Flow cytometric detection of degranulation reveals phenotypic heterogeneity of degranulating CMV-specific CD8+ T lymphocytes in rhesus macaques

Journal of Immunological Methods

Volumn 325, Issue 1-2, 2007, Pages 20-34

  Chan, Kenneth S ^a   Kaur, Amitinder ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CD107a; CD8+ T lymphocytes; CTL; Degranulation; Rhesus CMV; SIV

Indexed keywords

CD28 ANTIGEN; CD45RA ANTIGEN; GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PERFORIN;

ANIMAL CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL COMPOSITION; CELL STIMULATION; COMPARATIVE STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DEGRANULATION; EFFECTOR CELL; FLOW CYTOMETRY; GENETIC HETEROGENEITY; IN VITRO STUDY; KINETICS; MACACA; MEMORY CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; SECRETORY CELL; STATISTICAL SIGNIFICANCE; VIRUS REPLICATION;

ANIMALS; ANTIGENS, CD28; ANTIGENS, CD45; ANTIGENS, CD95; BREFELDIN A; CELL DEGRANULATION; CYTOMEGALOVIRUS; EPITOPES, T-LYMPHOCYTE; FLOW CYTOMETRY; IMMEDIATE-EARLY PROTEINS; IMMUNOPHENOTYPING; INTERFERON TYPE II; LEUKOCYTES, MONONUCLEAR; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MACACA MULATTA; MEMBRANE GLYCOPROTEINS; MONENSIN; PEPTIDE FRAGMENTS; PORE FORMING CYTOTOXIC PROTEINS; SUPERANTIGENS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC; TRANS-ACTIVATORS; TUMOR NECROSIS FACTOR-ALPHA; VIRAL PROTEINS;

CERCOPITHECINE HERPESVIRUS 8; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 34547774150     PISSN: 00221759     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jim.2007.05.011     Document Type: Article

References (37)

1. Alter G., Malenfant J.M., and Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294 (2004) 15
2. Anonymous. The Institute of Laboratory Animal Resources, National Research Council: Guide for the Care and Use of Laboratory Animals (1996) 86
3. Appay V., Dunbar P.R., Callan M., Klenerman P., Gillespie G.M., Papagno L., Ogg G.S., King A., Lechner F., Spina C.A., Little S., Havlir D.V., Richman D.D., Gruener N., Pape G., Waters A., Easterbrook P., Salio M., Cerundolo V., McMichael A.J., and Rowland-Jones S.L. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8 (2002) 379
4. Baars P.A., Ribeiro Do Couto L.M., Leusen J.H., Hooibrink B., Kuijpers T.W., Lens S.M., and van Lier R.A. Cytolytic mechanisms and expression of activation-regulating receptors on effector-type CD8 + CD45RA + CD27-human T cells. J. Immunol. 165 (2000) 1910
5. Bachmann M.F., Barner M., Viola A., and Kopf M. Distinct kinetics of cytokine production and cytolysis in effector and memory T cells after viral infection. Eur. J. Immunol. 29 (1999) 291
6. Barry M., and Bleackley R.C. Cytotoxic T lymphocytes: all roads lead to death. Nat. Rev., Immunol. 2 (2002) 401
7. Betts M.R., and Koup R.A. Detection of T-cell degranulation: CD107a and b. Methods Cell Biol. 75 (2004) 497
8. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., and Koup R.A. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281 (2003) 65
9. Betts M.R., Price D.A., Brenchley J.M., Lore K., Guenaga F.J., Smed-Sorensen A., Ambrozak D.R., Migueles S.A., Connors M., Roederer M., Douek D.C., and Koup R.A. The functional profile of primary human antiviral CD8+ T cell effector activity is dictated by cognate peptide concentration. J. Immunol. 172 (2004) 6407
10. Betts M.R., Nason M.C., West S.M., De Rosa S.C., Migueles S.A., Abraham J., Lederman M.M., Benito J.M., Goepfert P.A., Connors M., Roederer M., and Koup R.A. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107 (2006) 4781
11. Bunde T., Kirchner A., Hoffmeister B., Habedank D., Hetzer R., Cherepnev G., Proesch S., Reinke P., Volk H.D., Lehmkuhl H., and Kern F. Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J. Exp. Med. 201 (2005) 1031
12. Calarota S.A., Otero M., Robinson T.M., Dai A., Lewis M.G., Boyer J.D., and Weiner D.B. Independence of granzyme B secretion and interferon-gamma production during acute simian immunodeficiency virus infection. J. Infect. Dis. 193 (2006) 1441
13. Champagne P., Ogg G.S., King A.S., Knabenhans C., Ellefsen K., Nobile M., Appay V., Rizzardi G.P., Fleury S., Lipp M., Forster R., Rowland-Jones S., Sekaly R.P., McMichael A.J., and Pantaleo G. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410 (2001) 106
14. Chang M.H., Karageorgos L.E., and Meikle P.J. CD107a (LAMP-1) and CD107b (LAMP-2). J. Biol. Regul. Homeost. Agents 16 (2002) 147
15. De Rosa S.C., Lu F.X., Yu J., Perfetto S.P., Falloon J., Moser S., Evans T.G., Koup R., Miller C.J., and Roederer M. Vaccination in humans generates broad T cell cytokine responses. J. Immunol. 173 (2004) 5372
16. Ellefsen K., Harari A., Champagne P., Bart P.A., Sekaly R.P., and Pantaleo G. Distribution and functional analysis of memory antiviral CD8 T cell responses in HIV-1 and cytomegalovirus infections. Eur. J. Immunol. 32 (2002) 3756
17. Fukuda M. Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking. J. Biol. Chem. 266 (1991) 21327
18. Gamadia L.E., Rentenaar R.J., Baars P.A., Remmerswaal E.B., Surachno S., Weel J.F., Toebes M., Schumacher T.N., ten Berge I.J., and van Lier R.A. Differentiation of cytomegalovirus-specific CD8(+) T cells in healthy and immunosuppressed virus carriers. Blood 98 (2001) 754
19. Gillespie G.M., Wills M.R., Appay V., O'Callaghan C., Murphy M., Smith N., Sissons P., Rowland-Jones S., Bell J.I., and Moss P.A. Functional heterogeneity and high frequencies of cytomegalovirus-specific CD8(+) T lymphocytes in healthy seropositive donors. J. Virol. 74 (2000) 8140
20. Hamann D., Baars P.A., Rep M.H., Hooibrink B., Kerkhof-Garde S.R., Klein M.R., and van Lier R.A. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186 (1997) 1407
21. Jones N., Eggena M., Baker C., Nghania F., Baliruno D., Mugyenyi P., Ssali F., Barugahare B., and Cao H. Presence of distinct subsets of cytolytic CD8+ T cells in chronic HIV infection. AIDS Res. Hum. Retrovir. 22 (2006) 1007
22. Kagi D., Vignaux F., Ledermann B., Burki K., Depraetere V., Nagata S., Hengartner H., and Golstein P. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 265 (1994) 528
23. Kaur A., Hale C.L., Noren B., Kassis N., Simon M.A., and Johnson R.P. Decreased frequency of cytomegalovirus (CMV)-specific CD4+ T lymphocytes in simian immunodeficiency virus-infected rhesus macaques: inverse relationship with CMV viremia. J. Virol. 76 (2002) 3646
24. Kleen T.O., Asaad R., Landry S.J., Boehm B.O., and Tary-Lehmann M. Tc1 effector diversity shows dissociated expression of granzyme B and interferon-gamma in HIV infection. Aids 18 (2004) 383
25. Lacey S.F., Martinez J., Gallez-Hawkins G., Thao L., Longmate J., Haq W., Spielberger R., Forman S.J., Zaia J.A., and Diamond D.J. Simultaneous reconstitution of multiple cytomegalovirus-specific CD8+ cell populations with divergent functionality in hematopoietic stem-cell transplant recipients. J. Infect. Dis. 191 (2005) 977
26. Lacey S.F., La Rosa C., Zhou W., Sharma M.C., Martinez J., Krishnan A., Gallez-Hawkins G., Thao L., Longmate J., Spielberger R., Forman S.J., Limaye A., Zaia J.A., and Diamond D.J. Functional comparison of T cells recognizing cytomegalovirus pp65 and intermediate-early antigen polypeptides in hematopoietic stem-cell transplant and solid organ transplant recipients. J. Infect. Dis. 194 (2006) 1410
27. Mongkolsapaya J., Duangchinda T., Dejnirattisai W., Vasanawathana S., Avirutnan P., Jairungsri A., Khemnu N., Tangthawornchaikul N., Chotiyarnwong P., Sae-Jang K., Koch M., Jones Y., McMichael A., Xu X., Malasit P., and Screaton G. T cell responses in dengue hemorrhagic fever: are cross-reactive T cells suboptimal?. J. Immunol. 176 (2006) 3821
28. O'Neil-Andersen N.J., and Lawrence D.A. Differential modulation of surface and intracellular protein expression by T cells after stimulation in the presence of monensin or brefeldin A. Clin. Diagn. Lab. Immunol. 9 (2002) 243
29. Peters P.J., Borst J., Oorschot V., Fukuda M., Krahenbuhl O., Tschopp J., Slot J.W., and Geuze H.J. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 173 (1991) 1099
30. Pitcher C.J., Hagen S.I., Walker J.M., Lum R., Mitchell B.L., Maino V.C., Axthelm M.K., and Picker L.J. Development and homeostasis of T cell memory in rhesus macaque. J. Immunol. 168 (2002) 29
31. Rubio V., Stuge T.B., Singh N., Betts M.R., Weber J.S., Roederer M., and Lee P.P. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat. Med. 9 (2003) 1377
32. 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 401 (1999) 708
33. Snyder J.E., Bowers W.J., Livingstone A.M., Lee F.E., Federoff H.J., and Mosmann T.R. Measuring the frequency of mouse and human cytotoxic T cells by the Lysispot assay: independent regulation of cytokine secretion and short-term killing. Nat. Med. 9 (2003) 231
34. Snyder-Cappione J.E., Divekar A.A., Maupin G.M., Jin X., Demeter L.M., and Mosmann T.R. HIV-specific cytotoxic cell frequencies measured directly ex vivo by the Lysispot assay can be higher or lower than the frequencies of IFN-gamma-secreting cells: anti-HIV cytotoxicity is not generally impaired relative to other chronic virus responses. J. Immunol. 176 (2006) 2662
35. 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., and Picker L.J. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 202 (2005) 673
36. Wills M.R., Okecha G., Weekes M.P., Gandhi M.K., Sissons P.J., and Carmichael A.J. Identification of naive or antigen-experienced human CD8(+) T cells by expression of costimulation and chemokine receptors: analysis of the human cytomegalovirus-specific CD8(+) T cell response. J. Immunol. 168 (2002) 5455
37. Wolint P., Betts M.R., Koup R.A., and Oxenius A. Immediate cytotoxicity but not degranulation distinguishes effector and memory subsets of CD8+ T cells. J. Exp. Med. 199 (2004) 925