T-cell aging in rheumatoid arthritis

Current Opinion in Rheumatology

Volumn 26, Issue 1, 2014, Pages 93-100

  Weyand, Cornelia M ^a,b   Yang, Zhen ^a,b   Goronzy, Jörg J ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

DNA damage; immune aging; SASP; T cell signaling; telomere

Indexed keywords

ADENOSINE DEAMINASE; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 6; PHOSPHATASE; PHOSPHOTRANSFERASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; TELOMERASE;

APOPTOSIS; AUTOIMMUNE DISEASE; CARDIOVASCULAR DISEASE; CD4+ T LYMPHOCYTE; CELL AGING; CELL CYCLE ARREST; CELL STRESS; CHRONIC INFLAMMATION; COMORBIDITY; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; GENE MUTATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; IMMUNE DYSREGULATION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOCOMPETENCE; IMMUNOLOGICAL MEMORY; LIFE EXPECTANCY; MEMORY CELL; METABOLIC SYNDROME X; MICROENVIRONMENT; MORBIDITY; MORTALITY; NEOPLASM; NONHUMAN; OSTEOLYSIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; TELOMERE; TISSUE DEGENERATION; TISSUE INJURY; TUMOR SUPPRESSOR GENE;

AGING; ARTHRITIS, RHEUMATOID; CELL AGING; DNA DAMAGE; DNA REPAIR; HUMANS; T-LYMPHOCYTES;

EID: 84890213024     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0000000000000011     Document Type: Review

References (77)

1. Vigen R, Maddox TM, Allen LA. Aging of the United States population: Impact on heart failure. Curr Heart Fail Rep 2012; 9:369-374.
2. McEniry M. Early-life conditions and older adult health in low- And middleincome countries: A review. J Dev Orig Health Dis 2013; 4:10-29.
3. Catindig JA, Venketasubramanian N, Ikram MK, et al. Epidemiology of dementia in Asia: Insights on prevalence, trends and novel risk factors. J Neurol Sci 2012; 321:11-16.
4. Hurd MD, Martorell P, Delavande A, et al. Monetary costs of dementia in the United States. N Engl J Med 2013; 368:1326-1334.
5. Goronzy JJ, Li G, Yang Z, et al. The janus head of T cell aging - Autoimmunity and immunodeficiency. Front Immunol 2013; 4:131.
6. Goronzy JJ, Weyand CM. Understanding immunosenescence to improve responses to vaccines. Nat Immunol 2013; 14:428-436
7. Weyand CM, Fujii H, Shao L, et al. Rejuvenating the immune system in rheumatoid arthritis. Nat Rev Rheumatol 2009; 5:583-588.
8. Mayerl C, Prelog M. Immunosenescence and juvenile idiopathic arthritis. Autoimmun Rev 2012; 11:297-300.
9. Tarjanyi O, Boldizsar F, Nemeth P, et al. Age-related changes in arthritis susceptibility and severity in a murine model of rheumatoid arthritis. Immun Ageing 2009; 6:8.
10. Erlandson KM, Allshouse AA, Jankowski CM, et al. Association of functional impairment with inflammation and immune activation in HIV type 1-infected adults receiving effective antiretroviral therapy. J Infect Dis 2013; 208:249- 259.
11. Smith RL, de Boer R, Brul S, et al. Premature and accelerated aging: HIV or HAART? Front Genet 2012; 3:328.
12. Deeks SG, Verdin E, McCune JM. Immunosenescence HIV. Curr Opin Immunol 2012; 24:501-506.
13. Andrews NP, Fujii H, Goronzy JJ, et al. Telomeres and immunological diseases of aging. Gerontology 2010; 56:390-403.
14. Fujii H, Shao L, Colmegna I, et al. Telomerase insufficiency in rheumatoid arthritis. Proc Natl Acad Sci USA 2009; 106:4360-4365.
15. Arnold CR, Wolf J, Brunner S, et al. Gain and loss of T cell subsets in old age: Age-related reshaping of the T cell repertoire. J Clin Immunol 2011; 31:137- 146.
16. Czesnikiewicz-Guzik M, Lee WW, Cui D, et al. T cell subset-specific susceptibility to aging. Clin Immunol 2008; 127:107-118.
17. Bektas A, Zhang Y, Wood WH 3rd, et al. Age-associated alterations in inducible gene transcription in human CD4 T lymphocytes. Aging (Albany NY) 2013; 5:18-36.
18. Seok J, Warren HS, Cuenca AG, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 2013; 110:3507-3512.
19. Chou JP, Effros RB. T cell replicative senescence in human aging. Curr Pharm Des 2013; 19:1680-1698.
20. Broux B, Markovic-Plese S, Stinissen P, et al. Pathogenic features of CD4CD28- T cells in immune disorders. Trends Mol Med 2012; 18:446-453.
21. Nakajima T, Schulte S, Warrington KJ, et al. T-cell-mediated lysis of endothelial cells in acute coronary syndromes. Circulation 2002; 105:570-575.
22. Warrington KJ, Takemura S, Goronzy JJ, et al. CD4, CD28- T cells in rheumatoid arthritis patients combine features of the innate and adaptive immune systems. Arthritis Rheum 2001; 44:13-20.
23. Liuzzo G, Goronzy JJ, Yang H, et al. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation 2000; 101:2883-2888.
24. Liuzzo G, Kopecky SL, Frye RL, et al. Perturbation of the T-cell repertoire in patients with unstable angina. Circulation 1999; 100:2135-2139.
25. Nakajima T, Goek O, Zhang X, et al. De novo expression of killer immunoglobulin- like receptors and signaling proteins regulates the cytotoxic function of CD4 T cells in acute coronary syndromes. Circ Res 2003; 93:106-113.
26. Zhang X, Nakajima T, Goronzy JJ, et al. Tissue trafficking patterns of effector memory CD4 T cells in rheumatoid arthritis. Arthritis Rheum 2005; 52:3839- 3849.
27. Turner JE, Campbell JP, Edwards KM, et al. Rudimentary signs of immunosenescence in Cytomegalovirus-seropositive healthy young adults. Age (Dordr) 2013. [Epub ahead of print]
28. Pawelec G, Derhovanessian E. Role of CMV in immune senescence. Virus Res 2011; 157:175-179.
29. SavvaGM, Pachnio A, Kaul B, et al.Cytomegalovirus infection is associated with increased mortality in the older population. Aging Cell 2013; 12:381-387.
30. Derhovanessian E, Maier AB, Hahnel K, et al. Lower proportion of naive peripheral CD8 T cells and an unopposed pro-inflammatory response to human Cytomegalovirus proteins in vitro are associated with longer survival in very elderly people. Age (Dordr) 2013; 35:1387-1399.
31. Bartlett DB, Firth CM, Phillips AC, et al. The age-related increase in low-grade systemic inflammation (Inflammaging) is not driven by cytomegalovirus infection. Aging Cell 2012; 11:912-915.
32. Griffiths SJ, Riddell NE, Masters J, et al. Age-associated increase of lowavidity cytomegalovirus-specific CD8 T cells that re-express CD45RA. J Immunol 2013; 190:5363-5372.
33. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol 2011; 192:547-556.
34. Campisi J. Aging, cellular senescence, and cancer. Annu Rev Physiol 2013; 75:685-705.
35. Coppe JP, Desprez PY, Krtolica A, et al. The senescence-associated secretory phenotype: The dark side of tumor suppression. Annu Rev Pathol 2010; 5:99-118.
36. Braumuller H, Wieder T, Brenner E, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013; 494:361-365.
37. Kryczek I, Zhao E, Liu Y, et al. Human TH17 cells are long-lived effector memory cells. Sci Transl Med 2011; 3:104ra100.
38. Lubberts E. Th17 cytokines and arthritis. Semin Immunopathol 2010; 32:43- 53.
39. Annunziato F, Cosmi L, Liotta F, et al. Type 17T helper cells-origins, features and possible roles in rheumatic disease. Nat Rev Rheumatol 2009; 5:325-331.
40. Youngblood B, Wherry EJ, Ahmed R. Acquired transcriptional programming in functional and exhausted virus-specific CD8 T cells. Curr Opin HIV AIDS 2012; 7:50-57.
41. Wherry EJ. T cell exhaustion. Nat Immunol 2011; 12:492-499.
42. Akbar AN, Henson SM. Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat Rev Immunol 2011; 11:289-295.
43. Liu Y, Johnson SM, Fedoriw Y, et al. Expression of p16(INK4a) prevents cancer and promotes aging in lymphocytes. Blood 2011; 117:3257-3267.
44. Nelson JA, Krishnamurthy J, Menezes P, et al. Expression of p16(INK4a) as a biomarker of T-cell aging in HIV-infected patients prior to and during antiretroviral therapy. Aging Cell 2012; 11:916-918.
45. Chou JP, Ramirez CM, Wu JE, et al. Accelerated aging in HIV/AIDS: Novel biomarkers of senescent human CD8 T cells. PLoS One 2013; 8:e64702.
46. Goronzy JJ, Li G, Yu M, et al. Signaling pathways in aged T cells - A reflection of T cell differentiation, cell senescence and host environment. Semin Immunol 2012; 24:365-372.
47. Weng NP, Araki Y, Subedi K. The molecular basis of the memory T cell response: Differential gene expression and its epigenetic regulation. Nat Rev Immunol 2012; 12:306-315.
48. Chen G, Lustig A, Weng NP. T cell aging: A review of the transcriptional changes determined from genome-wide analysis. Front Immunol 2013; 4:121.
49. Yu M, Li G, Lee WW, et al. Signal inhibition by the dual-specific phosphatase 4 impairs T cell-dependent B-cell responses with age. Proc Natl Acad Sci USA 2012; 109:E879-E888.
50. Li G, Yu M, Lee WW, et al. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat Med 2012; 18:1518-1524.
51. Singh K, Deshpande P, Li G, et al. K-RAS GTPase- And B-RAF kinasemediated T-cell tolerance defects in rheumatoid arthritis. Proc Natl Acad Sci USA 2012; 109:E1629-E1637.
52. Goronzy JJ, Weyand CM. Immune aging and autoimmunity. Cell Mol Life Sci 2012; 69:1615-1623.
53. Hohensinner PJ, Goronzy JJ, Weyand CM. Telomere dysfunction, autoimmunity and aging. Aging Dis 2011; 2:524-537.
54. Schmidt D, Goronzy JJ, Weyand CM. CD4CD7-CD28- T cells are expanded in rheumatoid arthritis and are characterized by autoreactivity. J Clin Invest 1996; 97:2027-2037.
55. Wagner UG, Koetz K, Weyand CM, et al. Perturbation of the T cell repertoire in rheumatoid arthritis. Proc Natl Acad Sci USA 1998; 95:14447-14452.
56. Koetz K, Bryl E, Spickschen K, et al. T cell homeostasis in patients with rheumatoid arthritis. Proc Natl Acad Sci USA 2000; 97:9203-9208.
57. Schonland SO, Lopez C, Widmann T, et al. Premature telomeric loss in rheumatoid arthritis is genetically determined and involves both myeloid and lymphoid cell lineages. Proc Natl Acad Sci USA 2003; 100:13471-13476.
58. High KP, Brennan-Ing M, Clifford DB, et al. HIV and aging: State of knowledge and areas of critical need for research. A report to the NIH Office of AIDS Research by the HIV and Aging Working Group. J Acquir Immune Defic Syndr 2012; 60 (Suppl. 1):S1-S18.
59. Lohse N, Hansen AB, Pedersen G, et al. Survival of persons with and without HIV infection in Denmark, 1995-2005. Ann Intern Med 2007; 146:87-95.
60. Losina E, Schackman BR, Sadownik SN, et al. Racial and sex disparities in life expectancy losses among HIV-infected persons in the United States: Impact of risk behavior, late initiation, and early discontinuation of antiretroviral therapy. Clin Infect Dis 2009; 49:1570-1578.
61. Antiretroviral Therapy Cohort Collaboration. Life expectancy of individuals on combination antiretroviral therapy in high-income countries: A collaborative analysis of 14 cohort studies. Lancet 2008; 372:293-299.
62. Cavanagh MM, Weyand CM, Goronzy JJ. Chronic inflammation and aging: DNA damage tips the balance. Curr Opin Immunol 2012; 24:488-493.
63. Georgin-Lavialle S, Aouba A, Mouthon L, et al. The telomere/telomerase system in autoimmune and systemic immune-mediated diseases. Autoimmun Rev 2010; 9:646-651.
64. Colmegna I, Diaz-Borjon A, Fujii H, et al. Defective proliferative capacity and accelerated telomeric loss of hematopoietic progenitor cells in rheumatoid arthritis. Arthritis Rheum 2008; 58:990-1000.
65. Colmegna I, Weyand CM. Haematopoietic stem and progenitor cells in rheumatoid arthritis. Rheumatology (Oxford) 2011; 50:252-260.
66. Goto M. Hierarchical deterioration of body systems in Werner's syndrome: Implications for normal ageing. Mech Ageing Dev 1997; 98:239-254.
67. Carney EF, Srinivasan V, Moss PA, et al. Classical ataxia telangiectasia patients have a congenitally aged immune system with high expression of CD95. J Immunol 2012; 189:261-268.
68. Exley AR, Buckenham S, Hodges E, et al. Premature ageing of the immune system underlies immunodeficiency in ataxia telangiectasia. Clin Immunol 2011; 140:26-36.
69. Reinhardt HC, Schumacher B. The p53 network: Cellular and systemic DNA damage responses in aging and cancer. Trends Genet 2012; 28:128- 136.
70. Lichterfeld M, Cung T, Seiss K, et al. Shelterin dysfunction and p16(INK4a)- mediated growth inhibition in HIV-1-specific CD8 T cells. J Virol 2012; 86:5533-5540.
71. Gardano L, Pucci F, Christian L, et al. Telomeres, a busy platform for cell signaling. Front Oncol 2013; 3:146.
72. Reynolds JJ, Stewart GS. A nervous predisposition to unrepaired DNA double strand breaks. DNA Repair (Amst) 2013; 12:588-599.
73. Anheim M, Tranchant C, Koenig M. The autosomal recessive cerebellar ataxias. N Engl J Med 2012; 366:636-646.
74. Shao L, Fujii H, Colmegna I, et al. Deficiency of the DNA repair enzyme ATM in rheumatoid arthritis. J Exp Med 2009; 206:1435-1449.
75. Karaman A, Binici DN, Melikoglu MA. Comet assay and analysis of micronucleus formation in patients with rheumatoid arthritis. Mutat Res 2011; 721:1-5.
76. Shao L, Goronzy JJ, Weyand CM. DNA-dependent protein kinase catalytic subunit mediates T-cell loss in rheumatoid arthritis. EMBO Mol Med 2010; 2:415-427.
77. Yang Z, Fujii H, Mohan SV, et al. Phosphofructokinase deficiency impairs ATP generation, autophagy, and redox balance in rheumatoid arthritis T cells. J Exp Med 2013; 210:2119-2134.