Treatment-dependent loss of polyfunctional CD8+ T-cell responses in HIV-infected kidney transplant recipients is associated with herpesvirus reactivation

American Journal of Transplantation

Volumn 9, Issue 4, 2009, Pages 794-803

  Gasser, O ^a,d   Bihl, F ^b   Sanghavi, S ^c   Rinaldo, C ^c   Rowe, D ^c   Hess, C ^d   Stablein, D ^e   Roland, M ^f   Stock, P ^f   Brander, C ^a,g,h  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

^e EMMES CORPORATION   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^h INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

HIV; Immunological monitoring; Kidney transplantation; T cell

Indexed keywords

ACICLOVIR; ANTIRETROVIRUS AGENT; AZATHIOPRINE; BASILIXIMAB; CYCLOSPORIN A; GANCICLOVIR; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PREDNISONE; RAPAMYCIN; TACROLIMUS; THYMOCYTE ANTIBODY;

ADULT; AGED; ARTICLE; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; DRUG SUBSTITUTION; DRUG WITHDRAWAL; EPSTEIN BARR VIRUS; FEMALE; GRAFT RECIPIENT; HERPES VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL MONITORING; KIDNEY GRAFT REJECTION; KIDNEY TRANSPLANTATION; LYMPHOCYTE DEPLETION; MALE; PRIORITY JOURNAL; PROSPECTIVE STUDY; VIRUS INFECTION; VIRUS LOAD; VIRUS REACTIVATION;

ACYCLOVIR; ADULT; AGED; ANTIVIRAL AGENTS; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; CYTOMEGALOVIRUS; FLOW CYTOMETRY; GANCICLOVIR; HERPESVIRIDAE; HERPESVIRUS 4, HUMAN; HIV INFECTIONS; HLA-A ANTIGENS; HLA-B ANTIGENS; HLA-DR ANTIGENS; HUMANS; KIDNEY TRANSPLANTATION; MIDDLE AGED; PATIENT SELECTION; T-LYMPHOCYTES, CYTOTOXIC; VIRAL LOAD; VIRUS ACTIVATION;

EID: 63349108208     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2008.02539.x     Document Type: Article

References (49)

1. Kaplan JE, Hanson D, Dworkin MS et al. Epidemiology of human immunodeficiency virus-associated opportunistic infections in the United States in the era of highly active antiretroviral therapy. Clin Infect Dis 2000 30 (Suppl 1 S5 14.
2. Palella FJ Jr., Delaney KM, Moorman AC et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV outpatient study investigators. N Engl J Med 1998 338 : 853 860.
3. Selik RM, Byers RH Jr., Dworkin MS. Trends in diseases reported on U.S. death certificates that mentioned HIV infection, 1987-1999. J Acquir Immune Defic Syndr 2002 29 : 378 387.
4. U.S. Renal Data System, USRDS 2004 Annual Data Report: Atlas of end-stage renal disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD, 2004.
5. Gardenswartz MH, Lerner CW, Seligson GR et al. Renal disease in patients with AIDS: A clinicopathologic study. Clin Nephrol 1984 21 : 197 204.
6. Rao TK, Filippone EJ, Nicastri AD et al. Associated focal and segmental glomerulosclerosis in the acquired immunodeficiency syndrome. N Engl J Med 1984 310 : 669 673.
7. Abbott KC, Swanson SJ, Agodoa LY, Kimmel PL. Human immunodeficiency virus infection and kidney transplantation in the era of highly active antiretroviral therapy and modern immunosuppression. J Am Soc Nephrol 2004 15 : 1633 1639.
8. Kumar MS, Sierka DR, Damask AM et al. Safety and success of kidney transplantation and concomitant immunosuppression in HIV-positive patients. Kidney Int 2005 67 : 1622 1629.
9. Pelletier SJ, Norman SP, Christensen LL, Stock PG, Port FK, Merion RM. Review of transplantation in HIV patients during the HAART era. Clin Transpl 2004 : 63 82.
10. Qiu J, Terasaki PI, Waki K, Cai J, Gjertson DW. HIV-positive renal recipients can achieve survival rates similar to those of HIV-negative patients. Transplantation 2006 81 : 1658 1661.
11. Roland ME. Solid-organ transplantation in HIV-infected patients in the potent antiretroviral therapy era. Top HIV Med 2004 12 : 73 76.
12. Roland ME, Stock PG. Review of solid-organ transplantation in HIV-infected patients. Transplantation 2003 75 : 425 429.
13. Roland ME, Stock PG. Solid organ transplantation is a reality for patients with HIV infection. Curr HIV/AIDS Rep 2006 3 : 132 138.
14. Stock P, Roland M, Carlson L et al. Solid organ transplantation in HIV-positive patients. Transplant Proc 2001 33 : 3646 3648.
15. Carter JT, Melcher ML, Carlson LL, Roland ME Stock PG. Thymoglobulin-associated Cd4+ T-cell depletion and infection risk in HIV-infected renal transplant recipients. Am J Transplant 2006 6 : 753 760.
16. Boubenider S, Hiesse C, Goupy C et al. Incidence and consequences of post-transplantation lymphoproliferative disorders. J Nephrol 1997 10 : 136 145.
17. Cockfield SM. Identifying the patient at risk for post-transplant lymphoproliferative disorder. Transpl Infect Dis 2001 3 : 70 78.
18. Drew WL. Cytomegalovirus infection in patients with AIDS. J Infect Dis 1988 158 : 449 456.
19. Gottschalk S, Rooney CM, Heslop HE. Post-transplant lymphoproliferative disorders. Annu Rev Med 2005 56 : 29 44.
20. Jacobson MA, Mills J. Serious cytomegalovirus disease in the acquired immunodeficiency syndrome (AIDS). Clinical findings, diagnosis, and treatment. Ann Intern Med 1988 108 : 585 594.
21. Steininger C, Puchhammer-Stockl E, Popow-Kraupp T. Cytomegalovirus disease in the era of highly active antiretroviral therapy (HAART). J Clin Virol 2006 37 : 1 9.
22. van Doornum GJ, Guldemeester J, Osterhaus AD, Niesters HG. Diagnosing herpesvirus infections by real-time amplification and rapid culture. J Clin Microbiol 2003 41 : 576 580.
23. Sanghavi SK, Abu-Elmagd K, Keightley MC et al. Relationship of cytomegalovirus load assessed by real-time PCR to pp65 antigenemia in organ transplant recipients. J Clin Virol 2008 19 : 19.
24. Rowe DT, Qu L, Reyes J et al. Use of quantitative competitive PCR to measure Epstein-Barr virus genome load in the peripheral blood of pediatric transplant patients with lymphoproliferative disorders. J Clin Microbiol 1997 35 : 1612 1615.
25. Wadowsky RM, Laus S, Green M, Webber SA, Rowe D. Measurement of Epstein-Barr virus DNA loads in whole blood and plasma by TaqMan PCR and in peripheral blood lymphocytes by competitive PCR. J Clin Microbiol 2003 41 : 5245 5249.
26. Maurmann S, Fricke L, Wagner HJ et al. Molecular parameters for precise diagnosis of asymptomatic Epstein-Barr virus reactivation in healthy carriers. J Clin Microbiol 2003 41 : 5419 5428.
27. Bihl FK, Loggi E, Chisholm JV 3rd. et al. Simultaneous assessment of cytotoxic T lymphocyte responses against multiple viral infections by combined usage of optimal epitope matrices, anti- CD3 mAb T-cell expansion and "RecycleSpot". J Transl Med 2005 3 : 20.
28. Frahm N, Korber BT, Adams CM et al. Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J Virol 2004 78 : 2187 2200.
29. Frahm N, Goulder P, Brander C. Total assessment of HIV specific CTL responses: Epitope clustering, processing preferences and the impact of HIV sequence heterogeneity. In : Korber B CB, Walker B, Koup R, Moore J, Haynes B, Meyers G, eds. HIV Molecular immunology database. Los Alamos, NM : Los Alamos National Laboratory: Theoretical Biology and Biophysics, 2002.
30. Frahm N, Yusim K, Suscovich TJ et al. Extensive HLA class I allele promiscuity among viral CTL epitopes. Eur J Immunol 2007 37 : 2419 2433.
31. Brengel-Pesce K, Morand P, Schmuck A et al. Routine use of real-time quantitative PCR for laboratory diagnosis of Epstein-Barr virus infections. J Med Virol 2002 66 : 360 369.
32. Miller CS, Berger JR, Mootoor Y et al. High prevalence of multiple human herpesviruses in saliva from human immunodeficiency virus-infected persons in the era of highly active antiretroviral therapy. J Clin Microbiol 2006 44 : 2409 2415.
33. Green M, Reyes J, Webber S et al. The role of antiviral and immunoglobulin therapy in the prevention of Epstein-Barr virus infection and post-transplant lymphoproliferative disease following solid organ transplantation. Transpl Infect Dis 2001 3 : 97 103.
34. Halpern SD, Asch DA, Shaked A, Stock PG, Blumberg E. Determinants of transplant surgeons' willingness to provide organs to patients infected with HBV, HCV or HIV. Am J Transplant 2005 5 : 1319 1325.
35. Bower M, Palmieri C, Dhillon T. AIDS-related malignancies: changing epidemiology and the impact of highly active antiretroviral therapy. Curr Opin Infect Dis 2006 19 : 14 19.
36. Wood C, Harrington W Jr. AIDS and associated malignancies. Cell Res 2005 15 : 947 952.
37. Stock PG, Roland ME, Carlson L et al. Kidney and liver transplantation in human immunodeficiency virus-infected patients: A pilot safety and efficacy study. Transplantation 2003 76 : 370 375.
38. Excerpts from the United States renal data system 2003 Annual Data Report: Atlas of end-stage renal disease in the United States. Am J Kidney Dis 2003 42 (Suppl S5 1 230.
39. Spiegel HM, DeFalcon E, Ogg GS et al. Changes in frequency of HIV-1-specific cytotoxic T cell precursors and circulating effectors after combination antiretroviral therapy in children. J Infect Dis 1999 180 : 359 368.
40. Woodberry T, Suscovich TJ, Henry LM et al. Impact of Kaposi sarcoma-associated herpesvirus (KSHV) burden and HIV coinfection on the detection of T cell responses to KSHV ORF73 and ORF65 proteins. J Infect Dis 2005 192 : 622 629.
41. Almeida JR, Price DA, Papagno L et al. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 2007 204 : 2473 2485.
42. Daucher M, Price DA, Brenchley JM et al. Virological outcome after structured interruption of antiretroviral therapy for human immunodeficiency virus infection is associated with the functional profile of virus-specific CD8+ T cells. J Virol 2008 82 : 4102 4114.
43. Makedonas G, Betts MR. Polyfunctional analysis of human t cell responses: Importance in vaccine immunogenicity and natural infection. Springer Semin Immunopathol 2006 28 : 209 219.
44. Betts MR, Nason MC, West SM et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006 107 : 4781 4789.
45. Bihl F, Narayan M, Chisholm JV, 3rd. et al. Lytic and latent antigens of the human gammaherpesviruses Kaposi's sarcoma-associated herpesvirus and Epstein-Barr virus induce T-cell responses with similar functional properties and memory phenotypes. J Virol 2007 81 : 4904 4908.
46. McLaughlin BE, Baumgarth N, Bigos M et al. Nine-color flow cytometry for accurate measurement of T cell subsets and cytokine responses. Part II: Panel performance across different instrument platforms. Cytometry A 2008 73 : 411 420.
47. Nashan B, Luck R, Kliem V, Brunkhorst R, Schlitt HJ, Klempnauer J. CMV in kidney transplantation: A single center experience over 22 years. Clin Transpl 1999 : 181 188.
48. Rostaing L, Crespin A, Icart J et al. Cytomegalovirus (CMV) prophylaxis by acyclovir in pre-transplant CMV-positive renal transplant recipients. Transpl Int 1994 7 (Suppl 1 S331 335.
49. Streeck H, Brumme ZL, Anastario M et al. Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8+ T cells. PLoS Med 2008 5 : e100.