The RNA-Protein Interactome of Differentiated Kidney Tubular Epithelial Cells.


Journal

Journal of the American Society of Nephrology : JASN
ISSN: 1533-3450
Titre abrégé: J Am Soc Nephrol
Pays: United States
ID NLM: 9013836

Informations de publication

Date de publication:
04 2019
Historique:
received: 09 09 2018
accepted: 20 01 2019
pubmed: 15 3 2019
medline: 19 12 2019
entrez: 15 3 2019
Statut: ppublish

Résumé

RNA-binding proteins (RBPs) are fundamental regulators of cellular biology that affect all steps in the generation and processing of RNA molecules. Recent evidence suggests that regulation of RBPs that modulate both RNA stability and translation may have a profound effect on the proteome. However, regulation of RBPs in clinically relevant experimental conditions has not been studied systematically. We used RNA interactome capture, a method for the global identification of RBPs to characterize the global RNA-binding proteome (RBPome) associated with polyA-tailed RNA species in murine ciliated epithelial cells of the inner medullary collecting duct. To study regulation of RBPs in a clinically relevant condition, we analyzed hypoxia-associated changes of the RBPome. We identified >1000 RBPs that had been previously found using other systems. In addition, we found a number of novel RBPs not identified by previous screens using mouse or human cells, suggesting that these proteins may be specific RBPs in differentiated kidney epithelial cells. We also found quantitative differences in RBP-binding to mRNA that were associated with hypoxia versus normoxia. These findings demonstrate the regulation of RBPs through environmental stimuli and provide insight into the biology of hypoxia-response signaling in epithelial cells in the kidney. A repository of the RBPome and proteome in kidney tubular epithelial cells, derived from our findings, is freely accessible online, and may contribute to a better understanding of the role of RNA-protein interactions in kidney tubular epithelial cells, including the response of these cells to hypoxia.

Sections du résumé

BACKGROUND
RNA-binding proteins (RBPs) are fundamental regulators of cellular biology that affect all steps in the generation and processing of RNA molecules. Recent evidence suggests that regulation of RBPs that modulate both RNA stability and translation may have a profound effect on the proteome. However, regulation of RBPs in clinically relevant experimental conditions has not been studied systematically.
METHODS
We used RNA interactome capture, a method for the global identification of RBPs to characterize the global RNA-binding proteome (RBPome) associated with polyA-tailed RNA species in murine ciliated epithelial cells of the inner medullary collecting duct. To study regulation of RBPs in a clinically relevant condition, we analyzed hypoxia-associated changes of the RBPome.
RESULTS
We identified >1000 RBPs that had been previously found using other systems. In addition, we found a number of novel RBPs not identified by previous screens using mouse or human cells, suggesting that these proteins may be specific RBPs in differentiated kidney epithelial cells. We also found quantitative differences in RBP-binding to mRNA that were associated with hypoxia versus normoxia.
CONCLUSIONS
These findings demonstrate the regulation of RBPs through environmental stimuli and provide insight into the biology of hypoxia-response signaling in epithelial cells in the kidney. A repository of the RBPome and proteome in kidney tubular epithelial cells, derived from our findings, is freely accessible online, and may contribute to a better understanding of the role of RNA-protein interactions in kidney tubular epithelial cells, including the response of these cells to hypoxia.

Identifiants

pubmed: 30867249
pii: ASN.2018090914
doi: 10.1681/ASN.2018090914
pmc: PMC6442340
doi:

Substances chimiques

Proteome 0
RNA, Messenger 0
RNA-Binding Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

564-576

Informations de copyright

Copyright © 2019 by the American Society of Nephrology.

Références

Blood Adv. 2018 Feb 27;2(4):323-334
pubmed: 29444873
J Mol Biol. 2017 Oct 27;429(21):3139-3145
pubmed: 27693651
Kidney Int. 1997 Feb;51(2):381-5
pubmed: 9027710
Curr Pharm Des. 2009;15(33):3853-60
pubmed: 19671045
Nat Commun. 2015 Dec 03;6:10127
pubmed: 26632259
Nat Commun. 2017 Jan 30;8:14177
pubmed: 28134340
Ann N Y Acad Sci. 1994 Apr 15;718:72-81; discussion 81-2
pubmed: 8185253
Nature. 2012 May 06;486(7401):126-9
pubmed: 22678294
EMBO Mol Med. 2017 Jul;9(7):890-905
pubmed: 28500065
Nat Rev Mol Cell Biol. 2018 May;19(5):327-341
pubmed: 29339797
Nat Methods. 2016 Sep;13(9):731-40
pubmed: 27348712
Nat Biotechnol. 2011 Jul 07;29(8):731-4
pubmed: 21738127
Cell Rep. 2016 Aug 2;16(5):1456-1469
pubmed: 27452465
Trends Pharmacol Sci. 2012 Apr;33(4):207-14
pubmed: 22398146
Nucleic Acids Res. 2010 Apr;38(7):2332-45
pubmed: 20061373
Microrna. 2017;6(2):80-96
pubmed: 28294076
Cell. 2011 May 13;145(4):513-28
pubmed: 21565611
Crit Rev Biochem Mol Biol. 2014 Jan-Feb;49(1):1-15
pubmed: 24099156
Methods. 2014 Feb;65(3):302-9
pubmed: 24096003
Nucleic Acids Res. 2018 Jan 4;46(D1):D1271-D1281
pubmed: 29106664
Exp Neurol. 2014 Apr;254:29-40
pubmed: 24462670
Biochim Biophys Acta Gene Regul Mech. 2017 Oct;1860(10):1037-1046
pubmed: 28843785
Exp Cell Res. 2017 Jul 15;356(2):128-135
pubmed: 28336293
J Cell Biol. 2006 Nov 20;175(4):547-54
pubmed: 17101696
EMBO Rep. 2017 Sep;18(9):1521-1535
pubmed: 28710093
PLoS One. 2010 Nov 11;5(11):e15506
pubmed: 21085602
Nat Commun. 2016 May 13;7:11491
pubmed: 27173435
Nat Biotechnol. 2008 Dec;26(12):1367-72
pubmed: 19029910
Nat Biotechnol. 2009 Sep;27(9):851-7
pubmed: 19680244
Mol Cell Biol. 1987 Aug;7(8):2745-52
pubmed: 3670292
J Cell Sci. 2013 Mar 15;126(Pt 6):1355-65
pubmed: 23345402
Mol Cell. 2012 Jun 8;46(5):674-90
pubmed: 22681889
Methods Mol Biol. 2018;1649:405-417
pubmed: 29130213
Oncotarget. 2015 Jan 1;6(1):305-16
pubmed: 25622105
Acta Physiol (Oxf). 2018 Apr;222(4):e12999
pubmed: 29159875
FASEB J. 2017 Feb;31(2):457-468
pubmed: 27849555
Cell. 2010 Apr 2;141(1):129-41
pubmed: 20371350

Auteurs

Michael Ignarski (M)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Constantin Rill (C)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Rainer W J Kaiser (RWJ)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Madlen Kaldirim (M)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

René Neuhaus (R)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Reza Esmaillie (R)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Xinping Li (X)

Proteomics Core Facility, Max Planck Institute for Biology of Ageing, Cologne, Germany.

Corinna Klein (C)

Proteomics Facility, Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases.

Katrin Bohl (K)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Maike Petersen (M)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Christian K Frese (CK)

Proteomics Facility, Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases.

Martin Höhne (M)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Ilian Atanassov (I)

Proteomics Core Facility, Max Planck Institute for Biology of Ageing, Cologne, Germany.

Markus M Rinschen (MM)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Katja Höpker (K)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Bernhard Schermer (B)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.
Nephrolab, Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases, Faculty of Medicine and University Hospital Cologne, and.
Systems Biology of Ageing Cologne, University of Cologne, Cologne, Germany.

Thomas Benzing (T)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.
Nephrolab, Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases, Faculty of Medicine and University Hospital Cologne, and.
Systems Biology of Ageing Cologne, University of Cologne, Cologne, Germany.

Christoph Dieterich (C)

Department of Internal Medicine III, Klaus Tschira Institute for Integrative Computational Cardiology, University Hospital Heidelberg, Heidelberg, Germany; and.
German Center for Cardiovascular Research (DZHK)-Partner site, Heidelberg/Mannheim, Germany.

Francesca Fabretti (F)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany.

Roman-Ulrich Müller (RU)

Department II of Internal Medicine and Center for Molecular Medicine Cologne, University of Cologne, Faculty of Medicine and University Hospital of Cologne, Cologne, Germany; roman-ulrich.mueller@uk-koeln.de.
Nephrolab, Cologne Excellence Cluster on Cellular Stress Responses in Aging-associated Diseases, Faculty of Medicine and University Hospital Cologne, and.
Systems Biology of Ageing Cologne, University of Cologne, Cologne, Germany.

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