1887

Abstract

Picornaviruses are the most commonly encountered infectious agents in mankind. They typically cause mild infections of the gastrointestinal or respiratory tract, but sometimes also invade the central nervous system. There, they can cause severe diseases with long-term sequelae and even be lethal. The most infamous picornavirus is poliovirus, for which significant epidemics of poliomyelitis were reported from the end of the nineteenth century. A successful vaccination campaign has brought poliovirus close to eradication, but neurological diseases caused by other picornaviruses have increasingly been reported since the late 1990s. In this review we focus on enterovirus 71, coxsackievirus A16, enterovirus 68 and human parechovirus 3, which have recently drawn attention because of their links to severe neurological diseases. We discuss the clinical relevance of these viruses and the primary role of humoral immunity in controlling them, and summarize current knowledge on the neutralization of such viruses by antibodies.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000780
2017-06-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/6/1145.html?itemId=/content/journal/jgv/10.1099/jgv.0.000780&mimeType=html&fmt=ahah

References

  1. Adams MJ, Lefkowitz EJ, King AM, Bamford DH, Breitbart M et al. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2015). Arch Virol 2015; 160:1837–1850 [View Article][PubMed]
    [Google Scholar]
  2. Tapparel C, Siegrist F, Petty TJ, Kaiser L. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 2013; 14:282–293 [View Article][PubMed]
    [Google Scholar]
  3. Fairweather D, Stafford KA, Sung YK. Update on coxsackievirus B3 myocarditis. Curr Opin Rheumatol 2012; 24:401–407 [View Article][PubMed]
    [Google Scholar]
  4. Yeung WC, Rawlinson WD, Craig ME. Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 2011; 342:d35 [View Article][PubMed]
    [Google Scholar]
  5. Nathanson N, Kew OM. From emergence to eradication: the epidemiology of poliomyelitis deconstructed. Am J Epidemiol 2010; 172:1213–1229 [View Article][PubMed]
    [Google Scholar]
  6. Morales M, Tangermann RH, Wassilak SG. Progress toward polio eradication—worldwide, 2015–2016. MMWR Morb Mortal Wkly Rep 2016; 65:470–473 [View Article][PubMed]
    [Google Scholar]
  7. Piralla A, Mariani B, Stronati M, Marone P, Baldanti F. Human enterovirus and parechovirus infections in newborns with sepsis-like illness and neurological disorders. Early Hum Dev 2014; 90:S75–S77 [View Article][PubMed]
    [Google Scholar]
  8. Victoria JG, Kapoor A, Li L, Blinkova O, Slikas B et al. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 2009; 83:4642–4651 [View Article][PubMed]
    [Google Scholar]
  9. Boriskin YS, Rice PS, Stabler RA, Hinds J, Al-Ghusein H et al. DNA microarrays for virus detection in cases of central nervous system infection. J Clin Microbiol 2004; 42:5811–5818 [View Article][PubMed]
    [Google Scholar]
  10. Chen CS, Yao YC, Lin SC, Lee YP, Wang YF et al. Retrograde axonal transport: a major transmission route of enterovirus 71 in mice. J Virol 2007; 81:8996–9003 [View Article][PubMed]
    [Google Scholar]
  11. Harvala H, Griffiths M, Solomon T, Simmonds P. Distinct systemic and central nervous system disease patterns in enterovirus and parechovirus infected children. J Infect 2014; 69:69–74 [View Article][PubMed]
    [Google Scholar]
  12. Kim HJ, Kang B, Hwang S, Hong J, Kim K et al. Epidemics of viral meningitis caused by echovirus 6 and 30 in Korea in 2008. Virol J 2012; 9:38 [View Article][PubMed]
    [Google Scholar]
  13. Kreuter JD, Barnes A, McCarthy JE, Schwartzman JD, Oberste MS et al. A fatal central nervous system enterovirus 68 infection. Arch Pathol Lab Med 2011; 135:793–796 [View Article][PubMed]
    [Google Scholar]
  14. Ren R, Racaniello VR. Human poliovirus receptor gene expression and poliovirus tissue tropism in transgenic mice. J Virol 1992; 66:296–304[PubMed]
    [Google Scholar]
  15. Flint J, Racaniello VR, Rall GF, Skalka AM, Enquist L et al. Chapter 2: The infectious cycle. In: Principles of Virology, 4th ed. Washington, DC: ASM Press; 2015 pp. 24–52 [CrossRef]
    [Google Scholar]
  16. Evans DJ, Almond JW. Cell receptors for picornaviruses as determinants of cell tropism and pathogenesis. Trends Microbiol 1998; 6:198–202 [View Article][PubMed]
    [Google Scholar]
  17. Gromeier M, Solecki D, Patel DD, Wimmer E. Expression of the human poliovirus receptor/CD155 gene during development of the central nervous system: implications for the pathogenesis of poliomyelitis. Virology 2000; 273:248–257 [View Article][PubMed]
    [Google Scholar]
  18. Jiao XY, Guo L, Huang DY, Chang XL, Qiu QC. Distribution of EV71 receptors SCARB2 and PSGL-1 in human tissues. Virus Res 2014; 190:40–52 [View Article][PubMed]
    [Google Scholar]
  19. Wei W, Guo H, Chang J, Yu Y, Liu G et al. ICAM-5/telencephalin is a functional entry receptor for enterovirus D68. Cell Host Microbe 2016; 20:631–641 [View Article][PubMed]
    [Google Scholar]
  20. Daley JK, Gechman LA, Skipworth J, Rall GF. Poliovirus replication and spread in primary neuron cultures. Virology 2005; 340:10–20 [View Article][PubMed]
    [Google Scholar]
  21. Yoon SY, Ha YE, Choi JE, Ahn J, Lee H et al. Coxsackievirus B4 uses autophagy for replication after calpain activation in rat primary neurons. J Virol 2008; 82:11976–11978 [View Article][PubMed]
    [Google Scholar]
  22. Ida-Hosonuma M, Iwasaki T, Yoshikawa T, Nagata N, Sato Y et al. The alpha/beta interferon response controls tissue tropism and pathogenicity of poliovirus. J Virol 2005; 79:4460–4469 [View Article][PubMed]
    [Google Scholar]
  23. Ren R, Racaniello VR. Poliovirus spreads from muscle to the central nervous system by neural pathways. J Infect Dis 1992; 166:747–752 [View Article][PubMed]
    [Google Scholar]
  24. Wong KT, Munisamy B, Ong KC, Kojima H, Noriyo N et al. The distribution of inflammation and virus in human enterovirus 71 encephalomyelitis suggests possible viral spread by neural pathways. J Neuropathol Exp Neurol 2008; 67:162–169 [View Article][PubMed]
    [Google Scholar]
  25. Chai Q, He WQ, Zhou M, Lu H, Fu ZF. Enhancement of blood-brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J Virol 2014; 88:4698–4710 [View Article][PubMed]
    [Google Scholar]
  26. Daniels BP, Holman DW, Cruz-Orengo L, Jujjavarapu H, Durrant DM et al. Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals. MBio 2014; 5:e01476-14 [View Article][PubMed]
    [Google Scholar]
  27. Cheng HY, Huang YC, Yen TY, Hsia SH, Hsieh YC et al. The correlation between the presence of viremia and clinical severity in patients with enterovirus 71 infection: a multi-center cohort study. BMC Infect Dis 2014; 14:417 [View Article][PubMed]
    [Google Scholar]
  28. Yang WX, Terasaki T, Shiroki K, Ohka S, Aoki J et al. Efficient delivery of circulating poliovirus to the central nervous system independently of poliovirus receptor. Virology 1997; 229:421–428 [View Article][PubMed]
    [Google Scholar]
  29. Mizutani T, Ishizaka A, Nihei C. Transferrin receptor 1 facilitates poliovirus permeation of mouse brain capillary endothelial cells. J Biol Chem 2016; 291:2829–2836 [View Article][PubMed]
    [Google Scholar]
  30. Tabor-Godwin JM, Ruller CM, Bagalso N, An N, Pagarigan RR et al. A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS. J Neurosci 2010; 30:8676–8691 [View Article][PubMed]
    [Google Scholar]
  31. Vuorinen T, Vainionpää R, Vanharanta R, Hyypiä T. Susceptibility of human bone marrow cells and hematopoietic cell lines to coxsackievirus B3 infection. J Virol 1996; 70:9018–9023[PubMed]
    [Google Scholar]
  32. Wahid R, Cannon MJ, Chow M. Dendritic cells and macrophages are productively infected by poliovirus. J Virol 2005; 79:401–409 [View Article][PubMed]
    [Google Scholar]
  33. Irani DN. Aseptic meningitis and viral myelitis. Neurol Clin 2008; 26:635–655 [View Article][PubMed]
    [Google Scholar]
  34. Verboon-Maciolek MA, Krediet TG, Gerards LJ, de Vries LS, Groenendaal F et al. Severe neonatal parechovirus infection and similarity with enterovirus infection. Pediatr Infect Dis J 2008; 27:241–245 [View Article][PubMed]
    [Google Scholar]
  35. Nicolosi A, Hauser WA, Beghi E, Kurland LT. Epidemiology of central nervous system infections in Olmsted County, Minnesota, 1950–1981. J Infect Dis 1986; 154:399–408 [View Article][PubMed]
    [Google Scholar]
  36. Esposito S, Rahamat-Langendoen J, Ascolese B, Senatore L, Castellazzi L et al. Pediatric parechovirus infections. J Clin Virol 2014; 60:84–89 [View Article][PubMed]
    [Google Scholar]
  37. Koskiniemi M, Rantalaiho T, Piiparinen H, von Bonsdorff CH, Färkkilä M et al. Infections of the central nervous system of suspected viral origin: a collaborative study from Finland. J Neurovirol 2001; 7:400–408 [View Article][PubMed]
    [Google Scholar]
  38. Kincaid O, Lipton HL. Viral myelitis: an update. Curr Neurol Neurosci Rep 2006; 6:469–474 [View Article][PubMed]
    [Google Scholar]
  39. Schmidt NJ, Lennette EH, Ho HH. An apparently new enterovirus isolated from patients with disease of the central nervous system. J Infect Dis 1974; 129:304–309 [View Article][PubMed]
    [Google Scholar]
  40. Hagiwara A, Tagaya I, Yoneyama T. Epidemic of hand, foot and mouth disease associated with enterovirus 71 infection. Intervirology 1978; 9:60–63 [View Article][PubMed]
    [Google Scholar]
  41. Alexander JP, Baden L, Pallansch MA, Anderson LJ. Enterovirus 71 infections and neurologic disease—United States, 19771991. J Infect Dis 1994; 169:905–908 [View Article][PubMed]
    [Google Scholar]
  42. Blomberg J, Lycke E, Ahlfors K, Johnsson T, Wolontis S et al. Letter: new enterovirus type associated with epidemic of aseptic meningitis and/or hand, foot, and mouth disease. Lancet 1974; 2:112[PubMed]
    [Google Scholar]
  43. Ishimaru Y, Nakano S, Yamaoka K, Takami S. Outbreaks of hand, foot, and mouth disease by enterovirus 71. High incidence of complication disorders of central nervous system. Arch Dis Child 1980; 55:583–588 [View Article][PubMed]
    [Google Scholar]
  44. Kennett ML, Birch CJ, Lewis FA, Yung AP, Locarnini SA et al. Enterovirus type 71 infection in Melbourne. Bull World Health Organ 1974; 51:609–615[PubMed]
    [Google Scholar]
  45. Chumakov M, Voroshilova M, Shindarov L, Lavrova I, Gracheva L et al. Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol 1979; 60:329–340 [View Article][PubMed]
    [Google Scholar]
  46. Nagy G, Takátsy S, Kukán E, Mihály I, Dömök I. Virological diagnosis of enterovirus type 71 infections: experiences gained during an epidemic of acute CNS diseases in Hungary in 1978. Arch Virol 1982; 71:217–227 [View Article][PubMed]
    [Google Scholar]
  47. Shindarov LM, Chumakov MP, Voroshilova MK, Bojinov S, Vasilenko SM et al. Epidemiological, clinical, and pathomorphological characteristics of epidemic poliomyelitis-like disease caused by enterovirus 71. J Hyg Epidemiol Microbiol Immunol 1979; 23:284–295[PubMed]
    [Google Scholar]
  48. Chan LG, Parashar UD, Lye MS, Ong FG, Zaki SR et al. Deaths of children during an outbreak of hand, foot, and mouth disease in Sarawak, Malaysia: clinical and pathological characteristics of the disease. Clin Infect Dis 2000; 31:678–683 [View Article][PubMed]
    [Google Scholar]
  49. Huang CC, Liu CC, Chang YC, Chen CY, Wang ST et al. Neurologic complications in children with enterovirus 71 infection. N Engl J Med 1999; 341:936–942 [View Article][PubMed]
    [Google Scholar]
  50. Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT et al. An epidemic of enterovirus 71 infection in Taiwan. N Engl J Med 1999; 341:929–935 [View Article][PubMed]
    [Google Scholar]
  51. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P et al. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 2010; 10:778–790 [View Article][PubMed]
    [Google Scholar]
  52. McMinn P, Stratov I, Nagarajan L, Davis S. Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clin Infect Dis 2001; 32:236–242 [View Article][PubMed]
    [Google Scholar]
  53. Yang F, Ren L, Xiong Z, Li J, Xiao Y et al. Enterovirus 71 outbreak in the People's Republic of China in 2008. J Clin Microbiol 2009; 47:2351–2352 [View Article][PubMed]
    [Google Scholar]
  54. Liu SL, Pan H, Liu P, Amer S, Chan TC et al. Comparative epidemiology and virology of fatal and nonfatal cases of hand, foot and mouth disease in mainland China from 2008 to 2014. Rev Med Virol 2015; 25:115–128 [View Article][PubMed]
    [Google Scholar]
  55. Liu Y, Sheng J, Fokine A, Meng G, Shin WH et al. Structure and inhibition of EV-D68, a virus that causes respiratory illness in children. Science 2015; 347:71–74 [View Article][PubMed]
    [Google Scholar]
  56. Cabrerizo M, Tarragó D, Muñoz-Almagro C, Del Amo E, Domínguez-Gil M et al. Molecular epidemiology of enterovirus 71, coxsackievirus A16 and A6 associated with hand, foot and mouth disease in Spain. Clin Microbiol Infect 2014; 20:O150–O156 [View Article][PubMed]
    [Google Scholar]
  57. Fischer TK, Nielsen AY, Sydenham TV, Andersen PH, Andersen B et al. Emergence of enterovirus 71 C4a in Denmark, 2009 to 2013. Euro Surveill 2014; 19:pii:20911 [View Article][PubMed]
    [Google Scholar]
  58. van der Sanden S, van Eek J, Martin DP, van der Avoort H, Vennema H et al. Detection of recombination breakpoints in the genomes of human enterovirus 71 strains isolated in the Netherlands in epidemic and non-epidemic years, 1963–2010. Infect Genet Evol 2011; 11:886–894 [View Article][PubMed]
    [Google Scholar]
  59. Schuffenecker I, Mirand A, Antona D, Henquell C, Chomel JJ et al. Epidemiology of human enterovirus 71 infections in France, 2000–2009. J Clin Virol 2011; 50:50–56 [View Article][PubMed]
    [Google Scholar]
  60. Karrasch M, Fischer E, Scholten M, Sauerbrei A, Henke A et al. A severe pediatric infection with a novel enterovirus A71 strain, Thuringia, Germany. J Clin Virol 2016; 84:90–95 [View Article][PubMed]
    [Google Scholar]
  61. ECDC 2016; Rapid Risk Assessment: Enterovirus Detections Associated with Severe Neurological Symptoms in Children and Adults in European Countries. http://ecdc.europa.eu/en/publications/Publications/01-08-2016-RRA-Enterovirus%2071-Spain,%20France,%20Netherlands.pdf
  62. Chang LY, Lin TY, Huang YC, Tsao KC, Shih SR et al. Comparison of enterovirus 71 and coxsackie-virus A16 clinical illnesses during the Taiwan enterovirus epidemic, 1998. Pediatr Infect Dis J 1999; 18:1092–1096 [View Article][PubMed]
    [Google Scholar]
  63. Wright HT, Landing BH, Lennette EH, Mcallister RM. Fatal infection in an infant associated with coxsackie virus group A, type 16. N Engl J Med 1963; 268:1041–1044 [View Article][PubMed]
    [Google Scholar]
  64. Wang CY, Li Lu F, Wu MH, Lee CY, Huang LM. Fatal coxsackievirus A16 infection. Pediatr Infect Dis J 2004; 23:275–276 [View Article][PubMed]
    [Google Scholar]
  65. Legay F, Lévêque N, Gacouin A, Tattevin P, Bouet J et al. Fatal coxsackievirus A-16 pneumonitis in adult. Emerg Infect Dis 2007; 13:1084–1086 [View Article][PubMed]
    [Google Scholar]
  66. Goto K, Sanefuji M, Kusuhara K, Nishimura Y, Shimizu H et al. Rhombencephalitis and coxsackievirus A16. Emerg Infect Dis 2009; 15:1689–1691 [View Article][PubMed]
    [Google Scholar]
  67. Chen WJ, Arnold JC, Fairchok MP, Danaher PJ, McDonough EA et al. Epidemiologic, clinical, and virologic characteristics of human rhinovirus infection among otherwise healthy children and adults: rhinovirus among adults and children. J Clin Virol 2015; 64:74–82 [View Article][PubMed]
    [Google Scholar]
  68. Robinson CR, Doane FW, Rhodes AJ. Report of an outbreak of febrile illness with pharyngeal lesions and exanthem: Toronto, summer 1957; isolation of group A coxsackie virus. Can Med Assoc J 1958; 79:615–621[PubMed]
    [Google Scholar]
  69. Ferson MJ, Bell SM. Outbreak of coxsackievirus A16 hand, foot, and mouth disease in a child day-care center. Am J Public Health 1991; 81:1675–1676 [View Article][PubMed]
    [Google Scholar]
  70. Bendig JW, Fleming DM. Epidemiological, virological, and clinical features of an epidemic of hand, foot, and mouth disease in England and Wales. Commun Dis Rep CDR Rev 1996; 6:R81–R86[PubMed]
    [Google Scholar]
  71. Kar BR, Dwibedi B, Kar SK. An outbreak of hand, foot and mouth disease in Bhubaneswar, Odisha. Indian Pediatr 2013; 50:139–142 [View Article][PubMed]
    [Google Scholar]
  72. Chang LY. Enterovirus 71 in Taiwan. Pediatr Neonatol 2008; 49:103–112 [View Article][PubMed]
    [Google Scholar]
  73. Tu PV, Thao NT, Perera D, Huu TK, Tien NT et al. Epidemiologic and virologic investigation of hand, foot, and mouth disease, southern Vietnam, 2005. Emerg Infect Dis 2007; 13:1733–1741 [View Article][PubMed]
    [Google Scholar]
  74. Liu JK. The history of monoclonal antibody development – progress, remaining challenges and future innovations. Ann Med Surg (Lond) 2014; 3:113–116 [View Article][PubMed]
    [Google Scholar]
  75. Ang LW, Koh BK, Chan KP, Chua LT, James L et al. Epidemiology and control of hand, foot and mouth disease in Singapore, 2001–2007. Ann Acad Med Singapore 2009; 38:106–112[PubMed]
    [Google Scholar]
  76. He SJ, Han JF, Ding XX, Wang YD, Qin CF. Characterization of enterovirus 71 and coxsackievirus A16 isolated in hand, foot, and mouth disease patients in Guangdong, 2010. Int J Infect Dis 2013; 17:e1025e1030 [View Article][PubMed]
    [Google Scholar]
  77. Zhang Y, Zhu Z, Yang W, Ren J, Tan X et al. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J 2010; 7:94 [View Article][PubMed]
    [Google Scholar]
  78. McWilliam Leitch EC, Cabrerizo M, Cardosa J, Harvala H, Ivanova OE et al. The association of recombination events in the founding and emergence of subgenogroup evolutionary lineages of human enterovirus 71. J Virol 2012; 86:2676–2685 [View Article][PubMed]
    [Google Scholar]
  79. Oberste MS, Maher K, Schnurr D, Flemister MR, Lovchik JC et al. Enterovirus 68 is associated with respiratory illness and shares biological features with both the enteroviruses and the rhinoviruses. J Gen Virol 2004; 85:2577–2584 [View Article][PubMed]
    [Google Scholar]
  80. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA. Centers for Disease Control and Prevention Enterovirus surveillance—United States, 1970–2005. MMWR Surveill Summ 2006; 55:1–20[PubMed]
    [Google Scholar]
  81. Imamura T, Suzuki A, Meijer A, Niesters HGM, Lojo JC et al. Clusters of acute respiratory illness associated with human enterovirus 68—Asia, Europe, and United States, 2008–2010. MMWR Morb Mortal Wkly Rep 2011; 60:1301–1304[PubMed]
    [Google Scholar]
  82. Meijer A, Benschop KS, Donker GA, van der Avoort HG. Continued seasonal circulation of enterovirus D68 in the Netherlands, 2011–2014. Euro Surveill 2014; 19:pii:20935 [View Article][PubMed]
    [Google Scholar]
  83. Esposito S, Zampiero A, Ruggiero L, Madini B, Niesters H et al. Enterovirus D68-associated community-acquired pneumonia in children living in Milan, Italy. J Clin Virol 2015; 68:94–96 [View Article][PubMed]
    [Google Scholar]
  84. Gimferrer L, Campins M, Codina MG, Esperalba J, Martin MC et al. First enterovirus D68 (EV-D68) cases detected in hospitalised patients in a tertiary care university hospital in Spain, October 2014. Enferm Infecc Microbiol Clin 2015; 33:585–589 [View Article][PubMed]
    [Google Scholar]
  85. Imamura T, Suzuki A, Lupisan S, Okamoto M, Aniceto R et al. Molecular evolution of enterovirus 68 detected in the Philippines. PLoS One 2013; 8:e74221 [View Article][PubMed]
    [Google Scholar]
  86. Lu QB, Wo Y, Wang HY, Wei MT, Zhang L et al. Detection of enterovirus 68 as one of the commonest types of enterovirus found in patients with acute respiratory tract infection in China. J Med Microbiol 2014; 63:408–414 [View Article][PubMed]
    [Google Scholar]
  87. Khan F. Enterovirus D68: acute respiratory illness and the 2014 outbreak. Emerg Med Clin North Am 2015; 33:e19e32[PubMed] [CrossRef]
    [Google Scholar]
  88. Messacar K, Schreiner TL, Maloney JA, Wallace A, Ludke J et al. A cluster of acute flaccid paralysis and cranial nerve dysfunction temporally associated with an outbreak of enterovirus D68 in children in Colorado, USA. Lancet 2015; 385:1662–1671 [View Article][PubMed]
    [Google Scholar]
  89. Lang M, Mirand A, Savy N, Henquell C, Maridet S et al. Acute flaccid paralysis following enterovirus D68 associated pneumonia, France, 2014. Euro Surveill 2014; 19:pii:20952 [View Article][PubMed]
    [Google Scholar]
  90. Pfeiffer HC, Bragstad K, Skram MK, Dahl H, Knudsen PK et al. Two cases of acute severe flaccid myelitis associated with enterovirus D68 infection in children, Norway, autumn 2014. Euro Surveill 2015; 20:21062 [View Article][PubMed]
    [Google Scholar]
  91. Greninger AL, Naccache SN, Messacar K, Clayton A, Yu G et al. A novel outbreak enterovirus D68 strain associated with acute flaccid myelitis cases in the USA (2012–14): a retrospective cohort study. Lancet Infect Dis 2015; 15:671–682 [View Article][PubMed]
    [Google Scholar]
  92. Du J, Zheng B, Zheng W, Li P, Kang J et al. Analysis of enterovirus 68 strains from the 2014 North American outbreak reveals a new clade, indicating viral evolution. PLoS One 2015; 10:e0144208 [View Article][PubMed]
    [Google Scholar]
  93. Romero JR, Selvarangan R. The human parechoviruses: an overview. Adv Pediatr 2011; 58:65–85 [View Article][PubMed]
    [Google Scholar]
  94. Ito M, Yamashita T, Tsuzuki H, Takeda N, Sakae K. Isolation and identification of a novel human parechovirus. J Gen Virol 2004; 85:391–398 [View Article][PubMed]
    [Google Scholar]
  95. Harvala H, Robertson I, Chieochansin T, McWilliam Leitch EC, Templeton K et al. Specific association of human parechovirus type 3 with sepsis and fever in young infants, as identified by direct typing of cerebrospinal fluid samples. J Infect Dis 2009; 199:1753–1760 [View Article][PubMed]
    [Google Scholar]
  96. Harvala H, McLeish N, Kondracka J, McIntyre CL, McWilliam Leitch EC et al. Comparison of human parechovirus and enterovirus detection frequencies in cerebrospinal fluid samples collected over a 5-year period in Edinburgh: HPeV type 3 identified as the most common picornavirus type. J Med Virol 2011; 83:889–896 [View Article][PubMed]
    [Google Scholar]
  97. van der Sanden S, de Bruin E, Vennema H, Swanink C, Koopmans M et al. Prevalence of human parechovirus in the Netherlands in 2000 to 2007. J Clin Microbiol 2008; 46:2884–2889 [View Article][PubMed]
    [Google Scholar]
  98. Wolthers KC, Benschop KS, Schinkel J, Molenkamp R, Bergevoet RM et al. Human parechoviruses as an important viral cause of sepsislike illness and meningitis in young children. Clin Infect Dis 2008; 47:358–363 [View Article][PubMed]
    [Google Scholar]
  99. Benschop KS, Schinkel J, Minnaar RP, Pajkrt D, Spanjerberg L et al. Human parechovirus infections in Dutch children and the association between serotype and disease severity. Clin Infect Dis 2006; 42:204–210 [View Article][PubMed]
    [Google Scholar]
  100. Boivin G, Abed Y, Boucher FD. Human parechovirus 3 and neonatal infections. Emerg Infect Dis 2005; 11:103–107 [View Article][PubMed]
    [Google Scholar]
  101. Yamamoto M, Abe K, Kuniyori K, Kunii E, Ito F et al. Epidemic of human parechovirus type 3 in Hiroshima city, Japan in 2008. Jpn J Infect Dis 2009; 62:244–245[PubMed]
    [Google Scholar]
  102. Cumming G, Khatami A, Mcmullan BJ, Musto J, Leung K et al. Parechovirus genotype 3 outbreak among infants, New South Wales, Australia, 2013-2014. Emerg Infect Dis 2015; 21:1144–1152 [View Article][PubMed]
    [Google Scholar]
  103. Tapia G, Cinek O, Witsø E, Kulich M, Rasmussen T et al. Longitudinal observation of parechovirus in stool samples from Norwegian infants. J Med Virol 2008; 80:1835–1842 [View Article][PubMed]
    [Google Scholar]
  104. Selvarangan R, Nzabi M, Selvaraju SB, Ketter P, Carpenter C et al. Human parechovirus 3 causing sepsis-like illness in children from midwestern United States. Pediatr Infect Dis J 2011; 30:238–242 [View Article][PubMed]
    [Google Scholar]
  105. Shoji K, Komuro H, Miyata I, Miyairi I, Saitoh A. Dermatologic manifestations of human parechovirus type 3 infection in neonates and infants. Pediatr Infect Dis J 2013; 32:233–236 [View Article][PubMed]
    [Google Scholar]
  106. Schuffenecker I, Javouhey E, Gillet Y, Kugener B, Billaud G et al. Human parechovirus infections, Lyon, France, 2008–10: evidence for severe cases. J Clin Virol 2012; 54:337–341 [View Article][PubMed]
    [Google Scholar]
  107. Khatami A, Mcmullan BJ, Webber M, Stewart P, Francis S et al. Sepsis-like disease in infants due to human parechovirus type 3 during an outbreak in Australia. Clin Infect Dis 2015; 60:228–236 [View Article][PubMed]
    [Google Scholar]
  108. Kurz H, Prammer R, Bock W, Ollerieth R, Bernert G et al. Intracranial hemorrhage and other symptoms in infants associated with human parechovirus in Vienna, Austria. Eur J Pediatr 2015; 174:1639–1647 [View Article][PubMed]
    [Google Scholar]
  109. Aviner S, Sofer D, Shulman LM, Bibi H, Weitzman S. Hemophagocytic lymphohistiocytosis associated with parechovirus 3 infection. J Pediatr Hematol Oncol 2014; 36:e251e253 [View Article][PubMed]
    [Google Scholar]
  110. Mizuta K, Yamakawa T, Nagasawa H, Itagaki T, Katsushima F et al. Epidemic myalgia associated with human parechovirus type 3 infection among adults occurs during an outbreak among children: findings from Yamagata, Japan, in 2011. J Clin Virol 2013; 58:188–193 [View Article][PubMed]
    [Google Scholar]
  111. Yamamoto SP, Kaida A, Naito T, Hosaka T, Miyazato Y et al. Human parechovirus infections and child myositis cases associated with genotype 3 in Osaka City, Japan, 2014. J Med Microbiol 2015; 64:1415–1424 [View Article][PubMed]
    [Google Scholar]
  112. Bissel SJ, Auer RN, Chiang CH, Kofler J, Murdoch GH et al. Human parechovirus 3 meningitis and fatal leukoencephalopathy. J Neuropathol Exp Neurol 2015; 74:767–777 [View Article][PubMed]
    [Google Scholar]
  113. van Zwol AL, Lequin M, Aarts-Tesselaar C, van der Eijk AA, Driessen GA et al. Fatal neonatal parechovirus encephalitis. BMJ Case Rep 2009:bcr0520091883 [View Article][PubMed]
    [Google Scholar]
  114. Wildenbeest JG, Harvala H, Pajkrt D, Wolthers KC. The need for treatment against human parechoviruses: how, why and when?. Expert Rev Anti Infect Ther 2010; 8:1417–1429 [View Article][PubMed]
    [Google Scholar]
  115. Dotzauer A, Kraemer L. Innate and adaptive immune responses against picornaviruses and their counteractions: an overview. World J Virol 2012; 1:91–107 [View Article][PubMed]
    [Google Scholar]
  116. Halliday E, Winkelstein J, Webster AD. Enteroviral infections in primary immunodeficiency (PID): a survey of morbidity and mortality. J Infect 2003; 46:1–8 [View Article][PubMed]
    [Google Scholar]
  117. Winkelstein JA, Marino MC, Lederman HM, Jones SM, Sullivan K et al. X-linked agammaglobulinemia: report on a United States registry of 201 patients. Medicine (Baltimore) 2006; 85:193–202 [View Article][PubMed]
    [Google Scholar]
  118. van de Ven AA, Douma JW, Rademaker C, van Loon AM, Wensing AM et al. Pleconaril-resistant chronic parechovirus-associated enteropathy in agammaglobulinaemia. Antivir Ther 2011; 16:611–614 [View Article][PubMed]
    [Google Scholar]
  119. Mardekian SK, Fortuna D, Nix A, Bhatti T, Wiley CA et al. Severe human parechovirus type 3 myocarditis and encephalitis in an adolescent with hypogammaglobulinemia. Int J Infect Dis 2015; 36:6–8 [View Article][PubMed]
    [Google Scholar]
  120. Servais S, Caers J, Warling O, Frusch N, Baron F et al. Enteroviral meningoencephalitis as complication of Rituximab therapy in a patient treated for diffuse large B-cell lymphoma. Br J Haematol 2010; 150:379–381 [View Article][PubMed]
    [Google Scholar]
  121. Liao CC, Liou AT, Chang YS, Wu SY, Chang CS et al. Immunodeficient mouse models with different disease profiles by in vivo infection with the same clinical isolate of enterovirus 71. J Virol 2014; 88:12485–12499 [View Article][PubMed]
    [Google Scholar]
  122. Rodriguez M, Kenny JJ, Thiemann RL, Woloschak GE. Theiler's virus-induced demyelination in mice immunosuppressed with anti-IgM and in mice expressing the xid gene. Microb Pathog 1990; 8:23–35 [View Article][PubMed]
    [Google Scholar]
  123. van der Linden L, Wolthers KC, van Kuppeveld FJ. Replication and inhibitors of enteroviruses and parechoviruses. Viruses 2015; 7:4529–4562 [View Article][PubMed]
    [Google Scholar]
  124. Quartier P, Foray S, Casanova JL, Hau-Rainsard I, Blanche S et al. Enteroviral meningoencephalitis in X-linked agammaglobulinemia: intensive immunoglobulin therapy and sequential viral detection in cerebrospinal fluid by polymerase chain reaction. Pediatr Infect Dis J 2000; 19:1106–1108 [View Article][PubMed]
    [Google Scholar]
  125. Nathanson N, Bodian D. Experimental poliomyelitis following intramuscular virus injection. III. The effect of passive antibody on paralysis and viremia. Bull Johns Hopkins Hosp 1962; 111:198–220[PubMed]
    [Google Scholar]
  126. Wildenbeest JG, Wolthers KC, Straver B, Pajkrt D. Successful IVIG treatment of human parechovirus-associated dilated cardiomyopathy in an infant. Pediatrics 2013; 132:e243e247 [View Article][PubMed]
    [Google Scholar]
  127. Bessaud M, Razafindratsimandresy R, Nougairède A, Joffret ML, Deshpande JM et al. Molecular comparison and evolutionary analyses of VP1 nucleotide sequences of new African human enterovirus 71 isolates reveal a wide genetic diversity. PLoS One 2014; 9:e90624 [View Article][PubMed]
    [Google Scholar]
  128. Brown BA, Oberste MS, Alexander JP, Kennett ML, Pallansch MA. Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 1999; 73:9969–9975[PubMed]
    [Google Scholar]
  129. Chong P, Liu CC, Chow YH, Chou AH, Klein M. Review of enterovirus 71 vaccines. Clin Infect Dis 2015; 60:797–803 [View Article][PubMed]
    [Google Scholar]
  130. Huang ML, Chiang PS, Chia MY, Luo ST, Chang LY et al. Cross-reactive neutralizing antibody responses to enterovirus 71 infections in young children: implications for vaccine development. PLoS Negl Trop Dis 2013; 7:e2067 [View Article][PubMed]
    [Google Scholar]
  131. Mizuta K, Aoki Y, Suto A, Ootani K, Katsushima N et al. Cross-antigenicity among EV71 strains from different genogroups isolated in Yamagata, Japan, between 1990 and 2007. Vaccine 2009; 27:3153–3158 [View Article][PubMed]
    [Google Scholar]
  132. van der Sanden S, van der Avoort H, Lemey P, Uslu G, Koopmans M. Evolutionary trajectory of the VP1 gene of human enterovirus 71 genogroup B and C viruses. J Gen Virol 2010; 91:1949–1958 [View Article][PubMed]
    [Google Scholar]
  133. Chen Y, Li C, He D, Cheng T, Ge S et al. Antigenic analysis of divergent genotypes human enterovirus 71 viruses by a panel of neutralizing monoclonal antibodies: current genotyping of EV71 does not reflect their antigenicity. Vaccine 2013; 31:425–430 [View Article][PubMed]
    [Google Scholar]
  134. Zhang Y, Wang D, Yan D, Zhu S, Liu J et al. Molecular evidence of persistent epidemic and evolution of subgenotype B1 coxsackievirus A16-associated hand, foot, and mouth disease in China. J Clin Microbiol 2010; 48:619–622 [View Article][PubMed]
    [Google Scholar]
  135. Bible JM, Pantelidis P, Chan PK, Tong CY. Genetic evolution of enterovirus 71: epidemiological and pathological implications. Rev Med Virol 2007; 17:371–379 [View Article][PubMed]
    [Google Scholar]
  136. Arita M, Nagata N, Iwata N, Ami Y, Suzaki Y et al. An attenuated strain of enterovirus 71 belonging to genotype a showed a broad spectrum of antigenicity with attenuated neurovirulence in cynomolgus monkeys. J Virol 2007; 81:9386–9395 [View Article][PubMed]
    [Google Scholar]
  137. Liu Q, Tong X, Huang Z. Towards broadly protective polyvalent vaccines against hand, foot and mouth disease. Microbes Infect 2015; 17:155–162 [View Article][PubMed]
    [Google Scholar]
  138. Mao QY, Wang Y, Bian L, Xu M, Liang Z. EV71 vaccine, a new tool to control outbreaks of hand, foot and mouth disease (HFMD). Expert Rev Vaccines 2016; 15:599–606 [View Article][PubMed]
    [Google Scholar]
  139. Liu CC, Guo MS, Lin FH, Hsiao KN, Chang KH et al. Purification and characterization of enterovirus 71 viral particles produced from Vero cells grown in a serum-free microcarrier bioreactor system. PLoS One 2011; 6:e20005 [View Article][PubMed]
    [Google Scholar]
  140. Chung YC, Ho MS, Wu JC, Chen WJ, Huang JH et al. Immunization with virus-like particles of enterovirus 71 elicits potent immune responses and protects mice against lethal challenge. Vaccine 2008; 26:1855–1862 [View Article][PubMed]
    [Google Scholar]
  141. Li HY, Han JF, Qin CF, Chen R. Virus-like particles for enterovirus 71 produced from Saccharomyces cerevisiae potently elicits protective immune responses in mice. Vaccine 2013; 31:3281–3287 [CrossRef]
    [Google Scholar]
  142. Gong M, Zhu H, Zhou J, Yang C, Feng J et al. Cryo-electron microscopy study of insect cell-expressed enterovirus 71 and coxsackievirus A16 virus-like particles provides a structural basis for vaccine development. J Virol 2014; 88:6444–6452 [View Article][PubMed]
    [Google Scholar]
  143. Lin YL, Yu CI, Hu YC, Tsai TJ, Kuo YC et al. Enterovirus type 71 neutralizing antibodies in the serum of macaque monkeys immunized with EV71 virus-like particles. Vaccine 2012; 30:1305–1312 [View Article][PubMed]
    [Google Scholar]
  144. Liu L, Mo Z, Liang Z, Zhang Y, Li R et al. Immunity and clinical efficacy of an inactivated enterovirus 71 vaccine in healthy Chinese children: a report of further observations. BMC Med 2015; 13:226 [View Article][PubMed]
    [Google Scholar]
  145. Mao Q, Cheng T, Zhu F, Li J, Wang Y et al. The cross-neutralizing activity of enterovirus 71 subgenotype c4 vaccines in healthy Chinese infants and children. PLoS One 2013; 8:e79599 [View Article][PubMed]
    [Google Scholar]
  146. Ku Z, Liu Q, Ye X, Cai Y, Wang X et al. A virus-like particle based bivalent vaccine confers dual protection against enterovirus 71 and coxsackievirus A16 infections in mice. Vaccine 2014; 32:4296–4303 [View Article][PubMed]
    [Google Scholar]
  147. Liu CC, Chow YH, Chong P, Klein M. Prospect and challenges for the development of multivalent vaccines against hand, foot and mouth diseases. Vaccine 2014; 32:6177–6182 [View Article][PubMed]
    [Google Scholar]
  148. Caine EA, Fuchs J, das SC, Partidos CD, Osorio JE. Efficacy of a trivalent hand, foot, and mouth disease vaccine against enterovirus 71 and coxsackieviruses A16 and A6 in mice. Viruses 2015; 7:5919–5932 [View Article][PubMed]
    [Google Scholar]
  149. Chang GH, Luo YJ, Wu XY, Si BY, Lin L et al. Monoclonal antibody induced with inactived EV71-Hn2 virus protects mice against lethal EV71-Hn2 virus infection. Virol J 2010; 7:106 [View Article][PubMed]
    [Google Scholar]
  150. Foo DG, Alonso S, Phoon MC, Ramachandran NP, Chow VT et al. Identification of neutralizing linear epitopes from the VP1 capsid protein of enterovirus 71 using synthetic peptides. Virus Res 2007; 125:61–68 [View Article][PubMed]
    [Google Scholar]
  151. Lim XF, Jia Q, Khong WX, Yan B, Premanand B et al. Characterization of an isotype-dependent monoclonal antibody against linear neutralizing epitope effective for prophylaxis of enterovirus 71 infection. PLoS One 2012; 7:e29751 [View Article][PubMed]
    [Google Scholar]
  152. Lee H, Cifuente JO, Ashley RE, Conway JF, Makhov AM et al. A strain-specific epitope of enterovirus 71 identified by cryo-electron microscopy of the complex with Fab from neutralizing antibody. J Virol 2013; 87:11363–11370 [View Article][PubMed]
    [Google Scholar]
  153. Liu CC, Chou AH, Lien SP, Lin HY, Liu SJ et al. Identification and characterization of a cross-neutralization epitope of enterovirus 71. Vaccine 2011; 29:4362–4372 [View Article][PubMed]
    [Google Scholar]
  154. Kiener TK, Jia Q, Meng T, Chow VT, Kwang J. A novel universal neutralizing monoclonal antibody against enterovirus 71 that targets the highly conserved "knob" region of VP3 protein. PLoS Negl Trop Dis 2014; 8:e2895 [View Article][PubMed]
    [Google Scholar]
  155. Kirk K, Poh CL, Fecondo J, Pourianfar H, Shaw J et al. Cross-reactive neutralizing antibody epitopes against enterovirus 71 identified by an in silico approach. Vaccine 2012; 30:7105–7110 [View Article][PubMed]
    [Google Scholar]
  156. Zhao M, Bai Y, Liu W, Xiao X, Huang Y et al. Immunization of N terminus of enterovirus 71 VP4 elicits cross-protective antibody responses. BMC Microbiol 2013; 13:287 [View Article][PubMed]
    [Google Scholar]
  157. Plevka P, Perera R, Cardosa J, Kuhn RJ, Rossmann MG. Crystal structure of human enterovirus 71. Science 2012; 336:1274 [View Article][PubMed]
    [Google Scholar]
  158. Ren J, Wang X, Zhu L, Hu Z, Gao Q et al. Structures of coxsackievirus A16 capsids with native antigenicity: implications for particle expansion, receptor binding, and immunogenicity. J Virol 2015; 89:10500–10511 [View Article][PubMed]
    [Google Scholar]
  159. Shi J, Huang X, Liu Q, Huang Z. Identification of conserved neutralizing linear epitopes within the VP1 protein of coxsackievirus A16. Vaccine 2013; 31:2130–2136 [View Article][PubMed]
    [Google Scholar]
  160. Chong P, Guo MS, Lin FH, Hsiao KN, Weng SY et al. Immunological and biochemical characterization of coxsackie virus A16 viral particles. PLoS One 2012; 7:e49973 [View Article][PubMed]
    [Google Scholar]
  161. Zhang X, Sun C, Xiao X, Pang L, Shen S et al. Phage display-derived cross-reactive neutralizing antibody against enterovirus 71 and coxsackievirus A16. Jpn J Infect Dis 2016; 69:66–74 [View Article][PubMed]
    [Google Scholar]
  162. Li YX, Zhao H, Cao RY, Deng YQ, Han JF et al. Recombinant tandem multi-linear neutralizing epitopes of human enterovirus 71 elicited protective immunity in mice. Virol J 2014; 11:79 [View Article][PubMed]
    [Google Scholar]
  163. Li W, Joshi MD, Singhania S, Ramsey KH, Murthy AK. Peptide vaccine: progress and challenges. Vaccines 2014; 2:515–536 [View Article][PubMed]
    [Google Scholar]
  164. Lyu K, Wang GC, He YL, Han JF, Ye Q et al. Crystal structures of enterovirus 71 (EV71) recombinant virus particles provide insights into vaccine design. J Biol Chem 2015; 290:3198–3208 [View Article][PubMed]
    [Google Scholar]
  165. Zhao H, Li HY, Han JF, Deng YQ, Zhu SY et al. Novel recombinant chimeric virus-like particle is immunogenic and protective against both enterovirus 71 and coxsackievirus A16 in mice. Sci Rep 2015; 5:7878 [View Article][PubMed]
    [Google Scholar]
  166. Imamura T, Okamoto M, Nakakita S, Suzuki A, Saito M et al. Antigenic and receptor binding properties of enterovirus 68. J Virol 2014; 88:2374–2384 [View Article][PubMed]
    [Google Scholar]
  167. Meijer A, van der Sanden S, Snijders BE, Jaramillo-Gutierrez G, Bont L et al. Emergence and epidemic occurrence of enterovirus 68 respiratory infections in The Netherlands in 2010. Virology 2012; 423:49–57 [View Article][PubMed]
    [Google Scholar]
  168. Smura T, Ylipaasto P, Klemola P, Kaijalainen S, Kyllönen L et al. Cellular tropism of human enterovirus D species serotypes EV-94, EV-70, and EV-68 in vitro: implications for pathogenesis. J Med Virol 2010; 82:1940–1949 [View Article][PubMed]
    [Google Scholar]
  169. Shakeel S, Westerhuis BM, Ora A, Koen G, Bakker AQ et al. Structural basis of human parechovirus neutralization by human monoclonal antibodies. J Virol 2015; 89:9571–9580 [View Article][PubMed]
    [Google Scholar]
  170. Shakeel S, Westerhuis BM, Domanska A, Koning RI, Matadeen R et al. Multiple capsid-stabilizing interactions revealed in a high-resolution structure of an emerging picornavirus causing neonatal sepsis. Nat Commun 2016; 7:11387 [View Article][PubMed]
    [Google Scholar]
  171. Stanway G, Hyypiä T. Parechoviruses. J Virol 1999; 73:5249–5254[PubMed]
    [Google Scholar]
  172. Joki-Korpela P, Roivainen M, Lankinen H, Pöyry T, Hyypiä T. Antigenic properties of human parechovirus 1. J Gen Virol 2000; 81:1709–1718 [View Article][PubMed]
    [Google Scholar]
  173. Alho A, Marttila J, Ilonen J, Hyypiä T. Diagnostic potential of parechovirus capsid proteins. J Clin Microbiol 2003; 41:2294–2299 [View Article][PubMed]
    [Google Scholar]
  174. Westerhuis BM, Benschop KS, Koen G, Claassen YB, Wagner K et al. Human memory B cells producing potent cross-neutralizing antibodies against human parechovirus: implications for prevalence, treatment, and diagnosis. J Virol 2015; 89:7457–7464 [View Article][PubMed]
    [Google Scholar]
  175. Westerhuis B, Kolehmainen P, Benschop K, Nurminen N, Koen G et al. Human parechovirus seroprevalence in Finland and the Netherlands. J Clin Virol 2013; 58:211–215 [View Article][PubMed]
    [Google Scholar]
  176. Aizawa Y, Watanabe K, Oishi T, Hirano H, Hasegawa I et al. Role of maternal antibodies in infants with severe diseases related to human parechovirus type 3. Emerg Infect Dis 2015; 21:1966–1972 [View Article][PubMed]
    [Google Scholar]
  177. Westerhuis BM, Koen G, Wildenbeest JG, Pajkrt D, de Jong MD et al. Specific cell tropism and neutralization of human parechovirus types 1 and 3: implications for pathogenesis and therapy development. J Gen Virol 2012; 93:2363–2370 [View Article][PubMed]
    [Google Scholar]
  178. Sun S, Jiang L, Liang Z, Mao Q, Su W et al. Evaluation of monovalent and bivalent vaccines against lethal enterovirus 71 and coxsackievirus A16 infection in newborn mice. Hum Vaccin Immunother 2014; 10:2885–2895 [View Article][PubMed]
    [Google Scholar]
  179. Hansen LB, Buus S, Schafer-Nielsen C. Identification and mapping of linear antibody epitopes in human serum albumin using high-density peptide arrays. PLoS One 2013; 8:e68902 [View Article][PubMed]
    [Google Scholar]
  180. Palm K, Kasak L, Kivil A, Lend A, Neuman T et al. Peptide profiling and monitoring humoral immunity. US Patent and Trademark Office Priority number US 14/079,626; 2013
  181. Xu GJ, Kula T, Xu Q, Li MZ, Vernon SD et al. Viral immunology. Comprehensive serological profiling of human populations using a synthetic human virome. Science 2015; 348:aaa0698 [View Article][PubMed]
    [Google Scholar]
  182. Kwakkenbos MJ, Bakker AQ, van Helden PM, Wagner K, Yasuda E et al. Genetic manipulation of B cells for the isolation of rare therapeutic antibodies from the human repertoire. Methods 2014; 65:38–43 [View Article][PubMed]
    [Google Scholar]
  183. Lannes N, Python S, Summerfield A. Interplay of foot-and-mouth disease virus, antibodies and plasmacytoid dendritic cells: virus opsonization under non-neutralizing conditions results in enhanced interferon-alpha responses. Vet Res 2012; 43:64 [View Article][PubMed]
    [Google Scholar]
  184. McCullough KC, Parkinson D, Crowther JR. Opsonization-enhanced phagocytosis of foot-and-mouth disease virus. Immunology 1988; 65:187–191[PubMed]
    [Google Scholar]
  185. Chen IC, Wang SM, Yu CK, Liu CC. Subneutralizing antibodies to enterovirus 71 induce antibody-dependent enhancement of infection in newborn mice. Med Microbiol Immunol 2013; 202:259–265 [View Article][PubMed]
    [Google Scholar]
  186. Girn J, Kavoosi M, Chantler J. Enhancement of coxsackievirus B3 infection by antibody to a different coxsackievirus strain. J Gen Virol 2002; 83:351–358 [View Article][PubMed]
    [Google Scholar]
  187. Georgiou G, Ippolito GC, Beausang J, Busse CE, Wardemann H et al. The promise and challenge of high-throughput sequencing of the antibody repertoire. Nat Biotechnol 2014; 32:158–168 [View Article][PubMed]
    [Google Scholar]
  188. Bradbury AR, Sidhu S, Dübel S, Mccafferty J. Beyond natural antibodies: the power of in vitro display technologies. Nat Biotechnol 2011; 29:245–254 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000780
Loading
/content/journal/jgv/10.1099/jgv.0.000780
Loading

Data & Media loading...

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