Mutant FUS induces endoplasmic reticulum stress in amyotrophic lateral sclerosis and interacts with protein disulfide-isomerase

Neurobiology of Aging

Volumn 33, Issue 12, 2012, Pages 2855-2868

  Farg, Manal A ^a   Soo, Kai Y ^a   Walker, Adam K ^a,b   Pham, Hong ^a   Orian, Jacqueline ^a   Horne, Malcolm K ^b   Warraich, Sadaf T ^c,d   Williams, Kelly L ^c,d   Blair, Ian P ^c,d   Atkin, Julie D ^a,b  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ANZAC RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Amyotrophic lateral sclerosis; Endoplasmic reticulum stress; FUS fused in sarcoma; Protein disulfide isomerase; Translocated in liposarcoma

Indexed keywords

CHAPERONE; COPPER ZINC SUPEROXIDE DISMUTASE; FUSED IN SARCOMA PROTEIN; MUTANT PROTEIN; PROTEIN DISULFIDE ISOMERASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN TISSUE; MALE; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; MOTONEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; ARGININE; CALRETICULIN; CELL LINE, TRANSFORMED; CYSTEINE; CYTOPLASM; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; GREEN FLUORESCENT PROTEINS; HISTIDINE; HUMANS; IMMUNOPRECIPITATION; MICE; MUTATION; NEURONS; PROTEIN DISULFIDE-ISOMERASES; RNA-BINDING PROTEIN FUS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84866748196     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.02.009     Document Type: Article

References (53)

1. Andersson M.K., Ståhlberg A., Arvidsson Y., Olofsson A., Semb H., Stenman G., Nilsson O., Aman P. The multifunctional FUS, EWS and TAF15 proto-oncoproteins show cell type-specific expression patterns and involvement in cell spreading and stress response. BMC Cell Biol. 2008, 9:37.
2. Atkin J.D., Farg M.A., Turner B.J., Tomas D., Lysaght J.A., Nunan J., Rembach A., Nagley P., Beart P.M., Cheema S.S., Horne M.K. Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1. J. Biol. Chem. 2006, 281:30152-30165.
3. Atkin J.D., Farg M.A., Walker A.K., McLean C., Tomas D., Horne M.K. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol. Dis. 2008, 30:400-407.
4. Back S.H., Schröder M., Lee K., Zhang K., Kaufman R.J. ER stress signaling by regulated splicing: IRE1/HAC1/XBP1. Methods 2005, 35:395-416.
5. Bäumer D., Hilton D., Paine S.M., Turner M.R., Lowe J., Talbot K., Ansorge O. Juvenile ALS with basophilic inclusions is a FUS proteinopathy with FUS mutations. Neurology 2010, 75:611-618.
6. Blair I.P., Williams K.L., Warraich S.T., Durnall J.C., Thoeng A.D., Manavis J., Blumbergs P.C., Vucic S., Kiernan M.C., Nicholson G.A. FUS mutations in amyotrophic lateral sclerosis: clinical, pathological, neurophysiological and genetic analysis. J. Neurol. Neurosurg., Psychiatry 2010, 81:639-645.
7. Bosco D.A., Lemay N., Ko H.K., Zhou H., Burke C., Kwiatkowski T.J., Sapp P., McKenna-Yasek D., Brown R.H., Hayward L.J. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum. Mol. Genet. 2010, 19:4160-4175.
8. Cleveland D.W., Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2001, 2:806-819.
9. Corrado L., Del Bo R., Castellotti B., Ratti A., Cereda C., Penco S., Sorarù G., Carlomagno Y., Ghezzi S., Pensato V., Colombrita C., Gagliardi S., Cozzi L., Orsetti V., Mancuso M., Siciliano G., Mazzini L., Comi G.P., Gellera C., Ceroni M., D'Alfonso S., Silani V. Mutations of FUS gene in sporadic amyotrophic lateral sclerosis. J. Med. Genet 2010, 47:190-194.
10. Damme P.V., Goris A., Race V., Hersmus N., Dubois B., Bosch L.V., Matthijs G., Robberecht W. The occurrence of mutations in FUS in a Belgian cohort of patients with familial ALS. Eur. J. Neurol. 2010, 17:754-756.
11. De Vos K.J., Grierson A.J., Ackerley S., Miller C.C. Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci. 2008, 31:151-173.
12. Deng H.X., Zhai H., Bigio E.H., Yan J., Fecto F., Ajroud K., Mishra M., Ajroud-Driss S., Heller S., Sufit R., Siddique N., Mugnaini E., Siddique T. FUS-immunoreactive inclusions are a common feature in sporadic and non-SOD1 familial amyotrophic lateral sclerosis. Ann. Neurol 2010, 67:739-748.
13. Ding F., Dokholyan N.V. Dynamical roles of metal ions and the disulfide bond in Cu, Zn superoxide dismutase folding and aggregation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19696-19701.
14. Dormann D., Rodde R., Edbauer D., Bentmann E., Fischer I., Hruscha A., Than M.E., Mackenzie I.R., Capell A., Schmid B., Neumann M., Haass C. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. EMBO J 2010, 29:2841-2857.
15. Drepper C., Herrmann T., Wessig C., Beck M., Sendtner M. C-terminal FUS/TLS mutations in familial and sporadic ALS in Germany. Neurobiol. Aging 2011, 32:548.e1-548.e4.
16. Forsberg K., Jonsson P.A., Andersen P.M., Bergemalm D., Graffmo K.S., Hultdin M., Jacobsson J., Rosquist R., Marklund S.L., Brännström T. Novel antibodies reveal inclusions containing non-native SOD1 in sporadic ALS patients. PLoS One 2010, 5:e11552.
17. Freedman R.B., Hirst T.R., Tuite M.F. Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci 1994, 19:331-336.
18. Gal J., Zhang J., Kwinter D.M., Zhai J., Jia H., Jia J., Zhu H. Nuclear localization sequence of FUS and induction of stress granules by ALS mutants. Neurobiol. Aging 2011, 32:2323.e27-2323.e40.
19. Hart P.J. Pathogenic superoxide dismutase structure, folding, aggregation and turnover. Curr. Opin. Chem. Biol. 2006, 10:131-138.
20. Haynes C.M., Titus E.A., Cooper A.A. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell 2004, 15:767-776.
21. Hitomi J., Katayama T., Taniguchi M., Honda A., Imaizumi K., Tohyama M. Apoptosis induced by endoplasmic reticulum stress depends on activation of caspase-3 via caspase-12. Neurosci. Lett. 2004, 357:127-130.
22. Honjo Y., Kaneko S., Ito H., Horibe T., Nagashima M., Nakamura M., Fujita K., Takahashi R., Kusaka H., Kawakami K. Protein disulfide isomerase-immunopositive inclusions in patients with amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2011, 12:444-450.
23. Huang E.J., Zhang J., Geser F., Trojanowski J.Q., Strober J.B., Dickson D.W., Brown R.H., Shapiro B.E., Lomen-Hoerth C. Extensive FUS-immunoreactive pathology in juvenile amyotrophic lateral sclerosis with basophilic inclusions. Brain Pathol 2010, 20:1069-1076.
24. Ilieva E.V., Ayala V., Jove M., Dalfo E., Cacabelos D., Povedano M., Bellmunt M.J., Ferrer I., Pamplona R., Portero-Otin M. Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain 2007, 130:3111-3123.
25. Iwawaki T., Akai R., Kohno K., Miura M. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat. Med. 2004, 10:98-102.
26. Kanai Y., Dohmae N., Hirokawa N. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 2004, 43:513-525.
27. Kwiatkowski T.J., Bosco D.A., Leclerc A.L., Tamrazian E., Vanderburg C.R., Russ C., Davis A., Gilchrist J., Kasarskis E.J., Munsat T., Valdmanis P., Rouleau G.A., Hosler B.A., Cortelli P., de Jong P.J., Yoshinaga Y., Haines J.L., Pericak-Vance M.A., Yan J., Ticozzi N., Siddique T., McKenna-Yasek D., Sapp P.C., Horvitz H.R., Landers J.E., Brown R.H. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
28. Lagier-Tourenne C., Polymenidou M., Cleveland D.W. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet. 2010, 19:R46-R64.
29. Manders E.M.M., Verbeek F.J., Aten J.A. Measurement of Colocalization of Objects in Dual-Color Confocal Images. J. Microsc. Oxf. 1993, 169:375-382.
30. Neumann M., Rademakers R., Roeber S., Baker M., Kretzschmar H.A., Mackenzie I.R. A newsubtype of frontotemporal lobar degeneration with FUS pathology. Brain 2009, 132:2922-2931.
31. Niwa J., Yamada S., Ishigaki S., Sone J., Takahashi M., Katsuno M., Tanaka F., Doyu M., Sobue G. Disulfide bond mediates aggregation, toxicity, and ubiquitylation of familial amyotrophic lateral sclerosis-linked mutant SOD1. J. Biol. Chem. 2007, 282:28087-28095.
32. Perlson E., Maday S., Fu M.M., Moughamian A.J., Holzbaur E.L. Retrograde axonal transport: pathways to cell death?. Trends Neurosci 2010, 33:335-344.
33. Pincus D., Chevalier M.W., Aragon T., van Anken E., Vidal S.E., El-Samad H., Walter P. BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biol 2010, 8:e1000415.
34. Puig A., Gilbert H.F. Protein disulfide isomerase exhibits chaperone and anti-chaperone activity in the oxidative refolding of lysozyme. J. Biol. Chem. 1994, 269:7764-7771.
35. Salminen A., Kauppinen A., Hyttinen J.M., Toropainen E., Kaarniranta K. Endoplasmic reticulum stress in age-related macular degeneration: trigger for neovascularization. Mol. Med. 2010, 16:535-542.
36. Saxena S., Cabuy E., Caroni P. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat. Neurosci. 2009, 12:627-636.
37. Schröder M. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 2008, 65:862-894.
38. Schröder M., Kaufman R.J. ER stress and the unfolded protein response. Mutat. Res. 2005, 569:29-63.
39. Sproviero W., La Bella V., Mazzei R., Valentino P., Rodolico C., Simone I.L., Logroscino G., Ungaro C., Magariello A., Patitucci A., Tedeschi G., Spataro R., Condino F., Bono F., Citrigno L., Monsurrò M.R., Muglia M., Gambardella A., Quattrone A., Conforti F.L. FUS mutations in sporadic amyotrophic lateral sclerosis: Clinical and genetic analysis. Neurobiol Aging 2012, 33:837.e1-837.e5.
40. Sun Z., Diaz Z., Fang X., Hart M.P., Chesi A., et al. Molecular Determinants and Genetic Modifiers of Aggregation and Toxicity for the ALS Disease Protein FUS/TLS. PLoS Biol 2011, 9:e1000614.
41. Tabata Y., Takano K., Ito T., Iinuma M., Yoshimoto T., Miura H., Kitao Y., Ogawa S., Hori O. Vaticanol B, a resveratrol tetramer, regulates endoplasmic reticulum stress and inflammation. Am. J. Physiol. Cell Physiol. 2007, 293:C411-C418.
42. Tateishi T., Hokonohara T., Yamasaki R., Miura S., Kikuchi H., Iwaki A., Tashiro H., Furuya H., Nagara Y., Ohyagi Y., Nukina N., Iwaki T., Fukumaki Y., Kira J. Multiple system degeneration with basophilic inclusions in Japanese ALS patients with FUS mutation. Acta Neuropathol. 2010, 119:355-364.
43. Tsuda H., Han S.M., Yang Y., Tong C., Lin Y.Q., Mohan K., Haueter C., Zoghbi A., Harati Y., Kwan J., Miller M.A., Bellen H.J. The amyotrophic lateral sclerosis 8 protein VAPB is cleaved, secreted, and acts as a ligand for Eph receptors. Cell 2008, 133:963-977.
44. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
45. Vance C., Rogelj B., Hortobágyi T., De Vos K.J., Nishimura A.L., Sreedharan J., Hu X., Smith B., Ruddy D., Wright P., Ganesalingam J., Williams K.L., Tripathi V., Al-Saraj S., Al-Chalabi A., Leigh P.N., Blair I.P., Nicholson G., de Belleroche J., Gallo J.M., Miller C.C., Shaw C.E. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
46. Walker A.K., Farg M.A., Bye C.R., McLean C.A., Horne M.K., Atkin J.D. Protein disulphide isomerase protects against protein aggregation and is S-nitrosylated in amyotrophic lateral sclerosis. Brain 2010, 133:105-116.
47. Wang J., Xu G., Borchelt D.R. Mapping superoxide dismutase 1 domains of non-native interaction: roles of intra- and intermolecular disulfide bonding in aggregation. J. Neurochem. 2006, 96:1277-1288.
48. Wilkinson B., Gilbert H.F. Protein disulfide isomerase. Biochim. Biophys. Acta 2004, 1699:35-44.
49. Yamagishi S., Koyama Y., Katayama T., Taniguchi M., Hitomi J., Kato M., Aoki M., Itoyama Y., Kato S., Tohyama M. An in vitro model for Lewy body-like hyaline inclusion/astrocytic hyaline inclusion: induction by ER stress with an ALS-linked SOD1 mutation. PLoS One 2007, 2:e1030.
50. Yang Y.S., Harel N.Y., Strittmatter S.M. Reticulon-4A (Nogo-A) redistributes protein disulfide isomerase to protect mice from SOD1-dependent amyotrophic lateral sclerosis. J. Neurosci. 2009, 29:13850-13859.
51. Yoshimura T., Arimura N., Kaibuchi K. Molecular mechanisms of axon specification and neuronal disorders. Ann. N. Y. Acad. Sci. 2006, 1086:116-125.
52. Zhang T., Mullane P.C., Periz G., Wang J. TDP-43 neurotoxicity and protein aggregation modulated by heat shock factor and insulin/IGF-1 signaling. Hum. Mol. Genet. 2011, 20:1952-1965.
53. Zinszner H., Sok J., Immanuel D., Yin Y., Ron D. TLS (FUS) binds RNA in vivo and engages in nucleo-cytoplasmic shuttling. J. Cell Sci. 1997, 110:1741-1750.