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Plakophilin-associated RNA-binding proteins in prostate cancer and their implications in tumor progression and metastasis

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Abstract

Both plakophilins (PKP) 1 and 3 play a role in the progression of prostate cancer. The RNA-binding proteins (RBPs) GAP-SH3-binding protein (G3BP), fragile-X-related protein 1 (FXR1), poly(A)-binding protein, cytoplasmic 1 (PABPC1), and up-frameshift factor 1 (UPF1) are associated with PKP3. All these RBPs have an impact on RNA metabolism. Until recently, the PKP-associated RBPs have not been analyzed in prostate cancer. In the current study, we showed by affinity purification that the PKP3-associated RBPs were also binding partners of PKP1. We examined the expression of PKP1/3-associated RBPs and PKP1/3 in prostate cell lines, tumor-free prostate, and 136 prostatic adenocarcinomas by immunofluorescence and immunoblot. All four RBPs G3BP, FXR1, UPF1, and PABPC1 were expressed in the glandular epithelium of the normal prostate. PKP1 and FXR1 were strongly reduced in tumor tissues with Gleason score >7 and diminished expression of PKP1 and FXR1 also appeared to be associated with a metastatic phenotype. Additionally, the predominant nuclear localization of UPF1 in normal glandular cells and low grade tumors was switched to a more cytoplasmic pattern in carcinomas with Gleason score >7. Our findings suggest that PKP1 and FXR1 may have a tumor-suppressive function and are downregulated in more aggressive tumors. Collectively, PKP1/3-associated RBPs FXR1 and UPF1 may have a functional role in prostate cancer progression and metastasis and highlight the potential importance of posttranscriptional regulation of gene expression and nonsense-mediated decay in cancer.

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Acknowledgments

The authors thank Dr. Tim Holland-Letz (Biostatistics, DKFZ, Heidelberg, Germany) for advice in statistical analysis. This study was supported by grants from the German Cancer Aid and the “Deutsche Forschungsgemeinschaft” (STR 638/2-1). Cheng Yang acknowledges a fellowship from the Chinese Scholarship Council.

Conflict of interest statement

The authors declare that there are no conflicts of interest.

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Authors and Affiliations

  1. Division of Vascular Oncology and Metastasis, German Cancer Research Center, DKFZ-ZMBH Alliance, Im Neuenheimer Feld 280, 69120, Heidelberg, Germany

    Cheng Yang & Ilse Hofmann

  2. Department of Vascular Biology and Tumor Angiogenesis (CBTM), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany

    Cheng Yang & Ilse Hofmann

  3. Institute of Pathology, University Medical Center Göttingen, Göttingen, Germany

    Philipp Ströbel

  4. Institute of Pathology, University Medical Center Mannheim, Heidelberg University, Mannheim, Germany

    Alexander Marx

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Correspondence to Ilse Hofmann.

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Supple Fig. 1

Double immunofluorescence of PKP1, symplekin, and UPF1 using two different UPF1 antibodies in BPH-1 cells (UPF1-ab1, antibody from Bethyl Laboratories; UPF2-ab2, antibody from Sigma-Aldrich). Localization of PKP1 and symplekin is shown in the red channel (a, b, c). Occurrence of the UPF1 (a’, b’, c’) is shown in the green channel. Merged pictures are also presented (a”, c”, c”). Cells were fixed with formaldehyde. Scale bar, 20 μm (JPEG 174 kb)

High-resolution image (TIFF 5564 kb)

Supple Fig. 2

Detection of G3BP on formaldehyde-fixed, paraffin-embedded tissues of tumor-free human prostate (a) compared with the localization of keratin 14 (a’). The merged picture is given in (a”). Although G3BP is detectable in both luminal and basal cells, basal cells show a stronger G3BP expression. Scale bar, 20 μm (JPEG 30 kb)

High-resolution image (TIFF 1320 kb)

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Yang, C., Ströbel, P., Marx, A. et al. Plakophilin-associated RNA-binding proteins in prostate cancer and their implications in tumor progression and metastasis. Virchows Arch 463, 379–390 (2013). https://doi.org/10.1007/s00428-013-1452-y

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