Sorting Signals That Mediate Traffic of Chitin Synthase III between the TGN/Endosomes and to the Plasma Membrane in Yeast

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Starr, Trevor L ^a   Pagant, Silvere ^a,b   Wang, Chao Wen ^a,c   Schekman, Randy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CELL PROTEIN; CHITIN SYNTHASE III; LEUCINE; MEMBRANE ENZYME; PROTEIN AP 3; TRANSCRIPTION FACTOR AP 1; TRYPTOPHAN; UNCLASSIFIED DRUG;

ACIDITY; AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELL SELECTION; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; ENDOSOME; EXOCYTOSIS; INTRACELLULAR TRANSPORT; NONHUMAN; PROTEIN DOMAIN; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANS GOLGI NETWORK; YEAST CELL;

CELL MEMBRANE; CHITIN SYNTHASE; CHROMATOGRAPHY, AFFINITY; ENDOSOMES; EXOCYTOSIS; GOLGI APPARATUS; MUTATION; PROTEIN SORTING SIGNALS; YEASTS;

EID: 84867051116     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046386     Document Type: Article

References (52)

1. Pelham HR, (1995) Sorting and retrieval between the endoplasmic reticulum and Golgi apparatus. Curr Opin Cell Biol 7: 530-535.
2. Teasdale RD, Jackson MR, (1996) Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Annu Rev Cell Dev Biol 12: 27-54.
3. Hinners I, Tooze SA, (2003) Changing directions: clathrin-mediated transport between the Golgi and endosomes. J Cell Sci 116: 763-771.
4. Bonifacino JS, (2004) The GGA proteins: adaptors on the move. Nat Rev Mol Cell Biol 5: 23-32.
5. Legendre-Guillemin V, Wasiak S, Hussain NK, Angers A, McPherson PS, (2004) ENTH/ANTH proteins and clathrin-mediated membrane budding. J Cell Sci 117: 9-18.
6. Bonifacino JS, Traub LM, (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72: 395-447.
7. Owen DJ, Collins BM, Evans PR, (2004) Adaptors for clathrin coats: structure and function. Annu Rev Cell Dev Biol 20: 153-191.
8. Owen DJ, (2004) Linking endocytic cargo to clathrin: structural and functional insights into coated vesicle formation. Biochem Soc Trans 32: 1-14.
9. Newell-Litwa K, Seong E, Burmeister M, Faundez V, (2007) Neuronal and non-neuronal functions of the AP-3 sorting machinery. J Cell Sci 120: 531-541.
10. Odorizzi G, Cowles CR, Emr SD, (1998) The AP-3 complex: a coat of many colours. Trends Cell Biol 8: 282-288.
11. Simmen T, Honing S, Icking A, Tikkanen R, Hunziker W, (2002) AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells. Nat Cell Biol 4: 154-159.
12. Aguilar RC, Boehm M, Gorshkova I, Crouch RJ, Tomita K, et al. (2001) Signal-binding specificity of the mu4 subunit of the adaptor protein complex AP-4. J Biol Chem 276: 13145-13152.
13. 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: 425-436.
14. Doray B, Lee I, Knisely J, Bu G, Kornfeld S, (2007) The gamma/sigma1 and alpha/sigma2 hemicomplexes of clathrin adaptors AP-1 and AP-2 harbor the dileucine recognition site. Mol Biol Cell 18: 1887-1896.
15. 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 gamma-sigma1 and AP-3 delta-sigma3 hemicomplexes. J Cell Biol 163: 1281-1290.
16. Kelly BT, McCoy AJ, Spate K, Miller SE, Evans PR, et al. (2008) A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456: 976-979.
17. Vowels JJ, Payne GS, (1998) A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole. Embo J 17: 2482-2493.
18. Darsow T, Burd CG, Emr SD, (1998) Acidic di-leucine motif essential for AP-3-dependent sorting and restriction of the functional specificity of the Vam3p vacuolar t-SNARE. J Cell Biol 142: 913-922.
19. Scott PM, Bilodeau PS, Zhdankina O, Winistorfer SC, Hauglund MJ, et al. (2004) GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nat Cell Biol 6: 252-259.
20. Misra S, Puertollano R, Kato Y, Bonifacino JS, Hurley JH, (2002) Structural basis for acidic-cluster-dileucine sorting-signal recognition by VHS domains. Nature 415: 933-937.
21. Foote C, Nothwehr SF, (2006) The clathrin adaptor complex 1 directly binds to a sorting signal in Ste13p to reduce the rate of its trafficking to the late endosome of yeast. J Cell Biol 173: 615-626.
22. Renard HF, Demaegd D, Guerriat B, Morsomme P, (2010) Efficient ER exit and vacuole targeting of yeast Sna2p require two tyrosine-based sorting motifs. Traffic 11: 931-946.
23. Anitei M, Hoflack B, (2011) Exit from the trans-Golgi network: from molecules to mechanisms. Curr Opin Cell Biol 23: 443-451.
24. Munro S, (1995) An investigation of the role of transmembrane domains in Golgi protein retention. Embo J 14: 4695-4704.
25. Watson RT, Pessin JE, (2001) Transmembrane domain length determines intracellular membrane compartment localization of syntaxins 3, 4, and 5. Am J Physiol Cell Physiol 281: C215-223.
26. Hofherr A, Fakler B, Klocker N, (2005) Selective Golgi export of Kir2.1 controls the stoichiometry of functional Kir2.x channel heteromers. J Cell Sci 118: 1935-1943.
27. Ma D, Taneja TK, Hagen BM, Kim BY, Ortega B, et al. (2011) Golgi export of the Kir2.1 channel is driven by a trafficking signal located within its tertiary structure. Cell 145: 1102-1115.
28. Barfield RM, Fromme JC, Schekman R, (2009) The exomer coat complex transports Fus1p to the plasma membrane via a novel plasma membrane sorting signal in yeast. Mol Biol Cell 20: 4985-4996.
29. Trautwein M, Schindler C, Gauss R, Dengjel J, Hartmann E, et al. (2006) Arf1p, Chs5p and the ChAPs are required for export of specialized cargo from the Golgi. Embo J 25: 943-954.
30. Sanchatjate S, Schekman R, (2006) Chs5/6 complex: a multiprotein complex that interacts with and conveys chitin synthase III from the trans-Golgi network to the cell surface. Mol Biol Cell 17: 4157-4166.
31. Wang CW, Hamamoto S, Orci L, Schekman R, (2006) Exomer: A coat complex for transport of select membrane proteins from the trans-Golgi network to the plasma membrane in yeast. J Cell Biol 174: 973-983.
32. Ziman M, Chuang JS, Schekman RW, (1996) Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol Biol Cell 7: 1909-1919.
33. Valdivia RH, Baggott D, Chuang JS, Schekman RW, (2002) The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev Cell 2: 283-294.
34. Santos B, Snyder M, (1997) Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p. J Cell Biol 136: 95-110.
35. Ziman M, Chuang JS, Tsung M, Hamamoto S, Schekman R, (1998) Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Mol Biol Cell 9: 1565-1576.
36. Copic A, Starr TL, Schekman R, (2007) Ent3p and Ent5p exhibit cargo-specific functions in trafficking proteins between the trans-Golgi network and the endosomes in yeast. Mol Biol Cell 18: 1803-1815.
37. Gueldener U, Heinisch J, Koehler GJ, Voss D, Hegemann JH, (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30: e23.
38. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
39. Bulik DA, Olczak M, Lucero HA, Osmond BC, Robbins PW, et al. (2003) Chitin synthesis in Saccharomyces cerevisiae in response to supplementation of growth medium with glucosamine and cell wall stress. Eukaryot Cell 2: 886-900.
40. Valdivia RH, Schekman R, (2003) The yeasts Rho1p and Pkc1p regulate the transport of chitin synthase III (Chs3p) from internal stores to the plasma membrane. Proc Natl Acad Sci U S A 100: 10287-10292.
41. Braun A, Pinyol R, Dahlhaus R, Koch D, Fonarev P, et al. (2005) EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell 16: 3642-3658.
42. Naslavsky N, Caplan S, (2005) C-terminal EH-domain-containing proteins: consensus for a role in endocytic trafficking, EH? J Cell Sci 118: 4093-4101.
43. Naslavsky N, Rahajeng J, Sharma M, Jovic M, Caplan S, (2006) Interactions between EHD Proteins and Rab11-FIP2: A Role for EHD3 in Early Endosomal Transport. Mol Biol Cell 17: 163-177.
44. de Beer T, Hoofnagle AN, Enmon JL, Bowers RC, Yamabhai M, et al. (2000) Molecular mechanism of NPF recognition by EH domains. Nat Struct Biol 7: 1018-1022.
45. Piper RC, Bryant NJ, Stevens TH, (1997) The membrane protein alkaline phosphatase is delivered to the vacuole by a route that is distinct from the VPS-dependent pathway. J Cell Biol 138: 531-545.
46. Stepp JD, Huang K, Lemmon SK, (1997) The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J Cell Biol 139: 1761-1774.
47. Santos B, Duran A, Valdivieso MH, (1997) CHS5, a gene involved in chitin synthesis and mating in Saccharomyces cerevisiae. Mol Cell Biol 17: 2485-2496.
48. Santos B, Snyder M, (2003) Specific protein targeting during cell differentiation: polarized localization of Fus1p during mating depends on Chs5p in Saccharomyces cerevisiae. Eukaryot Cell 2: 821-825.
49. Barlowe C, (2003) Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol 13: 295-300.
50. Chuang JS, Schekman RW, (1996) Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J Cell Biol 135: 597-610.
51. Kato Y, Misra S, Puertollano R, Hurley JH, Bonifacino JS, (2002) Phosphoregulation of sorting signal-VHS domain interactions by a direct electrostatic mechanism. Nat Struct Biol 9: 532-536.
52. Sikorski RS, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.