Yuan F, Chilkoti A. Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers. J Natl Cancer Inst. 2006;98(5):335-44. (Pubitemid 43338213)
151. Nakamura T, Dhawan V, Chaly T, Fukuda M, Ma Y, Breeze R, et al. Blinded positron emission tomography study of dopamine cell implantation for Parkinson's disease. Ann Neurol. 2001;50(2):181-7. (Pubitemid 32738142)
152. Wang J, Tian M, Zhang H. PET molecular imaging in stem cell therapy for neurological diseases. Eur J Nucl Med Mol Imaging. 2011;38(10):1926-38.
153. Lappalainen RS, Narkilahti S, Huhtala T, Liimatainen T, Suuronen T, Narvanen A, et al. The SPECT imaging shows the accumulation of neural progenitor cells into internal organs after systemic administration in middle cerebral artery occlusion rats. Neurosci Lett. 2008;440(3):246-50.
154. Urakami T, Kawaguchi AT, Akai S, Hatanaka K, Koide H, Shimizu K, et al. In vivo distribution of liposome-encapsulated hemoglobin determined by positron emission tomography. Artif Organs. 2009;33(2):164-8.
155. Oku N, Yamashita M, Katayama Y, Urakami T, Hatanaka K, Shimizu K, et al. PET imaging of brain cancer with positron emitter-labeled liposomes. Int J Pharm. 2011;403(1-2):170-7.
156. Liu HS, Jan MS, Chou CK, Chen PH, Ke NJ. Is green fluorescent protein toxic to the living cells? Biochem Biophys Res Commun. 1999;260(3):712-7.
157. Klein RL, Dayton RD, Leidenheimer NJ, Jansen K, Golde TE, Zweig RM. Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol Ther. 2006;13(3):517-27. (Pubitemid 43257619)
158. Davidson MW, Campbell RE. Engineered fluorescent proteins: innovations and applications. Nat Methods. 2009;6(10):713-7.
159. Tiffen JC, Bailey CG, Ng C, Rasko JE, Holst J. Luciferase expression and bioluminescence does not affect tumor cell growth in vitro or in vivo. Mol Cancer. 2010;9:299.
160. Fernandez P, Bordenave L, Celerier C, Bareille R, Brouillaud B, Basse-Cathalinat B. A novel potential application for 99mTc-HMPAO: endothelial cell labeling for in vitro investigation of cell-biomaterial interactions. J Nucl Med. 1999;40(10):1756-63. (Pubitemid 29471169)
161. Deliolanis NC, Kasmieh R, Wurdinger T, Tannous BA, Shah K, Ntziachristos V. Performance of the red-shifted fluorescent proteins in deep-tissue molecular imaging applications. J Biomed Opt. 2008;13(4):044008.
162. Patterson GH, Knobel SM, Sharif WD, Kain SR, Piston DW. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys J. 1997;73(5):2782-90. (Pubitemid 27471487)
163. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol. 2004;22(12):1567-72. (Pubitemid 40039460)
164. Wang L, Jackson WC, Steinbach PA, Tsien RY. Evolution of new nonantibody proteins via iterative somatic hypermutation. Proc Natl Acad Sci U S A. 2004;101(48):16745-9. (Pubitemid 39601309)
165. Shcherbo D, Merzlyak EM, Chepurnykh TV, Fradkov AF, Ermakova GV, Solovieva EA, et al. Bright far-red fluorescent protein for whole-body imaging. Nat Methods. 2007;4(9):741-6. (Pubitemid 47338169)
166. Fraga H. Firefly luminescence: a historical perspective and recent developments. Photochem Photobiol Sci. 2008;7(2):146-58. (Pubitemid 351248642)
167. Wood KV, Lam YA, Seliger HH, McElroy WD. Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors. Science. 1989;244(4905):700-2.
168. Lorenz WW, McCann RO, Longiaru M, Cormier MJ. Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Proc Natl Acad Sci U S A. 1991;88(10):4438-42. (Pubitemid 21914555)
169. Loening AM, Wu AM, Gambhir SS. Red-shifted Renilla reniformis luciferase variants for imaging in living subjects. Nat Methods. 2007;4(8):641-3. (Pubitemid 47202475)
170. Ji X, Cheng L, Wei F, Li H, Wang M, Tian Y, et al. Noninvasive visualization of retinoblastoma growth and metastasis via bioluminescence imaging. Invest Ophthalmol Vis Sci. 2009;50(12):5544-51.
171. Tannous BA, Kim DE, Fernandez JL, Weissleder R, Breakefield XO. Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol Ther. 2005;11(3):435-43. (Pubitemid 40277320)
172. Tjuvajev JG, Doubrovin M, Akhurst T, Cai S, Balatoni J, Alauddin MM, et al. Comparison of radiolabeled nucleoside probes (FIAU, FHBG, and FHPG) for PET imaging of HSV1-tk gene expression. J Nucl Med. 2002;43(8):1072-83. (Pubitemid 34847932)
173. MacLaren DC, Gambhir SS, Satyamurthy N, Barrio JR, Sharfstein S, Toyokuni T, et al. Repetitive, non-invasive imaging of the dopamine D2 receptor as a reporter gene in living animals. Gene Ther. 1999;6(5):785-91. (Pubitemid 29243651)
174. Auricchio A, Acton PD, Hildinger M, Louboutin JP, Plossl K, O'Connor E, et al. In vivo quantitative noninvasive imaging of gene transfer by single-photon emission computerized tomography. Hum Gene Ther. 2003;14(3):255-61. (Pubitemid 36423444)
175. Shin JH, Chung JK, Kang JH, Lee YJ, Kim KI, So Y, et al. Noninvasive imaging for monitoring of viable cancer cells using a dual-imaging reporter gene. J Nucl Med. 2004;45(12):2109-15. (Pubitemid 47611643)
176. Zinn KR, Buchsbaum DJ, Chaudhuri TR, Mountz JM, Grizzle WE, Rogers BE. Noninvasive monitoring of gene transfer using a reporter receptor imaged with a high-affinity peptide radiolabeled with 99mTc or 188Re. J Nucl Med. 2000;41(5):887-95. (Pubitemid 30266035)
177. Rogers BE, Chaudhuri TR, Reynolds PN, Della Manna D, Zinn KR. Non-invasive gamma camera imaging of gene transfer using an adenoviral vector encoding an epitopetagged receptor as a reporter. Gene Ther. 2003;10(2):105-14. (Pubitemid 36582582)
178. Doubrovin M, Ponomarev V, Serganova I, Soghomonian S, Myagawa T, Beresten T, et al. Development of a new reporter gene system-dsRed/xanthine phosphoribosyltransferase-xanthine for molecular imaging of processes behind the intact blood-brain barrier. Mol Imaging. 2003;2(2):93-112.