Brain uptake of a fluorescent vector targeting the transferrin receptor: A novel application of in situ brain perfusion

Molecular Pharmaceutics

Volumn 11, Issue 1, 2014, Pages 243-253

  Alata, Wael ^a,b   Paris Robidas, Sarah ^a,b   Emond, Vincent ^b   Bourasset, Fanchon ^c   Calon, Frédéric ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

blood brain barrier; fluorescence; in situ brain perfusion; transferrin receptor

Indexed keywords

ANTIBODY CONJUGATE; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; TRANSFERRIN RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BALB/C NUDE MOUSE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN HOMOGENATE; BRAIN PERFUSION; COMMON CAROTID ARTERY; DISTRIBUTION VOLUME; DRUG TARGETING; EXTERNAL CAROTID ARTERY; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; IN VITRO STUDY; INTERNALIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOACTIVITY; RECEPTOR BINDING;

ANIMALS; ANTIBODIES, MONOCLONAL; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; DRUG DELIVERY SYSTEMS; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC VECTORS; MALE; MICE; MICE, INBRED BALB C; NEUROBLASTOMA; PERFUSION; RECEPTORS, TRANSFERRIN; TISSUE DISTRIBUTION; TUMOR CELLS, CULTURED;

EID: 84891778255     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400421a     Document Type: Article

References (61)

1. Pardridge, W. M. Alzheimer's disease drug development and the problem of the blood-brain barrier Alzheimer's Dementia 2009, 5, 427-432
2. Vlieghe, P.; Khrestchatisky, M. Medicinal chemistry based approaches and nanotechnology-based systems to improve CNS drug targeting and delivery Med. Res. Rev. 2013, 33, 457-516
3. Pangalos, M. N.; Schechter, L. E.; Hurko, O. Drug development for CNS disorders: Strategies for balancing risk and reducing attrition Nat. Rev. Drug Discovery 2007, 6, 521-532
4. Weiss, N.; Miller, F.; Cazaubon, S.; Couraud, P. O. The blood-brain barrier in brain homeostasis and neurological diseases Biochim. Biophys. Acta 2009, 1788, 842-857
5. Sa-Pereira, I.; Brites, D.; Brito, M. A. Neurovascular unit: A focus on pericytes Mol. Neurobiol. 2012, 45, 327-347
6. Jeffrey, P.; Summerfield, S. Assessment of the blood-brain barrier in CNS drug discovery Neurobiol. Dis. 2010, 37, 33-37
7. Mensch, J.; Oyarzabal, J.; Mackie, C.; Augustijns, P. In vivo, in vitro and in silico methods for small molecule transfer across the BBB J. Pharm. Sci. 2009, 98, 4429-4468
8. Dash, A. K.; Elmquist, W. F. Separation methods that are capable of revealing blood-brain barrier permeability J. Chromatogr., B 2003, 797, 241-254
9. Hawkins, B. T.; Egleton, R. D. Pathophysiology of the blood-brain barrier: Animal models and methods Curr. Top. Dev. Biol. 2008, 80, 277-309
10. Takasato, Y.; Rapoport, S. I.; Smith, Q. R. An in situ brain perfusion technique to study cerebrovascular transport in the rat Am. J. Physiol. 1984, 247, H484-H493
11. Dagenais, C.; Rousselle, C.; Pollack, G. M.; Scherrmann, J. M. Development of an in situ mouse brain perfusion model and its application to mdr1a P-glycoprotein-deficient mice J. Cereb. Blood Flow Metab. 2000, 381-386
12. Bickel, U. How to measure drug transport across the blood-brain barrier NeuroRx 2005, 2, 15-26
13. Smith, Q. R. A review of blood-brain barrier transport techniques Methods Mol. Med. 2003, 89, 193-208
14. Nicolazzo, J. A.; Charman, S. A.; Charman, W. N. Methods to assess drug permeability across the blood-brain barrier J. Pharm. Pharmacol. 2006, 58, 281-293
15. Egawa, T.; Hanaoka, K.; Koide, Y.; Ujita, S.; Takahashi, N.; Ikegaya, Y.; Matsuki, N.; Terai, T.; Ueno, T.; Komatsu, T.; Nagano, T. Development of a far-red to near-infrared fluorescence probe for calcium ion and its application to multicolor neuronal imaging J. Am. Chem. Soc. 2011, 133, 14157-14159
16. Pardridge, W. M.; Boado, R. J. Reengineering biopharmaceuticals for targeted delivery across the blood-brain barrier Methods Enzymol. 2012, 503, 269-292
17. Dennis, M. S.; Watts, R. J. Transferrin antibodies into the brain Neuropsychopharmacology 2012, 37, 302-303
18. Jefferies, W. A.; Brandon, M. R.; Hunt, S. V.; Williams, A. F.; Gatter, K. C.; Mason, D. Y. Transferrin receptor on endothelium of brain capillaries Nature 1984, 312, 162-163
19. Boado, R. J.; Zhang, Y.; Wang, Y.; Pardridge, W. M. Engineering and expression of a chimeric transferrin receptor monoclonal antibody for blood-brain barrier delivery in the mouse Biotechnol. Bioeng. 2009, 102, 1251-1258
20. Friden, P. M.; Walus, L. R.; Musso, G. F.; Taylor, M. A.; Malfroy, B.; Starzyk, R. M. Anti-transferrin receptor antibody and antibody-drug conjugates cross the blood-brain barrier Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 4771-4775
21. Lee, H. J.; Engelhardt, B.; Lesley, J.; Bickel, U.; Pardridge, W. M. Targeting rat anti-mouse transferrin receptor monoclonal antibodies through blood-brain barrier in mouse J. Pharmacol. Exp. Ther. 2000, 292, 1048-1052
22. Paris-Robidas, S.; Emond, V.; Tremblay, C.; Soulet, D.; Calon, F. In vivo labeling of brain capillary endothelial cells after intravenous injection of monoclonal antibodies targeting the transferrin receptor Mol. Pharmacol. 2011, 80, 32-39
23. Qian, Z. M.; Li, H.; Sun, H.; Ho, K. Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway Pharmacol. Rev. 2002, 54, 561-587
24. Watts, R. J.; Dennis, M. S. Bispecific antibodies for delivery into the brain Curr. Opin. Chem. Biol. 2013, 17, 393-399
25. Zhang, Y.; Calon, F.; Zhu, C.; Boado, R. J.; Pardridge, W. M. Intravenous nonviral gene therapy causes normalization of striatal tyrosine hydroxylase and reversal of motor impairment in experimental Parkinsonism Hum. Gene Ther. 2003, 14, 1-12
26. Olmsted, J. B.; Carlson, K.; Klebe, R.; Ruddle, F.; Rosenbaum, J. Isolation of microtubule protein from cultured mouse neuroblastoma cells Proc. Natl. Acad. Sci. U.S.A. 1970, 65, 129-136
27. Williams, R. L.; Risau, W.; Zerwes, H. G.; Drexler, H.; Aguzzi, A.; Wagner, E. F. Endothelioma cells expressing the polyoma middle T oncogene induce hemangiomas by host cell recruitment Cell 1989, 57, 1053-1063
28. Wagner, E. F.; Risau, W. Oncogenes in the study of endothelial cell growth and differentiation Semin. Cancer Biol. 1994, 5, 137-145
29. Rohnelt, R. K.; Hoch, G.; Reiss, Y.; Engelhardt, B. Immunosurveillance modelled in vitro: Naive and memory T cells spontaneously migrate across unstimulated microvascular endothelium Int. Immunol. 1997, 9, 435-450
30. Ouellet, M.; Emond, V.; Chen, C. T.; Julien, C.; Bourasset, F.; Oddo, S.; LaFerla, F.; Bazinet, R. P.; Calon, F. Diffusion of docosahexaenoic and eicosapentaenoic acids through the blood-brain barrier: An in situ cerebral perfusion study Neurochem. Int. 2009, 55, 476-482
31. Lesley, J. F.; Schulte, R. J. Selection of cell lines resistant to anti-transferrin receptor antibody: Evidence for a mutation in transferrin receptor Mol. Cell. Biol. 1984, 4, 1675-1681
32. Do, T. M.; Noel-Hudson, M. S.; Ribes, S.; Besengez, C.; Smirnova, M.; Cisternino, S.; Buyse, M.; Calon, F.; Chimini, G.; Chacun, H.; Scherrmann, J. M.; Farinotti, R.; Bourasset, F. ABCG2- and ABCG4-mediated efflux of amyloid-β peptide 1-40 at the mouse blood-brain barrier J. Alzheimer's Dis. 2012, 30, 155-166
33. Cattelotte, J.; Andre, P.; Ouellet, M.; Bourasset, F.; Scherrmann, J. M.; Cisternino, S. In situ mouse carotid perfusion model: Glucose and cholesterol transport in the eye and brain J. Cereb. Blood Flow Metab. 2008, 1449-1459
34. Pardridge, W. M. Drug transport across the blood-brain barrier J. Cereb. Blood Flow Metab. 2012, 1959-1972
35. Broadwell, R. D.; Baker-Cairns, B. J.; Friden, P. M.; Oliver, C.; Villegas, J. C. Transcytosis of protein through the mammalian cerebral epithelium and endothelium. III. Receptor-mediated transcytosis through the blood-brain barrier of bloodborne transferrin and antibody against the transferrin receptor Exp. Neurol. 1996, 142, 47-65
36. Shi, N.; Zhang, Y.; Zhu, C.; Boado, R. J.; Pardridge, W. M. Brain-specific expression of an exogenous gene after i.v. administration Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 12754-12759
37. Fu, A.; Hui, E. K.; Lu, J. Z.; Boado, R. J.; Pardridge, W. M. Neuroprotection in stroke in the mouse with intravenous erythropoietin-Trojan horse fusion protein Brain Res. 2011, 1369, 203-207
38. Zhou, Q. H.; Hui, E. K.; Lu, J. Z.; Boado, R. J.; Pardridge, W. M. Brain penetrating IgG-erythropoietin fusion protein is neuroprotective following intravenous treatment in Parkinson's disease in the mouse Brain Res. 2011, 1382, 315-320
39. Zhou, Q. H.; Fu, A.; Boado, R. J.; Hui, E. K.; Lu, J. Z.; Pardridge, W. M. Receptor-mediated abeta amyloid antibody targeting to Alzheimer's disease mouse brain Mol. Pharmaceutics 2011, 8, 280-285
40. Lee, H. J.; Zhang, Y.; Zhu, C.; Duff, K.; Pardridge, W. M. Imaging brain amyloid of Alzheimer disease in vivo in transgenic mice with an Abeta peptide radiopharmaceutical J. Cereb. Blood Flow Metab. 2002, 223-231
41. 125I]transferrin through the rat blood-brain barrier Brain Res. 1995, 683, 164-171
42. Cerletti, A.; Drewe, J.; Fricker, G.; Eberle, A. N.; Huwyler, J. Endocytosis and transcytosis of an immunoliposome-based brain drug delivery system J. Drug Targeting 2000, 8, 435-446
43. Bickel, U.; Kang, Y. S.; Yoshikawa, T.; Pardridge, W. M. In vivo demonstration of subcellular localization of anti-transferrin receptor monoclonal antibody-colloidal gold conjugate in brain capillary endothelium J. Histochem. Cytochem. 1994, 42, 1493-1497
44. Gosk, S.; Vermehren, C.; Storm, G.; Moos, T. Targeting anti-transferrin receptor antibody (OX26) and OX26-conjugated liposomes to brain capillary endothelial cells using in situ perfusion J. Cereb. Blood Flow Metab. 2004, 1193-1204
45. Moos, T.; Morgan, E. H. Restricted transport of anti-transferrin receptor antibody (OX26) through the blood-brain barrier in the rat J. Neurochem. 2001, 79, 119-129
46. Zhang, P.; Hu, L.; Yin, Q.; Zhang, Z.; Feng, L.; Li, Y. Transferrin-conjugated polyphosphoester hybrid micelle loading paclitaxel for brain-targeting delivery: Synthesis, preparation and in vivo evaluation J. Controlled Release 2012, 159, 429-434
47. Rivest, V.; Phivilay, A.; Julien, C.; Belanger, S.; Tremblay, C.; Emond, V.; Calon, F. Novel liposomal formulation for targeted gene delivery Pharm. Res. 2007, 24, 981-990
48. Thomas, F. C.; Taskar, K.; Rudraraju, V.; Goda, S.; Thorsheim, H. R.; Gaasch, J. A.; Mittapalli, R. K.; Palmieri, D.; Steeg, P. S.; Lockman, P. R.; Smith, Q. R. Uptake of ANG1005, a novel paclitaxel derivative, through the blood-brain barrier into brain and experimental brain metastases of breast cancer Pharm. Res. 2009, 26, 2486-2494
49. Visser, C. C.; Stevanovic, S.; Heleen Voorwinden, L.; Gaillard, P. J.; Crommelin, D. J.; Danhof, M.; De Boer, A. G. Validation of the transferrin receptor for drug targeting to brain capillary endothelial cells in vitro J. Drug Targeting 2004, 12, 145-150
50. Kohlhaas, S. L.; Craxton, A.; Sun, X. M.; Pinkoski, M. J.; Cohen, G. M. Receptor-mediated endocytosis is not required for tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis J. Biol. Chem. 2007, 282, 12831-12841
51. Bourasset, F.; Ouellet, M.; Tremblay, C.; Julien, C.; Do, T. M.; Oddo, S.; LaFerla, F.; Calon, F. Reduction of the cerebrovascular volume in a transgenic mouse model of Alzheimer's disease Neuropharmacology 2009, 56, 808-813
52. Bourasset, F.; Cisternino, S.; Temsamani, J.; Scherrmann, J. M. Evidence for an active transport of morphine-6-β- d -glucuronide but not P-glycoprotein-mediated at the blood-brain barrier J. Neurochem. 2003, 86, 1564-1567
53. Kang, Y. S.; Bickel, U.; Pardridge, W. M. Pharmacokinetics and saturable blood-brain barrier transport of biotin bound to a conjugate of avidin and a monoclonal antibody to the transferrin receptor Drug Metab. Dispos. 1994, 22, 99-105
54. Dautry-Varsat, A.; Ciechanover, A.; Lodish, H. F. pH and the recycling of transferrin during receptor-mediated endocytosis Proc. Natl. Acad. Sci. U.S.A. 1983, 80, 2258-2262
55. Jones, A. R.; Shusta, E. V. Blood-brain barrier transport of therapeutics via receptor-mediation Pharm. Res. 2007, 24, 1759-1771
56. Papademetriou, I. T.; Garnacho, C.; Schuchman, E. H.; Muro, S. In vivo performance of polymer nanocarriers dually-targeted to epitopes of the same or different receptors Biomaterials 2013, 34, 3459-3466
57. Sumbria, R. K.; Zhou, Q. H.; Hui, E. K.; Lu, J. Z.; Boado, R. J.; Pardridge, W. M. Pharmacokinetics and brain uptake of an IgG-TNF decoy receptor fusion protein following intravenous, intraperitoneal, and subcutaneous administration in mice Mol. Pharmaceutics 2013, 10, 1425-1431
58. Zhou, Q. H.; Boado, R. J.; Hui, E. K.; Lu, J. Z.; Pardridge, W. M. Chronic dosing of mice with a transferrin receptor monoclonal antibody-glial-derived neurotrophic factor fusion protein Drug Metab. Dispos. 2011, 39, 1149-1154
59. Yu, Y. J.; Zhang, Y.; Kenrick, M.; Hoyte, K.; Luk, W.; Lu, Y.; Atwal, J.; Elliott, J. M.; Prabhu, S.; Watts, R. J.; Dennis, M. S. Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target Sci. Transl. Med. 2011, 3 84ra44
60. Couch, J. A.; Yu, Y. J.; Zhang, Y.; Tarrant, J. M.; Fuji, R. N.; Meilandt, W. J.; Solanoy, H.; Tong, R. K.; Hoyte, K.; Luk, W.; Lu, Y.; Gadkar, K.; Prabhu, S.; Ordonia, B. A.; Nguyen, Q.; Lin, Y.; Lin, Z.; Balazs, M.; Scearce-Levie, K.; Ernst, J. A.; Dennis, M. S.; Watts, R. J. Addressing Safety Liabilities of TfR Bispecific Antibodies That Cross the Blood-Brain Barrier Sci Transl Med. 2013, 5 183ra157
61. Barrett, B.; Stiles, M.; Patterson, J. Radiation risks: Critical analysis and commentary Prev. Med. 2012, 54, 280-282