2,631
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Differential effects of Usutu and West Nile viruses on neuroinflammation, immune cell recruitment and blood–brain barrier integrity

, ORCID Icon, , , , , , ORCID Icon, ORCID Icon & ORCID Icon show all
Article: 2156815 | Received 18 Aug 2022, Accepted 05 Dec 2022, Published online: 02 Jan 2023

References

  • Schwerk C, Tenenbaum T, Kim KS, et al. The choroid plexus – a multi-role player during infectious diseases of the CNS. Front Cell Neurosci. 2015;9:1–11.
  • Mustafá YM, Meuren LM, Coelho SVA, et al. Pathways exploited by flaviviruses to counteract the blood-brain barrier and invade the central nervous system. Front Microbiol. 2019;10:525.
  • Kadry H, Noorani B, Cucullo L. A blood–brain barrier overview on structure, function, impairment, and biomarkers of integrity. Fluids Barriers CNS. 2020;17:1–24.
  • Tohidpour A, Morgun AV, Boitsova EB, et al. Neuroinflammation and infection: molecular mechanisms associated with dysfunction of neurovascular unit. Front Cell Infect Microbiol. 2017;7:276.
  • Schaeffer S, Iadecola C. Revisiting the neurovascular unit. Nat Neurosci. 2021;24:1198–1209.
  • Clé M, Eldin P, Briant L, et al. Neurocognitive impacts of arbovirus infections. J Neuroinflammation. 2020;17:1–14.
  • Hsieh JT, St John AL. Japanese encephalitis virus and its mechanisms of neuroinvasion. PLoS Pathog. 2020;16:1–6.
  • Weaver SC, Charlier C, Vasilakis N, et al. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu Rev Med. 2018;69:395–408.
  • Debiasi RL. West Nile virus neuroinvasive disease. Curr Infect Dis Rep. 2011;13:350–359.
  • Simonin Y, Sillam O, Carles MJ, et al. Human usutu virus infection with atypical neurologic presentation, Montpellier, France, 2016. Emerg Infect Dis. 2018;24:875–878.
  • Zou SS, Zou QC, Xiong WJ, et al. Brain microvascular endothelial cell-derived HMGB1 facilitates monocyte adhesion and transmigration to promote JEV neuroinvasion. Front Cell Infect Microbiol. 2021;11:1–13.
  • Clé M, Desmetz C, Barthelemy J, et al. Zika virus infection promotes local inflammation, cell adhesion molecule upregulation, and leukocyte recruitment at the blood-brain barrier. In: Diamond MS, editor. MBio. Baltimore: ASM; 2020;11:e01183-20.
  • Michalicová A, Bhide K, Bhide M, et al. How viruses infiltrate the central nervous system. Acta Virol. 2017;61:393–400.
  • Constant O, Maarifi G, Blanchet FP, et al. Role of dendritic cells in viral brain infections. Front Immunol. 2022;13:1–15.
  • Marchetti L, Engelhardt B. Immune cell trafficking across the blood-brain barrier in the absence and presence of neuroinflammation. Vasc Biol. 2020;2:H1–H18.
  • Tiong V, Shu MH, Wong WF, et al. Nipah virus infection of immature dendritic cells increases its transendothelial migration across human brain microvascular endothelial cells. Front Microbiol. 2018;9:1–12.
  • Nagy A, Mezei E, Nagy O, et al. Extraordinary increase in West Nile virus cases and first confirmed human Usutu virus infection in Hungary, 2018. Eurosurveillance. 2019;24:1–9.
  • Pfeffer M, Dobler G. Emergence of zoonotic arboviruses by animal trade and migration. Parasit Vectors. 2010;3:35.
  • Vilibic-Cavlek T, Savic V, Petrovic T, et al. Emerging trends in the epidemiology of West Nile and usutu virus infections in Southern Europe. Front Vet Sci. 2019;6:437.
  • Constant O, Gil P, Barthelemy J, et al. One health surveillance of West Nile and Usutu viruses: a repeated cross-sectional study exploring seroprevalence and endemicity in Southern France, 2016 to 2020. Eurosurveillance. 2022;(25):2200068.
  • Clé M, Constant O, Barthelemy J, et al. Differential neurovirulence of Usutu virus lineages in mice and neuronal cells. J Neuroinflammation. 2021;18:11.
  • Soung A, Klein RS. Viral encephalitis and neurologic diseases: focus on astrocytes. Trends Mol Med. 2018;24:950–962.
  • Miner JJ, Daniels BP, Shrestha B, et al. The TAM receptor Mertk protects against neuroinvasive viral infection by maintaining blood-brain barrier integrity. Nat Med. 2015;21:1464–1472.
  • Roe K, Orillo B, Verma S. West Nile virus-induced cell adhesion molecules on human brain microvascular endothelial cells regulate leukocyte adhesion and modulate permeability of the in vitro blood-brain barrier model. PLoS One. 2014;9:1–12.
  • Roe K, Kumar M, Lum S, et al. West Nile virus-induced disruption of the blood-brain barrier in mice is characterized by the degradation of the junctional complex proteins and increase in multiple matrix metalloproteinases. J Gen Virol. 2012;93:1193–1203.
  • Verma S, Lo Y, Chapagain M, et al. 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. 2009;385:425–433.
  • Daniels BP, Holman DW, Cruz-Orengo L, et al. Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals. In: Griffin DE, editor. MBio. Baltimore: ASM; 2014;5:e01476-14.
  • Pan Y, Cai W, Cheng A, et al. Flaviviruses: innate immunity, inflammasome activation, inflammatory cell death, and cytokines. Front Immunol. 2022;13:1–15.
  • Martin MF, Maarifi G, Abiven H, et al. Usutu virus escapes langerin-induced restriction to productively infect human Langerhans cells, unlike West Nile virus. Emerg Microbes Infect. 2022;11:761–774.
  • Kärber G. Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol. 1931;162:480–483.
  • Cecchelli R, Aday S, Sevin E, et al. A stable and reproducible human blood-brain barrier model derived from hematopoietic stem cells. PLoS One. (San-Francisco) 2014;9:e99733.
  • Heymans M, Figueiredo R, Dehouck L, et al. Contribution of brain pericytes in blood-brain barrier formation and maintenance: a transcriptomic study of cocultured human endothelial cells derived from hematopoietic stem cells. Fluids Barriers CNS. 2020;17:1–28.
  • Candela P, Saint-Pol J, Kuntz M, et al. In vitro discrimination of the role of LRP1 at the BBB cellular level: focus on brain capillary endothelial cells and brain pericytes. Brain Res. 2015;1594:15–26.
  • Lyck R, Lécuyer MA, Abadier M, et al. ALCAM (CD166) is involved in extravasation of monocytes rather than T cells across the blood–brain barrier. J Cereb Blood Flow Metab. 2017;37:2894–2909.
  • Clé M, Beck C, Salinas S, et al. Usutu virus: a new threat? Epidemiol Infect. 2019;147:e232.
  • Martin M-F, Simonin Y. West Nile virus historical progression in Europe. Virologie. 2019;23:265–270.
  • Rochfort KD, Cummins PM. Cytokine-mediated dysregulation of zonula occludens-1 properties in human brain microvascular endothelium. Microvasc Res. 2015;100:48–53.
  • Hartsock A, Nelson WJ. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta - Biomembr. 2008;1778:660–669.
  • Benzarti E, Sarlet M, Franssen M, et al. New insights into the susceptibility of immunocompetent mice to Usutu virus. Viruses. 2020;12:189.
  • De Laere M, Berneman ZN, Cools N. To the brain and back: migratory paths of dendritic cells in multiple sclerosis. J Neuropathol Exp Neurol. 2018;77:178–192.
  • Mencattelli G, Ndione MHD, Rosà R, et al. Epidemiology of west Nile virus in Africa: An underestimated threat. In: Fuehrer H-P, editor. PLos negl trop Dis. San-Francisco: PLOS; 2022;16:e0010075.
  • Zannoli S, Sambri V. West Nile virus and usutu virus co-circulation in Europe: epidemiology and implications. Microorganisms. 2019;7:1–13.
  • Cernuda-Morollón E, Ridley AJ. Rho GTPases and leukocyte adhesion receptor expression and function in endothelial cells. Circ Res. 2006;98:757–767.
  • Martin M-F, Nisole S. West Nile virus restriction in mosquito and human cells: a virus under confinement. Vaccines. 2020;8:256.
  • Erickson MA, Banks WA. Neuroimmune axes of the blood-brain barriers and blood-brain interfaces: bases for physiological regulation, disease states, and pharmacological interventions. Pharmacol Rev. 2018;70:278–314.
  • Wang T, Town T, Alexopoulou L, et al. Toll-like receptor 3 mediates west Nile virus entry into the brain causing lethal encephalitis. Nat Med. 2004;10:1366–1373.
  • Bardina SV, Michlmayr D, Hoffman KW, et al. Differential roles of chemokines CCL2 and CCL7 in monocytosis and leukocyte migration during west Nile virus infection. J Immunol. 2015;195:4306–4318.
  • Bardina SV, Brown JA, Michlmayr D, et al. Chemokine receptor Ccr7 restricts fatal west Nile virus encephalitis. In: Jung JU, editor. J virol. Baltimore: American Society for Microbiology; 2017;91:1–14.
  • Yewdell JW, Brooke CB. Monocytes, viruses and metaphors: hanging the Trojan horse. Cell Cycle. 2012;11:1748–1749.
  • Lim JK, Obara CJ, Rivollier A, et al. Chemokine receptor Ccr2 is critical for monocyte accumulation and survival in west Nile virus encephalitis. J Immunol. 2011;186:471–478.
  • Ifergan I, Kébir H, Bernard M, et al. The blood-brain barrier induces differentiation of migrating monocytes into Th17-polarizing dendritic cells. Brain. 2008;131:785–799.
  • Puerta-Guardo H, Glasner DR, Espinosa DA, et al. Flavivirus NS1 triggers tissue-specific vascular endothelial dysfunction reflecting disease tropism. Cell Rep. 2019;26:1598–1613.e8.
  • Liu Y, Tang XP, McArthur JC, et al. Analysis of human immunodeficiency virus type 1 gp160 sequences from a patient with HIV dementia: evidence for monocyte trafficking into brain. J Neurovirol. 2000;6(Suppl 1):S70–S81.
  • Ludewig P, Gallizioli M, Urra X, et al. Dendritic cells in brain diseases. Biochim Biophys Acta - Mol Basis Dis. 2016;1862:352–367.
  • Zozulya AL, Reinke E, Baiu DC, et al. Dendritic cell transmigration through brain microvessel endothelium is regulated by MIP-1α chemokine and matrix metalloproteinases. J Immunol. 2007;178:520–529.
  • Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2:361–367.
  • Ogasawara N, Kojima T, Go M, et al. Induction of JAM-A during differentiation of human THP-1 dendritic cells. Biochem Biophys Res Commun. 2009;389:543–549.
  • Cusi MG, Gandolfo C, Terrosi C, et al. Toscana virus infects dendritic and endothelial cells opening the way for the central nervous system. J Neurovirol. 2016;22:307–315.