Ex vivo peptide-MHC II tetramer analysis reveals distinct end-differentiation patterns of human pertussis-specific CD4+ T cells following clinical infection

Clinical Immunology

Volumn 157, Issue 2, 2015, Pages 205-215

  Han, Wanda G H ^a   Helm, Kina ^a   Poelen, Martien M C ^a   Otten, Henny G ^b   van Els, Cécile A C M ^a  

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

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

CD4; CD4 memory differentiation; Peptide MHC class II tetramers; Pertussis; T cell clone; T cell epitope

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TETRAMER; TUMOR NECROSIS FACTOR ALPHA; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY; BORDETELLA VIRULENCE FACTOR; EPITOPE; HLA DRB1 ANTIGEN; HLA-DRB4*01:01 ANTIGEN; OUTER MEMBRANE PROTEIN; PERTACTIN; PERTUSSIS TOXIN;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CHILD; CLINICAL ARTICLE; CYTOKINE RELEASE; EX VIVO STUDY; HLA TYPING; HUMAN; IMMUNOLOGICAL MEMORY; MEMORY T LYMPHOCYTE; MIDDLE AGED; PERTUSSIS; PRESCHOOL CHILD; PRIORITY JOURNAL; ADOLESCENT; AGED; BORDETELLA PERTUSSIS; FEMALE; IMMUNOLOGY; MALE; MONONUCLEAR CELL; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORDETELLA PERTUSSIS; CD4-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; EPITOPES, T-LYMPHOCYTE; FEMALE; HLA-DRB1 CHAINS; HUMANS; IMMUNOLOGIC MEMORY; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; PERTUSSIS TOXIN; VIRULENCE FACTORS, BORDETELLA; WHOOPING COUGH; YOUNG ADULT;

EID: 84924586021     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.02.009     Document Type: Article

References (45)

1. Crowcroft N.S., Pebody R.G. Recent developments in pertussis. Lancet 2006, 367(9526):1926-1936.
2. De Serres G., et al. Pertussis in Quebec: ongoing epidemic since the late 1980s. Can. Commun. Dis. Rep. 1995, 21(5):45-48.
3. de Melker H.E., et al. Pertussis in The Netherlands: an outbreak despite high levels of immunization with whole-cell vaccine. Emerg. Infect. Dis. 1997, 3(2):175-178.
4. Bass J.W., Wittler R.R. Return of epidemic pertussis in the United States. Pediatr. Infect. Dis. J. 1994, 13(5):343-345.
5. Andrews R., Herceg A., Roberts C. Pertussis notifications in Australia, 1991 to 1997. Commun. Dis. Intell. 1997, 21(11):145-148.
6. Guris D., et al. Changing epidemiology of pertussis in the United States: increasing reported incidence among adolescents and adults, 1990-1996. Clin. Infect. Dis. 1999, 28(6):1230-1237.
7. Gzyl A., et al. Pertussis in Poland. Int. J. Epidemiol. 2004, 33(2):358-365.
8. Leef M., et al. Protective immunity to Bordetella pertussis requires both B cells and CD4(+) T cells for key functions other than specific antibody production. J. Exp. Med. 2000, 191(11):1841-1852.
9. Ryan M., et al. Bordetella pertussis respiratory infection in children is associated with preferential activation of type 1 T helper cells. J. Infect. Dis. 1997, 175(5):1246-1250.
10. Ross P.J., et al. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS Pathog. 2013, 9(4):e1003264.
11. Vermeulen F., et al. Cellular immune responses of preterm infants after vaccination with whole-cell or acellular pertussis vaccines. Clin. Vaccine Immunol. 2010, 17(2):258-262.
12. Wendelboe A.M., et al. Duration of immunity against pertussis after natural infection or vaccination. Pediatr. Infect. Dis. J. 2005, 24(5 Suppl):S58-S61.
13. Gattinoni L., et al. A human memory T cell subset with stem cell-like properties. Nat. Med. 2011, 17(10):1290-1297.
14. Sallusto F., et al. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999, 401(6754):708-712.
15. Appay V., et al. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 2008, 73(11):975-983.
16. Harari A., Vallelian F., Pantaleo G. Phenotypic heterogeneity of antigen-specific CD4 T cells under different conditions of antigen persistence and antigen load. Eur. J. Immunol. 2004, 34(12):3525-3533.
17. Seder R.A., Darrah P.A., Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 2008, 8(4):247-258.
18. Smits K., et al. Different T cell memory in preadolescents after whole-cell or acellular pertussis vaccination. Vaccine 2013, 32(1):111-118.
19. Sharma S.K., Pichichero M.E. Functional deficits of pertussis-specific CD4+ T cells in infants compared to adults following DTaP vaccination. Clin. Exp. Immunol. 2012, 169(3):281-291.
20. Schure R.M., et al. Pertussis circulation has increased T-cell immunity during childhood more than a second acellular booster vaccination in Dutch children 9years of age. PLoS One 2012, 7(7):e41928.
21. Novak E.J., et al. MHC class II tetramers identify peptide-specific human CD4(+) T cells proliferating in response to influenza A antigen. J. Clin. Invest. 1999, 104(12):R63-R67.
22. Nepom G.T. MHC class II tetramers. J. Immunol. 2012, 188(6):2477-2482.
23. Stenger R.M., et al. Immunodominance in mouse and human CD4+ T-cell responses specific for the Bordetella pertussis virulence factor P.69 pertactin. Infect. Immun. 2009, 77(2):896-903.
24. Han W.G., et al. Loss of multi-epitope specificity in memory CD4(+) T cell responses to B. pertussis with age. PLoS One 2013, 8(12):e83583.
25. Hijnen M., et al. The Bordetella pertussis virulence factor P.69 pertactin retains its immunological properties after overproduction in Escherichia coli. Protein Expr. Purif. 2005, 41(1):106-112.
26. Lissina A., et al. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J. Immunol. Methods 2009, 340(1):11-24.
27. van Twillert I., et al. Age related differences in dynamics of specific memory B cell populations after clinical pertussis infection. PLoS One 2014, 9(1):e85227.
28. de Greeff S.C., et al. Seroprevalence of pertussis in The Netherlands: evidence for increased circulation of Bordetella pertussis. PLoS One 2010, 5(12):e14183.
29. James E.A., et al. Yellow fever vaccination elicits broad functional CD4+ T cell responses that recognize structural and nonstructural proteins. J. Virol. 2013, 87(23):12794-12804.
30. Danke N.A., Kwok W.W. HLA class II-restricted CD4+ T cell responses directed against influenza viral antigens postinfluenza vaccination. J. Immunol. 2003, 171(6):3163-3169.
31. Day C.L., et al. Ex vivo analysis of human memory CD4 T cells specific for hepatitis C virus using MHC class II tetramers. J. Clin. Invest. 2003, 112(6):831-842.
32. Lucas M., et al. Tracking virus-specific CD4+ T cells during and after acute hepatitis C virus infection. PLoS One 2007, 2(7):e649.
33. Scriba T.J., et al. HIV-1-specific CD4+ T lymphocyte turnover and activation increase upon viral rebound. J. Clin. Invest. 2005, 115(2):443-450.
34. Vingert B., et al. HIV controllers maintain a population of highly efficient Th1 effector cells in contrast to patients treated in the long term. J. Virol. 2012, 86(19):10661-10674.
35. Long H.M., et al. MHC II tetramers visualize human CD4+ T cell responses to Epstein-Barr virus infection and demonstrate atypical kinetics of the nuclear antigen EBNA1 response. J. Exp. Med. 2013, 210(5):933-949.
36. Bronke C., et al. Direct ex vivo detection of HLA-DR3-restricted cytomegalovirus- and Mycobacterium tuberculosis-specific CD4+ T cells. Hum. Immunol. 2005, 66(9):950-961.
37. Meyer A.L., et al. Direct enumeration of Borrelia-reactive CD4 T cells ex vivo by using MHC class II tetramers. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(21):11433-11438.
38. Kannian P., et al. Decline in the frequencies of Borrelia burgdorferi OspA161 175-specific T cells after antibiotic therapy in HLA-DRB1*0401-positive patients with antibiotic-responsive or antibiotic-refractory lyme arthritis. J. Immunol. 2007, 179(9):6336-6342.
39. James E.A., et al. Tetramer-guided epitope mapping reveals broad, individualized repertoires of tetanus toxin-specific CD4+ T cells and suggests HLA-based differences in epitope recognition. Int. Immunol. 2007, 19(11):1291-1301.
40. Lanzavecchia A., Sallusto F. Progressive differentiation and selection of the fittest in the immune response. Nat. Rev. Immunol. 2002, 2(12):982-987.
41. Fulop T., Larbi A., Pawelec G. Human T cell aging and the impact of persistent viral infections. Front. Immunol. 2013, 4:271.
42. Klein N.P., et al. Comparative effectiveness of acellular versus whole-cell pertussis vaccines in teenagers. Pediatrics 2013, 131(6):e1716-e1722.
43. Sheridan S.L., et al. Number and order of whole cell pertussis vaccines in infancy and disease protection. JAMA 2012, 308(5):454-456.
44. Schure R.M., et al. T-cell responses before and after the fifth consecutive acellular pertussis vaccination in 4-year-old Dutch children. Clin. Vaccine Immunol. 2012, 19(11):1879-1886.
45. Andersen R.S., et al. Parallel detection of antigen-specific T cell responses by combinatorial encoding of MHC multimers. Nat. Protoc. 2012, 7(5):891-902.