Comparative Analysis of B-Cell Receptor Repertoires Induced by Live Yellow Fever Vaccine in Young and Middle-Age Donors
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30356675
PubMed Central
PMC6189279
DOI
10.3389/fimmu.2018.02309
Knihovny.cz E-zdroje
- Klíčová slova
- age, immunoglobulin repertoire, plasma cell, vaccination, yellow fever,
- MeSH
- aktivní imunita * genetika MeSH
- B-lymfocyty imunologie metabolismus MeSH
- dospělí MeSH
- imunoglobuliny - konstantní oblasti genetika MeSH
- lidé středního věku MeSH
- lidé MeSH
- mladý dospělý MeSH
- protilátky virové imunologie MeSH
- receptory antigenů B-buněk genetika metabolismus MeSH
- somatická hypermutace imunoglobulinových genů MeSH
- těžké řetězce imunoglobulinů genetika MeSH
- vakcína proti žluté zimnici imunologie MeSH
- vakcinace MeSH
- žlutá zimnice prevence a kontrola MeSH
- zvířata MeSH
- Check Tag
- dospělí MeSH
- lidé středního věku MeSH
- lidé MeSH
- mladý dospělý MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- imunoglobuliny - konstantní oblasti MeSH
- protilátky virové MeSH
- receptory antigenů B-buněk MeSH
- těžké řetězce imunoglobulinů MeSH
- vakcína proti žluté zimnici MeSH
Age-related changes can significantly alter the state of adaptive immune system and often lead to attenuated response to novel pathogens and vaccination. In present study we employed 5'RACE UMI-based full length and nearly error-free immunoglobulin profiling to compare plasma cell antibody repertoires in young (19-26 years) and middle-age (45-58 years) individuals vaccinated with a live yellow fever vaccine, modeling a newly encountered pathogen. Our analysis has revealed age-related differences in the responding antibody repertoire ranging from distinct IGH CDR3 repertoire properties to differences in somatic hypermutation intensity and efficiency and antibody lineage tree structure. Overall, our findings suggest that younger individuals respond with a more diverse antibody repertoire and employ a more efficient somatic hypermutation process than elder individuals in response to a newly encountered pathogen.
Adaptive Immunity Group Central European Institute of Technology Brno Czechia
Center of Life Sciences Skolkovo Institute of Science and Technology Moscow Russia
Faculty of Bioengineering and Bioinformatics Lomonosov Moscow State University Moscow Russia
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Castelo-Branco C, Soveral I. The immune system and aging: a review. Gynecol Endocrinol. (2014) 30:16–22. 10.3109/09513590.2013.852531 PubMed DOI
DelaRosa O, Pawelec G, Peralbo E, Wikby A, Mariani E, Mocchegiani E, et al. . Immunological biomarkers of ageing in man: changes in both innate and adaptive immunity are associated with health and longevity. Biogerontology (2006) 7:471–81. 10.1007/s10522-006-9062-6 PubMed DOI
Nikolich-Zugich J. Aging of the T cell compartment in mice and humans: from no naive expectations to foggy memories. J Immunol. (2014) 193:2622–9. 10.4049/jimmunol.1401174 PubMed DOI PMC
Goronzy JJ, Fang F, Cavanagh MM, Qi Q, Weyand CM. Naive T cell maintenance and function in human aging. J Immunol. (2015) 194:4073–80. 10.4049/jimmunol.1500046 PubMed DOI PMC
Britanova OV, Shugay M, Merzlyak EM, Staroverov DB, Putintseva EV, Turchaninova MA, et al. . Dynamics of individual T cell repertoires: from cord blood to centenarians. J Immunol. (2016) 196:5005–13. 10.4049/jimmunol.1600005 PubMed DOI
Gibson KL, Wu YC, Barnett Y, Duggan O, Vaughan R, Kondeatis E, et al. . B-cell diversity decreases in old age and is correlated with poor health status. Aging Cell (2009) 8:18–25. 10.1111/j.1474-9726.2008.00443.x PubMed DOI PMC
Dunn-Walters DK. The ageing human B cell repertoire: a failure of selection? Clin Exp Immunol. (2016) 183:50–6. 10.1111/cei.12700 PubMed DOI PMC
Martin V, Bryan Wu YC, Kipling D, Dunn-Walters D. Ageing of the B-cell repertoire. Philos Trans R Soc Lond B Biol Sci. (2015) 370:20140237. 10.1098/rstb.2014.0237 PubMed DOI PMC
Goodwin K, Viboud C, Simonsen L. Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine (2006) 24:1159–69. 10.1016/j.vaccine.2005.08.105 PubMed DOI
Aspinall R, Del Giudice G, Effros RB, Grubeck-Loebenstein B, Sambhara S. Challenges for vaccination in the elderly. Immun Ageing (2007) 4:9. 10.1186/1742-4933-4-9 PubMed DOI PMC
Frasca D, Diaz A, Romero M, Landin AM, Blomberg BB. Cytomegalovirus (CMV) seropositivity decreases B cell responses to the influenza vaccine. Vaccine (2015) 33:1433–9. 10.1016/j.vaccine.2015.01.071 PubMed DOI PMC
Frasca D, Diaz A, Romero M, Mendez NV, Landin AM, Blomberg BB. Effects of age on H1N1-specific serum IgG1 and IgG3 levels evaluated during the 2011-2012 influenza vaccine season. Immun Age (2013) 10:14. 10.1186/1742-4933-10-14 PubMed DOI PMC
Pinti M, Appay V, Campisi J, Frasca D, Fulop T, Sauce D, et al. . Aging of the immune system: focus on inflammation and vaccination. Eur J Immunol. (2016) 46:2286–301. 10.1002/eji.201546178 PubMed DOI PMC
Park S, Nahm MH. Older adults have a low capacity to opsonize pneumococci due to low IgM antibody response to pneumococcal vaccinations. Infect Immun. (2011) 79:314–20. 10.1128/IAI.00768-10 PubMed DOI PMC
Siegrist CA, Aspinall R. B-cell responses to vaccination at the extremes of age. Nat Rev Immunol. (2009) 9:185–94. 10.1038/nri2508 PubMed DOI
Del Giudice G, Weinberger B, Grubeck-Loebenstein B. Vaccines for the elderly. Gerontology (2015) 61:203–10. 10.1159/000366162 PubMed DOI
Shelly MA, Jacoby H, Riley GJ, Graves BT, Pichichero M, Treanor JJ. Comparison of pneumococcal polysaccharide and CRM197-conjugated pneumococcal oligosaccharide vaccines in young and elderly adults. Infect Immun. (1997) 65:242–7. PubMed PMC
Romero-Steiner S, Musher DM, Cetron MS, Pais LB, Groover JE, Fiore AE, et al. . Reduction in functional antibody activity against Streptococcus pneumoniae in vaccinated elderly individuals highly correlates with decreased IgG antibody avidity. Clin Infect Dis. (1999) 29:281–8. 10.1086/520200 PubMed DOI
Wolters B, Junge U, Dziuba S, Roggendorf M. Immunogenicity of combined hepatitis A and B vaccine in elderly persons. Vaccine (2003) 21:3623–8. 10.1016/S0264-410X(03)00399-2 PubMed DOI
Shi Y, Yamazaki T, Okubo Y, Uehara Y, Sugane K, Agematsu K. Regulation of aged humoral immune defense against pneumococcal bacteria by IgM memory B cell. J Immunol. (2005) 175:3262–7. 10.4049/jimmunol.175.5.3262 PubMed DOI
Kaml M, Weiskirchner I, Keller M, Luft T, Hoster E, Hasford J, et al. . Booster vaccination in the elderly: their success depends on the vaccine type applied earlier in life as well as on pre-vaccination antibody titers. Vaccine (2006) 24:6808–11. 10.1016/j.vaccine.2006.06.037 PubMed DOI
Schenkein JG, Park S, Nahm MH. Pneumococcal vaccination in older adults induces antibodies with low opsonic capacity and reduced antibody potency. Vaccine (2008) 26:5521–6. 10.1016/j.vaccine.2008.07.071 PubMed DOI PMC
Lord JM. The effect of ageing of the immune system on vaccination responses. Hum Vaccin Immunother. (2013) 9:1364–7. 10.4161/hv.24696 PubMed DOI PMC
Vollmers C, Sit RV, Weinstein JA, Dekker CL, Quake SR. Genetic measurement of memory B-cell recall using antibody repertoire sequencing. Proc Natl Acad Sci USA. (2013) 110:13463–8. 10.1073/pnas.1312146110 PubMed DOI PMC
Jiang N, He J, Weinstein JA, Penland L, Sasaki S, He XS, et al. . Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci Transl Med. (2013) 5:171ra119. 10.1126/scitranslmed.3004794 PubMed DOI PMC
Greiff V, Menzel U, Haessler U, Cook SC, Friedensohn S, Khan TA, et al. . Quantitative assessment of the robustness of next-generation sequencing of antibody variable gene repertoires from immunized mice. BMC Immunol. (2014) 15:40. 10.1186/s12865-014-0040-5 PubMed DOI PMC
Laserson U, Vigneault F, Gadala-Maria D, Yaari G, Uduman M, Vander Heiden JA, et al. . High-resolution antibody dynamics of vaccine-induced immune responses. Proc Natl Acad Sci USA. (2014) 111:4928–33. 10.1073/pnas.1323862111 PubMed DOI PMC
Kaplinsky J, Li A, Sun A, Coffre M, Koralov SB, Arnaout R. Antibody repertoire deep sequencing reveals antigen-independent selection in maturing B cells. Proc Natl Acad Sci USA. (2014) 111:E2622–9. 10.1073/pnas.1403278111 PubMed DOI PMC
Georgiou G, Ippolito GC, Beausang J, Busse CE, Wardemann H, Quake SR. The promise and challenge of high-throughput sequencing of the antibody repertoire. Nat Biotechnol. (2014) 32:158–68. 10.1038/nbt.2782 PubMed DOI PMC
Friedensohn S, Khan TA, Reddy ST. Advanced methodologies in high-throughput sequencing of immune repertoires. Trends Biotechnol. (2017) 35:203–14. 10.1016/j.tibtech.2016.09.010 PubMed DOI
Wang C, Liu Y, Xu LT, Jackson KJ, Roskin KM, Pham TD, et al. . Effects of aging, Cytomegalovirus infection, and EBV infection on human B cell repertoires. J Immunol. (2014) 192:603–11. 10.4049/jimmunol.1301384 PubMed DOI PMC
de Bourcy CF, Angel CJ, Vollmers C, Dekker CL, Davis MM, Quake SR. Phylogenetic analysis of the human antibody repertoire reveals quantitative signatures of immune senescence and aging. Proc Natl Acad Sci USA. (2017) 114:1105–10. 10.1073/pnas.1617959114 PubMed DOI PMC
Miles JJ, Silins SL, Brooks AG, Davis JE, Misko I, Burrows SR. T-cell grit: large clonal expansions of virus-specific CD8+ T cells can dominate in the peripheral circulation for at least 18 years. Blood (2005) 106:4412–3. 10.1182/blood-2005-06-2261 PubMed DOI
Fulop T, Larbi A, Pawelec G. Human T cell aging and the impact of persistent viral infections. Front Immunol. (2013) 4:271. 10.3389/fimmu.2013.00271 PubMed DOI PMC
Qi Q, Liu Y, Cheng Y, Glanville J, Zhang D, Lee JY, et al. . Diversity and clonal selection in the human T-cell repertoire. Proc Natl Acad Sci USA. (2014) 111:13139–44. 10.1073/pnas.1409155111 PubMed DOI PMC
Goronzy JJ, Fulbright JW, Crowson CS, Poland GA, O'Fallon WM, Weyand CM. Value of immunological markers in predicting responsiveness to influenza vaccination in elderly individuals. J Virol. (2001) 75:12182–7. 10.1128/JVI.75.24.12182-12187.2001 PubMed DOI PMC
Lavinder JJ, Wine Y, Giesecke C, Ippolito GC, Horton AP, Lungu OI, et al. . Identification and characterization of the constituent human serum antibodies elicited by vaccination. Proc Natl Acad Sci USA. (2014) 111:2259–64. 10.1073/pnas.1317793111 PubMed DOI PMC
Galson JD, Truck J, Fowler A, Clutterbuck EA, Munz M, Cerundolo V, et al. . Analysis of B cell repertoire dynamics following hepatitis B vaccination in humans, and enrichment of vaccine-specific antibody sequences. EBioMedicine (2015) 2:2070–9. 10.1016/j.ebiom.2015.11.034 PubMed DOI PMC
Galson JD, Truck J, Clutterbuck EA, Fowler A, Cerundolo V, Pollard AJ, et al. B-cell repertoire dynamics after sequential hepatitis B vaccination and evidence for cross-reactive B-cell activation. Genome Med. (2016) 8:68 10.1186/s13073-016-0322-z PubMed DOI PMC
Blanchard-Rohner G, Pulickal AS, Jol-van der Zijde CM, Snape MD, Pollard AJ. Appearance of peripheral blood plasma cells and memory B cells in a primary and secondary immune response in humans. Blood (2009) 114:4998–5002. 10.1182/blood-2009-03-211052 PubMed DOI PMC
Jackson KJ, Liu Y, Roskin KM, Glanville J, Hoh RA, Seo K, et al. . Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe (2014) 16:105–14. 10.1016/j.chom.2014.05.013 PubMed DOI PMC
Truck J, Ramasamy MN, Galson JD, Rance R, Parkhill J, Lunter G, et al. . Identification of antigen-specific B cell receptor sequences using public repertoire analysis. J Immunol. (2015) 194:252–61. 10.4049/jimmunol.1401405 PubMed DOI PMC
Wu YC, Kipling D, Dunn-Walters DK. Age-related changes in human peripheral blood IGH repertoire following vaccination. Front Immunol. (2012) 3:193. 10.3389/fimmu.2012.00193 PubMed DOI PMC
Turchaninova MA, Davydov A, Britanova OV, Shugay M, Bikos V, Egorov ES, et al. . High-quality full-length immunoglobulin profiling with unique molecular barcoding. Nat Protoc. (2016) 11:1599–616. 10.1038/nprot.2016.093 PubMed DOI
Shugay M, Britanova OV, Merzlyak EM, Turchaninova MA, Mamedov IZ, Tuganbaev TR, et al. . Towards error-free profiling of immune repertoires. Nat Methods (2014) 11:653–5. 10.1038/nmeth.2960 PubMed DOI
Khan TA, Friedensohn S, de Vries AR, Straszewski J, Ruscheweyh HJ, Reddy ST. Accurate and predictive antibody repertoire profiling by molecular amplification fingerprinting. Sci Adv. (2016) 2:e1501371. 10.1126/sciadv.1501371 PubMed DOI PMC
Shugay M, Zaretsky AR, Shagin DA, Shagina IA, Volchenkov IA, Shelenkov AA, et al. . MAGERI. Computational pipeline for molecular-barcoded targeted resequencing. PLoS Comput Biol. (2017) 13:e1005480. 10.1371/journal.pcbi.1005480 PubMed DOI PMC
Wrammert J, Smith K, Miller J, Langley WA, Kokko K, Larsen C, et al. . Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature (2008) 453:667–71. 10.1038/nature06890 PubMed DOI PMC
Miyazawa S, Jernigan RL. Residue-residue potentials with a favorable contact pair term and an unfavorable high packing density term, for simulation and threading. J Mol Biol. (1996) 256:623–44. 10.1006/jmbi.1996.0114 PubMed DOI
Yaari G, Uduman M, Kleinstein SH. Quantifying selection in high-throughput Immunoglobulin sequencing data sets. Nucleic Acids Res. (2012) 40:e134. 10.1093/nar/gks457 PubMed DOI PMC
Gupta NT, Vander Heiden JA, Uduman M, Gadala-Maria D, Yaari G, Kleinstein SH. Change-O: a toolkit for analyzing large-scale B cell immunoglobulin repertoire sequencing data. Bioinformatics (2015) 31:3356–8. 10.1093/bioinformatics/btv359 PubMed DOI PMC
Egorov ES, Kasatskaya SA, Zubov VN, Izraelson M, Nakonechnaya TO, Staroverov DB, et al. . The changing landscape of naive T cell receptor repertoire with human aging. Front Immunol. (2018) 9:1618. 10.3389/fimmu.2018.01618 PubMed DOI PMC
Shugay M, Bagaev DV, Turchaninova MA, Bolotin DA, Britanova OV, Putintseva EV, et al. . VDJtools: unifying post-analysis of T cell receptor repertoires. PLoS Comput Biol. (2015) 11:e1004503. 10.1371/journal.pcbi.1004503 PubMed DOI PMC
Kidera A, Konishi Y, Oka M. Statistical analysis of the physical properties of the 20 naturally occurring amino acids. J Protein Chem. (1985) 4:23–55. 10.1007/BF01025492 DOI
Rackovsky S. Global characteristics of protein sequences and their implications. Proc Natl Acad Sci USA. (2010) 107:8623–6. 10.1073/pnas.1001299107 PubMed DOI PMC
Peng HP, Lee KH, Jian JW, Yang AS. Origins of specificity and affinity in antibody-protein interactions. Proc Natl Acad Sci USA. (2014) 111:E2656–65. 10.1073/pnas.1401131111 PubMed DOI PMC
Barak M, Zuckerman NS, Edelman H, Unger R, Mehr R. IgTree: creating Immunoglobulin variable region gene lineage trees. J Immunol Methods (2008) 338:67–74. 10.1016/j.jim.2008.06.006 PubMed DOI
Sela-Culang I, Kunik V, Ofran Y. The structural basis of antibody-antigen recognition. Front Immunol. (2013) 4:302. 10.3389/fimmu.2013.00302 PubMed DOI PMC
Laffy JMJ, Dodev T, Macpherson JA, Townsend C, Lu HC, Dunn-Walters D, et al. . Promiscuous antibodies characterised by their physico-chemical properties: from sequence to structure and back. Prog Biophys Mol Biol. (2017) 128:47–56. 10.1016/j.pbiomolbio.2016.09.002 PubMed DOI PMC
Padlan EA. Anatomy of the antibody molecule. Mol Immunol. (1994) 31:169–217. 10.1016/0161-5890(94)90001-9 PubMed DOI
Tas JM, Mesin L, Pasqual G, Targ S, Jacobsen JT, Mano YM, et al. . Visualizing antibody affinity maturation in germinal centers. Science (2016) 351:1048–54. 10.1126/science.aad3439 PubMed DOI PMC
Tabibian-Keissar H, Hazanov L, Schiby G, Rosenthal N, Rakovsky A, Michaeli M, et al. . Aging affects B-cell antigen receptor repertoire diversity in primary and secondary lymphoid tissues. Eur J Immunol. (2016) 46:480–92. 10.1002/eji.201545586 PubMed DOI
Frasca D, Landin AM, Lechner SC, Ryan JG, Schwartz R, Riley RL, et al. . Aging down-regulates the transcription factor E2A, activation-induced cytidine deaminase, and Ig class switch in human B cells. J Immunol. (2008) 180:5283–90. 10.4049/jimmunol.180.8.5283 PubMed DOI
Bulati M, Caruso C, Colonna-Romano G. From lymphopoiesis to plasma cells differentiation, the age-related modifications of B cell compartment are influenced by “inflamm-ageing.” Ageing Res Rev. (2017) 36:125–36. 10.1016/j.arr.2017.04.001 PubMed DOI
Labrie JE III, Borghesi L, Gerstein RM. Bone marrow microenvironmental changes in aged mice compromise V(D)J recombinase activity and B cell generation. Semin Immunol. (2005) 17:347–55. 10.1016/j.smim.2005.05.012 PubMed DOI
Frasca D, Diaz A, Romero M, Landin AM, Blomberg BB. Age effects on B cells and humoral immunity in humans. Ageing Res Rev. (2011) 10:330–5. 10.1016/j.arr.2010.08.004 PubMed DOI PMC
Banerjee M, Mehr R, Belelovsky A, Spencer J, Dunn-Walters DK. Age- and tissue-specific differences in human germinal center B cell selection revealed by analysis of IgVH gene hypermutation and lineage trees. Eur J Immunol. (2002) 32:1947–57. 10.1002/1521-4141(200207)32:7<1947::AID-IMMU1947>3.0.CO;2-1 PubMed DOI
Troutaud D, Drouet M, Decourt C, Le Morvan C, Cogne M. Age-related alterations of somatic hypermutation and CDR3 lengths in human Vkappa4-expressing B lymphocytes. Immunology (1999) 97:197–203. 10.1046/j.1365-2567.1999.00779.x PubMed DOI PMC
Khurana S, Frasca D, Blomberg B, Golding H. AID activity in B cells strongly correlates with polyclonal antibody affinity maturation in-vivo following pandemic 2009-H1N1 vaccination in humans. PLoS Pathog (2012) 8:e1002920. 10.1371/journal.ppat.1002920 PubMed DOI PMC
Frasca D, Diaz A, Romero M, Phillips M, Mendez NV, Landin AM, et al. . Unique biomarkers for B-cell function predict the serum response to pandemic H1N1 influenza vaccine. Int Immunol. (2012) 24:175–82. 10.1093/intimm/dxr123 PubMed DOI PMC
Miyaji KT, Avelino-Silva VI, Simoes M, Freire MD, Medeiros CR, Braga PE, et al. . Prevalence and titers of yellow fever virus neutralizing antibodies in previously vaccinated adults. Rev Inst Med Trop Sao Paulo (2017) 59:e2. 10.1590/s1678-9946201759002 PubMed DOI PMC
Vratskikh O, Stiasny K, Zlatkovic J, Tsouchnikas G, Jarmer J, Karrer U, et al. . Dissection of antibody specificities induced by yellow fever vaccination. PLoS Pathog. (2013) 9:e1003458. 10.1371/journal.ppat.1003458 PubMed DOI PMC
Collaborative group for studies on yellow fever vaccines. Duration of post-vaccination immunity against yellow fever in adults. Vaccine (2014) 32:4977–84. 10.1016/j.vaccine.2014.07.021 PubMed DOI