The multifaceted role of CD4+ T cells in CD8+ T cell memory

Laidlaw, Brian J.; Craft, Joseph E.; Kaech, Susan M.

doi:10.1038/nri.2015.10

Cited by 657T-cell and B-cell ImmunologyImmunotherapy and Immune ResponsesImmune responses and vaccinations

The multifaceted role of CD4+ T cells in CD8+ T cell memory

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Laidlaw, Brian J., Craft, Joseph E., Kaech, Susan M.·2016·Nature Reviews Immunology

DOI 10.1038/nri.2015.10PMC PMC4860014

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Abstract

Following infection, T cells differentiate into a heterogeneous population of effector T cells that can mediate pathogen clearance. A subset of these effector T cells possesses the ability to survive long term and mature into memory T cells that can provide long-term immunity. Understanding the signals that regulate the development of memory T cells is crucial to efforts to design vaccines capable of eliciting T cell-based immunity. CD4(+) T cells are essential in the formation of protective memory CD8(+) T cells following infection or immunization. However, until recently, the mechanisms by which CD4(+) T cells act to support memory CD8(+) T cell development following infection were unclear. Here, we discuss recent studies that provide insight into the multifaceted role of CD4(+) T cells in the regulation of memory CD8(+) T cell differentiation.

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The thymus is a crucial lymphoid organ responsible for the proliferation and differentiation of T cells.
“The thymus is a crucial lymphoid organ that is responsible for the proliferation and differentiation of T cells.”
From Chronic stress-induced depression requires the recruitment of peripheral Th17 cells into the brain (2022) · cites this paper as [61]
The sections on CD4+ T-cell help following systemic infection and on memory T cells discuss T-cell differentiation and proliferation, but do not describe the thymus as responsible for either process. Searches for thymus and thymic T-cell development found no passage addressing that claim in our copy; page numbers were not provided. (LLM, conf=0.76)
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Autocrine IL-2 is required for secondary population expansion of CD8+ memory T cells
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Dynamic Treg interactions with intratumoral APCs promote local CTL dysfunction
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Functional analysis of T lymphocyte subsets in antiviral host defense.
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Transcription Factor STAT3 and Type I Interferons Are Corepressive Insulators for Differentiation of Follicular Helper and T Helper 1 Cells
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The generation of protective memory-like CD8+ T cells during homeostatic proliferation requires CD4+ T cells
Hamilton, S. E., Wolkers, M. C., Schoenberger, S. P., & Jameson, S. C. (2006) · Nature Immunology · doi:10.1038/ni1326 · Cited by 216 · see citing works
Interplay between regulatory T cells and PD-1 in modulating T cell exhaustion and viral control during chronic LCMV infection
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Regulatory CD4+CD25+ T Cells Restrict Memory CD8+ T Cell Responses
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Skin-resident memory CD4+ T cells enhance protection against Leishmania major infection
Glennie, N. D., Yeramilli, V. A., Beiting, D. P., Volk, S. W., Weaver, C. T., & Scott, P. (2015) · Journal of Experimental Medicine · doi:10.1084/jem.20142101 · Cited by 204 · see citing works
Epigenetic Remodeling of the IL-2 and IFN -γ Loci in Memory CD8 T Cells Is Influenced by CD4 T Cells
Northrop, J. K., Thomas, R. M., Wells, A. D., & Shen, H. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.2.1062 · Cited by 203 · see citing works
CD4 + CD25 + regulatory T cells control CD8 + T-cell effector differentiation by modulating IL-2 homeostasis
McNally, A., Hill, G. R., Sparwasser, T. D., Thomas, R., & Steptoe, R. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103782108 · Cited by 201 · see citing works
CD4 + T cell regulation of CD25 expression controls development of short-lived effector CD8 + T cells in primary and secondary responses
Obar, J. J., Molloy, M. J., Jellison, E. R., Stoklasek, T. A., Zhang, W., Usherwood, E. J., & Lefrançois, L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909945107 · Cited by 198 · see citing works
Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection
Aubert, R. D., Kamphorst, A. O., Sarkar, S., Vezys, V., Ha, S., Barber, D. L., Ye, L., Sharpe, A. H., Freeman, G. J., & Ahmed, R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118450109 · Cited by 198 · see citing works
Production of IL-10 by CD4+ regulatory T cells during the resolution of infection promotes the maturation of memory CD8+ T cells
Laidlaw, B. J., Cui, W., Amezquita, R. A., Gray, S. M., Guan, T., Lu, Y., Kobayashi, Y., Flavell, R. A., Kleinstein, S. H., Craft, J. E., et al. (2015) · Nature Immunology · doi:10.1038/ni.3224 · Cited by 194 · see citing works
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HIV-1-Specific Interleukin-21 + CD4 + T Cell Responses Contribute to Durable Viral Control through the Modulation of HIV-Specific CD8 + T Cell Function
Chevalier, M. F., Jülg, B. D., Pyo, A., Flanders, M., Ranasinghe, S., Soghoian, D. Z., Kwon, D. S., Rychert, J. A., Lian, J., Muller, M. I., et al. (2010) · Journal of Virology · doi:10.1128/jvi.02030-10 · Cited by 189 · see citing works
Differential role of IL‐2R signaling for CD8+ T cell responses in acute and chronic viral infections
Bachmann, M. F., Wolint, P., Walton, S. M., Schwarz, K., & Oxenius, A. (2007) · European Journal of Immunology · doi:10.1002/eji.200637023 · Cited by 184 · see citing works
IL-21 receptor signaling is integral to the development of Th2 effector responses in vivo.
Fröhlich, A., Marsland, B., Sonderegger, I., Kurrer, M., Hodge, M., Harris, N., & Kopf, M. (2007) · Blood · doi:10.1182/blood-2006-05-021600 · Cited by 184 · see citing works
Role of CD4 T Cell Help and Costimulation in CD8 T Cell Responses During Listeria monocytogenes Infection
Shedlock, D. J., Whitmire, J. K., Tan, J. T., MacDonald, A. S., Ahmed, R., & Shen, H. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.4.2053 · Cited by 171 · see citing works
Antibody-targeted vaccination to lung dendritic cells generates tissue-resident memory CD8 T cells that are highly protective against influenza virus infection
Wakim, L. M., Smith, J., Caminschi, I., Lahoud, M. H., & Villadangos, J. A. (2015) · Mucosal Immunology · doi:10.1038/mi.2014.133 · Cited by 167 · see citing works
T cell mediated immunity to influenza: mechanisms of viral control
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IL-10 directly suppresses CD4 but not CD8 T cell effector and memory responses following acute viral infection
Brooks, D. G., Walsh, K. B., Elsaesser, H. J., & Oldstone, M. B. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914500107 · Cited by 161 · see citing works
Type I interferons directly inhibit regulatory T cells to allow optimal antiviral T cell responses during acute LCMV infection
Srivastava, S., Koch, M. A., Pepper, M., & Campbell, D. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20131556 · Cited by 160 · see citing works
IL-15 as a mediator of CD4 + help for CD8 + T cell longevity and avoidance of TRAIL-mediated apoptosis
Oh, S., Perera, L. P., Terabe, M., Ni, L., Waldmann, T. A., & Berzofsky, J. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801003105 · Cited by 154 · see citing works
Regulatory T Cells Increase the Avidity of Primary CD8 + T Cell Responses and Promote Memory
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CD4 T Cells Are Required for CD8 T Cell Survival during Both Primary and Memory Recall Responses
Novy, P., Quigley, M. M., Huang, X., & Yang, Y. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.12.8243 · Cited by 145 · see citing works
Tumor-Specific CD4+ T Cells Render the Tumor Environment Permissive for Infiltration by Low-Avidity CD8+ T Cells
Wong, S. B. J., Bos, R., & Sherman, L. A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.5.3122 · Cited by 144 · see citing works
T-Cell Vaccine Strategies for Human Immunodeficiency Virus, the Virus with a Thousand Faces
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A Critical Role of IL-21-Induced BATF in Sustaining CD8-T-Cell-Mediated Chronic Viral Control
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Diminished Primary and Secondary Influenza Virus-Specific CD8+T-Cell Responses in CD4-Depleted Ig−/−Mice
Riberdy, J. M., Christensen, J. P., Branum, K. C., & Doherty, P. C. (2000) · Journal of Virology · doi:10.1128/jvi.74.20.9762-9765.2000 · Cited by 138 · see citing works
Immune-based antitumor effects of BRAF inhibitors rely on signaling by CD40L and IFNγ
Ho, P.-C., Meeth, K. M., Tsui, Y.-C., Srivastava, B., Bosenberg, M. W., & Kaech, S. M. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-3461 · Cited by 126 · see citing works
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IL-2 Receptor Signaling Is Essential for the Development of Klrg1+ Terminally Differentiated T Regulatory Cells
Cheng, G., Yuan, X., Tsai, M. S., Podack, E. R., Yu, A., & Malek, T. R. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103768 · Cited by 125 · see citing works
Fully Functional Memory CD8 T Cells in the Absence of CD4 T Cells
Marzo, A. L., Vezys, V., Klonowski, K. D., Lee, S., Muralimohan, G., Moore, M. W., Tough, D. F., & Lefrançois, L. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.2.969 · Cited by 123 · see citing works
CTLA-4 regulates cell cycle progression during a primary immune response
Greenwald, R. J., Oosterwegel, M. A., van der Woude, D., Kubal, A., Mandelbrot, D. A., Boussiotis, V. A., & Sharpe, A. H. (2002) · European Journal of Immunology · doi:10.1002/1521-4141(200202)32:2 · Cited by 120 · see citing works
Tapping CD4 T Cells for Cancer Immunotherapy: The Choice of Personalized Genomics
Zanetti, M. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402669 · Cited by 119 · see citing works
Characteristics of the influenza virus-specific CD8+ T cell response in mice homozygous for disruption of the H-2lAb gene
Tripp, R. A., Sarawar, S. R., & Doherty, P. C. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.6.2955 · Cited by 118 · see citing works
From crucial to negligible: Functional CD 8+ T ‐cell responses and their dependence on CD 4+ T ‐cell help
Wiesel, M., & Oxenius, A. (2012) · European Journal of Immunology · doi:10.1002/eji.201142205 · Cited by 117 · see citing works
Differential Localization of Effector and Memory CD8 T Cell Subsets in Lymphoid Organs during Acute Viral Infection
Jung, Y. W., Rutishauser, R. L., Joshi, N. S., Haberman, A. M., & Kaech, S. M. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001948 · Cited by 111 · see citing works
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Regulatory T cells shape the resident memory T cell response to virus infection in the tissues.
Graham, J. B., da Costa, A. D., & Lund, J. M. (2013) · Journal of Immunology · doi:10.4049/jimmunol.1202153 · Cited by 110 · see citing works
Quiescence of Memory CD8+ T Cells Is Mediated by Regulatory T Cells through Inhibitory Receptor CTLA-4
Kalia, V., Penny, L. A., Yuzefpolskiy, Y., Baumann, F. M., & Sarkar, S. (2015) · Immunity · doi:10.1016/j.immuni.2015.05.023 · Cited by 108 · see citing works
Interleukin-21 Is a Critical Cytokine for the Generation of Virus-Specific Long-Lived Plasma Cells
Rasheed, M. A. U., Latner, D. R., Aubert, R. D., Gourley, T. S., Spolski, R. J., Davis, C. W., Langley, W. A., Ha, S., Ye, L., Sarkar, S., et al. (2013) · Journal of Virology · doi:10.1128/jvi.00063-13 · Cited by 106 · see citing works
Chronic Bystander Infections and Immunity to Unrelated Antigens
Stelekati, E., & Wherry, E. J. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.10.001 · Cited by 104 · see citing works
IL-10 Is Required for Optimal CD8 T Cell Memory following Listeria monocytogenes Infection
Foulds, K. E., Rotte, M. J., & Seder, R. A. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.4.2565 · Cited by 100 · see citing works
Cutting Edge: CD4+ T Cell-Derived IL-2 Is Essential for Help-Dependent Primary CD8+ T Cell Responses
Wilson, E. B., & Livingstone, A. M. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.11.7445 · Cited by 98 · see citing works
Bystander Chronic Infection Negatively Impacts Development of CD8+ T Cell Memory
Stelekati, E., Shin, H., Doering, T. A., Dolfi, D. V., Ziegler, C. G. K., Beiting, D. P., Dawson, L. A., Liboon, J., Wolski, D., Ali, M.-A., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.04.010 · Cited by 97 · see citing works
Cutting Edge: Long-Lived CD8 Memory and Protective Immunity in the Absence of CD40 Expression on CD8 T Cells
Sun, J. C.-Y., & Bevan, M. J. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.6.3385 · Cited by 96 · see citing works
CD4 + T cells support cytotoxic T lymphocyte priming by controlling lymph node input
Kumamoto, Y., Mattei, L. M., Sellers, S., Payne, G. W., & Iwasaki, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100567108 · Cited by 94 · see citing works
Type‐I IFN drives the differentiation of short‐lived effector CD8+ T cells in vivo
Wiesel, M., Crouse, J., Bedenikovic, G., Sutherland, A. P. R., Joller, N., & Oxenius, A. (2011) · European Journal of Immunology · doi:10.1002/eji.201142091 · Cited by 91 · see citing works
CD40-deficient, Influenza-specific CD8 Memory T Cells Develop and Function Normally in a CD40-sufficient Environment
Lee, B. O., Hartson, L., & Randall, T. D. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20031440 · Cited by 91 · see citing works
Chemokine-Guided CD4+ T Cell Help Enhances Generation of IL-6RαhighIL-7Rαhigh Prememory CD8+ T Cells
Castellino, F., & Germain, R. N. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.2.778 · Cited by 90 · see citing works
Interleukin-21-Producing HIV-1-Specific CD8 T Cells Are Preferentially Seen in Elite Controllers
Williams, L. D., Bansal, A., Sabbaj, S., Heath, S. L., Song, W., Tang, J., Zajac, A. J., & Goepfert, P. (2010) · Journal of Virology · doi:10.1128/jvi.01476-10 · Cited by 90 · see citing works
Cutting Edge: Chromatin Remodeling as a Molecular Basis for the Enhanced Functionality of Memory CD8 T Cells
Northrop, J. K., Wells, A. D., & Shen, H. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.2.865 · Cited by 89 · see citing works
Chronic viral infection promotes sustained Th1-derived immunoregulatory IL-10 via BLIMP-1
Parish, I. A., Marshall, H. D., Staron, M. M., Lang, P. A., Brüstle, A., Chen, J. H., Cui, W., Tsui, Y.-C., Perry, C. J., Laidlaw, B. J., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci66108 · Cited by 88 · see citing works
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CD4+ T Cell Help Has an Epitope-Dependent Impact on CD8+ T Cell Memory Inflation during Murine Cytomegalovirus Infection
Snyder, C. M., Loewendorf, A. I., Bonnett, E. L., Croft, M., Benedict, C. A., & Hill, A. B. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900227 · Cited by 78 · see citing works
CD4 T-Cell Immunotherapy for Chronic Viral Infections and Cancer
Kamphorst, A. O., & Ahmed, R. (2013) · Immunotherapy · doi:10.2217/imt.13.91 · Cited by 67 · see citing works
Maintenance of memory CTL responses by T helper cells and CD40‐CD40 ligand: antibodies provide the key
Bachmann, M. F., Hunziker, L., Zinkernagel, R. M., Storni, T., & Köpf, M. (2004) · European Journal of Immunology · doi:10.1002/eji.200324717 · Cited by 67 · see citing works
NKG2D signaling on CD8+ T cells represses T-bet and rescues CD4-unhelped CD8+ T cell memory recall but not effector responses
Zloza, A., Kohlhapp, F. J., Lyons, G. E., Schenkel, J. M., Moore, T. V., Lacek, A. T., O’Sullivan, J. A., Varanasi, V., Williams, J. W., Jagoda, M. C., et al. (2012) · Nature Medicine · doi:10.1038/nm.2683 · Cited by 66 · see citing works
TLR3 ligand stimulates fully functional memory CD8+ T cells in the absence of CD4+ T-cell help
Hervás‐Stubbs, S., Olivier, A., Boisgérault, F., Thiéblemont, N., & Leclerc, C. (2007) · Blood · doi:10.1182/blood-2006-10-053256 · Cited by 61 · see citing works
FoxP3+ regulatory CD4 T cells control the generation of functional CD8 memory
de Herve, M. G. D. G., Jaafoura, S., Vallée, M., & Taoufik, Y. (2012) · Nature Communications · doi:10.1038/ncomms1992 · Cited by 53 · see citing works
Listeria monocytogenes Infection Overcomes the Requirement for CD40 Ligand in Exogenous Antigen Presentation to CD8+ T Cells
Hamilton, S. E., Tvinnereim, A., & Harty, J. T. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.10.5603 · Cited by 49 · see citing works
CD4+ T helper cells use CD154–CD40 interactions to counteract T reg cell–mediated suppression of CD8+ T cell responses to influenza
Ballesteros‐Tato, A., León, B., Lund, F. E., & Randall, T. D. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20130097 · Cited by 46 · see citing works
Th Cells Act Via Two Synergistic Pathways To Promote Antiviral CD8+ T Cell Responses
Wiesel, M., Joller, N., Ehlert, A.-K., Crouse, J., Spörri, R., Bachmann, M. F., & Oxenius, A. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001990 · Cited by 42 · see citing works
The Antiviral CD8+ T Cell Response Is Differentially Dependent on CD4+ T Cell Help Over the Course of Persistent Infection
Kemball, C. C., Pack, C. D., Guay, H., Li, Z.-N., Steinhauer, D. A., Szomolanyi‐Tsuda, E., & Lukacher, A. E. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.2.1113 · Cited by 40 · see citing works
TRAIL Deficiency Does Not Rescue Impaired CD8+ T Cell Memory Generated in the Absence of CD4+ T Cell Help
Sacks, J. A., & Bevan, M. J. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.7.4570 · Cited by 39 · see citing works
Nab2 regulates secondary CD8+ T-cell responses through control of TRAIL expression
Wolkers, M. C., Gerlach, C., Arens, R., Janssen, E. M., Fitzgerald, P., Schumacher, T. N., Medema, J. P., Green, D. R., & Schoenberger, S. P. (2011) · Blood · doi:10.1182/blood-2011-08-373910 · Cited by 30 · see citing works
Regulatory T Cells Target Chemokine Secretion by Dendritic Cells Independently of Their Capacity To Regulate T Cell Proliferation
Morlacchi, S., Secco, V. D., Soldani, C., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003265 · Cited by 26 · see citing works
Tunable Chemokine Production by Antigen Presenting Dendritic Cells in Response to Changes in Regulatory T Cell Frequency in Mouse Reactive Lymph Nodes
Secco, V. D., Soldani, C., Debrat, C., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007696 · Cited by 24 · see citing works
CD8 T Cell Tolerance to a Tumor-Associated Self-Antigen Is Reversed by CD4 T Cells Engineered To Express the Same T Cell Receptor
Ghorashian, S., Veliça, P., Chua, I. C., McNicol, A., Carpenter, B., Holler, A., Nicholson, E., Ahmadi, M., Zech, M., Xue, S., et al. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1401703 · Cited by 22 · see citing works
CD154 and IL-2 Signaling of CD4+ T Cells Play a Critical Role in Multiple Phases of CD8+ CTL Responses Following Adenovirus Vaccination
Umeshappa, C. S., Nanjundappa, R. H., Xie, Y., Freywald, A., Deng, Y., Ma, H., & Xiang, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047004 · Cited by 17 · see citing works
CD4+ T Cell Effects on CD8+ T Cell Location Defined Using Bioluminescence
Azadniv, M., Bowers, W., Topham, D., & Crispe, I. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016222 · Cited by 6 · see citing works

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CD4+ T cell help in cancer immunology and immunotherapy
Borst, J., Ahrends, T., Bąbała, N., Melief, C. J. M., & Kastenmüller, W. (2018) · Nature Reviews Immunology · doi:10.1038/s41577-018-0044-0 · Cited by 1,585 · see citing works
Tissue-resident memory T cells: local specialists in immune defence
Mueller, S. N., & Mackay, L. K. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2015.3 · Cited by 1,006 · see citing works
cDC1 prime and are licensed by CD4(+) T cells to induce anti-tumour immunity
Ferris, S. T., Durai, V., Wu, R., Theisen, D. J., Ward, J. P., Bern, M. D., Davidson, J. T., Bagadia, P., Liu, T., Briseño, C. G., et al. (2020) · Nature · doi:10.1038/s41586-020-2611-3 · Cited by 611 · see citing works
Metal Drugs and the Anticancer Immune Response
Englinger, B., Pirker, C., Heffeter, P., Terenzi, A., Kowol, C. R., Keppler, B. K., & Berger, W. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00396 · Cited by 355 · see citing works
CD4+ T cell memory
Künzli, M., & Masopust, D. (2023) · Nature Immunology · doi:10.1038/s41590-023-01510-4 · Cited by 338 · see citing works
The Evolving Role of CD8+CD28− Immunosenescent T Cells in Cancer Immunology
Huff, W. X., Kwon, J. H., Henriquez, M., Fetcko, K., & Dey, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112810 · Cited by 217 · see citing works
Role of inflammasomes in multiple sclerosis and their potential as therapeutic targets
Govindarajan, V., de Rivero Vaccari, J. P., & Keane, R. W. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01944-9 · Cited by 110 · see citing works
Chronic stress-induced depression requires the recruitment of peripheral Th17 cells into the brain
Peng, Z., Peng, S., Lin, K., Zhao, B., Wei, L., Tuo, Q., Liao, D., Yuan, T., & Shi, Z. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02543-6 · Cited by 95 · see citing works
Intestinal Barrier Interactions with Specialized CD8 T Cells
Konjar, Š., Ferreira, C., Blankenhaus, B., & Veldhoen, M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01281 · Cited by 77 · see citing works
Scientific rationale for combination immunotherapy of hepatocellular carcinoma with anti–PD-1/PD-L1 and anti–CTLA-4 antibodies
Kudo, M. (2019) · Liver Cancer · doi:10.1159/000503254 · Cited by 70 · see citing works
High-titer AAV disrupts cerebrovascular integrity and induces lymphocyte infiltration in adult mouse brain
Guo, Y., Chen, J., Ji, W., Xu, L., Xie, Y., He, S., Lai, C., Hou, K., Li, Z., Chen, G., et al. (2023) · Molecular Therapy Methods & Clinical Development · doi:10.1016/j.omtm.2023.08.021 · Cited by 47 · see citing works

Bim regulates the entry of poorly functional and/or low avidity Th1 effector cells into the memory pool (85.15)
Williams, M., & Jay, D. C. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.184.supp.85.15
Activated CD4+ CD25+ T cells suppress antigen‐specific CD4+ and CD8+ T cells but induce a suppressive phenotype only in CD4+ T cells
Dieckmann, D., Plöttner, H., Dotterweich, S., et al. (2005) · Immunology · doi:10.1111/j.1365-2567.2005.02144.x · Cited by 37 · see citing works
Characterization of mouse CD4 T cell subsets defined by expression of KLRG1
Beyersdorf, N., Ding, X., Tietze, J. K., & Hanke, T. (2007) · European Journal of Immunology · doi:10.1002/eji.200737126 · Cited by 81 · see citing works
CD25+ CD4+ T Cells Regulate the Expansion of Peripheral CD4 T Cells Through the Production of IL-10
Annacker, O., Pimenta‐Araujo, R., Burlen‐Defranoux, O., Barbosa, T., Cumano, A., & Bandeira, A. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.5.3008 · Cited by 553 · see citing works
CD4+CD25+ Immunoregulatory T Cells Suppress Polyclonal T Cell Activation In Vitro by Inhibiting Interleukin 2 Production
Thornton, A. M., & Shevach, E. M. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.2.287 · Cited by 2,637 · see citing works

Authors: Laidlaw, B. J., Craft, J. E., & Kaech, S. M.
Affiliations: University of California, San Francisco (US)
Yale University (US)
Howard Hughes Medical Institute (US)
Corresponding author: Laidlaw, Brian J.
ORCID: Laidlaw, Brian J.
Craft, Joseph E.
Kaech, Susan M.
Venue: Nature Reviews Immunology
Publisher: Springer Science and Business Media LLC
Published: 2016-01-19
Volume: 16
Issue: 2
Pages: 102-111
ISSN: 1474-1733 (ISSN-L)
1474-1741
DOI: 10.1038/nri.2015.10
PMC: PMC4860014
OpenAlex: W2264544376
Cited by: 657
References: 145
Citations by year: 2026: 63 · 2025: 71 · 2024: 98 · 2023: 86 · 2022: 80 · 2021: 77 · 2020: 51 · 2019: 46 · 2018: 47 · 2017: 22 · 2016: 14 · 2015: 2
FWCI: 4.15
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature reviews. Immunology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
National Institute on Aging (F31AG047777, F31AG07777)
National Institute of Allergy and Infectious Diseases (T32 AI-07019, R37AI066232, R01AI074699, T32AI007019, R01AI066232)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R21AR063942, P30AR053495, R01 AR40072, R01AR040072, R37AR040072)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Keywords: CD4+ T cells, CD8+ T cell memory, memory T cell differentiation, T cell help, vaccine design, T cell-based immunotherapy, effector T cells, long-term immunity, infection-induced immunity
MeSH terms: Humans, Immunization, Immunologic Memory, Infections, Vaccination, CD4-Positive T-Lymphocytes, CD8-Positive T-Lymphocytes

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The multifaceted role of CD4+ T cells in CD8+ T cell memory

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