Glutaredoxin1 protects neuronal cells from copper-induced toxicity

BioMetals

Volumn 27, Issue 4, 2014, Pages 661-672

  Cater, Michael A ^a,b   Materia, Stephanie ^a   Xiao, Zhiguang ^c   Wolyniec, Kamil ^d   Ackland, Susan M ^a   Yap, Yann W ^a   Cheung, Nam Sang ^a   La Fontaine, Sharon ^a,e  

^a DEAKIN UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

^e FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

Author keywords

Copper; Glutaredoxin1; Glutathione; Metal; Oxidative stress; Thiol oxidoreductase

Indexed keywords

COPPER; GLRX PROTEIN, HUMAN; GLUTAREDOXIN; REACTIVE OXYGEN METABOLITE;

ANIMAL; CELL SURVIVAL; ENZYMOLOGY; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; NERVE CELL; OXIDATIVE STRESS; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; COPPER; GLUTAREDOXINS; HEK293 CELLS; HUMANS; MICE; NEURONS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84905087025     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-014-9748-1     Document Type: Article

References (41)

1. Akterin S, Cowburn RF, Miranda-Vizuete A, Jimenez A, Bogdanovic N, Winblad B, Cedazo-Minguez A (2005) Involvement of glutaredoxin-1 and thioredoxin-1 in β-amyloid toxicity and Alzheimer's disease. Cell Death Differ 13:1454-1465
2. Allen EM, Mieyal JJ (2012) Protein-thiol oxidation and cell death: regulatory role of glutaredoxins. Antioxid Redox Signal 17:1748-1763
3. Aon-Bertolino ML, Romero JI, Galeano P, Holubiec M, Badorrey MS, Saraceno GE, Hanschmann EM, Lillig CH, Capani F (2011) Thioredoxin and glutaredoxin system proteins-immunolocalization in the rat central nervous system. Biochim Biophys Acta 1810:93-110
4. Arciello M, Rotilio G, Rossi L (2005) Copper-dependent toxicity in SH-SY5Y neuroblastoma cells involves mitochondrial damage. Biochem Biophys Res Commun 327:454-459 (Pubitemid 40040497)
5. Ayton S, Lei P, Bush AI (2013) Metallostasis in Alzheimer's disease. Free Rad Biol Med 62:76-89
6. Balijepalli S, Tirumalai PS, Swamy KV, Boyd MR, Mieyal JJ, Ravindranath V (1999) Rat brain thioltransferase: regional distribution, immunological characterization, and localization by fluorescent in situ hybridization. J Neurochem 72:1170-1178 (Pubitemid 29085033)
7. Barnham KJ, Masters CL, Bush AI (2004) Neurodegenerative diseases and oxidative stress. Nat Rev 3:205-214
8. Biedler JL, Roffler-Tarlov S, Schachner M, Freedman LS (1978) Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 38:3751-3757 (Pubitemid 9045201)
9. Bouldin SD, Darch MA, Hart PJ, Outten CE (2012) Redox properties of the disulfide bond of human Cu, Zn superoxide dismutase and the effects of human glutaredoxin 1. Biochem J 446:59-67
10. Brose J, La Fontaine S, Wedd AG, Xiao Z (2014) Redox sulfur chemistry of the copper chaperone Atox1 is regulated by the enzyme glutaredoxin 1, the reduction potential of the glutathione couple GSSG/2GSH and the availability of Cu(I). Metallomics 6:793-808
11. Cater MA, McInnes KT, Li Q-X, Volitakis I, La Fontaine S, Mercer JFB, Bush AI (2008) Intracellular copper deficiency increases amyloid-β secretion by diverse mechanisms. Biochem J 412:141-152 (Pubitemid 351678344)
12. Cozzolino M, Amori I, Pesaresi MG, Ferri A, Nencini M, Carri MT (2008) Cysteine 111 affects aggregation and cytotoxicity of mutant Cu, Zn-superoxide dismutase associated with familial amyotrophic lateral sclerosis. J Biol Chem 283:866-874
13. De Benedetto ML, Capo CR, Ferri A, Valle C, Polimanti R, Carri MT, Rossi L (2014) Glutaredoxin 1 is a major player in copper metabolism in neuroblastoma cells. Biochim Biophys Acta 1840:255-261
14. Diwakar L, Kenchappa RS, Annepu J, Saeed U, Sujanitha R, Ravindranath V (2006) Down-regulation of glutaredoxin by estrogen receptor antagonist renders female mice susceptible to excitatory amino acid mediated complex I inhibition in CNS. Brain Res 1125:176-184 (Pubitemid 44848320)
15. Diwakar L, Kenchappa RS, Annepu J, Ravindranath V (2007) Downregulation of glutaredoxin but not glutathione loss leads to mitochondrial dysfunction in female mice CNS: implications in excitotoxicity. Neurochem Int 51:37-46 (Pubitemid 47009000)
16. Freedman JH, Peisach J (1989) Intracellular copper transport in cultured hepatoma cells. Biochem Biophys Res Commun 164:134-140 (Pubitemid 19269706)
17. Freedman JH, Ciriolo MR, Peisach J (1989) The role of glutathione in copper metabolism and toxicity. J Biol Chem 264:5598-5605 (Pubitemid 19098017)
18. Hatori Y, Clasen S, Hasan NM, Barry AN, Lutsenko S (2012) Functional partnership of the copper export machinery and glutathione balance in human cells. J Biol Chem 287:26678-26687
19. Ho Y-S, Xiong Y, Ho DS, Gao J, Chua BHL, Pai H, Mieyal JJ (2007) Targeted disruption of the glutaredoxin 1 gene does not sensitize adult mice to tissue injury induced by ischemia/reperfusion and hyperoxia. Free Rad Biol Med 43:1299-1312 (Pubitemid 47440124)
20. Ke B-X, Llanos RM, Wright M, Deal Y, Mercer JFB (2006) Alteration of copper physiology in mice overexpressing the human Menkes protein ATP7A. Am J Physiol Regul Integr Comp Physiol 290:R1460-R1467
21. Kenchappa RS, Ravindranath V (2003) Glutaredoxin is essential for maintenance of brain mitochondrial complex I: studies with MPTP. FASEB J. 17:717-719
22. Kenchappa RS, Diwakar L, Boyd MR, Ravindranath V (2002) Thioltransferase (glutaredoxin) mediates recovery of motor neurons from excitotoxic mitochondrial injury. J Neurosci 22:8402-8410 (Pubitemid 35387580)
23. Kenchappa RS, Diwakar L, Annepu J, Ravindranath V (2004) Estrogen and neuroprotection: higher constitutive expression of glutaredoxin in female mice offers protection against MPTP-mediated neurodegeneration. FASEB J 18:1102-1104 (Pubitemid 39561537)
24. Kim B-E, Nevitt T, Thiele DJ (2008) Mechanisms for copper acquisition, distribution and regulation. Nat Chem Biol 4:176-185 (Pubitemid 351264130)
25. Kozlowski H, Janicka-Klos A, Brasun J, Gaggelli E, Valensin D, Valensin G (2009) Copper, iron, and zinc ions homeostasis and their role in neurodegenerative disorders (metal uptake, transport, distribution and regulation). Coord Chem Rev 253:2665-2685
26. La Fontaine S, Mercer JFB (2007) Trafficking of the copper-ATPases, ATP7A and ATP7B: role in copper homeostasis. Arch Biochem Biophys 463:149-167 (Pubitemid 47030343)
27. Lillig CH, Berndt C (2013) Glutaredoxins in thiol/disulfide exchange. Antioxid Redox Signal 18:1654-1665
28. Lim CM, Cater MA, Mercer JF, La Fontaine S (2006) Copper-dependent interaction of glutaredoxin with the N termini of the copper-ATPases (ATP7A and ATP7B) defective in Menkes and Wilson diseases. Biochem Biophys Res Commun 348:428-436 (Pubitemid 44188587)
29. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY (2007) Function and regulation of human copper-transporting ATPases. Physiol Rev 87:1011-1046 (Pubitemid 47084675)
30. Maryon EB, Molloy SA, Kaplan JH (2013) Cellular glutathione plays a key role in copper uptake mediated by human copper transporter 1. Am J Physiol Cell Physiol 304:C768-C779
31. Matus A (1991) Microtubule-associated proteins and neuronal morphogenesis. J Cell Sci Suppl 15:61-67
32. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, Shelton MD (2008) Molecular mechanisms and clinical implications of reversible protein s-glutathionylation. Antioxid Redox Signal 10:1941-1988
33. Mot AI, Wedd AG, Sinclair L, Brown DR, Collins SJ, Brazier MW (2011) Metal attenuating therapies in neurodegenerative disease. Expert Rev Neurother 11:1717-1745
34. Rodriguez-Rocha H, Garcia Garcia A, Zavala-Flores L, Li S, Madayiputhiya N, Franco R (2012) Glutaredoxin 1 protects dopaminergic cells by increased protein glutathionylation in experimental Parkinson's disease. Antioxid Redox Signal 17:1676-1693
35. Sabens Liedhegner EA, Gao XH, Mieyal JJ (2012) Mechanisms of altered redox regulation in neurodegenerative diseases - focus on S-glutathionylation. Antioxid Redox Signal 16:543-566
36. Saeed U, Durgadoss L, Valli RK, Joshi DC, Joshi PG, Ravindranath V (2008) Knockdown of cytosolic glutaredoxin 1 leads to loss of mitochondrial membrane potential: implication in neurodegenerative diseases. PLoS One 3:e2459
37. Singleton WC, McInnes KT, Cater MA, Winnall WR, McKirdy R, Yu Y, Taylor PE, Ke BX, Richardson DR, Mercer JF, La Fontaine S (2010) Role of glutaredoxin1 and glutathione in regulating the activity of the copper-transporting P-type ATPases, ATP7A and ATP7B. J Biol Chem 285:27111-27121
38. Watt NT, Hooper NM (2001) The response of neurones and glial cells to elevated copper. Brain Res Bull 55:219-224 (Pubitemid 32725026)
39. Wolyniec K, Levav-Cohen Y, Jiang YH, Haupt S, Haupt Y (2013) The E6AP E3 ubiquitin ligase regulates the cellular response to oxidative stress. Oncogene 32:3510-3519
40. Xiao Z, Brose J, Schimo S, Ackland SM, La Fontaine S, Wedd AG (2011) Unification of the copper(I) binding affinities of the metallo-chaperones Atx1, Atox1 and related proteins: detection probes and affinity standards. J Biol Chem 286:11047-11055
41. Zhang C, Kuo CC, Chiu AW, Feng J (2012) Prediction of S-glutathionylated proteins progression in Alzheimer's transgenic mouse model using principle component analysis. J Alzheimers Dis 30:919-934