West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: Transmigration across the in vitro blood-brain barrier

Virology

Volumn 385, Issue 2, 2009, Pages 425-433

  Verma, Saguna ^a   Lo, Yeung ^a   Chapagain, Moti ^a   Lum, Stephanie ^a   Kumar, Mukesh ^a   Gurjav, Ulziijargal ^a,b   Luo, Haiyan ^a   Nakatsuka, Austin ^a   Nerurkar, Vivek R ^a,b  

^a Asia Pacific Institute of Tropical Medicine and Infectious Diseases   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

BBB; CAM; Claudin; FITC dextran permeability assay; Flavivirus; HBMVE; TEER; TJP; WNV

Indexed keywords

CD31 ANTIGEN; CLAUDIN 1; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 3; MESSENGER RNA; PROTEIN ZO1; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; GENE EXPRESSION; HUMAN; HUMAN CELL; MICROVASCULATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA VIRUS INFECTION; TIGHT JUNCTION; VASCULAR ENDOTHELIUM; VIRUS ENTRY; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE; WEST NILE FLAVIVIRUS;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL ADHESION MOLECULES; CELL LINE; CERCOPITHECUS AETHIOPS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE PROTEINS; TIGHT JUNCTIONS; VERO CELLS; WEST NILE FEVER; WEST NILE VIRUS;

EQUIDAE; FLAVIVIRUS; WEST NILE VIRUS;

EID: 60949114530     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.11.047     Document Type: Article

References (55)

1. Afonso P.V., Ozden S., Prevost M.C., Schmitt C., Seilhean D., Weksler B., Couraud P.O., Gessain A., Romero I.A., and Ceccaldi P.E. Human blood-brain barrier disruption by retroviral-infected lymphocytes: role of myosin light chain kinase in endothelial tight-junction disorganization. J. Immunol. 179 4 (2007) 2576-2583
2. Andras I.E., Pu H., Deli M.A., Nath A., Hennig B., and Toborek M. HIV-1 Tat protein alters tight junction protein expression and distribution in cultured brain endothelial cells. J. Neurosci. Res. 74 2 (2003) 255-265
3. Arjona A., Foellmer H.G., Town T., Leng L., McDonald C., Wang T., Wong S.J., Montgomery R.R., Fikrig E., and Bucala R. Abrogation of macrophage migration inhibitory factor decreases West Nile virus lethality by limiting viral neuroinvasion. J. Clin. Invest. 117 10 (2007) 3059-3066
4. Avolio C., Giuliani F., Liuzzi G.M., Ruggieri M., Paolicelli D., Riccio P., Livrea P., and Trojano M. Adhesion molecules and matrix metalloproteinases in multiple sclerosis: effects induced by interferon-beta. Brain Res. Bull. 61 3 (2003) 357-364
5. Bentz G.L., Jarquin-Pardo M., Chan G., Smith M.S., Sinzger C., and Yurochko A.D. Human cytomegalovirus (HCMV) infection of endothelial cells promotes naive monocyte extravasation and transfer of productive virus to enhance hematogenous dissemination of HCMV. J. Virol. 80 23 (2006) 11539-11555
6. Brankin B., Hart M.N., Cosby S.L., Fabry Z., and Allen I.V. Adhesion molecule expression and lymphocyte adhesion to cerebral endothelium: effects of measles virus and herpes simplex 1 virus. J. Neuroimmunol. 56 1 (1995) 1-8
7. Bunning M.L., Bowen R.A., Cropp C.B., Sullivan K.G., Davis B.S., Komar N., Godsey M.S., Baker D., Hettler D.L., Holmes D.A., Biggerstaff B.J., and Mitchell C.J. Experimental infection of horses with West Nile virus. Emerg. Infect. Dis. 8 4 (2002) 380-386
8. Chapagain M.L., Nguyen T., Bui T., Verma S., and Nerurkar V.R. Comparison of real-time PCR and hemagglutination assay for quantitation of human polyomavirus JC. Virol. J. 3 (2006) 3
9. Chapagain M.L., Verma S., Mercier F., Yanagihara R., and Nerurkar V.R. Polyomavirus JC infects human brain microvascular endothelial cells independent of serotonin receptor 2A. Virology 364 1 (2007) 55-63
10. Chaudhuri A., Yang B., Gendelman H.E., Persidsky Y., and Kanmogne G.D. STAT1 signaling modulates HIV-1-induced inflammatory responses and leukocyte transmigration across the blood-brain barrier. Blood 111 4 (2008) 2062-2072
11. Cheeran M.C., Hu S., Sheng W.S., Rashid A., Peterson P.K., and Lokensgard J.R. Differential responses of human brain cells to West Nile virus infection. J. Neurovirol. 11 6 (2005) 512-524
12. Cosby S.L., and Brankin B. Measles virus infection of cerebral endothelial cells and effect on their adhesive properties. Vet. Microbiol. 44 2-4 (1995) 135-139
13. Davis L.E., DeBiasi R., Goade D.E., Haaland K.Y., Harrington J.A., Harnar J.B., Pergam S.A., King M.K., DeMasters B.K., and Tyler K.L. West Nile virus neuroinvasive disease. Ann. Neurol. 60 3 (2006) 286-300
14. Deli M.A., Abraham C.S., Kataoka Y., and Niwa M. Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell. Mol. Neurobiol. 25 1 (2005) 59-127
15. Diamond M.S., Shrestha B., Mehlhop E., Sitati E., and Engle M. Innate and adaptive immune responses determine protection against disseminated infection by West Nile encephalitis virus. Viral Immunol. 16 3 (2003) 259-278
16. Eugenin E.A., Osiecki K., Lopez L., Goldstein H., Calderon T.M., and Berman J.W. CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the blood-brain barrier: a potential mechanism of HIV-CNS invasion and NeuroAIDS. J. Neurosci. 26 4 (2006) 1098-1106
17. German A.C., Myint K.S., Mai N.T., Pomeroy I., Phu N.H., Tzartos J., Winter P., Collett J., Farrar J., Barrett A., Kipar A., Esiri M.M., and Solomon T. A preliminary neuropathological study of Japanese encephalitis in humans and a mouse model. Trans. R. Soc. Trop. Med. Hyg. 100 12 (2006) 1135-1145
18. Glass W.G., Lim J.K., Cholera R., Pletnev A.G., Gao J.L., and Murphy P.M. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J. Exp. Med. 202 8 (2005) 1087-1098
19. Hayes E.B., and Gubler D.J. West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annu. Rev. Med. 57 (2006) 181-194
20. Jong A.Y., Stins M.F., Huang S.H., Chen S.H., and Kim K.S. Traversal of Candida albicans across human blood-brain barrier in vitro. Infect. Immun. 69 7 (2001) 4536-4544
21. Jordan I., Briese T., Fischer N., Lau J.Y., and Lipkin W.I. Ribavirin inhibits West Nile virus replication and cytopathic effect in neural cells. J. Infect. Dis. 182 4 (2000) 1214-1217
22. Kanmogne G.D., Primeaux C., and Grammas P. HIV-1 gp120 proteins alter tight junction protein expression and brain endothelial cell permeability: implications for the pathogenesis of HIV-associated dementia. J. Neuropathol. Exp. Neurol. 64 6 (2005) 498-505
23. Kanmogne G.D., Schall K., Leibhart J., Knipe B., Gendelman H.E., and Persidsky Y. HIV-1 gp120 compromises blood-brain barrier integrity and enhances monocyte migration across blood-brain barrier: implication for viral neuropathogenesis. J. Cereb. Blood Flow Metab. 27 1 (2007) 123-134
24. Kim Y.C., Bang D., Lee S., and Lee K.H. The effect of herpesvirus infection on the expression of cell adhesion molecules on cultured human dermal microvascular endothelial cells. J. Dermatol. Sci. 24 1 (2000) 38-47
25. Lanciotti R.S., Ebel G.D., Deubel V., Kerst A.J., Murri S., Meyer R., Bowen M., McKinney N., Morrill W.E., Crabtree M.B., Kramer L.D., and Roehrig J.T. Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 298 1 (2002) 96-105
26. Lathey J.L., Wiley C.A., Verity M.A., and Nelson J.A. Cultured human brain capillary endothelial cells are permissive for infection by human cytomegalovirus. Virology 176 1 (1990) 266-273
27. Liu N.Q., Lossinsky A.S., Popik W., Li X., Gujuluva C., Kriederman B., Roberts J., Pushkarsky T., Bukrinsky M., Witte M., Weinand M., and Fiala M. Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway. J. Virol. 76 13 (2002) 6689-6700
28. Lopes H., Redig P., Glaser A., Armien A., and Wunschmann A. Clinical findings, lesions, and viral antigen distribution in great gray owls (Strix nebulosa) and barred owls (Strix varia) with spontaneous West Nile virus infection. Avian Dis. 51 1 (2007) 140-145
29. Luabeya M.K., Dallasta L.M., Achim C.L., Pauza C.D., and Hamilton R.L. Blood-brain barrier disruption in simian immunodeficiency virus encephalitis. Neuropathol. Appl. Neurobiol. 26 5 (2000) 454-462
30. Maclean A.G., Rasmussen T.A., Bieniemy D.N., Alvarez X., and Lackner A.A. SIV-induced activation of the blood-brain barrier requires cell-associated virus and is not restricted to endothelial cell activation. J. Med. Primatol. 33 5-6 (2004) 236-242
31. Mahajan S.D., Aalinkeel R., Sykes D.E., Reynolds J.L., Bindukumar B., Adal A., Qi M., Toh J., Xu G., Prasad P.N., and Schwartz S.A. Methamphetamine alters blood brain barrier permeability via the modulation of tight junction expression: implication for HIV-1 neuropathogenesis in the context of drug abuse. Brain Res. 1203 (2008) 133-148
32. Morrey J.D., Olsen A.L., Siddharthan V., Motter N.E., Wang H., Taro B.S., Chen D., Ruffner D., and Hall J.O. Increased blood-brain barrier permeability is not a primary determinant for lethality of West Nile virus infection in rodents. J. Gen. Virol. 89 Pt 2 (2008) 467-473
33. Mukhtar M., and Pomerantz R.J. Development of an in vitro blood-brain barrier model to study molecular neuropathogenesis and neurovirologic disorders induced by human immunodeficiency virus type 1 infection. J. Hum. Virol. 3 6 (2000) 324-334
34. Muller W.A. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24 6 (2003) 327-334
35. Murray K., Baraniuk S., Resnick M., Arafat R., Kilborn C., Cain K., Shallenberger R., York T.L., Martinez D., Hellums J.S., Hellums D., Malkoff M., Elgawley N., McNeely W., Khuwaja S.A., and Tesh R.B. Risk factors for encephalitis and death from West Nile virus infection. Epidemiol. Infect. 134 6 (2006) 1325-1332
36. 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. Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J. Immunol. 156 3 (1996) 1284-1295
37. Persidsky Y., Stins M., Way D., Witte M.H., Weinand M., Kim K.S., Bock P., Gendelman H.E., and Fiala M. A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. J. Immunol. 158 7 (1997) 3499-3510
38. Persidsky Y., Ramirez S.H., Haorah J., and Kanmogne G.D. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J. Neuroimmune Pharmacol. 1 3 (2006) 223-236
39. Petri B., and Bixel M.G. Molecular events during leukocyte diapedesis. FEBS J. 273 19 (2006) 4399-4407
40. Pu H., Tian J., Andras I.E., Hayashi K., Flora G., Hennig B., and Toborek M. HIV-1 Tat protein-induced alterations of ZO-1 expression are mediated by redox-regulated ERK 1/2 activation. J. Cereb. Blood Flow Metab. 25 10 (2005) 1325-1335
41. Rios M., Zhang M.J., Grinev A., Srinivasan K., Daniel S., Wood O., Hewlett I.K., and Dayton A.I. Monocytes-macrophages are a potential target in human infection with West Nile virus through blood transfusion. Transfusion 46 4 (2006) 659-667
42. Rudd P.A., Cattaneo R., and von Messling V. Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J. Virol. 80 19 (2006) 9361-9370
43. Samuel M.A., and Diamond M.S. Pathogenesis of West Nile Virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J. Virol. 80 19 (2006) 9349-9360
44. Seigneur M., Constans J., Blann A., Renard M., Pellegrin J.L., Amiral J., Boisseau M., and Conri C. Soluble adhesion molecules and endothelial cell damage in HIV infected patients. Thromb. Haemost. 77 4 (1997) 646-649
45. Shen J., SS T.T., Schrieber L., and King N.J. Early E-selectin, VCAM-1, ICAM-1, and late major histocompatibility complex antigen induction on human endothelial cells by flavivirus and comodulation of adhesion molecule expression by immune cytokines. J. Virol. 71 12 (1997) 9323-9332
46. Shrestha B., Gottlieb D., and Diamond M.S. Infection and injury of neurons by West Nile encephalitis virus. J. Virol. 77 24 (2003) 13203-13213
47. Sitati E., McCandless E.E., Klein R.S., and Diamond M.S. CD40-CD40 ligand interactions promote trafficking of CD8+ T cells into the brain and protection against West Nile virus encephalitis. J. Virol. 81 18 (2007) 9801-9811
48. Strelow L.I., Watry D.D., Fox H.S., and Nelson J.A. Efficient infection of brain microvascular endothelial cells by an in vivo-selected neuroinvasive SIVmac variant. J. Neurovirol. 4 3 (1998) 269-280
49. Verma S., Ziegler K., Ananthula P., Co J.K., Frisque R.J., Yanagihara R., and Nerurkar V.R. JC virus induces altered patterns of cellular gene expression: interferon-inducible genes as major transcriptional targets. Virology 345 2 (2006) 457-467
50. Verma S., Molina Y., Lo Y.Y., Cropp B., Nakano C., Yanagihara R., and Nerurkar V.R. In vitro effects of selenium deficiency on West Nile virus replication and cytopathogenicity. Virol. J. 5 (2008) 66
51. Wang T., Town T., Alexopoulou L., Anderson J.F., Fikrig E., and Flavell R.A. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 10 12 (2004) 1366-1373
52. Wang P., Dai J., Bai F., Kong K.F., Wong S.J., Montgomery R.R., Madri J.A., and Fikrig E. Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J. Virol. 82 18 (2008) 8978-8985
53. Williams M.R., Kataoka N., Sakurai Y., Powers C.M., Eskin S.G., and McIntire L.V. Gene expression of endothelial cells due to interleukin-1 beta stimulation and neutrophil transmigration. Endothelium 15 1 (2008) 73-165
54. Wolf K., Tsakiris D.A., Weber R., Erb P., and Battegay M. Antiretroviral therapy reduces markers of endothelial and coagulation activation in patients infected with human immunodeficiency virus type 1. J. Infect. Dis. 185 4 (2002) 456-462
55. Wunschmann A., Shivers J., Bender J., Carroll L., Fuller S., Saggese M., van Wettere A., and Redig P. Pathologic findings in red-tailed hawks (Buteo jamaicensis) and Cooper's hawks (Accipiter cooper) naturally infected with West Nile virus. Avian Dis. 48 3 (2004) 570-580