A new perspective on the role of CuZn superoxide dismutase (SOD1)

D. Harman: “The aging process”, Proc. Natl. Acad. Sci. U.S.A., Vol. 78, (1981), pp. 7124–7128. W. Droge: “Free radicals in the physiological control of cell function”, Physiol. Rev., Vol. 82, (2002), pp. 47–95. K.B. Beckman and B.N. Ames: “The free radical theory of aging matures”, Physiol. Rev., Vol. 78, (1998), pp. 547–581. S.E. Schriner, N.J. Linford, G.M. Martin, P. Treuting, C.E. Ogburn, M Emond, P.E. Coskun, W. Ladiges, N. Wolf, H. Van Remmen, D.C Wallace and P.S. Rabinovitch: “Extension of murine life span by overexpression of catalase targeted to mitochondria”, Science, Vol. 308, (2005), pp. 1909–1911. B. Halliwell and J.M.C. Gutteridge: Free Radicals in Biology and Medicine, 2° Ed., Oxford, UK, Clarendon, 1989. M.U. Shiloh, J.D. MacMicking, S. Nicholson, J.E. Brause, S. Potter, M. Marino, F. Fang, M. Dinauer and C. Nathan: “Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase”, Immunity, Vol. 10, (1999), pp. 29–38. A.W. Roberts, C. Kim, L. Zhen, J.B Lowe, R. Kapur, B. Petryniak, A Spaetti, J.D. Pollock, J.B. Borneo, G.B. Bradford, S.J. Atkinson, M.C. Dinauer and D.A Williams: “Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense”, Immunity, Vol. 10, (1999), pp. 183–196. J.D. Pollock, D.A. Williams, M.A. Gifford, L.L. Li, X. Du, J. Fisherman, S.H. Orkin, C.M. Doerschuk and M.C. Dinauer: “Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production”, Nat. Genet., Vol. 9, (1995), pp. 202–209. J.M. McCord and I. Fridovich: “Superoxide dismutase: an enzymic function for erythrocuprein (hemocupreine)”, J. Biol. Chem., Vol. 244, (1969), pp. 6049–6055. R.A. Weisiger and I. Fridovich: “Superoxide dismutase. Organelle specificity”, J. Biol. Chem., Vol. 248, (1973), 3582–3592. S.L. Marklund: “Human copper-containing superoxide dismutase of high molecular weight”, Proc. Natl. Acad. Sci. U. S. A., Vol. 79, (1982), pp. 7634–7638. F.J. Yost Jr. and I. Fridovich: “An iron-containing superoxide dismutase from Escherichia coli”, J. Biol. Chem., Vol. 248, (1973), pp. 4905–4908. H.D. Youn, E.J. Kim, J.H. Roe, Y.C. Hah and S.O. Kang: “A novel nickel-containing superoxide dismutase from Streptomyces spp.”, Biochem. J., Vol. 318, (1996), pp. 889–896. T. Grune, T. Reinheckel and K.J. Davies: “Degradation of oxidized proteins in mammalian cells”, FASEB J., Vol. 11, (1997), pp. 526–534. V.J. Thannickal and B.L. Fanburg: “Reactive oxygen species in cell signalling”, Am. J. Physiol. Lung Cell. Mol. Physiol., Vol. 279, (2000), L1005–L1028. C.K. Mittal and F. Murad: “Activation of guanylate cyclase by superoxide dismutase and hydroxyl radical: a physiological regulator of guanosine 3′,5′-monophosphate formation”, Proc. Natl. Acad. Sci. U. S. A., Vol. 74, (1977), pp. 4360–4364. A.A. White, K.M. Crawford, C.S. Patt and P.J. Lad: “Activation of soluble guanylate cyclase from rat lung by incubation or by hydrogen peroxide”, J. Biol. Chem., Vol. 251, (1976), pp. 7304–7312. A.B. Parekh and R. Penner: “Store depletion and calcium influx”, Physiol. Rev., Vol. 77, (1997), pp. 901–930. H. Acker: “Mechanisms and meaning of cellular oxygen sensing in the organism”, Respir. Physiol., Vol. 95, (1994), pp. 1–10. H. Bunn and R.O. Poyton: “Oxygen sensing and molecular adaptation to hypoxia”, Physiol. Rev., Vol. 76, (1996), pp. 839–885. C.M. Atkins and J.D. Sweatt: “Reactive oxygen species mediate activity-dependent neuron-glia signalling in output fibers of the hippocampus”, J. Neurosci., Vol. 19, (1999), pp. 7241–7248. B.T. Chen, M.V. Avshalumov and M.E. Rice: “H(2)O(2) is a novel, endogenous modulator of synaptic dopamine release”, J. Neurophysiol., Vol. 85, (2001), pp. 2468–2476. C. Hidalgo, P. Aracena, G. Sanchez and P. Donoso: “Redox regulation of calcium release in skeletal and cardiac muscle”, Biol. Res., Vol. 35, (2002), pp. 183–193. K.K. Griendling, D. Sorescu and M. Ushio-Fukai: “NAD(P)H oxidase: role in cardiovascular biology and disease”, Circ. Res., Vol. 86, (2000), pp. 494–501. Y.J. Suzuki and G.D. Ford: “Redox regulation of signal transduction in cardiac and smooth muscle”, J. Mol. Cell. Cardiol., Vol. 31, (1999), pp. 345–353. L.J. Ignarro and P.J. Kadowitz: “The pharmacological and physiological role of cyclic GMP in vascular smooth muscle relaxation”, Annu. Rev. Pharmacol. Toxicol., Vol. 25, (1985), pp. 171–191. W.P. Arnold, C.K. Mittal, S. Katsuki and F. Murad: “Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations”, Proc. Natl. Acad. Sci. U. S. A., Vol. 74, (1977), pp. 3203–3207. M.S. Wolin, T.M. Burke-Wolin and KM. Mohazzab-H: “Roles for NAD(P)H oxidases and reactive oxygen species in vascular oxygen sensing mechanisms”, Respir. Physiol., Vol. 115, (1999), pp. 229–328. A.A. White, K.M. Crawford, C.S. Patt and P.J. Lad: “Activation of soluble guanylate cyclase from rat lung by incubation or by hydrogen peroxide”, J. Biol. Chem., Vol. 251, (1976), pp. 7304–7312. A.N. Lyle and K.K. Griendling: “Modulation of vascular smooth muscle signaling by reactive oxygen species”, Physiology, Vol. 21, (2006), pp. 269–280. Z. Ungvari, M.S. Wolin and A. Csiszar: “Mechanosensitive production of reactive oxygen species in endothelial and smooth muscle cells: role in microvascular remodeling?”, Antioxid. Redox Signal., Vol. 8, (2006), pp. 1121–1129. A.A. Miller, G.R. Drummond and C.G. Sobey: “Reactive oxygen species in the cerebral circulation: are they all bad?”, Antioxid. Redox Signal., Vol. 8, (2006), pp. 1113–1120. N.S. Chandel and G.R. Budinger: “The cellular basis for diverse responses to oxygen”, Free rad. Biol. Med., Vol. 42, (2007), pp. 165–174. J.V. Bannister, W.H. Bannister and G. Rotilio: “Aspects of the structure, function, and applications of superoxide dismutase”, CRC Crit. Rev. Biochem., Vol. 22, (1987), pp. 111–180. J.M. Delabar, A. Nicole, L. D’Auriol, Y. Jacob, M. Meunier-Rotival, F. Galibert, P.M. Sinet and H. Jerome: “Cloning and sequencing of a rat CuZn superoxide dismutase cDNA. Correlation between CuZn superoxide dismutase mRNA level and enzyme activity in rat and mouse tissues”, Eur. J. Biochem., Vol. 166, (1987), pp. 181–187. S.L. Marklund: “Extracellular superoxide dismutase and other superoxide dismutase isoenzymes in tissues from nine mammalian species”, Biochem. J., Vol. 222, (1984), pp. 649–655. S.L. Marklund: “Expression of extracellular superoxide dismutase by human cell lines”, Biochem J., Vol. 266, (1990), pp. 213–219. P. Mondola, T. Annella, M. Santillo and F. Santangelo: “Evidence for secretion of cytosolic CuZn superoxide dismutase by Hep G2 cells and human fibroblasts”, Int. J. Biochem. Cell. Biol., Vol. 28, (1996), pp. 677–681. P. Mondola, M. Bifulco, R. Seru, T. Annella, M.R. Circolo and M. Santillo: “Presence of CuZn superoxide dismutase in human serum lipoproteins”, FEBS Lett., Vol. 467, (2000), pp. 57–60. M.S. Brown and J.L. Goldstein: “Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis”, Annu. Rev. Biochem., Vol. 52, (1983), pp.223–261. S.T. Kunitake, M.R. Jarvis, R.L. Hamilton and J.P. Kane: “Binding of transition metals by lipolipoprotein A-I-containing plasma lipoproteins: inhibition of oxidation of low density lipoproteins”, Proc. Natl. Acad. Sci. U. S. A., Vol. 89, (1992), pp. 6993–6997. P. Mondola, T. Annella, R. Seru, F. Santangelo, S. Iossa, A. Gioielli and M. Santillo: “Secretion and increase of intracellular CuZn superoxide dismutase content in human neuroblastoma SK-N-BE cells subjected to oxidative stress”, Brain Res. Bull., Vol. 45, (1998), pp. 517–520. V. Cimini, G. Ruggiero, T. Buonomo, R. Seru, S. Sciorio, C. Zanzi, F. Santangelo and P. Mondola: “CuZn-superoxide dismutase in human thymus: immunocytochemical localisation and secretion in thymus-derived epithelial and fibroblast cell lines”, Histochem. Cell. Biol., Vol. 118, (2002), pp. 163–169. P. Mondola, G. Ruggiero, R. Seru, S. Damiano, S. Grimaldi, C. Garbi, M. Monda, D. Greco and M. Santillo: “The Cu,Zn superoxide dismutase in neuroblastoma SKN-BE cells is exported by a microvesicles dependent pathway”, Mol. Brain Res., Vol. 110, (2003), pp. 45–51. M. Santillo, A. Secondo, R. Seru, S. Damiano, C. Garbi, E. Taverna, P. Rosa, S. Giovedi, F. Benfenati and P. Mondola: “Evidence of calcium-and SNARE-dependent release of CuZn Superoxide Dismutase from rat pituitary GH3 cells and synaptosomes in response to depolarization”, J. Neurochem., (2007), Epub, 2 Apr. 2007. F. Aguado, G. Majo, B. Ruiz-Montasell, J.M. Canals, A. Casanova, J. Marsal and J. Blasi: “Expression of synaptosomal-associated protein SNAP-25 in endocrine anterior pituitary cells”, Eur. J. Cell Biol., Vol. 69, (1996), pp. 351–359. P. Mondola, M. Santillo, R. Seru, S. Damiano, C. Alvino, G. Ruggiero, P Formisano, G. Terrazzano, A. Secondo and L. Annunziato: “Cu,Zn superoxide dismutase increases intracellular calcium levels via a phospholipase C-protein kinase C pathway in SK-N-BE neuroblastoma cells”, Biochem. Biophys. Res. Commun., Vol. 324, (2004), pp. 887–892. P. Mondola, R. Seru, M. Santillo, S. Damiano, M. Bifulco, C. Laezza, P. Formisano, G. Rotilio and M.R. Ciriolo: “Effect of Cu,Zn superoxide dismutase on cholesterol metabolism in human hepatocarcinoma (HepG2) cells”, Biochem. Biophys. Res. Commun., Vol. 295, (2002), pp. 603–609. M. Wu, H. Lee, R.E. Bellas, S.L. Schauer, M. Arsura, D. Katz, M.J. FitzGerald, T.L. Rothstein, D.H. Sherr and G.E. Sonenshein: “Inhibition of NF-kappaB/Rel induces apoptosis of murine B cells”, EMBO J., Vol. 15, (1996), pp. 4682–4690. V.J. Thannickal, R.M. Day, S.G. Klinz, M.C. Bastien, J.M. Larios and B.L. Fanburg: “Ras-dependent and-independent regulation of reactive oxygen species by mitogenic growth factors and TGF-beta1”, FASEB J., Vol. 14, (2000), pp. 1741–1748. K. Suzukawa, K. Miura, J. Mitsushita, J. Resau, K. Hirose, R. Crystal and T. Kamata: “Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species”, J. Biol. Chem., Vol. 275, (2000), pp. 13175–13178. E. Klann, E.D. Roberson, L.T. Knapp and J.D. Sweatt: “A role for superoxide in protein kinase C activation and induction of long-term potentiation”, J. Biol. Chem., Vol. 273, (1998), pp. 4516–4522. K.W. Roche, R.J. O’Brien, A.L. Mammen, J. Bernhardt and R.L. Huganir: “Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit”, Neuron, Vol. 16, (1996), pp. 1179–1188. S.E. Tan, R.J. Wenthold and T.R. Soderling: “Phosphorylation of AMPA-type glutamate receptors by calcium/calmodulin-dependent protein kinase II and protein kinase C in cultured hippocampal neurons”, J. Neurosci., Vol. 14, (1994), pp. 1123–1129. J.H. Wang and D.P. Feng: “Postsynaptic protein kinase C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region”, Proc. Natl. Acad. Sci. U. S. A., Vol. 89, (1992), pp. 2576–2580. L.P. Rowland and N.A. Shneider: “Amyotrophic lateral sclerosis”, N. Engl. J. Med., Vol. 344, (2001), pp. 1688–1700. C. Bendotti and M.T. Carri: “Lessons from models of SOD1-linked familial ALS”, Trends Mol. Med., Vol. 10, (2004), pp. 393–400. L.I. Bruijn, T.M. Miller and D.W. Cleveland: “Unraveling the mechanisms involved in motor neuron degeneration in ALS”, Annu. Rev. Neurosci., Vol. 27, (2004), pp. 723–749. Z. Mourelatos, H. Adler, A. Hirano, H. Donnenfeld, J.O. Gonatas and N.K. Gonatas: “Fragmentation of the Golgi apparatus of motor neurons in amyotrophic lateral sclerosis revealed by organelle-specific antibodies”, Proc. Natl. Acad. Sci. U. S. A., Vol. 87, (1990), pp. 4393–4395. Z. Mourelatos, N.K. Gonatas, A. Stieber, M.E. Gurney and M.C. Dal Canto: “The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu,Zn superoxide dismutase becomes fragmented in early, preclinical stages of the disease”, Proc. Natl. Acad. Sci. U. S. A., Vol. 93, (1996), pp. 5472–5477. Y. Fujita, K. Okamoto, A. Sakurai, N.K. Gonatas and A. Hirano: “Fragmentation of the Golgi apparatus of the anterior horn cells in patients with familial amyotrophic lateral sclerosis with SOD1 mutations and posterior column involvement”, J. Neurol. Sci., Vol. 174, (2000), pp. 137–140. M.E. Gurney, H. Pu, A.Y. Chiu, M.C. Dal Canto, C.Y. Polchow, D.D. Alexander, J. Caliendo, A. Hentati, Y.W. Kwon and H.X. Deng: “Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation”, Science, Vol. 264, (1994), pp. 1772–1775. A. Stieber, J.O Gonatas and N.K. Gonatas: “Aggregates of mutant protein appear progressively in dendrites, in periaxonal processes of oligodendrocytes, and in neuronal and astrocytic perikarya of mice expressing the SOD1(G93A) mutation of familial amyotrophic lateral sclerosis”, J. Neurol. Sci., Vol. 177, (2000), pp. 114–123. S. Tobisawa, Y. Hozumi, S. Arawaka, S. Koyama, M. Wada, M. Nagai, M. Aoki, Y. Itoyama, K. Goto and T. Kato: “Mutant SOD1 linked to familial amyotrophic lateral sclerosis, but not wild-type SOD1, induces ER stress in COS7 cells and transgenic mice”, Biochem. Biophys. Res. Commun., Vol. 303, (2003), pp. 496–503. H. Wootz, I. Hansson, L. Korhonen, U. Napankangas and D. Lindholm: “Caspase-12 cleavage and increased oxidative stress during motoneuron degeneration in transgenic mouse model of ALS”, Biochem. Biophys. Res. Commun., Vol. 322, (2004), pp. 281–286. P.A. Doucette, L.J. Whitson, X. Cao, V. Schirf, B. Demeler, J.S. Valentine, J.C. Hansen and P.J. Hart: “Dissociation of human copper-zinc superoxide dismutase dimers using chaotrope and reductant. Insights into the molecular basis for dimer stability”, J. Biol. Chem., Vol. 279, (2004), pp. 54558–54566. A. Tiwari and L.J. Hayward: “Familial amyotrophic lateral sclerosis mutants of copper/zinc superoxide dismutase are susceptible to disulfide reduction”, J. Biol. Chem., Vol. 278, (2003), pp. 5984–5992. Y. Furukawa and T.V. O’Halloran: “Amyotrophic lateral sclerosis mutations have the greatest destabilizing effect on the apo-and reduced form of SOD1, leading to unfolding and oxidative aggregation”, J. Biol. Chem., Vol. 280, (2005), pp. 17266–17274. A. Tiwari, Z. Xu and L.J. Hayward: “Aberrantly increased hydrophobicity shared by mutants of Cu,Zn-superoxide dismutase in familial amyotrophic lateral sclerosis”, J. Biol. Chem., Vol. 280, (2005), pp. 29771–29779. J.D. Atkin, M.A. Farg, B.J. Turner, D and J.A. Tomas: Lysaght, Nunan J, Rembach A, Nagley P, Beart PM, Cheema SS and M.K. Horne: “Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of proteindisulfide isomerase with superoxide dismutase 1”, J. Biol. Chem., Vol. 281, (2006), pp. 30152–30165. B.J. Turner, J.D. Atkin, M.A. Farg, D.W. Zang, A. Rembach, E.C. Lopes, J.D. Patch, A.F. Hilland and S.S. Cheema: “Impaired extracellular secretion of mutant superoxide dismutase 1 associates with neurotoxicity in familial amyotrophic lateral sclerosis”, J. Neurosci., Vol. 25, (2005), pp. 108–117. B. De Felice, M. Santillo, R. Seru, S. Damiano, G. Matrone, R.R. Wilson and P. Mondola: “Modulation of 3-hydroxy-3-methylglutaryl-CoA reductase gene expression by CuZn superoxide dismutase in human fibroblasts and HepG2 cells”, Gene Expr., Vol. 12, (2004), pp. 29–38.