The role of motor proteins in endosomal sorting

Biochemical Society Transactions

Volumn 39, Issue 5, 2011, Pages 1179-1184

  Hunt, Sylvie D ^a   Stephens, David J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Early endosome; Endosomal sorting; Motor protein; Rab protein; Sorting nexin (SNX)

Indexed keywords

CLATHRIN; CYTOPLASMIC DYNEIN; G PROTEIN COUPLED RECEPTOR; KINESIN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MOLECULAR MOTOR; RAB PROTEIN; RAB11 PROTEIN; RAB7 PROTEIN; SNX1 PROTEIN; SNX2 PROTEIN; SNX5 PROTEIN; SNX6 PROTEIN; UNCLASSIFIED DRUG;

CELL ACTIVITY; CELL MIGRATION; CELL SELECTION; DICTYOSTELIUM; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOMAL SORTING; ENDOSOME; GOLGI COMPLEX; LYSOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

ANIMALS; ENDOPLASMIC RETICULUM; ENDOSOMES; GOLGI APPARATUS; HUMANS; MICROTUBULES; MOLECULAR MOTOR PROTEINS; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; TRANSPORT VESICLES;

EID: 80053364693     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0391179     Document Type: Review

References (50)

1. Hsu, V.W. and Prekeris, R. (2010) Transport at the recycling endosome. Curr. Opin. Cell Biol. 22, 528-534
2. Maxfield, F.R. and McGraw, T.E. (2004) Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132 (Pubitemid 38160255)
3. Cullen, P.J. (2008) Endosomal sorting and signalling: an emerging role for sorting nexins. Nat. Rev. Mol. Cell Biol. 9, 574-582
4. 1-adaptin in membrane recycling from endosomes. EMBO J. 22, 2645-2657
5. van der Sluijs, P., Hull, M., Webster, P., Male, P., Goud, B. and Mellman, I. (1992) The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70, 729-740
6. Jovic, M., Sharma, M., Rahajeng, J. and Caplan, S. (2010) The early endosome: a busy sorting station for proteins at the crossroads. Histol. Histopathol. 25, 99-112
7. Bonifacino, J.S. and Hurley, J.H. (2008) Retromer. Curr. Opin. Cell Biol. 20, 427-436
8. van Weering, J.R., Verkade, P. and Cullen, P.J. (2010) SNX-BAR proteins in phosphoinositide-mediated, tubular-based endosomal sorting. Semin. Cell Dev. Biol. 21, 371-380
9. Puthenveedu, M.A. and Von Zastrow, M. (2006) Cargo regulates clathrin-coated pit dynamics. Cell 127, 113-124 (Pubitemid 44466633)
10. Lakadamyali, M., Rust, M.J. and Zhuang, X. (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124, 997-1009 (Pubitemid 43344239)
11. Akhmanova, A. and Hammer, III, J.A. (2010) Linking molecular motors to membrane cargo. Curr. Opin. Cell Biol. 22, 479-487
12. Soppina, V., Rai, A.K., Ramaiya, A.J., Barak, P. and Mallik, R. (2009) Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc. Natl. Acad. Sci. U.S.A. 106, 19381-19386
13. Loubery, S., Wilhelm, C., Hurbain, I., Neveu, S., Louvard, D. and Coudrier, E. (2008) Different microtubule motors move early and late endocytic compartments. Traffic 9, 492-509 (Pubitemid 351351611)
14. Schuster, M., Lipowsky, R., Assmann, M.A., Lenz, P. and Steinberg, G. (2011) Transient binding of dynein controls bidirectional long-range motility of early endosomes. Proc. Natl. Acad. Sci. U.S.A. 108, 3618-3623
15. Delevoye, C., Hurbain, I., Tenza, D., Sibarita, J.B., Uzan-Gafsou, S., Ohno, H., Geerts, W.J., Verkleij, A.J., Salamero, J., Marks, M.S. and Raposo, G. (2009) AP-1 and KIF13A coordinate endosomal sorting and positioning during melanosome biogenesis. J. Cell Biol. 187, 247-264
16. Hoepfner, S., Severin, F., Cabezas, A., Habermann, B., Runge, A., Gillooly, D., Stenmark, H. and Zerial, M. (2005) Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121, 437-450 (Pubitemid 40692303)
17. Driskell, O.J., Mironov, A., Allan, V.J. and Woodman, P.G. (2007) Dynein is required for receptor sorting and the morphogenesis of early endosomes. Nat. Cell Biol. 9, 113-120 (Pubitemid 46024205)
18. Bomsel, M., Parton, R., Kuznetsov, S.A., Schroer, T.A. and Gruenberg, J. (1990) Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell 62, 719-731
19. Aniento, F., Emans, N., Griffiths, G. and Gruenberg, J. (1993) Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123, 1373-1387 (Pubitemid 24012018)
20. Burkhardt, J.K., Echeverri, C.J., Nilsson, T. and Vallee, R.B. (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139, 469-484 (Pubitemid 27459318)
21. Valetti, C., Wetzel, D.M., Schrader, M., Hasbani, M.J., Gill, S.R., Kreis, T.E. and Schroer, T.A. (1999) Role of dynactin in endocytic traffic: effects of dynamitin overexpression and colocalization with CLIP-170. Mol. Biol. Cell 10, 4107-4120
22. Habermann, A., Schroer, T.A., Griffiths, G. and Burkhardt, J.K. (2001) Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles. J. Cell Sci. 114, 229-240
23. Gill, S.R., Schroer, T.A., Szilak, I., Steuer, E.R., Sheetz, M.P. and Cleveland, D.W. (1991) Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115, 1639-1650 (Pubitemid 21910004)
24. Blocker, A., Severin, F.F., Burkhardt, J.K., Bingham, J.B., Yu, H., Olivo, J.C., Schroer, T.A., Hyman, A.A. and Griffiths, G. (1997) Molecular requirements for bi-directional movement of phagosomes along microtubules. J. Cell Biol. 137, 113-129 (Pubitemid 27167300)
25. Tynan, S.H., Purohit, A., Doxsey, S.J. and Vallee, R.B. (2000) Light intermediate chain 1 defines a functional subfraction of cytoplasmic dynein which binds to pericentrin. J. Biol. Chem. 275, 32763-32768
26. Palmer, K.J., Hughes, H. and Stephens, D.J. (2009) Specificity of cytoplasmic dynein subunits in discrete membrane-trafficking steps. Mol. Biol. Cell 20, 2885-2899
27. Tan, S.C., Scherer, J. and Vallee, R.B. (2010) Recruitment of dynein to late endosomes and lysosomes through light intermediate chains. Mol. Biol. Cell 22, 467-477
28. Schmoranzer, J., Fawcett, J.P., Segura, M., Tan, S., Vallee, R.B., Pawson, T. and Gundersen, G.G. (2009) Par3 and dynein associate to regulate local microtubule dynamics and centrosome orientation during migration. Curr. Biol. 19, 1065-1074
29. Horgan, C.P., Hanscom, S.R. and McCaffrey, M.W. (2010) Dynein LIC1 localizes to the mitotic spindle and midbody and LIC2 localizes to spindle poles during cell division. Cell Biol. Int. 35, 171-178
30. Horgan, C.P., Hanscom, S.R., Jolly, R.S., Futter, C.E. and McCaffrey, M.W. (2010) Rab11-FIP3 binds dynein light intermediate chain 2 and its overexpression fragments the Golgi complex. Biochem. Biophys. Res. Commun. 394, 387-392
31. Horgan, C.P., Hanscom, S.R., Jolly, R.S., Futter, C.E. and McCaffrey, M.W. (2010) Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment. J. Cell Sci. 123, 181-191
32. Gupta, V., Palmer, K.J., Spence, P., Hudson, A. and Stephens, D.J. (2008) Kinesin-1 (uKHC/KIF5B) is required for bidirectional motility of ER exit sites and efficient ER-to-Golgi transport. Traffic 9, 1850-1866
33. Welte, M.A. (2010) Bidirectional transport: matchmaking for motors. Curr. Biol. 20, R410-R413
34. Kural, C., Kim, H., Syed, S., Goshima, G., Gelfand, V.I. and Selvin, P.R. (2005) Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308, 1469-1472 (Pubitemid 40791301)
35. Zerial, M. and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117 (Pubitemid 33674039)
36. van Weering, J.R., Verkade, P. and Cullen, P.J. (2009) SNX-BAR proteins in phosphoinositide-mediated, tubular-based endosomal sorting. Semin. Cell. Dev. Biol. 21, 371-380
37. Jordens, I., Marsman, M., Kuijl, C. and Neefjes, J. (2005) Rab proteins, connecting transport and vesicle fusion. Traffic 6, 1070-1077 (Pubitemid 41632260)
38. Haft, C.R., De la Luz Sierra, M., Barr, V.A., Haft, D.H. and Taylor, S.I. (1998) Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol. Cell. Biol. 18, 7278-7287 (Pubitemid 28533047)
39. Carlton, J., Bujny, M., Peter, B.J., Oorschot, V.M., Rutherford, A., Mellor, H., Klumperman, J., McMahon, H.T. and Cullen, P.J. (2004) Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr. Biol. 14, 1791-1800 (Pubitemid 39408768)
40. Traer, C.J., Rutherford, A.C., Palmer, K.J., Wassmer, T., Oakley, J., Attar, N., Carlton, J.G., Kremerskothen, J., Stephens, D.J. and Cullen, P.J. (2007) SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat. Cell Biol. 9, 1370-1380 (Pubitemid 350201750)
41. Skanland, S.S., Walchli, S., Brech, A. and Sandvig, K. (2009) SNX4 in complex with clathrin and dynein: implications for endosome movement. PLoS ONE 4, e5935
42. Wassmer, T., Attar, N., Harterink, M., van Weering, J.R., Traer, C.J., Oakley, J., Goud, B., Stephens, D.J., Verkade, P., Korswagen, H.C. and Cullen, P.J. (2009) The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev. Cell 17, 110-122
43. Puthenveedu, M.A., Lauffer, B., Temkin, P., Vistein, R., Carlton, P., Thorn, K., Taunton, J., Weiner, O.D., Parton, R.G. and Von Zastrow, M. (2010) Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143, 761-773
44. Roux, A., Uyhazi, K., Frost, A. and De Camilli, P. (2006) GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441, 528-531 (Pubitemid 44050156)
45. Dyve, A.B., Bergan, J., Utskarpen, A. and Sandvig, K. (2009) Sorting nexin 8 regulates endosome-to-Golgi transport. Biochem. Biophys. Res. Commun. 390, 109-114
46. Mukhopadhyay, A., Nieves, E., Che, F.Y., Wang, J., Jin, L., Murray, J.W., Gordon, K., Angeletti, R.H. and Wolkoff, A.W. (2011) Proteomic analysis of endocytic vesicles: Rab1a regulates motility of early endocytic vesicles. J. Cell Sci. 124, 765-775
47. Imamura, T., Huang, J., Usui, I., Satoh, H., Bever, J. and Olefsky, J.M. (2003) Insulin-induced GLUT4 translocation involves protein kinase Cλ-mediated functional coupling between Rab4 and the motor protein kinesin. Mol. Cell. Biol. 23, 4892-4900 (Pubitemid 36793335)
48. Satoh, D., Sato, D., Tsuyama, T., Saito, M., Ohkura, H., Rolls, M.M., Ishikawa, F. and Uemura, T. (2008) Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat. Cell Biol. 10, 1164-1171
49. 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. (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183, 513-526
50. Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R. and Neefjes, J. (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11, 1680-1685 (Pubitemid 33037779)