Prostate cancer (PCa) is a major cause of cancer morbidity and mortality among men. Common therapy involves the reduction of circulating androgens to castrated levels. However, after the initial response, PCa eventually starts growing despite castrate levels of androgens, thereby becoming castration-resistant PCa (CRPC). There are no curative treatments for CRPC, and once PCa develops metastases, it becomes lethal. Therefore, elucidating the mechanisms of survival, growth, and metastasis in CRPC is necessary to develop improved therapies against CRPC. In this thesis, I have investigated new molecular mechanisms in CRPC, specifically, the interplay between androgen receptor (AR) signaling and BRCA1, the role of the BRCA1 protein in PCa, and metastasis formation regulation by the stress fiber contraction regulator caldesmon (CaD). We described AR-mediated activation of NRF2 via BRCA1 in CRPC by assaying PCa cell lines, murine xenografts, and patient samples. Moreover, this study showed that the dynamic regulation of BRCA1 by AR signaling may predispose to genetic alterations and promote castration resistance via enhanced reactive oxygen species defense. Additionally, we found that silencing CALD1 reduced metastasis in zebrafish PCa xenografts and spheroids in 3D culture. Our experimental and bioinformatic analyses suggest that CaD correlates with metastasis-associated epithelial-to mesenchymal transition in PCa. We discovered that antiandrogen resistance gives rise to cell populations expressing CaD and glucocorticoid receptor (GR), and found that GR upregulated CaD in PCa using a castration-resistant murine xenograft. Furthermore, we explored the potential for CaD as a drug target by characterizing a cald1 mutant zebrafish, which exhibited a non-lethal phenotype with a mild neural defect. This thesis demonstrated that different AR signaling states have the capacity to induce transient genomic instability and enhance defense against ROS via regulation of BRCA1 and BRCA1-mediated NRF2-activation. In this thesis, we have also identified the oncogenic properties of CaD as a mediator of PCa metastasis. Additionally, we found that cald1 mutations were tolerated and non-lethal in early zebrafish development, suggesting potential for CaD as a drug target.