1887

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Volume 86, Issue 3

Rhesus brain microvascular endothelial cells are permissive for rhesus cytomegalovirus infection Free

Abstract

Endothelial cells (EC) are an important cell type for human cytomegalovirus (CMV) pathogenesis. To characterize better the role of EC in primate CMV natural history, rhesus macaque microvascular EC (MVEC) were purified from fetal brain and analysed for infectivity by rhesus cytomegalovirus (RhCMV). Rhesus brain MVEC (BrMVEC) in culture were positive for von Willebrand factor and CD105 expression, uptake of acetylated low-density lipoprotein, and formation of capillary-like tubules on Matrigel, all phenotypic hallmarks of EC. BrMVEC were fully permissive for infection by RhCMV strain 68-1, and detectable plaques formed within 5 days of infection. Infectivity of BrMVEC by RhCMV could be reduced, but not abolished, by treatment of cells either before or during infection with pro-inflammatory mediators tumour necrosis factor-, interleukin-1 or phorbol 12-myristate 13-acetate. These results demonstrate that infection of rhesus BrMVEC is a dynamic process that is influenced by activation conditions.

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2005-03-01
2024-04-19
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References

  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
     [Google Scholar]
  2. Alford C. A., Britt W. J. 1993; Cytomegalovirus. In The Human Herpesviruses pp  227–255 Edited by Roizman B., Whitley R. J., Lopez C. New York: Raven Press;
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  6. Bierhaus A., Chen J., Liliensiek B., Nawroth P. P. 2000; LPS and cytokine-activated endothelium. Semin Thromb Hemost 26:571–587 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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 25248–254 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 27A312–326
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  22. Jarvis M. A., Nelson J. A. 2002; Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr Opin Microbiol 5:403–407 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  30. Manconi F., Markham R., Fraser I. S. 2000; Culturing endothelial cells of microvascular origin. Methods Cell Sci 22:89–99 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  32. Page C., Rose M., Yacoub M., Pigott R. 1992; Antigenic heterogeneity of vascular endothelium. Am J Pathol 141:673–683
     [Google Scholar]
  33. Plachter B., Sinzger C., Jahn G. 1996; Cell types involved in replication and distribution of human cytomegalovirus. Adv Virus Res 46:195–261
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  39. Stanness K. A., Guatteo E., Janigro D. 1996; A dynamic model of the blood-brain barrier "in vitro". Neurotoxicology 17:481–496
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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 38273–281 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  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
     [Google Scholar]
  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 [CrossRef]
     [Google Scholar]
  52. Yamamoto-Tabata T., McDonagh S., Chang H. T., Fisher S., Pereira L. 2004; Human cytomegalovirus interleukin-10 downregulates metalloproteinase activity and impairs endothelial cell migration and placental cytotrophoblast invasiveness in vitro. J Virol 78:2831–2840 [CrossRef]
     [Google Scholar]
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Rhesus brain microvascular endothelial cells are permissive for rhesus cytomegalovirus infection
J. Gen. Virol. 86, 545 (2005); https://doi.org/10.1099/vir.0.80432-0
/content/journal/jgv/10.1099/vir.0.80432-0
/content/journal/jgv/10.1099/vir.0.80432-0
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