The cellular prion protein is a stress protein secreted by renal tubular cells and a urinary marker of kidney injury.


Journal

Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092

Informations de publication

Date de publication:
17 04 2020
Historique:
received: 28 01 2020
accepted: 19 03 2020
revised: 19 03 2020
entrez: 19 4 2020
pubmed: 19 4 2020
medline: 1 4 2021
Statut: epublish

Résumé

Endoplasmic Reticulum (ER) stress underlies the pathogenesis of numerous kidney diseases. A better care of patients with kidney disease involves the identification and validation of ER stress biomarkers in the early stages of kidney disease. For the first time to our knowledge, we demonstrate that the prion protein PrP

Identifiants

pubmed: 32303684
doi: 10.1038/s41419-020-2430-3
pii: 10.1038/s41419-020-2430-3
pmc: PMC7165184
doi:

Substances chimiques

Biomarkers 0
Prion Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

243

Références

Chovatiya, R. & Medzhitov, R. Stress, inflammation, and defense of homeostasis. Mol. Cell 54, 281–288 (2014).
pubmed: 24766892 pmcid: 4048989 doi: 10.1016/j.molcel.2014.03.030
Duffield, J. S. Cellular and molecular mechanisms in kidney fibrosis. J. Clin. Invest 124, 2299–2306 (2014).
pubmed: 24892703 pmcid: 4038570 doi: 10.1172/JCI72267
Ferenbach, D. A. & Bonventre, J. V. Mechanisms of maladaptive repair after AKI leading to accelerated kidney ageing and CKD. Nat. Rev. Nephrol. 11, 264–276 (2015).
pubmed: 25643664 pmcid: 4412815 doi: 10.1038/nrneph.2015.3
Fedeles, S. V. et al. Sec63 and Xbp1 regulate IRE1alpha activity and polycystic disease severity. J. Clin. Invest 125, 1955–1967 (2015).
pubmed: 25844898 pmcid: 4463201 doi: 10.1172/JCI78863
Shao, D. et al. Suppression of XBP1S mediates high glucose-induced oxidative stress and extracellular matrix synthesis in renal mesangial cell and kidney of diabetic rats. PLoS ONE 8, e56124 (2013).
pubmed: 23457509 pmcid: 3573021 doi: 10.1371/journal.pone.0056124
Madhusudhan, T. et al. Defective podocyte insulin signalling through p85-XBP1 promotes ATF6-dependent maladaptive ER-stress response in diabetic nephropathy. Nat. Commun. 6, 6496 (2015).
pubmed: 25754093 pmcid: 4366504 doi: 10.1038/ncomms7496
Kaufman, D. R., Papillon, J., Larose, L., Iwawaki, T. & Cybulsky, A. V. Deletion of inositol-requiring enzyme-1alpha in podocytes disrupts glomerular capillary integrity and autophagy. Mol. Biol. Cell 28, 1636–1651 (2017).
pubmed: 28428258 pmcid: 5469607 doi: 10.1091/mbc.e16-12-0828
Ferre, S. et al. Renal tubular cell spliced X-box binding protein 1 (Xbp1s) has a unique role in sepsis-induced acute kidney injury and inflammation. Kidney Int 96, 1359–1373 (2019).
pubmed: 31601454 doi: 10.1016/j.kint.2019.06.023
Hirsch, T. Z., Martin-Lanneree, S. & Mouillet-Richard, S. Functions of the prion protein. Prog. Mol. Biol. Transl. Sci. 150, 1–34 (2017).
pubmed: 28838656 doi: 10.1016/bs.pmbts.2017.06.001
Pallet, N. et al. Rapamycin inhibits human renal epithelial cell proliferation: effect on cyclin D3 mRNA expression and stability. Kidney Int 67, 2422–2433 (2005).
pubmed: 15882288 doi: 10.1111/j.1523-1755.2005.00350.x
Mami, I. et al. Angiogenin mediates cell-autonomous translational control under endoplasmic reticulum stress and attenuates kidney injury. J. Am. Soc. Nephrol. 27, 863–876 (2016).
pubmed: 26195817 doi: 10.1681/ASN.2015020196
Fohlen, B. et al. Real-time and non-invasive monitoring of the activation of the ire1alpha-xbp1 pathway in individuals with hemodynamic impairment. EBioMedicine 27, 284–292 (2018).
pubmed: 29276149 doi: 10.1016/j.ebiom.2017.12.023
Amrhein, V., Greenland, S. & McShane, B. Scientists rise up against statistical significance. Nature 567, 305–307 (2019).
pubmed: 30894741 doi: 10.1038/d41586-019-00857-9
Leek, J. et al. Five ways to fix statistics. Nature 551, 557–559 (2017).
pubmed: 29189798 doi: 10.1038/d41586-017-07522-z
Nuzzo, R. Scientific method: statistical errors. Nature 506, 150–152 (2014).
doi: 10.1038/506150a
Tkacz, J. S. & Lampen, O. Tunicamycin inhibition of polyisoprenyl N-acetylglucosaminyl pyrophosphate formation in calf-liver microsomes. Biochem. Biophys. Res. Commun. 65, 248–257 (1975).
pubmed: 167767 doi: 10.1016/S0006-291X(75)80086-6
Misiewicz, M. et al. Identification of a novel endoplasmic reticulum stress response element regulated by XBP1. J. Biol. Chem. 288, 20378–20391 (2013).
pubmed: 23737521 pmcid: 3711304 doi: 10.1074/jbc.M113.457242
Dery, M. A. et al. Endoplasmic reticulum stress induces PRNP prion protein gene expression in breast cancer. Breast Cancer Res. 15, R22 (2013).
pubmed: 23497519 pmcid: 3672785 doi: 10.1186/bcr3398
Linsenmeier, L. et al. Diverse functions of the prion protein—does proteolytic processing hold the key? Biochim. Biophys. Acta Mol. Cell Res. 1864, 2128–2137 (2017).
pubmed: 28693923 doi: 10.1016/j.bbamcr.2017.06.022
Sarnataro, D., Pepe, A. & Zurzolo, C. Cell biology of prion protein. Prog. Mol. Biol. Transl. Sci. 150, 57–82 (2017).
pubmed: 28838675 doi: 10.1016/bs.pmbts.2017.06.018
Fujiwara, T., Oda, K., Yokota, S., Takatsuki, A. & Ikehara, Y. Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum. J. Biol. Chem. 263, 18545–18552 (1988).
pubmed: 3192548
Mami, I. et al. A novel extrinsic pathway for the unfolded protein response in the kidney. J. Am. Soc. Nephrol. 27, 2670–2683 (2016).
pubmed: 26823555 pmcid: 5004651 doi: 10.1681/ASN.2015060703
Maiti, N. R. & Surewicz, W. K. The role of disulfide bridge in the folding and stability of the recombinant human prion protein. J. Biol. Chem. 276, 2427–2431 (2001).
pubmed: 11069909 doi: 10.1074/jbc.M007862200
Ellgaard, L. & Helenius, A. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181–191 (2003).
pubmed: 12612637 doi: 10.1038/nrm1052
Yoo, J. et al. GlcNAc-1-P-transferase-tunicamycin complex structure reveals basis for inhibition of N-glycosylation. Nat. Struct. Mol. Biol. 25, 217–224 (2018).
pubmed: 29459785 pmcid: 5840018 doi: 10.1038/s41594-018-0031-y
Akella, N. M., Ciraku, L. & Reginato, M. J. Fueling the fire: emerging role of the hexosamine biosynthetic pathway in cancer. BMC Biol. 17, 52 (2019).
pubmed: 31272438 pmcid: 6610925 doi: 10.1186/s12915-019-0671-3
Han, J. et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 15, 481–490 (2013).
pubmed: 23624402 pmcid: 3692270 doi: 10.1038/ncb2738
Pallet, N. et al. A comprehensive characterization of membrane vesicles released by autophagic human endothelial cells. Proteomics 13, 1108–1120 (2013).
pubmed: 23436686 doi: 10.1002/pmic.201200531
Guillot-Sestier, M. V. & Checler, F. alpha-Secretase-derived cleavage of cellular prion yields biologically active catabolites with distinct functions. Neurodegener. Dis. 10, 294–297 (2012).
pubmed: 22261541 doi: 10.1159/000333804
El Karoui, K. et al. Endoplasmic reticulum stress drives proteinuria-induced kidney lesions via Lipocalin 2. Nat. Commun. 7, 10330 (2016).
pubmed: 26787103 pmcid: 4735759 doi: 10.1038/ncomms10330
Chawla, L. S., Eggers, P. W., Star, R. A. & Kimmel, P. L. Acute kidney injury and chronic kidney disease as interconnected syndromes. N. Engl. J. Med. 371, 58–66 (2014).
pubmed: 24988558 doi: 10.1056/NEJMra1214243
Devuyst, O. et al. Autosomal dominant tubulointerstitial kidney disease. Nat. Rev. Dis. Prim. 5, 60 (2019).
pubmed: 31488840 doi: 10.1038/s41572-019-0109-9
Dvela-Levitt, M. et al. Small molecule targets TMED9 and promotes lysosomal degradation to reverse proteinopathy. Cell 178, 521–535. e523 (2019).
pubmed: 31348885 doi: 10.1016/j.cell.2019.07.002
Dihazi, H. et al. Secretion of ERP57 is important for extracellular matrix accumulation and progression of renal fibrosis, and is an early sign of disease onset. J. Cell Sci. 126, 3649–3663 (2013).
pubmed: 23781031 doi: 10.1242/jcs.125088
Kim, Y. et al. Mesencephalic astrocyte-derived neurotrophic factor as a urine biomarker for endoplasmic reticulum stress-related kidney diseases. J. Am. Soc. Nephrol. 27, 2974–2982 (2016).
pubmed: 26940092 pmcid: 5042655 doi: 10.1681/ASN.2014100986
Tavernier, Q. et al. Urinary angiogenin reflects the magnitude of kidney injury at the infrahistologic level. J. Am. Soc. Nephrol. 28, 678–690 (2017).
pubmed: 27436854 doi: 10.1681/ASN.2016020218
Bonventre, J. V. Diagnosis of acute kidney injury: from classic parameters to new biomarkers. Contrib. Nephrol. 156, 213–219 (2007).
pubmed: 17464130 doi: 10.1159/000102086
Kim, Y. et al. Elevated urinary CRELD2 is associated with endoplasmic reticulum stress-mediated kidney disease. JCI Insight. https://doi.org/10.1172/jci.insight.92896 (2017).
Haldar, S. et al. Prion protein promotes kidney iron uptake via its ferrireductase activity. J. Biol. Chem. 290, 5512–5522 (2015).
pubmed: 25572394 pmcid: 4342466 doi: 10.1074/jbc.M114.607507
Zhang, B. et al. Prion protein protects against renal ischemia/reperfusion injury. PLoS ONE 10, e0136923 (2015).
pubmed: 26327228 pmcid: 4556704 doi: 10.1371/journal.pone.0136923
Mehrpour, M. & Codogno, P. Prion protein: from physiology to cancer biology. Cancer Lett. 290, 1–23 (2010).
pubmed: 19674833 doi: 10.1016/j.canlet.2009.07.009
Lopes, M. H. et al. Disruption of prion protein-HOP engagement impairs glioblastoma growth and cognitive decline and improves overall survival. Oncogene 34, 3305–3314 (2015).
pubmed: 25151961 doi: 10.1038/onc.2014.261
Provenzano, L. et al. Cellular prion protein (PrP(C)) in the development of Merlin-deficient tumours. Oncogene 36, 6132–6142 (2017).
pubmed: 28692055 doi: 10.1038/onc.2017.200
Du, L. et al. CD44-positive cancer stem cells expressing cellular prion protein contribute to metastatic capacity in colorectal cancer. Cancer Res. 73, 2682–2694 (2013).
pubmed: 23418321 doi: 10.1158/0008-5472.CAN-12-3759
de Lacerda, T. C. et al. Prion protein binding to HOP modulates the migration and invasion of colorectal cancer cells. Clin. Exp. Metastasis 33, 441–451 (2016).
pubmed: 27112151 doi: 10.1007/s10585-016-9788-8
Iglesia, R. P. et al. Engagement of cellular prion protein with the co-chaperone Hsp70/90 organizing protein regulates the proliferation of glioblastoma stem-like cells. Stem Cell Res. Ther. 8, 76 (2017).
pubmed: 28412969 pmcid: 5392955 doi: 10.1186/s13287-017-0518-1
Falke, L. L., Gholizadeh, S., Goldschmeding, R., Kok, R. J. & Nguyen, T. Q. Diverse origins of the myofibroblast-implications for kidney fibrosis. Nat. Rev. Nephrol. 11, 233–244 (2015).
pubmed: 25584804 doi: 10.1038/nrneph.2014.246

Auteurs

Yohan Bignon (Y)

INSERM U1138, Centre de Recherche des Cordeliers, INSERM, Sorbonne Université de Paris, F-75006, Paris, France.

Virginie Poindessous (V)

INSERM U1138, Centre de Recherche des Cordeliers, INSERM, Sorbonne Université de Paris, F-75006, Paris, France.

Hélène Lazareth (H)

Service de Néphrologie, Hôpital Européen Georges Pompidou, Assistance Publique Hôpitaux de Paris, Paris, France.

Bruno Passet (B)

Université Paris Saclay, INRAE, AgroparisTech, UMR1313, Génétique animale et biologie intégrative, F78350, Jouy-en-Josas, France.

Jean-Luc Vilotte (JL)

Université Paris Saclay, INRAE, AgroparisTech, UMR1313, Génétique animale et biologie intégrative, F78350, Jouy-en-Josas, France.

Fatima Djouadi (F)

INSERM U1138, Centre de Recherche des Cordeliers, INSERM, Sorbonne Université de Paris, F-75006, Paris, France.

Sophie Mouillet-Richard (S)

INSERM U1138, Centre de Recherche des Cordeliers, INSERM, Sorbonne Université de Paris, F-75006, Paris, France. sophie.mouillet-richard@parisdescartes.fr.

Nicolas Pallet (N)

INSERM U1138, Centre de Recherche des Cordeliers, INSERM, Sorbonne Université de Paris, F-75006, Paris, France. nicolas.pallet@aphp.fr.
Service de Biochimie, Hôpital Européen Georges Pompidou, Assistance Publique Hôpitaux de Paris, Paris, France. nicolas.pallet@aphp.fr.

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