Identification of intracellular cavin target proteins reveals cavin-PP1alpha interactions regulate apoptosis.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
22 07 2019
Historique:
received: 29 04 2018
accepted: 14 06 2019
entrez: 24 7 2019
pubmed: 25 7 2019
medline: 18 12 2019
Statut: epublish

Résumé

Caveolae are specialized domains of the plasma membrane. Formation of these invaginations is dependent on the expression of Caveolin-1 or -3 and proteins of the cavin family. In response to stress, caveolae disassemble and cavins are released from caveolae, allowing cavins to potentially interact with intracellular targets. Here, we describe the intracellular (non-plasma membrane) cavin interactome using biotin affinity proteomics and mass spectrometry. We validate 47 potential cavin-interactor proteins using a cell-free expression system and protein-protein binding assays. These data, together with pathway analyses, reveal unknown roles for cavin proteins in metabolism and stress signaling. We validated the interaction between one candidate interactor protein, protein phosphatase 1 alpha (PP1α), and Cavin-1 and -3 and show that UV treatment causes release of Cavin3 from caveolae allowing interaction with, and inhibition of, PP1α. This interaction increases H2AX phosphorylation to stimulate apoptosis, identifying a pro-apoptotic signaling pathway from surface caveolae to the nucleus.

Identifiants

pubmed: 31332168
doi: 10.1038/s41467-019-11111-1
pii: 10.1038/s41467-019-11111-1
pmc: PMC6646387
doi:

Substances chimiques

CAVIN1 protein, human 0
CAVIN3 protein, human 0
H2AX protein, human 0
Histones 0
Intracellular Signaling Peptides and Proteins 0
RNA-Binding Proteins 0
Protein Phosphatase 1 EC 3.1.3.16

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3279

Références

Proc Natl Acad Sci U S A. 2010 Apr 13;107(15):6870-5
pubmed: 20351298
Cardiovasc Hematol Disord Drug Targets. 2014;14(2):142-8
pubmed: 24801727
Cell Mol Life Sci. 2009 Apr;66(8):1467-78
pubmed: 19266163
Chem Biol. 2009 Apr 24;16(4):365-71
pubmed: 19389623
Oncogene. 2002 Apr 4;21(15):2365-75
pubmed: 11948420
J Proteomics. 2016 Oct 21;149:3-6
pubmed: 27084685
Glycoconj J. 2010 Oct;27(7-9):723-34
pubmed: 19823931
EMBO Rep. 2018 Sep;19(9):
pubmed: 30021837
Acta Obstet Gynecol Scand. 2010 May;89(5):629-35
pubmed: 20423276
EMBO J. 2009 Apr 22;28(8):1001-15
pubmed: 19262564
Oncogene. 2006 Sep 7;25(40):5517-26
pubmed: 16619035
J Cell Sci. 2002 Jan 15;115(Pt 2):241-56
pubmed: 11839776
Biotechnol Bioeng. 2016 Feb;113(2):292-300
pubmed: 26301602
Front Oncol. 2013 Jan 31;3:8
pubmed: 23386996
Nat Biotechnol. 2009 Aug;27(8):747-52
pubmed: 19648909
Cell Cycle. 2010 Dec 15;9(24):4908-21
pubmed: 21150319
Biochem Biophys Res Commun. 2004 Oct 29;323(4):1313-20
pubmed: 15451440
Mol Cell Proteomics. 2014 Sep;13(9):2233-45
pubmed: 24866125
J Cell Biochem. 2003 Oct 1;90(2):327-38
pubmed: 14505349
Elife. 2013 Sep 24;2:e00905
pubmed: 24069528
Cancer Res. 2001 Nov 1;61(21):7943-9
pubmed: 11691816
Biochem J. 1990 Aug 1;269(3):729-34
pubmed: 2390065
Cancer Biother Radiopharm. 2014 Aug;29(6):257-64
pubmed: 25003799
Transl Cancer Res. 2013;2(3):107-129
pubmed: 24058901
Oncotarget. 2015 Nov 10;6(35):37135-50
pubmed: 26431273
Interface Focus. 2013 Oct 6;3(5):20130018
pubmed: 24511386
Nat Rev Cancer. 2016 Jan;16(1):20-33
pubmed: 26678314
FEBS J. 2013 Jan;280(2):596-611
pubmed: 22284538
Physiol Rev. 2004 Jan;84(1):1-39
pubmed: 14715909
Cell. 2013 Aug 1;154(3):704-704.e1
pubmed: 23911330
Transl Res. 2014 Nov;164(5):366-91
pubmed: 25090308
J Proteome Res. 2007 Mar;6(3):1165-75
pubmed: 17274640
Cell. 2011 Feb 4;144(3):402-13
pubmed: 21295700
Nat Cell Biol. 2009 Jul;11(7):807-14
pubmed: 19525939
Mutagenesis. 2009 Mar;24(2):161-7
pubmed: 19064695
Cell Res. 2011 Jul;21(7):1088-101
pubmed: 21445100
Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3080-5
pubmed: 11248035
Breast Cancer Res Treat. 2010 Feb;119(3):575-91
pubmed: 19288272
Cell. 2008 Jan 11;132(1):113-24
pubmed: 18191225
Mol Cell Proteomics. 2015 Nov;14(11):2848-56
pubmed: 26355100
Methods Mol Biol. 2012;920:613-26
pubmed: 22941631
Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5426-30
pubmed: 8202502
BMC Cancer. 2011 Feb 11;11:66
pubmed: 21314941
Nature. 2005 Jul 7;436(7047):128-33
pubmed: 16001074
Jpn J Cancer Res. 1990 Dec;81(12):1272-80
pubmed: 2177460
Elife. 2016 Aug 16;5:
pubmed: 27528195
J Cell Biol. 1998 May 4;141(3):601-10
pubmed: 9566962
Methods. 2011 Sep;55(1):58-64
pubmed: 21704167
Mol Biol Cell. 2015 Oct 15;26(20):3561-9
pubmed: 26269585
Mol Cell Proteomics. 2012 Feb;11(2):M111.012245
pubmed: 22030351
Cell Cycle. 2004 Oct;3(10):1312-9
pubmed: 15467450
Int J Cancer. 2008 Apr 1;122(7):1573-84
pubmed: 18059034
Oncogene. 2014 May 22;33(21):2728-36
pubmed: 23770857
Cell Prolif. 2005 Aug;38(4):223-43
pubmed: 16098182
Biochem Biophys Res Commun. 2008 Nov 7;376(1):215-20
pubmed: 18778685
Oncogene. 2005 Sep 15;24(41):6249-55
pubmed: 15940253
Cell. 2000 Jan 7;100(1):57-70
pubmed: 10647931
Biochimie. 2014 Dec;107 Pt B:188-202
pubmed: 25241255
Biochimie. 2003 Aug;85(8):721-6
pubmed: 14585537
J Cell Sci. 2015 Apr 1;128(7):1269-78
pubmed: 25829513
Elife. 2013 Jan 01;3:e01434
pubmed: 24473072
J Cell Biol. 2012 Mar 19;196(6):801-10
pubmed: 22412018
PLoS One. 2014 Jul 18;9(7):e102935
pubmed: 25036884
EMBO Rep. 2012 Dec;13(12):1138-44
pubmed: 23079727
Methods Mol Biol. 2014;1118:1-15
pubmed: 24395406
J Cell Biol. 2009 Jun 29;185(7):1259-73
pubmed: 19546242
PLoS One. 2016 Apr 28;11(4):e0154263
pubmed: 27123980
J Cell Biol. 2015 Aug 31;210(5):833-49
pubmed: 26323694
Epigenetics. 2009 May 16;4(4):255-64
pubmed: 19550145
Chem Asian J. 2010 Mar 1;5(3):410-20
pubmed: 20013999
Clin Cancer Res. 2011 Dec 15;17(24):7551-62
pubmed: 21980136
EMBO J. 1998 May 15;17(10):2855-64
pubmed: 9582279
Nucleic Acids Res. 2018 Nov 30;46(21):11381-11395
pubmed: 30335167
J Proteome Res. 2013 Feb 1;12(2):605-14
pubmed: 23214712
Nat Rev Mol Cell Biol. 2013 Feb;14(2):98-112
pubmed: 23340574

Auteurs

Kerrie-Ann McMahon (KA)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Yeping Wu (Y)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Yann Gambin (Y)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.
EMBL Australia Node in Single Molecule Science, Lowy Cancer Building, Level 3 Medical Sciences UNSW Kensington Campus, Sydney, NSW, 2052, Australia.

Emma Sierecki (E)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.
EMBL Australia Node in Single Molecule Science, Lowy Cancer Building, Level 3 Medical Sciences UNSW Kensington Campus, Sydney, NSW, 2052, Australia.

Vikas A Tillu (VA)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Thomas Hall (T)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Nick Martel (N)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Satomi Okano (S)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Shayli Varasteh Moradi (SV)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.
Science and Engineering Faculty, Earth, Environmental and Biological Sciences, Genetics & Biotechnology, Queensland University of Technology, Brisbane, QLD, 4000, Australia.

Jayde E Ruelcke (JE)

The University of Queensland Diamantina Institute, Faculty of Medicine, The University of Queensland, Translational Research Institute, Brisbane, QLD, 4102, Australia.

Charles Ferguson (C)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Alpha S Yap (AS)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.

Kirill Alexandrov (K)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia.
Institute for Future Environments, IFE Centres, CTCB Centre Office, Queensland University of Technology, Brisbane, QLD, 4000, Australia.

Michelle M Hill (MM)

The University of Queensland Diamantina Institute, Faculty of Medicine, The University of Queensland, Translational Research Institute, Brisbane, QLD, 4102, Australia.

Robert G Parton (RG)

The University of Queensland, Institute for Molecular Bioscience, Brisbane, QLD, 4072, Australia. r.parton@imb.uq.edu.au.
The University of Queensland, Centre for Microscopy and Microanalysis, Brisbane, QLD, 4072, Australia. r.parton@imb.uq.edu.au.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH