Bim links ER stress and apoptosis in cells expressing mutant SOD1 associated with amyotrophic lateral sclerosis

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Soo, Kai Y ^a,b   Atkin, Julie D ^b,c   Farg, Manal ^b   Walker, Adam K ^b,c,e   Horne, Malcolm K ^c,d   Nagley, Phillip ^a  

^a MONASH UNIVERSITY   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d ST VINCENT S HOSPITAL   (Australia)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; SMALL INTERFERING RNA; ACTIVATING TRANSCRIPTION FACTOR 6; APOPTOSIS REGULATORY PROTEIN; ATF6 PROTEIN, MOUSE; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; DDIT3 PROTEIN, MOUSE; MEMBRANE PROTEIN; ONCOPROTEIN; PROTEIN BAX; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL INCLUSION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; GENE; GENE MUTATION; MITOCHONDRION; MOUSE; NEUROBLASTOMA CELL; NEUROTOXICITY; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SOD1 GENE; UPREGULATION; ANIMAL; DOWN REGULATION; GENETICS; HUMAN; METABOLISM; NEUROBLASTOMA; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

MURINAE;

ACTIVATING TRANSCRIPTION FACTOR 6; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CYTOCHROMES C; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; HUMANS; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; NEUROBLASTOMA; PROTO-ONCOGENE PROTEINS; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR CHOP; UP-REGULATION;

EID: 84859867839     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035413     Document Type: Article

References (37)

1. Cleveland DW, Rothstein JD, (2001) From Charcot to Lou Gehrig: Deciphering selective motor neuron death in ALS. Nature 2: 806-819.
2. Boillee S, Velde CV, Cleveland DW, (2006) ALS: A disease of motor neurons and their nonneuronal neighbours. Neuron 52: 39-59.
3. Talbot K, (2002) Motor neuron disease. Postgraduate Medical Journal 78: 513-517.
4. Wang J, Xu G, Gonzales V, Coonfield M, Fromholt D, et al. (2002) Fibrillar inclusions and motor neuron degeneration in transgenic mice expressing superoxide dismutase 1 with a disrupted copper-binding site. Neurobiol Disease 10: 128-138.
5. Johnston JA, Dalton MJ, Gurney ME, Kopito RR, (2000) Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 97: 12571-12576.
6. Kato S, Horiuchi S, Liu J, Cleveland DW, Shibata N, et al. (2000) Advanced glycation endproduct-modified superoxide dismutase-1 (SOD1)-positive inclusions are common to familial amyotrophic lateral sclerosis patients with SOD1 gene mutations and transgenic mice expressing human SOD1 with a G85R mutation. Acta Neuropathol 1000: 490-505.
7. Shibata N, Asayama K, Hirano A, Kobayashi Y, (1996) Immunohistochemical study on superoxide dismutases in spinal cords from autopsied patients with amyotrophic lateral sclerosis. Dev Neurosci 18: 492-498.
8. Shaw BF, Valentine JS, (2007) How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein. Trends Biochem Sci 32: 78-85.
9. Shaw P, (2005) Molecular and cellular pathways of neurodegeneration in motor neuron disease. J Neurol Neurosurg Psych 76: 1046-1057.
10. Atkin JD, Farg MA, Turner BJ, Tomas D, Lysaght JA, et al. (2006) Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1. J Biol Chem 281: 30152-30165.
11. Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, et al. (2008) Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol Disease 30: 400-407.
12. Oh YK, Shin KS, Yuan J, Kang SJ, (2008) Superoxide dismutase 1 mutants related to amyotrophic lateral sclerosis induce endoplasmic stress in neuro2a cells. J Neurochem 104: 993-1005.
13. Saxena S, Cabuy E, Caroni P, (2009) A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nature Neurosci 12: 627-636.
14. Soo KY, Atkin JD, Horne MK, Nagley P, (2009) Recruitment of mitochondria into apoptotic signaling correlates with the presence of inclusions formed by amyotrophic lateral sclerosis-associated SOD1 mutations. J Neurochem 108: 578-590.
15. Zetterstrom P, Stewart HG, Bergemalm D, Jonsson PA, Graffmo KS, et al. (2007) Soluble misfolded subfractions of mutant superoxide dismutase-1s are enriched in spinal cords throughout life in murine ALS models. Proc Natl Acad Sci USA 104: 14157-14162.
16. Karch CM, Prudencio M, Winkler DD, Hart PJ, Borchelt DR, (2009) Role of mutant SOD1 disulfide oxidation and aggregation in the pathogenesis of familial ALS. Proc Natl Acad Sci USA 106: 7774-7779.
17. Winklhofer KF, Tatzelt J, Haass C, (2008) The two faces of protein misfolding: gain- and loss-of-function in neurodegenerative diseases. EMBO J 27: 336-349.
18. Williams A, Jahreiss L, Sarkar S, Saiki S, Menzies FM, et al. (2006) Aggregate-prone proteins are cleared from the cytosol by autophagy: therapeutic implications. Curr Top Dev Biol 76: 89-101.
19. Walker AK, Farg MA, Bye CR, McLean CA, Horne MK, et al. (2010) Protein disulphide isomerase protects against protein aggregation and is S-nitrosylated in amyotrophic lateral sclerosis. Brain 133: 105-116.
20. Woehlbier U, Hetz C, (2011) Modulating stress responses by the UPRosome: a matter of life and death. Trends Biochem Sci 36: 329-337.
21. Heath-Engel HM, Chang NC, Shore GC, (2008) The endoplasmic reticulum in apoptosis and autophagy: role of the Bcl-2 protein family. Oncogene 27: 6419-6433.
22. Hetz C, (2007) ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antiox Redox Signal 9: 2345-2355.
23. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, et al. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129: 1337-1349.
24. Reimertz C, Kogel D, Rami A, Chittenden T, Prehn JH, (2003) Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol 162: 587-597.
25. Hetz C, Thielen P, Fisher J, Pasinelli P, Brown RHJ, et al. (2007) The proapoptotic Bcl-2 family member Bim mediates motoneuron loss in a model of amyotrophic lateral sclerosis. Cell Death Diff 14: 1386-1389.
26. Nagley P, Higgins GC, Atkin JD, Beart PM, (2010) Multifaceted deaths orchestrated by mitochondria in neurones. Biochim Biophys Acta 1802: 167-185.
27. Olzmann JA, Li L, Chin LS, (2008) Aggresome formation and neurodegenerative diseases: therapeutic implications. Curr Med Chem 15: 47-60.
28. Ilieva H, Polymenidou M, Cleveland DW, (2009) Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J Cell Biol 187: 761-772.
29. Lei K, Davis RJ, (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 100: 2432-2437.
30. Okuno S, Saito A, Hayashi T, Chan PH, (2004) The c-Jun N-terminal protein kinase signaling pathway mediates Bax activation and subsequent neuronal apoptosis through interaction with Bim after transient focal cerebral ischemia. J Neurosci 24: 7879-7887.
31. Puthalakath H, Huang DC, O'Reilly LA, King SM, Strasser A, (1999) The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 3: 287-296.
32. Kieran D, Hafezparast M, Bohnert S, Dick JR, Martin JE, et al. (2005) A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J Cell Biol 169: 561-567.
33. Teuling E, van Dis V, Wulf PS, Haasdijk ED, Akhmanova A, et al. (2008) A novel mouse model with impaired dynein/dynactin function develops amyotrophic lateral sclerosis (ALS)-like features in motor neurons and improves lifespan in SOD1-ALS mice. Hum Mol Gen 17: 2849-2862.
34. Shi P, Strom AL, Gal J, Zhu H, (2010) Effects of ALS-related SOD1 mutants on dynein- and KIF5-mediated retrograde and anterograde axonal transport. Biochim Biophys Acta 1802: 707-716.
35. Kieran D, Woods I, Villunger A, Strasser A, Prehn JH, (2007) Deletion of the BH3-only protein puma protects motoneurons from ER stress-induced apoptosis and delays motoneuron loss in ALS mice. Proc Natl Acad Sci USA 104: 20606-20611.
36. Nickson P, Toth A, Erhardt P, (2007) PUMA is critical for neonatal cardiomyocyte apoptosis induced by endoplasmic reticulum stress. Cardiovasc Res 73: 48-56.
37. Turner BJ, Atkin JD, Farg MA, Zang DW, Rembach A, et al. (2005) Impaired extracellular secretion of mutant superxide dismutase 1 associates with neurotoxicity in familial amyotrophic lateral sclerosis. J Neurosci 25: 108-117.