Mice overexpressing both non-mutated human SOD1 and mutated SOD1G93A genes: A competent experimental model for studying iron metabolism in amyotrophic lateral sclerosis

Frontiers in Molecular Neuroscience

Volumn 8, Issue JAN2016, 2016, Pages

  Gajowiak, Anna ^a   Styiś, Agnieszka ^a   Starzyński, Rafał R ^a   Bednarz, Aleksandra ^b   Lenartowicz, Małgorzata ^b   Staroń, Robert ^a   Lipmski, Paweł ^a  

^a INSTITUTE OF GENETICS AND ANIMAL BREEDING   (Poland)

^b JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Als; G93A; Heme oxygenase 1; Iron; Neurons; Oxidative stress; Skeletal muscle; SOD1

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; FERRITIN; H FERRITIN; HEME OXYGENASE 1; IRON REGULATORY PROTEIN 1; L FERRITIN; RNA 18S; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPPER ZINC SUPEROXIDE DISMUTASE GENE; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; GEL ELECTROPHORESIS; GENE; GENE OVEREXPRESSION; HISTOLOGY; IMMUNOREACTIVITY; IRON METABOLISM; MALE; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SPINAL CORD; WESTERN BLOTTING;

EID: 84957900504     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2015.00082     Document Type: Article

References (58)

1. Atkin, J. D., Scott, R. L., West, J. M., Lopes, E., Quah, A. K., and Cheema, S. S. (2005 Properties of slow- and fast-twitch muscle fibres in a mouse model of amyotrophic lateral sclerosis). Neuromuscul Disord. 2005, 377-388. doi: 10.1016/j.nmd.2005.02.005
2. Balla, G., Jacob, H. S., Balla, J., Rosenberg, M., Nath, K., Apple, F., et al. (1992). Ferritin: a cytoprotective antioxidant strategem of endothelium. J. Biol. Chem 267, 18148-18153
3. Barber, S. C., Mead, R. J., and Shaw, P. J. (2006). Oxidative stress in ALS: a mechanism of neurodegeneration and a therapeutic target. Biochim. Biophys. Acta 1762, 1051-1067. doi: 10.1016/j.bbadis.2006.03.008
4. Beauchamp, C., and Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276-287. doi: 10.1016/0003-2697(71)90370-8
5. Bouton, C., Chauveau, M. J., Lazereg, S., and Drapier, J. C. (2002). Recycling of RNA binding iron regulatory protein 1 into an aconitase after nitric oxide removal depends on mitochondrial ATP. J. Biol. Chem. 277, 31220-31227. doi: 10.1074/jbc.M203276200
6. Canonne-Hergaux, F., Gruenheid, S., Ponka, P., and Gros, P. (1999). Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood 93, 4406-4417
7. Carri, M. T., Ferri, A., Cozzolino, M., Calabrese, L., and Rotilio, G. (2003). Neurodegeneration in amyotrophic lateral sclerosis: the role of oxidative stress and altered homeostasis of metals. Brain Res. Bull. 61, 365-374. doi: 10.1016/S0361-9230(03)00179-5
8. Conti, A., Iannaccone, S., Sferrazza, B., De Monte, L., Cappa, S., Franciotta, D., et al. (2008). Differential expression of ceruloplasmin isoforms in the cerebrospinal fluid of amyotrophic lateral sclerosis patients. Proteomics Clin. Appl. 2, 1628-1637. doi:10.1002/prca.200780081
9. Danzeisen, R., Achsel, T., Bederke, U., Cozzolino, M., Crosio, C., Ferri, A., et al. (2006). Superoxide dismutase 1 modulates expression of transferrin receptor. J. Biol Inorg Chem. 11,489-498. doi: 10.1007/s00775-006-0099-4
10. De Domenico, I., Vaughn, M. B., Li, L., Bagley, D., Musci, G., Ward, D. M., et al. (2006). Ferroportin-mediated mobilization of ferritin iron precedes ferritin degradation by the proteasome. EMBO J. 25, 5396-5404. doi: 10.1038/sj.emboj.7601409
11. Dobrowolny, G., Aucello, M., Rizzuto, E., Beccafico, S., Mammucari, C., Boncompagni, S., et al. (2008). Skeletal muscle is a primary target of SŒD1G93A-mediated toxicity. Cell Metab. 8, 425-436. doi: 10.1016/j.cmet.2008.09.002
12. Dwyer, B. E., Lu, S. Y., and Nishimura, R. N. (1998). Heme oxygenase in the experimental ALS mouse. Exp. Neurol. 150, 206-212. doi: 10.1006/exnr.1997.6763
13. Ganz, T., and Nemeth, E. (2012). Hepcidin andiron homeostasis. Biochim. Biophys. Acta 1823, 1434-1443. doi:10.1016/j.bbamcr.2012.01.014
14. Gozzelino, R., and Soares, M. P. (2014). Coupling heme and iron metabolism via ferritin H chain. Antioxid. Redox Signal. 20, 1754-1769. doi: 10.1089/ars.2013.5666
15. Grochot-Przeczek, A., Dulak, J., and Jozkowicz, A. (2012). Haem oxygenase-1: non-canonical roles in physiology and pathology. Clin. Sci. (Lond.) 122, 93-103. doi: 10.1042/CS20110147
16. Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., et al. (1994). Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775. doi: 10.1126/science.8209258
17. Hadzhieva, M., Kirches, E., and Mawrin, C. (2014). Review: iron metabolism and the role of iron in neurodegenerative disorders. Neuropathol. Appl. Neurobiol. 40, 240-257. doi: 10.1111/nan.12096
18. Hadzhieva, M., Kirches, E., Wilisch-Neumann, A., Pachow, D., Wallesch, M., Schoenfeld, P., et al. (2013). Dysregulation of iron protein expression in the G93A model of amyotrophic lateral sclerosis. Neuroscience 230, 94-101. doi: 10.1016/j.neuroscience.2012.11.021
19. Halon, M., Kaczor, J. J., Ziolkowski, W., Flis, D. J., Borkowska, A., Popowska, U., et al. (2014). Changes in skeletal muscle iron metabolism outpace amyotrophic lateral sclerosis onset in transgenic rats bearing the G93A hmSOD1 gene mutation. Free Radic. Res. 48, 1363-1370. doi: 10.3109/10715762.2014.955484
20. Halon, M., Sielicka-Dudzin, A., Wozniak, M., Ziolkowski, W., Nyka, W., Herbik, M., et al. (2010). Up-regulation of ferritin ubiquitination in skeletal muscle of transgenic rats bearing the G93A hmSOD1 gene mutation. Neuromuscul. Disord. 20, 29-33. doi: 10.1016/j.nmd.2009.08.014
21. Harrison, P. M., and Arosio, P. (1996). The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275, 161-203. doi: 10.1016/0005-2728(96)00022-9
22. Hellman, N. E., and Gitlin, J. D. (2002). Ceruloplasmin metabolism and function. Annu. Rev. Nutr. 22, 439-458. doi: 10.1146/annurev.nutr.22.012502.114457
23. Ignjatovic, A., Stevic, Z., Lavrnic, S., Dakovic, M., and Bačic, G. (2013). Brain iron MRI: a biomarker for amyotrophic lateral sclerosis. J. Magn. Reson. Imaging 38, 1472-1479. doi: 10.1002/jmri.24121
24. Jeong, S. Y., Rathore, K. I., Schulz, K., Ponka, P., Arosio, P., and David, S. (2009) Dysregulation of iron homeostasis in the CNS contributes to disease progression in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 29, 610-619. doi: 10.1523/JNEUROSCI.5443-08.2009
25. Kasarskis, E. J., Tandon, L., Lovell, M. A., and Ehmann, W. D. (1995). Aluminum, calcium, and iron in the spinal cord of patients with sporadic amyotrophic lateral sclerosis using laser microprobe mass spectroscopy: a preliminary study. J. Neurol. Sci. 130, 203-208. doi: 10.1016/0022-510X(95)00037-3
26. Kovtunovych, G., Eckhaus, M. A., Ghosh, M. C., 이livierre-Wilson, H., and Rouault, T. A. (2010). Dysfunction of the heme recycling system in heme oxygenase 1-deficient mice: effects on macrophage viability and tissue iron distribution. Blood 116, 6054-6062. doi: 10.1182/blood-2010-03-272138
27. Kupershmidt, L., Weinreb, ᄋ., Amit, T., Mandel, S., Carri, M. T., and Youdim, M. B. (2009). Neuroprotective and neuritogenic activities of novel multimodal iron-chelating drugs in motor-neuron-like NSC-34 cells and transgenic mouse model of amyotrophic lateral sclerosis. FASEB J. 23, 3766-3779. doi: 10.1096/fj.09-130047
28. Kwan, J. Y., Jeong, S. Y., Van Gelderen, P., Deng, H. X., Quezado, M. M., Danielian, L. E., et al. (2012). Iron accumulation in deep cortical layers accounts for MRI signal abnormalities in ALS: correlating 7 tesla MRI and pathology. PLoS ONE 7:e35241. doi:10.1371/journal.pone.0035241
29. Lee, J. K., Shin, J. H., Gwag, B. J., and Choi, E. J. (2015). Iron accumulation promotes TACE-mediated TNF-a secretion and neurodegeneration in a mouse model of ALS. Neurobiol. Dis. 80, 63-69. doi: 10.1016/j.nbd.2015.05.009
30. Lee, M. H., Hyun, D.-H., Jenner, P., and Halliwell, B. (2001). Effect of overexpression of wild-type and mutant Cu/Zn-superoxide dismutases on oxidative damage and antioxidant defences: relevance to Down's syndrome and familial amyotrophic lateral sclerosis. J. Neurochem. 76, 957-965. doi: 10.1046/j.1471-4159.2001.00107.x
31. Léger, B., Vergani, L., Sorarù, G., Hespel, P., Derave, W., Gobelet, C., et al. (2006). Human skeletal muscle atrophy in amyotrophic lateral sclerosis reveals a reduction in Akt and an increase in atrogin-1. F ASEB J. 20, 583-585
32. Lipinski, P., Drapier, J. C., Oliveira, L., Retmańska, H., Sochanowicz, B., and Kruszewski, M. (2000). Intracellular iron status as a hallmark of mammalian cell susceptibility to oxidative stress: a study of L5178Y mouse lymphoma cell lines differentially sensitive to H(2)O(2). Blood 95, 2960-2966
33. M artins, E. A., Robalinho, R. L., and Meneghini, R. (1995). Oxidative stress induces activation of a cytosolic protein responsible for control of iron uptake. Arch. Biochem. Biophys. 316, 128-134. doi: 10.1006/abbi.1995.1019
34. Massignan, T., Casoni, F., Basso, M., Stefanazzi, P., Biasini, E., Tortarolo, M., et al. (2007). Proteomic analysis of spinal cord of presymptomatic amyotrophic lateral sclerosis G93A SOD1 mouse. Biochem. Biophys. Res. Commun. 353, 719-725. doi: 10.1016/j.bbrc.2006.12.075
35. McCord, J. M., and Fridovich, I. (1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244, 6049-6055
36. M issirlis, F., Hu, J., Kirby, K., Hilliker, A. J., Rouault, T. A., and Phillips, J. (2003). Compartment-specific protection of iron-sulfur proteins by superoxide dismutase. J. Biol. Chem. 278, 47365-47369. doi: 10.1074/jbc.M307700200
37. Mitchell, R. M., Simmons, Z., Beard, J. L., Stephens, H. E., and Connor, J. R. (2010) Plasma biomarkers associated with ALS and their relationship to iron homeostasis. Muscle Nerve 42, 95-103. doi: 10.1002/mus.21625
38. Orino, K., Lehman, L., Tsuji, Y., Ayaki, H., Torti, S. V., and Torti, F. M. (2001). Ferritin and the response to oxidative stress. Biochem. J. 357, 241-247. doi: 10.1042/bj3570241
39. Oshiro, S., Morioka, M. S., and Kikuchi, M. (2011). Dysregulation of iron metabolism in Alzheimer's disease, Parkinson's disease, and amyotrophic lateral sclerosis. Adv. Pharmacol. Sci. 2011:378278. doi: 10.1155/2011/378278
40. Pansarasa, O., Rossi, D., Berardinelli, A., and Cereda, C. (2014). Amyotrophic lateral sclerosis and skeletal muscle: an update. Mol. Neurobiol. 49, 984-990. doi:10.1007/s12035-013-8578-4
41. Pantopoulos, K., and Hentze, M. W. (1995). Rapid responses to oxidative stress mediated by iron regulatory protein. EMBO J. 14, 2917-2924
42. Pantopoulos, K., Porwal, S. K., Tartakoff, A., and Devireddy, L. (2012). Mechanisms of mammalian iron homeostasis. Biochemistry 51, 5705-5724. doi: 10.1021/bi300752r
43. Pratt, A. J., Getzoff, E. D., and Perry, J. J. (2012). Amyotrophic lateral sclerosis: update and new developments. Degener. Neurol. Neuromuscul. Dis. 2012, 1-14
44. R eaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J., Siwek, D. F., et al. (1996). Motor neurons in Cu/Zn Superoxide dismutase deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 13, 43-47. doi: 10.1038/ng0596-43
45. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., et al. (1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62. doi: 10.1038/362059a0
46. Rothstein, J. D. (2009). Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann. Neurol. 65(Suppl. 1), S3-S9. doi: 10.1002/ana.21543
47. Salin, M. L., and Bridges, S. M. (1981). Absence of the iron-containing superoxide dismutase in mitochondria from mustard (Brassica campestris). Biochem. J. 195, 229-233. doi: 10.1042/bj1950229
48. Schipper, H. M., Song, W., Zukor, H., Hascalovici, J. R., and Zeligman, D. (2009). Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement. J. Neurochem. 110, 469-485. doi: 10.1111/j.1471-4159.2009.06160.x
49. Starzynski, R. R., Canonne-Hergaux, F., Lenartowicz, M., Krzeptowski, W., Willemetz, A., Stys, A., et al. (2013). Ferroportin expression in haem oxygenase 1-deficient mice. Biochem. J. 449, 69-78. doi: 10.1042/BJ20121139
50. Starzynski, R. R., Canonne-Hergaux, F., Willemetz, A., Gralak, M. A., Woliński, J., Styś, A., et al. (2009). Haemolytic anaemia and alterations in hepatic iron metabolism in aged mice lacking Cu,Zn-superoxide dismutase. Biochem. J. 420, 383-390. doi: 10.1042/BJ20082137
51. Starzynski, R. R., Gonçalves, A. S., Muzeau, F., Tyrolczyk, Z., Smuda, E., Drapier, J. C., et al. (2006). STAT5 proteins are involved in down-regulation of iron regulatory protein 1 gene expression by nitric oxide. Biochem. J. 400, 367-375. doi: 10.1042/BJ20060623
52. Starzynski, R. R., Lipiiiski, P., Drapier, J. C., Diet, A., Smuda, E., Bartłomiejczyk, et al. (2005). Down-regulation of iron regulatory protein 1 activities and expression in superoxide dismutase 1 knock-out mice is not associated with alterations in iron metabolism. J. Biol. Chem. 280, 4207-4212. doi:10.1074/jbc.M411055200
53. Torti, F. M., and 丁orti, S.V. (2002). Regulation of ferritin genes and protein. Blood 99, 3505-3516. doi: 10.1182/blood.V99.10.3505
54. Turner, B. J., and Talbot, K. (2008). Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog. Neurobiol. 85, 94-134. doi: 10.1016/j.pneurobio.2008.01.001
55. Urrutia, P., Aguirre, P., Esparza, A., Tapia, V., Mena, N. P., Arredondo, M., et al. (2013). Inflammation alters the expression of DM丁1, FPN1 and hepcidin, and it causes iron accumulation in central nervous system cells. J. Neurochem. 126, 541-549. doi: 10.1111/jnc.12244
56. Wang, Q., Zhang, X., Chen, S., Zhang, X., Zhang, S., Youdium, M., et al. (2011). Prevention of motor neuron degeneration by novel iron chelators in SOD1(G93A) transgenic mice of amyotrophic lateral sclerosis. Neurodegener. Dis. 8, 310-321. doi:10.1159/000323469
57. Wilkinson, N., and Pantopoulos, K. (2014). The IRP/IRE system in vivo: insights from mouse models. Front. Pharmacol. 5:176. doi: 10.3389/fphar.2014.00176
58. Zelko, I. N., Mariani, T. J., and Folz, R. J. (2002). Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC- SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med. 33, 337-349. doi: 10.1016/S0891-5849(02)00905-X