HIV-1 mRNA electroporation of PBMC: A simple and efficient method to monitor T-cell responses against autologous HIV-1 in HIV-1-infected patients

Journal of Immunological Methods

Volumn 380, Issue 1-2, 2012, Pages 40-55

  Etschel, Jennifer K ^a   Hückelhoven, Angela G ^a   Hofmann, Christian ^a   Zitzelsberger, Kathrin ^a   Maurer, Katja ^a   Bergmann, Silke ^a   Mueller Schmucker, Sandra M ^a   Wittmann, Jürgen ^a   Spriewald, Bernd M ^a   Dörrie, Jan ^a   Schaft, Niels ^a   Harrer, Thomas ^a,b  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b German Competence Network on HIV/AIDS   (Germany)

Author keywords

CTL; HIV 1; Immunomonitoring; MRNA electroporation

Indexed keywords

GAG PROTEIN; GAMMA INTERFERON; MESSENGER RNA; NEF PROTEIN;

ADULT; AGED; ARTICLE; CD8+ T LYMPHOCYTE; CELL COUNT; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; ELECTROPORATION; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN TISSUE; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; VIRUS STRAIN;

ADULT; AGED; ELECTROPORATION; FEMALE; GENE PRODUCTS, GAG; GENE PRODUCTS, NEF; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; MONITORING, IMMUNOLOGIC; RNA, MESSENGER; RNA, VIRAL; T-LYMPHOCYTES, CYTOTOXIC;

HUMAN IMMUNODEFICIENCY VIRUS 1; VACCINIA VIRUS;

EID: 84861186775     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2012.03.005     Document Type: Article

References (53)

1. Allard S.D., Pletinckx K., Breckpot K., Heirman C., Bonehill A., Michiels A., van Baalen C.A., Gruters R.A., Osterhaus A.D., Lacor P., Thielemans K., Aerts J.L. Functional T-cell responses generated by dendritic cells expressing the early HIV-1 proteins Tat, Rev and Nef. Vaccine 2008, 26:3735.
2. Allen T.M., Altfeld M., Geer S.C., Kalife E.T., Moore C., O'Sullivan K.M., Desouza I., Feeney M.E., Eldridge R.L., Maier E.L., Kaufmann D.E., Lahaie M.P., Reyor L., Tanzi G., Johnston M.N., Brander C., Draenert R., Rockstroh J.K., Jessen H., Rosenberg E.S., Mallal S.A., Walker B.D. Selective escape from CD8+ T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J. Virol. 2005, 79:13239.
3. Altfeld M., Rosenberg E.S., Shankarappa R., Mukherjee J.S., Hecht F.M., Eldridge R.L., Addo M.M., Poon S.H., Phillips M.N., Robbins G.K., Sax P.E., Boswell S., Kahn J.O., Brander C., Goulder P.J., Levy J.A., Mullins J.I., Walker B.D. Cellular immune responses and viral diversity in individuals treated during acute and early HIV-1 infection. J. Exp. Med. 2001, 193:169.
4. Altfeld M., Kalife E.T., Qi Y., Streeck H., Lichterfeld M., Johnston M.N., Burgett N., Swartz M.E., Yang A., Alter G., Yu X.G., Meier A., Rockstroh J.K., Allen T.M., Jessen H., Rosenberg E.S., Carrington M., Walker B.D. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med. 2006, 3:e403.
5. Bangham C.R. CTL quality and the control of human retroviral infections. Eur. J. Immunol. 2009, 39:1700.
6. Barouch D.H., O'Brien K.L., Simmons N.L., King S.L., Abbink P., Maxfield L.F., Sun Y.H., La Porte A., Riggs A.M., Lynch D.M., Clark S.L., Backus K., Perry J.R., Seaman M.S., Carville A., Mansfield K.G., Szinger J.J., Fischer W., Muldoon M., Korber B. Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat. Med. 2010, 16:319.
7. Beattie T., Kaul R., Rostron T., Dong T., Easterbrook P., Jaoko W., Kimani J., Plummer F., McMichael A., Rowland-Jones S. Screening for HIV-specific T-cell responses using overlapping 15-mer peptide pools or optimized epitopes. AIDS 2004, 18:1595.
8. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., Koup R.A. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 2003, 281:65.
9. Bonehill A., Heirman C., Tuyaerts S., Michiels A., Breckpot K., Brasseur F., Zhang Y., Van Der Bruggen P., Thielemans K. Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules. J. Immunol. 2004, 172:6649.
10. Borrow P., Lewicki H., Hahn B.H., Shaw G.M., Oldstone M.B. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 1994, 68:6103.
11. Chesebro B., Wehrly K., Nishio J., Perryman S. Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. J. Virol. 1992, 66:6547.
12. Corey L., McElrath M.J. HIV vaccines: mosaic approach to virus diversity. Nat. Med. 2010, 16:268.
13. Czerkinsky C.C., Nilsson L.A., Nygren H., Ouchterlony O., Tarkowski A. A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J. Immunol. Methods 1983, 65:109.
14. Goulder P., Price D., Nowak M., Rowland-Jones S., Phillips R., McMichael A. Co-evolution of human immunodeficiency virus and cytotoxic T-lymphocyte responses. Immunol. Rev. 1997, 159:17.
15. Goulder P.J., Sewell A.K., Lalloo D.G., Price D.A., Whelan J.A., Evans J., Taylor G.P., Luzzi G., Giangrande P., Phillips R.E., McMichael A.J. Patterns of immunodominance in HIV-1-specific cytotoxic T lymphocyte responses in two human histocompatibility leukocyte antigens (HLA)-identical siblings with HLA-A*0201 are influenced by epitope mutation. J. Exp. Med. 1997, 185:1423.
16. Goulder P.J., Tang Y., Pelton S.I., Walker B.D. HLA-B57-restricted cytotoxic T-lymphocyte activity in a single infected subject toward two optimal epitopes, one of which is entirely contained within the other. J. Virol. 2000, 74:5291.
17. Harrer T., Harrer E., Kalams S.A., Barbosa P., Trocha A., Johnson R.P., Elbeik T., Feinberg M.B., Buchbinder S.P., Walker B.D. Cytotoxic T lymphocytes in asymptomatic long-term nonprogressing HIV-1 infection. Breadth and specificity of the response and relation to in vivo viral quasispecies in a person with prolonged infection and low viral load. J. Immunol. 1996, 156:2616.
18. Harrer T., Harrer E., Kalams S.A., Elbeik T., Staprans S.I., Feinberg M.B., Cao Y., Ho D.D., Yilma T., Caliendo A.M., Johnson R.P., Buchbinder S.P., Walker B.D. Strong cytotoxic T cell and weak neutralizing antibody responses in a subset of persons with stable nonprogressing HIV type 1 infection. AIDS Res. Hum. Retroviruses 1996, 12:585.
19. Harrer E.G., Bergmann S., Eismann K., Rittmaier M., Goldwich A., Muller S.M., Spriewald B.M., Harrer T. A conserved HLA B13-restricted cytotoxic T lymphocyte epitope in Nef is a dominant epitope in HLA B13-positive HIV-1-infected patients. AIDS 2005, 19:734.
20. Herr W., Protzer U., Lohse A.W., Gerken G., Meyer zum Buschenfelde K.H., Wolfel T. Quantification of CD8+ T lymphocytes responsive to human immunodeficiency virus (HIV) peptide antigens in HIV-infected patients and seronegative persons at high risk for recent HIV exposure. J. Infect. Dis. 1998, 178:260.
21. Hofmann C., Harrer T., Kubesch V., Maurer K., Metzner K.J., Eismann K., Bergmann S., Schmitt-Haendle M., Schuler G., Dorrie J., Schaft N. Generation of HIV-1-specific T cells by electroporation of T-cell receptor RNA. AIDS 2008, 22:1577.
22. Honeyborne I., Prendergast A., Pereyra F., Leslie A., Crawford H., Payne R., Reddy S., Bishop K., Moodley E., Nair K., van der Stok M., McCarthy N., Rousseau C.M., Addo M., Mullins J.I., Brander C., Kiepiela P., Walker B.D., Goulder P.J. Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple gag-specific CD8+ T-cell epitopes. J. Virol. 2007, 81:3667.
23. Johnson L.A., Heemskerk B., Powell D.J., Cohen C.J., Morgan R.A., Dudley M.E., Robbins P.F., Rosenberg S.A. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J. Immunol. 2006, 177:6548.
24. Kavanagh D.G., Kaufmann D.E., Sunderji S., Frahm N., Le Gall S., Boczkowski D., Rosenberg E.S., Stone D.R., Johnston M.N., Wagner B.S., Zaman M.T., Brander C., Gilboa E., Walker B.D., Bhardwaj N. Expansion of HIV-specific CD4+ and CD8+ T cells by dendritic cells transfected with mRNA encoding cytoplasm- or lysosome-targeted Nef. Blood 2006, 107:1963.
25. Kern F., Faulhaber N., Frommel C., Khatamzas E., Prosch S., Schonemann C., Kretzschmar I., Volkmer-Engert R., Volk H.D., Reinke P. Analysis of CD8 T cell reactivity to cytomegalovirus using protein-spanning pools of overlapping pentadecapeptides. Eur. J. Immunol. 2000, 30:1676.
26. Klein M.R., van Baalen C.A., Holwerda A.M., Kerkhof Garde S.R., Bende R.J., Keet I.P., Eeftinck-Schattenkerk J.K., Osterhaus A.D., Schuitemaker H., Miedema F. Kinetics of Gag-specific cytotoxic T lymphocyte responses during the clinical course of HIV-1 infection: a longitudinal analysis of rapid progressors and long-term asymptomatics. J. Exp. Med. 1995, 181:1365.
27. Kyte J.A., Gaudernack G. Immuno-gene therapy of cancer with tumour-mRNA transfected dendritic cells. Cancer Immunol. Immunother. 2006, 55:1432.
28. Larsson M., Jin X., Ramratnam B., Ogg G.S., Engelmayer J., Demoitie M.A., McMichael A.J., Cox W.I., Steinman R.M., Nixon D., Bhardwaj N. A recombinant vaccinia virus based ELISPOT assay detects high frequencies of Pol-specific CD8 T cells in HIV-1-positive individuals. AIDS 1999, 13:767.
29. Maurer K., Harrer E.G., Goldwich A., Eismann K., Bergmann S., Schmitt-Haendle M., Spriewald B., Mueller S.M., Harrer T. Role of cytotoxic T-lymphocyte-mediated immune selection in a dominant human leukocyte antigen-B8-restricted cytotoxic T-lymphocyte epitope in Nef. J. Acquir. Immune Defic. Syndr. 2008, 48:133.
30. Ndhlovu Z.M., Piechocka-Trocha A., Vine S., McMullen A., Koofhethile K.C., Goulder P.J., Ndung'u T., Barouch D.H., Walker B.D. Mosaic HIV-1 Gag antigens can be processed and presented to human HIV-specific CD8+ T cells. J. Immunol. 2011, 186:6914.
31. Nixon D.F., Townsend A.R., Elvin J.G., Rizza C.R., Gallwey J., McMichael A.J. HIV-1 gag-specific cytotoxic T lymphocytes defined with recombinant vaccinia virus and synthetic peptides. Nature 1988, 336:484.
32. Santra S., Liao H.X., Zhang R., Muldoon M., Watson S., Fischer W., Theiler J., Szinger J., Balachandran H., Buzby A., Quinn D., Parks R.J., Tsao C.Y., Carville A., Mansfield K.G., Pavlakis G.N., Felber B.K., Haynes B.F., Korber B.T., Letvin N.L. Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat. Med. 2010, 16:324.
33. Schmitt M., Harrer E., Goldwich A., Bauerle M., Graedner I., Kalden J.R., Harrer T. Specific recognition of lamivudine-resistant HIV-1 by cytotoxic T lymphocytes. AIDS 2000, 14:653.
34. Schmitt-Haendle M., Bachmann O., Harrer E., Schmidt B., Bauerle M., Harrer T. Recognition patterns of HLA-A2-restricted human immunodeficiency virus-1-specific cytotoxic T-lymphocytes in a cohort of HIV-1-infected individuals. Viral Immunol. 2005, 18:627.
35. Seillier-Moiseiwitsch F., Margolin B.H., Swanstrom R. Genetic variability of the human immunodeficiency virus: statistical and biological issues. Annu. Rev. Genet. 1994, 28:559.
36. Sewell A.K., Price D.A., Oxenius A., Kelleher A.D., Phillips R.E. Cytotoxic T lymphocyte responses to human immunodeficiency virus: control and escape. Stem Cells 2000, 18:230.
37. Shugars D.C., Smith M.S., Glueck D.H., Nantermet P.V., Seillier-Moiseiwitsch F., Swanstrom R. Analysis of human immunodeficiency virus type 1 nef gene sequences present in vivo. J. Virol. 1993, 67:4639.
38. Simm M., Shahabuddin M., Chao W., Allan J.S., Volsky D.J. Aberrant Gag protein composition of a human immunodeficiency virus type 1 vif mutant produced in primary lymphocytes. J. Virol. 1995, 69:4582.
39. Sun Y., Iglesias E., Samri A., Kamkamidze G., Decoville T., Carcelain G., Autran B. A systematic comparison of methods to measure HIV-1 specific CD8 T cells. J. Immunol. Methods 2003, 272:23.
40. Teufel R., Carralot J.P., Scheel B., Probst J., Walter S., Jung G., Hoerr I., Rammensee H.G., Pascolo S. Human peripheral blood mononuclear cells transfected with messenger RNA stimulate antigen-specific cytotoxic T-lymphocytes in vitro. Cell. Mol. Life Sci. 2005, 62:1755.
41. Thornburg C., Boczkowski D., Gilboa E., Nair S.K. Induction of cytotoxic T lymphocytes with dendritic cells transfected with human papillomavirus E6 and E7 RNA: implications for cervical cancer immunotherapy. J. Immunother. 2000, 23:412.
42. Thurmond J., Yoon H., Kuiken C., Yusim K., Perkins S., Theiler J., Bhattacharya T., Korber B., Fischer W. Web-based design and evaluation of T-cell vaccine candidates. Bioinformatics 2008, 24:1639.
43. Tobery T.W., Wang S., Wang X.M., Neeper M.P., Jansen K.U., McClements W.L., Caulfield M.J. A simple and efficient method for the monitoring of antigen-specific T cell responses using peptide pool arrays in a modified ELISpot assay. J. Immunol. Methods 2001, 254:59.
44. Toohey K., Wehrly K., Nishio J., Perryman S., Chesebro B. Human immunodeficiency virus envelope V1 and V2 regions influence replication efficiency in macrophages by affecting virus spread. Virology 1995, 213:70.
45. Van Camp K., Cools N., Stein B., Van de Velde A., Goossens H., Berneman Z.N., Van Tendeloo V. Efficient mRNA electroporation of peripheral blood mononuclear cells to detect memory T cell responses for immunomonitoring purposes. J. Immunol. Methods 2010, 354:1-10.
46. Van Gulck E.R., Ponsaerts P., Heyndrickx L., Vereecken K., Moerman F., De Roo A., Colebunders R., Van den Bosch G., Van Bockstaele D.R., Van Tendeloo V.F., Allard S., Verrier B., Maranon C., Hoeffel G., Hosmalin A., Berneman Z.N., Vanham G. Efficient stimulation of HIV-1-specific T cells using dendritic cells electroporated with mRNA encoding autologous HIV-1 Gag and Env proteins. Blood 2006, 107:1818.
47. Verheyen J., Schweitzer F., Harrer E.G., Knops E., Mueller S.M., Daumer M., Eismann K., Bergmann S., Spriewald B.M., Kaiser R., Harrer T. Analysis of immune selection as a potential cause for the presence of cleavage site mutation 431V in treatment-naive HIV type-1 isolates. Antivir. Ther. 2010, 15:907.
48. Walker B.D., Chakrabarti S., Moss B., Paradis T.J., Flynn T., Durno A.G., Blumberg R.S., Kaplan J.C., Hirsch M.S., Schooley R.T. HIV-specific cytotoxic T lymphocytes in seropositive individuals. Nature 1987, 328:345.
49. Walker B.D., Flexner C., Birch-Limberger K., Fisher L., Paradis T.J., Aldovini A., Young R., Moss B., Schooley R.T. Long-term culture and fine specificity of human cytotoxic T-lymphocyte clones reactive with human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:9514.
50. Wehrly K., Chesebro B. p24 antigen capture assay for quantification of human immunodeficiency virus using readily available inexpensive reagents. Methods 1997, 12:288.
51. Wilgenhof S., Van Nuffel A.M., Corthals J., Heirman C., Tuyaerts S., Benteyn D., De Coninck A., Van Riet I., Verfaillie G., Vandeloo J., Bonehill A., Thielemans K., Neyns B. Therapeutic vaccination with an autologous mRNA electroporated dendritic cell vaccine in patients with advanced melanoma. J. Immunother. 2011, 34:448.
52. Wilson C.C., McKinney D., Anders M., MaWhinney S., Forster J., Crimi C., Southwood S., Sette A., Chesnut R., Newman M.J., Livingston B.D. Development of a DNA vaccine designed to induce cytotoxic T lymphocyte responses to multiple conserved epitopes in HIV-1. J. Immunol. 2003, 171:5611.
53. Zhai S., Zhuang Y., Song Y., Li S., Huang D., Kang W., Li X., Liao Q., Liu Y., Zhao Z., Lu Y., Sun Y. HIV-1-specific cytotoxic T lymphocyte (CTL) responses against immunodominant optimal epitopes slow the progression of AIDS in China. Curr. HIV Res. 2008, 6:335.