Cellular glutathione plays a key role in copper uptake mediated by human copper transporter 1

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 8, 2013, Pages

  Maryon, Edward B ^a   Molloy, Shannon A ^a   Kaplan, Jack H ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Copper chaperones; Copper transport; Glutathione; HCTR1

Indexed keywords

BUTHIONINE SULFOXIMINE; CARRIER PROTEIN; COPPER; COPPER TRANSPORTER 1; CYSTEINE; GLUTATHIONE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; ION TRANSPORT; OXIDATION; PRIORITY JOURNAL; PROTEIN MOTIF;

BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; CELL MEMBRANE; COPPER; GLUTATHIONE; HEK293 CELLS; HUMANS;

EID: 84878653071     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00417.2012     Document Type: Article

References (50)

1. Aller SG, Unger VM. Projection structure of the human copper transporter CTR1 at 6-A resolution reveals a compact trimer with a novel channel-like architecture. Proc Natl Acad Sei USA 103: 3627-3632, 2006.
2. Anderson ME. Glutathione: an overview of biosynthesis and modulation. Chem Biol Interact 111-112: 1-14, 1998.
3. Ashino T, Sudhahar V, Urao N, Oshikawa J, Chen GF, Wang H, Huo Y, Finney L, Vogt S, McKinney RD, Maryon EB, Kaplan JH, Ushio-Fukai M, Fukai T. Unexpected role of the copper transporter ATP7A in PDGF-induced vascular smooth muscle cell migration. Circ Res 107: 787-799, 2010.
4. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, Hammond CL. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 390: 191-214, 2009.
5. Band L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, Palumaa P. Affinity gradients drive copper to cellular destinations. Nature 465: 645-648, 2010.
6. Beck M, Schmidt A, Malmstroem J, Ciaassen M, Ori A, Szymborska A, Herzog F, Rinner O, Ellenberg J, Aebersold R. The quantitative proteome of a human cell line. Mol Syst Biol 7: 549, 2011.
7. Berger SJ, Gosky D, Zborowska E, Willson JK, Berger NA. Sensitive enzymatic cycling assay for glutathione: measurements of glutathione content and its modulation by buthionine sulfoximine in vivo and in vitro in human colon cancer. Cancer Res 54: 4077-4083, 1994.
8. Bertinato J, Cheung L, Hoque R, Plouffe LJ. Ctrl transports silver into mammalian cells. J. Trace Elem Med Biol 24: 178-184, 2010.
9. Brouwer M, Brouwer-Hoexum T. Glutathione-mediated transfer of copper(I) into American lobster apohemocyanin. Biochemistry 31: 4096-4102, 1992.
10. Carroll MC, Girouard JB, Ulloa JL, Subramaniam JR, Wong PC, Valentine JS, Culotta VC. Mechanisms for activating Cu- and Zn-containing Superoxide dismutase in the absence of the CCS Cu chaperone. Proc Natl Acad Sei USA 101: 5964-5969, 2004.
11. Celli A, Que FG, Gores GJ, LaRusso NF. Glutathione depletion is associated with decreased Bcl-2 expression and increased apoptosis in cholangiocytes. Am J Physiol Gastrointest Liver Physiol 275: G749-G757, 1998.
12. Chen HH, Song IS, Hossain A, Choi MK, Yamane Y, Liang ZD, Lu J, Wu LY, Siddik ZH, Klomp LW, Savaraj N, Kuo MT. Elevated glutathione levels confer cellular sensitization to cisplatin toxicity by up-regulation of copper transporter hCtrl. Mol Pharmacol 74: 697-704, 2008.
13. De Feo CJ, Aller SG, Siluvai GS, Blackburn NJ, Unger VM. Three-dimensional structure of the human copper transporter hCTRl. Proc Natl Acad Sei USA 106: 4237-4242, 2009.
14. Eisses JF, Kaplan JH. The mechanism of copper uptake mediated by human CTR1: a mutational analysis. J. Biol Chem 280: 37159-37168, 2005.
15. Eisses JF, Kaplan JH. Molecular characterization of hCTRl, the human-copper uptake protein. J Biol Chem 277: 29162-29171, 2002.
16. Ferreira AM, Ciriolo MR, Marcocci L, Rotilio G. Copper® transfer into metallothionein mediated by glutathione. Biochem J 292: 673-676, 1993.
17. Ford JM, Yang JM, Hait WN. Effect of buthionine sulfoximine on toxicity of verapamil and doxorubicin to multidrug resistant cells and to mice. Cancer Res 51: 67-72, 1991.
18. Freedman JH, Ciriolo MR, Peisach J. The role of glutathione in copper metabolism and toxicity. J Biol Chem 264: 5598-5605, 1989.
19. Gupta A, Lutsenko S. Human copper transporters: mechanism, role in human diseases and therapeutic potential. Future Med Chem 1: 1125-1142, 2009.
20. Hamza I, Prohaska J, Gitlin JD. Essential role for Atoxl in the copper-mediated intracellular trafficking of the Menkes ATPase. Proc Natl Acad Sei USA 100: 1215-1220, 2003.
21. Harrison MD, Jones CE, Solioz M, Dameron CT. Intracellular copper routing: the role of copper chaperones. Trends Biochem Sei 25: 29-32, 2000.
22. Hatori Y, Clasen S, Hasan NM, Barry AN, Lutsenko S. Functional partnership of the copper export machinery and glutathione balance in human cells. J Biol Chem 287: 26678-26687, 2012.
23. Horng YC, Cobine PA, Maxfleld AB, Carr HS, Winge DR. Specific copper transfer from the Coxl7 metallochaperone to both Scol and Coxl 1 in the assembly of yeast cytochrome C oxidase. J. Biol Chem 279: 35334-35340, 2004.
24. Kaplan JH, Lutsenko S. Copper transport in mammalian cells: special care for a metal with special needs. J Biol Chem 284: 25461-25465, 2009.
25. Kimelberg HK, O'Connor ER, Sankar P, Keese C. Methods for determination of cell volume in tissue culture. Can J Physiol Pharmacol 70 Suppl: S323-333, 1992.
26. Klomp AE, Juijn JA, van der Gun LT, van den Berg IE, Berger R, Klomp LW. The N-terminus of the human copper transporter 1 (hCTRl) is localized extracellularly, and interacts with itself. Biochem J 370: 881-889, 2003.
27. Lee J, Pena MM, Nose Y, Thiele DJ. Biochemical characterization of the human copper transporter Ctrl. J Biol Chem 277: 4380-4387, 2002.
28. Lee J, Petris MJ, Thiele DJ. Characterization of mouse embryonic cells deficient in the Ctrl high affinity copper transporter. Identification of a Ctrl-independent copper transport system. J. Biol Chem 277: 40253-40259, 2002.
29. Levy EJ, Anderson ME, Meister A. Transport of glutathione diethyl ester into human cells. Proc Natl Acad Sei USA 90: 9171-9175, 1993.
30. Liang ZD, Stockton D, Savaraj N, Tien Kuo M. Mechanistic comparison of human high-affinity copper transporter 1-mediated transport between copper ion and cisplatin. Mol Pharmacol 76: 843-853, 2009.
31. Linz R, Lutsenko S. Copper-transporting ATPases ATP7A and ATP7B: cousins, not twins. J. Bioenerg Biomembr 39: 403-407, 2007.
32. MacPherson IS, Murphy ME. Type-2 copper-containing enzymes. Cell Mol Life Sei 64: 2887-2899, 2007.
33. Markovic J, Mora NJ, Broseta AM, Gimeno A, de-la-Concepcion N, Vina J, Pallardo FV. The depletion of nuclear glutathione impairs cell proliferation in 3t3 fibroblasts. PLos One 4: e6413, 2009.
34. Maryon EB, Molloy SA, Kaplan JH. O-linked glycosylation at threonine 27 protects the copper transporter hCTRl from proteolytic cleavage in mammalian cells. J Biol Chem 282: 20376-20387, 2007.
35. Mercer JF. The molecular basis of copper-transport diseases. Trends Mol Med 7: 64-69, 2001.
36. Merker K, Hapke D, Reckzeh K, Schmidt H, Lochs H, Grüne T. Copper related toxic effects on cellular protein metabolism in human astrocytes. Biofactors 24: 255-261, 2005.
37. Molloy SA, Kaplan JH. Copper-dependent recycling of hCTRl, the human high affinity copper transporter. J Biol Chem 284: 29704-29713, 2009.
38. O'Halloran TV, Culotta VC. Metallochaperones, an intracellular shuttle service for metal ions. J. Biol Chem 275: 25057-25060, 2000.
39. Ogra Y, Aoyama M, Suzuki KT. Protective role of metallothionein against copper depletion. Arch Biochem Biophys 451: 112-118, 2006.
40. Pope CR, Flores AG, Kaplan JH, Unger VM. Structure and function of copper uptake transporters. Curr Top Membr 69: 97-112, 2012.
41. Puig S, Lee J, Lau M, Thiele DJ. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J. Biol Chem 277: 26021-26030, 2002.
42. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. Unde-tectable intracellular free copper: the requirement of a copper chaperone for Superoxide dismutase. Science 284: 805-808, 1999.
43. Safaei R, Howell SB. Copper transporters regulate the cellular pharmacology and sensitivity to Pt drugs. Crit Rev Oncol Hematol 53: 13-23, 2005.
44. Shiloh MU, Ruan J, Nathan C. Evaluation of bacterial survival and phagocyte function with a fluorescence-based microplate assay. Infect Immun 65: 3193-3198, 1997.
45. Wernimont AK, Huffman DL, Lamb AL, O'Halloran TV, Rosenzweig AC. Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nat Struct Biol 7: 766-771, 2000.
46. White C, Lee J, Kambe T, Fritsche K, Petris MJ. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol Chem 284: 33949-33956, 2009.
47. Wong PC, Waggoner D, Subramaniam JR, Tessarollo L, Bartnikas TB, Culotta VC, Price DL, Rothstein J, Gitlin JD. Copper chaperone for Superoxide dismutase is essential to activate mammalian Cu/Zn super-oxide dismutase. Proc Natl Acad Sei USA 97: 2886-2891, 2000.
48. Xiao Z, Brose J, Schimo S, Ackland SM, La Fontaine S, Wedd AG. Unification of the copper(I) binding affinities of the metallo-chaperones Atxl, Atoxl, and related proteins: detection probes and affinity standards. JBiol Chem 286: 11047-11055, 2011.
49. Zhou B, Gitschier J. hCTRl: a human gene for copper uptake identified by complementation in yeast. Proc Natl Acad Sei USA 94: 7481-7486, 1997.
50. Zimnicka AM, Maryon EB, Kaplan JH. Human copper transporter hCTRl mediates basolateral uptake of copper into enterocytes: implications for copper homeostasis. J Biol Chem 282: 26471-26480, 2007.