Multiple routes of protein transport from endosomes to the trans Golgi network

FEBS Letters

Volumn 583, Issue 23, 2009, Pages 3811-3816

  Pfeffer, Suzanne R ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endosome; Golgi; Mannose 6 phosphate receptor; Rab GTPase; Shiga and cholera toxin

Indexed keywords

BINDING PROTEIN; CHOLERA TOXIN; PROTEIN TIP47; RAB PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SHIGA TOXIN; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG;

CELL TRANSPORT; ENDOSOME; MAMMAL CELL; MOLECULAR EVOLUTION; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; TRANS GOLGI NETWORK; TRANSPORT KINETICS; VIRUS PARTICLE;

ANIMALS; ENDOCYTOSIS; ENDOSOMES; GOLGI APPARATUS; HUMANS; PROTEIN TRANSPORT; RECEPTOR, IGF TYPE 2; TRANS-GOLGI NETWORK;

MAMMALIA;

EID: 70450223884     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.10.075     Document Type: Review

References (66)

1. Duncan J.R., and Kornfeld S. Intracellular movement of two mannose 6-phosphate receptors: return to the Golgi apparatus. J. Cell. Biol. 106 (1988) 617-628
2. Snider M.D., and Rogers O.C. Intracellular movement of cell surface receptors after endocytosis: resialylation of asialo-transferrin receptor in human erythroleukemia cells. J. Cell. Biol. 100 (1985) 826-834
3. Johannes L., and Popoff V. Tracing the retrograde route in protein trafficking. Cell 1357 (2008) 1175-1187
4. Bonifacino J.S., and Rojas R. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7 (2006) 568-579
5. Mallet W.G., and Maxfield F.R. Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146 (1999) 345-359
6. Mallard F., Antony C., Tenza D., Salamero J., Goud B., and Johannes L. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J. Cell Biol. 143 (1998) 973-990
7. Wilcke M., Johannes L., Galli T., Mayau V., Goud B., and Salamero J. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell. Biol. 151 (2000) 1207-1220
8. Naslavsky N., McKenzie J., Altan-Bonnet N., Sheff D., and Caplan S. EHD3 regulates early-endosome-to-Golgi transport and preserves Golgi morphology. J. Cell. Sci. 122 (2009) 389-400
9. Fuchs E., Haas A.K., Spooner R.A., Yoshimura S., Lord J.M., and Barr F.A. Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways. J. Cell. Biol. 177 (2007) 1133-1143
10. Ghosh P., Dahms N.M., and Kornfeld S. Mannose 6-phosphate receptors: new twists in the t10le. Nat. Rev. Mol. Cell Biol. 4 (2003) 202-212
11. Doray B., Ghosh P., Griffith J., Geuze H.J., and Kornfeld S. Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 297 (2002) 1700-1703
12. Puertollano R., van der Wel N.N., Greene L.E., Eisenberg E., Peters P.J., and Bonifacino J.S. Morphology and dynamics of clathrin/GGA1-coated carriers budding from the trans-Golgi network. Mol. Biol. Cell 14 (2003) 1545-1557
13. Waguri S., Dewitte F., Le Borgne R., Rouille Y., Uchiyama Y., Dubremetz J.F., and Hoflack B. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol. Biol. Cell 14 (2003) 142-155
14. Rodriguez-Gabin A.G., Yin X., Si Q., and Larocca J.N. Transport of mannose-6-phosphate receptors from the trans-Golgi network to endosomes requires Rab31. Exp. Cell Res. 315 (2009) 2215-2230
15. Meyer C., Zizioli D., Lausmann S., Eskelinen E.L., Hamann J., Saftig P., von Figura K., and Schu P. Mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19 (2000) 2193-2203
16. Arighi C.N., Hartnell L.M., Aguilar R.C., Haft C.R., and Bonifacino J.S. Role of the mammalian Retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell. Biol. 165 (2004) 123-133
17. Seaman M.N. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell. Biol. 165 (2004) 111-122
18. Tong P.Y., and Kornfeld S. Ligand interactions of the cation-dependent Mannose 6-phosphate receptor. Comparison with the cation-independent Mannose 6-phosphate receptor. J. Biol. Chem. 264 (1989) 7970-7975
19. Griffiths G., Hoflack B., Simons K., Mellman I., and Kornfeld S. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 12 (1988) 329-341
20. Lombardi D., Soldati T., Riederer M.A., Goda Y., Zerial M., and Pfeffer S.R. Rab9 functions in transport between late endosomes and the trans-Golgi network. EMBO J. 12 (1993) 677-682
21. Riederer M.A., Soldati T., Shapiro A.D., Lin J., and Pfeffer S.R. Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network. J. Cell. Biol. 125 (1994) 573-582
22. Ganley I.G., Carroll K., Bittova L., and Pfeffer S. Rab9 GTPase regulates late endosome size and requires effector interaction for its stability. Mol. Biol. Cell. 15 (2004) 5420-5430
23. Rojas R., van Vlijmen T., Mardones G.A., Prabhu Y., Rojas A.L., Mohammed S., Heck A.J., Raposo G., van der Sluijs P., and Bonifacino J.S. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell. Biol. 183 (2008) 513-526
24. Seaman M.N., Harbour M.E., Tattersall D., Read E., and Bright N. 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 (2009) 2371-2382
25. Barbero P., Bittova L., and Pfeffer S.R. Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J. Cell. Biol. 156 (2002) 511-518
26. Ganley I.G., Espinosa E., and Pfeffer S.R. A syntaxin 10-SNARE complex distinguishes two distinct transport routes from endosomes to the trans-Golgi in human cells. J. Cell. Biol. 180 (2008) 159-172
27. Diaz E., and Pfeffer S.R. TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93 (1998) 433-443
28. Reddy J.V., Burguete A.S., Sridevi K., Ganley I.G., Nottingham R.M., and Pfeffer S.R. A functional role for the GCC185 golgin in mannose 6-phosphate receptor recycling. Mol. Biol. Cell 17 (2006) 4353-4363
29. Espinosa E.J., Calero M., Sridevi K., and Pfeffer S.R. RhoBTB3: a Rho GTPase-family ATPase required for endosome to Golgi transport. Cell 137 (2009) 938-948
30. Saint-Pol A., Yelamos B., Amessou M., Mills I.G., Dugast M., Tenza D., Schu P., Antony C., McMahon H.T., Lamaze C., and Johannes L. Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev. Cell 6 (2004) 525-538
31. Seaman M.N. Cargo-selective endosomal sorting for retrieval to the Golgi requires Retromer. J. Cell. Biol. 165 (2004) 111-122
32. Amessou M., Fradagrada A., Falguieres T., Lord J.M., Smith D.C., Roberts L.M., Lamaze C., and Johannes L. Syntaxin 16 and syntaxin 5 are required for efficient retrograde transport of several exogenous and endogenous cargo proteins. J. Cell. Sci. 120 (2007) 1457-1468
33. Mallard F., Tang B.L., Galli T., Tenza D., Saint-Pol A., Yue X., Antony C., Hong W., Goud B., and Johannes L. Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell. Biol. 156 (2002) 653-664
34. Iversen T.G., Skretting G., Llorente A., Nicoziani P., van Deurs B., and Sandvig K. Endosome to Golgi transport of ricin is independent of clathrin and of the Rab9- and Rab11-GTPases. Mol. Biol. Cell 12 (2001) 2099-2107
35. Smith D.C., Spooner R.A., Watson P.D., Murray J.L., Hodge T.W., Amessou M., Johannes L., Lord J.M., and Roberts L.M. Internalized Pseudomonas exotoxin A can exploit multiple pathways to reach the endoplasmic reticulum. Traffic 7 (2006) 379-393
36. Lu L., Tai G., and Hong W. Autoantigen Golgin-97, an effector of Arl1 GTPase, participates in traffic from the endosome to the trans-Golgi network. Mol. Biol. Cell 15 (2004) 4426-4443
37. Yoshino A., Setty S.R., Poynton C., Whiteman E.L., Saint-Pol A., Burd C.G., Johannes L., Holzbaur E.L., Koval M., McCaffery J.M., and Marks M.S. TGolgin-1 (p230, golgin-245) modulates Shiga-toxin transport to the Golgi and Golgi motility towards the microtubule-organizing centre. J. Cell. Sci. 118 (2005) 2279-2293
38. Lieu Z.Z., Derby M.C., Teasdale R.D., Hart C., Gunn P., and Gleeson P.A. The golgin GCC88 is required for efficient retrograde transport of cargo from the early endosomes to the trans-Golgi network. Mol. Biol. Cell 18 (2007) 4979-4991
39. Diaz E., Schimmoller F., and Pfeffer S.R. A novel Rab9 effector required for endosome-to-TGN transport. J. Cell. Biol. 138 (1997) 283-290
40. Carroll K.S., Hanna J., Simon I., Krise J., Barbero P., and Pfeffer S.R. Role of Rab9 GTPase in facilitating receptor recruitment by TIP47. Science 292 (2001) 1373-1376
41. Derby M.C., Lieu Z.Z., Brown D., Stow J.L., Goud B., and Gleeson P.A. The trans-Golgi network golgin, GCC185, is required for endosome-to-Golgi transport and maintenance of Golgi structure. Traffic 8 (2007) 758-773
42. Hayes G.L., Brown F.C., Haas A.K., Nottingham R.M., Barr F.A., and Pfeffer S.R. Multiple Rab GTPase binding sites in GCC185 suggest a model for vesicle tethering at the trans-Golgi. Mol. Biol. Cell 20 (2009) 209-217
43. Orsel J.G., Sincock P.M., Krise J.P., and Pfeffer S.R. Recognition of the 300K mannose 6-phosphate receptor cytoplasmic domain by TIP47. Proc. Natl. Acad. Sci. USA 97 (2000) 9047-9051
44. Krise J.P., Sincock P.M., Orsel J.G., and Pfeffer S.R. Quantitative Analysis of TIP47 (Tail-interacting protein of 47 kDa)-receptor cytoplasmic domain interactions: implications for endosome-to-trans-Golgi network trafficking. J. Biol. Chem. 275 (2000) 25188-25193
45. Sincock P.M., Ganley I.G., Krise J., Diederichs S., Sivars U., O'Connor B., Ding L., and Pfeffer S.R. Self-assembly is important for TIP47 function in mannose 6-phosphate receptor transport. Traffic 4 (2003) 18-25
46. Hanna J., Carroll K., and Pfeffer S.R. Identification of residues in TIP47 essential for Rab9 binding. Proc. Natl. Acad. Sci. USA 99 (2002) 7450-7454
47. Burguete A.S., Harbury P.B., and Pfeffer S.R. In vitro selection and prediction of TIP47 protein-interaction interfaces. Nat. Meth. 1 (2004) 55-60
48. Hickenbottom S.J., Kimmel A.R., Londos C., and Hurley J.H. Structure of a lipid droplet protein; the PAT family member TIP47. Structure 12 (2004) 1199-1207
49. Burguete A.S., Sivars U., and Pfeffer S. Purification and analysis of TIP47 function in Rab9-dependent mannose 6-phosphate receptor trafficking. Meth. Enzymol. 403 (2005) 357-366
50. Aivazian D., Serrano R.L., and Pfeffer S. TIP47 is a key effector for Rab9 localization. J. Cell. Biol. 173 (2006) 917-926
51. Bickel P.E., Tansey J.T., and Welte M.A. PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim. Biophys. Acta 1791 (2009) 419-440
52. Bulankina A.V., Deggerich A., Wenzel D., Mutenda K., Wittmann J.G., Rudolph M.G., Burger K.N., and Höning S. TIP47 functions in the biogenesis of lipid droplets. J. Cell. Biol. 185 (2009) 641-655
53. Riederer M.A., Soldati T., and Pfeffer S.R. Expression, purification and in vitro isoprenylation of rab9 protein produced in E. coli. Meth. Enzymol. 257 (1995) 15-21
54. Blot G., Janvier K., Le Panse S., Benarous R., and Berlioz-Torrent C. Targeting of the human immunodeficiency virus type 1 envelope to the trans-Golgi network through binding to TIP47 is required for Env incorporation into virions and infectivity. J. Virol. 77 (2003) 6931-6945
55. Lopez-Vergès S., Camus G., Blot G., Beauvoir R., Benarous R., and Berlioz-Torrent C. Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions. Proc. Natl. Acad. Sci. USA 103 (2006) 14947-14952
56. Brass A.L., Dykxhoorn D.M., Benita Y., Yan N., Engelman A., Xavier R.J., Lieberman J., and Elledge S.J. Identification of host proteins required for HIV infection through a functional genomic screen. Science 319 (2008) 921-926
57. Murray J.L., Mavrakis M., McDonald N.J., Yilla M., Sheng J., Bellini W.J., Zhao L., Le Doux J.M., Shaw M.W., Luo C.C., Lippincott-Schwartz J., Sanchez A., Rubin D.H., and Hodge T.W. Rab9 GTPase is required for replication of human immunodeficiency virus type 1, filoviruses, and measles virus. J. Virol. 79 (2005) 11742-11751
58. Chen, Y., Honeychurch, K.M., Yang, G., Byrd, C.M., Harver, C., Hruby, D.E. and Jordan, R. (2009) Vaccinia virus p37 interacts with host proteins associated with LE-derived transport vesicle biogenesis. Virol. J. 6, 44.
59. Burguete A.S., Fenn T.D., Brunger A.T., and Pfeffer S.R. Rab and Arl GTPase family members cooperate in the localization of the golgin GCC185. Cell 132 (2008) 286-298
60. Houghton F.J., Chew P.L., Lodeho S., Goud B., and Gleeson P.A. The localization of the golgin, GCC185 is independent of Rab6A/A′ and Arl1. Cell 138 (2009) 787-794
61. Grigoriev I., Splinter D., Keijzer N., Wulf P.S., Demmers J., Ohtsuka T., Modesti M., Maly I.V., Grosveld F., Hoogenraad C.C., and Akhmanova A. Rab6 regulates transport and targeting of exocytotic carriers. Dev. Cell 13 (2007) 305-314
62. Yamane J., Kubo A., Nakayama K., Yuba-Kubo A., Katsuno T., Tsukita S., and Tsukita S. Functional involvement of TMF/ARA160 in Rab6-dependent retrograde membrane traffic. Exp. Cell Res. 313 (2007) 3472-3485
63. Rink J., Ghigo E., Kalaidzidis Y., and Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122 (2005) 735-749
64. Rivera-Molina, F.E. and Novick, P.J. (2009) A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc. Natl. Acad. Sci. USA 4 [Epub ahead of print].
65. Pérez-Victoria F.J., Mardones G.A., and Bonifacino J.S. Requirement of the human GARP complex for mannose 6-phosphate-receptor-dependent sorting of cathepsin D to lysosomes. Mol. Biol. Cell 19 (2008) 2350-2362
66. Panic B., Perisic O., Veprintsev D.B., Williams R.L., and Munro S. Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus. Mol. Cell. 12 (2003) 863-874