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Long COVID manifests with T cell dysregulation, inflammation and an uncoordinated adaptive immune response to SARS-CoV-2

Authors: Kailin Yin,Michael J. Peluso,Xiaoyu Luo,Reuben Thomas,Min-Gyoung Shin,Jason Neidleman,Alicer Andrew,Kyrlia C. Young,Tongcui Ma,Rebecca Hoh,Khamal Anglin,Beatrice Huang,Urania Argueta,Monica Lopez,Daisy Valdivieso,Kofi Asare,Tyler-Marie Deveau,Sadie E. Munter,Rania Ibrahim,Ludger Ständker,Scott Lu,Sarah A. Goldberg,Sulggi A. Lee,Kara L. Lynch,J. Daniel Kelly,Jeffrey N. Martin,Jan Münch,Steven G. Deeks,Timothy J. Henrich,Nadia R. Roan
Journal: Nature Immunology
Publisher: Springer Science and Business Media LLC
Publish date: 2024-1-11
ISSN: 1529-2908 DOI: 10.1038/s41590-023-01724-6
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The authors define antigen-specificity based on the induction of IFN-γ, TNF, or CCL4 following peptide stimulation. The use of CCL4 (MIP-1β) as a defining marker for virus-specific CD8⁺ T cells is highly atypical and problematic.

1: CCL4 is a chemokine produced by a wide variety of immune cells (including CD4⁺ T cells, NK cells, monocytes, and dendritic cells) in response to inflammatory stimuli. Its expression is not a canonical or standard marker for antigen-specific CD8⁺ T cell activation, which is typically defined by IFN-γ±TNF production and/or degranulation (CD107a). Could the authors provide precedent or validation data demonstrating that CCL4 production, in the absence of IFN-γ/TNF, reliably identifies a mono-specific, SARS-CoV-2-reactive CD8⁺ T cell population, and not a bystander-activated or innate-like cell? The noted background staining with the CCL4 antibody in flow cytometry (Methods, page 10) further raises concerns about signal-to-noise ratio in the CyTOF assay.
2: A key finding is the increased frequency of PD1⁺CTLA4⁺ “exhausted” cells within the SARS-CoV-2-specific CD8⁺ T cell compartment in LC. If the “specific” pool is contaminated with non-specific, activated cells (which may also express checkpoint molecules), this phenotypic difference could be an artifact of the gating strategy rather than a true virological phenomenon. Were control stimulations with irrelevant peptides (e.g., CMV, EBV, or a mock pool) performed to establish the baseline frequency of CCL4⁺CD8⁺ T cells in this assay and confirm the SARS-CoV-2-specificity of the gated population?
3: The LC cohort had a higher proportion of previously hospitalized individuals (26% vs. 12.5% in R) and higher BMI/comorbidity burden. Severe acute COVID-19 is known to induce profound, long-lasting immune alterations. Have the authors performed sub-analyses comparing only non-hospitalized LC vs. R participants, or included hospitalization status as a covariate in their models, to ensure that the observed immune “dysregulation” is attributable to the Long COVID clinical trajectory itself, and not to the legacy of more severe initial infection?

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