Activation of superoxide dismutases: Putting the metal to the pedal

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1763, Issue 7, 2006, Pages 747-758

  Culotta, Valeria Cizewski ^a   Yang, Mei ^a   O'Halloran, Thomas V ^b  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

ALS; CCS; Copper; Copper chaperone; Disulfide isomerase; EC SOD; Iron; Manganese; Mitochondria; Posttranslational modification; SOD; SOD1; SOD2; Superoxide dismutase

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; DISULFIDE; IRON; MANGANESE SUPEROXIDE DISMUTASE; METAL; POLYPEPTIDE; PROTEIN; PROTEIN MTM1; PROTEIN SMF2; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; CELL SURVIVAL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CHEMISTRY; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME STRUCTURE; EUKARYOTE; IN VIVO STUDY; METAL BINDING; METALLATION; MUTANT; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW;

ENZYME ACTIVATION; IRON; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN CONFORMATION; SUBCELLULAR FRACTIONS; SUPEROXIDE DISMUTASE;

EUKARYOTA;

EID: 33746932518     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2006.05.003     Document Type: Review

References (122)

1. McCord J.M., and Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244 (1969) 6049-6055
2. Kakko S., Paivansalo M., Koistinen P., Kesaniemi Y.A., Kinnula V.L., and Savolainen M.J. The signal sequence polymorphism of the MnSOD gene is associated with the degree of carotid atherosclerosis. Atherosclerosis 168 (2003) 147-152
3. Haskins K., Kench J., Powers K., Bradley B., Pugazhenthi S., Reusch J., and McDuffie M. Role for oxidative stress in the regeneration of islet beta cells?. J. Investig. Med. 52 (2004) 45-49
4. Ookawara T., Kawamura N., Kitagawa Y., and Taniguchi N. Site-specific and random fragmentation of Cu,Zn-superoxide dismutase by glycation reaction. Implication of reactive oxygen species. J. Biol. Chem. 267 (1992) 18505-18510
5. Engidawork E., and Lubec G. Protein expression in Down syndrome brain. Amino Acids 21 (2001) 331-361
6. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362 (1993) 59-62
7. Kurtz Jr. D.M. Microbial detoxification of superoxide: the non-heme iron reductive paradigm for combating oxidative stress. Acc. Chem. Res. 37 (2004) 902-908
8. Liochev S.I., and Fridovich I. Copper- and zinc-containing superoxide dismutase can act as a superoxide reductase and a superoxide oxidase. J. Biol. Chem. 275 (2000) 38482-38485
9. Barondeau D.P., Kassmann C.J., Bruns C.K., Tainer J.A., and Getzoff E.D. Nickel superoxide dismutase structure and mechanism. Biochemistry 43 (2004) 8038-8047
10. Wintjens R., Noel C., May A.C., Gerbod D., Dufernez F., Capron M., Viscogliosi E., and Rooman M. Specificity and phenetic relationships of iron- and manganese-containing superoxide dismutases on the basis of structure and sequence comparisons. J. Biol. Chem. 279 (2004) 9248-9254
11. Keele B.B., McCord J.M., and Fridovich I. Superoxide dismutase from Escherichia coli B: a new manganese containing enzyme. J. Biol. Chem. 245 (1970) 6176-6181
12. Hunter T., Bannister W.H., and Hunter G.J. Cloning, expression and characterization of two manganese superoxide dismutases from Caenorhabditis elegans. J. Biol. Chem. 272 (1997) 28652-28659
13. Brouwer M., Hoexum Brouwer T., Grater W., and Brown-Peterson N. Replacement of a cytosolic copper/zinc superoxide dismutase by a novel cytosolic manganese superoxide dismutase in crustaceans that use copper (haemocyanin) for oxygen transport. Biochem. J. 374 (2003) 219-228
14. Lamarre C., LeMay J.D., Deslauriers N., and Bourbonnais Y. Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) upon the entry and during the stationary phase. J. Biol. Chem. 276 (2001) 43784-43791
15. Ravindranath S.D., and Fridovich I. Isolation and characterization of a manganese-containing superoxide dismutase from yeast. J. Biol. Chem. 250 (1975) 6107-6112
16. Yost F.J., and Fridovich I. An iron-containing superoxide dismutase from Escherichia coli. J. Biol. Chem. 248 (1973) 4905-4908
17. Larsen P.L. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 8905-8909
18. Jensen L.T., and Culotta V.C. Activation of Cu/Zn superoxide dismutases from C. elegans does not require the copper chaperone CCS. J. Biol. Chem. 280 (2005) 41373-41379
19. Benov L., Chang L.Y., Day B., and Fridovich I. Copper, zinc superoxide dismutase in Escherichia coli: periplasmic localization. Arch. Biochem. Biophys. 319 (1995) 508-511
20. Stralin P., Karlsson K., Johansson B.O., and Marklund S.L. The interstitium of the human arterial wall contains very large amounts of extracellular superoxide dismutase. Arterioscler. Thromb. Vasc. Biol. 15 (1995) 2032-2036
21. Field L.S., Furukawa Y., O'Halloran T.V., and Culotta V.C. Factors controlling the uptake of yeast copper/zinc superoxide dismutase into mitochondria. J. Biol. Chem. 278 (2003) 28052-28059
22. Lindenau J., Noack H., Possel H., Asayama K., and Wolf G. Cellular distribution of superoxide dismutases in the rat CNS. Glia 29 (2000) 25-34
23. Okado-Matsumoto A., and Fridovich I. Amyotrophic lateral sclerosis: a proposed mechanism. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9010-9014
24. Sturtz L.A., Diekert K., Jensen L.T., Lill R., and Culotta V.C. A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria-A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 276 (2001) 38084-38089
25. Weisiger R.A., and Fridovich I. Mitochondrial superoxide dismutase. J. Biol. Chem. 248 (1973) 4793-4796
26. Chang L.Y., Slot J.W., Geuze H.J., and Crapo J.D. Molecular immunocytochemistry of the CuZn superoxide dismutase in rat hepatocytes. J. Cell Biol. 107 (1988) 2169-2179
27. Moriwaki Y., Yamamoto T., Suda M., Nasako Y., Takahashi S., Agbedana O.E., Hada T., and Higashino K. Purification and immunohistochemical tissue localization of human xanthine oxidase. Biochim. Biophys. Acta 1164 (1993) 327-330
28. Cadenas E., and Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29 (2000) 222-230
29. Tyler D.D. Polarographic assay and intracellular distribution of superoxide dismutase in rat liver. Biochem. J. 147 (1975) 493-504
30. Vijayvergiya C., Beal M.F., Buck J., and Manfredi G. Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice. J. Neurosci. 25 (2005) 2463-2470
31. Han D., Williams E., and Cadenas E. Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space. Biochem. J. 353 (2001) 411-416
32. Benov L., Sage H., and Fridovich I. The copper- and zinc-containing superoxide dismutase from Escherichia coli: molecular weight and stability. Arch. Biochem. Biophys. 340 (1997) 305-310
33. Kroll J.S., Langford P.R., Wilks K.E., and Keil A.D. Bacterial [Cu,Zn]-superoxide dismutase: phylogenetically distinct from the eukaryotic enzyme, and not so rare after all!. Microbiology 141 (1995) 2271-2279
34. St John G., and Steinman H.M. Periplasmic copper-zinc superoxide dismutase of Legionella pneumophila: role in stationary-phase survival. J. Bacteriol. 178 (1996) 1578-1584
35. Asayama K., and Burr I.M. Rat superoxide dismutases. Purification, labeling, immunoassay, and tissue concentration. J. Biol. Chem. 260 (1985) 2212-2217
36. Pardo C.A., Xu Z., Borchelt D.R., Price D.L., Sisodia S.S., and Cleveland D.W. Superoxide dismutase is an abundant component in cell bodies, dendrites, and axons of motor neurons and in a subset of other neurons. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 954-958
37. Kessova I.G., Ho Y.S., Thung S., and Cederbaum A.I. Alcohol-induced liver injury in mice lacking Cu, Zn-superoxide dismutase. Hepatology 38 (2003) 1136-1145
38. Polavarapu R., Spitz D.R., Sim J.E., Follansbee M.H., Oberley L.W., Rahemtulla A., and Nanji A.A. Increased lipid peroxidation and impaired antioxidant enzyme function is associated with pathological liver injury in experimental alcoholic liver disease in rats fed diets high in corn oil and fish oil. Hepatology 27 (1998) 1317-1323
39. Elchuri S., Oberley T.D., Qi W., Eisenstein R.S., Jackson Roberts L., Van Remmen H., Epstein C.J., and Huang T.T. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24 (2005) 367-380
40. Matzuk M.M., Dionne L., Guo Q., Kumar T.R., and Lebovitz R.M. Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 139 (1998) 4008-4011
41. McFadden S.L., Ding D., Reaume A.G., Flood D.G., and Salvi R.J. Age-related cochlear hair cell loss is enhanced in mice lacking copper/zinc superoxide dismutase. Neurobiol. Aging 20 (1999) 1-8
42. Reaume A.G., Elliott J.L., Hoffman E.K., Kowall N.W., Ferrante R.J., Siwek D.F., Wilcox H.M., Flood D.G., Beal M.F., Brown Jr. R.H., Scott R.W., and Snider W.D. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 13 (1996) 43-47
43. Arai K., Iizuka S., Tada Y., Oikawa K., and Taniguchi N. Increase in the glucosylated form of erythrocyte Cu-Zn-superoxide dismutase in diabetes and close association of the nonenzymatic glucosylation with the enzyme activity. Biochim. Biophys. Acta 924 (1987) 292-296
44. Bruijn L.I., Miller T.M., and Cleveland D.W. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27 (2004) 723-749
45. Y. Furukawa, T.V. O'Halloran, Post-translational modifications in Cu, Zn-superoxide dismutase and mutations associated with ALS. Antioxid Redox Signal (in press).
46. Valentine J.S., Doucette P.A., and Potter S.Z. Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu. Rev. Biochem. 74 (2005) 563-593
47. Valentine J.S., and Hart P.J. Misfolded CuZnSOD and amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 3617-3622
48. Bertini I., Mangani S., and Viezzoli M.S. Structure and properties of copper-zinc superoxide dismutases. Adv. Inorg. Chem. 45 (1998) 127-250
49. Hottinger A.F., Fine E.G., Gurney M.E., Zurn A.D., and Aebischer P. The copper chelator d-penicillamine delays onset of disease and extends survival in a transgenic mouse model of familial amyotrophic lateral sclerosis. Eur. J. Neurosci. 9 (1997) 1548-1551
50. Changela A., Chen K., Xue Y., Holschen J., Outten C.E., O'Halloran T.V., and Mondragon A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301 (2003) 1383-1387
51. Finney L.A., and O'Halloran T.V. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300 (2003) 931-936
52. Outten C.E., and O'Halloran T.V. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292 (2001) 2488-2492
53. Rae T.D., Torres A.S., Pufahl R.A., and O'Halloran T.V. Mechanism of Cu,Zn-superoxide dismutase activation by the human metallochaperone hCCS. J. Biol. Chem. 276 (2001) 5166-5176
54. Tottey S., Harvie D.R., and Robinson N.J. Understanding how cells allocate metals using metal sensors and metallochaperones. Acc. Chem. Res. 38 (2005) 775-783
55. Srinivasan C., Liba A., Imlay J.A., Valentine J.S., and Gralla E.B. Yeast lacking superoxide dismutase(s) show elevated levels of "free iron" as measured by whole cell electron paramagnetic resonance. J. Biol. Chem. 275 (2000) 29187-29192
56. Bordo D., Djinovic K., and Bolognesi M. Conserved patterns in the Cu,Zn superoxide dismutase family. J. Mol. Biol. 238 (1994) 366-386
57. Khare S.D., Caplow M., and Dokholyan N.V. The rate and equilibrium constants for a multistep reaction sequence for the aggregation of superoxide dismutase in amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15094-15099
58. Furukawa Y., Torres A.S., and O'Halloran T.V. Oxygen-induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS. EMBO J. 23 (2004) 2872-2881
59. Battistoni A., and Rotilio G. Isolation of an active and heat-stable monomeric form of Cu,Zn superoxide dismutase from the periplasmic space of Escherichia coli. FEBS Lett. 374 (1995) 199-202
60. Pacello F., Langford P.R., Kroll J.S., Indiani C., Smulevich G., Desideri A., Rotilio G., and Battistoni A. A novel heme protein, the Cu,Zn-superoxide dismutase from Haemophilus ducreyi. J. Biol. Chem. 276 (2001) 30326-30334
61. Spagnolo L., Toro I., D'Orazio M., O'Neill P., Pedersen J.Z., Carugo O., Rotilio G., Battistoni A., and Djinovic-Carugo K. Unique features of the sodC-encoded superoxide dismutase from Mycobacterium tuberculosis, a fully functional copper-containing enzyme lacking zinc in the active site. J. Biol. Chem. 279 (2004) 33447-33455
62. Culotta V.C., Klomp L.W., Strain J., Casareno R.L., Krems B., and Gitlin J.D. The copper chaperone for superoxide dismutase. J. Biol. Chem. 272 (1997) 23469-23472
63. Elam J.S., Thomas S.T., Holloway S.P., Taylor A.B., and Hart P.J. Copper chaperones. Adv. Protein Chem. 60 (2002) 151-219
64. Huffman D.L., and O'Halloran T.V. Function, structure, and mechanism of intracellular copper trafficking proteins. Annu. Rev. Biochem. 70 (2001) 677-701
65. O'Halloran T.V., and Culotta V.C. Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275 (2000) 25057-25060
66. Rosenzweig A.C. Copper delivery by metallochaperone proteins. Acc. Chem. Res. 34 (2001) 119-128
67. Hwang C., Sinskey A.J., and Lodish H.F. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257 (1992) 1496-1502
68. Brown N.M., Torres A.S., Doan P.E., and O'Halloran T.V. Oxygen and the copper chaperone CCS regulate posttranslational activation of Cu,Zn superoxide dismutase. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 5518-5523
69. Furukawa Y., Fu R., Deng H.-X., Siddique T., and O'Halloran T.V. Disulfide cross-linked protein represents a significant fraction of ALS-associated SOD1 aggregates in spinal cords of model mice. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 7148-7153
70. Higgins C.M., Jung C., Ding H., and Xu Z. Mutant Cu, Zn superoxide dismutase that causes motoneuron degeneration is present in mitochondria in the CNS. J. Neurosci. 22 (2002) RC215
71. Jaarsma D., Rognoni F., van Duijn W., Verspaget H.W., Haasdijk E.D., and Holstege J.C. CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol. (Berl.) 102 (2001) 293-305
72. Liu J., Lillo C., Jonsson P.A., Vande Velde C., Ward C.M., Miller T.M., Subramaniam J.R., Rothstein J.D., Marklund S., Andersen P.M., Brannstrom T., Gredal O., Wong P.C., Williams D.S., and Cleveland D.W. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43 (2004) 5-17
73. Mattiazzi M., D'Aurelio M., Gajewski C.D., Martushova K., Kiaei M., Beal M.F., and Manfredi G. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J. Biol. Chem. 277 (2002) 29626-29633
74. Furukawa Y., and O'Halloran T.V. 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. 280 (2005) 17266-17274
75. Arnesano F., Banci L., Bertini I., Martinelli M., Furukawa Y., and O'Halloran T.V. The unusually stable quaternary structure of human Cu,Zn-superoxide dismutase 1 is controlled by both metal occupancy and disulfide status. J. Biol. Chem. 279 (2004) 47998-48003
76. Doucette P.A., Whitson L.J., Cao X., Schirf V., Demeler B., Valentine J.S., Hansen J.C., and Hart P.J. Dissociation of human copper-zinc superoxide dismutase dimers using chaotrope and reductant: insights into the molecular basis for dimer stability. J. Biol. Chem. 279 (2004) 54558-54566
77. Lamb A.L., Torres A.S., O'Halloran T.V., and Rosenzweig A.C. Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat. Struct. Biol. 8 (2001) 751-755
78. Rodriguez J.A., Shaw B.F., Durazo A., Sohn S.H., Doucette P.A., Nersissian A.M., Faull K.F., Eggers D.K., Tiwari A., Hayward L.J., and Valentine J.S. Destabilization of apoprotein is insufficient to explain Cu,Zn-superoxide dismutase-linked ALS pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10516-10521
79. Wang J., Xu G., and Borchelt D.R. Mapping superoxide dismutase 1 domains of non-native interaction: roles of intra- and intermolecular disulfide bonding in aggregation. J. Neurochem. 96 (2006) 1277-1288
80. Deng H.X., Shi Y., Furukawa Y., Zhai H., Fu R., Liu E., Gorrie G.H., Khan M.S., Hung W.Y., Bigio E.H., Lukas T., Dal Canto M.C., O'Halloran V., and Siddique T. Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 7142-7147
81. Jonsson P.A., Graffmo K.S., Andersen P.M., Brannstrom T., Lindberg M., Oliveberg M., and Marklund S.L. Disulphide-reduced superoxide dismutase-1 in CNS of transgenic amyotrophic lateral sclerosis models. Brain 129 (2006) 451-464
82. Wong P.C., Waggoner D., Subramaniam J.R., Tessarollo L., Bartnikas T.B., Culotta V.C., Price D.L., Rothstein J., and Gitlin J.D. Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 2886-2891
83. Subramaniam J.R., Lyons W.E., Liu J., Bartnikas T.B., Rothstein J., Price D.L., Cleveland D.W., Gitlin J.D., and Wong P.C. Mutant SOD1 causes motor neuron disease independent of copper chaperone-mediated copper loading. Nat. Neurosci. 5 (2002) 301-307
84. Beckman J.S., Estvez A.G., Barbeito L., and Crow J.P. CCS knockout mice establish an alternative source for copper for SOD in ALS. Free Radic. Biol. Med. 33 (2002) 1433-1435
85. Carroll M.C., Girouard J.B., Ulloa J.L., Subramaniam J.R., Wong P.C., Valentine J.S., and Culotta V.C. Mechanisms for activating Cu- and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 5964-5969
86. Petersen S.V., Oury T.D., Valnickova Z., Thogersen I.B., Hojrup P., Crapo J.D., and Enghild J.J. The dual nature of human extracellular superoxide dismutase: one sequence and two structures. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 13875-13880
87. Jeney V., Itoh S., Wendt M., Gradek Q., Ushio-Fukai M., Harrison D.G., and Fukai T. Role of antioxidant-1 in extracellular superoxide dismutase function and expression. Circ.Res. 96 (2005) 723-729
88. Qin Z., Itoh S., Jeney V., Ushio-Fukai M., and Fukai T. Essential role for the Menkes ATPase in activation of extracellular superoxide dismutase: implication for vascular oxidative stress. FASEB J. 20 (2006) 334-336
89. Field L.S., Luk E., and Culotta V.C. Copper chaperones: personal escorts for metal ions. J. Bioenerg. Biomembr. 34 (2002) 373-379
90. Mizuno K., Whittaker M.M., Bachinger H.P., and Whittaker J.W. Calorimetric studies on the tight-binding metal interactions of Escherichia coli manganese superoxide dismutase. J. Biol. Chem. 279 (2004) 27339-27344
91. Beyer W.F., and Fridovich I. In vivo competition between iron and manganese for occupancy of the active site region of the manganese-superoxide dismutase of Escherichia coli. J. Biol. Chem. 266 (1991) 303-308
92. Whittaker J.W. The irony of manganese superoxide dismutase. Biochem. Soc. Trans. 31 (2003) 11318-11321
93. Privalle C.T., and Fridovich I. Transcriptional and maturation effects of manganese and iron on the biosynthesis of manganese-superoxide dismutase in Escherichia coli. J. Biol. Chem. 267 (1992) 9140-9145
94. Schafer G., and Kardinahl S. Iron superoxide dismutases: structure and function of an archaic enzyme. Biochem. Soc. Trans. 31 (2003) 1330-1334
95. Vance C.K., and Miller A.F. A simple proposal that can explain the inactivity of metal-substituted superoxide dismutases. J. Am. Chem. Soc. 120 (1998) 461-467
96. Jackson T.A., and Brunold T.C. Combined spectroscopic/computational studies on Fe- and Mn-dependent superoxide dismutases: insights into second-sphere tuning of active site properties. Acc. Chem. Res. 37 (2004) 461-470
97. Strassburger M., Bloch W., Sulyok S., Schuller J., Keist A.F., Schmidt A., Wenk J., Peters T., Wlaschek M., Krieg T., Hafner M., Kumin A., Werner S., Muller W., and Scharffetter-Kochanek K. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic. Biol. Med. 38 (2005) 1458-1470
98. Duttaroy A., Paul A., Kundu M., and Belton A. A Sod2 null mutation confers severely reduced adult life span in Drosophila. Genetics 165 (2003) 2295-2299
99. Kirby K., Hu J., Hilliker A.J., and Phillips J.P. RNA interference-mediated silencing of Sod2 in Drosophila leads to early adult-onset mortality and elevated endogenous oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 16162-16167
100. Li Y., Huang T.T., Carlson E.J., Melov S., Ursell P.C., Olson J.L., Noble L.J., Yoshimura M.P., Berger C., Chan P.H., Wallace D.C., and Epstein C.J. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11 (1995) 376-381
101. Melov S., Coskun P., Patel M., Tuinstra R., Cottrell B., Jun A.S., Zastawny T.H., Dizdaroglu M., Goodman S.I., Huang T.T., Miziorko H., Epstein C.J., and Wallace D.C. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 846-851
102. Lebovitz R.M., Zhang H., Vogel H., Cartwright Jr. J., Dionne L., Lu N., Huang S., and Matzuk M.M. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 9782-9787
103. Luk E., Yang M., Jensen L.T., Bourbonnais Y., and Culotta V.C. Manganese activation of superoxide dismutase 2 in the mitochondria of Saccharomyces cerevisiae. J. Biol. Chem. 280 (2005) 22715-22720
104. Schmidt P., Kunst C., and Culotta V.C. Copper activation of SOD1 in vivo: Role for protein-protein interactions with the CCS metallochaperone. J. Biol. Chem. 275 (2000) 33771-33776
105. Bartnikas T.B., and Gitlin J.D. Mechanisms of biosynthesis of mammalian copper/zinc superoxide dismutase. J. Biol. Chem. 278 (2003) 33602-33608
106. Ginsberg M.D., Feliciello A., Jones J.K., Avvedimento E.V., and Gottesman M.E. PKA-dependent binding of mRNA to the mitochondrial AKAP121 protein. J. Mol. Biol. 327 (2003) 885-897
107. Marc P., Margeot A., Devaux F., Blugeon C., Corral-Debrinski M., and Jacq C. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3 (2002) 159-164
108. Whittaker M.M., Mizuno K., Bachinger H.P., and Whittaker J.W. Kinetic analysis of the metal binding mechanism of Escherichia coli manganese superoxide dismutase. Biophys. J. 274 (2005) 34751-34757
109. Whittaker M., and Whittaker J. Thermally triggered metal binding by recombinant Thermus thermophilus manganese superoxide dismutase, expressed as the apo-enzyme. J. Biol. Chem. 274 (1999) 34751-34757
110. Luk E., and Culotta V.C. Manganese superoxide dismutase in S. cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. J. Biol. Chem. 276 (2001) 47556-47562
111. Yang M., Cobine P.A., Molik S., Naranuntarat A., Lill R., Winge D., and Culotta V.C. The effects of mitochondrial iron homeostasis on co-factor specificity of superoxide dismutase 2. EMBO J. 25 (2006) 1775-1783
112. Palmieri L., Lasorsa F.M., Vozza A., Agrimi G., Fiermonte G., Runswick M.J., Walker J.E., and Palmieri F. Identification and functions of new transporters in yeast mitochondria. Biochim. Biophys. Acta 1459 (2000) 363-369
113. Luk E., Carroll M., Baker M., and Culotta V.C. Manganese activation of superoxide dismutase 2 in Saccharomyces cerevisiae requires MTM1, a member of the mitochondrial carrier family. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 10353-10357
114. Cobine P.A., Ojeda L.D., Rigby K.M., and Winge D.R. Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J. Biol. Chem. 279 (2004) 14447-14455
115. Dancis A. Genetic analysis of iron uptake in the yeast Saccharomyces cerevisiae. J. Pediatr. 132 (1998) S24-S29
116. Leopold J.A., and Loscalzo J. Oxidative enzymopathies and vascular disease. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1332-1340
117. Immenschuh S., and Baumgart-Vogt E. Peroxiredoxins, oxidative stress, and cell proliferation. Antioxid. Redox Signal. 7 (2005) 768-777
118. Bertinato J., Iskandar M., and L'Abbe M.R. Copper deficiency induces the upregulation of the copper chaperone for Cu/Zn superoxide dismutase in weanling male rats. J. Nutr. 133 (2003) 28-31
119. Van Remmen H., Ikeno Y., Hamilton M., Pahlavani M., Wolf N., Thorpe S.R., Alderson N.L., Baynes J.W., Epstein C.J., Huang T.T., Nelson J., Strong R., and Richardson A. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genomics 16 (2003) 29-37
120. Cellier M., Prive G., Belouchi A., Kwan T., Rodrigues V., Chia W., and Gros P. Nramp defines a family of membrane proteins. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 10089-10093
121. Napier I., Ponka P., and Richardson D.R. Iron trafficking in the mitochondrion: novel pathways revealed by disease. Blood 105 (2005) 1867-1874
122. Rouault T.A. Iron on the brain. Nat. Genet. 28 (2001) 299-300