Clusterin and COMMD1 independently regulate degradation of the mammalian copper ATPases ATP7A and ATP7B

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2485-2499

  Materia, Stephanie ^a   Cater, Michael A ^b   Klomp, Leo W J ^c   Mercer, Julian F B ^a   La Fontaine, Sharon ^a  

^a DEAKIN UNIVERSITY   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ATPASES; CLUSTERIN; COPPER HOMEOSTASIS; COPPER TOXICITY; DEGRADATION PATHWAYS; ENDOGENOUS LEVEL; GENES ENCODING; INDEPENDENT SYSTEMS; MISFOLDING; OVER-EXPRESSION; PROTEASOMAL PATHWAY; STRESS CONDITION; WILSON DISEASE;

COPPER; DEGRADATION; GENES; MAMMALS; PHYSIOLOGY;

GLYCOPROTEINS;

CELL PROTEIN; CLUSTERIN; COPPER; COPPER METABOLISM MURR1 DOMAIN; MENKES PROTEIN; PROTEASOME; UNCLASSIFIED DRUG; WILSON DISEASE PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CHO CELL; COMPLEX FORMATION; CONTROLLED STUDY; COPPER METABOLISM; DOWN REGULATION; ENZYME DEGRADATION; ENZYME REGULATION; FEMALE; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; LYSOSOME; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; QUALITY CONTROL; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATASES; ANIMALS; CATION TRANSPORT PROTEINS; CHO CELLS; CLUSTERIN; CRICETINAE; CRICETULUS; HEK293 CELLS; HEPATOLENTICULAR DEGENERATION; HUMANS; MENKES KINKY HAIR SYNDROME; MICE; MUTATION; PROTEOLYSIS; RATS;

MAMMALIA;

EID: 84856076045     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.302216     Document Type: Article

References (69)

1. Lutsenko, S., Petrukhin, K., Cooper, M. J., Gilliam, C. T., and Kaplan, J. H. (1997) N-terminal domains of human copper-transporting adenosine triphosphatases (the Wilson and Menkes disease proteins) bind copper selectively in vivo and in vitro with stoichiometry of one copper per metal-binding repeat. J. Biol. Chem. 272, 18939-18944 (Pubitemid 27318247)
2. Lutsenko, S., Barnes, N. L., Bartee, M. Y., and Dmitriev, O. Y. (2007) Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87, 1011-1046 (Pubitemid 47084675)
3. Monty, J. F., Llanos, R. M., Mercer, J. F., and Kramer, D. R. (2005) Copper exposure induces trafficking of the Menkes protein in intestinal epithelium of ATP7A transgenic mice. J. Nutr. 135, 2762-2766 (Pubitemid 43156538)
4. Nyasae, L., Bustos, R., Braiterman, L., Eipper, B., and Hubbard, A. (2007) Dynamics of endogenous ATP7A (Menkes protein) in intestinal epithelial cells. Copper-dependent redistribution between two intracellular sites. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1181-1194 (Pubitemid 46557793)
5. Roelofsen, H., Wolters, H., Van Luyn, M. J., Miura, N., Kuipers, F., and Vonk, R. J. (2000) Copper-induced apical trafficking of ATP7B in polarized hepatoma cells provides a mechanism for biliary copper excretion. Gastroenterology 119, 782-793
6. Cater, M. A., La Fontaine, S., Shield, K., Deal, Y., and Mercer, J. F. (2006) ATP7B mediates vesicular sequestration of copper. Insight into biliary copper excretion. Gastroenterology 130, 493-506 (Pubitemid 43202046)
7. 2-terminal signals in ATP7B Cu-ATPase mediate its Cu-dependent anterograde traffic in polarized hepatic cells. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G904-916
8. La Fontaine, S., and Mercer, J. F. (2007) Trafficking of the copper-ATPases, ATP7A and ATP7B. Role in copper homeostasis. Arch. Biochem. Biophys. 463, 149-167 (Pubitemid 47030343)
9. Danks, D. M. (1995) in The Metabolic and Molecular Basis of Inherited Disease (Scriver, C. R., Beaudet, A. L., Sly, W. M., and Valle, D., eds) pp. 2211-2235, McGraw-Hill, New York
10. Kim, B. E., and Petris, M. J. (2007) Phenotypic diversity of Menkes disease in mottled mice is associated with defects in localization and trafficking of the ATP7A protein. J. Med. Genet. 44, 641-646
11. Kaler, S. G. (2011) ATP7A-related copper transport disease-emerging concepts and future trends. Nat. Rev. Neurol. 7, 15-29
12. Terada, K., Aiba, N., Yang, X. L., Iida, M., Nakai, M., Miura, N., and Sugiyama, T. (1999) Biliary excretion of copper in LEC rat after introduction of copper transporting P-type ATPase, ATP7B. FEBS Lett. 448, 53-56 (Pubitemid 29151630)
13. Das, S. K., and Ray, K. (2006) Wilsons disease. An update. Nat. Clin. Pract. Neurol. 2, 482-493
14. Gouider-Khouja, N. (2009) Wilsons disease. Parkinsonism Relat. Disord. 15, S126-129
15. Materia, S., Cater, M. A., Klomp, L. W., Mercer, J. F., and La Fontaine, S. (2011) Clusterin (apolipoprotein J), a molecular chaperone that facilitates degradation of the copper-ATPases ATP7A and ATP7B. J. Biol. Chem. 286, 10073-10083
16. Tao, T. Y., Liu, F., Klomp, L., Wijmenga, C., and Gitlin, J. D. (2003) The copper toxicosis gene product Murr1 directly interacts with the Wilson disease protein. J. Biol. Chem. 278, 41593-41596 (Pubitemid 37310414)
17. de Bie, P., van de Sluis, B., Burstein, E., van de Berghe, P. V., Muller, P., Berger, R., Gitlin, J. D., Wijmenga, C., and Klomp, L. W. (2007) Distinct Wilsons disease mutations in ATP7B are associated with enhanced binding to COMMD1 and reduced stability of ATP7B. Gastroenterology 133, 1316-1326 (Pubitemid 47494457)
18. van den Berghe, P. V., Stapelbroek, J. M., Krieger, E., de Bie, P., van de Graaf, S. F., de Groot, R. E., van Beurden, E., Spijker, E., Houwen, R. H., Berger, R., and Klomp, L. W. (2009) Reduced expression of ATP7B affected by Wilson disease-causing mutations is rescued by pharmacological folding chaperones 4-phenylbutyrate and curcumin. Hepatology 50, 1783-1795
19. 2-independent Proteolysis of HIF-1α via HSP90/70. PLoS One 4, e7332
20. van de Sluis, B., Mao, X., Zhai, Y., Groot, A. J., Vermeulen, J. F., van der Wall, E., van Diest, P. J., Hofker, M. H., Wijmenga, C., Klomp, L. W., Cho, K. R., Fearon, E. R., Vooijs, M., and Burstein, E. (2010) COMMD1 disrupts HIF-1α/β dimerization and inhibits human tumor cell invasion. J. Clin. Invest. 120, 2119-2130
21. Maine, G. N., Mao, X., Komarck, C. M., and Burstein, E. (2007) COMMD1 promotes the ubiquitination of NF-κB subunits through a cullin-containing ubiquitin ligase. EMBO J. 26, 436-447 (Pubitemid 46160944)
22. van de Sluis, B., Muller, P., Duran, K., Chen, A., Groot, A. J., Klomp, L. W., Liu, P. P., and Wijmenga, C. (2007) Increased activity of hypoxia-inducible factor 1 is associated with early embryonic lethality in Commd1 null mice. Mol. Cell Biol. 27, 4142-4156 (Pubitemid 47011010)
23. Zoubeidi, A., Ettinger, S., Beraldi, E., Hadaschik, B., Zardan, A., Klomp, L. W., Nelson, C. C., Rennie, P. S., and Gleave, M. E. (2010) Clusterin facilitates COMMD1 and IκB degradation to enhance NF-κB activity in prostate cancer cells. Mol. Cancer Res. 8, 119-130
24. Humphreys, D. T., Carver, J. A., Easterbrook-Smith, S. B., and Wilson, M. R. (1999) Clusterin has chaperone-like activity similar to that of small heat shock proteins. J. Biol. Chem. 274, 6875-6881
25. Balantinou, E., Trougakos, I. P., Chondrogianni, N., Margaritis, L. H., and Gonos, E. S. (2009) Transcriptional and post-translational regulation of clusterin by the two main cellular proteolytic pathways. Free Radic. Biol. Med. 46, 1267-1274
26. Wyatt, A. R., Yerbury, J. J., Berghofer, P., Greguric, I., Katsifis, A., Dobson, C. M., and Wilson, M. R. (2011) Clusterin facilitates in vivo clearance of extracellular misfolded proteins. Cell. Mol. Life Sci. 68, 3919-3931
27. Vonk, W. I., de Bie, P., Wichers, C. G., van den Berghe, P. V., van der Plaats, R., Berger, R., Wijmenga, C., Klomp, L. W., and van de Sluis, B. (2011) The copper-transporting capacity of ATP7A mutants associated with Menkes disease is ameliorated by COMMD1 as a result of improved protein expression. Cell. Mol. Life Sci. 69, 149-163
28. Aronow, B. J., Lund, S. D., Brown, T. L., Harmony, J. A., and Witte, D. P. (1993) Apolipoprotein J expression at fluid-tissue interfaces. Potential role in barrier cytoprotection. Proc. Natl. Acad. Sci. U.S.A. 90, 725-729 (Pubitemid 23028938)
29. Wilson, M. R., Yerbury, J. J., and Poon, S. (2008) Potential roles of abundant extracellular chaperones in the control of amyloid formation and toxicity. Mol. Biosyst. 4, 42-52 (Pubitemid 350261753)
30. Leskov, K. S., Klokov, D. Y., Li, J., Kinsella, T. J., and Boothman, D. A. (2003) Synthesis and functional analyses of nuclear clusterin, a cell death protein. J. Biol. Chem. 278, 11590-11600 (Pubitemid 36792721)
31. Trougakos, I. P., and Gonos, E. S. (2006) Regulation of clusterin/apolipo-protein J, a functional homologue to the small heat shock proteins, by oxidative stress in ageing and age-related diseases. Free Radic. Res. 40, 1324-1334 (Pubitemid 44698281)
32. Pucci, S., Mazzarelli, P., Nucci, C., Ricci, F., and Spagnoli, L. G. (2009) CLU "in and out." Looking for a link. Adv. Cancer Res. 105, 93-113
33. van De Sluis, B., Rothuizen, J., Pearson, P. L., van Oost, B. A., and Wijmenga, C. (2002) Identification of a new copper metabolism gene by positional cloning in a purebred dog population. Hum. Mol. Genet. 11, 165-173 (Pubitemid 34157008)
34. Klomp, A. E., van de Sluis, B., Klomp, L. W., and Wijmenga, C. (2003) The ubiquitously expressed MURR1 protein is absent in canine copper toxicosis. J. Hepatol. 39, 703-709 (Pubitemid 37372177)
35. Maine, G. N., and Burstein, E. (2007) COMMD proteins. COMMing to the scene. Cell. Mol. Life Sci. 64, 1997-2005
36. de Bie, P., van de Sluis, B., Klomp, L., and Wijmenga, C. (2005) The many faces of the copper metabolism protein MURR1/COMMD1. J. Hered. 96, 803-811 (Pubitemid 41752441)
37. van de Sluis, B., Groot, A. J., Wijmenga, C., Vooijs, M., and Klomp, L. W. (2007) COMMD1. A novel protein involved in the proteolysis of proteins. Cell Cycle 6, 2091-2098 (Pubitemid 47450407)
38. Bailey, R. W., Dunker, A. K., Brown, C. J., Garner, E. C., and Griswold, M. D. (2001) Clusterin, a binding protein with a molten globule-like region. Biochemistry 40, 11828-11840 (Pubitemid 32906044)
39. Nuutinen, T., Suuronen, T., Kauppinen, A., and Salminen, A. (2009) Clusterin, a forgotten player in Alzheimers disease. Brain Res. Rev. 61, 89-104
40. Burkhead, J. L., Morgan, C. T., Shinde, U., Haddock, G., and Lutsenko, S. (2009) COMMD1 forms oligomeric complexes targeted to the endocytic membranes via specific interactions with phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 284, 696-707
41. Sommerhalter, M., Zhang, Y., and Rosenzweig, A. C. (2007) Solution structure of the COMMD1 N-terminal domain. J. Mol. Biol. 365, 715-721 (Pubitemid 44960358)
42. Cater, M. A., Forbes, J., La Fontaine, S., Cox, D., and Mercer, J. F. (2004) Intracellular trafficking of the human Wilson protein. The role of the six N-terminal metal-binding sites. Biochem. J. 380, 805-813 (Pubitemid 38850522)
43. Strausak, D., La Fontaine, S., Hill, J., Firth, S. D., Lockhart, P. J., and Mercer, J. F. (1999) The role of GMXCXXC metal binding sites in the copper-induced redistribution of the Menkes protein. J. Biol. Chem. 274, 11170-11177
44. La Fontaine, S., Theophilos, M. B., Firth, S. D., Gould, R., Parton, R. G., and Mercer, J. F. (2001) Effect of the toxic milk mutation (tx) on the function and intracellular localization of Wnd, the murine homologue of the Wilson copper ATPase. Hum. Mol. Genet. 10, 361-370 (Pubitemid 32166547)
45. van den Berghe, P. V., Folmer, D. E., Malingré, H. E., van Beurden, E., Klomp, A. E., van de Sluis, B., Merkx, M., Berger, R., and Klomp, L. W. (2007) Human copper transporter 2 is localized in late endosomes and lysosomes and facilitates cellular copper uptake. Biochem. J. 407, 49-59 (Pubitemid 47535580)
46. Ke, B. X., Llanos, R. M., Wright, M., Deal, Y., and Mercer, J. F. (2006) Alteration of copper physiology in mice overexpressing the human Menkes protein ATP7A. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R1460-1467
47. Payne, A. S., Kelly, E. J., and Gitlin, J. D. (1998) Functional expression of the Wilson disease protein reveals mislocalization and impaired copper-dependent trafficking of the common H1069Q mutation. Proc. Natl. Acad. Sci. U.S.A. 95, 10854-10859 (Pubitemid 28413158)
48. de Bie, P., Muller, P., Wijmenga, C., and Klomp, L. W. (2007) Molecular pathogenesis of Wilson and Menkes disease. Correlation of mutations with molecular defects and disease phenotypes. J. Med. Genet. 44, 673-688 (Pubitemid 350161581)
49. Theophilos, M. B., Cox, D. W., and Mercer, J. F. (1996) The toxic milk mouse is a murine model of Wilson disease. Hum. Mol. Genet. 5, 1619-1624 (Pubitemid 26328879)
50. Voskoboinik, I., Greenough, M., La Fontaine, S., Mercer, J. F., and Camakaris, J. (2001) Functional studies on the Wilson copper P-type ATPase and toxic milk mouse mutant. Biochem. Biophys. Res. Commun. 281, 966-970 (Pubitemid 32917826)
51. Majumdar, R., Al Jumah, M., Al Rajeh, S., Fraser, M., Al Zaben, A., Awada, A., Al Traif, I., and Paterson, M. (2000) A novel deletion mutation within the carboxyl terminus of the copper-transporting ATPase gene causes Wilson disease. J. Neurol. Sci. 179, 140-143
52. Burstein, E., Ganesh, L., Dick, R. D., van De Sluis, B., Wilkinson, J. C., Klomp, L. W., Wijmenga, C., Brewer, G. J., Nabel, G. J., and Duckett, C. S. (2004) A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J. 23, 244-254 (Pubitemid 38165764)
53. Rizzi, F., Caccamo, A. E., Belloni, L., and Bettuzzi, S. (2009) Clusterin is a short half-life, polyubiquitinated protein, which controls the fate of prostate cancer cells. J. Cell. Physiol. 219, 314-323
54. Huang, Y., Wu, M., and Li, H. Y. (2008) Tumor suppressor ARF promotes non-classic proteasome-independent polyubiquitination of COMMD1. J. Biol. Chem. 283, 11453-11460
55. Miyayama, T., Hiraoka, D., Kawaji, F., Nakamura, E., Suzuki, N., and Ogra, Y. (2010) Roles of COMM-domain-containing 1 in stability and recruitment of the copper-transporting ATPase in a mouse hepatoma cell line. Biochem. J. 429, 53-61
56. Spee, B., Arends, B., van Wees, A. M., Bode, P., Penning, L. C., and Rothuizen, J. (2007) Functional consequences of RNA interference targeting COMMD1 in a canine hepatic cell line in relationship to copper toxicosis. Anim. Genet. 38, 168-170 (Pubitemid 46525327)
57. Barnes, N., Bartee, M. Y., Braiterman, L., Gupta, A., Ustiyan, V., Zuzel, V., Kaplan, J. H., Hubbard, A. L., and Lutsenko, S. (2009) Cell-specific trafficking suggests a new role for renal ATP7B in the intracellular copper storage. Traffic 10, 767-779
58. Sarkar, B., and Roberts, E. A. (2011) The puzzle posed by COMMD1. A newly discovered protein binding Cu(II). Metallomics 3, 20-27
59. Thoms, H. C., Loveridge, C. J., Simpson, J., Clipson, A., Reinhardt, K., Dunlop, M. G., and Stark, L. A. (2010) Nucleolar targeting of RelA(p65) is regulated by COMMD1-dependent ubiquitination. Cancer Res. 70, 139-149
60. Biasio, W., Chang, T., McIntosh, C. J., and McDonald, F. J. (2004) Identification of Murr1 as a regulator of the human δ-epithelial sodium channel. J. Biol. Chem. 279, 5429-5434 (Pubitemid 38220566)
61. Ke, Y., Butt, A. G., Swart, M., Liu, Y. F., and McDonald, F. J. (2010) COMMD1 down-regulates the epithelial sodium channel through Nedd4-2. Am. J. Physiol. Renal Physiol. 298, F1445-1456
62. Vonk, W. I., Wijmenga, C., Berger, R., van de Sluis, B., and Klomp, L. W. (2010) Cu,Zn superoxide dismutase maturation and activity are regulated by COMMD1. J. Biol. Chem. 285, 28991-29000
63. Horslen, S., and Hahn, S. (2010) Genotype-phenotype correlation in Wilson disease. J. Clin. Gastroenterol. 44, 387-388
64. Møller, L. B., Mogensen, M., and Horn, N. (2009) Molecular diagnosis of Menkes disease. Genotype-phenotype correlation. Biochimie 91, 1273-1277
65. Senzolo, M., Loreno, M., Fagiuoli, S., Zanus, G., Canova, D., Masier, A., Russo, F. P., Sturniolo, G. C., and Burra, P. (2007) Different neurological outcome of liver transplantation for Wilsons disease in two homozygotic twins. Clin. Neurol. Neurosurg. 109, 71-75 (Pubitemid 44855276)
66. Borm, B., Møller, L. B., Hausser, I., Emeis, M., Baerlocher, K., Horn, N., and Rossi, R. (2004) Variable clinical expression of an identical mutation in the ATP7A gene for Menkes disease/occipital horn syndrome in three affected males in a single family. J. Pediatr. 145, 119-121 (Pubitemid 38962463)
67. Takeshita, Y., Shimizu, N., Yamaguchi, Y., Nakazono, H., Saitou, M., Fujikawa, Y., and Aoki, T. (2002) Two families with Wilson disease in which siblings showed different phenotypes. J. Hum. Genet. 47, 543-547 (Pubitemid 35238971)
68. Gupta, A., Bhattacharjee, A., Dmitriev, O. Y., Nokhrin, S., Braiterman, L., Hubbard, A. L., and Lutsenko, S. (2011) Cellular copper levels determine the phenotype of the Arg-875 variant of ATP7B/Wilson disease protein. Proc. Natl. Acad. Sci. U.S.A. 108, 5390-5395
69. Drévillon, L., Tanguy, G., Hinzpeter, A., Arous, N., de Becdelièvre, A., Aissat, A., Tarze, A., Goossens, M., and Fanen, P. (2011) COMMD1-mediated ubiquitination regulates CFTR trafficking. PLoS One 6, e18334