Ammonium transporter C of Dictyostelium discoideum is required for correct prestalk gene expression and for regulating the choice between slug migration and culmination

Developmental Biology

Volumn 287, Issue 1, 2005, Pages 146-156

  Kirsten, Janet H ^a   Xiong, Yanhua ^a   Dunbar, Andrew J ^a   Rai, Meena ^a   Singleton, Charles K ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Adenylyl cyclase; Ammonia; Ammonium transporter; CudA; DhkC; Dictyostelium; Histidine kinase; Phosphorelay; STATa

Indexed keywords

CYCLIC AMP; MESSENGER RNA; NUCLEAR PROTEIN; PROTEIN HISTIDINE KINASE; STAT PROTEIN;

ARTICLE; CELL MIGRATION; CELL NUCLEUS; CELL TYPE; DICTYOSTELIUM DISCOIDEUM; GENE EXPRESSION; GENE EXPRESSION REGULATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; GASTROPODA;

EID: 27744494925     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.08.043     Document Type: Article

References (60)

1. C. Anjard, S. Pinaud, R.R. Kay, and C.D. Reymond Overexpression of DdPK2 protein kinase causes rapid development and affects the intracellular cAMP pathway of Dictyostelium discoideum Development 115 1992 785 790
2. C. Anjard, M. van Bemmelen, M. Veron, and C.D. Reymond A new spore differentiation factor (SDF) secreted by Dictyostelium cells is phosphorylated by the cAMP dependent protein kinase Differentation 62 1997 43 49
3. C. Anjard, W.T. Chang, J. Gross, and W. Nellen Production and activity of spore differentiation factors (SDFs) in Dictyostelium Development 125 1998 4067 4075
4. C. Anjard, C. Zeng, W.F. Loomis, and W. Nellen Signal transduction pathways leading to spore differentiation in Dictyostelium discoideum Dev. Biol. 193 1998 146 155
5. T. Araki, M. Gamper, A. Early, M. Fukuzawa, T. Abe, T. Kawata, E. Kim, R.A. Firtel, and J.G. Williams Developmentally and spatially regulated activation of a Dictyostelium STAT protein by a serpentine receptor EMBO J. 17 1998 4018 4028
6. A. Ceccarelli, H. Mahbubani, and J.G. Williams Positively and negatively acting signals regulating stalk cell and anterior-like cell differentiation in Dictyostelium Cell 65 1991 983 989
7. G. Coutts, G. Thomas, D. Blakely, and M. Merrick Membrane sequestration of signal transduction protein GlnK by the ammonium transporter AmtB EMBO J. 21 2002 536 545
8. A. De Lozanne, and J.A. Spudich Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination Science 236 1987 1086 1091
9. S. Detterbeck, P. Morandini, B. Wetterauer, A. Bachmair, K. Fischer, and H.K. MacWilliams The 'prespore-like cells' of Dictyostelium have ceased to express a prespore gene: analysis using short-lived beta-galactosidases as reporters Development 120 1994 2847 2855
10. T. Dingermann, N. Reindl, H. Werner, M. Hildebrandt, W. Nellen, A. Harwood, J. Williams, and K. Nerke Optimization and in situ detection of Escherichia coli beta-galactosidase gene expression in Dictyostelium discoideum Gene 85 1989 353 362
11. D. Dormann, T. Abe, C.J. Weijer, and J. Williams Inducible nuclear translocation of a STAT protein in Dictyostelium prespore cells: implications for morphogenesis and cell-type regulation Dev. 128 2001 1081 1088
12. D. Dormann, J.Y. Kim, P.N. Devreotes, and C.J. Weijer cAMP receptor affinity controls wave dynamics, geometry and morphogenesis in Dictyostelium J. Cell Sci. 114 2001 2513 2523
13. A.J. Durston Tip formation is regulated by an inhibitory gradient in the Dictyostelium discoideum slug Nature 263 1976 126 129
14. P.A. Farnsworth Morphogenesis in the cellular slime mould Dictyostelium discoideum; the formation and regulation of aggregate tips and the specification of developmental axes J. Embryol. Exp. Morphol. 29 1973 253 266
15. S.C. Follstaedt, J.H. Kirsten, and C.K. Singleton Temporal and spatial expression of ammonium transporter genes during growth and development of Dictyostelium discoideum Differentation 71 2003 557 566
16. M. Fukuzawa, and J.G. Williams Analysis of the promoter of the cudA gene reveals novel mechanisms of Dictyostelium cell type differentiation Development 127 2000 2705 2713
17. M. Fukuzawa, N. Hopper, and J. Williams cudA: a Dictyostelium gene with pleiotropic effects on cellular differentiation and slug behaviour Development 124 1997 2719 2728
18. A.J. Harwood, A.E. Early, K.A. Jermyn, and J. Williams Unexpected localisation of cells expressing a prespore marker of Dictyostelium discoideum Differentiation 46 1991 7 13
19. A.J. Harwood, N.A. Hopper, M.N. Simon, S. Bouzid, M. Veron, and J.G. Williams Multiple roles for cAMP-dependent protein kinase during Dictyostelium development Dev. Biol. 149 1992 90 99
20. A.J. Harwood, N.A. Hopper, M.N. Simon, D.M. Driscoll, M. Veron, and J.G. Williams Culmination in Dictyostelium is regulated by the cAMP-dependent protein kinase Cell 69 1992 615 624
21. A.J. Harwood, A. Early, and J.G. Williams A repressor controls the timing and spatial localisation of stalk cell-specific gene expression in Dictyostelium Development 118 1993 1041 1048
22. N.A. Hopper, A.J. Harwood, S. Bouzid, M. Veron, and J.G. Williams Activation of the prespore and spore cell pathway of Dictyostelium differentiation by cAMP-dependent protein kinase and evidence for its upstream regulation by ammonia EMBO J. 12 1993 2459 2466
23. K.A. Jermyn, and J.G. Williams An analysis of culmination in Dictyostelium using prestalk and stalk-specific cell autonomous markers Development 111 1991 779 787
24. K.A. Jermyn, K.T. Duffy, and J.G. Williams A new anatomy of the prestalk zone in Dictyostelium Nature 340 1989 144 146
25. R.R. Kay Evidence that elevated intracellular cyclic AMP triggers spore maturation in Dictyostelium Development 105 1989 753 759
26. S. Khademi, J. O'Connel, J. Remis, Y. Robles-Colmenares, L.J.W. Miercke, and R.M. Stroud Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1. 35 Å Science 305 2004 1587 1594
27. D.A. Knecht, S.M. Cohen, W.F. Loomis, and H.F. Lodish Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors Mol. Cell. Biol. 6 1986 3973 3983
28. M.T. Laub, and W.F. Loomis A molecular network that produces spontaneous oscillations in excitable cells of Dictyostelium Mol. Biol. Cell 9 1998 3521 3532
29. M.C. Lorenz, and J. Heitman The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae EMBO J. 17 1998 1236 1247
30. M. Maeda, S.J. Lu, G. Shaulsky, Y. Miyazaki, H. Kuwayama, Y. Tanaka, A. Kuspa, and W.F. Loomis Periodic signaling controlled by an oscillatory circuit that includes protein kinases ERK2 and PKA Science 304 2004 875 878
31. S.K.O. Mann, W.M. Yonemoto, S.S. Taylor, and R.A. Firtel DdPK3, which plays essential roles during Dictyostelium development, encodes the catalytic subunit of cAMP-dependent protein kinase Proc. Natl. Acad. Sci. U. S. A. 89 1992 10701 10705
32. S.K.O. Mann, D.L. Richardson, S. Lee, A.R. Kimmel, and R.A. Firtel Expression of cAMP-dependent protein kinase in prespore cells is sufficient to induce spore cell differentiation in Dictyostelium Proc. Natl. Acad. Sci. U. S. A. 91 1994 10561 10565
33. S. Mohanty, K.A. Jermyn, A. Early, T. Kawata, L. Aubry, A. Ceccarelli, P. Schaap, J.G. Williams, and R.A. Firtel Evidence that the Dictyostelium Dd-STATa protein is a repressor that regulates commitment to stalk cell differentiation and is also required for efficient chemotaxis Development 126 1999 3391 3405
34. P.C. Newell, A. Telser, and M. Sussman Alternative developmental pathways determined by environmental conditions in the cellular slime mold Dictyostelium discoideum J. Bacteriol. 100 1969 763 768
35. S.R. Pekovich, P.R. Martin, and C.K. Singleton Thiamine deficiency decreases steady-state mRNA levels for transketolase and pyruvate dehydrogenase but not for β-ketoglutarate dehydrogenase in three human cell types J. Nutr. 128 1998 683 687
36. K.B. Raper Pseudoplasmodium formation and organization in Dictyostelium discoideum J. Elisha Mitchell Sci. Soc. 56 1940 241 282
37. D.L. Richardson, W.F. Loomis, and A.R. Kimmel Progression of an inductive signal activates sporulation in Dictyostelium discoideum Development 120 1994 2891 2900
38. B.B. Riley, and S.L. Barclay Ammonia promotes accumulation of intracellular cAMP in differentiating amoebae of Dictyostelium discoideum Development 109 1990 715 722
39. J.M. Schindler The Control of Morphogenesis in the Cellular Slime Mold Dictyostelium discoideum 1978 University of Pittsburgh Pittsburgh, PA 150
40. J. Schindler, and M. Sussman Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum J. Mol. Biol. 116 1977 161 169
41. J. Schindler, and M. Sussman Inhibition by ammonia of intracellular cAMP accumulation in Dictyostelium discoideum: its significance for the regulation of morphogenesis Dev. Genet. 1 1979 13 20
42. G. Shaulsky, R. Escalante, and W.F. Loomis Developmental signal transduction pathways uncovered by genetic suppressors Proc. Natl. Acad. Sci. U. S. A. 93 1996 15260 15265
43. G. Shaulsky, D. Fuller, and W.F. Loomis A cAMP-phosphodiesterase controls PKA-dependent differentiation Development 125 1998 691 699
44. N. Shimada, M. Maeda, H. Urushihara, and T. Kawata Identification of new modes of Dd-STATa regulation of gene expression in Dictyostelium by in situ hybridisation Int. J. Dev. Biol. 48 2004 679 682
45. N. Shimada, T. Maruo, M. Maeda, H. Urushihara, and T. Kawata Evidence that the Dictyostelium STAT protein Dd-STATa plays a role in the differentiation of inner basal disc cells and identification of a promoter element essential for expression in these cells Differentation 73 2005 50 60
46. C.K. Singleton, R.L. Delude, and C.E. McPherson Characterization of genes which are deactivated upon the onset of development in Dictyostelium discoideum Dev. Biol. 119 1987 433 441
47. C.K. Singleton, M.J. Zinda, B. Mykytka, and P. Yang The histidine kinase DhkC regulates the choice between migrating slugs and terminal differentiation in Dictyostelium discoideum Dev. Biol. 203 1998 345 357
48. M.K. Slifkin, and J.T. Bonner The effect of salts and organic solutes on the migration time of the slime mold Dictyostelium discoideum Biol. Bull. 102 1952 273 277
49. E. Smith, and K. Williams Evidence for tip control of the "slug/fruit" switch in slugs of Dictyostelium discoideum J. Embryol. Exp. Morphol. 57 1980 233 240
50. D. Smith, M. Garcia-Pedrajas, S. Gold, and M. Perlin Isolation and characterization from pathogenic fungi of genes encoding ammonium permeases and their roles in dimorphism Mol. Microbiol. 50 2003 259 276
51. M. Sussman Biochemical and genetic methods in the study of cellular slime mold development D. Prescott Methods of Cell Physiology 1966 Academic Press New York 392 410
52. M. Sussman, J. Schindler, and H. Kim Cell interaction controlling morphogenesis and gene expression in Dictyostelium Birth Defects, Orig. Artic. Ser. 14 2 1978 473 489
53. P.A. Thomason, D. Traynor, G. Cavet, W.T. Chang, A.J. Harwood, and R.R. Kay An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium EMBO J. 17 1998 2838 2845
54. I. Verkerke-van Wijk, M. Fukuzawa, P.N. Devreotes, and P. Schaap Adenylyl cyclase A expression is tip-specific in Dictyostelium slugs and directs StatA nuclear translocation and CudA gene expression Dev. Biol. 234 2001 151 160
55. M. Wang, J.H. Roelfsema, J.G. Williams, and P. Schaap Cytoplasmic acidification facilitates but does not mediate DIF-induced prestalk gene expression in Dictyostelium discoideum Dev. Biol. 140 1990 182 188
56. G.B. Williams, E.M. Elders, and M. Sussman Modulation of the cAMP relay in Dictyostelium discoideum by ammonia and other metabolites: possible morphogenetic consequences Dev. Biol. 105 1984 377 388
57. Q. Zhang Studies of H7 Gene Function and Regulation of its Expression by a Bidirectional Promoter in Dictyostelium discoideum 1995 Vanderbilt University Nashville, TN 139
58. L. Zheng, D. Kostrewa, S. Berneche, F. Winkler, and X.-D. Li The mechanism of ammonia transport based on the crystal structure of AmtB of Escheriscia coli Proc. Natl. Acad. Sci. U. S. A. 101 2004 17090 17095
59. N. Zhukovskaya, A. Early, T. Kawata, T. Abe, and J. Williams cAMP-dependent protein kinase is required for the expression of a gene specifically expressed in Dictyostelium prestalk cells Dev. Biol. 179 1996 27 40
60. M.J. Zinda, and C.K. Singleton The hybrid histidine kinase DhkB regulates spore germination in Dictyostelium discoideum Dev. Biol. 196 1998 171 183