Role of the AP-5 adaptor protein complex in late endosome-to-Golgi retrieval

PLoS Biology

Volumn 16, Issue 1, 2018, Pages

  Hirst, Jennifer ^a   Itzhak, Daniel N ^b   Antrobus, Robin ^a   Borner, Georg H H ^b   Robinson, Margaret S ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; CATION INDEPENDENT MANNOSE 6 PHOSPHATE RECEPTOR; PROTEIN AP 5; PROTEIN GOLIM1; PROTEIN GOLIM4; PROTEIN SPG11; PROTEIN SPG15; RECEPTOR; SORTILIN; UNCLASSIFIED DRUG; AP5B1 PROTEIN, HUMAN; GOLIM4 PROTEIN, HUMAN; GOLM1 PROTEIN, HUMAN; MEMBRANE PROTEIN; VESICULAR TRANSPORT ADAPTOR PROTEIN; VESICULAR TRANSPORT PROTEIN;

AP5Z1 GENE; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; CRISPR-CAS9 SYSTEM; ENDOSOME; GENE; GOLGI COMPLEX; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; MASS SPECTROMETRY; MUTATIONAL ANALYSIS; PHENOTYPE; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; STEADY STATE; CRISPR CAS SYSTEM; GENETICS; HEREDITARY MOTOR SENSORY NEUROPATHY; LYSOSOME; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; CRISPR-CAS SYSTEMS; ENDOSOMES; GOLGI APPARATUS; HELA CELLS; HUMANS; LYSOSOMES; MASS SPECTROMETRY; MEMBRANE PROTEINS; PHENOTYPE; PROTEIN TRANSPORT; SPASTIC PARAPLEGIA, HEREDITARY; VESICULAR TRANSPORT PROTEINS;

EID: 85041376087     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.2004411     Document Type: Article

References (62)

1. Robinson MS, (2015) Forty years of clathrin-coated vesicles. Traffic16: 1210–1238. doi: 10.1111/tra.12335 26403691
2. Hirst J, Barlow LD, Francisco GC, Sahlender DA, Seaman MNJ, et al. (2011) The fifth adaptor protein complex. PLoS Biol9: e1001170. doi: 10.1371/journal.pbio.1001170 22022230
3. Hirst J, Borner GHH, Edgar J, Hein MY, Mann M, et al. (2013) Interaction between AP-5 and the hereditary spastic paraplegia proteins SPG11 and SPG15. Mol Biol Cell24: 2558–2569. doi: 10.1091/mbc.E13-03-0170 23825025
4. Hein MY, Hubner NC, Poser I, Cox J, Nagaraj N, et al. (2015) A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell163: 712–723. doi: 10.1016/j.cell.2015.09.053 26496610
5. Itzhak DN, Tyanova S, Cox J, Borner GHH, (2016) Global, quantitative and dynamic mapping of protein subcellular localization. eLife5: e16950. doi: 10.7554/eLife.16950 27278775
6. Hirst J, Irving C, Borner GHH, (2013) Adaptor protein complexes AP-4 and AP-5: new players in endosomal trafficking and progressive spastic paraplegia. Traffic14: 153–164. doi: 10.1111/tra.12028 23167973
7. Słabicki 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 Biol8: e1000408. doi: 10.1371/journal.pbio.1000408 20613862
8. Blackstone C, O'Kane CJ, Reid E, (2011) Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat Rev Neurosci12: 31–42. doi: 10.1038/nrn2946 21139634
9. 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 Genet24: 4984–4896. doi: 10.1093/hmg/ddv220 26085577
10. 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 Genet9: e1003988. doi: 10.1371/journal.pgen.1003988 24367272
11. 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 Neurol1: 379–389. doi: 10.1002/acn3.64 24999486
12. Allison R, Edgar JR, Pearson G, Rizo T, Newton T, et al. (2017) Defects in ER-endosome contacts impact lysosome function in hereditary spastic paraplegia. J Cell Biol216: 1337–1355. doi: 10.1083/jcb.201609033 28389476
13. Traub LM, Bonifacino JS, (2013) Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol5: a016790. doi: 10.1101/cshperspect.a016790 24186068
14. Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, et al. (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics13: 2513–2526. doi: 10.1074/mcp.M113.031591 24942700
15. Hirst J, Madeo M, Smets K, Edgar JR, Schols L, et al. (2016) Complicated spastic paraplegia in patients with AP5Z1 mutations (SPG48). Neurol Genet2: e98. doi: 10.1212/NXG.0000000000000098 27606357
16. Itzhak DN, Colin Davies C, Tyanova S, Mishra A, Williamson J, et al. (2017) A mass-spectrometry based approach for mapping protein subcellular localization reveals the spatial proteome of mouse primary neurons. Cell Rep In press.
17. Breusegem SY, Seaman MNJ, (2014) Genome-wide RNAi screen reveals a role for multipass membrane proteins in endosome-to-Golgi retrieval. Cell Rep: 1931–1945. doi: 10.1016/j.celrep.2014.10.053 25464851
18. Kamiyama S, Suda T, Ueda R, Suzuki M, Okubo R, et al. (2003) Molecular cloning and identification of 3'-phosphoadenosine 5'-phosphosulfate transporter. J Biol Chem278: 25958–25963. doi: 10.1074/jbc.M302439200 12716889
19. Kladney RD, Bulla GA, Guo L, Mason AL, Tollefson AE, et al. (2000) GP73, a novel Golgi-localized protein upregulated by viral infection. Gene249: 53–65. 10831838
20. Linstedt AD, Mehta A, Suhan J, Reggio H, Hauri HP, (1997) Sequence and overexpression of GPP130/GIMPc: evidence for saturable pH-sensitive targeting of a type II early Golgi membrane protein. Mol Biol Cell8: 1073–1087. 9201717
21. Mourelatos Z, Gonatas JO, Nycum LM, Gonatas NK, Biegel JA, (1995) Assignment of the GLG1 gene for MGF-160, a fibroblast growth factor and E-selectin binding membrane sialoglycoprotein of the Golgi apparatus, to chromosome 16q22-q23 by fluorescence in situ hybridization. Genomics28: 354–355. 8530051
22. White T, Bennett EP, Takio K, Sørensen T, Bonding N, et al. (1995) Purification and cDNA cloning of a human UDP-N-acetyl-alpha-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase. J Biol Chem270: 24156–24165. 7592619
23. Bachert C, Lee TH, Linstedt AD, (2001) Lumenal endosomal and Golgi-retrieval determinants involved in pH-sensitive targeting of an early Golgi protein. Mol Biol Cell12: 3152–3160. 11598199
24. Puri S, Bachert C, Fimmel CJ, Linstedt AD, (2002) Cycling of early Golgi proteins via the cell surface and endosomes upon lumenal pH disruption. Traffic3: 641–653. 12191016
25. Natarajan R, Linstedt AD, (2004) A cycling cis-Golgi protein mediates endosome-to-Golgi traffic. Mol Biol Cell15: 4798–4806. doi: 10.1091/mbc.E04-05-0366 15331763
26. Mukhopadhyay S, Bachert C, Smith DR, Linstedt AD, (2010) Manganese-induced trafficking and turnover of the cis-Golgi glycoprotein GPP130. Mol Biol Cell21: 1282–1292. doi: 10.1091/mbc.E09-11-0985 20130081
27. Robinson MS, Sahlender DA, Foster SD, (2010) Rapid inactivation of proteins by rapamycin-induced rerouting to mitochondria. Dev Cell18: 324–331. doi: 10.1016/j.devcel.2009.12.015 20159602
28. Hirst J, Borner GHH, Antrobus R, Peden AA, Hodson NA, et al. (2012) Distinct and overlapping roles for AP-1 and GGAs revealed by the "knocksideways" system. Curr Biol22: 1711–1716. doi: 10.1016/j.cub.2012.07.012 22902756
29. Tewari R, Bachert C, Linstedt AD, (2015) Induced oligomerization targets Golgi proteins for degradation in lysosomes. Mol Biol Cell26: 4427–4437. doi: 10.1091/mbc.E15-04-0207 26446839
30. Chapman RE, Munro S, (1994) Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO J13: 2305–2312. 8194522
31. Bonifacino JS, Traub LM, (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Ann Rev Biochem72: 395–447. doi: 10.1146/annurev.biochem.72.121801.161800 12651740
32. Seaman MNJ, (2007) Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J Cell Sci120: 2378–2389. doi: 10.1242/jcs.009654 17606993
33. Bogan JS, Kandror KV, (2010) Biogenesis and regulation of insulin-responsive vesicles containing GLUT4. Curr Opin Cell Biol22: 506–512. doi: 10.1016/j.ceb.2010.03.012 20417083
34. Canuel M, Libin Y, Morales CR, (2009) The interactomics of sortilin: an ancient lysosomal receptor evolving new functions. Histol Histopathol24: 481–492. doi: 10.14670/HH-24.481 19224451
35. Nykjaer A, Willnow TE, (2012) Sortilin: a receptor to regulate neuronal viability and function. Trends Neurosci35: 261–270. doi: 10.1016/j.tins.2012.01.003 22341525
36. Braulke T, Bonifacino JS, (2009) Sorting of lysosomal proteins. Biochim Biophys Acta1793: 605–614. doi: 10.1016/j.bbamcr.2008.10.016 19046998
37. Nielsen MS, Madsen P, Christensen EI, Nykjaer A, Gliemann J, et al. (2001) The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J In press.
38. Venkat S, Linstedt AD, (2017) Manganese-induced trafficking and turnover of GPP130 is mediated by sortilin. Mol Biol Cell E17-05-0326.
39. Hirst J, Schlacht A, Norcott JP, Traynor D, Bloomfield G, et al. (2014) Characterization of TSET, an ancient and widespread membrane trafficking complex. eLife3: e02866. doi: 10.7554/eLife.02866 24867644
40. Dacks JB, Robinson MS, (2017) Outerwear through the ages: evolutionary cell biology of vesicle coats. Curr Opin Cell Biol47: 108–116. doi: 10.1016/j.ceb.2017.04.001 28622586
41. Jackson LP, Lewis MJ, Kent HM, Edeling MA, Evans PR, et al. (2012) Molecular basis for recognition of dilysine trafficking motifs by COPI. Dev Cell11: 1255–1262.
42. Peden AA, Ooeschot V, Hesser BA, Austin CD, Scheller RH, et al. (2003) Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J Cell Biol164: 1065–1076.
43. Seaman MNJ, (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol165: 111–122. doi: 10.1083/jcb.200312034 15078902
44. Dell'Angelica EC, Shotelersuk V, Aguilar RC, Gahl WA, Bonifacino JS, (1999) Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol Cell3: 11–21. 10024875
45. Peden AA, Rudge RE, Lui WW, Robinson MS, (2002) Assembly and function of AP-3 complexes in cells expressing mutant subunits. J Cell Biol156: 327–336. doi: 10.1083/jcb.200107140 11807095
46. Chang J, Lee S, Blackstone C, (2014) Spastic paraplegia proteins spastizin and spatacsin mediate autophagic lysosome reformation. J Clin Invest124: 5249–5262. doi: 10.1172/JCI77598 25365221
47. 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 Genet11: e1005454. doi: 10.1371/journal.pgen.1005454 26284655
48. Tsukita S, Ishikawa H, (1980) The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles. J Cell Biol84: 513–530. 6153657
49. Freeman C, Seaman MNJ, Reid E, (2013) The hereditary spastic paraplegia protein strumpellin: characterisation in neurons and of the effect of disease mutations on WASH complex assembly and function. Biochim Biophys Acta1832: 160–173. doi: 10.1016/j.bbadis.2012.10.011 23085491
50. Vilariño-Güell C, Wider C, Ross OA, Dachsel JC, Kachergus JM, et al. (2011) VPS35 mutations in Parkinson disease. Am J Hum Genet89: 162–167. doi: 10.1016/j.ajhg.2011.06.001 21763482
51. Zimprich A, Benet-Pagès 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 Genet89: 168–175. doi: 10.1016/j.ajhg.2011.06.008 21763483
52. Aschner M, Erikson KM, Herrero Hernández E, Tjalkens R, (2009) Manganese and its role in Parkinson's disease: from transport to neuropathology. Neuromolecular Med11: 252–266. doi: 10.1007/s12017-009-8083-0 19657747
53. Simpson F, Bright NA, West MA, Newman LS, Darnell RB, et al. (1996) A novel adaptor-related protein complex. J Cell Biol133: 749–760. 8666661
54. Cost GJ, Cozzarelli NR, (2007) Directed assembly of DNA molecules via simultaneous ligation and digestion. Biotechniques42: 86–89.
55. Gokool S, Tattersall D, Seaman MNJ, (2007) EHD1 interacts with retromer to stabilize SNX1 tubules and facilitate endosome-to-Golgi retrieval. Traffic8: 1873–1886. doi: 10.1111/j.1600-0854.2007.00652.x 17868075
56. Tiwari RK, Kusari J, Sen GC, (1987) Functional equivalents of interferon-mediated signals needed for induction of an mRNA can be generated by double-stranded RNA and growth factors. EMBO J6: 3373–3378. 2828026
57. Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, et al. (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods13: 731–740. doi: 10.1038/nmeth.3901 27348712
58. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, et al. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics1: 376–386. 12118079
59. Borner GHH, Antrobus R, Hirst J, Bhumbra GS, Kozik P, et al. (2012) Multivariate proteomic profiling identifies novel accessory proteins of coated vesicles. J Cell Biol197: 141–160. doi: 10.1083/jcb.201111049 22472443
60. Wiśniewski JR, Zougman A, Nagaraj N, Mann M, (2009) Universal sample preparation method for proteome analysis. Nat Methods6: 359–362. doi: 10.1038/nmeth.1322 19377485
61. Kulak NA, Pichler G, Paron I, Nagaraj N, Mann M, (2014) Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat Methods11: 319–324. doi: 10.1038/nmeth.2834 24487582
62. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol26: 1367–1372. doi: 10.1038/nbt.1511 19029910