1887

Journal of General Virology header logo

Volume 96, Issue 9

CX3CR1 is an important surface molecule for respiratory syncytial virus infection in human airway epithelial cells Free

Abstract

Respiratory syncytial virus (RSV) is a major cause of severe pneumonia and bronchiolitis in infants and young children, and causes disease throughout life. Understanding the biology of infection, including virus binding to the cell surface, should help develop antiviral drugs or vaccines. The RSV F and G glycoproteins bind cell surface heparin sulfate proteoglycans (HSPGs) through heparin-binding domains. The G protein also has a CX3C chemokine motif which binds to the fractalkine receptor CX3CR1. G protein binding to CX3CR1 is not important for infection of immortalized cell lines, but reportedly is so for primary human airway epithelial cells (HAECs), the primary site for human infection. We studied the role of CX3CR1 in RSV infection with CX3CR1-transfected cell lines and HAECs with variable percentages of CX3CR1-expressing cells, and the effect of anti-CX3CR1 antibodies or a mutation in the RSV CX3C motif. Immortalized cells lacking HSPGs had low RSV binding and infection, which was increased markedly by CX3CR1 transfection. CX3CR1 was expressed primarily on ciliated cells, and ∼50 % of RSV-infected cells in HAECs were CX3CR1. HAECs with more CX3CR1-expressing cells had a proportional increase in RSV infection. Blocking G binding to CX3CR1 with anti-CX3CR1 antibody or a mutation in the CX3C motif significantly decreased RSV infection in HAECs. The kinetics of cytokine production suggested that the RSV/CX3CR1 interaction induced RANTES (regulated on activation normal T-cell expressed and secreted protein), IL-8 and fractalkine production, whilst it downregulated IL-15, IL1-RA and monocyte chemotactic protein-1. Thus, the RSV G protein/CX3CR1 interaction is likely important in infection and infection-induced responses of the airway epithelium, the primary site of human infection.

  • Received:
  • Accepted:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.000218
2015-09-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/9/2543.html?itemId=/content/journal/jgv/10.1099/vir.0.000218&mimeType=html&fmt=ahah

References

  1. Anderson L.J., Hierholzer J.C., Bingham P.G., Stone Y.O. 1985; Microneutralization test for respiratory syncytial virus based on an enzyme immunoassay. J Clin Microbiol 22:1050–1052[PubMed]
     [Google Scholar]
  2. Aoyama T., Inokuchi S., Brenner D.A., Seki E. 2010; CX3CL1-CX3CR1 interaction prevents carbon tetrachloride-induced liver inflammation and fibrosis in mice. Hepatology 52:1390–1400 [CrossRef]
     [Google Scholar]
  3. Bar-On L., Birnberg T., Lewis K.L., Edelson B.T., Bruder D., Hildner K., Buer J., Murphy K.M., Reizis B., Jung S. 2010; CX3CR1+ CD8alpha+ dendritic cells are a steady-state population related to plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 107:14745–14750 [CrossRef]
     [Google Scholar]
  4. Bermejo-Martin J.F., Garcia-Arevalo M.C., De Lejarazu R.O., Ardura J., Eiros J.M., Alonso A., Matías V., Pino M., Bernardo D., other authors. 2007; Predominance of Th2 cytokines, CXC chemokines and innate immunity mediators at the mucosal level during severe respiratory syncytial virus infection in children. Eur Cytokine Netw 18:162–167[PubMed]
     [Google Scholar]
  5. Bernfield M., Götte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. 1999; Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729–777 [CrossRef]
     [Google Scholar]
  6. Blatt E.N., Yan X.H., Wuerffel M.K., Hamilos D.L., Brody S.L. 1999; Forkhead transcription factor HFH-4 expression is temporally related to ciliogenesis. Am J Respir Cell Mol Biol 21:168–176 [CrossRef]
     [Google Scholar]
  7. Chandrasekar B., Mummidi S., Perla R.P., Bysani S., Dulin N.O., Liu F., Melby P.C. 2003; Fractalkine (CX3CL1) stimulated by nuclear factor kappaB (NF-kappaB)-dependent inflammatory signals induces aortic smooth muscle cell proliferation through an autocrine pathway. Biochem J 373:547–558 [CrossRef]
     [Google Scholar]
  8. Chen J., Kinter M., Shank S., Cotton C., Kelley T.J., Ziady A.G. 2008; Dysfunction of Nrf-2 in CF epithelia leads to excess intracellular H2O2 and inflammatory cytokine production. PLoS One 3:e3367 [CrossRef]
     [Google Scholar]
  9. Chen P., Abacherli L.E., Nadler S.T., Wang Y., Li Q., Parks W.C. 2009; MMP7 shedding of syndecan-1 facilitates re-epithelialization by affecting alpha2beta1 integrin activation. PLoS One 4:e6565 [CrossRef]
     [Google Scholar]
  10. Chirkova T., Boyoglu-Barnum S., Gaston K.A., Malik F.M., Trau S.P., Oomens A.G., Anderson L.J. 2013; Respiratory syncytial virus G protein CX3C motif impairs human airway epithelial and immune cell responses. J Virol 87:13466–13479 [CrossRef]
     [Google Scholar]
  11. Combadiere C., Gao J., Tiffany H.L., Murphy P.M. 1998a; Gene cloning, RNA distribution, and functional expression of mCX3CR1, a mouse chemotactic receptor for the CX3C chemokine fractalkine. Biochem Biophys Res Commun 253:728–732 [CrossRef]
     [Google Scholar]
  12. Combadiere C., Salzwedel K., Smith E.D., Tiffany H.L., Berger E.A., Murphy P.M. 1998b; Identification of CX3CR1.A chemotactic receptor for the human CX3C chemokine fractalkine and a fusion coreceptor for HIV-1. J Biol Chem 273:23799–23804 [CrossRef]
     [Google Scholar]
  13. Drobni P., Mistry N., McMillan N., Evander M. 2003; Carboxy-fluorescein diacetate, succinimidyl ester labeled papillomavirus virus-like particles fluoresce after internalization and interact with heparan sulfate for binding and entry. Virology 310:163–172 [CrossRef]
     [Google Scholar]
  14. Duan D., Yue Y., Yan Z., McCray P.B. Jr, Engelhardt J.F. 1998; Polarity influences the efficiency of recombinant adenoassociated virus infection in differentiated airway epithelia. Hum Gene Ther 9:2761–2776 [CrossRef]
     [Google Scholar]
  15. Falsey A.R., Hennessey P.A., Formica M.A., Cox C., Walsh E.E. 2005; Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352:1749–1759 [CrossRef]
     [Google Scholar]
  16. Feldman S.A., Hendry R.M., Beeler J.A. 1999; Identification of a linear heparin binding domain for human respiratory syncytial virus attachment glycoprotein G. J Virol 73:6610–6617[PubMed]
     [Google Scholar]
  17. Feldman S.A., Audet S., Beeler J.A. 2000; The fusion glycoprotein of human respiratory syncytial virus facilitates virus attachment and infectivity via an interaction with cellular heparan sulfate. J Virol 74:6442–6447 [CrossRef]
     [Google Scholar]
  18. Feldman S.A., Crim R.L., Audet S.A., Beeler J.A. 2001; Human respiratory syncytial virus surface glycoproteins F, G and SH form an oligomeric complex. Arch Virol 146:2369–2383 [CrossRef]
     [Google Scholar]
  19. Fonceca A.M., Flanagan B.F., Trinick R., Smyth R.L., McNamara P.S. 2012; Primary airway epithelial cultures from children are highly permissive to respiratory syncytial virus infection. Thorax 67:42–48 [CrossRef]
     [Google Scholar]
  20. Hall C.B., Weinberg G.A., Iwane M.K., Blumkin A.K., Edwards K.M., Staat M.A., Auinger P., Griffin M.R., Poehling K.A., other authors. 2009; The burden of respiratory syncytial virus infection in young children. N Engl J Med 360:588–598 [CrossRef]
     [Google Scholar]
  21. Hallak L.K., Spillmann D., Collins P.L., Peeples M.E. 2000; Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J Virol 74:10508–10513 [CrossRef]
     [Google Scholar]
  22. Harcourt J., Alvarez R., Jones L.P., Henderson C., Anderson L.J., Tripp R.A. 2006; Respiratory syncytial virus G protein and G protein CX3C motif adversely affect CX3CR1+T cell responses. J Immunol 176:1600–1608 [CrossRef]
     [Google Scholar]
  23. Harrison J.K., Jiang Y., Chen S., Xia Y., Maciejewski D., McNamara R.K., Streit W.J., Salafranca M.N., Adhikari S., other authors. 1998; Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A 95:10896–10901 [CrossRef]
     [Google Scholar]
  24. Hasegawa M., Sato S., Echigo T., Hamaguchi Y., Yasui M., Takehara K. 2005; Up regulated expression of fractalkine/CX3CL1 and CX3CR1 in patients with systemic sclerosis. Ann Rheum Dis 64:21–28 [CrossRef]
     [Google Scholar]
  25. Hayashida A., Bartlett A.H., Foster T.J., Park P.W. 2009; Staphylococcus aureus beta-toxin induces lung injury through syndecan-1. Am J Pathol 174:509–518 [CrossRef]
     [Google Scholar]
  26. Haynes L.M., Jones L.P., Barskey A., Anderson L.J., Tripp R.A. 2003; Enhanced disease and pulmonary eosinophilia associated with formalin-inactivated respiratory syncytial virus vaccination are linked to G glycoprotein CX3C-CX3CR1 interaction and expression of substance P. J Virol 77:9831–9844 [CrossRef]
     [Google Scholar]
  27. Heminway B.R., Yu Y., Tanaka Y., Perrine K.G., Gustafson E., Bernstein J.M., Galinski M.S. 1994; Analysis of respiratory syncytial virus F, G, and SH proteins in cell fusion. Virology 200:801–805 [CrossRef]
     [Google Scholar]
  28. Imai T., Hieshima K., Haskell C., Baba M., Nagira M., Nishimura M., Kakizaki M., Takagi S., Nomiyama H., other authors. 1997; Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell 91:521–530 [CrossRef]
     [Google Scholar]
  29. Ioannidis I., McNally B., Willette M., Peeples M.E., Chaussabel D., Durbin J.E., Ramilo O., Mejias A., Flaño E. 2012; Plasticity and virus specificity of the airway epithelial cell immune response during respiratory virus infection. J Virol 86:5422–5436 [CrossRef]
     [Google Scholar]
  30. Jamieson W.L., Shimizu S., D'Ambrosio J.A., Meucci O., Fatatis A. 2008; CX3CR1 is expressed by prostate epithelial cells and androgens regulate the levels of CX3CL1/fractalkine in the bone marrow: potential role in prostate cancer bone tropism. Cancer Res 68:1715–1722 [CrossRef]
     [Google Scholar]
  31. Jensen-Smith H.C., Ludueña R.F., Hallworth R. 2003; Requirement for the betaI and betaIV tubulin isotypes in mammalian cilia. Cell Motil Cytoskeleton 55:213–220 [CrossRef]
     [Google Scholar]
  32. Johnson S.M., McNally B.A., Ioannidis I., Flano E., Oomens A.G., Partida-Sanchez S., Peeples M.E. 2013; Identification of CX3CR1 as a cellular receptor for respiratory syncytial virus on primary well-differentiated human airway epithelial cultures. In American Society for Virology 32nd Annual Meeting . University Park, PA
    [Google Scholar]
  33. Johnson T.R., McLellan J.S., Graham B.S. 2012; Respiratory syncytial virus glycoprotein G interacts with DC-SIGN and L-SIGN to activate ERK1 and ERK2. J Virol 86:1339–1347 [CrossRef]
     [Google Scholar]
  34. Johnston I.N., Milligan E.D., Wieseler-Frank J., Frank M.G., Zapata V., Campisi J., Langer S., Martin D., Green P., other authors. 2004; A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci 24:7353–7365 [CrossRef]
     [Google Scholar]
  35. Karron R.A., Buonagurio D.A., Georgiu A.F., Whitehead S.S., Adamus J.E., Clements-Mann M.L., Harris D.O., Randolph V.B., Udem S.A., other authors. 1997; Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc Natl Acad Sci U S A 94:13961–13966 [CrossRef]
     [Google Scholar]
  36. Keswani S.G., Balaji S., Le L., Leung A., Katz A.B., Lim F.Y., Habli M., Jones H.N., Wilson J.M., Crombleholme T.M. 2012; Pseudotyped AAV vector-mediated gene transfer in a human fetal trachea xenograft model: implications for in utero gene therapy for cystic fibrosis. PLoS One 7:e43633 [CrossRef]
     [Google Scholar]
  37. Kim K.W., Vallon-Eberhard A., Zigmond E., Farache J., Shezen E., Shakhar G., Ludwig A., Lira S.A., Jung S. 2011; In vivo structure/function and expression analysis of the CX3C chemokine fractalkine. Blood 118:e156–e167 [CrossRef]
     [Google Scholar]
  38. Li Q., Park P.W., Wilson C.L., Parks W.C. 2002; Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111:635–646 [CrossRef]
     [Google Scholar]
  39. Martínez I., Melero J.A. 2000; Binding of human respiratory syncytial virus to cells: implication of sulfated cell surface proteoglycans. J Gen Virol 81:2715–2722[PubMed] [CrossRef]
     [Google Scholar]
  40. McComb J.G., Ranganathan M., Liu X.H., Pilewski J.M., Ray P., Watkins S.C., Choi A.M., Lee J.S. 2008; CX3CL1 up-regulation is associated with recruitment of CX3CR1+ mononuclear phagocytes and T lymphocytes in the lungs during cigarette smoke-induced emphysema. Am J Pathol 173:949–961 [CrossRef]
     [Google Scholar]
  41. McNamara P.S., Fonceca A.M., Howarth D., Correia J.B., Slupsky J.R., Trinick R.E., Al Turaiki W., Smyth R.L., Flanagan B.F. 2013; Respiratory syncytial virus infection of airway epithelial cells, in vivo in vitro, supports pulmonary antibody responses by inducing expression of the B cell differentiation factor BAFF. Thorax 68:76–81 [CrossRef]
     [Google Scholar]
  42. Million K., Larcher J., Laoukili J., Bourguignon D., Marano F., Tournier F. 1999; Polyglutamylation and polyglycylation of alpha- and beta-tubulins during in vitro ciliated cell differentiation of human respiratory epithelial cells. J Cell Sci 112:4357–4366[PubMed]
     [Google Scholar]
  43. Mitra R., Baviskar P., Duncan-Decocq R.R., Patel D., Oomens A.G. 2012; The human respiratory syncytial virus matrix protein is required for maturation of viral filaments. J Virol 86:4432–4443 [CrossRef]
     [Google Scholar]
  44. Nair H., Nokes D.J., Gessner B.D., Dherani M., Madhi S.A., Singleton R.J., O'Brien K.L., Roca A., Wright P.F., other authors. 2010; Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375:1545–1555 [CrossRef]
     [Google Scholar]
  45. Nishimura M., Umehara H., Nakayama T., Yoneda O., Hieshima K., Kakizaki M., Dohmae N., Yoshie O., Imai T. 2002; Dual functions of fractalkine/CX3C ligand 1 in trafficking of perforin+/granzyme B+ cytotoxic effector lymphocytes that are defined by CX3CR1 expression. J Immunol 168:6173–6180 [CrossRef]
     [Google Scholar]
  46. Olszewska-Pazdrak B., Casola A., Saito T., Alam R., Crowe S.E., Mei F., Ogra P.L., Garofalo R.P. 1998; Cell-specific expression of RANTES, MCP-1, and MIP-1alpha by lower airway epithelial cells and eosinophils infected with respiratory syncytial virus. J Virol 72:4756–4764[PubMed]
     [Google Scholar]
  47. Oshansky C.M., Barber J.P., Crabtree J., Tripp R.A. 2010; Respiratory syncytial virus F and G proteins induce interleukin 1alpha, CC, and CXC chemokine responses by normal human bronchoepithelial cells. J Infect Dis 201:1201–1207 [CrossRef]
     [Google Scholar]
  48. Park P.W., Reizes O., Bernfield M. 2000; Cell surface heparan sulfate proteoglycans: selective regulators of ligand-receptor encounters. J Biol Chem 275:29923–29926 [CrossRef]
     [Google Scholar]
  49. Park P.W., Pier G.B., Hinkes M.T., Bernfield M. 2001; Exploitation of syndecan-1 shedding by Pseudomonas aeruginosa enhances virulence. Nature 411:98–102 [CrossRef]
     [Google Scholar]
  50. Perros F., Dorfmüller P., Souza R., Durand-Gasselin I., Godot V., Capel F., Adnot S., Eddahibi S., Mazmanian M., other authors. 2007; Fractalkine-induced smooth muscle cell proliferation in pulmonary hypertension. Eur Respir J 29:937–943 [CrossRef]
     [Google Scholar]
  51. Polack F.P., Irusta P.M., Hoffman S.J., Schiatti M.P., Melendi G.A., Delgado M.F., Laham F.R., Thumar B., Hendry R.M., other authors. 2005; The cysteine-rich region of respiratory syncytial virus attachment protein inhibits innate immunity elicited by the virus and endotoxin. Proc Natl Acad Sci U S A 102:8996–9001 [CrossRef]
     [Google Scholar]
  52. Popova T.G., Millis B., Bradburne C., Nazarenko S., Bailey C., Chandhoke V., Popov S.G. 2006; Acceleration of epithelial cell syndecan-1 shedding by anthrax hemolytic virulence factors. BMC Microbiol 6:8 [CrossRef]
     [Google Scholar]
  53. Pruessmeyer J., Martin C., Hess F.M., Schwarz N., Schmidt S., Kogel T., Hoettecke N., Schmidt B., Sechi A., other authors. 2010; A disintegrin and metalloproteinase 17 (ADAM17) mediates inflammation-induced shedding of syndecan-1 and -4 by lung epithelial cells. J Biol Chem 285:555–564 [CrossRef]
     [Google Scholar]
  54. Qin L., Hu C.P., Feng J.T., Xia Q. 2011; Activation of lymphocytes induced by bronchial epithelial cells with prolonged RSV infection. PLoS One 6:e27113 [CrossRef]
     [Google Scholar]
  55. Ray R., Hoft D.F., Meyer K., Brown R., Lagging L.M., Belshe R.B. 2001; Immunoregulatory role of secreted glycoprotein G from respiratory syncytial virus. Virus Res 75:147–154 [CrossRef]
     [Google Scholar]
  56. Rimaniol A.C., Till S.J., Garcia G., Capel F., Godot V., Balabanian K., Durand-Gasselin I., Varga E.M., Simonneau G., other authors. 2003; The CX3C chemokine fractalkine in allergic asthma and rhinitis. J Allergy Clin Immunol 112:1139–1146 [CrossRef]
     [Google Scholar]
  57. Shay D.K., Holman R.C., Newman R.D., Liu L.L., Stout J.W., Anderson L.J. 1999; Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA 282:1440–1446 [CrossRef]
     [Google Scholar]
  58. Shingai M., Azuma M., Ebihara T., Sasai M., Funami K., Ayata M., Ogura H., Tsutsumi H., Matsumoto M., Seya T. 2008; Soluble G protein of respiratory syncytial virus inhibits Toll-like receptor 3/4-mediated IFN-beta induction. Int Immunol 20:1169–1180 [CrossRef]
     [Google Scholar]
  59. Sincock P.M., Mayrhofer G., Ashman L.K. 1997; Localization of the transmembrane 4 superfamily (TM4SF) member PETA-3 (CD151) in normal human tissues: comparison with CD9, CD63, and alpha5beta1 integrin. J Histochem Cytochem 45:515–525 [CrossRef]
     [Google Scholar]
  60. Song Y., Coleman L., Shi J., Beppu H., Sato K., Walsh K., Loscalzo J., Zhang Y.Y. 2008; Inflammation, endothelial injury, and persistent pulmonary hypertension in heterozygous BMPR2-mutant mice. Am J Physiol Heart Circ Physiol 295:H677–H690 [CrossRef]
     [Google Scholar]
  61. Suzuki F., Kubota T., Miyazaki Y., Ishikawa K., Ebisawa M., Hirohata S., Ogura T., Mizusawa H., Imai T., other authors. 2012; Serum level of soluble CX3CL1/fractalkine is elevated in patients with polymyositis and dermatomyositis, which is correlated with disease activity. Arthritis Res Ther 14:R48 [CrossRef]
     [Google Scholar]
  62. Tachibana K., Nakamura S., Wang H., Iwasaki H., Tachibana K., Maebara K., Cheng L., Hirabayashi J., Narimatsu H. 2006; Elucidation of binding specificity of Jacalin toward O-glycosylated peptides: quantitative analysis by frontal affinity chromatography. Glycobiology 16:46–53 [CrossRef]
     [Google Scholar]
  63. Tayyari F., Marchant D., Moraes T.J., Duan W., Mastrangelo P., Hegele R.G. 2011; Identification of nucleolin as a cellular receptor for human respiratory syncytial virus. Nat Med 17:1132–1135 [CrossRef]
     [Google Scholar]
  64. Techaarpornkul S., Collins P.L., Peeples M.E. 2002; Respiratory syncytial virus with the fusion protein as its only viral glycoprotein is less dependent on cellular glycosaminoglycans for attachment than complete virus. Virology 294:296–304 [CrossRef]
     [Google Scholar]
  65. Tripp R.A., Jones L.P., Haynes L.M., Zheng H., Murphy P.M., Anderson L.J. 2001; CX3C chemokine mimicry by respiratory syncytial virus G glycoprotein. Nat Immunol 2:732–738 [CrossRef]
     [Google Scholar]
  66. Tripp R.A., Dakhama A., Jones L.P., Barskey A., Gelfand E.W., Anderson L.J. 2003; The G glycoprotein of respiratory syncytial virus depresses respiratory rates through the CX3C motif and substance P. J Virol 77:6580–6584 [CrossRef]
     [Google Scholar]
  67. Tristram D.A., Hicks W. Jr, Hard R. 1998; Respiratory syncytial virus and human bronchial epithelium. Arch Otolaryngol Head Neck Surg 124:777–783 [CrossRef]
     [Google Scholar]
  68. Villenave R., O'Donoghue D., Thavagnanam S., Touzelet O., Skibinski G., Heaney L.G., McKaigue J.P., Coyle P.V., Shields M.D., Power U.F. 2011; Differential cytopathogenesis of respiratory syncytial virus prototypic and clinical isolates in primary pediatric bronchial epithelial cells. Virol J 8:43 [CrossRef]
     [Google Scholar]
  69. Welliver R.C., Garofalo R.P., Ogra P.L. 2002; Beta-chemokines, but neither T helper type 1 nor T helper type 2 cytokines, correlate with severity of illness during respiratory syncytial virus infection. Pediatr Infect Dis J 21:457–461 [CrossRef]
     [Google Scholar]
  70. You Y., Huang T., Richer E.J., Schmidt J.E., Zabner J., Borok Z., Brody S.L. 2004; Role of f-box factor foxj1 in differentiation of ciliated airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 286:L650–L657 [CrossRef]
     [Google Scholar]
  71. Zhang L., Peeples M.E., Boucher R.C., Collins P.L., Pickles R.J. 2002; Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J Virol 76:5654–5666 [CrossRef]
     [Google Scholar]
  72. Zhang H., Xia T., Meng H., Xue M., George S., Ji Z., Wang X., Liu R., Wang M., other authors. 2011; Differential expression of syndecan-1 mediates cationic nanoparticle toxicity in undifferentiated versus differentiated normal human bronchial epithelial cells. ACS Nano 5:2756–2769 [CrossRef]
     [Google Scholar]
  73. Zhang M., Xu G., Liu W., Ni Y., Zhou W. 2012; Role of fractalkine/CX3CR1 interaction in light-induced photoreceptor degeneration through regulating retinal microglial activation and migration. PLoS One 7:e35446 [CrossRef]
     [Google Scholar]
  74. Ziady A.G., Sokolow A., Shank S., Corey D., Myers R., Plafker S., Kelley T.J. 2012; Interaction with CREB binding protein modulates the activities of Nrf2 and NF-κB in cystic fibrosis airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 302:L1221–L1231 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.000218
Loading
CX3CR1 is an important surface molecule for respiratory syncytial virus infection in human airway epithelial cells
J. Gen. Virol. 96, 2543 (2015); https://doi.org/10.1099/vir.0.000218
/content/journal/jgv/10.1099/vir.0.000218
/content/journal/jgv/10.1099/vir.0.000218
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error