The role of actin, actomyosin and microtubules in defining cell shape during the differentiation of Naegleria amebae into flagellates

European Journal of Cell Biology

Volumn 86, Issue 2, 2007, Pages 85-98

  Walsh, Charles J ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Actin; Actomyosin; Cytoskeleton; Microtubules; Naegleria; Tubulin

Indexed keywords

ACTIN; ANTIBODY; CYTOCHALASIN D; DEOXYRIBONUCLEASE I; F ACTIN; G ACTIN; LATRUNCULIN A; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN KINASE; PHALLOIDIN; TUBULIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL SHAPE; CONFOCAL MICROSCOPY; CYTOSKELETON; FLAGELLATE; FLUORESCENCE MICROSCOPY; MICROTUBULE; NAEGLERIA; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; STAINING;

MASTIGOPHORA (FLAGELLATES); NAEGLERIA; PSEUDOPODA;

EID: 33846405239     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2006.10.003     Document Type: Article

References (82)

1. Ahn T.I., and Jeon K.W. Antigenic reactivity of a monoclonal antibody against Amoeba proteus actin. J. Protozool. 36 (1989) 560-562
2. Ayscough K.R., Stryker J., Pokala N., Sanders M., Crews P., and Drubin D.G. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137 (1997) 399-416
3. Baines I.C., and Korn E.D. Localization of myosin IC and myosin II in Acanthamoeba castellanii by indirect immunofluorescence and immunogold electron microscopy. J. Cell Biol. 111 (1990) 1895-1904
4. Bamburg J.R. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15 (1999) 185-230
5. Bubb M.R., Baines I.C., and Korn E.D. Localization of actobindin, profilin I, profilin II, and phosphatidylinositol-4,5-bisphosphate (PIP2) in Acanthamoeba castellanii. Cell Motil. Cytoskeleton 39 (1998) 134-146
6. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351 (2000) 95-105
7. De Jonckheere J.F. Molecular definition and the ubiquity of species in the genus Naegleria. Protist 155 (2004) 89-103
8. Dehmelt L., and Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol. 6 (2004) 204-213
9. Dingle A.D., and Fulton C. Development of the flagellar apparatus of Naegleria. J. Cell Biol. 31 (1966) 43-54
10. Edmonds B.T., and Koenig E. ATP and calmodulin dependent actomyosin aggregates induced by cytochalasin D in goldfish retinal ganglion cell axons in vitro. J. Neurobiol. 21 (1990) 555-566
11. Fahrni J.F., Bolivar I., Berney C., Nassonova E., Smirnov A., and Pawlowski J. Phylogeny of lobose amoebae based on actin and small-subunit ribosomal RNA genes. Mol. Biol. Evol. 20 (2003) 1881-1886
12. Forstermann U., Pollock J., Schmidt H., Heller M., and Murad F. Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA 88 (1991) 1788-1792
13. Fujita M., Ichinose S., Kiyono T., Tsurumi T., and Omori A. Establishment of latrunculin-A resistance in HeLa cells by expression of R183A D184A mutant beta-actin. Oncogene 22 (2003) 627-631
14. Fukui Y. Mechanistics of amoeboid locomotion: signal to forces. Cell. Biol. Int. 26 (2002) 933-944
15. Fukui Y., Uyeda T.Q., Kitayama C., and Inoue S. How well can an amoeba climb?. Proc. Natl. Acad. Sci. USA 97 (2000) 10020-10025
16. Fulton C. Amebo-flagellates as research partners: the laboratory biology of Naegleria and Tetramitus. Methods Cell Physiol. 4 (1970) 341-476
17. Fulton C. Cell differentiation in Naegleria gruberi. Annu. Rev. Microbiol. 31 (1977) 597-629
18. Fulton C. Intracellular regulation of cell shape and motility in Naegleria. First insights and a working hypothesis. J. Supramol. Struct. 6 (1977) 13-43
19. Fulton C. Naegleria: a research partner for cell and developmental biology. J. Eukaryot. Microbiol. 40 (1993) 520-532
20. Fulton C., and Dingle A.D. Appearance of the flagellate phenotype in populations of Naegleria amebae. Dev. Biol. 15 (1967) 165-191
21. Fulton C., and Dingle A.D. Basal bodies, but not centrioles, in Naegleria. J. Cell Biol. 51 (1971) 826-836
22. Fulton C., Lai E.Y., Lamoyi E., and Sussman D.J. Naegleria actin elicits species-specific antibodies. J. Protozool. 33 (1986) 322-327
23. Gard D.L., Becker B.E., and Josh Romney S. MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. Int. Rev. Cytol. 239 (2004) 179-272
24. Gavin R.H. Myosins in protists. Int. Rev. Cytol. 206 (2001) 97-134
25. Gertler F.B., Niebuhr K., Reinhard M., Wehland J., and Soriano P. Mena, a relative of VASP and Drosophila enabled, is implicated in the control of microfilament dynamics. Cell 87 (1996) 227-239
26. Giuliano K.A., Kolega J., DeBiasio R.L., and Taylor D.L. Myosin II phosphorylation and the dynamics of stress fibers in serum-deprived and stimulated fibroblasts. Mol. Biol. Cell 3 (1992) 1037-1048
27. Goode B.L., Drubin D.G., and Barnes G. Functional cooperation between the microtubule and actin cytoskeletons. Curr. Opin. Cell Biol. 12 (2000) 63-71
28. Gordon-Weeks P.R. Actin dynamics: re-drawing the map. Nat. Cell Biol. 6 (2004) 390-391
29. Grebecka L., Pomorski P., Gre A., and Lopatowska A. Adhesion-dependent F-actin pattern in Amoeba proteus a common feature of amoebae and metazoan motile cells. Cell Biol. Int. 21 (1997) 565-573
30. Griffith L., and Pollard T. The interaction of actin filaments with microtubules and microtubule-associated proteins. J. Biol. Chem. 257 (1982) 9143-9151
31. Grimme S.J., Gao X.-D., Martin P.S., Tu K., Tcheperegine S.E., Corrado K., Farewell A.E., Orlean P., and Bi E. Deficiencies in the endoplasmic reticulum (ER)-membrane protein Gab1p perturb transfer of glycosylphosphatidylinositol to proteins and cause perinuclear ER-associated actin bar formation. Mol. Biol. Cell 15 (2004) 2758-2770
32. Han J.W., Park J.H., Kim M., and Lee J. mRNAs for microtubule proteins are specifically colocalized during the sequential formation of basal body, flagella, and cytoskeletal microtubules in the differentiation of Naegleria gruberi. J. Cell Biol. 137 (1997) 871-879
33. Hardie D.G., Haystead T.A., and Sim A.T. Use of okadaic acid to inhibit protein phosphatases in intact cells. Methods Enzymol. 201 (1991) 469-476
34. Hellsten M., and Roos U.P. The actomyosin cytoskeleton of amoebae of the cellular slime molds Acrasis rosea and Protostelium mycophaga: structure, biochemical properties, and function. Fungal Genet. Biol. 24 (1998) 123-145
35. Henson J.H., Svitkina T.M., Burns A.R., Hughes H.E., MacPartland K.J., Nazarian R., and Borisy G.G. Two components of actin-based retrograde flow in sea urchin coelomocytes. Mol. Biol. Cell 10 (1999) 4075-4090
36. Hestermann A., and Graf R. The XMAP215-family protein DdCP224 is required for cortical interactions of microtubules. BMC Cell Biol. 5 (2004) 24-32
37. Hidaka H., Watanabe M., and Kobayashi R. Properties and uses of H-series compounds as protein kinase inhibitors. Methods Enzymol. 201 (1991) 328-339
38. Kaiser D.A., Vinson V.K., Murphy D.B., and Pollard T.D. Profilin is predominantly associated with monomeric actin in Acanthamoeba. J. Cell Sci. 112 (1999) 3779-3790
39. Kim H.-K., Kang J.-G., Yumura S., Walsh C.J., Cho J.W., and Lee J. De novo formation of basal bodies in Naegleria gruberi: regulation by phosphorylation. J. Cell Biol. 169 (2005) 719-724
40. Kolega J., Janson L.W., and Taylor D.L. The role of solation-contraction coupling in regulating stress fiber dynamics in nonmuscle cells. J. Cell Biol. 114 (1991) 993-1003
41. Kowit J.D., and Fulton C. Programmed synthesis of tubulin for the flagella that develop during cell differentiation in Naegleria gruberi. Proc. Natl. Acad. Sci. USA 71 (1974) 2877-2881
42. Krendel M., and Mooseker M.S. Myosins: tails (and heads) of functional diversity. Physiology 20 (2005) 239-251
43. Laevsky G., and Knecht D.A. Cross-linking of actin filaments by myosin II is a major contributor to cortical integrity and cell motility in restrictive environments. J. Cell Sci. 116 (2003) 3761-3770
44. Landsverk M., and Epstein H. Genetic analysis of myosin II assembly and organization in model organisms. Cell. Mol. Life Sci. 62 (2005) 2270-2282
45. Larson D.E., and Dingle A.D. Development of the flagellar rootlet during Naegleria flagellate differentiation. Dev. Biol. 86 (1981) 227-235
46. Lee E., Pang K., and Knecht D. The regulation of actin polymerization and cross-linking in Dictyostelium. Biochim. Biophys. Acta 1525 (2001) 217-227
47. Limouze J., Straight A., Mitchison T., and Sellers J. Specificity of blebbistatin, an inhibitor of myosin II. J. Muscle Res. Cell Motil. 25 (2004) 337-341
48. Medalia O., Weber I., Frangakis A.S., Nicastro D., Gerisch G., and Baumeister W. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298 (2002) 1209-1213
49. Mulvihill D.P., and Hyams J.S. Shedding a little light on light chains. Nat. Cell Biol. 3 (2001) E10-F12
50. Ostap E. 2,3-Butanedione monoxime (BDM) as a myosin inhibitor. J. Muscle Res. Cell Motil. 23 (2002) 305-308
51. Ozer R.S., and Halpain S. Phosphorylation-dependent localization of microtubule-associated protein MAP2c to the actin cytoskeleton. Mol. Biol. Cell 11 (2000) 3573-3587
52. Podolski J., and Steck T. Length distribution of F-actin in Dictyostelium discoideum. J. Biol. Chem. 265 (1990) 1312-1318
53. Pollard T.D., and Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112 (2003) 453-465
54. Pollard T.D., Blanchoin L., and Mullins R.D. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29 (2000) 545-576
55. Ponti A., Vallotton P., Salmon W.C., Waterman-Storer C.M., and Danuser G. Computational analysis of F-actin turnover in cortical actin meshworks using fluorescent speckle microscopy. Biophys. J. 84 (2003) 3336-3352
56. Potma E.O., Boeij W.P.d., Bosgraaf L., Roelofs J., van Haastert P.J.M., and Wiersma D.A. Reduced protein diffusion rate by cytoskeleton in vegetative and polarized Dictyostelium cells. Biophys. J. 81 (2001) 2010-2019
57. Pring M., Cassimeris L., and Zigmond S.H. An unexplained sequestration of latrunculin A is required in neutrophils for inhibition of actin polymerization. Cell Motil. Cytoskeleton 52 (2002) 122-130
58. Roger B., Al-Bassam J., Dehmelt L., Milligan R.A., and Halpain S. MAP2c, but not tau, binds and bundles F-actin via its microtubule binding domain. Curr. Biol. 14 (2004) 363-371
59. Schuster F. An electron microscope study of the amoebo-flagellate, Naegleria gruberi (Schardinger). I. The amoeboid and flagellate stages. J. Protozool. 10 (1963) 297-313
60. Shu S., Liu X., and Korn E.D. Blebbistatin and blebbistatin-inactivated myosin II inhibit myosin II-independent processes in Dictyostelium. Proc. Natl. Acad. Sci. USA 102 (2005) 1472-1477
61. Simpson A.G.B., Inagaki Y., and Roger A.J. Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes. Mol. Biol. Evol. 23 (2006) 615-625
62. Somlyo A.P., and Somlyo A.V. Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83 (2003) 1325-1358
63. Spector I., Shochet N.R., Kashman Y., and Groweiss A. Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219 (1983) 493-495
64. Straight A.F., Cheung A., Limouze J., Chen I., Westwood N.J., Sellers J.R., and Mitchison T.J. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299 (2003) 1743-1747
65. Suh M.R., Han J.W., No Y.R., and Lee J. Transient concentration of a gamma-tubulin-related protein with a pericentrin-related protein in the formation of basal bodies and flagella during the differentiation of Naegleria gruberi. Cell Motil. Cytoskeleton 52 (2002) 66-81
66. Svitkina T.M., Verkhovsky A.B., McQuade K.M., and Borisy G.G. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol. 139 (1997) 397-415
67. Tamaoki T. Use and specificity of staurosporine, UCN-01, and calphostin C as protein kinase inhibitors. Methods Enzymol. 201 (1991) 340-347
68. Uehata M., Ishizaki T., Satoh H., Ono T., Kawahara T., Morishita T., Tamakawa H., Yamagami K., Inui J., Maekawa M., and Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389 (1997) 990-994
69. Urwyler N., Eggli P., and Keller H.U. Effects of the myosin inhibitor 2,3-butanedione monoxime (BDM) on cell shape, locomotion and fluid pinocytosis in human polymorphonuclear leucocytes. Cell Biol. Int. 24 (2000) 863-870
70. Van Belle H. R 24 571: a potent inhibitor of calmodulin-activated enzymes. Cell Calcium 2 (1981) 483-494
71. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Polarity sorting of actin filaments in cytochalasin-treated fibroblasts. J. Cell Sci. 110 (1997) 1693-1704
72. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Network contraction model for cell translocation and retrograde flow. Biochem. Soc. Symp. 65 (1999) 207-222
73. Wakatsuki T., Schwab B., Thompson N.C., and Elson E.L. Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J. Cell Sci. 114 (2001) 1025-1036
74. Walsh C. Synthesis and assembly of the cytoskeleton of Naegleria gruberi flagellates. J. Cell Biol. 98 (1984) 449-456
75. Westphal M., Jungbluth A., Heidecker M., Muhlbauer B., Heizer C., Schwartz J.M., Marriott G., and Gerisch G. Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr. Biol. 7 (1997) 176-183
76. Yarmola E.G., Somasundaram T., Boring T.A., Spector I., and Bubb M.R. Actin-latrunculin a structure and function. Differential modulation of actin-binding protein function by latrunculin A. J. Biol. Chem. 275 (2000) 28120-28127
77. Yarrow J.C., Lechler T., Li R., and Mitchison T.J. Rapid de-localization of actin leading edge components with BDM treatment. BMC Cell Biol. 4 (2003) 5-13
78. Yonemura S., and Pollard T.D. The localization of myosin I and myosin II in Acanthamoeba by fluorescence microscopy. J. Cell Sci. 102 (1992) 629-642
79. Yumura S. Spatial distribution of fluorescently labeled actin in living Dictyostelium amoebae. Cell Struct. Funct. 21 (1996) 189-197
80. Yumura S., and Kitanishi-Yumura T. Fluorescence-mediated visualization of actin and myosin filaments in the contractile membrane-cytoskeleton complex of Dictyostelium discoideum. Cell Struct. Funct. 15 (1990) 355-364
81. Yumura S., and Uyeda T.Q. Myosins and cell dynamics in cellular slime molds. Int. Rev. Cytol. 224 (2003) 173-225
82. Yumura S., Mori H., and Fukui Y. Localization of actin and myosin for the study of ameboid movement in Dictyostelium using improved immunofluorescence. J. Cell Biol. 99 (1984) 894-899