Rhesus brain microvascular endothelial cells are permissive for rhesus cytomegalovirus infection

Journal of General Virology

Volumn 86, Issue 3, 2005, Pages 545-549

  Carlson, James R ^a   Chang, W L William ^a   Zhou, Shan Shan ^a   Tarantal, Alice F ^b   Barry, Peter A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOGLIN; INTERLEUKIN 1BETA; LOW DENSITY LIPOPROTEIN; LYMPHOCYTE ANTIGEN; MATRIGEL; PHORBOL 13 ACETATE 12 MYRISTATE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ACETYLATION; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BRAIN BLOOD VESSEL; CAPILLARY; CELL CULTURE; CELL ISOLATION; CELL TYPE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE COURSE; ENDOTHELIUM CELL; FETUS; IN VITRO STUDY; MACACA; MICROVASCULATURE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TRANSPORT; PURIFICATION; RHESUS MONKEY; VASCULAR ENDOTHELIUM; VIRUS INFECTIVITY; VIRUS PLAQUE; VIRUS STRAIN;

ANIMALS; BRAIN; CYTOMEGALOVIRUS; ENDOTHELIAL CELLS; MACACA MULATTA;

CERCOPITHECINE HERPESVIRUS 8; CUCUMBER MOSAIC VIRUS; HUMAN HERPESVIRUS 5; MACACA MULATTA; PRIMATES;

EID: 14744291512     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80432-0     Document Type: Article

References (52)

1. Abbott, N. J., Hughes, C. C., Revest, P. A. & Greenwood, J. (1992). Development and characterisation of a rat brain capillary endothelial culture: towards an in vitro blood-brain barrier. J Cell Sci 103, 23-37.
2. Alford, C. A. & Britt, W. J. (1993). Cytomegalovirus. In The Human Herpesviruses, pp. 227-255. Edited by B. Roizman, R. J. Whitley & C. Lopez. New York: Raven Press.
3. Audus, K. L., Bartel, R. L., Hidalgo, I. J. & Borchardt, R. T. (1990). The use of cultured epithelial and endothelial cells for drug transport and metabolism studies. Pharm Res 7, 435-451.
4. Baldanti, F., Revello, M. G., Percivalle, E., Labo, N. & Gerna, G. (2003). Genomes of the endothelial cell-tropic variant and the parental Toledo strain of human cytomegalovirus are highly divergent. J Med Virol 69, 76-81.
5. Biegel, D., Spencer, D. D. & Pachter, J. S. (1995). Isolation and culture of human brain microvessel endothelial cells for the study of blood-brain barrier properties in vitro. Brain Res 692, 183-189.
6. Bierhaus, A., Chen, J., Liliensiek, B. & Nawroth, P. P. (2000). LPS and cytokine-activated endothelium. Semin Thromb Hemost 26, 571-587.
7. Bolovan-Fritts, C. & Wiedeman, J. A. (2001). Human cytomegalovirus strain Toledo lacks a virus-encoded tropism factor required for infection of aortic endothelial cells. J Infect Dis 184, 1252-1261.
8. Bolovan-Fritts, C. A. & Wiedeman, J. A. (2002). Mapping the viral genetic determinants of endothelial cell tropism in human cytomegalovirus. J Clin Virol 25, S97-S109.
9. Carson, M. P., Saenz de Tejada, I., Goldstein, I. & Haudenschild, C. C. (1989). Culture of human corpus cavernosum endothelium. In Vitro Cell Dev Biol 25, 248-254.
10. Chang, W. L., Kirchoff, V., Pari, G. S. & Barry, P. A. (2002a). Replication of rhesus cytomegalovirus in life-expanded rhesus fibroblasts expressing human telomerase. J Virol Methods 104, 135-146.
11. Chang, W. L., Tarantal, A. F., Zhou, S. S., Borowsky, A. D. & Barry, P. A. (2002b). A recombinant rhesus cytomegalovirus expressing enhanced green fluorescent protein retains the wild-type phenotype and pathogenicity in fetal macaques. J Virol 76, 9493-9504.
12. Craig, L. E., Spelman, J. P., Strandberg, J. D. & Zink, M. C. (1998). Endothelial cells from diverse tissues exhibit differences in growth and morphology. Microvasc Res 55, 65-76.
13. de Vries, H. E., Breedveld, B., Kuiper, J., de Boer, A. G., Van Berkel, T. J. & Breimer, D. D. (1995). High-density lipoprotein and cerebral endothelial cells in vitro: interactions and transport. Biochem Pharmacol 50, 271-273.
14. Dorovini-Zis, K., Prameya, R. & Bowman, P. D. (1991). Culture and characterization of microvascular endothelial cells derived from human brain. Lab Invest 64, 425-436.
15. Fish, K. N., Soderberg-Naucler, C., Mills, L. K., Stenglein, S. & Nelson, J. A. (1998). Human cytomegalovirus persistently infects aortic endothelial cells. J Virol 72, 5661-5668.
16. Gerna, G., Percivalle, E., Sarasini, A., Baldanti, F. & Revello, M. G. (2002). The attenuated Towne strain of human cytomegalovirus may revert to both endothelial cell tropism and leuko- (neutrophil- and monocyte-) tropism in vitro. J Gen Virol 83, 1993-2000.
17. Gerna, G., Percivalle, E., Sarasini, A., Baldanti, F., Campanini, G. & Revello, M. G. (2003). Rescue of human cytomegalovirus strain AD169 tropism for both leukocytes and human endothelial cells. J Gen Virol 84, 1431-1436.
18. Gordon, E. L., Danielsson, P. E., Nguyen, T. S. & Winn, H. R. (1991). A comparison of primary cultures of rat cerebral microvascular endothelial cells to rat aortic endothelial cells. In Vitro Cell Dev Biol 27A, 312-326.
19. Greenwood, J. (1992). Characterization of a rat retinal endothelial cell culture and the expression of P-glycoprotein in brain and retinal endothelium in vitro. J Neuroimmunol 39, 123-132.
20. Grundy, J. E., Lawson, K. M., MacCormac, L. P., Fletcher, J. M. & Yong, K. L. (1998). Cytomegalovirus-infected endothelial cells recruit neutrophils by the secretion of C-X-C chemokines and transmit virus by direct neutrophil-endothelial cell contact and during neutrophil transendothelial migration. J Infect Dis 177, 1465-1474.
21. Hahn, G., Khan, H., Baldanti, F., Koszinowski, U. H., Revello, M. G. & Gerna, G. (2002). The human cytomegalovirus ribonucleotide reductase homolog UL45 is dispensable for growth in endothelial cells, as determined by a BAC-cloned clinical isolate of human cytomegalovirus with preserved wild-type characteristics. J Virol 76, 9551-9555.
22. Jarvis, M. A. & Nelson, J. A. (2002). Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr Opin Microbiol 5, 403-407.
23. Kahl, M., Siegel-Axel, D., Stenglein, S., Jahn, G. & Sinzger, C. (2000). Efficient lytic infection of human arterial endothelial cells by human cytomegalovirus strains. J Virol 74 7628-7635.
24. Kubota, Y., Kleinman, H. K., Martin, G. R. & Lawley, T. J. (1988). Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107, 1589-1598.
25. Lamszus, K., Schmidt, N. O., Ergun, S. & Westphal, M. (1999). Isolation and culture of human neuromicrovascular endothelial cells for the study of angiogenesis in vitro. J Neurosci Res 55 370-381.
26. Lockridge, K. M., Sequar, G., Zhou, S. S., Yue, Y., Mandell, C. P. & Barry, P. A. (1999). Pathogenesis of experimental rhesus cytomegalovirus infection. J Virol 73, 9576-9583.
27. MacCormac, L. P. & Grundy, J. E. (1999). Two clinical isolates and the Toledo strain of cytomegalovirus contain endothelial cell tropic variants that are not present in the AD169, Towne, or Davis strains. J Med Virol 57, 298-307.
28. MacLean, A. G., Orandle, M. S., Alvarez, X., Williams, K. C. & Lackner, A. A. (2001). Rhesus macaque brain microvessel endothelial cells behave in a manner phenotypically distinct from umbilical vein endothelial cells. J Neuroimmunol 118, 223-232.
29. Maidji, E., Percivalle, E., Gerna, G., Fisher, S. & Pereira, L. (2002). Transmission of human cytomegalovirus from infected uterine microvascular endothelial cells to differentiating/invasive placental cytotrophoblasts. Virology 304, 53-69.
30. Manconi, F., Markham, R. & Fraser, I. S. (2000). Culturing endothelial cells of microvascular origin. Methods Cell Sci 22, 89-99.
31. Myerson, D., Hackman, R. C., Nelson, J. A., Ward, D. C. & McDougall, J. K. (1984). Widespread presence of histologically occult cytomegalovirus. Hum Pathol 15, 430-439.
32. Page, C., Rose, M., Yacoub, M. & Pigott, R. (1992). Antigenic heterogeneity of vascular endothelium. Am J Pathol 141 673-683.
33. Plachter, B., Sinzger, C. & Jahn, G. (1996). Cell types involved in replication and distribution of human cytomegalovirus. Adv Virus Res 46, 195-261.
34. Rauh, J., Meyer, J., Beuckmann, C. & Galla, H. J. (1992). Development of an in vitro cell culture system to mimic the blood-brain barrier. Prog Brain Res 91, 117-121.
35. Sedmak, D. D., Guglielmo, A. M., Knight, D. A., Birmingham, D. J., Huang, E. H. & Waldman, W. J. (1994). Cytomegalovirus inhibits major histocompatibility class II expression on infected endothelial cells. Am J Pathol 144, 683-692.
36. Sequar, G., Britt, W. J., Lakeman, F. D., Lockridge, K. M., Tarara, R. P., Canfield, D. R., Zhou, S. S., Gardner, M. B. & Barry, P. A. (2002). Experimental coinfection of rhesus macaques with rhesus cytomegalovirus and simian immunodeficiency virus: pathogenesis. J Virol 76, 7661-7671.
37. Sinzger, C., Schmidt, K., Knapp, J., Kahl, M., Beck, R., Waldman, J., Hebart, H., Einsele, H. & Jahn, G. (1999). Modification of human cytomegalovirus tropism through propagation in vitro is associated with changes in the viral genome. J Gen Virol 80, 2867-2877.
38. Slobbe-van Drunen, M. E., Vossen, R. C., Couwenberg, F. M., Hulsbosch, M. M., Heemskerk, J. W., van Dam-Mieras, M. C. & Bruggeman, C. A. (1997). Activation of protein kinase C enhances the infection of endothelial cells by human cytomegalovirus. Virus Res 48, 207-213.
39. Stanness, K. A., Guatteo, E. & Janigro, D. (1996). A dynamic model of the blood-brain barrier "in vitro". Neurotoxicology 17, 481-496.
40. Steffan, A. M., Lafon, M. E., Gendrault, J. L., Koehren, F., De Monte, M., Royer, C., Kirn, A. & Gut, J. P. (1994). Feline immunodeficiency virus can productively infect cultured endothelial cells from cat brain microvessels. J Gen Virol 75, 3647-3653.
41. Stins, M. F., Gilles, F. & Kim, K. S. (1997). Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76, 81-90.
42. Strelow, L. I., Watry, D. D., Fox, H. S. & Nelson, J. A. (1998). Efficient infection of brain microvascular endothelial cells by an in vivo-selected neuroinvasive SIVmac variant. J Neurovirol 4, 269-280.
43. Takakura, Y., Audus, K. L. & Borchardt, R. T. (1991). Blood-brain barrier: transport studies in isolated brain capillaries and in cultured brain endothelial cells. Adv Pharmacol 22, 137-165.
44. Tarantal, A. F., Salamat, S., Britt, W. J., Luciw, P. A., Hendrickx, A. G. & Barry, P. A. (1998). Neuropathogenesis induced by rhesus cytomegalovirus in fetal rhesus monkeys (Macaca mulatta). J Infect Dis 177, 446-450.
45. Turner, R. R., Beckstead, J. H., Warnke, R. A. & Wood, G. S. (1987). Endothelial cell phenotypic diversity. In situ demonstration of immunologic and enzymatic heterogeneity that correlates with specific morphologic subtypes. Am J Clin Pathol 87, 569-575.
46. Unger, R. E., Oltrogge, J. B., von Briesen, H., Engelhardt, B., Woelki, U., Schlote, W., Lorenz, R., Bratzke, H. & Kirkpatrick, C. J. (2002). Isolation and molecular characterization of brain microvascular endothelial cells from human brain tumors. In Vitro Cell Dev Biol Anim 38, 273-281.
47. Vinters, H. V., Reave, S., Costello, P., Girvin, J. P. & Moore, S. A. (1987). Isolation and culture of cells derived from human cerebral microvessels. Cell Tissue Res 249, 657-667.
48. Waldman, W., Roberts, W. H., Davis, D. H., Williams, M. V., Sedmark, D. D. & Stephens, R. E. (1991). Preservation of natural endothelial cytopathogenicity of cytomegalovirus by propagation in endothelial cells. Arch Virol 117, 143-164.
49. Washington, R., Burton, J., Todd, R. F., III, Newman, W., Dragovic, L. & Dore-Duffy, P. (1994). Expression of immunologically relevant endothelial cell activation antigens on isolated central nervous system microvessels from patients with multiple sclerosis. Ann Neurol 35, 89-97.
50. Wolburg, H., Neuhaus, J., Kniesel, U., Krauss, B., Schmid, E. M., Ocalan, M., Farrell, C. & Risau, W. (1994). Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J Cell Sci 107, 1347-1357.
51. Wong, D. & Dorovini-Zis, K. (1992). Upregulation of intercellular adhesion molecule-1 (ICAM-1) expression in primary cultures of human brain microvessel endothelial cells by cytokines and lipopolysaccharide. J Neuroimmunol 39, 11-21.
52. Yamamoto-Tabata, T., McDonagh, S., Chang, H. T., Fisher, S. & Pereira, L. (2004). Human cytomegalovirus interleukin-10 down-regulates metalloproteinase activity and impairs endothelial cell migration and placental cytotrophoblast invasiveness in vitro. J Virol 78, 2831-2840.