The blood-brain barrier transmigrating single domain antibody: Mechanisms of transport and antigenic epitopes in human brain endothelial cells

Journal of Neurochemistry

Volumn 95, Issue 4, 2005, Pages 1201-1214

  Abulrob, Abedelnasser ^a   Sprong, Hein ^b   Van Bergen En Henegouwen, Paul ^b   Stanimirovic, Danica ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Blood brain barrier; Glycocalyx; Receptor mediated endocytosis; Sialic acid; Single domain antibodies; Transcytosis

Indexed keywords

AGGLUTININ; ALPHA 2,3 NEURAMINIDASE; ALPHA 2,3 SIALOGLYCOPROTEIN RECEPTOR; ANTIBODY; ANTIBODY FC5; CAVEOLIN 1; CLATHRIN; EPITOPE; FILIPIN; LIPID; METHYL BETA CYCLODEXTRIN; NYSTATIN; PHOSPHATIDYLINOSITOL 3 KINASE; RECEPTOR PROTEIN; SIALIC ACID; SIALIDASE; SINGLE DOMAIN ANTIBODY; UNCLASSIFIED DRUG;

ANTIGEN ANTIBODY REACTION; ANTIGEN RECOGNITION; ANTIGENICITY; ARTICLE; BLOOD BRAIN BARRIER; CELL POLARITY; CONTROLLED STUDY; CYTOSKELETON; DRUG DELIVERY SYSTEM; DRUG TARGETING; ENDOCYTOSIS; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; LYSOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; TEMPERATURE DEPENDENCE; TRANSCYTOSIS; WESTERN BLOTTING; WHEAT GERM;

AMILORIDE; ANTIBODIES; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; CAVEOLIN 1; CELLS, CULTURED; CLATHRIN; DEOXYGLUCOSE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENDOSOMES; ENDOTHELIAL CELLS; ENZYME INHIBITORS; FLUORESCENT ANTIBODY TECHNIQUE; HEPARIN ANTAGONISTS; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; NEURAMINIDASE; PROTAMINES; SODIUM AZIDE; SODIUM CHANNEL BLOCKERS; SUCROSE; TEMPERATURE; TRITIUM;

MAACKIA AMURENSIS; SAMBUCUS NIGRA; TRITICUM AESTIVUM;

EID: 28244432240     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03463.x     Document Type: Article

References (70)

1. Abbott N. J. and Romero I. A. (1996) Transporting therapeutics across the blood-brain barrier. Mol. Med. Today 2, 106-113.
2. Abulrob A., Giuseppin S., Andrade M. F., McDermid A., Moreno M. and Stanimirovic D. (2004) Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae. Oncogene 23, 6967-6979.
3. Abulrob A., Zhang J., Tanha J., MacKenzie R. and Stanimirovic D. (2005) Single domain antibodies as blood-brain barrier delivery vectors. Intern. Cong. Series 1277, 212-223.
4. Anand N. N., Dubuc G., Phipps J., MacKenzie C. R., Sadowska J., Young N. M., Bundle D. R. and Narang S. A. (1991) Synthesis and expression in Escherichia coli of cistronic DNA encoding an antibody fragment specific for a Salmonella serotype B O-antigen. Gene 100, 39-44.
5. Bandtlow C. E. and Zimmermann D. R. (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 80, 1267-1290.
6. Banks W. A., Akerstrom V. and Kastin A. J. (1998) Adsorptive endocytosis mediates the passage of HIV-1 across the blood-brain barrier: evidence for a post-internalization coreceptor. J. Cell Sci. 111, 533-540.
7. Basu S. K., Goldstein J. L., Anderson R. G. and Brown M. S. (1981) Monensin interrupts the recycling of low density lipoprotein receptors in human fibroblasts. Cell 24, 493-502.
8. Bayer N., Schober D., Prchla E., Murphy R. F., Blaas D. and Fuchs R. (1998) Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J. Virol. 72, 9645-9655.
9. Beck K. A. and Keen J. H. (1991) Interaction of phosphoinositide cycle intermediates with the plasma membrane-associated clathrin assembly protein AP-2. J. Biol Chem. 266, 4442-4447.
10. Begley D. J. and Brightman M. W. (2003) Structural and functional aspects of the blood-brain barrier. Prog. Drug Res. 61, 39-78.
11. 125I-labeled RGD peptide are improved by PEGylation. Nucl Med. Biol. 31, 11-19.
12. Dehouck B., Fenart L., Dehouck M. P., Pierce A., Torpier G. and Cecchelli R. (1997) A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier. J. Cell Biol. 138, 877-889.
13. Demeule M., Poirier J., Jodoin J. et al. (2002) High transcytosis of melanotransferrin (P97) across the blood-brain barrier. J. Neurochem. 83, 924-933.
14. Drin G., Rousselle C., Scherrmann J. M., Rees A. R. and Temsamani J. (2002) Peptide delivery to the brain via adsorptive-mediated endocytosis: advances with SynB vectors. AAPS Pharmsci. 4, E26.
15. Drin G., Cottin S., Blanc E., Rees A. R. and Temsamani J. (2003) Studies on the internalization mechanism of cationic cell-penetrating peptides. J. Biol Chem. 278, 31 192-31 201.
16. Duvar S., Suzuki M., Muruganandam A. and Yu R. K. (2000) Glycosphingolipid composition of a new immortalized human cerebromicrovascular endothelial cell line. J. Neurochem. 75, 1970-1976.
17. Fillebeen C., Descamps L., Dehouck M. P., Fenart L., Benaissa M., Spik G., Cecchelli R. and Pierce A. (1999) Receptor-mediated transcytosis of lactoferrin through the blood-brain barrier. J. Biol. Chem. 274, 7011-7017.
18. Floris S., van den Born J., van der Pol S. M., Dijkstra C. D. and De Vries H. E. (2003) Heparan sulfate proteoglycans modulate monocyte migration across cerebral endothelium. J. Neuropathol. Exp. Neurol. 62, 780-790.
19. Gaidarov I., Smith M. E., Domin J. and Keen J. H. (2001) The class II phosphoinositide 3-kinase C2α is activated by clathrin and regulates clathrin-mediated membrane trafficking. Mol. Cell 7, 443-449.
20. Garberg P., Ball M., Borg N. et al. (2005) In vitro models for the blood-brain barrier. Toxicol. In Vitro 19, 299-334.
21. Gekle M., Mildenberger S., Freudinger R., Schwerdt G. and Silbernag I. S. (1997) Albumin endocytosis in OK cells: dependence on actin and microtubules and regulation by protein kinases. Am. J. Physiol. 272, F668-F677.
22. Goretzki L. and Mueller B. M. (1997) Receptor-mediated endocytosis of urokinase-type plasminogen activator is regulated by cAMP-dependent protein kinase. J. Cell Sci. 110, 1395-1402.
23. Gumbleton M., Abulrob A. G. and Campbell L. (2000) Caveolae: an alternative membrane transport compartment. Pharm. Res. 17, 1035-1048.
24. Hansen S. H., Sandvig K. and van Deurs B. (1993) Clathrin and HA2 adaptors: effects of potassium depletion, hypertonic medium, and cytosol acidification. J. Cell Biol. 121, 61-72.
25. Hansen S. H., Olsson A. and Casanova J. E. (1995) Wortmannin, an inhibitor of phosphoinositide 3-kinase, inhibits transcytosis in polarized epithelial cells. J. Biol. Chem. 270, 28 425-28 432.
26. Harris J. M. and Chess R. B. (2003) Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discov. 2, 214-221.
27. Hayes G. R., Enns C. A. and Lucas J. J. (1992) Identification of the O-linked glycosylation site of the human transferrin receptor. Glycobiology 2, 355-359.
28. Jefferies W. A., Brandon M. R., Hunt S. V., Williams A. F., Gatter K. C. and Mason D. Y. (1984) Transferrin receptor on endothelium of brain capillaries. Nature 312, 162-163.
29. Kanda T., Ariga T., Kubodera H., Jin H. L., Owada K., Kasama T., Yamawaki M. and Mizusawa H. (2004) Glycosphingolipid composition of primary cultured human brain microvascular endothelial cells. J. Neurosci. Res. 78, 141-150.
30. Liu S. M., Magnusson K. E. and Sundqvist T. (1993) Microtubules are involved in transport of macromolecules by vesicles in cultured bovine aortic endothelial cells. J. Cell Physiol. 156, 311-316.
31. McPherson P. S. (2002) The endocytic machinery at an interface with the actin cytoskeleton: a dynamic, hip intersection. Trends Cell Biol. 12, 312-315.
32. Muruganandam A., Herx L. M., Monette R., Durkin J. P. and Stanimirovic D. B. (1997) Development of immortalized human cerebromicrovascular endothelial cell line as an in vitro model of the human blood-brain barrier. FASEB J. 11, 1187-1197.
33. Muruganandam A., Tanha J., Narang S. and Stanimirovic D. (2002) Selection of phage-displayed llama single-domain antibodies that transmigrate across human blood-brain barrier endothelium. FASEB J. 16, 240-242.
34. Muyldermans S. (2001) Single domain camel antibodies: current status. J. Biotechnol 74, 277-302.
35. Orberger G., Fuchs H., Geyer R., Gessner R., Kottgen E. and Tauber R. (2001) Structural and functional stability of the mature transferrin receptor from human placenta. Arch. Biochem. Biophys. 386, 79-88.
36. Osburg B., Peiser C., Domling D., Schomburg L., Ko Y. T., Voigt K. and Bickel U. (2002) Effect of endotoxin on expression of TNF receptors and transport of TNF-α at the blood-brain barrier of the rat. Am. J. Physiol. Endocrinol. Metab. 283, 899-908.
37. Pardridge W. M. (2002a) Drug and gene delivery to the brain: the vascular route. Neuron 36, 555-558.
38. Pardridge W. M. (2002b) Blood-brain barrier drug targeting enables neuroprotection in brain ischemia following delayed intravenous administration of neurotrophins. Adv. Exp. Med. Biol. 513, 397-430.
39. Parillo F., Dall'Aglio C., Verini Supplizi A., Ceccarelli P. and Gargiulo A. M. (2003) Immunogold study on lectin binding in the porcine zonapellucida and granulosa cells. Eur. J. Histochem. 47, 353-358.
40. Pries A. R., Secomb T. W. and Gaehtgens P. (2000) The endothelial surface layer. Pflugers Arch. 440, 653-666.
41. Qian Z. M., Li H., Sun H. and Ho K. (2002) Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol. Rev. 54, 561-587.
42. Qualmann B., Kessels M. M. and Kelly R. B. (2000) Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150, 111-116.
43. Ronner P., Friel E., Czerniawski K. and Frankle S. (1999) Luminometric assays of ATP, phosphocreatine, and creatine for estimation of free ADP and free AMP. Anal. Biochem. 275, 208-216.
44. Roovers R. C., Henderikx P., Helfrich W., van der Linden E., Reurs A., de Bruine A. P., Arends J. W., de Leij L. and Hoogenboom H. R. (1998) High-affinity recombinant phage antibodies to the pancarcinoma marker epithelial glycoprotein-2 for tumour targeting. Br. J. Cancer 78, 1407-1416.
45. Roshy S., Sloane B. F. and Moin K. (2003) Pericellular cathepsin B and malignant progression. Cancer Metastasis Rev. 22, 271-286.
46. Rotsch C. and Radmacher M. (2000) Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys. J. 78, 520-535.
47. Sai Y., Kajita M., Tamai I., Wakama J., Wakamiya T. and Tsuji A. (1998) Adsorptive-mediated endocytosis of a basic peptide in enterocyte-like Caco-2 cells. Am. J. Physiol. 275, G514-G520.
48. Schafer D. A. (2002) Coupling actin dynamics and membrane dynamics during endocytosis. Curr. Opin. Cell Biol. 14, 76-81.
49. Schlachetzki F., Zhu C. and Pardridge W. M. (2002) Expression of the neonatal Fc receptor (FcRn) at the blood-brain barrier. J. Neurochem. 81, 203-206.
50. Schnitzer J. E., Oh P., Pinney E. and Allard J. (1994) Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127, 1217-1232.
51. Sonnichsen B., De Renzis S., Nielsen E., Rietdorf J. and Zerial M. (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rabl1. J. Cell Biol. 149, 901-914.
52. Stanimirovic D., Morley P., Ball R., Hamel E., Mealing G. and Durkin J. P. (1996) Angiotensin II-induced fluid phase endocytosis in human cerebromicrovascular endothelial cells is regulated by the inositolphosphate signaling pathway. J. Cell Physiol. 169, 455-467.
53. Subtil A., Hemar A. and Dautry-Varsat A. (1994) Rapid endocytosis of interleukin 2 receptors when clathrin-coated pit endocytosis is inhibited. J. Cell Sci. 107, 3461-3468.
54. Suzuki T., Futaki S., Niwa M., Tanaka S., Ueda K. and Sugiura Y. (2002) Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem. 277, 2437-2443.
55. Taghon M. S. and Sadler S. E. (1994) Insulin-like growth factor 1 receptor-mediated endocytosis in Xenopus laevis oocytes. A role for receptor tyrosine kinase activity. Dev. Biol. 163, 66-74.
56. Tamai I. and Tsuji A. (2000) Transporter-mediated permeation of drugs across the blood-brain barrier. J. Pharm. Sci. 89, 1371-1388.
57. HH properties. J. Immunol. Meth. 263, 97-109.
58. Tanha J., Muruganadam A. and Stanimirovic D. (2003) Phage display technology for identifying specific antigens on brain endothelial cells. Meth. Mol. Med. 89, 435-449.
59. Tulp A., Verwoerd D. and Neefjes J. (1999) Lectin-induced retardation of subcellular organelles during preparative density gradient electrophoresis: selective purification of plasma membranes. Electrophoresis 20, 438-444.
60. Tycko B., Keith C. H. and Maxfield F. R. (1983) Rapid acidification of endocytic vesicles containing asialoglycoprotein in cells of a human hepatoma line. J. Cell Biol. 97, 1762-1776.
61. Urayama A., Grubb J. H., Sly W. S. and Banks W. A. (2004) Developmentally regulated mannose 6-phosphate receptor-mediated transport of a lysosomal enzyme across the blood-brain barrier. Prac. Natl Acad. Sci. USA 101, 12 658-12 663.
62. Wang W., Smith D. K., Moulding K. and Chen H. M. (1998) The dependence of membrane permeability by the antibacterial peptide cecropin B and its analogs, CB-1 and CB-3, on liposomes of different composition. J. Biol. Chem. 273, 27 438-27 448.
63. Wessel D. and Flugge U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143.
64. West M. A., Bretscher M. S. and Watts C. (1989) Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J. Cell Biol. 109, 2731-2739.
65. Willuda J., Kubetzko S., Waibel R., Schubiger P. A., Zangemeister-Wittke U. and Plückthun A. (2001) Tumor targeting of mono-, di-, and tetravalent anti-p185 (HER-2) miniantibodies multimerized by self-associating peptides. J. Biol. Chem. 276, 14 385-14 392.
66. Zhang J., Tanha J., Hirama T., Khieu N. H., To R., Tong-Sevinc H., Stone E., Brisson J. R. and MacKenzie C. R. (2004) Pentamerization of single-domain antibodies from phage libraries: a novel strategy for the rapid generation of high-avidity antibody reagents. J. Mol. Biol. 335, 49-56.
67. Zhang J., Li Q., Nguyen T., Tremblay T., Stone E., Kelly J. and MacKenzie R. (2005) A pentavalent single domain antibody approach to tumor antibody discovery and the development of novel proteomics reagents. J. Mol. Biol. 341, 161-169.
68. Zhang Y. and Pardridge W. M. (2001) Mediated efflux of IgG molecules from brain to blood across the blood-brain barrier. J. Neuroimmunol 104, 168-172.
69. Zhang Y., Jeong Lee H., Boado R. J. and Pardridge W. M. (2002) Receptor-mediated delivery of an antisense gene to human brain cancer cells. J. Gene Med. 4, 183-194.
70. Zheng J., Cahill S. M., Lemmon M. A., Fushman D., Schlessinger J, and Cowburn D. (1996) Identification of the binding site for acidic phospholipids on the pH domain of dynamin: implications for stimulation of GTPase activity. J. Mol Biol. 255, 14-21.