Protein sorting in the Golgi complex: Shifting paradigms

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1744, Issue 3 SPEC. ISS., 2005, Pages 455-464

  Rodriguez Boulan, Enrique ^a   Müsch, Anne ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Default pathway; Golgi complex; Polarized secretion; Protein trafficking; Sorting signal

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; LIPID;

BIOSYNTHESIS; CELL STRUCTURE; CYTOPLASM; ENDOSOME; EXOCYTOSIS; GOLGI COMPLEX; LIPID RAFT; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TRANS GOLGI NETWORK;

EID: 20544431747     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2005.04.007     Document Type: Review

References (94)

1. S.R. Pfeffer, and J.E. Rothman Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi Annu. Rev. Biochem. 56 1987 829 852
2. H.R. Pelham Control of protein exit from the endoplasmic reticulum Annu. Rev. Cell Biol. 5 1989 1 23
3. A. Dautry-Varsat, and H.F. Lodish The Golgi complex and the sorting of membrane and secreted proteins TINS 6 1983 484 490
4. J.E. Rothman, E. Fries, W.G. Dunphy, and L.J. Urbani The Golgi apparatus, coated vesicles, and the sorting problem Cold Spring Harbor Symp. Quant. Biol. 46 2-P 1982 797 805
5. P. Ghosh, N.M. Dahms, and S. Kornfeld Mannose 6-phosphate receptors: new twists in the tale Nat. Rev., Mol. Cell Biol. 4 2003 202 212
6. K. Simons, and A. Wandinger-Ness Polarized sorting in epithelia Cell 62 1990 207 210
7. G. Griffiths, and K. Simons The trans Golgi network: sorting at the exit site of the Golgi complex Science 234 1986 438 443
8. J.S. Bonifacino, and B.S. Glick The mechanisms of vesicle budding and fusion Cell 116 2004 153 166
9. J.S. Bonifacino, and L.M. Traub Signals for sorting of transmembrane proteins to endosomes and lysosomes Annu. Rev. Biochem. 72 2003 395 447
10. E. Rodriguez-Boulan, G. Kreitzer, and A. Musch Organization of vesicular traffic in epithelia Nat. Rev., Mol. Cell Biol. 6 2005 233 247
11. A. Musch, H. Xu, D. Shields, and E. Rodriguez-Boulan Transport of vesicular stomatitis virus G protein to the cell surface is signal mediated in polarized and nonpolarized cells J. Cell Biol. 133 1996 543 558
12. A. Soza Sorting competition with membrane-permeable peptides in intact epithelial cells revealed discrimination of transmembrane proteins not only at the trans-Golgi network but also at pre-Golgi stages J. Biol. Chem. 279 2004 17376 17383
13. G. Kreitzer, A. Marmorstein, P. Okamoto, R. Vallee, and E. Rodriguez-Boulan Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein Nat. Cell Biol. 2 2000 125 127
14. T. Yoshimori, P. Keller, M.G. Roth, and K. Simons Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells J. Cell Biol. 133 1996 247 256
15. C. Yeaman Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network Nat. Cell Biol. 6 2004 106 112
16. K.E. Mostov, A.B. Kops, and D.L. Deitcher Deletion of the cytoplasmic domain of the polymeric immunoglobulin receptor prevents basolateral localization and endocytosis Cell 47 1986 359 364
17. J.E. Casanova, G. Apodaca, and K.E. Mostov An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor Cell 66 1991 65 75
18. W. Hunziker, C. Harter, K. Matter, and I. Mellman Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant Cell 66 1991 907 920
19. K. Matter, W. Hunziker, and I. Mellman Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants Cell 71 1992 741 753
20. C.B. Brewer, and M.G. Roth A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza viral hemagglutin J. Cell Biol. 114 1991 413 421
21. A. Le Bivic An internal deletion in the cytoplasmic tail reverses the apical localization of human NGF receptor in transfected MDCK cells J. Cell Biol. 115 1991 607 618
22. I.R. Nabi, A. Le Bivic, D. Fambrough, and E. Rodriguez-Boulan An endogenous MDCK lysosomal membrane glycoprotein is targeted basolaterally before delivery to lysosomes J. Cell Biol. 115 1991 1573 1584
23. W. Hunziker, and C. Fumey A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells EMBO J. 13 1994 2963
24. B. Wehrle-Haller, and B.A. Imhof Stem cell factor presentation to c-Kit. Identification of a basolateral targeting domain J. Biol. Chem. 276 2001 12667 12674
25. A. Deora The basolateral targeting signal of CD147 (EMMPRIN) consists of a single leucine and is not recognized by Retinal Pigment Epithelium Mol. Biol. Cell 15 2004 4148 4165
26. T.R. Muth, and M.J. Caplan Transport protein trafficking in polarized cells Annu. Rev. Cell Dev. Biol. 19 2003 333 366
27. A. Gut Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins EMBO J. 17 1998 1919 1929
28. N. Nishimura, and W.E. Balch A di-acidic signal required for selective export from the endoplasmic reticulum Science 277 1997 556 558
29. K. Matter, J.A. Whitney, E.M. Yamamoto, and I. Mellman Common signals control low density lipoprotein receptor sorting in endosomes and in the Golgi complex of MDCK cells Cell 74 1993 1053 1064
30. B. Aroeti, and K.E. Mostov Polarized sorting of the polymeric immunoglobulin receptor in the exocytic and endocytic pathway is controlled by the same amino acids EMBO J. 13 1994 2297
31. J.S. Bonifacino, and J. Lippincott-Schwartz Coat proteins: shaping membrane transport Nat. Rev., Mol. Cell Biol. 4 2003 409 414
32. H. Folsch, H. Ohno, J.S. Bonifacino, and I. Mellman A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells Cell 99 1999 189 198
33. T. Simmen, S. Honing, A. Icking, R. Tikkanen, and W. Hunziker AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells Nat. Cell Biol. 4 2002 154 159
34. H. Ohno Mu1B, a novel adaptor medium chain expressed in polarized epithelial cells FEBS Lett. 449 1999 215 220
35. N. Nishimura, H. Plutner, K. Hahn, and W.E. Balch The delta subunit of AP-3 is required for efficient transport of VSV-G from the trans-Golgi network to the cell surface Proc. Natl. Acad. Sci. U. S. A. 99 2002 6755 6760
36. R. Puertollano, R.C. Aguilar, I. Gorshkova, R.J. Crouch, and J.S. Bonifacino Sorting of mannose 6-phosphate receptors mediated by the GGAs Science 292 2001 1712 1716
37. P. Ghosh, J. Griffith, H.J. Geuze, and S. Kornfeld Mammalian GGAs act together to sort mannose 6-phosphate receptors J. Cell Biol. 163 2003 755 766
38. N. Barois, and O. Bakke The adaptor protein AP4 as a component of the clathrin coat machinery: a morphological study Biochem. J. 385 2005 503 510
39. M. Lisanti, I.P. Caras, M.A. Davitz, and E. Rodriguez-Boulan A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells J.Cell Biol. 109 1989 2145 2156
40. D.A. Brown, B. Crise, and J.K. Rose Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells Science 245 1989 1499 1501
41. M. Lisanti, M. Sargiacomo, L. Graeve, A. Saltiel, and E. Rodriguez-Boulan Polarized apical distribution of glycosyl phosphatidylinositol anchored proteins in a renal epithelial line Proc. Nat. Acad. Sci. U. S. A. 85 1988 9557 9561
42. P. Scheiffele, J. Peranen, and K. Simons N-glycans as apical sorting signals in epithelial cells Nature 378 1995 96 98
43. C. Yeaman The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells J. Cell Biol. 139 1997 929 940
44. M. Alfalah O-linked glycans mediate apical sorting of human intestinal sucrase-isomaltase through association with lipid rafts Curr. Biol. 9 1999 593 596
45. E. Rodriguez-Boulan, and A. Gonzalez Glycans in post-Golgi apical targeting: sorting signals or structural props? Trends Cell Biol. 9 1999 291 294
46. M.P. Marzolo, P. Bull, and A. Gonzalez Apical sorting of hepatitis B surface antigen (HBsAg) is independent of N-glycosylation and glycosylphosphatidylinositol-anchored protein segregation Proc. Natl. Acad. Sci. U. S. A. 94 1997 1834 1839
47. M. Bravo-Zehnder Apical sorting of a voltage- and Ca2+-activated K+ channel alpha-subunit in Madin-Darby canine kidney cells is independent of N-glycosylation Proc. Natl. Acad. Sci. U. S. A. 97 2000 13114 13119
48. P. Scheiffele, M.G. Roth, and K. Simons Interaction of influenza virus hemagglutinin with sphingolipid-cholesterol membrane rafts via its transmembrane domain EMBO J. 16 1997 5501 5508
49. A.W. Tai, J.Z. Chuang, C. Bode, U. Wolfrum, and C.H. Sung Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1 Cell 97 1999 877 887
50. T. Takeda, H. Yamazaki, and M.G. Farquhar Identification of an apical sorting determinant in the cytoplasmic tail of megalin Am. J. Physiol.: Cell Physiol. 284 2003 C1105 C1113
51. M.P. Marzolo Differential distribution of low-density lipoprotein-receptor-related protein (LRP) and megalin in polarized epithelial cells is determined by their cytoplasmic domains Traffic 4 2003 273 288
52. Y. Altschuler, C. Hodson, and S.L. Milgram The apical compartment: trafficking pathways, regulators and scaffolding proteins Curr. Opin. Cell Biol. 15 2003 423 429
53. K. Fiedler, and K. Simons The role of N-glycans in the secretory pathway Cell 81 1995 309 312
54. K. Matter, and I. Mellman Mechanisms of cell polarity: sorting and transport in epithelial cells Curr. Opin. Cell Biol. 6 1994 545 554
55. A.D. Marmorstein Saturation of, and competition for entry into, the apical secretory pathway Proc. Natl. Acad. Sci. U. S. A. 97 2000 3248 3253
56. J. Fullekrug, P. Scheiffele, and K. Simons VIP36 localisation to the early secretory pathway J. Cell Sci. 112 Pt 17 1999 2813 2821
57. G. van Meer, and K. Simons Lipid polarity and sorting in epithelial cells J. Cell Biochem. 36 1988 51 58
58. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
59. S. Paladino Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins J. Cell Biol. 167 2004 699 709
60. J.H. Benting, A.G. Rietveld, and K. Simons N-glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells J. Cell Biol. 146 1999 313 320
61. P. Sharma Nanoscale organization of multiple GPI-anchored proteins in living cell membranes Cell 116 2004 577 589
62. L.A. Hannan, M.P. Lisanti, E. Rodriguez-Boulan, and M. Edidin Correctly sorted molecules of a GPI-anchored protein are clustered and immobile when they arrive at the apical surface of MDCK cells J. Cell Biol. 120 1993 353 358
63. P. Scheiffele Caveolin-1 and -2 in the exocytic pathway of MDCK cells J. Cell Biol. 140 1998 795 806
64. R. Puertollano, J.A. Martinez-Menarguez, A. Batista, J. Ballesta, and M.A. Alonso An intact dilysine-like motif in the carboxyl terminus of MAL is required for normal apical transport of the influenza virus hemagglutinin cargo protein in epithelial Madin-Darby canine kidney cells Mol. Biol. Cell 12 2001 1869 1883
65. L. Bonfanti Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation Cell 95 1998 993 1003
66. A. Trucco Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments Nat. Cell Biol. 6 2004 1071 1081
67. J. Malsam, A. Satoh, L. Pelletier, and G. Warren Golgin tethers define subpopulations of COPI vesicles Science 307 2005 1095 1098
68. M.S. Ladinsky, J.R. Kremer, P.S. Furcinitti, J.R. McIntosh, and K.E. Howell HVEM tomography of the trans-Golgi network: structural insights and identification of a lace-like vesicle coat J. Cell Biol. 127 1994 29 38
69. S. Mogelsvang, B.J. Marsh, M.S. Ladinsky, and K.E. Howell Predicting function from structure: 3D structure studies of the mammalian Golgi complex Traffic 5 2004 338 345
70. K. Hirschberg Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells J. Cell Biol. 143 1998 1485 1503
71. R.S. Polishchuk Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane J. Cell Biol. 148 2000 45 58
72. E.V. Polishchuk, A. Di Pentima, A. Luini, and R.S. Polishchuk Mechanism of Constitutive Export from the Golgi: bulk flow via the formation, protrusion, and En Bloc Cleavage of large trans-Golgi network tubular domains Mol. Biol. Cell 14 2003 4470 4485
73. A.W. Tai, J.Z. Chuang, C. Bode, U. Wolfrum, and C.H. Sung Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1 Cell 97 1999 877 887
74. A.W. Tai, J.Z. Chuang, and C.H. Sung Cytoplasmic dynein regulation by subunit heterogeneity and its role in apical transport J. Cell Biol. 153 2001 1499 1509
75. A. Kamal, G.B. Stokin, Z. Yang, C.H. Xia, and L.S. Goldstein Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I Neuron 28 2000 449 459
76. T. Nakagawa A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex Cell 103 2000 569 581
77. Y. Noda KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes J. Cell Biol. 155 2001 77 88
78. C.E. Futter, C.N. Connolly, D.F. Cutler, and C.R. Hopkins Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface J. Biol. Chem. 270 1995 10999 11003
79. E. Orzech, S. Cohen, A. Weiss, and B. Aroeti Interactions between the exocytic and endocytic pathways in polarized Madin-Darby canine kidney cells J. Biol. Chem. 275 2000 15207 15219
80. H. Folsch, M. Pypaert, S. Maday, L. Pelletier, and I. Mellman The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains J. Cell Biol. 163 2003 351 362
81. A.L. Ang Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells J. Cell Biol. 167 2004 531 543
82. J.G. Lock, and J.L. Stow Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin Mol. Biol. Cell 16 2005 1744 1755
83. D.A. Brown, and J.K. Rose Sorting of GPI-anchored proteins to glycolipid enriched membrane subdomains during transport to the apical cell surface Cell 68 1992 533 544
84. P. Arvan, and D. Castle Sorting and storage during secretory granule biogenesis: looking backward and looking forward Biochem. J. 332 Pt 3 1998 593 610
85. A. Le Bivic, F.X. Real, and E. Rodriguez-Boulan Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line Proc. Natl. Acad. Sci. U. S. A. 86 1989 9313 9317
86. T. Simmen, S. Honing, A. Icking, R. Tikkanen, and W. Hunziker AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells Nat. Cell Biol. 4 2002 154 159
87. M.J. Caplan, D.G. Bole, and J.D. Jamieson The Man-6-P receptor is a component of MDCK basolateral plasma membranes J. Cell Biol. 105 1987 60a
88. K. Prydz, A.W. Brandli, M. Bomsel, and K. Simons Surface distribution of the mannose 6-phosphate receptors in epithelial Madin-Darby canine kidney cells J. Biol. Chem. 265 1990 12629 12635
89. A. Godi FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P Nat. Cell Biol. 6 2004 393 404
90. M.A. De Matteis, and A. Godi PI-loting membrane traffic Nat. Cell Biol. 6 2004 487 492
91. Y. Gan, T.E. McGraw, and E. Rodriguez-Boulan The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane Nat. Cell Biol. 8 2002 8
92. Y.J. Wang Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi Cell 114 2003 299 310
93. R. Kroschewski, A. Hall, and I. Mellman Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells Nat. Cell Biol. 1 1999 8 13 (java/Propub/cellbio/ncb0599_8fulltext) (java/Propub/cellbio/ ncb0599_8.abstract)
94. A. Musch, D. Cohen, G. Kreitzer, and E. Rodriguez-Boulan cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network EMBO J. 20 2001 2171 2179