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Background  Accumulating evidence suggests tRNA-derived fragments (tRFs) play important roles in cellular homeostasis. Here we aimed to explore aberrant expression of tRFs in CD4 +  T cells from patients with systemic lupus erythematosus (SLE) and their potential function in the SLE pathogenesis.    Methods  First, small RNA sequencing was performed on CD4 +  T cells from four SLE patients and three healthy controls (HCs). Candidate tRFs were then validated in CD4 +  T cells from 97 SLE patients and their relevant disease controls using qRT-PCR. Then sequencing was used to investigate the profiles of HC-derived CD4 +  T cells transfected with  tRF-3009 . Lastly,  tRF-3009  siRNA or  tRF-3009  mimics were transfected into CD4 +  T cells with/without IFN-α. Changes in oxygen consumption rate (OCR), ATP, and ROS production were analyzed.    Results  We identified 482 differentially expressed tRFs from SLE CD4 +  T cells and chose tRF-3009 for further analysis due to its upregulation and the positive correlations between its expression and SLEDAI, active lupus nephritis and serum IFN-α levels. In vitro,  tRF-3009  over-expressing CD4 +  T cell profiling and putative analysis linked this product to the type I IFN and oxidative phosphorylation (OXPHOS) pathways. Interestingly, IFN-α is capable of inducing ROS and ATP production in CD4 +  T cells, while knockdown of  tRF-3009  reversed this process. Overexpression of  tRF-3009  in CD4 +  T cells alone was sufficient to upregulate OCR, ROS, and ATP production.    Conclusions  Our study is the first to link aberrant tRF expression and SLE.  tRF-3009  may participate in metabolic modulation of IFN-α-induced CD4 +  T cell OXPHOS in lupus.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12967-021-02967-3.

tRNA derived fragment (tRF)-3009 participates in modulation of IFN-α-induced CD4+ T cell oxidative phosphorylation in lupus patients