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Liver-Resident Memory CD8+ T Cells Form a Front-Line Defense against Malaria Liver-Stage Infection
Open accessAbstract
In recent years, various intervention strategies have reduced malaria morbidity and mortality, but further improvements probably depend upon development of a broadly protective vaccine. To better understand immune requirement for protection, we examined liver-stage immunity after vaccination with irradiated sporozoites, an effective though logistically difficult vaccine. We identified a population of memory CD8+ T cells that expressed the gene signature of tissue-resident memory T (Trm) cells and remained permanently within the liver, where they patrolled the sinusoids. Exploring the requirements for liver Trm cell induction, we showed that by combining dendritic cell-targeted priming with liver inflammation and antigen recognition on hepatocytes, high frequencies of Trm cells could be induced and these cells were essential for protection against malaria sporozoite challenge. Our study highlights the immune potential of liver Trm cells and provides approaches for their selective transfer, expansion, or depletion, which may be harnessed to control liver infections or autoimmunity.
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“In the present study, we found similar evidence, which likely indicates that liver tissue-resident CD8 T cells play an important role not only in infectious diseases as previously reported [34, 35] but also in improving liver damage.”
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Valencia‐Hernandez, A. M., Zillinger, T., Ge, Z., Tan, P. S., Cozijnsen, A. J., McFadden, G. I., Lahoud, M. H., Caminschi, I., Barchet, W., Heath, W. R., et al. (2023) · Vaccine · doi:10.1016/j.vaccine.2022.12.047 · Cited by 11
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“This is inherently challenging to study in humans, as the human liver is not readily accessible for sampling and a very small fraction of its cells get infected [9, 12, 13].”
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“Accordingly, CD8 TRM have been found to be patrolling vascular compartments, such as liver sinusoids (51), as well as neuronal and muscle tissue (32, 52).”
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“In contrast to the conventional epithelial tissues, CD8+ Trm cells in the liver sinusoid entirely lack the expression of CD103, presumably reflecting the lack of tight junctions in the sinusoidal epithelium (Fernandez-Ruiz et al. 2016).”
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“Additionally, CXCR6, a receptor for C-X-C motif chemokine ligand 16 (CXCL16), is also one of the core transcriptional signatures of T RM and plays a crucial role in their maintenance, localization, and function [44–47].”
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6″-Modifed α-GalCer-peptide conjugate vaccine candidates protect against liver-stage malaria
Meijlink, M. A., Chua, Y. C., Chan, S. T. S., Anderson, R. J., Rosenberg, M. W., Cozijnsen, A. J., Mollard, V., McFadden, G. I., Draper, S. L., Holz, L. E., et al. (2022) · RSC Chemical Biology · doi:10.1039/d1cb00251a · Cited by 20
Self-citationCellular interactions in resident memory T cell establishment and function
Hasan, M. H., & Beura, L. K. (2021) · Current Opinion in Immunology · doi:10.1016/j.coi.2021.10.005 · Cited by 9
Moita, D., Nunes‐Cabaço, H., Mendes, A. M., & Prudêncio, M. (2021) · FEBS Journal · doi:10.1111/febs.16016 · Cited by 8
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GITR differentially affects lung effector T cell subpopulations during influenza virus infection
Chu, K.-L., Batista, N. V., Girard, M., Law, J. C., & Watts, T. H. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.4ab1219-254r · Cited by 7
de Menezes, M. N., Ge, Z.-Y., Cozijnsen, A., Gras, S., Bertolino, P., Caminschi, I., Lahoud, M., Yui, K., McFadden, G. I., Beattie, L., et al. (2024) · bioRxiv · doi:10.1371/journal.ppat.1012731 · Cited by 6
“Although both types of memory CD8 + T cells are elicited by RAS vaccination and can contribute to protection [24,25], tissue-resident memory T cells appear to be critical in C57BL/6 mice [25], which are highly susceptible to infection by P. berghei and require higher doses of RAS for sterilising…”
InfluentialSelf-citationA Plasmodium late liver stage arresting GAP provides superior protection in mice
Mishra, A., Paul, P., Srivastava, M., & Mishra, S. (2024) · npj Vaccines · doi:10.1038/s41541-024-00975-0 · Cited by 6
“Recent studies have highlighted the major role of CD8 + T RM cells in eliminating infected hepatocytes 31,33,40,71,73,74 .”
InfluentialFerrer, P., Berry, A., Bucşan, A. N., Prajapati, S., Krishnan, K., Barbeau, M. C., Rickert, D. M., Guerrero, S. M., Usui, M., Abebe, Y., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-49041-2 · Cited by 6
“In mice, CD8+ liver-resident memory T cells (Trm) are required for the protective immune response generated against radiation-attenuated sporozoite vaccines 37 .”
BackgroundLi, J., Panetta, F., O'Keeffe, M., Rojas, I. M. L., Radford, K., Zhang, J.-G., Fernandez-Ruiz, D., Davey, G. M., Gully, B., Tullett, K., et al. (2021) · Journal of Immunology · doi:10.4049/jimmunol.2001153 · Cited by 6
Self-citationHepatic Inflammation Confers Protective Immunity Against Liver Stages of Malaria Parasite
Grand, M., Waqasi, M., Demarta‐Gatsi, C., Yu, W., Péronet, R., Commère, P., Puig, A., Axelrod, J. H., Caldelari, R., Heussler, V. T., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.585502 · Cited by 8
Intravital imaging of skin infections
Zaid, A. (2019) · Cellular Immunology · doi:10.1016/j.cellimm.2019.04.001 · Cited by 6
Self-citationReeder, S. M., Reuschel, E. L., Bah, M. A., Yun, K., Tursi, N. J., Kim, K. Y., Chu, J. D., Zaidi, F. I., Yilmaz, I., Hart, R. J., et al. (2020) · Vaccines · doi:10.3390/vaccines8010021 · Cited by 6
“Doses of 250 sporozoites in 150 µL incomplete RPMI were prepared as previously described [22, 23, 26 ].”
BackgroundMethodResultInfluentialWei, C. Y., Zhu, Y., Lu, X., Goodier, K. D., Yu, D., Liu, X., Choy, J., Calderón, A. T., Su, Y., Ma, J., et al. (2026) · Nature Biomedical Engineering · doi:10.1038/s41551-026-01706-7 · Cited by 8
Self-citationKeeping it local: how CD8 TRMs regulate viral and cancer immunity
Rodrigues, L. C., Bonorino, C., Haubert, A. F., Lins, M. P., Pereira, G. P., Romão, P. R. T., & Rouse, B. T. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1618700 · Cited by 5
“…fi c CD8 + T cells Mouse polyoma virus infection (61), Toxoplasma gondii infection (67), Vaccinia virus model (65), Lung In fl uenza infection (63), Mouse polyomavirus infection in brain (62), Listeria monocytogenes strain carrying ovalbumin peptides (23), Review in lung TRMs (68), TRM in…”
Yu, C.-C., Draper, S. L., Le, S., de Menezes, M. N., Ganley, M., Ge, Z.-Y., Lee, A. R., Phabmixay, T., Hirschmann, D., Robinson, S., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115295 · Cited by 5
Self-citationAl‐Adra, D. P., Lan, R., Jennings, H., Weinstein, K. N., Liu, Y.-J., Verhoven, B. M., Zeng, W., Heise, G. W., Levitsky, M., Chlebeck, P. J., et al. (2024) · Transplant Immunology · doi:10.1016/j.trim.2024.102104 · Cited by 5
Beumer‐Chuwonpad, A., Behr, F. M., van Alphen, F. P. J., Kragten, N. A. M., Hoogendijk, A. J., van den Biggelaar, M., & van Gisbergen, K. P. J. M. (2024) · European Journal of Immunology · doi:10.1002/eji.202350873 · Cited by 6
CD8+ Trms against malaria liver-stage: prospects and challenges
Zhu, C., Jiao, S., & Xu, W. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1344941 · Cited by 8
A Unique Epigenomic Landscape Defines CD8 + Tissue-Resident Memory T CellsPreprint
Buquicchio, F. A., Fonseca, R., Belk, J. A., Evrard, M., Obers, A., Qi, Y., Dániel, B., Yost, K. E., Satpathy, A. T., & Mackay, L. K. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4099073
Sedegah, M., Hollingdale, M., Ganeshan, H., Belmonte, M., Huang, J., Belmonte, A., Inoue, S., Velasco, R., Hickey, B. W., Teneza-mora, N., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0256396 · Cited by 5
Kumashie, K. G., Cebula, M., Hagedorn, C., Kreppel, F., Pils, M. C., Koch‐Nolte, F., Rissiek, B., & Wirth, D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.592328 · Cited by 5
Self-citationImpact of multiple hits with cognate antigen on memory CD8+ T-cell fate
Takamura, S. (2020) · International Immunology · doi:10.1093/intimm/dxaa039 · Cited by 5
Chronic Viral Liver Diseases: Approaching the Liver Using T Cell Receptor-Mediated Gene Technologies
Healy, K., Pasetto, A., Sobkowiak, M. J., Soon, C. F., Cornberg, M., Aleman, S., & Chen, M. (2020) · Cells · doi:10.3390/cells9061471 · Cited by 6
Frank, R., Gabel, M., Heiss, K., Mueller, A., & Graw, F. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01137 · Cited by 5
Gajón, J. A., Juárez-Flores, Á., Mendoza-Roldan, F., Hernández-Aceves, J. A., Muñoz-Cruz, S., Pérez‐Torres, A., Fuentes‐Pananá, E. M., & Bonifaz, L. C. (2025) · OncoImmunology · doi:10.1080/2162402x.2025.2595360 · Cited by 5
“20 22–24 Their development and functional programming rely on transcription factors including RUNX3, Hobit, and Blimp1.”
GPR25 promotes the formation of lung and liver tissue-resident memory CD8 T cells
Han, F., Park, S., Shin, J. W., Castañeda-Castro, F. E., Hernández, J., Schmiedel, B. J., Liu, C., Jackson, M. R., Ottensmeier, C. H. H., & Vijayanand, P. (2025) · Science Immunology · doi:10.1126/sciimmunol.adu2089 · Cited by 4
Targeting T-Cell Activation for Malaria Immunotherapy: Scoping Review
Gustifante, B. N., Khairani, S., Fauziah, N., Riswari, S. F., & Berbudi, A. (2025) · Pathogens · doi:10.3390/pathogens14010071 · Cited by 4
Fighting the enemy within: Systemic immune defense against mucosal Salmonella infection
Nguyen, A. T., & McSorley, S. J. (2024) · Immunology Letters · doi:10.1016/j.imlet.2024.106930 · Cited by 7
Watson, F. N., Shears, M. J., Kalata, A. C., Duncombe, C., Seilie, A., Chavtur, C., Conrad, E., Talavera, I. C., Raappana, A., Sather, D., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-53118-9 · Cited by 4
“Consistent with other studies, we also found that CXCR6 hi -defined CD8 + Trm cells were important for sterile protection in our model 18,27 .”
BackgroundResultInfluentialDepew, C. E., & McSorley, S. J. (2023) · Vaccine · doi:10.1016/j.vaccine.2023.09.011 · Cited by 5
Moine, M. L., Azouz, A., Sanchez, G. S., Dejolier, S., Nguyen, M., Thomas, S., Shala, V., Dreidi, H., Denanglaire, S., Libert, F., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112876 · Cited by 8
Staying home or leaving for a party: tissue-dependent choices of tissue-resident memory T cells
van Gisbergen, K. P. J. M., & den Haan, J. M. M. (2022) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00828-z · Cited by 4
“Prime-trap approaches in which priming of T cells in the lymph nodes is combined with inflammatory and antigenic stimulation of primed T cells in the liver are a very potent strategy to achieve liver Trm cell formation [10].”
BackgroundBelhimeur, S., Briquet, S., Péronet, R., Pham, J., Commère, P., Formaglio, P., Amino, R., Scherf, A., Silvie, O., & Mécheri, S. (2021) · bioRxiv · doi:10.3389/fimmu.2023.1143012 · Cited by 4
da Silva, H. B. (2021) · ImmunoHorizons · doi:10.4049/immunohorizons.2000102 · Cited by 4
“The notable exception for intravascular labeling is the liver, where Trm (defined as resident by parabiosis) are positioned in the intravascular sinusoids (49).”
BackgroundComplete attenuation of Plasmodium falciparum sporozoites by atovaquone–proguanil
Borrmann, S., Sulyok, Z., Müller, K., Fendel, R., Sulyok, M., Friesen, J., Lalremruata, A., Sandri, T., Nguyen, T., Calle, C. L., et al. (2025) · EMBO Molecular Medicine · doi:10.1038/s44321-025-00301-8 · Cited by 3
“To overcome the limitation of low numbers of tissue-resident cytotoxic CD8 + T cells in the liver (Fernandez-Ruiz et al, 2016) we isolated the more abundant splenic antigen-speci fi c CD8 + effector memory (T em ) cells, which are established for systematic quantitative comparisons of vaccine…”
Overview of the host immune response to P. falciparum malaria
Antwi-Baffour, S. S., Mensah, B. T., & Annison, L. (2025) · Journal of Parasitic Diseases · doi:10.1007/s12639-025-01802-6 · Cited by 4
“CD8+ T cells recognize specific epitopes presented by MHC-I molecules on infected hepatocytes and form clusters around these cells (Perlmann and Troye-Blomberg 2002 ; Fernandez-Ruiz et al. 2016 ).”
Junge, M., Liaukouskaya, N., Schwarz, N., Pinto-Espinoza, C., Schaffrath, A. Z., Rissiek, B., Krebs, C. F., Rattay, G., Mittrücker, H., Tomas, N., et al. (2024) · Journal of the American Society of Nephrology · doi:10.1681/asn.0000000564 · Cited by 3
“2-antagonistic Nb s 1 16a. 18,19,29,36,37 To this end, we used the fl ow cytometry assay described in Figure 2 to monitor targeting of ARTC2.”
Self-citationAccelerated prime-and-trap vaccine regimen in mice using repRNA-based CSP malaria vaccine
MacMillen, Z., Hatzakis, K., Simpson, A. C., Shears, M. J., Watson, F. N., Erasmus, J. H., Khandhar, A. P., Wilder, B. K., Murphy, S., Reed, S., et al. (2023) · bioRxiv · doi:10.21203/rs.3.rs-3045076/v1 · Cited by 3
Tumwine-Downey, I., Deroost, K., Lévy, P., McLaughlin, S., Hosking, C., & Langhorne, J. (2022) · Current Research in Immunology · doi:10.1016/j.crimmu.2022.100054 · Cited by 3
Cryopreservation of Plasmodium Sporozoites
Bowers, C., Hancox, L. S., Peissig, K., Shiau, J. C., Vantaux, A., Witkowski, B., Phal, S., Maher, S., Harty, J., Kyle, D., et al. (2022) · Pathogens · doi:10.3390/pathogens11121487 · Cited by 3
Malaria research in Australia: looking through the lens of the past towards the future.
Doolan, D. (2021) · International Journal of Parasitology · doi:10.1016/j.ijpara.2021.11.005 · Cited by 3
Chemovaccination with a late-liver-stage antimalarial induces durable immunity against malaria.
Steel, R., Yu, C.-C., Abdalla, W. A., McConville, R., Ford, A., Caiazzo, S., Hesping, E., Fernandez-Ruiz, D., Holz, L. E., Heath, W. R., et al. (2026) · Science · doi:10.1126/science.aea7605 · Cited by 2
Self-citationPoly(I:C) and R848 adjuvants elicit sizeable humoral immunity to liver stage malaria antigens
Tandel, N., Thakkar, M., Ahuja, M., Shah, J., Trivedi, D. D., Pied, S., Singh, A. P., Prajapati, C., Tyagi, R. K., & Dalai, S. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1705839 · Cited by 2
mRNA vaccination overcomes haemozoin-mediated impairment of whole-parasite malaria vaccines in mice
Hassert, M., Drewry, L. L., Pewe, L. L., Hancox, L. S., He, R., Arumugam, S. A., Mix, M. R., Salem, A. K., & Harty, J. T. (2026) · Nature Microbiology · doi:10.1038/s41564-026-02263-0 · Cited by 5
Lee, J., Kang, M.-H., Kwon, K.-H., Cha, M.-S., Hong, J., Bae, Y.-S., Park, S., Yang, S., Kim, H. Y., Yoon, K. C., et al. (2025) · Experimental and Molecular Medicine · doi:10.1038/s12276-025-01565-3 · Cited by 2
A Trojan horse: Chemical boosting of Plasmodium falciparum whole sporozoite vaccine immunogenicity
Naar, C. M., van Schuijlenburg, R., van Meerbeek, M. P., Almeida, L., van Leeuwen, F. W. B., & Roestenberg, M. (2025) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2025.118666 · Cited by 2
Metadata
- Authors
- Fernandez-Ruiz, D., Ng, W. Y., Holz, L. E., Ma, J. Z., Zaid, A., Wong, Y. C., Lau, L. S., Mollard, V., Cozijnsen, A., Collins, N., Li, J., Davey, G. M., Kato, Y., Devi, S., Skandari, R., Pauley, M., Manton, J. H., Godfrey, D. I., Braun, A., Tay, S. S., Tan, P. S., Bowen, D. G., Koch-Nolte, F., Rissiek, B., Carbone, F. R., Crabb, B. S., Lahoud, M., Cockburn, I. A., Mueller, S. N., Bertolino, P., McFadden, G. I., Caminschi, I., & Heath, W. R.
- Affiliations
- Burnet Institute (AU)
- The University of Melbourne (AU)
- The University of Sydney (AU)
- University Medical Center Hamburg-Eppendorf (DE)
- Australian National University (AU)
- Corresponding author
- Caminschi, Irina
- Heath, William R.
- ORCID
- Ng, Wei Yi
- Holz, Lauren E.
- Ma, Joel Z.
- Zaid, Ali
- Mollard, Vanessa
- Cozijnsen, Anton
- Li, Jessica
- Davey, Gayle M.
- Kato, Yu
- Devi, Sapna
- Pauley, Michael
- Manton, Jonathan H.
- Godfrey, Dale I.
- Braun, Asolina
- Tay, Szun Szun
- Tan, Peck Szee
- Bowen, David G.
- Rissiek, Björn
- Crabb, Brendan S.
- Lahoud, Mireille
- Cockburn, Ian A.
- Mueller, Scott N.
- Bertolino, Patrick
- McFadden, Geoffrey I.
- Caminschi, Irina
- Heath, William R.
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 45
- Issue
- 4
- Pages
- 889-902
- ISSN
- 1074-7613 (ISSN-L)
- OpenAlex
- W2525642000
- Cited by
- 438
- References
- 0
- Citations by year
- 2026: 30 · 2025: 42 · 2024: 38 · 2023: 41 · 2022: 42 · 2021: 70 · 2020: 59 · 2019: 47 · 2018: 47 · 2017: 18 · 2016: 3
- FWCI
- 38.01
- Type
- journal article
- Language
- en
- Update notices
- erratum (2019-10-15)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Griffith Research Online (submittedVersion)
- Funders
- National Health and Medical Research Council of Australia
- Australian Research Council
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- malaria, liver-stage immunity, tissue-resident memory T cells, CD8+ T cells, Plasmodium, dendritic cell priming, liver inflammation, malaria vaccine
- MeSH terms
- Animals, Dendritic Cells, Immunologic Memory, Liver, Liver Diseases, Malaria, Culicidae, Plasmodium berghei, Vaccination, Malaria Vaccines, CD8-Positive T-Lymphocytes, Hepatocytes, Sporozoites, Mice
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