Age-associated differences in MiRNA signatures are restricted to CD45RO negative T cells and are associated with changes in the cellular composition, activation and cellular ageing

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Teteloshvili, Nato ^a   Kluiver, Joost ^a   Van Der Geest, Kornelis S M ^a   Van Der Lei, Roelof Jan ^a   Jellema, Pytrick ^a   Pawelec, Graham ^b,c   Brouwer, Elisabeth ^a   Kroesen, Bart Jan ^a   Boots, Annemieke M H ^a   Van Den Berg, Anke ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD31 ANTIGEN; CD4 ANTIGEN; CD45RO ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR7; MICRORNA; MICRORNA 15A; MICRORNA 21; MICRORNA 223; MONOCLONAL ANTIBODY; CD45 ANTIGEN; MIRN21 MICRORNA, HUMAN; MIRN223 MICRORNA, HUMAN; TRANSCRIPTOME;

ADULT; AGING; ANTIGEN EXPRESSION; ARTICLE; BLOOD CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL AGING; CELL COMPOSITION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; HUMAN; HUMAN EXPERIMENT; MEMORY T LYMPHOCYTE; MICROARRAY ANALYSIS; NORMAL HUMAN; PHENOTYPE; RNA EXTRACTION; RNA PURIFICATION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; AGED; CELL CULTURE; FEMALE; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MIDDLE AGED; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD45; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL AGING; CELLS, CULTURED; FEMALE; HUMANS; LYMPHOCYTE ACTIVATION; MALE; MICRORNAS; MIDDLE AGED; TRANSCRIPTOME;

EID: 84945283397     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137556     Document Type: Article

References (40)

1. Michie CA, McLean A, Alcock C, Beverley PC. Lifespan of human lymphocyte subsets defined by CD45 isoforms. Nature 1992 Nov 19; 360(6401): 264-265. PMID: 1436108
2. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999 Oct 14; 401(6754): 708-712. PMID: 10537110
3. Fagnoni FF, Vescovini R, Mazzola M, Bologna G, Nigro E, Lavagetto G, et al. Expansion of cytotoxic CD8+ CD28-T cells in healthy ageing people, including centenarians. Immunology 1996 Aug; 88 (4): 501-507. PMID: 8881749
4. Kimmig S, Przybylski GK, Schmidt CA, Laurisch K, Mowes B, Radbruch A, et al. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J Exp Med 2002 Mar 18; 195(6): 789-794. PMID: 11901204
5. Kohler S, Thiel A. Life after the thymus: CD31+and CD31-human naive CD4+T-cell subsets. Blood 2009 Jan 22; 113(4): 769-774. doi: 10.1182/blood-2008-02-139154 PMID: 18583570
6. Kohler S, Wagner U, Pierer M, Kimmig S, Oppmann B, Mowes B, et al. Post-thymic in vivo proliferation of naive CD4+T cells constrains the TCR repertoire in healthy human adults. Eur J Immunol 2005 Jun; 35(6): 1987-1994. PMID: 15909312
7. Effros RB Replicative senescence: the final stage of memory T cell differentiation? Curr HIV Res 2003 Apr; 1(2): 153-165. PMID: 15043200
8. Goronzy JJ, Weyand CM. Aging, autoimmunity and arthritis: T-cell senescence and contraction of T-cell repertoire diversity - catalysts of autoimmunity and chronic inflammation. Arthritis Res Ther 2003; 5 (5): 225-234. PMID: 12932282
9. Effros RB The role of CD8 T cell replicative senescence in human aging. Discov Med 2005 Jun; 5 (27): 293-297. PMID: 20704891
10. Pawelec G, Rehbein A, Haehnel K, Merl A, Adibzadeh M. Human T-cell clones in long-term culture as a model of immunosenescence. Immunol Rev 1997 Dec; 160: 31-42. PMID: 9476663
11. Bartel DP MicroRNAs: target recognition and regulatory functions. Cell 2009 Jan 23; 136(2): 215-233. doi: 10.1016/j.cell.2009.01.002 PMID: 19167326
12. Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004 Jan 2; 303(5654): 83-86. PMID: 14657504
13. Hackl M, Brunner S, Fortschegger K, Schreiner C, Micutkova L, Muck C, et al. miR-17, miR-19b, miR-20a, and miR-106a are down-regulated in human aging. Aging Cell 2010 Apr; 9(2): 291-296. doi: 10.1111/j.1474-9726.2010.00549.x PMID: 20089119
14. Brunner S, Herndler-Brandstetter D, Arnold CR, Wiegers GJ, Villunger A, Hackl M, et al. Upregulation of miR-24 is associated with a decreased DNA damage response upon etoposide treatment in highly differentiated CD8(+) T cells sensitizing them to apoptotic cell death. Aging Cell 2012 Aug; 11(4): 579-587. doi: 10.1111/j.1474-9726.2012.00819.x PMID: 22435726
15. Ohyashiki M, Ohyashiki JH, Hirota A, Kobayashi C, Ohyashiki K. Age-related decrease of miRNA-92a levels in human CD8+ T-cells correlates with a reduction of naive T lymphocytes. Immun Ageing 2011 Nov 15; 8(1): 11-4933-8-11.
16. Li G, Yu M, Lee WW, Tsang M, Krishnan E, Weyand CM, et al. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat Med 2012 Oct; 18(10): 1518-1524. doi: 10.1038/nm.2963 PMID: 23023500
17. Ligthart GJ, Corberand JX, Fournier C, Galanaud P, Hijmans W, Kennes B, et al. Admission criteria for immunogerontological studies in man: the SENIEUR protocol. Mech Ageing Dev 1984 Nov; 28(1): 47-55. PMID: 6513613
18. Pawelec G, Barnett Y, Mariani E, Solana R. Human CD4+T cell clone longevity in tissue culture: lack of influence of donor age or cell origin. Exp Gerontol 2002 Jan-Mar; 37(2-3): 265-269. PMID: 11772512
19. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002 Jan; 18(1): 207-208. PMID: 11836235
20. Kluiver J, Slezak-Prochazka I, van den Berg A. Studying microRNAs in lymphoma. Methods Mol Biol 2013; 971: 265-276. doi: 10.1007/978-1-62703-269-815 PMID: 23296969
21. Wu H, Neilson JR, Kumar P, Manocha M, Shankar P, Sharp PA, et al. miRNA profiling of naive, effector and memory CD8T cells. PLoS One 2007 Oct 10; 2(10): e1020. PMID: 17925868
22. Smigielska-Czepiel K, van den Berg A, Jellema P, van der Lei RJ, Bijzet J, Kluiver J, et al. Comprehensive analysis of miRNA expression in T-cell subsets of rheumatoid arthritis patients reveals defined signatures of naive and memory Tregs. Genes Immun 2014 Mar; 15(2): 115-125. doi: 10.1038/gene.2013.69 PMID: 24401767
23. Olivieri F, Spazzafumo L, Santini G, Lazzarini R, Albertini MC, Rippo MR, et al. Age-related differences in the expression of circulating microRNAs: miR-21 as a new circulating marker of inflammaging. Mech Ageing Dev 2012 Nov-Dec; 133(11-12): 675-685. doi: 10.1016/j.mad.2012.09.004 PMID: 23041385
24. ∗ and MicroRNA-21 modulate endothelial progenitor cell senescence via suppressing high-mobility group A2. Circ Res 2013 Jan 4; 112(1): 152-164. doi: 10.1161/CIRCRESAHA.112.280016 PMID: 23072816
25. Mercken EM, Majounie E, Ding J, Guo R, Kim J, Bernier M, et al. Age-associated miRNA alterations in skeletal muscle from rhesus monkeys reversed by caloric restriction. Aging (Albany NY) 2013 Sep; 5 (9): 692-703.
26. Olivieri F, Spazzafumo L, Santini G, Lazzarini R, Albertini MC, Rippo MR, et al. Age-related differences in the expression of circulating microRNAs: miR-21 as a new circulating marker of inflammaging. Mech Ageing Dev 2012 Nov-Dec; 133(11-12): 675-685. doi: 10.1016/j.mad.2012.09.004 PMID: 23041385
27. Jazbutyte V, Fiedler J, Kneitz S, Galuppo P, Just A, Holzmann A, et al. MicroRNA-22 increases senescence and activates cardiac fibroblasts in the aging heart. Age (Dordr) 2013 Jun; 35(3): 747-762.
28. Park S, Kang S, Min KH, Woo Hwang K, Min H. Age-associated changes in microRNA expression in bone marrow derived dendritic cells. Immunol Invest 2013; 42(3): 179-190. doi: 10.3109/08820139.2012.717328 PMID: 23252865
29. Smigielska-Czepiel K, van den Berg A, Jellema P, Slezak-Prochazka I, Maat H, van den Bos H, et al. Dual role of miR-21 in CD4+T-cells: activation-induced miR-21 supports survival of memory T-cells and regulates CCR7 expression in naive T-cells. PLoS One 2013 Oct 1; 8(10): e76217. doi: 10.1371/journal.pone.0076217 PMID: 24098447
30. Fornasa G, Groyer E, Clement M, Dimitrov J, Compain C, Gaston AT, et al. TCR stimulation drives cleavage and shedding of the ITIM receptor CD31. J Immunol 2010 May 15; 184(10): 5485-5492. doi: 10.4049/jimmunol.0902219 PMID: 20400708
31. Wang L, He L, Zhang R, Liu X, Ren Y, Liu Z, et al. Regulation of T lymphocyte activation by microRNA-21. Mol Immunol 2014 Jun; 59(2): 163-171. doi: 10.1016/j.molimm.2014.02.004 PMID: 24631982
32. Koch S, Larbi A, Derhovanessian E, Ozcelik D, Naumova E, Pawelec G. Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun Ageing 2008 Jul 25; 5: 6-6-4933-5-6.
33. Ouyang Q, Wagner WM, Zheng W, Wikby A, Remarque EJ, Pawelec G. Dysfunctional CMV-specific CD8(+) T cells accumulate in the elderly. Exp Gerontol 2004 Apr; 39(4): 607-613. PMID: 15050296
34. Henson SM, Riddell NE, Akbar AN. Properties of end-stage human T cells defined by CD45RA re-expression. Curr Opin Immunol 2012 Aug; 24(4): 476-481. doi: 10.1016/j.coi.2012.04.001 PMID: 22554789
35. van der Geest KS, Smigielska-Czepiel K, Park JA, Abdulahad WH, Kim HW, Kroesen BJ, et al. SFTreg cells transcribing high levels of Bcl-2 and microRNA-21 demonstrate limited apoptosis in RA. Rheumatology (Oxford) 2015 May; 54(5): 950-958.
36. Buscaglia LE, Li Y. Apoptosis and the target genes of microRNA-21. Chin J Cancer 2011 Jun; 30 (6): 371-380. PMID: 21627859
37. Ruan Q, Wang P, Wang T, Qi J, Wei M, Wang S, et al. MicroRNA-21 regulates T-cell apoptosis by directly targeting the tumor suppressor gene Tipe2. Cell Death Dis 2014 Feb 27; 5: e1095. doi: 10.1038/cddis.2014.47 PMID: 24577093
38. Medina PP, Nolde M, Slack FJ. OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 2010 Sep 2; 467(7311): 86-90. doi: 10.1038/nature09284 PMID: 20693987
39. Dellago H, Preschitz-Kammerhofer B, Terlecki-Zaniewicz L, Schreiner C, Fortschegger K, Chang MW, et al. High levels of oncomiR-21 contribute to the senescence-induced growth arrest in normal human cells and its knock-down increases the replicative lifespan. Aging Cell 2013 Jun; 12(3): 446-458. doi: 10.1111/acel.12069 PMID: 23496142
40. Fulci V, Scappucci G, Sebastiani GD, Giannitti C, Franceschini D, Meloni F, et al. miR-223 is overex-pressed in T-lymphocytes of patients affected by rheumatoid arthritis. Hum Immunol 2010 Feb; 71 (2): 206-211. doi: 10.1016/j.humimm.2009.11.008 PMID: 19931339