COMMD1 is linked to the WASH complex and regulates endosomal trafficking of the copper transporter ATP7A

Molecular Biology of the Cell

Volumn 26, Issue 1, 2015, Pages 91-103

  Phillips Krawczak, Christine A ^a   Singla, Amika ^b   Starokadomskyy, Petro ^b   Deng, Zhihui ^a,b   Osborne, Douglas G ^a   Li, Haiying ^b   Dick, Christopher J ^a   Gomez, Timothy S ^a   Koenecke, Megan ^b   Zhang, Jin San ^a,c   Dai, Haiming ^d   Sifuentes Dominguez, Luis F ^b   Geng, Linda N ^b   Kaufmann, Scott H ^d   Hein, Marco Y ^e   Wallis, Mathew ^f   McGaughran, Julie ^f,g   Gecz, Jozef ^h,i   Van De Sluis, Bart ^j   Billadeau, Daniel D ^a,k   Burstein, Ezra ^b,l   more..

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e QIQIHAR MEDICAL UNIVERSITY   (China)

^f WENZHOU MEDICAL UNIVERSITY   (China)

^g MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^h ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

ⁱ UNIVERSITY OF QUEENSLAND   (Australia)

^j UNIVERSITY OF ADELAIDE   (Australia)

^k UNIVERSITY OF ADELAIDE   (Australia)

^l UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COILED COIL DOMAIN CONTAINING PROTEIN 22; COILED COIL DOMAIN CONTAINING PROTEIN 93; COPPER; COPPER METABOLISM MURR1 DOMAIN CONTAINING 1 PROTEIN; F ACTIN; MENKES PROTEIN; MULTIPROTEIN COMPLEX; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN AND SCAR HOMOLOGUE COMPLEX; ACTIN BINDING PROTEIN; ADENOSINE TRIPHOSPHATASE; ATP7A PROTEIN, HUMAN; C16ORF62 PROTEIN, HUMAN; CATION TRANSPORT PROTEIN; CCDC22 PROTEIN, HUMAN; COMMD1 PROTEIN, HUMAN; PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR PROTEIN; WASH PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CERULOPLASMIN BLOOD LEVEL; CHROMOSOME 16; COMMD1 GENE; CONTROLLED STUDY; COPPER BLOOD LEVEL; COPPER METABOLISM; COPPER METABOLISM MURR1 DOMAIN CONTAINING 1 GENE; EMBRYO; ENDOSOME; FEMALE; GENE; GENE MUTATION; GENETIC CONSERVATION; HELA CELL LINE; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SURFACE PLASMON RESONANCE; ACTIN FILAMENT; ANIMAL; CELL MOTION; CYTOPLASM; GENETICS; HEK293 CELL LINE; METABOLISM; MUTATION; TRANSPORT VESICLE;

ACTIN CYTOSKELETON; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATASES; ANIMALS; CATION TRANSPORT PROTEINS; CELL MOVEMENT; COPPER; CYTOPLASM; ENDOSOMES; HEK293 CELLS; HELA CELLS; HOMEOSTASIS; HUMANS; MICE; MICROFILAMENT PROTEINS; MUTATION; NEOPLASM PROTEINS; PROTEINS; TRANSPORT VESICLES;

EID: 84920402748     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-06-1073     Document Type: Article

References (53)

1. Biasio W, Chang T, McIntosh C.J., McDonald FJ (2004). Identification of Murr1 as a regulator of the human d epithelial sodium channel. J Biol Chem 279, 5429-5434.
2. Burkhead JL, Morgan CT, Shinde U, Haddock G., Lutsenko S (2009). COMMD1 forms oligomeric complexes targeted to the endocytic membranes via specific interactions with PtdIns(4,5)p2. J Biol Chem 284, 696-707.
3. Burstein E, Ganesh L, Dick R.D., van De Sluis B, Wilkinson JC, Klomp LW, Wijmenga C, Brewer GJ, Nabel GJ, Duckett CS (2004). A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J 23, 244-254.
4. Burstein E, Hoberg JE, Wilkinson A.S., Rumble JM, Csomos RA, Komarck CM, Maine G.N., Wilkinson JC, Mayo MW, Duckett CS (2005). COMMD proteins: a novel family of structural and functional homologs of MURR1. J Biol Chem 280, 22222-22232.
5. Cullen PJ, Korswagen HC (2012). Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 14, 29-37.
6. Dai H, Smith A, Meng X.W., Schneider PA, Pang Y P, Faufmann SH (2011). Transient binding of an activator BH3 domain to the Bak BH3-binding groove initiates Bak oligomerization. J Cell Biol 194, 39-48.
7. Derivery E, Sousa C, Gautier J.J., Lombard B., Loew D, Gautreau A (2009). The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 17, 712-723.
8. Drevillon L, Tanguy G, Hinzpeter A., Arous N, de Becdelievre A, Aissat A, Tarze A., Goossens M, Fanen P (2011). COMMD1-mediated ubiquitination regulates CFTR trafficking. PLoS One 6, e18334.
9. Freeman CL, Hesketh G, Seaman MN (2014). RME-8 coordinates the activity of the WASH complex with the function of the retromer SNX dimer to control endosomal tubulation. J Cell Sci 127, 2053-2070.
10. Gomez TS, Billadeau DD (2009). A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev Cell 17, 699-711.
11. Gomez TS, Gorman JA, de Narvajas AA, Koenig AO, Billadeau DD (2012). Trafficking defects in WASH-knockout fibroblasts originate from collapsed endosomal and lysosomal networks. Mol Biol Cell 23, 3215-3228.
12. Haft CR, de la Luz Sierra M, Bafford R, Lesniak MA, Barr VA, Taylor SI (2000). Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol Biol Cell 11, 4105-4116.
13. Ham H, Guerrier S, Kim J., Schoon RA, Anderson EL, Hamann MJ, Lou Z, Billadeau DD (2013). Dedicator of cytokinesis 8 interacts with talin and Wiskott-Aldrich syndrome protein to regulate NK cell cytotoxicity. J Immunol 190, 3661-3669.
14. Hamza I, Prohaska J, Gitlin JD (2003). Essential role for Atox1 in the copper-mediated intracellular trafficking of the Menkes ATPase. Proc Natl Acad Sci USA 100, 1215-1220.
15. Hao YH, Doyle JM, Ramanathan S, Gomez T.S., Jia D., Xu M, Chen ZJ, Billadeau D.D., Rosen MK, Potts PR (2013). Regulation of WASH-dependent actin polymerization and protein trafficking by ubiquitination. Cell 152, 1051-1064.
16. Harbour ME, Breusegem SY, Antrobus R, Freeman C., Reid E, Seaman MN (2010). The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J Cell Sci 123, 3703-3717.
17. Harbour ME, Breusegem SY, Seaman MN (2012). Recruitment of the endosomal WASH complex is mediated by the extended "tail" of Fam21 binding to the retromer protein Vps35. Biochem J 442, 209-220.
18. Harvey LJ, McArdle HJ (2008). Biomarkers of copper status: a brief update. Br J Nutr 99(Suppl 3), S10-S13.
19. Holloway ZG, Velayos-Baeza A, Howell G.J., Levecque C., Ponnambalam S, Sztul E, Monaco AP (2013). Trafficking of the Menkes copper transporter ATP7A is regulated by clathrin-, AP-2-, AP-1-, and Rab22-dependent steps. Mol Biol Cell 24, 1735-1748, S1-S8.
20. Ishizaki H, Spitzer M, Wildenhain J., Anastasaki C, Zeng Z, Dolma S., Shaw M, Madsen E, Gitlin J, Marais R, Tyers M, et al. (2010). Combined zebrafish-yeast chemical-genetic screens reveal gene-copper-nutrition interactions that modulate melanocyte pigmentation. Dis Models Mech 3, 639-651.
21. Jia D, Gomez TS, Billadeau D.D., Rosen MK (2012). Multiple repeat elements within the FAM21 tail link the WASH actin regulatory complex to the retromer. Mol Biol Cell 23, 2352-2361.
22. Jia D, Gomez TS, Metlagel Z, Umetani J., Otwinowski Z, Rosen MK, Billadeau DD (2010). WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes. Proc Natl Acad Sci USA 107, 10442-10447.
23. Kolanczyk M, Krawitz P, Hecht J., Hupalowska A, Miaczynska M, Marschner K., Schlack C, Emerich D, Kobus K, Kornak U, et al. (2014). Missense variant in CCDC22 causes X-linked recessive intellectual disability with features of Ritscher-Schinzel/3C syndrome. Eur J Hum Genet, doi 10.1038/ejhg.2014.109.
24. Li Y, Calvo SE, Gutman R, Liu J.S., Mootha VK (2014b). Expansion of biological pathways based on evolutionary inference. Cell 158, 213-225.
25. Li H, Chan L, Bartuzi P., Melton SD, Weber A, Ben-Shlomo S, Varol C, Raetz M., Mao X, Starokadomskyy P, et al. (2014a). Copper metabolism domain-containing 1 represses genes that promote inflammation and protects mice from colitis and colitis-associated cancer. Gastroenterology 147, 184-195.
26. Lovicu M, Dessi V, Lepori M.B., Zappu A., Zancan L, Giacchino R, Marazzi M.G., Iorio R., Vegnente A, Vajro P, et al. (2006). The canine copper toxicosis gene MURR1 is not implicated in the pathogenesis of Wilson disease. J Gastroenterol 41, 582-587.
27. Maine GN, Gluck N, Zaidi I.W., Burstein E (2009). Bimolecular affinity purification (BAP): tandem affinity purification using two protein baits. Cold Spring Harb Protoc 10.1101/pdb.prot5318.
28. Maine GN, Mao X, Komarck C.M., Burstein E (2007). COMMD1 promotes the ubiquitination of NF-kB subunits through a Cullin-containing ubiquitin ligase. EMBO J 26, 436-447.
29. Mali P, Yang L, Esvelt K.M., Aach J., Guell M, DiCarlo JE, Norville J.E., Church GM (2013). RNA-guided human genome engineering via Cas9. Science 339, 823-826.
30. Mao X, Gluck N, Li D., Maine GN, Li H, Zaidi IW, Repaka A, Mayo M.W., Burstein E (2009). GCN5 is a required cofactor for a ubiquitin ligase that targets NF-kB/RelA. Genes Dev 23, 849-861.
31. Martinelli D, Travaglini L, Drouin C.A., Ceballos-Picot I, Rizza T, Bertini E., Carrozzo R, Petrini S, de Lonlay P, El Hachem M, et al. (2013). MED-NIK syndrome: a novel defect of copper metabolism treatable by zinc acetate therapy. Brain 136, 872-881.
32. Materia S, Cater MA, Klomp L.W., Mercer JF, La Fontaine S (2012). Clusterin and COMMD1 independently regulate degradation of the mammalian copper-ATPases ATP7A and ATP7B. J Biol Chem 287, 2485-2499.
33. Miyayama T, Hiraoka D, Kawaji F., Nakamura E, Suzuki N, Ogra Y (2010). Roles of COMM-domain-containing 1 in stability and recruitment of the copper-transporting ATPase in a mouse hepatoma cell line. Bio-chem J 429, 53-61.
34. Muller T, van de Sluis B, Zhernakova A, van Binsbergen E, Janecke AR, Bavdekar A, Pandit A, Weirich-Schwaiger H, Witt H, Ellemunter H, et al. (2003). The canine copper toxicosis gene MURR1 does not cause non-Wilsonian hepatic copper toxicosis. J Hepatol 38, 164-168.
35. Ryder PV, Vistein R, Gokhale A., Seaman MN, Puthenveedu MA, Faundez V (2013). The WASH complex, an endosomal Arp2/3 activator, interacts with the Hermansky-Pudlak syndrome complex BLOC-1 and its cargo phosphatidylinositol-4-kinase type IIα. Mol Biol Cell 24, 2269-2284.
36. Schou KB, Andersen JS, Pedersen LB (2014). A divergent calponin homol-ogy (NN-CH) domain defines a novel family: implications for evolution of ciliary IFT complex B proteins. Bioinformatics 30, 899-902.
37. Seaman MN, McCaffery JM, Emr SD (1998). A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol 142, 665-681.
38. Shim H, Harris ZL (2003). Genetic defects in copper metabolism. J Nutr 133, 1527S-1531S.
39. Spee B, Arends B, van Wees AM, Bode P, Penning LC, Rothuizen J (2007). Functional consequences of RNA interference targeting COMMD1 in a canine hepatic cell line in relation to copper toxicosis. Anim Genet 38, 168-170.
40. Starokadomskyy P, Gluck N, Li H., Chen B, Wallis M, Maine G.N., Mao X., Zaidi IW, Hein MY, McDonald FJ, et al. (2013). CCDC22 deficiency in humans blunts activation of proinflammatory NF-kB signaling. J Clin Invest 123, 2244-2256.
41. Steinberg F, Gallon M, Winfeld M., Thomas EC, Bell AJ, Heesom KJ, Tavare J.M., Cullen PJ (2013). A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat Cell Biol 15, 461-471.
42. Stuehler B, Reichert J, Stremmel W., Schaefer M (2004). Analysis of the human homologue of the canine copper toxicosis gene MURR1 in Wilson disease patients. J Mol Med 82, 629-634.
43. Su LC, Ravanshad S, Owen CA Jr, McCall JT, Zollman PE, Hardy RM (1982). A comparison of copper-loading disease in Bedlington terriers and Wilson's disease in humans. Am J Physiol 243, G226-G230.
44. Tao TY, Liu F, Klomp L., Wijmenga C, Gitlin JD (2003). The copper toxicosis gene product Murr1 directly interacts with the Wilson disease protein. J Biol Chem 278, 41593-41596.
45. van de Sluis B, Mao X, Zhai Y, Groot AJ, Vermeulen J F, van der Wall E, van Diest PJ, Hofker MH, Wijmenga C, Klomp LW, et al. (2010). COMMD1 disrupts HIF-1a/b dimerization and inhibits human tumor cell invasion. J Clin Invest 120, 2119-2130.
46. van de Sluis B, Muller P, Duran K, Chen A, Groot AJ, Klomp LW, Liu P P, 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.
47. van de Sluis B, Rothuizen J, Pearson PL, van Oost BA, Wijmenga C (2002). Identification of a new copper metabolism gene by positional cloning in a purebred dog population. Hum Mol Genet 11, 165-173.
48. Voineagu I, Huang L, Winden K., Lazaro M, Haan E, Nelson J., McGaughran J, Nguyen LS, Friend K, Hackett A, et al. (2012). CCDC22: a novel candidate gene for syndromic X-linked intellectual disability. Mol Psychiatry 17, 4-7.
49. Vonk WI, Bartuzi P, de Bie P, Kloosterhuis N, Wichers C.G., Berger R., Haywood S, Klomp LW, Wijmenga C, van de Sluis B (2011). Liver-specific Commd1 knockout mice are susceptible to hepatic copper accumulation. PLoS One 6, e29183.
50. Wang Y, Hodgkinson V, Zhu S., Weisman GA, Petris MJ (2011). Advances in the understanding of mammalian copper transporters. Adv Nutr 2, 129-137.
51. Weiss KH, Lozoya JC, Tuma S, Gotthardt D., Reichert J, Ehehalt R, Stremmel W., Fullekrug J (2008). Copper-induced translocation of the Wilson disease protein ATP7B independent of Murr1/ COMMD1 and Rab7. Am J Pathol 173, 1783-1794.
52. Yi L, Kaler S (2014). ATP7A trafficking and mechanisms underlying the distal motor neuropathy induced by mutations in ATP7A. Ann NY Acad Sci 1314, 49-54.
53. Zech T, Calaminus SD, Caswell P, Spence H.J., Carnell M., Insall RH, Norman J, Machesky LM (2011). The Arp2/3 activator WASH regulates a5b1-integrin-mediated invasive migration. J Cell Sci 124, 3753-3759.