Global analyses revealed age-related alterations in innate immune responses after stimulation of pathogen recognition receptors

Aging Cell

Volumn 14, Issue 3, 2015, Pages 421-432

  Metcalf, Talibah U ^a   Cubas, Rafael A ^a   Ghneim, Khader ^b   Cartwright, Michael J ^a   Grevenynghe, Julien Van ^c   Richner, Justin M ^d   Olagnier, David P ^a   Wilkinson, Peter A ^b   Cameron, Mark J ^b   Park, Byung S ^e   Hiscott, John B ^a   Diamond, Michael S ^d   Wertheimer, Anne M ^f,g   Nikolich Zugich, Janko ^f,g   Haddad, Elias K ^a  

^a Vaccine and Gene Therapy Institute   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^f UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF ARIZONA   (United States)

Author keywords

Immunosenescence; Innate immune agonists; Innate immunity; Interferon signaling; Pattern recognition receptors; Peripheral blood mononuclear cells

Indexed keywords

CD40 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PATHOGEN RECOGNITION RECEPTOR; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; V SET DOMAIN CONTAINING T CELL ACTIVATION INHIBITOR 1; CHEMOKINE; CYTOKINE;

ADAPTIVE IMMUNITY; ADULT; AGED; AGING; ARTICLE; CD3+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; IMMUNOSTIMULATION; INNATE IMMUNITY; INTERFERON PRODUCTION; LYMPHOCYTE PROLIFERATION; MALE; MEMORY CELL; MIXED LYMPHOCYTE REACTION; MONOCYTE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; UPREGULATION; B LYMPHOCYTE; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MONONUCLEAR CELL; VERY ELDERLY; YOUNG ADULT;

ADAPTIVE IMMUNITY; ADULT; AGED; AGED, 80 AND OVER; AGING; B-LYMPHOCYTES; CHEMOKINES; CYTOKINES; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MONOCYTES; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84927711067     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12320     Document Type: Article

References (49)

1. Abb J, Abb H, Deinhardt F (1984) Age-related decline of human interferon alpha and interferon gamma production. Blut 48, 285-289.
2. Alberti S, Cevenini E, Ostan R, Capri M, Salvioli S, Bucci L, Ginaldi L, De Martinis M, Franceschi C, Monti D (2006) Age-dependent modifications of Type 1 and Type 2 cytokines within virgin and memory CD4+ T cells in humans. Mech. Ageing Dev. 127, 560-566.
3. Alvarez-Rodriguez L, Lopez-Hoyos M, Munoz-Cacho P, Martinez-Taboada VM (2012) Aging is associated with circulating cytokine dysregulation. Cell. Immunol. 273, 124-132.
4. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.
5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300.
6. Borson S, Scanlan JM, Chen P, Ganguli M (2003) The Mini-Cog as a screen for dementia: validation in a population-based sample. J. Am. Geriatr. Soc. 51, 1451-1454.
7. Bouillon K, Kivimaki M, Hamer M, Sabia S, Fransson EI, Singh-Manoux A, Gale CR, Batty GD (2013) Measures of frailty in population-based studies: an overview. BMC Geriatr. 13, 64.
8. Canaday DH, Parker KE, Aung H, Chen HE, Nunez-Medina D, Burant CJ (2013) Age-dependent changes in the expression of regulatory cell surface ligands in activated human T-cells. BMC Immunol. 14, 45.
9. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25, 288-289.
10. Colonna-Romano G, Bulati M, Aquino A, Scialabba G, Candore G, Lio D, Motta M, Malaguarnera M, Caruso C (2003) B cells in the aged: CD27, CD5, and CD40 expression. Mech. Ageing Dev. 124, 389-393.
11. Commins SP, Borish L, Steinke JW (2010) Immunologic messenger molecules: cytokines, interferons, and chemokines. J. Allergy Clin. Immunol. 125, S53-S72.
12. van Duin D, Allore HG, Mohanty S, Ginter S, Newman FK, Belshe RB, Medzhitov R, Shaw AC (2007a) Prevaccine determination of the expression of costimulatory B7 molecules in activated monocytes predicts influenza vaccine responses in young and older adults. J. Infect. Dis. 195, 1590-1597.
13. van Duin D, Mohanty S, Thomas V, Ginter S, Montgomery RR, Fikrig E, Allore HG, Medzhitov R, Shaw AC (2007b) Age-associated defect in human TLR-1/2 function. J. Immunol. 178, 970-975.
14. Fagiolo U, Cossarizza A, Scala E, Fanales-Belasio E, Ortolani C, Cozzi E, Monti D, Franceschi C, Paganelli R (1993) Increased cytokine production in mononuclear cells of healthy elderly people. Eur. J. Immunol. 23, 2375-2378.
15. Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F, Panourgia MP, Invidia L, Celani L, Scurti M, Cevenini E, Castellani GC, Salvioli S (2007) Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech. Ageing Dev. 128, 92-105.
16. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC, Horton HF, Fouser L, Carter L, Ling V, Bowman MR, Carreno BM, Collins M, Wood CR, Honjo T (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192, 1027-1034.
17. Gaucher D, Therrien R, Kettaf N, Angermann BR, Boucher G, Filali-Mouhim A, Moser JM, Mehta RS, Drake DR 3rd, Castro E, Akondy R, Rinfret A, Yassine-Diab B, Said EA, Chouikh Y, Cameron MJ, Clum R, Kelvin D, Somogyi R, Greller LD, Balderas RS, Wilkinson P, Pantaleo G, Tartaglia J, Haddad EK, Sekaly RP (2008) Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J. Exp. Med. 205, 3119-3131.
18. Gavazzi G, Krause KH (2002) Ageing and infection. Lancet. Infect. Dis. 2, 659-666.
19. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
20. Gomez CR, Boehmer ED, Kovacs EJ (2005) The aging innate immune system. Curr. Opin. Immunol. 17, 457-462.
21. Gon Y, Hashimoto S, Hayashi S, Koura T, Matsumoto K, Horie T (1996) Lower serum concentrations of cytokines in elderly patients with pneumonia and the impaired production of cytokines by peripheral blood monocytes in the elderly. Clin. Exp. Immunol. 106, 120-126.
22. Goulet ML, Olagnier D, Xu Z, Paz S, Belgnaoui SM, Lafferty EI, Janelle V, Arguello M, Paquet M, Ghneim K, Richards S, Smith A, Wilkinson P, Cameron M, Kalinke U, Qureshi S, Lamarre A, Haddad EK, Sekaly RP, Peri S, Balachandran S, Lin R, Hiscott J (2013) Systems analysis of a RIG-I agonist inducing broad spectrum inhibition of virus infectivity. PLoS Pathog. 9, e1003298.
23. Hearps AC, Martin GE, Angelovich TA, Cheng WJ, Maisa A, Landay AL, Jaworowski A, Crowe SM (2012) Aging is associated with chronic innate immune activation and dysregulation of monocyte phenotype and function. Aging Cell 11, 867-875.
24. da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
25. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J (2003) Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 19, 225-234.
26. Jing Y, Shaheen E, Drake RR, Chen N, Gravenstein S, Deng Y (2009) Aging is associated with a numerical and functional decline in plasmacytoid dendritic cells, whereas myeloid dendritic cells are relatively unaltered in human peripheral blood. Hum. Immunol. 70, 777-784.
27. Katz S, Downs TD, Cash HR, Grotz RC (1970) Progress in development of the index of ADL. Gerontologist 10, 20-30.
28. Katz JM, Plowden J, Renshaw-Hoelscher M, Lu X, Tumpey TM, Sambhara S (2004) Immunity to influenza: the challenges of protecting an aging population. Immunol. Res. 29, 113-124.
29. Kinsella K, Wan H (2009). An Aging World: 2008, International Population Reports P95/09-1. (USC Bureau, eds). Washington, DC: U.S. Government Printing Office.
30. Kong KF, Delroux K, Wang X, Qian F, Arjona A, Malawista SE, Fikrig E, Montgomery RR (2008) Dysregulation of TLR3 impairs the innate immune response to West Nile virus in the elderly. J. Virol. 82, 7613-7623.
31. Leng Q, Bentwich Z, Borkow G (2002) CTLA-4 upregulation during aging. Mech. Ageing Dev. 123, 1419-1421.
32. Linterman MA (2014) How T follicular helper cells and the germinal centre response change with age. Immunol. Cell Biol. 92, 72-79.
33. Molteni M, Della Bella S, Mascagni B, Coppola C, De Micheli V, Zulian C, Birindelli S, Vanoli M, Scorza R (1994) Secretion of cytokines upon allogeneic stimulation: effect of aging. J. Biol. Regul. Homeost. Agents 8, 41-47.
34. Nakaya HI, Wrammert J, Lee EK, Racioppi L, Marie-Kunze S, Haining WN, Means AR, Kasturi SP, Khan N, Li GM, McCausland M, Kanchan V, Kokko KE, Li S, Elbein R, Mehta AK, Aderem A, Subbarao K, Ahmed R, Pulendran B (2011) Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 12, 786-795.
35. Nikolich-Zugich J (2008) Ageing and life-long maintenance of T-cell subsets in the face of latent persistent infections. Nature reviews. Immunology 8, 512-522.
36. Ouyang Q, Cicek G, Westendorp RG, Cools HJ, van der Klis RJ, Remarque EJ (2000) Reduced IFN-gamma production in elderly people following in vitro stimulation with influenza vaccine and endotoxin. Mech. Ageing Dev. 121, 131-137.
37. Panda A, Arjona A, Sapey E, Bai F, Fikrig E, Montgomery RR, Lord JM, Shaw AC (2009) Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol. 30, 325-333.
38. Panda A, Qian F, Mohanty S, van Duin D, Newman FK, Zhang L, Chen S, Towle V, Belshe RB, Fikrig E, Allore HG, Montgomery RR, Shaw AC (2010) Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J. Immunol. 184, 2518-2527.
39. Pulsatelli L, Meliconi R, Mazzetti I, Dolzani P, Meneghetti A, Neri S, Silvestri T, Ravaglia G, Forti P, Facchini A, Mariani E (2000) Chemokine production by peripheral blood mononuclear cells in elderly subjects. Mech. Ageing Dev. 121, 89-100.
40. Qian F, Wang X, Zhang L, Chen S, Piecychna M, Allore H, Bockenstedt L, Malawista S, Bucala R, Shaw AC, Fikrig E, Montgomery RR (2012) Age-associated elevation in TLR5 leads to increased inflammatory responses in the elderly. Aging Cell 11, 104-110.
41. R Core Team (2010) R: A Language and Environment for Statistical computing. Vienna, Austria: R Foundation for Statistical computing.
42. Samuel MA, Diamond MS (2005) Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J. Virol. 79, 13350-13361.
43. Seidler S, Zimmermann HW, Bartneck M, Trautwein C, Tacke F (2010) Age-dependent alterations of monocyte subsets and monocyte-related chemokine pathways in healthy adults. BMC Immunol. 11, 30.
44. Shaw AC, Panda A, Joshi SR, Qian F, Allore HG, Montgomery RR (2011) Dysregulation of human Toll-like receptor function in aging. Ageing Res. Rev. 10, 346-353.
45. Smyth G, (2005). Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor (Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W ed.). New York, NY: Springer, pp. 397-420.
46. Solana R, Tarazona R, Gayoso I, Lesur O, Dupuis G, Fulop T (2012) Innate immunosenescence: effect of aging on cells and receptors of the innate immune system in humans. Semin. Immunol. 24, 331-341.
47. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550.
48. You J, Dong H, Mann ER, Knight SC, Yaqoob P (2013) Ageing impairs the T cell response to dendritic cells. Immunobiology 218, 1077-1084.
49. Zhu LM, Fang YS, Sun ZG, Yu LZ, Xu H (2012) Monocyte-derived CD40 expression is regulated by interferon-gamma/interferon-gamma receptor-1 pathway when acting as a bridge during their interaction with T cells and allogeneic endothelial cells. Transpl. Proc. 44, 996-998.