Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions

Journal of Cell Biology

Volumn 133, Issue 2, 1996, Pages 305-323

  Jung, Goeh ^a   Wu, Xufeng ^a   Hammer III, John A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; MYOSIN;

ARTICLE; CELL AGGREGATION; CELL MOTILITY; ENDOCYTOSIS; NONHUMAN; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; SARCODINA;

ANIMALS; ANTIBODY SPECIFICITY; CELL AGGREGATION; CELL MOVEMENT; DEXTRANS; DICTYOSTELIUM; ENDOCYTOSIS; FLUORESCENT DYES; KINETICS; MUTATION; MYOSINS; PHAGOCYTOSIS; PINOCYTOSIS; PSEUDOPODIA; RNA, ANTISENSE; RNA, PROTOZOAN; XANTHENES;

EID: 0029925627     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.133.2.305     Document Type: Article

References (61)

1. Bacon, R.A., C J. Cohen, D.A Lewin, and I. Mellman. 1994 Dictyostelium discoideum mutants with temperature-sensitive defects in endocytosis. J Cell Biol. 127:387-399
2. Baines, I.C , H. Brzeska, and E.D. Korn. 1992. Differential localization of Acanthamoeba myosin I isoforrns. J. Cell Biol. 119.1193-1203.
3. Baines, I.C., A. Congliano-Murphy, and E.D. Korn. 1995. Quantification and localization of phosphroylated myosin 1 isoforrns in Acanthamoeba castellanii. J. Cell Biol. 130:591-603.
4. Cohen, C.J., R. Bacon, M Clarke, K Joines, and I Mellman. 1994. Dictyostelium discoideum mutants with conditional defects in phagocytosis. J. Cell Biol. 126:955-966.
5. Condeelis, J. 1993. Understanding the cortex of cawling cells: insights from Dictyostelium. Trends Cell Biol. 3:371-376.
6. Cox, D., J.A. Ridsdale, J. Condeelis, and J. Hartwig. 1994. Genetic deletion of ABP-120 alters the three-dimensional organisation of actin filaments in Dictyostelium pseudopods. J. Cell Biol. 128.819-835.
7. Cupers, P., A. Viethen, A Kiss, P. Bavdhiun, and P.S. Courtoy. 1994. Clathnn polymerization is not required for bulk-phase endocytosis in rat fetal fibroblasts. J. Cell Biol. 127:725-735.
8. DeLozanne, A., and J.A Spudich. 1987 Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination Science (Wash. DC). 236.1080-1091
9. Doberstein, S.K., I.C. Baines, G. Wiegand, E D Korn, and T.D. Pollard. 1993. Inhibition of contractile vacuole function in vivo by antibodies against myosm-I. Nature (Lond.). 356:841-843.
10. Fukui, Y., T.J. Lynch, H. Brzeska, and E.D. Korn. 1989 Myosin I is located at the leading edges of locomoting Diciyostelium amoebae. Nature (Lond.). 341:328-331.
11. Gottlieb, T A., I.E. Ivanov, M. Adesnik, and D.D. Sabatini. 1993. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120:695-710.
12. Hammer, J.A., III. 1994. The structure and function of unconventional myosins: a review. J. Muscle Res Cell Motil. 15:1-10
13. Hammer, J.A., III, and G. Jung. 1996. The sequence of the Dictyostelium myoJ heavy chain gene predicts a novel, dimeric. unconventional myosin with a heavy chain molecular mass of 258 kDa J Biol. Chem 271:7120-7127.
14. Hansen, S H., K. Sandvig, and B. van Deurs. 1993. Molecules internalized by clathrin-independent endocytosis are delivered to endosomes containing transferrin receptors. J. Cell Biol. 123:89-97
15. Hewlett, L J., A.R. Prescott, and C. Watts 1994 The coated pit and macropinocytic pathways serve distinct endosome populations. J. Cell Biol 124. 689-703.
16. Hug, C , P.Y. Jay, I. Reddy, J.G. McNally, P.C. Bridgeman, E.L. Elson, and J.A. Cooper. 1995 Capping protein levels influence actin assembly and cell motility in Dictyostelium. Cell 81:591-600.
17. Janmey, P A 1991. Mechanical properties of cytoskeletal polymers. Curr. Opin. Cell Biol 2:4-11.
18. Jung, G , and J.A. Hammer III. 1990. Generation and characterization of Dictyostelium cells deficient in a myosin I heavy chain isoform J Cell Biol 110:1955-1964.
19. Jung, G., and J.A. Hammer III. 1994 The actin binding site in the tail domain of Diciyostelium myosin IC (myoC) resides within the glycine- and proline-rich sequence (tail homology region 2). FEBS Lett 342.197-201.
20. Jung, G., C.L. Saxe III, A.R. Kimmel, and J A. Hammer III. 1989. Dictyostelium discoideum contains a gene encoding a myosin I heavy chain Proc. Natl. Acad. Sci. USA. 86:6186-6190.
21. Jung, G., Y. Fukui, B. Martin, and J A. Hammer III. 1993. Sequence, expression pattern, intracellular localization and targeted disruption of the Dictyostelium myosin-ID heavy chain isoform. J. Biol. Chem. 268:14981-14990.
22. Klein, G., and M. Satre. 1986. Kinetics of fluid phase pinocytosis in Dictyostelium discoideum amoebae. Biochem Biophys Res Commun. 138: 1140-1152.
23. Korn, E.D., M.A.L. Atkinson, H Brzeska, J.A. Hammer III, G Jung, and T.J. Lynch. 1988. Structure-function studies of Acanthamoeba myosins IA, IB, and II. J. Cell Biochem. 36:37-50.
24. Kubler, E., and H. Riezman. 1983. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO (Eur Mol. Biol. Organ.) J. 12:2855-2862.
25. Laemmli, U.K. 1970. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature (Lond.) 227.680-685.
26. Lee, S., and G.P. Côte. 1993. Isolation and characterization of three Dictyostelium myosin-I isozymes. J. Biol. Chem. 268:20923-20929.
27. McGoldrick, C.A., C Gruver, and G.S. May. 1995. myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth. J. Cell Biol. 128:577-587.
28. Mooseker, M.S., and R.E. Cheney. 1995. Unconventional myosins. Annu. Rev. Cell Develop. Biol. 11:633-675.
29. Nolta, K.V., J.M. Rodriguez-Paris, and T.L. Steck. 1994. Analysis of successive endocytic compartments isolated from Dictyostelium discoideum by magnetic fractionation. Biochem Biophys. Acta. 1224:237-246.
30. Novak, K.D., M.D Peterson, M.C. Reedy, and M.A. Titus. 1995. Dictyostelium myosin I double mutants exhibit conditional defects in pinocytosis. J. Cell Biol. 131:1205-1221.
31. 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.
32. Padh, H , J. Ha, M. Lavasa, and T.L. Steck 1993. A post-lysosomal compartment in Dictyostelium discoideum. J. Biol. Chem 268:6742-6747.
33. Pasternak, C J., J A Spudich, and E Elson. 1989. Capping of surface receptor and concomitant cortical tension are generated by conventional myosin. Nature (Lond.). 341:549-551.
34. Peterson, M.D., K.D. Novak, M.C. Reedy, J.I. Ruman, and M.A. Titus. 1995. Molecular genetic analysis of myoC. a Dictyostelium myosin I. J. Cell Sci. 108:1093-1103.
35. Podolski, J.L., and T.L. Steck. 1990. Length distribution of F-actin in Dictyostelium discoideum. J. Biol. Chem. 265:1312-1318.
36. Pollard, T.D., S.K. Doberstein, and H.G. Zot 1991 Myosin-I. Annu Rev. Physiol. 53:653-681.
37. Racoosin, E.L., and J.A. Swanson. 1992. M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J. Cell Sci 102.867-880.
38. Reinhard, J., A.A. Scheel, D. Diekman, A. Hall, C. Ruppert, and M. Bahler. 1995. A novel type of myosin implicated in signalling by rho family GTPases. EMBO (Eur. Mol. Biol. Organ.) J. 14:697-704.
39. Riezman, H. 1985. Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis. Cell. 40:1001-1009.
40. Riezman, H. 1993. Three clathrin-dependent budding steps and cell polarity. Trends Cell Biol. 3:330-332.
41. Rodriquez-Paris, J.M., and K.V. Nolta, and T.L. Steck 1993. Characterization of lysosomes isolated from Dictyostelium discoideum by magnetic fractionation J. Biol Chem 268:9110-9116.
42. Rosenfeld, S.S., and B. Rener. 1994. The GPQ-rich segment of Dictyostelium myosin IB contains an actin binding site. Biochemistry 33:2322-2328.
43. Rubino, S., and J.V. Small. 1987. The cytoskeleton of spreading Dictyostelium amoebae. Protoplasma 136:63-69.
44. 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.
45. Sambrook, J., F. Fritsch, and T.E. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory. Cold Spring Harbor, New York. 545 pp.
46. Sandvig, K., and B. van Deurs 1994 Endocytosis without clathrin. Trends Cell Biol 4:275-277.
47. Sole, C.K., R.H. Derfler, G.M. Duyk, and D.P. Corey. 1994. Molecular cloning of myosins from bullfrog saccular maculla: a candidate for the hair cell adaption motor. Auditory Neurosci 1:63-75.
48. Soll, D.R., E Voss, B. Varnum-Finney, and D. Wessels. 1988. The dynamic morphology system: a method for quantitating changes in shape, pseudopod formation and motion in normal and mutant amoebae of Dictyostelium discoideum. J. Cell Biochem. 37:177-192.
49. Spudich, J.A., editor. 1987. Dictyostelium discoideum: molecular approaches to cell bioiogy. In Methods in Cell Biology. Vol. 28 Academic Press, New York. 516 pp
50. Stoller, H., C. Ruppert, J. Reinhard, and M. Bahler. 1995. A novel mammalian myosin I from rat with an SH3 domain localizes to Con A inducible, F-actin-rich structures at cell-cell contacts. J. Cell Biol. 129:819-830.
51. Swanson, J A., and S.C. Baer. 1995. Phagocytosis by zippers and triggers. Trends Cell Biol. 5:89-93.
52. Swanson, J.A., and C. Watts 1995. Macropinocytosis. Trends Cell Biol. 5: 424-428.
53. Thomas, J.H. 1993. Thinking about genetic redundancy. Trends Genet. 9: 395-399.
54. Titus, M.A., H.M Warrick, and J.A. Spudich. 1989. Multiple actin-based motor genes in Dictyostelium. Cell Regul. 1:55-63.
55. Titus, M.A., D. Wessels, J A. Spudich, and D Soil 1993. The unconventional myosin encoded by the myo A gene plays a role in Dictyostelium motility. Mol. Cell. Biol. 4:233-246.
56. Titus, M.A., A. Kuspa, and W.F. Loomis. 1994. Discovery of myosin genes by physical mapping in Dictyostelium. Proc. Natl. Acad. Sci. USA. 91: 9446-9450.
57. Urrutia, R A., G. Jung, and J.A. Hammer III. 1993. The Dictyostelium myosin IE heavy chain gene encodes a truncated isoform that lacks sequences corresponding to the actin binding site in the tail. Biochem. Biophys. Acta. 1173:225-229.
58. Varnum, B., K Edwards, and D.R. Soil. 1985. The developmental regulation of single cell motility in Dictyostelium discoideum. Dev. Biol. 113: 218-227.
59. Vogel, G., L. Thilo, H. Schwarz, and R. Steinhart. 1980. Mechanism of phagocytosis is mediated by different recognition sites as disclosed by mutants with altered phagocytic properties. J. Cell Biol. 86:456-465.
60. Watts. C., and M. Marsh. 1992. Endocytosis: what goes in and how? J Cell. Sci 103:1-8.
61. Wessels, D J., J. Murray, G. Jung, J A Hammer III. and D.R. Soll. 1991. Myosin IB null mutants of Dictyostelium exhibit abnormalities in motility. Cell Motil. Cyloskelelon. 20:301-315.