Evidence for a recycling role for Rab7 in regulating a late step in endocytosis and in retention of lysosomal enzymes in Dictyostelium discoideum

Molecular Biology of the Cell

Volumn 8, Issue 7, 1997, Pages 1343-1360

  Buczynski, Greg ^a   Bush, John ^a,b   Zhang, Linyi ^a   Rodriguez Paris, Juan ^a   Cardelli, James ^a  

^a LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

^b University of Arkansas   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA MANNOSIDASE; GUANOSINE TRIPHOSPHATASE; HYDROLASE; LYSOSOME ENZYME; RAB PROTEIN;

ARTICLE; CELL LINE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; ENDOCYTOSIS; INTERNALIZATION; LYSOSOME; MEMBRANE VESICLE; MOLECULAR CLONING; PRIORITY JOURNAL;

DICTYOSTELIUM DISCOIDEUM; MAMMALIA;

EID: 0030820676     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.7.1343     Document Type: Article

References (65)

1. Aubry, L., Klein, G., Martiel, J., and Satre, M. (1993). Kinetics of endosomal pH evolution in Dictyostelium discoideum amoebae. J. Cell Sci. 305, 861-866.
2. Bucci, C., Parton, R., Mather, I., Stunnenberg, H., Simons, K., Hoflack, B., and Zerial, M. (1992). The GTPase Rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70, 715-728.
3. Buczynski, G., Grove, B., Nomura, A., Kleve, M., Bush, J., Firtel, R., and Cardelli, J. (1997). Inactivation of two Dictyostelium genes, DdPIK1 and DdPIK2, encoding proteins related to mammalian phosphatidylinositide 3-kinases results in defects in endocytosis, lyso- some to post-lysosome transport and actin cytoskeleton organization. J. Cell Biol. 136, 1271-1286.
4. Bush, J., and Cardelli, J. (1989). Processing, transport, and secretion of acid phosphatase in Dictyostelium discoideum. J. Biol. Chem. 264, 7630-7636.
5. Bush, J., and Cardelli, J. (1995). Dictyostelium discoideum rab and rho related genes. In: Guidebook to the Small Molecular Weight GT-Pases, ed. M. Zerial, L. Huber, and J. Tooze, London: Oxford University Press, 385-390.
6. Bush, J., Franek, K., and Cardelli, J. (1993a). Cloning and characterization of seven novel Dictyostelium discoideum rac-related genes belonging to the rho family of GTPases. Gene 136, 61-68.
7. Bush, J., Franek, K., Daniel, J., Speigelman, G., Weeks, G., and Cardelli, J.A. (1993b). Cloning and characterization of five novel Dictyostelium discoideum rab-related genes. Gene 136, 55-60.
8. +-ATPases in reticular membranes of the contractile vacuole complex and lysosomes. J. Cell Sci. 107, 2801-2812.
9. Bush, J., Temesvari, L., Rodriguez-Paris, J., Buczynski, G., and Cardelli, J. (1996). A role for a Rab4-like GTPase in endocytosis and in regulation of contractile vacuole structure and function in Dictyostelium discoideum Mol. Biol. Cell 7, 1623-1638.
10. Cardelli, J. (1993). Regulation of lysosomal trafficking and function during growth and development of Dictyostelium discoideum. In: Endosomes and Lysosomes: A Dynamic Relationship, ed. B. Storrie and R. Murphy, Greenwich, CT: JAI Press, 341-390.
11. Cardelli, J.A., Golumbeski, G.S., and Dimond, R.L. (1986). Lysosomal enzymes in Dictyostelium discoideum are transported at distinctly different rates. J. Cell Biol. 102, 1264-1270.
12. Cardelli, J.A., Richardson, J.M., and Miears, D. (1989). Role of acidic intracellular compartments in the biosynthesis of Dictyostelium lysosomal enzymes: the weak bases ammonium chloride and chloroquine differentially affect proteolytic processing and sorting. J. Biol. Chem. 264, 3454-3463.
13. Cardelli, J.A., Schatzle, J., Bush, J.M., Richardson, J.M., Ebert, D.L., and Freeze, H.H. (1990). Biochemical and genetic analysis of the biosynthesis, sorting and secretion of Dictyostelium lysosomal enzymes. Dev. Genet. 21, 454-462.
14. Chavrier, P., Parton, R.G., Hauri, H.P., Simons, K., and Zerial, M. (1990). Localization of low molecular weight GTP-binding proteins to exocytic and endocytic compartments. Cell 62, 317-329.
15. Cohen, C., Bacon, R., Clarke, M., Joiner, K., and Mellman, I. (1994). Dictyostelium mutants with conditional defects in phagocytosis. J. Cell Biol. 126, 955-966.
16. Daniels, J., Bush, J., Cardelli, J. Spiegelman, G., and Weeks, G. (1993), Characterization of two novel ras genes that are maximally expressed during aggregation of Dictyostelium. Oncogene 9, 501-509.
17. Desjardin, M., Celis, J., van Meer, G., Dieplinger, H., Jahraus, A., Griffiths, G., and Huber, L. (1994). Molecular characterization of phagosomes. J. Biol. Chem. 269, 32194-32200.
18. Farnsworth, C., and Feig, L. (1991). Dominant inhibitory mutations in the magnesium binding site of RasH prevent its activation by GTP. Mol. Cell. Biol. 11, 4822-4829.
19. Feig, L., and Cooper, G., (1988). Inhibition of NIH 3T3 cell proliferation by mutated Ras proteins with preferential affinity for GDP. Mol. Cell. Biol. 8, 3235-3243.
20. Feng, Y., Press, B., and Wandinger-Ness, A. (1995). Rab7: An important regulator of late endocytic membrane traffic. J. Cell Biol. 131, 1435-1452.
21. +-ATPase of Dictyostelium discoideum: a monoclonal antibody study. J. Cell Sci. 106, 1103-1113.
22. H-ras: an experimental and theoretical study. Biochemistry 33, 3237-3244.
23. Freeze, H.H., Bush, J., and Cardelli, J. (1990). Biochemical and genetic analysis of an antigenic determinant found on N-linked oligosaccharides in Dictyostelium. Dev. Genet. 11, 463-472.
24. Heuser, J., Zhu, Q., and Clarke, M. (1993). Proton pumps populate the contractile vacuoles of Dictyostelium discoideum. J. Cell Biol. 121, 1311-1327.
25. Jahraus, A., Storrie, B., Griffiths, G., and Desjardin, M. (1994). Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosomal compartment. J. Cell Sci. 107, 145-157.
26. H-ras. J. Biol. Chem. 268, 923-929.
27. Jung, G., Wu, X., and Hammer, J. (1996). Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions. J. Cell Biol. 133, 305-323.
28. Laemmli, U.K. (1970). Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680-685.
29. Lombardi, D., Soldati, T., Riederer, N., Goda, Y., Zerial, M., and Pfeffer, S. (1993). Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 72, 677-682.
30. Maniak, M., Rauchenberger, R., Albrecht, R., Murphy, J., and Gerish, G. (1995). Coronin involved in phagocytosis: dynamics of particle induced relocalization visualized by green fluorescent protein tag. Cell 83, 915-924.
31. Martinez, O., Schmidt, A., Salamero, J., Hoflack, B., Roa, M., and Goud, B. (1994), The small GTP-binding protein rab6 functions in intra-Golgi transport. J. Cell Biol. 727, 1575-1588.
32. Meresse, S., Gorvel, J., and Chavrier, P. (1995). The Rab7 GTPase resides in a vesicular compartment connected to lysosomes. J. Cell Sci. 108, 3349-3358.
33. Mierendorf, R.C., Cardelli, J.A., and Dimond, R.L. (1985). Pathways involved in targeting and secretion of a lysosomal enzyme in Dictyostelium discoideum. J. Cell Biol. 100, 1777-1787.
34. Mikaelian, I., and Sergeant, A. (1992). A general and fast method to generate multiple site directed mutations. Nucleic. Acids Res. 20, 376.
35. Nolta, K., Padh, H., and Steck, T. (1993). An immunochemical analysis of the vacuolar proton pump in Dictyostelium discoideum. J. Cell Sci. 105, 849-859.
36. Nolta, K., Rodriguez-Paris, J., and Steck, T. (1995). Analysis of successive endocytic compartments isolated from Dictyostelium discoideum by magnetic fractionation. Biochim. Biophys. Acta 1224, 237-246.
37. Novak, K., Peterson, M., Reedy, M.C., and Titus, M. (1995). Dictyostelium myosin I double mutants exhibit conditional defects in pinocytosis. J. Cell Biol. 131, 1205-1221.
38. O'Halloran, T.J., and Anderson, R.G. (1992). Clathrin heavy chain is required for pinocytosis, the presence of large vacuoles, and development in Dictyostelium. J. Cell Biol. 118, 1371-1377.
39. Padh, H., Ha, J., Lavasa, M., and Steck, T.L. (1993). A post-lysosomal compartment in Dictyostelium discoideum. J. Biol. Chem. 268, 6742-6747.
40. Padh, H., and Tanjore, S. (1995). Colocalization of cyclic AMP receptors with acidosomes in Dictyostelium. FEBS Lett. 368, 358-362.
41. Papini, E., Satin, B., Bucci, C., de Bernard, M., Telford, J.L., Manetti, R., Rappuoli, R., Zerial, M., and Montecucco, C. (1997). The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicolacter pylori cytotoxin. EMBO J. 16, 15-24.
42. Pfeffer, S., (1994). Rab GTPases: master regulators of membrane trafficking. Curr. Biol. 6, 522-526.
43. Rezabek, B., Rodriguez-Paris, J., Cardelli, J., and Chia, C. (1997). Characterization of phagosomal proteins in Dictyostelium discoideum. J. Eukaryot. Microbiol. (in press).
44. Richardson, J.R., Woychik, N.A., Ebert, D.L., Dimond, R.L., and Cardelli, J.A. (1988). Inhibition of early but not late proteolytic processing events induces the missorting and oversecretion of precursor forms of lysosomal enzymes in Dictyostelium discoideum. J. Cell Biol. 107, 2097-2107.
45. Riederer, M., Soldati, T., Shapiro, A., Lin, J., and Pfeffer, S. (1994). Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network. J. Cell Biol. 125, 573-582.
46. Rodriguez-Paris, J., Grove, B., Buczynski, G., and Cardelli, J. (1996). Phosphatidylinositide 3-kinases regulate a late stage in phagocytosis in Dictyostelium. Mol. Biol. Cell 7, 593a (Abstract).
47. Rodriguez-Paris, J.M., Nolta, K.V., and Steck, T.L. (1993). Characterization of lysosomes isolated from Dictyostelium discoideum by magnetic fractionation. J. Biol. Chem. 268, 9110-9116.
48. Rothman, J.E., and Wieland, T. (1996). Protein sorting by transport vesicles. Science 272, 227-234.
49. Ruscetti, T., Cardelli, J., Niswonger, M., and O'Halloran, T. (1994). The clathrin heavy chain functions in the sorting and secretion of lysosomal enzymes in D. discoideum. J. Cell Biol, 126, 343-352.
50. Sadeghi, H., DaSilva, A.M., and Klein, C. (1988). Evidence that a glycoprotein tail anchors antigen 117 to the plasma membrane of Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA 85, 5512-5515.
51. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
52. Saxe, S., and Kimmel, A.R. (1990). SAS1 and SAS2, GTP-binding protein genes in Dictyostelium discoideum with sequence similarities to essential genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 2367-2378.
53. Schimmoller, F., and Riezman, H. (1993). Involvement of Ypt7P, a small GTPase, in traffic from late endosomes to the vacuole in yeast. J. Cell Sci. 106, 823-830.
54. Temesvari, L., Bush, J., Peterson, M., Titus, M., and Cardelli, J. (1996a). Examination of the endosomal and lysosomal pathways in Dictyostelium discoideum myosin I mutants. J. Cell Sci. 109, 663-673.
55. +-ATPase subunits. J. Biol. Chem. 269, 25719-25727.
56. Temesvari, L., Rodriguez-Paris, J., Bush, J., Zhang, L., and Cardelli, J. (1996b). Involvement of the vacuolar proton-translocating ATPase in multiple steps of the endo-lysosomal system and in the contractile vacuole system of Dictyostelium discoideum. J. Cell Sci. 209, 1479-1495.
57. Thilo, L., and Vogel, G. (1980). Kinetics of membrane internalization and recycling during pinocytosis in Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA 77, 1015-1019.
58. Valencia, A., Chardin, P., Wittinghofer, A., and Sander, C. (1991). The ras protein family & evolutionary tree and role of conserved amino acids. Biochemistry 30, 4637-4648.
59. 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.
60. van der Sluijs, P., Hull, M., Zahraoui, A., Tavitian, A., Goud, B., and Mellman, I. (1991). The small GTP binding protein Rab4 is associated with early endosomes. Proc. Natl. Acad. Sci. USA 88, 6313-6317.
61. Vitelli, R., Santillo, M., Lattero, D., Chiariello, M., Bifalco, M., Bruni, C.B., and Bucci, C. (1997). Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem. 272, 4391-4397.
62. Vogel, G., Thilo, L., Schwarz, H., and Steinhart, N. (1980). Mechanism of phagocytosis in Dictyostelium: phagocytosis is mediated by different recognition sites as described by mutant with altered phagocytic properties. J. Cell Biol. 86, 456-465.
63. Wichmann, H., Hengst, L, and Gallwitz, D. (1992). Endocytosis in yeast: evidence for the involvement of a small GTP binding protein (Ypt7p). Cell 71, 1131-1142.
64. Wood, L., and Kaplan, A. (1985). Transit of α-mannosidase during its maturation in Dictyostelium discoideum. J. Cell Biol. 101, 2063-2069.
65. Wu, L., Valkema, R., Van Haastert, P., and Devreotes, P. (1995), The G-protein β subunit is essential for multiple responses to chemoattractants in Dictyostelium. J. Cell Biol. 129, 1667-1675.