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Abstract

Protein coats are supramolecular complexes that assemble on the cytosolic face of membranes to promote cargo sorting and transport carrier formation in the endomembrane system of eukaryotic cells. Several types of protein coats have been described, including COPI, COPII, AP-1, AP-2, AP-3, AP-4, AP-5, and retromer, which operate at different stages of the endomembrane system. Defects in these coats impair specific transport pathways, compromising the function and viability of the cells. In humans, mutations in subunits of these coats cause various congenital diseases that are collectively referred to as coatopathies. In this article, we review the fundamental properties of protein coats and the diseases that result from mutation of their constituent subunits.

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2019-10-06
2024-03-28
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Literature Cited

  1. Abou Jamra R, Philippe O, Raas-Rothschild A, Eck SH, Graf E 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. 88:788–95
    [Google Scholar]
  2. Alazami AM, Hijazi H, Kentab AY, Alkuraya FS 2014. NECAP1 loss of function leads to a severe infantile epileptic encephalopathy. J. Med. Genet. 51:224–28
    [Google Scholar]
  3. Alwadei AH, Benini R, Mahmoud A, Alasmari A, Kamsteeg EJ et al. 2016. Loss-of-function mutation in RUSC2 causes intellectual disability and secondary microcephaly. Dev. Med. Child Neurol. 58:1317–22
    [Google Scholar]
  4. Ammann S, Schulz A, Krägeloh-Mann I, Dieckmann NM, Niethammer K et al. 2016. Mutations in AP3D1 associated with immunodeficiency and seizures define a new type of Hermansky-Pudlak syndrome. Blood 127:997–1006
    [Google Scholar]
  5. Arakel EC, Schwappach B. 2018. Formation of COPI-coated vesicles at a glance. J. Cell Sci. 131:jcs209890
    [Google Scholar]
  6. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS 2004. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165:123–33
    [Google Scholar]
  7. Asensio CS, Sirkis DW, Maas JW, Egami K, To TL et al. 2013. Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway. Dev. Cell 27:425–37
    [Google Scholar]
  8. Assoum M, Philippe C, Isidor B, Perrin L, Makrythanasis P et al. 2016. Autosomal-recessive mutations in AP3B2, adaptor-related protein complex 3 beta 2 subunit, cause an early-onset epileptic encephalopathy with optic atrophy. Am. J. Hum. Genet. 99:1368–76
    [Google Scholar]
  9. Attree O, Olivos IM, Okabe I, Bailey LC, Nelson DL et al. 1992. The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature 358:239–42
    [Google Scholar]
  10. Baines AC, Adams EJ, Zhang B, Ginsburg D 2013. Disruption of the Sec24d gene results in early embryonic lethality in the mouse. PLOS ONE 8:e61114
    [Google Scholar]
  11. Ball CL, Hunt SP, Robinson MS 1995. Expression and localization of alpha-adaptin isoforms. J. Cell Sci. 108:2865–75
    [Google Scholar]
  12. Banne E, Atawneh O, Henneke M, Brockmann K, Gärtner J et al. 2013. West syndrome, microcephaly, grey matter heterotopia and hypoplasia of corpus callosum due to a novel ARFGEF2 mutation. J. Med. Genet. 50:772–75
    [Google Scholar]
  13. Barlowe C, Helenius A. 2016. Cargo capture and bulk flow in the early secretory pathway. Annu. Rev. Cell Dev. Biol. 32:197–222
    [Google Scholar]
  14. Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S et al. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:895–907
    [Google Scholar]
  15. Bauer P, Leshinsky-Silver E, Blumkin L, Schlipf N, Schroder C et al. 2012. Mutation in the AP4B1 gene cause hereditary spastic paraplegia type 47 (SPG47). Neurogenetics 13:73–76
    [Google Scholar]
  16. Baust T, Anitei M, Czupalla C, Parshyna I, Bourel L et al. 2008. Protein networks supporting AP-3 function in targeting lysosomal membrane proteins. Mol. Biol. Cell 19:1942–51
    [Google Scholar]
  17. Bianchi P, Fermo E, Vercellati C, Boschetti C, Barcellini W et al. 2009. Congenital dyserythropoietic anemia type II (CDAII) is caused by mutations in the SEC23B gene. Hum. Mutat. 30:1292–98
    [Google Scholar]
  18. Bitoun M, Maugenre S, Jeannet PY, Lacène E, Ferrer X et al. 2005. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat. Genet. 37:1207–9
    [Google Scholar]
  19. Boehm M, Aguilar RC, Bonifacino JS 2001. Functional and physical interactions of the adaptor protein complex AP-4 with ADP-ribosylation factors (ARFs). EMBO J 20:6265–76
    [Google Scholar]
  20. Bonifacino JS. 2014. Adaptor proteins involved in polarized sorting. J. Cell Biol. 204:7–17
    [Google Scholar]
  21. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116:153–66
    [Google Scholar]
  22. Bonifacino JS, Rojas R. 2006. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7:568–79
    [Google Scholar]
  23. Borner GH, Harbour M, Hester S, Lilley KS, Robinson MS 2006. Comparative proteomics of clathrin-coated vesicles. J. Cell Biol. 175:571–78
    [Google Scholar]
  24. Boyadjiev SA, Fromme JC, Ben J, Chong SS, Nauta C et al. 2006. Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nat. Genet. 38:1192–97
    [Google Scholar]
  25. Branchu J, Boutry M, Sourd L, Depp M, Leone C et al. 2017. Loss of spatacsin function alters lysosomal lipid clearance leading to upper and lower motor neuron degeneration. Neurobiol. Dis. 102:21–37
    [Google Scholar]
  26. Burgos PV, Mardones GA, Rojas AL, daSilva LL, Prabhu Y et al. 2010. Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev. Cell 18:425–36
    [Google Scholar]
  27. Bykov YS, Schaffer M, Dodonova SO, Albert S, Plitzko JM et al. 2017. The structure of the COPI coat determined within the cell. eLife 6:e32493
    [Google Scholar]
  28. Cataldi S, Follett J, Fox JD, Tatarnikov I, Kadgien C et al. 2018. Altered dopamine release and monoamine transporters in Vps35 p.D620N knock-in mice. NPJ Parkinsons Dis 4:27
    [Google Scholar]
  29. Chaudhuri R, Lindwasser OW, Smith WJ, Hurley JH, Bonifacino JS 2007. Downregulation of CD4 by human immunodeficiency virus type 1 Nef is dependent on clathrin and involves direct interaction of Nef with the AP2 clathrin adaptor. J. Virol. 81:3877–90
    [Google Scholar]
  30. Chen WJ, Goldstein JL, Brown MS 1990. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit–mediated internalization of the low-density lipoprotein receptor. J. Biol. Chem. 265:3116–23
    [Google Scholar]
  31. Chen Y, Gershlick DC, Park SY, Bonifacino JS 2017. Segregation in the Golgi complex precedes export of endolysosomal proteins in distinct transport carriers. J. Cell Biol. 216:4141–51
    [Google Scholar]
  32. Clark RH, Stinchcombe JC, Day A, Blott E, Booth S et al. 2003. Adaptor protein 3–dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat. Immunol. 4:1111–20
    [Google Scholar]
  33. Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ 2002. Molecular architecture and functional model of the endocytic AP2 complex. Cell 109:523–35
    [Google Scholar]
  34. Cosson P, Letourneur F. 1994. Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263:1629–31
    [Google Scholar]
  35. Crowther RA, Finch JT, Pearse BM 1976. On the structure of coated vesicles. J. Mol. Biol. 103:785–98
    [Google Scholar]
  36. Damseh N, Danson CM, Al-Ashhab M, Abu-Libdeh B, Gallon M et al. 2015. A defect in the retromer accessory protein, SNX27, manifests by infantile myoclonic epilepsy and neurodegeneration. Neurogenetics 16:215–21
    [Google Scholar]
  37. Dannhauser PN, Camus SM, Sakamoto K, Sadacca LA, Torres JA et al. 2017. CHC22 and CHC17 clathrins have distinct biochemical properties and display differential regulation and function. J. Biol. Chem. 292:20834–44
    [Google Scholar]
  38. Davies AK, Itzhak DN, Edgar JR, Archuleta TL, Hirst J et al. 2018. AP-4 vesicles contribute to spatial control of autophagy via RUSC-dependent peripheral delivery of ATG9A. Nat. Commun. 9:3958
    [Google Scholar]
  39. De Pace R, Skirzewski M, Damme M, Mattera R, Mercurio J et al. 2018. Altered distribution of ATG9A and accumulation of axonal aggregates in neurons from a mouse model of AP-4 deficiency syndrome. PLOS Genet 14:e1007363
    [Google Scholar]
  40. Dell'Angelica EC, Klumperman J, Stoorvogel W, Bonifacino JS 1998. Association of the AP-3 adaptor complex with clathrin. Science 280:431–34
    [Google Scholar]
  41. Dell'Angelica EC, Mullins C, Bonifacino JS 1999a. AP-4, a novel protein complex related to clathrin adaptors. J. Biol. Chem. 274:7278–85
    [Google Scholar]
  42. Dell'Angelica EC, Ohno H, Ooi CE, Rabinovich E, Roche KW et al. 1997. AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO J 16:917–28
    [Google Scholar]
  43. Dell'Angelica EC, Shotelersuk V, Aguilar RC, Gahl WA, Bonifacino JS 1999b. Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the β3A subunit of the AP-3 adaptor. Mol. Cell 3:11–21
    [Google Scholar]
  44. DeMari J, Mroske C, Tang S, Nimeh J, Miller R et al. 2016. CLTC as a clinically novel gene associated with multiple malformations and developmental delay. Am. J. Med. Genet. A 170:958–66
    [Google Scholar]
  45. Denora PS, Smets K, Zolfanelli F, Ceuterick–de Groote C, Casali C et al. 2016. Motor neuron degeneration in spastic paraplegia 11 mimics amyotrophic lateral sclerosis lesions. Brain 139:1723–34
    [Google Scholar]
  46. di Ronza A, Bajaj L, Sharma J, Sanagasetti D, Lotfi P et al. 2018. CLN8 is an endoplasmic reticulum cargo receptor that regulates lysosome biogenesis. Nat. Cell Biol. 20:1370–77
    [Google Scholar]
  47. DiStasio A, Driver A, Sund K, Donlin M, Muraleedharan RM et al. 2017. Copb2 is essential for embryogenesis and hypomorphic mutations cause human microcephaly. Hum. Mol. Genet. 26:4836–48
    [Google Scholar]
  48. Dodonova SO, Diestelkoetter-Bachert P, von Appen A, Hagen WJ, Beck R et al. 2015. A structure of the COPI coat and the role of coat proteins in membrane vesicle assembly. Science 349:195–98
    [Google Scholar]
  49. Doray B, Lee I, Knisely J, Bu G, Kornfeld S 2007. The γ/σ1 and α/σ2 hemicomplexes of clathrin adaptors AP-1 and AP-2 harbor the dileucine recognition site. Mol. Biol. Cell 18:1887–96
    [Google Scholar]
  50. Edvardson S, Cinnamon Y, Ta-Shma A, Shaag A, Yim YI et al. 2012. A deleterious mutation in DNAJC6 encoding the neuronal-specific clathrin-uncoating co-chaperone auxilin, is associated with juvenile parkinsonism. PLOS ONE 7:e36458
    [Google Scholar]
  51. Elsayed LE, Drouet V, Usenko T, Mohammed IN, Hamed AA et al. 2016. A novel nonsense mutation in DNAJC6 expands the phenotype of autosomal-recessive juvenile-onset Parkinson's disease. Ann. Neurol. 79:335–37
    [Google Scholar]
  52. Espenshade P, Gimeno RE, Holzmacher E, Teung P, Kaiser CA 1995. Yeast SEC16 gene encodes a multidomain vesicle coat protein that interacts with Sec23p. J. Cell Biol. 131:311–24
    [Google Scholar]
  53. EuroEPINOMICS-RES Consortium, Epilepsy Phenome/Genome Project, Epi4K Consortium 2014. De novo mutations in synaptic transmission genes including DNM1 cause epileptic encephalopathies. Am. J. Hum. Genet. 95:360–70
    [Google Scholar]
  54. Fabrizi GM, Ferrarini M, Cavallaro T, Cabrini I, Cerini R et al. 2007. Two novel mutations in dynamin-2 cause axonal Charcot-Marie-Tooth disease. Neurology 69:291–95
    [Google Scholar]
  55. Farías GG, Cuitino L, Guo X, Ren X, Jarnik M et al. 2012. Signal-mediated, AP-1/clathrin-dependent sorting of transmembrane receptors to the somatodendritic domain of hippocampal neurons. Neuron 75:810–23
    [Google Scholar]
  56. Fellin R, Arca M, Zuliani G, Calandra S, Bertolini S 2015. The history of Autosomal Recessive Hypercholesterolemia (ARH): from clinical observations to gene identification. Gene 555:23–32
    [Google Scholar]
  57. Feng L, Seymour AB, Jiang S, To A, Peden AA et al. 1999. The β3A subunit gene (Ap3B1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky-Pudlak syndrome and night blindness. Hum. Mol. Genet. 8:323–30
    [Google Scholar]
  58. Follett J, Norwood SJ, Hamilton NA, Mohan M, Kovtun O et al. 2014. The Vps35 D620N mutation linked to Parkinson's disease disrupts the cargo sorting function of retromer. Traffic 15:230–44
    [Google Scholar]
  59. Folsch H, Ohno H, Bonifacino JS, Mellman I 1999. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99:189–98
    [Google Scholar]
  60. Fontana S, Parolini S, Vermi W, Booth S, Gallo F et al. 2006. Innate immunity defects in Hermansky-Pudlak type 2 syndrome. Blood 107:4857–64
    [Google Scholar]
  61. Fotin A, Cheng Y, Sliz P, Grigorieff N, Harrison SC et al. 2004. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432:573–79
    [Google Scholar]
  62. Gallon M, Clairfeuille T, Steinberg F, Mas C, Ghai R et al. 2014. A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. PNAS 111:E3604–13
    [Google Scholar]
  63. Garbes L, Kim K, Riess A, Hoyer-Kuhn H, Beleggia F et al. 2015. Mutations in SEC24D, encoding a component of the COPII machinery, cause a syndromic form of osteogenesis imperfecta. Am. J. Hum. Genet. 96:432–39
    [Google Scholar]
  64. Garcia CK, Wilund K, Arca M, Zuliani G, Fellin R et al. 2001. Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 292:1394–98
    [Google Scholar]
  65. Garuti R, Jones C, Li WP, Michaely P, Herz J et al. 2005. The modular adaptor protein autosomal recessive hypercholesterolemia (ARH) promotes low density lipoprotein receptor clustering into clathrin-coated pits. J. Biol. Chem. 280:40996–1004
    [Google Scholar]
  66. Ge X, Gong H, Dumas K, Litwin J, Phillips JJ et al. 2016. Missense-depleted regions in population exomes implicate Ras superfamily nucleotide-binding protein alteration in patients with brain malformation. NPJ Genom. Med. 1:16036
    [Google Scholar]
  67. Ghai R, Bugarcic A, Liu H, Norwood SJ, Skeldal S et al. 2013. Structural basis for endosomal trafficking of diverse transmembrane cargos by PX-FERM proteins. PNAS 110:E643–52
    [Google Scholar]
  68. Giehl KA, Eckstein GN, Pasternack SM, Praetzel-Wunder S, Ruzicka T et al. 2012. Nonsense mutations in AAGAB cause punctate palmoplantar keratoderma type Buschke-Fischer-Brauer. Am. J. Hum. Genet. 91:754–59
    [Google Scholar]
  69. Ginn SL, Amaya AK, Alexander IE, Edelstein M, Abedi MR 2018. Gene therapy clinical trials worldwide to 2017: an update. J. Gene Med. 20:e3015
    [Google Scholar]
  70. Gomez TS, Billadeau DD. 2009. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17:699–711
    [Google Scholar]
  71. Gorur A, Yuan L, Kenny SJ, Baba S, Xu K et al. 2017. COPII-coated membranes function as transport carriers of intracellular procollagen I. J. Cell Biol. 216:1745–59
    [Google Scholar]
  72. Gorvin CM, Metpally R, Stokes VJ, Hannan FM, Krishnamurthy SB et al. 2018. Large-scale exome datasets reveal a new class of adaptor-related protein complex 2 sigma subunit (AP2σ) mutations, located at the interface with the AP2 alpha subunit, that impair calcium-sensing receptor signalling. Hum. Mol. Genet. 27:901–11
    [Google Scholar]
  73. Gravotta D, Carvajal-Gonzalez JM, Mattera R, Deborde S, Banfelder JR et al. 2012. The clathrin adaptor AP-1A mediates basolateral polarity. Dev. Cell 22:811–23
    [Google Scholar]
  74. Guo X, Mattera R, Ren X, Chen Y, Retamal C et al. 2013. The adaptor protein-1 μ1B subunit expands the repertoire of basolateral sorting signal recognition in epithelial cells. Dev. Cell 27:353–66
    [Google Scholar]
  75. Guo Y, Zanetti G, Schekman R 2013. A novel GTP-binding protein-adaptor protein complex responsible for export of Vangl2 from the trans Golgi network. eLife 2:e00160
    [Google Scholar]
  76. Gustavsson EK, Guella I, Trinh J, Szu-Tu C, Rajput A et al. 2015. Genetic variability of the retromer cargo recognition complex in parkinsonism. Mov. Disord. 30:580–84
    [Google Scholar]
  77. Hamdan FF, Myers CT, Cossette P, Lemay P, Spiegelman D et al. 2017. High rate of recurrent de novo mutations in developmental and epileptic encephalopathies. Am. J. Hum. Genet. 101:664–85
    [Google Scholar]
  78. Hanein S, Martin E, Boukhris A, Byrne P, Goizet C et al. 2008. Identification of the SPG15 gene, encoding spastizin, as a frequent cause of complicated autosomal-recessive spastic paraplegia, including Kjellin syndrome. Am. J. Hum. Genet. 82:992–1002
    [Google Scholar]
  79. Hannan FM, Howles SA, Rogers A, Cranston T, Gorvin CM et al. 2015. Adaptor protein-2 sigma subunit mutations causing familial hypocalciuric hypercalcaemia type 3 (FHH3) demonstrate genotype-phenotype correlations, codon bias and dominant-negative effects. Hum. Mol. Genet. 24:5079–92
    [Google Scholar]
  80. Hardies K, Cai Y, Jardel C, Jansen AC, Cao M et al. 2016. Loss of SYNJ1 dual phosphatase activity leads to early onset refractory seizures and progressive neurological decline. Brain 139:2420–30
    [Google Scholar]
  81. Hase K, Nakatsu F, Ohmae M, Sugihara K, Shioda N et al. 2013. AP-1B-mediated protein sorting regulates polarity and proliferation of intestinal epithelial cells in mice. Gastroenterology 145:625–35
    [Google Scholar]
  82. He G, Gupta S, Yi M, Michaely P, Hobbs HH et al. 2002. ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin, and AP-2. J. Biol. Chem. 277:44044–49
    [Google Scholar]
  83. Heldwein EE, Macia E, Wang J, Yin HL, Kirchhausen T et al. 2004. Crystal structure of the clathrin adaptor protein 1 core. PNAS 101:14108–13
    [Google Scholar]
  84. Heuser J. 1980. Three-dimensional visualization of coated vesicle formation in fibroblasts. J. Cell Biol. 84:560–83
    [Google Scholar]
  85. Hierro A, Rojas AL, Rojas R, Murthy N, Effantin G et al. 2007. Functional architecture of the retromer cargo-recognition complex. Nature 449:1063–67
    [Google Scholar]
  86. Hirst J, Barlow LD, Francisco GC, Sahlender DA, Seaman MN et al. 2011. The fifth adaptor protein complex. PLOS Biol 9:e1001170
    [Google Scholar]
  87. Hirst J, Borner GH, Antrobus R, Peden AA, Hodson NA et al. 2012. Distinct and overlapping roles for AP-1 and GGAs revealed by the “knocksideways” system. Curr. Biol. 22:1711–16
    [Google Scholar]
  88. Hirst J, Borner GH, Edgar J, Hein MY, Mann M et al. 2013. Interaction between AP-5 and the hereditary spastic paraplegia proteins SPG11 and SPG15. Mol. Biol. Cell 24:2558–69
    [Google Scholar]
  89. Hirst J, Bright NA, Rous B, Robinson MS 1999. Characterization of a fourth adaptor-related protein complex. Mol. Biol. Cell 10:2787–802
    [Google Scholar]
  90. Hirst J, Edgar JR, Esteves T, Darios F, Madeo M et al. 2015. Loss of AP-5 results in accumulation of aberrant endolysosomes: defining a new type of lysosomal storage disease. Hum. Mol. Genet. 24:4984–96
    [Google Scholar]
  91. Hirst J, Itzhak DN, Antrobus R, Borner GHH, Robinson MS 2018. Role of the AP-5 adaptor protein complex in late endosome-to-Golgi retrieval. PLOS Biol 16:e2004411
    [Google Scholar]
  92. Holmes SE, Riazi MA, Gong W, McDermid HE, Sellinger BT et al. 1997. Disruption of the clathrin heavy chain–like gene (CLTCL) associated with features of DGS/VCFS: a balanced (21;22)(p12;q11) translocation. Hum. Mol. Genet. 6:357–67
    [Google Scholar]
  93. Hood FE, Royle SJ. 2009. Functional equivalence of the clathrin heavy chains CHC17 and CHC22 in endocytosis and mitosis. J. Cell Sci. 122:2185–90
    [Google Scholar]
  94. Hoopes RR, Shrimpton AE, Knohl SJ, Hueber P, Hoppe B et al. 2005. Dent disease with mutations in OCRL1. Am. J. Hum. Genet 76:260–67
    [Google Scholar]
  95. Huizing M, Helip-Wooley A, Westbroek W, Gunay-Aygun M, Gahl WA 2008. Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics. Annu. Rev. Genom. Hum. Genet. 9:359–86
    [Google Scholar]
  96. Huizing M, Sarangarajan R, Strovel E, Zhao Y, Gahl WA et al. 2001. AP-3 mediates tyrosinase but not TRP-1 trafficking in human melanocytes. Mol. Biol. Cell 12:2075–85
    [Google Scholar]
  97. Hutchings J, Stancheva V, Miller EA, Zanetti G 2018. Subtomogram averaging of COPII assemblies reveals how coat organization dictates membrane shape. Nat. Commun. 9:4154
    [Google Scholar]
  98. Incecik F, Bisgin A, Yılmaz M 2018. MEDNIK syndrome with a frame shift causing mutation in AP1S1 gene and literature review of the clinical features. Metab. Brain Dis. 33:2065–68
    [Google Scholar]
  99. Ivankovic D, Drew J, Lesept F, White IJ, López Doménech G 2019. Axonal autophagosome maturation defect through failure of ATG9A sorting underpins pathology in AP-4 deficiency syndrome. Autophagy https://doi.org/10.1080/15548627.2019.1615302
    [Crossref] [Google Scholar]
  100. Izumi K, Brett M, Nishi E, Drunat S, Tan ES et al. 2016. ARCN1 mutations cause a recognizable craniofacial syndrome due to COPI-mediated transport defects. Am. J. Hum. Genet. 99:451–59
    [Google Scholar]
  101. Jackson AP, Seow HF, Holmes N, Drickamer K, Parham P 1987. Clathrin light chains contain brain-specific insertion sequences and a region of homology with intermediate filaments. Nature 326:154–59
    [Google Scholar]
  102. Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC et al. 2010. A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141:1220–29
    [Google Scholar]
  103. Jackson LP, Lewis M, Kent HM, Edeling MA, Evans PR et al. 2012. Molecular basis for recognition of dilysine trafficking motifs by COPI. Dev. Cell 23:1255–62
    [Google Scholar]
  104. Janvier K, Kato Y, Boehm M, Rose JR, Martina JA et al. 2003. Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 γ-σ1 and AP-3 δ-σ3 hemicomplexes. J. Cell Biol. 163:1281–90
    [Google Scholar]
  105. Jensson BO, Hansdottir S, Arnadottir GA, Sulem G, Kristjansson RP et al. 2017. COPA syndrome in an Icelandic family caused by a recurrent missense mutation in COPA. BMC Med. Genet 18:129
    [Google Scholar]
  106. Jia X, Weber E, Tokarev A, Lewinski M, Rizk M et al. 2014. Structural basis of HIV-1 Vpu-mediated BST2 antagonism via hijacking of the clathrin adaptor protein complex 1. eLife 3:e02362
    [Google Scholar]
  107. Jones B, Jones EL, Bonney SA, Patel HN, Mensenkamp AR et al. 2003. Mutations in a Sar1 GTPase of COPII vesicles are associated with lipid absorption disorders. Nat. Genet. 34:29–31
    [Google Scholar]
  108. Kantheti P, Qiao X, Diaz ME, Peden AA, Meyer GE et al. 1998. Mutation in AP-3 δ in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21:111–22
    [Google Scholar]
  109. Karampini E, Schillemans M, Hofman M, van Alphen F, de Boer M et al. 2019. Defective AP-3-dependent VAMP8 trafficking impairs Weibel-Palade body exocytosis in Hermansky-Pudlak Syndrome type 2 blood outgrowth endothelial cells. Haematologica haematol.2018.207787 . https://doi.org/10.3324/haematol.2018.207787
    [Crossref] [Google Scholar]
  110. Kelly BT, Graham SC, Liska N, Dannhauser PN, Höning S et al. 2014. AP2 controls clathrin polymerization with a membrane-activated switch. Science 345:459–63
    [Google Scholar]
  111. Kelly BT, McCoy AJ, Späte K, Miller SE, Evans PR et al. 2008. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456:976–79
    [Google Scholar]
  112. Khoriaty R, Hesketh GG, Bernard A, Weyand AC, Mellacheruvu D et al. 2018. Functions of the COPII gene paralogs SEC23A and SEC23B are interchangeable in vivo. PNAS 115:E7748–57
    [Google Scholar]
  113. Khoriaty R, Vasievich MP, Jones M, Everett L, Chase J et al. 2014. Absence of a red blood cell phenotype in mice with hematopoietic deficiency of SEC23B. Mol. Cell. Biol. 34:3721–34
    [Google Scholar]
  114. Khundadze M, Kollmann K, Koch N, Biskup C, Nietzsche S et al. 2013. A hereditary spastic paraplegia mouse model supports a role of ZFYVE26/SPASTIZIN for the endolysosomal system. PLOS Genet 9:e1003988
    [Google Scholar]
  115. Kirchhausen T, Owen D, Harrison SC 2014. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb. Perspect. Biol. 6:a016725
    [Google Scholar]
  116. Korogi Y, Gotoh S, Ikeo S, Yamamoto Y, Sone N et al. 2019. In vitro disease modeling of Hermansky-Pudlak syndrome type 2 using human induced pluripotent stem cell–derived alveolar organoids. Stem Cell Rep 12:431–40
    [Google Scholar]
  117. Koutsopoulos OS, Kretz C, Weller CM, Roux A, Mojzisova H et al. 2013. Dynamin 2 homozygous mutation in humans with a lethal congenital syndrome. Eur. J. Hum. Genet. 21:637–42
    [Google Scholar]
  118. Kovtun O, Leneva N, Bykov YS, Ariotti N, Teasdale RD et al. 2018. Structure of the membrane-assembled retromer coat determined by cryo-electron tomography. Nature 561:561–64
    [Google Scholar]
  119. Krebs CE, Karkheiran S, Powell JC, Cao M, Makarov V et al. 2013. The Sac1 domain of SYNJ1 identified mutated in a family with early-onset progressive Parkinsonism with generalized seizures. Hum. Mutat. 34:1200–7
    [Google Scholar]
  120. Kurokawa K, Okamoto M, Nakano A 2014. Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER. Nat. Commun. 5:3653
    [Google Scholar]
  121. Le Borgne R, Alconada A, Bauer U, Hoflack B 1998. The mammalian AP-3 adaptor-like complex mediates the intracellular transport of lysosomal membrane glycoproteins. J. Biol. Chem. 273:29451–61
    [Google Scholar]
  122. Lee JJ, Radice G, Perkins CP, Costantini F 1992. Identification and characterization of a novel, evolutionarily conserved gene disrupted by the murine H beta 58 embryonic lethal transgene insertion. Development 115:277–88
    [Google Scholar]
  123. Lee JY, Shoback DM. 2018. Familial hypocalciuric hypercalcemia and related disorders. Best Pract. Res. Clin. Endocrinol. Metab. 32:609–19
    [Google Scholar]
  124. Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E 2016. Analysis of protein-coding genetic variation in 60,706 humans. Nature 536:285–91
    [Google Scholar]
  125. Lewis MJ, Pelham HR. 1990. A human homologue of the yeast HDEL receptor. Nature 348:162–63
    [Google Scholar]
  126. Li W, Puertollano-Moro R, Bonifacino J, Overbeek P, Everett E 2010. Disruption of the murine Ap2b1 gene causes nonsyndromic cleft palate. Cleft Palate Craniofac. J. 47:566–73
    [Google Scholar]
  127. Liu L, Doray B, Kornfeld S 2018. Recycling of Golgi glycosyltransferases requires direct binding to coatomer. PNAS 115:8984–89
    [Google Scholar]
  128. Liu SH, Towler MC, Chen E, Chen CY, Song W et al. 2001. A novel clathrin homolog that co-distributes with cytoskeletal components functions in the trans-Golgi network. EMBO J 20:272–84
    [Google Scholar]
  129. Lorenzi L, Tabellini G, Vermi W, Moratto D, Porta F 2013. Occurrence of nodular lymphocyte–predominant Hodgkin lymphoma in Hermansky-Pudlak type 2 syndrome is associated to natural killer and natural killer T cell defects. PLOS ONE 8:e80131
    [Google Scholar]
  130. Lucas M, Gershlick DC, Vidaurrazaga A, Rojas AL, Bonifacino JS et al. 2016. Structural mechanism for cargo recognition by the retromer complex. Cell 167:1623–35.e14
    [Google Scholar]
  131. Lunn ML, Nassirpour R, Arrabit C, Tan J, McLeod I et al. 2007. A unique sorting nexin regulates trafficking of potassium channels via a PDZ domain interaction. Nat. Neurosci. 10:1249–59
    [Google Scholar]
  132. Ma W, Goldberg J. 2013. Rules for the recognition of dilysine retrieval motifs by coatomer. EMBO J 32:926–37
    [Google Scholar]
  133. Ma W, Goldberg J. 2016. TANGO1/cTAGE5 receptor as a polyvalent template for assembly of large COPII coats. PNAS 113:10061–66
    [Google Scholar]
  134. Mahil SK, Twelves S, Farkas K, Setta-Kaffetzi N, Burden AD et al. 2016. AP1S3 mutations cause skin autoinflammation by disrupting keratinocyte autophagy and up-regulating IL-36 production. J. Investig. Dermatol. 136:2251–59
    [Google Scholar]
  135. Majoul I, Sohn K, Wieland FT, Pepperkok R, Pizza M et al. 1998. KDEL receptor (Erd2p)-mediated retrograde transport of the cholera toxin A subunit from the Golgi involves COPI, p23, and the COOH terminus of Erd2p. J. Cell Biol. 143:601–12
    [Google Scholar]
  136. Mancias JD, Goldberg J. 2008. Structural basis of cargo membrane protein discrimination by the human COPII coat machinery. EMBO J 27:2918–28
    [Google Scholar]
  137. Mardones GA, Burgos PV, Lin Y, Kloer DP, Magadan JG et al. 2013. Structural basis for the recognition of tyrosine-based sorting signals by the μ3A subunit of the AP-3 adaptor complex. J. Biol. Chem. 288:9563–71
    [Google Scholar]
  138. Martinelli D, Travaglini L, Drouin CA, Ceballos-Picot I, Rizza T et al. 2013. MEDNIK syndrome: a novel defect of copper metabolism treatable by zinc acetate therapy. Brain 136:872–81
    [Google Scholar]
  139. Matsuda S, Miura E, Matsuda K, Kakegawa W, Kohda K et al. 2008. Accumulation of AMPA receptors in autophagosomes in neuronal axons lacking adaptor protein AP-4. Neuron 57:730–45
    [Google Scholar]
  140. Mattera R, Boehm M, Chaudhuri R, Prabhu Y, Bonifacino JS 2011. Conservation and diversification of dileucine signal recognition by adaptor protein (AP) complex variants. J. Biol. Chem. 286:2022–30
    [Google Scholar]
  141. Mattera R, Farias GG, Mardones GA, Bonifacino JS 2014. Co-assembly of viral envelope glycoproteins regulates their polarized sorting in neurons. PLOS Pathog 10:e1004107
    [Google Scholar]
  142. Mattera R, Park SY, De Pace R, Guardia CM, Bonifacino JS 2017. AP-4 mediates export of ATG9A from the trans-Golgi network to promote autophagosome formation. PNAS 114:E10697–706
    [Google Scholar]
  143. McCaughey J, Stevenson NL, Cross S, Stephens DJ 2019. ER-to-Golgi trafficking of procollagen in the absence of large carriers. J. Cell Biol. 218:929–48
    [Google Scholar]
  144. McGough IJ, Steinberg F, Jia D, Barbuti PA, McMillan KJ et al. 2014. Retromer binding to FAM21 and the WASH complex is perturbed by the Parkinson disease–linked VPS35(D620N) mutation. Curr. Biol. 24:1670–76
    [Google Scholar]
  145. McMillan KJ, Gallon M, Jellett AP, Clairfeuille T, Tilley FC et al. 2016. Atypical parkinsonism-associated retromer mutant alters endosomal sorting of specific cargo proteins. J. Cell Biol. 214:389–99
    [Google Scholar]
  146. Meng R, Wang Y, Yao Y, Zhang Z, Harper DC et al. 2012. SLC35D3 delivery from megakaryocyte early endosomes is required for platelet dense granule biogenesis and is differentially defective in Hermansky-Pudlak syndrome models. Blood 120:404–14
    [Google Scholar]
  147. Meyer C, Zizioli D, Lausmann S, Eskelinen EL, Hamann J et al. 2000. μ1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J 19:2193–203
    [Google Scholar]
  148. Miller EA, Beilharz TH, Malkus PN, Lee MC, Hamamoto S et al. 2003. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114:497–509
    [Google Scholar]
  149. Miller EA, Schekman R. 2013. COPII: a flexible vesicle formation system. Curr. Opin. Cell Biol. 25:420–27
    [Google Scholar]
  150. Mir R, Tonelli F, Lis P, Macartney T, Polinski NK et al. 2018. The Parkinson's disease VPS35[D620N] mutation enhances LRRK2-mediated Rab protein phosphorylation in mouse and human. Biochem. J. 475:1861–83
    [Google Scholar]
  151. Mironov AA, Beznoussenko GV, Trucco A, Lupetti P, Smith JD et al. 2003. ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev. Cell 5:583–94
    [Google Scholar]
  152. Mishra SK, Watkins SC, Traub LM 2002. The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. PNAS 99:16099–104
    [Google Scholar]
  153. Mitsunari T, Nakatsu F, Shioda N, Love PE, Grinberg A et al. 2005. Clathrin adaptor AP-2 is essential for early embryonal development. Mol. Cell. Biol. 25:9318–23
    [Google Scholar]
  154. Mohammed M, Al-Hashmi N, Al-Rashdi S, Al-Sukaiti N, Al-Adawi K et al. 2018. Biallelic mutations in AP3D1 cause Hermansky-Pudlak syndrome type 10 associated with immunodeficiency and seizure disorder. Eur. J. Med. Genet. In press . https://doi.org/10.1016/j.ejmg.2018.11.017
    [Crossref] [Google Scholar]
  155. Montecchiani C, Pedace L, Lo Giudice T, Casella A, Mearini M et al. 2016. ALS5/SPG11/KIAA1840 mutations cause autosomal recessive axonal Charcot-Marie-Tooth disease. Brain 139:73–85
    [Google Scholar]
  156. Montpetit A, Cote S, Brustein E, Drouin CA, Lapointe L et al. 2008. Disruption of AP1S1, causing a novel neurocutaneous syndrome, perturbs development of the skin and spinal cord. PLOS Genet 4:e1000296
    [Google Scholar]
  157. Moravec R, Conger KK, D'Souza R, Allison AB, Casanova JE 2012. BRAG2/GEP100/IQSec1 interacts with clathrin and regulates α5β1 integrin endocytosis through activation of ADP ribosylation factor 5 (Arf5). J. Biol. Chem. 287:31138–47
    [Google Scholar]
  158. Moreno-De-Luca A, Helmers SL, Mao H, Burns TG, Melton AM et al. 2011. Adaptor protein complex-4 (AP-4) deficiency causes a novel autosomal recessive cerebral palsy syndrome with microcephaly and intellectual disability. J. Med. Genet. 48:141–44
    [Google Scholar]
  159. Morrow BE, McDonald-McGinn DM, Emanuel BS, Vermeesch JR, Scambler PJ 2018. Molecular genetics of 22q11.2 deletion syndrome. Am. J. Med. Genet. A 176:2070–81
    [Google Scholar]
  160. Mossessova E, Bickford LC, Goldberg J 2003. SNARE selectivity of the COPII coat. Cell 114:483–95
    [Google Scholar]
  161. Munsie LN, Milnerwood AJ, Seibler P, Beccano-Kelly DA, Tatarnikov I et al. 2015. Retromer-dependent neurotransmitter receptor trafficking to synapses is altered by the Parkinson's disease VPS35 mutation p.D620N. Hum. Mol. Genet. 24:1691–703
    [Google Scholar]
  162. Nahorski MS, Al-Gazali L, Hertecant J, Owen DJ, Borner GH et al. 2015. A novel disorder reveals clathrin heavy chain-22 is essential for human pain and touch development. Brain 138:2147–60
    [Google Scholar]
  163. Navarro Negredo P, Edgar JR, Wrobel AG, Zaccai NR, Antrobus R et al. 2017. Contribution of the clathrin adaptor AP-1 subunit μ1 to acidic cluster protein sorting. J. Cell Biol. 216:2927–43
    [Google Scholar]
  164. Nesbit MA, Hannan FM, Howles SA, Reed AA, Cranston T et al. 2013. Mutations in AP2S1 cause familial hypocalciuric hypercalcemia type 3. Nat. Genet. 45:93–97
    [Google Scholar]
  165. Newell-Litwa K, Salazar G, Smith Y, Faundez V 2009. Roles of BLOC-1 and adaptor protein-3 complexes in cargo sorting to synaptic vesicles. Mol. Biol. Cell 20:1441–53
    [Google Scholar]
  166. Newman LS, McKeever MO, Okano HJ, Darnell RB 1995. β-NAP, a cerebellar degeneration antigen, is a neuron-specific vesicle coat protein. Cell 82:773–83
    [Google Scholar]
  167. Noorelahi R, Perez G, Otero HJ 2018. Imaging findings of Copa syndrome in a 12-year-old boy. Pediatr. Radiol 48:279–82
    [Google Scholar]
  168. Ohno H, Fournier MC, Poy G, Bonifacino JS 1996. Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains. J. Biol. Chem. 271:29009–15
    [Google Scholar]
  169. Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I et al. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269:1872–75
    [Google Scholar]
  170. Ohno H, Tomemori T, Nakatsu F, Okazaki Y, Aguilar RC et al. 1999. μ1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett 449:215–20
    [Google Scholar]
  171. Ooi CE, Dell'Angelica EC, Bonifacino JS 1998. ADP-ribosylation factor 1 (ARF1) regulates recruitment of the AP-3 adaptor complex to membranes. J. Cell Biol. 142:391–402
    [Google Scholar]
  172. Orlacchio A, Babalini C, Borreca A, Patrono C, Massa R et al. 2010. SPATACSIN mutations cause autosomal recessive juvenile amyotrophic lateral sclerosis. Brain 133:591–98
    [Google Scholar]
  173. Owen DJ, Evans PR. 1998. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282:1327–32
    [Google Scholar]
  174. Pearse BM. 1975. Coated vesicles from pig brain: purification and biochemical characterization. J. Mol. Biol. 97:93–98
    [Google Scholar]
  175. Pearse BM, Robinson MS. 1984. Purification and properties of 100-kd proteins from coated vesicles and their reconstitution with clathrin. EMBO J 3:1951–57
    [Google Scholar]
  176. Peden AA, Oorschot V, Hesser BA, Austin CD, Scheller RH et al. 2004. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 164:1065–76
    [Google Scholar]
  177. Peden AA, Rudge RE, Lui WW, Robinson MS 2002. Assembly and function of AP-3 complexes in cells expressing mutant subunits. J. Cell Biol. 156:327–36
    [Google Scholar]
  178. Pickrell AM, Youle RJ. 2015. The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron 85:257–73
    [Google Scholar]
  179. Pohler E, Mamai O, Hirst J, Zamiri M, Horn H et al. 2012. Haploinsufficiency for AAGAB causes clinically heterogeneous forms of punctate palmoplantar keratoderma. Nat. Genet. 44:1272–76
    [Google Scholar]
  180. Polishchuk RS, San Pietro E, Di Pentima A, Tete S, Bonifacino JS 2006. Ultrastructure of long-range transport carriers moving from the trans Golgi network to peripheral endosomes. Traffic 7:1092–103
    [Google Scholar]
  181. Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ et al. 1997. ER-to-Golgi transport visualized in living cells. Nature 389:81–85
    [Google Scholar]
  182. Quadri M, Fang M, Picillo M, Olgiati S, Breedveld GJ et al. 2013. Mutation in the SYNJ1 gene associated with autosomal recessive, early-onset Parkinsonism. Hum. Mutat. 34:1208–15
    [Google Scholar]
  183. Raza MH, Mattera R, Morell R, Sainz E, Rahn R et al. 2015. Association between rare variants in AP4E1, a component of intracellular trafficking, and persistent stuttering. Am. J. Hum. Genet. 97:715–25
    [Google Scholar]
  184. Ren X, Farias GG, Canagarajah BJ, Bonifacino JS, Hurley JH 2013. Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1. Cell 152:755–67
    [Google Scholar]
  185. Renvoisé B, Chang J, Singh R, Yonekawa S, FitzGibbon EJ et al. 2014. Lysosomal abnormalities in hereditary spastic paraplegia types SPG15 and SPG11. Ann. Clin. Transl. Neurol. 1:379–89
    [Google Scholar]
  186. Robinson MS. 2015. Forty years of clathrin-coated vesicles. Traffic 16:1210–38
    [Google Scholar]
  187. Rojas R, van Vlijmen T, Mardones GA, Prabhu Y, Rojas AL et al. 2008. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183:513–26
    [Google Scholar]
  188. Roth TF, Porter KR. 1964. Yolk protein uptake in the oocyte of the mosquito Aedes aegypti. J. Cell Biol 20:313–32
    [Google Scholar]
  189. Rout MP, Field MC. 2017. The evolution of organellar coat complexes and organization of the eukaryotic cell. Annu. Rev. Biochem. 86:637–57
    [Google Scholar]
  190. Saba TG, Montpetit A, Verner A, Rioux P, Hudson TJ et al. 2005. An atypical form of erythrokeratodermia variabilis maps to chromosome 7q22. Hum. Genet. 116:167–71
    [Google Scholar]
  191. Saillour Y, Zanni G, Des Portes V, Heron D, Guibaud L et al. 2007. Mutations in the AP1S2 gene encoding the sigma 2 subunit of the adaptor protein 1 complex are associated with syndromic X–linked mental retardation with hydrocephalus and calcifications in basal ganglia. J. Med. Genet. 44:739–44
    [Google Scholar]
  192. Saito K, Chen M, Bard F, Chen S, Zhou H et al. 2009. TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136:891–902
    [Google Scholar]
  193. Saito K, Yamashiro K, Ichikawa Y, Erlmann P, Kontani K et al. 2011. cTAGE5 mediates collagen secretion through interaction with TANGO1 at endoplasmic reticulum exit sites. Mol. Biol. Cell 22:2301–8
    [Google Scholar]
  194. Sato K, Sato M, Nakano A 2001. Rer1p, a retrieval receptor for endoplasmic reticulum membrane proteins, is dynamically localized to the Golgi apparatus by coatomer. J. Cell Biol. 152:935–44
    [Google Scholar]
  195. Schaletzki Y, Kromrey ML, Bröderdorf S, Hammer E, Grube M et al. 2017. Several adaptor proteins promote intracellular localisation of the transporter MRP4/ABCC4 in platelets and haematopoietic cells. Thromb. Haemost. 117:105–15
    [Google Scholar]
  196. Schwarz K, Iolascon A, Verissimo F, Trede NS, Horsley W et al. 2009. Mutations affecting the secretory COPII coat component SEC23B cause congenital dyserythropoietic anemia type II. Nat. Genet. 41:936–40
    [Google Scholar]
  197. Seaman MN. 2004. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165:111–22
    [Google Scholar]
  198. Seaman MN. 2007. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J. Cell Sci. 120:2378–89
    [Google Scholar]
  199. Seaman MN. 2012. The retromer complex: endosomal protein recycling and beyond. J. Cell Sci. 125:4693–702
    [Google Scholar]
  200. Seaman MN, Harbour ME, Tattersall D, Read E, Bright N 2009. Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J. Cell Sci. 122:2371–82
    [Google Scholar]
  201. Serafini T, Orci L, Amherdt M, Brunner M, Kahn RA et al. 1991. ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell 67:239–53
    [Google Scholar]
  202. Setta-Kaffetzi N, Simpson MA, Navarini AA, Patel VM, Lu HC et al. 2014. AP1S3 mutations are associated with pustular psoriasis and impaired Toll-like receptor 3 trafficking. Am. J. Hum. Genet. 94:790–97
    [Google Scholar]
  203. Sheen VL, Ganesh VS, Topcu M, Sebire G, Bodell A et al. 2004. Mutations in ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex. Nat. Genet. 36:69–76
    [Google Scholar]
  204. Shen QT, Ren X, Zhang R, Lee IH, Hurley JH 2015. HIV-1 Nef hijacks clathrin coats by stabilizing AP-1:Arf1 polygons. Science 350:aac5137
    [Google Scholar]
  205. Shi H, Rojas R, Bonifacino JS, Hurley JH 2006. The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat. Struct. Mol. Biol. 13:540–48
    [Google Scholar]
  206. Shotelersuk V, Dell'Angelica EC, Hartnell L, Bonifacino JS, Gahl WA 2000. A new variant of Hermansky-Pudlak syndrome due to mutations in a gene responsible for vesicle formation. Am. J. Med. 108:423–27
    [Google Scholar]
  207. Silvain M, Bligny D, Aparicio T, Laforêt P, Grodet A et al. 2008. Anderson's disease (chylomicron retention disease): a new mutation in the SARA2 gene associated with muscular and cardiac abnormalities. Clin. Genet. 74:546–52
    [Google Scholar]
  208. Simpson F, Peden AA, Christopoulou L, Robinson MS 1997. Characterization of the adaptor-related protein complex, AP-3. J. Cell Biol. 137:835–45
    [Google Scholar]
  209. Singh R, Stoneham C, Lim C, Jia X, Guenaga J et al. 2018. Phosphoserine acidic cluster motifs bind distinct basic regions on the μ subunits of clathrin adaptor protein complexes. J. Biol. Chem. 293:15678–90
    [Google Scholar]
  210. Sirinian MI, Belleudi F, Campagna F, Ceridono M, Garofalo T et al. 2005. Adaptor protein ARH is recruited to the plasma membrane by low density lipoprotein (LDL) binding and modulates endocytosis of the LDL/LDL receptor complex in hepatocytes. J. Biol. Chem. 280:38416–23
    [Google Scholar]
  211. Sirkis DW, Edwards RH, Asensio CS 2013. Widespread dysregulation of peptide hormone release in mice lacking adaptor protein AP-3. PLOS Genet 9:e1003812
    [Google Scholar]
  212. Slabicki M, Theis M, Krastev DB, Samsonov S, Mundwiller E et al. 2010. A genome-scale DNA repair RNAi screen identifies SPG48 as a novel gene associated with hereditary spastic paraplegia. PLOS Biol 8:e1000408
    [Google Scholar]
  213. Steinberg F, Gallon M, Winfield M, Thomas EC, Bell AJ et al. 2013. A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat. Cell Biol. 15:461–71
    [Google Scholar]
  214. Stephens DJ, Pepperkok R. 2002. Imaging of procollagen transport reveals COPI-dependent cargo sorting during ER-to-Golgi transport in mammalian cells. J. Cell Sci. 115:1149–60
    [Google Scholar]
  215. Stevanin G, Santorelli FM, Azzedine H, Coutinho P, Chomilier J et al. 2007. Mutations in SPG11, encoding spatacsin, are a major cause of spastic paraplegia with thin corpus callosum. Nat. Genet. 39:366–72
    [Google Scholar]
  216. Strochlic TI, Setty TG, Sitaram A, Burd CG 2007. Grd19/Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling. J. Cell Biol. 177:115–25
    [Google Scholar]
  217. Tarpey PS, Stevens C, Teague J, Edkins S, O'Meara S 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. 79:1119–24
    [Google Scholar]
  218. Taveira-DaSilva AM, Markello TC, Kleiner DE, Jones AM, Groden C et al. 2018. Expanding the phenotype of COPA syndrome: a kindred with typical and atypical features. J. Med. Genet. https://doi.org/10.1136/jmedgenet-2018-105560
    [Crossref] [Google Scholar]
  219. Temkin P, Lauffer B, Jäger S, Cimermancic P, Krogan NJ et al. 2011. SNX27 mediates retromer tubule entry and endosome–to–plasma membrane trafficking of signalling receptors. Nat. Cell Biol. 13:715–21
    [Google Scholar]
  220. Theos AC, Tenza D, Martina JA, Hurbain I, Peden AA et al. 2005. Functions of adaptor protein (AP)-3 and AP-1 in tyrosinase sorting from endosomes to melanosomes. Mol. Biol. Cell 16:5356–72
    [Google Scholar]
  221. Ungewickell E, Branton D. 1981. Assembly units of clathrin coats. Nature 289:420–22
    [Google Scholar]
  222. Varga RE, Khundadze M, Damme M, Nietzsche S, Hoffmann B et al. 2015. In vivo evidence for lysosome depletion and impaired autophagic clearance in hereditary spastic paraplegia type SPG11. PLOS Genet 11:e1005454
    [Google Scholar]
  223. Vassilopoulos S, Esk C, Hoshino S, Funke BH, Chen CY et al. 2009. A role for the CHC22 clathrin heavy-chain isoform in human glucose metabolism. Science 324:1192–96
    [Google Scholar]
  224. Verkerk AJ, Schot R, Dumee B, Schellekens K, Swagemakers S et al. 2009. Mutation in the AP4M1 gene provides a model for neuroaxonal injury in cerebral palsy. Am. J. Hum. Genet. 85:40–52
    [Google Scholar]
  225. Vilariño-Güell C, Wider C, Ross OA, Dachsel JC, Kachergus JM et al. 2011. VPS35 mutations in Parkinson disease. Am. J. Hum. Genet. 89:162–67
    [Google Scholar]
  226. Volpi S, Tsui J, Mariani M, Pastorino C, Caorsi R et al. 2018. Type I interferon pathway activation in COPA syndrome. Clin. Immunol. 187:33–36
    [Google Scholar]
  227. Wang W, Wang X, Fujioka H, Hoppel C, Whone AL et al. 2016. Parkinson's disease–associated mutant VPS35 causes mitochondrial dysfunction by recycling DLP1 complexes. Nat. Med. 22:54–63
    [Google Scholar]
  228. Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX et al. 2003. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114:299–310
    [Google Scholar]
  229. Waters MG, Serafini T, Rothman JE 1991. ‘Coatomer’: a cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature 349:248–51
    [Google Scholar]
  230. Watkin LB, Jessen B, Wiszniewski W, Vece TJ, Jan M et al. 2015. COPA mutations impair ER-Golgi transport and cause hereditary autoimmune-mediated lung disease and arthritis. Nat. Genet. 47:654–60
    [Google Scholar]
  231. Wienert B, Martyn GE, Funnell APW, Quinlan KGR, Crossley M 2018. Wake-up sleepy gene: reactivating fetal globin for β-hemoglobinopathies. Trends Genet 34:927–40
    [Google Scholar]
  232. Wong JKL, Gui H, Kwok M, Ng PW, Lui CHT et al. 2018. Rare variants and de novo variants in mesial temporal lobe epilepsy with hippocampal sclerosis. Neurol. Genet. 4:e245
    [Google Scholar]
  233. Yang W, Li C, Ward DM, Kaplan J, Mansour SL 2000. Defective organellar membrane protein trafficking in Ap3b1-deficient cells. J. Cell Sci. 113:4077–86
    [Google Scholar]
  234. Yang XY, Zhou XY, Wang QQ, Li H, Chen Y et al. 2013. Mutations in the COPII vesicle component gene SEC24B are associated with human neural tube defects. Hum. Mutat. 34:1094–101
    [Google Scholar]
  235. Yap CC, Murate M, Kishigami S, Muto Y, Kishida H et al. 2003. Adaptor protein complex-4 (AP-4) is expressed in the central nervous system neurons and interacts with glutamate receptor delta2. Mol. Cell. Neurosci. 24:283–95
    [Google Scholar]
  236. Yehia L, Niazi F, Ni Y, Ngeow J, Sankunny M et al. 2015. Germline heterozygous variants in SEC23B are associated with Cowden syndrome and enriched in apparently sporadic thyroid cancer. Am. J. Hum. Genet. 97:661–76
    [Google Scholar]
  237. Yu X, Breitman M, Goldberg J 2012. A structure-based mechanism for Arf1-dependent recruitment of coatomer to membranes. Cell 148:530–42
    [Google Scholar]
  238. Zanetti G, Prinz S, Daum S, Meister A, Schekman R et al. 2013. The structure of the COPII transport-vesicle coat assembled on membranes. eLife 2:e00951
    [Google Scholar]
  239. Zavodszky E, Seaman MN, Moreau K, Jimenez-Sanchez M, Breusegem SY et al. 2014. Mutation in VPS35 associated with Parkinson's disease impairs WASH complex association and inhibits autophagy. Nat. Commun. 5:3828
    [Google Scholar]
  240. Zerangue N, Malan MJ, Fried SR, Dazin PF, Jan YN et al. 2001. Analysis of endoplasmic reticulum trafficking signals by combinatorial screening in mammalian cells. PNAS 98:2431–36
    [Google Scholar]
  241. Zimprich A, Benet-Pages A, Struhal W, Graf E, Eck SH et al. 2011. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am. J. Hum. Genet. 89:168–75
    [Google Scholar]
  242. Zizioli D, Meyer C, Guhde G, Saftig P, von Figura K et al. 1999. Early embryonic death of mice deficient in γ-adaptin. J. Biol. Chem. 274:5385–90
    [Google Scholar]
  243. Zlatic SA, Grossniklaus EJ, Ryder PV, Salazar G, Mattheyses AL et al. 2013. Chemical-genetic disruption of clathrin function spares adaptor complex 3–dependent endosome vesicle biogenesis. Mol. Biol. Cell 24:2378–88
    [Google Scholar]
  244. Züchner S, Noureddine M, Kennerson M, Verhoeven K, Claeys K et al. 2005. Mutations in the pleckstrin homology domain of dynamin 2 cause dominant intermediate Charcot-Marie-Tooth disease. Nat. Genet. 37:289–94
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100818-125234
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