Dissociated production of perforin, granzyme B, and IFN-γ by HIV-specific CD8+ cells in HIV infection

AIDS Research and Human Retroviruses

Volumn 24, Issue 1, 2008, Pages 62-71

  Kuerten, Stefanie ^a,b   Nowacki, Tobias M ^a   Kleen, Thomas O ^c   Asaad, Robert J ^d   Lehmann, Paul V ^a,c   Tary Lehmann, Magdalena ^a,c,d  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

^c Cellular Technology Limited   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANZYME B; PERFORIN; T LYMPHOCYTE RECEPTOR;

ADULT; AGED; ARTICLE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EFFECTOR CELL; ENZYME LINKED IMMUNOSPOT ASSAY; EX VIVO STUDY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; LYMPHOCYTE FUNCTION; MALE; MEASUREMENT; MEMORY T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN SECRETION; TARGET CELL; VACCINATION;

ADULT; AGED; CD8-POSITIVE T-LYMPHOCYTES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GRANZYMES; HIV INFECTIONS; HIV-1; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOLOGIC MEMORY; INTERFERON TYPE II; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; PERFORIN;

EID: 38149094433     PISSN: 08892229     EISSN: None     Source Type: Journal    
DOI: 10.1089/aid.2007.0125     Document Type: Article

References (58)

1. Wong P and Pamer EG: CD8 T cell responses to infectious pathogens. Annu Rev Immunol 2003;21:29-70.
2. Butz E and Bevan MJ: Dynamics of the CD8+ T cell response during acute LCMV infection. Adv Exp Med Biol 1998;452:111-122.
3. Walker CM, Moody DJ, Stites DP, and Levy JA: CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 1986;234:1563-1566.
4. Yang OO and Walker BD: CD8+ cells in human immunodeficiency virus type I pathogenesis: Cytolytic and noncytolytic inhibition of viral replication. Adv Immunol 1997;66:273-311.
5. Ogg GS, Jin X, Bonhoeffer S, et al.: Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998;279:2103-2106.
6. Edwards BH, Bansal A, Sabbaj S, Bakari J, Mulligan MJ, and Goepfert PA: Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J Virol 2002;76:2298-2305.
7. Lieberman J, Shankar P, Manjunath N, and Andersson J: Dressed to kill? A review of why antiviral CD8 T lymphocytes fail to prevent progressive immunodeficiency in HIV-1 infection. Blood 2001;98:1667-1677.
8. McMichael AJ and Rowland-Jones SL: Cellular immune responses to HIV. Nature 2001;410:980-987.
9. Le Page C, Genin P, Baines MG, and Hiscott J: Interferon activation and innate immunity. Rev Immunogenet 2000;2:374-386.
10. Sarol LC, Imai K, Asamitsu K, Tetsuka T, Barzaga NG, and Okamoto T: Inhibitory effects of IFN-gamma on HIV-1 replication in latently infected cells. Biochem Biophys Res Commun 2002;291:890-896.
11. Creery D, Weiss W, Lim WT, Aziz Z, Angel JB, and Kumar A: Down-regulation of CXCR-4 and CCR-5 expression by interferongamma is associated with inhibition of chemotaxis and human immunodeficiency virus (HIV) replication but not HIV entry into human monocytes. Clin Exp Immunol 2004;137:156-165.
12. Hamann D, Baars PA, Rep MH, Hooibrink B, Kerkhof-Garde SR, Klein MR, and van Lier RA: Phenotypic and functional separation of memory and effector human CD8+ T cells. J Exp Med 1997;186:1407-1418.
13. Thornton S., Kuhn KA, Finkelman FD, and Hirsch R: NK cells secrete high levels of IFN-gamma in response to in vivo administration of IL-2. Eur J Immunol 2001;31:3355-3360.
14. Forthal DN, Landucci G, Phan TB, and Becerra J: Interactions between natural killer cells and antibody Fc result in enhanced antibody neutralization of human immunodeficiency virus type 1. J Virol 2005;79:2042-2049.
15. Zimmerli SC, Harari A, Cellerai C, Vallelian F, Bart PA, and Pantaleo G: HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc Natl Acad Sci USA 2005;102:7239-7244.
16. Ware CF, VanArsdale S, and VanArsdale TL: Apoptosis mediated by the TNF-related cytokine and receptor families. J Cell Biochem 1996;60:47-55.
17. Benedict CA, Banks TA, and Ware CF: Death and survival: Viral regulation of TNF signaling pathways. Curr Opin Immunol 2003;15:59-65.
18. Henkart PA: Lymphocyte-mediated cytotoxicity: Two pathways and multiple effector molecules. Immunity 1994;1:343-346.
19. van den Brink MR and Burakoff SJ: Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol 2002;2:273-281.
20. Andersson J, Behbahani H, Lieberman J, et al.: Perforin is not coexpressed with granzyme A within cytotoxic granules in CD8 T lymphocytes present in lymphoid tissue during chronic HIV infection. AIDS 1999;13:1295-1303.
21. Sandberg JK, Fast NM, and Nixon DF: Functional heterogeneity of cytokines and cytolytic effector molecules in human CD8+ T lymphocytes. J Immunol 2001;167:181-187.
22. Kelso A, Costelloe EO, Johnson BJ, Groves P, Buttigieg K, and Fitzpatrick DR: The genes for perforin, granzymes A-C and IFNgamma are differentially expressed in single CD8(+) T cells during primary activation. Int Immunol 2002;14:605-613.
23. Kleen TO, Asaad R, Landry SJ, Boehm BO, and Tary-Lehmann M: Tc1 effector diversity shows dissociated expression of granzyme B and interferon-gamma in HIV infection. AIDS 2004;18:383-392.
24. van den Brink MR and Burakoff SJ: Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol 2002;2:273-281.
25. Shresta S, Pham CT, Thomas DA, Graubert TA, and Ley TJ: How do cytotoxic lymphocytes kill their targets? Curr Opin Immunol 1998;10:581-587.
26. Trapani JA and Smyth MJ: Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2002;2:735-747.
27. Rininsland FH, Helms T, Asaad RJ, Boehm BO, and Tary-Lehmann M: Granzyme B ELISPOT assay for ex vivo measurements of T cell immunity. J Immunol Methods 2000;240:143-155.
28. Calarota SA, Otero M, Robinson TM, Dai A, Lewis MG, Boyer JD, and Weiner DB: Independence of granzyme B secretion and interferon- gamma production during acute simian immunodeficiency virus infection. J Infect Dis 2006;193:1441-1450.
29. Young JD, Hengartner H, Podack ER, and Cohn ZA: Purification and characterization of a cytolytic pore-forming protein from granules of cloned lymphocytes with natural killer activity. Cell 1986;44:849-859.
30. Motyka B, Korbutt G, Pinkoski MJ, et al.: Mannose 6-phosphate/insulin-like growth factor II receptor is a death receptor for granzyme B during cytotoxic T cell-induced apoptosis. Cell 2003;103:491-500.
31. Currier JR, Kuta EG, Turk E, Earhart LB, Loomis-Price L, Janetzki S, Ferrari G, Birx DL, and Cox JH: A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J Immunol Methods 2002;260:157-172.
32. Hesse DM, Karulin AY, Boehm BO, Lehmann PV, and Tary-Lehmann M: A T cell clone's avidity is a function of its activation state. J Immunol 2001;167:1353-1361.
33. Hawkins N, Self S, and Wakefield J: The automated counting of spots for the ELISpot assay. J Immunol Methods 2006;316:52-58.
34. Helms T, Boehm BO, Asaad RJ, Trezza RP, Lehmann PV, and Tary-Lehmann M: Direct visualization of cytokine-producing recall antigen-specific CD4 memory T cells in healthy individuals and HIV patients. J Immunol 2000;164:3723-3732.
35. Heeger PS, Greenspan NS, Kuhlenschmidt S, Dejelo C, Hricik DE, Schulak JA, and Tary-Lehmann M: Pretransplant frequency of donor-specific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J Immunol 1999;163:2267-2275.
36. Malyguine A, Strobl SL, Shafer-Weaver KA, Ulderich T, Troke A, Baseler M, Kwak ML, and Neelapu SS: A modified human ELISPOT assay to detect specific responses to primary tumor cell targets. J Transl Med 2004;2:9.
37. Tary-Lehmann M, Hricik DE, Justice AC, Potter NS, and Heeger PS: Enzyme-linked immunosorbent assay spot detection of interferon-gamma and interleukin 5-producing cells as a predictive marker for renal allograft failure. Transplantation 1998;66:219-224.
38. Barber DL, Wherry EJ, and Ahmed R: Cutting edge: Rapid in vivo killing by memory CD8 T cells. J Immunol 2003;171:27-31.
39. Shresta S, Pham CT, Thomas DA, Graubert TA, and Ley TJ: How do cytotoxic lymphocytes kill their targets? Curr Opin Immunol 1998;10:581-587.
40. Isaaz S, Baetz K, Olsen K, Podack E, and Griffiths GM: Serial killing by cytotoxic T lymphocytes: T cell receptor triggers degranulation, re-filling of the lytic granules and secretion of lytic proteins via a non-granule pathway. Eur J Immunol 1995;25:1071-1079.
41. Froelich CJ, Orth K, Turbov J, et al.: New paradigm for lymphocyte granule-mediated cytotoxicity. Target cells bind and internalize granzyme B, but an endosomolytic agent is necessary for cytosolic delivery and subsequent apoptosis. J Biol Chem 1996;271:29073-29079.
42. Chen SF, Tu WW, Sharp MA, et al.: Antiviral CD8 T cells in the control of primary human cytomegalovirus infection in early childhood. J Infect Dis 2004;189:1619-1627.
43. Vetsika EK and Callan M: Infectious mononucleosis and Epstein-Barr virus. Expert Rev Mol Med 2004;6:1-16.
44. Wolint P, Betts MR, Koup RA, and Oxenius A: Immediate cytotoxicity but not degranulation distinguishes effector and memory subsets of CD8+ T cells. J Exp Med 2004;199:925-936.
45. Post JJ, Pan Y, Freeman AJ, Harvey CE, et al.: Clearance of hepatitis C viremia associated with cellular immunity in the absence of seroconversion in the hepatitis C incidence and transmission in prisons study cohort. J Infect Dis 2004:189:1846-1855.
46. Garcia-Sanz JA, MacDonald HR, Jenne DE, Tschopp J, and Nabholz M: Cell specificity of granzyme gene expression. J Immunol 1990;145:3111-3118.
47. Takata H and Takiguchi M: Three memory subsets of human CD8+ T cells differently expressing three cytolytic effector molecules. J Immunol 2006;177:4330-4340.
48. Rock MT, Yoder SM, Wright PF, Talbot TR, Edwards KM, and Crowe JE Jr: Differential regulation of granzyme and perforin in effector and memory T cells following smallpox immunization. J Immunol 2005;174:3757-3764.
49. Sallusto F, Lenig D, Forster R, Lipp M, and Lanzavecchia A: Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999;401:708-712.
50. Weninger W, Crowley MA, Manjunath N, and von Andrian UH: Migratory properties of naive, effector, and memory CD8(+) T cells. J Exp Med 2001;194:953-966.
51. Lehmann PV, Schumm G, Moon D, Hurtenbach U, Falcioni F, Muller S, and Nagy ZA: Acute lethal graft-versus-host reaction induced by major histocompatibility complex class II-reactive T helper cell clones. J Exp Med 1990;171:1485-1496.
52. Sprent J and von Boehmer H: Activation of T lymphocytes to M locus determinants in vivo. I. Quantitation of T cell proliferation and migration into thoracic duct lymph. Eur J Immunol 1976;6:352-358.
53. Egan MA, Chong SY, Rose NF, et al.: Immunogenicity of attenuated vesicular stomatitis virus vectors expressing HIV type 1 Env and SIV Gag proteins: Comparison of intranasal and intramuscular vaccination routes. AIDS Res Hum Retroviruses 2004;20:989-1004.
54. Kaufhold RM, Field JA, Caulfield MJ, et al.: Memory T-cell response to rotavirus detected with a gamma interferon enzyme-linked immunospot assay. J Virol 2005;79:5684-5694.
55. Scheibenbogen C, Lee KH, Mayer S, Stevanovic S, Moebius U, Herr W, Rammensee HG, and Keilholz U: A sensitive ELISPOT assay for detection of CD8+ T lymphocytes specific for HLA class I-binding peptide epitopes derived from influenza proteins in the blood of healthy donors and melanoma patients. Clin Cancer Res 1997;3:221-226.
56. Terajima M, Cruz J, Raines G, Kilpatrick ED, Kennedy JS, Rothman AL, and Ennis FA: Quantitation of CD8+ T cell responses to newly identified HLA-A*0201-restricted T cell epitopes conserved among vaccinia and variola (smallpox) viruses. J Exp Med 2003;197:927-932.
57. Calarota SA, Otero M, Robinson TM, Dai A, Lewis MG, Boyer JD, and Weiner DB: Independence of granzyme B secretion and interferon-gamma production during acute simian immunodeficiency virus infection. J Infect Dis 2006;193:1441-1450.
58. Apostolopoulos V, Yu M, Corper AL, Teyton L, Pietersz GA, McKenzie IF, Wilson IA, and Plebanski M: Crystal structure of a non-canonical low-affinity peptide complexed with MHC class I: A new approach for vaccine design. J Mol Biol 2002;318:1293-1305.