HLA-A02:01-restricted epitopes identified from the herpes simplex virus tegument protein VP11/12 preferentially recall polyfunctional effector memory CD8+ T cells from seropositive asymptomatic individuals and protect humanized HLA-A02:01 transgenic mice against ocular herpes
The HSV type 1 tegument virion phosphoprotein (VP) 11/12 (VP11/12) is a major Ag targeted by CD8(+) T cells from HSV-seropositive individuals. However, whether and which VP11/12 epitope-specific CD8(+) T cells play a role in the "natural" protection seen in seropositive healthy asymptomati...
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Published in | The Journal of immunology (1950) Vol. 194; no. 5; pp. 2232 - 2248 |
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Main Authors | , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
01.03.2015
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Abstract | The HSV type 1 tegument virion phosphoprotein (VP) 11/12 (VP11/12) is a major Ag targeted by CD8(+) T cells from HSV-seropositive individuals. However, whether and which VP11/12 epitope-specific CD8(+) T cells play a role in the "natural" protection seen in seropositive healthy asymptomatic (ASYMP) individuals (who have never had clinical herpes disease) remain to be determined. In this study, we used multiple prediction computer-assisted algorithms to identify 10 potential HLA-A*02:01-restricted CD8(+) T cell epitopes from the 718-aa sequence of VP11/12. Three of 10 epitopes exhibited high-to-moderate binding affinity to HLA-A*02:01 molecules. In 10 sequentially studied HLA-A*02:01-positive and HSV-1-seropositive ASYMP individuals, the most frequent, robust, and polyfunctional effector CD8(+) T cell responses, as assessed by a combination of tetramer frequency, granzyme B, granzyme K, perforin, CD107(a/b) cytotoxic degranulation, IFN-γ, and multiplex cytokines assays, were predominantly directed against three epitopes: VP11/1266-74, VP11/12220-228, and VP11/12702-710. Interestingly, ASYMP individuals had a significantly higher proportion of CD45RA(low)CCR7(low)CD44(high)CD62L(low)CD27(low)CD28(low)CD8(+) effector memory CD8(+) T cells (TEMs) specific to the three epitopes, compared with symptomatic individuals (with a history of numerous episodes of recurrent ocular herpetic disease). Moreover, immunization of HLA-A*02:01 transgenic mice with the three ASYMP CD8(+) TEM cell epitopes induced robust and polyfunctional epitope-specific CD8(+) TEM cells that were associated with a strong protective immunity against ocular herpes infection and disease. Our findings outline phenotypic and functional features of protective HSV-specific CD8(+) T cells that should guide the development of an effective T cell-based herpes vaccine. |
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AbstractList | The HSV type 1 tegument virion phosphoprotein (VP) 11/12 (VP11/12) is a major Ag targeted by CD8+ T cells from HSV-seropositive individuals. However, whether and which VP11/12 epitope-specific CD8+ T cells play a role in the "natural" protection seen in seropositive healthy asymptomatic (ASYMP) individuals (who have never had clinical herpes disease) remain to be determined. In this study, we used multiple prediction computer-assisted algorithms to identify 10 potential HLA-A*02:01-restricted CD8+ T cell epitopes from the 718-aa sequence of VP11/12. Three of 10 epitopes exhibited high-to-moderate binding affinity to HLA-A*02:01 molecules. In 10 sequentially studied HLA-A*02:01-positive and HSV-1-seropositive ASYMP individuals, the most frequent, robust, and polyfunctional effector CD8+ T cell responses, as assessed by a combination of tetramer frequency, granzyme B, granzyme K, perforin, CD107a/b cytotoxic degranulation, IFN- gamma , and multiplex cytokines assays, were predominantly directed against three epitopes: VP11/1266-74, VP11/12220-228, and VP11/12702-710. Interestingly, ASYMP individuals had a significantly higher proportion of CD45RAlowCCR7lowCD44highCD62LlowCD27lowCD28lowCD8+ effector memory CD8+ T cells (TEMs) specific to the three epitopes, compared with symptomatic individuals (with a history of numerous episodes of recurrent ocular herpetic disease). Moreover, immunization of HLA-A*02:01 transgenic mice with the three ASYMP CD8+ TEM cell epitopes induced robust and polyfunctional epitope-specific CD8+ TEM cells that were associated with a strong protective immunity against ocular herpes infection and disease. Our findings outline phenotypic and functional features of protective HSV-specific CD8+ T cells that should guide the development of an effective T cell-based herpes vaccine. The HSV type 1 tegument virion phosphoprotein (VP) 11/12 (VP11/12) is a major Ag targeted by CD8+ T cells from HSV-seropositive individuals. However, whether and which VP11/12 epitope–specific CD8+ T cells play a role in the “natural” protection seen in seropositive healthy asymptomatic (ASYMP) individuals (who have never had clinical herpes disease) remain to be determined. In this study, we used multiple prediction computer-assisted algorithms to identify 10 potential HLA-A*02:01–restricted CD8+ T cell epitopes from the 718-aa sequence of VP11/12. Three of 10 epitopes exhibited high-to-moderate binding affinity to HLA-A*02:01 molecules. In 10 sequentially studied HLA-A*02:01–positive and HSV-1–seropositive ASYMP individuals, the most frequent, robust, and polyfunctional effector CD8+ T cell responses, as assessed by a combination of tetramer frequency, granzyme B, granzyme K, perforin, CD107a/b cytotoxic degranulation, IFN-γ, and multiplex cytokines assays, were predominantly directed against three epitopes: VP11/1266–74, VP11/12220–228, and VP11/12702–710. Interestingly, ASYMP individuals had a significantly higher proportion of CD45RAlowCCR7lowCD44highCD62LlowCD27lowCD28lowCD8+ effector memory CD8+ T cells (TEMs) specific to the three epitopes, compared with symptomatic individuals (with a history of numerous episodes of recurrent ocular herpetic disease). Moreover, immunization of HLA-A*02:01 transgenic mice with the three ASYMP CD8+ TEM cell epitopes induced robust and polyfunctional epitope-specific CD8+ TEM cells that were associated with a strong protective immunity against ocular herpes infection and disease. Our findings outline phenotypic and functional features of protective HSV-specific CD8+ T cells that should guide the development of an effective T cell–based herpes vaccine. The Herpes Simplex Virus type 1 virion tegument phosphoprotein 11/12 (HSV-1 VP11/12) is a major antigen targeted by CD8 + T cells from HSV-seropositive individuals. However, whether and which VP11/12-epitope-specific CD8 + T cells play a role in the “natural” protection seen in seropositive healthy asymptomatic (ASYMP) individuals (who have never had clinical herpes disease) remain to be determined. In this study, we used multiple prediction computer-assisted algorithms to identify 10 potential HLA-A*02:01-restricted CD8 + T cell epitopes from the 716 amino acids sequence of VP11/12. Three out of ten epitopes exhibited high to moderate binding affinity to HLA-A*02:01 molecules. In ten sequentially studied HLA-A*02:01 positive and HSV-1-seropositive ASYMP individuals, the most frequent, robust and polyfunctional effector CD8 + T-cell responses, as assessed by a combination of tetramer frequency, granzyme B, granzyme K, perforin, CD107 a/b cytotoxic degranulation, IFN-γ and multiplex cytokines assays, were predominantly directed against three epitopes: VP11/12 66–74 , VP11/12 220–228 and VP11/12 702–710 . Interestingly, ASYMP individuals had significantly higher proportion of CD45RA low CCR7 low CD44 high CD62L low CD27 low CD28 low CD8 + effector memory T cells (T EM ) specific to the three epitopes, compared to symptomatic (SYMP) individuals (with a history of numerous episodes of recurrent ocular herpetic disease). Moreover, immunization of HLA-A*02:01 transgenic mice with the three ASYMP CD8 + T EM cell epitopes induced robust and polyfunctional epitope-specific CD8 + T EM cells that were associated with a strong protective immunity against ocular herpes infection and disease. Our findings outline phenotypic and functional features of protective HSV-specific CD8 + T cells that should guide the development of an effective T-cell-based herpes vaccine. The HSV type 1 tegument virion phosphoprotein (VP) 11/12 (VP11/12) is a major Ag targeted by CD8(+) T cells from HSV-seropositive individuals. However, whether and which VP11/12 epitope-specific CD8(+) T cells play a role in the "natural" protection seen in seropositive healthy asymptomatic (ASYMP) individuals (who have never had clinical herpes disease) remain to be determined. In this study, we used multiple prediction computer-assisted algorithms to identify 10 potential HLA-A*02:01-restricted CD8(+) T cell epitopes from the 718-aa sequence of VP11/12. Three of 10 epitopes exhibited high-to-moderate binding affinity to HLA-A*02:01 molecules. In 10 sequentially studied HLA-A*02:01-positive and HSV-1-seropositive ASYMP individuals, the most frequent, robust, and polyfunctional effector CD8(+) T cell responses, as assessed by a combination of tetramer frequency, granzyme B, granzyme K, perforin, CD107(a/b) cytotoxic degranulation, IFN-γ, and multiplex cytokines assays, were predominantly directed against three epitopes: VP11/1266-74, VP11/12220-228, and VP11/12702-710. Interestingly, ASYMP individuals had a significantly higher proportion of CD45RA(low)CCR7(low)CD44(high)CD62L(low)CD27(low)CD28(low)CD8(+) effector memory CD8(+) T cells (TEMs) specific to the three epitopes, compared with symptomatic individuals (with a history of numerous episodes of recurrent ocular herpetic disease). Moreover, immunization of HLA-A*02:01 transgenic mice with the three ASYMP CD8(+) TEM cell epitopes induced robust and polyfunctional epitope-specific CD8(+) TEM cells that were associated with a strong protective immunity against ocular herpes infection and disease. Our findings outline phenotypic and functional features of protective HSV-specific CD8(+) T cells that should guide the development of an effective T cell-based herpes vaccine. |
Author | Khan, Arif A Pham, Thanh T Thai, Nhi Thi Uyen Vahed, Hawa Scarfone, Vanessa M Lopes, Patricia P Wechsler, Steven L Wang, Christine Spencer, Doran BenMohamed, Lbachir Srivastava, Ruchi Huang, Jiawei Nesburn, Anthony B |
AuthorAffiliation | 2 Stem Cell Research Center, University of California Irvine, Irvine, CA 92697 6 Department of Molecular Biology & Biochemistry, University of California Irvine, School of Medicine, Irvine, CA 92697 7 Institute for Immunology; University of California Irvine, School of Medicine, Irvine, CA 92697 4 Department of Microbiology and Molecular Genetics, University of California Irvine, School of Medicine, Irvine, California 92697 5 Center for Virus Research, University of California Irvine, Irvine, California 92697 1 Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 3 Virology Research, Gavin Herbert Eye Institute and Department of Ophthalmology, University of California Irvine, School of Medicine, Irvine, California 92697 |
AuthorAffiliation_xml | – name: 4 Department of Microbiology and Molecular Genetics, University of California Irvine, School of Medicine, Irvine, California 92697 – name: 1 Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – name: 6 Department of Molecular Biology & Biochemistry, University of California Irvine, School of Medicine, Irvine, CA 92697 – name: 2 Stem Cell Research Center, University of California Irvine, Irvine, CA 92697 – name: 5 Center for Virus Research, University of California Irvine, Irvine, California 92697 – name: 7 Institute for Immunology; University of California Irvine, School of Medicine, Irvine, CA 92697 – name: 3 Virology Research, Gavin Herbert Eye Institute and Department of Ophthalmology, University of California Irvine, School of Medicine, Irvine, California 92697 |
Author_xml | – sequence: 1 givenname: Ruchi surname: Srivastava fullname: Srivastava, Ruchi organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 2 givenname: Arif A surname: Khan fullname: Khan, Arif A organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 3 givenname: Doran surname: Spencer fullname: Spencer, Doran organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 4 givenname: Hawa surname: Vahed fullname: Vahed, Hawa organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 5 givenname: Patricia P surname: Lopes fullname: Lopes, Patricia P organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 6 givenname: Nhi Thi Uyen surname: Thai fullname: Thai, Nhi Thi Uyen organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 7 givenname: Christine surname: Wang fullname: Wang, Christine organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 8 givenname: Thanh T surname: Pham fullname: Pham, Thanh T organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 9 givenname: Jiawei surname: Huang fullname: Huang, Jiawei organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 10 givenname: Vanessa M surname: Scarfone fullname: Scarfone, Vanessa M organization: Stem Cell Research Center, University of California Irvine, Irvine, CA 92697 – sequence: 11 givenname: Anthony B surname: Nesburn fullname: Nesburn, Anthony B organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697 – sequence: 12 givenname: Steven L surname: Wechsler fullname: Wechsler, Steven L organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697; Virology Research, Gavin Herbert Eye Institute and Department of Ophthalmology, University of California Irvine, School of Medicine, Irvine, CA 92697; Department of Microbiology and Molecular Genetics, University of California Irvine, School of Medicine, Irvine, CA 92697; Center for Virus Research, University of California Irvine, Irvine, CA 92697 – sequence: 13 givenname: Lbachir surname: BenMohamed fullname: BenMohamed, Lbachir email: Lbenmoha@uci.edu organization: Laboratory of Cellular and Molecular Immunology, Gavin Herbert Eye Institute, University of California Irvine, School of Medicine, Irvine, CA 92697; Department of Molecular Biology and Biochemistry, University of California Irvine, School of Medicine, Irvine, CA 92697; and Institute for Immunology, University of California Irvine, School of Medicine, Irvine, CA 92697 Lbenmoha@uci.edu |
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PublicationTitleAlternate | J Immunol |
PublicationYear | 2015 |
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Snippet | The HSV type 1 tegument virion phosphoprotein (VP) 11/12 (VP11/12) is a major Ag targeted by CD8(+) T cells from HSV-seropositive individuals. However, whether... The HSV type 1 tegument virion phosphoprotein (VP) 11/12 (VP11/12) is a major Ag targeted by CD8+ T cells from HSV-seropositive individuals. However, whether... The Herpes Simplex Virus type 1 virion tegument phosphoprotein 11/12 (HSV-1 VP11/12) is a major antigen targeted by CD8 + T cells from HSV-seropositive... |
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SubjectTerms | Adolescent Adult Aged Algorithms Amino Acid Sequence Animals Antigens, Viral - chemistry Antigens, Viral - immunology Asymptomatic Diseases CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - pathology CD8-Positive T-Lymphocytes - virology Epitopes, T-Lymphocyte - chemistry Epitopes, T-Lymphocyte - immunology Female Herpes simplex virus Herpesvirus 1, Human - chemistry Herpesvirus 1, Human - immunology Herpesvirus 2, Human - chemistry Herpesvirus 2, Human - immunology HLA-A2 Antigen - chemistry HLA-A2 Antigen - immunology Humans Immunity, Cellular Immunization Immunologic Memory Keratitis, Herpetic - immunology Keratitis, Herpetic - pathology Keratitis, Herpetic - prevention & control Keratitis, Herpetic - virology Male Mice Mice, Transgenic Middle Aged Molecular Sequence Data Peptides - administration & dosage Peptides - chemistry Peptides - immunology Viral Proteins - chemistry Viral Proteins - immunology |
Title | HLA-A02:01-restricted epitopes identified from the herpes simplex virus tegument protein VP11/12 preferentially recall polyfunctional effector memory CD8+ T cells from seropositive asymptomatic individuals and protect humanized HLA-A02:01 transgenic mice against ocular herpes |
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