Cell signaling during development of dictyostelium

Developmental Biology

Volumn 391, Issue 1, 2014, Pages 1-16

  Loomis, William F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dependent sequence; Intercellular communication; Signal transduction

Indexed keywords

CELL PROTEIN; CELL SURFACE RECEPTOR; CONDITIONED MEDIUM FACTOR; CYCLIC AMP; CYCLIC GMP; CYTOKININ; DIFFERENTIATION INDUCING FACTOR; DIFFERENTIATION INDUCING FACTOR 1; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; PRESTARVATION FACTOR; PROTEIN APRA; PROTEIN CFAD; STROMAL CELL DERIVED FACTOR 1; STROMAL CELL DERIVED FACTOR 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CELL AGGREGATION; CELL CONTACT; CELL DENSITY; CELL DIFFERENTIATION; CELL GROWTH; CELL TYPE; CHEMOTAXIS; CYTOPLASM; DEVELOPMENTAL STAGE; DICTYOSTELIUM DISCOIDEUM; EUKARYOTIC CELL; FRUITING BODY; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; NUTRIENT; PARASITE DEVELOPMENT; PRIORITY JOURNAL; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION;

ANIMALIA; DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM;

DEPENDENT SEQUENCE; INTERCELLULAR COMMUNICATION; SIGNAL TRANSDUCTION;

CELL COMMUNICATION; CHEMOTAXIS; CULTURE MEDIA, CONDITIONED; CYCLIC AMP; CYTOKININS; DICTYOSTELIUM; MORPHOGENESIS; NUCLEIC ACIDS; PEPTIDES; POLYKETIDES; QUORUM SENSING; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STEROIDS;

EID: 84899897127     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.04.001     Document Type: Review

References (140)

1. Abe H., Uchiyama M., Tanaka Y., Saito H. Structure of discadenine, a spore germination inhibitor from the cellular slime mold Dictyostelium discoideum. Tetrahedron Lett. 1976, 42:3807-3810.
2. Anjard C., Loomis W.F. Peptide signaling during terminal differentiation of Dictyostelium. Proc. Natl. Acad. Sci. USA 2005, 102:7607-7611.
3. Anjard C., Loomis W.F. GABA induces terminal differentiation of Dictyostelium through a GABA(B) receptor. Development 2006, 133:2253-2261.
4. Anjard C., Loomis W.F. Cytokinins induce sporulation in Dictyostelium. Development 2008, 135:819-827.
5. Anjard C., Su Y., Loomis W.F. Steroids initiate a signaling cascade that triggers rapid sporulation in Dictyostelium. Development 2009, 136:803-812.
6. Anjard C., Su Y., Loomis W.F. The polyketide MPBD initiates the SDF-1 signaling cascade that coordinates terminal differentiation in Dictyostelium. Eukaryot. Cell 2011, 10:956-963.
7. Anjard C., Zeng C., Loomis W.F., Nellen W. Signal transduction pathways leading to spore differentiation in Dictyostelium discoideum. Dev. Biol. 1998, 193:146-155.
8. Araki T., Langenick J., Gamper M., Firtel R.A., Williams J.G. Evidence that DIF-1 and hyper-osmotic stress activate a Dictyostelium STAT by inhibiting a specific protein tyrosine phosphatase. Development 2008, 135:1347-1353.
9. Austin M.B., Saito T., Bowman M.E., Haydock S., Kato A., Moore B.S., Kay R.R., Noel J.P. Biosynthesis of Dictyostelium discoideum differentiation-inducing factor by a hybrid type I fatty acid-type III polyketide synthase. Nat. Chem. Biol. 2006, 2:494-502.
10. Bakthavatsalam D., Brock D.A., Nikravan N.N., Houston K.D., Hatton R.D., Gomer R.H. The secreted Dictyostelium protein CfaD is a chalone. J Cell Sci. 2008, 121:2473-2480.
11. Bakthavatsalam D., Choe J.M., Hanson N.E., Gomer R.H. A Dictyostelium chalone uses G proteins to regulate proliferation. BMC Biol. 2009, 7:44.
12. Benabentos R., Hirose S., Sucgang R., Curk T., Katoh M., Ostrowski E.A., Strassmann J.E., Queller D.C., Zupan B., Shaulsky G., Kuspa A. Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr. Biol. 2009, 19:567-572.
13. Berger E.A., Bozzone D.M., Berman M.B., Morgenthaler J.A., Clark J.M. Regulation of discoidin I gene expression in Dictyostelium discoideum by cell-cell contact and cAMP. J. Cell. Biochem. 1985, 27:391-400.
14. Berks M., Kay R.R. Cyclic AMP is an inhibitor of stalk cell differentiation in Dictyostelium discoideum. Dev. Biol. 1988, 126:108-114.
15. Bonner J.T. Evidence for the formation of cell aggregates by chemotaxis in the development of the slime mold Dictyostelium discoideum. J. Exp. Zool. 1947, 106:1-26.
16. Bonner J.T. The Cellular Slime Molds 1959, Princeton University Press, Princeton, NJ.
17. Bonner J.T. Induction of stalk cell differentiation by cyclic AMP in the cellular slime mold Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA 1970, 65:110-113.
18. Brock D.A., Gomer R.H. A cell-counting factor regulating structure size in Dictyostelium. Genes Dev. 1999, 13:1960-1969.
19. Burdine V., Clarke M. Genetic and physiologic modulation of the prestarvation response in Dictyostelium discoideum. Mol. Biol. Cell 1995, 6:311-325.
20. Cai H., Katoh-Kurasawa M., Muramoto T., Santhanam B., Long Y., Li L., Ueda M., Iglesias P., Shaulsky G., Devreotes P. Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer. Science 2014, 343:1329. (1249531).
21. Chen Z.H., Schaap P. The prokaryote messenger c-di-GMP triggers stalk cell differentiation in Dictyostelium. Nature 2012, 488:680-683.
22. Clarke M., Dominguez N., Yuen I.S., Gomer R.H. Growing and starving Dictyostelium cells produce distinct density-sensing factors. Dev. Biol. 1992, 152:403-406.
23. Clarke M., Gomer R.H. PSF and CMF, autocrine factors that regulate gene expression during growth and early development of Dictyostelium. Experientia 1995, 51:1124-1134.
24. Clarke M., Kayman S.C., Riley K. Density-dependent induction of discoidin-I synthesis in exponentially growing cells of Dictyostelium discoideum. Differentiation 1987, 34:79-87.
25. Deery W.J., Gomer R.H. A putative receptor mediating cell-density sensing in Dictyostelium. J. Biol. Chem. 1999, 274:34476-34482.
26. Dynes J.L., Clark A.M., Shaulsky G., Kuspa A., Loomis W.F., Firtel R.A. LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium. Genes Dev. 1994, 8:948-958.
27. Eichinger L., Pachebat J.A., Glockner G., Rajandream M.A., Sucgang R., Berriman M., Song J., Olsen R., Szafranski K., Xu Q., Tunggal B., Kummerfeld S., Madera M., Konfortov B.A., Rivero F., Bankier A.T., Lehmann R., Hamlin N., Davies R., Gaudet P., Fey P., Pilcher K., Chen G., Saunders D., Sodergren E., Davis P., Kerhornou A., Nie X., Hall N., Anjard C., Hemphill L., Bason N., Farbrother P., Desany B., Just E., Morio T., Rost R., Churcher C., Cooper J., Haydock S., van Driessche N., Cronin A., Goodhead I., Muzny D., Mourier T., Pain A., Lu M., Harper D., Lindsay R., et al. The genome of the social amoeba Dictyostelium discoideum. Nature 2005, 435:43-57.
28. Evans M., Kaufman M. Establishment in culture of pluripotent cells from mouse embryos. Nature 1981, 292:154-156.
29. Firtel R.A. Signal transduction pathways controlling multicellular development in Dictyostelium. Trends Genet. 1991, 7:381-388.
30. Firtel R.A. Interacting signaling pathways controlling multicellular development in Dictyostelium. Curr. Opin. Genet. Dev. 1996, 6:545-554.
31. Franke J., Kessin R.H. The cyclic nucleotide phosphodiesterase inhibitory protein of Dictyostelium discoideum. Purification and characterization. J. Biol. Chem. 1981, 256:7628-7637.
32. Franke J., Kessin R.H. The cyclic nucleotide phosphodiesterases of Dictyostelium discoideum: molecular genetics and biochemistry. Cell Signal. 1992, 4:471-478.
33. Fukuzawa M. Control of prestalk-cell differentiation by transcription factors. Dev. Growth Differ. 2011, 53:538-547.
34. Fukuzawa M., Abe T., Williams J.G. The Dictyostelium prestalk cell inducer DIF regulates nuclear accumulation of a STAT protein by controlling its rate of export from the nucleus. Development 2003, 130:797-804.
35. Fukuzawa M., Araki T., Adrian I., Williams J.G. Tyrosine phosphorylation-independent nuclear translocation of a Dictyostelium STAT in response to DIF signaling. Mol. Cell 2001, 7:779-788.
36. Garcia R., Ray S., Brown I., Irom J., Brazill D. PakD, a putative p21-activated protein kinase in Dictyostelium discoideum regulates actin. Eukaryot. Cell 2014, 13:119-126.
37. Garrod D.R., Ashworth J.M. Effect of growth conditions on development of the cellular slime mould, Dictyostelium discoideum. J. Embryol. Exp. Morphol. 1972, 28:463-479.
38. Gerisch G., Fromm H., Huesgen A., Wick U. Control of cell-contact sites by cyclic AMP pulses in differentiating Dictyostelium cells. Nature 1975, 255:547-549.
39. Gerisch G., Wick U. Intracellular oscillations and release of cyclic AMP from Dictyostelium cells. Biochem. Biophys. Res. Commun. 1975, 65:364-370.
40. Gilbert S. Developmental Biology 2013, Sinauer Associates, Sunderland, Massachusetts.
41. Gomer R.H., Jang W., Brazill D. Cell density sensing and size determination. Dev. Growth Differ. 2011, 53:482-494.
42. Gomer R.H., Yuen I.S., Firtel R.A. A secreted 80×10(3)Mr protein mediates sensing of cell density and the onset of development in Dictyostelium. Development 1991, 112:269-278.
43. Grabel L., Loomis W.F. Effector controlling accumulation of N-acteylglucosaminidase during development of Dictyostelium discoideum. Dev. Biol. 1978, 64:203-209.
44. Hirose S., Benabentos R., Ho H.I., Kuspa A., Shaulsky G. Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 2011, 333:467-470.
45. Ho H.I., Hirose S., Kuspa A., Shaulsky G. Kin recognition protects cooperators against cheaters. Curr. Biol. 2013, 23:1590-1595.
46. Huang E.Y., Blagg S.L., Keller T., Katoh M., Shaulsky G., Thompson C.R.L. bZlP transcription factor interactions regulate DIF responses in Dictyostelium. Development 2006, 133:449-458.
47. Insall R., Kuspa A., Lilly P.J., Shaulsky G., Levin L.R., Loomis W.F., Devreotes P. CRAC, a cytosolic protein containing a pleckstrin homology domain, is required for receptor and G protein-mediated activation of adenylyl cyclase in Dictyostelium. J. Cell Biol. 1994, 126:1537-1545.
48. Iranfar N., Fuller D., Loomis W.F. Genome-wide expression analyses of gene regulation during early development of Dictyostelium discoideum. Eukaryot. Cell 2003, 2:664-670.
49. Iranfar N., Fuller D., Loomis W.F. Transcriptional regulation of post-aggregation genes in Dictyostelium by a feed-forward loop involving GBF and LagC. Dev. Biol. 2006, 290:460-469.
50. Jang W., Chiem B., Gomer R.H. A secreted cell number counting factor represses intracellular glucose levels to regulate group size in Dictyostelium. J. Biol. Chem. 2002, 277:39202-39208.
51. Jang W., Gomer R.H. Exposure of cells to a cell number-counting factor decreases the activity of glucose-6-phosphatase to decrease intracellular glucose levels in Dictyostelium discoideum. Eukaryot. Cell. 2005, 4:72-81.
52. Jang W., Gomer R.H. Combining experiments and modelling to understand size regulation in Dictyostelium discoideum. J. R. Soc. Interface 2008, 5(Suppl. 1):S49-S58.
53. Jang W., Schwartz O.G., Gomer R.H. A cell number counting factor alters cell metabolism. Commun. Integr. Biol. 2009, 2:293-297.
54. Jain R., Gomer R.H. A developmentally regulated cell surface receptor for a density-sensing factor in Dictyostelium. J. Biol. Chem. 1994, 269:9128-9136.
55. Jermyn K.A., Duffy K.T., Williams J.G. A new anatomy of the prestalk zone in Dictyostelium. Nature 1989, 340:144-146.
56. 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.
57. Kay R.R. The biosynthesis of differentiation-inducing factor, a chlorinated signal molecule regulating Dictyostelium development. J. Biol. Chem. 1998, 273:2669-2675.
58. Kay R.R., Dhokia B., Jermyn K.A. Purification of stalk-cell-inducing morphogens from Dictyostelium discoideum. Eur. J. Biochem. 1983, 136:51-56.
59. Kay R.R., Jermyn K.A. A possible morphogen controlling differentiation in Dictyostelium. Nature 1983, 303:242-244.
60. Keller T., Thompson C.R. Cell type specificity of a diffusible inducer is determined by a GATA family transcription factor. Development 2008, 135:1635-1645.
61. Kessin R.H., Orlow S.J., Shapiro R.I., Franke J. Binding of inhibitor alters kinetic and physical properties of extracellular cyclic AMP phosphodiesterase from Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA 1979, 76:5450-5454.
62. Kessin R.H. Dictyostelium - Evolution, Cell Biology, and the Development of Multicellularity 2001, Cambridge University Press, Cambridge, UK.
63. Kim L., Liu J.C., Kimmel A.R. The novel tyrosine kinase ZAK1 activates GSK3 to direct cell fate specification. Cell 1999, 99:399-408.
64. Kimmel A.R. Different molecular mechanisms for cAMP regulation of gene expression during Dictyostelium development. Dev. Biol. 1987, 122:163-171.
65. Kinseth M.A., Anjard C., Fuller D., Guizzunti G., Loomis W.F., Malhotra V. The Golgi-associated protein Grasp is required for unconventional protein secretion during development. Cell 2007, 130:524-534.
66. Klein C. Induction of phosphodiesterase by cyclic adenosine 3',5'-monophosphate in differentiating Dictyostelium discoideum. J. Biol. Chem. 1975, 250:7134-7138.
67. Klein P., Vaughan R., Borleis J., Devreotes P. The surface cAMP receptor in Dictyostelium - levels of ligand-induced phosphorylation, solubilization, identification of primary transcript, and developmental regulation of expression. J. Biol. Chem. 1987, 262:358-364.
68. Konijn T.M., van de Meene J.G.C., Bonner J.T., Barkley D.S. The acrasin activity of adenosine-3',5'-cyclic phosphate. Proc. Natl. Acad. Sci. USA 1967, 58:1152-1154.
69. Kuspa A., Loomis W.F. The genome of Dictyostelium discoideum. Meth. Mol. Biol. 2006, 346:15-30.
70. Laub M.T., Loomis W.F. A molecular network that produces spontaneous oscillations in excitable cells of Dictyostelium. Mol. Biol. Cell 1998, 9:3521-3532.
71. Lawrence P. The Making of a Fly: The Genetics of Animal Design 1992, Blackwell Sci. Pub., Oxford, UK.
72. Loomis W.F. Dictyostelium discoideum. A Developmental System 1975, Academic Press, New York.
73. Loomis W.F. Biochemistry of aggregation in Dictyostelium. Dev. Biol. 1979, 70:1-12.
74. Loomis W.F. The Development of Dictyostelium discoideum 1982, Academic Press, New York.
75. Loomis W.F. Genetic tools for Dictyostelium discoideum. Methods Cell Biol. 1987, 28:31-65.
76. Loomis W.F. Lateral inhibition and pattern formation in Dictyostelium. Curr. Top. Dev. Biol. 1993, 28:1-46.
77. Loomis W.F. Role of PKA in the timing of developmental events in Dictyostelium cells. Microbiol. Mol. Biol. Rev. 1998, 62:684.
78. Loomis W.F., Behrens M.M., Williams M., Anjard C. Pregnenolone sulfate and cortisol induce secretion of acyl CoA binding protein and its conversion into endozepines from astrocytes. J. Biol. Chem. 2010, 285:21359-21365.
79. Loomis W.F., White S., Dimond R. A sequence of dependent stages in the development of Dictyostelium discoideum. Dev. Biol. 1976, 53:171-177.
80. Maeda M., Aubry L., Insall R., Gaskins C., Devreotes P.N., Firtel R.A. Seven helix chemoattractant receptors transiently stimulate mitogen-activated protein kinase in Dictyostelium - role of heterotrimeric G proteins. J. Biol. Chem. 1996, 271:3351-3354.
81. Maeda M., Lu S.J., Shaulsky G., Miyazaki Y., Kuwayama H., Tanaka Y., Kuspa A., Loomis W.F. Periodic signaling controlled by an oscillatory circuit that includes protein kinases ERK2 and PKA. Science 2004, 304:875-878.
82. 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. Eukaryot. Cell 2003, 2:627-637.
83. Mann S.K., Firtel R.A. Two-phase regulatory pathway controls cAMP receptor-mediated expression of early genes in Dictyostelium. Proc. Natl. Acad. Sci. USA 1989, 86:1924-1928.
84. Mann S.K.O., Brown J.M., Briscoe C., Parent C., Pitt G., Devreotes P.N., Firtel R.A. Role of cAMP-dependent protein kinase in controlling aggregation and postaggregative development in Dictyostelium. Dev. Biol. 1997, 183:208-221.
85. Mann S.K.O., Firtel R.A. Cyclic AMP regulation of early gene expression in Dictyostelium discoideum: mediation via the cell surface cyclic AMP receptor. Mol. Cell. Biol. 1987, 7:458-469.
86. Mann S.K.O., Firtel R.A. A developmentally regulated, putative serine/threonine protein kinase is essential for development in Dictyostelium. Mech. Dev. 1991, 35:89-101.
87. Marin F.T. Regulation of development in Dictyostelium discoideum: I. Initiation of the growth to developmental transition by amino acid starvation. Dev. Biol. 1976, 48:110-117.
88. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 1981, 78:7634-7638.
89. Mok D.W., Mok M.C. Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52:89-118.
90. Morris H.R., Taylor G.W., Masento M.S., Jermyn K.A., Kay R.R. Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoideum. Nature 1987, 328:811-814.
91. Morrissey J.H., Devine K.M., Loomis W.F. The timing of cell-type specific differentiation in Dictyostelium discoideum. Dev. Biol. 1984, 103:414-424.
92. Neumann C.S., Walsh C.T., Kay R.R. A flavin-dependent halogenase catalyzes the chlorination step in the biosynthesis of Dictyostelium differentiation-inducing factor 1. Proc. Natl. Acad. Sci. USA 2010, 107:5798-5803.
93. Newell P.C., Williams K.L., Kuspa A., Loomis W.F. Genetic map of Dictyostelium. Genetic Maps: Locus Maps of Complex Genomes 1993, 3.1-3.10. CSH Laboratory Press, Cold Spring Harbor. 6th edition. S.J. O[U+05F3]Brien (Ed.).
94. Norman A.W., Mizwicki M.T., Norman D.P. Steroid-hormone rapid actions, membrane receptors and a conformational ensemble model. Nat. Rev. Drug Discov. 2004, 3:27-41.
95. Nüsslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 1980, 287:795-801.
96. Orlow S.J., Shapiro I., Franke J., Kessin R.H. The extracellular cyclic nucleotide phosphodiesterase of Dictyostelium discoideum. Purification and characterization. J. Biol. Chem. 1981, 256:7620-7627.
97. Parikh A., Miranda E.R., Katoh-Kurasawa M., Fuller D., Rot G., Zagar L., Curk T., Sucgang R., Chen R., Zupan B., Loomis W.F., Kuspa A., Shaulsky G. Conserved developmental transcriptomes in evolutionarily divergent species. Genome Biol. 2010, 11:R35.
98. Payne S.H., Loomis W.F. Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences. Eukaryot. Cell. 2006, 5:272-276.
99. Phillips J., Gomer R. The p21-activated kinase (PAK) family member PakD is required for chemorepulsion and proliferation inhibition by autocrine signals in Dictyostelium discoideum. PLoS One 2014, (in press).
100. Phillips J.E., Huang E., Shaulsky G., Gomer R.H. The putative bZIP transcription factor BzpN slows proliferation and functions in the regulation of cell density by autocrine signals in Dictyostelium. PLoS One 2011, 6:e21765.
101. Prossnitz E.R., Arterburn J.B., Sklar L.A. GPR30: a G protein-coupled receptor for estrogen. Mol. Cell. Endocrinol. 2007, 265:138-142.
102. Raper K.B. Dictyostelium discoideum, a new species of slime mold from decaying forest leaves. J. Agric. Res. 1935, 50:135-147.
103. Raper K.B. Pseudoplasmodium formation and organization in Dictyostelium discoideum. J. Elisha Mitchell Sci. Soc. 1940, 56:241-282.
104. Raper K.B. The Dictyostelids 1984, Princeton University Press, Princeton, NJ.
105. Reymond C.D., Schaap P., Veron M., Williams J.G. Dual role of cAMP during Dictyostelium development. Experientia 1995, 51:1166-1174.
106. Richardson D.L., Loomis W.F., Kimmel A.R. Progression of an inductive signal activates sporulation in Dictyostelium discoideum. Development 1994, 120:2891-2900.
107. Rossier C., Franke J., Mullens I.A., Kessin R.H. Regulation of the mRNA for the inhibitor of extracellular cyclic AMP phosphodiesterase of Dictyostelium discoideum. Experientia 1983, 39:672.
108. Saito T., Kato A., Kay R.R. DIF-1 induces the basal disc of the Dictyostelium fruiting body. Dev. Biol. 2008, 317:444-453.
109. Saito T., Taylor G.W., Yang J.C., Neuhaus D., Stetsenko D., Kato A., Kay R.R. Identification of new differentiation inducing factors from Dictyostelium discoideum. Biochim. Biophys. Acta 2006, 1760:754-761.
110. Schaap P. Evolution of developmental cyclic adenosine monophosphate signaling in the Dictyostelia from an amoebozoan stress response. Dev Growth Differ. 2011, 53:452-462.
111. Schilde C., Schaap P. The amoebozoa. Methods Mol. Biol. 2013, 983:1-15.
112. Schulkes C., Schaap P. cAMP-dependent protein kinase activity is essential for preaggregative gene expression in Dictyostelium. FEBS Lett. 1995, 368:381-384.
113. Skoge M., Yue H., Erickstad M., Bae A., Levine H., Groisman A., Loomis W.F., Rappel W.-J. Cellular memory in eukaryotic chemotaxis 2014, (submitted for publication).
114. Soderbom F., Anjard C., Iranfar N., Fuller D., Loomis W.F. An adenylyl cyclase that functions during late development of Dictyostelium. Development 1999, 126:5463-5471.
115. Soderbom F., Loomis W.F. Cell-cell signaling during Dictyostelium development. Trends Microbiol. 1998, 6:402-406.
116. Souza G.M., da Silva A.M., Kuspa A. Starvation promotes Dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway. Development 1999, 126:3263-3274.
117. Souza G.M., Lu S., Kuspa A. YakA, a protein kinase required for the transition from growth to development in Dictyostelium. Development 1998, 125:2291-2302.
118. Sucgang R., Weijer C.J., Siegert F., Franke J., Kessin R.H. Null mutations of the Dictyostelium cyclic nucleotide phosphodiesterase gene block chemotactic cell movement in developing aggregates. Dev. Biol. 1997, 192:181-192.
119. Swaney K.F., Huang C.H., Devreotes P.N. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu. Rev. Biophys. 2010, 39:265-289.
120. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
121. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
122. Takeda K., Shao D., Adler M., Charest P., Loomis W.F., Levine H., Groisman A., Rappel W.-J., Firtel R.A. Incoherent feedforward control governs adaptation of activated Ras in a eukaryotic chemotaxis pathway. Sci. Signal. 2012, 5:ra2.
123. Tanaka Y., Abe H., Uchiyama M., Taya Y., Nishimura S. Isopentenyladenine from Dictyostelium discoideum. Phytochemistry 1978, 17:543-544.
124. Tang L., Gao T., McCollum C., Jang W., Vicker M.G., Ammann R.R., Gomer R.H. A cell number-counting factor regulates the cytoskeleton and cell motility in Dictyostelium. Proc. Natl. Acad. Sci. USA 2002, 99:1371-1376.
125. Thompson C.R.L., Fu Q., Buhay C., Kay R.R., Shaulsky G. A bZIP/bRLZ transcription factor required for DIF signaling in Dictyostelium. Development 2004, 131:513-523.
126. Thompson C.R.L., Kay R.R. The role of DIF-1 signaling in Dictyostelium development. Mol. Cell 2000, 6:1509-1514.
127. Thomson J., Itskovitz-Eldor J., Shapiro S., Waknitz M., Swiergiel J., Marshall V., Jones J. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
128. Tomchik K.J., Devreotes P.N. Adenosine 3',5'-monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution-fluorography technique. Science 1981, 212:443-446.
129. Town C.D., Gross J.D., Kay R.R. Cell differentiation without morphogenesis in Dictyostelium discoideum. Nature 1976, 262:717-719.
130. Velazquez F., Peak-Chew S.Y., Fernandez I.S., Neumann C.S., Kay R.R. Identification of a eukaryotic reductive dechlorinase and characterization of its mechanism of action on its natural substrate. Chem. Biol. 2011, 18:1252-1260.
131. Waddington C.H. Canalization of development and the inheritance of acquired characters. Nature 1942, 150:563-565.
132. Wang J., Hou L.S., Awrey D., Loomis W.F., Firtel R.A., Siu C.H. The membrane glycoprotein gp150 is encoded by the lagC gene and mediates cell-cell adhesion by heterophilic binding during Dictyostelium development. Dev. Biol. 2000, 227:734-745.
133. Wang N., Shaulsky G., Escalante R., Loomis W.F. A two-component histidine kinase gene that functions in Dictyostelium development. EMBO J. 1996, 15:3890-3898.
134. Wang N., Soderbom F., Anjard C., Shaulsky G., Loomis W.F. SDF-2 induction of terminal differentiation in Dictyostelium discoideum is mediated by the membrane-spanning sensor kinase DhkA. Mol. Cell. Biol. 1999, 19:4750-4756.
135. Yamada Y., Kay R.R., Bloomfield G., Ross S., Ivens A., Williams J.G. A new Dictyostelium prestalk cell sub-type. Dev. Biol. 2010, 339:390-397.
136. You C., Okano H., Hui S., Zhang Z., Gunderson C.W., Wang Y.P., Lenz P., Yan D., Hwa T. Coordination of bacterial proteome with metabolism by cyclic AMP signalling. Nature 2013, 500:301-306.
137. Yu J., Vodyanik M., Smuga-Otto K., Antosiewicz-Bourget J., Frane J., Tian S., Nie J., Jonsdottir G., Ruotti V., Stewart R., Slukvin I., Thomson J. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.
138. Yuen I.S., Jain R., Bishop J.D., Lindsey D.F., Deery W.J., van Haastert P.J.M., Gomer R.H. A density-sensing factor regulates signal transduction in Dictyostelium. J. Cell Biol. 1995, 129:1251-1262.
139. Zhang S., Charest P.G., Firtel R.A. Spatiotemporal regulation of Ras activity provides directional sensing. Curr. Biol. 2008, 18:1587-1593.
140. Zhukovskaya N.V., Fukuzawa M., Yamada Y., Araki T., Williams J.G. The Dictyostelium bZIP transcription factor DimB regulates prestalk-specific gene expression. Development 2006, 133:439-448.