The University of Southampton
University of Southampton Institutional Repository

PIP4K2B is mechanoresponsive and controls heterochromatin-driven nuclear softening through UHRF1

PIP4K2B is mechanoresponsive and controls heterochromatin-driven nuclear softening through UHRF1
PIP4K2B is mechanoresponsive and controls heterochromatin-driven nuclear softening through UHRF1
Phosphatidylinositol-5-phosphate (PtdIns5P)-4-kinases (PIP4Ks) are stress-regulated phosphoinositide kinases able to phosphorylate PtdIns5P to PtdIns(4,5)P2. In cancer patients their expression is typically associated with bad prognosis. Among the three PIP4K isoforms expressed in mammalian cells, PIP4K2B is the one with more prominent nuclear localisation. Here, we unveil the role of PIP4K2B as a mechanoresponsive enzyme. PIP4K2B protein level strongly decreases in cells growing on soft substrates. Its direct silencing or pharmacological inhibition, mimicking cell response to softness, triggers a concomitant reduction of the epigenetic regulator UHRF1 and induces changes in nuclear polarity, nuclear envelope tension and chromatin compaction. This substantial rewiring of the nucleus mechanical state drives YAP cytoplasmic retention and impairment of its activity as transcriptional regulator, finally leading to defects in cell spreading and motility. Since YAP signalling is essential for initiation and growth of human malignancies, our data suggest that potential therapeutic approaches targeting PIP4K2B could be beneficial in the control of the altered mechanical properties of cancer cells.
humans 1-phosphatidylinositol 4-kinase/metabolism CCAAT-Enhancer-Binding Proteins/genetics/metabolism Cell Nucleus/metabolism *Heterochromatin/genetics/metabolism *Neoplasms/metabolism Phosphatidylinositol Phosphates/metabolism Protein Isoforms/metabolism Signal Transduction Ubiquitin-Protein Ligases/genetics/metabolism
2041-1723
Poli, A.
e856efa4-09b7-41fc-a169-0a1f9eb9bdab
Pennacchio, F.A.
57ba5508-d0bb-4db1-beb5-2af5dc682765
Ghisleni, A.
ea429676-8225-4053-b8c9-841a065434fa
di Gennaro, M.
d059211d-85b2-4b66-97c0-4e42f6dc6238
Lecacheur, M.
059f6d98-5da2-4d76-baef-3916533f23e9
Nastaly, P.
bcd936a2-ae12-45bc-99db-0db4b2360437
Crestani, M.
71c9f6cb-9853-4fc8-ba6b-60f59032e70a
Pramotton, F.M.
5036bac8-34ec-4dfb-89a5-c252e9d95645
Iannelli, F.
0a415730-38ec-484e-81f3-a7a17d765619
Beznusenko, G.
e3a137b7-bb2f-4f0e-83a4-e42a06a09bf5
Mironov, A. A
d0e39c34-f3c2-4549-bbee-198d0fc63b16
Panzetta, V.
8a5b18bc-af9c-4ac2-99ee-2eece5a8b478
Fusco, S.
693ce1c4-3f73-4e24-b12b-09e03fdfb9b7
Sheth, B.
2ca6ed58-a992-47b7-b3a5-3c5df82aada7
Poulikakos, D.
3df3e2fa-857c-420d-9454-450bea151d4d
Ferrari, A.
4033f6b5-95d4-4c7f-85cc-ba842df65518
Gauthier, N.
3b303bbf-42de-4e42-84df-2a05c04ee559
Netti, P.A.
617c95b4-4f6d-41b0-9ebf-297fc3176acc
Divecha, N.
5c2ad0f8-4ce7-405f-8a15-2fc4ab96d787
Maiuri, P.
27a46229-37f8-49b3-9f1a-eb42865ea7c4
Poli, A.
e856efa4-09b7-41fc-a169-0a1f9eb9bdab
Pennacchio, F.A.
57ba5508-d0bb-4db1-beb5-2af5dc682765
Ghisleni, A.
ea429676-8225-4053-b8c9-841a065434fa
di Gennaro, M.
d059211d-85b2-4b66-97c0-4e42f6dc6238
Lecacheur, M.
059f6d98-5da2-4d76-baef-3916533f23e9
Nastaly, P.
bcd936a2-ae12-45bc-99db-0db4b2360437
Crestani, M.
71c9f6cb-9853-4fc8-ba6b-60f59032e70a
Pramotton, F.M.
5036bac8-34ec-4dfb-89a5-c252e9d95645
Iannelli, F.
0a415730-38ec-484e-81f3-a7a17d765619
Beznusenko, G.
e3a137b7-bb2f-4f0e-83a4-e42a06a09bf5
Mironov, A. A
d0e39c34-f3c2-4549-bbee-198d0fc63b16
Panzetta, V.
8a5b18bc-af9c-4ac2-99ee-2eece5a8b478
Fusco, S.
693ce1c4-3f73-4e24-b12b-09e03fdfb9b7
Sheth, B.
2ca6ed58-a992-47b7-b3a5-3c5df82aada7
Poulikakos, D.
3df3e2fa-857c-420d-9454-450bea151d4d
Ferrari, A.
4033f6b5-95d4-4c7f-85cc-ba842df65518
Gauthier, N.
3b303bbf-42de-4e42-84df-2a05c04ee559
Netti, P.A.
617c95b4-4f6d-41b0-9ebf-297fc3176acc
Divecha, N.
5c2ad0f8-4ce7-405f-8a15-2fc4ab96d787
Maiuri, P.
27a46229-37f8-49b3-9f1a-eb42865ea7c4

Poli, A., Pennacchio, F.A., Ghisleni, A., di Gennaro, M., Lecacheur, M., Nastaly, P., Crestani, M., Pramotton, F.M., Iannelli, F., Beznusenko, G., Mironov, A. A, Panzetta, V., Fusco, S., Sheth, B., Poulikakos, D., Ferrari, A., Gauthier, N., Netti, P.A., Divecha, N. and Maiuri, P. (2023) PIP4K2B is mechanoresponsive and controls heterochromatin-driven nuclear softening through UHRF1. Nature Communications, 14 (1), [1432]. (doi:10.1038/s41467-023-37064-0).

Record type: Article

Abstract

Phosphatidylinositol-5-phosphate (PtdIns5P)-4-kinases (PIP4Ks) are stress-regulated phosphoinositide kinases able to phosphorylate PtdIns5P to PtdIns(4,5)P2. In cancer patients their expression is typically associated with bad prognosis. Among the three PIP4K isoforms expressed in mammalian cells, PIP4K2B is the one with more prominent nuclear localisation. Here, we unveil the role of PIP4K2B as a mechanoresponsive enzyme. PIP4K2B protein level strongly decreases in cells growing on soft substrates. Its direct silencing or pharmacological inhibition, mimicking cell response to softness, triggers a concomitant reduction of the epigenetic regulator UHRF1 and induces changes in nuclear polarity, nuclear envelope tension and chromatin compaction. This substantial rewiring of the nucleus mechanical state drives YAP cytoplasmic retention and impairment of its activity as transcriptional regulator, finally leading to defects in cell spreading and motility. Since YAP signalling is essential for initiation and growth of human malignancies, our data suggest that potential therapeutic approaches targeting PIP4K2B could be beneficial in the control of the altered mechanical properties of cancer cells.

Text
s41467-023-37064-0 - Version of Record
Available under License Creative Commons Attribution.
Download (3MB)

More information

Accepted/In Press date: 23 February 2023
e-pub ahead of print date: 14 March 2023
Published date: 14 March 2023
Additional Information: Funding Information: This project was supported by Italian Association for Cancer Research (AIRC) Investigator Grant (Paolo Maiuri, #24976) and individual fellowship (Fabrizio A. Pennacchio, #23966). Alessandro Poli’s work was founded by Fondazione Umberto Veronesi Post-doctoral fellowships (#000359) and Short-EMBO Fellowship (#8386). Polish National Science Centre grant founded Paulina Nastaly (#2020/39/D/NZ3/00882). We thank Kristina Havas, Giorgio Scita and Simona Polo for suggestions and discussions. RNA-sequencing and RT-qPCR analyses were performed by Cogentech. The authors would like to also thank IFOM Imaging Facility for help with performing experiments, Dr. Carlos Nino for help in setting the Ubiquitination assay, Giorgio Scita’s group for providing pCDNA3.1_H2B-GFP, pBabe_H2B-mCherry, pLX304_YAP1-(S6A) ( https://doi.org/10.1073/pnas.1703096114 ) and pCSDEST2_NLS-GFP, Kristina Havas’ team for providing hydrogel preparation protocols and PI5P, and Maria Cristina Patroni Griffi for concept visualisation of Fig. (mariacristina.patronigriffi@gmail.com).
Keywords: humans 1-phosphatidylinositol 4-kinase/metabolism CCAAT-Enhancer-Binding Proteins/genetics/metabolism Cell Nucleus/metabolism *Heterochromatin/genetics/metabolism *Neoplasms/metabolism Phosphatidylinositol Phosphates/metabolism Protein Isoforms/metabolism Signal Transduction Ubiquitin-Protein Ligases/genetics/metabolism

Identifiers

Local EPrints ID: 478674
URI: http://eprints.soton.ac.uk/id/eprint/478674
ISSN: 2041-1723
PURE UUID: 885c5f6b-44cb-4eaf-a87f-005ac5a81c59

Catalogue record

Date deposited: 07 Jul 2023 16:30
Last modified: 17 Mar 2024 03:00

Export record

Altmetrics

Contributors

Author: A. Poli
Author: F.A. Pennacchio
Author: A. Ghisleni
Author: M. di Gennaro
Author: M. Lecacheur
Author: P. Nastaly
Author: M. Crestani
Author: F.M. Pramotton
Author: F. Iannelli
Author: G. Beznusenko
Author: A. A Mironov
Author: V. Panzetta
Author: S. Fusco
Author: B. Sheth
Author: D. Poulikakos
Author: A. Ferrari
Author: N. Gauthier
Author: P.A. Netti
Author: N. Divecha
Author: P. Maiuri

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of http://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×