Immune response to respiratory syncytial virus infection (Orthopneumovirus)

Cover Page

Cite item

Abstract

Respiratory syncytial virus (RSV) infects children as well as elderly and immunocompromised subjects. In 2016, RSV was renamed to Orthopneumovirus owing to virus taxonomy latinization and was also included into the Pneumoviridae family. However, in this review we will use the old and more common RSV name. RSV infection may occur throughout human lifetime as it does not induce sterilizing immunity. During RSV infection, diverse immune cells such as dendritic cells, macrophages, T cells, B cells and eosinophils are involved in the antiviral response. Some of them play an important role in eliminating RSV, while the others can provoke tissue damage. An interaction between these cells occurs through the induced cytokines and chemokines, some of which emerge at early disease stages, whereas the others — at later stages. In addition, the mentioned cells can affect the course of both primary and secondary RSV infection. A prolonged or persistent RSV infection is observed in children with T-cell immunodeficiency, emphasizing the importance of T cells in resolution of acute infection as well as for virus-specific immunological memory development. Almost all the adults and children bear RSV-specific antibodies, but that doesn't protect against the repeated infection. It was shown that high mucosal rather than serum IgG level correlated better with reduced RSV load. A growing body of RSV vaccine candidates has emerged: live-attenuated, protein-based, whole-inactivated, particle-based, subunit antigens, and nucleic acid-based vaccines. While developing vaccines, there should be taken into consideration features of anti-RSV immune response as well as age of subjects to be vaccinated. In particular, to avoid vaccine-associated aggravation of RSV infection it is justified to use live attenuated vaccines in children, whereas middle-aged and the elderly subjects might be applied with subunit vaccines. Currently, no licensed vaccine for RSV infection is available. In this review, we will detail an interaction of the RSV with diverse immune cells as well as our contemporary understanding regarding preventive vaccines in RSV infection.

About the authors

A. A. Nikonova

Mechnikov Research Institute for Vaccines and Sera

Author for correspondence.
Email: aa.nikonova@nrcii.ru
ORCID iD: 0000-0001-9610-0935

Alexandra A. Nikonova - PhD (Biology), Head of the Laboratory of Molecular Biotechnology, I.I. Mechnikov Scientific Research Institute of Vaccines and Sera.

115088, Moscow, 1 st Dubrovskaya str., 15.

Phone: +7 (495) 674-08-43

Russian Federation

I. Y. Isakov

Mechnikov Research Institute for Vaccines and Sera

Email: darkdgr@yandex.ru
ORCID iD: 0000-0002-5742-6550

Junior Researcher, I.I. Mechnikov Scientific Research Institute of Vaccines and Sera.

115088, Moscow, 1 st Dubrovskaya str., 15.

Russian Federation

V. V. Zverev

Mechnikov Research Institute for Vaccines and Sera

Email: vitalyzverev@outlook.com
ORCID iD: 0000-0002-0017-1892

RAS Full Member, PhD, MD (Biology), Professor, Scientific Director, I.I. Mechnikov Scientific Research Institute of Vaccines and Sera.

115088, Moscow, 1 st Dubrovskaya str., 15.

Russian Federation

References

  1. Agoti C.N., Otieno J.R., Munywoki P.K., Mwihuri A.G., Cane P.A., Nokes D.J., Kellam P., Cotten M. Local evolutionary patterns of human respiratory syncytial virus derived from whole-genome sequencing. J. Virol., 2015, vol. 89, no. 7, pp. 3444—3454. doi: 10.3181/00379727-92-22538
  2. Ampuero S., Luchsinger V., Tapia L., Palomino M.A., Larranaga C.E. SP-A1, SP-A2 and SP-D gene polymorphisms in severe acute respiratory syncytial infection in Chilean infants. Infect. Genet. Evol., 2011, vol. 11, no. 6, pp. 1368—1377. doi: 10.1016/j.meegid.2011.04.033
  3. Bardoel B.W., Kenny E.F., Sollberger G., Zychlinsky A. The balancing act of neutrophils. Cell Host Microbe, 2014, vol. 15, no. 5, pp. 526-536. doi: 10.1016/j.chom.2014.04.011
  4. Bartz H., Buning-Pfaue F., Turkel O., Schauer U. Respiratory syncytial virus induces prostaglandin E2, IL-10 and IL-11 generation in antigen presenting cells. Clin. Exp. Immunol., 2002, vol. 129, no. 3, pp. 438-445. doi: 10.1046/j.1365-2249.2002.01927.x
  5. Bartz H., Turkel O., Hoffjan S., Rothoeft T., Gonschorek A., Schauer U. Respiratory syncytial virus decreases the capacity of myeloid dendritic cells to induce interferon-gamma in naive T cells. Immunology, 2003, vol. 109, no. 1, pp. 49-57. doi: 10.1046/j.1365-2567.2003.01629.x
  6. Blount R.E. Jr., Morris J.A., Savage R.E. Recovery of cytopathogenic agent from chimpanzees with coryza. Proc. Soc. Exp. Biol. Med., 1956, vol. 92, no. 3, pp. 544-549. doi: 10.3181/00379727-92-22538
  7. Borchers A.T., Chang C., Gershwin M.E., Gershwin L.J. Respiratory syncytial virus — a comprehensive review. Clin. Rev. Allergy Immunol., 2013, vol. 45, no. 3, pp. 331-379. doi: 10.1007/s12016-013-8368-9
  8. Bystrom J., Al-Adhoubi N., Al-Bogami M., Jawad A.S., Mageed R.A. Th17 lymphocytes in respiratory syncytial virus infection. Viruses, 2013, vol. 5, no. 3, pp. 777-791. doi: 10.3390/v5030777
  9. Cortjens B., de Boer O.J., de Jong R., Antonis A.F., Sabogal Pineros Y.S., Lutter R., van Woensel J.B., Bem R.A. Neutrophil extracellular traps cause airway obstruction during respiratory syncytial virus disease. J. Pathol., 2016, vol. 238, no. 3, pp. 401-411. doi: 10.1002/path.4660
  10. Currie S.M., Gwyer Findlay E., McFarlane A.J., Fitch P.M., Bottcher B., Colegrave N., Paras A., Jozwik A., Chiu C., Schwarze J., Davidson D.J. Cathelicidins have direct antiviral activity against respiratory syncytial virus in vitro and protective function in vivo in mice and humans. J. Immunol., 2016, vol. 196, no. 6, pp. 2699-2710. doi: 10.4049/jimmunol.1502478
  11. Currier M.G., Lee S., Stobart C.C., Hotard A.L., Villenave R., Meng J., Pretto C.D., Shields M.D., Nguyen M.T., Todd S.O., Chi M.H., Hammonds J., Krumm S.A., Spearman P., Plemper R.K., Sakamoto K., Peebles R.S. Jr., Power U.F., Moore M.L. EGFR interacts with the fusion protein of respiratory syncytial virus strain 2—20 and mediates infection and mucin expression. PLoS Pathog., 2016, vol. 12, no. 5: e1005622. doi: 10.1371/journal.ppat.1005622
  12. Day N.D., Branigan P.J., Liu C., Gutshall L.L., Luo J., Melero J.A., Sarisky R.T., Del Vecchio A.M. Contribution of cysteine residues in the extracellular domain of the F protein of human respiratory syncytial virus to its function. Virol J., 2006, vol. 3: 34. doi: 10.1186/1743-422X-3-34
  13. Detalle L., Stohr T., Palomo C., Piedra P.A., Gilbert B.E., Mas V., Millar A., Power U.F., Stortelers C., Allosery K., Melero J.A., Depla E. Generation and characterization of ALX-0171, a potent novel therapeutic nanobody for the treatment of respiratory syncytial virus infection. Antimicrob. Agents Chemother., 2016, vol. 60, no. 1, pp. 6-13. doi: 10.1128/AAC.01802-15
  14. Dodd J., Riffault S., Kodituwakku J.S., Hayday A.C., Openshaw P.J. Pulmonary V gamma 4+ gamma delta T cells have pro-inflammatory and antiviral effects in viral lung disease. J. Immunol., 2009, vol. 182, no. 2, pp. 1174-1181. doi: 10.4049/jimmunol.182.2.1174
  15. Durbin R.K., Kotenko S.V., Durbin J.E. Interferon induction and function at the mucosal surface. Immunol. Rev., 2013, vol. 255, no. 1, pp. 25-39. doi: 10.1111/imr.12101
  16. Faber T.E., Groen H., Welfing M., Jansen K.J., Bont L.J. Specific increase in local IL-17 production during recovery from primary RSV bronchiolitis. J. Med. Virol., 2012, vol. 84, no. 7, pp. 1084-1088. doi: 10.1002/jmv.23291
  17. Falsey A.R., Hennessey P.A., Formica M.A., Cox C., Walsh E.E. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med., 2005, vol. 352, no. 17, pp. 1749-1759. doi: 10.1056/NEJMoa043951
  18. Falsey A.R., Singh H.K., Walsh E.E. Serum antibody decay in adults following natural respiratory syncytial virus infection. J. Med. Virol., 2006, vol. 78, no. 11, pp. 1493-1497. doi: 10.1002/jmv.20724
  19. Frost E.L., Kersh A.E., Evavold B.D., Lukacher A.E. Cutting edge: resident memory CD8 T cells express high-affinity TCRs. J. Immunol., 2015, vol. 195, no. 8, pp. 3520-3524. doi: 10.4049/jimmunol.1501521
  20. Fulton R.B., Meyerholz D.K., Varga S.M. Foxp3+ CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol., 2010, vol. 185, no. 4, pp. 2382-2392. doi: 10.4049/jimmunol.1000423
  21. Garofalo R.P., Patti J., Hintz K.A., Hill V., Ogra P.L., Welliver R.C. Macrophage inflammatory protein-1alpha (not T helper type 2 cytokines) is associated with severe forms of respiratory syncytial virus bronchiolitis. J. Infect. Dis., 2001, vol. 184, no. 4, pp. 393-399. doi: 10.1086/322788
  22. Geerdink R.J., Pillay J., Meyaard L., Bont L. Neutrophils in respiratory syncytial virus infection: a target for asthma prevention. J. Allergy Clin. Immunol., 2015, vol. 136, no. 4, pp. 838-847. doi: 10.1016/j.jaci.2015.06.034
  23. Gill M.A., Long K., Kwon T., Muniz L., Mejias A., Connolly J., Roy L., Banchereau J., Ramilo O. Differential recruitment of dendritic cells and monocytes to respiratory mucosal sites in children with influenza virus or respiratory syncytial virus infection. J. Infect. Dis., 2008, vol. 198, no. 11, pp. 1667-1676. doi: 10.1086/593018
  24. Gimferrer L., Andres C., Campins M., Codina M.G., Rodrigo J.A., Melendo S., Martin M.C., Fuentes F., Saiz M.R., Esperalba J., Bruguera A., Vilca L.M., Armadans L., Pumarola T., Anton A. Circulation of a novel human respiratory syncytial virus group B genotype during the 2014—2015 season in Catalonia (Spain). Clin. Microbiol. Infect., 2016, vol. 22, no. 1, pp. 97. e5-97.e8. doi: 10.1016/j.cmi.2015.09.013
  25. Goritzka M., Makris S., Kausar F., Durant L.R., Pereira C., Kumagai Y., Culley F.J., Mack M., Akira S., Johansson C. Alveolar macrophage-derived type I interferons orchestrate innate immunity to RSV through recruitment of antiviral monocytes. J. Exp. Med., 2015, vol. 212, no. 5, pp. 699-714. doi: 10.1084/jem.20140825
  26. Griffiths C., Drews S.J., Marchant D.J. Respiratory syncytial virus: infection, detection, and new options for prevention and treatment. Clin. Microbiol. Rev., 2017, vol. 30, no. 1, pp. 277-319. doi: 10.1128/cmr.00010-16
  27. Groppo R., DiNapoli J., Il Jeong K., Kishko M., Jackson N., Kleanthous H., Delagrave S., Zhang L., Parrington M. Effect of genetic background and delivery route on the preclinical properties of a live attenuated RSV vaccine. PLoS One, 2018, vol. 13, no. 6: e0199452. doi: 10.1371/journal.pone.0199452
  28. Habibi M.S., Jozwik A., Makris S., Dunning J., Paras A., DeVincenzo J.P., de Haan C.A., Wrammert J., Openshaw P.J., Chiu C. Impaired antibody-mediated protection and defective IgA B-cell memory in experimental infection of adults with respiratory syncytial virus. Am. J. Respir. Crit. Care Med., 2015, vol. 191, no. 9, pp. 1040-1049. doi: 10.1164/rccm.201412-2256OC
  29. Halfhide C.P., Flanagan B.F., Brearey S.P., Hunt J.A., Fonceca A.M., McNamara P.S., Howarth D., Edwards S., Smyth R.L. Respiratory syncytial virus binds and undergoes transcription in neutrophils from the blood and airways of infants with severe bronchiolitis. J. Infect. Dis., 2011, vol. 204, no. 3, pp. 451-458. doi: 10.1093/infdis/jir280
  30. Hall C.B. The burgeoning burden of respiratory syncytial virus among children. Infect. Disord. Drug Targets, 2012, vol. 12, no. 2, pp. 92-97. doi: 10.2174/187152612800100099
  31. Harker J.A., Godlee A., Wahlsten J.L., Lee D.C., Thorne L.G., Sawant D., Tregoning J.S., Caspi R.R., Bukreyev A., Collins P.L., Openshaw P.J. Interleukin 18 coexpression during respiratory syncytial virus infection results in enhanced disease mediated by natural killer cells. J. Virol., 2010, vol. 84, no. 8, pp. 4073-4082. doi: 10.1128/JVI.02014-09
  32. Heidema J., Lukens M.V., van Maren W.W., van Dijk M.E., Otten H.G., van Vught A.J., van der Werff D.B., van Gestel S.J., Semple M.G., Smyth R.L., Kimpen J.L., van Bleek G.M. CD8+ T cell responses in bronchoalveolar lavage fluid and peripheral blood mononuclear cells of infants with severe primary respiratory syncytial virus infections. J. Immunol., 2007, vol. 179, no. 12, pp. 8410-8417. doi: 10.4049/jimmunol.179.12.8410
  33. Higgins D., Trujillo C., Keech C. Advances in RSV vaccine research and development — a global agenda. Vaccine, 2016, vol. 34, no. 26, pp. 2870-2875. doi: 10.1016/j.vaccine.2016.03.109
  34. Hussell T., Bell T.J. Alveolar macrophages: plasticity in a tissue-specific context. Nat. Rev. Immunol., 2014, vol. 14, no. 2, pp. 8193. doi: 10.1038/nri3600
  35. Hussell T., Openshaw P.J. IL-12-activated NK cells reduce lung eosinophilia to the attachment protein of respiratory syncytial virus but do not enhance the severity of illness in CD8 T cell-immunodeficient conditions. J. Immunol., 2000, vol. 165, no. 12, pp. 7109-7115. doi: 10.4049/jimmunol.165.12.7109
  36. Johnson S.M., McNally B.A., Ioannidis I., Flano E., Teng M.N., Oomens A.G., Walsh E.E., Peeples M.E. Respiratory syncytial virus uses CX3CR1 as a receptor on primary human airway epithelial cultures. PLoS Pathog., 2015, vol. 11, no. 12: e1005318. doi: 10.1371/journal.ppat.1005318
  37. Jozwik A., Habibi M.S., Paras A., Zhu J., Guvenel A., Dhariwal J., Almond M., Wong E.H.C., Sykes A., Maybeno M., Del Rosario J., Trujillo-Torralbo M.B., Mallia P., Sidney J., Peters B., Kon O.M., Sette A., Johnston S.L., Openshaw P.J., Chiu C. RSV-specific airway resident memory CD8+ T cells and differential disease severity after experimental human infection. Nat. Commun., 2015, vol. 6: 10224. doi: 10.1038/ncomms10224
  38. Karron R.A., Buchholz U.J., Collins P.L. Live-attenuated respiratory syncytial virus vaccines. Curr. Top. Microbiol. Immunol., 2013, vol. 372, pp. 259-284. doi: 10.1007/978-3-642-38919-1_13
  39. Karron R.A., Luongo C., Thumar B., Loehr K.M., Englund J.A., Collins P.L., Buchholz U.J. A gene deletion that up-regulates viral gene expression yields an attenuated RSV vaccine with improved antibody responses in children. Sci. Transl. Med., 2015, vol. 7, no. 312: 312ra175. doi: 10.1126/scitranslmed.aac8463
  40. Kawasaki Y., Hosoya M., Kanno H., Suzuki H. Serum regulated upon activation, normal T cell expressed and presumably secreted concentrations and eosinophils in respiratory syncytial virus infection. Pediatr. Int., 2006, vol. 48, no. 3, pp. 257-260. doi: 10.1111/j.1442-200X.2006.02199.x
  41. Kerr M.H., Paton J.Y. Surfactant protein levels in severe respiratory syncytial virus infection. Am. J. Respir. Crit. Care Med., 1999, vol. 159, no. 4, pt. 1, pp. 1115-1118. doi: 10.1164/ajrccm.159.4.9709065
  42. Kerrin A., Fitch P., Errington C., Kerr D., Waxman L., Riding K., McCormack J., Mehendele F., McSorley H., MacKenzie K., Wronski S., Braun A., Levin R., Theilen U., Schwarze J. Differential lower airway dendritic cell patterns may reveal distinct endotypes of RSV bronchiolitis. Thorax, 2017, vol. 72, no. 7, pp. 620-627. doi: 10.1136/thoraxjnl-2015-207358
  43. Killikelly A.M., Kanekiyo M., Graham B.S. Pre-fusion F is absent on the surface of formalin-inactivated respiratory syncytial virus. Sci. Rep., 2016, vol. 6: 34108. doi: 10.1038/srep34108
  44. Kim H.H., Lee M.H., Lee J.S. Eosinophil cationic protein and chemokines in nasopharyngeal secretions of infants with respiratory syncytial virus (RSV) bronchiolitis and non-RSV bronchiolitis. J. Korean Med. Sci., 2007, vol. 22, no. 1, pp. 37—42. doi: 10.3346/jkms.2007.22.1.37
  45. Kim T.H., Lee H.K. Innate immune recognition of respiratory syncytial virus infection. BMB Rep., 2014, vol. 47, no. 4, pp. 184— 191. doi: 10.5483/bmbrep.2014.47.4.050
  46. Kinnear E., Lambert L., McDonald J.U., Cheeseman H.M., Caproni L.J., Tregoning J.S. Airway T cells protect against RSV infection in the absence of antibody. Mucosal Immunol., 2018, vol. 11, no. 1: 290. doi: 0.1038/mi.2017.79
  47. Krug R.M. Functions of the influenza A virus NS1 protein in antiviral defense. Curr. Opin. Virol., 2015, vol. 12, pp. 1—6. doi: 10.1016/j.coviro.2015.01.007
  48. Larranaga C.L., Ampuero S.L., Luchsinger V.F., Carrion F.A., Aguilar N.V., Morales P.R., Palomino M.A., Tapia L.F., Avendano L.F. Impaired immune response in severe human lower tract respiratory infection by respiratory syncytial virus. Pediatr. Infect. Dis. J., 2009, vol. 28, no. 10, pp. 867—873. doi: 10.1086/512615
  49. Legg J.P., Hussain I.R., Warner J.A., Johnston S.L., Warner J.O. Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am. J. Respir. Crit. Care Med., 2003, vol. 168, no. 6, pp. 633—639. doi: 10.1164/rccm.200210-1148OC
  50. LeVine A.M., Gwozdz J., Stark J., Bruno M., Whitsett J., Korfhagen T. Surfactant protein-A enhances respiratory syncytial virus clearance in vivo. J. Clin. Invest, 1999, vol. 103, no. 7, pp. 1015—1021. doi: 10.1172/JCI5849
  51. Li F., Zhu H., Sun R., Wei H., Tian Z. Natural killer cells are involved in acute lung immune injury caused by respiratory syncytial virus infection. J. Virol., 2012, vol. 86, no. 4, pp. 2251—2258. doi: 10.1128/JVI.06209-11
  52. Lindemans C.A., Kimpen J.L., Luijk B., Heidema J., Kanters D., van der Ent C.K., Koenderman L. Systemic eosinophil response induced by respiratory syncytial virus. Clin. Exp. Immunol., 2006, vol. 144, no. 3, pp. 409—417. doi: 10.1111/j.1365-2249.2006.03084.x
  53. Loebbermann J., Durant L., Thornton H., Johansson C., Openshaw P.J. Defective immunoregulation in RSV vaccine-augmented viral lung disease restored by selective chemoattraction of regulatory T cells. Proc. Natl. Acad. Sci. USA, 2013, vol. 110, no. 8, pp. 2987-2992. doi: 10.1073/pnas.1217580110
  54. Magro M., Mas V., Chappell K., Vazquez M., Cano O., Luque D., Terron M.C., Melero J.A., Palomo C. Neutralizing antibodies against the preactive form of respiratory syncytial virus fusion protein offer unique possibilities for clinical intervention. Proc. Natl Acad. Sci. USA, 2012, vol. 109, no. 8, pp. 3089-3094. doi: 10.1073/pnas.1115941109
  55. Marr N., Turvey S.E., Grandvaux N. Pathogen recognition receptor crosstalk in respiratory syncytial virus sensing: a host and cell type perspective. Trends Microbiol., 2013, vol. 21, no. 11, pp. 568- 574. doi: 10.1016/j.tim.2013.08.006
  56. McGill A., Greensill J., Marsh R., Craft A.W., Toms G.L. Detection of human respiratory syncytial virus genotype specific antibody responses in infants. J. Med. Virol., 2004, vol. 74, no. 3, pp. 492-498. doi: 10.1002/jmv.20203
  57. 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. Respiratory syncytial virus infection of airway epithelial cells, in vivo and in vitro, supports pulmonary antibody responses by inducing expression of the B cell differentiation factor BAFF. Thorax, 2013, vol. 68, no. 1, pp. 76- 81. doi: 10.1136/tho-raxjnl-2012-202288
  58. Mejias A., Dimo B., Suarez N.M., Garcia C., Suarez-Arrabal M.C., Jartti T., Blankenship D., Jordan-Villegas A., Ardura M.I., Xu Z., Banchereau J., Chaussabel D., Ramilo O. Whole blood gene expression profiles to assess pathogenesis and disease severity in infants with respiratory syncytial virus infection. PLoS Med., 2013, vol. 10, no. 11: e1001549. doi: 10.1371/journal.pmed.1001549
  59. Midulla F., Villani A., Panuska J.R., Dab I., Kolls J.K., Merolla R., Ronchetti R. Respiratory syncytial virus lung infection in infants: immunoregulatory role of infected alveolar macrophages. J. Infect. Dis., 1993, vol. 168, no. 6, pp. 1515-1519. doi: 10.1093/infdis/168.6.1515
  60. Moffett H.F., Harms C.K., Fitzpatrick K.S., Tooley M.R., Boonyaratanakornkit J., Taylor J.J. B cells engineered to express pathogen-specific antibodies protect against infection. Sci. Immunol., 2019, vol. 4, no. 35: eaax0644. doi: 10.1126/sciimmunol.aax0644
  61. Mohr E., Siegrist C.A. Vaccination in early life: standing up to the challenges. Curr. Opin. Immunol., 2016, vol. 41, pp. 1-8. doi: 10.1016/j.coi.2016.04.004
  62. Mueller S.N., Mackay L.K. Tissue-resident memory T cells: local specialists in immune defence. Nat. Rev. Immunol., 2016, vol. 16, no. 2, pp. 79-89. doi: 10.1038/nri.2015.3
  63. Mufson M.A., Orvell C., Rafnar B., Norrby E. Two distinct subtypes of human respiratory syncytial virus. J. Gen. Virol., 1985, vol. 66 (pt. 10), pp. 2111-2124. doi: 10.1099/0022-1317-66-10-2111
  64. Mukherjee S., Lindell D.M., Berlin A.A., Morris S.B., Shanley T.P., Hershenson M.B., Lukacs N.W. IL-17-induced pulmonary pathogenesis during respiratory viral infection and exacerbation of allergic disease. Am. J. Pathol., 2011, vol. 179, no. 1, pp. 248258. doi: 10.1016/j.ajpath.2011.03.003
  65. Munoz F.M., Piedra P.A., Glezen W.P. Safety and immunogenicity of respiratory syncytial virus purified fusion protein-2 vaccine in pregnant women. Vaccine, 2003, vol. 21, no. 24, pp. 3465-3467. doi: 10.1016/s0264-410x(03)00352-9
  66. Openshaw P.J., Chiu C. Protective and dysregulated T cell immunity in RSV infection. Curr. Opin. Virol., 2013, vol. 3, no. 4, pp. 468-474. doi: 10.1016/j.coviro.2013.05.005
  67. Openshaw P.J.M., Chiu C., Culley F.J., Johansson C. Protective and harmful immunity to RSV infection. Annu. Rev. Immunol., 2017, vol. 35, pp. 501-532. doi: 10.1146/annurev-immunol-051116-052206
  68. Owczarczyk A.B., Schaller M.A., Reed M., Rasky A.J., Lombard D.B., Lukacs N.W. Sirtuin 1 regulates dendritic cell activation and autophagy during respiratory syncytial virus-induced immune responses. J. Immunol., 2015, vol. 195, no. 4, pp. 1637-1646. doi: 10.4049/jimmunol.1500326
  69. Panuska J.R., Hertz M.I., Taraf H., Villani A., Cirino N.M. Respiratory syncytial virus infection of alveolar macrophages in adult transplant patients. Am. Rev. Respir. Dis., 1992, vol. 145, no. 4, pt. 1, pp. 934- 939. doi: 10.1164/ajrccm/145.4_Pt_1.934
  70. Pastey M.K., Crowe J.E. Jr., Graham B.S. RhoA interacts with the fusion glycoprotein of respiratory syncytial virus and facilitates virus-induced syncytium formation. J. Virol., 1999, vol. 73, no. 9, pp. 7262- 7270. doi: 10.1128/JVI.73.9.7262-7270.1999
  71. Pennings J.L.A., Mariman R., Hodemaekers H.M., Reemers S.S.N., Janssen R., Guichelaar T. Transcriptomics in lung tissue upon respiratory syncytial virus infection reveals aging as important modulator of immune activation and matrix maintenance. Sci. Rep., 2018, vol. 8, no. 1: 16653. doi: 10.1038/s41598-018-35180-2
  72. Ptaschinski C., Mukherjee S., Moore M.L., Albert M., Helin K., Kunkel S.L., Lukacs N.W. RSV-induced H3K4 demethylase KDM5B leads to regulation of dendritic cell-derived innate cytokines and exacerbates pathogenesis in vivo. PLoS Pathog., 2015, vol. 11, no. 6: e1004978. doi: 10.1371/journal.ppat.1004978
  73. Roe M.F., Bloxham D.M., White D.K., Ross-Russell R.I., Tasker R.T., O'Donnell D.R. Lymphocyte apoptosis in acute respiratory syncytial virus bronchiolitis. Clin. Exp. Immunol., 2004, vol. 137, no. 1, pp. 139—145. doi: 10.1111/j.1365-2249.2004.02512.x
  74. Rosenberg H.F., Dyer K.D., Domachowske J.B. Respiratory viruses and eosinophils: exploring the connections. Antiviral Res., 2009, vol. 83, no. 1, pp. 1—9. doi: 10.1016/j.antiviral.2009.04.005
  75. Russell C.D., Unger S.A., Walton M., Schwarze J. The human immune response to respiratory syncytial virus infection. Clin. Microbiol. Rev, 2017, vol. 30, no. 2, pp. 481-502. doi: 10.1128/CMR.00090-16
  76. Russell C.J., Simoes E.A.F., Hurwitz J.L. Vaccines for the paramyxoviruses and pneumoviruses: successes, candidates, and hurdles. Viral Immunol., 2018, vol. 31, no. 2, pp. 133-141. doi: 10.1089/vim.2017.0137
  77. Sande C.J., Mutunga M.N., Medley G.F., Cane P.A., Nokes D.J. Group- and genotype-specific neutralizing antibody responses against respiratory syncytial virus in infants and young children with severe pneumonia. J. Infect. Dis., 2013, vol. 207, no. 3, pp. 489-492. doi: 10.1093/infdis/jis700
  78. Schenkel J.M., Fraser K.A., Beura L.K., Pauken K.E., Vezys V., Masopust D. T cell memory. Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science, 2014, vol. 346, no. 6205, pp. 98-101. doi: 10.1126/science.1254536
  79. Schmidt M.E., Knudson C.J., Hartwig S.M., Pewe L.L., Meyerholz D.K., Langlois R.A., Harty J.T., Varga S.M. Memory CD8 T cells mediate severe immunopathology following respiratory syncytial virus infection. PLoS Pathog., 2018, vol. 14, no. 1: e1006810. doi: 10.1371/journal.ppat.1006810
  80. Schobel S.A., Stucker K.M., Moore M.L., Anderson L.J., Larkin E.K., Shankar J., Bera J., Puri V., Shilts M.H., Rosas-Salazar C., Halpin R.A., Fedorova N., Shrivastava S., Stockwell T.B., Peebles R.S., Hartert T.V., Das S.R. Respiratory syncytial virus wholegenome sequencing identifies convergent evolution of sequence duplication in the C-terminus of the G gene. Sci. Rep., 2016, vol. 6: 26311. doi: 10.1038/srep26311
  81. Sharma A., Wendland R., Sung B., Wu W., Grunwald T., Worgall S. Maternal immunization with chimpanzee adenovirus expressing RSV fusion protein protects against neonatal RSV pulmonary infection. Vaccine, 2014, vol. 32, no. 43, pp. 5761-5768. doi: 10.1016/j.vaccine.2014.08.049
  82. Shi T., McAllister D.A., O'Brien K.L., Simoes E.A.F., Madhi S.A., Gessner B.D., Polack F.P., Balsells E., Acacio S., Aguayo C., Alassani I., Ali A., Antonio M., Awasthi S., Awori J.O., Azziz-Baumgartner E., Baggett H.C., Baillie V.L., Balmaseda A., Barahona A., Basnet S., Bassat Q., Basualdo W., Bigogo G., Bont L., Breiman R.F., Brooks W.A., Broor S., Bruce N., Bruden D., Buchy P., Campbell S., Carosone-Link P., Chadha M., Chipeta J., Chou M., Clara W., Cohen C., de Cuellar E., Dang D.A., Dash-Yandag B., Deloria-Knoll M., Dherani M., Eap T., Ebruke B.E., Echavarria M., de Freitas Lazaro Emediato C.C., Fasce R.A., Feikin D.R., Feng L., Gentile A., Gordon A., Goswami D., Goyet S., Groome M., Halasa N., Hirve S., Homaira N., Howie S.R.C., Jara J., Jroundi I., Kartasasmita C.B., Khuri-Bulos N., Kotloff K.L., Krishnan A., Libster R., Lopez O., Lucero M.G., Lucion F., Lupisan S.P., Marcone D.N., McCracken J.P., Mejia M., Moisi J.C., Montgomery J.M., Moore D.P., Moraleda C., Moyes J., Munywoki P., Mutyara K., Nicol M.P., Nokes D.J., Nymadawa P., da Costa Oliveira M.T., Oshitani H., Pandey N., Paranhos-Baccala G., Phillips L.N., Picot V.S., Rahman M., Rakoto-Andrianarivelo M., Rasmussen Z.A., Rath B.A., Robinson A., Romero C., Russomando G., Salimi V., Sawatwong P., Scheltema N., Schweiger B., Scott J.A.G., Seidenberg P., Shen K., Singleton R., Sotomayor V., Strand T.A., Sutanto A., Sylla M., Tapia M.D., Thamthitiwat S., Thomas E.D., Tokarz R., Turner C., Venter M., Waicharoen S., Wang J., Watthanaworawit W., Yoshida L.M., Yu H., Zar H.J., Campbell H., Nair H., Network R.S.V.G.E. Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in young children in 2015: a systematic review and modelling study. Lancet, 2017, vol. 390, no. 10098, pp. 946-958. doi: 10.1016/S0140-6736(17)30938-8
  83. Shinoff J.J., O'Brien K.L., Thumar B., Shaw J.B., Reid R., Hua W., Santosham M., Karron R.A. Young infants can develop protective levels of neutralizing antibody after infection with respiratory syncytial virus. J. Infect. Dis., 2008, vol. 198, no. 7, pp. 10071015. doi: 10.1086/591460
  84. Shirey K.A., Pletneva L.M., Puche A.C., Keegan A.D., Prince G.A., Blanco J.C., Vogel S.N. Control of RSV-induced lung injury by alternatively activated macrophages is IL-4R alpha-, TLR4-, and IFN-beta-dependent. Mucosal. Immunol., 2010, vol. 3, no. 3, pp. 291-300. doi: 10.1038/mi.2010.6
  85. Smith D.B., Bukh J., Kuiken C., Muerhoff A.S., Rice C.M., Stapleton J.T., Simmonds P. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource. Hepatology, 2014, vol. 59, no. 1, pp. 318-327. doi: 10.1002/hep.26744
  86. Smyth R.L., Mobbs K.J., O'Hea U., Ashby D., Hart C.A. Respiratory syncytial virus bronchiolitis: disease severity, interleukin-8, and virus genotype. Pediatr. Pulmonol., 2002, vol. 33, no. 5, pp. 339-346. doi: 10.1002/ppul.10080
  87. Spann K.M., Tran K.C., Chi B., Rabin R.L., Collins P.L. Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J. Virol., 2004, vol. 78, no. 8, pp. 4363-4369. doi: 10.1128/jvi.78.8.4363-4369.2004
  88. Stokes K.L., Currier M.G., Sakamoto K., Lee S., Collins P.L., Plemper R.K., Moore M.L. The respiratory syncytial virus fusion protein and neutrophils mediate the airway mucin response to pathogenic respiratory syncytial virus infection. J. Virol., 2013, vol. 87, no. 18, pp. 10070-10082. doi: 10.1128/JVI.01347-13
  89. Sun Y., Jain D., Koziol-White C.J., Genoyer E., Gilbert M., Tapia K., Panettieri R.A. Jr., Hodinka R.L., Lopez C.B. Immunostimulatory defective viral genomes from respiratory syncytial virus promote a strong innate antiviral response during infection in mice and humans. PLoS Pathog., 2015, vol. 11, no. 9: e1005122. doi: 10.1371/journal.ppat.1005122
  90. Teijaro J.R. Type I interferons in viral control and immune regulation. Curr. Opin. Virol., 2016, vol. 16, pp. 31-40. doi: 10.1016/j.coviro.2016.01.001
  91. Turi K.N., Shankar J., Anderson L.J., Rajan D., Gaston K., Gebretsadik T., Das S.R., Stone C., Larkin E.K., Rosas-Salazar C., Brunwasser S.M., Moore M.L., Peebles R.S. Jr., Hartert T.V. Infant viral respiratory infection nasal immune-response patterns and their association with subsequent childhood recurrent wheeze. Am. J. Respir. Crit. Care Med., 2018, vol. 198, no. 8, pp. 10641073. doi: 10.1164/rccm.201711-2348OC
  92. Turner T.L., Kopp B.T., Paul G., Landgrave L.C., Hayes D. Jr., Thompson R. Respiratory syncytial virus: current and emerging treatment options. Clinicoecon. Outcomes Res., 2014, vol. 6, pp. 217-225. doi: 10.2147/CEOR.S60710
  93. Villenave R., Broadbent L., Douglas I., Lyons J.D., Coyle P.V., Teng M.N., Tripp R.A., Heaney L.G., Shields M.D., Power U.F. Induction and antagonism of antiviral responses in respiratory syncytial virus-infected pediatric airway epithelium. J. Virol., 2015, vol. 89, no. 24, pp. 12309-12318. doi: 10.1128/JVI.02119-15
  94. Vissers M., Ahout I.M., de Jonge M.I., Ferwerda G. Mucosal IgG levels correlate better with respiratory syncytial virus load and inflammation than plasma IgG levels. Clin. Vaccine Immunol., 2015, vol. 23, no. 3, pp. 243-245. doi: 10.1128/CVI.00590-15
  95. Wang S.Z., Rosenberger C.L., Bao Y.X., Stark J.M., Harrod K.S. Clara cell secretory protein modulates lung inflammatory and immune responses to respiratory syncytial virus infection. J. Immunol., 2003, vol. 171, no. 2, pp. 1051- 1060. doi: 10.4049/jimmunol.171.2.1051
  96. Welliver T.P., Garofalo R.P., Hosakote Y., Hintz K.H., Avendano L., Sanchez K., Velozo L., Jafri H., Chavez-Bueno S., Ogra P.L., McKinney L., Reed J.L., Welliver R.C. Sr. Severe human lower respiratory tract illness caused by respiratory syncytial virus and influenza virus is characterized by the absence of pulmonary cytotoxic lymphocyte responses. J. Infect. Dis., 2007, vol. 195, no. 8, pp. 1126-1136. doi: 10.1097/INF.0b013e3181a3ea71
  97. Widjaja I., Wicht O., Luytjes W., Leenhouts K., Rottier P.J.M., van Kuppeveld F.J.M., Haijema B.J., de Haan C.A.M. Characterization of epitope-specific anti-respiratory syncytial virus (Anti-RSV) antibody responses after natural infection and after vaccination with formalin-inactivated RSV. J. Virol., 2016, vol. 90, no. 13, pp. 5965-5977. doi: 10.1128/JVI.00235-16
  98. Wright P.F., Ikizler M.R., Gonzales R.A., Carroll K.N., Johnson J.E., Werkhaven J.A. Growth of respiratory syncytial virus in primary epithelial cells from the human respiratory tract. J. Virol., 2005, vol. 79, no. 13, pp. 8651- 8654. doi: 10.1128/JVI.79.13.8651-8654.2005
  99. Yao S., Jiang L., Moser E.K., Jewett L.B., Wright J., Du J., Zhou B., Davis S.D., Krupp N.L., Braciale T.J., Sun J. Control of pathogenic effector T-cell activities in situ by PD-L1 expression on respiratory inflammatory dendritic cells during respiratory syncytial virus infection. Mucosal Immunol., 2015, vol. 8, no. 4, pp. 746- 759. doi: 10.1038/mi.2014.106
  100. Yin H.S., Wen X., Paterson R.G., Lamb R.A., Jardetzky T.S. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature, 2006, vol. 439, no. 7072, pp. 38- 44. doi: 10.1038/nature04322
  101. Zanin M., Baviskar P., Webster R., Webby R. The interaction between respiratory pathogens and mucus. Cell. Host Microbe, 2016, vol. 19, no. 2, pp. 159-168. doi: 10.1016/j.chom.2016.01.001

Supplementary files

There are no supplementary files to display.


Copyright (c) 2020 Nikonova A.A., Isakov I.Y., Zverev V.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies