Broad Blockade Antibody Responses in Human Volunteers after Immunization with a Multivalent Norovirus VLP Candidate Vaccine: Immunological Analyses from a Phase I Clinical Trial

1. World Health Organization (2013) Diarrhoeal disease. Fact sheet No. 330. Geneva: World Health Organization.

2. Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention (2011) Updated norovirus outbreak management and disease prevention guidelines. MMWR Recomm Rep 60: 1–18. 22108587

3. Trivedi TK, Desai R, Hall AJ, Patel M, Parashar UD, et al. (2013) Clinical characteristics of norovirus-associated deaths: a systematic literature review. Am J Infect Control 41: 654–657. doi: 10.1016/j.ajic.2012.08.002 23266383

4. Bok K, Green KY (2012) Norovirus gastroenteritis in immunocompromised patients. N Engl J Med 367: 2126–2132. doi: 10.1056/NEJMra1207742 23190223

5. Trivedi TK, DeSalvo T, Lee L, Palumbo A, Moll M, et al. (2012) Hospitalizations and mortality associated with norovirus outbreaks in nursing homes, 2009–2010. JAMA 308: 1668–1675. 23079758

6. Hutson AM, Atmar RL, Estes MK (2004) Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol 12: 279–287. 15165606

7. Estes MK, Prasad BV, Atmar RL (2006) Noroviruses everywhere: has something changed? Curr Opin Infect Dis 19: 467–474. 16940871

8. Koopmans M, Vinje J, de Wit M, Leenen I, van der Poel W, et al. (2000) Molecular epidemiology of human enteric caliciviruses in The Netherlands. J Infect Dis 181 (Suppl 2): S262–S269. 10804135

9. Centers for Disease Control and Prevention (2007) Norovirus activity—United States, 2006–2007. MMWR Morb Mortal Wekly Rep 56: 842–846. 17717513

10. Okada M, Tanaka T, Oseto M, Takeda N, Shinozaki K (2006) Genetic analysis of noroviruses associated with fatalities in healthcare facilities. Arch Virol 151: 1635–1641. 16521046

11. Harris JP, Edmunds WJ, Pebody R, Brown DW, Lopman BA (2008) Deaths from norovirus among the elderly, England and Wales. Emerg Infect Dis 14: 1546–1552. doi: 10.3201/eid1410.080188 18826817

12. Schorn R, Hohne M, Meerbach A, Bossart W, Wuthrich RP, et al. (2010) Chronic norovirus infection after kidney transplantation: molecular evidence for immune-driven viral evolution. Clin Infect Dis 51: 307–314. doi: 10.1086/653939 20575662

13. Hall AJ, Eisenbart VG, Etingue AL, Gould LH, Lopman BA, et al. (2012) Epidemiology of foodborne norovirus outbreaks, United States, 2001–2008. Emerg Infect Dis 18: 1566–1573. doi: 10.3201/eid1810.120833 23017158

14. Kroneman A, Harris J, Vennema H, Duizer E, van Duynhoven Y, et al. (2008) Data quality of 5 years of central norovirus outbreak reporting in the European Network for food-borne viruses. J Public Health (Oxf) 30: 82–90.

15. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, et al. (2006) Norovirus classification and proposed strain nomenclature. Virology 346: 312–323. 16343580

16. Green KY, Lew JF, Jiang X, Kapikian AZ, Estes MK (1993) Comparison of the reactivities of baculovirus-expressed recombinant Norwalk virus capsid antigen with those of the native Norwalk virus antigen in serologic assays and some epidemiologic observations. J Clin Microbiol 31: 2185–2191. 8396590

17. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, et al. (1999) X-ray crystallographic structure of the Norwalk virus capsid. Science 286: 287–290. 10514371

18. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, et al. (2003) Human susceptibility and resistance to Norwalk virus infection. Nat Med 9: 548–553. 12692541

19. Lindesmith LC, Donaldson EF, Lobue AD, Cannon JL, Zheng DP, et al. (2008) Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med 5: e0050031. doi: 10.1371/journal.pmed.0050031 18271619

20. Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, et al. (2013) Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol 87: 2803–2813. doi: 10.1128/JVI.03106-12 23269783

21. Bok K, Parra GI, Mitra T, Abente E, Shaver CK, et al. (2011) Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci U S A 108: 325–330. doi: 10.1073/pnas.1014577107 21173246

22. Reeck A, Kavanagh O, Estes MK, Opekun AR, Gilger MA, et al. (2010) Serological correlate of protection against norovirus-induced gastroenteritis. J Infect Dis 202: 1212–1218. doi: 10.1086/656364 20815703

23. Atmar RL, Bernstein DI, Harro CD, Al-Ibrahim MS, Chen WH, et al. (2011) Norovirus vaccine against experimental human Norwalk Virus illness. N Engl J Med 365: 2178–2187. doi: 10.1056/NEJMoa1101245 22150036

24. Siebenga JJ, Vennema H, Renckens B, de Bruin E, van der Veer B, et al. (2007) Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol 81: 9932–9941. 17609280

25. Lindesmith LC, Beltramello M, Donaldson EF, Corti D, Swanstrom J, et al. (2012) Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog 8: e1002705. doi: 10.1371/journal.ppat.1002705 22615565

26. Lindesmith LC, Donaldson EF, Baric RS (2011) Norovirus GII.4 strain antigenic variation. J Virol 85: 231–242. doi: 10.1128/JVI.01364-10 20980508

27. Debbink K, Donaldson EF, Lindesmith LC, Baric RS (2012) Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J Virol 86: 1214–1226. doi: 10.1128/JVI.06189-11 22090110

28. Cannon JL, Lindesmith LC, Donaldson EF, Saxe L, Baric RS, et al. (2009) Herd immunity to GII.4 noroviruses is supported by outbreak patient sera. J Virol 83: 5363–5374. doi: 10.1128/JVI.02518-08 19297483

29. Debbink K, Lindesmith LC, Donaldson EF, Costantini V, Beltramello M, et al. (2013) Emergence of new pandemic GII.4 Sydney norovirus strain correlates with escape from herd immunity. J Infect Dis 208: 1877–1887. doi: 10.1093/infdis/jit370 23908476

30. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS (2008) Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol Rev 225: 190–211. doi: 10.1111/j.1600-065X.2008.00680.x 18837783

31. Lindesmith LC, Debbink K, Swanstrom J, Vinje J, Costantini V, et al. (2012) Monoclonal antibody-based antigenic mapping of norovirus GII.4-2002. J Virol 86: 873–883. doi: 10.1128/JVI.06200-11 22090098

32. Lindesmith LC, Donaldson EF, Beltramello M, Pintus S, Corti D, et al. (2014) Particle conformation regulates antibody access to a conserved GII.4 norovirus blockade epitope. J Virol 88: 8826–8842. doi: 10.1128/JVI.01192-14 24872579

33. Eden JS, Tanaka MM, Boni MF, Rawlinson WD, White PA (2013) Recombination within the pandemic norovirus GII.4 lineage. J Virol 87: 6270–6282. doi: 10.1128/JVI.03464-12 23536665

34. Bull RA, Eden JS, Rawlinson WD, White PA (2010) Rapid evolution of pandemic noroviruses of the GII.4 lineage. PLoS Pathog 6: e1000831. doi: 10.1371/journal.ppat.1000831 20360972

35. Siebenga JJ, Lemey P, Kosakovsky Pond SL, Rambaut A, Vennema H, et al. (2010) Phylodynamic reconstruction reveals norovirus GII.4 epidemic expansions and their molecular determinants. PLoS Pathog 6: e1000884. doi: 10.1371/journal.ppat.1000884 20463813

36. Richardson C, Bargatze RF, Goodwin R, Mendelman PM (2013) Norovirus virus-like particle vaccines for the prevention of acute gastroenteritis. Expert Rev Vaccines 12: 155–167. doi: 10.1586/erv.12.145 23414407

37. Treanor JJ, Atmar RL, Frey SE, Gormley R, Chen WH, et al. (2014) A novel intramuscular bivalent norovirus virus-like particle vaccine candidate-reactogenicity, safety, and immunogenicity in a phase 1 trial in healthy adults. J Infect Dis 210: 1763–1771. doi: 10.1093/infdis/jiu337 24951828

38. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS (2010) Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol 8: 231–241. doi: 10.1038/nrmicro2296 20125087

39. Nordgren J, Kindberg E, Lindgren PE, Matussek A, Svensson L (2010) Norovirus gastroenteritis outbreak with a secretor-independent susceptibility pattern, Sweden. Emerg Infect Dis 16: 81–87. doi: 10.3201/eid1601.090633 20031047

40. Frenck R, Bernstein DI, Xia M, Huang P, Zhong W, et al. (2012) Predicting susceptibility to norovirus GII.4 by use of a challenge model involving humans. J Infect Dis 206: 1386–1393. doi: 10.1093/infdis/jis514 22927452

41. Lindesmith L, Moe C, Lependu J, Frelinger JA, Treanor J, et al. (2005) Cellular and humoral immunity following Snow Mountain virus challenge. J Virol 79: 2900–2909. 15709009

42. Bernstein DI, Atmar RL, Lyon GM, Treanor JJ, Chen WH, et al. (2014) Norovirus vaccine against experimental human GII.4 virus illness: a challenge study in healthy adults. J Infect Dis. E-pub ahead of print. doi: 10.1093/infdis/jiu497

43. Swanstrom J, Lindesmith LC, Donaldson EF, Yount B, Baric RS (2014) Characterization of blockade antibody responses in GII.2.1976 Snow Mountain virus-infected subjects. J Virol 88: 829–837. doi: 10.1128/JVI.02793-13 24173225

44. LoBue AD, Lindesmith L, Yount B, Harrington PR, Thompson JM, et al. (2006) Multivalent norovirus vaccines induce strong mucosal and systemic blocking antibodies against multiple strains. Vaccine 24: 5220–5234. 16650512

45. Debbink K, Lindesmith LC, Ferris MT, Swanstrom J, Beltramello M, et al. (2014) Within-host evolution results in antigenically distinct GII.4 noroviruses. J Virol 88: 7244–7255. doi: 10.1128/JVI.00203-14 24648459

46. Cai Z, Zhang T, Wan XF (2010) A computational framework for influenza antigenic cartography. PLoS Comput Biol 6: e1000949. doi: 10.1371/journal.pcbi.1000949 20949097

47. Wang F, Sen S, Zhang Y, Ahmad I, Zhu X, et al. (2013) Somatic hypermutation maintains antibody thermodynamic stability during affinity maturation. Proc Natl Acad Sci U S A 110: 4261–4266. doi: 10.1073/pnas.1301810110 23440204

48. Hoffmann D, Hutzenthaler M, Seebach J, Panning M, Umgelter A, et al. (2012) Norovirus GII.4 and GII.7 capsid sequences undergo positive selection in chronically infected patients. Infect Genet Evol 12: 461–466. doi: 10.1016/j.meegid.2012.01.020 22310302

49. Barnett JL, Yang J, Cai Z, Zhang T, Wan XF (2012) AntigenMap 3D: an online antigenic cartography resource. Bioinformatics 28: 1292–1293. doi: 10.1093/bioinformatics/bts105 22399675

50. Debbink K, Lindesmith LC, Donaldson EF, Baric RS (2012) Norovirus immunity and the great escape. PLoS Pathog 8: e1002921. doi: 10.1371/journal.ppat.1002921 23093932

51. Lindesmith LC, Donaldson E, Leon J, Moe CL, Frelinger JA, et al. (2010) Heterotypic humoral and cellular immune responses following Norwalk virus infection. J Virol 84: 1800–1815. doi: 10.1128/JVI.02179-09 20007270

52. Schmidt AG, Xu H, Khan AR, O’Donnell T, Khurana S, et al. (2013) Preconfiguration of the antigen-binding site during affinity maturation of a broadly neutralizing influenza virus antibody. Proc Natl Acad Sci U S A 110: 264–269. doi: 10.1073/pnas.1218256109 23175789

53. Li GM, Chiu C, Wrammert J, McCausland M, Andrews SF, et al. (2012) Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci U S A 109: 9047–9052. doi: 10.1073/pnas.1118979109 22615367

54. Kobayashi M, Ohfuji S, Fukushima W, Maeda A, Maeda K, et al. (2012) Immunogenicity and reactogenicity of a monovalent inactivated 2009 influenza A vaccine in adolescents: with special reference to pre-existing antibody. J Pediatr 160: 632–637. doi: 10.1016/j.jpeds.2011.09.055 22094234

55. Knuchel MC, Marty RR, Morin TN, Ilter O, Zuniga A, et al. (2013) Relevance of a pre-existing measles immunity prior immunization with a recombinant measles virus vector. Hum Vaccin Immunother 9: 599–606. 23324399

56. Liang XF, Wang HQ, Wang JZ, Fang HH, Wu J, et al. (2010) Safety and immunogenicity of 2009 pandemic influenza A H1N1 vaccines in China: a multicentre, double-blind, randomised, placebo-controlled trial. Lancet 375: 56–66. doi: 10.1016/S0140-6736(09)62003-1 20018364

57. Zhu FC, Wang H, Fang HH, Yang JG, Lin XJ, et al. (2009) A novel influenza A (H1N1) vaccine in various age groups. N Engl J Med 361: 2414–2423. doi: 10.1056/NEJMoa0908535 19846844

58. Wrammert J, Smith K, Miller J, Langley WA, Kokko K, et al. (2008) Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453: 667–671. doi: 10.1038/nature06890 18449194

59. Mora JR (2008) Homing imprinting and immunomodulation in the gut: role of dendritic cells and retinoids. Inflamm Bowel Dis 14: 275–289. 17924560

60. Kuklin NA, Rott L, Feng N, Conner ME, Wagner N, et al. (2001) Protective intestinal anti-rotavirus B cell immunity is dependent on alpha 4 beta 7 integrin expression but does not require IgA antibody production. J Immunol 166: 1894–1902. 11160237

61. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, et al. (2004) Mapping the antigenic and genetic evolution of influenza virus. Science 305: 371–376. 15218094

62. Huang SW, Hsu YW, Smith DJ, Kiang D, Tsai HP, et al. (2009) Reemergence of enterovirus 71 in 2008 in taiwan: dynamics of genetic and antigenic evolution from 1998 to 2008. J Clin Microbiol 47: 3653–3662. doi: 10.1128/JCM.00630-09 19776232

63. Debbink K, Lindesmith LC, Donaldson EF, Swanstrom J, Baric RS (2014) Chimeric GII.4 norovirus virus-like-particle-based vaccines induce broadly blocking immune responses. J Virol 88: 7256–7266. doi: 10.1128/JVI.00785-14 24741081

64. Corti D, Suguitan AL Jr, Pinna D, Silacci C, Fernandez-Rodriguez BM, et al. (2010) Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest 120: 1663–1673. doi: 10.1172/JCI41902 20389023

65. Lessler J, Riley S, Read JM, Wang S, Zhu H, et al. (2012) Evidence for antigenic seniority in influenza A (H3N2) antibody responses in southern China. PLoS Pathog 8: e1002802. doi: 10.1371/journal.ppat.1002802 22829765