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Review

Role of the epithelial cell-specific clathrin adaptor complex AP-1B in cell polarity

Article: e1074331 | Received 27 May 2015, Accepted 09 Jul 2015, Published online: 11 Sep 2015

References

  • Weisz OA, Rodriguez-Boulan E. Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci 2009; 122:4253-66; PMID:19923269; http://dx.doi.org/10.1242/jcs.032615
  • Fölsch H. Regulation of membrane trafficking in polarized epithelial cells. Curr Opin Cell Biol 2008; 20:208-13; PMID:18282697; http://dx.doi.org/10.1016/j.ceb.2008.01.003
  • Rodriguez-Boulan E, Kreitzer G, Musch A. Organization of vesicular trafficking in epithelia. Nat Rev 2005; 6:233-47; PMID:15738988; http://dx.doi.org/10.1038/nrm1593
  • Bomsel M, Parton R, Kuznetsov SA, Schroer TA, Gruenberg J. Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell 1990; 62:719-31; PMID:2143699; http://dx.doi.org/10.1016/0092-8674(90)90117-W
  • Sheff DR, Kroschewski R, Mellman I. Actin dependence of polarized receptor recycling in Madin-Darby canine kidney cell endosomes. Mol Biol Cell 2002; 13:262-75; PMID:11809838; http://dx.doi.org/10.1091/mbc.01-07-0320
  • Ang AL, Taguchi T, Francis S, Fölsch H, Murrells LJ, Pypaert M, Warren G, Mellman I. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol 2004; 167:531-43; PMID:15534004; http://dx.doi.org/10.1083/jcb.200408165
  • Fölsch H, Mattila PE, Weisz OA. Taking the scenic route: biosynthetic traffic to the plasma membrane in polarized epithelial cells. Traffic (Copenhagen, Denmark) 2009; 10:972-81; PMID:19453969; http://dx.doi.org/10.1111/j.1600-0854.2009.00927.x
  • Ang SF, Fölsch H. The role of secretory and endocytic pathways in the maintenance of cell polarity. Essays Biochem 2012; 53:29-39; PMID:22928506; http://dx.doi.org/10.1042/bse0530029
  • Mostov K, Su T, ter Beest M. Polarized epithelial membrane traffic: conservation and plasticity. Nat Cell Biol 2003; 5:287-93; PMID:12669082; http://dx.doi.org/10.1038/ncb0403-287
  • Boehm M, Bonifacino JS. Adaptins: the final recount. Mol Biol Cell 2001; 12:2907-20; PMID:11598180; http://dx.doi.org/10.1091/mbc.12.10.2907
  • Hirst J, Robinson MS. Clathrin and adaptors. Biochim Biophys Acta 1998; 1404:173-93; PMID:9714795; http://dx.doi.org/10.1016/S0167-4889(98)00056-1
  • Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 2001; 17:517-68; PMID:11687498; http://dx.doi.org/10.1146/annurev.cellbio.17.1.517
  • Nakatsu F, Ohno H. Adaptor protein complexes as the key regulators of protein sorting in the post-Golgi network. Cell Struct Funct 2003; 28:419-29; PMID:14745134; http://dx.doi.org/10.1247/csf.28.419
  • Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino JS. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Sci (New York, N.Y) 1995; 269:1872-5; PMID:7569928; http://dx.doi.org/10.1126/science.7569928
  • Owen DJ, Evans PR. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science (New York, N.Y) 1998; 282:1327-32; PMID:9812899; http://dx.doi.org/10.1126/science.282.5392.1327
  • Janvier K, Kato Y, Boehm M, Rose JR, Martina JA, Kim BY, Venkatesan S, Bonifacino JS. Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 gamma-sigma1 and AP-3 delta-sigma3 hemicomplexes. J Cell Biol 2003; 163:1281-90; PMID:14691137; http://dx.doi.org/10.1083/jcb.200307157
  • Mattera R, Boehm M, Chaudhuri R, Prabhu Y, Bonifacino JS. Conservation and diversification of dileucine signal recognition by adaptor protein (AP) complex variants. J Biol Chem 2011; 286:2022-30; PMID:21097499; http://dx.doi.org/10.1074/jbc.M110.197178
  • Doray B, Lee I, Knisely J, Bu G, Kornfeld S. The gamma/sigma1 and alpha/sigma2 hemicomplexes of clathrin adaptors AP-1 and AP-2 harbor the dileucine recognition site. Mol Biol Cell 2007; 18:1887-96; PMID:17360967; http://dx.doi.org/10.1091/mbc.E07-01-0012
  • de la Fuente-Ortega E, Gravotta D, Perez Bay A, Benedicto I, Carvajal-Gonzalez JM, Lehmann GL, Lagos CF, Rodríguez-Boulan E. Basolateral sorting of chloride channel 2 is mediated by interactions between a dileucine motif and the clathrin adaptor AP-1. Mol Biol Cell 2015; 26:1728-42; PMID:25739457; http://dx.doi.org/10.1091/mbc.E15-01-0047
  • Traub LM. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J Cell Biol 2003; 163:203-8; PMID:14581447; http://dx.doi.org/10.1083/jcb.200309175
  • Mishra SK, Keyel PA, Edeling MA, Dupin AL, Owen DJ, Traub LM. Functional dissection of an AP-2 beta2 appendage-binding sequence within the autosomal recessive hypercholesterolemia protein. J Biol Chem 2005; 280:19270-80; PMID:15728179; http://dx.doi.org/10.1074/jbc.M501029200
  • Kang RS, Fölsch H. ARH cooperates with AP-1B in the exocytosis of LDLR in polarized epithelial cells. J Cell Biol 2011; 193:51-60; PMID:21444685; http://dx.doi.org/10.1083/jcb.201012121
  • Fölsch H, Ohno H, Bonifacino JS, Mellman I. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 1999; 99:189-98; PMID:10535737; http://dx.doi.org/10.1016/S0092-8674(00)81650-5
  • Gravotta D, Carvajal-Gonzalez JM, Mattera R, Deborde S, Banfelder JR, Bonifacino JS, Rodriguez-Boulan E. The clathrin adaptor AP-1A mediates basolateral polarity. Dev Cell 2012; 22:811-23; PMID:22516199; http://dx.doi.org/10.1016/j.devcel.2012.02.004
  • Simmen T, Honing S, Icking A, Tikkanen R, Hunziker W. AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells. Nat Cell Biol 2002; 4:154-9; PMID:11802162; http://dx.doi.org/10.1038/ncb745
  • Burgos PV, Mardones GA, Rojas AL, daSilva LL, Prabhu Y, Hurley JH, Bonifacino JS. Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev Cell 2010; 18:425-36; PMID:20230749; http://dx.doi.org/10.1016/j.devcel.2010.01.015
  • Haass C, Koo EH, Teplow DB, Selkoe DJ. Polarized secretion of beta-amyloid precursor protein and amyloid beta-peptide in MDCK cells. Proc Natl Acad Sci U S A 1994; 91:1564-8; PMID:8108445; http://dx.doi.org/10.1073/pnas.91.4.1564
  • De Strooper B, Craessaerts K, Dewachter I, Moechars D, Greenberg B, Van Leuven F, Van den Berghe H. Basolateral secretion of amyloid precursor protein in Madin-Darby canine kidney cells is disturbed by alterations of intracellular pH and by introducing a mutation associated with familial Alzheimer's disease. J Biol Chem 1995; 270:4058-65; PMID:7876155; http://dx.doi.org/10.1074/jbc.270.51.30310
  • Meyer C, Zizioli D, Lausmann S, Eskelinen EL, Hamann J, Saftig P, von Figura K, Schu P. µ1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J 2000; 19:2193-203; PMID:10811610; http://dx.doi.org/10.1093/emboj/19.10.2193
  • Fölsch H, Pypaert M, Maday S, Pelletier L, Mellman I. The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains. J Cell Biol 2003; 163:351-62; PMID:14581457; http://dx.doi.org/10.1083/jcb.200309020
  • Gan Y, McGraw TE, Rodriguez-Boulan E. The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nat Cell Biol 2002; 4:605-9; PMID:12105417
  • Traub LM, Apodaca G. AP-1B: polarized sorting at the endosome. Nat Cell Biol 2003; 5:1045-7; PMID:14647300; http://dx.doi.org/10.1038/ncb1203-1045
  • Meyer C, Eskelinen EL, Guruprasad MR, von Figura K, Schu P. Mu 1A deficiency induces a profound increase in MPR300/IGF-II receptor internalization rate. J Cell Sci 2001; 114:4469-76; PMID:11792812
  • Fölsch H, Pypaert M, Schu P, Mellman I. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J Cell Biol 2001; 152:595-606; PMID:11157985; http://dx.doi.org/10.1083/jcb.152.3.595
  • Distel B, Bauer U, Le Borgne R, Hoflack B. Basolateral sorting of the cation-dependent mannose 6-phosphate receptor in Madin-Darby canine kidney cells. Identification of a basolateral determinant unrelated to clathrin-coated pit localization signals. J Biol Chem 1998; 273:186-93; PMID:9417063; http://dx.doi.org/10.1074/jbc.273.1.186
  • Nabi IR, Le Bivic A, Fambrough D, Rodriguez-Boulan E. An endogenous MDCK lysosomal membrane glycoprotein is targeted basolaterally before delivery to lysosomes. J Cell Biol 1991; 115:1573-84; PMID:1757463; http://dx.doi.org/10.1083/jcb.115.6.1573
  • Hunziker W, Harter C, Matter K, Mellman I. Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell 1991; 66:907-20; PMID:1909606; http://dx.doi.org/10.1016/0092-8674(91)90437-4
  • Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC, Collins BM, Höning S, Evans PR, Owen DJ. A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 2010; 141:1220-9; PMID:20603002; http://dx.doi.org/10.1016/j.cell.2010.05.006
  • Thomas DC, Brewer CB, Roth MG. Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine. J Biol Chem 1993; 268:3313-20; PMID:8381425
  • Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ. Molecular architecture and functional model of the endocytic AP2 complex. Cell 2002; 109:523-35; PMID:12086608; http://dx.doi.org/10.1016/S0092-8674(02)00735-3
  • Kirchhausen T. Clathrin adaptors really adapt. Cell 2002; 109:413-6; PMID:12086597; http://dx.doi.org/10.1016/S0092-8674(02)00751-1
  • Canagarajah BJ, Ren X, Bonifacino JS, Hurley JH. The clathrin adaptor complexes as a paradigm for membrane-associated allostery. Protein Sci: Pub Protein Soc 2013; 22:517-29; PMID:23424177; http://dx.doi.org/10.1002/pro.2235
  • Ren X, Farias GG, Canagarajah BJ, Bonifacino JS, Hurley JH. Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1. Cell 2013; 152:755-67; PMID:23415225; http://dx.doi.org/10.1016/j.cell.2012.12.042
  • Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 2003; 114:299-310; PMID:12914695; http://dx.doi.org/10.1016/S0092-8674(03)00603-2
  • Heldwein EE, Macia E, Wang J, Yin HL, Kirchhausen T, Harrison SC. Crystal structure of the clathrin adaptor protein 1 core. Proc Natl Acad Sci U S A 2004; 101:14108-13; PMID:15377783; http://dx.doi.org/10.1073/pnas.0406102101
  • Krauss M, Kinuta M, Wenk MR, De Camilli P, Takei K, Haucke V. ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J Cell Biol 2003; 162:113-24; PMID:12847086; http://dx.doi.org/10.1083/jcb.200301006
  • Fields IC, King SM, Shteyn E, Kang RS, Fölsch H. Phosphatidylinositol 3,4,5-trisphosphate localization in recycling endosomes is necessary for AP-1B-dependent sorting in polarized epithelial cells. Mol Biol Cell 2010; 21:95-105; PMID:19864464; http://dx.doi.org/10.1091/mbc.E09-01-0036
  • Shteyn E, Pigati L, Fölsch H. Arf6 regulates AP-1B-dependent sorting in polarized epithelial cells. J Cell Biol 2011; 194:873-87; PMID:21911479; http://dx.doi.org/10.1083/jcb.201106010
  • Pasqualato S, Menetrey J, Franco M, Cherfils J. The structural GDP/GTP cycle of human Arf6. EMBO Rep 2001; 2:234-8; PMID:11266366; http://dx.doi.org/10.1093/embo-reports/kve043
  • Guo X, Mattera R, Ren X, Chen Y, Retamal C, González A, Bonifacino JS. The adaptor protein-1 mu1B subunit expands the repertoire of basolateral sorting signal recognition in epithelial cells. Dev Cell 2013; 27:353-66; PMID:24229647; http://dx.doi.org/10.1016/j.devcel.2013.10.006
  • Eskelinen EL, Meyer C, Ohno H, von Figura K, Schu P. The polarized epithelia-specific mu 1B-adaptin complements mu 1A-deficiency in fibroblasts. EMBO Rep 2002; 3:471-7; PMID:11964383; http://dx.doi.org/10.1093/embo-reports/kvf092
  • Shiba Y, Takatsu H, Shin HW, Nakayama K. Gamma-adaptin interacts directly with Rabaptin-5 through its ear domain. J Biochem 2002; 131:327-36; PMID:11872161; http://dx.doi.org/10.1093/oxfordjournals.jbchem.a003107
  • Deborde S, Perret E, Gravotta D, Deora A, Salvarezza S, Schreiner R, Rodriguez-Boulan E. Clathrin is a key regulator of basolateral polarity. Nature 2008; 452:719-23; PMID:18401403; http://dx.doi.org/10.1038/nature06828
  • Fields IC, Shteyn E, Pypaert M, Proux-Gillardeaux V, Kang RS, Galli T, Fölsch H. v-SNARE cellubrevin is required for basolateral sorting of AP-1B-dependent cargo in polarized epithelial cells. J Cell Biol 2007; 177:477-88; PMID:17485489; http://dx.doi.org/10.1083/jcb.200610047
  • Au JS, Puri C, Ihrke G, Kendrick-Jones J, Buss F. Myosin VI is required for sorting of AP-1B-dependent cargo to the basolateral domain in polarized MDCK cells. J Cell Biol 2007; 177:103-14; PMID:17403927; http://dx.doi.org/10.1083/jcb.200608126
  • Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, Scheller RH, Nelson WJ. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 1998; 93:731-40; PMID:9630218; http://dx.doi.org/10.1016/S0092-8674(00)81435-X
  • Reales E, Sharma N, Low SH, Fölsch H, Weimbs T. Basolateral sorting of syntaxin 4 is dependent on its N-terminal domain and the AP1B clathrin adaptor, and required for the epithelial cell polarity. PloS One 2011; 6:e21181; PMID:21698262; http://dx.doi.org/10.1371/journal.pone.0021181
  • Fukai S, Matern HT, Jagath JR, Scheller RH, Brunger AT. Structural basis of the interaction between RalA and Sec5, a subunit of the sec6/8 complex. EMBO J 2003; 22:3267-78; PMID:12839989; http://dx.doi.org/10.1093/emboj/cdg329
  • Mott HR, Nietlispach D, Hopkins LJ, Mirey G, Camonis JH, Owen D. Structure of the GTPase-binding domain of Sec5 and elucidation of its Ral binding site. J Biol Chem 2003; 278:17053-9; PMID:12624092; http://dx.doi.org/10.1074/jbc.M300155200
  • Jin R, Junutula JR, Matern HT, Ervin KE, Scheller RH, Brunger AT. Exo84 and Sec5 are competitive regulatory Sec6/8 effectors to the RalA GTPase. EMBO J 2005; 24:2064-74; PMID:15920473; http://dx.doi.org/10.1038/sj.emboj.7600699
  • Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, White MA. The exocyst is a Ral effector complex. Nat Cell Biol 2002; 4:66-72; PMID:11740492; http://dx.doi.org/10.1038/ncb728
  • Moskalenko S, Tong C, Rosse C, Mirey G, Formstecher E, Daviet L, Camonis J, White MA. Ral GTPases regulate exocyst assembly through dual subunit interactions. J Biol Chem 2003; 278:51743-8; PMID:14525976; http://dx.doi.org/10.1074/jbc.M308702200
  • Ryan S, Verghese S, Cianciola NL, Cotton CU, Carlin CR. Autosomal recessive polycystic kidney disease epithelial cell model reveals multiple basolateral epidermal growth factor receptor sorting pathways. Mol Biol Cell 2010; 21:2732-45; PMID:20519437; http://dx.doi.org/10.1091/mbc.E09-12-1059
  • Ling K, Bairstow SF, Carbonara C, Turbin DA, Huntsman DG, Anderson RA. Type Igamma phosphatidylinositol phosphate kinase modulates adherens junction and E-cadherin trafficking via a direct interaction with micro1B adaptin. J Cell Biol 2007; 176:343-53; PMID:17261850; http://dx.doi.org/10.1083/jcb.200606023
  • Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B. The emerging mechanisms of isoform-specific PtdIns3K signalling. Nat Rev 2010; 11:329-41; PMID:20379207; http://dx.doi.org/10.1038/nrm2882
  • Ang AL, Fölsch H, Koivisto UM, Pypaert M, Mellman I. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J Cell Biol 2003; 163:339-50; PMID:14581456; http://dx.doi.org/10.1083/jcb.200307046
  • Kroschewski R, Hall A, Mellman I. Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells. Nat Cell Biol 1999; 1:8-13; PMID:10559857; http://dx.doi.org/10.1038/8977
  • Cohen D, Musch A, Rodriguez-Boulan E. Selective control of basolateral membrane protein polarity by cdc42. Traffic (Copenhagen, Denmark) 2001; 2:556-64; PMID:11489213; http://dx.doi.org/10.1034/j.1600-0854.2001.20805.x
  • Fullekrug J, Shevchenko A, Shevchenko A, Simons K. Identification of glycosylated marker proteins of epithelial polarity in MDCK cells by homology driven proteomics. BMC Biochem 2006; 7:8; PMID:16533391; http://dx.doi.org/10.1186/1471-2091-7-8
  • Musch A, Cohen D, Kreitzer G, Rodriguez-Boulan E. cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. EMBO J 2001; 20:2171-9; PMID:11331583; http://dx.doi.org/10.1093/emboj/20.9.2171
  • DiNitto JP, Delprato A, Gabe Lee MT, Cronin TC, Huang S, Guilherme A, Czech MP, Lambright DG. Structural basis and mechanism of autoregulation in 3-phosphoinositide-dependent Grp1 family Arf GTPase exchange factors. Mol Cell 2007; 28:569-83; PMID:18042453; http://dx.doi.org/10.1016/j.molcel.2007.09.017
  • Langille SE, Patki V, Klarlund JK, Buxton JM, Holik JJ, Chawla A, Corvera S, Czech MP. ADP-ribosylation factor 6 as a target of guanine nucleotide exchange factor GRP1. J Biol Chem 1999; 274:27099-104; PMID:10480924; http://dx.doi.org/10.1074/jbc.274.38.27099
  • Schuck S, Gerl MJ, Ang A, Manninen A, Keller P, Mellman I, Simons K. Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic (Copenhagen, Denmark) 2007; 8:47-60; PMID:17132146; http://dx.doi.org/10.1111/j.1600-0854.2006.00506.x
  • Nokes RL, Fields IC, Collins RN, Fölsch H. Rab13 regulates membrane trafficking between TGN and recycling endosomes in polarized epithelial cells. J Cell Biol 2008; 182:845-53; PMID:18779367; http://dx.doi.org/10.1083/jcb.200802176
  • Henry L, Sheff DR. Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol Biol Cell 2008; 19:2059-68; PMID:18287531; http://dx.doi.org/10.1091/mbc.E07-09-0902
  • Sato T, Iwano T, Kunii M, Matsuda S, Mizuguchi R, Jung Y, Hagiwara H, Yoshihara Y, Yuzaki M, Harada R, et al. Rab8a and Rab8b are essential for several apical transport pathways but insufficient for ciliogenesis. J Cell Sci 2014; 127:422-31; PMID:24213529; http://dx.doi.org/10.1242/jcs.136903
  • Sato T, Mushiake S, Kato Y, Sato K, Sato M, Takeda N, Ozono K, Miki K, Kubo Y, Tsuji A, et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 2007; 448:366-9; PMID:17597763; http://dx.doi.org/10.1038/nature05929
  • Shi A, Liu O, Koenig S, Banerjee R, Chen CC, Eimer S, Grant BD. RAB-10-GTPase-mediated regulation of endosomal phosphatidylinositol-4,5-bisphosphate. Proc Natl Acad Sci U S A 2012; 109:E2306-15; PMID:22869721; http://dx.doi.org/10.1073/pnas.1205278109
  • Ohno H, Tomemori T, Nakatsu F, Okazaki Y, Aguilar RC, Foelsch H, Mellman I, Saito T, Shirasawa T, Bonifacino JS. Mu1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett 1999; 449:215-20; PMID:10338135; http://dx.doi.org/10.1016/S0014-5793(99)00432-9
  • Diaz F, Gravotta D, Deora A, Schreiner R, Schoggins J, Falck-Pedersen E, Rodriguez-Boulan E. Clathrin adaptor AP1B controls adenovirus infectivity of epithelial cells. Proc Natl Acad Sci U S A 2009; 106:11143-8; PMID:19549835; http://dx.doi.org/10.1073/pnas.0811227106
  • Schreiner R, Frindt G, Diaz F, Carvajal-Gonzalez JM, Perez Bay AE, Palmer LG, Marshansky V, Brown D, Philp NJ, Rodriguez-Boulan E. The absence of a clathrin adapter confers unique polarity essential to proximal tubule function. Kidney Int 2010; 78:382-8; PMID:20531453; http://dx.doi.org/10.1038/ki.2010.166
  • Martensson S, Brunmark C, Ohlsson L, Bak-Jensen E, Butkowski R, Boketoft A, Wieslander J. Heterogeneity of renal carcinoma. Nephrol Dial Transplant 1995; 10:1637-43; PMID:8559482
  • Gu FL, Cai SL, Cai BJ, Wu CP. Cellular origin of renal cell carcinoma–an immunohistological study on monoclonal antibodies. Scand J Urol Nephrol Suppl 1991; 138:203-6; PMID:1785005
  • Holthofer H, Miettinen A, Paasivuo R, Lehto VP, Linder E, Alfthan O, Virtanen I. Cellular origin and differentiation of renal carcinomas. A fluorescence microscopic study with kidney-specific antibodies, antiintermediate filament antibodies, and lectins. Lab Invest 1983; 49:317-26; PMID:6193332
  • Mimura M, Masuda A, Nishiumi S, Kawakami K, Fujishima Y, Yoshie T, Mizuno S, Miki I, Ohno H, Hase K, et al. AP1B plays an important role in intestinal tumorigenesis with the truncating mutation of an APC gene. Int J Cancer 2011; 130:1011-20; PMID:21484796; http://dx.doi.org/10.1002/ijc.26131
  • Takahashi D, Hase K, Kimura S, Nakatsu F, Ohmae M, Mandai Y, Sato T, Date Y, Ebisawa M, Kato T, et al. The epithelia-specific membrane trafficking factor AP-1B controls gut immune homeostasis in mice. Gastroenterology 2011; 141:621-32; PMID:21669204; http://dx.doi.org/10.1053/j.gastro.2011.04.056
  • Hase K, Nakatsu F, Ohmae M, Sugihara K, Shioda N, Takahashi D, Obata Y, Furusawa Y, Fujimura Y, Yamashita T, et al. AP-1B-mediated protein sorting regulates polarity and proliferation of intestinal epithelial cells in mice. Gastroenterology 2013; 145:625-35; PMID:23684748; http://dx.doi.org/10.1053/j.gastro.2013.05.013
  • Lee J, Jongeward GD, Sternberg PW. unc-101, a gene required for many aspects of Caenorhabditis elegans development and behavior, encodes a clathrin-associated protein. Genes Dev 1994; 8:60-73; PMID:8288128; http://dx.doi.org/10.1101/gad.8.1.60
  • Shim J, Sternberg PW, Lee J. Distinct and redundant functions of mu1 medium chains of the AP-1 clathrin-associated protein complex in the nematode Caenorhabditis elegans. Mol Biol Cell 2000; 11:2743-56; PMID:10930467; http://dx.doi.org/10.1091/mbc.11.8.2743
  • Gariano G, Guarienti M, Bresciani R, Borsani G, Carola G, Monti E, Giuliani R, Rezzani R, Bonomini F, Preti A, et al. Analysis of three mu1-AP1 subunits during zebrafish development. Dev Dyn 2014; 243:299-314; PMID:24123392; http://dx.doi.org/10.1002/dvdy.24071
  • Zizioli D, Forlanelli E, Guarienti M, Nicoli S, Fanzani A, Bresciani R, Borsani G, Preti A, Cotelli F, Schu P. Characterization of the AP-1 mu1A and mu1B adaptins in zebrafish (Danio rerio). Dev Dyn 2010; 239:2404-12; PMID:20652956; http://dx.doi.org/10.1002/dvdy.22372
  • Benhra N, Lallet S, Cotton M, Le Bras S, Dussert A, Le Borgne R. AP-1 controls the trafficking of Notch and Sanpodo toward E-cadherin junctions in sensory organ precursors. Curr Biol 2011; 21:87-95; PMID:21194948; http://dx.doi.org/10.1016/j.cub.2010.12.010
  • Burgess J, Jauregui M, Tan J, Rollins J, Lallet S, Leventis PA, Boulianne GL, Chang HC, Le Borgne R, Krämer H, et al. AP-1 and clathrin are essential for secretory granule biogenesis in Drosophila. Mol Biol Cell 2011; 22:2094-105; PMID:21490149; http://dx.doi.org/10.1091/mbc.E11-01-0054
  • Peng YH, Yang WK, Lin WH, Lai TT, Chien CT. Nak regulates Dlg basal localization in Drosophila salivary gland cells. Biochem Biophys Res Commun 2009; 382:108-13; PMID:19258011; http://dx.doi.org/10.1016/j.bbrc.2009.02.139

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