Reduced calreticulin levels link endoplasmic reticulum stress and fas-triggered cell death in motoneurons vulnerable to ALS

Journal of Neuroscience

Volumn 32, Issue 14, 2012, Pages 4901-4912

  Bernard Marissal, Nathalie ^a,b   Moumen, Anice ^a,b   Sunyach, Claire ^a,b   Pellegrino, Christophe ^a,b   Dudley, Keith ^a,b   Henderson, Christopher E ^c   Raoul, Cédric ^a,b,d   Pettmann, Brigitte ^a,b  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c NewYork Presbyterian Hospital   (United States)

^d HÔPITAL SAINT ELOI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALRETICULIN; FAS ANTIGEN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2; NEURON SPECIFIC NUCLEAR PROTEIN; NITRIC OXIDE; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LUMBAR SPINAL CORD; MOTONEURON; MOUSE; MUSCLE DENERVATION; NERVE CRUSH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCIATIC NERVE; TRANSGENIC MOUSE; WESTERN BLOTTING;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIGENS, CD95; CALRETICULIN; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR NEURONS; MUTATION; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84859328507     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/jneurosci.5431-11.2012     Document Type: Article

References (46)

1. Aebischer J, Cassina P, Otsmane B, Moumen A, Seilhean D, Meininger V, Barbeito L, Pettmann B, Raoul C (2011) IFNgamma triggers a LIGHTdependent selective death of motoneurons contributing to the non-cellautonomous effects of mutant SOD1. Cell Death Differ 18:754-768.
2. Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK (2008) Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol Dis 30:400-407.
3. Bergemalm D, Forsberg K, Srivastava V, Graffmo KS, Andersen PM, Brännström T, Wingsle G, Marklund SL (2010) Superoxide dismutase-1 and other proteins in inclusions from transgenic amyotrophic lateral sclerosis model mice. J Neurochem 114:408-418.
4. Boillée S, Vande Velde C, Cleveland DW (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39-59.
5. Bosco DA, Morfini G, Karabacak NM, Song Y, Gros-Louis F, Pasinelli P, Goolsby H, Fontaine BA, Lemay N, McKenna-Yasek D, Frosch MP, Agar JN, Julien JP, Brady ST, Brown RH Jr (2010) Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat Neurosci 13:1396-1403.
6. Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC (2003) Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22:8608-8618.
7. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG, Sisodia SS, Rothstein JD, Borchelt DR, Price DL, Cleveland DW (1997) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18:327-338.
8. Bruijn LI, Miller TM, Cleveland DW (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci 27:723-749.
9. Cashman NR, Durham HD, Blusztajn JK, Oda K, Tabira T, Shaw IT, Dah-rouge S, Antel JP (1992) Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev Dyn 194:209-221.
10. Corbett EF, Michalak KM, Oikawa K, Johnson S, Campbell ID, Eggleton P, Kay C, Michalak M (2000) The conformation of calreticulin is influenced by the endoplasmic reticulum luminal environment. J Biol Chem 275:27177-27185.
11. Duplan L, Bernard N, Casseron W, Dudley K, Thouvenot E, Honnorat J, Rogemond V, De Bovis B, Aebischer P, Marin P, Raoul C, Henderson CE, Pettmann B (2010) Collapsin response mediator protein 4a (CRMP4a) is upregulated in motoneurons of mutant SOD1 mice and can trigger motoneuron axonal degeneration and cell death. J Neurosci 30:785-796.
12. Frey D, Schneider C, Xu L, Borg J, Spooren W, Caroni P (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20:2534-2542.
13. Frost B, Diamond MI (2010) Prion-like mechanisms in neurodegenerative diseases. Nat Rev Neurosci 11:155-159.
14. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264:1772-1775.
15. Ilieva EV, Ayala V, Jové M, Dalfó E, Cacabelos D, Povedano M, Bellmunt MJ, Ferrer I, Pamplona R, Portero-Otín M (2007) Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain 130:3111-3123.
16. Kanning KC, Kaplan A, Henderson CE (2010) Motor neuron diversity in development and disease. Annu Rev Neurosci 33:409-440.
17. Kikuchi H, Almer G, Yamashita S, Guégan C, Nagai M, Xu Z, Sosunov AA, McKhann GM 2nd, Przedborski S (2006) 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 103:6025-6030.
18. Knee R, Ahsan I, Mesaeli N, Kaufman RJ, Michalak M (2003) Compromised calnexin function in calreticulin-deficient cells. Biochem Biophys Res Commun 304:661-666.
19. Langou K, Moumen A, Pellegrino C, Aebischer J, Medina I, Aebischer P, Raoul C (2010) AAV-mediated expression of wild-type and ALS-linked mutant VAPB selectively triggers death of motoneurons through a Ca2+-dependent ER-associated pathway. J Neurochem 114:795-809.
20. Lee JH, Won SM, Suh J, Son SJ, Moon GJ, Park UJ, Gwag BJ (2010) Induction of the unfolded protein response and cell death pathway in Alzheimer's disease, but not in aged Tg2576 mice. Exp MolMed42:386-394.
21. Lessner G, Schmitt O, Haas SJ, Mikkat S, Kreutzer M, Wree A, Glocker MO (2010) Differential proteome of the striatum from hemiparkinsonian rats displays vivid structural remodeling processes. J Proteome Res 9:4671-4687.
22. Magill CK, Tong A, Kawamura D, Hayashi A, Hunter DA, Parsadanian A, Mackinnon SE, Myckatyn TM (2007) Reinnervation of the tibialis anterior following sciatic nerve crush injury: a confocal microscopic study in transgenic mice. Exp Neurol 207:64-74.
23. Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause KH, Opas M, MacLennan DH, Michalak M (1999) Calreticulin is essential for cardiac development. J Cell Biol 144:857-868.
24. Molinari M, Eriksson KK, Calanca V, Galli C, Cresswell P, Michalak M, Helenius A (2004) Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol Cell 13:125-135.
25. Nakamura K, Robertson M, Liu G, Dickie P, Nakamura K, Guo JQ, Duff HJ, Opas M, Kavanagh K, Michalak M (2001) Complete heart block and sudden death in mice overexpressing calreticulin. J Clin Invest 107:1245-1253.
26. Nardo G, Pozzi S, Pignataro M, Lauranzano E, Spano G, Garbelli S, Mantovani S, Marinou K, Papetti L, Monteforte M, Torri V, Paris L, Bazzoni G, Lunetta C, Corbo M, Mora G, Bendotti C, Bonetto V (2011) Amyotrophic lateral sclerosis multiprotein biomarkers in peripheral blood mononuclear cells. PLoS One 6:e25545.
27. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ11:381-389.
28. Perrin FE, Boisset G, Docquier M, Schaad O, Descombes P, Kato AC (2005) No widespread induction of cell death genes occurs in pure motoneurons in an amyotrophic lateral sclerosis mouse model. Hum Mol Genet 14:3309-3320.
29. Pun S, Santos AF, Saxena S, Xu L, Caroni P (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9:408-419.
30. Rao RV, Poksay KS, Castro-Obregon S, Schilling B, Row RH, del Rio G, Gibson BW, Ellerby HM, Bredesen DE (2004) Molecular components of a cell death pathway activated by endoplasmic reticulum stress. J Biol Chem 279:177-187.
31. Raoul C, Henderson CE, Pettmann B (1999) Programmed cell death of embryonic motoneurons triggered through the Fas death receptor. J Cell Biol 147:1049-1062.
32. Raoul C, Estévez AG, Nishimune H, Cleveland DW, de Lapeyrière O, Henderson CE, Haase G, Pettmann B (2002) Motoneuron death triggered by a specific pathway downstream of Fas. potentiation by ALS-linked SOD1 mutations. Neuron 35:1067-1083.
33. Raoul C, Buhler E, Sadeghi C, Jacquier A, Aebischer P, Pettmann B, Henderson CE, Haase G (2006) Chronic activation in presymptomatic amyotrophic lateral sclerosis (ALS) mice of a feedback loop involving Fas, Daxx, and FasL. Proc Natl Acad Sci U S A 103:6007-6012.
34. Roth DM, Balch WE (2011) Modeling general proteostasis: proteome balance in health and disease. Curr Opin Cell Biol 23:126-134.
35. Saxena S, Caroni P (2011) Selective neuronal vulnerability in neurodegenerative diseases: from stressor thresholds to degeneration. Neuron 71:35-48.
36. Saxena S, Cabuy E, Caroni P (2009) A role for motoneuron subtypeselective ER stress in disease manifestations of FALS mice. Nat Neurosci 12:627-636.
37. Smith MJ, Koch GL (1989) Multiple zones in the sequence of calreticulin (CRP55, calregulin, HACBP), a major calcium binding ER/SR protein. EMBO J 8:3581-3586.
38. Taguchi J, Fujii A, Fujino Y, Tsujioka Y, Takahashi M, Tsuboi Y, Wada I, Yamada T (2000) Different expression of calreticulin and immunoglobulin binding protein in Alzheimer's disease brain. Acta Neuropathol 100:153-160.
39. Tarr JM, Young PJ, Morse R, Shaw DJ, Haigh R, Petrov PG, Johnson SJ, Winyard PG, Eggleton P (2010) A mechanism of release of calreticulin from cells during apoptosis. J Mol Biol 401:799-812.
40. Teuling E, Ahmed S, Haasdijk E, Demmers J, Steinmetz MO, Akhmanova A, Jaarsma D, Hoogenraad CC (2007) Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. J Neurosci 27:9801-9815.
41. Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP (2006) Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 9:108-118.
42. Vanselow BK, Keller BU (2000) Calcium dynamics and buffering in oculomotor neurones from mouse that are particularly resistant during amyotrophic lateral sclerosis (ALS)-related motoneurone disease. J Physiol 525:433-445.
43. Verkhratsky A (2002) The endoplasmic reticulum and neuronal calcium signalling. Cell Calcium 32:393-404.
44. Wang HQ, Takahashi R (2007) Expanding insights on the involvement of endoplasmic reticulum stress in Parkinson's disease. Antioxid Redox Signal 9:553-561.
45. Wijesekera LC, Leigh PN (2009) Amyotrophic lateral sclerosis. Orphanet J Rare Dis 4:3.
46. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, Sisodia SS, Cleveland DW, Price DL (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14:1105-1116.