Cytomegalovirus is associated with reduced telomerase activity in the Whitehall II cohort

Experimental Gerontology

Volumn 48, Issue 4, 2013, Pages 385-390

  Dowd, Jennifer B ^a,b   Bosch, Jos A ^c,d   Steptoe, Andrew ^e   Blackburn, Elizabeth H ^f   Lin, Jue ^f   Rees Clayton, Erin ^g   Aiello, Allison E ^g  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Cytomegalovirus; Infections; Telomerase; Telomeres; Whitehall II

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; TELOMERASE;

ADULT; AGED; ANTIBODY DETECTION; ARTICLE; CELL AGING; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SEX DIFFERENCE; TELOMERE HOMEOSTASIS; VIRUS REACTIVATION;

AGE FACTORS; AGED; ANTIBODIES, VIRAL; ASYMPTOMATIC INFECTIONS; COHORT STUDIES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; HUMANS; IMMUNOGLOBULIN G; MALE; MIDDLE AGED; RISK FACTORS; SEROLOGIC TESTS; SEX FACTORS; T-LYMPHOCYTES; TELOMERASE; TELOMERE; TELOMERE SHORTENING; VIRUS ACTIVATION;

EID: 84874679009     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2013.01.016     Document Type: Article

References (67)

1. Aiello A.E., Haan M.N., Blythe L., Moore K., Gonzalez J.M., Jagust W. The influence of latent viral infection on rate of cognitive decline over 4years. J. Am. Geriatr. Soc. 2006, 54:1046-1054.
2. Akbar A.N., Henson S.M. Are senescence and exhaustion intertwined or unrelated processes that compromise immunity?. Nat. Rev. Immunol. 2011, 11:289-295.
3. Armanios M., Blackburn E.H. The telomere syndromes. Nat. Rev. Genet. 2012, 13:693-704.
4. Baird D.M., Kipling D. The extent and significance of telomere loss with age. Ann. N. Y. Acad. Sci. 2004, 1019:265-268.
5. Bakaysa S., Mucci L., Slagboom P.E., Boomsma D.I., McClearn G.E., Johansson B., Pedersen N.L. Telomere length predicts survival independent of genetic influences. Aging Cell 2007, 6:769-774.
6. Bate S.L., Dollard S.C., Cannon M.J. Cytomegalovirus seroprevalence in the United States: The National Health and Nutrition Examination Surveys, 1988-2004. Clin. Infect. Dis. 2010, 50:1439-1447.
7. Blackburn E.H. Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett. 2005, 579:859-862.
8. Blackburn E.H., Greider C.W., Szostak J.W. Telomeres and telomerase: the path from maize, tetrahymena and yeast to human cancer and aging. Nat. Med. 2006, 12:1133-1138.
9. Blum A., Peleg A., Weinberg M. Anti-cytomegalovirus (CMV) IgG antibody titer in patients with risk factors to atherosclerosis. Clin. Exp. Med. 2003, 3:157-160.
10. Brouilette S., Singh R.K., Thompson J.R., Goodall A.H., Samani N.J. White cell telomere length and risk of premature myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 2003, 23:842-846.
11. Buka S.L., Tsuang M.T., Torrey E., Klebanoff M.A., Bernstein D., Yolken R.H. Maternal infections and subsequent psychosis among offspring. Arch. Gen. Psychiatry 2001, 58:1032-1037.
12. Cannon M., Schmid D.S., Hyde T. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev. Med. Virol. 2010, 20:202-213.
13. Cawthon R.M. Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res. 2009, 37:e21.
14. Cawthon R.M., Smith K.R., O'Brien E., Sivatchenko A., Kerber R.A. Association between telomere length in blood and mortality in people aged 60years or older. Lancet 2003, 361:393-395.
15. Choi J., Fauce S.R., Effros R.B. Reduced telomerase activity in human T lymphocytes exposed to cortisol. Brain Behav. Immun. 2008, 22:600-605.
16. Colugnati F.A., Staras S.A., Dollard S.C., Cannon M.J. Incidence of cytomegalovirus infection among the general population and pregnant women in the United States. BMC Infect. Dis. 2007, 7:71.
17. Demissie S., Levy D., Benjamin E.J., Cupples L.A., Gardner J.P., Herbert A., Kimura M., Larson M.G., Meigs J.B., Keaney J.F., Aviv A. Insulin resistance, oxidative stress, hypertension, and leukocyte telomere length in men from the Framingham Heart Study. Aging Cell 2006, 5:325-330.
18. Dock J.N. Role of CD8 T cell replicative senescence in human aging and in HIV-mediated immunosenescence. Aging Dis. 2011, 2:382-397.
19. Donate L.E., Blasco M.A. Telomeres in cancer and ageing. Philos. Trans. R Soc. Lond. B Biol. Sci. 2011, 366:76-84.
20. Edwards K.M., Bosch J.A., Engeland C.G., Cacioppo J.T., Marucha P.T. Elevated macrophage migration inhibitory factor (MIF) is associated with depressive symptoms, blunted cortisol reactivity to acute stress, and lowered morning cortisol. Brain Behav. Immun. 2010, 24:1202-1208.
21. Effros R.B. Telomere/telomerase dynamics within the human immune system: effect of chronic infection and stress. Exp. Gerontol. 2011, 46:135-140.
22. Epel E.S., Lin J., Dhabhar F.S., Wolkowitz O.M., Puterman E., Karan L., Blackburn E.H. Dynamics of telomerase activity in response to acute psychological stress. Brain Behav. Immun. 2010, 24:531-539.
23. Gabriele S., Thomas Z. Replicative aging, telomeres, and oxidative stress. Ann. N. Y. Acad. Sci. 2002, 959:24-29.
24. Gattone M., Iacoviello L., Colombo M., Castelnuovo A.D., Soffiantino F., Gramoni A., Picco D., Benedetta M., Giannuzzi P. Chlamydia pneumoniae and cytomegalovirus seropositivity, inflammatory markers, and the risk of myocardial infarction at a young age. Am. Hear. J. 2001, 142:633-640.
25. Gladych M., Wojtyla A., Rubis B. Human telomerase expression regulation. Biochem. Cell Biol. 2011, 89:359-376.
26. Hecker M., Qiu D., Marquardt K., Bein G., Hackstein H. Continuous cytomegalovirus seroconversion in a large group of healthy blood donors. Vox Sang. 2004, 86:41-44.
27. Hodes R.J., Hathcock K.S., Weng N.-p. Telomeres in T and B cells. Nat. Rev. Immunol. 2002, 2:699-706.
28. Honig L., Schupf Nicole, Lee Joseph H., Tang Ming X., Mayeux Richard Shorter telomeres are associated with mortality in those with APOE ε4 and dementia. Ann. Neurol. 2006, 60:181-187.
29. Ilmonen P., Kotrschal A., Penn D.J. Telomere attrition due to infection. PLoS One 2008, 3:e2143.
30. Imanishi T. Estrogen reduces endothelial progenitor cell senescence through augmentation of telomerase activity. J. Hypertens. 2005, 23:1699-1706.
31. Iwama H., Ohyashiki K., Ohyashiki J.H., Hayashi S., Yahata N., Ando K., Toyama K., Hoshika A., Takasaki M., Mori M., Shay J.W. Telomeric length and telomerase activity vary with age in peripheral blood cells obtained from normal individuals. Hum. Genet. 1998, 102:397-402.
32. Kroenke C.H., Pletcher M.J., Lin J., Blackburn E., Adler N., Matthews K., Epel E. Telomerase, telomere length, and coronary artery calcium in black and white men in the CARDIA study. Atherosclerosis 2012, 220:506-512.
33. Kuo C.P., Wu C.L., Ho H.T., Chen C.G., Liu S.I., Lu Y.T. Detection of cytomegalovirus reactivation in cancer patients receiving chemotherapy. Clin. Microbiol. Infect. 2008, 14:221-227.
34. Lathey J.L., Spector S.A. Unrestricted replication of human cytomegalovirus in hydrocortisone-treated macrophages. J. Virol. 1991, 65:6371-6375.
35. Lee D.-C., Im J.-A., Kim J.-H., Lee H.-R., Shim J.-Y. Effect of long-term hormone therapy on telomere length in postmenopausal women. Yonsei Med. J. 2005, 46:471-479.
36. Lin J., Epel E., Cheon J., Kroenke C., Sinclair E., Bigos M., Wolkowitz O., Mellon S., Blackburn E. Analyses and comparisons of telomerase activity and telomere length in human T and B cells: insights for epidemiology of telomere maintenance. J. Immunol. Methods 2010, 352:71-80.
37. Martin-Ruiz C., Dickinson H.O., Keys B., Rowan E., Kenny R.A., Von Zglinicki T. Telomere length predicts poststroke mortality, dementia, and cognitive decline. Ann. Neurol. 2006, 60:174-180.
38. Matthews K., Schwartz J., Cohen S., Seeman T. Diurnal cortisol decline is related to coronary calcification: CARDIA study. Psychosom. Med. 2006, 68:657-661.
39. Miller A.H., Ancoli-Israel S., Bower J.E., Capuron L., Irwin M.R. Neuroendocrine-immune mechanisms of behavioral comorbidities in patients with cancer. J. Clin. Oncol. 2008, 26:971-982.
40. Moss P. The emerging role of cytomegalovirus in driving immune senescence: a novel therapeutic opportunity for improving health in the elderly. Curr. Opin. Immunol. 2010, 22:529-534.
41. Mostad S.B., Kreiss J.K., Ryncarz A., Chohane B., Mandaliya K., Ndinya-Achola J., Bwayo J.J., Corey L. Cervical shedding of herpes simplex virus and cytomegalovirus throughout the menstrual cycle in women infected with human immunodeficiency virus type 1. Am. J. Obstet. Gynecol. 2000, 183:948-955.
42. Nieto F.J. Infections and atherosclerosis: new clues from an old hypothesis?. Am. J. Epidemiol. 1998, 148:937-948.
43. Pawelec G., Akbar A., Caruso C., Effros R., Grubeck-Loebenstein B., Wikby A. Is immunosenescence infectious?. Trends Immunol. 2004, 25:406-410.
44. Pawelec G., Akbar A., Caruso C., Solana R., Grubeck-Loebenstein B., Wikby A. Human immunosenescence: is it infectious?. Immunol. Rev. 2005, 205:257-268.
45. Pawelec G., Derhovanessian E., Larbi A., Strindhall J., Wikby A. Cytomegalovirus and human immunosenescence. Rev. Med. Virol. 2009, 19:47-56.
46. Pawelec G., McElhaney J.E., Aiello A.E., Derhovanessian E. The impact of CMV infection on survival in older humans. Curr. Opin. Immunol. 2012, 24(4):507-511.
47. Pourgheysari B., Khan N., Best D., Bruton R., Nayak L., Moss P.A.H. The cytomegalovirus-specific CD4+ T-cell response expands with age and markedly alters the CD4+ T-cell repertoire. J. Virol. 2007, 81:7759-7765.
48. Roberts E., Haan M., Dowd J., Aiello A. Cytomegalovirus antibody levels, inflammation, and mortality among elderly Latinos over 9years of follow-up. Am. J. Epidemiol. 2010, 172:363-371.
49. Rufer N., Brmmendorf T.H., Kolvraa S., Bischoff C., Christensen K., Wadsworth L., Schulzer M., Lansdorp P.M. Telomere fluorescence measurements in granulocytes and T lymphocyte subsets point to a high turnover of hematopoietic stem cells and memory t cells in early childhood. J Exp. Med. 1999, 190:157-168.
50. Sanders J.L., Fitzpatrick A.L., Boudreau R.M., Arnold A.M., Aviv A., Kimura M., Fried L.F., Harris T.B., Newman A.B. Leukocyte telomere length is associated with noninvasively measured age-related disease: the Cardiovascular Health Study. J. Gerontol. A Biol. Sci. Med. Sci. 2012, 67A:409-416.
51. Schmaltz H.N., Fried L.P., Xue Q.L., Walston J., Leng S.X., Semba R.D. Chronic cytomegalovirus infection and inflammation are associated with prevalent frailty in community-dwelling older women. J. Am. Geriatr. Soc. 2005, 53:747-754.
52. Sorlie P.D., Nieto F.J., Adam E., Folsom A.R., Shahar E., Massing M. A prospective study of cytomegalovirus, herpes Simplex Virus 1, and coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) Study. Arch. Intern. Med. 2000, 160:2027-2032.
53. Speir E., Yu Z.-X., Takeda K., Ferrans V.J., Cannon R.O. Antioxidant effect of estrogen on cytomegalovirus-induced gene expression in coronary artery smooth muscle cells. Circulation 2000, 102:2990-2996.
54. Steptoe A., Gylfe, Shamaei-Tousi A., Bergstrom S., Henderson B. Pathogen burden and cortisol profiles over the day. Epidemiol. Infect. 2009, 137(12):1816-1824. (Dec).
55. Steptoe A., Hamer M., O'Donnell K., Venuraju S., Marmot M.G., Lahiri A. Socioeconomic Status and subclinical coronary disease in the Whitehall II Epidemiological Study. PLoS One 2010, 5:e8874.
56. Strandberg T.E., Pitkala K.H., Linnavuori K., Tilvis R.S. Cognitive impairment and infectious burden in the elderly. Arch. Gerontol. Geriatr. Suppl. 2004, 9:419-423.
57. Sylwester A.W., Mitchell B.L., Edgar J.B., Taormina C., Pelte C., Ruchti F., Sleath P.R., Grabstein K.H., Hosken N.A., Kern F., Nelson J.A., Picker L.J. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 2005, 202:673-685.
58. Trevisan M., Matkovic U., Cusinato R., Toppo S., Pal G., Barzon L. Human cytomegalovirus productively infects adrenocortical cells and induces an early cortisol response. J. Cell. Physiol. 2009, 221:629-641.
59. Trzonkowski P., Mysliwska J., Szmit E., Wieckiewicz J., Lukaszuk K., Brydak L.B., Machala M., Mysliwski A. Association between cytomegalovirus infection, enhanced proinflammatory response and low level of anti-hemagglutinins during the anti-influenza vaccination - an impact of immunosenescence. Vaccine 2003, 21:3826-3836.
60. Turner J.E., Burns V.E., Edwards K.E., Moss P.A., Pawelec G., Long J., Bosch J.A. A Mild Immune Risk Profile in CMV Seropositive Healthy Young Adults 2012.
61. Valdes A.M., Andrew T., Gardner J.P., Kimura M., Oelsner E., Cherkas L.F., Aviv A., Spector T.D. Obesity, cigarette smoking, and telomere length in women. Lancet 2005, 366:662-664.
62. Valenzuela H.F., Effros R.B. Divergent telomerase and CD28 expression patterns in human CD4 and CD8 T cells following repeated encounters with the same antigenic stimulus. Clin. Immunol. 2002, 105:117-125.
63. van de Berg P.J.E.J., Griffiths S.J., Yong S.-L., Macaulay R., Bemelman F.J., Jackson S., Henson S.M., ten Berge I.J.M., Akbar A.N., van Lier R.A.W. Cytomegalovirus infection reduces telomere length of the circulating T cell pool. J. Immunol. 2010, 184:3417-3423.
64. van Zanten J., Harmsen M.C., van der Giessen M., van der Bij W., Prop J., de Leij L., The T.H. Humoral immune response against human cytomegalovirus (HCMV)-specific proteins after HCMV infection in lung transplantation as detected with recombinant and naturally occurring proteins. Clin. Diagn. Lab. Immunol. 1995, 2:214-218.
65. Wang Z., Kyo S., Takakura M., Tanaka M., Yatabe N., Maida Y., Fujiwara M., Hayakawa J., Ohmichi M., Koike K., Inoue M. Progesterone regulates human telomerase reverse transcriptase gene expression via activation of mitogen-activated protein kinase signaling pathway. Cancer Res. 2000, 60:5376-5381.
66. Weng N.-p. Telomeres and immune competency. Curr. Opin. Immunol. 2012, 24:470-475.
67. Zglinicki T.v., Saretzki G., Ladhoff J., Fagagna F.d.A.d., Jackson S.P. Human cell senescence as a DNA damage response. Mech. Ageing. Dev. 2005, 126:111-117.