Characterization of the Rab8-specific membrane traffic route linked to protrusion formation

Journal of Cell Science

Volumn 119, Issue 23, 2006, Pages 4866-4877

  Hattula, Katarina ^a   Furujelm, Johanna ^a   Tikkanen, Jaana ^a   Tanhuanpää, Kimmo ^a   Laakkonen, Pirjo ^b   Peränen, Johan ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Arf6; GTPase; Membrane recycling; Protrusion; Rab8

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CHOLERA TOXIN B SUBUNIT; MUTANT PROTEIN; PROTEIN RAB8; RAB PROTEIN; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL ADHESION; CELL COMPARTMENTALIZATION; CELL FUSION; CELL MEMBRANE TRANSPORT; CENTRIOLE; CONTROLLED STUDY; GOLGI COMPLEX; HUMAN; HUMAN CELL; MICROTUBULE; MOLECULAR DYNAMICS; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA INTERFERENCE; STRESS FIBER;

ACTINS; ADP-RIBOSYLATION FACTORS; ANIMALS; CELL COMPARTMENTATION; CELL SURFACE EXTENSIONS; CHOLERA TOXIN; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICROTUBULES; NIH 3T3 CELLS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFERRIN; TUMOR CELLS, CULTURED;

EID: 33845903831     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03275     Document Type: Article

References (57)

1. Ang, A. L., Fölsch, H., Koivisto, U.-M., Pypaert, M. and Mellman, I. (2003). The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J. Cell Biol. 163, 339-350.
2. Armstrong, J., Thompson, N., Squire, J. H., Smith, J., Hayes, B. and Solari, R. (1996). Identification of a novel member of the Rab8 family from the rat basophilic leukemia cell line, RBL.2H3. J. Cell Sci. 109, 1265-1274.
3. Bergmann, J. E., Kupfer, A. and Singer, S. J. (1983). Membrane insertion at the leading edge of motile fibroblasts. Proc. Natl. Acad. Sci. USA 80, 1367-1371.
4. Bertling, E., Hotulainen, P., Mattila, P. K., Matilainen, T., Salminen, M. and Lappalainen, P. (2004). Cyclase-associated protein 1 (CAP1) promotes cofilin-induced actin dynamics in mammalian nonmuscle cells. Mol. Biol. Cell 15, 2324-2334.
5. Bretscher, M. S. (1996). Getting membrane flow and the cytoskeleton to cooperate in moving cells. Cell 15, 601-606.
6. Brown, F. D., Rozelle, A. L., Yin, H. L., Balla, T. and Donaldson, J. G. (2001). Phosphatidylinositol 4, 5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 154, 1007-1017.
7. Buss, F., Luszio, J. P. and Kendrick-Jones, J. (2002). Myosin VI, an actin motor for membrane traffic and cell migration. Traffic 3, 851-858.
8. Chabrillat, M. L., Wilhelm, C., Wasmeier, C., Sviderskaya, E. V., Louvard, D. and Coudrier, E. (2005). Rab8 regulates the actin-based movement of melanosomes. Mol. Biol. Cell 16, 1640-1650.
9. Chen, P., Hutter, D., Liu, P. and Liu, Y. (2002). A mammalian expression system for rapid production and purification of active MAP kinase phosphatases. Protein Expr. Purif. 24, 481-488.
10. Deretic, D., Traverso, V., Parkins, N., Jackson, F., Rodriguez de Turco, E. B. and Ransom, N. (2004). Phosphoinositides, ezrin/moesin, and rac1 regulate fusion of rhodopsin transport carriers in retinal photoreceptors. Mol. Biol. Cell 15, 359-370.
11. D'Souza, C. and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
12. Fukuda, M. (2003). S1p4-a/granuphilin-a inhibits dense-core vesicle exocytosis through interaction with the GDP-bound form of Rab27a in PC12 cells. J. Biol. Chem. 278, 15390-15396.
13. Fukuda, M. and Mikoshiba, K. (2001). Synaptotagmin-like protein 1-3: novel family of C-terminal-type tandem C2 proteins. Biochem. Biophys. Res. Commun. 281, 1226-1233.
14. Fukuda, M., Kanno, E., Saegusa, C., Ogata, Y. and Kuroda, T. S. (2002). Slp4-a/Granuphilin-a regulates dense-core vesicle exocytosis in PC12 cells. J. Biol. Chem. 42, 39673-39678.
15. Furuhjelm, J. and Peränen, J. (2003). The C-terminal end of R-Ras contains a focal adhesion targeting signal. J. Cell Sci. 116, 3729-3738.
16. Gerges, N. Z., Backos, D. S. and Esteban, J. A. (2004). Local control of AMPA recptor traffickinf at the postsynaptic terminal by a small GTPase of the Rab family. J. Biol. Chem. 279, 43870-43878.
17. Hashimoto, S., Onodera, Y., Hashimoto, A., Tanaka, M., Hamaguchi, M., Yamada, A. and Sabe, H. (2004). Requirement for Arf6 in breast cancer invasive activities. Proc. Natl. Acad. Sci. USA 101, 6647-6652.
18. Hattula, K. and Peränen, J. (2000). FIP-2, a coiled-coil protein, links Huntingtin to Rab8 and modulates cellular morphogenesis. Curr. Biol. 10, 1603-1606.
19. Hattula, K., Furuhjelm, J., Arffman, A. and Peränen, J. (2002). A Rab8-specific GDP/GTP exchange factor is involved in actin remodelling and polarized membrane transport. Mol. Biol. Cell 13, 3268-3280.
20. Heat, J. P. and Holifield, B. F. (1991). Cell locomotion: new research tests old indeas on membrane and cytoskeletal flow. Cell Motil. Cytoskeleton 18, 245-257.
21. Hopkins, C. R., Gibson, A., Shipman, M., Strickland, D. K. and Trowbridge, I. S. (1994). In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 125, 1265-1274.
22. Höttä-Vuori, M., Määttä, J., Ulbrich, E., Kuismanen, E. and Ikonen, E. (2000). Mobilization of late-endosimal cholesterol is inhibited by Rab guanine nucleotide dissociation inhibitor. Curr. Biol. 10, 95-98.
23. Huber, L. A., Pimplikar, S., Parton, R. G., Virta, H., Zerial, M. and Simons, K. (1993). Rab8, a small GTPase in vesicular traffic between the TGN and the basolateral plasma membrane. J. Cell Biol. 123, 35-45.
24. Huber, L. A., Dupree, P. and Dotti, C. G. (1995). A deficiency of the small GTPase rab8 inhibits membrane traffic in developing neurons. Mol. Cell. Biol. 15, 918-924.
25. Johnson, J. J., Ellis, B. A., Noack, D., Seabra, M. C. and Catz, S. D. (2005a). The Rab27a-binding protein, JFC1, regulates androgen-dependent secretion of prostate-specific antigen and prostatic-specific acid phospatase. Biochem. J. 391, 699-710.
26. Johnson, J. J., Pacquelet, S., Lane, W. S., Eam, B. and Catz, S. D. (2005b). Akt regulates the subcellular localization of the Rab27a-binding protein JFC1 by phosphorylation. Traffic 6, 667-681.
27. Kametani, F., Usami, M., Tanaka, K., Kume, H. and Mori, H. (2004). Mutant presenilin (A260V) affects Rab8 in PC12D cell. Neurochem. Int. 44, 313-320.
28. Kirkham, M., Fujita, A., Chadda, R., Nixon, S. J., Kurzchalia, T. V., Sharma, D. K., Pagano, R. E., Hancock, J. F., Mayor, S. and Parton, R. G. (2005). Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465-476.
29. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physical integrated molecular process. Cell 84, 358-369.
30. Laukaitis, C. M., Webb, D. J., Donais, K. and Horwitz, A. F. (2001). Differential dynamics of alpha5 integrin, paxillin, and alpha-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153, 1427-1440.
31. MacAdara-Berkowitz, J. K., Catz, S. D., Johnson, J. L., Ruedi, J. M., Thon, V. and Babior, B. M. (2001). JFC1, a novel tandem C2 domain-containing protein associated with the leukocyte NADPH oxidase. J. Biol. Chem. 276, 18855-18962.
32. Massol, R. H., Larsen, J. E., Fujinga, Y., Lencer, W. I. and Kirchhausen, T. (2004). Cholera toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. Mol. Biol. Cell 15, 3631-3641.
33. Mesa, R., Magadán, J., Barbieri, A., López, C., Stahl, P. D. and Mayorga, L. S. (2005). Overexpression of Rab22a hampers the transport between endosomes and the Golgi apparatus. Exp. Cell Res. 304, 339-353.
34. Mitchison, T. J. and Cramer, L. P. (1996). Actin-based cell motility and cell locomotion. Cell 84, 371-379.
35. Moritz, O. L., Tam, B. M., Hurd, L. L., Peränen, J., Deretic, D. and Papermaster, D. S. (2001). Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol. Biol. Cell 12, 2341-2351.
36. Naslavsky, N., Weigert, R. and Donaldson, J. G. (2004). Charcterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 15, 3542-3552.
37. Ng, T., Shima, D., Squire, A., Bastiaens, P. I., Gschmeissner, S., Humphries, M. J. and Parker, F. J. (1999). PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18, 3909-3923.
38. Nobes, C. D. and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
39. Palacios, F., Price, L., Schweitzer, J., Collard, J. G. and D'Souza-Schorey, C. (2001). An essential role for Arf6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20, 4973-4986.
40. Peränen, J. and Furuhjelm, J. (2000). Expression, purification, and properties of Rab8 function in actin cortical skeleton organization and polarized transport. Methods Enzymol. 329, 188-196.
41. Peränen, J., Auvinen, P., Virta, H., Wepf, R. and Simons, K. (1996). Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts. J. Cell Biol. 135, 153-167.
42. Powelka, A. M., Sun, J., Li, J., Gao, M., Shaw, L. M., Sonnenberg, A. and Hsu, V. W. (2004). Stimulation-dependent recycling of integrin beta1 regulated by Arf6 and Rab11. Traffic 5, 20-36.
43. Powell, R. R. and Temesvari, L. A. (2004). Involvement of a Rab8-like protein of Dictyostelium discoideum, Sas1, in the formation of membrane extensions, secretion and adhesion during development. Microbiology 150, 2513-2525.
44. Prignet, M., Dubois, T., Raposo, G., Derrien, V., Tenza, D., Rossé, C., Camonis, J. and Chavrier, P. (2003). Arf6 controls post-endocytic recycling through its downstream exocyst complex effector. J. Cell Biol. 163, 1111-1121.
45. Radhakrishna, H. and Donaldson, J. G. (1997). ADP-ribosylafion factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49-61.
46. Rezaie, T., Child, A., Hitchings, R., Brice, G., Miller, L., Coca-Prados, M., Heon, E., Krupin, T., Ritch, R., Kreutzer, D. et al. (2002). Adult-onset primary open-angle glaucoma caused by mutations in optineurin. Science 295, 1077-1079.
47. Rodriguez, O. C. and Cheney, R. E. (2002). Human myosin-Vc is a novel class V myosin expressed in epithelial cells. J. Cell Sci. 115, 991-1004.
48. Rodriguez-Gabin, A. G., Cammer, M., Amlazan, G., Charron, M. and Larocca, J. N. (2001). Role of rRab22b, an oligodendrocyte protein, in regulation of transport of vesicles from trans Golgi to endocytic compartments. J. Neurosci. Res. 66, 1149-1160.
49. Sahlender, D. A., Roberts, R. C., Arden, S. D., Spudich, G., Taylor, M. J., Luzio, J. P., Kendrick-Jones, J. and Buss, F. (2005). Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J. Cell Biol. 169, 285-295.
50. Santy, L. C. (2002). Characterization of a fast-cycling ADP-ribosylation factor 6 mutant. J. Biol. Chem. 277, 40185-40188.
51. Schlunck, G., Damke, H., Kiosses, W. B., Rusk, N., Symons, M. H., Waterman-Storer, C. M., Schmid, S. L. and Schwartz, M. A. (2004). Modulation of Rac localization and function by dynamin. Mol. Biol. Cell 15, 256-267.
52. Schuck, S., Manninen, A., Honsho, M., Fullekrug, J. and Simons, K. (2004). Generation of single and double knockdowns in polarized epithelial cells by retrovirus-mediated RNA intereference. Proc. Natl. Acad. Sci. USA 101, 4912-4917.
53. Shogomori, H. and Futerman, A. H. (2001). Cholera toxin is found in detergent-insoluble rafts/domains at the cell surface of hippocampal neurons but is internalized via a raft-independent mechanism. J. Biol. Chem. 276, 9182-9188.
54. Ullrich, O., Reinsch, S., Urbé, S., Zerial, M. and Parton, R. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924.
55. Vartiainen, M., Ojala, P. J., Auvinen, P., Peränen, J. and Lappalainen, P. (2000). Mouse A6/twinfilin is an actin monomer-binding protein that localizes to the regions of rapid actin dynamics. Mol. Cell. Biol. 20, 1772-1783.
56. Zerial, M. and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.
57. Zhang, K.-Z., Westberg, J. A., Hölttä, E. and Andersson, L. C. (1996). BCL2 regulates neural differentiation. Proc. Natl. Acad. Sci. USA 93, 4504-4508.