Cited by 1,339Cytomegalovirus and herpesvirus researchT-cell and B-cell Immunologyvaccines and immunoinformatics approaches

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Broadly targeted human cytomegalovirus-specific CD4 + and CD8 + T cells dominate the memory compartments of exposed subjects

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Sylwester, Andrew W., Mitchell, Bridget L., Edgar, John B., Taormina, Cara, Pelte, Christian, Ruchti, Franziska, Sleath, Paul R., Grabstein, Kenneth H., Hosken, Nancy A., Kern, Florian, Nelson, Jay A., Picker, Louis J.·2005·The Journal of Experimental Medicine

DOI 10.1084/jem.20050882PMC PMC2212883

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Abstract

Human cytomegalovirus (HCMV) infections of immunocompetent hosts are characterized by a dynamic, life-long interaction in which host immune responses, particularly of T cells, restrain viral replication and prevent disease but do not eliminate the virus or preclude transmission. Because HCMV is among the largest and most complex of known viruses, the T cell resources committed to maintaining this balance have never been characterized completely. Here, using cytokine flow cytometry and 13,687 overlapping 15mer peptides comprising 213 HCMV open reading frames (ORFs), we found that 151 HCMV ORFs were immunogenic for CD4+ and/or CD8+ T cells, and that ORF immunogenicity was influenced only modestly by ORF expression kinetics and function. We further documented that total HCMV-specific T cell responses in seropositive subjects were enormous, comprising on average ∼10% of both the CD4+ and CD8+ memory compartments in blood, whereas cross-reactive recognition of HCMV proteins in seronegative individuals was limited to CD8+ T cells and was rare. These data provide the first glimpse of the total human T cell response to a complex infectious agent and will provide insight into the rules governing immunodominance and cross-reactivity in complex viral infections of humans.

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Background
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BackgroundResultSelf-citation
Coding potential of laboratory and clinical strains of human cytomegalovirus
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BackgroundSelf-citation
Primary immune responses to human CMV: a critical role for IFN-γ–producing CD4+ T cells in protection against CMV disease
Gamadia, L. E., Remmerswaal, E. B. M., Weel, J. F. L., Bemelman, F. J., van Lier, R. A. W., & ten Berge, I. J. M. (2003) · Blood · doi:10.1182/blood-2002-08-2502 · Cited by 423

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BackgroundResult
Demarcated thresholds of tumor-specific CD8 T cells elicited by MCMV-based vaccine vectors provide robust correlates of protection
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MethodInfluential
DNA Immunization Using Highly Conserved Murine Cytomegalovirus Genes Encoding Homologs of Human Cytomegalovirus UL54 (DNA Polymerase) and UL105 (Helicase) Elicits Strong CD8 T-Cell Responses and Is Protective against Systemic Challenge
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“lations in the circulation of healthy hosts, accounting for an average of 5% of all circulating T cells.(22) Thus, in theory,”
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Background
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Background
Cytomegalovirus infection disrupts the influence of short-chain fatty acid producers on Treg/Th17 balance
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Background
Identification and HLA-Tetramer-Validation of Human CD4+ and CD8+ T Cell Responses against HCMV Proteins IE1 and IE2
Brændstrup, P., Mortensen, B. K., Justesen, S. F. L., Østerby, T., Rasmussen, M., Hansen, A. M., Christiansen, C. B., Hansen, M. B., Nielsen, M., Vindeløv, L. L., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094892 · Cited by 26
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“We evaluated CMV-specific cellular responses by monitoring the levels of CD137 surface marker expressed on CMV-specific T-cells[26,35].”
BackgroundMethodResultInfluential
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BackgroundMethod
Novel Strategies to Combat CMV-Related Cardiovascular Disease
Vasilieva, E., Gianella, S., & Freeman, M. L. (2020) · Pathogens and Immunity · doi:10.20411/pai.v5i1.382 · Cited by 27
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Background
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Reus, B., Caserta, S., Larsen, M., Morrow, G. W., Bano, A., Hallensleben, M., Rajkumar, C., Pera, A., & Kern, F. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.707830 · Cited by 25
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BackgroundResultInfluentialSelf-citation
Characterization of humoral and cellular immunologic responses to an mRNA-based human cytomegalovirus vaccine from a phase 1 trial of healthy adults
Wu, K., Hou, Y. J., Makrinos, D. L., Liu, R., Zhu, A. L., Koch, M., Yu, W., Paila, Y. D., Chandramouli, S., Panther, L., et al. (2024) · Journal of Virology · doi:10.1128/jvi.01603-23 · Cited by 26
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Background
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“, 2000) or by flow cytometry intracellular cytokine staining (Sylwester et al., 2005).”
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“It has been reported, however, that some CD4 T cells also respond to pp65 and IE-1 peptide stimulation (2, 37 ), and we cannot rule out the possibility that our approach underestimates the contribution of CD4 T cells to defense against HCMV.”
BackgroundResult
Identification of Major Histocompatibility Complex Restriction and Anchor Residues of Foot-and-Mouth Disease Virus-Derived Bovine T-Cell Epitopes
Gerner, W., Hammer, S. E., Wiesmüller, K., & Saalmüller, A. (2009) · Journal of Virology · doi:10.1128/jvi.01534-08 · Cited by 25
Primate betaherpesviruses
Barry, P. A., & Chang, W. L. W. (2007) · Cambridge University Press eBooks · doi:10.1017/cbo9780511545313.060 · Cited by 25
Acute metabolic, hormonal, and psychological responses to strength training with superimposed EMS at the beginning and the end of a 6 week training period.
Wirtz, N., Wahl, P., Kleinöder, H., Wechsler, K., Achtzehn, S., & Mester, J. (2015) · Europe PMC (PubMed Central) · Cited by 25
Qa-1-Restricted CD8+ T Cells Can Compensate for the Absence of Conventional T Cells during Viral Infection
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PD‐1‐specific “Blocking” antibodies that deplete PD‐1 + T cells present an inconvenient variable in preclinical immunotherapy experiments
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“Cytomegaloviruses (CMV) are ubiquitous herpesvirus family members that infect most mammalian species and induce robust CD8 T cell responses (Munks et al., 2006; Snyder et al., 2011; Sylwester et al., 2005).”
Background
Modeling T Cell Fate
de Boer, R. J., & Yates, A. J. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101721-040924 · Cited by 29
Development of a novel, guinea pig-specific IFN-γ ELISPOT assay and characterization of guinea pig cytomegalovirus GP83-specific cellular immune responses following immunization with a modified vaccinia virus Ankara (MVA)-vectored GP83 vaccine
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CMV drives the expansion of highly functional memory T cells expressing NK‐cell receptors in renal transplant recipients
Makwana, N., Foley, B. A., Fernández, S., Lee, S., Irish, A. B., Pircher, H., & Price, P. (2017) · European Journal of Immunology · doi:10.1002/eji.201747018 · Cited by 24
Immune Protection by a Cytomegalovirus Vaccine Vector Expressing a Single Low-Avidity Epitope
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“It induces a life-long effector memory T cell response that is stronger than any other reported in human medicine (13).”
Background
T-cell immunity against cytomegalovirus in HIV infection and aging: relationships with inflammation, immune activation, and frailty
Tavenier, J., Margolick, J. B., & Leng, S. X. (2019) · Medical Microbiology and Immunology · doi:10.1007/s00430-019-00591-z · Cited by 25
High-Quality CMV-Specific CD4+ Memory Is Enriched in the Lung Allograft and Is Associated With Mucosal Viral Control
Akulian, J., Pipeling, M., John, E. R., Orens, J., Lechtzin, N., & McDyer, J. (2012) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2012.04282.x · Cited by 23
“While our studies predominantly focused on responses to pp65 (49), we recognize the total CMV memory response is considerably larger as additional antigens contribute to a broad CD4+ and CD8+ T cell response to CMV (50).”
Method
Cross‐presentation of peptides from intracellular pathogens by MHC class I molecules
Blanchard, N., & Shastri, N. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05135.x · Cited by 24
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Background
A single-dose cytomegalovirus-based vaccine encoding tetanus toxin fragment C induces sustained levels of protective tetanus toxin antibodies in mice
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Multiple sclerosis and drug discovery: A work of translation
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“nodominance of the major epitopes (18, 23, 32 ).”
Background
Cytomegalovirus Infection- and Age-Dependent Changes in Human CD8 + T-Cell Cytokine Expression Patterns
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Impact of Persistent Cytomegalovirus Infection on Dynamic Changes in Human Immune System Profile
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Cytomegalovirus mediates expansion of IL-15–responsive innate-memory cells with SIV killing function
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BackgroundInfluential
In vitro expansion of polyclonal T-cell subsets for adoptive immunotherapy by recombinant modified vaccinia Ankara
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Robust Expansion of Viral Antigen-specific CD4+ and CD8+ T Cells for Adoptive T Cell Therapy Using Gene-modified Activated T Cells as Antigen Presenting Cells
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Clinical implications of cytomegalovirus in glioblastoma progression and therapy
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Evidence for Less Marked Potential Signs of T-Cell Immunosenescence in Centenarian Offspring Than in the General Age-Matched Population
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“In general, CD4 as well as CD8 T cells are affected by chronic CMV response, although the magnitude of the effect is greater for CD8 T cells (38,39), and other herpes viruses probably contribute little (40).”
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Specific removal of alloreactive T-cells to prevent GvHD in hemopoietic stem cell transplantation: rationale, strategies and perspectives
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Background
A B Cell-Driven Autoimmune Pathway Leading to Pathological Hallmarks of Progressive Multiple Sclerosis in the Marmoset Experimental Autoimmune Encephalomyelitis Model
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“This mechanism involves the cross talk of B cells infected with Callithrichine herpesvirus-3 (CalHV3) and CD8+ CD56+ effector memory cytotoxic T cells, which are reactive with a cytomegalovirus (CMV) antigen (26).”
BackgroundInfluential
Vaccine Development for Cytomegalovirus
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Chimeric Antigen Receptors Targeting Human Cytomegalovirus
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Is It Feasible to Use CMV-Specific T-Cell Adoptive Transfer as Treatment Against Infection in SOT Recipients?
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Cytomegalovirus Seropositivity in Older Adults Changes the T Cell Repertoire but Does Not Prevent Antibody or Cellular Responses to SARS-CoV-2 Vaccination
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Cytomegalovirus‐specific CD8 + T cells targeting different HLA/peptide combinations correlate with protection but at different threshold frequencies
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“It is, however, clear from extensive profiling studies that pp65, IE-1 and pp50 (presented by HLA-A1) and possibly UL48 (Sylwester et al, 2005) are the most dominant CMV antigens recognised by CD8+ T cells in the background of different HLA specificities whereas CD8+ T cells targeting gB, gH, pp28,…”
Background
Vaccination with synthetic constructs expressing cytomegalovirus immunogens is highly T cell immunogenic in mice
Shedlock, D. J., Talbott, K. T., Wu, S. J., Wilson, C., Muthumani, K., Boyer, J., Sardesai, N. Y., Awasthi, S., & Weiner, D. B. (2012) · Human Vaccines & Immunotherapeutics · doi:10.4161/hv.22447 · Cited by 22
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“In fact, ,10% of memory CD4 and CD8 T-cells in long-term infected hosts are HCMV-specific [2], and generate antibodies against multiple HCMV glycoproteins that neutralize the virus [3,4].”
Background
Expression of the Human Cytomegalovirus UL11 Glycoprotein in Viral Infection and Evaluation of Its Effect on Virus-Specific CD8 T Cells
Gabaev, I., Elbasani, E., Ameres, S., Steinbrück, L., Stanton, R. J., Döring, M., Roviš, T. L., Kalinke, U., Jonjić, S., Moosmann, A., et al. (2014) · Journal of Virology · doi:10.1128/jvi.01691-14 · Cited by 21
Assessment of the T-SPOT.CMV interferon-γ release assay in renal transplant recipients: A single center cohort study
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From Vaccine Vector to Oncomodulation: Understanding the Complex Interplay between CMV and Cancer
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Repertoire characterization and validation of gB-specific human IgGs directly cloned from humanized mice vaccinated with dendritic cells and protected against HCMV
Theobald, S. J., Kreer, C., Khailaie, S., Bonifacius, A., Eiz‐Vesper, B., Figueiredo, C., Mach, M., Backović, M., Ballmaier, M., Koenig, J., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008560 · Cited by 22
“Interestingly, these markers have also been associated with protection against HCMV in humans in keeping the infection dormant [38, 39].”
Background
How to Define Biomarkers of Human T Cell Aging and Immunocompetence?
Herndler‐Brandstetter, D., Ishigame, H., & Flavell, R. A. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00136 · Cited by 22
“This indicates that the expansion and accumulation of high numbers of HCMV-specific effector-memory T cells (T EM ) leads to an exhaustion of the naïve T cell pool (Sylwester et al., 2005).”
Background
Measurement of antigen specific immune responses: 2006 update
Pira, G. L., Kern, F., Gratama, J. W., Roederer, M., & Manca, F. (2007) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.20186 · Cited by 22
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BackgroundSelf-citation
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“The dominant antibodies binding to HCMV recognize gB, and gB-specific CD4 and CD8 T-cell responses are found in HCMV seropositive individuals.(14)”
Background
Comparison of the Cytomegalovirus (CMV) Enzyme-Linked Immunosorbent Spot and CMV QuantiFERON Cell-Mediated Immune Assays in CMV-Seropositive and -Seronegative Pregnant and Nonpregnant Women
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The Basis and Advances in Clinical Application of Cytomegalovirus-Specific Cytotoxic T Cell Immunotherapy for Glioblastoma Multiforme
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“Characteristics of CMV-Specific T Cells Derived From GB Patients In healthy individuals, CMV-specific CD8 and CD4 T cells account for 10% and 9% of blood CD8 and CD4 T cells, respectively (119).”
Background
Decoding Viral Infection by Ribosome Profiling
Stern‐Ginossar, N. (2015) · Journal of Virology · doi:10.1128/jvi.02528-14 · Cited by 21
“We reasoned that if humans with a history of HCMV infection displayed a memory T cell response to novel peptides, as they do to canonical HCMV proteins (14), it would indicate that these peptides were produced in the course of the normal viral life cycle in a human host.”
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“The factor(s) determining the magnitude of the HIV-1–specific CTL response during chronic infection are poorly understood; despite persistent viremia, this response is often lower in frequency than that of CMV-specific CTLs in chronic human CMV infection, which averages ∼10% of all blood CD8 T cells (26).”
Background
T-cell therapy for cytomegalovirus infection
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“By contrast, up to 20% of memory CD4 and CD8 T cells are specific for HCMV in seropositive persons (106).”
Background
A model for HCMV infection in immunosuppressed patients
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“6% (median) with a range of 0− 36% of the overall CD8+ population in blood [33].”
INFUSION OF CYTOMEGALOVIRUS SPECIFIC CYTOTOXIC T LYMPHOCYTES FROM A SERO-NEGATIVE DONOR CAN FACILITATE RESOLUTION OF INFECTION AND IMMUNE RECONSTITUTION
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Human Cytomegalovirus Enters the Primary CD34 + Hematopoietic Progenitor Cells Where It Establishes Latency by Macropinocytosis
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Characterization of the HCMV-Specific CD4 T Cell Responses that Are Associated with Protective Immunity
Wunsch, M., Zhang, W., Hanson, J., Caspell, R., Karulin, A. Y., Recks, M. S., Küerten, S., Sundararaman, S., & Lehmann, P. (2015) · Viruses · doi:10.3390/v7082828 · Cited by 20
“These episodes of virus reactivations lead to recurring stimulations and expansions of HCMV-specific T cells as a result of which up to 10% of all memory T cells can be HCMV specific in healthy individuals [7].”
Background

Authors: 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., & Picker, L. J.
Affiliations: Oregon National Primate Research Center (US)
Corixa Corporation (US)
Stiftung Charité (DE)
ORCID: Hosken, Nancy A.
Kern, Florian
Nelson, Jay A.
Picker, Louis J.
Venue: The Journal of Experimental Medicine
Publisher: Rockefeller University Press
Published: 2005-09-05
Volume: 202
Issue: 5
Pages: 673-685
ISSN: 0022-1007 (ISSN-L)
1540-9538
DOI: 10.1084/jem.20050882
PMC: PMC2212883
OpenAlex: W2103849595
Cited by: 1,339
References: 41
Citations by year: 2026: 39 · 2025: 53 · 2024: 56 · 2023: 41 · 2022: 56 · 2021: 70 · 2020: 67 · 2019: 81 · 2018: 71 · 2017: 86 · 2016: 74 · 2015: 77 · 2014: 56 · 2013: 83 · 2012: 64
FWCI: 38.39
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: The Journal of Experimental Medicine (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Funders: National Institutes of Health (RR 00163, AI21640)
National Institute of Allergy and Infectious Diseases (R01AI047606, AI 47606, R01AI021640)
National Center for Research Resources (P51RR000163, M01RR000334)
Topics: Health Sciences › Medicine › Epidemiology › Cytomegalovirus and herpesvirus research
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
Keywords: human cytomegalovirus, CD4+ T cells, CD8+ T cells, immunodominance, seropositive individuals, viral persistence
MeSH terms: Adult, Cytomegalovirus Infections, Cytomegalovirus, Female, Flow Cytometry, Humans, Immunogenetics, Immunologic Memory, Male, Middle Aged, Peptides, Serologic Tests, CD4-Positive T-Lymphocytes, Open Reading Frames, CD8-Positive T-Lymphocytes

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Broadly targeted human cytomegalovirus-specific CD4 + and CD8 + T cells dominate the memory compartments of exposed subjects

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