Background
HTLV-1 subtype-C (HTLV-1c) infection is endemic in Central Australia with prevalence rates ~40% in some First Nations communities. HTLV-1c is a genetically divergent subtype and commonly associated with pulmonary disease (HAPD) and early all-cause mortality. This study determines the host-virus factors of HTLV-1c-related pathologies.
Methods
Matching plasma and PBMCs (n=77) were collected at Alice Springs Hospital. Plasma cytokine levels were measured by bead-array and PBMC proviral load (PVL) by ddPCR. HTLV-1c-specific T-cell responses were determined by activation induced marker (AIM) assay (n=40). The phenotypes of HTLV-1c-infected cells (n=34) were characterised by FACS. Integrated proviruses were amplified by limiting dilution nested PCR (n=6) and long-read sequenced using Nanopore.
Results
We observed HTLV-1c-specific T-cells and ubiquitous activation. We determined a dysfunctional cytokine network in HTLV-1c infection (positively-associated TNF-α, IL-2, age; negatively-associated IFN-γ, IL-8). Furthermore, we showed a unique HAPD cytokine profile (positively-associated IL-10, IL-6, PVL; negatively-associated IFN-γ, IL-8). We determined effector-memory T-cells are enriched for exhaustion markers, and corresponding soluble plasma markers, in HTLV-1c+ participants.
Notably, we observed activation and expansion of CCR4+CD4+ lung-homing proxy-phenotype cells correlating to PVL. All participants harboured highly-defective provirus, however HAPD+ differentially retained hbz gene. We detected exclusively replication competent provirus in CCR4-CD4+ T-cells. Proviral deletion breakpoints frequently occurred at LTR-like sequences. Lastly, we characterised novel HTLV-1c-host chimeric proviruses.
Conclusions
We identified a dysfunctional T-cell and cytokine response leading to exhaustion in all HTLV-1c-infected individuals, which may contribute to increased all-cause mortality. HTLV-1c-infected and activated cells with lung-homing potential may contribute to HAPD, however CCR4-CD4+ T-cells containing full-length provirus may facilitate transmission. Retention of hbz gene in HAPD+ subjects suggests its’ expression is crucial in driving disease. Chimeric proviruses may further contribute to cell dysfunction and pathogenesis.
Phenotypic characterisation of HTLV-1c-infected cells, and the provirus structure within, provides a focus for future studies developing therapeutic strategies.