Antibody-targeted vaccination to lung dendritic cells generates tissue-resident memory CD8 T cells that are highly protective against influenza virus infection
Open accessAbstract
Influenza virus gains entry into the body by inhalation and initiates its replication cycle within the lung. The early stage of infection, while the virus is confined to the lung mucosa, provides the ideal window of opportunity for an effective immune response to control the infection. Tissue-resident memory (Trm) CD8 T cells, located in a variety of tissues including the lung, are ideally situated to act during this window and stall the infection. The factors involved in the differentiation of lung Trm cells remain poorly defined. We demonstrate that recognition of antigen presented locally by dendritic cells (DCs) and transforming growth factor-β (TGFβ) signaling are both required. We exploited this knowledge to develop an antibody-targeted vaccination approach to generate lung Trm cells. Delivering antigen exclusively to respiratory DCs results in the development of lung CD8 Trm cells that are highly protective against lethal influenza challenge. Our results describe an effective vaccination strategy that protects against influenza virus infection.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Insufficient local TGF-β signaling may result in sustained high Eomes expression and an abundance of CD103−CD69+CD8+ Trm cells in the liver.
“As downregulation of Eomes is required for CD103+CD8+ Trm development via TGF-β signaling32, insufficient local TGF-β signaling may result in sustained high Eomes expression and an abundance of CD103−CD69+CD8+ Trm cells in the liver, consistent with previous reports28,33.”
From CD8+ tissue-resident memory T cells promote liver fibrosis resolution by inducing apoptosis of hepatic stellate cells (2021) · cites this paper as [32]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The developmental pathway for CD103+CD8+ tissue-resident memory T cells of skin
Mackay, L. K., Rahimpour, A., Ma, J. Z., Collins, N., Stock, A. T., Hafon, M.-L., Vega-Ramos, J., Lauzurica, P., Mueller, S. N., Stefanovic, T., et al. (2013) · Nature Immunology · doi:10.1038/ni.2744 · Cited by 1,331 · see citing works
Gebhardt, T., Wakim, L. M., Eidsmo, L., Reading, P. C., Heath, W. R., & Carbone, F. R. (2009) · Nature Immunology · doi:10.1038/ni.1718 · Cited by 1,157 · see citing works
Self-citationSensing and alarm function of resident memory CD8+ T cells
Schenkel, J., Fraser, K. A., Vezys, V., & Masopust, D. (2013) · Nature Immunology · doi:10.1038/ni.2568 · Cited by 648 · see citing works
A vaccine strategy that protects against genital herpes by establishing local memory T cells
Shin, H., & Iwasaki, A. (2012) · Nature · doi:10.1038/nature11522 · Cited by 646 · see citing works
Casey, K. A., Fraser, K. A., Schenkel, J. M., Moran, A. E., Abt, M. C., Beura, L. K., Lucas, P. J., Artis, D., Wherry, E. J., Hogquist, K. A., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200402 · Cited by 642 · see citing works
Mackay, L. K., Stock, A. T., Ma, J., Jones, C. M., Kent, S., Mueller, S. N., Heath, W., Carbone, F., & Gebhardt, T. (2012) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1202288109 · Cited by 638 · see citing works
Wakim, L. M., Davis, A. S. W., & Bevan, M. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010201107 · Cited by 577 · see citing works
Self-citationResponse of naïve and memory CD8+ T cells to antigen stimulation in vivo
Veiga‐Fernandes, H., Walter, U., Bourgeois, C., McLean, A. R., & Rocha, B. (2000) · Nature Immunology · doi:10.1038/76907 · Cited by 547 · see citing works
Wu, T., Hu, Y., Lee, Y.-T., Bouchard, K. R., Benechet, A. P., Khanna, K., & Cauley, L. S. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.0313180 · Cited by 537 · see citing works
Yewdell, J. W., Bennink, J. R., Smith, G. L., & Moss, B. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.6.1785 · Cited by 521 · see citing works
Zhang, N., & Bevan, M. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.019 · Cited by 403 · see citing works
Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity.
Liang, S., Mozdzanowska, K., Palladino, G., & Gerhard, W. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.152.4.1653 · Cited by 400 · see citing works
Lung niches for the generation and maintenance of tissue-resident memory T cells
Turner, D., Bickham, K. L., Thome, J. J. C., Kim, C. Y., D’Ovidio, F., Wherry, E. J., & Färber, D. L. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.67 · Cited by 399 · see citing works
The Molecular Signature of Tissue Resident Memory CD8 T Cells Isolated from the Brain
Wakim, L. M., Davis, A. S. W., Liu, R., Hu, Y., Villadangos, J. A., Smyth, G. K., & Bevan, M. J. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1201305 · Cited by 365 · see citing works
Self-citationIntravascular staining redefines lung CD8 T cell responses
Anderson, K., Sung, H., Skon, C. N., Lefrançois, L., Deisinger, A., Vezys, V., & Masopust, D. (2012) · Journal of Immunology · doi:10.4049/jimmunol.1201682 · Cited by 309 · see citing works
Purwar, R., Campbell, J. J., Murphy, G. F., Richards, W. G., Clark, R. A., & Kupper, T. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016245 · Cited by 286 · see citing works
Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses
Boscardin, S. B., Hafalla, J. C. R., Masilamani, R. F., Kamphorst, A. O., Zebroski, H. A., Rai, U., Morrot, A., Zavala, F. P., Steinman, R. M., Nussenzweig, R. S., et al. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20051639 · Cited by 269 · see citing works
CCR5 plays a key role in the early memory CD8+ T cell response to respiratory virus infections
Kohlmeier, J., Miller, S. C., Smith, J., Lu, B., Gerard, C., Cookenham, T., Roberts, A. D., & Woodland, D. (2008) · Immunity · doi:10.1016/j.immuni.2008.05.011 · Cited by 248 · see citing works
Self-citationLahoud, M. H., Ahmet, F., Kitsoulis, S., Wan, S. S., Vremec, D., Lee, C., Phipson, B., Shi, W., Smyth, G. K., Lew, A. M., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101176 · Cited by 227 · see citing works
Self-citationWakim, L. M., Gupta, N., Mintern, J. D., & Villadangos, J. A. (2013) · Nature Immunology · doi:10.1038/ni.2525 · Cited by 214 · see citing works
Self-citationLee, Y., Suarez-Ramirez, J. E., Wu, T., Redman, J. M., Bouchard, K. R., Hadley, G. A., & Cauley, L. S. (2011) · Journal of Virology · doi:10.1128/jvi.02493-10 · Cited by 187 · see citing works
Piet, B., de Bree, G. J., Smids-Dierdorp, B. S., van der Loos, C. M., Remmerswaal, E. B. M., von der Thüsen, J. H., van Haarst, J. M. W., Eerenberg, J. P., ten Brinke, A., van der Bij, W., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44675 · Cited by 183 · see citing works
Yu, C. I., Becker, C., Wang, Y., Marches, F., Helft, J., Leboeuf, M., Anguiano, E., Pourpe, S., Göller, K., Pascual, V., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.03.004 · Cited by 176 · see citing works
Immunologic recognition of influenza virus-infected cells
Braciale, T. J. (1977) · Cellular Immunology · doi:10.1016/0008-8749(77)90170-8 · Cited by 158 · see citing works
Braciale, T. J. (1977) · The Journal of Experimental Medicine · doi:10.1084/jem.146.3.673 · Cited by 114 · see citing works
Kees, U. R., & Krammer, P. H. (1984) · The Journal of Experimental Medicine · doi:10.1084/jem.159.2.365 · Cited by 112 · see citing works
Lahoud, M. H., Proietto, A. I., Ahmet, F., Kitsoulis, S., Eidsmo, L., Wu, L., Sathe, P., Pietersz, S., Chang, H.-W., Walker, I. D., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900464 · Cited by 106 · see citing works
Self-citationImproving vaccines by targeting antigens to dendritic cells
Shortman, K., Lahoud, M. H., & Caminschi, I. (2009) · Experimental & Molecular Medicine · doi:10.3858/emm.2009.41.2.008 · Cited by 104 · see citing works
Self-citationLocal immunity by tissue-resident CD8+ memory T cells
Gebhardt, T., & Mackay, L. K. (2012) · Front. Immun. · doi:10.3389/fimmu.2012.00340 · Cited by 103 · see citing works
Prospects for an influenza vaccine that induces cross‐protective cytotoxic T lymphocytes
Brown, L. E., & Kelso, A. (2009) · Immunology and Cell Biology · doi:10.1038/icb.2009.16 · Cited by 103 · see citing works
Memory T cells as an occupying force
Bevan, M. (2011) · European Journal of Immunology · doi:10.1002/eji.201041377 · Cited by 73 · see citing works
Maamary, J., Array, F., Gao, Q., García-Sastre, A., Steinman, R., Palese, P., & Nchinda, G. (2010) · Journal of Virology · doi:10.1128/jvi.02036-10 · Cited by 45 · see citing works
Bourges, D., Zhan, Y., Brady, J. L., Braley, H., Caminschi, I., Prato, S., Villadangos, J. A., & Lew, A. M. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.9.5678 · Cited by 13 · see citing works
Self-citationHu, Y., & Cauley, L. S. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00227 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Location, location, location: Tissue resident memory T cells in mice and humans
Szabo, P. A., Miron, M., & Farber, D. L. (2019) · Science Immunology · doi:10.1126/sciimmunol.aas9673 · Cited by 651 · see citing works
The multifaceted role of CD4+ T cells in CD8+ T cell memory
Laidlaw, B. J., Craft, J. E., & Kaech, S. M. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2015.10 · Cited by 657 · see citing works
Tissue-Resident T Cells and Other Resident Leukocytes
Masopust, D., & Soerens, A. G. (2019) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053214 · Cited by 608 · see citing works
Zens, K. D., Chen, J. K., & Färber, D. L. (2016) · JCI Insight · doi:10.1172/jci.insight.85832 · Cited by 415 · see citing works
Resident memory T cells, critical components in tumor immunology
Mami‐Chouaib, F., Blanc, C., Corgnac, S., Hans, S., Malenica, I., Granier, C., Tihy, I., & Tartour, É. (2018) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-018-0399-6 · Cited by 328 · see citing works
Pizzolla, A., Nguyen, T. H. O., Smith, J. M., Brooks, A., Kedzierska, K., Heath, W., Reading, P., & Wakim, L. (2017) · Science immunology · doi:10.1126/sciimmunol.aam6970 · Cited by 284 · see citing works
Self-citationThe precursors of CD8+ tissue resident memory T cells: from lymphoid organs to infected tissues
Kok, L., Masopust, D., & Schumacher, T. N. (2022) · Nature Reviews Immunology · doi:10.1038/s41577-021-00590-3 · Cited by 230 · see citing works
Koda, Y., Teratani, T., Chu, P.-S., Hagihara, Y., Mikami, Y., Harada, Y., Tsujikawa, H., Miyamoto, K., Suzuki, T., Taniki, N., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24734-0 · Cited by 219 · see citing works
Tissue‐resident memory T cells in tissue homeostasis, persistent infection, and cancer surveillance
Gebhardt, T., Palendira, U., Tscharke, D. C., & Bedoui, S. (2018) · Immunological Reviews · doi:10.1111/imr.12650 · Cited by 199 · see citing works
Tissue resident memory T cells in the respiratory tract
Zheng, M. Z. M., & Wakim, L. (2021) · Mucosal Immunology · doi:10.1038/s41385-021-00461-z · Cited by 177 · see citing works
Self-citationRoquilly, A., McWilliam, H. E. G., Jacqueline, C., Tian, Z., Cinotti, R., Rimbert, M., Wakim, L. M., Caminschi, I., Lahoud, M. H., Belz, G. T., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.06.021 · Cited by 186 · see citing works
Self-citationPizzolla, A., Nguyen, T. H. O., Sant, S. A., Jaffar, J., Loudovaris, T., Mannering, S. I., Thomas, P. G., Westall, G. P., Kedzierska, K., & Wakim, L. M. (2018) · Journal of Clinical Investigation · doi:10.1172/jci96957 · Cited by 181 · see citing works
Self-citationInfluenza virus-specific CD4+ and CD8+ T cell-mediated immunity induced by infection and vaccination
Jansen, J. M., Gerlach, T. H., Elbahesh, H., Rimmelzwaan, G. F., & Saletti, G. (2019) · Journal of Clinical Virology · doi:10.1016/j.jcv.2019.08.009 · Cited by 168 · see citing works
McMaster, S. R., Wein, A. N., Dunbar, P. R., Hayward, S. L., Cartwright, E. K., Denning, T. L., & Kohlmeier, J. E. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0003-x · Cited by 161 · see citing works
Immune responses during COVID-19 infection
Melenotte, C., Silvin, A., Goubet, A., Lahmar, I., Dubuisson, A., Zumla, A. I., Raoult, D., Merad-Boudia, M., Gachot, B., Henon, C., et al. (2020) · OncoImmunology · doi:10.1080/2162402x.2020.1807836 · Cited by 162 · see citing works
Niches for the Long-Term Maintenance of Tissue-Resident Memory T Cells
Takamura, S. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01214 · Cited by 123 · see citing works
Knight, F. C., Gilchuk, P., Kumar, A., Becker, K. W., Sevimli, S., Jacobson, M. E., Suryadevara, N., Wang-Bishop, L., Boyd, K., Crowe, J., et al. (2019) · ACS Nano · doi:10.1021/acsnano.9b00326 · Cited by 113 · see citing works
Verbeke, R., Lentacker, I., Wayteck, L., Breckpot, K., Van Bockstal, M., Descamps, B., Vanhove, C., De Smedt, S. C., & Dewitte, H. (2017) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.09.041 · Cited by 132 · see citing works
Hirai, T., Yang, Y., Zenke, Y., Li, H., Chaudhri, V. K., Diaz, J. S. D. L. C., Zhou, P. Y., Nguyen, B. A., Bartholin, L., Workman, C. J., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.10.022 · Cited by 120 · see citing works
Harnessing the Power of T Cells: The Promising Hope for a Universal Influenza Vaccine
Clemens, E. B., van de Sandt, C. E., Wong, S., Wakim, L. M., & Valkenburg, S. A. (2018) · Vaccines · doi:10.3390/vaccines6020018 · Cited by 118 · see citing works
Self-citationAirway T cells protect against RSV infection in the absence of antibody
Kinnear, E., Lambert, L., McDonald, J. U., Cheeseman, H. M., Caproni, L. J., & Tregoning, J. S. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.46 · Cited by 108 · see citing works
Sridhar, S. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00195 · Cited by 101 · see citing works
Influenza Pathogenesis: The Effect of Host Factors on Severity of Disease
Gounder, A. P., & Boon, A. C. M. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801010 · Cited by 100 · see citing works
IL-15 supports the generation of protective lung-resident memory CD4 T cells
Strutt, T. M., Dhume, K., Finn, C. M., Hwang, J. H., Castonguay, C. H., Swain, S. L., & McKinstry, K. K. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.101 · Cited by 97 · see citing works
Lapuente, D., Bonsmann, M. S. G., Maaske, A., Stab, V., Heinecke, V., Watzstedt, K., Heß, R., Westendorf, A. M., Bayer, W., Ehrhardt, C., et al. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0017-4 · Cited by 86 · see citing works
Hirai, T., Zenke, Y., Yang, Y., Bartholin, L., Beura, L. K., Masopust, D., & Kaplan, D. H. (2019) · Immunity · doi:10.1016/j.immuni.2019.03.002 · Cited by 86 · see citing works
Bone Marrow T Cells and the Integrated Functions of Recirculating and Tissue-Resident Memory T Cells
Rosa, F. D., & Gebhardt, T. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00051 · Cited by 84 · see citing works
Smith, S. E., Busse, D. C., Binter, Š., Weston, S. M., Soria, C. L. D., Laksono, B. M., Clare, S., van Nieuwkoop, S., van den Hoogen, B. G., Clement, M., et al. (2018) · Journal of Virology · doi:10.1128/jvi.02003-18 · Cited by 83 · see citing works
Ge, C., Monk, I., Pizzolla, A., Wang, N., Bedford, J. G., Stinear, T., Westall, G., & Wakim, L. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.11.103 · Cited by 69 · see citing works
Self-citationPrime and target immunization protects against liver-stage malaria in mice
Gola, A., Silman, D., Walters, A., Sridhar, S., Uderhardt, S., Salman, A. M., Halbroth, B. R., Bellamy, D., Bowyer, G. S., Powlson, J., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aap9128 · Cited by 68 · see citing works
Carbone, F. R. (2022) · Nature reviews. Immunology · doi:10.1038/s41577-022-00815-z · Cited by 70 · see citing works
Muruganandah, V., Sathkumara, H. D., Navarro, S., & Kupz, A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01574 · Cited by 71 · see citing works
Targeting Resident Memory T Cells for Cancer Immunotherapy
Blanc, C., Hans, S., Tran, T., Granier, C., Saldmann, A., Anson, M., Oudard, S. M., & Tartour, É. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01722 · Cited by 68 · see citing works
Myers, M. A., Smith, A. P., Lane, L. C., Moquin, D. J., Aogo, R., Woolard, S., Thomas, P. G., Vogel, P., & Smith, A. M. (2021) · eLife · doi:10.7554/elife.68864 · Cited by 70 · see citing works
Tumor-resident memory T cells as a biomarker of the response to cancer immunotherapy
Damei, I., Trickovic, T., Mami‐Chouaib, F., & Corgnac, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1205984 · Cited by 62 · see citing works
Chrisikos, T. T., Zhou, Y., Slone, N., Babcock, R. L., Watowich, S. S., & Li, H. S. (2018) · Molecular Immunology · doi:10.1016/j.molimm.2018.01.014 · Cited by 58 · see citing works
TGF-β: Many Paths to CD103+ CD8 T Cell Residency
Qiu, Z.-J., Chu, T. H., & Sheridan, B. (2021) · Cells · doi:10.3390/cells10050989 · Cited by 43 · see citing works
Opportunities and challenges for T cell-based influenza vaccines
Mosmann, T. R., McMichael, A. J., LeVert, A., McCauley, J. W., & Almond, J. W. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-01030-8 · Cited by 56 · see citing works
Hasan, F., Chiu, Y., Shaw, R., Wang, J., & Yee, C. (2021) · JCI Insight · doi:10.1172/jci.insight.138970 · Cited by 56 · see citing works
Tissue‐resident memory T cells and lung immunopathology
Cheon, I. S., Son, Y. M., & Sun, J. (2023) · Immunological Reviews · doi:10.1111/imr.13201 · Cited by 57 · see citing works
TGF-β Controls the Formation of Kidney-Resident T Cells via Promoting Effector T Cell Extravasation
Ma, C., Mishra, S., Demel, E. L., Liu, Y., & Zhang, N. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1601500 · Cited by 55 · see citing works
Raulf, M., Johannssen, T., Matthiesen, S., Neumann, K., Hachenberg, S., Mayer-Lambertz, S., Steinbeis, F., Hegermann, J., Seeberger, P. H., Baumgärtner, W., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.015 · Cited by 54 · see citing works
Ayasoufi, K., Wolf, D. M., Namen, S. L., Jin, F., Tritz, Z. P., Pfaller, C. K., Zheng, J., Goddery, E. N., Fain, C. E., Gulbicki, L. R., et al. (2022) · SSRN Electronic Journal · doi:10.1016/j.bbi.2023.05.009 · Cited by 54 · see citing works
Memory T Cell Dynamics in the Lung during Influenza Virus Infection
Pizzolla, A., & Wakim, L. M. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1800979 · Cited by 53 · see citing works
Self-citationDevelopment of Cross-Protective Influenza A Vaccines Based on Cellular Responses
Soema, P. C., van Riet, E., Kersten, G. F. A., & Amorij, J. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00237 · Cited by 51 · see citing works
Dunbar, P. R., Cartwright, E. K., Wein, A. N., Tsukamoto, T., Li, Z.-R. T., Kumar, N., Uddback, I. E. M., Hayward, S. L., Ueha, S., Takamura, S., et al. (2019) · Mucosal Immunology · doi:10.1038/s41385-019-0224-7 · Cited by 51 · see citing works
Targeting dendritic cells to advance cross-presentation and vaccination outcomes.
Macri, C., Jenika, D., Ouslinis, C., & Mintern, J. (2023) · Seminars in Immunology · doi:10.1016/j.smim.2023.101762 · Cited by 47 · see citing works
Clinical Advances in Viral-Vectored Influenza Vaccines
Sebastian, S., & Lambe, T. (2018) · Vaccines · doi:10.3390/vaccines6020029 · Cited by 43 · see citing works
New Insights into the Generation of CD4 Memory May Shape Future Vaccine Strategies for Influenza
Devarajan, P., Bautista, B., Vong, A. M., McKinstry, K. K., Strutt, T. M., & Swain, S. L. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00136 · Cited by 41 · see citing works
van Gisbergen, K. P. J. M., Zens, K. D., & Münz, C. (2021) · European Journal of Immunology · doi:10.1002/eji.202049062 · Cited by 39 · see citing works
Nguyen, T. H. O., McAuley, J., Kim, Y., Zheng, M. Z. M., Gherardin, N. A., Godfrey, D. I., Purcell, D. F. J., Sullivan, L. C., Westall, G. P., Reading, P. C., et al. (2021) · Clinical & Translational Immunology · doi:10.1002/cti2.1242 · Cited by 41 · see citing works
Self-citationPersistence in Temporary Lung Niches: A Survival Strategy of Lung-Resident Memory CD8 + T Cells
Takamura, S. (2017) · Viral Immunology · doi:10.1089/vim.2017.0016 · Cited by 40 · see citing works
Ainsua‐Enrich, E., HATİPOGLU, I. H., Kadel, S., Turner, S., Paul, J. A., Singh, S. P., Bagavant, H., & Kovats, S. (2019) · Mucosal Immunology · doi:10.1038/s41385-019-0173-1 · Cited by 40 · see citing works
Hendriks, A., Mnich, M. E., Clemente, B., Cruz, A. R., Tavarini, S., Bagnoli, F., & Soldaini, E. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.642711 · Cited by 40 · see citing works
McEntee, C. P., Gunaltay, S., & Travis, M. A. (2020) · Immunology · doi:10.1111/imm.13162 · Cited by 39 · see citing works
Tissue Distribution of Memory T and B Cells in Rhesus Monkeys following Influenza A Infection
Pichyangkul, S., Yongvanitchit, K., Limsalakpetch, A., Kum-Arb, U., Im‐Erbsin, R., Boonnak, K., Arunee, T., Jongkaewwattana, A., Wiboon-ut, S., Mongkolsirichaikul, D., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1501702 · Cited by 39 · see citing works
The Nontoxic Cholera B Subunit Is a Potent Adjuvant for Intradermal DC-Targeted Vaccination
Antonio-Herrera, L., Badillo, O., Contreras, O. M., Tepale-Segura, A., García-Lozano, A., Gutiérrez‐Xicoténcatl, L., Soldevila, G., Esquivel-Guadarrama, F. R., Idoyaga, J., & Bonifaz, L. C. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02212 · Cited by 39 · see citing works
Schmidt, A. P., & Lapuente, D. (2021) · Viruses · doi:10.3390/v13020199 · Cited by 39 · see citing works
Influenza and Memory T Cells: How to Awake the Force
Spitaels, J., Roose, K., & Saelens, X. (2016) · Vaccines · doi:10.3390/vaccines4040033 · Cited by 36 · see citing works
Takamura, S., & Kohlmeier, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00733 · Cited by 30 · see citing works
Matyushenko, V., Kotomina, T. S., Kudryavtsev, I. V., Mezhenskaya, D. А., Игоревна, П. П., Matushkina, A., Сивак, К. В., Muzhikyan, A., Георгиевна, Р. Л., & Николаевна, И.-С. И. (2020) · Antiviral Research · doi:10.1016/j.antiviral.2020.104864 · Cited by 36 · see citing works
CMV-Specific CD8 T Cell Differentiation and Localization: Implications for Adoptive Therapies
Smith, C. J., Quinn, M. A., & Snyder, C. M. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00352 · Cited by 34 · see citing works
Mechanisms of cellular and humoral immunity through the lens of VLP-based vaccines
McFall-Boegeman, H., & Huang, X. (2022) · Expert Review of Vaccines · doi:10.1080/14760584.2022.2029415 · Cited by 33 · see citing works
Past Life and Future Effects—How Heterologous Infections Alter Immunity to Influenza Viruses
Souquette, A. H., & Thomas, P. G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01071 · Cited by 33 · see citing works
Hodgins, B., Pillet, S., Landry, N., & Ward, B. J. (2019) · Immunity & Ageing · doi:10.1186/s12979-019-0167-6 · Cited by 32 · see citing works
Tissue-Specific Control of Tissue-Resident Memory T Cells
Liu, Y., Ma, C., & Zhang, N. (2018) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.2018025653 · Cited by 29 · see citing works
Tissue-Resident Macrophages Limit Pulmonary CD8 Resident Memory T Cell Establishment
Goplen, N. P., Huang, S., Zhu, B., Cheon, I. S., Son, Y. M., Wang, Z., Li, C., Dai, Q., Jiang, L., & Sun, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02332 · Cited by 31 · see citing works
Formation of Tissue-Resident CD8+ T-Cell Memory.Preprint
Dijkgraaf, F. E., Kok, L., & Schumacher, T. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a038117 · Cited by 28 · see citing works
Influenza-Specific Lung-Resident Memory CD8+T CellsPreprint
van de Wall, S., Badovinac, V. P., & Harty, J. T. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a037978 · Cited by 30 · see citing works
Caminschi, I., Lahoud, M. H., Pizzolla, A., & Wakim, L. M. (2019) · Mucosal Immunology · doi:10.1038/s41385-018-0124-2 · Cited by 29 · see citing works
Self-citationMartini, V., Paudyal, B., Chrun, T., McNee, A., Edmans, M. D., Maze, E. A., Clark, B., Núñez, A., Dolton, G. M., Sewell, A. K., et al. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2001086 · Cited by 29 · see citing works
Martini, V., Edmans, M. D., Gubbins, S., Jayaraman, S., Paudyal, B., Morgan, S. B., McNee, A., Morin, T., Rijal, P., Gerner, W., et al. (2022) · Mucosal Immunology · doi:10.1038/s41385-021-00478-4 · Cited by 24 · see citing works
Retamal-Díaz, A., Covián, C., Pacheco, G. A., Castiglione-Matamala, A. T., Bueno, S., González, P., & Kalergis, A. (2019) · Pathogens · doi:10.3390/pathogens8030147 · Cited by 29 · see citing works
Editorial: Tissue Resident Memory T Cells
Mami‐Chouaib, F., & Tartour, É. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01018 · Cited by 27 · see citing works
Braverman, J., Monk, I. R., Ge, C., Westall, G. P., Stinear, T. P., & Wakim, L. M. (2022) · Mucosal Immunology · doi:10.1038/s41385-022-00529-4 · Cited by 27 · see citing works
Self-citationTargeting Skin-Resident Memory T Cells via Vaccination to Combat Staphylococcus aureus Infections
Clegg, J., Soldaini, E., Bagnoli, F., & McLoughlin, R. M. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.11.005 · Cited by 26 · see citing works
Zheng, M. Z. M., Tan, T. K., Villalón‐Letelier, F., Lau, H., Deng, Y., Fritzlar, S., Valkenburg, S. A., Gu, H., Poon, L. L. M., Reading, P. C., et al. (2023) · Science Advances · doi:10.1126/sciadv.adg3469 · Cited by 25 · see citing works
Self-citationAxes of heterogeneity in human tissue‐resident memory T cells
Szabo, P. A. (2023) · Immunological Reviews · doi:10.1111/imr.13210 · Cited by 25 · see citing works
Longet, S., & Paul, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1216402 · Cited by 24 · see citing works
Engineering Vaccines for Tissue-Resident Memory T Cells
Knight, F. C., & Wilson, J. T. (2021) · Advances in Therapy · doi:10.1002/adtp.202000230 · Cited by 22 · see citing works
Influenza‐induced lung Trm: not all memories last forever
Budimir, N., & Harty, J. T. (2017) · Immunology and Cell Biology · doi:10.1038/icb.2017.32 · Cited by 21 · see citing works
Roy, S. B., Williams, C. M., Wijesundara, D. K., & Furuya, Y. (2020) · Vaccines · doi:10.3390/vaccines8040683 · Cited by 20 · see citing works
Tissue‐resident memory T (T RM ) cells: Front‐line workers of the immune system
Osman, M., Park, S. L., & Mackay, L. K. (2023) · European Journal of Immunology · doi:10.1002/eji.202250060 · Cited by 20 · see citing works
Mittra, S., Harding, S. M., & Kaech, S. M. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2300049 · Cited by 19 · see citing works
Lobby, J. L., Uddback, I. E. M., Scharer, C. D., Tian, M., Boss, J. M., Thomsen, A. R., Christensen, J. P., & Kohlmeier, J. E. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2200082 · Cited by 19 · see citing works
Zhang, M., Li, N., He, Y., Shi, T., & Jie, Z. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.943331 · Cited by 18 · see citing works
Decoding Tissue-Residency: Programming and Potential of Frontline Memory T CellsPreprint
Park, S. L., & Mackay, L. K. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a037960 · Cited by 18 · see citing works
Oltmanns, F., Antão, A. V., Irrgang, P., Viherlehto, V., Jörg, L., Schmidt, A. P., Wagner, J. T., Rückert, M., Flohr, A.-S., Geppert, C. I., et al. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2023-008652 · Cited by 17 · see citing works
Lambert, L., Kinnear, E., McDonald, J. U., Grødeland, G., Bogen, B., Stubsrud, E., Lindeberg, M. M., Fredriksen, A. B., & Tregoning, J. S. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00321 · Cited by 17 · see citing works
Extending the Breadth of Influenza Vaccines: Status and Prospects for a Universal Vaccine
Fox, A., Quinn, K. M., & Subbarao, K. (2018) · Drugs · doi:10.1007/s40265-018-0958-7 · Cited by 17 · see citing works
Homeostasis and Durability of T-Cell Memory—The Resting and the Restless T-Cell Memory
Radbruch, A., McGrath, M. A., Siracusa, F., Hoffmann, U., Sercan-Alp, Ö., Hutloff, A., Tokoyoda, K., Chang, H.-D., & Dong, J. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a038083 · Cited by 16 · see citing works
Tissue‐resident memory T cells in diseases and therapeutic strategies
Xie, D., Lu, G., Mai, G., Guo, Q., & Xu, G. (2025) · MedComm · doi:10.1002/mco2.70053 · Cited by 18 · see citing works
Wang, Z., He, Y., Wang, W., Tian, Y., Ge, C., Jia, F., Zhang, T., Zhang, G., Wang, M., Gong, J.-S., et al. (2023) · Journal of Nanobiotechnology · doi:10.1186/s12951-023-02229-y · Cited by 15 · see citing works
Metabolic Regulation of Tissue-Resident Memory CD8+ T cells
Vardam-Kaur, T., Sun, J., & da Silva, H. B. (2021) · Current opinion in pharmacology (Print) · doi:10.1016/j.coph.2021.02.004 · Cited by 11 · see citing works
Xu, L., Ye, L., & Huang, Q. (2025) · MedComm · doi:10.1002/mco2.70132 · Cited by 15 · see citing works
Wang, Z., Kedzierski, Ł., Nüssing, S., Chua, B. Y. L., Quiñones‐Parra, S. M., Huber, V. C., Jackson, D. C., Thomas, P. G., & Kedzierska, K. (2016) · Journal of General Virology · doi:10.1099/jgv.0.000651 · Cited by 14 · see citing works
Zhou, G., Hollenberg, M. D., Vliagoftis, H., & Kane, K. P. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1800915 · Cited by 14 · see citing works
“Gnothi Seauton”: Leveraging the Host Response to Improve Influenza Virus Vaccine Efficacy
Stacey, H. D., Barjesteh, N., Mapletoft, J., & Miller, M. S. (2018) · Vaccines · doi:10.3390/vaccines6020023 · Cited by 12 · see citing works
Legend of the Sentinels: Development of Lung Resident Memory T Cells and Their Roles in Diseases
Qian, Y., Zhu, Y., Li, Y., & Li, B. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.624411 · Cited by 13 · see citing works
Divergence of Tissue-Memory T Cells: Distribution and Function-Based Classification.Preprint
Takamura, S. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a037762 · Cited by 10 · see citing works
- Authors
- Wakim, L. M., Smith, J., Caminschi, I., Lahoud, M. H., & Villadangos, J. A.
- Affiliations
- The University of Melbourne (AU)
- Burnet Institute (AU)
- Corresponding author
- Wakim, L M
- Villadangos, J A
- Venue
- Mucosal Immunology
- Publisher
- Elsevier BV
- Published
- 2015-09
- Volume
- 8
- Issue
- 5
- Pages
- 1060-1071
- ISSN
- 1933-0219 (ISSN-L)
- OpenAlex
- W1994014992
- Cited by
- 167
- References
- 34
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 13 · 2023: 12 · 2022: 14 · 2021: 24 · 2020: 14 · 2019: 23 · 2018: 19 · 2017: 8 · 2016: 12 · 2015: 4
- FWCI
- 11.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Mucosal Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Melbourne
- Medical Research Council
- National Health and Medical Research Council
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- tissue-resident memory T cells, CD8+ T cells, lung dendritic cells, influenza, TGF-beta signaling, antigen presentation, respiratory mucosa, protective immunity
- MeSH terms
- Animals, Antibodies, Viral, Dendritic Cells, Influenza Vaccines, Lung, Mice, Transgenic, Orthomyxoviridae Infections, Influenza A virus, Vaccination, 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