Copper Directs ATP7B to the apical domain of hepatic cells via basolateral endosomes

Traffic

Volumn 15, Issue 12, 2014, Pages 1344-1365

  Nyasae, Lydia K ^a   Schell, Michael J ^a   Hubbard, Ann L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bafliomycin A1; Bile canaliculus; Endosomes; Hepatocytes; Polarity; Proton ATPase; Retromer; Wilson's disease

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE (COPPER); BAFILOMYCIN A1; COPPER; UNCLASSIFIED DRUG; ATP7B PROTEIN, RAT; CATION TRANSPORT PROTEIN; MACROLIDE;

ACIDIFICATION; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; IN VIVO STUDY; LIVER CELL; NONHUMAN; RAT; TRANS GOLGI NETWORK; ANIMAL; DRUG EFFECTS; METABOLISM; PROTEIN TRANSPORT; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE, TUMOR; COPPER; ENDOSOMES; HEPATOCYTES; MACROLIDES; PROTEIN TRANSPORT; RATS; TRANS-GOLGI NETWORK;

EID: 84911448442     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12229     Document Type: Article

References (46)

1. Scheiber I, Dringen R, Mercer JF. Copper: effects of deficiency and overload. Met Ions Life Sci 2013;13:359-387.
2. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY. Function and regulation of human copper-transporting ATPases. Physiol Rev 2007;87:1011-1046.
3. Gupta A, Lutsenko S. Human copper transporters: mechanism, role in human diseases and therapeutic potential. Future Med Chem 2009;1:1125-1142.
4. Schaefer M, Hopkins RG, Failla ML, Gitlin JD. Hepatocyte-specific localization and copper-dependent trafficking of the Wilson's disease protein in the liver. Am J Physiol 1999;276:G639-G646.
5. Braiterman LT, Murthy A, Jayakanthan S, Nyasae L, Tzeng E, Gromadzka G, Woolf TB, Lutsenko S, Hubbard AL. Distinct phenotype of a Wilson disease mutation reveals a novel trafficking determinant in the copper transporter ATP7B. Proc Natl Acad Sci USA 2014;111:E1364-E1373.
6. Demaurex N. pH homeostasis of cellular organelles. News Physiol Sci 2002;17:1-5.
7. Beyenbach KW, Wieczorek H. The V-type H+ATPase: molecular structure and function, physiological roles and regulation. J Exp Biol 2006;209:577-589.
8. Drose S, Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 1997;200:1-8.
9. Clague MJ, Urbe S, Aniento F, Gruenberg J. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J Biol Chem 1994;269:21-24.
10. van Weert AW, Dunn KW, Geuze HJ, Maxfield FR, Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 1995;130:821-834.
11. Harada M, Sakisaka S, Yoshitake M, Kin M, Ohishi M, Shakado S, Mimura Y, Noguchi K, Sata M, Tanikawa K. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPases, inhibits the receptor-mediated endocytosis of asialoglycoproteins in isolated rat hepatocytes. J Hepatol 1996;24:594-603.
12. Presley JF, Mayor S, McGraw TE, Dunn KW, Maxfield FR. Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J Biol Chem 1997;272:13929-13936.
13. 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.
14. 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.
15. Weiss KH, Lozoya JC, Tuma S, Gotthardt D, Reichert J, Ehehalt R, Stremmel W, Fullekrug J. Copper-induced translocation of the Wilson disease protein ATP7B independent of Murr1/COMMD1 and Rab7. Am J Pathol 2008;173:1783-1794.
16. Lalioti V, Hernandez-Tiedra S, Sandoval IV. DKWSLLL, a versatile DXXXLL-type signal with distinct roles in the Cu-regulated trafficking of ATP7B. Traffic 2014;15:839-860.
17. Polishchuk EV, Concilli M, Iacobacci S, Chesi G, Pastore N, Piccolo P, Paladino S, Baldantoni D, van ISC, Chan J, Chang CJ, Amoresano A, Pane F, Pucci P, Tarallo A, et al. Wilson disease protein ATP7B utilizes lysosomal exocytosis to maintain copper homeostasis. Dev Cell 2014;29:686-700.
18. Harada M, Kawaguchi T, Kumemura H, Terada K, Ninomiya H, Taniguchi E, Hanada S, Baba S, Maeyama M, Koga H, Ueno T, Furuta K, Suganuma T, Sugiyama T, Sata M. The Wilson disease protein ATP7B resides in the late endosomes with Rab7 and the Niemann-Pick C1 protein. Am J Pathol 2005;166:499-510.
19. 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.
20. McMillin GA, Travis JJ, Hunt JW. Direct measurement of free copper in serum or plasma ultrafiltrate. Am J Clin Pathol 2009;131:160-165.
21. Tuma PL, Nyasae LK, Backer JM, Hubbard AL. Vps34p differentially regulates endocytosis from the apical and basolateral domains in polarized hepatic cells. J Cell Biol 2001;154:1197-1208.
22. Ihrke G, Martin GV, Shanks MR, Schrader M, Schroer TA, Hubbard AL. Apical plasma membrane proteins and endolyn-78 travel through a subapical compartment in polarized WIF-B hepatocytes. J Cell Biol 1998;141:115-133.
23. Marshansky V, Futai M. The V-type H+-ATPase in vesicular trafficking: targeting, regulation and function. Curr Opin Cell Biol 2008;20:415-426.
24. Sobota JA, Back N, Eipper BA, Mains RE. Inhibitors of the V0 subunit of the vacuolar H+-ATPase prevent segregation of lysosomal- and secretory-pathway proteins. J Cell Sci 2009;122:3542-3553.
25. Xie Z, Xie Y, Xu Y, Zhou H, Xu W, Dong Q. Bafilomycin A1 inhibits autophagy and induces apoptosis in MG63 osteosarcoma cells. Mol Med Rep 2014;10:1103-1107.
26. Li M, Khambu B, Zhang H, Kang JH, Chen X, Chen D, Vollmer L, Liu PQ, Vogt A, Yin XM. Suppression of lysosome function induces autophagy via a feedback down-regulation of MTOR complex 1 (MTORC1) activity. J Biol Chem 2013;288:35769-35780.
27. Payne AS, Kelly EJ, Gitlin JD. Functional expression of the Wilson disease protein reveals mislocalization and impaired copper-dependent trafficking of the common H1069Q mutation. Proc Natl Acad Sci USA 1998;95:10854-10859.
28. Hanada H, Moriyama Y, Maeda M, Futai M. Kinetic studies of chromaffin granule H+-ATPase and effects of bafilomycin A1. Biochem Biophys Res Commun 1990;170:873-878.
29. Petris MJ, Mercer JF, Culvenor JG, Lockhart P, Gleeson PA, Camakaris J. Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. EMBO J 1996;15:6084-6095.
30. 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.
31. Harada M, Sakisaka S, Terada K, Kimura R, Kawaguchi T, Koga H, Kim M, Taniguchi E, Hanada S, Suganuma T, Furuta K, Sugiyama T, Sata M. A mutation of the Wilson disease protein, ATP7B, is degraded in the proteasomes and forms protein aggregates. Gastroenterology 2001;120:967-974.
32. 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.
33. Gross JB Jr, Myers BM, Kost LJ, Kuntz SM, LaRusso NF. Biliary copper excretion by hepatocyte lysosomes in the rat. Major excretory pathway in experimental copper overload. J Clin Invest 1989;83:30-39.
34. Harada M, Sakisaka S, Yoshitake M, Shakadoh S, Gondoh K, Sata M, Tanikawa K. Biliary copper excretion in acutely and chronically copper-loaded rats. Hepatology 1993;17:111-117.
35. Camacho M, Machado JD, Montesinos MS, Criado M, Borges R. Intragranular pH rapidly modulates exocytosis in adrenal chromaffin cells. J Neurochem 2006;96:324-334.
36. Bartles JR, Feracci HM, Stieger B, Hubbard AL. Biogenesis of the rat hepatocyte plasma membrane in vivo: comparison of the pathways taken by apical and basolateral proteins using subcellular fractionation. J Cell Biol 1987;105:1241-1251.
37. Cullen PJ, Korswagen HC. Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 2012;14:29-37.
38. Steinberg F, Gallon M, Winfield M, Thomas EC, Bell AJ, Heesom KJ, Tavare JM, Cullen PJ. A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat Cell Biol 2013;15:461-471.
39. Ueno K, Saito M, Nagashima M, Kojima A, Nishinoaki S, Toshima JY, Toshima J. V-ATPase-dependent luminal acidification is required for endocytic recycling of a yeast cell wall stress sensor, Wsc1p. Biochem Biophys Res Commun 2014;443:549-555.
40. Kojima A, Toshima JY, Kanno C, Kawata C, Toshima J. Localization and functional requirement of yeast Na+/H+ exchanger, Nhx1p, in the endocytic and protein recycling pathway. Biochim Biophys Acta 2012;1823:534-543.
41. Barr VA, Hubbard AL. Newly synthesized hepatocyte plasma membrane proteins are transported in transcytotic vesicles in the bile duct-ligated rat. Gastroenterology 1993;105:554-571.
42. Cassio D, Hamon-Benais C, Guerin M, Lecoq O. Hybrid cell lines constitute a potential reservoir of polarized cells: isolation and study of highly differentiated hepatoma-derived hybrid cells able to form functional bile canaliculi in vitro. J Cell Biol 1991;115:1397-1408.
43. Nyasae L, Bustos R, Braiterman L, Eipper B, Hubbard A. Dynamics of endogenous ATP7A (Menkes protein) in intestinal epithelial cells: copper-dependent redistribution between two intracellular sites. Am J Physiol Gastrointest Liver Physiol 2007;292:G1181-G1194.
44. Zack GW, Rogers WE, Latt SA. Automatic measurement of sister chromatid exchange frequency. J Histochem Cytochem 1977;25:741-753.
45. Doube M, Klosowski MM, Arganda-Carreras I, Cordelieres FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ. BoneJ: free and extensible bone image analysis in ImageJ. Bone 2010;47:1076-1079.
46. Anderson RG, Falck JR, Goldstein JL, Brown MS. Visualization of acidic organelles in intact cells by electron microscopy. Proc Natl Acad Sci USA 1984;81:4838-4842.