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The RNA-binding protein ZFP36 is involved in tumorigenesis. To systematically elucidate its pan-cancer role, we conducted an integrated analysis of ZFP36 across malignancies, combining bioinformatic exploration with experimental validation. Utilizing datasets from TCGA, GEO, GTEx, HPA, CPTAC, GEPIA2, TIMER2, cBioPortal, and STRING, we employed bioinformatics methods to investigate the potential carcinogenic properties of ZFP36. This included examining correlations between ZFP36 and gene expression, prognosis, gene mutation, immunohistochemistry staining, immune cell infiltration, and constructing an interaction network of 50 ZFP36-binding proteins. Additionally, we performed enrichment analysis of ZFP36-related partners. Furthermore, to validate key bioinformatic predictions, quantitative real-time PCR (qRT-PCR) was performed on paired cancer/normal cell lines (LIHC, LUAD, BRCA). ZFP36 expression was found to be dysregulated in a cancer type-dependent manner, with significant upregulation observed in most tumor types analyzed, including BLCA, BRCA, LIHC, and LUAD. Furthermore, ZFP36 demonstrated early diagnostic value across 33 types of tumors and showed varying associations with prognosis depending on the tumor type. ZFP36 was also significantly associated with most immune-infiltrating cells in pan-cancer analyses. High ZFP36 expression was linked to pathways related to tumor progression. Critically, these bioinformatic predictions were experimentally validated, as qRT-PCR confirmed the significant upregulation of ZFP36 and its functional network genes (SOCS3, JUN, SLC7A11, CSRNP1) in LIHC, LUAD, and BRCA cell lines. This study provides a comprehensive pan-cancer analysis of ZFP36, integrating bioinformatics with experimental validation. We demonstrated its dysregulation across cancers in a type-dependent manner, correlations with immune infiltration and tumor-associated pathways. Critically, qRT-PCR experiments confirmed the significant co-upregulation of ZFP36 and its functional network genes (SOCS3, JUN, SLC7A11, CSRNP1) in LIHC, LUAD, and BRCA cell lines. These findings establish ZFP36 as a promising diagnostic and prognostic biomarker and suggest its role as a pivotal post-transcriptional regulator in tumorigenesis, supporting its potential for clinical application in cancer assessment.