Collective cell migration requires vesicular trafficking for chemoattractant delivery at the trailing edge

Journal of Cell Biology

Volumn 183, Issue 5, 2008, Pages 949-961

  Kriebel, Paul W ^a   Barr, Valarie A ^a   Rericha, Erin C ^a,c   Zhang, Guofeng ^b   Parent, Carole A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

^c The Institute for Research in Electronics and Applied Physics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENYLATE CYCLASE; CHEMOATTRACTANT; CHEMOTACTIC FACTOR; CLATHRIN; HYBRID PROTEIN;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MIGRATION; CELL MOTION; CELL POLARITY; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; EMBRYO DEVELOPMENT; MAMMAL CELL; MEMBRANE TRANSPORT; MEMBRANE VESICLE; METASTASIS; MICROTUBULE; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; WOUND HEALING; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CHEMOTAXIS; DICTYOSTELIUM; ENDOSOME; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN TRANSPORT; TIME; TRANSPORT VESICLE; ULTRASTRUCTURE;

DICTYOSTELIUM DISCOIDEUM; MAMMALIA;

ACTINS; ADENYLATE CYCLASE; ANIMALS; CELL POLARITY; CELLS, CULTURED; CHEMOTACTIC FACTORS; CHEMOTAXIS; CLATHRIN; DICTYOSTELIUM; ENDOSOMES; MICROTUBULES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSPORT VESICLES;

EID: 58149280347     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200808105     Document Type: Article

References (61)

1. Affolter, M., and C.J. Weijer. 2005. Signaling to cytoskeletal dynamics during chemotaxis. Dev. Cell. 9:19-34.
2. Aguado-Velasco, C., and M.S. Bretscher. 1999. Circulation of the plasma membrane in Dictyostelium. Mol. Biol. Cell. 10:4419-4427.
3. Bagorda, A., V.A. Mihaylov, and C.A. Parent. 2006. Chemotaxis: moving forward and holding on to the past. Thromb. Haemost. 95:12-21.
4. Brodsky, F.M., C.Y. Chen, C. Knuehl, M.C. Towler, and D.E. Wakeham. 2001. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17:517-568.
5. Catalfamo, M., T. Karpova, J. McNally, S.V. Costes, S.J. Lockett, E. Bos, P.J. Peters, and P.A. Henkart. 2004. Human CD8+ T cells store RANTES in a unique secretory compartment and release it rapidly after TcR stimulation. Immunity. 20:219-230.
6. Clotworthy, M., and D. Traynor. 2006. On the effects of cycloheximide on cell motility and polarisation in Dictyostelium discoideum. BMC Cell Biol. 7:5.
7. Comer, F.I., and C.A. Parent. 2006. Phosphoinositide 3-kinase activity controls the chemoattractant-mediated activation and adaptation of adenylyl cy-clase. Mol. Biol. Cell. 17:357-366.
8. Comer, EL, C.K. Lippincott, J.J. Masbad, and C.A. Parent. 2005. The PI3K-mediated activation of CRAC independently regulates adenylyl cyclase activation and chemotaxis. Curr. Biol. 15:134-139.
9. Damer, C.K., and T.J. O'Halloran. 2000. Spatially regulated recruitment of clath-rin to the plasma membrane during capping and cell translocation. Mol. Biol. Cell. 11:2151-2159.
10. Devreotes, P., D. Fontana, P. Klein, J. Sherring, and A. Theibert. 1987. Transmembrane signaling in Dictyostelium. Methods Cell Biol. 28:299-331.
11. Dinauer, M.C., S.A. MacKay, and P.N. Devreotes. 1980. Cyclic 3',5'-AMP relay in Dictyostelium discoideum III. The relationship of cAMP synthesis and secretion during the cAMP signaling response. J. Cell Biol. 86:537-544.
12. Dolo, V., A. Ginestra, D. Cassara, S. Violini, G. Lucania, M.R. Torrisi, H. Nagase, S. Canevari, A. Pavan, and M.L. Vittorelli. 1998. Selective localization of matrix metalloproteinase 9, beta1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells. Cancer Res. 58:4468-4474.
13. Eddy, R.J., L.M. Pierini, and F.R. Maxfield. 2002. Microtubule asymmetry during neutrophil polarization and migration. Mol. Biol. Cell. 13:4470-4483.
14. Franca-Koh, J., Y. Kamimura, and P. Devreotes. 2006. Navigating signaling networks: chemotaxis in Dictyostelium discoideum. Curr. Opin. Genet. Dev. 16:333-338.
15. Franke, J., and R.H. Kessin. 1992. The cyclic nucleotide phosphodiesterases of Dictyostelium discoideum: molecular genetics and biochemistry. Cell. Signal. 4:471-478.
16. Gerald, N.J., C.K. Damer, T.J. O'Halloran, and A. De Lozanne. 2001. Cytokinesis failure in clathrin-minus cells is caused by cleavage furrow instability. Cell Motil. Cytoskeleton. 48:213-223.
17. Giepmans, B.N., S.R. Adams, M.H. Ellisman, and R.Y. Tsien. 2006. The fluorescent toolbox for assessing protein location and function. Science. 312:217-224.
18. Gundersen, G.G., and J.C. Bulinski. 1988. Selective stabilization of micro-tubules oriented toward the direction of cell migration. Proc. Natl. Acad. Sci. USA. 85:5946-5950.
19. Gundersen, G.G., E.R. Gomes, and Y. Wen. 2004. Cortical control of microtubule stability and polarization. Curr. Opin. Cell Biol. 16:106-112.
20. Hacker, U., R. Albrecht, and M. Maniak. 1997. Fluid-phase uptake by macropi-nocytosis in Dictyostelium. J. Cell Sci. 110:105-112.
21. Hammer, J.A., III, and G. Jung. 1996. The sequence of the Dictyostelium myo J heavy chain gene predicts a novel, dimeric, unconventional myosin with a heavy chain molecular mass of 258 kDa. J. Biol. Chem. 271:7120-7127.
22. Hawari, F.I., F.N. Rouhani, X. Cui, Z.X. Yu, C. Buckley, M. Kaler, and S.J. Levine. 2004. Release of full-length 55-kDa TNF receptor 1 in exosome-like vesicles: a mechanism for generation of soluble cytokine receptors. Proc. Natl. Acad. Sci. USA. 101:1297-1302.
23. Heijnen, H.F., A.E. Schiel, R. Fijnheer, H.J. Geuze, and J.J. Sixma. 1999. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multi-vesicular bodies and alpha-granules. Blood. 94:3791-3799.
24. Hintermann, R., and R.W. Parish. 1979. The intracellular location of adenylyl cyclase in the cellular slime molds Dictyostelium discoideum and Polysphondylium pallidum. Exp. Cell Res. 123:429-434.
25. Kimmel, A.R., and C.A. Parent. 2003. The signal to move: D. discoideum go orienteering. Science. 300:1525-1527.
26. Kriebel, P.W., and C.A. Parent. 2004. Adenylyl cyclase expression and regulation during the differentiation of Dictyostelium discoideum. IUBMB Life. 56:541-546.
27. Kriebel, P.W., V.A. Barr, and C.A. Parent. 2003. Adenylyl cyclase localization regulates streaming during chemotaxis. Cell. 112:549-560.
28. Kupfer, A., D. Louvard, and S.J. Singer. 1982. Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc. Natl. Acad. Sci. USA. 79:2603-2607.
29. Laemmli, U.K. 1970. Cleavage of sructural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
30. Maeda, Y., and G. Gerisch. 1977. Vesicle formation in Dictyostelium discoideum cells during oscillations of cAMP synthesis and release. Exp. Cell Res. 110:119-126.
31. Mayer, C., K. Maaser, N. Daryab, K.S. Zanker, E.B. Brocker, and P. Friedl. 2004. Release of cell fragments by invading melanoma cells. Eur. J. Cell Biol. 83:709-715.
32. Neujahr, R., R. Albrecht, J. Kohler, M. Matzner, J.M. Schwartz, M. Westphal, and G. Gerisch. 1998. Microtubule-mediated centrosome motility and the positioning of cleavage furrows in multinucleate myosin II-null cells. J. Cell Sci. 111:1227-1240.
33. Niggli, V. 2003. Microtubule-disruption-induced and chemotactic-peptide- induced migration of human neutrophils: implications for differential sets of signalling pathways. J. Cell Sci. 116:813-822.
34. Niswonger, M.L., and T.J. O'Halloran. 1997. Clathrin heavy chain is required for spore cell but not stalk cell differentiation in Dictyostelium discoideum. Development. 124:443-451.
35. O'Halloran, T.J., and R.G. Anderson. 1992. Clathrin heavy chain is required for pinocytosis, the presence of large vacuoles, and development in Dictyostelium. J. Cell Biol. 118:1371-1377.
36. Parent, C.A. 2004. Making all the right moves: chemotaxis in neutrophils and Dictyostelium. Curr. Opin. Cell Biol. 16:4-13.
37. Parent, C.A., and P.N. Devreotes. 1996a. Constitutively active adenylyl cyclase mutant requires neither G proteins nor cytosolic regulators. J. Biol. Chem. 271:18333-18336.
38. Parent, C.A., and P.N. Devreotes. 1996b. Molecular genetics of signal transduc-tion in Dictyostelium. Annu. Rev. Biochem. 65:411-440.
39. Parent, C.A., B.J. Blacklock, W.M. Froehlich, D.B. Murphy, and P.N. Devreotes. 1998. G protein signaling events are activated at the leading edge of chemo-tactic cells. Cell. 95:81-91.
40. Peterson, M.D., A.S. Urioste, and M.A. Titus. 1996. Dictyostelium discoideum myoJ: a member of a broadly denned myosin V class or a class XI unconventional myosin? J. Muscle Res. Cell Motil. 17:411-424.
41. Polishchuk, R.S., E.V. Polishchuk, P. Marra, S. Alberti, R. Buccione, A. Luini, and A. A. Mironov. 2000. Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J. Cell Biol. 148:45-58.
42. Raposo, G., H.W. Nijman, W. Stoorvogel, R. Liejendekker, C.V. Harding, C.J. Melief, and H.J. Geuze. 1996. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183:1161-1172.
43. Ratner, S., W.S. Sherrod, and D. Lichlyter. 1997. Microtubule retraction into the uropod and its role in T cell polarization and motility. J. Immunol. 159:1063-1067.
44. Reipert, S., I. Fischer, and G. Wiche. 2004. High-pressure freezing of epithelial cells on sapphire coverslips. J. Microsc. 213:81-85.
45. Ridley, A.J., M.A. Schwartz, K. Burridge, R.A. Firtel, M.H. Ginsberg, G. Borisy, J.T. Parsons, and A.R. Horwitz. 2003. Cell migration: integrating signals from front to back. Science. 302:1704-1709.
46. Ruscetti, T., J.A. Cardelli, M.L. Niswonger, and T.J. O'Halloran. 1994. Clathrin heavy chain functions in sorting and secretion of lysosomal enzymes in Dictyostelium discoideum. J. Cell Biol. 126:343-352.
47. Sasaki, A.T., C. Chun, K. Takeda, and R.A. Firtel. 2004. Localized Ras signaling at the leading edge regulates PI3K, cell polarity, and directional cell movement. J. Cell Biol. 167:505-518.
48. Taverna, S., G. Ghersi, A. Ginestra, S. Rigogliuso, S. Pecorella, G. Alaimo, F. Saladino, V. Dolo, P. Dell'Era, A. Pavan, et al. 2003. Shedding of membrane vesicles mediates fibroblast growth factor-2 release from cells. J. Biol. Chem. 278:51911-51919.
49. Thery, C., L. Zitvogel, and S. Amigorena. 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2:569-579.
50. Uchida, K., and S. Yumura. 1999. Novel cellular tracks of migrating Dictyostelium cells. Eur. J. Cell Biol. 78:757-766.
51. Van Haastert, P.J., and P.N. Devreotes. 2004. Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell Biol. 5:626-634.
52. Vida, T.A., and S.D. Emr. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128:779-792.
53. Wang, J., V.C. Virta, K. Riddelle-Spencer, and T.J. O'Halloran. 2003. Compromise of clathrin function and membrane association by clathrin light chain deletion. Traffic. 4:891-901.
54. Weiner, O.D., P.O. Neilsen, G.D. Prestwich, M.W. Kirschner, L.C. Cantley, and H.R. Bourne. 2002. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4:509-513.
55. Wessels, D., J. Reynolds, O. Johnson, E. Voss, R. Burns, K. Daniels, E. Garrard, T.J. O'Halloran, and D.R. Soll. 2000. Clathrin plays a novel role in the regulation of cell polarity, pseudopod formation, uropod stability and motility in Dictyostelium. J. Cell Sci. 113:21-36.
56. Wu, X., X. Xiang, and J.A. Hammer III. 2006. Motor proteins at the microtubule plus-end. Trends Cell Biol. 16:135-143.
57. Xiao, Z., N. Zhang, D.B. Murphy, and P.N. Devreotes. 1997. Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J. Cell Biol. 139:365-374.
58. Xu, J., F. Wang, A. Van Keymeulen, M. Rentel, and H.R. Bourne. 2005. Neutrophil microtubules suppress polarity and enhance directional migration. Proc. Natl. Acad. Sci. USA. 102:6884-6889.
59. Yamaguchi, H., J. Wyckoff, and J. Condeelis. 2005. Cell migration in tumors. Curr. Opin. Cell Biol. 17:559-564.
60. Zhu, Q., and M. Clarke. 1992. Association of calmodulin and an unconventional myosin with the contractile vacuole complex of Dictyostelium discoideum. J. Cell Biol. 118:347-358.
61. Zitvogel, L., A. Regnault, A. Lozier, J. Wolfers, C. Flament, D. Tenza, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena. 1998. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 4:594-600.