Chronic resveratrol intake reverses pro-inflammatory cytokine profile and oxidative DNA damage in ageing hybrid mice

Age

Volumn 33, Issue 3, 2011, Pages 229-246

  Wong, Yee Ting ^a,b   Gruber, Jan ^b   Jenner, Andrew M ^b   Tay, Francis Eng Hock ^a,b   Ruan, Runsheng ^a  

^a INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Aging; Cytokines; Inflammation; Oxidative DNA damage; Resveratrol; Surface markers; T lymphocytes

Indexed keywords

CELL SURFACE MARKER; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; RESVERATROL;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD25+ T LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD72 GENE; CD8+ T LYMPHOCYTE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CYTOKINE RESPONSE; DNA DAMAGE; DNA MICROARRAY; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; GENE; GENE EXPRESSION REGULATION; LOW DRUG DOSE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION;

AGING; ANIMALS; ANTIGENS, SURFACE; ANTIOXIDANTS; CELL COUNT; CYTOKINES; DNA DAMAGE; INFLAMMATION; MICE; MICE, INBRED STRAINS; MODELS, ANIMAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; SPLEEN; STILBENES; T-LYMPHOCYTE SUBSETS;

EID: 80655132173     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-010-9174-4     Document Type: Article

References (78)

1. Adolfsson O, Huber BT, Meydani SN (2001) Vitamin E-enhanced IL-2 production in old mice: naive but not memory T cells show increased cell division cycling and IL-2-producing capacity. J Immunol 167(7):3809-3817 (Pubitemid 32910826)
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(6):560-566
3. Ansar Ahmed S, Dauphinee MJ, Montoya AI, Talal N (1989) Estrogen induces normal murine CD5+ B cells to produce autoantibodies. J Immunol 142(8):2647-2653 (Pubitemid 19115776)
4. Aspinall R, Andrew D (2000) Thymic atrophy in the mouse is a soluble problem of the thymic environment. Vaccine 18 (16):1629-1637 (Pubitemid 30109520)
5. Aw D, Silva AB, Palmer DB (2007) Immunosenescence: emerging challenges for an ageing population. Immunology 120(4):435-446 (Pubitemid 46365019)
6. Aw D, Silva AB, Maddick M, von Zglinicki T, Palmer DB (2008) Architectural changes in the thymus of aging mice. Aging Cell 7(2):158-167 (Pubitemid 351359649)
7. Baur JA, Sinclair DA (2006) Therapeutic potential of resver-atrol: the in vivo evidence. Nat Rev Drug Discov 5 (6):493-506 (Pubitemid 44136961)
8. Bisht K, Wagner KH, Bulmer AC (2009) Curcumin, resveratrol and flavonoids as anti-inflammatory, cyto-and DNA-protective dietary compounds. Toxicology doi:10.1016/ j.tox.2009.11.008
9. Bonafe M, Valensin S, Gianni W, Marigliano V, Franceschi C (2001) The unexpected contribution ofimmunosenescence to the leveling off of cancer incidence and mortality in the oldest old. Crit Rev Oncol Hematol 39(3):227-233 (Pubitemid 32743431)
10. Bruunsgaard H (2002) Effects of tumor necrosis factor-alpha and interleukin-6 in elderly populations. Eur Cytokine Netw 13(4):389-391 (Pubitemid 36174091)
11. Bruunsgaard H, Pedersen BK (2003) Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am 23(1):15-39 (Pubitemid 36268302)
12. Burns EA, Goodwin JS (1997) Immunodeficiency of aging. Drugs Aging 11(5):374-397 (Pubitemid 27483225)
13. Callahan JE, Kappler JW, Marrack P (1993) Unexpected expansions of CD8-bearing cells in old mice. J Immunol 151(12):6657-6669 (Pubitemid 24001040)
14. Castle SC (2000) Clinical relevance of age-related immune dysfunction. Clin Infect Dis 31(2):578-585 (Pubitemid 32289594)
15. Castle S, Uyemura K, Wong W, Modlin R, Effros R (1997) Evidence of enhanced type 2 immune response and impaired upregulation of a type 1 response in frail elderly nursing home residents. Mech Ageing Dev 94(1-3):7-16 (Pubitemid 27216092)
16. Castle SC, Uyemura K, Crawford W, Wong W, Klaustermeyer WB, Makinodan T (1999) Age-related impaired prolifer-ation of peripheral blood mononuclear cells is associated with an increase in both IL-10 and IL-12. Exp Gerontol 34 (2):243-252 (Pubitemid 29153021)
17. Chen J, Astle CM, Harrison DE (1998) Delayed immune aging in diet-restricted B6CBAT6 F1 mice is associated with preservation of naive T cells. J Gerontol A Biol Sci Med Sci 53(5):B330-B337, discussion B338-9 (Pubitemid 29010731)
18. Collins DP, Luebering BJ, Shaut DM (1998) T-lymphocyte functionality assessed by analysis of cytokine receptor expression, intracellular cytokine expression, and femto-molar detection of cytokine secretion by quantitative flow cytometry. Cytometry 33(2):249-255 (Pubitemid 28447151)
19. Das S, Das DK (2007) Anti-inflammatory responses of resveratrol. Inflamm Allergy Drug Targets 6(3):168-173 (Pubitemid 47455785)
20. De la Fuente M, Miquel J (2009) An update of the oxidation-inflammation theory of aging: the involvement of the immune system in oxi-inflamm-aging. Curr Pharm Des 15 (26):3003-3026
21. Dejaco C, Duftner C, Schirmer M (2006) Are regulatory T-cells linked with aging? Exp Gerontol 41(4):339-345
22. Erol A (2007) Interleukin-6 (IL-6) is still the leading biomarker of the metabolic and aging-related disorders. Med Hy-potheses 69(3):708 (Pubitemid 47043244)
23. 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 (9):2375-2378 (Pubitemid 23265910)
24. Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY (2005) A function for interleukin 2 in Foxp3-expressing regula-tory T cells. Nat Immunol 6(11):1142-1151 (Pubitemid 41541792)
25. Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G (2000a) Inflamm-aging. An evolutionary perspective on immunosenescence. Ann NY Acad Sci 908:244-254 (Pubitemid 30462008)
26. Franceschi C, Valensin S, Bonafe M, Paolisso G, Yashin AI, Monti D, De Benedictis G (2000b) The network and the remodeling theories of aging: historical background and new perspectives. Exp Gerontol 35(6-7):879-896
27. 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(1):92-105 (Pubitemid 46073065)
28. Gabriel P, Cakman I, Rink L (2002) Overproduction of monokines by leukocytes after stimulation with lipopoly-saccharide in the elderly. Exp Gerontol 37(2-3):235-247 (Pubitemid 34073540)
29. Gao X, Xu YX, Janakiraman N, Chapman RA, Gautam SC (2001) Immunomodulatory activity of resveratrol: sup-pression of lymphocyte proliferation, development of cell-mediated cytotoxicity, and cytokine production. Biochem Pharmacol 62(9):1299-1308 (Pubitemid 33055634)
30. Gedik CM, Collins A (2005) Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study. Faseb J 19(1):82-84 (Pubitemid 40069925)
31. Globerson A, Effros RB (2000) Ageing of lymphocytes and lymphocytes in the aged. Immunol Today 21(10):515-521
32. Gonzalez-Quintial R, Theofilopoulos AN (1992) V beta gene repertoires in aging mice. J Immunol 149(1):230-236
33. Gregg R, Smith CM, Clark FJ, Dunnion D, Khan N, Chakraverty R, Nayak L, Moss PA (2005) The number of human peripheral blood CD4+ CD25high regulatory T cells increases with age. Clin Exp Immunol 140(3):540-546 (Pubitemid 40813966)
34. Grossmann A, Maggio-Price L, Jinneman JC, Rabinovitch PS (1991) Influence of aging on intracellular free calcium and proliferation of mouse T-cell subsets from various lym-phoid organs. Cell Immunol 135(1):118-131
35. Han GM, Zhao B, Jeyaseelan S, Feng JM (2009) Age-associated parallel increase of Foxp3(+)CD4(+) regulatory and CD44(+)CD4(+) memory T cells in SJL/J mice. Cell Immunol 258(2):188-196
36. Hannet I, Erkeller-Yuksel F, Lydyard P, Deneys V, De Bruyere M (1992) Developmental and maturational changes in human blood lymphocyte subpopulations. Immunol Today 13(6):215-218
37. Harper JM, Galecki AT, Burke DT, Miller RA (2004) Body weight, hormones and T cell subsets as predictors of life span in genetically heterogeneous mice. Mech Ageing Dev 125(5):381-390 (Pubitemid 38595190)
38. Horwitz DA, Zheng SG, Wang J, Gray JD (2008) The real role of TGF-beta in regulatory T cells physiology. Eur J Immunol 38(11):901-937
39. Huang H, Patel DD, Manton KG (2005) The immune system in aging: roles of cytokines, T cells and NK cells. Front Biosci 10:192-215
40. Kiecolt-Glaser JK, Preacher KJ, Mac Callum RC, Atkinson C, Malarkey WB, Glaser R (2003) Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci USA 100(15):9090-9095 (Pubitemid 36899228)
41. Kirschmann DA, Murasko DM (1992) Splenic and inguinal lymph node T cells of aged mice respond differently to polyclonal and antigen-specific stimuli. Cell Immunol 139 (2):426-437
42. Komuro T, Sano K, Asano Y, Tada T (1990) Analysis of age-related degeneracy of T-cell repertoire: localized function-al failure in CD8+ T cells. Scand J Immunol 32(5):545-553 (Pubitemid 20358358)
43. Kowalski J, Samojedny A, Paul M, Pietsz G, Wilczok T (2005) Effect of apigenin, kaempferol and resveratrol on the expression of interleukin-1beta and tumor necrosis factor-alpha genes in J774.2 macrophages. Pharmacol Rep 57 (3):390-394 (Pubitemid 41030701)
44. Krabbe KS, Pedersen M, Bruunsgaard H (2004) Inflammatory mediators in the elderly. Exp Gerontol 39(5):687-699 (Pubitemid 38586809)
45. Kulinsky VI (2007) Biochemical aspects of inflammation. Biochemistry (Mosc) 72(6):595-607 (Pubitemid 47142359)
46. Li DH, Winslow MM, Cao TM, Chen AH, Davis CR, Mellins ED, Utz PJ, Crabtree GR, Parnes JR (2008) Modulation of peripheral B cell tolerance by CD72 in a murine model. Arthritis Rheum 58(10):3192-3204
47. Linton PJ, Haynes L, Klinman NR, Swain SL (1996) Antigen-independent changes in naive CD4 T cells with aging. J Exp Med 184(5):1891-1900 (Pubitemid 26404479)
48. Manna SK, Mukhopadhyay A, Aggarwal BB (2000) Resver-atrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen inter-mediates and lipid peroxidation. J Immunol 164 (12):6509-6519 (Pubitemid 30408836)
49. Mc Elhaney JE, Effros RB (2009) Immunosenescence: what does it mean to health outcomes in older adults? Curr Opin Immunol 21(4):418-424
50. Miller RA (1996) The aging immune system: primer and prospectus. Science 273(5271):70-74 (Pubitemid 26255423)
51. Miller RA (1997) Age-related changes in T cell surface markers: a longitudinal analysis in genetically heteroge-neous mice. Mech Ageing Dev 96(1-3):181-196 (Pubitemid 27279825)
52. Miller RA (2001) Biomarkers of aging: prediction oflongevity by using age-sensitive T-cell subset determinations in a middle-aged, genetically heterogeneous mouse population. J Gerontol A Biol Sci Med Sci 56(4):B180-B186 (Pubitemid 32290883)
53. Miller JF (2002) The discovery of thymus function and of thymus-derived lymphocytes. Immunol Rev 185:7-14 (Pubitemid 34994926)
54. Nagel JE, Chopra RK, Chrest FJ, Mc Coy MT, Schneider EL, Holbrook NJ, Adler WH (1988) Decreased proliferation, interleukin 2 synthesis, and interleukin 2 receptor expres-sion are accompanied by decreased m RNA expression in phytohemagglutinin-stimulated cells from elderly donors. J Clin Invest 81(4):1096-1102
55. Nikolich-Zugich J, Messaoudi I (2005) Mice and flies and monkeys too: caloric restriction rejuvenates the aging immune system of non-human primates. Exp Gerontol 40 (11):884-893 (Pubitemid 41540438)
56. Ostan R, Bucci L, Capri M, Salvioli S, Scurti M, Pini E, Monti D, Franceschi C (2008) Immunosenescence and immuno-genetics of human longevity. Neuroimmunomodulation 15 (4-6):224-240
57. Pahlavani MA (2004) Influence of caloric restriction on aging immune system. J Nutr Health Aging 8(1):38-47 (Pubitemid 38200261)
58. Park SK, Kim K, Page GP, Allison DB, Weindruch R, Prolla TA (2009) Gene expression profiling of aging in multiple mouse strains: identification of aging biomarkers and impact of dietary antioxidants. Aging Cell 8(4):484-495
59. Pawelec G (1999) Immunosenescence: impact in the young as well as the old? Mech Ageing Dev 108(1):1-7 (Pubitemid 29210235)
60. Pawelec G, Barnett Y, Forsey R, Frasca D, Globerson A, Mc Leod J, Caruso C, Franceschi C, Fulop T, Gupta S, Mariani E, Mocchegiani E, Solana R (2002) T cells and aging, January 2002 update. Front Biosci 7:d1056-d1183
61. Pawelec G, Akbar A, Caruso C, Solana R, Grubeck-Loebenstein B, Wikby A (2005) Human immunosenes-cence: is it infectious? Immunol Rev 205:257-268
62. Pervaiz S, Holme AL, Aggarwal BB, Anekonda TS, Baur JA, Gojkovic-Bukarica L, Ragione FD, Kim AL, Pirola L, Saiko P (2009) Resveratrol: its biologic targets and functional activity. Antioxid Redox Signal 11(11):2851-2897
63. Pfister G, Weiskopf D, Lazuardi L, Kovaiou RD, Cioca DP, Keller M, Lorbeg B, Parson W, Grubeck-Loebenstein B (2006) Naive T cells in the elderly: are they still there? Ann NY Acad Sci 1067:152-157 (Pubitemid 43806319)
64. Rink L, Cakman I, Kirchner H (1998) Altered cytokine production in the elderly. Mech Ageing Dev 102(2-3):199-209 (Pubitemid 28353539)
65. Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, Shimizu J, Takahashi T, Nomura T (2006) Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 212:8-27 (Pubitemid 44116697)
66. Sander M, Avlund K, Lauritzen M, Gottlieb T, Halliwell B, Stevnsner T, Wewer U, Bohr VA (2008) Aging-from molecules to populations. Mech Ageing Dev 129(10):614-623
67. Sansoni P, Vescovini R, Fagnoni F, Biasini C, Zanni F, Zanlari L, Telera A, Lucchini G, Passeri G, Monti D, Franceschi C, Passeri M (2007) The immune system in extreme longevity. Exp Gerontol 43(2):61-65
68. Saule P, Trauet J, Dutriez V, Lekeux V, Dessaint JP, Labalette M (2006) Accumulation of memory T cells from child-hood to old age: central and effector memory cells in CD4 (+) versus effector memory and terminally differentiated memory cells in CD8(+) compartment. Mech Ageing Dev 127(3):274-281 (Pubitemid 43214500)
69. Sharma S, Dominguez AL, Lustgarten J (2006) High accumu-lation of T regulatory cells prevents the activation of immune responses in aged animals. J Immunol 177 (12):8348-8355 (Pubitemid 44893796)
70. Taub DD, Longo DL (2005) Insights into thymic aging and regeneration. Immunol Rev 205:72-93 (Pubitemid 40780178)
71. Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2'- deoxyguanosine (8-OHd G): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27(2):120-139
72. Walford RL (1982) Studies in immunogerontology. J Am Geriatr Soc 30(10):617-625 (Pubitemid 12003742)
73. Weiskopf D, Weinberger B, Grubeck-Loebenstein B (2009) The aging of the immune system. Transpl Int 22 (11):1041-1050
74. Witkowski JM, Miller RA (1993) Increased function of P-glycoprotein in T lymphocyte subsets of aging mice. J Immunol 150(4):1296-1306 (Pubitemid 23127419)
75. Wong YT, Gruber J, Jenner AM, Ng MP, Ruan R, Tay FE (2009) Elevation of oxidative-damage biomarkers during aging in F2 hybrid mice: protection by chronic oral intake of resveratrol. Free Radic Biol Med 46(6):799-809
76. Wu HJ, Bondada S (2009) CD72, a coreceptor with both positive and negative effects on B lymphocyte develop-ment and function. J Clin Immunol 29(1):12-21
77. Wu LL, Chiou CC, Chang PY, Wu JT (2004) Urinary 8-OHd G: a marker of oxidative stress to DNA and a risk factor for cancer, atherosclerosis and diabetics. Clin Chim Acta 339 (1-2):1-9 (Pubitemid 37542453)
78. Zhao L, Sun L, Wang H, Ma H, Liu G, Zhao Y (2007) Changes of CD4+CD25+Foxp3+ regulatory T cells in aged Balb/c mice. J Leukoc Biol 81(6):1386-1394