Profiling of measles-specific humoral immunity in individuals following two doses of MMR vaccine using proteome microarrays

Viruses

Volumn 7, Issue 3, 2015, Pages 1113-1133

  Haralambieva, Iana H ^a   Simon, Whitney L ^a   Kennedy, Richard B ^a   Ovsyannikova, Inna G ^a   Warner, Nathaniel D ^a   Grill, Diane E ^a   Poland, Gregory A ^a  

^a MAYO CLINIC   (United States)

Author keywords

Antibodies; Humoral; Immunity; Measles; Measles virus; Measles mumps rubella vaccine; Neutralizing; Protein array analysis; Viral vaccines

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 29; INTERLEUKIN 6; MEASLES MUMPS RUBELLA VACCINE; NUCLEOPROTEIN; PHOSPHOPROTEIN; TUMOR NECROSIS FACTOR ALPHA; NEUTRALIZING ANTIBODY; PROTEOME; VIRUS ANTIBODY; VIRUS ANTIGEN;

ADOLESCENT; ADULT; ANTIBODY RESPONSE; ARTICLE; CHILD; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; MALE; MEASLES VIRUS; NORMAL HUMAN; PLAQUE REDUCTION MICRONEUTRALIZATION ASSAY; POLYMERASE CHAIN REACTION; PROTEIN DETERMINATION; PROTEIN MICROARRAY; SEROPREVALENCE; BLOOD; IMMUNOLOGY; STATISTICAL MODEL; YOUNG ADULT;

MEASLES VIRUS;

ADOLESCENT; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CHILD; FEMALE; HUMANS; MALE; MEASLES VIRUS; MEASLES-MUMPS-RUBELLA VACCINE; MODELS, STATISTICAL; PROTEIN ARRAY ANALYSIS; PROTEOME; YOUNG ADULT;

EID: 84925860535     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7031113     Document Type: Article

References (74)

1. Perry, R.T.; Gacic-Dobo, M.; Dabbagh, A.; Mulders, M.N.; Strebel, P.M.; Okwo-Bele, J.M.; Rota, P.A.; Goodson, J.L. Global control and regional elimination of measles, 2000–2012. Morb. Mortal. Wkly. Rep. 2014, 63, 103–107.
2. Fields, R.; Dabbagh, A.; Jain, M.; Sagar, K.S. Moving forward with strengthening routine immunization delivery as part of measles and rubella elimination activities. Vaccine 2013, 31, B115–B121.
3. Poland, G.A.; Jacobson, R.M. Failure to reach the goal of measles elimination. Apparent paradox of measles infections in immunized persons. Arch. Int. Med. 1994, 154, 1815–1820.
4. Elliman, D.; Sengupta, N. Measles. Curr. Opin. Infect. Dis. 2005, 18, 229–234.
5. Orenstein, W.A.; Herrmann, K.; Albrecht, P.; Bernier, R.; Holmgreen, P.; Bart, K.J.; Hinman, A.R. Immunity against measles and rubella in Massachusetts schoolchildren. Dev. Biol. Stand. 1986, 65, 75–83.
6. Poland, G.A.; Jacobson, R.M.; Schaid, D.J.; Moore, S.B.; Jacobsen, S.J. The association between HLA class I alleles and measles vaccine-induced antibody response: Evidence of a significant association. Vaccine 1998, 16, 1869–1871.
7. Sheppeard, V.; Forssman, B.; Ferson, M.J.; Moreira, C.; Campbell-Lloyd, S.; Dwyer, D.E.; McAnulty, J.M. Vaccine failures and vaccine effectiveness in children during measles outbreaks in New South Wales, March-May 2006. Commun. Dis. Intel. 2009, 33, 21–26.
8. Zipprich, J.; Winter, K.; Hacker, J.; Xia, D.; Watt, J.; Harriman, K. Measles outbreak-California, December 2014–February 2015. Morb. Mortal. Wkly. Rep. 2015, 64, 153–154.
9. He, H.; Chen, E.F.; Li, Q.; Wang, Z.; Yan, R.; Fu, J.; Pan, J. Waning immunity to measles in young adults and booster effects of revaccination in secondary school students. Vaccine 2013, 31, 533–537.
10. Carrillo-Santisteve, P.; Lopalco, P.L. Measles still spreads in Europe: Who is responsible for the failure to vaccinate? Clin. Microbiol. Infect. 2012, 18, 50–56.
11. Poland, G.A.; Jacobson, R.M. The re-emergence of measles in developed countries: Time to develop the next-generation measles vaccines? Vaccine 2012, 30, 103–104.
12. Whitaker, J.A.; Poland, G.A. Measles and mumps outbreaks in the United States: Think globally, vaccinate locally. Vaccine 2014, 32, 4703–4704.
13. Haralambieva, I.H.; Ovsyannikova, I.G.; Pankratz, V.S.; Kennedy, R.B.; Jacobson, R.M.; Poland, G.A. The genetic basis for interindividual immune response variation to measles vaccine: New understanding and new vaccine approaches. Exp. Rev. Vaccines 2013, 12, 57–70.
14. Rosen, J.B.; Rota, J.S.; Hickman, C.J.; Sowers, S.B.; Mercader, S.; Rota, P.A.; Bellini, W.J.; Huang, A.J.; Doll, M.K.; Zucker, J.R., et al. Outbreak of measles among persons with prior evidence of immunity, New York City, 2011. Clin. Infect. Dis. 2014, 58, 1205–1210.
15. De Serres, G.; Boulianne, N.; Defay, F.; Brousseau, N.; Benoit, M.; Lacoursiere, S.; Guillemette, F.; Soto, J.; Ouakki, M.; Ward, B.J., et al. Higher risk of measles when the first dose of a 2-dose schedule of measles vaccine is given at 12–14 months versus 15 months of age. Clin. Infect. Dis. 2012, 55, 394–402.
16. Haralambieva, I.H.; Ovsyannikova, I.G.; O’Byrne, M.; Pankratz, V.S.; Jacobson, R.M.; Poland, G.A. A large observational study to concurrently assess persistence of measles specific B-cell and T-cell immunity in individuals following two doses of MMR vaccine. Vaccine 2011, 29, 4485–4491.
17. Poland, G.A.; Jacobson, R.M.; Thampy, A.M.; Colbourne, S.A.; Wollan, P.C.; Lipsky, J.J.; Jacobson, S.J. Measles re-immunization in children seronegative after initial immunization. JAMA 1997, 277, 1156–1158.
18. Paunio, M.; Peltola, H.; Valle, M.; Davidkin, I.; Virtanen, M.; Heinonen, O.P. Explosive school-based measles outbreak: Intense exposure may have resulted in high risk, even among revaccinees. Am. J. Epidemiol. 1998, 148, 1103–1110.
19. Pannuti, C.S.; Morello, R.J.; Moraes, J.C.; Curti, S.P.; Afonso, A.M.S.; Camargo, M.C.; Souza, V.A. Identification of primary and secondary measles vaccine failures by measurement of immunoglobulin G avidity in measles cases during the 1997 Sao Paulo epidemic. Clin. Diagn. Lab. Immunol. 2004, 11, 119–122.
20. Hickman, C.J.; Hyde, T.B.; Sowers, S.B.; Mercader, S.; McGrew, M.; Williams, N.J.; Beeler, J.A.; Audet, S.; Kiehl, B.; Nandy, R., et al. Laboratory characterization of measles virus infection in previously vaccinated and unvaccinated individuals. J. Infect. Dis. 2011, 204, S549–S558.
21. Glass, K.; Grenfell, B.T. Waning immunity and subclinical measles infections in England. Vaccine 2004, 22, 4110–4116.
22. Mossong, J.; Nokes, D.J.; Edmunds, W.J.; Cox, M.J.; Ratnam, S.; Muller, C.P. Modeling the impact of subclinical measles transmission in vaccinated populations with waning immunity. Am. J. Epidemiol. 1999, 150, 1238–1249.
23. Levin, A.; Burgess, C.; Garrison, L.P., Jr.; Bauch, C.; Babigumira, J.; Simons, E.; Dabbagh, A. Global eradication of measles: An epidemiologic and economic evaluation. J. Infect. Dis. 2011, 204, S98–S106.
24. Haralambieva, I.H.; Ovsyannikova, I.G.; Vierkant, R.A.; Poland, G.A. Development of a novel efficient fluorescence-based plaque reduction microneutralization assay for measles immunity. Clin. Vaccine Immunol. 2008, 15, 1054–1059.
25. Wild, T.F.; Malvoisin, E.; Buckland, R. Measles virus: Both the haemagglutinin and fusion glycoproteins are required for fusion. J. Gen. Virol. 1991, 72, 439–442.
26. Cattaneo, R.; Rose, J.K. Cell fusion by the envelope glycoproteins of persistent measles viruses which caused lethal human brain disease. J. Virol. 1993, 67, 1493–1502.
27. Navaratnarajah, C.K.; Leonard, V.H.; Cattaneo, R. Measles virus glycoprotein complex assembly, receptor attachment, and cell entry. Curr. Top. Microbiol. Immunol. 2009, 329, 59–76.
28. De Swart, R.L.; Yuksel, S.; Osterhaus, A.D. Relative contributions of measles virus hemagglutinin- and fusion protein-specific serum antibodies to virus neutralization. J. Virol. 2005, 79, 11547–11551.
29. De Swart, R.L.; Yuksel, S.; Langerijs, C.N.; Muller, C.P.; Osterhaus, A.D. Depletion of measles virus glycoprotein-specific antibodies from human sera reveals genotype-specific neutralizing antibodies. J. Gen. Virol. 2009, 90, 2982–2989.
30. Patterson, J.B.; Thomas, D.; Lewicki, H.; Billeter, M.A.; Oldstone, M.B. V and C proteins of measles virus function as virulence factors in vivo. Virology 2000, 267, 80–89.
31. McAllister, C.S.; Toth, A.M.; Zhang, P.; Devaux, P.; Cattaneo, R.; Samuel, C.E. Mechanisms of protein kinase PKR-mediated amplification of beta interferon induction by C protein-deficient measles virus. J. Virol. 2010, 84, 380–386.
32. Devaux, P.; Hodge, G.; McChesney, M.B.; Cattaneo, R. Attenuation of V- or C-defective measles viruses: Infection control by the inflammatory and interferon responses of rhesus monkeys. J. Virol. 2008, 82, 5359–5367.
33. Haralambieva, I.H.; Ovsyannikova, I.G.; Dhiman, N.; Vierkant, R.A.; Jacobson, R.M.; Poland, G.A. Differential cellular immune responses to wild-type and attenuated edmonston tag measles virus strains are primarily defined by the viral phosphoprotein gene. J. Med. Virol. 2010, 82, 1966–1975.
34. Takeuchi, K.; Kadota, S.I.; Takeda, M.; Miyajima, N.; Nagata, K. Measles virus V protein blocks interferon (IFN)-alpha/beta but not IFN-gamma signaling by inhibiting STAT1 and STAT2 phosphorylation. FEBS Lett. 2003, 545, 177–182.
35. Tober, C.; Seufert, M.; Schneider, H.; Billeter, M.A.; Johnston, I.C.; Niewiesk, S.; Ter, M.V.; Schneider-Schaulies, S. Expression of measles virus V protein is associated with pathogenicity and control of viral RNA synthesis. J. Virol. 1998, 72, 8124–8132.
36. Davies, D.H.; Liang, X.; Hernandez, J.E.; Randall, A.; Hirst, S.; Mu, Y.; Romero, K.M.; Nguyen, T.T.; Kalantari-Dehaghi, M.; Crotty, S., et al. Profiling the humoral immune response to infection by using proteome microarrays: High-throughput vaccine and diagnostic antigen discovery. Proc. Natl. Acad. Sci. USA 2005, 102, 547–552.
37. Luevano, M.; Bernard, H.U.; Barrera-Saldana, H.A.; Trevino, V.; Garcia-Carranca, A.; Villa, L.L.; Monk, B.J.; Tan, X.; Davies, D.H.; Felgner, P.L., et al. High-throughput profiling of the humoral immune responses against thirteen human papillomavirus types by proteome microarrays. Virology 2010, 405, 31–40.
38. Kalantari-Dehaghi, M.; Chun, S.; Chentoufi, A.A.; Pablo, J.; Liang, L.; Dasgupta, G.; Molina, D.M.; Jasinskas, A.; Nakajima-Sasaki, R.; Felgner, J., et al. Discovery of potential diagnostic and vaccine antigens in herpes simplex virus 1 and 2 by proteome-wide antibody profiling. J. Virol. 2012, 86, 4328–4339.
39. Umlauf, B.J.; Haralambieva, I.H.; Ovsyannikova, I.G.; Kennedy, R.B.; Pankratz, V.S.; Jacobson, R.M.; Poland, G.A. Associations between demographic variables and multiple measles-specific innate and cell-mediated immune responses after measles vaccination. Viral. Immunol. 2012, 25, 29–36.
40. Kennedy, R.B.; Ovsyannikova, I.G.; Haralambieva, I.H.; O’Byrne, M.M.; Jacobson, R.M.; Pankratz, V.S.; Poland, G.A. Multigenic control of measles vaccine immunity mediated by polymorphisms in measles receptor, innate pathway, and cytokine genes. Vaccine 2012, 30, 2159–2167.
41. Taylor, M.J.; Haralambieva, I.H.; Vierkant, R.A.; Ovsyannikova, I.G.; Poland, G.A. Response surface methodology to determine optimal measles-specific cytokine responses in human peripheral blood mononuclear cells. J. Immunol. Methods 2012, 382, 220–223.
42. Ovsyannikova, I.G.; Haralambieva, I.H.; Vierkant, R.A.; O’Byrne, M.M.; Jacobson, R.M.; Poland, G.A. The association of CD46, SLAM, and CD209 cellular receptor gene SNPs with variations in measles vaccine-induced immune responses—A replication study and examination of novel polymorphisms. Hum. Hered. 2011, 72, 206–223.
43. Ovsyannikova, I.G.; Haralambieva, I.H.; Vierkant, R.A.; O’Byrne, M.M.; Jacobson, R.M.; Poland, G.A. Effects of vitamin A and D receptor gene polymophisms/haplotypes on immune responses to measles vaccine. Pharm. Genom. 2012, 22, 20–31.
44. Haralambieva, I.H.; Ovsyannikova, I.G.; Umlauf, B.J.; Vierkant, R.A.; Pankratz, S.V.; Jacobson, R.M.; Poland, G.A. Genetic polymorphisms in host antiviral genes: Associations with humoral and cellular immunity to measles vaccine. Vaccine 2011, 29, 8988–8997.
45. Haralambieva, I.H.; Ovsyannikova, I.G.; Kennedy, R.B.; Vierkant, R.A.; Pankratz, S.V.; Jacobson, R.M.; Poland, G.A. Associations between single nucleotide polymorphisms and haplotypes in cytokine and cytokine receptor genes and immunity to measles vaccination. Vaccine 2011, 29, 7883–7895.
46. Ovsyannikova, I.G.; Haralambieva, I.H.; Vierkant, R.A.; Pankratz, V.S.; Poland, G.A. The role of polymorphisms in toll-like receptors and their associated intracellular signaling genes in measles vaccine immunity. Hum. Genet. 2011, 130, 547–561.
47. Jacobson, R.M.; Ovsyannikova, I.G.; Vierkant, R.A.; Pankratz, V.S.; Poland, G.A. Independence of measles-specific humoral and cellular immune responses to vaccination. Hum. Immunol. 2012, 73, 474–479.
48. Friedman, J.; Hastie, T.; Tibshirani, R. Regularization Paths for Generalized Linear Models via Coordinate Descent. J. Stat. Softw. 2010, 33, 1–22.
49. Team, R.D.C. R: A Language for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2009.
50. Chen, R.T.; Markowitz, L.E.; Albrecht, P.; Stewart, J.A.; Mofenson, L.M.; Preblud, S.R.; Orenstein, W.A. Measles antibody: Reevaluation of protective titers. J. Infect. Dis. 1990, 162, 1036–1042.
51. Albrecht, P.; Herrmann, K.; Burns, G.R. Role of virus strain in conventional and enhanced measles plaque neutralization test. J. Virol. Methods 1981, 3, 251–260.
52. Ratnam, S.; Gadag, V.; West, R.; Burris, J.; Oates, E.; Stead, F.; Bouilianne, N. Comparison of commercial enzyme immunoassay kits with plaque reduction neutralization test for detection of measles virus antibody. J. Clin. Microbiol. 1995, 33, 811–815.
53. Cohen, B.J.; Parry, R.P.; Doblas, D.; Samuel, D.; Warrener, L.; Andrews, N.; Brown, D. Measles immunity testing: Comparison of two measles IgG ELISAs with plaque reduction neutralisation assay. J. Virol. Methods 2006, 131, 209–212.
54. Cohen, B.J.; Audet, S.; Andrews, N.; Beeler, J. Plaque reduction neutralization test for measles antibodies: Description of a standardised laboratory method for use in immunogenicity studies of aerosol vaccination. Vaccine 2007, 26, 59–66.
55. Cohen, B.J.; Parry, R.P.; Andrews, N.; Bennett, A.M.; Dennis, J.H. Laboratory methods for assessing vaccine potency retained in aerosol outputs from nebulizers: Application to World Health Organization measles aerosol project. Vaccine 2008, 26, 3534–3539.
56. Ward, B.J.; Aouchiche, S.; Martel, N.; Bertley, F.M.; Bautista-Lopez, N.; Serhir, B.; Ratnam, S. Measurement of measles virus-specific neutralizing antibodies: Evaluation of the syncytium inhibition assay in comparison with the plaque reduction neutralization test. Diagn. Microbiol. Infect. Dis. 1999, 33, 147–152.
57. Hesketh, L.; Charlett, A.; Farrington, P.; Miller, E.; Forsey, T.; Morgan-Capner, P. An evaluation of nine commercial EIA kits for the detection of measles specific IgG. J. Virol. Methods 1997, 66, 51–59.
58. Bouche, F.B.; Ertl, O.T.; Muller, C.P. Neutralizing B cell response in measles. Viral. Immunol. 2002, 15, 451–471.
59. LeBaron, C.W.; Beeler, J.; Sullivan, B.J.; Forghani, B.; Bi, D.; Beck, C.; Audet, S.; Gargiullo, P. Persistence of measles antibodies after 2 doses of measles vaccine in a postelimination environment. Arch. Pediatr. Adolesc. Med. 2007, 161, 294–301.
60. Cohen, B.J.; Doblas, D.; Andrews, N. Comparison of plaque reduction neutralisation test (PRNT) and measles virus-specific IgG ELISA for assessing immunogenicity of measles vaccination. Vaccine 2008, 26, 6392–6397.
61. Fujino, M.; Yoshida, N.; Kimura, K.; Zhou, J.; Motegi, Y.; Komase, K.; Nakayama, T. Development of a new neutralization test for measles virus. J. Virol. Methods 2007, 142, 15–20.
62. Eick, A.A.; Hu, Z.; Wang, Z.; Nevin, R.L. Incidence of mumps and immunity to measles, mumps and rubella among US military recruits, 2000–2004. Vaccine 2008, 26, 494–501.
63. Hermanson, G.; Chun, S.; Felgner, J.; Tan, X.; Pablo, J.; Nakajima-Sasaki, R.; Molina, D.M.; Felgner, P.L.; Liang, X.; Davies, D.H. Measurement of antibody responses to Modified Vaccinia virus Ankara (MVA) and Dryvax((R)) using proteome microarrays and development of recombinant protein ELISAs. Vaccine 2012, 30, 614–625.
64. Baum, E.; Badu, K.; Molina, D.M.; Liang, X.; Felgner, P.L.; Yan, G. Protein microarray analysis of antibody responses to Plasmodium falciparum in western Kenyan highland sites with differing transmission levels. PLOS ONE 2013, 8, e82246.
65. Kunnath-Velayudhan, S.; Salamon, H.; Wang, H.Y.; Davidow, A.L.; Molina, D.M.; Huynh, V.T.; Cirillo, D.M.; Michel, G.; Talbot, E.A.; Perkins, M.D., et al. Dynamic antibody responses to the Mycobacterium tuberculosis proteome. Proc. Natl. Acad. Sci. USA 2010, 107, 14703–14708.
66. Bouche, F.; Ammerlaan, W.; Berthet, F.; Houard, S.; Schneider, F.; Muller, C.P. Immunosorbent assay based on recombinant hemagglutinin protein produced in a high-efficiency mammalian expression system for surveillance of measles immunity. J. Clin. Microbiol. 1998, 36, 721–726.
67. Bouche, F.; Ammerlaan, W.; Fournier, P.; Schneider, F.; Muller, C.P. A simplified immunoassay based on measles virus recombinant hemagglutinin protein for testing the immune status of vaccinees. J. Virol. Methods 1998, 74, 77–87.
68. Ertl, O.T.; Wenz, D.C.; Bouche, F.B.; Berbers, G.A.; Muller, C.P. Immunodominant domains of the Measles virus hemagglutinin protein eliciting a neutralizing human B cell response. Arch. Virol. 2003, 148, 2195–2206.
69. Moss, W.J.; Griffin, D.E. Global measles elimination. Nat. Rev. Microbiol. 2006, 4, 900–908.
70. Duprex, W.P.; Collins, F.M.; Rima, B.K. Modulating the function of the measles virus RNA-dependent RNA polymerase by insertion of green fluorescent protein into the open reading frame. J. Virol. 2002, 76, 7322–7328.
71. Dochow, M.; Krumm, S.A.; Crowe, J.E., Jr.; Moore, M.L.; Plemper, R.K. Independent structural domains in paramyxovirus polymerase protein. J. Biol. Chem. 2012, 287, 6878–6891.
72. Forthal, D.N.; Landucci, G.; Katz, J.; Tilles, J.G. Comparison of measles virus-specific antibodies with antibody-dependent cellular cytotoxicity and neutralizing functions. J. Infect. Dis. 1993, 168, 1020–1023.
73. Forthal, D.N.; Landucci, G. In vitro reduction of virus infectivity by antibody-dependent cell-mediated immunity. J. Immunol. Methods 1998, 220, 129–138.
74. Atabani, S.; Landucci, G.; Steward, M.W.; Whittle, H.; Tilles, J.G.; Forthal, D.N. Sex-associated differences in the antibody-dependent cellular cytotoxicity antibody response to measles vaccines. Clin. Diagn. Lab. Immunol. 2000, 7, 111–113.