Calcium-dependent protein folding in amyotrophic lateral sclerosis

Cell Calcium

Volumn 54, Issue 2, 2013, Pages 132-143

  Prell, Tino ^a   Lautenschläger, Janin ^a   Grosskreutz, Julian ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Calcium; Calreticulin; Endoplasmin; Grp78; Protein misfolding; SOD1

Indexed keywords

CALCIUM; CALNEXIN; CALRETICULIN; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; GLYCOSYLATED PROTEIN; PROTEIN DISULFIDE ISOMERASE; SOMATOMEDIN;

AMYOTROPHIC LATERAL SCLEROSIS; CALCIUM BALANCE; CALCIUM BINDING; CALCIUM CELL LEVEL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN; MITOCHONDRION; NERVE CELL DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

MUS;

EID: 84883830112     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2013.05.007     Document Type: Review

References (203)

1. Renton A.E., Majounie E., Waite A., et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
2. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
3. Lautenschlaeger J., Prell T., Grosskreutz J. Endoplasmic reticulum stress and the ER mitochondrial calcium cycle in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis 2012, 13:166-177.
4. Grosskreutz J., Van Den B.L., Keller B.U. Calcium dysregulation in amyotrophic lateral sclerosis. Cell Calcium 2010, 47:165-174.
5. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002, 32:235-249.
6. 2+ regulation of interactions between endoplasmic reticulum chaperones. Journal of Biological Chemistry 1999, 274:6203-6211.
7. Ashby M.C., Tepikin A.V. ER calcium and the functions of intracellular organelles. Seminars in Cell and Developmental Biology 2001, 12:11-17.
8. Coe H., Michalak M. Calcium binding chaperones of the endoplasmic reticulum. General Physiology and Biophysics 2009, 28:F96-F103. (Spec No Focus).
9. Verkhratsky A. Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiological Reviews 2005, 85:201-279.
10. Meissner G. Regulation of mammalian ryanodine receptors. Frontiers in Bioscience 2002, 7:d2072-d2080.
11. Lanner J.T., Georgiou D.K., Joshi A.D., Hamilton S.L. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harbor Perspectives in Biology 2010, 2:a003996.
12. Hammadi M., Oulidi A., Gackiere F., et al. Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: involvement of GRP78. FASEB Journal 2013, 27:1600-1609.
13. Taylor C.W., Tovey S.C. IP(3) receptors: toward understanding their activation. Cold Spring Harbor Perspectives in Biology 2010, 2:a004010.
14. Lipskaia L., Hulot J.S., Lompre A.M. Role of sarco/endoplasmic reticulum calcium content and calcium ATPase activity in the control of cell growth and proliferation. Pflugers Archiv 2009, 457:673-685.
15. Wuytack F., Raeymaekers L., Missiaen L. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 2002, 32:279-305.
16. 2+ pumps of the endoplasmic reticulum and Golgi apparatus. Cold Spring Harbor Perspectives in Biology 2011, 3:3.
17. Rhodes J.D., Sanderson J. The mechanisms of calcium homeostasis and signalling in the lens. Experimental Eye Research 2009, 88:226-234.
18. Gunter T.E., Sheu S.S. Characteristics and possible functions of mitochondrial Ca(2+) transport mechanisms. Biochimica et Biophysica Acta 2009, 1787:1291-1308.
19. 2+ concentration. Current Biology 2006, 16:1672-1677.
20. Pivovarova N.B., Andrews S.B. Calcium-dependent mitochondrial function and dysfunction in neurons. FEBS Journal 2010, 277:3622-3636.
21. Leung A.W., Halestrap A.P. Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochimica et Biophysica Acta 2008, 1777:946-952.
22. Martin L.J. The mitochondrial permeability transition pore: a molecular target for amyotrophic lateral sclerosis therapy. Biochimica et Biophysica Acta 2010, 1802:186-197.
23. 2+ sequestration system. FEBS Journal 2010, 277:3652-3663.
24. 2+ sequestration and precipitation revisited. FEBS Journal 2010, 277:3637-3651.
25. Duffy L.M., Chapman A.L., Shaw P.J., Grierson A.J. The role of mitochondria in the pathogenesis of amyotrophic lateral sclerosis. Neuropathology and Applied Neurobiology 2011, 37:336-352.
26. Van Den Bosch L., Vandenberghe W., Klaassen H., Van Houtte E., Robberecht W. Ca(2+)-permeable AMPA receptors and selective vulnerability of motor neurons. Journal of the Neurological Sciences 2000, 180:29-34.
27. 2+ concentration in transfected neuroblastoma SH-SY5Y cells. FEBS Letters 1997, 414:365-368.
28. Vanselow B.K., Keller B.U. Calcium dynamics and buffering in oculomotor neurones from mouse that are particularly resistant during amyotrophic lateral sclerosis (ALS)-related motoneurone disease. Journal of Physiology 2000, 525(Pt 2):433-445.
29. Kruman I.I., Pedersen W.A., Springer J.E., Mattson M.P. ALS-linked Cu/Zn-SOD mutation increases vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Experimental Neurology 1999, 160:28-39.
30. Bilsland L.G., Nirmalananthan N., Yip J., Greensmith L., Duchen M.R. Expression of mutant SOD1 in astrocytes induces functional deficits in motoneuron mitochondria. Journal of Neurochemistry 2008, 107:1271-1283.
31. 2+ buffering in hypoglossal motoneurons of mutant SOD1 (G93A) mice. Neuroscience Letters 2008, 445:224-228.
32. 2+ homeostasis in SOD1G93A mice. Molecular Pharmacology 2009, 75:478-489.
33. Kuner R., Groom A.J., Muller G., et al. Mechanisms of disease: motoneuron disease aggravated by transgenic expression of a functionally modified AMPA receptor subunit. Annals of the New York Academy of Sciences 2005, 1053:269-286.
34. Kim H.J., Im W., Kim S., et al. Calcium-influx increases SOD1 aggregates via nitric oxide in cultured motor neurons. Experimental and Molecular Medicine 2007, 39:574-582.
35. Van Damme P., Braeken D., Callewaert G., Robberecht W., Van Den B.L. GluR2 deficiency accelerates motor neuron degeneration in a mouse model of amyotrophic lateral sclerosis. Journal of Neuropathology and Experimental Neurology 2005, 64:605-612.
36. Van Damme P., Leyssen M., Callewaert G., Robberecht W., Van Den B.L. The AMPA receptor antagonist NBQX prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis. Neuroscience Letters 2003, 343:81-84.
37. Tateno M., Sadakata H., Tanaka M., et al. Calcium-permeable AMPA receptors promote misfolding of mutant SOD1 protein and development of amyotrophic lateral sclerosis in a transgenic mouse model. Human Molecular Genetics 2004, 13:2183-2196.
38. Beers D.R., Ho B.K., Siklos L., et al. Parvalbumin overexpression alters immune-mediated increases in intracellular calcium, and delays disease onset in a transgenic model of familial amyotrophic lateral sclerosis. Journal of Neurochemistry 2001, 79:499-509.
39. Cozzolino M., Carri M.T. Mitochondrial dysfunction in ALS. Progress in Neurobiology 2012, 97:54-66.
40. Dudek J., Benedix J., Cappel S., et al. Functions and pathologies of BiP and its interaction partners. Cellular and Molecular Life Sciences 2009, 66:1556-1569.
41. Kozutsumi Y., Segal M., Normington K., Gething M.J., Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 1988, 332:462-464.
42. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107:881-891.
43. Korennykh A., Walter P. Structural basis of the unfolded protein response. Annual Review of Cell and Developmental Biology 2012, 28:251-277.
44. Nakagawa T., Zhu H., Morishima N., et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
45. Firtina Z., Duncan M.K. Unfolded protein response (UPR) is activated during normal lens development. Gene Expression Patterns 2011, 11:135-143.
46. Hayashi A., Kasahara T., Iwamoto K., et al. The role of brain-derived neurotrophic factor (BDNF)-induced XBP1 splicing during brain development. Journal of Biological Chemistry 2007, 282:34525-34534.
47. 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. Neurobiology of Disease 2008, 30:400-407.
48. Atkin J.D., Farg M.A., Turner B.J., et al. Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein disulfide isomerase with superoxide dismutase 1. Journal of Biological Chemistry 2006, 281:30152-30165.
49. Oh Y.K., Shin K.S., Yuan J., Kang S.J. Superoxide dismutase 1 mutants related to amyotrophic lateral sclerosis induce endoplasmic stress in neuro2a cells. Journal of Neurochemistry 2008, 104:993-1005.
50. 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. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:6025-6030.
51. Prell T., Lautenschlager J., Witte O.W., Carri M.T., Grosskreutz J. The unfolded protein response in models of human mutant G93A amyotrophic lateral sclerosis. European Journal of Neuroscience 2012, 35:652-660.
52. Saxena S., Cabuy E., Caroni P. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nature Neuroscience 2009, 12:627-636.
53. Mori A., Yamashita S., Uchino K., et al. Derlin-1 overexpression ameliorates mutant SOD1-induced endoplasmic reticulum stress by reducing mutant SOD1 accumulation. Neurochemistry International 2011, 58:344-353.
54. Soo K.Y., Atkin J.D., Farg M., Walker A.K., Horne M.K., Nagley P. Bim links ER stress and apoptosis in cells expressing mutant SOD1 associated with amyotrophic lateral sclerosis. PLoS ONE 2012, 7:e35413.
55. Lodish H.F., Kong N. Perturbation of cellular calcium blocks exit of secretory proteins from the rough endoplasmic reticulum. Journal of Biological Chemistry 1990, 265:10893-10899.
56. Kuznetsov G., Brostrom M.A., Brostrom C.O. Demonstration of a calcium requirement for secretory protein processing and export. Differential effects of calcium and dithiothreitol. Journal of Biological Chemistry 1992, 267:3932-3939.
57. Hebert D.N., Foellmer B., Helenius A. Calnexin and calreticulin promote folding, delay oligomerization and suppress degradation of influenza hemagglutinin in microsomes. EMBO Journal 1996, 15:2961-2968.
58. Borges J.C., Ramos C.H. Protein folding assisted by chaperones. Protein and Peptide Letters 2005, 12:257-261.
59. High S., Lecomte F.J., Russell S.J., Abell B.M., Oliver J.D. Glycoprotein folding in the endoplasmic reticulum: a tale of three chaperones. FEBS Letters 2000, 476:38-41.
60. Brostrom M.A., Brostrom C.O. Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium 2003, 34:345-363.
61. 2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 2002, 32:269-278.
62. 2+, and calcineurin - signaling from the endoplasmic reticulum. Molecules and Cells 2004, 17:383-389.
63. Burdakov D., Petersen O.H., Verkhratsky A. Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium 2005, 38:303-310.
64. Walker A.K., Atkin J.D. Mechanisms of neuroprotection by protein disulphide isomerase in amyotrophic lateral sclerosis. Neurology Research International 2011, 2011:317340.
65. Szydlowska K., Tymianski M. Calcium, ischemia and excitotoxicity. Cell Calcium 2010, 47:122-129.
66. 2+ stores and reveals aspects of their lumenal microenvironment and function. Journal of Cell Biology 1995, 130:847-855.
67. 2+ binding domains. Journal of Biological Chemistry 1991, 266:21458-21465.
68. Nakamura K., Zuppini A., Arnaudeau S., et al. Functional specialization of calreticulin domains. Journal of Cell Biology 2001, 154:961-972.
69. 2+ buffers in the heart. BMB Reports 2010, 43:151-157.
70. Michalak M., Groenendyk J., Szabo E., Gold L.I., Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochemical Journal 2009, 417:651-666.
71. 2+-binding chaperone of the endoplasmic reticulum. International Journal of Biochemistry and Cell Biology 2005, 37:260-266.
72. Hebert D.N., Foellmer B., Helenius A. Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 1995, 81:425-433.
73. Ware F.E., Vassilakos A., Peterson P.A., Jackson M.R., Lehrman M.A., Williams D.B. The molecular chaperone calnexin binds Glc1Man9GlcNAc2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. Journal of Biological Chemistry 1995, 270:4697-4704.
74. Ireland B.S., Brockmeier U., Howe C.M., Elliott T., Williams D.B. Lectin-deficient calreticulin retains full functionality as a chaperone for class I histocompatibility molecules. Molecular Biology of the Cell 2008, 19:2413-2423.
75. Buzzi L.I., Simonetta S.H., Parodi A.J., Castro O.A. The two Caenorhabditis elegans UDP-glucose:glycoprotein glucosyltransferase homologues have distinct biological functions. PLoS ONE 2011, 6:e27025.
76. Trombetta S.E., Parodi A.J. Purification to apparent homogeneity and partial characterization of rat liver UDP-glucose:glycoprotein glucosyltransferase. Journal of Biological Chemistry 1992, 267:9236-9240.
77. D'Alessio C., Caramelo J.J., Parodi A.J. UDP-GlC:glycoprotein glucosyltransferase-glucosidase II, the ying-yang of the ER quality control. Seminars in Cell and Developmental Biology 2010, 21:491-499.
78. Arnaudeau S., Frieden M., Nakamura K., Castelbou C., Michalak M., Demaurex N. Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. Journal of Biological Chemistry 2002, 277:46696-46705.
79. 2+ store depletion. Journal of Biological Chemistry 2000, 275:36676-36682.
80. Molinari M., Helenius A. Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 1999, 402:90-93.
81. Turano C., Gaucci E., Grillo C., Chichiarelli S. ERp57/GRP58: a protein with multiple functions. Cellular and Molecular Biology Letters 2011, 16:539-563.
82. Nardo G., Pozzi S., Pignataro M., et al. Amyotrophic lateral sclerosis multiprotein biomarkers in peripheral blood mononuclear cells. PLoS ONE 2011, 6:e25545.
83. Mesaeli N., Nakamura K., Zvaritch E., et al. Calreticulin is essential for cardiac development. Journal of Cell Biology 1999, 144:857-868.
84. Denzel A., Molinari M., Trigueros C., et al. Early postnatal death and motor disorders in mice congenitally deficient in calnexin expression. Molecular and Cellular Biology 2002, 22:7398-7404.
85. Zhang X., Szabo E., Michalak M., Opas M. Endoplasmic reticulum stress during the embryonic development of the central nervous system in the mouse. International Journal of Developmental Neuroscience 2007, 25:455-463.
86. Knee R., Ahsan I., Mesaeli N., Kaufman R.J., Michalak M. Compromised calnexin function in calreticulin-deficient cells. Biochemical and Biophysical Research Communications 2003, 304:661-666.
87. Perrin F.E., Boisset G., Docquier M., Schaad O., Descombes P., Kato A.C. No widespread induction of cell death genes occurs in pure motoneurons in an amyotrophic lateral sclerosis mouse model. Human Molecular Genetics 2005, 14:3309-3320.
88. Teuling E., Ahmed S., Haasdijk E., et al. Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. Journal of Neuroscience 2007, 27:9801-9815.
89. Corbett E.F., Michalak K.M., Oikawa K., et al. The conformation of calreticulin is influenced by the endoplasmic reticulum luminal environment. Journal of Biological Chemistry 2000, 275:27177-27185.
90. Bergemalm D., Forsberg K., Srivastava V., et al. Superoxide dismutase-1 and other proteins in inclusions from transgenic amyotrophic lateral sclerosis model mice. Journal of Neurochemistry 2010, 114:408-418.
91. Bernard-Marissal N., Moumen A., Sunyach C., et al. Reduced calreticulin levels link endoplasmic reticulum stress and Fas-triggered cell death in motoneurons vulnerable to ALS. Journal of Neuroscience 2012, 32:4901-4912.
92. O'Connor V., El Far O., Bofill-Cardona E., et al. Calmodulin dependence of presynaptic metabotropic glutamate receptor signaling. Science 1999, 286:1180-1184.
93. Minor D.L., Findeisen F. Progress in the structural understanding of voltage-gated calcium channel (CaV) function and modulation. Channels (Austin) 2010, 4:459-474.
94. Zhou L., Zhu D.Y. Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 2009, 20:223-230.
95. Trebak M., Ginnan R., Singer H.A., Jourd'heuil D. Interplay between calcium and reactive oxygen/nitrogen species: an essential paradigm for vascular smooth muscle signaling. Antioxidants and Redox Signalling 2010, 12:657-674.
96. Majava V., Wang C., Myllykoski M., et al. Structural analysis of the complex between calmodulin and full-length myelin basic protein, an intrinsically disordered molecule. Amino Acids 2010, 39:59-71.
97. Gallo D., Jacquot Y., Laurent G., Leclercq G. Calmodulin, a regulatory partner of the estrogen receptor alpha in breast cancer cells. Molecular and Cellular Endocrinology 2008, 291:20-26.
98. Yamaguchi N., Xu L., Pasek D.A., Evans K.E., Chen S.R., Meissner G. Calmodulin regulation and identification of calmodulin binding region of type-3 ryanodine receptor calcium release channel. Biochemistry 2005, 44:15074-15081.
99. Ohrtman J., Ritter B., Polster A., Beam K.G., Papadopoulos S. Sequence differences in the IQ motifs of CaV1.1 and CaV1.2 strongly impact calmodulin binding and calcium-dependent inactivation. Journal of Biological Chemistry 2008, 283:29301-29311.
100. 2+ sensitivity of bound calmodulin. Journal of Biological Chemistry 2009, 284:20041-20051.
101. Min D., Guo F., Zhu S., et al. The alterations of Ca(2+)/calmodulin/CaMKII/Ca(V)1.2 signaling in experimental models of Alzheimer's disease and vascular dementia. Neuroscience Letters 2013.
102. Racioppi L., Means A.R. Calcium/calmodulin-dependent protein kinase kinase 2: roles in signaling and pathophysiology. Journal of Biological Chemistry 2012, 287:31658-31665.
103. Hu J.H., Zhang H., Wagey R., Krieger C., Pelech S.L. Protein kinase and protein phosphatase expression in amyotrophic lateral sclerosis spinal cord. Journal of Neurochemistry 2003, 85:432-442.
104. Liu G., Zhao J., Chang Z., Guo G. CaMKII activates ASK1 to induce apoptosis of spinal astrocytes under oxygen-glucose deprivation. Cellular and Molecular Neurobiology 2013, 33:543-549.
105. Spalloni A., Origlia N., Sgobio C., et al. Postsynaptic alteration of NR2A subunit and defective autophosphorylation of alphaCaMKII at threonine-286 contribute to abnormal plasticity and morphology of upper motor neurons in presymptomatic SOD1G93A mice, a murine model for amyotrophic lateral sclerosis. Cerebral Cortex 2011, 21:796-805.
106. Odagiri K., Katoh H., Kawashima H., et al. Local control of mitochondrial membrane potential, permeability transition pore and reactive oxygen species by calcium and calmodulin in rat ventricular myocytes. Journal of Molecular and Cellular Cardiology 2009, 46:989-997.
107. Matsuda H., Iyanagi T. Calmodulin activates intramolecular electron transfer between the two flavins of neuronal nitric oxide synthase flavin domain. Biochimica et Biophysica Acta 1999, 1473:345-355.
108. Roman L.J., Masters B.S. Electron transfer by neuronal nitric-oxide synthase is regulated by concerted interaction of calmodulin and two intrinsic regulatory elements. Journal of Biological Chemistry 2006, 281:23111-23118.
109. Guan Z.W., Iyanagi T. Electron transfer is activated by calmodulin in the flavin domain of human neuronal nitric oxide synthase. Archives of Biochemistry and Biophysics 2003, 412:65-76.
110. 2+, calmodulin and phospholipids regulate nitricoxide synthase activity in the rabbit submandibular gland. Journal of Comparative Physiology B 2004, 174:593-599.
111. Almer G., Vukosavic S., Romero N., Przedborski S. Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. Journal of Neurochemistry 1999, 72:2415-2425.
112. Hensley K., Abdel-Moaty H., Hunter J., et al. Primary glia expressing the G93A-SOD1 mutation present a neuroinflammatory phenotype and provide a cellular system for studies of glial inflammation. Journal of Neuroinflammation 2006, 3:2.
113. Lee J., Ryu H., Kowall N.W. Differential regulation of neuronal and inducible nitric oxide synthase (NOS) in the spinal cord of mutant SOD1 (G93A) ALS mice. Biochemical and Biophysical Research Communications 2009, 387:202-206.
114. Martin L.J., Liu Z., Chen K., et al. Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: mechanisms of mitochondriopathy and cell death. Journal of Comparative Neurology 2007, 500:20-46.
115. Chen K., Northington F.J., Martin L.J. Inducible nitric oxide synthase is present in motor neuron mitochondria and Schwann cells and contributes to disease mechanisms in ALS mice. Brain Structure and Function 2010, 214:219-234.
116. Bernardi P., Krauskopf A., Basso E., et al. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS Journal 2006, 273:2077-2099.
117. Mitochondrial Martin L.J. Cell death mechanisms in neurodegenerative diseases. Pharmaceuticals (Basel) 2010, 3:839-915.
118. Waldmeier P.C., Zimmermann K., Qian T., Tintelnot-Blomley M., Lemasters J.J. Cyclophilin D as a drug target. Current Medicinal Chemistry 2003, 10:1485-1506.
119. Martin L.J., Gertz B., Pan Y., Price A.C., Molkentin J.D., Chang Q. The mitochondrial permeability transition pore in motor neurons: involvement in the pathobiology of ALS mice. Experimental Neurology 2009, 218:333-346.
120. Grimm S., Brdiczka D. The permeability transition pore in cell death. Apoptosis 2007, 12:841-855.
121. Ferri A., Gabbianelli R., Casciati A., Celsi F., Rotilio G., Carri M.T. Oxidative inactivation of calcineurin by Cu,Zn superoxide dismutase G93A, a mutant typical of familial amyotrophic lateral sclerosis. Journal of Neurochemistry 2001, 79:531-538.
122. Ferri A., Nencini M., Battistini S., et al. Activity of protein phosphatase calcineurin is decreased in sporadic and familial amyotrophic lateral sclerosispatients. Journal of Neurochemistry 2004, 90:1237-1242.
123. Ferri A., Gabbianelli R., Casciati A., Paolucci E., Rotilio G., Carri M.T. Calcineurin activity is regulated both by redox compounds and by mutant familial amyotrophic lateral sclerosis-superoxide dismutase. Journal of Neurochemistry 2000, 75:606-613.
124. Namgaladze D., Hofer H.W., Ullrich V. Redox control of calcineurin by targeting the binuclear Fe(2+)-Zn(2+) center at the enzyme active site. Journal of Biological Chemistry 2002, 277:5962-5969.
125. Volkel H., Scholz M., Link J., et al. Superoxide dismutase mutations of familial amyotrophic lateral sclerosis and the oxidative inactivation of calcineurin. FEBS Letters 2001, 503:201-205.
126. Marzec M., Eletto D., Argon Y.G.R.P94. An HSP90-like protein specialized for protein folding and quality control in the endoplasmic reticulum. Biochimica et Biophysica Acta 2011, 1823:774-787.
127. Ostrovsky O., Eletto D., Makarewich C., Barton E.R., Argon Y. Glucose regulated protein 94 is required for muscle differentiation through its control of the autocrine production of insulin-like growth factors. Biochimica Biophysica Acta 2010, 1803:333-341.
128. Ostrovsky O., Ahmed N.T., Argon Y. The chaperone activity of GRP94 toward insulin-like growth factor II is necessary for the stress response to serum deprivation. Molecular Biology of the Cell 2009, 20:1855-1864.
129. Eletto D., Dersh D., Argon Y. GRP94 in ER quality control and stress responses. Seminars in Cell and Developmental Biology 2010, 21:479-485.
130. Marzec M., Eletto D., Argon Y. GRP94. An HSP90-like protein specialized for protein folding and quality control in the endoplasmic reticulum. Biochimica Biophysica Acta 2012, 1823:774-787.
131. Badiola N., Penas C., Minano-Molina A., et al. Induction of ER stress in response to oxygen-glucose deprivation of cortical cultures involves the activation of the PERK and IRE-1 pathways and of caspase-12. Cell Death and Disease 2011, 2:e149.
132. Mao C., Wang M., Luo B., et al. Targeted mutation of the mouse Grp94 gene disrupts development and perturbs endoplasmic reticulum stress signaling. PLoS ONE 2010, 5:e10852.
133. Dejeans N., Tajeddine N., Beck R., et al. Endoplasmic reticulum calcium release potentiates the ER stress and cell death caused by an oxidative stress in MCF-7 cells. Biochemical Pharmacology 2010, 79:1221-1230.
134. Bull V.H., Thiede B. Proteome analysis of tunicamycin-induced ER stress. Electrophoresis 2012, 33:1814-1823.
135. Biswas C., Ostrovsky O., Makarewich C.A., Wanderling S., Gidalevitz T., Argon Y. The peptide-binding activity of GRP94 is regulated by calcium. Biochemical Journal 2007, 405:233-241.
136. 2+. FEBS Journal 2006, 273:513-522.
137. Hu M.C., Gong H.Y., Lin G.H., et al. XBP-1, a key regulator of unfolded protein response, activates transcription of IGF1 and Akt phosphorylation in zebrafish embryonic cell line. Biochemical and Biophysical Research Communications 2007, 359:778-783.
138. Marchand A., Tomkiewicz C., Magne L., Barouki R., Garlatti M. Endoplasmic reticulum stress induction of insulin-like growth factor-binding protein-1 involves ATF4. Journal of Biological Chemistry 2006, 281:19124-19133.
139. Novosyadlyy R., Kurshan N., Lann D., Vijayakumar A., Yakar S., LeRoith D. Insulin-like growth factor-I protects cells from ER stress-induced apoptosis via enhancement of the adaptive capacity of endoplasmic reticulum. Cell Death and Differentiation 2008, 15:1304-1317.
140. Pu S.F., Zhuang H.X., Marsh D.J., Ishii D.N. Insulin-like growth factor-II increases and IGF is required for postnatal rat spinal motoneuron survival following sciatic nerve axotomy. Journal of Neuroscience Research 1999, 55:9-16.
141. Koopmans G.C., Brans M., Gomez-Pinilla F., et al. Circulating insulin-like growth factor I and functional recovery from spinal cord injury under enriched housing conditions. European Journal of Neuroscience 2006, 23:1035-1046.
142. Pellecchia M.T., Pivonello R., Monsurro M.R., et al. The GH-IGF system in amyotrophic lateral sclerosis: correlations between pituitary GH secretion capacity, insulin-like growth factors and clinical features. European Journal of Neurology 2010, 17:666-671.
143. Hosback S., Hardiman O., Nolan C.M., et al. Circulating insulin-like growth factors and related binding proteins are selectively altered in amyotrophic lateral sclerosis and multiple sclerosis. Growth Hormone and IGF Research 2007, 17:472-479.
144. Bilic E., Bilic E., Rudan I., et al. Comparison of the growth hormone, IGF-1 and insulin in cerebrospinal fluid and serum between patients with motor neuron disease and healthy controls. European Journal of Neurology 2006, 13:1340-1345.
145. Reinhardt R.R., Bondy C.A. Insulin-like growth factors cross the blood-brain barrier. Endocrinology 1994, 135:1753-1761.
146. Nagano I., Ilieva H., Shiote M., et al. Therapeutic benefit of intrathecal injection of insulin-like growth factor-1 in a mouse model of Amyotrophic Lateral Sclerosis. Journal of the Neurological Sciences 2005, 235:61-68.
147. Borasio G.D., Robberecht W., Leigh P.N., et al. A placebo-controlled trial of insulin-like growth factor-I in amyotrophic lateral sclerosis. European ALS/IGF-I Study Group. Neurology 1998, 51:583-586.
148. Lai E.C., Felice K.J., Festoff B.W., et al. Effect of recombinant human insulin-like growth factor-I on progression of ALS. A placebo-controlled study. The North America ALS/IGF-I Study Group. Neurology 1997, 49:1621-1630.
149. Neumann M., Sampathu D.M., Kwong L.K., et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
150. Mackenzie I.R., Rademakers R., Neumann M. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurology 2010, 9:995-1007.
151. 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. Human Molecular Genetics 2011, 20:1952-1965.
152. Feng H.L., Leng Y., Ma C.H., Zhang J., Ren M., Chuang D.M. Combined lithium and valproate treatment delays disease onset, reduces neurological deficits and prolongs survival in an amyotrophic lateral sclerosis mouse model. Neuroscience 2008, 155:567-572.
153. Sugai F., Yamamoto Y., Miyaguchi K., et al. Benefit of valproic acid in suppressing disease progression of ALS model mice. European Journal of Neuroscience 2004, 20:3179-3183.
154. Piepers S., Veldink J.H., de Jong S.W., et al. Randomized sequential trial of valproic acid in amyotrophic lateral sclerosis. Annals of Neurology 2009, 66:227-234.
155. Bown C.D., Wang J.F., Chen B., Young L.T. Regulation of ER stress proteins by valproate: therapeutic implications. Bipolar Disorders 2002, 4:145-151.
156. Shiu R.P., Pouyssegur J., Pastan I. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proceedings of the National Academy of Sciences of the United States of America 1977, 74:3840-3844.
157. Jiang J., Prasad K., Lafer E.M., Sousa R. Structural basis of interdomain communication in the Hsc70 chaperone. Molecular Cell 2005, 20:513-524.
158. 2+. Journal of Biological Chemistry 1997, 272:30873-30879.
159. 2+ binding site on GRP78 is differentially enhanced by ADP and ATP. Journal of Biological Chemistry 2006, 281:8796-8805.
160. Suzuki C.K., Bonifacino J.S., Lin A.Y., Davis M.M., Klausner R.D. Regulating the retention of T-cell receptor alpha chain variants within the endoplasmic reticulum: Ca(2+)-dependent association with BiP. Journal of Cell Biology 1991, 114:189-205.
161. Hamman B.D., Hendershot L.M., Johnson A.E. BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 1998, 92:747-758.
162. Alder N.N., Shen Y., Brodsky J.L., Hendershot L.M., Johnson A.E. The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum. Journal of Cell Biology 2005, 168:389-399.
163. Pfaffenbach K.T., Lee A.S. The critical role of GRP78 in physiologic and
164. Inageda K. Insulin modulates induction of glucose-regulated protein 78 during endoplasmic reticulum stress via augmentation of ATF4 expression in human neuroblastoma cells. FEBS Letters 2010, 584:3649-3654.
165. 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 COS7 cells and transgenic mice. Biochemical and Biophysical Research Communications 2003, 303:496-503.
166. Sasaki S. Endoplasmic reticulum stress in motor neurons of the spinal cord in sporadic amyotrophic lateral sclerosis. Journal of Neuropathology and Experimental Neurology 2010, 69:346-355.
167. Ilieva E.V., Ayala V., Jove M., et al. Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain 2007, 130:3111-3123.
168. Kieran D., Woods I., Villunger A., Strasser A., Prehn J.H. Deletion of the BH3-only protein puma protects motoneurons from ER stress-induced apoptosis and delays motoneuron loss in ALS mice. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:20606-20611.
169. Nagata T., Ilieva H., Murakami T., et al. Increased ER stress during motor neuron degeneration in a transgenic mouse model of amyotrophic lateral sclerosis. Neurological Research 2007, 29:767-771.
170. Wootz H., Hansson I., Korhonen L., Napankangas U., Lindholm D. Caspase-12 cleavage and increased oxidative stress during motoneuron degeneration in transgenic mouse model of ALS. Biochemical and Biophysical Research Communications 2004, 322:281-286.
171. Wate R., Ito H., Zhang J.H., Ohnishi S., Nakano S., Kusaka H. Expression of an endoplasmic reticulum-resident chaperone, glucose-regulated stress protein 78, in the spinal cord of a mouse model of amyotrophic lateral sclerosis. Acta Neuropathologica 2005, 110:557-562.
172. Lee S.O., Cho K., Cho S., Kim I., Oh C., Ahn K. Protein disulphide isomerase is required for signal peptide peptidase-mediated protein degradation. EMBO Journal 2010, 29:363-375.
173. Laurindo F.R., Pescatore L.A., Fernandes D.C. Protein disulfide isomerase in redox cell signaling and homeostasis. Free Radical Biology and Medicine 2012, 52:1954-1969.
174. Sevier C.S., Kaiser C.A. Ero1 and redox homeostasis in the endoplasmic reticulum. Biochimica Biophysica Acta 2008, 1783:549-556.
175. Ramming T., Appenzeller-Herzog C. The physiological functions of mammalian endoplasmic oxidoreductin 1: on disulfides and more. Antioxidants and Redox Signalling 2012, 16:1109-1118.
176. Benham A.M., van Lith M., Sitia R., Braakman I. Ero1-PDI interactions, the response to redox flux and the implications for disulfide bond formation in the mammalian endoplasmic reticulum. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2013, 368:20110403.
177. Merksamer P.I., Trusina A., Papa F.R. Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 2008, 135:933-947.
178. Denisov A.Y., Maattanen P., Dabrowski C., Kozlov G., Thomas D.Y., Gehring K. Solution structure of the bb' domains of human protein disulfide isomerase. FEBS Journal 2009, 276:1440-1449.
179. Jessop C.E., Watkins R.H., Simmons J.J., Tasab M., Bulleid N.J. Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. Journal of Cell Science 2009, 122:4287-4295.
180. Zapun A., Darby N.J., Tessier D.C., Michalak M., Bergeron J.J., Thomas D.Y. Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. Journal of Biological Chemistry 1998, 273:6009-6012.
181. Jonsson P.A., Graffmo K.S., Andersen P.M., et al. Disulphide-reduced superoxide dismutase-1 in CNS of transgenic amyotrophic lateral sclerosis models. Brain 2006, 129:451-464.
182. Niwa J., Yamada S., Ishigaki S., et al. Disulfide bond mediates aggregation, toxicity, and ubiquitylation of familial amyotrophic lateral sclerosis-linked mutant SOD1. Journal of Biological Chemistry 2007, 282:28087-28095.
183. Cozzolino M., Amori I., Pesaresi M.G., Ferri A., Nencini M., Carri M.T. Cysteine 111 affects aggregation and cytotoxicity of mutant Cu,Zn-superoxide dismutase associated with familial amyotrophic lateral sclerosis. Journal of Biological Chemistry 2008, 283:866-874.
184. Furukawa Y., Fu R., Deng H.X., Siddique T., O'Halloran T.V. Disulfide cross-linked protein represents a significant fraction of ALS-associated Cu, Zn-superoxide dismutase aggregates in spinal cords of model mice. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:7148-7153.
185. Turner B.J., Atkin J.D., Farg M.A., et al. Impaired extracellular secretion of mutant superoxide dismutase 1 associates with neurotoxicity in familial amyotrophic lateral sclerosis. Journal of Neuroscience 2005, 25:108-117.
186. Soo K.Y., Atkin J.D., Horne M.K., Nagley P. Recruitment of mitochondria into apoptotic signaling correlates with the presence of inclusions formed by amyotrophic lateral sclerosis-associated SOD1 mutations. Journal of Neurochemistry 2009, 108:578-590.
187. Matsumoto G., Stojanovic A., Holmberg C.I., Kim S., Morimoto R.I. Structural properties and neuronal toxicity of amyotrophic lateral sclerosis-associated Cu/Zn superoxide dismutase 1 aggregates. Journal of Cell Biology 2005, 171:75-85.
188. Kabuta T., Suzuki Y., Wada K. Degradation of amyotrophic lateral sclerosis-linked mutant Cu,Zn-superoxide dismutase proteins by macroautophagy and the proteasome. Journal of Biological Chemistry 2006, 281:30524-30533.
189. 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.
190. Uehara T. Accumulation of misfolded protein through nitrosative stress linked to neurodegenerative disorders. Antioxidants and Redox Signalling 2007, 9:597-601.
191. Walker A.K. Protein disulfide isomerase and the endoplasmic reticulum in amyotrophic lateral sclerosis. Journal of Neuroscience 2010, 30:3865-3867.
192. Gavrin L.K., Denny R.A., Saiah E. Small molecules that target protein misfolding. Journal of Medicinal Chemistry 2012, 55:10823-10843.
193. Suh D.H., Kim M.K., Kim H.S., Chung H.H., Song Y.S. Unfolded protein response to autophagy as a promising druggable target for anticancer therapy. Annals of the New York Academy of Sciences 2012, 1271:20-32.
194. Lee A.H., Iwakoshi N.N., Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Molecular and Cellular Biology 2003, 23:7448-7459.
195. Sriburi R., Jackowski S., Mori K., Brewer J.W. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. Journal of Cell Biology 2004, 167:35-41.
196. Hetz C., Lee A.H., Gonzalez-Romero D., et al. Unfolded protein response transcription factor XBP-1 does not influence prion replication or pathogenesis. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:757-762.
197. Matus S., Lisbona F., Torres M., Leon C., Thielen P., Hetz C. The stress rheostat: an interplay between the unfolded protein response (UPR) and autophagy in neurodegeneration. Current Molecular Medicine 2008, 8:157-172.
198. Parker R., Phan T., Baumeister P., et al. Identification of TFII-I as the endoplasmic reticulum stress response element binding factor ERSF: its autoregulation by stress and interaction with ATF6. Molecular and Cellular Biology 2001, 21:3220-3233.
199. Thuerauf D.J., Marcinko M., Belmont P.J., Glembotski C.C. Effects of the isoform-specific characteristics of ATF6 alpha and ATF6 beta on endoplasmic reticulum stress response gene expression and cell viability. Journal of Biological Chemistry 2007, 282:22865-22878.
200. Thuerauf D.J., Morrison L., Glembotski C.C. Opposing roles for ATF6alpha and ATF6beta in endoplasmic reticulum stress response gene induction. Journal of Biological Chemistry 2004, 279:21078-21084.
201. Wang Y., Shen J., Arenzana N., Tirasophon W., Kaufman R.J., Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. Journal of Biological Chemistry 2000, 275:27013-27020.
202. Ellgaard L., Helenius A. Quality control in the endoplasmic reticulum. Nature Reviews Molecular Cell Biology 2003, 4:181-191.
203. Caramelo J.J., Parodi A.J. Getting in and out from calnexin/calreticulin cycles. Journal of Biological Chemistry 2008, 283:10221-10225.