Endoplasmic Reticulum Stress in Motor Neurons of the Spinal Cord in Sporadic Amyotrophic Lateral Sclerosis

Journal of Neuropathology and Experimental Neurology

Volumn 69, Issue 4, 2010, Pages 346-355

  Sasaki, Shoichi ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Electron microscopy; Endoplasmic reticulum; ER stress; Motor neuron; Rough endoplasmic reticulum; Unfolded protein response

Indexed keywords

CHAPERONE; GLUCOSE REGULATED PROTEIN 78;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ANTERIOR HORN CELL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE STRUCTURE; MOTONEURON; NERVE DEGENERATION; PATHOGENESIS; PRIORITY JOURNAL; RIBOSOME; SPINAL CORD; SPORADIC AMYOTROPHIC LATERAL SCLEROSIS;

ADULT; AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; CASE-CONTROL STUDIES; ENDOPLASMIC RETICULUM; FEMALE; HEAT-SHOCK PROTEINS; HUMANS; MALE; MIDDLE AGED; MOTOR NEURONS; SPINAL CORD; UBIQUITIN;

EID: 77950853379     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181d44992     Document Type: Article

References (57)

1. Hammond C, Helenius A. Quality control in the secretory pathway: Retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J Cell Biol 1994;126:41-52
2. Balch WE, Morimoto RI, Dillin A, et al. Adapting proteostasis for disease intervention. Science 2008;319:916-19
3. Oberdorf J, Carlson EJ, Skach WR. Redundancy of mammalian proteasome beta subunit function during endoplasmic reticulum associated degradation. Biochemistry 2001;40:13397-405
4. Bush KT, Goldberg AI, Nigam SK. Proteasome inhibition leads to a heat shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J Biol Chem 1997;272:9086-92
5. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes Dev 1999;13:1211-33
6. Shen X, Zhang K, Kaufman RJ. The unfolded protein response-a stress signaling pathway of the endoplasmic reticulum. J Chem Neruoanat 2004;28:79-92 (Pubitemid 39195253)
7. Hetz C, Bernasconi P, Fisher J, et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 2006;312:572-76
8. Nakagawa T, Zhu H, Morishima N, et al. Caspase-12 mediates endoplasmic reticulum-specific apoptosis and cytotoxicity by amyloid-A. Nature 2000;403:98-103
9. Nishitoh H, Matsuzawa A, Tobiume K, et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002;16:1345-55
10. Imai Y, Soda M, Takahashi R. Parkin suppresses unfolded protein stressinduced cell death through its E3 ubiquitin-protein ligase activity. J Biol Chem 2000;275:35661-64
11. Herz C, Russelakis-Carneiro M, Maundrell K, et al. Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. Embo J 2003;22:5435-45
12. Tobisawa S, Hozumi Y, Arawaka S, et al. Mutant SOD1 linked to familial amyotrophic lateral sclerosis, but not wild-type SOD1, induces ER stress in CO57 cells and transgenic mice. Biochem Biophys Res Commun 2003;303:496-503
13. Wate R, Ito H, Zhang JH, et al. Expression of an endoplasmic reticulumresistant chaperone, glucose-regulated stress protein 78, in the spinal cord of a mouse model of amyotrophic lateral sclerosis. Acta Neuropathol 2005;110:57-62
14. Kikuchi H, Almer G, Yamashita S, et al. Spinal cord endoplasmic reticulum stress associated with a microsomal accumulation of mutant superoxide dismutase-1 in an ALS model. Proc Natl Acad Sci U S A 2006;103:6025-30
15. Atkin JD, Farg MA, Turner BJ, et al. 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; 281:30152-65
16. IIieva EV, Ayala V, Jové M, et al. Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain 2007; 130:3111-23
17. Saxena S, Cabuy E, Caroni P. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci 2009; 12:627-36
18. Zhao L, Ackerman SL. Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol 2006;18:444-52
19. Hoozemans JJ, Veerhuis R, Van Haastert ES, et al. The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol 2005; 110:165-72
20. Turner BJ, Atkin JD. ER stress and UPR in familial amyotrophic lateral sclerosis. Curr Mol Med 2006;6:79-86
21. Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 2006;13:385-92
22. Bertolotti A, Zhang Y, Hendershot LM, et al. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000;2:26-32
23. Shen J, Chen X, Hendershot L, et al. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 2002;3:99-111
24. Rao RV, Peel A, Logvinova A, et al. Coupling endoplasmic reticulum stress to the cell death program: Role of the ER chaperone GRP78. FEBS Lett 2002;514:122-28
25. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008;454:455-62
26. Morimoto RI. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease. Genes Dev 2008;22:1427-38
27. 2+. J Biol Chem 1997;272:30873-79
28. Van PN, Peter F, Soling HD. Four intracisternal calcium-binding glycoproteins from rat liver microsomes with high affinity for calcium. No indication for calsequestrin-like proteins in inositol 1,4,5- trisphosphatesensitive calcium sequestering rat liver vesicles. J Biol Chem 1989;264: 17494-501
29. Milner RE, Baksh S, Shemanko C, et al. Calreticulin, and not calsequestrin, is the major calcium binding protein of smooth muscle sarcoplasmic reticulum and liver endoplasmic reticulum. J Biol Chem 1991; 266:7155-65
30. Wada I, Rindress D, Cameron PH, et al. SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 1991;266:19599-610
31. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: Cell life and death decisions. J Clin Invest 2005;115:2656-64
32. Shibata N, Asayama K, Hirano A, et al. Immunohistochemical study on superoxide dismutase in spinal cords from autopsied patients with amyotrophic lateral sclerosis. Dev Neurosci 1996;18:492-98
33. Arai T, Hasegawa M, Akiyama H, et al. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 2006;351:602-11
34. Mackenzie IR, Bigio EH, Ince PG, et al. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol 2007;61:427-34
35. Urushitani M, Kurisu J, Tsukita K, et al. Proteasomal inhibition by misfolded mutant superoxide dismutase 1 induces selective motor neuron death in familial amyotrophic lateral sclerosis. J Neurochem 2002;83:1030-42
36. Cheroni C, Peviani M, Cascio P, et al. Accumulation of human SOD1 and ubiquitinated deposits in the spinal cord of SOD1G93A mice during motor neuron disease progression correlates with a decrease of proteasome. Neurobiol Dis 2005;18:509-22
37. Koyama S, Arawaka S, Chang-Hong R, et al. Alteration of familial ALS-linked mutant SOD1 solubility with disease progression: Its modulation by the proteasome and Hsp70. Biochem Biophys Res Commun 2006;343:719-30
38. Mendonca DMF, Chimelli L, Martinez AMB. Expression of ubiquitin and proteasome in motorneurons and astrocytes of spinal cords from patients with amyotrophic lateral sclerosis. Neurosci Lett 2006;404: 315-19
39. Grune T, Reinheckel T, Davies J. Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J Biol Chem 1996;271: 15504-9
40. Zhang K, Kaufman RJ. The unfolded protein response: A stress signaling pathway critical for health and disease. Neurology 2006;66: S102-9
41. Sasaki S, Shibata N, Komori T, et al. iNOS and nitrotyrosine immunoreactivity in amyotrophic lateral sclerosis. Neurosci Lett 2000;291: 44-48
42. Sasaki S, Warita H, Abe K, et al. Inducible nitric oxide synthase (iNOS) and nitrotyrosine immunoreactivity in the spinal cords of transgenic mice with a G93A mutant SOD1 gene. J Neuropathol Exp Neurol 2001;60: 839-46
43. Kieran D, Woods I, Villunger A, et al. Deletion of the BH3-only protein puma protects motoneurons from ER stressYinduced apoptosis and delays motoneuron loss in ALS mice. Proc Natl Acad Sci U S A 2007;104: 20606-11
44. Nagata T, Ilieva H, Murakami T, et al. Increased ER stress during motor neuron degeneration in a transgenic mouse model of amyotrophic lateral sclerosis. Neurol Res 2007;29:767-71
45. Atkin JD, Farg MA, Walker AK, et al. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol Dis 2008;30:400-7
46. Urushitani M, Sik A, Sakurai T, et al. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 2006;9:108-18
47. Nishitoh H, Kadowaki H, Nagai A, et al. ALS-like mutant SOD1 induces ER stress- and Ask-dependent motor neuron death by targeting Derlin-1. Genes Dev 2008;22:1451-64
48. Tarabal O, Calderó J, Casas C, et al. Protein retention in the endoplasmic reticulum, blockade of programmed cell death and autophagy selectively occur in spinal cord motoneurons after glutamate receptorYmediated injury. Mol Cell Neurosci 2005;29:283-98
49. Oyanagi K, Yamazaki M, Takahashi H, et al. Spinal anterior horn cells in sporadic amyotrophic lateral sclerosis show ribosomal detachment from, and cisternal distention of the rough endoplasmic reticulum. Neuropathol Appl Neurobiol 2008;34:650-58
50. Kozutsumi Y, Segal M, Normington K, et al. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucoseregulated proteins. Nature 1988;332:62-64
51. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: Significance for the molecular mechanism of Bcl-2 action. EMBO J 2001; 20:2690-701
52. Hirano A. Changes of the neuronal endoplasmic reticulum in the peripheral nervous system in mutant hamsters with hind leg paralysis and normal controls. J Neuropathol Exp Neurol 1978;37:75-84
53. Hirano A, Sax DS, Zimmerman HM. The fine structure of the cerebella of jimpy mice and their Bnormal[ litter mates. J Neuropathol Exp Neurol 1969;28:388-400
54. Sotelo C, Palay SL. Altered axons and axon terminals in the lateral vestibular nucleus of the rat: Possible example of axonal remodeling. Lab Invest 1971;25:653-71
55. Sasaki S, Hirano A, Donnenfeld H, et al. Honeycomb-like and aggregated filamentous structures in the anterior horn cells. Electron microscopic study in cases of amyotrophic lateral sclerosis. Neurol Med Chir (Tokyo) 1983;18:298-301
56. Pannese E. Unusual membrane-particle complexes within nerve cells of the spinal ganglia. J Ultrastruct Res 1969;29:334-42
57. Norman MG. Hyaline (Bcolloid[) cytoplasmic inclusions in motoneurons in association with familial microencephaly, retardation and seizures. J Neurol Sci 1974;23:63-70