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Published in: Seminars in Immunopathology 5/2020

Open Access 01-10-2020 | Review

The untwining of immunosenescence and aging

Authors: Weili Xu, Glenn Wong, You Yi Hwang, Anis Larbi

Published in: Seminars in Immunopathology | Issue 5/2020

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Abstract

From a holistic point of view, aging results from the cumulative erosion of the various systems. Among these, the immune system is interconnected to the rest as immune cells are present in all organs and recirculate through bloodstream. Immunosenescence is the term used to define the remodelling of immune changes during aging. Because immune cells—and particularly lymphocytes—can further differentiate after their maturation in response to pathogen recognition, it is therefore unclear when senescence is induced in these cells. Additionally, it is also unclear which signals triggers senescence in immune cells (i) aging per se, (ii) specific response to pathogens, (iii) underlying conditions, or (iv) inflammaging. In this review, we will cover the current knowledge and concepts linked to immunosenescence and we focus this review on lymphocytes and T cells, which represent the typical model for replicative senescence. With the evidence presented, we propose to disentangle the senescence of immune cells from chronological aging.
Literature
2.
go back to reference Metchnikoff E, Mitchell PC (1907) The prolongation of life: optimistic studies. Editor: Peter Chalmers Mitchell Metchnikoff E, Mitchell PC (1907) The prolongation of life: optimistic studies. Editor: Peter Chalmers Mitchell
10.
go back to reference Raz N (2004) Aging brain: structural changes and their implications for cognitive aging - Oxford Scholarship. In: Dixon R, Backman L, Nilsson L-G (eds) New frontiers in cognitive aging. Oxford University Press, Oxford, pp 115–134CrossRef Raz N (2004) Aging brain: structural changes and their implications for cognitive aging - Oxford Scholarship. In: Dixon R, Backman L, Nilsson L-G (eds) New frontiers in cognitive aging. Oxford University Press, Oxford, pp 115–134CrossRef
15.
go back to reference Baruch K, Deczkowska A, David E, Castellano JM, Miller O, Kertser A, Berkutzki T, Barnett-Itzhaki Z, Bezalel D, Wyss-Coray T, Amit I, Schwartz M (2014) Aging. Aging-induced type I interferon response at the choroid plexus negatively affects brain function. Science (New York, N.Y.) 346(6205):89–93. https://doi.org/10.1126/science.1252945CrossRef Baruch K, Deczkowska A, David E, Castellano JM, Miller O, Kertser A, Berkutzki T, Barnett-Itzhaki Z, Bezalel D, Wyss-Coray T, Amit I, Schwartz M (2014) Aging. Aging-induced type I interferon response at the choroid plexus negatively affects brain function. Science (New York, N.Y.) 346(6205):89–93. https://​doi.​org/​10.​1126/​science.​1252945CrossRef
21.
31.
go back to reference Burzyn D, Kuswanto W, Kolodin D, Shadrach JL, Cerletti M, Jang Y, Sefik E, Tan TG, Wagers AJ, Benoist C et al (2013) A special population of regulatory T cells potentiates muscle repair. Cell 155:1282–1295CrossRef Burzyn D, Kuswanto W, Kolodin D, Shadrach JL, Cerletti M, Jang Y, Sefik E, Tan TG, Wagers AJ, Benoist C et al (2013) A special population of regulatory T cells potentiates muscle repair. Cell 155:1282–1295CrossRef
32.
go back to reference Castiglioni A, Corna G, Rigamonti E, Basso V, Vezzoli M, Monno A, Almada AE, Mondino A, Wagers AJ, Manfredi AA et al (2015) FOXP3+ T cells recruited to sites of sterile skeletal muscle injury regulate the fate of satellite cells and guide effective tissue regeneration. PLoS One 10:e0128094CrossRef Castiglioni A, Corna G, Rigamonti E, Basso V, Vezzoli M, Monno A, Almada AE, Mondino A, Wagers AJ, Manfredi AA et al (2015) FOXP3+ T cells recruited to sites of sterile skeletal muscle injury regulate the fate of satellite cells and guide effective tissue regeneration. PLoS One 10:e0128094CrossRef
34.
go back to reference Shinpo K, Kikuchi S, Sasaki H, Ogata A, Moriwaka F, Tashiro K (2000) Selective vulnerability of spinal motor neurons to reactive dicarbonyl compounds, intermediate products of glycation, in vitro: implication of inefficient glutathione system in spinal motor neurons. Brain Res. https://doi.org/10.1016/S0006-8993(00)02047-3 Shinpo K, Kikuchi S, Sasaki H, Ogata A, Moriwaka F, Tashiro K (2000) Selective vulnerability of spinal motor neurons to reactive dicarbonyl compounds, intermediate products of glycation, in vitro: implication of inefficient glutathione system in spinal motor neurons. Brain Res. https://​doi.​org/​10.​1016/​S0006-8993(00)02047-3
41.
go back to reference Kulkarni U et al (2019) Excessive neutrophil levels in the lung underlie the age-associated increase in influenza mortality. Mucosal Immunol 12(2):545–554CrossRef Kulkarni U et al (2019) Excessive neutrophil levels in the lung underlie the age-associated increase in influenza mortality. Mucosal Immunol 12(2):545–554CrossRef
42.
go back to reference Wong CK et al (2017) Aging impairs alveolar macrophage phagocytosis and increases influenza-induced mortality in mice. J Immunol 199(3):1060–1068CrossRef Wong CK et al (2017) Aging impairs alveolar macrophage phagocytosis and increases influenza-induced mortality in mice. J Immunol 199(3):1060–1068CrossRef
43.
go back to reference Zhao J, Zhao J, Legge K, Perlman S (2011) Age-related increases in PGD 2 expression impair respiratory DC migration, resulting in diminished T cell responses upon respiratory virus infection in mice. J Clin Invest. https://doi.org/10.1172/JCI59777 Zhao J, Zhao J, Legge K, Perlman S (2011) Age-related increases in PGD 2 expression impair respiratory DC migration, resulting in diminished T cell responses upon respiratory virus infection in mice. J Clin Invest. https://​doi.​org/​10.​1172/​JCI59777
44.
74.
go back to reference Salam N, Rane S, Das R, Faulkner M, Gund R, Kandpal U, Lewis V, Mattoo H, Prabhu S, Ranganathan V, Durdik J, George A, Rath S, Bal V (2013) T cell ageing: effects of age on development, survival & function. Indian J Med Res 138(5):595–608PubMedPubMedCentral Salam N, Rane S, Das R, Faulkner M, Gund R, Kandpal U, Lewis V, Mattoo H, Prabhu S, Ranganathan V, Durdik J, George A, Rath S, Bal V (2013) T cell ageing: effects of age on development, survival & function. Indian J Med Res 138(5):595–608PubMedPubMedCentral
75.
go back to reference Chiu BC et al (2013) Cutting edge: central memory CD8 T cells in aged mice are virtual memory cells. J Immunol 191(12):5793–5796CrossRef Chiu BC et al (2013) Cutting edge: central memory CD8 T cells in aged mice are virtual memory cells. J Immunol 191(12):5793–5796CrossRef
76.
go back to reference Renkema KR et al (2014) Two separate defects affecting true naive or virtual memory T cell precursors combine to reduce naive T cell responses with aging. J Immunol 192(1):151–159CrossRef Renkema KR et al (2014) Two separate defects affecting true naive or virtual memory T cell precursors combine to reduce naive T cell responses with aging. J Immunol 192(1):151–159CrossRef
77.
go back to reference Lanzer KG et al (2018) Virtual memory cells make a major contribution to the response of aged influenza-naive mice to influenza virus infection. Immun Ageing 15:17CrossRef Lanzer KG et al (2018) Virtual memory cells make a major contribution to the response of aged influenza-naive mice to influenza virus infection. Immun Ageing 15:17CrossRef
78.
85.
go back to reference Campbell L, Chen C, Bhagat SS, Parker RA, Östör AJK (2011) Risk of adverse events including serious infections in rheumatoid arthritis patients treated with tocilizumab: a systematic literature review and meta-analysis of randomized controlled trials. Rheumatology. https://doi.org/10.1093/rheumatology/keq343 Campbell L, Chen C, Bhagat SS, Parker RA, Östör AJK (2011) Risk of adverse events including serious infections in rheumatoid arthritis patients treated with tocilizumab: a systematic literature review and meta-analysis of randomized controlled trials. Rheumatology. https://​doi.​org/​10.​1093/​rheumatology/​keq343
89.
go back to reference Koch S, Larbi A, Ozcelik D, Solana R, Gouttefangeas C, Attig S, Wikby A, Strindhall J, Franceschi C, Pawelec G (2007) Cytomegalovirus infection: a driving force in human T cell immunosenescence. Ann N Y Acad Sci 1114:23–35CrossRef Koch S, Larbi A, Ozcelik D, Solana R, Gouttefangeas C, Attig S, Wikby A, Strindhall J, Franceschi C, Pawelec G (2007) Cytomegalovirus infection: a driving force in human T cell immunosenescence. Ann N Y Acad Sci 1114:23–35CrossRef
93.
go back to reference Petersen LE, Baptista T, Molina JK, Motta JG, do Prado A, Piovesan DM, de Nardi T, Viola TW, Vieira É, Teixeira AL, Grassi-Oliveira R, Bauer ME (2018) Cognitive impairment in rheumatoid arthritis: role of lymphocyte subsets, cytokines and neurotrophic factors. Clin Rheumatol 37(5):1171–1181. https://doi.org/10.1007/s10067-018-3990-9CrossRefPubMed Petersen LE, Baptista T, Molina JK, Motta JG, do Prado A, Piovesan DM, de Nardi T, Viola TW, Vieira É, Teixeira AL, Grassi-Oliveira R, Bauer ME (2018) Cognitive impairment in rheumatoid arthritis: role of lymphocyte subsets, cytokines and neurotrophic factors. Clin Rheumatol 37(5):1171–1181. https://​doi.​org/​10.​1007/​s10067-018-3990-9CrossRefPubMed
95.
go back to reference Rizzo LB, Do Prado CH, Grassi-Oliveira R, Wieck A, Correa BL, Teixeira AL, Bauer ME (2013) Immunosenescence is associated with human cytomegalovirus and shortened telomeres in type I bipolar disorder. Bipolar Disord 15:832–838 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.CrossRef Rizzo LB, Do Prado CH, Grassi-Oliveira R, Wieck A, Correa BL, Teixeira AL, Bauer ME (2013) Immunosenescence is associated with human cytomegalovirus and shortened telomeres in type I bipolar disorder. Bipolar Disord 15:832–838 © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.CrossRef
98.
go back to reference Aw D, Palmer DB (2011) The origin and implication of thymic involution. Aging Dis 2011 Oct; 2(5):437–443 Aw D, Palmer DB (2011) The origin and implication of thymic involution. Aging Dis 2011 Oct; 2(5):437–443
112.
117.
122.
go back to reference Bertin E, Nguyen P, Guenounou M, Durlach V, Potron G, Leutenegger M (2000) Plasma levels of tumor necrosis factor alpha (TNF-α) are essentially dependent on visceral fat amount in type 2 diabetic patients. Diabetes Metab. 2000 May;26(3):178–82 Bertin E, Nguyen P, Guenounou M, Durlach V, Potron G, Leutenegger M (2000) Plasma levels of tumor necrosis factor alpha (TNF-α) are essentially dependent on visceral fat amount in type 2 diabetic patients. Diabetes Metab. 2000 May;26(3):178–82
159.
go back to reference Hayhoe RP, Henson SM, Akbar AN, Palmer DB (2010) Variation of human natural killer cell phenotypes with age: identification of a unique KLRG1-negative subset. Hum Immunol 71(7):676–681CrossRef Hayhoe RP, Henson SM, Akbar AN, Palmer DB (2010) Variation of human natural killer cell phenotypes with age: identification of a unique KLRG1-negative subset. Hum Immunol 71(7):676–681CrossRef
165.
go back to reference Pereira BI, De Maeyer R, Covre LP, Nehar-Belaid D, Lanna A, Ward S, Marches R, Chambers ES, Gomes D, Riddell NE, Maini MK, Teixeira VH, Janes SM, Gilroy DW, Larbi A, Mabbott NA, Ucar D, Kuchel GA, Henson SM, Strid J et al (2020) Sestrins induce natural killer function in senescent-like CD8+ T cells. Nat Immunol 21(6):684–694. https://doi.org/10.1038/s41590-020-0643-3CrossRefPubMed Pereira BI, De Maeyer R, Covre LP, Nehar-Belaid D, Lanna A, Ward S, Marches R, Chambers ES, Gomes D, Riddell NE, Maini MK, Teixeira VH, Janes SM, Gilroy DW, Larbi A, Mabbott NA, Ucar D, Kuchel GA, Henson SM, Strid J et al (2020) Sestrins induce natural killer function in senescent-like CD8+ T cells. Nat Immunol 21(6):684–694. https://​doi.​org/​10.​1038/​s41590-020-0643-3CrossRefPubMed
Metadata
Title
The untwining of immunosenescence and aging
Authors
Weili Xu
Glenn Wong
You Yi Hwang
Anis Larbi
Publication date
01-10-2020
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 5/2020
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-020-00824-x

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