Immunosenescence in renal transplantation: a changing balance of innate and adaptive immunity.
Authors:
Journal: Current opinion in organ transplantation
Publication Type: Journal Article
Date: 2015
DOI: NIHMS708425
ID: 26154914
Abstract
With global demographic changes and an overall improved healthcare, more older end-stage renal disease (ESRD) patients receive kidney transplants. At the same time, organs from older donors are utilized more frequently. Those developments have and will continue to impact allocation, immunosuppression and efforts improving organ quality.
Reference List
- Effros RB. Telomerase induction in T cells: a cure for aging and disease? Exp Gerontol. 2007;42:416–20.|||Tso PL. Access to renal transplantation for the elderly in the face of new allocation policy: a review of contemporary perspectives on “older” issues. Transplant Rev. 2014;28:6–14.|||Nathan HM, Conrad SL, Held PJ, et al. Organ donation in the United States. Am J Transplant. 2003;3:29–40.|||Schold JD, Kaplan B, Baliga RS, et al. The broad spectrum of quality in deceased donor kidneys. Am J Transplant. 2005;5:757–65.|||Nyberg SL, Baskin-Bey ES, Kremers W, et al. Improving the prediction of donor kidney quality: deceased donor score and resistive indices. Transplantation. 2005;80:925–9.|||Tanriover B, Mohan S, Cohen DJ, et al. Kidneys at higher risk of discard: expanding the role of dual kidney transplantation. Am J Transplant. 2014;14:404–15.|||Frei U, Noeldeke J, Machold-Fabrizii V, et al. Prospective age-matching in elderly kidney transplant recipients--a 5-year analysis of the Eurotransplant Senior Program. Am J Transplant. 2008;8:50–7.|||Fritsche L, Hörstrup J, Budde K, et al. Old-for-old kidney allocation allows successful expansion of the donor and recipient pool. Am J Transplant. 2003;3:1434–9.|||Kauffman HM, McBride MA, Cors CS, et al. Early mortality rates in older kidney recipients with comorbid risk factors. Transplantation. 2007;83:404–10.|||Ponticelli C. Should renal transplantation be offered to older patients? Nephrol Dial Transplant. 2000;15:315–7.|||Tullius SG, Tran H, Guleria I, et al. The combination of donor and recipient age is critical in determining host immunoresponsiveness and renal transplant outcome. Ann Surg. 2010;252:662–74.|||Shammas MA. Telomeres, lifestyle, cancer, and aging. Curr Opin Clin Nutr Metab Care. 2011;14:28–34.|||Lin Y, Damjanovic A, Metter EJ, et al. Age-associated telomere attrition of lymphocytes in vivo is co-ordinated with changes in telomerase activity, composition of lymphocyte subsets and health conditions. Clin Sci. 2015;128:367–77.|||Kaszubowska L. Telomere shortening and ageing of the immune system. J Physiol Pharmacol. 2008;59 (Suppl 9):169–86.|||Westhoff JH, Schildhorn C, Jacobi C, et al. Telomere shortening reduces regenerative capacity after acute kidney injury. J Am Soc Nephrol. 2010;21:327–36.|||Yan J, Greer JM, Hull R, et al. The effect of ageing on human lymphocyte subsets: comparison of males and females. Immun Ageing. 2010;7:4.|||Linton PJ, Dorshkind K. Age-related changes in lymphocyte development and function. Nat Immunol. 2004;5:133–9.|||Koch S, Larbi A, Derhovanessian E, et al. Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun Ageing. 2008;5:6.|||Le Garff-Tavernier M, Béziat V, Decocq J, et al. Human NK cells display major phenotypic and functional changes over the life span. Aging Cell. 2010;9:527–35.|||Douziech N, Seres I, Larbi A, et al. Modulation of human lymphocyte proliferative response with aging. Exp Gerontol. 37:369–87.|||Jiang J, Gross D, Elbaum P, et al. Aging affects initiation and continuation of T cell proliferation. Mech Ageing Dev. 2007;128:332–9.|||Morbach H, Eichhorn EM, Liese JG, et al. Reference values for B cell subpopulations from infancy to adulthood. Clin Exp Immunol. 2010;162:271–9.|||Park J, Miyakawa T, Shiokawa A, et al. Attenuation of migration properties of CD4+ T cells from aged mice correlates with decrease in chemokine receptor expression, response to retinoic acid, and RALDH expression compared to young mice. Biosci Biotechnol Biochem. 2014;78:976–80.|||Moro-García MA, Alonso-Arias R, López-Larrea C. When Aging Reaches CD4+ T-Cells: Phenotypic and Functional Changes. Front Immunol. 2013;4:107.|||Turka LA, Linsley PS, Lin H, et al. T-cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo. Proc Natl Acad Sci U S A. 1992;89:11102–5.|||Zhang T, Fresnay S, Welty E, et al. Selective CD28 blockade attenuates acute and chronic rejection of murine cardiac allografts in a CTLA-4-dependent manner. Am J Transplant. 2011;11:1599–609.|||Trzonkowski P, Debska-Slizie A, Jankowska M, et al. Immunosenescence increases the rate of acceptance of kidney allotransplants in elderly recipients through exhaustion of CD4+ T-cells. Mech Ageing Dev. 2010;131:96–104.|||Parish ST, Wu JE, Effros RB. Sustained CD28 expression delays multiple features of replicative senescence in human CD8 T lymphocytes. J Clin Immunol. 2010;30:798–805.|||Leng Q, Bentwich Z, Borkow G. CTLA-4 upregulation during aging. Mech Ageing Dev. 2002;123:1419–21.|||Alonso-Arias R, Moro-García MA, López-Vázquez A, et al. NKG2D expression in CD4+ T lymphocytes as a marker of senescence in the aged immune system. Age (Dordr) 2011;33:591–605.|||Chen G, Lustig A, Weng N-P. T cell aging: a review of the transcriptional changes determined from genome-wide analysis. Front Immunol. 2013;4:121.|||Tarazona R, DelaRosa O, Alonso C, et al. Increased expression of NK cell markers on T lymphocytes in aging and chronic activation of the immune system reflects the accumulation of effector/senescent T cells. Mech Ageing Dev. 2001;121:77–88.|||Zou Y, Stastny P, Süsal C, et al. Antibodies against MICA antigens and kidney-transplant rejection. N Engl J Med. 2007;357:1293–300.|||Cox ST, Stephens HAF, Fernando R, et al. Major histocompatibility complex class I-related chain A allele mismatching, antibodies, and rejection in renal transplantation. Hum Immunol. 2011;72:827–34.|||Neudoerfl C, Mueller BJ, Blume C, et al. The Peripheral NK Cell Repertoire after Kidney Transplantation is Modulated by Different Immunosuppressive Drugs. Front Immunol. 2013;4:46.|||Chidrawar SM, Khan N, Chan YLT, et al. Ageing is associated with a decline in peripheral blood CD56bright NK cells. Immun Ageing. 2006;3:10.|||Brenchley JM, Karandikar NJ, Betts MR, et al. Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells. Blood. 2003;101:2711–20.|||Borrego F, Alonso MC, Galiani MD, et al. NK phenotypic markers and IL2 response in NK cells from elderly people. Exp Gerontol. 1999;34:253–265.|||Bandrés E, Merino J, Vázquez B, et al. The increase of IFN-gamma production through aging correlates with the expanded CD8(+high)CD28(−)CD57(+) subpopulation. Clin Immunol. 2000;96:230–5.|||Ducloux D, Courivaud C, Bamoulid J, et al. Alloimmune responses and atherosclerotic disease after kidney transplantation. Transplantation. 2015;99:220–5. This study gives indications that the increased circulation of CD57+ CD8+ T cells may be associated with HLA mismatches in kidney transplantation.|||Yap M, Boeffard F, Clave E, et al. Expansion of highly differentiated cytotoxic terminally differentiated effector memory CD8+ T cells in a subset of clinically stable kidney transplant recipients: a potential marker for late graft dysfunction. J Am Soc Nephrol. 2014;25:1856–68. First clinical study that links the CD57+ CD8+ T cells and its associated high cytotoxic potential to late graft dysfunction.|||Lopez-Vergès S, Milush JM, Pandey S, et al. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood. 2010;116:3865–74.|||Le Priol Y, Puthier D, Lécureuil C, et al. High cytotoxic and specific migratory potencies of senescent CD8+ CD57+ cells in HIV-infected and uninfected individuals. J Immunol. 2006;177:5145–54.|||Chattopadhyay PK, Betts MR, Price DA, et al. The cytolytic enzymes granyzme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression. J Leukoc Biol. 2009;85:88–97.|||Crepin T, Carron C, Roubiou C, et al. ATG-Induced Accelerated Immune Senescence: Clinical Implications in Renal Transplant Recipients. Am J Transplant. 2015;15:1028–38. This study suggests that the CD57 expression on CD4+ T cells is associated with the occurence of rejection in ATG-treated patients and links it to the cellular senescence triggered by ATG.|||Bottomley M, Harden P, Wood K. CD57 expression in CD8 T cells and development of cutaneous squamous cell carcinoma in renal transplant recipients: a prospective cohort study. Lancet. 2015;385:S23. This study is the first one to indicate that the CD57 expression on CD8+ T cells may be used as a marker for the prediction of the cutaneous squamous cell carcinoma in kidney recipients.|||Borrego F, Alonso MC, Galiani MD, et al. NK phenotypic markers and IL2 response in NK cells from elderly people. Exp Gerontol. 1999;34:253–65.|||Onyema OO, Njemini R, Bautmans I, et al. Cellular aging and senescence characteristics of human T-lymphocytes. Biogerontology. 2012;13:169–81.|||Focosi D, Bestagno M, Burrone O, et al. CD57+ T lymphocytes and functional immune deficiency. J Leukoc Biol. 2010;87:107–16.|||Hirohashi T, Chase CM, Della Pelle P, et al. A novel pathway of chronic allograft rejection mediated by NK cells and alloantibody. Am J Transplant. 2012;12:313–21.|||Akiyoshi T, Hirohashi T, Alessandrini A, et al. Role of complement and NK cells in antibody mediated rejection. Hum Immunol. 2012;73:1226–32.|||Elrefaei M, Blank KJ, Murasko DM. Decreased IL-2, IFN-gamma, and IL-10 production by aged mice during the acute phase of E55+ retrovirus infection. Virology. 2002;299:8–19.|||Haynes L, Linton PJ, Eaton SM, et al. Interleukin 2, but not other common gamma chain-binding cytokines, can reverse the defect in generation of CD4 effector T cells from naive T cells of aged mice. J Exp Med. 1999;190:1013–24.|||Gong Z, Liu T, Wan Y, et al. Decreased c-rel activation contributes to aberrant interleukin-2 expression in CD4(+)T cells of aged rats. Mol Immunol. 2014;61:1–6.|||Gomez I, Marx F, Gould EA, et al. T cells from elderly persons respond to neoantigenic stimulation with an unimpaired IL-2 production and an enhanced differentiation into effector cells. Exp Gerontol. 2004;39:597–605.|||Eaton SM, Burns EM, Kusser K, et al. Age-related defects in CD4 T cell cognate helper function lead to reductions in humoral responses. J Exp Med. 2004;200:1613–22.|||Frasca D, Riley RL, Blomberg BB. Humoral immune response and B-cell functions including immunoglobulin class switch are downregulated in aged mice and humans. Semin Immunol. 2005;17:378–384.|||Blaeser A, McGlauchlen K, Vogel LA. Aged B lymphocytes retain their ability to express surface markers but are dysfunctional in their proliferative capability during early activation events. Immun Ageing. 2008;5:15.|||Goenka R, Scholz JL, Naradikian MS, et al. Memory B cells form in aged mice despite impaired affinity maturation and germinal center kinetics. Exp Gerontol. 2014;54:109–15.|||Rossi DJ, Bryder D, Zahn JM, et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci U S A. 2005;102:9194–9.|||Dykstra B, Olthof S, Schreuder J, et al. Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells. J Exp Med. 2011;208:2691–703.|||Veneri D, Ortolani R, Franchini M, et al. Expression of CD27 and CD23 on peripheral blood B lymphocytes in humans of different ages. Blood Transfus. 2009;7:29–34.|||Hao Y, O’Neill P, Naradikian MS, et al. A B-cell subset uniquely responsive to innate stimuli accumulates in aged mice. Blood. 2011;118:1294–304.|||Rubtsov AV, Rubtsova K, Fischer A, et al. Toll-like receptor 7 (TLR7)-driven accumulation of a novel CD11c+ B-cell population is important for the development of autoimmunity. Blood. 2011;118:1305–15.|||Hidalgo LG, Campbell PM, Sis B, et al. De novo donor-specific antibody at the time of kidney transplant biopsy associates with microvascular pathology and late graft failure. Am J Transplant. 2009;9:2532–41.|||Rodríguez Ferrero ML, Arroyo D, Panizo N, et al. Monitoring of circulating antibodies in a renal transplantation population: preliminary results. Transplant Proc. 2012;44:2548–50.|||Xia MJ, Shan J, Li YP, et al. Adoptive transfusion of tolerant dendritic cells prolong the survival of renal allografts: a systematic review. J Evid Based Med. 2013;6:250–64.|||Lechler RI, Batchelor JR. Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donor strain dendritic cells. J Exp Med. 1982;155:31–41.|||Agrawal A, Gupta S. Impact of aging on dendritic cell functions in humans. Ageing Res Rev. 2011;10:336–45.|||Hajishengallis G. Too old to fight? Aging and its toll on innate immunity. Immun ageing. 2010;25:25–37.|||Butcher SK, Chahal H, Nayak L, et al. Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans. J Leukoc Biol. 2001;70:881–6.|||Fülöp T, Fóris G, Wórum I, et al. Age-dependent alterations of Fc gamma receptor-mediated effector functions of human polymorphonuclear leucocytes. Clin Exp Immunol. 1985;61:425–32.|||Panda A, Qian F, Mohanty S, et al. Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J Immunol. 2010;184:2518–27.|||Hearps AC, Martin GE, Angelovich TA, et al. Aging is associated with chronic innate immune activation and dysregulation of monocyte phenotype and function. Aging Cell. 2012;11:867–75.|||Kono H, Rock KL. How dying cells alert the immune system to danger. Nat Rev Immunol. 2008;8:279–89.|||Rabadi MM, Ghaly T, Goligorksy MS, et al. HMGB1 in renal ischemic injury. Am J Physiol Renal Physiol. 2012;303:F873–85.|||Rosin DL, Okusa MD. Dangers within: DAMP responses to damage and cell death in kidney disease. J Am Soc Nephrol. 2011;22:416–25.|||Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120:483–95.|||Fan Q, Chen M, Fang X, et al. Aging might augment reactive oxygen species (ROS) formation and affect reactive nitrogen species (RNS) level after myocardial ischemia/reperfusion in both humans and rats. Age (Dordr) 2013;35:1017–26.|||Benito MJ, Lopez-Hoyos M, Fernandez-Fresnedo G, et al. Changes in the expression of the immunoglobulin-like transcript 3 (ILT3) and ILT4 receptors in renal allograft recipients: effect of donor and recipient aging. Transplant Proc. 2008;40:2894–6.|||Melk A, Halloran PF. Cell senescence and its implications for nephrology. J Am Soc Nephrol. 2001;12:385–93.