Loss of function of the ALS protein SigR1 leads to ER pathology associated with defective autophagy and lipid raft disturbances

Cell Death and Disease

Volumn 5, Issue 6, 2014, Pages

  Vollrath, J T ^a   Sechi, A ^b   Dreser, A ^a   Katona, I ^a   Wiemuth, D ^a   Vervoorts, J ^b   Dohmen, M ^b   Chandrasekar, A ^a   Prause, J ^a   Brauers, E ^a   Jesse, C M ^a   Weis, J ^a   Goswami, A ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SIGMA OPIATE RECEPTOR; SIGMA RECEPTOR 1; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; CALCIUM; SIGMA-1 RECEPTOR;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; AUTOPHAGY; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FAMILIAL DISEASE; FRONTOTEMPORAL DEMENTIA; GOLGI COMPLEX; HUMAN; HUMAN CELL; LIPID RAFT; MORPHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; ULTRASTRUCTURE; VESICULAR STOMATITIS VIRUS; 3T3 CELL LINE; ANIMAL; CELL MEMBRANE; ENDOPLASMIC RETICULUM; GENETICS; HELA CELL LINE; LYSOSOME; METABOLISM; MOUSE; PATHOLOGY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AUTOPHAGY; CALCIUM; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HELA CELLS; HUMANS; LYSOSOMES; MEMBRANE MICRODOMAINS; MICE; NIH 3T3 CELLS; RECEPTORS, SIGMA;

EID: 84903774616     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.243     Document Type: Article

References (68)

1. Benbrook DM, Long A. Integration of autophagy, proteasomal degradation, unfolded protein response and apoptosis. Exp Oncol 2012; 34: 286-297.
2. Chua CE, Tang BL. Linking membrane dynamics and trafficking to autophagy and the unfolded protein response. J Cell Physiol 2013; 228: 1638-1640.
3. Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007; 14: 1576-1582.
4. Matus S, Glimcher LH, Hetz C. Protein folding stress in neurodegenerative diseases: a glimpse into the ER. Curr Opin Cell Biol 2011; 23: 239-252.
5. Ross CA, Poirier MA. Protein aggregation and neurodegenerative disease. Nat Med 2004; 10(Suppl): S10-S17.
6. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292: 1552-1555.
7. Ciechanover A, Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003; 40: 427-446.
8. Goswami A, Dikshit P, Mishra A, Mulherkar S, Nukina N, Jana NR. Oxidative stress promotes mutant huntingtin aggregation and mutant huntingtin-dependent cell death by mimicking proteasomal malfunction. Biochem Biophys Res Commun 2006; 342: 184-190.
9. Ross CA, Poirier MA. Opinion: What is the role of protein aggregation in neurodegeneration? Nat Rev Mol Cell Biol 2005; 6: 891-898.
10. Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy 2007; 3: 181-206.
11. Mizushima N, Ohsumi Y, Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct Funct 2002; 27: 421-429.
12. Nixon RA. The role of autophagy in neurodegenerative disease. Nat Med 2013; 19: 983-997.
13. Williams A, Jahreiss L, Sarkar S, Saiki S, Menzies FM, Ravikumar B et al. Aggregate-prone proteins are cleared from the cytosol by autophagy: therapeutic implications. Curr Top Dev Biol 2006; 76: 89-101.
14. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 1998; 23: 33-42.
15. Lee S, Sato Y, Nixon RA. Primary lysosomal dysfunction causes cargo-specific deficits of axonal transport leading to Alzheimer-like neuritic dystrophy. Autophagy 2011; 7: 1562-1563.
16. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 2004; 305: 1292-1295.
17. Winslow AR, Chen CW, Corrochano S, Acevedo-Arozena A, Gordon DE, Peden AA et al. alpha-Synuclein impairs macroautophagy: implications for Parkinson's disease. J Cell Biol 2010; 190: 1023-1037.
18. Hayashi T, Su TP. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 2007; 131: 596-610.
19. Al-Saif A, Al-Mohanna F, Bohlega S. A mutation in sigma-1 receptor causes juvenile amyotrophic lateral sclerosis. Ann Neurol 2011; 70: 913-919.
20. Prause J, Goswami A, Katona I, Roos A, Schnizler M, Bushuven E et al. Altered localization, abnormal modification and loss of function of Sigma receptor-1 in amyotrophic lateral sclerosis. Hum Mol Genet 2013; 22: 1581-1600.
21. Mavlyutov TA, Epstein ML, Andersen KA, Ziskind-Conhaim L, Ruoho AE. The sigma-1 receptor is enriched in postsynaptic sites of C-terminals in mouse motoneurons. An anatomical and behavioral study. Neuroscience 2010; 167: 247-255.
22. Mavlyutov TA, Epstein ML, Verbny YI, Huerta MS, Zaitoun I, Ziskind-Conhaim L et al. Lack of sigma-1 receptor exacerbates ALS progression in mice. Neuroscience 2013; 240: 129-134.
23. Mancuso R, Olivan S, Rando A, Casas C, Osta R, Navarro X. Sigma-1R agonist improves motor function and motoneuron survival in ALS mice. Neurotherapeutics 2012; 9: 814-826.
24. Engedal N, Torgersen ML, Guldvik IJ, Barfeld SJ, Bakula D, Saetre F et al. Modulation of intracellular calcium homeostasis blocks autophagosome formation. Autophagy 2013; 9: 1475-1490.
25. Ge L, Melville D, Zhang M, Schekman R. The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. Elife 2013; 2: e00947.
26. Kim J, Huang WP, Stromhaug PE, Klionsky DJ. Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J Biol Chem 2002; 277: 763-773.
27. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-5728.
28. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, Kaushik S et al. In search of an 'autophagomometer'. Autophagy 2009; 5: 585-589.
29. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15: 1101-1111.
30. Carpenter G. Receptors for epidermal growth factor and other polypeptide mitogens. Annu Rev Biochem 1987; 56: 881-914.
31. Derynck R. Transforming growth factor-alpha: structure and biological activities. J Cell Biochem 1986; 32: 293-304.
32. Sorkin A, von Zastrow M. Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 2009; 10: 609-622.
33. Kimura S, Fujita N, Noda T, Yoshimori T. Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol 2009; 452: 1-12.
34. Nehls S, Snapp EL, Cole NB, Zaal KJ, Kenworthy AK, Roberts TH et al. Dynamics and retention of misfolded proteins in native ER membranes. Nat Cell Biol 2000; 2: 288-295.
35. Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ, Lippincott-Schwartz J. ER-to-Golgi transport visualized in living cells. Nature 1997; 389: 81-85.
36. Brazer SC, Singh BB, Liu X, Swaim W, Ambudkar IS. Caveolin-1 contributes to assembly of store-operated Ca2+ influx channels by regulating plasma membrane localization of TRPC1. J Biol Chem 2003; 278: 27208-27215.
37. Isshiki M, Anderson RG. Calcium signal transduction from caveolae. Cell Calcium 1999; 26: 201-208.
38. Hayashi T, Rizzuto R, Hajnoczky G, Su TP. MAM: more than just a housekeeper. Trends Cell Biol 2009; 19: 81-88.
39. Kilsdonk EP, Yancey PG, Stoudt GW, Bangerter FW, Johnson WJ, Phillips MC et al. Cellular cholesterol efflux mediated by cyclodextrins. J Biol Chem 1995; 270: 17250-17256.
40. Shioda N, Ishikawa K, Tagashira H, Ishizuka T, Yawo H, Fukunaga K. Expression of a truncated form of the endoplasmic reticulum chaperone protein, sigma-1 receptor, promotes mitochondrial energy depletion and apoptosis. J Biol Chem 2012; 287: 23318-23331.
41. Aguib Y, Heiseke A, Gilch S, Riemer C, Baier M, Schatzl HM et al. Autophagy induction by trehalose counteracts cellular prion infection. Autophagy 2009; 5: 361-369.
42. Berger Z, Ravikumar B, Menzies FM, Oroz LG, Underwood BR, Pangalos MN et al. Rapamycin alleviates toxicity of different aggregate-prone proteins. Hum Mol Genet 2006; 15: 433-442.
43. Fornai F, Longone P, Cafaro L, Kastsiuchenka O, Ferrucci M, Manca ML et al. Lithium delays progression of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2008; 105: 2052-2057.
44. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441: 885-889.
45. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441: 880-884.
46. Renna M, Jimenez-Sanchez M, Sarkar S, Rubinsztein DC. Chemical inducers of autophagy that enhance the clearance of mutant proteins in neurodegenerative diseases. J Biol Chem 2010; 285: 11061-11067.
47. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010; 141: 1146-1158.
48. Bache KG, Stuffers S, Malerod L, Slagsvold T, Raiborg C, Lechardeur D et al. The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol Biol Cell 2006; 17: 2513-2523.
49. Doyotte A, Russell MR, Hopkins CR, Woodman PG. Depletion of TSG101 forms a mammalian 'Class E' compartment: a multicisternal early endosome with multiple sorting defects. J Cell Sci 2005; 118: 3003-3017.
50. Jiang Y, Mullaney KA, Peterhoff CM, Che S, Schmidt SD, Boyer-Boiteau A et al. Alzheimer's-related endosome dysfunction in Down syndrome is Abeta-independent but requires APP and is reversed by BACE-1 inhibition. Proc Natl Acad Sci USA 2010; 107: 1630-1635.
51. Saxena S, Bucci C, Weis J, Kruttgen A. The small GTPase Rab7 controls the endosomal trafficking and neuritogenic signaling of the nerve growth factor receptor TrkA. J Neurosci 2005; 25: 10930-10940.
52. Yamanaka K, Vande Velde C, Eymard-Pierre E, Bertini E, Boespflug-Tanguy O, Cleveland DW. Unstable mutants in the peripheral endosomal membrane component ALS2 cause early-onset motor neuron disease. Proc Natl Acad Sci USA 2003; 100: 16041-16046.
53. Schmitt-John T, Drepper C, Mussmann A, Hahn P, Kuhlmann M, Thiel C et al. Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the wobbler mouse. Nat Genet 2005; 37: 1213-1215.
54. Skibinski G, Parkinson NJ, Brown JM, Chakrabarti L, Lloyd SL, Hummerich H et al. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 2005; 37: 806-808.
55. Lee JA, Beigneux A, Ahmad ST, Young SG, Gao FB. ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr Biol 2007; 17: 1561-1567.
56. Anderson RG, Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 2002; 296: 1821-1825.
57. Pani B, Ong HL, Liu X, Rauser K, Ambudkar IS, Singh BB. Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of storeoperated Ca2+ entry (SOCE). J Biol Chem 2008; 283: 17333-17340.
58. Sarnataro D, Campana V, Paladino S, Stornaiuolo M, Nitsch L, Zurzolo C. PrP(C) association with lipid rafts in the early secretory pathway stabilizes its cellular conformation. Mol Biol Cell 2004; 15: 4031-4042.
59. Vinten J, Johnsen AH, Roepstorff P, Harpoth J, Tranum-Jensen J. Identification of a major protein on the cytosolic face of caveolae. Biochim Biophys Acta 2005; 1717: 34-40.
60. Shogomori H, Futerman AH. Cholesterol depletion by methyl-beta- cyclodextrin blocks cholera toxin transport from endosomes to the Golgi apparatus in hippocampal neurons. J Neurochem 2001; 78: 991-999.
61. Bezprozvanny I. Calcium signaling and neurodegenerative diseases. Trends Mol Med 2009; 15: 89-100.
62. Fung C, Lock R, Gao S, Salas E, Debnath J. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 2008; 19: 797-806.
63. N'Diaye EN, Kajihara KK, Hsieh I, Morisaki H, Debnath J, Brown EJ. PLIC proteins or ubiquilins regulate autophagy-dependent cell survival during nutrient starvation. EMBO Rep 2009; 10: 173-179.
64. Morita S, Kojima T, Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Therapy 2000; 7: 1063-1066.
65. Usachev Y, Shmigol A, Pronchuk N, Kostyuk P, Verkhratsky A. Caffeine-induced calcium release from internal stores in cultured rat sensory neurons. Neuroscience 1993; 57: 845-859.
66. Schroder JM, Hoheneck M, Weis J, Deist H. Ethylene oxide polyneuropathy: clinical follow-up study with morphometric and electron microscopic findings in a sural nerve biopsy. J Neurol 1985; 232: 83-90.
67. Rapsomaniki MA, Kotsantis P, Symeonidou IE, Giakoumakis NN, Taraviras S, Lygerou Z. easyFRAP: an interactive, easy-to-use tool for qualitative and quantitative analysis of FRAP data. Bioinformatics 2012; 28: 1800-1801.
68. Brauers E, Dreier A, Roos A, Wormland B, Weis J, Kruttgen A. Differential effects of myopathy-associated caveolin-3 mutants on growth factor signaling. Am J Pathol 2010; 177: 261-270.