Colchicine affects cell motility, pattern formation and stalk cell differentiation in Dictyostelium by altering calcium signaling

Differentiation

Volumn 83, Issue 4, 2012, Pages 185-199

  Poloz, Yekaterina ^a   H O'Day, Danton ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Calcium mediated signaling; Cell motility; Colchicine; Dictyostelium; Morphogenesis; Stalk cell differentiation

Indexed keywords

CALCIUM ION; CALMODULIN; COLCHICINE; DIFFERENTIATION INDUCING FACTOR; DIFFERENTIATION INDUCING FACTOR 1; GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOLIPASE C; UNCLASSIFIED DRUG;

ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL MOTILITY; CELL VIABILITY; CYTOSKELETON; DEPOLYMERIZATION; DEVELOPMENTAL STAGE; DICTYOSTELIUM DISCOIDEUM; ECMB GENE; GENE; GENE EXPRESSION; MICROTUBULE; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPIA GENE;

BLOTTING, NORTHERN; BLOTTING, WESTERN; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL MOVEMENT; COLCHICINE; DICTYOSTELIUM; EXTRACELLULAR MATRIX PROTEINS; PROTOZOAN PROTEINS;

DICTYOSTELIUM;

EID: 84857381075     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.12.006     Document Type: Article

References (109)

1. 2+ concentration during chemotactic signal transduction in Dictyostelium discoideum cells. Differentiation 1988, 39:90-96.
2. 2+-concentration. Protoplasma 1989, 151:175-178.
3. Abe T., Early A., Siegert F., Weijer C., Williams J. Patterns of cell movement within the Dictyostelium slug revealed by cell type-specific, surface labeling of living cells. Cell 1994, 77:687-699.
4. Alberch P., Gale E.A. Size dependence during the development of the amphibian foot. Colchicine-induced digital loss, reduction. Journal of Embryology and Experimental Morphology 1983, 76:177-197.
5. Arai Y., Shibata T., Matsuoka S., Sato M.J., Yanagida T., Ueda M. Self-organization of the phosphatidylinositol lipids signaling system for random cell migration. Proceedings of the National Academy of Sciences of United States of America 2010, 107:12399-12404.
6. Baskar R., Chhabra P., Mascarenhas P., Nanjundiah V. A cell type-specific effect of calcium on pattern formation, differentiation in Dictyostelium discoideum. International Journal of Developmental Biology 2000, 44:491-498.
7. Bleasdale J.E., Bundy G.L., Bunting S., Fitzpatrick F.A., Huff R.M., Sun F.F., Pike J.E. Inhibition of phospholipase C dependent processes by U-73122. Advances in Prostaglandin, Thromboxane, and Leukotriene Research 1989, 19:590-593.
8. Bominaar A.A., Kesbeke F., Van Haastert P.J.M. Phospholipase C in Dictyostelium discoideum. Cyclic AMP surface receptor, G-protein-regulated activity in vitro. Biochemical Journal 1994, 297:181-187.
9. Bonner J.T. The pattern of differentiation in amoeboid slime molds. American Naturalist 1952, 86:79-89.
10. Bosgraaf L., Van Haastert P.J. The ordered extension of pseudopodia by amoeboid cells in the absence of external cues. PLoS One 2009, 4:e5253.
11. Bradford M.M. A rapid, sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 1976, 72:248-254.
12. Brown J.M., Firtel R.A. Regulation of cell-fate determination in Dictyostelium. Developmental Biology 1999, 216:426-441.
13. Browning D.D., O'Day D.H. Comparative analysis of chemotaxis in Dictyostelium using a radial bioassay method, protein tyrosine kinase activity is required for chemotaxis to folate but not to cAMP. Cellular Signalling 1995, 7:481-489.
14. Brundage R.A., Fogarty K.E., Tuft R.A., Fay F.S. Calcium gradients underlying polarization, chemotaxis of eosinophils. Science 1991, 254:703-706.
15. Cao X., Chen Y. Mitochondria, calcium signaling in embryonic development. Seminars in Cell and Developmental Biology 2009, 20:337-345.
16. Catalano A., O'Day D.H. Calmodulin-binding proteins in the model organism Dictyostelium: a complete & critical review. Cellular Signalling 2008, 20:277-291.
17. Ceccarelli A., Mahbubani H., Williams J.G. Positively, negatively acting signals regulating stalk cell, anterior-like cell differentiation in Dictyostelium. Cell 1991, 65:983-989.
18. Chae S.-C., Fuller D., Loomis W.F. Altered cell-type proportioning in Dictyostelium lacking adenosine monophosphate deaminase. Developmental Biology 2002, 241:183-194.
19. Chance K., Hemmingsen S., Weeks G. Effect of cerulenin on the growth and differentiation of Dictyostelium discoideum. Journal of Bacteriology 1976, 128:21-27.
20. Chen L., Iijima M., Tang M., Landree M.A., Huang Y.E., Xiong Y., Iglesias P.A., Devreotes P.N. PLA2, PI3K/PTEN pathways act in parallel to mediate chemotaxis. Developmental Cell 2007, 12:603-614.
21. Corff S.C., Burnett A.L. Morphogenesis in hydra. I. Peduncle, basal disc formation at the distal end of regenerating hydra after exposure to colchicine. Journal of Embryology and Experimental Morphology 1969, 21:417-443.
22. Cubitt A.B., Firtel R.A., Fischer G., Jaffe L.F., Miller A.L. Patterns of free calcium in multicellular stages of Dictyostelium expressing jellyfish apoaequorin. Development 1995, 121:2291-2301.
23. Cubitt A.B., Reddy I., Lee S., McNally J.G., Firtel R.A. Coexpression of a constitutively active plasma membrane calcium pump with GFP identifies roles for intracellular calcium in controlling cell sorting during morphogenesis in Dictyostelium. Developmental Biology 1998, 196:77-94.
24. Detterbeck S., Morandini P., Wetterauer B., Bachmair A., Fischer K., MacWilliams H.K. The 'prespore-like cells' of Dictyostelium have ceased to express a prespore gene, analysis using short-lived Β-galactosidases as reporters. Development 1994, 120:2847-2855.
25. Dingermann T., Reindl N., Werner H., Hildebrandt M., Nellen W., Harwood A., Williams J., Nerke K. Optimization, in situ detection of Escherichia coli Β-galactosidase gene expression in Dictyostelium discoideum. Gene 1989, 85:353-362.
26. Diwan B.A. A study of the effects of colchicine on the process of morphogenesis, induction in chick embryos. Journal of Embryology and Experimental Morphology 1966, 16:245-257.
27. Diwan B.A. A study of the mechanism of action of colchicine on embryos of Microhyla ornata. W. Roux' Archiv fur Entwicklungsmechanik 1967, 158:164-169.
28. Dormann D., Siegert F., Weijer C.J. Analysis of cell movement during the culmination phase of Dictyostelium development. Development 1996, 122:761-769.
29. Dormann D., Vasiev B., Weijer C.J. The control of chemotactic cell movement during Dictyostelium morphogenesis. Philosophical Transactions of the Royal Society B: Biological Sciences 2000, 355:983-991.
30. 2+-dependence. The Biochemical Journal 1995, 311:505-510.
31. Drozdovskaya L.N., Rapoport I.A. Influence of colchicine on Drosophila morphogenesis. Izvestiya Akademii Nauk SSSR, Seriya Biologicheskie 1988, 125-128.
32. Early A.E., Gaskell M.J., Traynor D., Williams J.G. Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination. Development 1993, 118:353-362.
33. Fey P., Kowal A.S., Gaudet P., Pilcher K.E., Chisholm R.L. Protocols for growth, development of Dictyostelium discoideum. Nature Protocols 2007, 2:1307-1316.
34. Firtel R.A., Meili R. Dictyostelium, a model for regulated cell movement during morphogenesis. Current Opinion in Genetics & Development 2000, 10:421-427.
35. Fosnaugh K.L., Loomis W.F. Enhancer regions responsible for temporal, cell-type-specific expression of a spore coat gene in Dictyostelium. Developmental Biology 1993, 157:38-48.
36. Francis D., O'Day D.H. Sorting out in pseudoplasmodia of Dictyostelium discoideum. The Journal of Experimental Zoology 1971, 176:265-272.
37. Fukuzawa M., Zhukovskaya N.V., Yamada Y., Araki T., Williams J.G. Regulation of Dictyostelium prestalk-specific gene expression by a SHAQKY family MYB transcription factor. Development 2006, 133:1715-1724.
38. Funamoto S., Milan K., Meili R., Firtel R.A. Role of phosphatidylinositol 3' kinase, a downstream pleckstrin homology domain-containing protein in controlling chemotaxis in Dictyostelium. The Journal of Cell Biology 2001, 153:795-809.
39. Gauthier M.L., O'Day D.H. Detection of calmodulin-binding proteins, calmodulin-dependent phosphorylation linked to calmodulin-dependent chemotaxis to folic, cAMP in Dictyostelium. Cellular Signalling 2001, 13:575-584.
40. Hagedorn M., Neuhaus E.M., Soldati T. Optimized fixation, immunofluorescence staining methods for Dictyostelium cells. Methods in Molecular Biology 2006, 346:327-338.
41. Hepler P.K. Calcium, a central regulator of plant growth, development. Plant Cell 2005, 17:2142-2155.
42. Hidaka H., Sasaki Y., Tanaka T. N-(6-aminohexyl-5-chloro-1-naphthalenesulfonamide, a calmodulin antagonist, inhibits cell proliferation. Proceedings of the National Academy of Sciences of the United States of America 1981, 78:4354-4357.
43. Huang E., Blagg S.L., Keller T., Katoh M., Shaulsky G., Thompson C.R.L. bZIP transcription factor interactions regulate DIF responses in Dictyostelium. Development 2005, 133:449-458.
44. Huber R., O'Day D.H. An EGF-like peptide sequence from Dictyostelium enhances cell motility, chemotaxis. Biochemical and Biophysical Research Communications 2009, 379:470-475.
45. 2+/calmodulin signaling. Cellular Signalling 2011, 23:731-738.
46. Jermyn K.A., Williams J.G. An analysis of culmination in Dictyostelium using prestalk and stalk-specific cell autonomous markers. Development 1991, 111:779-787.
47. Jermyn K., Traynor D., Williams J. The initiation of basal disc formation in Dictyostelium discoideum is an early event in culmination. Development 1996, 122:753-760.
48. Jermyn K.A., Duffy K.T.I., Williams J.G. A new anatomy of the prestalk zone in Dictyostelium. Nature 1989, 340:144-146.
49. Kay R.R. The biosynthesis of differentiation-inducing factor, a chlorinated signal molecule regulating Dictyostelium development. Journal of Biological Chemistry 1998, 273(5):26669-26675.
50. Kay R.R., Flatman P., Thompson C.R.L. DIF signalling, cell fate. Seminars In Cell & Developmental Biology 1999, 10:577-585.
51. Kay R.R., Thompson C.R.L. Cross-induction of cell types in Dictyostelium: evidence that DIF-1 is made by prespore cells. Development 2001, 128:4959-4966.
52. Keller H.U., Naef A., Zimmermann A. Effects of colchicine, vinblastine, nocodazole on polarity, motility, chemotaxis, cAMP levels of human polymorphonuclear leukocytes. Experimental Cell Research 1984, 153:173-185.
53. Keller T., Thompson C.R.L. Cell type specificity of a diffusible inducer is determined by a GATA family transcription factor. Development 2008, 135:1635-1645.
54. Keller H.U., Zimmermann A. Shape changes, chemokinesis of Walker 256 carcinosarcoma cells in response to colchicine, vinblastine, nocodazole, taxol. Invasion & Metastasis 1986, 6:33-43.
55. Kerfant B.G., Vassort G., Gómez A.M. Microtubule disruption by colchicine reversibly enhances calcium signaling in intact rat cardiac myocytes. Circulation Research 2001, 88:E59-65.
56. Kitanishi T., Shibaoka H., Fukui Y. Disruption of microtubules, retardation of development of Dictyostelium with ethyl N-phenylcarbamate, thiabendazole. Protoplasma 1984, 120:185-196.
57. Koch E.A., Spitzer R.H. Autoradiographic studies of protein, polysaccharide synthesis during vitellogenesis in Drosophila. Cell and Tissue Research 1982, 224:315-333.
58. Koch E.A., Spitzer R.H. Multiple effects of colchicine on oogenesis in Drosophila, induced sterility, switch of potential oocyte to nurse-cell developmental pathway. Cell and Tissue Research 1983, 228:21-32.
59. + concentrations in Dictyostelium discoideum. Development, Growth & Differentiation 2007, 49:253-264.
60. + concentrations determine cell fate in Dictyostelium discoideum. FASEB Journal 1994, 8:869-874.
61. Lim C.J., Zawadzki K.A., Khosla M., Secko D.M., Spiegelman G.B., Weeks G. Loss of the Dictyostelium RasC protein alters vegetative cell size, motility, endocytosis. Experimental Cell Research 2005, 306:47-55.
62. 2+-dependent binding of calmodulin to an N-terminal motif of the heterotrimeric G protein Β subunit. The Journal of Biological Chemistry 1997, 272:18801-18807.
63. Lombardi M.L., Knecht D.A., Lee J. Mechano-chemical signaling maintains the rapid movement of Dictyostelium cells. Experimental Cell Research 2008, 314:1850-1859.
64. Lusche D.F., Wessels D., Soll D.R. The effects of extracellular calcium on motility, pseudopod, uropod formation, chemotaxis, the cortical localization of myosin II in Dictyostelium discoideum. Cell Motility and the Cytoskeleton 2009, 66:567-587.
65. Maeda M., Sakamoto H., Iranfar N., Fuller D., Maruo T., Ogihara S., Morio T., Urushihara H., Tanaka Y., Loomis W.F. Changing patterns of gene expression in Dictyostelium prestalk cell subtypes recognized by in situ hybridization with genes from microarray analyses. Eukaryotic Cell 2003, 2:627-637.
66. Maeda Y., Maeda M. The calcium content of the cellular slime mold, Dictyostelium discoideum, during development, differentiation. Experimental Cell Research 1973, 82:125-130.
67. 2+ antagonist, 8(N,N diethylamino. octyl 3,4,5 trimethoxybenzoate hydrochloride (TMB 8., studies in smooth muscles. European Journal of Pharmacology 1974, 27:25-33.
68. Malchow D., Mutzel R., Schlatterer C. On the role of calcium during chemotactic signalling, differentiation of the cellular slime mould Dictyostelium discoideum. The International Journal of Developmental Biology 1996, 40:135-139.
69. McCullar J.S., Larsen S.A., Millimaki R.A., Filtz T.M. Calmodulin is a phospholipase C-Β interacting protein. The Journal of Biological Chemistry 2003, 278:33708-33713.
70. 2+ influx. Journal of Cell Science 1997, 110:2845-2853.
71. Nelsen E.M. Division delays, abnormal oral development produced by colchicine in Tetrahymena. The Journal of Experimental Zoology 1970, 175:69-83.
72. Newell P.C., Malchow D., Gross J.D. The role of calcium in aggregation, development of Dictyostelium. Experientia 1995, 51:1155-1165.
73. Niggli V. Microtubule-disruption-induced, chemotactic-peptide-induced migration of human neutrophils: implications for differential sets of signalling pathways. Journal of Cell Science 2003, 116:813-822.
74. O'Day D.H., Durston A.J. Colchicine induces multiple axis formation, stalk cell differentiation in Dictyostelium discoideum. Journal of Embryology and Experimental Morphology 1978, 47:195-206.
75. Okaichi K., Cubitt A.B., Pitt G.S., Firtel R.A. Amino acid substitutions in the Dictyostelium Gα subunit Gα2 produce dominant negative phenotypes, inhibit the activation of adenylyl cyclase, guanylyl cyclase, phospholipase C. Molecular Biology of the Cell 1992, 3:735-747.
76. Paranjape V., Gupta Roy B., Datta A. Involvement of calcium, calmodulin, protein phosphorylation in morphogenesis of Candida albicans. Journal of General Microbiology 1990, 136:2149-2154.
77. Raper K.B. Pseudoplasmodium formation, organization in Dictyostelium discoideum. Journal of the Elisha Mitchell Scientific Society 1940, 56:240-282.
78. Raper K.B., Fennell D.I. Stalk formation in Dictyostelium. Bulletin of the Torrey Botanical Club 1952, 79:25-51.
79. Richardson D.L., Loomis W.F. Disruption of the sporulation-specific gene spiA in Dictyostelium discoideum leads to spore instability. Genes & Development 1992, 6:1058-1070.
80. Saito T., Kato A., Kay R.R. DIF-1 induces the basal disc of the Dictyostelium fruiting body. Developmental Biology 2008, 317:444-453.
81. Sakai Y. Cell type conversion in isolated prestalk, prespore fragments of the cellular slime mold Dictyostelium discoideum. Development, Growth & Differentiation 1973, 15:11-19.
82. Saran S., Nakao H., Tasaka M., Lida H., Tsuji F.I., Nanjundiah V., Takeuchi I. Intracellular free calcium level, its response to cAMP stimulation in developing Dictyostelium cells transformed with jellyfish apoaequorin cDNA. FEBS Letters 1994, 337:43-47.
83. Sasaki A.T., Janetopoulos C., Lee S., Charest P.G., Takeda K., Sundheimer L.W., Meili R., Devreotes P.N., Firtel R.A. G protein-independent Ras/PI3K/F-actin circuit regulates basic cell motility. The Journal of Cell Biology 2007, 178:185-191.
84. Sawyer D.W., Sullivan J.A., Mandell G.L. Intracellular free calcium localization in neutrophils during phagocytosis. Science 1985, 230:663-666.
85. 2+ levels mediates stalk gene induction by differentiation inducing factor in Dictyostelium. The EMBO Journal 1996, 15:5177-5183.
86. Schaap P. Evolutionary crossroads in developmental biology, Dictyostelium discoideum. Development 2011, 138:387-396.
87. Schlatterer C., Gollnick F., Schmidt E., Meyer R., Knoll G. Challenge with high concentrations of cyclic AMP induces transient changes in the cytosolic free calcium concentrations in Dictyostelium discoideum. Journal of Cell Science 1994, 107:2107-2115.
88. Siegert F., Weijer C.J. Analysis of optical density wave propagation, cell movement in the cellular slime mould Dictyostelium discoideum. Physica D: Nonlinear Phenomena 1991, 49:224-232.
89. Siegert F., Weijer C.J. Three-dimensional scroll waves organize Dictyostelium slugs. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:6433-6437.
90. Sternfeld J. A study of pstB cells during Dictyostelium migration, culmination reveals a unidirectional cell type conversion process. Roux's Archives of Developmental Biology 1992, 201:354-363.
91. Sternfeld J., David C.N. Fate, regulation of anterior-like cells in Dictyostelium slugs. Developmental Biology 1982, 93:111-118.
92. Sternfeld J., David C.N. Cell sorting during pattern formation in Dictyostelium. Differentiation 1981, 20:10-21.
93. Sundharadas G., Cheung H.T. Enhancement of movement of mouse peritoneal macrophages caused by colchicine treatment. Cell Biology International Reports 1977, 1:439-443.
94. Swaney K.F., Huang C.-H., Devreotes P.N. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, polarity. Annual Reviews in Biophysics 2010, 39:265-289.
95. Thompson C.R.L., Kay R.R. The role of DIF-1 signaling in Dictyostelium development. Molecular Cell 2000, 6:1509-1514.
96. Tsujioka M., Zhukovskaya N., Yamada Y., Fukuzawa M., Ross S., Williams J.G. Dictyostelium Myb transcription factors function at culmination as activators of ancillary stalk differentiation. Eukaryotic Cell 2007, 6:568-570.
97. Verkerke-van Wijk I., Brandt R., Bosman L., Schaap P. Two distinct signaling pathways mediate DIF induction of prestalk gene expression in Dictyostelium. Experimental Cell Research 1998, 245:179-185.
98. Vigo C., Lewis G.P., Piper P.J. Mechanisms of inhibition of phospholipase A2. Biochemical Pharmacology 1980, 29:623-627.
99. Vlahos C.J., Matter W.F., Hui K.Y., Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). Journal of Biological Chemistry 1994, 269:5241-5248.
100. Williams J.G. Transcriptional regulation of Dictyostelium pattern formation. EMBO Reports 2006, 7:694-698.
101. Williams J.G., Ceccarelli A., McRobbie S., Mahbubani H., Kay R.R., Early A., Berks M., Jermyn K.A. Direct induction of Dictyostelium prestalk gene expression by DIF provides evidence that DIF is a morphogen. Cell 1987, 49:185-192.
102. Yamada Y., Sakamoto H., Ogihara S., Maeda M. Novel patterns of the gene expression regulation in the prestalk region along the antero-posterior axis during multicellular development of Dictyostelium. Gene Expression Patterns 2005, 6:63-68.
103. Yamada Y., Kay R.R., Bloomfield G., Ross S., Ivens A., Williams J.G. A new Dictyostelium prestalk cell sub-type. Developmental Biology 2010, 339:390-397.
104. Yamada Y., Nunez-Corcuera B., Williams J.G. DIF-1 regulates Dictyostelium basal disc differentiation by inducing the nuclear accumulation of a bZIP transcription factor. Developmental Biology 2011, 354:77-86.
105. Yumura S., Furuya K., Takeuchi I. Intracellular free calcium responses during chemotaxis of Dictyostelium cells. Journal of Cell Science 1996, 109:2673-2678.
106. Zefirova O.N., Diikov A.G., Zyk N.V., Zefirov N.S. Ligands of the colchicine site of tubulin: a common pharmacophore, new structural classes. Russian Chemistry Bulletin 2007, 56:680-688.
107. Zhai A., Zhang Y., Zhu X., Liang J., Wang X., Lin Y., Chen R. Secalonic acid: a reduced colchicine cytotoxicity through suppression of JNK, p38 MAPKs, calcium influx. Neurochemistry International 2011, 58:85-91.
108. Zhukovskaya N.V., Fukuzawa M., Yamada Y., Tsutoshi A., Williams J.G. The Dictyostelium bZIP transcription factor DimB regulates prestalk-specific gene expression. Development 2005, 133:439-448.
109. Zouwail S., Pettitt T.R., Dove S.K., Chibalina M.V., Powner D.J., Haynes L., Wakelam M.J.O., Insall R.H. Phospholipase D activity is essential for actin localization, actin-based motility in Dictyostelium. Biochemistry Journal 2005, 389:207-214.