Combinatorial approaches for the identification of brain drug delivery targets

Current Pharmaceutical Design

Volumn 20, Issue 10, 2014, Pages 1564-1576

  Stutz, Charles C ^a   Zhang, Xiaobin ^a   Shusta, Eric V ^a  

^a University of Wisconsin Madison   (United States)

Author keywords

Blood brain barrier; Brain drug delivery; Receptor mediated transport

Indexed keywords

PARVOVIRUS VECTOR; TRANSFERRIN RECEPTOR;

ANTIBODY LIBRARY; ANTIBODY VARIABLE HEAVY CHAIN; ANTIBODY VARIABLE LIGHT CHAIN; BLOOD BRAIN BARRIER; COMBINATORIAL LIBRARY; DRUG BINDING SITE; DRUG DELIVERY SYSTEM; DRUG RECEPTOR BINDING; DRUG TRANSPORT; ENDOTHELIUM CELL; IMMUNOPRECIPITATION; LIGHT CHAIN; NONHUMAN; PEPTIDE LIBRARY; PHAGE DISPLAY; PRIORITY JOURNAL; RECEPTOR MEDIATED TRANSCYTOSIS; REVIEW; TANDEM MASS SPECTROMETRY; TRANSCYTOSIS; YEAST;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; DRUG DELIVERY SYSTEMS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MEMBRANE TRANSPORT PROTEINS; PHARMACEUTICAL PREPARATIONS;

EID: 84897457211     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990459     Document Type: Review

References (102)

1. Pardridge WM. Biopharmaceutical drug targeting to the brain. J Drug Target 2010; 18: 157-67.
2. Pardridge WM. Blood-brain barrier delivery. Drug Discov Today 2007; 12: 54-61.
3. Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis 2010; 37: 13-25.
4. Weiss N, Miller F, Cazaubon S, Couraud PO. The blood-brain barrier in brain homeostasis and neurological diseases. Biochim Biophys Acta 2009; 1788: 842-57.
5. Jones AR, Shusta EV. Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm Res 2007; 24: 1759-71.
6. 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: 1882-8.
7. Pardridge WM. Blood-brain barrier delivery of protein and nonviral gene therapeutics with molecular Trojan horses. J Control Release 2007; 122: 345-8.
8. Bickel U, Yoshikawa T, Pardridge WM. Delivery of peptides and proteins through the blood-brain barrier. Adv Drug Deliv Rev 2001; 46: 247-79.
9. Pardridge WM. Drug and gene targeting to the brain with molecular Trojan horses. Nat Rev Drug Discov 2002; 1: 131-9.
10. Paolino D, Cosco D, Molinaro R, Celia C, Fresta M. Supramolecular devices to improve the treatment of brain diseases. Drug Discov Today 2011; 16: 311-24.
11. Shin SU, Friden P, Moran M, et al. Transferrin antibody fusion proteins are effective in brain targeting. Proc Natl Acad Sci USA 1995; 92: 2820-4.
12. Mishra V, Mahor S, Rawat A, et al. Targeted brain delivery of AZT via transferrin anchored pegylated albumin nanoparticles. J Drug Target 2006; 14: 45-53.
13. Staquicini FI, Ozawa MG, Moya CA, et al. Systemic combinatorial peptide selection yields a non-canonical iron-mimicry mechanism for targeting tumors in a mouse model of human glioblastoma. J Clin Invest 2011; 121: 161-73.
14. Pang ZQ, Lu W, Gao HL, et al. Preparation and brain delivery property of biodegradable polymersomes conjugated with OX26. J Control Release 2008; 128: 120-7.
15. Zhang Y, Pardridge WM. Conjugation of brain-derived neurotrophic factor to a blood-brain barrier drug targeting system enables neuroprotection in regional brain ischemia following intravenous injection of tbe neurotrophin. Brain Res 2001; 889: 49-56.
16. Pardridge WM, Kang YS, Buciak JL. Transport of human recombinant brain-derived neuotrophic factor (BDNF) through the rat blood-brain-barrier in-vivo using vector-mediated peptide drugdelivery. Pharm Res 1994; 11: 738-46.
17. Ulbrich K, Hekmatara T, Herbert E, Kreuter J. Transferrin-and transferrin-receptor-antibody-modified nanoparticles enable drug delivery across the blood-brain barrier (BBB). Eur J Pharm Biopharm 2009; 71: 251-6.
18. Zhang Y, Pardridge WM. Neuroprotection in transient focal brain ischemia after delayed intravenous administration of brain-derived neurotrophic factor conjugated to a blood-brain barrier drug targeting system. Stroke 2001; 32: 1378-83.
19. Yu YJ, Zhang Y, Kenrick M, et al. Boosting Brain Uptake of a Therapeutic Antibody by Reducing Its Affinity for a Transcytosis Target. Sci Transl Med 2011; 3.
20. Ueno M, Nakagawa T, Wu B, et al. Transporters in the Brain Endothelial Barrier. Curr Med Chem 2010; 17: 1125-38.
21. Shusta EV, Boado RJ, Mathern GW, Pardridge WM. Vascular genomics of the human brain. J Cereb Blood Flow Metab 2002; 22: 245-52.
22. Enerson BE, Drewes LR. The rat blood-brain barrier transcriptome. J Cereb Blood Flow Metab 2006; 26: 959-73.
23. Daneman R, Zhou L, Agalliu D, Cahoy JD, Kaushal A, Barres BA. The Mouse Blood-Brain Barrier Transcriptome: A New Resource for Understanding the Development and Function of Brain Endothelial Cells. Plos One 2010; 5: e13741.
24. Bradbury ARM, Marks JD. Antibodies from phage antibody libraries. J Immunol Methods 2004; 290: 29-49.
25. Tanha J, Dubuc G, Hirama T, Narang SA, MacKenzie CR. Selection by phage display of llama conventional V-H fragments with heavy chain antibody VHH properties. J Immunol Methods 2002; 263: 97-109.
26. Muruganandam A, Tanha J, Narang S, Stanimirovic D. Selection of phage-displayed llama single-domain antibodies that transmigrate across human blood-brain barrier endothelium. FASEB J 2001; 15: 240-56.
27. Zhou HY, Zhang YL, Lu GD, Ji H, Rodi CP. Recombinant antibody libraries and selection technologies. New Biotech 2011; 28: 448-52.
28. Chen YH, Chang M, Davidson BL. Molecular signatures of disease brain endothelia provide new sites for CNS-directed enzyme therapy. Nat Med 2009; 15: 1215-U145.
29. van Rooy I, Cakir-Tascioglu S, Couraud PO, et al. Identification of Peptide Ligands for Targeting to the Blood-Brain Barrier. Pharm Res 2010; 27: 673-82.
30. Pasqualini R, Ruoslahti E. Organ targeting in vivo using phage display peptide libraries. Nature 1996; 380: 364-6.
31. Rakonjac J, Bennett NJ, Spagnuolo J, Gagic D, Russel M. Filamentous Bacteriophage: Biology, Phage Display and Nanotechnology Applications. Curr Issues Mol Biol 2011; 13: 51-75.
32. Arap MA. Phage display technology-Applications and innovations. Genet Mol Biol 2005; 28: 1-9.
33. Castillo J, Goodson B, Winter J. T7 displayed peptides as targets for selecting peptide specific scFvs from M13 scFv display libraries. J Immunol Methods 2001; 257: 117-22.
34. Tohidkia MR, Barar J, Asadi F, Omidi Y. Molecular considerations for development of phage antibody libraries. J Drug Target 2012; 20: 195-208.
35. O'Connell D, Becerril B, Roy-Burman A, Daws M, Marks JD. Phage versus phagemid libraries for generation of human monoclonal antibodies. J Mol Biol 2002; 321: 49-56.
36. Poul MA, Becerril B, Nielsen UB, Morisson P, Marks JD. Selection of tumor-specific internalizing human antibodies from phage libraries. J Mol Bio 2000; 301: 1149-61.
37. Bowley DR, Labrijn AF, Zwick MB, Burton DR. Antigen selection from an HIV-1 immune antibody library displayed on yeast yields many novel antibodies compared to selection from the same library displayed on phage. Protein Eng Des Sel 2007; 20: 81-90.
38. Boder ET, Wittrup KD. Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol 1997; 15: 553-7.
39. Wang XX, Shusta EV. The use of scFv-displaying yeast in mammalian cell surface selections. J Immunol Methods 2005; 304: 30-42.
40. Wang XX, Cho YK, Shusta EV. Mining a yeast library for brain endothelial cell-binding antibodies. Nat Methods 2007; 4: 143-5.
41. Cho YK, Chen I, Wei X, Li LJ, Shusta EV. A yeast display immunoprecipitation method for efficient isolation and characterization of antigens. J Immunol Methods 2009; 341: 117-26.
42. McCown TJ. Adeno-Associated Virus (AAV) Vectors in the CNS. Curr Gene Ther 2011; 11: 181-8.
43. Grieger JC, Samulski RJ. In Methods in Enzymology, Vol 507: Gene Transfer Vectors for Clinical Application, T. Friedmann, ed.; Elsevier Academic Press Inc: San Diego, 2012; Vol. 507, pp. 229-54.
44. Li W, Asokan A, Wu Z, et al. Engineering and selection of shuffled AAV genomes: A new strategy for producing targeted biological nanoparticles. Mol Ther 2008; 16: 1252-60.
45. Maguire CA, Gianni D, Meijer DH, et al. Directed evolution of adeno-associated virus for glioma cell transduction. J Neurooncol 2010; 96: 337-47.
46. Bevan AK, Duque S, Foust KD, et al. Systemic Gene Delivery in Large Species for Targeting Spinal Cord, Brain, and Peripheral Tissues for Pediatric Disorders. Mol Ther 2011; 19: 1971-80.
47. Gray SJ, Blake BL, Criswell HE, Nicolson SC, Samulski RJ, McCown TJ. Directed Evolution of a Novel Adeno-associated Virus (AAV) Vector That Crosses the Seizure-compromised Blood-Brain Barrier (BBB). Mol Ther 2010; 18: 570-8.
48. Michelfelder S, Kohlschutter J, Skorupa A, et al. Successful expansion but not complete restriction of tropism of adeno-associated virues by in vivo biopanning of random virus display peptide libraries. Plos One 2009; 4: e5122.
49. Adachi K, Naki H. A new Recombinant Adeno-Associated Virus (AAV)-based Random Peptide Display Library System: Infectiondefective AAV1. 9-3 as a Novel Detargeted Platform for Vector Evolution. Gene Ther Regul 2010; 5: 31-55.
50. Feldhaus MJ, Siegel RW, Opresko LK, et al. Flow-cytometric isolation of human antibodies from a nonimmune Saccharomyces cerevisiae surface display library. Nat Biotechnol 2003; 21: 163-70.
51. Cho YK, Shusta EV. Antibody library screens using detergentsolubilized mammalian cell lysates as antigen sources. Protein Eng Des Sel 2010; 23: 567-77.
52. Urich E, Lazic SE, Molnos J, Wells I, Freskgard PO. Transcriptional Profiling of Human Brain Endothelial Cells Reveals Key Properties Crucial for Predictive In vitro Blood-Brain Barrier Models. Plos One 2012; 7.
53. Weksler BB, Subileau EA, Perriere N, et al. Blood-brain barrierspecific properties of a human adult brain endothelial cell line. FASEB J 2005; 19: 1872-4.
54. Lyck R, Ruderisch N, Moll AG, et al. Culture-induced changes in blood-brain barrier transcriptome: implications for amino-acid transporters in vivo. J Cereb Blood Flow Metab 2009; 29: 1491-502.
55. Calabria AR, Shusta EV. A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. J Cereb Blood Flow Metab 2008; 28: 135-48.
56. Li JW, Feng L, Fan L, et al. Targeting the brain with PEG-PLGA nanoparticles modified with phage-displayed peptides. Biomaterials 2011; 32: 4943-50.
57. Li JW, Zhang QZ, Pang ZQ, et al. Identification of peptide sequences that target to the brain using in vivo phage display. Amino Acids 2012; 42: 2373-81.
58. Valadon P, Garnett JD, Testa JE, Bauerle M, Oh P, Schnitzer JE. Screening phage display libraries for organ-specific vascular immunotargeting in vivo. Proc Natl Acad Sci USA 2006; 103: 407-12.
59. Roodink I, Franssen M, Zuidscherwoude M, et al. Isolation of targeting nanobodies against co-opted tumor vasculature. Lab Invest 2010; 90: 61-7.
60. Sokoloff AV, Bock I, Zhang GF, Sebestyen MG, Wolff JA. The interactions of peptides with the innate immune system studied with use of T7 phage peptide display. Mol. Ther. 2000; 2: 131-9.
61. van Rooy I, Hennink WE, Storm G, Schiffelers RM, Mastrobattista E. Attaching the phage display-selected GLA peptide to liposomes: Factors influencing target binding. Eur J Pharm Sci 2012; 45: 330-5.
62. Wan XM, Chen YP, Xu WR, Yang WJ, Wen LP. Identification of nose-to-brain homing peptide through phage display. Peptides 2009; 30: 343-50.
63. Gonzalez AM, Leadbeater WE, Burg M, et al. Targeting choroid plexus epithelia and ventricular ependyma for drug delivery to the central nervous system. BMC Neurosci 2011; 12: 4.
64. Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci 2011; 12: 723-38.
65. Hong HY, Choi JS, Kim YJ, et al. Detection of apoptosis in a rat model of focal cerebral ischemia using a homing peptide selected from in vivo phage display. J Control Release 2008; 131: 167-72.
66. Demeule M, Regina A, Che C, et al. Identification and design of peptides as a new drug delivery system for the brain. J Pharmacol Exp Ther 2008; 324: 1064-72.
67. Yan HH, Wang L, Wang JY, et al. Two-Order Targeted Brain Tumor Imaging by Using an Optical/Paramagnetic Nanoprobe across the Blood Brain Barrier. ACS Nano 2012; 6: 410-20.
68. Sun XY, Pang ZQ, Ye HX, et al. Co-delivery of pEGFP-hTRAIL and paclitaxel to brain glioma mediated by an angiopep-conjugated liposome. Biomaterials 2012; 33: 916-24.
69. Ren JF, Shen S, Wang DG, et al. The targeted delivery of anticancer drugs to brain glioma by PEGylated oxidized multi-walled carbon nanotubes modified with angiopep-2. Biomaterials 2012; 33: 3324-33.
70. Kurzrock R, Gabrail N, Chandhasin C, et al. Safety, Pharmacokinetics, and Activity of GRN1005, a Novel Conjugate of Angiopep-2, a Peptide Facilitating Brain Penetration, and Paclitaxel, in Patients with Advanced Solid Tumors. Mol Cancer Ther 2012; 11: 308-16.
71. Carter P, Smith L, Ryan M. Identification and validation of cell surface antigens for antibody targeting in oncology. Endocr Relat Cancer 2004; 11: 659-87.
72. Smith GP, Petrenko VA, Matthews LJ. Cross-linked filamentous phage as an affinity matrix. J Immunol Methods 1998; 215: 151-61.
73. Minana R, Duran JM, Tomas M, Renau-Piqueras J, Guerri C. Neural cell adhesion molecule is endocytosed via a clathrin-dependent pathway. Eur J Neurosci 2001; 13: 749-56.
74. Patel K, Frost G, Kiely F, Phimister E, Coakham HB, Kemshead JT. Expression of the cluster 1 antigen (neural cell adhesion molecule) in neuroectodermal tumours. Br J Cancer Suppl 1991; 14: 20-3.
75. Todaro L, Christiansen S, Varela M, et al. Alteration of serum and tumoral neural cell adhesion molecule (NCAM) isoforms in patients with brain tumors. J Neurooncol 2007; 83: 135-44.
76. Abulrob A, Sprong H, Van Bergen en Henegouwen P, Stanimirovic D. The blood-brain barrier transmigrating single domain antibody: mechanisms of transport and antigenic epitopes in human brain endothelial cells. J Neurochem 2005; 95: 1201-14.
77. Abulrob A, Stanimirovic D, Muruganandam A. National Research Council of Canada, assignee. Blood-brain barrier epitopes and uses thereof. Canada Patent CA 2623841. 2007.
78. Agarwal N, Shusta EV. Multiplex expression cloning of bloodbrain barrier membrane proteins. Proteomics 2009; 9: 1099-108.
79. Agarwal N, Lippmann ES, Shusta EV. Identification and expression profiling of blood-brain barrier membrane proteins. J Neurochem 2010; 112: 625-35.
80. Santi E, Capone S, Mennuni C, et al. Bacteriophage lambda display of complex cDNA libraries: a new approach to functional genomics. J Mol Biol 2000; 296: 497-508.
81. Ansuini H, Cicchini C, Nicosia A, Tripodi M, Cortese R, Luzzago A. Biotin-tagged cDNA expression libraries displayed on lambda phage: a new tool for the selection of natural protein ligands. Nucleic Acids Res 2002; 30: e78.
82. Bidlingmaier S, Liu B. Interrogating yeast surface-displayed human proteome to identify small molecule-binding proteins. Mol Cell Proteomics 2007; 6: 2012-20.
83. Bidlingmaier S, Liu B. Construction and application of a yeast surface-displayed human cDNA library to identify posttranslational modification-dependent protein-protein interactions. Mol Cell Proteomics 2006; 5: 533-40.
84. Vidal CI, Mintz PJ, Lu K, et al. An HSP90-mimic peptide revealed by fingerprinting the pool of antibodies from ovarian cancer patients. Oncogene 2004; 23: 8859-67.
85. Shibata T, Misawa N, Takeo C, Saeki N, Saito Y, Tatsuno I. Analysis of genes dominantly expressed in rat cerebral endothelial cells using suppression subtractive hybridization. J Atheroscler Thromb 2005; 12: 330-7.
86. Li JY, Boado RJ, Pardridge WM. Blood-brain barrier genomics. J Cereb Blood Flow Metab 2001; 21: 61-8.
87. Chu C, Li JY, Boado RJ, Pardridge WM. Blood-brain barrier genomics and cloning of a novel organic anion transporter. J Cereb Blood Flow Metab 2008; 28: 291-301.
88. Pen A, Moreno MJ, Martin J, Stanimirovic DB. Molecular markers of extracellular matrix remodeling in glioblastoma vessels: microarray study of laser-captured glioblastoma vessels. Glia 2007; 55: 559-72.
89. Bergerat A, Decano J, Wu CJ, et al. Prestroke proteomic changes in cerebral microvessels in stroke-prone, transgenic[hCETP]-Hyperlipidemic, Dahl salt-sensitive hypertensive rats. Mol Med 2011; 17: 588-98.
90. Ji K, Tsirka SE. Inflammation modulates expression of laminin in the central nervous system following ischemic injury. J Neuroinflammation 2012; 9: 159-70.
91. Zeng XN, Xie LL, Liang R, Sun XL, Fan Y, Hu G. AQP4 knockout aggravates ischemia/reperfusion injury in mice. CNS Neurosci Ther 2012; 18: 388-94.
92. Ito K, Uchida Y, Ohtsuki S, et al. Quantitative membrane protein expression at the blood-brain barrier of adult and younger cynomolgus monkeys. J Pharm Sci 2011; 100: 3939-50.
93. Uchida Y, Ohtsuki S, Katsukura Y, et al. Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors. J Neurochem 2011; 117: 333-45.
94. Macdonald JA, Murugesan N, Pachter JS. Endothelial cell heterogeneity of blood-brain barrier gene expression along the cerebral microvasculature. J Neurosci Res 2010; 88: 1457-74.
95. Nakagawa S, Deli MA, Kawaguchi H, et al. A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem Int 2009; 54: 253-63.
96. Cucullo L, Couraud PO, Weksler B, et al. Immortalized human brain endothelial cells and flow-based vascular modeling: a marriage of convenience for rational neurovascular studies. J Cereb Blood Flow Metab 2008; 28: 312-28.
97. Cucullo L, Hossain M, Rapp E, Manders T, Marchi N, Janigro D. Development of a humanized in vitro blood-brain barrier model to screen for brain penetration of antiepileptic drugs. Epilepsia 2007; 48: 505-16.
98. Santaguida S, Janigro D, Hossain M, Oby E, Rapp E, Cucullo L. Side by side comparison between dynamic versus static models of blood-brain barrier in vitro: a permeability study. Brain Res 2006; 1109: 1-13.
99. Booth R, Kim H. Characterization of a microfluidic in vitro model of the blood-brain barrier (muBBB). Lab Chip 2012; 12: 1784-92.
100. Lippmann ES, Azarin SM, Kay JE, et al. Derivation of blood-brain barrier endothelial cells from human pluripotent stem cells. Nat Biotechnol 2012; 30: 783-91.
101. Hotzel I, Chiang V, Diao JY, Pantua H, Maun HR, Kapadia SB. Efficient production of antibodies against a mammalian integral membrane protein by phage display. Protein Eng Des Sel 2011; 24: 679-89.
102. Ryan DA, Mastrangelo MA, Narrow WC, Sullivan MA, Federoff HJ, Bowers WJ. A beta-directed Single-chain Antibody Delivery Via a Serotype-1 AAV Vector Improves Learning Behavior and Pathology in Alzheimer's Disease Mice. Mol Ther 2010; 18: 1471-81.