Aging affects B-cell antigen receptor repertoire diversity in primary and secondary lymphoid tissues

European Journal of Immunology

Volumn 46, Issue 2, 2016, Pages 480-492

  Tabibian Keissar, Hilla ^a,b   Hazanov, Lena ^a   Schiby, Ginette ^b,c   Rosenthal, Noemie ^a   Rakovsky, Aviya ^a   Michaeli, Miri ^a   Shahaf, Gitit Lavy ^a   Pickman, Yishai ^a   Rosenblatt, Kinneret ^b   Melamed, Doron ^d   Dunn Walters, Deborah ^e   Mehr, Ramit ^a   Barshack, Iris ^b,c  

^a BAR ILAN UNIVERSITY   (Israel)

^b SHEBA MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Aging; B cells; Bone marrow; Immunoglobulin repertoire; Secondary lymphoid tissues

Indexed keywords

B CELL ANTIGEN RECEPTOR; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LYMPHOCYTE ANTIGEN RECEPTOR; UNCLASSIFIED DRUG;

ADULT; AGED; AGING; ARTICLE; BONE MARROW; CONTROLLED STUDY; FEMALE; HIGH THROUGHPUT SEQUENCING; HOMEOSTASIS; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; LYMPH NODE; LYMPHOID TISSUE; MALE; MEMORY CELL; PRIMARY LYMPHOID TISSUE; PRIORITY JOURNAL; RECEPTOR AFFINITY; SECONDARY LYMPHOID TISSUE; SOMATIC HYPERMUTATION; SPLEEN; VERY ELDERLY; YOUNG ADULT; ADOLESCENT; ANTIBODY SPECIFICITY; B LYMPHOCYTE; CELL CULTURE; GENETICS; IMMUNOLOGY; MIDDLE AGED; PHYSIOLOGY;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; ANTIBODY DIVERSITY; B-LYMPHOCYTES; BONE MARROW; CELLS, CULTURED; FEMALE; HUMANS; LYMPHOID TISSUE; MALE; MIDDLE AGED; RECEPTORS, ANTIGEN, B-CELL; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; YOUNG ADULT;

EID: 84956906071     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545586     Document Type: Article

References (47)

1. Dunn-Walters, D. K. and Ademokun, A., B cell repertoire and ageing. Curr. Opin. Immunol. 2010. 22: 514-520.
2. Gibson, K. L., Wu, Y.-C., Barnett, Y., Duggan, O., Vaughan, R., Kondeatis, E., Nilsson, B.-O. et al., B-cell diversity decreases in old age and is correlated with poor health status. Aging Cell. 2009. 8: 18-25.
3. Siegrist, C.-A. and Aspinall, R., B-cell responses to vaccination at the extremes of age. Nat. Rev. Immunol. 2009. 9: 185-194.
4. Caruso, C., Buffa, S., Candore, G., Colonna-Romano, G., Dunn-Walters, D. K., Kipling, D. and Pawelec, G., Mechanisms of immunosenescence. Immun. Ageing I A. 2009. 6: 10.
5. Kogut, I., Scholz, J. L., Cancro, M. P. and Cambier, J. C., B cell maintenance and function in aging. Semin. Immunol. 2012. 24: 342-349.
6. Frasca, D., Diaz, A., Romero, M., Landin, A. M., Phillips, M., Lechner, S. C., Ryan, J. G. et al., Intrinsic defects in B cell response to seasonal influenza vaccination in elderly humans. Vaccine 2010. 28: 8077-8084.
7. Goodwin, K., Viboud, C. and Simonsen, L., Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine 2006. 24: 1159-1169.
8. Ademokun, A., Wu, Y.-C. and Dunn-Walters, D. K., The ageing B cell population: composition and function. Biogerontology 2010. 11: 125-137.
9. Calame, KL. Plasma cells: finding new light at the end of B cell development. Nat. Immunol. 2001. 2: 1103-1108.
10. Aberle, J. H., Stiasny, K., Kundi, M. and Heinz, F. X., Mechanistic insights into the impairment of memory B cells and antibody production in the elderly. Age (Dordr). 2013. 35: 371-381.
11. Banerjee, M., Sanderson, J. D., Spencer, J. and Dunn-Walters, D. K., Immunohistochemical analysis of ageing human B and T cell populations reveals an age-related decline of CD8 T cells in spleen but not gut-associated lymphoid tissue (GALT). Mech. Ageing Dev. 2000. 115: 85-99.
12. Weiskopf, D., Weinberger, B. and Grubeck-Loebenstein, B., The aging of the immune system. Transpl. Int. 2009. 22: 1041-1050.
13. Boraschi, D., Del Giudice, G., Dutel, C., Ivanoff, B., Rappuoli, R. and Grubeck-Loebenstein, B., Ageing and immunity: addressing immune senescence to ensure healthy ageing. Vaccine. 2010. 28: 3627-31.
14. Lazuardi, L., Jenewein, B., Wolf, A. M., Pfister, G., Tzankov, A. and Grubeck-Loebenstein, B., Age-related loss of naïve T cells and dysregulation of T-cell/B-cell interactions in human lymph nodes. Immunology 2005. 114: 37-43.
15. Luscieti, P., Hubschmid, T., Cottier, H., Hess, M. W. and Sobin, L. H., Human lymph node morphology as a function of age and site. J. Clin. Pathol. 1980. 33: 454-461.
16. Howard, W. A., Gibson, K. L. and Dunn-Walters, D. K., Antibody quality in old age. Rejuvenation Res. 2006. 9: 117-125.
17. Monroe, J. G. and Dorshkind, K., Fate decisions regulating bone marrow and peripheral B lymphocyte development. Adv. Immunol. 2007. 95: 1-50.
18. Cancro, M. P., Hao, Y., Scholz, J. L., Riley, R. L., Frasca, D., Dunn-Walters, D. K. and Blomberg, B. B., B cells and aging: molecules and mechanisms. Trends Immunol. 2009. 30: 313-318.
19. Wu, Y.-C. B., Kipling, D. and Dunn-Walters, D. K., Age-related changes in human peripheral blood igh repertoire following vaccination. Front. Immunol. 2012. 3: 193.
20. Shahaf, G., Barak, M., Zuckerman, N. S., Swerdlin, N., Gorfine, M. and Mehr, R., Antigen-driven selection in germinal centers as reflected by the shape characteristics of immunoglobulin gene lineage trees: a large-scale simulation study. J. Theor. Biol. 2008. 255: 210-222.
21. Keren, Z., Naor, S., Nussbaum, S., Golan, K., Itkin, T., Sasaki, Y., Schmidt-Supprian, M. et al., B-cell depletion reactivates B lymphopoiesis in the BM and rejuvenates the B lineage in aging. Blood 2011. 117: 3104-3112.
22. Mehr, R. and Melamed, D., Reversing B cell aging. Aging (Albany. NY). 2011. 3: 438-443.
23. Melamed, D. and Scott, D. W., Aging and neoteny in the B lineage. Blood 2012. 120: 4143-4149.
24. Birjandi, S. Z., Ippolito, J. A., Ramadorai, A. K. and Witte, P. L., Alterations in marginal zone macrophages and marginal zone B cells in old mice. J. Immunol. 2011. 186: 3441-3451.
25. Lossos, I. S., Tibshirani, R., Narasimhan, B. and Levy, R., The inference of antigen selection on Ig genes. J. Immunol. 2000. 165: 5122-5126.
26. Spencer, J. and Dunn-Walters, D. K., Hypermutation at A-T base pairs: the A nucleotide replacement spectrum is affected by adjacent nucleotides and there is no reverse complementarity of sequences flanking mutated A and T nucleotides. J. Immunol. 2005. 175: 5170-5177.
27. Matsuda, F., Shin, E. K., Nagaoka, H., Matsumura, R., Haino, M., Fukita, Y., Taka-ishi, S. et al., Structure and physical map of 64 variable segments in the 3'0.8-megabase region of the human immunoglobulin heavy-chain locus. Nat Genet. 1993. 3: 88-94.
28. Wu, Y.-C., Kipling, D., Leong, H. S., Martin, V., Ademokun, A. and Dunn-Walters, D. K., High-throughput immunoglobulin repertoire analysis distinguishes between human IgM memory and switched memory B-cell populations. Blood 2010. 116: 1070-1078.
29. Kolar, G. R., Mehta, D., Wilson, P. C. and Capra, J. D., Diversity of the Ig repertoire is maintained with age in spite of reduced germinal centre cells in human tonsil lymphoid tissue. Scand. J. Immunol. 2006. 64: 314-324.
30. Kolar, G. R. and Capra, J. D., The NOD/SCID chimeric mouse model of human B cell development: studies on the VH4 family immunoglobulin repertoire and implications for SLE. Lupus 2003. 12: 158-162.
31. Tabibian-Keissar, H., Schibby, G., Michaeli, M., Rakovsky-Shapira, A., Azogui-Rosenthal, N., Dunn-Walters, D. K., Rosenblatt, K. et al., PCR amplification and high throughput sequencing of immunoglobulin heavy chain genes from formalin-fixed paraffin-embedded human biopsies. Exp. Mol. Pathol. 2013.94:182-187.
32. Tabibian-Keissar, H., Zuckerman, N. S., Barak, M., Dunn-Walters, D. K., Steiman-Shimony, A., Chowers, Y., Ofek, E. et al., B-cell clonal diversification and gut-lymph node trafficking in ulcerative colitis revealed using lineage tree analysis. Eur. J. Immunol. 2008.38:2600-2609.
33. Michaeli, M., Noga, H., Tabibian-Keissar, H., Barshack, I. and Mehr, R., Automated cleaning and pre-processing of immunoglobulin gene sequences from high-throughput sequencing. Front. B cell Biol. 2012.3:386
34. Huse, S. M., Huber, J. A., Morrison, H. G., Sogin, M. L. and Welch, D. M., Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 2007. 8: R143-R151.
35. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J. et al., Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005. 437: 376-380.
36. Volpe, J. M., Cowell, L. G. and Kepler, T. B., SoDA: implementation of a 3D alignment algorithm for inference of antigen receptor recombinations. Bioinformatics 2006. 22: 438-444.
37. Giudicelli, V., Chaume, D. and Lefranc, M.-P. IMGT/V-QUEST, an integrated software program for immunoglobulin and T cell receptor V-J and V-D-J rearrangement analysis. Nucleic Acids Res. 2004. 32(Web Server issue):W435-W440.
38. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F. et al., Clustal W and Clustal X version 2.0. Bioinformatics 2007. 23: 2947-2948.
39. Michaeli, M., Barak, M., Hazanov, L., Noga, H. and Mehr, R., Automated analysis of immunoglobulin genes from high-throughput sequencing: life without a template. J. Clin, Bioinformat. 2013. 3: 15.
40. Chao, A. and Shen, T. J., Program SPADE (Species Prediction and Diversity Estimation). Progr. User's Guid. available http//chao.stat.nthu.edu.tw. 2003.
41. Michaeli, M., Tabibian-Keissar, H., Schiby, G., Shahaf, G., Pickman, Y., Hazanov, L., Rosenblatt, K. et al., Immunoglobulin gene repertoire diversification and selection in the stomach - from gastritis to gastric lymphomas. Front. Immunol. 2014. 5: 264.
42. Barak, M., Zuckerman, N. S., Edelman, H., Unger, R. and Mehr, R., IgTree: creating Immunoglobulin variable region gene lineage trees. J. Immunol. Methods 2008. 338: 67-74.
43. Zuckerman, N. S., McCann, K. J., Ottensmeier, C. H., Barak, M., Shahaf, Gitit, Edelman, H., Dunn-Walters, D. K. et al., Ig gene diversification and selection in follicular lymphoma, diffuse large B cell lymphoma and primary central nervous system lymphoma revealed by lineage tree and mutation analyses. Int. Immunol. 2010. 22: 875-887.
44. Benjamini, Y. and Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B Met. 1995. 57: 289-300.
45. Zhou, J., Lottenbach, K. R., Barenkamp, S. J. and Reason, D. C., Somatic hypermutation and diverse immunoglobulin gene usage in the human antibody response to the capsular polysaccharide of Streptococcus pneumoniae Type 6B. Infect. Immun. 2004. 72: 3505-3514.
46. Zhou, J., Lottenbach, K. R., Barenkamp, S. J., Lucas, A. H. and Reason, D. C., Recurrent variable region gene usage and somatic mutation in the human antibody response to the capsular polysaccharide of Streptococcus pneumoniae type 23F. Infect. Immun. 2002. 70: 4083-4091.
47. Dörner, T. and Lipsky, P. E., Immunoglobulin variable-region gene usage in systemic autoimmune diseases. Arthritis Rheum. 2001. 44: 2715-2727.