Functional profile of cytomegalovirus (CMV)-specific CD8 + T cells and kinetics of NKG2C + NK Cells associated with the resolution of CMV DNAemia in allogeneic stem cell transplant recipients

Journal of Medical Virology

Volumn 84, Issue 2, 2012, Pages 259-267

  Muñoz Cobo, Beatriz ^a   Solano, Carlos ^a,b   Benet, Isabel ^a,b   Costa, Elisa ^a   Remigia, María José ^a   de la Cámara, Rafael ^c   Nieto, José ^d   López, Javier ^e   Amat, Paula ^a   Garcia Noblejas, Ana ^f   Bravo, Dayana ^a   Clari, María Ángeles ^a   Navarro, David ^a,b  

^a HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

^c Hospital de la Zarzuela   (Spain)

^d HOSPITAL MORALES MESEGUER   (Spain)

^e HOSPITAL RAMÓN Y CAJAL   (Spain)

^f HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

Author keywords

Allogeneic stem cell transplantation; CD8 + T cell response; CMV DNAemia; Cytomegalovirus; NK cells; Polyfunctional CD8 + T cells

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; CYTOMEGALOVIRUS ANTIGEN PP65; FOSCARNET; GAMMA INTERFERON; GANCICLOVIR; LYMPHOCYTE RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NK CELL ACTIVATING RECEPTOR NKG2C; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VALGANCICLOVIR; VIRUS DNA;

ADULT; ALLOGENEIC STEM CELL TRANSPLANTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL KINETICS; CELL POPULATION; CELL SIZE; CLINICAL ARTICLE; CORTICOSTEROID THERAPY; CYTOMEGALOVIRUS DNAEMIA; CYTOMEGALOVIRUS INFECTION; FEMALE; GRAFT RECIPIENT; HUMAN; MALE; VIRUS REPLICATION;

ADULT; ANTIGENS, CD56; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DNA, VIRAL; FEMALE; HUMANS; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MIDDLE AGED; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; PHOSPHOPROTEINS; RECEPTORS, IGG; STEM CELL TRANSPLANTATION; TRANSPLANTATION, HOMOLOGOUS; TUMOR NECROSIS FACTOR-ALPHA; VIRAL MATRIX PROTEINS; YOUNG ADULT;

EID: 83655197282     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.22254     Document Type: Article

References (35)

1. Almeida JR, Sauce D, Price DA, Papagno L, Shin SY, Moris A, Larsen M, Pancino G, Douek DC, Autran B, Sáez-Cirión A, Appay V. 2009. Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood 113:6351-6360.
2. Appay V, van Lier RA, Sallusto F, Roederer M. 2008. Phenotype and function of human T lymphocyte subsets: Consensus and issues. Cytometry A 73:975-983.
3. Barron MA, Gao D, Springer KL, Patterson JA, Brunvand MW, McSweeney PA, Zeng C, Barón AE, Weinberg A. 2009. Relationship of reconstituted adaptive and innate cytomegalovirus (CMV)-specific immune responses with CMV viremia in hematopoietic stem cell transplant recipients. Clin Infect Dis 49:1777-1783.
4. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, Abraham J, Lederman MM, Benito JM, Goepfert PA, Connors M, Roederer M, Koup RA. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781-4789.
5. Biron CA, Byron KS, Sullivan JL. 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med 320:1731-1735.
6. Björkström NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, Michaëlsson J, Malmberg KJ, Klingström 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 208:13-21.
7. Caligury MA. 2008. Human natural killer cells. Blood 112:461-469.
8. Einsele H, Roosnek E, Rufer N, Sinzger C, Riegler S, Löffler J, Grigoleit U, Moris A, Rammensee HG, Kanz L, Kleihauer A, Frank F, Jahn G, Hebart H. 2002. Infusion of cytomegalovirus (CMV)-specific T-cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 99:3916-3922.
9. Gimeno C, Solano C, Latorre JC, Hernández-Boluda JC, Clari MA, Remigia MJ, Furió S, Calabuig M, Tormo N, Navarro D. 2008. Quantification of DNA in plasma by an automated real-time PCR assay (cytomegalovirus PCR kit) for surveillance of active cytomegalovirus infection and guidance of preemptive therapy for allogeneic hematopoietic stem cell transplant recipients. J Clin Microbiol 46:3311-3318.
10. Gumá M, Angulo A, Vilches C, Gómez-Lozano N, Malats N, López-Botet M. 2004. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104:3664-3671.
11. Gumá M, Budt M, Sáez A, Brckalo T, Hengel H, Angulo A, López-Botet M. 2006. Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 107:3624-3631.
12. Hakki M, Riddell SR, Storek J, Carter RA, Stevens-Ayers T, Sudour P, White K, Corey L, Boeckh M. 2003. Immune reconstitution to cytomegalovirus after allogeneic stem cell transplantation: Impact of host factors, drug therapy, and subclinical reactivation. Blood 102:3060-3067.
13. Harari A, Vallelian F, Pantaleo G. 2004. Phenotypic heterogeneity of antigen-specific CD4 T cells under different conditions of antigen persistence and antigen load. Eur J Immunol 34:3525-3533.
14. Harari A, Dutoit V, Cellerai C, Bart PA, Du Pasquier RA, Pantaleo G. 2006. Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol Rev 211:236-254.
15. Król L, Stuchlý J, Hubáreck P, Keslová P, Sedláček P, Starý J, Hrušák O, Kalina T. 2011. Signature profiles of CMV-specific T cells in patients with CMV reactivation after hematopoietic SCT. Bone Marrow Transplant 46:1089-1098.
16. 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 112:914-915.
17. Lacey S, La Rosa C, Zhou W, Sharma MC, Martinez J, Krishnan A, Gallez-Hawkins G, Thao L, Longmate J, Spielberger R, Forman SJ, Limaye A, Zaia JA, Diamond DJ. 2006. Functional comparison of T cells recognizing cytomegalovirus pp65 and immediate-early antigen polypeptides in hematopoietic stem-cell transplant and solid organ transplant recipients. J Infect Dis 194:1410-1421.
18. Li CR, Greenberg PD, Gilbert MJ, Goodrich JM, Riddell SR. 1994. Recovery of HLA-restricted cytomegalovirus (CMV)-specific T-cell responses after allogeneic bone marrow transplant: Correlation with CMV disease and effect of ganciclovir prophylaxis. Blood 83:1971-1979.
19. Lilleri D, Fornara C, Chiesa A, Caldera D, Alessandrino EP, Gerna G. 2008. Human cytomegalovirus-specific CD4+ and CD8+ T-cell reconstitution in adult allogeneic hematopoietic stem cell transplant recipients and immune control of viral infection. Haematologica 93:248-256.
20. Makedonas G, Hutnick N, Haney D, Amick AC, Gardner J, Cosma G, Hersperger AR, Dolfi D, Wherry EJ, Ferrari G, Betts MR. 2010. Perforin and IL-2 upregulation define qualitative differences among highly functional virus-specific human CD8 T cells. PLoS Pathog 6:e1000798.
21. Nebbia G, Mattes FM, Smith C, Hainsworth E, Kopycinski J, Burroughs A, Griffiths PD, Klenerman P, Emery VC. 2008. Polyfunctional cytomegalovirus-specific CD4+ and pp65 CD8+ T cells protect against high-level replication after liver transplantation. Am J Transplant 8:2590-2599.
22. Quinnan GV, Kirmani N, Rook AH, Manischewitz JF, Jackson L, Moreschi G, Santos GW, Saral R, Burns WH. 1982. Cytotoxic T cells in cytomegalovirus infection: HLA-restricted T-lymphocyte and non T-lymphocyte cytotoxic responses correlate with recovery from cytomegalovirus infection in bone-marrow-transplant recipients. N Engl J Med 307:7-13.
23. Rehr M, Cahenzli J, Haas A, Price DA, Gostick E, Huber M, Kerrer U, Oxenius A. 2008. Emergence of polyfunctional CD8+ T cells after prolonged suppression of human immunodeficiency virus replication by antiretroviral therapy. J Virol 82:3391-3404.
24. Reusser P, Riddell SR, Meyers JD, Greenberg PD. 1991. Cytotoxic T-lymphocyte response to cytomegalovirus after human allogeneic bone marrow transplantation: Pattern of recovery and correlation with cytomegalovirus infection and disease. Blood 78:1373-1380.
25. Riddell SR, Watanabe KS, Goodrich JM, Li CR, Agha ME, Greenberg PD. 1992. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257:238-241.
26. Robbins SH, Bessou G, Cornillon A, Zucchini N, Rupp B, Ruzsics Z, Sacher T, Tomasello E, Vivier E, Koszinowski UH, Dalod M. 2007. Natural killer cells promote early CD8+ T cell responses against cytomegalovirus. PLoS Pathog 3: e123.
27. Sáez-Borderías A, Romo N, Magri G, Gumá M, Angulo A, López-Botet M. 2009. IL-12-dependent inducible expression of the CD94/NKG2A inhibitory receptor regulates CD94/NKG2C+ NK cell function. J Immunol 182:829-836.
28. Solano C, Navarro D. 2010. Clinical virology of cytomegalovirus infection following hematopoietic transplantation. Future Virol 5:111-124.
29. Solano C, Benet I, Clari MA, Nieto J, de la Cámara R, López J, Hernández-Boluda JC, Remigia MJ, Jarque I, Calabuig ML, Garcia-Noblejas A, Alberola J, Tamarit A, Gimeno C, Navarro D. 2008. Enumeration of cytomegalovirus-specific interferongamma CD8+ and CD4+ T cells early after allogeneic stem cell transplantation may identify patients at risk of active cytomegalovirus infection. Haematologica 93:1434-1436.
30. Tormo N, Solano C, Benet I, Clari MA, Nieto J, de la Cámara R, López J, López-Aldeguer N, Hernández-Boluda JC, Remigia MJ, Garcia-Noblejas A, Gimeno C, Navarro D. 2010a. Lack of prompt expansion of cytomegalovirus pp65 and IE-1-specific IFNgamma CD8+ and CD4+ T cells is associated with rising levels of pp65 antigenemia and DNAemia during pre-emptive therapy in allogeneic hematopoietic stem cell transplant recipients. Bone Marrow Transplant 45:543-549.
31. Tormo N, Solano C, Benet I, Nieto J, de la Cámara R, Garcia-Noblejas A, Clari MA, Chilet M, López J, Hernández-Boluda JC, Remigia MJ, Navarro D. 2010b. Kinetics of cytomegalovirus (CMV) pp65 and IE-1-specific IFNgamma CD8+ and CD4+ T cells during episodes of viral DNAemia in allogeneic stem cell transplant recipients: Potential implications for the management of active CMV infection. J Med Virol 82:1208-1215.
32. Tormo N, Solano C, Benet I, Nieto J, de la Cámara R, López J, Garcia-Noblejas A, Muñoz-Cobo B, Costa E, Clari MA, Hernández-Boluda JC, Remigia MJ, Navarro D. 2011. Reconstitution of CMV pp65 and IE-1-specific IFN-γ CD8(+) and CD4(+) T-cell responses affording protection from CMV DNAemia following allogeneic hematopoietic SCT. Bone Marrow Transplant 46:1437-1443.
33. Venema H, van den Berg AP, van Zanten C, van Son WJ, van der Giessen M, The TH. 1994. Natural killer cell responses in renal transplant patients with cytomegalovirus infection. J Med Virol 42:188-192.
34. Widmann T, Sester U, Gärtner BC, Schubert J, Pfreundschuh M, Köhler H, Sester M. 2008. Levels of CMV specific CD4+ T cells are dynamic and correlate with CMV viremia after allogeneic stem cell transplantation. PLoS ONE 3:e3634.
35. Zhou W, Longmate J, Lacey SF, Palmer JM, Gallez-Hawkins G, Thao L, Spielberger R, Nakamura R, Forman SJ, Zaia JA, Diamond DJ. 2009. Impact of donor CMV status on viral infection and reconstitution of multifunction CMV-specific T cells in CMV-positive transplant recipients. Blood 113:6465-6476.