NUAK1 promotes organ fibrosis via YAP and TGF-β/SMAD signaling

Tianzhou Zhang1, Xiaolin He1, Lauren Caldwell2, Santosh Kumar Goru1, Luisa Ulloa Severino1, Monica F. Tolosa1, Paraish S. Misra1, Caitríona M. McEvoy1, Tania Christova3, Yong Liu4, Cassandra Atin1, Johnny Zhang1, Catherine Hu1, Noah Vukosa1, Xiaolan Chen1, Adriana Krizova5, Anish Kirpalani6, Alex Gregorieff2, Ruoyu Ni2, Kin Chan2, Mandeep Gill3, Liliana Attisano3, Jeffrey L. Wrana2, Darren A. Yuen1
1Keenan Research Centre for Biomedical Science, Li Ka Shing Knowledge Institute, St. Michael’s Hospital (Unity Health Toronto) and Department of Medicine, University of Toronto, Toronto, Ontario M5B 1T8, Canada.
2Center for Systems Biology, Lunenfeld-Tanenbaum Research Institute, Mt. Sinai Hospital and Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5G 1X5, Canada.
3Donnelly Centre and Department of Biochemistry, University of Toronto, Toronto, Ontario M5S 1A8, Canada.
4Ontario Institute of Cancer Research, Toronto, Ontario M5G OA3, Canada.
5Department of Laboratory Medicine and Pathobiology, School of Graduate Studies, University of Toronto, Toronto, Ontario M5S 1A8, Canada.
6Department of Medical Imaging, St. Michael’s Hospital (Unity Health Toronto) and University of Toronto, Toronto, Ontario M5B 1W8, Canada.

Tóm tắt

Fibrosis is a central pathway that drives progression of multiple chronic diseases, yet few safe and effective clinical antifibrotic therapies exist. In most fibrotic disorders, transforming growth factor–β (TGF-β)–driven scarring is an important pathologic feature and a key contributor to disease progression. Yes-associated protein (YAP) and transcriptional coactivator with PDZ-binding motif (TAZ) are two closely related transcription cofactors that are important for coordinating fibrogenesis after organ injury, but how they are activated in response to tissue injury has, so far, remained unclear. Here, we describe NUAK family kinase 1 (NUAK1) as a TGF-β–inducible profibrotic kinase that is up-regulated in multiple fibrotic organs in mice and humans. Mechanistically, we show that TGF-β induces a rapid increase in NUAK1 in fibroblasts. NUAK1, in turn, can promote profibrotic YAP and TGF-β/SMAD signaling, ultimately leading to organ scarring. Moreover, activated YAP and TAZ can induce further NUAK1 expression, creating a profibrotic positive feedback loop that enables persistent fibrosis. Using mouse models of kidney, lung, and liver fibrosis, we demonstrate that this fibrogenic signaling loop can be interrupted via fibroblast-specific loss of NUAK1 expression, leading to marked attenuation of fibrosis. Pharmacologic NUAK1 inhibition also reduced scarring, either when initiated immediately after injury or when initiated after fibrosis was already established. Together, our data suggest that NUAK1 plays a critical, previously unrecognized role in fibrogenesis and represents an attractive target for strategies that aim to slow fibrotic disease progression.

Từ khóa


Tài liệu tham khảo

10.1172/JCI31487

10.1056/NEJMra1300575

10.1681/ASN.2005070757

10.1038/ki.2008.350

10.1056/NEJM199411103311907

10.1172/JCI115821

10.1096/fj.03-1273rev

10.1681/ASN.2015050499

10.1016/j.ajpath.2015.08.011

10.1681/ASN.2015121354

10.1167/iovs.18-24258

10.1152/ajplung.00300.2014

10.1016/j.jhep.2015.04.011

10.1038/nature10137

10.1038/ncb1748

10.1016/j.devcel.2010.11.012

10.1038/ncomms11642

10.1038/srep42595

10.1096/fj.201700722R

10.1111/ajt.14107

10.1080/14728222.2017.1370455

10.1038/mt.2016.109

10.1183/23120541.00138-2016

10.1101/gad.1653708

10.1038/srep46565

D. F. Higgins, K. Kimura, W. M. Bernhardt, N. Shrimanker, Y. Akai, B. Hohenstein, Y. Saito, R. S. Johnson, M. Kretzler, C. D. Cohen, K. U. Eckardt, M. Iwano, V. H. Haase, Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J. Clin. Invest. 117, 3810–3820 (2007).

10.1038/s41467-018-07987-0

E. P. Bottinger W. Ju in Smad Signal Transduction: Proteins and Cell Regulation P. Dijke C. H. Heldin Eds. (Springer 2006) pp. 335–360.

10.1074/jbc.RA118.004984

10.1038/ncb3216

10.1016/S0002-9440(10)61108-X

10.1371/journal.pgen.1003380

10.1016/j.celrep.2013.11.021

10.1161/01.RES.88.1.30

10.1111/j.0022-202X.2005.23750.x

10.1016/j.canlet.2006.02.019

10.1126/scisignal.2004712

10.1038/s41467-018-07394-5

10.1042/BJ20131152

10.1074/jbc.M117.780502

10.1007/s00467-011-1938-2

10.1038/nm.3282

10.1016/j.stem.2014.11.004

10.1242/dev.045500

10.1101/gad.1602907

10.1016/S0092-8674(03)00549-X

10.1038/ncb3113

10.1038/ncb3111

10.1016/j.celrep.2014.09.036

10.15252/embj.201490379

10.1016/j.cell.2012.06.037

10.1016/j.cell.2013.07.042

10.1038/emboj.2011.157

10.1242/dev.070987

10.1038/emboj.2009.342

10.1038/s41467-018-05939-2

10.1172/jci.insight.146243

H. Wickham ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag 2016).

10.1038/nature08460

10.1016/j.neuron.2016.09.022

10.1681/ASN.2012090890

10.1189/jlb.0609391

10.1371/journal.pone.0009543

10.1002/stem.1502

10.2337/db11-1365

10.1136/jcp.41.4.467

10.1126/scitranslmed.aau6296