Cited by 1,635T-cell and B-cell ImmunologyImmunotherapy and Immune ResponsesImmune responses and vaccinations

The DOI matches its Crossref record; 28 of the 28 references it cites were found in a registry or an index.

CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes

Janssen, Edith M., Lemmens, Edward E., Wolfe, Tom, Christen, Urs, von Herrath, Matthias G., Schoenberger, Stephen P.·2003·Nature

DOI 10.1038/nature01441

Open this paper in CoChat — free account

Abstract

A long-standing paradox in cellular immunology concerns the conditional requirement for CD4+ T-helper (T(H)) cells in the priming of cytotoxic CD8+ T lymphocyte (CTL) responses in vivo. Whereas CTL responses against certain viruses can be primed in the absence of CD4+ T cells, others, such as those mediated through 'cross-priming' by host antigen-presenting cells, are dependent on T(H) cells. A clearer understanding of the contribution of T(H) cells to CTL development has been hampered by the fact that most T(H)-independent responses have been demonstrated ex vivo as primary cytotoxic effectors, whereas T(H)-dependent responses generally require secondary in vitro re-stimulation for their detection. Here, we have monitored the primary and secondary responses of T(H)-dependent and T(H)-independent CTLs and find in both cases that CD4+ T cells are dispensable for primary expansion of CD8+ T cells and their differentiation into cytotoxic effectors. However, secondary CTL expansion (that is, a secondary response upon re-encounter with antigen) is wholly dependent on the presence of T(H) cells during, but not after, priming. Our results demonstrate that T-cell help is 'programmed' into CD8+ T cells during priming, conferring on these cells a hallmark of immune response memory: the capacity for functional expansion on re-encounter with antigen.

Integrity signals

Registry

Crossref · 10.1038/nature01441

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Tolerance, Danger, and the Extended Family
Matzinger, P. (1994) · Annual Review of Immunology · doi:10.1146/annurev.iy.12.040194.005015 · Cited by 4,848
T-cell help for cytotoxic T lymphocytes is mediated by CD40–CD40L interactions
Schoenberger, S. P., Toes, R. E. M., van der Voort, E. I. H., Offringa, R., & Melief, C. J. M. (1998) · Nature · doi:10.1038/31002 · Cited by 2,615
Self-citation
A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell
Ridge, J. P., Rosa, F. D., & Matzinger, P. (1998) · Nature · doi:10.1038/30989 · Cited by 2,360
Help for cytotoxic-T-cell responses is mediated by CD40 signalling
Bennett, S. R. M., Carbone, F., Karamalis, F., Flavell, R. A., Miller, J. F. A. P., & Heath, W. R. (1998) · Nature · doi:10.1038/30996 · Cited by 2,091
Effector and memory T-cell differentiation: implications for vaccine development
Kaech, S. M., Wherry, E. J., & Ahmed, R. (2002) · Nature Reviews Immunology · doi:10.1038/nri778 · Cited by 1,865
Immunological memory and protective immunity: understanding their relation
Ahmed, R., & Gray, D. (1996) · Science · doi:10.1126/science.272.5258.54 · Cited by 1,775 · cited 1×
“Although transition through these stages was thought to be governed by the presence and eventual elimination of antigen, mounting evidence suggests that CD8 p T-cell development is guided by an instructional programme that, once set into motion during priming, is executed independentl”
Background
Characterization of the murine T cell surface molecule, designated L3T4, identified by monoclonal antibody GK1.5: similarity of L3T4 to the human Leu-3/T4 molecule.
Dialynas, D. P., Quan, Z., Wall, K. A., Pierrès, A., Quintáns, J., Loken, M. R., Pierres, M., & Fitch, F. W. (1983) · The Journal of Immunology · doi:10.4049/jimmunol.131.5.2445 · Cited by 1,273
Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells
Kaech, S. M., & Ahmed, R. (2001) · Nature Immunology · doi:10.1038/87720 · Cited by 1,265
Naïve CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation
van Stipdonk, M. J. B., Lemmens, E. E., & Schoenberger, S. P. (2001) · Nature Immunology · doi:10.1038/87730 · Cited by 843
Self-citation
T Cell-Dependent B Cell Activation
Parker, D. C. (1993) · Annual Review of Immunology · doi:10.1146/annurev.iy.11.040193.001555 · Cited by 739

Flagged first, then by citations

Show all 28 references

Sorted by citations

Items 601–700 of 1,000

Death of CD4+ T Cells from Lymph Nodes during Primary SIVmac251 Infection Predicts the Rate of AIDS Progression
Viollet, L., Monceaux, V., Petit, F., Fang, R. H. T., Cumont, M., Hurtrel, B., & Estaquier, J. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.10.6685 · Cited by 42
Genetically programmed B lymphocytes are highly efficient in inducing anti-virus protective immunity mediated by central memory CD8 T cells
Castiglioni, P., Gerloni, M., & Zanetti, M. (2004) · Vaccine · doi:10.1016/j.vaccine.2004.06.028 · Cited by 42
The CD4+ T-cell response to adenovirus is focused against conserved residues within the hexon protein
Onion, D., Crompton, L. J., Milligan, D. W., Moss, P. A. H., Lee, S. P., & Mautner, V. (2007) · Journal of General Virology · doi:10.1099/vir.0.82867-0 · Cited by 42
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
TLR2 Engagement on Dendritic Cells Promotes High Frequency Effector and Memory CD4 T Cell Responses
Chandran, S. S., Verhoeven, D. E., Teijaro, J. R., Fenton, M. J., & Färber, D. L. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901683 · Cited by 44
Comparison of Different Live Vaccine Strategies In Vivo for Delivery of Protein Antigen or Antigen-Encoding DNA and mRNA by Virulence-AttenuatedListeria monocytogenes
Loeffler, D. I. M., Schoen, C. U., Goebel, W., & Pilgrim, S. (2006) · Infection and Immunity · doi:10.1128/iai.00112-06 · Cited by 42
A review concerning the breast cancer-related tumour microenvironment
Rodríguez-Bejarano, O. H., Parra-López, C., & Patarroyo, M. A. (2024) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2024.104389 · Cited by 47
Identification of CD4+ T Cell Epitopes in C. burnetii Antigens Targeted by Antibody Responses
Chen, C., Dow, C., Wang, P., Sidney, J., Read, A., Harmsen, A. G., Samuel, J. E., & Peters, B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017712 · Cited by 41
Allogeneic lymphocyte-licensed DCs expand T cells with improved antitumor activity and resistance to oxidative stress and immunosuppressive factors
Jin, C., Yu, D., Hillerdal, V., Wallgren, A., Karlsson‐Parra, A., & Essand, M. (2014) · Molecular Therapy — Methods & Clinical Development · doi:10.1038/mtm.2014.1 · Cited by 41
Cross-Presentation of Cell-Associated Antigens by Mouse Splenic Dendritic Cell Populations
Thacker, R. I., & Janssen, E. M. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00041 · Cited by 44
Self-citation
The expression of MHC class II molecules on murine breast tumors delays T-cell exhaustion, expands the T-cell repertoire, and slows tumor growth
McCaw, T. R., Li, M., Starenki, D., Cooper, S. J., Liu, M., Meza‐Perez, S., Arend, R. C., Buchsbaum, D. J., Forero, A., & Randall, T. D. (2018) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-018-2262-5 · Cited by 41
TACI-BLyS signaling via B-cell–dendritic cell cooperation is required for naive CD8+ T-cell priming in vivo
Durana, Y. D. D., Mantchev, G. T., Bram, R. J., & Franco, A. (2005) · Blood · doi:10.1182/blood-2004-12-4708 · Cited by 41
On the Role of CD4+ T Cells in the CD8+ T-Cell Response Elicited by Recombinant Adenovirus Vaccines
Yang, T. C., Millar, J., Groves, T., Zhou, W., Grinshtein, N., Parsons, R., Evelegh, C. M., Xing, Z., Wan, Y., & Bramson, J. L. (2007) · Molecular Therapy · doi:10.1038/sj.mt.6300130 · Cited by 41
Immune Exhaustion: Past Lessons and New Insights from Lymphocytic Choriomeningitis Virus
Kahan, S. M., & Zajac, A. J. (2019) · Viruses · doi:10.3390/v11020156 · Cited by 44
Studies using a viral challenge and CD8 T cell depletions on the roles of cellular and humoral immunity in the control of an SHIV-89.6P challenge in DNA/MVA-vaccinated macaques
Amara, R. R., Ibegbu, C., Villinger, F. J., Montefiori, D. C., Sharma, S., Nigam, P., Xu, Y., McClure, H. M., & Robinson, H. L. (2005) · Virology · doi:10.1016/j.virol.2005.08.027 · Cited by 41
Metastatic Melanoma Cells Evade Immune Detection by Silencing STAT1
Osborn, J. L., & Greer, S. F. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16024343 · Cited by 43
Tumor-Associated Antigen Expressing Listeria monocytogenes Induces Effective Primary and Memory T-Cell Responses Against Hepatic Colorectal Cancer Metastases
Olino, K. L., Wada, S., Edil, B. H., Pan, X., Meckel, K. F., Weber, W. P., Slansky, J. E., Tamada, K., Lauer, P., Brockstedt, D. G., et al. (2011) · Annals of Surgical Oncology · doi:10.1245/s10434-011-2037-0 · Cited by 40
Protective immunity towards intracellular pathogens
Huster, K. M., Stemberger, C., & Busch, D. H. (2006) · Current Opinion in Immunology · doi:10.1016/j.coi.2006.05.008 · Cited by 42
Coadministration of the fungal immunomodulatory protein FIP‐Fve and a tumour‐associated antigen enhanced antitumour immunity
Ding, Y., Seow, S. V., Huang, C. H., Liew, L. M., Lim, Y. C., Kuo, I.-C., & Chua, K. Y. (2009) · Immunology · doi:10.1111/j.1365-2567.2009.03099.x · Cited by 40
Impact of Cytotoxic-T-Lymphocyte Memory Induction without Virus-Specific CD4 + T-Cell Help on Control of a Simian Immunodeficiency Virus Challenge in Rhesus Macaques
Tsukamoto, T., Takeda, A., Yamamoto, T., Yamamoto, H., Kawada, M., & Matano, T. (2009) · Journal of Virology · doi:10.1128/jvi.01120-09 · Cited by 40
Induction of T cell-mediated immunity using a c-Myb DNA vaccine in a mouse model of colon cancer
Williams, B. B., Wall, M., Miao, Y. R., Williams, B., Bertoncello, I., Kershaw, M. H., Mantamadiotis, T., Haber, M., Norris, M. D., Gautam, A. M., et al. (2008) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-008-0497-2 · Cited by 40
Personalized peptide vaccines and their relation to other therapies in urological cancer
Kimura, T., Egawa, S., & Uemura, H. (2017) · Nature Reviews Urology · doi:10.1038/nrurol.2017.77 · Cited by 40
Requirement for CD4 T Cell Help in Maintenance of Memory CD8 T Cell Responses Is Epitope Dependent
Ramsburg, E. A., Publicover, J., Coppock, D., & Rose, J. K. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.10.6350 · Cited by 40
Cognate Memory CD4+ T Cells Generated with Dendritic Cell Priming Influence the Expansion, Trafficking, and Differentiation of Secondary CD8+ T Cells and Enhance Tumor Control
Hwang, M. L., Lukens, J. R., & Bullock, T. N. J. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.9.5829 · Cited by 40
Selective antigen‐specific CD4+T‐cell, but not CD8+T‐ or B‐cell, tolerance corrupts cancer immunotherapy
Snook, A. E., Magee, M. S., Schulz, S., & Waldman, S. A. (2014) · European Journal of Immunology · doi:10.1002/eji.201444539 · Cited by 40
CD8 and B cell memory: same strategy, same signals
Tanchot, C., & Rocha, B. (2003) · Nature Immunology · doi:10.1038/ni0503-431 · Cited by 40
Adoptive transfer of allogeneic tumor-specific T cells mediates effective regression of large tumors across major histocompatibility barriers
Boni, A., Muranski, P. J., Cassard, L., Wrzesinski, C., Paulos, C. M., Palmer, D. C., Gattinoni, L., Hinrichs, C. S., Chan, C., Rosenberg, S. A., et al. (2008) · Blood · doi:10.1182/blood-2008-07-169797 · Cited by 41
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
DNA and Adenoviral Vectors Encoding Carcinoembryonic Antigen Fused to Immunoenhancing Sequences Augment Antigen-Specific Immune Response and Confer Tumor Protection
Facciabene, A., Aurisicchio, L., Elia, L., Palombo, F., Mennuni, C., Ciliberto, G., & Monica, N. L. (2006) · Human Gene Therapy · doi:10.1089/hum.2006.17.81 · Cited by 40
Deletion of Naive CD8 T Cells Requires Persistent Antigen and Is Not Programmed by an Initial Signal from the Tolerogenic APC
Redmond, W. L., Hernández, J., & Sherman, L. A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.12.6349 · Cited by 40
Delivery of Interferon-α Transfected Dendritic Cells into Central Nervous System Tumors Enhances the Antitumor Efficacy of Peripheral Peptide-Based Vaccines
Okada, H., Tsugawa, T., Sato, H., Kuwashima, N., Gambotto, A. A., Okada, K., Dusak, J. E., Fellows-Mayle, W. K., Papworth, G. D., Watkins, S. C., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0130 · Cited by 40
Antigen presentation by an immature myeloid dendritic cell line does not cause CTL deletion in vivo, but generates CD8+ central memory-like T cells that can be rescued for full effector function
Dumortier, H., van Mierlo, G. J. D., Egan, D., van Ewijk, W., Toes, R. E. M., Offringa, R., & Melief, C. J. M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.2.855 · Cited by 39
Low GILT Expression is Associated with Poor Patient Survival in Diffuse Large B-Cell Lymphoma
Phipps‐Yonas, H., Cui, H., Sebastiao, N., Brunhoeber, P., Haddock, E. S., Deymier, M. J., Klapper, W., Lybarger, L. P., Roe, D. J., & Hastings, K. T. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00425 · Cited by 39
CD8 T Cell Memory Recall Is Enhanced by Novel Direct Interactions with CD4 T Cells Enabled by MHC Class II Transferred from APCs
Romagnoli, P. A., Premenko‐Lanier, M., Loria, G. D., & Altman, J. D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056999 · Cited by 40
Human papilloma virus status of penile squamous cell carcinoma is associated with differences in tumour-infiltrating T lymphocytes
Lohneis, P., Boral, Ş., Kaufmann, A. M., Lehmann, A., Schewe, C., Dietel, M., Anagnostopoulos, I., & Jöhrens, K. (2014) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-014-1713-4 · Cited by 39
Prolonged Antigen Storage Endows Merocytic Dendritic Cells with Enhanced Capacity To Prime Anti-Tumor Responses in Tumor-Bearing Mice
Reboulet, R. A., Hennies, C. M., Garcia, Z., Nierkens, S., & Janssen, E. M. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001619 · Cited by 39
Self-citation
Modulation of CD4 T Cell Response According to Tumor Cytokine Microenvironment
Accogli, T., Bruchard, M., & Végran, F. (2021) · Cancers · doi:10.3390/cancers13030373 · Cited by 43
Frontline: An in‐depth evaluation of the production of IL‐2 by antigen‐specific CD8 T cells in vivo
D’Souza, W. N., & Lefrançois, L. (2004) · European Journal of Immunology · doi:10.1002/eji.200425485 · Cited by 39
Striking Immunodominance Hierarchy of Naturally Occurring CD8+ and CD4+ T Cell Responses to Tumor Antigen NY-ESO-1
Jackson, H. M., Dimopoulos, N., Mifsud, N. A., Tai, T. Y., Chen, Q., Svobodová, S., Browning, J., Luescher, I. F., Stockert, L., Old, L. J., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.10.5908 · Cited by 39
Antibodies designed as effective cancer vaccines
Metheringham, R. L., Pudney, V. A., Gunn, B., Towey, M., Spendlove, I., & Durrant, L. G. (2009) · mAbs · doi:10.4161/mabs.1.1.7492 · Cited by 39
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 41
LV305, a dendritic cell-targeting integration-deficient ZVex TM -based lentiviral vector encoding NY-ESO-1, induces potent anti-tumor immune response
Albershardt, T. C., Campbell, D. J., Parsons, A. J., Slough, M. M., ter Meulen, J., & Berglund, P. (2016) · Molecular Therapy - Oncolytics · doi:10.1038/mto.2016.10 · Cited by 38
Analysis of SARS-CoV-2 isolates, namely the Wuhan strain, Delta variant, and Omicron variant, identifies differential immune profiles
Shahbaz, S., Bozorgmehr, N., Lu, J., Osman, M. S., Sligl, W., Tyrrell, D. L., & Elahi, S. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.01256-23 · Cited by 40
Comprehensive Review of Human Plasmodium falciparum-Specific CD8+ T Cell Epitopes
Heide, J., Vaughan, K. C., Sette, A., Jacobs, T., & Wiesch, J. S. Z. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00397 · Cited by 42
The role of sialic acid-binding immunoglobulin-like-lectin-1 (siglec-1) in immunology and infectious disease
Prenzler, S., Rudrawar, S., Waespy, M., Kelm, S., Anoopkumar‐Dukie, S., & Haselhorst, T. (2021) · International Reviews of Immunology · doi:10.1080/08830185.2021.1931171 · Cited by 40
Expansion and Contraction of HIV-Specific CD4 T Cells with Short Bursts of Viremia, but Physical Loss of the Majority of These Cells with Sustained Viral Replication
Seth, N. P., Kaufmann, D., Lahey, T., Rosenberg, E. S., & Wucherpfennig, K. W. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.10.6948 · Cited by 38
Prime-Boost with Alternating DNA Vaccines Designed to Engage Different Antigen Presentation Pathways Generates High Frequencies of Peptide-Specific CD8+ T Cells
Radcliffe, J. N., Roddick, J. S., Friedmann, P. S., Stevenson, F. K., & Thirdborough, S. M. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.10.6626 · Cited by 38
The dual role of dendritic cells in the immune response to human immunodeficiency virus type 1 infection
Hogue, I. B., Bajaria, S. H., Fallert, B. A., Qin, S., Reinhart, T. A., & Kirschner, D. E. (2008) · Journal of General Virology · doi:10.1099/vir.0.83600-0 · Cited by 38
MHC Class II–Transduced Tumor Cells Originating in the Immune-Privileged Eye Prime and Boost CD4+ T Lymphocytes that Cross-react with Primary and Metastatic Uveal Melanoma Cells
Bosch, J. J., Thompson, J. A., Srivastava, M. K., Iheagwara, U. K., Murray, T. G., Lotem, M., Ksander, B. R., & Ostrand‐Rosenberg, S. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3770 · Cited by 38
Invariant NKT Cells Exacerbate Type 1 Diabetes Induced by CD8 T Cells
Griseri, T., Beaudoin, L., Novák, J., Mars, L. T., Lepault, F., Liblau, R., & Lehuen, A. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.4.2091 · Cited by 38
Neoantigen-specific CD4+ tumor-infiltrating lymphocytes are potent effectors identified within adoptive cell therapy products for metastatic melanoma patients
Hall, M. S., Teer, J. K., Yu, X., Branthoover, H., Snedal, S. A., Rodríguez-Valentín, M., Nagle, L., Scott, E. N., Schachner, B. I., Innamarato, P., et al. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2023-007288 · Cited by 39
A coordinated cellular network regulates tolerance to food
Rudnitsky, A., Oh, H., Margolin, M., Dassa, B., Shteinberg, I., Stoler‐Barak, L., Shulman, Z., & Kedmi, R. (2025) · Nature · doi:10.1038/s41586-025-09173-x · Cited by 37
Vaccine-Induced CD107a + CD4 + T Cells Are Resistant to Depletion following AIDS Virus Infection
Terahara, K., Ishii, H., Nomura, T., Takahashi, N., Takeda, A., Shiino, T., Tsunetsugu‐Yokota, Y., & Matano, T. (2014) · Journal of Virology · doi:10.1128/jvi.02032-14 · Cited by 37
Endogenous HLA class II epitopes that are immunogenic in vivo show distinct behavior toward HLA-DM and its natural inhibitor HLA-DO
Kremer, A. N., van der Meijden, E. D., Honders, M. W., Goeman, J. J., Wiertz, E. J. H. J., Falkenburg, J. H. F., & Griffioen, M. (2012) · Blood · doi:10.1182/blood-2011-12-399311 · Cited by 37
Heat Shock Protein 90-Mediated Peptide-Selective Presentation of Cytosolic Tumor Antigen for Direct Recognition of Tumors by CD4+ T Cells
Tsuji, T., Matsuzaki, J., Caballero, O. L., Jungbluth, A. A., Ritter, G., Odunsi, K. O., Old, L. J., & Gnjatic, S. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103269 · Cited by 38
Antigen targeting to dendritic cells combined with transient regulatory T cell inhibition results in long-term tumor regression
Unger, W. W. J., Mayer, C. T., Engels, S., Hesse, C., Perdicchio, M., Puttur, F. K., Streng‐Ouwehand, I., Litjens, M., Kalay, H., Berod, L., et al. (2014) · OncoImmunology · doi:10.4161/21624011.2014.970462 · Cited by 37
Staphylococcus aureus enterotoxins modulate IL-22-secreting cells in adults with atopic dermatitis
Orfali, R. L., Oliveira, L. M. D. S., de Lima, J. F., de Carvalho, G. C., Ramos, Y. Á. L., Pereira, N. Z., Pereira, N. V., Zaniboni, M. C., Sotto, M. N., Duarte, A. J. D. S., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-25125-0 · Cited by 37
Mathematical modeling of tumor growth: the MCF-7 breast cancer cell line
Wei, H. (2019) · Mathematical Biosciences & Engineering · doi:10.3934/mbe.2019325 · Cited by 37
Immunopeptidomics-Guided Warehouse Design for Peptide-Based Immunotherapy in Chronic Lymphocytic Leukemia
Nelde, A., Maringer, Y., Bilich, T., Salih, H. R., Roerden, M., Heitmann, J. S., Marcu, A., Bauer, J., Neidert, M. C., Denzlinger, C., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.705974 · Cited by 39
Chitosan hydrogel vaccine generates protective CD8 T cell memory against mouse melanoma
Highton, A. J., Kojarunchitt, T., Girardin, A., Hook, S. M., & Kemp, R. A. (2015) · Immunology and Cell Biology · doi:10.1038/icb.2015.14 · Cited by 37
Detection of E pstein– B arr virus‐specific memory CD 4+ T cells using a peptide‐based cultured enzyme‐linked immunospot assay
Calarota, S. A., Chiesa, A., Zelini, P., Comolli, G., Minoli, L., & Baldanti, F. (2013) · Immunology · doi:10.1111/imm.12106 · Cited by 37
Comparison of Human and Rhesus Macaque T-Cell Responses Elicited by Boosting with NYVAC Encoding Human Immunodeficiency Virus Type 1 Clade C Immunogens
Mooij, P., Balla-Jhagjhoorsingh, S. S., Beenhakker, N., Haaften, P. E. B.-V., Baak, I., Nieuwenhuis, I. G., Heidari, S., Wolf, H. J., Frachette, M.-J., Bieler, K., et al. (2009) · Journal of Virology · doi:10.1128/jvi.02345-08 · Cited by 37
Liposome-encapsulated HIV-1 Gag p24 containing lipid A induces effector CD4+ T-cells, memory CD8+ T-cells, and pro-inflammatory cytokines
Steers, N. J., Peachman, K. K., McClain, S., Alving, C. R., & Rao, M. (2009) · Vaccine · doi:10.1016/j.vaccine.2009.08.105 · Cited by 37
Eradication of HIV and Cure of AIDS, Now and How?
Zhang, J., & Crumpacker, C. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00337 · Cited by 36
Biomarkers of immune checkpoint inhibitor response and toxicity: Challenges and opportunities
Goodman, R. S., Jung, S., Balko, J. M., & Johnson, D. B. (2023) · Immunological Reviews · doi:10.1111/imr.13249 · Cited by 38
Involvement of IL‐10 in exhaustion of myeloid dendritic cells and rescue by CD40 stimulation
Kajino, K., Nakamura, I., Bamba, H., Sawai, T., & Ogasawara, K. (2006) · Immunology · doi:10.1111/j.1365-2567.2006.02474.x · Cited by 36
CD4+ T Cells Play a Critical Role in the Generation of Primary and Memory Antitumor Immune Responses Elicited by SA-4-1BBL and TAA-Based Vaccines in Mouse Tumor Models
Sharma, R. K., Yolcu, E. S., Srivastava, A. K., & Shirwan, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073145 · Cited by 40
Conventional CD4+ T cells present bacterial antigens to induce cytotoxic and memory CD8+ T cell responses
Cruz‐Adalia, A., Ramírez‐Santiago, G., Osuna‐Pérez, J., Torres‐Torresano, M., Zorita, V., Riaño, A. M., Boccasavia, V. L., Borroto, A., del Hoyo, G. M., González, J. M., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01661-7 · Cited by 36
Harnessing the Complete Repertoire of Conventional Dendritic Cell Functions for Cancer Immunotherapy
Amon, L., Hatscher, L., Heger, L., Dudziak, D., & Lehmann, C. H. K. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12070663 · Cited by 37
Construction and evaluation of DNA vaccine encoding Hantavirus glycoprotein N-terminal fused with lysosome-associated membrane protein
Jiang, D., Sun, Y., Cheng, L., Zhang, G.-F., Dong, C., Jin, B., Song, C., Ma, Y., Zhang, F., & Yang, K. (2015) · Vaccine · doi:10.1016/j.vaccine.2015.05.007 · Cited by 36
Molecular pathways regulating CD4+ T cell differentiation, anergy and memory with implications for vaccines
Ahlers, J. D., & Belyakov, I. M. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.07.007 · Cited by 37
KBMA Listeria monocytogenes is an effective vector for DC-mediated induction of antitumor immunity
Škoberne, M., Yewdall, A. W., Bahjat, K. S., Godefroy, E., Lauer, P., Lemmens, E. E., Liu, W., Luckett, W. S., Leong, M. L. L., Dubensky, T. W., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci31350 · Cited by 36
Self-citation
CD4+ T Cells Are Able to Promote Tumor Growth through Inhibition of Tumor-Specific CD8+ T-Cell Responses in Tumor-Bearing Hosts
den Boer, A. T., van Mierlo, G. J. D., Fransen, M. F., Melief, C. J. M., Offringa, R., & Toes, R. E. M. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3344 · Cited by 36
Large-Scale Depletion of CD25+ Regulatory T Cells from Patient Leukapheresis Samples
Powell, D. J., Parker, L. L., & Rosenberg, S. A. (2005) · Journal of Immunotherapy · doi:10.1097/01.cji.0000170363.22585.5a · Cited by 36
Reconstitution of EBV Latent but Not Lytic Antigen-Specific CD4+ and CD8+ T Cells after HIV Treatment with Highly Active Antiretroviral Therapy
Piriou, E., Jansen, C. A., van Dort, K. A., Cuyper, I. M. D., Nanlohy, N. M., Lange, J. M. A., van Oers, M. H. J., Miedema, F. F., & van Baarle, D. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.3.2010 · Cited by 36
Functional re-expression of CCR7 on CMV-specific CD8+ T cells upon antigenic stimulation
van Leeuwen, E. M. M., van Buul, J. D., Remmerswaal, E. B. M., Hordijk, P. L., ten Berge, I. J. M., & van Lier, R. A. W. (2005) · International Immunology · doi:10.1093/intimm/dxh251 · Cited by 36
Electroporation Enables Plasmid Vaccines to Elicit CD8+ T Cell Responses in the Absence of CD4+ T Cells
Dayball, K., Millar, J., Miller, M., Wan, Y. H., & Bramson, J. L. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.7.3379 · Cited by 36
DNA vaccination: the answer to stable, protective T-cell memory?
Kirman, J. R., & Seder, R. A. (2003) · Current Opinion in Immunology · doi:10.1016/s0952-7915(03)00068-2 · Cited by 36
CD40 on APCs Is Needed for Optimal Programming, Maintenance, and Recall of CD8+ T Cell Memory Even in the Absence of CD4+ T Cell Help
Hernandez, M. G. H., Shen, L., & Rock, K. L. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.7.4382 · Cited by 35
CD4+ T cells stimulate memory CD8+ T cell expansion via acquired pMHC I complexes and costimulatory molecules, and IL-2 secretion
Shi, M., Hao, S., Chan, T., & Xiang, J. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0506321 · Cited by 36
Regulation of CTL Infiltration Within the Tumor Microenvironment
Church, S., & Galon, J. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-67577-0_3 · Cited by 36
Self-Adjuvanting Cancer Vaccines from Conjugation-Ready Lipid A Analogues and Synthetic Long Peptides
Reintjens, N. R. M., Tondini, E., de Jong, A. R., Meeuwenoord, N. J., Chiodo, F., Peterse, E., Overkleeft, H. S., Filippov, D. V., van der Marel, G. A., OSSENDORP, F. A., et al. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.0c00851 · Cited by 35
Potential approaches for more successful dendritic cell-based immunotherapy
Chiang, C. L.-L., Balint, K., Coukos, G., & Kandalaft, L. E. (2015) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2015.1000298 · Cited by 35
Immune-modulating Effects of the Newest Cetuximab-based Chemoimmunotherapy Regimen in Advanced Colorectal Cancer Patients
Botta, C., Bestoso, E., Apollinari, S., Cusi, M. G., Pastina, P., Abbruzzese, A., Sperlongano, P., Misso, G., Caraglia, M., Tassone, P., et al. (2012) · Journal of Immunotherapy · doi:10.1097/cji.0b013e31825943aa · Cited by 35
Immunization with SARS-CoV S DNA vaccine generates memory CD4+ and CD8+ T cell immune responses
Huang, J., Ma, R., & Wu, C. Y. (2006) · Vaccine · doi:10.1016/j.vaccine.2006.03.058 · Cited by 35
The absence of invariant chain in MHC II cancer vaccines enhances the activation of tumor-reactive type 1 CD4+ T lymphocytes
Thompson, J. A., Srivastava, M. K., Bosch, J. J., Clements, V. K., Ksander, B. R., & Ostrand‐Rosenberg, S. (2007) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-007-0381-5 · Cited by 35
Profound tumor-specific Th2 bias in patients with malignant glioma
Shimato, S., Maier, L. M., Maier, R., Bruce, J. N., Anderson, R. C. E., & Anderson, D. E. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-561 · Cited by 35
Recent Advances in Design of Immunogenic and Effective Naked DNA Vaccines Against Cancer
Fioretti, D. P., Iurescia, S., & Rinaldi, M. (2013) · Recent Patents on Anti-Cancer Drug Discovery · doi:10.2174/1574891x113089990037 · Cited by 37
Sirtuin 1 in Host Defense during Infection
Kim, J. K., Silwal, P., & Jo, E. (2022) · Cells · doi:10.3390/cells11182921 · Cited by 35
CD71+ erythroid cells suppress T-cell effector functions and predict immunotherapy outcomes in patients with virus-associated solid tumors
Bozorgmehr, N., Okoye, I., Mashhouri, S., Lu, J., Koleva, P. T., Walker, J. W. T., & Elahi, S. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-006595 · Cited by 34
Destabilisation of T cell-dependent humoral immunity in sepsis
Davies, K., & McLaren, J. E. (2024) · Clinical Science · doi:10.1042/cs20230517 · Cited by 34
CD49b‐dependent establishment of T helper cell memory
Hanazawa, A., Hayashizaki, K., Shinoda, K., Yagita∥, H., Okumura, K., Löhning, M., Hara, T., Tani‐ichi, S., Ikuta, K., Eckes, B., et al. (2013) · Immunology and Cell Biology · doi:10.1038/icb.2013.36 · Cited by 34
Combination of cell penetrating peptides and heterologous DNA prime/protein boost strategy enhances immune responses against HIV-1 Nef antigen in BALB/c mouse model
Kadkhodayan, S., Jafarzade, B. S., Sadat, S. M., Motevalli, F., Agi, E., & Bolhassani, A. (2017) · Immunology Letters · doi:10.1016/j.imlet.2017.06.003 · Cited by 34
The Expansion and Maintenance of Antigen‐Selected CD8+ T Cell Clones
Fearon, D. T. (2007) · Advances in immunology · doi:10.1016/s0065-2776(07)96003-4 · Cited by 35
Immunization with Single-Cycle SIV Significantly Reduces Viral Loads After an Intravenous Challenge with SIVmac239
Jia, B., Ng, S. K., DeGottardi, M. Q., Piatak, M., Yuste, E., Carville, A., Mansfield, K. G., Li, W., Richardson, B. A., Lifson, J. D., et al. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000272 · Cited by 34
Therapy of Established Tumors in a Novel Murine Model Transgenic for Human Carcinoembryonic Antigen and HLA-A2 with a Combination of Anti-idiotype Vaccine and CTL Peptides of Carcinoembryonic Antigen
Saha, A., Chatterjee, S. K., Foon, K. A., Celis, E., & Bhattacharya‐Chatterjee, M. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3045 · Cited by 34
DNA immunization in combination with effective antiretroviral drug therapy controls viral rebound and prevents simian AIDS after treatment is discontinued
FULLER, D. H., Rajakumar, P. A., Wu, M. S., McMahon, C. W., Shipley, T., Fuller, J. T., Bazmi, A., Trichel, A. M., Allen, T. M., Mothé, B. R., et al. (2006) · Virology · doi:10.1016/j.virol.2005.12.008 · Cited by 34
Lymphocytic Choriomeningitis Virus Infection Yields Overlapping CD4 + and CD8 + T-Cell Responses
Dow, C., Oseroff, C., Peters, B., Nance-Sotelo, C., Sidney, J., Buchmeier, M. J., Sette, A., & Mothé, B. R. (2008) · Journal of Virology · doi:10.1128/jvi.00435-08 · Cited by 34
CD4+ T cell help improves CD8+ T cell memory by retained CD27 expression
Matter, M. S., Claus, C., & Ochsenbein, A. F. (2008) · European Journal of Immunology · doi:10.1002/eji.200737824 · Cited by 34
Direct in vivo evidence of CD4+ T cell requirement for CTL response and memory via pMHC-I targeting and CD40L signaling
Ahmed, K. A., Wang, L., Munegowda, M. A., Mulligan, S. J., Gordon, J., Griebel, P. J., & Xiang, J. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.1211631 · Cited by 35

Authors: Janssen, E. M., Lemmens, E. E., Wolfe, T., Christen, U., von Herrath, M. G., & Schoenberger, S. P.
Affiliations: La Jolla Institute for Immunology (US)
Corresponding author: Schoenberger, Stephen P.
ORCID: Janssen, Edith M.
Lemmens, Edward E.
Christen, Urs
Schoenberger, Stephen P.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2003-02
Volume: 421
Issue: 6925
Pages: 852-856
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature01441
OpenAlex: W1493822493
Cited by: 1,635
References: 28
Citations by year: 2026: 19 · 2025: 24 · 2024: 37 · 2023: 46 · 2022: 37 · 2021: 42 · 2020: 58 · 2019: 42 · 2018: 52 · 2017: 36 · 2016: 41 · 2015: 61 · 2014: 63 · 2013: 63 · 2012: 71
FWCI: 46.09
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institutes of Health
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 cells, cytotoxic T lymphocytes, T helper cells, secondary immune response, T cell memory, T cell help, cross-priming, antigen-presenting cells, T cell differentiation
MeSH terms: Animals, Antigens, Cell Line, Cytotoxicity, Immunologic, Flow Cytometry, T-Lymphocytes, Helper-Inducer, Immunologic Memory, Lymphocyte Activation, Lymphocytic choriomeningitis virus, T-Lymphocytes, Cytotoxic, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks