Cited by 287MicroRNA in disease regulationProstate Cancer Treatment and ResearchMechanisms of cancer metastasis

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Loss of p63 and its microRNA-205 target results in enhanced cell migration and metastasis in prostate cancer

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Tucci, Paola, Agostini, Massimiliano, Grespi, Francesca, Markert, Elke K., Terrinoni, Alessandro, Vousden, Karen H., Muller, Patricia A. J., Dötsch, Volker, Kehrloesser, Sebastian, Sayan, Berna S., Giaccone, Giuseppe, Lowe, Scott W., Takahashi, Nozomi, Vandenabeele, Peter, Knight, Richard A., Levine, Arnold J., Melino, Gerry·2012·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1110977109PMC PMC3458363

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Abstract

p63 inhibits metastasis. Here, we show that p63 (both TAp63 and ΔNp63 isoforms) regulates expression of miR-205 in prostate cancer (PCa) cells, and miR-205 is essential for the inhibitory effects of p63 on markers of epithelial-mesenchymal transition (EMT), such as ZEB1 and vimentin. Correspondingly, the inhibitory effect of p63 on EMT markers and cell migration is reverted by anti-miR-205. p53 mutants inhibit expression of both p63 and miR-205, and the cell migration, in a cell line expressing endogenous mutated p53, can be abrogated by pre-miR-205 or silencing of mutated p53. In accordance with this in vitro data, ΔNp63 or miR-205 significantly inhibits the incidence of lung metastasis in vivo in a mouse tail vein model. Similarly, one or both components of the p63/miR-205 axis were absent in metastases or colonized lymph nodes in a set of 218 human prostate cancer samples. This was confirmed in an independent clinical data set of 281 patients. Loss of this axis was associated with higher Gleason scores, an increased likelihood of metastatic and infiltration events, and worse prognosis. These data suggest that p63/miR-205 may be a useful clinical predictor of metastatic behavior in prostate cancer.

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Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978969
Additional file 5 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978984
Additional file 2 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978975
Additional file 6 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978987
Additional file 8 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978993
Additional file 9 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978996
Additional file 7 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978990
Additional file 4 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978981
Additional file 2 of LncRNA MIR205HG accelerates cell proliferation, migration and invasion in hepatoblastoma through the activation of MAPK signaling pathway and PI3K/AKT signaling pathway
Zhang, W., Liang, F., Li, Q., Sun, H., Li, F., Jiao, Z., & Lei, J. (2022) · Figshare · doi:10.6084/m9.figshare.18071035
Additional file 3 of ERK3 is transcriptionally upregulated by ∆Np63α and mediates the role of ∆Np63α in suppressing cell migration in non-melanoma skin cancers
Alshammari, E. S., Aljagthmi, A. A., Stacy, A. J., Bottomley, M., Shamma, H. N., Kadakia, M. P., & Long, W. (2021) · Figshare · doi:10.6084/m9.figshare.13978978
Additional file 3 of LncRNA MIR205HG accelerates cell proliferation, migration and invasion in hepatoblastoma through the activation of MAPK signaling pathway and PI3K/AKT signaling pathway
Zhang, W., Liang, F., Li, Q., Sun, H., Li, F., Jiao, Z., & Lei, J. (2022) · Figshare · doi:10.6084/m9.figshare.18071038
Mécanismes épigénétiques associés à la progression et à la chimiorésistance des sarcomes osseux
Jacques, C. (2016) · theses.fr (ABES) · doi:10.70675/6683be42z2eb1z41f0z9807z56236b95837b
Caractérisation moléculaire et immunité des cancers du sein triple-négatifs
Bonsang‐Kitzis, H. (2018) · theses.fr (ABES) · doi:10.70675/285c912cz8251z4099z9cf7ze121cd7350d0
Rôle de la surexpression des flotillines dans l'activation de voie de signalisation oncogéniques induisant la transition épithélio-mésenchymateuse
Genest, M. (2019) · theses.fr (ABES) · doi:10.70675/6205aed7zc520z4b11z8e40z67496f353e4b
TP63 expression correlates with mesenchymal-like gene signature in patient-derived recurrent glioblastoma cells
Martell, E., Kuzmychova, H., Grewal, A., Chawla, U., Jain, C., Venugopal, C., Anderson, C. M., Singh, S. K., & Sharif, T. (2026) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2026.153934
ZEB1 orchestrates cellular plasticity and therapy resistance in prostate cancer: From molecular mechanisms to clinical targeting
Wang, Q., Wang, J., Zhao, Y., Yan, J., Zhang, Y., Liu, Z., Zhao, Z., & Yu, H. (2026) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2026.105543
MicroRNAs in the Development and Progression of Prostate Cancer
Nadiminty, N., Tummala, R., & Gao, A. C. (2014) · Springer eBooks · doi:10.1007/978-1-4899-8065-6_14

Authors: Tucci, P., Agostini, M., Grespi, F., Markert, E. K., Terrinoni, A., Vousden, K. H., Muller, P. A. J., Dötsch, V., Kehrloesser, S., Sayan, B. S., Giaccone, G., Lowe, S. W., Takahashi, N., Vandenabeele, P., Knight, R. A., Levine, A. J., & Melino, G.
Affiliations: University of Leicester (GB)
Institute for Advanced Study (US)
University of Rome Tor Vergata (IT)
Cancer Research UK Scotland Institute (GB)
Goethe University Frankfurt (DE)
University of Southampton (GB)
National Institutes of Health (US)
Memorial Sloan Kettering Cancer Center (US)
Vlaams Instituut voor Biotechnologie (BE)
ORCID: Tucci, Paola
Agostini, Massimiliano
Grespi, Francesca
Terrinoni, Alessandro
Vousden, Karen H.
Muller, Patricia A. J.
Dötsch, Volker
Kehrloesser, Sebastian
Sayan, Berna S.
Giaccone, Giuseppe
Lowe, Scott W.
Takahashi, Nozomi
Vandenabeele, Peter
Knight, Richard A.
Levine, Arnold J.
Melino, Gerry
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2012-09-04
Volume: 109
Issue: 38
Pages: 15312-15317
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1110977109
PMC: PMC3458363
OpenAlex: W2113645544
Cited by: 286
References: 28
Citations by year: 2026: 4 · 2025: 6 · 2024: 11 · 2023: 14 · 2022: 12 · 2021: 20 · 2020: 17 · 2019: 15 · 2018: 18 · 2017: 19 · 2016: 37 · 2015: 30 · 2014: 41 · 2013: 36 · 2012: 6
FWCI: 12.00
Type: journal article
Language: en
Update notices: correction (2014-01-17)
Open access: bronze
doi.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
University of Salford Institutional Repository (University of Salford) (submittedVersion, cc-by)
Ghent University Academic Bibliography (Ghent University) (submittedVersion)
Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
Durham Research Online (Durham University) (submittedVersion, cc-by)
Archive of Doctoral Theses and Digital Collections (University of Calabria) (submittedVersion)
Research Explorer (The University of Manchester) (submittedVersion)
Funders: Ministero della Salute
Vlaams Instituut voor Biotechnologie
Associazione Italiana per la Ricerca sul Cancro (2008-2010_33-08)
Vlaamse regering
Alleanza Contro il Cancro
Medical Research Council (ACC12)
National Cancer Institute (P01CA087497, P01CA87497.)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Prostate Cancer Treatment and Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
Keywords: p63, miR-205, prostate cancer, metastasis, cell migration, epithelial-mesenchymal transition, ZEB1, vimentin, TP53 mutation, ΔNp63, TAp63, lung metastasis, lymph node metastasis, Gleason score, prognostic factors
MeSH terms: Animals, Cell Movement, Humans, Male, Mice, Inbred BALB C, Mutation, Neoplasm Metastasis, Neoplasm Transplantation, Phosphoproteins, Prostatic Neoplasms, Transcription Factors, Biomarkers, Tumor, Trans-Activators, Gene Expression Regulation, Neoplastic, Protein Isoforms, Gene Expression Profiling, Tumor Suppressor Proteins, MicroRNAs, Cell Line, Tumor, Cell Proliferation, Mice, Epithelial-Mesenchymal Transition

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Loss of p63 and its microRNA-205 target results in enhanced cell migration and metastasis in prostate cancer

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