Characterization of functional antibody and memory B-Cell responses to pH1N1 monovalent vaccine in HIV-infected children and youth

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Curtis, Donna J ^a   Muresan, Petronella ^b   Nachman, Sharon ^c   Fenton, Terence ^b   Richardson, Kelly M ^a   Dominguez, Teresa ^a   Flynn, Patricia M ^d   Spector, Stephen A ^e,f   Cunningham, Coleen K ^g   Bloom, Anthony ^h   Weinberg, Adriana ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f RADY CHILDREN'S HOSPITAL   (United States)

^g DUKE UNIVERSITY MEDICAL CENTER   (United States)

^h FRONTIER SCIENCE AND TECHNOLOGY RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLUENZA VACCINE; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 5; CYTOKINE; VIRUS ANTIBODY;

2009 H1N1 INFLUENZA; ADOLESCENT; ADULT; AGE DISTRIBUTION; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CHILD; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; FEMALE; HEMAGGLUTINATION INHIBITION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; MAJOR CLINICAL STUDY; MALE; MEMORY CELL; OPTICAL DENSITY; PHENOTYPE; PRESCHOOL CHILD; SCHOOL CHILD; TH1 CELL; TH2 CELL; VACCINATION; YOUNG ADULT; CLINICAL TRIAL; HEMAGGLUTINATION INHIBITION TEST; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); METABOLISM;

ADOLESCENT; ADULT; ANTIBODIES, VIRAL; B-LYMPHOCYTE SUBSETS; CHILD; CHILD, PRESCHOOL; CYTOKINES; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HIV INFECTIONS; HUMANS; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; MALE; YOUNG ADULT;

EID: 84925729318     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118567     Document Type: Article

References (50)

1. Fine AD, Bridges CB, De Guzman AM, Glover L, Zeller B, et al. (2001) Influenza A among patients with human immunodeficiency virus: an outbreak of infection at a residential facility in New York City. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 32: 1784-1791.
2. Madhi SA, Ramasamy N, Bessellar TG, Saloojee H, Klugman KP (2002) Lower respiratory tract infections associated with influenza A and B viruses in an area with a high prevalence of pediatric human immunodeficiency type 1 infection. The Pediatric infectious disease journal 21: 291-297. PMID: 120757599
3. Madhi SA, Schoub B, Simmank K, Blackburn N, Klugman KP (2000) Increased burden of respiratory viral associated severe lower respiratory tract infections in children infected with human immunodeficiency virus type-1. The Journal of pediatrics 137: 78-84. PMID: 108918266
4. Chadwick EG, Chang G, Decker MD, Yogev R, Dimichele D, et al. (1994) Serologic response to standard inactivated influenza vaccine in human immunodeficiency virus-infected children. The Pediatric infectious disease journal 13: 206-211. PMID: 81776299
5. Kroon FP, van Dissel JT, de Jong JC, van Furth R (1994) Antibody response to influenza, tetanus and pneumococcal vaccines in HIV-seropositive individuals in relation to the number of CD4+ lymphocytes. AIDS 8: 469-476. PMID: 79120866
6. Miotti PG, Nelson KE, Dallabetta GA, Farzadegan H, Margolick J, et al. (1989) The influence of HIV infection on antibody responses to a two-dose regimen of influenza vaccine. JAMA: the journal of the American Medical Association 262: 779-783. PMID: 27874166
7. King JC Jr, Treanor J, Fast PE, Wolff M, Yan L, et al. (2000) Comparison of the safety, vaccine virus shedding, and immunogenicity of influenza virus vaccine, trivalent, types A and B, live cold-adapted, administered to human immunodeficiency virus (HIV)-infected and non-HIV-infected adults. The Journal of infectious diseases 181: 725-728. PMID: 106693633
8. Levin MJ, Song LY, Fenton T, Nachman S, Patterson J, et al. (2008) Shedding of live vaccine virus, comparative safety, and influenza-specific antibody responses after administration of live attenuated and inactivated trivalent influenza vaccines to HIV-infected children. Vaccine 26: 4210-4217. doi: 10. 1016/j.vaccine.2008.05.054 PMID: 185979000
9. Vigano A, Zuccotti GV, Pacei M, Erba P, Castelletti E, et al. (2008) Humoral and cellular response to influenza vaccine in HIV-infected children with full viroimmunologic response to antiretroviral therapy. J Acquir Immune Defic Syndr 48: 289-296. doi: 10.1097/QAI.0b013e3181632cda PMID: 185451555
10. Pedersen GK, Madhun AS, Breakwell L, Hoschler K, Sjursen H, et al. (2012) T-helper 1 cells elicited by H5N1 vaccination predict seroprotection. J Infect Dis 206: 158- 166. doi: 10.1093/infdis/jis330 PMID: 225518111
11. Eto D, Lao C, DiToro D, Barnett B, Escobar TC, et al. (2011) IL-21 and IL-6 are critical for different aspects of B cell immunity and redundantly induce optimal follicular helper CD4 T cell (Tfh) differentiation. PLoS One 6: e17739. doi: 10.1371/journal.pone.0017739 PMID: 214238099
12. Cubas RA, Mudd JC, Savoye AL, Perreau M, van Grevenynghe J, et al. (2013) Inadequate T follicular cell help impairs B cell immunity during HIV infection. Nature medicine 19: 494-499. doi: 10.1038/nm. 3109 PMID: 234752011
13. Pallikkuth S, Parmigiani A, Silva SY, George VK, Fischl M, et al. (2012) Impaired peripheral blood T-follicular helper cell function in HIV-infected nonresponders to the 2009 H1N1/09 vaccine. Blood 120: 985-993. doi: 10.1182/blood-2011-12-396648 PMID: 226925100
14. Pallikkuth S, Pilakka Kanthikeel S, Silva SY, Fischl M, Pahwa R, et al. (2011) Upregulation of IL-21 receptor on B cells and IL-21 secretion distinguishes novel 2009 H1N1 vaccine responders from nonresponders among HIV-infected persons on combination antiretroviral therapy. Journal of immunology 186: 6173-6181. doi: 10.4049/jimmunol.1100264 PMID: 215318911
15. Moir S, Fauci AS (2009) B cells in HIV infection and disease. Nature reviews Immunology 9: 235-245. doi: 10.1038/nri2524 PMID: 193191422
16. Imbeault M, Ouellet M, Giguere K, Bertin J, Belanger D, et al. (2011) Acquisition of host-derived CD40L by HIV-1 in vivo and its functional consequences in the B-cell compartment. Journal of virology 85: 2189-2200. doi: 10.1128/JVI.01993-10 PMID: 211778033
17. Martin G, Roy J, Barat C, Ouellet M, Gilbert C, et al. (2007) Human immunodeficiency virus type 1-associated CD40 ligand transactivates B lymphocytes and promotes infection of CD4+ T cells. Journal of virology 81: 5872-5881. PMID: 173923622
18. Moir S, Malaspina A, Pickeral OK, Donoghue ET, Vasquez J, et al. (2004) Decreased survival of B cells of HIV-viremic patients mediated by altered expression of receptors of the TNF superfamily. The Journal of experimental medicine 200: 587-599. PMID: 155081844
19. Perise-Barrios AJ, Munoz-Fernandez MA, Pion M (2012) Direct phenotypical and functional dysregulation of primary human B cells by human immunodeficiency virus (HIV) type 1 in vitro. PloS one 7: e39472. doi: 10.1371/journal.pone.0039472 PMID: 227683022
20. Qiao X, He B, Chiu A, Knowles DM, Chadburn A, et al. (2006) Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nature immunology 7: 302-310. PMID: 164291388
21. Viau M, Veas F, Zouali M (2007) Direct impact of inactivated HIV-1 virions on B lymphocyte subsets. Molecular immunology 44: 2124-2134. PMID: 171347577
22. Rappocciolo G, Piazza P, Fuller CL, Reinhart TA, Watkins SC, et al. (2006) DC-SIGN on B lymphocytes is required for transmission of HIV-1 to T lymphocytes. PLoS Pathog 2: e70. PMID: 168392011
23. Moir S, Ho J, Malaspina A, Wang W, DiPoto AC, et al. (2008) Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. The Journal of experimental medicine 205: 1797-1805. doi: 10.1084/jem.20072683 PMID: 186257477
24. Pensieroso S, Galli L, Nozza S, Ruffin N, Castagna A, et al. (2013) B-cell subset alterations and correlated factors in HIV-1 infection. AIDS 27: 1209-1217. doi: 10.1097/QAD.0b013e32835edc47 PMID: 233439111
25. Titanji K, De Milito A, Cagigi A, Thorstensson R, Grutzmeier S, et al. (2006) Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 108: 1580-1587. PMID: 166451699
26. Fontaine J, Chagnon-Choquet J, Valcke HS, Poudrier J, Roger M (2011) High expression levels of B lymphocyte stimulator (BLyS) by dendritic cells correlate with HIV-related B-cell disease progression in humans. Blood 117: 145-155. doi: 10.1182/blood-2010-08-301887 PMID: 208709011
27. Hart M, Steel A, Clark SA, Moyle G, Nelson M, et al. (2007) Loss of discrete memory B cell subsets is associated with impaired immunization responses in HIV-1 infection and may be a risk factor for invasive pneumococcal disease. Journal of immunology 178: 8212-8220. PMID: 175486600
28. Ho J, Moir S, Malaspina A, Howell ML, Wang W, et al. (2006) Two overrepresented B cell populations in HIV-infected individuals undergo apoptosis by different mechanisms. Proceedings of the National Academy of Sciences of the United States of America 103: 19436-19441. PMID: 171587966
29. Swingler S, Brichacek B, Jacque JM, Ulich C, Zhou J, et al. (2003) HIV-1 Nef intersects the macrophage CD40L signalling pathway to promote resting-cell infection. Nature 424: 213-219. PMID: 128539622
30. Jacobsen MC, Thiebaut R, Fisher C, Sefe D, Clapson M, et al. (2008) Pediatric human immunodeficiency virus infection and circulating IgD+ memory B cells. The Journal of infectious diseases 198: 481-485. doi: 10.1086/590215 PMID: 185822000
31. Levesque MC, Moody MA, Hwang KK, Marshall DJ, Whitesides JF, et al. (2009) Polyclonal B cell differentiation and loss of gastrointestinal tract germinal centers in the earliest stages of HIV-1 infection. PLoS medicine 6: e1000107. doi: 10.1371/journal.pmed.1000107 PMID: 195821666
32. Flynn PM, Nachman S, Muresan P, Fenton T, Spector SA, et al. (2012) Safety and immunogenicity of 2009 pandemic H1N1 influenza vaccination in perinatally HIV-1-infected children, adolescents, and young adults. J Infect Dis 206: 421-430. doi: 10.1093/infdis/jis360 PMID: 226153111
33. Weinberg A, Muresan P, Fenton T, Richardson K, Dominguez T, et al. (2013) High proportions of regulatory B and T cells are associated with decreased cellular responses to pH1N1 influenza vaccine in HIV-infected children and youth (IMPAACT P1088). Hum Vaccin Immunother 9: 957-968. doi: 10. 4161/hv.23774 PMID: 233702811
34. Rowe T, Abernathy RA, Hu-Primmer J, Thompson WW, Lu X, et al. (1999) Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol 37: 937-943. PMID: 100745055
35. Hancock K (2011) Influenza Virus Microneutralization Assay. In: Immunology and Pathogenesis Branch ID, editor: Department of Health and Human Services, Centers for Disease Control and Prevention. pp. 1-32..
36. Hedman K, Rousseau SA (1989) Measurement of avidity of specific IgG for verification of recent primary rubella. J Med Virol 27: 288-292. PMID: 27236155
37. Weinberg A, Song LY, Walker R, Allende M, Fenton T, et al. (2010) Anti-influenza serum and mucosal antibody responses after administration of live attenuated or inactivated influenza vaccines to HIV-infected children. J Acquir Immune Defic Syndr 55: 189-196. doi: 10.1097/QAI.0b013e3181e46308 PMID: 205816900
38. Ho J, Moir S, Wang W, Posada JG, Gu W, et al. (2011) Enhancing effects of adjuvanted 2009 pandemic H1N1 influenza A vaccine on memory B-cell responses in HIV-infected individuals. AIDS 25: 295-302. doi: 10.1097/QAD.0b013e328342328b PMID: 211572977
39. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, et al. (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325: 197-201. doi: 10.1126/science.1176225 PMID: 194656833
40. Jegaskanda S, Laurie KL, Amarasena TH, Winnall WR, Kramski M, et al. (2013) Age-associated crossreactive antibody-dependent cellular cytotoxicity toward 2009 pandemic influenza A virus subtype H1N1. The Journal of infectious diseases 208: 1051-1061. doi: 10.1093/infdis/jit294 PMID: 238122388
41. Laurie KL, Carolan LA, Middleton D, Lowther S, Kelso A, et al. (2010) Multiple infections with seasonal influenza A virus induce cross-protective immunity against A(H1N1) pandemic influenza virus in a ferret model. The Journal of infectious diseases 202: 1011-1020. doi: 10.1086/656188 PMID: 207159300
42. Lee VJ, Tay JK, Chen MI, Phoon MC, Xie ML, et al. (2010) Inactivated trivalent seasonal influenza vaccine induces limited cross-reactive neutralizing antibody responses against 2009 pandemic and 1934 PR8 H1N1 strains. Vaccine 28: 6852-6857. doi: 10.1016/j.vaccine.2010.08.031 PMID: 207236266
43. Fang Y, Banner D, Kelvin AA, Huang SS, Paige CJ, et al. (2012) Seasonal H1N1 influenza virus infection induces cross-protective pandemic H1N1 virus immunity through a CD8-independent, B cell-dependent mechanism. J Virol 86: 2229-2238. doi: 10.1128/JVI.05540-11 PMID: 221305400
44. Marcelin G, Bland HM, Negovetich NJ, Sandbulte MR, Ellebedy AH, et al. (2010) Inactivated seasonal influenza vaccines increase serum antibodies to the neuraminidase of pandemic influenza A(H1N1) 2009 virus in an age-dependent manner. J Infect Dis 202: 1634-1638. doi: 10.1086/657084 PMID: 209794544
45. Qiu C, Huang Y, Wang Q, Tian D, Zhang W, et al. (2012) Boosting heterosubtypic neutralization antibodies in recipients of 2009 pandemic H1N1 influenza vaccine. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 54: 17-24. doi: 10.1093/cid/cir753 PMID: 220528877
46. Miller MS, Gardner TJ, Krammer F, Aguado LC, Tortorella D, et al. (2013) Neutralizing antibodies against previously encountered influenza virus strains increase over time: a longitudinal analysis. Science translational medicine 5: 198ra107. doi: 10.1126/scitranslmed.3006637 PMID: 239461966
47. Bodewes R, Fraaij PL, Kreijtz JH, Geelhoed-Mieras MM, Fouchier RA, et al. (2012) Annual influenza vaccination affects the development of heterosubtypic immunity. Vaccine 30: 7407-7410. doi: 10. 1016/j.vaccine.2012.04.086 PMID: 226432177
48. Khurana S, Verma N, Talaat KR, Karron RA, Golding H (2012) Immune response following H1N1pdm09 vaccination: differences in antibody repertoire and avidity in young adults and elderly populations stratified by age and gender. J Infect Dis 205: 610-620. doi: 10.1093/infdis/jir791 PMID: 222076499
49. Verma N, Dimitrova M, Carter DM, Crevar CJ, Ross TM, et al. (2012) Influenza virus H1N1pdm09 infections in the young and old: evidence of greater antibody diversity and affinity for the hemagglutinin globular head domain (HA1 Domain) in the elderly than in young adults and children. J Virol 86: 5515-5522. doi: 10.1128/JVI.07085-11 PMID: 223790977
50. Richardson K, Weinberg A (2011) Reduced immunogenicity of influenza vaccines in HIV-infected compared with uninfected pregnant women is associated with regulatory T cells. AIDS 25: 595-602. doi: 10.1097/QAD.0b013e32834411a8 PMID: 213685900