A Dictyostelium long chain fatty acyl coenzyme A-synthetase mediates fatty acid retrieval from endosomes

European Journal of Cell Biology

Volumn 82, Issue 10, 2003, Pages 505-514

  von Löhneysen, Katharina ^a   Pawolleck, Nadine ^a   Rühling, Harald ^a   Maniak, Markus ^a  

^a UNIVERSITY OF KASSEL   (Germany)

Author keywords

Endocytosis; Fatty acid metabolism; Phagocytosis

Indexed keywords

FATTY ACID; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LONG CHAIN FATTY ACID COENZYME A LIGASE;

ACIDITY; AMINO ACID SEQUENCE; ARTICLE; CELL MATURATION; CELL MUTANT; CONTROLLED STUDY; CULTURE MEDIUM; CYTOPLASM; CYTOSOL; DICTYOSTELIUM; ENDOSOME; EXOCYTOSIS; GENE MUTATION; GENETIC CODE; HOMOLOGOUS RECOMBINATION; IMMUNOFLUORESCENCE TEST; LIQUID CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING;

DICTYOSTELIUM;

EID: 0242574928     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1078/0171-9335-00342     Document Type: Article

References (50)

1. Adessi, C., Chapel, A., Vincon, M., Rabilloud, T., Klein, G., Satre, M., Garin, J. (1995): Identification of major proteins associated with Dictyostelium discoideum endocytic vesicles. J. Cell Sci. 108, 3331-3337.
2. Baumert, U., Vosskühler, C., Tiedtke, A. (1998): Formation and maturation of phagosomes labeled by magnetic micro particles - an ultrastructural study in Tetrahymena thermophila. Eur. J. Protistol. 34, 291-300.
3. Becker, M., Matzner, M., Gerisch, G. (1999): Drainin required for membrane fusion of the contractile vacuole in Dictyostelium is the prototype of a protein family also represented in man. EMBO J. 18, 3305-3316.
4. Black, P. N., Zhang, Q., Weimar, J. D., DiRusso, C. C. (1997): Mutational analysis of a fatty acyl-coenzyme A synthetase signature motif identifies seven amino acid residues that modulate fatty acid substrate specificity. J. Biol. Chem. 272, 4896-4903.
5. Bof, M., Brénot, F., Gonzalez, C., Klein, G., Martin, J. B., Satre, M. (1992): Dictyostelium discoideum mutants resistant to the toxic action of methylene diphosphonate are defective in endocytosis. J. Cell Sci. 101, 139-144.
6. Bomblies, L., Biegelmann, E., Döring, V., Gerisch, G., Krafft-Czepa, H., Noegel, A. A., Schleicher, M., Humbel, B. M. (1990): Membrane-enclosed crystals in Dictyostelium discoideum cells, consisting of developmentally regulated proteins with sequence similarities to known esterases. J. Cell Biol. 110, 669-678.
7. Cardelli, J. (2001): Phagocytosis and macropinocytosis in Dictyostelium: phosphoinositide-based processes, biochemically distinct. Traffic 2, 311-320.
8. Chiu, H. C., Kovacs, A., Ford, D. A., Hsu, F. F., Garcia, R., Herrero, P., Saffitz, J. E., Schaffer, J. E. (2001): A novel mouse model of lipotoxic cardiomyopathy. J. Clin. Invest. 107, 813-822.
9. Choi, J. Y., Martin, C. E. (1999): The Saccharomyces cerevisiae FAT1 gene encodes an acyl-CoA synthetase that is required for maintenance of very long chain fatty acid levels. J. Biol. Chem. 274, 4671-4683.
10. Desjardins, M., Celis, J. E., van Meer, G., Dieplinger, H., Jahraus, A., Griffiths, G., Huber, L. A. (1994): Molecular characterization of phagosomes. J. Biol. Chem. 269, 32194-32200.
11. Dimond, R. L., Burns, R. A., Jordan, K. B. (1981): Secretion of lysosomal enzymes in the cellular slime mold, Dictyostelium discoideum. J. Biol. Chem. 256, 6565-6572.
12. DiRusso, C. C., Black, P. N. (1999): Long-chain fatty acid transport in bacteria and yeast. Paradigms for defining the mechanism underlying this protein-mediated process. Mol. Cell. Biochem. 192, 41-52.
13. Emans, N., Nzala, N. N., Desjardins, M. (1996): Protein-phosphorylation during phagosome maturation. FEBS Lett. 398, 37-42.
14. Faergeman, N. J., Black, P. N., Zhao, X. D., Knudsen, J., DiRusso, C. C. (2001): The Acyl-CoA synthetases encoded within FAA1 and FAA4 in Saccharomyces cerevisiae function as components of the fatty acid transport system linking import, activation and intracellular utilization. J. Biol. Chem. 276, 37051-37059.
15. Faix, J., Dittrich, W. (1996): DGAP1, a homologue of rasGTPase activating proteins that controls growth, cytokinesis and development in Dictyostelium discoideum. FEBS Lett. 394, 251-257.
16. Fulda, M., Heinz, E., Wolter, F. P. (1994): The fadD gene of Escherichia coli K12 is located close to rnd at 39.6 min of the chromosomal map and is a new member of the AMP-binding protein family. Mol. Gen. Genet. 242, 241-249.
17. Gargiulo, C. E., Stuhlsatz-Krouper, S. M., Schaffer, J. E. (1999): Localization of adipocyte long-chain fatty acyl-CoA synthetase at the plasma membrane. J. Lipid Res. 40, 881-892.
18. Garin, J., Diez, R., Kieffer, S., Dermine, J. F., Duclos, S., Gagnon, E., Sadoul, R., Rondeau, C., Desjardins, M. (2001): The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152, 165-180.
19. Gerisch, G., Albrecht, R., Heizer, C., Hodgkinson, S., Maniak, M. (1995): Chemoattractant-controlled accumulation of coronin at the leading edge of Dictyostelium cells monitored using a green fluorescent protein-coronin fusion protein. Curr. Biol. 5, 1280-1285.
20. Gold, E. S., Morrissette, N. S., Underhill, D. M., Guo, J., Bassetti, M., Aderem, A. (2000): Amphiphysin IIm, a novel amphiphysin II isoform, is required for macrophage phagocytosis. Immunity 12, 285-292.
21. Hacker, U., Albrecht, R., Maniak, M. (1997): Fluid-phase uptake by macropinocytosis in Dictyostelium. J. Cell Sci. 110, 105-112.
22. Hanakam, F., Albrecht, R., Eckerskorn, C., Matzner, M., Gerisch, G. (1996): Myristoylated and non-myristoylated forms of the pH sensor protein hisactophilin II: intracellular shuttling to plasma membrane and nucleus monitored in real time by a fusion with green fluorescent protein. EMBO J. 15, 2935-2943.
23. Hed, J. (1986): Methods for distinguishing ingested from adhering particles. Methods Enzymol. 132, 198-204.
24. Heuser, J., Zhu, Q., Clarke, M. (1993): Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J. Cell Biol. 121, 1311-1327.
25. Jenne, N., Rauchenberger, R., Hacker, U., Kast, T., Maniak, M. (1998): Targeted gene disruption reveals a role for vacuolin B in the late endocytic pathway and exocytosis. J. Cell Sci. 111, 61-70.
26. Klein, K., Steinberg, R., Fiethen, B., Overath, P. (1971): Fatty acid degradation in Escherichia coli. An inducible system for the uptake of fatty acids and further characterisation of old mutants. Eur. J. Biochem. 19, 442-450.
27. Knoll, L. J., Johnson, D. R., Gordon, J. I. (1995): Complementation of Saccharomyces cerevisiae strains containing fatty acid activation gene (FAA) deletions with a mammalian acyl-CoA synthetase. J. Biol. Chem. 270, 10861-10867.
28. Malchow, D., Lüderitz, O., Kickhöfen, B., Westphal, O., Gerisch, G. (1969): Polysaccharides in vegetative and aggregation-competent amoebae of Dictyostelium discoideum. 2. Purification and characterization of amoeba-degraded bacterial polysaccharides. Eur. J. Biochem. 7, 239-246.
29. Malchow, D., Lüderitz, O., Westphal, O., Gerisch, G., Riedel, V. (1967): Polysaccharides of vegetative and aggregationally competent amoebae of the strain Dictyostelium discoideum. 1. In vivo degradation of bacterial lipopolysaccharides. Eur. J. Biochem. 2, 469-479.
30. Maniak, M. (2002): Conserved features of endocytosis in Dictyostelium. Int. Rev. Cytol. 221, 257-287.
31. Maniak, M. (2001): Fluid-phase uptake and transit in axenic Dictyostelium cells. Biochim. Biophys. Acta 1525, 197-204.
32. Maniak M., Rauchenberger, R., Albrecht, R., Murphy, J., Gerisch, G. (1995): Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein tag. Cell 83, 915-924.
33. Meloni, I., Muscettola, M., Raynaud, M., Longo, I., Bruttini, M., Moizard, M. P., Gomot, M., Chelly, J., des Portes, V., Fryns, J. P., Ropers, H. H., Magi, B., Bellan, C., Volpi, N., Yntema, H. G., Lewis, S. E., Schaffer, J. E., Renieri, A. (2002): FACL4, encoding fatty acid-CoA ligase 4, is mutated in nonspecific X-linked mental retardation. Nat. Genet. 30, 436-440.
34. Miyazawa, S., Hashimoto, T., Yokota, S. (1985): Identity of long-chain acyl-coenzyme A synthetase of microsomes, mitochondria and peroxisomes in rat liver. J. Biochem. (Tokyo) 98, 723-733.
35. Monnat, J., Hacker, U., Geissler, H., Rauchenberger, R., Neuhaus, E., Maniak, M., Soldati, T. (1997): Dictyostelium discoideum protein disulfide isomerase, an endoplasmatic reticulum resident enzyme lacking a KDEL-type retrieval signal. FEBS Lett. 418, 357-362.
36. Morrissette, N. S., Gold, E. S., Guo, J., Hamerman, J. A., Ozinsky, A., Bedian, V., Aderem, A. A. (1999): Isolation and characterization of monoclonal antibodies directed against novel components of macrophage phagosomes. J. Cell Sci. 112, 4705-4713.
37. Neuhaus, E. M., Horstmann, H., Almers, W., Maniak, M., Soldati, T. (1998): Ethane-freezing/methanol-fixation of cell monolayers: a procedure for improved preservation of structure and antigenicity for light and electron microscopies. J. Struct. Biol. 121, 326-342.
38. Nolta, K. V., Rodriguez-Paris, J. M., Steck, T. L. (1994): Analysis of successive endocytic compartments isolated from Dictyostelium discoideum by magnetic fractionation. Biochim. Biophys. Acta 1224, 237-246.
39. Oikawa, E., Iijima, H., Suzuki, T., Sasano, H., Sato, H., Kamataki, A., Nagura, H., Kang, M. J., Fujino, T., Suzuki, H., Yamamoto, T. T. (1998): A novel acyl-CoA synthetase, ACS5, expressed in intestinal epithelial cells and proliferating preadipocytes. J. Biochem. (Tokyo) 124, 679-685.
40. Ostermann, J., Orci, L., Tani, K., Amherdt, M., Ravazzola, M., Elazar, Z., Rothman, J. E. (1993): Stepwise assembly of functionally active transport vesicles. Cell 75, 1015-1025.
41. Pfanner, N., Glick, B. S., Arden, S. R., Rothman, J. E. (1990): Fatty acylation promotes fusion of transport vesicles with Golgi cisternae. J. Cell Biol. 110, 955-961.
42. Rauchenberger, R., Hacker, U., Murphy, J., Niewöhner, J., Maniak, M. (1997): Coronin and vacuolin identify consecutive stages of a late, actin-coated endocytic compartment in Dictyostelium. Curr. Biol. 7, 215-218.
43. Schaffer, J. E. (2001): Fatty acid transport: the roads taken. Am. J. Endocrinol. Metab. 282, E239-E246.
44. Troll, H., Malchow, D., Müller-Taubenberger, A., Humbel, B., Lottspeich, F., Ecke, M., Gerisch, G., Schmid, A., Benz, R. (1992): Purification, functional characterization and cDNA sequencing of mitochondrial porin from Dictyostelium discoideum. J. Biol. Chem. 267, 21072-21079.
45. Troll, H., Winckler, T., Lascu, I., Müller, N., Saurin, W., Veron, M., Mutzel, R. (1993): Separate nuclear genes encode cytosolic and mitochondrial nucleoside diphosphate kinase in Dictyostelium discoideum. J. Biol. Chem. 268, 25469-25475.
46. Vosskühler, C., Tiedtke, A. (1993): Magnetic separation of phagosomes of defined age from Tetrahymena thermophila. J. Euk. Microbiol. 40, 556-562.
47. Wienke, D. C., Knetsch, M. L. W., Neuhaus, E. M., Reedy, M. C., Manstein, D. J. (1999): Disruption of a dynamin homologue affects endocytosis, organelle morphology and cytokinesis in Dictyostelium discoideum. Mol. Biol. Cell 10, 225-243.
48. Witke, W., Nellen, W., Noegel, A. (1987): Homologous recombination in the Dictyostelium a-actinin gene leads to an altered mRNA and lack of the protein. EMBO J. 6, 4143-4148.
49. Yuan, A., Chia, C. P. (2000): Role of esterase gp70 and its influence on growth and development of Dictyostelium discoideum. Exp. Cell Res. 261, 336-347.
50. Zou, Z., Tong, F., Faergeman, N. J., Borsting, C., Black, P. N., DiRusso, C. C. (2003): Vectorial acylation in Saccharomyces cerevisiae. Fat1p and fatty acyl-CoA synthetase are interacting components of a fatty acid import complex. J. Biol. Chem. 278, 16414-16422.