DKWSLLL, a Versatile DXXXLL-Type Signal with Distinct Roles in the Cu+-Regulated Trafficking of ATP7B

Traffic

Volumn 15, Issue 8, 2014, Pages 839-860

  Lalioti, Vasiliki ^a   Hernandez Tiedra, Sonia ^a   Sandoval, Ignacio V ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

(DE)XXXLL type signals; ATP7B; Endocytosis; Endosomes; Golgi; PM; Traffic

Indexed keywords

COPPER; GLUCOSE TRANSPORTER 4; MENKES PROTEIN; WILSON DISEASE PROTEIN; ADENOSINE TRIPHOSPHATASE; ATP7A PROTEIN, MOUSE; CATION TRANSPORT PROTEIN; SIGNAL PEPTIDE;

ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; COS 7 CELL LINE; ENDOCYTOSIS; ENDOSOME; HEPG2 CELL LINE; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; INTRACELLULAR TRANSPORT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANS GOLGI NETWORK; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENETICS; HUMAN; METABOLISM; MOUSE; PROTEIN TRANSPORT;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CATION TRANSPORT PROTEINS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COPPER; COS CELLS; HEP G2 CELLS; HUMANS; MICE; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; TRANS-GOLGI NETWORK;

EID: 84904625473     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12176     Document Type: Article

References (37)

1. Bull PC, Thomas GR, Rommens JM, Forbes JR, Cox DW. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet 1993;5:327-337.
2. Tanzi RE, Petrukhin K, Chernov I, Pellequer JL, Wasco W, Ross B, Romano DM, Parano E, Pavone L, Brzustowicz LM, Devoto M, Peppercorn J, Bush AI, Sternlieb I, Pirastu M, et al. The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nat Genet 1993;5:344-350.
3. Roelofsen H, Wolters H, Van Luyn MJ, Miura N, Kuipers F, Vonk RJ. Copper-induced apical trafficking of ATP7B in polarized hepatoma cells provides a mechanism for biliary copper excretion. Gastroenterology 2000;119:782-793.
4. Hernandez S, Tsuchiya Y, Garcia-Ruiz JP, Lalioti V, Nielsen S, Cassio D, Sandoval IV. ATP7B copper-regulated traffic and association with the tight junctions: copper excretion into the bile. Gastroenterology 2008;134:1215-1223.
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. Am J Physiol Gastrointest Liver Physiol 2009;296:G433-G444.
6. Cater MA, La Fontaine S, Shield K, Deal Y, Mercer JF. ATP7B mediates vesicular sequestration of copper: insight into biliary copper excretion. Gastroenterology 2006;130:493-506.
7. Guo Y, Nyasae L, Braiterman LT, Hubbard AL. NH2-terminal signals in ATP7B Cu-ATPase mediate its Cu-dependent anterograde traffic in polarized hepatic cells. Am J Physiol Gastrointest Liver Physiol 2005;289:G904-G916.
8. Huster D, Hoppert M, Lutsenko S, Zinke J, Lehmann C, Mossner J, Berr F, Caca K. Defective cellular localization of mutant ATP7B in Wilson's disease patients and hepatoma cell lines. Gastroenterology 2003;124:335-345.
9. van den Berghe PV, Stapelbroek JM, Krieger E, de Bie P, van de Graaf SF, de Groot RE, van Beurden E, Spijker E, Houwen RH, Berger R, Klomp LW. Reduced expression of ATP7B affected by Wilson disease-causing mutations is rescued by pharmacological folding chaperones 4-phenylbutyrate and curcumin. Hepatology 2009;50:1783-1795.
10. Singleton WC, McInnes KT, Cater MA, Winnall WR, McKirdy R, Yu Y, Taylor PE, Ke BX, Richardson DR, Mercer JF, La Fontaine S. Role of glutaredoxin1 and glutathione in regulating the activity of the copper-transporting P-type ATPases, ATP7A and ATP7B. J Biol Chem 2010;285:27111-27121.
11. Pilankatta R, Lewis D, Inesi G. Involvement of protein kinase D in expression and trafficking of ATP7B (copper ATPase). J Biol Chem 2011;286:7389-7396.
12. Vanderwerf SM, Cooper MJ, Stetsenko IV, Lutsenko S. Copper specifically regulates intracellular phosphorylation of the Wilson's disease protein, a human copper-transporting ATPase. J Biol Chem 2001;276:36289-36294.
13. Hasan NM, Gupta A, Polishchuk E, Yu CH, Polishchuk R, Dmitriev OY, Lutsenko S. Molecular events initiating exit of a copper-transporting ATPase ATP7B from the trans-Golgi network. J Biol Chem 2012;287:36041-36050.
14. Lim CM, Cater MA, Mercer JF, La Fontaine S. Copper-dependent interaction of dynactin subunit p62 with the N terminus of ATP7B but not ATP7A. J Biol Chem 2006;281:14006-14014.
15. Cater MA, La Fontaine S, Mercer JF. 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). Biochem J 2007;401:143-153.
16. Braiterman L, Nyasae L, Leves F, Hubbard AL. Critical roles for the COOH terminus of the Cu-ATPase ATP7B in protein stability, trans-Golgi network retention, copper sensing, and retrograde trafficking. Am J Physiol Gastrointest Liver Physiol 2011;301:G69-G81.
17. Holloway ZG, Velayos-Baeza A, Howell GJ, Levecque C, Ponnambalam S, Sztul E, Monaco AP. Trafficking of the Menkes copper transporter ATP7A is regulated by clathrin-, AP-2-, AP-1-, and Rab22-dependent steps. Mol Biol Cell 2013;24:1735-1748, S1731-S1738.
18. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003;72:395-447.
19. Sandoval IV, Bakke O. Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol 1994;4:292-297.
20. Prasad R, Kaur G, Kumar S, Ram Thapa B. Two novel mutations (2976INSA, 4311insA) of ATP7B in a patient with Wilson's disease coexisting with glucose-6-phosphate dehydrogenase deficiency. J Gastroenterol Hepatol 2005;20:660-662.
21. Lepori MB, Lovicu M, Dessi V, Zappu A, Incollu S, Zancan L, Giacchino R, Iorio R, Vajro P, Maggiore G, Marcellini M, Barbera C, Pellecchia MT, Simonetti R, Kostic V, et al. Twenty-four novel mutations in Wilson disease patients of predominantly Italian origin. Genet Test 2007;11:328-332.
22. Loudianos G, Dessi V, Lovicu M, Angius A, Kanavakis E, Tzetis M, Kattamis C, Manolaki N, Vassiliki G, Karpathios T, Cao A, Pirastu M. Haplotype and mutation analysis in Greek patients with Wilson disease. Eur J Hum Genet 1998;6:487-491.
23. Loudianos G, Lovicu M, Solinas P, Kanavakis E, Tzetis M, Manolaki N, Panagiotakaki E, Karpathios T, Cao A. Delineation of the spectrum of Wilson disease mutations in the Greek population and the identification of six novel mutations. Genet Test 2000;4:399-402.
24. Butler P, McIntyre N, Mistry PK. Molecular diagnosis of Wilson disease. Mol Genet Metab 2001;72:223-230.
25. Greenough M, Pase L, Voskoboinik I, Petris MJ, O'Brien AW, Camakaris J. Signals regulating trafficking of Menkes (MNK; ATP7A) copper-translocating P-type ATPase in polarized MDCK cells. Am J Physiol Cell Physiol 2004;287:C1463-C1471.
26. Pilankatta R, Lewis D, Adams CM, 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. J Biol Chem 2009;284:21307-21316.
27. Sandoval IV, Arredondo JJ, Alcalde J, Gonzalez Noriega A, Vandekerckhove J, Jimenez MA, Rico M. The residues Leu(Ile)475-Ile(Leu, Val, Ala)476, contained in the extended carboxyl cytoplasmic tail, are critical for targeting of the resident lysosomal membrane protein LIMP II to lysosomes. J Biol Chem 1994;269:6622-6631.
28. Sandoval IV, Martinez-Arca S, Valdueza J, Palacios S, Holman GD. Distinct reading of different structural determinants modulates the dileucine-mediated transport steps of the lysosomal membrane protein LIMPII and the insulin-sensitive glucose transporter GLUT4. J Biol Chem 2000;275:39874-39885.
29. Martinez-Arca S, Lalioti VS, Sandoval IV. Intracellular targeting and retention of the glucose transporter GLUT4 by the perinuclear storage compartment involves distinct carboxyl-tail motifs. J Cell Sci 2000;113(Pt 10):1705-1715.
30. James DE, Brown R, Navarro J, Pilch PF. Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature 1988;333:183-185.
31. Gonzalez A, Rodriguez-Boulan E. Clathrin and AP1B: key roles in basolateral trafficking through trans-endosomal routes. FEBS Lett 2009;583:3784-3795.
32. Mattila PE, Kinlough CL, Bruns JR, Weisz OA, Hughey RP. MUC1 traverses apical recycling endosomes along the biosynthetic pathway in polarized MDCK cells. Biol Chem 2009;390:551-556.
33. Wan L, Molloy SS, Thomas L, Liu G, Xiang Y, Rybak SL, Thomas G. PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 1998;94:205-216.
34. Crump CM, Xiang Y, Thomas L, Gu F, Austin C, Tooze SA, Thomas G. PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J 2001;20:2191-2201.
35. Forbes JR, Cox DW. Copper-dependent trafficking of Wilson disease mutant ATP7B proteins. Hum Mol Genet 2000;9:1927-1935.
36. Huster D, Hoppert M, Lutsenko S, Zinke J, Lehmann C, Mossner J, Berr F, Caca K. Defective cellular localization of mutant ATP7B in Wilson's disease patients and hepatoma cell lines. Gastroenterology 2003;124:335-345.
37. Frost SC, Lane MD. Evidence for the involvement of vicinal sulfhydryl groups in insulin-activated hexose transport by 3T3-L1 adipocytes. J Biol Chem 1985;260:2646-2652.