In vitro methods in the study of viral and prion permeability across the blood-brain barrier

Cellular and Molecular Neurobiology

Volumn 25, Issue 1, 2005, Pages 171-181

  Nakaoke, Ryota ^a,b   Banks, William A ^b,c  

^a NAGASAKI UNIVERSITY   (Japan)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NONE   (United States)

Author keywords

Blood brain barrier; gp120; HIV 1; In vitro study; Prion

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; MEPACRINE; PENTOSAN POLYSULFATE;

ANTIVIRAL ACTIVITY; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN NERVE CELL; CENTRAL NERVOUS SYSTEM INFECTION; DISEASE ASSOCIATION; DRUG TARGETING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; NEUROPATHOLOGY; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; REVIEW; SCRAPIE AGENT; VIRUS INFECTIVITY; VIRUS PATHOGENESIS;

EID: 17644384471     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-004-1381-z     Document Type: Review

References (78)

1. Abbott, N. J. (2002). Astrocyte-endothelial interactions and blood-brain barrier. J. Anatomy 200:629-638.
2. Audus, K. L., and Borchardt, R. T. (1987). Bovine brain microvessel endothelial cell monolayers as a model system for the blood-brain barrier. Biological Approaches to the Controlled Delivery of Drugs, Ann. NY Acad. Sci., pp. 9-18, New York.
3. Bagasra, O., Lavi, E., Bobroski, L., Khalili, K., Pestaner, J. P., Tawadros. R., and Pomerantz, R. J. (1996). Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: Identification by the combination of in situ polymerase chain reaction and immunohistochemistry. AIDS 10:573-585.
4. 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.
5. Banks, W. A., Freed, E. O., Wolf, K. M., Robinson, S. M., Franko, M., and Kumar, V. B. (2001). Transport of human immunodeficiency virus type 1 pseudoviruses across the blood-brain barrier: Role of envelope proteins and adsorptive endocytosis. J. Virol. 75:4681-4691.
6. Banks, W. A., Kastin, A. J., and Akerstrom. V. (1997). HIV-1 protein gp120 crosses the blood-brain barrier: Role of adsorptive endocytosis. Life Sci. 61:L119-L125.
7. Britton, T. C., Al-Sarraj, S., Shaw, C., Campbell, T., and Collinge, J. (1995). Sporadic Creutzfeldt-Jakob disease in a 16-year-old in the UK. Lancet 3469:1155.
8. Brown, D. R. (2002). Mayhem of the multiple mechanisms: Modeling neurodegeneration in prion disease. J. Neurochem. 82:209-215
9. Caughy, B., and Raymond, G. J. (1993). Sulfated polyanion inhibition of scrapie-associated PrP accumulation in cultured cells. J. Virol. 67:643-650.
10. Chou, S., and Dix, R. D. (1989). Viral infections and the blood-brain barrier. In Neuwelt, E. A. (ed.) Implications of the Blood-Brain Barrier and Its Manipulation, Vol. 2, Clinical Aspects, Plenum Publishing Corporation, New York, pp. 449-468.
11. Deli, M. A., and Joo, F. (1996). Culture vascular endothelial cells of the brain. Keio J. Med. 45:183-198.
12. Deli, M. A., Niwa, M., Katamine, S., and Abraham, C. S. (1999). Pentosan in transmissible spongiform encephalopathies. Lancet 353:1272.
13. Deli, M. A., Sakaguchi, S., Nakaoke, R., Abraham, C. S., Takahata, H., Kopacek, J., Shigematsu, K., Katamine, S., and Niwa, M. (2000). PrP fragment 106-126 is toxic to cerebral endothelial cells expressing PrP(C). Neuroreport 11:3931-3936.
14. Di Stefano, M., Gray, F., Leitner, T., and Chiodi, F. (1996). Analysis of ENV V3 sequences from HIV-1-infected brain indicates restrained virus expression throughout the disease. J. Med. Virol 49:41-48.
15. Dubin, N. H., Strandberg, J. D, Craft, C. F, Parmley, T. H., Blake, D. A., and King, T. M. (1982). Effect of intrauterine and intravascular quinacrine administration on histopathology, blood chemistry, and hematology in cynomolgus monkeys. Fertil. Steril. 38:735-740.
16. Edinger, A. L., Mankowski, J. L., Doranz, B. J, Margulies, B. J., Lee, B., Rucker, J, Sharron, M., Hoffman, T. L., Berson, J. F, Zink, M. C, Hirsch, V. M., Clements. J. E., and Doms, R. W. (1997). CD4-independent, CCR5-dependent infection of brain capillary endothelial cells by a neurovirulent simian immunodeficiency virus strain. Proc. Natl Acad. Sci. USA 94:14742-14747.
17. Falangola, M. E., Hanly, A., Galvao-Castro, B., and Petito, C. K. (1995). HIV infection of human choroid plexus: A possible mechanism of viral entry into the CNS. J. Neuropathol. Exp. Neural. 54:497-503.
18. Farquhar, C., Dickinson, A., and Bruce, M. (1999). Prophylactic potential of pentosan polysulphate in transmissible spongiform encephalopathies. Lancet 353:117.
19. Feng, Y., Broder, C. C., Kennedy. P. E., and Berger. E. A. (1996). HIV-1 entry cofactor: Function cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877.
20. Filice, G., Cereda, P. M., and Varnier, O. E. (1988). Infection in rabbits with human immunodeficiency virus. Nature 335:366-369.
21. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O., and Tagliavini, F. (1993). Neurotoxicity of a prion protein fragment. Nature 362:543-546.
22. Furukawa, H., Takahashi, M., Nakajima, M., and Yamada, T. (2002). Prospects of the therapeutic approaches to Creutzfeldt-Jakob disease: A clinical trial of antimalarial, quinacrine. Nippon Rinsho 60:1649-1657.
23. Gilat, D., Hershkoviz, R., Mekori, Y. A., Vlodavsky, I., and Lider. O. (1994). Regulation of adhesion of CD4+ T lymphocytes to intact or heparinase-treated subendothelial extracellular matrix by diffusible or anchored RANTES and MIP-I beta. J. Immunol 153:4899-4906.
24. Grossman, D. M., Banks, W. A., LeBlanc, J., and Dejace, P. (1998). Prevalence of hypernatremia in HIV-infected VA patients. J. Invest. Med. 46:46A.
25. Gu, Y., Fujioka, H., Mishra, R. S., Li, R., and Singh, N. (2002). Prion peptide 106-126 modulates the aggregation of cellular prion protein and induces the synthesis of potentially neurotoxic transmembrane PrP. J. Biol. Chem. 277:2275-2286.
26. Hardebo, J. E., and Kahrstrom, J. (1985). Endothelial negative surface charge areas and blood-brain barrier function. Acta Physiol Scand. 125:495-499.
27. Hernandez, L. D, Hoffman. L. R., Wolfsber, T. G, and White, J. M. (1996). Virus-cell and cell-cell fusion. Annu. Rev. Dev. Biol 12:627-661.
28. Hill, J. M., Mervis, R. F, Avidor, R., Moody, T. W., and Brenneman, D. E. (1993). HIV envelope proteininduced neuronal damage and retardation of behavioral development in rat neonates. Brain Res. 603:222-233.
29. Hosmalin, A., Clerici, M., Houghten, R., Pendleton, C. D., Flexner, C., Lucey, D. R., Moss. B., Germain, R. N., Shearer, G. M., and Berzofsky, J. A. (1990). An epitope in human immunodeficiency virus 1 reverse transcriptase recognized by both mouse and human cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 87:2344-2348.
30. Hunter, N., Foster, J, Chong, A., McCutcheon, S., Parnham, D., Eaton, S., MacKenzie, C., and Houston, F. (2002). Transmission of prion disease by blood transfusion. J. Gen. Virol. 83:2897-2905.
31. Hurwitz, A. A., Berman, J W., and Lyman, W. D. (1994). The role of the blood-brain barrier in HIV infection of the central nervous system. Adv. Neuroimmunol. 4:249-256.
32. Joo, F (1992). The cerebral microvessels in culture, an update. J. Neurochem. 58:1-17.
33. Kalomiris, E. L., and Bourguignon, L. Y (1988). Mouse T lymphoma cells contain a transmembrane glycoprotein (GP85) that binds ankyrin. J. Cell Biol. 106:319-327.
34. Kopacek, J., Sakaguchi, S., Shigematsu, K., Nishida, N., Atarashi, R., Nakaoke, R., Moriuchi, R., Niwa, M., and Katamine, S. (2000). Upregulation of the genes encoding lysosomal hydrolases, a perforin-like protein, and peroxidases in the brains of mice affected with an experimental prion disease. J. Virol. 74:411-417.
35. Koperk, O., Kovacs, G. G., Ritchie, D., Ironside, J. W., Budka, H., and Wick, G. (2002). Disease-associated prion protein in vessel walls. Am. J. Pathol. 161:1979-1984.
36. Koyanagi, Y., Tanaka, Y., Kira, J., Ito, M., Hioki, K., Misawa, N., Kawano, Y., Yamasaki, K., Tanaka, R., Suzuki. Y., Ueyama, Y., Terada, E., Tanaka, T. Myasaka, M., Kobayashi, T., Kumazawa. Y., and Yamamoto, N. (1997). Primary human immunodeficiency virus type 1 viremia and central nervous system invasion in a novel hu-PBL-immunodeficient mouse strain. J. Virol. 71:2417-2424.
37. Lafon, M. E., Gendrault. J. L., Royer, C., Jaeck. D., Kirn, A., and Steffan, A. M. (1993). Human endothelial cells isolated from the hepatic sinusiods and the umbilical vein display a different permissiveness for HIV-1. Res. Virol. 144:99-104.
38. Lehto, V. P., and Virtanen, I. (1983). Immunolocalization of a novel, cytoskeleton-associated polypeptide of Mr 230,000 daltons (p230). J. Cell Biol. 96:703-716.
39. Li, A., Sakagchi, S., Shigematsu, K., Atarashi, R., Roy, B. C., Nakaoke, R., Arima, K., Okimura, N., Kopacek, J., and Katamine, S. (2000). Physiological expression of the gene for PrP-like protein, PrPLP/Dpl, by brain endothelial cells and its ectopic expression in neurons of PrP-deficient mice ataxic due to Purkinje cell degeneration. Am. J. Pathol. 157:1447-1452.
40. Lipton, S. A. (1991). HIV-related neurotoxicity. Brain Pathol. 1:193-199.
41. Lossinsky, A. S., Pluta. R., Song. M. J., Badmajew, V., Moretz, R. C., and Wisniewski, H. M. (1991). Mechanisms of inflammatory cell attachment in chronic relapsing experimental allergic encephalomyelitis: A scanning and high-voltage electron microscopic study of the injured mouse blood-brain barrier. Microvasc. Res. 41:299-310.
42. Mankowski, J. L., Spelman, J. P., Ressetar, H. G., Strandberg, J. D., Leterra, J., Carter, D. L., Clements, J. E., and Zink, M. C. (1999). Neurovirulent simian immunodeficiency virus replicated productively in endothelial cells of the central nervous system in vivo and in vitro. J. Virol. 68:8202-8208.
43. Marcus, C. D., Taylor-Robinson, S. D., Sargentoni, J., Ainsworth, J. G., Frize, G, Easterbrook, P. J., Shaunak, S., and Bryant, D. J. (1998). 1H MR spectroscopy of the brain in HIV-1-seropositive subjects: Evidence for diffuse metabolic abnormalities. Met. Brain Dis. 13:123-136.
44. Marsh, M. (1984). The entry of enveloped viruses into cells by endocytosis. Biochem. J. 218:1-10.
45. McKeating, J. A., McKnight, A., and Moore, J. P. (1991). Differential loss of envelope glycoprotein gp120 from virions of human immunodeficiency virus type 1 isolates: Effects on infectivity and neutralization. J. Virol. 65:852-860.
46. Mehta, R., Zingde, S., Advani, S., Desai, H., and Gothoskar, B. (1999). Protein 1a: A major wheat germ agglutinin binding protein on the surface of human granulocytes associated with the cytoskeleton. Mol. Cell. Biochem. 144:153-165.
47. Mellman, I., Fuchs, R., and Helenius, A. (1986). Acidification of the endocytic and exocytic pathways. Ann. Rev. Biochem. 55:663-700.
48. Moses, A. V., Bloom, F. E., Pauza, C. D., and Nelson, J. A. (1993). Human immunodeficiency virus infection of human brain capillary endothelial cells occurs via a CD4/galactosylceramide-independent mechanism. Proc. Natl Acad. Sci. USA 90:10474-10478.
49. Moses, A. V., and Nelson, J. A. (1994). HIV infection of human brain capillary endothelial cells-implications for AIDS dementia. Adv. Neuroimmunol. 4:239-247.
50. Moses, A. V., Stenglein, S. G., Strussenberg, J. G., Wehrly, K., Chesebro, B., and Nelson, J. A. (1996). Sequences regulating tropism of human immunodeficiency virus type 1 for brain capillary endothelial cells map to a unique region of the viral genome. J. Virol. 70:3401-3406.
51. Nakaoke, R., Sakaguchi, S., Atarashi, R., Nishida, N., Arima, K., Shigematsu. K., and Katamine, S. (2000). Early appearance but lagged accumulation of detergent-insoluble prion protein in the brains of mice inoculated with a mouse-adapted Creutzfeldt-Jakob disease agent. Cell. Mol. Neurobiol. 20:717-720.
52. Nishida, N., Katamine, S., Shigematsu, K., Nakatani, A., Sakamoto, N., Hasegawa, S., Nakaoke, R., Atarashi, R., Kataoka, Y., and Miyamoto, T. (1997). Prion protein is necessary for latent learning and long-term memory retention. Cell. Mol. Neurobiol. 17:537-545.
53. Nottet, H. S., Persidsky, Y., Sasseville, V. G., Nukuna, A. N., Bock, P., Zhai, Q. H., Sharer, L. R., McComb, R. D., Swindells, S., Soderland, C., and Gendelman, H. E. (1996). Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J. Immunol. 156:1284-1295.
54. Oster, S., Christoffersen, P., Gundersen, H. J., Nielsen, J. O., Pakkenberg, B., and Pedersen, C. (1993) Cerebral atrophy in AIDS: A stereological study. Acta Neuropathol. 85:617-622.
55. Persidsky, Y., Stins, M., Way, D., Witte, M. H., Weinand, M., Kim. K. S., Bock. P., Gendelman. H. E., and Fiala, M. (1997). A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. J. Immunol. 158:3499-3510.
56. Pleskoff, O., Sol, N., Labrosse, B., and Alizon, M. (1997a). Human immunodeficiency virus strains differ in their ability to infect CD4+ cells expressing the rat homolog of CXCR-4 (fusin). J. Virol. 71:3259-3262.
57. Pleskoff, O., Treboute, C. Brelot, A., Heveker, N., Seman, M., and Alizon, M. (1997b). Identification of a chemokine receptor encoded by human cytomegalovirus as a cofactor for HIV-1 entry. Science 276:1874-1878.
58. Poland, S. D., Rice, G. P., and Dekaban, G. A. (1995a). HIV-1 infection of human brain-derived microvascular endothelial cells in vitro. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 8:437-445.
59. Poland, S. D., Dekaban, G. A., Costello, P. C., Rice, G. P. (1995b). Cytomegalovirus-caused release of collagenase IV from human cerebral microvascular endothelial cells. Clin. Diagn. Virol. 4:301-309.
60. Poleshchuk, N. N., Votyakov, V. I., Ilkevich, Yu G, Duboiskaya, G. P., Grigoriev, D. G., and Kolomiets, N. D. (1992). Structural and functional changes of blood-brain barrier and indication of prion amyloid filaments in experimental amyotrophic leucospongiosis. Acta Virol. 36:293-303.
61. Prusiner, S. B. (1982). Novel proteinaceous infectious particles cause scrapie. Science 216:136-144.
62. Prusiner, S. B. (1998). Prions. Proc. Natl Acad. Sci. USA 95:13363-13383.
63. Prusiner, S. B., Groth, D. F., Bolton. D. C., Kent. S. B., and Hood. L. E. (1984). Purification and structural studies of a major scrapie prion protein. Cell 38:127-134.
64. Raeissi, S., and Audus, K. L. (1989). In-vitro characterization of blood-brain barrier permeability to delta sleep-inducing peptide. Ann. N Y Acad. Sci 41:848-852.
65. Resnick, L., Berger, J., Shapshak. P., and Tourtellotte, W. W. (1988). Early penetration of the blood-brain-barrier by HIV. Neurology 38:9-14.
66. Salmivirta, M., Lidholt, K., and Lindahl, U. (1996). Heparan sulfate: A piece of information. FASEB J. 10:1270-1279.
67. Salmona. M., Malesani, P., De Gioia, L., Gorla, S., Bruschi, M., Molinari, A., Della Vedova, F, Pedrotti. B., Marrari, M. A., Awan, T., Bugiani, O., Gorloni. G., and Tagliavini, F. (1999) Molecular determinants of the physicochemical properties of a critical prion protein region comprising residues 106-126. Biochem. J. 342:207-214.
68. Sakaguchi, S., Katamine, S., Nishida, N., Moriuchi, R., Shigematsu, K., Sugimoto, T., Nakatani, A., Kataoka, Y., Houtani. T., Shirabe, S., Okada, H., Hasegawa, S., Miyamoto, T., and Noda, T. (1996) Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature 380:528-531.
69. Sjolander. A., and Magnusson. K. E. (1988). Effects of wheat germ agglutinin on the cellular content of filamentous actin in Intestine 407 cells. Eur. J. Cell Biol. 47:32-35.
70. Steinman, J. L., Komisaruk, B. R., Pert, C., and Ruff, M. (1993). Monoparesis induced by gp-120 administered intrathecally in rats. Int. Conf. AIDS 9:193.
71. Strelow, L. I., Watry, D. D., Fox, H. S., and Nelson, J. A. (1998). Efficient infection of brain microvascular endothelial cells by an in vivo-selected neuroinvasive SIVmac variant. J. Neurovirol. 4:269-280.
72. Suchard, S. J. and Boxer, L. A. (1989). Characterization and cytoskeletal association of a major cell surface glycoprotein, GP 140, in human neutrophils. J. Clin. Invest. 84:484-492.
73. Vitkovic, L., da Cunha, A., and Tyor, W. R. (1994). Cytokine expression and pathogenesis in AIDS brain. In Price, R. W., and Perry, S. W. (eds.). HIV, AIDS and the Brain, Raven Press Ltd., New York, pp 203-221.
74. Weissmann, C., Enari, M., Klohn, P. C., Rossi, D., and Flechsig, D. (2002). Transmission of Prions. Proc. Natl. Acad. Sci. USA. 99:16378-16683.
75. Westergren, I., and Johansson, B. B. (1993). Altering the blood-brain barrier in the rat by intracarotid nfusion of polycations: A comparison between protamine, poly-L-lysine and poly-L-arginine. Acta Physiol. Scand. 149:99-104.
76. Wiley, C. A., Schrier, R. D., Nelson, J. A., Lampert, P. W., and Oldstone, M. B. A. (1986). Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc. Natl. Acad. Sci. USA 83:7089-7093.
77. Willey, R. L., Martin, M. A., and Peden. K. W. C. (1994). Increase in soluble CD4 binding to and CD4-induced dissociation of gp120 from virions correlates with infectivity of human immunodeficiency virus type 1. J. Virol. 68:1029-1039.
78. Winslow, B. J., and Trono, D. (1993). The blocks to human immunodeficiency virus type 1 Tat and Rev functions in mouse cell lines are independent. J. Virol. 67:2349-2354.