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Cited by 438Malaria Research and ControlT-cell and B-cell ImmunologyImmunotherapy and Immune Responses

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Liver-Resident Memory CD8+ T Cells Form a Front-Line Defense against Malaria Liver-Stage Infection

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Fernandez-Ruiz, Daniel, Ng, Wei Yi, Holz, Lauren E., Ma, Joel Z., Zaid, Ali, Wong, Yik Chun, Lau, Lei Shong, Mollard, Vanessa, Cozijnsen, Anton, Collins, Nicholas, Li, Jessica, Davey, Gayle M., Kato, Yu, Devi, Sapna, Skandari, Roghieh, Pauley, Michael, Manton, Jonathan H., Godfrey, Dale I., Braun, Asolina, Tay, Szun Szun, Tan, Peck Szee, Bowen, David G., Koch-Nolte, Friedrich, Rissiek, Björn, Carbone, Francis R., Crabb, Brendan S., Lahoud, Mireille, Cockburn, Ian A., Mueller, Scott N., Bertolino, Patrick, McFadden, Geoffrey I., Caminschi, Irina, Heath, William R.·2016·Immunity
DOI 10.1016/j.immuni.2016.08.011
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Abstract

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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Research works printed but not linked: 37

  1. Berenzon, 2003, Protracted protection to Plasmodium berghei malaria is linked to functionally and phenotypically heterogeneous liver memory CD8+ T cells, J. Immunol., 171, 2024, 10.4049/jimmunol.171.4.2024 · DOI
  2. Bergsbaken, 2015, Proinflammatory microenvironments within the intestine regulate the differentiation of tissue-resident CD8+ T cells responding to infection, Nat. Immunol., 16, 406, 10.1038/ni.3108 · DOI
  3. Butler, 2012, Whole parasite vaccination approaches for prevention of malaria infection, Trends Immunol., 33, 247, 10.1016/j.it.2012.02.001 · DOI
  4. Cabrera, 2013, In vivo CD8+ T cell dynamics in the liver of Plasmodium yoelii immunized and infected mice, PLoS ONE, 8, e70842, 10.1371/journal.pone.0070842 · DOI
  5. Cockburn, 2010, Prolonged antigen presentation is required for optimal CD8+ T cell responses against malaria liver stage parasites, PLoS Pathog., 6, e1000877, 10.1371/journal.ppat.1000877 · DOI
  6. Epstein, 2011, Live attenuated malaria vaccine designed to protect through hepatic CD8+ T cell immunity, Science, 334, 475, 10.1126/science.1211548 · DOI
  7. Galkina, 2005, Preferential migration of effector CD8+ T cells into the interstitium of the normal lung, J. Clin. Invest., 115, 3473, 10.1172/JCI24482 · DOI
  8. Geissmann, 2005, Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids, PLoS Biol., 3, e113, 10.1371/journal.pbio.0030113 · DOI
  9. Ishizuka, 2016, Protection against malaria at 1 year and immune correlates following PfSPZ vaccination, Nat. Med., 22, 614, 10.1038/nm.4110 · DOI
  10. Jiang, 2012, Skin infection generates non-migratory memory CD8+ T(RM) cells providing global skin immunity, Nature, 483, 227, 10.1038/nature10851 · DOI
  11. Krieg, 2006, Therapeutic potential of Toll-like receptor 9 activation, Nat. Rev. Drug Discov., 5, 471, 10.1038/nrd2059 · DOI
  12. Lahoud, 2011, Targeting antigen to mouse dendritic cells via Clec9A induces potent CD4 T cell responses biased toward a follicular helper phenotype, J. Immunol., 187, 842, 10.4049/jimmunol.1101176 · DOI
  13. Lau, 2014, CD8+ T cells from a novel T cell receptor transgenic mouse induce liver-stage immunity that can be boosted by blood-stage infection in rodent malaria, PLoS Pathog., 10, e1004135, 10.1371/journal.ppat.1004135 · DOI · Paper page
  14. Mackay, 2012, Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation, Proc. Natl. Acad. Sci. USA, 109, 7037, 10.1073/pnas.1202288109 · DOI
  15. Mackay, 2015, T-box transcription factors combine with the cytokines TGF-β and IL-15 to control tissue-resident memory T cell fate, Immunity, 43, 1101, 10.1016/j.immuni.2015.11.008 · DOI
  16. Melloul, 2014, Small animal magnetic resonance imaging: an efficient tool to assess liver volume and intrahepatic vascular anatomy, J. Surg. Res., 187, 458, 10.1016/j.jss.2013.11.1079 · DOI
  17. Nganou-Makamdop, 2012, Long term protection after immunization with P. berghei sporozoites correlates with sustained IFNγ responses of hepatic CD8+ memory T cells, PLoS ONE, 7, e36508, 10.1371/journal.pone.0036508 · DOI
  18. Nussenzweig, 1967, Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei, Nature, 216, 160, 10.1038/216160a0 · DOI
  19. Ramakrishnan, 2013, Laboratory maintenance of rodent malaria parasites, Methods Mol. Biol., 923, 51, 10.1007/978-1-62703-026-7_5 · DOI
  20. Rissiek, 2014, Technical Advance: a new cell preparation strategy that greatly improves the yield of vital and functional Tregs and NKT cells, J. Leukoc. Biol., 95, 543, 10.1189/jlb.0713407 · DOI
  21. Rodrigues, 1993, The relative contribution of antibodies, CD4+ and CD8+ T cells to sporozoite-induced protection against malaria, Immunology, 80, 1
  22. 2014, Efficacy and safety of the RTS,S/AS01 malaria vaccine during 18 months after vaccination: a phase 3 randomized, controlled trial in children and young infants at 11 African sites, PLoS Med., 11, e1001685, 10.1371/journal.pmed.1001685 · DOI
  23. Samulowitz, 2010, A novel class of immune-stimulatory CpG oligodeoxynucleotides unifies high potency in type I interferon induction with preferred structural properties, Oligonucleotides, 20, 93, 10.1089/oli.2009.0210 · DOI
  24. Schenkel, 2013, Sensing and alarm function of resident memory CD8+ T cells, Nat. Immunol., 14, 509, 10.1038/ni.2568 · DOI
  25. Schmidt, 2008, Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria, Proc. Natl. Acad. Sci. USA, 105, 14017, 10.1073/pnas.0805452105 · DOI
  26. Seder, 2013, Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine, Science, 341, 1359, 10.1126/science.1241800 · DOI
  27. Seman, 2003, NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor, Immunity, 19, 571, 10.1016/S1074-7613(03)00266-8 · DOI
  28. Shin, 2012, A vaccine strategy that protects against genital herpes by establishing local memory T cells, Nature, 491, 463, 10.1038/nature11522 · DOI
  29. Smith, 2003, Cutting edge: conventional CD8 α+ dendritic cells are preferentially involved in CTL priming after footpad infection with herpes simplex virus-1, J. Immunol., 170, 4437, 10.4049/jimmunol.170.9.4437 · DOI
  30. Tay, 2014, Intrahepatic activation of naive CD4+ T cells by liver-resident phagocytic cells, J. Immunol., 193, 2087, 10.4049/jimmunol.1400037 · DOI
  31. Thomas, 2011, PLZF induces an intravascular surveillance program mediated by long-lived LFA-1-ICAM-1 interactions, J. Exp. Med., 208, 1179, 10.1084/jem.20102630 · DOI
  32. Tse, 2013, Unique transcriptional profile of liver-resident memory CD8+ T cells induced by immunization with malaria sporozoites, Genes Immun., 14, 302, 10.1038/gene.2013.20 · DOI
  33. Tse, 2014, The chemokine receptor CXCR6 is required for the maintenance of liver memory CD8+ T cells specific for infectious pathogens, J. Infect. Dis., 210, 1508, 10.1093/infdis/jiu281 · DOI
  34. Wakim, 2010, Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence, Proc. Natl. Acad. Sci. USA, 107, 17872, 10.1073/pnas.1010201107 · DOI
  35. Warren, 2006, T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells, Hepatology, 44, 1182, 10.1002/hep.21378 · DOI · Paper page
  36. Weiss, 1988, CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites, Proc. Natl. Acad. Sci. USA, 85, 573, 10.1073/pnas.85.2.573 · DOI
  37. Zaid, 2014, Persistence of skin-resident memory T cells within an epidermal niche, Proc. Natl. Acad. Sci. USA, 111, 5307, 10.1073/pnas.1322292111 · DOI

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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
Venue
Immunity
Publisher
Elsevier BV
Published
2016-10
Volume
45
Issue
4
Pages
889-902
ISSN
1074-7613 (ISSN-L)
DOI
10.1016/j.immuni.2016.08.011
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
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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