Adaptor proteins involved in polarized sorting

Journal of Cell Biology

Volumn 204, Issue 1, 2014, Pages 7-17

  Bonifacino, Juan S ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 4 PHOSPHONOBUTYRIC ACID; ADAPTOR PROTEIN; COAT PROTEIN;

ASYMMETRIC CELL DIVISION; CELL FATE; CELL POLARITY; CELL SELECTION; ENDOSOME; EPITHELIUM CELL; HUMAN; MUTANT; NERVE CELL; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TRANS GOLGI NETWORK;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL MEMBRANE; CELL POLARITY; HUMANS; MEMBRANE PROTEINS; PROTEIN TRANSPORT;

EID: 84891894909     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201310021     Document Type: Review

References (100)

1. Abou Jamra, R., O. Philippe, A. Raas-Rothschild, S.H. Eck, E. Graf, R. Buchert, G. Borck, A. Ekici, F.F. Brockschmidt, M.M. Nöthen, et al. 2011. Adaptor protein complex 4 deficiency causes severe autosomal-recessive intellectual disability, progressive spastic paraplegia, shy character, and short stature. Am. J. Hum. Genet. 88:788-795. http://dx.doi.org/10.1016/j.ajhg.2011.04.019
2. Anderson, E., S. Maday, J. Sfakianos, M. Hull, B. Winckler, D. Sheff, H. Fölsch, and I. Mellman. 2005. Transcytosis of NgCAM in epithelial cells reflects differential signal recognition on the endocytic and secretory pathways. J. Cell Biol. 170:595-605. http://dx.doi.org/10.1083/jcb.200506051
3. Ang, A.L., T. Taguchi, S. Francis, H. Fölsch, L.J. Murrells, M. Pypaert, G. Warren, and I. Mellman. 2004. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J. Cell Biol. 167:531-543. http://dx.doi.org/10.1083/jcb.200408165
4. Apodaca, G., L.I. Gallo, and D.M. Bryant. 2012. Role of membrane traffic in the generation of epithelial cell asymmetry. Nat. Cell Biol. 14:1235-1243. http://dx.doi.org/10.1038/ncb2635
5. Arimura, N., and K. Kaibuchi. 2007. Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8:194-205. http://dx.doi.org/10.1038/nrn2056
6. Aroeti, B., P.A. Kosen, I.D. Kuntz, F.E. Cohen, and K.E. Mostov. 1993. Mutational and secondary structural analysis of the basolateral sorting signal of the polymeric immunoglobulin receptor. J. Cell Biol. 123:1149-1160. http://dx.doi.org/10.1083/jcb.123.5.1149
7. Bae, Y.K., H. Qin, K.M. Knobel, J. Hu, J.L. Rosenbaum, and M.M. Barr. 2006. General and cell-type specific mechanisms target TRPP2/PKD-2 to cilia. Development. 133:3859-3870. http://dx.doi.org/10.1242/dev.02555
8. Barfield, R.M., J.C. Fromme, and R. Schekman. 2009. The exomer coat complex transports Fus1p to the plasma membrane via a novel plasma membrane sorting signal in yeast. Mol. Biol. Cell. 20:4985-4996. http://dx.doi.org/10.1091/mbc. E09-04-0324
9. Benhra, N., S. Lallet, M. Cotton, S. Le Bras, A. Dussert, and R. Le Borgne. 2011. AP-1 controls the trafficking of Notch and Sanpodo toward E-cadherin junctions in sensory organ precursors. Curr. Biol. 21:87-95. http://dx.doi.org/10.1016/j.cub.2010.12.010
10. Berdnik, D., T. Török, M. González-Gaitán, and J.A. Knoblich. 2002. The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev. Cell. 3:221-231. http://dx.doi.org/10.1016/S1534-5807(02)00215-0
11. Bryant, D.M., and K.E. Mostov. 2008. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9:887-901. http://dx.doi.org/10.1038/nrm2523
12. Cao, X., M.A. Surma, and K. Simons. 2012. Polarized sorting and trafficking in epithelial cells. Cell Res. 22:793-805. http://dx.doi.org/10.1038/cr.2012.64
13. Carvajal-Gonzalez, J.M., D. Gravotta, R. Mattera, F. Diaz, A. Perez Bay, A.C. Roman, R.P. Schreiner, R. Thuenauer, J.S. Bonifacino, and E. Rodriguez-Boulan. 2012. Basolateral sorting of the Coxsackie and adenovirus receptor through interaction of a canonical YXXPhi motif with the clathrin adaptors AP-1A and AP-1B. Proc. Natl. Acad. Sci. USA. 109:3820-3825. http://dx.doi.org/10.1073/pnas.1117949109
14. Casanova, J.E., G. Apodaca, and K.E. Mostov. 1991. An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell. 66:65-75. http://dx.doi.org/10.1016/0092-8674(91)90139-P
15. Clemens Grisham, R., K. Kindt, K. Finger-Baier, B. Schmid, and T. Nicolson. 2013. Mutations in ap1b1 cause mistargeting of the Na(+)/K(+)-ATPase pump in sensory hair cells. PLoS ONE. 8:e60866. http://dx.doi.org/10.1371/journal.pone.0060866
16. Cohen, C.J., J. Gaetz, T. Ohman, and J.M. Bergelson. 2001. Multiple regions within the Coxsackievirus and adenovirus receptor cytoplasmic domain are required for basolateral sorting. J. Biol. Chem. 276:25392-25398. http://dx.doi.org/10.1074/jbc. M009531200
17. Cotton, M., N. Benhra, and R. Le Borgne. 2013. Numb inhibits the recycling of Sanpodo in Drosophila sensory organ precursor. Curr. Biol. 23:581-587. http://dx.doi.org/10.1016/j.cub.2013.02.020
18. Couturier, L., K. Mazouni, and F. Schweisguth. 2013. Numb localizes at endosomes and controls the endosomal sorting of notch after asymmetric division in Drosophila. Curr. Biol. 23:588-593. http://dx.doi.org/10.1016/j.cub.2013.03.002
19. Deborde, S., E. Perret, D. Gravotta, A. Deora, S. Salvarezza, R. Schreiner, and E. Rodriguez-Boulan. 2008. Clathrin is a key regulator of basolateral polarity. Nature. 452:719-723. http://dx.doi.org/10.1038/nature06828
20. Delevoye, C., I. Hurbain, D. Tenza, J.B. Sibarita, S. Uzan-Gafsou, H. Ohno, W.J. Geerts, A.J. Verkleij, J. Salamero, M.S. Marks, and G. Raposo. 2009. AP-1 and KIF13A coordinate endosomal sorting and positioning during melanosome biogenesis. J. Cell Biol. 187:247-264. http://dx.doi.org/10.1083/jcb.200907122
21. Dell'Angelica, E.C., C. Mullins, and J.S. Bonifacino. 1999. AP-4, a novel protein complex related to clathrin adaptors. J. Biol. Chem. 274:7278-7285. http://dx.doi.org/10.1074/jbc.274.11.7278
22. Diaz, F., D. Gravotta, A. Deora, R. Schreiner, J. Schoggins, E. Falck-Pedersen, and E. Rodriguez-Boulan. 2009. Clathrin adaptor AP1B controls adenovirus infectivity of epithelial cells. Proc. Natl. Acad. Sci. USA. 106:11143-11148. http://dx.doi.org/10.1073/pnas.0811227106
23. Donoso, M., J. Cancino, J. Lee, P. van Kerkhof, C. Retamal, G. Bu, A. Gonzalez, A. Cáceres, and M.P. Marzolo. 2009. Polarized traffic of LRP1 involves AP1B and SNX17 operating on Y-dependent sorting motifs in different pathways. Mol. Biol. Cell. 20:481-497. http://dx.doi.org/10.1091/mbc.E08-08-0805
24. Dotti, C.G., and K. Simons. 1990. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell. 62:63-72. http://dx.doi.org/10.1016/0092-8674(90)90240-F
25. Duffield, A., M.J. Caplan, and T.R. Muth. 2008. Protein trafficking in polarized cells. Int Rev Cell Mol Biol. 270:145-179. http://dx.doi.org/10.1016/S1937-6448(08)01404-4
26. Dwyer, N.D., C.E. Adler, J.G. Crump, N.D. L'Etoile, and C.I. Bargmann. 2001. Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron. 31:277-287. http://dx.doi.org/10.1016/S0896-6273(01)00361-0
27. Eskelinen, E.L., C. Meyer, H. Ohno, K. von Figura, and P. Schu. 2002. The polarized epithelia-specific mu 1B-adaptin complements mu 1A-deficiency in fibroblasts. EMBO Rep. 3:471-477. http://dx.doi.org/10.1093/embo-reports/kvf092
28. Farfán, P., J. Lee, J. Larios, P. Sotelo, G. Bu, and M.P. Marzolo. 2013. A sorting nexin 17-binding domain within the LRP1 cytoplasmic tail mediates receptor recycling through the basolateral sorting endosome. Traffic. 14:823-838. http://dx.doi.org/10.1111/tra.12076
29. Farías, G.G., L. Cuitino, X. Guo, X. Ren, M. Jarnik, R. Mattera, and J.S. Bonifacino. 2012. Signal-mediated, AP-1/clathrin-dependent sorting of transmembrane receptors to the somatodendritic domain of hippocampal neurons. Neuron. 75:810-823. http://dx.doi.org/10.1016/j.neuron.2012.07.007
30. Fields, I.C., E. Shteyn, M. Pypaert, V. Proux-Gillardeaux, R.S. Kang, T. Galli, and H. Fölsch. 2007. v-SNARE cellubrevin is required for basolateral sorting of AP-1B-dependent cargo in polarized epithelial cells. J. Cell Biol. 177:477-488. http://dx.doi.org/10.1083/jcb.200610047
31. Fields, I.C., S.M. King, E. Shteyn, R.S. Kang, and H. Fölsch. 2010. Phosphatidylinositol 3,4,5-trisphosphate localization in recycling endosomes is necessary for AP-1B-dependent sorting in polarized epithelial cells. Mol. Biol. Cell. 21:95-105. http://dx.doi.org/10.1091/mbc. E09-01-0036
32. Fölsch, H., H. Ohno, J.S. Bonifacino, and I. Mellman. 1999. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell. 99:189-198. http://dx.doi.org/10.1016/S0092-8674(00)81650-5
33. Fölsch, H., M. Pypaert, P. Schu, and I. Mellman. 2001. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152:595-606. http://dx.doi.org/10.1083/jcb.152.3.595
34. Fölsch, H., M. Pypaert, S. Maday, L. Pelletier, and I. Mellman. 2003. The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains. J. Cell Biol. 163:351-362. http://dx.doi.org/10.1083/jcb.200309020
35. Futter, C.E., A. Gibson, E.H. Allchin, S. Maxwell, L.J. Ruddock, G. Odorizzi, D. Domingo, I.S. Trowbridge, and C.R. Hopkins. 1998. In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules. J. Cell Biol. 141:611-623. http://dx.doi.org/10.1083/jcb.141.3.611
36. Gan, Y., T.E. McGraw, and E. Rodriguez-Boulan. 2002. The epithelialspecific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nat. Cell Biol. 4:605-609.
37. Garrido, J.J., F. Fernandes, P. Giraud, I. Mouret, E. Pasqualini, M.P. Fache, F. Jullien, and B. Dargent. 2001. Identification of an axonal determinant in the C-terminus of the sodium channel Na(v)1.2. EMBO J. 20:5950-5961. http://dx.doi.org/10.1093/emboj/20.21.5950
38. Gonzalez, A., and E. Rodriguez-Boulan. 2009. Clathrin and AP1B: key roles in basolateral trafficking through trans-endosomal routes. FEBS Lett. 583:3784-3795. http://dx.doi.org/10.1016/j.febslet.2009.10.050
39. Gravotta, D., J.M. Carvajal-Gonzalez, R. Mattera, S. Deborde, J.R. Banfelder, J.S. Bonifacino, and E. Rodriguez-Boulan. 2012. The clathrin adaptor AP-1A mediates basolateral polarity. Dev. Cell. 22:811-823. http://dx.doi.org/10.1016/j.devcel.2012.02.004
40. Guo, X., R. Mattera, X. Ren, Y. Chen, C. Retamal, A. González, and J.S. Bonifacino. 2013. The adaptor protein-1 ?1B subunit expands the repertoire of basolateral sorting signal recognition in epithelial cells. Dev. Cell. 27:353-366. http://dx.doi.org/10.1016/j.devcel.2013.10.006
41. Guo, Y., G. Zanetti, and R. Schekman. 2013. A novel GTP-binding proteinadaptor protein complex responsible for export of Vangl2 from the trans Golgi network. Elife. 2:e00160. http://dx.doi.org/10.7554/eLife.00160
42. Hase, K., F. Nakatsu, M. Ohmae, K. Sugihara, N. Shioda, D. Takahashi, Y. Obata, Y. Furusawa, Y. Fujimura, T. Yamashita, et al. 2013. AP-1Bmediated protein sorting regulates polarity and proliferation of intestinal epithelial cells in mice. Gastroenterology. 145:625-635. http://dx.doi.org/10.1053/j.gastro.2013.05.013
43. Hirst, J., N.A. Bright, B. Rous, and M.S. Robinson. 1999. Characterization of a fourth adaptor-related protein complex. Mol. Biol. Cell. 10:2787-2802. http://dx.doi.org/10.1091/mbc.10.8.2787
44. Hirst, J., G.H. Borner, R. Antrobus, A.A. Peden, N.A. Hodson, D.A. Sahlender, and M.S. Robinson. 2012. Distinct and overlapping roles for AP-1 and GGAs revealed by the "knocksideways" system. Curr. Biol. 22:1711-1716. http://dx.doi.org/10.1016/j.cub.2012.07.012
45. Hirst, J., C. Irving, and G.H. Borner. 2013. Adaptor protein complexes AP-4 and AP-5: new players in endosomal trafficking and progressive spastic paraplegia. Traffic. 14:153-164. http://dx.doi.org/10.1111/tra.12028
46. Jareb, M., and G. Banker. 1998. The polarized sorting of membrane proteins expressed in cultured hippocampal neurons using viral vectors. Neuron. 20:855-867. http://dx.doi.org/10.1016/S0896-6273(00)80468-7
47. Kang, R.S., and H. Fölsch. 2011. ARH cooperates with AP-1B in the exocytosis of LDLR in polarized epithelial cells. J. Cell Biol. 193:51-60. http://dx.doi.org/10.1083/jcb.201012121
48. Klumperman, J., A. Hille, T. Veenendaal, V. Oorschot, W. Stoorvogel, K. von Figura, and H.J. Geuze. 1993. Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J. Cell Biol. 121:997-1010. http://dx.doi.org/10.1083/jcb.121.5.997
49. Klumperman, J., R. Kuliawat, J.M. Griffith, H.J. Geuze, and P. Arvan. 1998. Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles. J. Cell Biol. 141:359-371. http://dx.doi.org/10.1083/jcb.141.2.359
50. Koivisto, U.M., A.L. Hubbard, and I. Mellman. 2001. A novel cellular phenotype for familial hypercholesterolemia due to a defect in polarized targeting of LDL receptor. Cell. 105:575-585. http://dx.doi.org/10.1016/S0092-8674(01)00371-3
51. Lasiecka, Z.M., C.C. Yap, M. Vakulenko, and B. Winckler. 2009. Compartmentalizing the neuronal plasma membrane from axon initial segments to synapses. Int Rev Cell Mol Biol. 272:303-389. http://dx.doi.org/10.1016/S1937-6448(08)01607-9
52. Lee, I., B. Doray, J. Govero, and S. Kornfeld. 2008. Binding of cargo sorting signals to AP-1 enhances its association with ADP ribosylation factor 1-GTP. J. Cell Biol. 180:467-472. http://dx.doi.org/10.1083/jcb.200709037
53. Lui-Roberts, W.W., L.M. Collinson, L.J. Hewlett, G. Michaux, and D.F. Cutler. 2005. An AP-1/clathrin coat plays a novel and essential role in forming the Weibel-Palade bodies of endothelial cells. J. Cell Biol. 170:627-636. http://dx.doi.org/10.1083/jcb.200503054
54. Margeta, M.A., G.J. Wang, and K. Shen. 2009. Clathrin adaptor AP-1 complex excludes multiple postsynaptic receptors from axons in C. elegans. Proc. Natl. Acad. Sci. USA. 106:1632-1637. http://dx.doi.org/10.1073/pnas.0812078106
55. Matsuda, S., and M. Yuzaki. 2008. AP-4: autophagy-four mislocalized proteins in axons. Autophagy. 4:815-816.
56. Matsuda, S., E. Miura, K. Matsuda, W. Kakegawa, K. Kohda, M. Watanabe, and M. Yuzaki. 2008. Accumulation of AMPA receptors in autophagosomes in neuronal axons lacking adaptor protein AP-4. Neuron. 57:730-745. http://dx.doi.org/10.1016/j.neuron.2008.02.012
57. Matter, K., W. Hunziker, and I. Mellman. 1992. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell. 71:741-753. http://dx.doi.org/10.1016/0092-8674(92)90551-M
58. Mattera, R., M. Boehm, R. Chaudhuri, Y. Prabhu, and J.S. Bonifacino. 2011. Conservation and diversification of dileucine signal recognition by adaptor protein (AP) complex variants. J. Biol. Chem. 286:2022-2030. http://dx.doi.org/10.1074/jbc. M110.197178
59. McGill, M.A., S.E. Dho, G. Weinmaster, and C.J. McGlade. 2009. Numb regulates post-endocytic trafficking and degradation of Notch1. J. Biol. Chem. 284:26427-26438. http://dx.doi.org/10.1074/jbc. M109.014845
60. Mellman, I., and W.J. Nelson. 2008. Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9:833-845. http://dx.doi.org/10.1038/nrm2525
61. Meyer, C., D. Zizioli, S. Lausmann, E.L. Eskelinen, J. Hamann, P. Saftig, K. von Figura, and P. Schu. 2000. mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19:2193-2203. http://dx.doi.org/10.1093/emboj/19.10.2193
62. Mimura, M., A. Masuda, S. Nishiumi, K. Kawakami, Y. Fujishima, T. Yoshie, S. Mizuno, I. Miki, H. Ohno, K. Hase, et al. 2012. AP1B plays animportant role in intestinal tumorigenesis with the truncating mutation of an APC gene. Int. J. Cancer. 130:1011-1020. http://dx.doi.org/10.1002/ijc.26131
63. Montpetit, A., S. Côté, E. Brustein, C.A. Drouin, L. Lapointe, M. Boudreau, C. Meloche, R. Drouin, T.J. Hudson, P. Drapeau, and P. Cossette. 2008. Disruption of AP1S1, causing a novel neurocutaneous syndrome, perturbs development of the skin and spinal cord. PLoS Genet. 4:e1000296. http://dx.doi.org/10.1371/journal.pgen.1000296
64. Moreno-De-Luca, A., S.L. Helmers, H. Mao, T.G. Burns, A.M. Melton, K.R. Schmidt, P.M. Fernhoff, D.H. Ledbetter, and C.L. Martin. 2011. Adaptor protein complex-4 (AP-4) deficiency causes a novel autosomal recessive cerebral palsy syndrome with microcephaly and intellectual disability. J. Med. Genet. 48:141-144. http://dx.doi.org/10.1136/jmg.2010.082263
65. Nakagawa, T., M. Setou, D. Seog, K. Ogasawara, N. Dohmae, K. Takio, and N. Hirokawa. 2000. A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex. Cell. 103:569-581. http://dx.doi.org/10.1016/S0092-8674(00) 00161-6
66. Nilsson, L., B. Conradt, A.F. Ruaud, C.C. Chen, J. Hatzold, J.L. Bessereau, B.D. Grant, and S. Tuck. 2008. Caenorhabditis elegans num-1 negatively regulates endocytic recycling. Genetics. 179:375-387. http://dx.doi.org/10.1534/genetics.108.087247
67. Odorizzi, G., and I.S. Trowbridge. 1997. Structural requirements for basolateral sorting of the human transferrin receptor in the biosynthetic and endocytic pathways of Madin-Darby canine kidney cells. J. Cell Biol. 137:1255-1264. http://dx.doi.org/10.1083/jcb.137.6.1255
68. Ohno, H., T. Tomemori, F. Nakatsu, Y. Okazaki, R.C. Aguilar, H. Foelsch, I. Mellman, T. Saito, T. Shirasawa, and J.S. Bonifacino. 1999. Mu1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett. 449:215-220. http://dx.doi.org/10.1016/S0014-5793(99)00432-9
69. Pathak, R.K., M. Yokode, R.E. Hammer, S.L. Hofmann, M.S. Brown, J.L. Goldstein, and R.G. Anderson. 1990. Tissue-specific sorting of the human LDL receptor in polarized epithelia of transgenic mice. J. Cell Biol. 111:347-359. http://dx.doi.org/10.1083/jcb.111.2.347
70. Pocha, S.M., T. Wassmer, C. Niehage, B. Hoflack, and E. Knust. 2011. Retromer controls epithelial cell polarity by trafficking the apical determinant Crumbs. Curr. Biol. 21:1111-1117. http://dx.doi.org/10.1016/j.cub.2011.05.007
71. Polishchuk, R.S., E. San Pietro, A. Di Pentima, S. Teté, and J.S. Bonifacino. 2006. Ultrastructure of long-range transport carriers moving from the trans Golgi network to peripheral endosomes. Traffic. 7:1092-1103. http://dx.doi.org/10.1111/j.1600-0854.2006.00453.x
72. Reales, E., N. Sharma, S.H. Low, H. Fölsch, and T. Weimbs. 2011. 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. 6:e21181. http://dx.doi.org/10.1371/journal.pone.0021181
73. Ren, X., G.G. Farías, B.J. Canagarajah, J.S. Bonifacino, and J.H. Hurley. 2013. Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1. Cell. 152:755-767. http://dx.doi.org/10.1016/j.cell.2012.12.042
74. Robinson, M.S. 2004. Adaptable adaptors for coated vesicles. Trends Cell Biol. 14:167-174. http://dx.doi.org/10.1016/j.tcb.2004.02.002
75. Roush, D.L., C.J. Gottardi, H.Y. Naim, M.G. Roth, and M.J. Caplan. 1998. Tyrosine-based membrane protein sorting signals are differentially interpreted by polarized Madin-Darby canine kidney and LLC-PK1 epithelial cells. J. Biol. Chem. 273:26862-26869. http://dx.doi.org/10.1074/jbc.273.41.26862
76. Sampo, B., S. Kaech, S. Kunz, and G. Banker. 2003. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron. 37:611-624. http://dx.doi.org/10.1016/S0896-6273(03)00058-8
77. Schmidt, M.R., T. Maritzen, V. Kukhtina, V.A. Higman, L. Doglio, N.N. Barak, H. Strauss, H. Oschkinat, C.G. Dotti, and V. Haucke. 2009. Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proc. Natl. Acad. Sci. USA. 106:15344-15349. http://dx.doi.org/10.1073/pnas.0904268106
78. Schreiner, R., G. Frindt, F. Diaz, J.M. Carvajal-Gonzalez, A.E. Perez Bay, L.G. Palmer, V. Marshansky, D. Brown, N.J. Philp, and E. Rodriguez-Boulan. 2010. The absence of a clathrin adapter confers unique polarity essential to proximal tubule function. Kidney Int. 78:382-388. http://dx.doi.org/10.1038/ki.2010.166
79. Seaman, M.N., J.M. McCaffery, and S.D. Emr. 1998. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142:665-681. http://dx.doi.org/10.1083/jcb.142.3.665
80. Shafaq-Zadah, M., L. Brocard, F. Solari, and G. Michaux. 2012. AP-1 is required for the maintenance of apico-basal polarity in the C. elegans intestine. Development. 139:2061-2070. http://dx.doi.org/10.1242/dev.076711
81. Shteyn, E., L. Pigati, and H. Fölsch. 2011. Arf6 regulates AP-1B-dependent sorting in polarized epithelial cells. J. Cell Biol. 194:873-887. http://dx.doi.org/10.1083/jcb.201106010
82. Simmen, T., S. Höning, A. Icking, R. Tikkanen, and W. Hunziker. 2002. AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells. Nat. Cell Biol. 4:154-159. http://dx.doi.org/10.1038/ncb745
83. Starr, T.L., S. Pagant, C.W. Wang, and R. Schekman. 2012. Sorting signals that mediate traffic of chitin synthase III between the TGN/endosomes and to the plasma membrane in yeast. PLoS ONE. 7:e46386. http://dx.doi.org/10.1371/journal.pone.0046386
84. Takahashi, D., K. Hase, S. Kimura, F. Nakatsu, M. Ohmae, Y. Mandai, T. Sato, Y. Date, M. Ebisawa, T. Kato, et al. 2011. The epithelia-specific membrane trafficking factor AP-1B controls gut immune homeostasis in mice. Gastroenterology. 141:621-632. http://dx.doi.org/10.1053/j.gastro.2011.04.056
85. Tarpey, P.S., C. Stevens, J. Teague, S. Edkins, S. O'Meara, T. Avis, S. Barthorpe, G. Buck, A. Butler, J. Cole, et al. 2006. Mutations in the gene encoding the Sigma 2 subunit of the adaptor protein 1 complex, AP1S2, cause X-linked mental retardation. Am. J. Hum. Genet. 79:1119-1124. http://dx.doi.org/10.1086/510137
86. Teh, O.K., Y. Shimono, M. Shirakawa, Y. Fukao, K. Tamura, T. Shimada, and I. Hara-Nishimura. 2013. The AP-1 ? adaptin is required for KNOLLE localization at the cell plate to mediate cytokinesis in Arabidopsis. Plant Cell Physiol. 54:838-847. http://dx.doi.org/10.1093/pcp/pct048
87. Tong, X., D. Zitserman, I. Serebriiskii, M. Andrake, R. Dunbrack, and F. Roegiers. 2010. Numb independently antagonizes Sanpodo membrane targeting and Notch signaling in Drosophila sensory organ precursor cells. Mol. Biol. Cell. 21:802-810. http://dx.doi.org/10.1091/mbc. E09-09-0831
88. Traub, L.M., and J.S. Bonifacino. 2013. Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb. Perspect. Biol. 5:a016790. http://dx.doi.org/10.1101/cshperspect.a016790
89. Valdivia, R.H., D. Baggott, J.S. Chuang, and R.W. Schekman. 2002. The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell. 2:283-294. http://dx.doi.org/10.1016/S1534-5807(02)00127-2
90. Vergés, M., F. Luton, C. Gruber, F. Tiemann, L.G. Reinders, L. Huang, A.L. Burlingame, C.R. Haft, and K.E. Mostov. 2004. The mammalian retromer regulates transcytosis of the polymeric immunoglobulin receptor. Nat. Cell Biol. 6:763-769. http://dx.doi.org/10.1038/ncb1153
91. Verkerk, A.J., R. Schot, B. Dumee, K. Schellekens, S. Swagemakers, A.M. Bertoli-Avella, M.H. Lequin, J. Dudink, P. Govaert, A.L. van Zwol, et al. 2009. Mutation in the AP4M1 gene provides a model for neuroaxonal injury in cerebral palsy. Am. J. Hum. Genet. 85:40-52. http://dx.doi.org/10.1016/j.ajhg.2009.06.004
92. Wang, C.W., S. Hamamoto, L. Orci, and R. Schekman. 2006. Exomer: A coat complex for transport of select membrane proteins from the trans-Golgi network to the plasma membrane in yeast. J. Cell Biol. 174:973-983. http://dx.doi.org/10.1083/jcb.200605106
93. Weisz, O.A., and E. Rodriguez-Boulan. 2009. Apical trafficking in epithelial cells: signals, clusters and motors. J. Cell Sci. 122:4253-4266. http://dx.doi.org/10.1242/jcs.032615
94. Xu, J., K.A. Toops, F. Diaz, J.M. Carvajal-Gonzalez, D. Gravotta, F. Mazzoni, R. Schreiner, E. Rodriguez-Boulan, and A. Lakkaraju. 2012. Mechanism of polarized lysosome exocytosis in epithelial cells. J. Cell Sci. 125:5937-5943. http://dx.doi.org/10.1242/jcs.109421
95. Yamamoto, H., C. Awada, H. Hanaki, H. Sakane, I. Tsujimoto, Y. Takahashi, T. Takao, and A. Kikuchi. 2013. The apical and basolateral secretion of Wnt11 and Wnt3a in polarized epithelial cells is regulated by different mechanisms. J. Cell Sci. 126:2931-2943. http://dx.doi.org/10.1242/jcs.126052
96. Yap, C.C., M. Murate, S. Kishigami, Y. Muto, H. Kishida, T. Hashikawa, and R. Yano. 2003. Adaptor protein complex-4 (AP-4) is expressed in the central nervous system neurons and interacts with glutamate receptor delta2. Mol. Cell. Neurosci. 24:283-295. http://dx.doi.org/10.1016/S1044-7431(03)00164-7
97. Yap, C.C., D. Wisco, P. Kujala, Z.M. Lasiecka, J.T. Cannon, M.C. Chang, H. Hirling, J. Klumperman, and B. Winckler. 2008. The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J. Cell Biol. 180:827-842. http://dx.doi.org/10.1083/jcb.200707143
98. Yin, X., S.J. Murphy, M.C. Wilkes, Y. Ji, and E.B. Leof. 2013. Retromer maintains basolateral distribution of the type II TGF-? receptor via the recycling endosome. Mol. Biol. Cell. 24:2285-2298. http://dx.doi.org/10.1091/mbc. E13-02-0093
99. Zhang, H., A. Kim, N. Abraham, L.A. Khan, D.H. Hall, J.T. Fleming, and V. Gobel. 2012. Clathrin and AP-1 regulate apical polarity and lumen formation during C. elegans tubulogenesis. Development. 139:2071-2083. http://dx.doi.org/10.1242/dev.077347
100. Zizioli, D., C. Meyer, G. Guhde, P. Saftig, K. von Figura, and P. Schu. 1999. Early embryonic death of mice deficient in gamma-adaptin. J. Biol. Chem. 274:5385-5390. http://dx.doi.org/10.1074/jbc.274.9.5385