CD8+ T Cells Induce Fatal Brainstem Pathology during Cerebral Malaria via Luminal Antigen-Specific Engagement of Brain Vasculature

Swanson, Phillip A.; Hart, Geoffrey T.; Russo, Matthew V.; Nayak, Debasis; Yazew, Takele; Peña, Mirna; Khan, Shahid M.; Janse, Chris J.; Pierce, Susan K.; McGavern, Dorian B.

doi:10.1371/journal.ppat.1006022

Cited by 126Malaria Research and ControlBarrier Structure and Function StudiesBacterial Infections and Vaccines

CD8+ T Cells Induce Fatal Brainstem Pathology during Cerebral Malaria via Luminal Antigen-Specific Engagement of Brain Vasculature

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Swanson, Phillip A., Hart, Geoffrey T., Russo, Matthew V., Nayak, Debasis, Yazew, Takele, Peña, Mirna, Khan, Shahid M., Janse, Chris J. +2 more·2016·PLOS Pathogens

DOI 10.1371/journal.ppat.1006022PMC PMC5131904

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Abstract

Cerebral malaria (CM) is a severe complication of Plasmodium falciparum infection that results in thousands of deaths each year, mostly in African children. The in vivo mechanisms underlying this fatal condition are not entirely understood. Using the animal model of experimental cerebral malaria (ECM), we sought mechanistic insights into the pathogenesis of CM. Fatal disease was associated with alterations in tight junction proteins, vascular breakdown in the meninges / parenchyma, edema, and ultimately neuronal cell death in the brainstem, which is consistent with cerebral herniation as a cause of death. At the peak of ECM, we revealed using intravital two-photon microscopy that myelomonocytic cells and parasite-specific CD8+ T cells associated primarily with the luminal surface of CNS blood vessels. Myelomonocytic cells participated in the removal of parasitized red blood cells (pRBCs) from cerebral blood vessels, but were not required for the disease. Interestingly, the majority of disease-inducing parasite-specific CD8+ T cells interacted with the lumen of brain vascular endothelial cells (ECs), where they were observed surveying, dividing, and arresting in a cognate peptide-MHC I dependent manner. These activities were critically dependent on IFN-γ, which was responsible for activating cerebrovascular ECs to upregulate adhesion and antigen-presenting molecules. Importantly, parasite-specific CD8+ T cell interactions with cerebral vessels were impaired in chimeric mice rendered unable to present EC antigens on MHC I, and these mice were in turn resistant to fatal brainstem pathology. Moreover, anti-adhesion molecule (LFA-1 / VLA-4) therapy prevented fatal disease by rapidly displacing luminal CD8+ T cells from cerebrovascular ECs without affecting extravascular T cells. These in vivo data demonstrate that parasite-specific CD8+ T cell-induced fatal vascular breakdown and subsequent neuronal death during ECM is associated with luminal, antigen-dependent interactions with cerebrovasculature.

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Displacement of these T cells from CNS vasculature by therapeutic administration of antibodies to LFA-1 and VLA-4 prevented the disease.
“Displacement of these T cells from CNS vasculature by means of therapeutic administration of antibodies to LFA-1 and VLA-4 prevented the disease (157).”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [157]
In rodents, BBB breakdown and fatal edema are caused by parasite-specific CD8+ T cell engagement of cerebrovascular endothelial cells that cross-present parasite antigen.
“In rodents, it was revealed that BBB breakdown and fatal edema are caused by parasite-specific CD8+ T cell engagement of cerebrovascular endothelial cells that cross-present parasite antigen (157, 158).”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [157]
Death from cerebral malaria results from the accumulation of water in the cranium and brainstem herniation.
“Similar to LCMV meningitis, death from cerebral malaria results from the accumulation of water in the cranium and brainstem herniation (156, 157).”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [157]

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The Subcellular Location of Ovalbumin in Plasmodium berghei Blood Stages Influences the Magnitude of T-Cell Responses
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Tsuchihashi (2000) · doi:10.1002/1521-4141(200006)30:6

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The anatomy and immunology of vasculature in the central nervous system
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CNS Infection and Immune Privilege
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Pathophysiology and neurologic sequelae of cerebral malaria
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The Ins and Outs of Cerebral Malaria Pathogenesis: Immunopathology, Extracellular Vesicles, Immunometabolism, and Trained Immunity
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Interleukin-15 Complex Treatment Protects Mice from Cerebral Malaria by Inducing Interleukin-10-Producing Natural Killer Cells
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Imaging the dynamic recruitment of monocytes to the blood–brain barrier and specific brain regions during Toxoplasma gondii infection
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CXCL10 stabilizes T cell–brain endothelial cell adhesion leading to the induction of cerebral malaria
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IL-33 receptor ST2 regulates the cognitive impairments associated with experimental cerebral malaria
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Immunological defense of CNS barriers against infections
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Perforin Expression by CD8 T Cells Is Sufficient To Cause Fatal Brain Edema during Experimental Cerebral Malaria
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Cerebral Malaria: Current Clinical and Immunological Aspects
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Comparison of CD8+ T Cell Accumulation in the Brain During Human and Murine Cerebral Malaria
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Brain Endothelium: The “Innate Immunity Response Hypothesis” in Cerebral Malaria Pathogenesis
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Profiling MHC II immunopeptidome of blood‐stage malaria reveals that cDC1 control the functionality of parasite‐specific CD4 T cells
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MRI demonstrates glutamine antagonist-mediated reversal of cerebral malaria pathology in mice
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Desperately Seeking Therapies for Cerebral Malaria
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Pathogenetic mechanisms and treatment targets in cerebral malaria
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Ferroptosis participates in neuron damage in experimental cerebral malaria and is partially induced by activated CD8+ T cells
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Overview of Plasmodium spp. and Animal Models in Malaria Research
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Endothelial cells and lymphatics at the interface between the immune and central nervous systems: implications for multiple sclerosis
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Cytotoxic T Cell-Derived Granzyme B Is Increased in Severe Plasmodium Falciparum Malaria
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Unravelling mysteries at the perivascular space: a new rationale for cerebral malaria pathogenesis
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Gamma Interferon Mediates Experimental Cerebral Malaria by Signaling within Both the Hematopoietic and Nonhematopoietic Compartments
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CD8+ and CD4+ T Cells Infiltrate into the Brain during Plasmodium berghei ANKA Infection and Form Long-Term Resident Memory
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Adenosine A2A Receptor Activation Enhances Blood–Tumor Barrier Permeability in a Rodent Glioma Model
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Mouse Models for Unravelling Immunology of Blood Stage Malaria
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Perivascular macrophages create an intravascular niche for CD8 + T cell localisation prior to the onset of fatal experimental cerebral malaria
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Effects of a Small-Molecule Perforin Inhibitor in a Mouse Model of CD8 T Cell–Mediated Neuroinflammation
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Intravital Microscopy of the Beating Murine Heart to Understand Cardiac Leukocyte Dynamics
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Neurovascular Interactions in Malaria
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PDL1 Fusion Protein Protects Against Experimental Cerebral Malaria via Repressing Over-Reactive CD8+ T Cell Responses
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The Liver-Stage Plasmodium Infection Is a Critical Checkpoint for Development of Experimental Cerebral Malaria
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Repetitive antigen stimulation in the periphery dictates the composition and recall responses of brain-resident memory CD8+ T cells
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IL-4 Treatment Mitigates Experimental Cerebral Malaria by Reducing Parasitemia, Dampening Inflammation, and Lessening the Cytotoxicity of T Cells
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The immunomodulatory effect of microglia on ECM neuroinflammation via the PD‐1/PD‐L1 pathway
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Intravital microscopy: Imaging host–parasite interactions in the brain
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Authors: Swanson, P. A., Hart, G. T., Russo, M. V., Nayak, D., Yazew, T., Peña, M., Khan, S. M., Janse, C. J., Pierce, S. K., & McGavern, D. B.
Affiliations: National Institutes of Health (US)
National Institute of Allergy and Infectious Diseases (US)
Indian Institute of Technology Indore (IN)
Leiden University Medical Center (NL)
Corresponding author: McGavern, Dorian B.
ORCID: Swanson, Phillip A.
Hart, Geoffrey T.
Russo, Matthew V.
Nayak, Debasis
Yazew, Takele
Khan, Shahid M.
Janse, Chris J.
Pierce, Susan K.
McGavern, Dorian B.
Venue: PLOS Pathogens
Publisher: Public Library of Science (PLoS)
Published: 2016-12-01
Volume: 12
Issue: 12
Pages: e1006022
ISSN: 1553-7366 (ISSN-L)
1553-7374
DOI: 10.1371/journal.ppat.1006022
PMC: PMC5131904
OpenAlex: W2558563646
Cited by: 125
References: 91
Citations by year: 2026: 4 · 2025: 14 · 2024: 10 · 2023: 11 · 2022: 13 · 2021: 12 · 2020: 12 · 2019: 26 · 2018: 12 · 2017: 11
FWCI: 16.20
Type: journal article
Language: en
Open access: gold
doi.org
Licence: public-domain
creativecommons.org/publicdomain/zero/1.0/ (vor)
Locations: PLoS Pathogens (publishedVersion, public-domain)
PubMed Central (publishedVersion, public-domain)
PubMed (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Leiden Repository (Leiden University) (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Funders: National Institutes of Health
National Institute of Mental Health
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
Keywords: cerebral malaria, experimental cerebral malaria, CD8+ T cells, Plasmodium falciparum, brainstem pathology, brain endothelial cells, tight junctions, brain herniation, neuronal cell death, myelomonocytic cells, parasitized red blood cells, interferon-gamma, MHC class I antigen presentation, LFA-1, VLA-4, adhesion molecules, cerebral edema
MeSH terms: Animals, Blood Vessels, Blood-Brain Barrier, Brain Stem, Disease Models, Animal, Flow Cytometry, Immunohistochemistry, Mice, Transgenic, Plasmodium berghei, Malaria, Cerebral, CD8-Positive T-Lymphocytes, Mice

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CD8+ T Cells Induce Fatal Brainstem Pathology during Cerebral Malaria via Luminal Antigen-Specific Engagement of Brain Vasculature

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