Regulation of Copper Transporters in Human Cells

Current Topics in Membranes

Volumn 69, Issue , 2012, Pages 137-161

  Hasan, Nesrin M ^a   Lutsenko, Svetlana ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

ATP7A; ATP7B; Copper; HCTR1; Trafficking

Indexed keywords

EID: 84867173057     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394390-3.00006-9     Document Type: Chapter

References (64)

1. Araya M., Nunez H., Pavez L., Arredondo M., Mendez M., Cisternas F., et al. Administration of high doses of copper to capuchin monkeys does not cause liver damage but induces transcriptional activation of hepatic proliferative responses. Journal of Nutrition 2012, 142(2):233-237.
2. Arredondo M., Nunez H., Lopez G., Pizarro F., Ayala M., Araya M. Influence of estrogens on copper indicators: in vivo and in vitro studies. Biological Trace Element Research 2010, 134(3):252-264.
3. Arredondo M., Munoz P., Mura C.V., Nunez M.T. DMT1, a physiologically relevant apical Cu1+ transporter of intestinal cells. American Journal of Physiology Cell Physiology 2003, 284(6):C1525-C1530.
4. Bartee M.Y., Ralle M., Lutsenko S. The loop connecting metal-binding domains 3 and 4 of ATP7B is a target of a kinase-mediated phosphorylation. Biochemistry 2009, 48(24):5573-5581.
5. Braiterman L., Nyasae L., Guo Y., Bustos R., Lutsenko S., Hubbard A. Apical targeting and Golgi retention signals reside within a 9-amino acid sequence in the copper-ATPase, ATP7B. American Journal of Physiology Gastrointestinal Liver Physiology 2009, 296(2):G433-G444.
6. Braiterman L., Nyasae L., Leves F., Hubbard A.L. Critical roles for the COOH terminus of the Cu-ATPase ATP7B in protein stability, trans-Golgi network retention, copper sensing, and retrograde trafficking. American Journal of Physiology Gastrointestinal Liver Physiology 2011, 301(1):G69-G81.
7. Cater M.A., La Fontaine S., Mercer J.F. Copper binding to the N-terminal metal-binding sites or the CPC motif is not essential for copper-induced trafficking of the human Wilson protein (ATP7B). Biochemical Journal 2007, 401(1):143-153.
8. Cater M.A., La Fontaine S., Shield K., Deal Y., Mercer J.F. ATP7B mediates vesicular sequestration of copper: insight into biliary copper excretion. Gastroenterology 2006, 130(2):493-506.
9. Chen H.H., Song I.S., Hossain A., Choi M.K., Yamane Y., Liang Z.D., et al. Elevated glutathione levels confer cellular sensitization to cisplatin toxicity by up-regulation of copper transporter hCtr1. Molecular Pharmacology 2008, 74(3):697-704.
10. Cobbold C., Ponnambalam S., Francis M.J., Monaco A.P. Novel membrane traffic steps regulate the exocytosis of the Menkes disease ATPase. Human Molecular Genetics 2002, 11(23):2855-2866.
11. de Bie P., van de Sluis B., Burstein E., van de Berghe P.V., Muller P., Berger R., et al. Distinct Wilson's disease mutations in ATP7B are associated with enhanced binding to COMMD1 and reduced stability of ATP7B. Gastroenterology 2007, 133(4):1316-1326.
12. De Feo C.J., Aller S.G., Siluvai G.S., Blackburn N.J., Unger V.M. Three-dimensional structure of the human copper transporter hCTR1. Proceedings of the National Academy of Sciences of the United States of Amercia 2009, 106(11):4237-4242.
13. DiDonato M., Hsu H.F., Narindrasorasak S., Que L., Sarkar B. Copper-induced conformational changes in the N-terminal domain of the Wilson disease copper-transporting ATPase. Biochemistry 2000, 39(7):1890-1896.
14. Dong-Yun S., Yu-Ru D., Shan-Lin L., Ya-Dong Z., Lian W. Redox stress regulates cell proliferation and apoptosis of human hepatoma through Akt protein phosphorylation. FEBS Letters 2003, 542(1-3):60-64.
15. Du X., Wang X., Li H., Sun H. Comparison between copper and cisplatin transport mediated by human copper transporter 1 (hCTR1). Metallomics 2012, 4(7). 679-685.
16. Eisses J.F., Chi Y., Kaplan J.H. Stable plasma membrane levels of hCTR1 mediate cellular copper uptake. Journal of Biological Chemistry 2005, 280(10):9635-9639.
17. Eisses J.F., Kaplan J.H. Molecular characterization of hCTR1, the human copper uptake protein. Journal of Biological Chemistry 2002, 277(32):29162-29171.
18. Fedjaev M., Parmar A., Xu Y., Vyetrogon K., Difalco M.R., Ashmarina M., et al. Global analysis of protein phosphorylation networks in insulin signaling by sequential enrichment of phosphoproteins and phosphopeptides. Molecular BioSystems 2012, 8(5):1461-1471.
19. Francis M.J., Jones E.E., Levy E.R., Martin R.L., Ponnambalam S., Monaco A.P. Identification of a di-leucine motif within the C terminus domain of the Menkes disease protein that mediates endocytosis from the plasma membrane. Journal of Cell Science 1999, 112(Pt 11):1721-1732.
20. Guo Y., Smith K., Lee J., Thiele D.J., Petris M.J. Identification of methionine-rich clusters that regulate copper-stimulated endocytosis of the human Ctr1 copper transporter. Journal of Biological Chemistry 2004, 279(17):17428-17433.
21. Gupta A., Bhattacharjee A., Dmitriev O.Y., Nokhrin S., Braiterman L., Hubbard A.L., et al. Cellular copper levels determine the phenotype of the Arg875 variant of ATP7B/Wilson disease protein. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(13):5390-5395.
22. Gupta A., Lutsenko S. Human copper transporters: mechanism, role in human diseases and therapeutic potential. Future Medicinal Chem 2009, 1(6):1125-1142.
23. Haas K.L., Putterman A.B., White D.R., Thiele D.J., Franz K.J. Model peptides provide new insights into the role of histidine residues as potential ligands in human cellular copper acquisition via Ctr1. Journal of American Chemical Society 2011, 133(12):4427-4437.
24. Hardman B., Manuelpillai U., Wallace E.M., Monty J.F., Kramer D.R., Kuo Y.M., et al. Expression, localisation and hormone regulation of the human copper transporter hCTR1 in placenta and choriocarcinoma Jeg-3 cells. Placenta 2006, 27(9-10):968-977.
25. Hasan N.M., Gupta A., Polishchuk E., Yu C.H., Polishchuk R., Dmitriev O.Y., et al. Molecular events initiating the exit of a copper-transporting ATPase ATP7B from the trans-Golgi network. Journal of Biological Chemistry 2012.
26. Hatori Y., Clasen S., Hasan N.M., Barry A.N., Lutsenko S. Functional partnership of the copper export machinery and glutathione balance in human cells. Journal of Biological Chemistry 2012, 287(32):26678-26687.
27. Huttlin E.L., Jedrychowski M.P., Elias J.E., Goswami T., Rad R., Beausoleil S.A., et al. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 2010, 143(7):1174-1189.
28. Kaplan J.H., Lutsenko S. Copper transport in mammalian cells: special care for a metal with special needs. Journal of Biological Chemistry 2009, 284(38):25461-25465.
29. Klomp A.E., Tops B.B., Van Denberg I.E., Berger R., Klomp L.W. Biochemical characterization and subcellular localization of human copper transporter 1 (hCTR1). Biochemical Journal 2002, 364(Pt 2):497-505.
30. Kuo Y.M., Gybina A.A., Pyatskowit J.W., Gitschier J., Prohaska J.R. Copper transport protein (Ctr1) levels in mice are tissue specific and dependent on copper status. Journal of Nutrition 2006, 136(1):21-26.
31. Lee J., Petris M.J., Thiele D.J. Characterization of mouse embryonic cells deficient in the ctr1 high affinity copper transporter. Identification of a Ctr1-independent copper transport system. Journal of Biological Chemistry 2002, 277(43):40253-40259.
32. Liang Z.D., Tsai W.B., Lee M.Y., Savaraj N., Kuo M.T. Specificity protein 1 (sp1) oscillation is involved in copper homeostasis maintenance by regulating human high-affinity copper transporter 1 expression. Molecular Pharmacology 2012, 81(3):455-464.
33. Lundby A., Secher A., Lage K., Nordsborg N.B., Dmytriyev A., Lundby C., et al. Quantitative maps of protein phosphorylation sites across 14 different rat organs and tissues. Nature Communications 2012, 3:876.
34. Lutsenko S., Petrukhin K., Cooper M.J., Gilliam C.T., Kaplan J.H. N-terminal domains of human copper-transporting adenosine triphosphatases (the Wilson's and Menkes disease proteins) bind copper selectively in vivo and in vitro with stoichiometry of one copper per metal-binding repeat. Journal of Biological Chemistry 1997, 272(30):18939-18944.
35. Markovic J., Mora N.J., Broseta A.M., Gimeno A., de-la-Concepcion N., Vina J., et al. The depletion of nuclear glutathione impairs cell proliferation in 3t3 fibroblasts. PLoS One 2009, 4(7):e6413.
36. Molloy S.A., Kaplan J.H. Copper-dependent recycling of hCTR1, the human high affinity copper transporter. Journal of Biological Chemistry 2009, 284(43):29704-29713.
37. Monetti M., Nagaraj N., Sharma K., Mann M. Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nature Methods 2011, 8(8):655-658.
38. Nkabyo Y.S., Ziegler T.R., Gu L.H., Watson W.H., Jones D.P. Glutathione and thioredoxin redox during differentiation in human colon epithelial (Caco-2) cells. American Journal of Physiology Gastrointestinal Liver Physiology 2002, 283(6):G1352-G1359.
39. Nose Y., Kim B.E., Thiele D.J. Ctr1 drives intestinal copper absorption and is essential for growth, iron metabolism, and neonatal cardiac function. Cell Metabolism 2006, 4(3):235-244.
40. Petris M.J., Smith K., Lee J., Thiele D.J. Copper-stimulated endocytosis and degradation of the human copper transporter, hCtr1. Journal of Biological Chemistry 2003, 278(11):9639-9646.
41. Pilankatta R., Lewis D., Adams C.M., Inesi G. High yield heterologous expression of wild-type and mutant Cu+-ATPase (ATP7B, Wilson disease protein) for functional characterization of catalytic activity and serine residues undergoing copper-dependent phosphorylation. Journal of Biological Chemistry 2009, 284(32):21307-21316.
42. Pilankatta R., Lewis D., Inesi G. Involvement of protein kinase D in expression and trafficking of ATP7B (copper ATPase). Journal of Biological Chemistry 2011, 286(9):7389-7396.
43. Pourvali K., Matak P., Latunde-Dada G.O., Solomou S., Mastrogiannaki M., Peyssonnaux C., et al. Basal expression of copper transporter 1 in intestinal epithelial cells is regulated by hypoxia-inducible factor 2alpha. FEBS Letters 2012, 586(16):2423-2427.
44. Puig S., Mira H., Dorcey E., Sancenon V., Andres-Colas N., Garcia-Molina A., et al. Higher plants possess two different types of ATX1-like copper chaperones. Biochemical and Biophysical Research Communications 2007, 354(2):385-390.
45. Ralle M., Huster D., Vogt S., Schirrmeister W., Burkhead J.L., Capps T.R., et al. Wilson disease at a single cell level: intracellular copper trafficking activates compartment-specific responses in hepatocytes. Journal of Biological Chemistry 2010, 285(40):30875-30883.
46. Ranjan P., Anathy V., Burch P.M., Weirather K., Lambeth J.D., Heintz N.H. Redox-dependent expression of cyclin D1 and cell proliferation by Nox1 in mouse lung epithelial cells. Antioxidants & Redox Signaling 2006, 8(9-10):1447-1459.
47. Singleton W.C., McInnes K.T., Cater M.A., Winnall W.R., McKirdy R., Yu Y., et al. Role of glutaredoxin1 and glutathione in regulating the activity of the copper-transporting P-type ATPases, ATP7A and ATP7B. Journal of Biological Chemistry 2010, 285(35):27111-27121.
48. Song I.S., Chen H.H., Aiba I., Hossain A., Liang Z.D., Klomp L.W., et al. Transcription factor Sp1 plays an important role in the regulation of copper homeostasis in mammalian cells. Molecular Pharmacology 2008, 74(3):705-713.
49. Stephenson S.E., Dubach D., Lim C.M., Mercer J.F., La Fontaine S. A single PDZ domain protein interacts with the Menkes copper ATPase, ATP7A. A new protein implicated in copper homeostasis. Journal of Biological Chemistry 2005, 280(39):33270-33279.
50. Strausak D., La Fontaine S., Hill J., Firth S.D., Lockhart P.J., Mercer J.F. The role of GMXCXXC metal binding sites in the copper-induced redistribution of the Menkes protein. Journal of Biological Chemistry 1999, 274(16):11170-11177.
51. Tennant J., Stansfield M., Yamaji S., Srai S.K., Sharp P. Effects of copper on the expression of metal transporters in human intestinal Caco-2 cells. FEBS Letters 2002, 527(1-3):239-244.
52. Tsigelny I.F., Sharikov Y., Greenberg J.P., Miller M.A., Kouznetsova V.L., Larson C.A., et al. An all-atom model of the structure of human copper transporter 1. Cell Biochemistry and Biophysics 2012, 63(3):223-234.
53. Tsivkovskii R., MacArthur B.C., Lutsenko S. The Lys1010-Lys1325 fragment of the Wilson's disease protein binds nucleotides and interacts with the N-terminal domain of this protein in a copper-dependent manner. Journal of Biological Chemistry 2001, 276(3):2234-2242.
54. Turski M.L., Brady D.C., Kim H.J., Kim B.E., Nose Y., Counter C.M., et al. A novel role for copper in Ras/mitogen-activated protein kinase signaling. Molecular Cell Biology 2012, 32(7):1284-1295.
55. Vanderwerf S.M., Cooper M.J., Stetsenko I.V., Lutsenko S. Copper specifically regulates intracellular phosphorylation of the Wilson's disease protein, a human copper-transporting ATPase. Journal of Biological Chemistry 2001, 276(39):36289-36294.
56. Vanderwerf S.M., Lutsenko S. The Wilson's disease protein expressed in Sf9 cells is phosphorylated. Biochemical Society Transactions 2002, 30(4):739-741.
57. Veldhuis N.A., et al. Phosphorylation regulates copper-responsive trafficking of the Menkes copper transporting P-type ATPase. International Journal of Biochemistry & Cell Biology 2009, 41(12):2403-2412.
58. Voskoboinik I., Fernando R., Veldhuis N., Hannan K.M., Marmy-Conus N., Pearson R.B., et al. Protein kinase-dependent phosphorylation of the Menkes copper P-type ATPase. Biochemical and Biophysics Research Communications 2003, 303(1):337-342.
59. Walker J.M., Huster D., Ralle M., Morgan C.T., Blackburn N.J., Lutsenko S. The N-terminal metal-binding site 2 of the Wilson's Disease Protein plays a key role in the transfer of copper from Atox1. Journal of Biological Chemistry 2004, 279(15):15376-15384.
60. White C., Kambe T., Fulcher Y.G., Sachdev S.W., Bush A.I., Fritsche K., et al. Copper transport into the secretory pathway is regulated by oxygen in macrophages. Journal of Cell Science 2009, 122(Pt 9):1315-1321.
61. Yamane Y., Furuichi M., Song R., Van N.T., Mulcahy R.T., Ishikawa T., et al. Expression of multidrug resistance protein/GS-X pump and gamma-glutamylcysteine synthetase genes is regulated by oxidative stress. Journal of Biological Chemistry 1998, 273(47):31075-31085.
62. Zheng G., Chen J., Zheng W. Relative contribution of CTR1 and DMT1 in copper transport by the blood-CSF barrier: implication in manganese-induced neurotoxicity. Toxicology and Applied Pharmacology 2012, 260(3):285-293.
63. Zheng Z., White C., Lee J., Peterson T.S., Bush A.I., Sun G.Y., et al. Altered microglial copper homeostasis in a mouse model of Alzheimer's disease. Journal of Neurochemistry 2010, 114(6):1630-1638.
64. Zimnicka A.M., Ivy K., Kaplan J.H. Acquisition of dietary copper: a role for anion transporters in intestinal apical copper uptake. American Journal of Physiology Cell Physiology 2011, 300(3):C588-C599.