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Analysis of the SNARE Stx8 recycling reveals that the retromer-sorting motif has undergone evolutionary divergence


Autoři: Francisco Yanguas aff001;  M.-Henar Valdivieso aff001
Působiště autorů: Departamento de Microbiología y Genética, Universidad de Salamanca. Salamanca. Spain aff001;  Instituto de Biología Funcional y Genómica (IBFG), Consejo Superior de Investigaciones Científicas (CSIC). Salamanca. Spain aff002
Vyšlo v časopise: Analysis of the SNARE Stx8 recycling reveals that the retromer-sorting motif has undergone evolutionary divergence. PLoS Genet 17(3): e1009463. doi:10.1371/journal.pgen.1009463
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009463

Souhrn

Fsv1/Stx8 is a Schizosaccharomyces pombe protein similar to mammalian syntaxin 8. stx8Δ cells are sensitive to salts, and the prevacuolar endosome (PVE) is altered in stx8Δ cells. These defects depend on the SNARE domain, data that confirm the conserved function of syntaxin8 and Stx8 in vesicle fusion at the PVE. Stx8 localizes at the trans-Golgi network (TGN) and the prevacuolar endosome (PVE), and its recycling depends on the retromer component Vps35, and on the sorting nexins Vps5, Vps17, and Snx3. Several experimental approaches demonstrate that Stx8 is a cargo of the Snx3-retromer. Using extensive truncation and alanine scanning mutagenesis, we identified the Stx8 sorting signal. This signal is an IEMeaM sequence that is located in an unstructured protein region, must be distant from the transmembrane (TM) helix, and where the 133I, 134E, 135M, and 138M residues are all essential for recycling. This sorting motif is different from those described for most retromer cargoes, which include aromatic residues, and resembles the sorting motif of mammalian polycystin-2 (PC2). Comparison of Stx8 and PC2 motifs leads to an IEMxx(I/M) consensus. Computer-assisted screening for this and for a loose Ψ(E/D)ΨXXΨ motif (where Ψ is a hydrophobic residue with large aliphatic chain) shows that syntaxin 8 and PC2 homologues from other organisms bear variation of this motif. The phylogeny of the Stx8 sorting motifs from the Schizosaccharomyces species shows that their divergence is similar to that of the genus, showing that they have undergone evolutionary divergence. A preliminary analysis of the motifs in syntaxin 8 and PC2 sequences from various organisms suggests that they might have also undergone evolutionary divergence, what suggests that the presence of almost-identical motifs in Stx8 and PC2 might be a case of convergent evolution.

Klíčová slova:

Alanine – Endosomes – Saccharomyces cerevisiae – Sequence motif analysis – Schizosaccharomyces pombe – Vacuoles – Yeast – Vesicle fusion


Zdroje

1. Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell. 2004 Jan 23;116(2):153–66. doi: 10.1016/s0092-8674(03)01079-1 14744428

2. Conibear E, Stevens TH. Multiple sorting pathways between the late Golgi and the vacuole in yeast. Biochim Biophys Acta. 1998 Aug 14;1404(1–2):211–30. doi: 10.1016/s0167-4889(98)00058-5 9714809

3. Risselada HJ, Grubmuller H. How SNARE molecules mediate membrane fusion: recent insights from molecular simulations. Curr Opin Struct Biol. 2012 Apr;22(2):187–96. doi: 10.1016/j.sbi.2012.01.007 22365575

4. Dingjan I, Linders PTA, Verboogen DRJ, Revelo NH, Ter Beest M, van den Bogaart G. Endosomal and Phagosomal SNAREs. Physiol Rev. 2018 Jul 1;98(3):1465–92. doi: 10.1152/physrev.00037.2017 29790818

5. Hong W. SNAREs and traffic. Biochim Biophys Acta. 2005 Jul 10;1744(3):493–517. 16038056

6. Wang T, Li L, Hong W. SNARE proteins in membrane trafficking. Traffic. 2017 Dec;18(12):767–75. doi: 10.1111/tra.12524 28857378

7. Antonin W, Holroyd C, Fasshauer D, Pabst S, Von Mollard GF, Jahn R. A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function. Embo J. 2000 Dec 1;19(23):6453–64. doi: 10.1093/emboj/19.23.6453 11101518

8. Pryor PR, Mullock BM, Bright NA, Lindsay MR, Gray SR, Richardson SC, et al. Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 2004 Jun;5(6):590–5. doi: 10.1038/sj.embor.7400150 15133481

9. Day KJ, Casler JC, Glick BS. Budding Yeast Has a Minimal Endomembrane System. Dev Cell. 2018 Jan 8;44(1):56–72 e4. doi: 10.1016/j.devcel.2017.12.014 29316441

10. Tojima T, Suda Y, Ishii M, Kurokawa K, Nakano A. Spatiotemporal dissection of the trans-Golgi network in budding yeast. J Cell Sci. 2019 Aug 2;132(15). doi: 10.1242/jcs.231159 31289195

11. Haft CR, de la Luz Sierra M, Bafford R, Lesniak MA, Barr VA, Taylor SI. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol Biol Cell. 2000 Dec;11(12):4105–16. doi: 10.1091/mbc.11.12.4105 11102511

12. Seaman MN, McCaffery JM, Emr SD. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol. 1998 Aug 10;142(3):665–81. doi: 10.1083/jcb.142.3.665 9700157

13. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol. 2004 Apr;165(1):123–33. doi: 10.1083/jcb.200312055 15078903

14. Nothwehr SF, Bruinsma P, Strawn LA. Distinct domains within Vps35p mediate the retrieval of two different cargo proteins from the yeast prevacuolar/endosomal compartment. Mol Biol Cell. 1999 Apr;10(4):875–90. doi: 10.1091/mbc.10.4.875 10198044

15. Nothwehr SF, Ha SA, Bruinsma P. Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J Cell Biol. 2000 Oct 16;151(2):297–310. doi: 10.1083/jcb.151.2.297 11038177

16. Seaman MN. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol. 2004 Apr;165(1):111–22. doi: 10.1083/jcb.200312034 15078902

17. Seaman MN, Marcusson EG, Cereghino JL, Emr SD. Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J Cell Biol. 1997 Apr 7;137(1):79–92. doi: 10.1083/jcb.137.1.79 9105038

18. Gallon M, Cullen PJ. Retromer and sorting nexins in endosomal sorting. Biochem Soc Trans. 2015 Feb;43(1):33–47. doi: 10.1042/BST20140290 25619244

19. Liu JJ. Retromer-Mediated Protein Sorting and Vesicular Trafficking. J Genet Genomics. 2016 Apr 20;43(4):165–77. doi: 10.1016/j.jgg.2016.02.006 27157806

20. Bean BD, Davey M, Conibear E. Cargo selectivity of yeast sorting nexins. Traffic. 2017 Feb;18(2):110–22. doi: 10.1111/tra.12459 27883263

21. Burd C, Cullen PJ. Retromer: a master conductor of endosome sorting. Cold Spring Harb Perspect Biol. 2018 Feb 1;6(2).

22. Clairfeuille T, Mas C, Chan AS, Yang Z, Tello-Lafoz M, Chandra M, et al. A molecular code for endosomal recycling of phosphorylated cargos by the SNX27-retromer complex. Nat Struct Mol Biol. 2016 Oct;23(10):921–32. doi: 10.1038/nsmb.3290 27595347

23. Gallon M, Clairfeuille T, Steinberg F, Mas C, Ghai R, Sessions RB, et al. A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. Proc Natl Acad Sci U S A. 2014 Sep 2;111(35):E3604–13. doi: 10.1073/pnas.1410552111 25136126

24. Harterink M, Port F, Lorenowicz MJ, McGough IJ, Silhankova M, Betist MC, et al. A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat Cell Biol. 2011 Jul 3;13(8):914–23. doi: 10.1038/ncb2281 21725319

25. Kurten RC, Cadena DL, Gill GN. Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science. 1996 May 17;272(5264):1008–10. doi: 10.1126/science.272.5264.1008 8638121

26. Lucas M, Gershlick DC, Vidaurrazaga A, Rojas AL, Bonifacino JS, Hierro A. Structural Mechanism for Cargo Recognition by the Retromer Complex. Cell. 2016 Dec 1;167(6):1623–35 e14. doi: 10.1016/j.cell.2016.10.056 27889239

27. Strochlic TI, Setty TG, Sitaram A, Burd CG. Grd19/Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling. J Cell Biol. 2007 Apr 9;177(1):115–25. doi: 10.1083/jcb.200609161 17420293

28. Wassmer T, Attar N, Bujny MV, Oakley J, Traer CJ, Cullen PJ. A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J Cell Sci. 2007 Jan 1;120(Pt 1):45–54. doi: 10.1242/jcs.03302 17148574

29. Yong X, Zhao L, Deng W, Sun H, Zhou X, Mao L, et al. Mechanism of cargo recognition by retromer-linked SNX-BAR proteins. PLoS Biol. 2020 Mar;18(3):e3000631. doi: 10.1371/journal.pbio.3000631 32150533

30. Best JT, Xu P, McGuire JG, Leahy SN, Graham TR. Yeast synaptobrevin, Snc1, engages distinct routes of postendocytic recycling mediated by a sorting nexin, Rcy1-COPI, and retromer. Mol Biol Cell. 2020 Apr 15;31(9):944–62. doi: 10.1091/mbc.E19-05-0290 32074001

31. Hettema EH, Lewis MJ, Black MW, Pelham HR. Retromer and the sorting nexins Snx4/41/42 mediate distinct retrieval pathways from yeast endosomes. Embo J. 2003 Feb 3;22(3):548–57. doi: 10.1093/emboj/cdg062 12554655

32. Ma M, Burd CG, Chi RJ. Distinct complexes of yeast Snx4 family SNX-BARs mediate retrograde trafficking of Snc1 and Atg27. Traffic. 2017 Feb;18(2):134–44. doi: 10.1111/tra.12462 28026081

33. Wang S, Bellen HJ. The retromer complex in development and disease. Development (Cambridge, England). 2015 Jul 15;142(14):2392–6. doi: 10.1242/dev.123737 26199408

34. Hosomi A, Higuchi Y, Yagi S, Takegawa K. Vsl1p cooperates with Fsv1p for vacuolar protein transport and homotypic fusion in Schizosaccharomyces pombe. Microbiology. 2015 Jan;161(Pt 1):89–98. doi: 10.1099/mic.0.080481-0 25378562

35. Takegawa K, Hosomi A, Iwaki T, Fujita Y, Morita T, Tanaka N. Identification of a SNARE protein required for vacuolar protein transport in Schizosaccharomyces pombe. Biochem Biophys Res Commun. 2003 Nov 7;311(1):77–82. doi: 10.1016/j.bbrc.2003.09.179 14575697

36. Seaman MN. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J Cell Sci. 2007 Jul 15;120(Pt 14):2378–89. doi: 10.1242/jcs.009654 17606993

37. Simonetti B, Danson CM, Heesom KJ, Cullen PJ. Sequence-dependent cargo recognition by SNX-BARs mediates retromer-independent transport of CI-MPR. J Cell Biol. 2017 Nov 6;216(11):3695–712. doi: 10.1083/jcb.201703015 28935633

38. Simonetti B, Paul B, Chaudhari K, Weeratunga S, Steinberg F, Gorla M, et al. Molecular identification of a BAR domain-containing coat complex for endosomal recycling of transmembrane proteins. Nat Cell Biol. 2019 Oct;21(10):1219–33. doi: 10.1038/s41556-019-0393-3 31576058

39. Suzuki SW, Chuang YS, Li M, Seaman MNJ, Emr SD. A bipartite sorting signal ensures specificity of retromer complex in membrane protein recycling. J Cell Biol. 2019 Sep 2;218(9):2876–86. doi: 10.1083/jcb.201901019 31337624

40. Tilley FC, Gallon M, Luo C, Danson CM, Zhou J, Cullen PJ. Retromer associates with the cytoplasmic amino-terminus of polycystin-2. J Cell Sci. 2018 Jun 6;131(11). doi: 10.1242/jcs.211342 29724910

41. Yanguas F, Moscoso-Romero E, Valdivieso MH. Ent3 and GGA adaptors facilitate diverse anterograde and retrograde trafficking events to and from the prevacuolar endosome. Scientific Reports. 2019;9(1):10747. doi: 10.1038/s41598-019-47035-5 31341193

42. Iwaki T, Hosomi A, Tokudomi S, Kusunoki Y, Fujita Y, Giga-Hama Y, et al. Vacuolar protein sorting receptor in Schizosaccharomyces pombe. Microbiology. 2006 May;152(Pt 5):1523–32. doi: 10.1099/mic.0.28627-0 16622069

43. Bonifacino JS, Lippincott-Schwartz J. Coat proteins: shaping membrane transport. Nat Rev Mol Cell Biol. 2003 May;4(5):409–14. doi: 10.1038/nrm1099 12728274

44. Katzmann DJ, Babst M, Emr SD. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell. 2001 Jul 27;106(2):145–55. doi: 10.1016/s0092-8674(01)00434-2 11511343

45. Reggiori F, Pelham HR. Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. Embo J. 2001 Sep 17;20(18):5176–86. doi: 10.1093/emboj/20.18.5176 11566881

46. Liu Q, Ma Y, Zhou X, Furuyashiki T. Constitutive Tor2 Activity Promotes Retention of the Amino Acid Transporter Agp3 at Trans-Golgi/Endosomes in Fission Yeast. PLoS One. 2015;10(10):e0139045. doi: 10.1371/journal.pone.0139045 26447710

47. Scott CC, Gruenberg J. Ion flux and the function of endosomes and lysosomes: pH is just the start: the flux of ions across endosomal membranes influences endosome function not only through regulation of the luminal pH. Bioessays. 2011 Feb;33(2):103–10. doi: 10.1002/bies.201000108 21140470

48. Vermeulen LMP, Brans T, Samal SK, Dubruel P, Demeester J, De Smedt SC, et al. Endosomal Size and Membrane Leakiness Influence Proton Sponge-Based Rupture of Endosomal Vesicles. ACS Nano. 2018 Mar 27;12(3):2332–45. doi: 10.1021/acsnano.7b07583 29505236

49. Chica N, Rozalen AE, Perez-Hidalgo L, Rubio A, Novak B, Moreno S. Nutritional Control of Cell Size by the Greatwall-Endosulfine-PP2A.B55 Pathway. Curr Biol. 2016 Feb 8;26(3):319–30. doi: 10.1016/j.cub.2015.12.035 26776736

50. Petersen J, Russell P. Growth and the Environment of Schizosaccharomyces pombe. Cold Spring Harb Protoc. 2016 Mar 1;2016(3):pdb top079764.

51. Hoya M, Yanguas F, Moro S, Prescianotto-Baschong C, Doncel C, de Leon N, et al. Traffic Through the Trans-Golgi Network and the Endosomal System Requires Collaboration Between Exomer and Clathrin Adaptors in Fission Yeast. Genetics. 2017 Feb;205(2):673–90. doi: 10.1534/genetics.116.193458 27974503

52. Onishi M, Iida M, Koga T, Yamada S, Hirata A, Iwaki T, et al. Schizosaccharomyces pombe Sst4p, a conserved Vps27/Hrs homolog, functions downstream of phosphatidylinositol 3-kinase Pik3p to mediate proper spore formation. Eukaryot Cell. 2007 Dec;6(12):2343–53. doi: 10.1128/EC.00211-07 17951524

53. Bhat SS, Friedmann KS, Knorck A, Hoxha C, Leidinger P, Backes C, et al. Syntaxin 8 is required for efficient lytic granule trafficking in cytotoxic T lymphocytes. Biochim Biophys Acta. 2016 Jul;1863(7 Pt A):1653–64. doi: 10.1016/j.bbamcr.2016.04.014 27094127

54. Subramaniam VN, Loh E, Horstmann H, Habermann A, Xu Y, Coe J, et al. Preferential association of syntaxin 8 with the early endosome. J Cell Sci. 2000 Mar;113 (Pt 6):997–1008. 10683148

55. Iwaki T, Onishi M, Ikeuchi M, Kita A, Sugiura R, Giga-Hama Y, et al. Essential roles of class E Vps proteins for sorting into multivesicular bodies in Schizosaccharomyces pombe. Microbiology. 2007 Aug;153(Pt 8):2753–64. doi: 10.1099/mic.0.2007/006072-0 17660439

56. Arcones I, Sacristan C, Roncero C. Maintaining protein homeostasis: early and late endosomal dual recycling for the maintenance of intracellular pools of the plasma membrane protein Chs3. Mol Biol Cell. 2016 Dec 15;27(25):4021–32. doi: 10.1091/mbc.E16-04-0239 27798229

57. Morrison KL, Weiss GA. Combinatorial alanine-scanning. Curr Opin Chem Biol. 2001 Jun;5(3):302–7. doi: 10.1016/s1367-5931(00)00206-4 11479122

58. Feng S, Streets AJ, Nesin V, Tran U, Nie H, Onopiuk M, et al. The Sorting Nexin 3 Retromer Pathway Regulates the Cell Surface Localization and Activity of a Wnt-Activated Polycystin Channel Complex. J Am Soc Nephrol. 2017 Oct;28(10):2973–84. doi: 10.1681/ASN.2016121349 28620080

59. Aasland R, Abrams C, Ampe C, Ball LJ, Bedford MT, Cesareni G, et al. Normalization of nomenclature for peptide motifs as ligands of modular protein domains. FEBS Lett. 2002 Feb 20;513(1):141–4. doi: 10.1016/s0014-5793(01)03295-1 11911894

60. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009 Dec 15;10:421. doi: 10.1186/1471-2105-10-421 20003500

61. Thompson J, Higgins D, Gibson T. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl Acids Research. 1994;22:4673–80. doi: 10.1093/nar/22.22.4673 7984417

62. Helston RM, Box JA, Tang W, Baumann P. Schizosaccharomyces cryophilus sp. nov., a new species of fission yeast. FEMS yeast research. 2010 Sep;10(6):779–86. doi: 10.1111/j.1567-1364.2010.00657.x 20618870

63. Sipiczki M. Phylogenesis of fission yeasts. Contradictions surrounding the origin of a century old genus. Antonie van Leeuwenhoek. 1995 Aug;68(2):119–49. doi: 10.1007/BF00873099 8546451

64. de Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, et al. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W362–5. doi: 10.1093/nar/gkl124 16845026

65. Hayles J, Wood V, Jeffery L, Hoe KL, Kim DU, Park HO, et al. A genome-wide resource of cell cycle and cell shape genes of fission yeast. Open Biol. 2013 May 22;3(5):130053. doi: 10.1098/rsob.130053 23697806

66. Kienle N, Kloepper TH, Fasshauer D. Phylogeny of the SNARE vesicle fusion machinery yields insights into the conservation of the secretory pathway in fungi. BMC Evol Biol. 2009 Jan 23;9:19. doi: 10.1186/1471-2148-9-19 19166604

67. Kim DU, Hayles J, Kim D, Wood V, Park HO, Won M, et al. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol. 2010 Jun;28(6):617–23. doi: 10.1038/nbt.1628 20473289

68. Lock A, Rutherford K, Harris MA, Wood V. PomBase: The Scientific Resource for Fission Yeast. Methods Mol Biol. 2018;1757:49–68. doi: 10.1007/978-1-4939-7737-6_4 29761456

69. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, et al. The genome sequence of Schizosaccharomyces pombe. Nature. 2002 Feb 21;415(6874):871–80. doi: 10.1038/nature724 11859360

70. Wood V, Harris MA, McDowall MD, Rutherford K, Vaughan BW, Staines DM, et al. PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res. 2012 Jan;40(Database issue):D695–9. doi: 10.1093/nar/gkr853 22039153

71. Hosomi A, Nakase M, Takegawa K. Schizosaccharomyces pombe Pep12p is required for vacuolar protein transport and vacuolar homotypic fusion. J Biosci Bioeng. 2011 Oct;112(4):309–14. doi: 10.1016/j.jbiosc.2011.06.009 21757403

72. Tsui MM, Banfield DK. Yeast Golgi SNARE interactions are promiscuous. J Cell Sci. 2000 Jan;113 (Pt 1):145–52. 10591633

73. Burri L, Lithgow T. A complete set of SNAREs in yeast. Traffic. 2004 Jan;5(1):45–52. doi: 10.1046/j.1600-0854.2003.00151.x 14675424

74. Dilcher M, Kohler B, von Mollard GF. Genetic interactions with the yeast Q-SNARE VTI1 reveal novel functions for the R-SNARE YKT6. J Biol Chem. 2001 Sep 14;276(37):34537–44. doi: 10.1074/jbc.M101551200 11445562

75. Gerrard SR, Levi BP, Stevens TH. Pep12p is a multifunctional yeast syntaxin that controls entry of biosynthetic, endocytic and retrograde traffic into the prevacuolar compartment. Traffic. 2000 Mar;1(3):259–69. doi: 10.1034/j.1600-0854.2000.010308.x 11208109

76. Bilan F, Thoreau V, Nacfer M, Derand R, Norez C, Cantereau A, et al. Syntaxin 8 impairs trafficking of cystic fibrosis transmembrane conductance regulator (CFTR) and inhibits its channel activity. J Cell Sci. 2004 Apr 15;117(Pt 10):1923–35. doi: 10.1242/jcs.01070 15039462

77. Renigunta V, Fischer T, Zuzarte M, Kling S, Zou X, Siebert K, et al. Cooperative endocytosis of the endosomal SNARE protein syntaxin-8 and the potassium channel TASK-1. Mol Biol Cell. 2014 Jun 15;25(12):1877–91. doi: 10.1091/mbc.E13-10-0592 24743596

78. Steinberg F, Gallon M, Winfield M, Thomas EC, Bell AJ, Heesom KJ, et al. A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat Cell Biol. 2013 May;15(5):461–71. doi: 10.1038/ncb2721 23563491

79. Ma M, Burd CG. Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain. Mol Biol Cell. 2019 Jul 1;30(14):1729–42. doi: 10.1091/mbc.E19-02-0117 31067149

80. Zhao D, Liu XM, Yu ZQ, Sun LL, Xiong X, Dong MQ, et al. Atg20- and Atg24-family proteins promote organelle autophagy in fission yeast. J Cell Sci. 2016 Nov 15;129(22):4289–304. doi: 10.1242/jcs.194373 27737912

81. Shi Y, Stefan CJ, Rue SM, Teis D, Emr SD. Two novel WD40 domain-containing proteins, Ere1 and Ere2, function in the retromer-mediated endosomal recycling pathway. Mol Biol Cell. 2011 Nov;22(21):4093–107. doi: 10.1091/mbc.E11-05-0440 21880895

82. Cereghino JL, Marcusson EG, Emr SD. The cytoplasmic tail domain of the vacuolar protein sorting receptor Vps10p and a subset of VPS gene products regulate receptor stability, function, and localization. Mol Biol Cell. 1995 Sep;6(9):1089–102. doi: 10.1091/mbc.6.9.1089 8534908

83. Cooper AA, Stevens TH. Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. J Cell Biol. 1996 May;133(3):529–41. doi: 10.1083/jcb.133.3.529 8636229

84. Finnigan GC, Cronan GE, Park HJ, Srinivasan S, Quiocho FA, Stevens TH. Sorting of the yeast vacuolar-type, proton-translocating ATPase enzyme complex (V-ATPase): identification of a necessary and sufficient Golgi/endosomal retention signal in Stv1p. J Biol Chem. 2012 Jun 1;287(23):19487–500. doi: 10.1074/jbc.M112.343814 22496448

85. Fjorback AW, Seaman M, Gustafsen C, Mehmedbasic A, Gokool S, Wu C, et al. Retromer binds the FANSHY sorting motif in SorLA to regulate amyloid precursor protein sorting and processing. J Neurosci. 2012 Jan 25;32(4):1467–80. doi: 10.1523/JNEUROSCI.2272-11.2012 22279231

86. Nothwehr SF, Roberts CJ, Stevens TH. Membrane protein retention in the yeast Golgi apparatus: dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues. J Cell Biol. 1993 Jun;121(6):1197–209. doi: 10.1083/jcb.121.6.1197 8509444

87. Nothwehr SF, Stevens TH. Sorting of membrane proteins in the yeast secretory pathway. J Biol Chem. 1994 Apr 8;269(14):10185–8. 8144594

88. Schweizer A, Kornfeld S, Rohrer J. Proper sorting of the cation-dependent mannose 6-phosphate receptor in endosomes depends on a pair of aromatic amino acids in its cytoplasmic tail. Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14471–6. doi: 10.1073/pnas.94.26.14471 9405637

89. Suzuki SW, Emr SD. Membrane protein recycling from the vacuole/lysosome membrane. J Cell Biol. 2018 May 7;217(5):1623–32. doi: 10.1083/jcb.201709162 29511122

90. Tabuchi M, Yanatori I, Kawai Y, Kishi F. Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J Cell Sci. 2010 Mar 1;123(Pt 5):756–66. doi: 10.1242/jcs.060574 20164305

91. Mukadam AS, Seaman MN. Retromer-mediated endosomal protein sorting: The role of unstructured domains. FEBS Lett. 2015 Sep 14;589(19 Pt A):2620–6. doi: 10.1016/j.febslet.2015.05.052 26072290

92. Rohrer J, Schweizer A, Russell D, Kornfeld S. The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J Cell Biol. 1996 Feb;132(4):565–76. doi: 10.1083/jcb.132.4.565 8647888

93. Kovtun O, Leneva N, Bykov YS, Ariotti N, Teasdale RD, Schaffer M, et al. Structure of the membrane-assembled retromer coat determined by cryo-electron tomography. Nature. 2018 Sep;561(7724):561–4. doi: 10.1038/s41586-018-0526-z 30224749

94. Lewis MJ, Nichols BJ, Prescianotto-Baschong C, Riezman H, Pelham HR. Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol Biol Cell. 2000 Jan;11(1):23–38. doi: 10.1091/mbc.11.1.23 10637288

95. Forsburg SL, Rhind N. Basic methods for fission yeast. Yeast. 2006 Feb;23(3):173–83. doi: 10.1002/yea.1347 16498704

96. Moreno S, Klar A, Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. doi: 10.1016/0076-6879(91)94059-l 2005825

97. Sambrook J, Russell D.W. molecular Cloning: A laboratory manual. New York: CSHL Press 2001.

98. Fennessy D, Grallert A, Krapp A, Cokoja A, Bridge AJ, Petersen J, et al. Extending the Schizosaccharomyces pombe molecular genetic toolbox. PLoS One. 2014;9(5):e97683. doi: 10.1371/journal.pone.0097683 24848109

99. Bähler J, Wu JQ, Longtine MS, Shah NG, McKenzie A, 3rd, Steever AB, et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast. 1998;14(10):943–51. doi: 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y 9717240

100. Marguerat S, Schmidt A, Codlin S, Chen W, Aebersold R, Bahler J. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell. 2012 Oct 26;151(3):671–83. doi: 10.1016/j.cell.2012.09.019 23101633

101. Cha-Aim K, Hoshida H, Fukunaga T, Akada R. Fusion PCR via novel overlap sequences. Methods Mol Biol. 2012;852:97–110. doi: 10.1007/978-1-61779-564-0_8 22328428

102. Kunkel TA, Roberts JD, Zakour RA. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–82. doi: 10.1016/0076-6879(87)54085-x 3323813

103. Fields S, Sternglanz R. The two-hybrid system: an assay for protein-protein interactions. Trends Genet. 1994 Aug;10(8):286–92. doi: 10.1016/0168-9525(90)90012-u 7940758

104. Kerppola TK. Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annual review of biophysics. 2008;37:465–87. doi: 10.1146/annurev.biophys.37.032807.125842 18573091

105. de Leon N, Sharifmoghadam MR, Hoya M, Curto MA, Doncel C, Valdivieso MH. Regulation of cell wall synthesis by the clathrin light chain is essential for viability in Schizosaccharomyces pombe. PLoS One. 2013;8(8):e71510. doi: 10.1371/journal.pone.0071510 23977061

106. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006 Dec;224(Pt 3):213–32. doi: 10.1111/j.1365-2818.2006.01706.x 17210054


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