A soluble endoplasmic reticulum factor as regenerative therapy for Wolfram syndrome.
Journal
Laboratory investigation; a journal of technical methods and pathology
ISSN: 1530-0307
Titre abrégé: Lab Invest
Pays: United States
ID NLM: 0376617
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
25
08
2019
accepted:
19
04
2020
revised:
18
04
2020
pubmed:
6
5
2020
medline:
24
11
2020
entrez:
6
5
2020
Statut:
ppublish
Résumé
Endoplasmic reticulum (ER) stress-mediated cell death is an emerging target for human chronic disorders, including neurodegeneration and diabetes. However, there is currently no treatment for preventing ER stress-mediated cell death. Here, we show that mesencephalic astrocyte-derived neurotrophic factor (MANF), a neurotrophic factor secreted from ER stressed cells, prevents ER stress-mediated β cell death and enhances β cell proliferation in cell and mouse models of Wolfram syndrome, a prototype of ER disorders. Our results indicate that molecular pathways regulated by MANF are promising therapeutic targets for regenerative therapy of ER stress-related disorders, including diabetes, retinal degeneration, neurodegeneration, and Wolfram syndrome.
Identifiants
pubmed: 32366942
doi: 10.1038/s41374-020-0436-1
pii: S0023-6837(22)00364-6
pmc: PMC7438202
mid: NIHMS1586015
doi:
Substances chimiques
MANF protein, mouse
0
Nerve Growth Factors
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1197-1207Subventions
Organisme : NCATS NIH HHS
ID : UH3 TR002065
Pays : United States
Organisme : NIDDK NIH HHS
ID : R21 DK113487
Pays : United States
Organisme : NIDDK NIH HHS
ID : F30 DK111070
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR000448
Pays : United States
Organisme : NIDDK NIH HHS
ID : P60 DK020579
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK020579
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK112921
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR002345
Pays : United States
Organisme : NCATS NIH HHS
ID : UH2 TR002065
Pays : United States
Références
Fonseca SG, Gromada J, Urano F. Endoplasmic reticulum stress and pancreatic beta-cell death. Trends Endocrinol Metab. 2011;22:266–74.
pubmed: 21458293
pmcid: 3130122
Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334:1081–6.
doi: 10.1126/science.1209038
Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol. 2012;197:857–67.
pubmed: 22733998
pmcid: 3384412
doi: 10.1083/jcb.201110131
Hetz C, Mollereau B. Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat Rev Neurosci. 2014;15:233–49.
pubmed: 24619348
doi: 10.1038/nrn3689
Mollereau B, Rzechorzek NM, Roussel BD, Sedru M, Van den Brink DM, Bailly-Maitre B, et al. Adaptive preconditioning in neurological diseases—therapeutic insights from proteostatic perturbations. Brain Res. 2016. https://doi.org/10.1016/j.brainres.2016.02.033.
Barrett TG, Bundey SE, Macleod AF. Neurodegeneration and diabetes: UK nationwide study of Wolfram (DIDMOAD) syndrome. Lancet. 1995;346:1458–63.
pubmed: 7490992
doi: 10.1016/S0140-6736(95)92473-6
Urano F. Wolfram syndrome: diagnosis, management, and treatment. Curr Diab Rep. 2016;16:6.
pubmed: 26742931
pmcid: 4705145
doi: 10.1007/s11892-015-0702-6
Fonseca SG, Fukuma M, Lipson KL, Nguyen LX, Allen JR, Oka Y, et al. WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells. J Biol Chem. 2005;280:39609–15.
pubmed: 16195229
doi: 10.1074/jbc.M507426200
Fonseca SG, Ishigaki S, Oslowski CM, Lu S, Lipson KL, Ghosh R, et al. Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells. J Clin Investig. 2010;120:744–55.
pubmed: 20160352
doi: 10.1172/JCI39678
pmcid: 2827948
Lu S, Kanekura K, Hara T, Mahadevan J, Spears LD, Oslowski CM, et al. A calcium-dependent protease as a potential therapeutic target for Wolfram syndrome. Proc Natl Acad Sci USA. 2014;111:E5292–301.
pubmed: 25422446
pmcid: 4267371
Urano F. Diabetes: targeting endoplasmic reticulum to combat juvenile diabetes. Nat Rev Endocrinol. 2014;10:129–30.
pubmed: 24393784
pmcid: 4049517
doi: 10.1038/nrendo.2013.261
Urano F. Wolfram syndrome iPS cells: the first human cell model of endoplasmic reticulum disease. Diabetes. 2014;63:844–6.
pubmed: 24556864
pmcid: 3931391
doi: 10.2337/db13-1809
Abreu D, Asada R, Revilla JMP, Lavagnino Z, Kries K, Piston DW, et al. Wolfram syndrome 1 gene regulates pathways maintaining beta-cell health and survival. Lab Investig. 2020. https://doi.org/10.1038/s41374-020-0408-5 .
Abreu D, Urano F. Current landscape of treatments for Wolfram syndrome. Trends Pharmacol Sci. 2019;40:711–4.
pubmed: 31420094
pmcid: 7547529
doi: 10.1016/j.tips.2019.07.011
Petrova P, Raibekas A, Pevsner J, Vigo N, Anafi M, Moore MK, et al. MANF: a new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J Mol Neurosci. 2003;20:173–88.
pubmed: 12794311
doi: 10.1385/JMN:20:2:173
Mizobuchi N, Hoseki J, Kubota H, Toyokuni S, Nozaki J, Naitoh M, et al. ARMET is a soluble ER protein induced by the unfolded protein response via ERSE-II element. Cell Struct Funct. 2007;32:41–50.
pubmed: 17507765
doi: 10.1247/csf.07001
Glembotski CC, Thuerauf DJ, Huang C, Vekich JA, Gottlieb RA, Doroudgar S. Mesencephalic astrocyte-derived neurotrophic factor protects the heart from ischemic damage and is selectively secreted upon sarco/endoplasmic reticulum calcium depletion. J Biol Chem. 2012;287:25893–904.
pubmed: 22637475
pmcid: 3406674
doi: 10.1074/jbc.M112.356345
Henderson MJ, Richie CT, Airavaara M, Wang Y, Harvey BK. Mesencephalic astrocyte-derived neurotrophic factor (MANF) secretion and cell surface binding are modulated by KDEL receptors. J Biol Chem. 2013;288:4209–25.
pubmed: 23255601
doi: 10.1074/jbc.M112.400648
Yu YQ, Liu LC, Wang FC, Liang Y, Cha DQ, Zhang JJ, et al. Induction profile of MANF/ARMET by cerebral ischemia and its implication for neuron protection. J Cereb Blood Flow Metab. 2010;30:79–91.
pubmed: 19773801
doi: 10.1038/jcbfm.2009.181
Lindahl M, Danilova T, Palm E, Lindholm P, Voikar V, Hakonen E, et al. MANF is indispensable for the proliferation and survival of pancreatic beta cells. Cell Rep. 2014;7:366–75.
pubmed: 24726366
pmcid: 7254957
doi: 10.1016/j.celrep.2014.03.023
Riggs AC, Bernal-Mizrachi E, Ohsugi M, Wasson J, Fatrai S, Welling C, et al. Mice conditionally lacking the Wolfram gene in pancreatic islet beta cells exhibit diabetes as a result of enhanced endoplasmic reticulum stress and apoptosis. Diabetologia. 2005;48:2313–21.
pubmed: 16215705
doi: 10.1007/s00125-005-1947-4
Hara T, Mahadevan J, Kanekura K, Hara M, Lu S, Urano F. Calcium efflux from the endoplasmic reticulum leads to beta-cell death. Endocrinology. 2014;155:758–68.
pubmed: 24424032
doi: 10.1210/en.2013-1519
Oh-Hashi K, Tanaka K, Koga H, Hirata Y, Kiuchi K. Intracellular trafficking and secretion of mouse mesencephalic astrocyte-derived neurotrophic factor. Mol Cell Biochem. 2012;363:35–41.
pubmed: 22120531
doi: 10.1007/s11010-011-1155-0
Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998;12:982–95.
pubmed: 9531536
pmcid: 316680
doi: 10.1101/gad.12.7.982
Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 2004;18:3066–77.
pubmed: 15601821
pmcid: 535917
doi: 10.1101/gad.1250704
Qian B, Wang H, Men X, Zhang W, Cai H, Xu S, et al. TRIB3 [corrected] is implicated in glucotoxicity- and endoplasmic reticulum-stress-induced [corrected] beta-cell apoptosis. J Endocrinol. 2008;199:407–16.
pubmed: 18818302
doi: 10.1677/JOE-08-0331
Kanekura K, Ma X, Murphy JT, Zhu LJ, Diwan A, Urano F. IRE1 prevents endoplasmic reticulum membrane permeabilization and cell death under pathological conditions. Sci Signal. 2015;8:ra62.
pubmed: 26106220
pmcid: 4492519
doi: 10.1126/scisignal.aaa0341
Barrett TG, Bundey SE. Wolfram (DIDMOAD) syndrome. J Med Genet. 1997;34:838–41.
pubmed: 9350817
pmcid: 1051091
doi: 10.1136/jmg.34.10.838
Ishihara H, Takeda S, Tamura A, Takahashi R, Yamaguchi S, Takei D, et al. Disruption of the WFS1 gene in mice causes progressive beta-cell loss and impaired stimulus-secretion coupling in insulin secretion. Hum Mol Genet. 2004;13:1159–70.
pubmed: 15056606
doi: 10.1093/hmg/ddh125
Sousa-Victor P, Neves J, Cedron-Craft W, Ventura PB, Liao CY, Riley RR, et al. MANF regulates metabolic and immune homeostasis in ageing and protects against liver damage. Nat Metab. 2019;1:276–90.
pubmed: 31489403
pmcid: 6727652
doi: 10.1038/s42255-018-0023-6
Hakonen E, Chandra V, Fogarty CL, Yu NY, Ustinov J, Katayama S, et al. MANF protects human pancreatic beta cells against stress-induced cell death. Diabetologia. 2018. https://doi.org/10.1007/s00125-018-4687-y .
Chen L, Feng L, Wang X, Du J, Chen Y, Yang W, et al. Mesencephalic astrocyte-derived neurotrophic factor is involved in inflammation by negatively regulating the NF-kappaB pathway. Sci Rep. 2015;5:8133.
pubmed: 25640174
pmcid: 4313098
doi: 10.1038/srep08133
Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ. 2006;13:385–92.
pubmed: 16397584
doi: 10.1038/sj.cdd.4401778
Lin W, Bailey SL, Ho H, Harding HP, Ron D, Miller SD, et al. The integrated stress response prevents demyelination by protecting oligodendrocytes against immune-mediated damage. J Clin Investig. 2007;117:448–56.
pubmed: 17273557
doi: 10.1172/JCI29571
pmcid: 1783809
Getts MT, Getts DR, Kohm AP, Miller SD. Endoplasmic reticulum stress response as a potential therapeutic target in multiple sclerosis. Therapy. 2008;5:631–40.
pubmed: 20357912
pmcid: 2847412
doi: 10.2217/14750708.5.5.631
Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell. 2008;134:743–56.
pubmed: 18775308
pmcid: 2586148
doi: 10.1016/j.cell.2008.07.021
Fonseca SG, Burcin M, Gromada J, Urano F. Endoplasmic reticulum stress in beta-cells and development of diabetes. Curr Opin Pharmacol. 2009;9:763–70.
pubmed: 19665428
pmcid: 2787771
doi: 10.1016/j.coph.2009.07.003
Kaufman RJ. Beta-cell failure, stress, and type 2 diabetes. N Engl J Med. 2011;365:1931–3.
pubmed: 22087686
pmcid: 3684425
doi: 10.1056/NEJMcibr1109442
Kroeger H, Chiang WC, Felden J, Nguyen A, Lin JH. ER stress and unfolded protein response in ocular health and disease. FEBS J. 2019;286:399–412.
pubmed: 29802807
doi: 10.1111/febs.14522
Galli E, Harkonen T, Sainio MT, Ustav M, Toots U, Urtti A, et al. Increased circulating concentrations of mesencephalic astrocyte-derived neurotrophic factor in children with type 1 diabetes. Sci Rep. 2016;6:29058.
pubmed: 27356471
pmcid: 4928177
doi: 10.1038/srep29058
Cardozo AK, Ortis F, Storling J, Feng YM, Rasschaert J, Tonnesen M, et al. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes. 2005;54:452–61.
pubmed: 15677503
doi: 10.2337/diabetes.54.2.452
O’Sullivan-Murphy B, Urano F. ER stress as a trigger for beta-cell dysfunction and autoimmunity in type 1 diabetes. Diabetes. 2012;61:780–1.
pubmed: 22442299
pmcid: 3314361
doi: 10.2337/db12-0091
Oslowski CM, Hara T, O’Sullivan-Murphy B, Kanekura K, Lu S, Hara M, et al. Thioredoxin-interacting protein mediates ER stress-induced beta cell death through initiation of the inflammasome. Cell Metab. 2012;16:265–73.
pubmed: 22883234
pmcid: 3418541
doi: 10.1016/j.cmet.2012.07.005
Tersey SA, Nishiki Y, Templin AT, Cabrera SM, Stull ND, Colvin SC, et al. Islet beta-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes. 2012;61:818–27.
pubmed: 22442300
pmcid: 3314371
doi: 10.2337/db11-1293
Yang C, Diiorio P, Jurczyk A, O’Sullivan-Murphy B, Urano F, Bortell R. Pathological endoplasmic reticulum stress mediated by the IRE1 pathway contributes to pre-insulitic beta cell apoptosis in a virus-induced rat model of type 1 diabetes. Diabetologia. 2013;56:2638–46.
pubmed: 24121653
pmcid: 4845659
doi: 10.1007/s00125-013-3044-4
Unanue ER, Urano F. Endoplasmic reticulum: an interface between the immune system and metabolism. Diabetes. 2014;63:48–49.
pubmed: 24357695
doi: 10.2337/db13-1478
Vomund AN, Zinselmeyer BH, Hughes J, Calderon B, Valderrama C, Ferris ST, et al. Beta cells transfer vesicles containing insulin to phagocytes for presentation to T cells. Proc Natl Acad Sci USA. 2015;112:E5496–5502.
pubmed: 26324934
doi: 10.1073/pnas.1515954112
pmcid: 4603448
Yavarna T, Al-Dewik N, Al-Mureikhi M, Ali R, Al-Mesaifri F, Mahmoud L, et al. High diagnostic yield of clinical exome sequencing in Middle Eastern patients with Mendelian disorders. Hum Genet. 2015;134:967–80.
pubmed: 26077850
doi: 10.1007/s00439-015-1575-0