Long-read sequencing with nanopore technology has been widely utilized for the identification of the full-length sequence of RNA molecules. It is especially suitable for the identification of circular RNAs (circRNAs), which are regulatory molecules that are regarded as promising non-invasive biomarkers for various human malignancies, including breast cancer. The impact of circRNAs derived from the protein arginine methyltransferase 1 (PRMT1) gene has not been clarified yet, even though the effect of PRMT1-mediated methylation on breast cancer cell characteristics has been well established. We have previously shown that several circRNAs are produced by PRMT1, and thus we aimed at identifying novel PRMT1 circRNAs in 12 breast cell lines, following a PCR-based, targeted nanopore sequencing work flow (described in detail in the supplementary materials and methods). This pipeline leads to the identification of the full circRNA sequence, including the backesplice junction, as a single read. Contrary to circRNA profiling studies, our targeted approach allows for the amplification and sequencing of circRNAs originating from the PRMT1 gene with higher specificity. Meanwhile, it enables the identification of rare circular transcripts that may be missed by a direct circRNA sequencing approach. In our study, a wide variety of novel PRMT1 circRNAs were identified. Their intricacy in structure and distinct expression profiles among breast cancer cells raises new questions about the functions of circRNAs and the regulatory role of PRMT1 in breast cancer.