Independent skewing of the T cell and NK cell compartments associated with cytomegalovirus infection suggests division of labor between innate and adaptive immunity

Age

Volumn 36, Issue 2, 2014, Pages 571-582

  Bengnér, Malin ^a   Béziat, Vivien ^b   Ernerudh, Jan ^c   Nilsson, Bengt Olof ^a   Löfgren, Sture ^a   Wikby, Anders ^d   Malmberg, Karl Johan ^b,e,f   Strindhall, Jan ^d  

^a RYHOV COUNTY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c LINKÖPING UNIVERSITY   (Sweden)

^d JÖNKÖPING UNIVERSITY   (Sweden)

^e OSLO UNIVERSITY HOSPITAL   (Norway)

^f UNIVERSITY OF OSLO   (Norway)

Author keywords

Cytomegalovirus; Immune risk profile; Immunosenescence; Natural killer cells

Indexed keywords

CD4 ANTIGEN; CD57 ANTIGEN; CD8 ANTIGEN; CELL PROTEIN; ILT 2 PROTEIN; NKG2C PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; AGED; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; FEMALE; FLOW CYTOMETRY; HUMAN; INNATE IMMUNITY; MALE; NATURAL KILLER CELL; NORMAL HUMAN; PROTEIN EXPRESSION; SERODIAGNOSIS; SEROLOGY; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; AGED; ANTIBODIES, ANTI-IDIOTYPIC; ANTIBODIES, VIRAL; CD4-CD8 RATIO; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNITY, INNATE; IMMUNOGLOBULIN G; KILLER CELLS, NATURAL; MALE;

EID: 84898630754     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-013-9587-y     Document Type: Article

References (44)

1. Beziat V, Dalgard O, Asselah T, Halfon P, Bedossa P, Boudifa A, Hervier B, Theodorou I, Martinot M, Debre P, Bjorkstrom NK, Malmberg KJ, Marcellin P, Vieillard V (2012) CMV drives clonal expansion of NKG2C + NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur J Immunol 42(2):447-457. doi: 10.1002/eji.201141826
2. Beziat V, Liu L, Malmberg JA, Ivarsson MA, Sohlberg E, Bjorklund AT, Retiere C, Sverremark-Ekstrom E, Traherne J, Ljungman P, Schaffer M, Price DA, Trowsdale J, Michaelsson J, Ljunggren HG, Malmberg KJ (2013) NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 121(14):2678-2688. doi: 10.1182/blood-2012- 10-459545
3. Biron CA, Byron KS, Sullivan JL (1989) Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med 320(26):1731-1735. doi: 10.1056/nejm198906293202605
4. Biron CA, Su HC, Orange JS (1996) Function and regulation of natural killer (NK) cells during viral infections: characterization of responses in vivo. Methods 9(2):379-393
5. Bjorkstrom NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, Michaelsson J, Malmberg KJ, Klingstrom J, Ahlm C, Ljunggren HG (2011) Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 208(1):13-21. doi: 10.1084/jem.20100762
6. Chidrawar S, Khan N, Wei W, McLarnon A, Smith N, Nayak L, Moss P (2009) Cytomegalovirus-seropositivity has a profound influence on the magnitude of major lymphoid subsets within healthy individuals. Clin Exp Immunol 155(3):423-432. doi: 10.1111/j.1365-2249.2008.03785.x
7. Cicin-Sain L, Brien JD, Uhrlaub JL, Drabig A, Marandu TF, Nikolich-Zugich J (2012) Cytomegalovirus infection impairs immune responses and accentuates T-cell pool changes observed in mice with aging. PLoS Pathog 8(8):e1002849. doi: 10.1371/journal.ppat.1002849
8. Davis MM (2008) A prescription for human immunology. Immunity 29(6):835-838. doi: 10.1016/j.immuni.2008.12.003
9. Derhovanessian E, Maier AB, Beck R, Jahn G, Hahnel K, Slagboom PE, de Craen AJ, Westendorp RG, Pawelec G (2010) Hallmark features of immunosenescence are absent in familial longevity. J Immunol 185(8):4618-4624. doi: 10.4049/jimmunol.1001629
10. Ferguson FG, Wikby A, Maxson P, Olsson J, Johansson B (1995) Immune parameters in a longitudinal study of a very old population of Swedish people: a comparison between survivors and nonsurvivors. J Gerontol A Biol Sci Med Sci 50(6):B378-382
11. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, Lopez-Verges S, Lanier LL, Weisdorf D, Miller JS (2012) Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C + natural killer cells with potent function. Blood 119(11):2665-2674. doi: 10.1182/blood-2011-10-386995
12. Gillespie GM, Wills MR, Appay V, O'Callaghan C, Murphy M, Smith N, Sissons P, Rowland-Jones S, Bell JI, Moss PA (2000) Functional heterogeneity and high frequencies of cytomegalovirus-specific CD8(+) T lymphocytes in healthy seropositive donors. J Virol 74(17):8140-8150
13. Grubeck-Loebenstein B, Della Bella S, Iorio AM, Michel JP, Pawelec G, Solana R (2009) Immunosenescence and vaccine failure in the elderly. Aging Clin Exp Res 21(3):201-209
14. Guma M, Angulo A, Vilches C, Gomez-Lozano N, Malats N, Lopez-Botet M (2004) Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104(12):3664-3671. doi: 10.1182/blood-2004-05-2058
15. Guma M, Budt M, Saez A, Brckalo T, Hengel H, Angulo A, Lopez-Botet M (2006a) Expansion of CD94/NKG2C + NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 107(9):3624-3631. doi: 10.1182/blood-2005-09-3682
16. Guma M, Cabrera C, Erkizia I, Bofill M, Clotet B, Ruiz L, Lopez-Botet M (2006b) Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94/NKG2C receptor in aviremic HIV-1-positive patients. J Infect Dis 194(1):38-41. doi: 10.1086/504719
17. Hadrup SR, Strindhall J, Kollgaard T, Seremet T, Johansson B, Pawelec G, Thor Straten P, Wikby A (2006) Longitudinal studies of clonally expanded CD8 T cells reveal a repertoire shrinkage predicting mortality and an increased number of dysfunctional cytomegalovirus-specific T cells in the very elderly. J Immunol 176(4):2645-2653
18. Hecker M, Qiu D, Marquardt K, Bein G, Hackstein H (2004) Continuous cytomegalovirus seroconversion in a large group of healthy blood donors. Vox Sang 86(1):41-44
19. Kern F, Bunde T, Faulhaber N, Kiecker F, Khatamzas E, Rudawski IM, Pruss A, Gratama JW, Volkmer-Engert R, Ewert R, Reinke P, Volk HD, Picker LJ (2002) Cytomegalovirus (CMV) phosphoprotein 65 makes a large contribution to shaping the T cell repertoire in CMV-exposed individuals. J Infect Dis 185(12):1709-1716. doi: 10.1086/340637
20. Kern F, Khatamzas E, Surel I, Frommel C, Reinke P, Waldrop SL, Picker LJ, Volk HD (1999) Distribution of human CMV-specific memory T cells among the CD8pos. subsets defined by CD57, CD27, and CD45 isoforms. Eur J Immunol 29(9):2908-2915. doi: 10.1002/(sici)1521-4141(199909)29:09<2908::aid- immu2908>3.0.co;2-8
21. Khan N, Hislop A, Gudgeon N, Cobbold M, Khanna R, Nayak L, Rickinson AB, Moss PA (2004) Herpesvirus-specific CD8 T cell immunity in old age: cytomegalovirus impairs the response to a coresident EBV infection. J Immunol 173(12):7481-7489
22. 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 1114:23-35. doi: 10.1196/annals.1396.043
23. Kuijpers TW, Baars PA, Dantin C, van den Burg M, van Lier RA, Roosnek E (2008) Human NK cells can control CMV infection in the absence of T cells. Blood 112(3):914-915. doi: 10.1182/blood-2008-05-157354
24. Lanier LL (1998) NK cell receptors. Annu Rev Immunol 16:359-393. doi: 10.1146/annurev.immunol.16.1.359
25. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225-274. doi: 10.1146/annurev.immunol.23.021704.115526
26. Le Garff-Tavernier M, Beziat V, Decocq J, Siguret V, Gandjbakhch F, Pautas E, Debre P, Merle-Beral H, Vieillard V (2010) Human NK cells display major phenotypic and functional changes over the life span. Aging Cell 9(4):527-535. doi: 10.1111/j.1474-9726.2010.00584.x
27. Lidehall AK, Sund F, Lundberg T, Eriksson BM, Totterman TH, Korsgren O (2005) T cell control of primary and latent cytomegalovirus infections in healthy subjects. J Clin Immunol 25(5):473-481. doi: 10.1007/s10875-005-5372-8
28. Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, York VA, Houchins JP, Miller S, Kang SM, Norris PJ, Nixon DF, Lanier LL (2011) Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci U S A 108(36):14725-14732. doi: 10.1073/pnas.1110900108
29. Marashi SM, Raeiszadeh M, Enright V, Tahami F, Workman S, Chee R, Webster AD, Milne RS, Emery VC (2012) Influence of cytomegalovirus infection on immune cell phenotypes in patients with common variable immunodeficiency. J Allergy Clin Immunol 129(5):1349-1356. doi: 10.1016/j.jaci.2012.02.011, e1343
30. Mekker A, Tchang VS, Haeberli L, Oxenius A, Trkola A, Karrer U (2012) Immune senescence: relative contributions of age and cytomegalovirus infection. PLoS Pathog 8(8):e1002850. doi: 10.1371/journal.ppat.1002850
31. Moretta A, Bottino C, Vitale M, Pende D, Biassoni R, Mingari MC, Moretta L (1996) Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol 14:619-648. doi: 10.1146/annurev.immunol.14.1.619
32. Northfield J, Lucas M, Jones H, Young NT, Klenerman P (2005) Does memory improve with age? CD85j (ILT-2/LIR-1) expression on CD8 T cells correlates with 'memory inflation' in human cytomegalovirus infection. Immunol Cell Biol 83(2):182-188. doi: 10.1111/j.1440-1711.2005.01321.x
33. O'Leary JG, Goodarzi M, Drayton DL, von Andrian UH (2006) T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 7(5):507-516. doi: 10.1038/ni1332
34. Olsson J, Wikby A, Johansson B, Lofgren S, Nilsson BO, Ferguson FG (2000) Age-related change in peripheral blood T-lymphocyte subpopulations and cytomegalovirus infection in the very old: the Swedish longitudinal OCTO immune study. Mech Ageing Dev 121(1-3):187-201
35. Orange JS (2002) Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect 4(15):1545-1558
36. Paust S, Senman B, von Andrian UH (2010) Adaptive immune responses mediated by natural killer cells. Immunol Rev 235(1):286-296. doi: 10.1111/j.0105-2896.2010.00906.x
37. Pawelec G, Derhovanessian E, Larbi A, Strindhall J, Wikby A (2009) Cytomegalovirus and human immunosenescence. Rev Med Virol 19(1):47-56. doi: 10.1002/rmv.598
38. Strindhall J, Skog M, Ernerudh J, Bengner M, Lofgren S, Matussek A, Nilsson BO, Wikby A (2013) The inverted CD4/CD8 ratio and associated parameters in 66-year-old individuals: the Swedish HEXA immune study. Age (Dordr) 35(3):985-991. doi: 10.1007/s11357-012-9400-3
39. Sun JC, Beilke JN, Lanier LL (2009) Adaptive immune features of natural killer cells. Nature 457(7229):557-561. doi: 10.1038/nature07665
40. Sylwester AW, Mitchell BL, Edgar JB, Taormina C, Pelte C, Ruchti F, Sleath PR, Grabstein KH, Hosken NA, Kern F, Nelson JA, Picker LJ (2005) Broadly targeted human cytomegalovirus-specific CD4 + and CD8 + T cells dominate the memory compartments of exposed subjects. J Exp Med 202(5):673-685. doi: 10.1084/jem.20050882
41. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S (2008) Functions of natural killer cells. Nat Immunol 9(5):503-510. doi: 10.1038/ni1582
42. Wikby A, Johansson B, Olsson J, Lofgren S, Nilsson BO, Ferguson F (2002) Expansions of peripheral blood CD8 T-lymphocyte subpopulations and an association with cytomegalovirus seropositivity in the elderly: the Swedish NONA immune study. Exp Gerontol 37(2-3):445-453
43. Wikby A, Mansson IA, Johansson B, Strindhall J, Nilsson SE (2008) The immune risk profile is associated with age and gender: findings from three Swedish population studies of individuals 20-100 years of age. Biogerontology 9(5):299-308. doi: 10.1007/s10522-008-9138-6
44. Wikby A, Maxson P, Olsson J, Johansson B, Ferguson FG (1998) Changes in CD8 and CD4 lymphocyte subsets, T cell proliferation responses and non-survival in the very old: the Swedish longitudinal OCTO-immune study. Mech Ageing Dev 102(2-3):187-198