Iron and ER stress in neurodegenerative disease

BioMetals

Volumn 25, Issue 4, 2012, Pages 837-845

  Liu, Yiting ^a   Connor, James R ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

Adaptive response; Chronic ER stress; Iron; Neurodegeneration

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; FERRITIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; IRON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; X BOX BINDING PROTEIN 1;

ARTICLE; CALCIUM HOMEOSTASIS; CELL FUNCTION; CELL SURVIVAL; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM STRESS; ENZYME RELEASE; GENETIC POLYMORPHISM; HOMEOSTASIS; INNATE IMMUNITY; IRON METABOLISM; NONHUMAN; PEROXIDATION; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; HUMANS; IRON; NEURODEGENERATIVE DISEASES;

EID: 84864913557     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-012-9544-8     Document Type: Article

References (78)

1. Ali-Rahmani F, Hengst JA, Connor JR, Schengrund CL (2011) Effect of HFE variants on sphingolipid expression by SHSY5Y human neuroblastoma cells. Neurochem Res 36: 1687-1696
2. Alizadeh BZ, Njajou OT, Millan MR, Hofman A, Breteler MM, van Duijn CM (2009) HFE variants, APOE and Alzheimer's disease: findings from the population-based Rotterdam study. Neurobiol Aging 30:330-332
3. Badrick AC, Jones CE (2011) Reorganizing metals: the use of chelating compounds as potential therapies for metalrelated neurodegenerative disease. Curr Top Med Chem 11:543-552
4. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2:326-332
5. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92-96
6. Chowdhury I, Tharakan B, Bhat GK (2008) Caspases-an update. Comp Biochem Physiol B Biochem Mol Biol 151: 10-27
7. Combarros O, Garcia-Roman M, Fontalba A, Fernandez-Luna JL, Llorca J, Infante J, Berciano J (2003) Interaction of the H63D mutation in the hemochromatosis gene with the apolipoprotein E epsilon 4 allele modulates age at onset of Alzheimer's disease. Dement Geriatr Cogn Disord 15: 151-154
8. Connor JR, Lee SY (2006) HFE mutations and Alzheimer's disease. J Alzheimers Dis 10:267-276
9. de Almeida SF, Fleming JV, Azevedo JE, Carmo-Fonseca M, de Sousa M (2007a) Stimulation of an unfolded protein response impairs MHC class I expression. J Immunol 178: 3612-3619
10. de Almeida SF, Picarote G, Fleming JV, Carmo-Fonseca M, Azevedo JE, de Sousa M (2007b) Chemical chaperones reduce endoplasmic reticulum stress and prevent mutant HFE aggregate formation. J Biol Chem 282:27905-27912
11. Dekker MC, Giesbergen PC, Njajou OT, van Swieten JC, Hofman A, Breteler MM, van Duijn CM (2003) Mutations in the hemochromatosis gene (HFE), Parkinson's disease and parkinsonism. Neurosci Lett 348:117-119
12. DuRose JB, Tam AB, Niwa M (2006) Intrinsic capacities of molecular sensors of the unfolded protein response to sense alternate forms of endoplasmic reticulum stress. Mol Biol Cell 17:3095-3107
13. Faye A, Ramey G, Foretz M, Vaulont S (2007) Haptoglobin is degraded by iron in C57BL/6 mice: a possible link with endoplasmic reticulum stress. Blood Cells Mol Dis 39:229-237
14. Feder JN, Gnirke A, Thomas W, Tsuchihashi Z, Ruddy DA, Basava A, Dormishian F, Domingo R Jr, Ellis MC, Fullan A et al (1996) A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat Genet 13:399-408
15. Feder JN, Tsuchihashi Z, Irrinki A, Lee VK, Mapa FA, Morikang E, Prass CE, Starnes SM, Wolff RK, Parkkila S et al (1997) The hemochromatosis founder mutation in HLA-H disrupts beta2-microglobulin interaction and cell surface expression. J Biol Chem 272:14025-14028
16. Feder JN, Penny DM, Irrinki A, Lee VK, Lebron JA, Watson N, Tsuchihashi Z, Sigal E, Bjorkman PJ, Schatzman RC (1998) The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding. Proc Natl Acad Sci USA 95:1472-1477
17. Gandin V, Pellei M, Tisato F, Porchia M, Santini C, Marzano C (2012) A novel copper complex induces paraptosis in colon cancer cells via the activation of ER stress signaling. J Cell Mol Med 16:142-151
18. Gao J, Chen J, De Domenico I, Koeller DM, Harding CO, Fleming RE, Koeberl DD, Enns CA (2010) Hepatocytetargeted HFE and TFR2 control hepcidin expression in mice. Blood 115:3374-3381
19. Goodall EF, Greenway MJ, van Marion I, Carroll CB, Hardiman O, Morrison KE (2005) Association of the H63D polymorphism in the hemochromatosis gene with sporadic ALS. Neurology 65:934-937
20. Granados DP, Tanguay PL, Hardy MP, Caron E, de Verteuil D, Meloche S, Perreault C (2009) ER stress affects processing of MHC class I-associated peptides. BMC Immunol 10:10
21. Gregersen N, Bross P (2010) Protein misfolding and cellular stress: an overview. Methods Mol Biol 648:3-23
22. Guerreiro RJ, Bras JM, Santana I, Januario C, Santiago B, Morgadinho AS, Ribeiro MH, Hardy J, Singleton A, Oliveira C (2006) Association of HFE common mutations with Parkinson's disease, Alzheimer's disease and mild cognitive impairment in a Portuguese cohort. BMC Neurol 6:24
23. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274
24. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108
25. He X, Lu X, Hu J, Xi J, Zhou D, Shang H, Liu L, Zhou H, Yan B, Yu L et al (2011) H63D polymorphism in the hemochromatosis gene is associated with sporadic amyotrophic lateral sclerosis in China. Eur J Neurol 18:359-361
26. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, Brandt GS, Iwakoshi NN, Schinzel A, Glimcher LH, Korsmeyer SJ (2006) Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312:572-576
27. Hollien J, Weissman JS (2006) Decay of endoplasmic reticulumlocalized mRNAs during the unfolded protein response. Science 313:104-107
28. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS (2009) Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186:323-331
29. Holmstrom P, Dzikaite V, Hultcrantz R, Melefors O, Eckes K, Stal P, Kinnman N, Smedsrod B, Gafvels M, Eggertsen G (2003) Structure and liver cell expression pattern of the HFE gene in the rat. J Hepatol 39:308-314
30. Ilieva H, Polymenidou M, Cleveland DW (2009) Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J Cell Biol 187:761-772
31. Kaufman RJ (2002) Orchestrating the unfolded protein response in health and disease. J Clin Invest 110:1389-1398
32. Lebron JA, West AP Jr, Bjorkman PJ (1999) The hemochromatosis protein HFE competes with transferrin for binding to the transferrin receptor. J Mol Biol 294:239-245
33. Lee AH, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448-7459
34. Lee SY, Patton SM, Henderson RJ, Connor JR (2007) Consequences of expressingmutants of the hemochromatosis gene (HFE) into a human neuronal cell line lacking endogenous HFE. FASEB J 21(2):564-576
35. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, Lavail MM, Walter P (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318:944-949
36. Lindholm D, Wootz H, Korhonen L (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13:385-392
37. Liu Y, Lee SY, Neely E, Nandar W, Moyo M, Simmons Z, Connor JR (2011) Mutant HFE H63D protein is associated with prolonged ER stress and increased neuronal vulnerability. J Biol Chem 286:13161-13170
38. Malhi H, Kaufman RJ (2011) Endoplasmic reticulum stress in liver disease. J Hepatol 54:795-809
39. Marciniak SJ, Ron D (2006) Endoplasmic reticulum stress signaling in disease. Physiol Rev 86:1133-1149
40. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP, Ron D (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18: 3066-3077
41. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249-1259
42. Mendes CS, Levet C, Chatelain G, Dourlen P, Fouillet A, Dichtel-Danjoy ML, Gambis A, Ryoo HD, Steller H, Mollereau B (2009) ER stress protects from retinal degeneration. EMBO J 28:1296-1307
43. Mitchell RM, Lee SY, Simmons Z, Connor JR (2011) HFE polymorphisms affect cellular glutamate regulation. Neurobiol Aging 32:1114-1123
44. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J (2000) Caspase-12 mediates endoplasmic-reticulum- specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98-103
45. Nandar W, Connor JR (2011) HFE gene variants affect iron in the brain. J Nutr 141:729S-739S
46. Nunez MT, Osorio A, Tapia V, Vergara A, Mura CV (2001) Iron-induced oxidative stress up-regulates calreticulin levels in intestinal epithelial (Caco-2) cells. J Cell Biochem 82:660-665
47. Oliveira SJ, Pinto JP, Picarote G, Costa VM, Carvalho F, Rangel M, de Sousa M, de Almeida SF (2009) ER stress-inducible factor CHOP affects the expression of hepcidin by modulating C/EBPalpha activity. PLoS ONE 4:e6618
48. Oliveira SJ, de Sousa M, Pinto JP (2011) ER stress and iron homeostasis: a new frontier for the UPR. Biochem Res Int 2011:896474
49. Petrak J, Myslivcova D, Man P, Cmejla R, Cmejlova J, Vyoral D, Elleder M, Vulpe CD (2007) Proteomic analysis of hepatic iron overload in mice suggests dysregulation of urea cycle, impairment of fatty acid oxidation, and changes in the methylation cycle. Am J Physiol Gastrointest Liver Physiol 292:G1490-G1498
50. Pulliam JF, Jennings CD, Kryscio RJ, Davis DG, Wilson D, Montine TJ, Schmitt FA, Markesbery WR (2003) Association of HFE mutations with neurodegeneration and oxidative stress in Alzheimer's disease and correlation with APOE. Am J Med Genet B Neuropsychiatr Genet 119B: 48-53
51. Restagno G, Lombardo F, Ghiglione P, Calvo A, Cocco E, Sbaiz L, Mutani R, Chio A (2007) HFE H63D polymorphism is increased in patients with amyotrophic lateral sclerosis of Italian origin. J Neurol Neurosurg Psychiatry 78:327
52. Ristic S, Lovrecic L, Brajenovic-Milic B, Starcevic-Cizmarevic N, Jazbec SS, Sepcic J, Kapovic M, Peterlin B (2005) Mutations in the hemochromatosis gene (HFE) and multiple sclerosis. Neurosci Lett 383:301-304
53. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529
54. Rutkowski DT, Kaufman RJ (2007) That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci 32:469-476
55. Rutkowski DT, Arnold SM, Miller CN, Wu J, Li J, Gunnison KM, Mori K, Sadighi Akha AA, Raden D, Kaufman RJ (2006) Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 4:e374
56. Sado M, Yamasaki Y, Iwanaga T, Onaka Y, Ibuki T, Nishihara S, Mizuguchi H, Momota H, Kishibuchi R, Hashimoto T et al (2009) Protective effect against Parkinson's diseaserelated insults through the activation of XBP1. Brain Res 1257:16-24
57. Salvador GA (2010) Iron in neuronal function and dysfunction. BioFactors 36:103-110
58. Salvador GA, Oteiza PI (2010) Iron overload triggers redoxsensitive signals in human IMR-32 neuroblastoma cells. Neurotoxicology 32:75-82
59. Saxena S, Caroni P (2011) Selective neuronal vulnerability in neurodegenerative diseases: from stressor thresholds to degeneration. Neuron 71:35-48
60. Saxena S, Cabuy E, Caroni P (2009) A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci 12:627-636
61. Schröder M (2007) Endoplasmic reticulum stress responses. Cell Mol Life Sci 65:862-894
62. Shinkai Y, Yamamoto C, Kaji T (2011) Lead induces the expression of endoplasmic reticulum chaperones GRP78 and GRP94 in vascular endothelial cells via the JNK-AP-1 pathway. Toxicol Sci 114:378-386
63. Sutedja NA, Sinke RJ, Van Vught PW, Van der Linden MW, Wokke JH, Van Duijn CM, Njajou OT, Van der Schouw YT, Veldink JH, Van den Berg LH (2007) The association between H63D mutations in HFE and amyotrophic lateral sclerosis in a Dutch population. Arch Neurol 64:63-67
64. Sutedja NA, Fischer K, Veldink JH, van der Heijden GJ, Kromhout H, Heederik D, Huisman MH, Wokke JJ, van den Berg LH (2009) What we truly know about occupation as a risk factor for ALS: a critical and systematic review. Amyotroph Lateral Scler 10:295-301
65. Tabas I, Ron D (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13:184-190
66. Tomatsu S, Orii KO, Fleming RE, Holden CC, Waheed A, Britton RS, Gutierrez MA, Velez-Castrillon S, Bacon BR, Sly WS (2003) Contribution of the H63D mutation in HFE to murine hereditary hemochromatosis. Proc Natl Acad Sci USA 100:15788-15793
67. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-666
68. Vecchi C, Montosi G, Zhang K, Lamberti I, Duncan SA, Kaufman RJ, Pietrangelo A (2009) ER stress controls iron metabolism through induction of hepcidin. Science 325: 877-880
69. Ventura JJ, Hubner A, Zhang C, Flavell RA, Shokat KM, Davis RJ (2006) Chemical genetic analysis of the time course of signal transduction by JNK. Mol Cell 21:701-710
70. Waheed A, Parkkila S, Zhou XY, Tomatsu S, Tsuchihashi Z, Feder JN, Schatzman RC, Britton RS, Bacon BR, Sly WS (1997) Hereditary hemochromatosis: effects of C282Y and H63D mutations on association with beta2-microglobulin, intracellular processing, and cell surface expression of the HFE protein in COS-7 cells. Proc Natl Acad Sci USA 94:12384-12389
71. Wang XS, Lee S, Simmons Z, Boyer P, Scott K, Liu W, Connor J (2004) Increased incidence of the Hfe mutation in amyotrophic lateral sclerosis and related cellular consequences. J Neurol Sci 227:27-33
72. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331
73. Yang Y, Hentati A, Deng HX, Dabbagh O, Sasaki T, Hirano M, Hung WY, Ouahchi K, Yan J, Azim AC et al (2001) The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat Genet 29: 160-165
74. Ye Z, Connor JR (2000) Identification of iron responsive genes by screening cDNA libraries from suppression subtractive hybridization with antisense probes from three iron conditions. Nucleic Acids Res 28:1802-1807
75. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355-1364
76. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881-891
77. You KR, Liu MJ, Han XJ, Lee ZW, Kim DG (2003) Transcriptional regulation of the human transferrin gene by GADD153 in hepatoma cells. Hepatology 38:745-755
78. Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR (2004) Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci 5:863-873