Loss of multi-epitope specificity in memory CD4+ T cell responses to B. Pertussis with age

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Han, Wanda G H ^a   Van Twillert, Inonge ^a   Poelen, Martien C M ^a   Helm, Kina ^a   Van De Kassteele, Jan ^a   Verheij, Theo J M ^b   Versteegh, Florens G A ^c   Boog, Claire J P ^d   Van Els, Cécile A C M ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c GROENE HART HOSPITAL   (Netherlands)

^d Institute for Translational Vaccinology   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGING; AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORDETELLA PERTUSSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; COHORT STUDIES; CROSS-SECTIONAL STUDIES; CYTOKINES; EPITOPES, T-LYMPHOCYTE; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; PERTUSSIS TOXIN; PERTUSSIS VACCINE; TH1 CELLS; TH2 CELLS; TIME FACTORS; VIRULENCE FACTORS, BORDETELLA; WHOOPING COUGH;

EID: 84894242069     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083583     Document Type: Article

References (51)

1. Crowcroft NS, Pebody RG (2006) Recent developments in pertussis. Lancet 367: 1926-1936. (Pubitemid 43831996)
2. De Serres G, Boulianne N, Douville Fradet M, Duval B (1995) Pertussis in Quebec: ongoing epidemic since the late 1980s. Can Commun Dis Rep 21: 45-48.
3. de Melker HE, Conyn-van Spaendonck MA, Rumke HC, van Wijngaarden JK, Mooi FR, et al. (1997) Pertussis in The Netherlands: an outbreak despite high levels of immunization with whole-cell vaccine. Emerg Infect Dis 3: 175-178. (Pubitemid 127431675)
4. Bass JW, Wittler RR (1994) Return of epidemic pertussis in the United States. Pediatr Infect Dis J 13: 343-345. (Pubitemid 24145675)
5. Andrews R, Herceg A, Roberts C (1997) Pertussis notifications in Australia, 1991 to 1997. Commun Dis Intell 21: 145-148.
6. Guris D, Strebel PM, Bardenheier B, Brennan M, Tachdjian R, et al. (1999) Changing epidemiology of pertussis in the United States: increasing reported incidence among adolescents and adults, 1990-1996. Clin Infect Dis 28: 1230-1237. (Pubitemid 29272795)
7. Gzyl A, Augustynowicz E, Rabczenko D, Gniadek G, Slusarczyk J (2004) Pertussis in Poland. Int J Epidemiol 33: 358-365. (Pubitemid 38578836)
8. Wendelboe AM, Van Rie A, Salmaso S, Englund JA (2005) Duration of immunity against pertussis after natural infection or vaccination. Pediatr Infect Dis J 24: S58-61. (Pubitemid 40676539)
9. Bouchez V, Brun D, Cantinelli T, Dore G, Njamkepo E, et al. (2009) First report and detailed characterization of B. pertussis isolates not expressing Pertussis Toxin or Pertactin. Vaccine 27: 6034-6041.
10. Otsuka N, Han HJ, Toyoizumi-Ajisaka H, Nakamura Y, Arakawa Y, et al. (2012) Prevalence and genetic characterization of pertactin-deficient Bordetella pertussis in Japan. PLoS One 7: e31985.
11. van Gent M, Bart MJ, van der Heide HG, Heuvelman KJ, Mooi FR (2012) Small mutations in Bordetella pertussis are associated with selective sweeps. PLoS One 7: e46407.
12. He Q, Mertsola J (2008) Factors contributing to pertussis resurgence. Future Microbiol 3: 329-339. (Pubitemid 352003143)
13. Cherry JD, Gornbein J, Heininger U, Stehr K (1998) A search for serologic correlates of immunity to Bordetella pertussis cough illnesses. Vaccine 16: 1901-1906. (Pubitemid 28473933)
14. Storsaeter J, Hallander HO, Gustafsson L, Olin P (1998) Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis. Vaccine 16: 1907-1916. (Pubitemid 28473934)
15. Mahon BP, Sheahan BJ, Griffin F, Murphy G, Mills KH (1997) Atypical disease after Bordetella pertussis respiratory infection of mice with targeted disruptions of interferon-gamma receptor or immunoglobulin mu chain genes. J Exp Med 186: 1843-1851. (Pubitemid 27524594)
16. Bruss JB, Siber GR (1999) Protective effects of pertussis immunoglobulin (PIGIV) in the aerosol challenge model. Clin Diagn Lab Immunol 6: 464-470. (Pubitemid 29330724)
17. Leef M, Elkins KL, Barbic J, Shahin RD (2000) Protective immunity to Bordetella pertussis requires both B cells and CD4(+) T cells for key functions other than specific antibody production. J Exp Med 191: 1841-1852. (Pubitemid 30390348)
18. Mills KH (2001) Immunity to Bordetella pertussis. Microbes Infect 3: 655-677.
19. Mahon BP, Brady MT, Mills KH (2000) Protection against Bordetella pertussis in mice in the absence of detectable circulating antibody: implications for longterm immunity in children. J Infect Dis 181: 2087-2091. (Pubitemid 30416182)
20. Redhead K, Watkins J, Barnard A, Mills KH (1993) Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity. Infect Immun 61: 3190-3198. (Pubitemid 23223404)
21. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH (2006) TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17- producing T cells. J Immunol 177: 7980-7989. (Pubitemid 44846315)
22. Ryan M, Murphy G, Ryan E, Nilsson L, Shackley F, et al. (1998) Distinct T-cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology 93: 1-10. (Pubitemid 28133089)
23. Ausiello CM, Urbani F, la Sala A, Lande R, Cassone A (1997) Vaccine- and antigen-dependent type 1 and type 2 cytokine induction after primary vaccination of infants with whole-cell or acellular pertussis vaccines. Infect Immun 65: 2168-2174. (Pubitemid 27237293)
24. Esposito S, Agliardi T, Giammanco A, Faldella G, Cascio A, et al. (2001) Longterm pertussis-specific immunity after primary vaccination with a combined diphtheria, tetanus, tricomponent acellular pertussis, and hepatitis B vaccine in comparison with that after natural infection. Infect Immun 69: 4516-4520. (Pubitemid 32574452)
25. Vermeulen F, Verscheure V, Damis E, Vermeylen D, Leloux G, et al. (2010) Cellular immune responses of preterm infants after vaccination with whole-cell or acellular pertussis vaccines. Clin Vaccine Immunol 17: 258-262.
26. Schulze zur Wiesch J, Lauer GM, Day CL, Kim AY, Ouchi K, et al. (2005) Broad repertoire of the CD4+ Th cell response in spontaneously controlled hepatitis C virus infection includes dominant and highly promiscuous epitopes. J Immunol 175: 3603-3613. (Pubitemid 41292019)
27. Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, et al. (2011) A human memory T cell subset with stem cell-like properties. Nat Med 17: 1290-1297.
28. Sallusto F, Lanzavecchia A (2011) Memory in disguise. Nat Med 17: 1182-1183.
29. Barnard A, Mahon BP, Watkins J, Redhead K, Mills KH (1996) Th1/Th2 cell dichotomy in acquired immunity to Bordetella pertussis: variables in the in vivo priming and in vitro cytokine detection techniques affect the classification of Tcell subsets as Th1, Th2 or Th0. Immunology 87: 372-380.
30. Schure RM, de Rond L, Ozturk K, Hendrikx L, Sanders E, et al. (2012) Pertussis circulation has increased T-cell immunity during childhood more than a second acellular booster vaccination in Dutch children 9 years of age. PLoS One 7: e41928.
31. Schure RM, Hendrikx LH, de Rond LG, Ozturk K, Sanders EA, et al. (2012) T-Cell Responses before and after the Fifth Consecutive Acellular Pertussis Vaccination in 4-Year-Old Dutch Children. Clin Vaccine Immunol 19: 1879-1886.
32. De Magistris MT, Romano M, Bartoloni A, Rappuoli R, Tagliabue A (1989) Human T cell clones define S1 subunit as the most immunogenic moiety of pertussis toxin and determine its epitope map. J Exp Med 169: 1519-1532. (Pubitemid 19126812)
33. Peppoloni S, Nencioni L, Di Tommaso A, Tagliabue A, Parronchi P, et al. (1991) Lymphokine secretion and cytotoxic activity of human CD4+ T-cell clones against Bordetella pertussis. Infect Immun 59: 3768-3773.
34. Carollo M, Palazzo R, Bianco M, Smits K, Mascart F, et al. (2012) Antigen-specific responses assessment for the evaluation of Bordetella pertussis T cell immunity in humans. Vaccine 30: 1667-1674.
35. Moore SM, Wilkerson MJ, Davis RD, Wyatt CR, Briggs DJ (2006) Detection of cellular immunity to rabies antigens in human vaccinees. J Clin Immunol 26: 533-545. (Pubitemid 44764263)
36. Gazagne A, Claret E, Wijdenes J, Yssel H, Bousquet F, et al. (2003) A Fluorospot assay to detect single T lymphocytes simultaneously producing multiple cytokines. J Immunol Methods 283: 91-98. (Pubitemid 37501061)
37. Probst HC, Tschannen K, Gallimore A, Martinic M, Basler M, et al. (2003) Immunodominance of an antiviral cytotoxic T cell response is shaped by the kinetics of viral protein expression. J Immunol 171: 5415-5422. (Pubitemid 37432828)
38. Lazarski CA, Chaves FA, Jenks SA, Wu S, Richards KA, et al. (2005) The kinetic stability of MHC class II:peptide complexes is a key parameter that dictates immunodominance. Immunity 23: 29-40. (Pubitemid 41019655)
39. van Hall T, Wolpert EZ, van Veelen P, Laban S, van der Veer M, et al. (2006) Selective cytotoxic T-lymphocyte targeting of tumor immune escape variants. Nat Med 12: 417-424.
40. Kwok WW, Tan V, Gillette L, Littell CT, Soltis MA, et al. (2012) Frequency of epitope-specific naive CD4(+) T cells correlates with immunodominance in the human memory repertoire. J Immunol 188: 2537-2544.
41. Trautmann L, Rimbert M, Echasserieau K, Saulquin X, Neveu B, et al. (2005) Selection of T cell clones expressing high-affinity public TCRs within Human cytomegalovirus-specific CD8 T cell responses. J Immunol 175: 6123-6132. (Pubitemid 41508100)
42. Mattoo S, Cherry JD (2005) Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 18: 326-382. (Pubitemid 40548297)
43. Hodder SL, Cherry JD, Mortimer Jr EA, Ford AB, Gornbein J, et al. (2000) Antibody responses to Bordetella pertussis antigens and clinical correlations in elderly community residents. Clin Infect Dis 31: 7-14. (Pubitemid 32268930)
44. White OJ, McKenna KL, Bosco A, A HJvdB, Richmond P, et al. (2012) A genomics-based approach to assessment of vaccine safety and immunogenicity in children. Vaccine 30: 1865-1874.
45. Schindowski K, Frohlich L, Maurer K, Muller WE, Eckert A (2002) Age-related impairment of human T lymphocytes' activation: specific differences between CD4(+) and CD8(+) subsets. Mech Ageing Dev 123: 375-390. (Pubitemid 34024925)
46. Sharma SK, Pichichero ME (2012) Functional deficits of pertussis-specific CD4+ T cells in infants compared to adults following DTaP vaccination. Clin Exp Immunol 169: 281-291.
47. Fritsch RD, Shen X, Sims GP, Hathcock KS, Hodes RJ, et al. (2005) Stepwise differentiation of CD4 memory T cells defined by expression of CCR7 and CD27. J Immunol 175: 6489-6497. (Pubitemid 41598891)
48. Hijnen M, van Gageldonk PG, Berbers GA, van Woerkom T, Mooi FR (2005) The Bordetella pertussis virulence factor P.69 pertactin retains its immunological properties after overproduction in Escherichia coli. Protein Expr Purif 41: 106-112. (Pubitemid 40406369)
49. Singh H, Raghava GP (2001) ProPred: prediction of HLA-DR binding sites. Bioinformatics 17: 1236-1237. (Pubitemid 33735355)
50. Greenland S (2006) Bayesian perspectives for epidemiological research: I. Foundations and basic methods. Int J Epidemiol 35: 765-775.
51. Stenger RM, Poelen MC, Moret EE, Kuipers B, Bruijns SC, et al. (2009) Immunodominance in mouse and human CD4+ T-cell responses specific for the Bordetella pertussis virulence factor P.69 pertactin. Infect Immun 77: 896-903.