Impairment of visual function and retinal ER stress activation in Wfs1-deficient mice

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Bonnet Wersinger, Delphine ^a   Benkafadar, Nesrine ^a   Jagodzinska, Jolanta ^a   Hamel, Christian ^a,b   Tanizawa, Yukio ^c   Lenaers, Guy ^a   Delettre, Cécile ^a  

^a UNIV MONTPELLIER   (France)

^b MONTPELLIER UNIVERSITY HOSPITAL   (France)

^c YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; CELL LOSS; CONTROLLED STUDY; DISEASE ASSOCIATION; ELECTRON MICROSCOPY; ELECTRORETINOGRAM; ENDOPLASMIC RETICULUM STRESS; EVOKED VISUAL RESPONSE; EYE FUNDUS; GENE MUTATION; GENETIC DISORDER; HISTOPATHOLOGY; MOUSE; MOUSE MUTANT; NONHUMAN; OPTIC NERVE; OPTIC NERVE DISEASE; PANCREAS ISLET BETA CELL; RETINA; RETINA GANGLION CELL; RETINA ROD; TRANSMISSION ELECTRON MICROSCOPY; VISUAL ACUITY; VISUAL IMPAIRMENT; WOLFRAM SYNDROME; AGE; ANIMAL; CONTRAST SENSITIVITY; DEFICIENCY; ELECTRORETINOGRAPHY; GENETICS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING;

ERN1 PROTEIN, MOUSE; HEAT SHOCK PROTEIN; MEMBRANE PROTEIN; MOLECULAR CHAPERONE GRP78; PRIMER DNA; PROTEIN DISULFIDE ISOMERASE; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE; WOLFRAMIN PROTEIN;

AGE FACTORS; ANIMALS; BLOTTING, WESTERN; CONTRAST SENSITIVITY; DNA PRIMERS; ELECTRORETINOGRAPHY; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; EVOKED POTENTIALS, VISUAL; HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; POLYMERASE CHAIN REACTION; PROTEIN DISULFIDE-ISOMERASES; PROTEIN-SERINE-THREONINE KINASES; RETINA; RETINAL GANGLION CELLS; UNFOLDED PROTEIN RESPONSE; VISUAL ACUITY;

EID: 84901255107     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097222     Document Type: Article

References (48)

1. Barrett TG, Bundey SE, Macleod AF (1995) Neurodegeneration and diabetes: UK nationwide study of Wolfram (DIDMOAD) syndrome. Lancet 346: 1458-1463.
2. Barrett TG, Bundey SE, Fielder AR, Good PA (1997) Optic atrophy in Wolfram (DIDMOAD) syndrome. Eye (Lond) 11 (Pt 6): 882-888. (Pubitemid 28024962)
3. Rando RA, Horton JC, Layzer RB (1992) Wolfram syndrome: evidence of a diffuse neurodegenerative disease by magnetic resonance imaging. Neurology 42: 1220-1224.
4. Wolfram DJ, Wagener HP (1938) Diabetes mellitus and simple optic atrophy among siblings: report of four cases. Mayo Clin Proc 9: 715-718.
5. Swift RG, Polymeropoulos MH, Torres R, Swift M (1998) Predisposition of Wolfram syndrome heterozygotes to psychiatric illness. Mol Psychiatry 3: 86-91. (Pubitemid 28045191)
6. Furlong RA, Ho LW, Rubinsztein JS, Michael A, Walsh C, et al. (1999) A rare coding variant within the wolframin gene in bipolar and unipolar affective disorder cases. Neurosci Lett 277: 123-126.
7. Rigoli L, Lombardo F, Di Bella C (2011) Wolfram syndrome and WFS1 gene. Clin Genet 79: 103-117.
8. Lopez de Heredia M, Cleries R, Nunes V (2013) Genotypic classification of patients with Wolfram syndrome : insights into the natural history of the disease and correlation with phenotype. Genetics in Medicine 15: 497-506.
9. Yu G, Yu ML, Wang JF, Gao CR, Chen ZJ (2010) WS1 gene mutation analysis of Wolfram syndrome in a Chinese patient and a systematic review of literatures. Endocrine 38: 147-152.
10. Hardy C, Poulton J, Barrett TG, Khanim F, Collier D, et al. (1999) Clinical and Molecular Genetic Analysis of 19 Wolfram Syndrome Kindreds Demonstrating a Wide Spectrum of Mutations in WFS1. Am J Hum Genet 65: 1279-1290. (Pubitemid 30460378)
11. Seynaeve H, Vermeiren A, Leys A, Dralands L (1994) Four cases of Wolfram syndrome: ophthalmologic findings and complications. Bull Soc Belge Ophtalmol 252: 75-80.
12. Galluzzi P, Filosomi G, Vallone IM, Bardelli AM, Venturi C (1999) MRI of Wolfram syndrome (DIDMOAD). Neuroradiology 41: 729-731. (Pubitemid 30011916)
13. Cillino S, Anastasi M, Lodato G (1989) Incomplete Wolfram syndrome: clinical and electrophysiologic study of two familial cases. Graefes Arch Clin Exp Ophthalmol 227: 131-135. (Pubitemid 19066677)
14. Simsek E, Simsek T, Tekgul S, Hosal S, Seyrantepe V, et al. (2003) Wolfram (DIDMOAD) syndrome: a multidisciplinary clinical study in nine Turkish patients and review of the literature. Acta Paediatr 92: 55-61. (Pubitemid 36255932)
15. Langwinska-Wosko E, Broniek-Kowalik K, Szulborski K (2012) A clinical case study of a Wolfram syndrome-affected family: pattern-reversal visual evoked potentials and electroretinography analysis. Doc Ophthalmol 124: 133-141.
16. Schmidt-Kastner R, Kreczmanski P, Preising M, Diederen R, Schmitz C, et al. (2009) Expression of the diabetes risk gene wolframin (WFS1) in the human retina. Exp Eye Res 89: 568-574.
17. Osman AA, Saito M, Makepeace C, Permutt MA, Schlesinger P, et al. (2003) Wolframin expression induces novel ion channel activity in endoplasmic reticulum membranes and increases intracellular calcium. J Biol Chem 278: 52755-52762. (Pubitemid 38035873)
18. Takei D, Ishihara H, Yamaguchi S, Yamada T, Tamura A, et al. (2006) WFS1 protein modulates the free Ca(2+) concentration in the endoplasmic reticulum. FEBS Lett 580: 5635-5640. (Pubitemid 44498662)
19. Hatanaka M, Tanabe K, Yanai A, Ohta Y, Kondo M, et al. (2011) Wolfram syndrome 1 gene (WFS1) product localizes to secretory granules and determines granule acidification in pancreatic beta-cells. Hum Mol Genet 20: 1274-1284.
20. Ishihara H, Takeda S, Tamura A, Takahashi R, Yamaguchi S, et al. (2004) Disruption of the WFS1 gene in mice causes progressive beta-cell loss and impaired stimulus-secretion coupling in insulin secretion. Hum Mol Genet 13: 1159-1170. (Pubitemid 38786998)
21. Yamada T, Ishihara H, Tamura A, Takahashi R, Yamaguchi S, et al. (2006) WFS1-deficiency increases endoplasmic reticulum stress, impairs cell cycle progression and triggers the apoptotic pathway specifically in pancreatic betacells. Hum Mol Genet 15: 1600-1609. (Pubitemid 43904826)
22. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2: 326-332.
23. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D (2000) Perk Is Essential for Translational Regulation and Cell Survival during the Unfolded Protein Response. Mol Cell 5: 897-904.
24. Patil C, Walter P (2001) Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 13: 349-356. (Pubitemid 32429501)
25. Fonseca SG, Fukuma M, Lipson KL, Nguyen LX, Allen JR, et al. (2005) WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells. J Biol Chem 280: 39609-39615. (Pubitemid 41713920)
26. Ueda K, Kawano J, Takeda K, Yujiri T, Tanabe K, et al. (2005) Endoplasmic reticulum stress induces Wfs1 gene expression in pancreatic beta-cells via transcriptional activation. Eur J Endocrinol 153: 167-176. (Pubitemid 41030528)
27. Fonseca SG, Ishigaki S, Oslowski CM, Lu S, Lipson KL, et al. (2010) Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells. J Clin Invest 120: 744-755.
28. Chekroud K, Arndt C, Basset D, Hamel CP, Brabet P, et al. (2011) Simple and efficient: validation of a cotton wick electrode for animal electroretinography. Ophthalmic Res 45: 174-179.
29. Labunskyy VM, Yoo MH, Hatfield DL, Gladyshev VN (2009) Sep15, a thioredoxin-like selenoprotein, is involved in the unfolded protein response and differentially regulated by adaptive and acute ER stresses. Biochemistry 48: 8458-8465.
30. Jeon CJ, Strettoi E, Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18: 8936-8946. (Pubitemid 28491758)
31. Yang Z, Quigley HA, Pease ME, Yang Y, Qian J, et al. (2007) Changes in gene expression in experimental glaucoma and optic nerve transection: the equilibrium between protective and detrimental mechanisms. Invest Ophthalmol Vis Sci 48: 5539-5548. (Pubitemid 351260855)
32. Baltanas R, Bush A, Couto A, Durrieu L, Hohmann S, et al. (2013) Pheromone-induced morphogenesis improves osmoadaptation capacity by activating the HOG MAPK pathway. Sci Signal 6: ra26.
33. Chaussenot A, Bannwarth S, Rouzier C, Vialettes B, Ait El Mkadem A, et al. (2011) Neurologic Features and Genotype-Phenotype Correlation in Wolfram Syndrome. ANN Neurol 69: 501-508.
34. Hershey T, Lugar HM, Shimony JS, Rutlin J, Koller J, et al. (2012) Early brain vulnerability in Wolfram syndrome. PLoS One 7: e40604.
35. AllenBrainAtlas (2013). http://www.brain-map.org/: Allen Institute for Brain Science.
36. Leigh RJ, Zee DS (2006) The Neurology of Eye Movements. Oxford: Oxford University Press. 762 p.
37. Safran AB, Landis T (1996) Plasticity in the adult visual cortex: implications for the diagnosis of visual field defects and visual rehabilitation. Curr Opin Ophthalmol 7: 53-64. (Pubitemid 27163575)
38. Cahill H, Nathans J (2008) The Optokinetic Reflex as a Tool for Quantitative Analyses of Nervous System Function in Mice: Application to Genetic and Drug-Induced Variation. PLoS One 3: e2055.
39. Yoshiki A, Moriwaki K (2006) Mouse phenome research: implications of genetic background. ILAR J 47: 94-102.
40. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, et al. (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26: 9220-9231. (Pubitemid 44904418)
41. Castillo K, Rojas-Rivera D, Lisbona F, Caballero B, Nassif M, et al. (2011) BAX inhibitor-1 regulates autophagy by controlling the IRE1alpha branch of the unfolded protein response. EMBO J 30: 4465-4478.
42. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, et al. (2003) Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112: 1809-1820. (Pubitemid 38063704)
43. Yue Z, Jin S, Yang C, Levine AJ, Heintz N (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 100: 15077-15082. (Pubitemid 37518019)
44. Daido S, Kanzawa T, Yamamoto A, Takeuchi H, Kondo Y, et al. (2004) Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res 64: 4286-4293. (Pubitemid 38802435)
45. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH (2006) Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26: 3071-3084.
46. Urano F (2000) Coupling of Stress in the ER to Activation of JNK Protein Kinases by Transmembrane Protein Kinase IRE1. Science 287: 664-666.
47. Fouillet A, Levet C, Virgone A, Robin M, Dourlen P, et al. (2012) ER stress inhibits neuronal death by promoting autophagy. Autophagy 8: 915-926.
48. Matus S, Castillo K, Hetz C (2012) Hormesis: protecting neurons against cellular stress in Parkinson disease. Autophagy 8: 997-1001.