Non-genetic heterogeneity and cell fate choice in Dictyostelium discoideum

Development Growth and Differentiation

Volumn 53, Issue 4, 2011, Pages 558-566

  Chattwood, Alex ^a   Thompson, Christopher R L ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cell fate; Dictyostelium discoideum; Differentiation; Heterogeneity

Indexed keywords

MESSENGER RNA;

CALCIUM CELL LEVEL; CELL CYCLE; CELL DIFFERENTIATION; CELL FATE; CELL HETEROGENEITY; CELL PH; CELL POPULATION; CELL TYPE; DICTYOSTELIUM DISCOIDEUM; GENE EXPRESSION; GENETIC HETEROGENEITY; NON GENETIC HETEROGENEITY; NONHUMAN; REVIEW;

CELL LINEAGE; DICTYOSTELIUM; GENETIC HETEROGENEITY;

DICTYOSTELIUM DISCOIDEUM; METAZOA;

EID: 79956070923     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2011.01270.x     Document Type: Review

References (84)

1. 2+ and DIF. Dev. Growth Differ. 33, 469-478.
2. Acar, M., Mettetal, J. T. & van Oudenaarden, A. 2008. Stochastic switching as a survival strategy in fluctuating environments. Nat. Genet. 40, 471-475.
3. Aerts, R. J. 1988. Changes in cytoplasmic pH are involved in the cell type regulation of Dictyostelium. Cell Differ. 23, 125-132.
4. Aerts, R. J., Durston, A. J. & Moolenaar, W. H. 1985. Cytoplasmic pH and the regulation of the Dictyostelium cell cycle. Cell 43, 653-657.
5. Altabef, M., Clarke, J. D. & Tickle, C. 1997. Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development 124, 4547-4556.
6. Araki, T., Nakao, H., Takeuchi, I. & Maeda, Y. 1994. Cell-cycle-dependent sorting in the development of Dictyostelium cells. Dev. Biol. 162, 221-228.
7. Arias, A. M. & Hayward, P. 2006. Filtering transcriptional noise during development: concepts and mechanisms. Nat. Rev. Genet. 7, 34-44.
8. 2+ and development in Dictyostelium discoideum. Int. J. Dev. Biol. 45, 405-414.
9. Baskar, R., Chhabra, P., Mascarenhas, P. & Nanjundiah, V. 2000. A cell type-specific effect of calcium on pattern formation and differentiation in Dictyostelium discoideum. Int. J. Dev. Biol. 44, 491-498.
10. Berks, M. & Kay, R. R. 1990. Combinatorial control of cell differentiation by cAMP and DIF-1 during development of Dictyostelium discoideum. Development 110, 977-984.
11. Blaschke, A., Weijer, C. & MacWilliams, H. 1986. Dictyostelium discoideum: cell-type proportioning, cell-differentiation preference, cell fate, and the behavior of anterior-like cells in Hs1/Hs2 and G+/G- mixtures. Differentiation 32, 1-9.
12. Brazill, D. T., Caprette, D. R., Myler, H. A., Hatton, R. D., Ammann, R. R., Lindsey, D. F., Brock, D. A. & Gomer, R. H. 2000. A protein containing a serine-rich domain with vesicle fusing properties mediates cell cycle-dependent cytosolic pH regulation. J. Biol. Chem. 275, 19231-19240.
13. Brookman, J. J., Town, C. D., Jermyn, K. A. & Kay, R. R. 1982. Developmental regulation of a stalk cell differentiation-inducing factor in Dictyostelium discoideum. Dev. Biol. 91, 191-196.
14. Bruce, A. W. & Zernicka-Goetz, M. 2010. Developmental control of the early mammalian embryo: competition among heterogeneous cells that biases cell fate. Curr. Opin. Genet. Dev. 20, 485-491.
15. Chambers, I., Silva, J., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrana, J., Jones, K., Grotewold, L. & Smith, A. 2007. Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234.
16. Chang, H. H., Hemberg, M., Barahona, M., Ingber, D. E. & Huang, S. 2008. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453, 544-547.
17. Chazaud, C., Yamanaka, Y., Pawson, T. & Rossant, J. 2006. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10, 615-624.
18. Chen, G. & Kuspa, A. 2005. Prespore cell fate bias in G1 phase of the cell cycle in Dictyostelium discoideum. Eukaryot. Cell 4, 1755-1764.
19. Colman-Lerner, A., Gordon, A., Serra, E., Chin, T., Resnekov, O., Endy, D., Pesce, C. G. & Brent, R. 2005. Regulated cell-to-cell variation in a cell-fate decision system. Nature 437, 699-706.
20. Dietrich, J. E. & Hiiragi, T. 2007. Stochastic patterning in the mouse pre-implantation embryo. Development 134, 4219-4231.
21. Dominov, J. A. & Town, C. D. 1986. Regulation of stalk and spore antigen expression in monolayer cultures of Dictyostelium discoideum by pH. J. Embryol. Exp. Morphol. 96, 131-150.
22. Early, V. E. & Williams, J. G. 1988. A Dictyostelium prespore-specific gene is transcriptionally repressed by DIF in vitro. Development 103, 519-524.
23. Eldar, A. & Elowitz, M. B. 2010. Functional roles for noise in genetic circuits. Nature 467, 167-173.
24. Elowitz, M. B., Levine, A. J., Siggia, E. D. & Swain, P. S. 2002. Stochastic gene expression in a single cell. Science 297, 1183-1186.
25. Forman, D. & Garrod, D. R. 1977. Pattern formation in Dictyostelium discoideum. I. Development of prespore cells and its relationship to the pattern of the fruiting body. J. Embryol. Exp. Morphol. 40, 215-228.
26. Fukuzawa, M., Hopper, N. & Williams, J. 1997. cudA: a Dictyostelium gene with pleiotropic effects on cellular differentiation and slug behaviour. Development 124, 2719-2728.
27. Fukuzawa, M., Zhukovskaya, N. V., Yamada, Y., Araki, T. & Williams, J. G. 2006. Regulation of Dictyostelium prestalk-specific gene expression by a SHAQKY family MYB transcription factor. Development 133, 1715-1724.
28. Furukawa, R., Wampler, J. E. & Fechheimer, M. 1990. Cytoplasmic pH of Dictyostelium discoideum amebae during early development - identification of 2 cell subpopulations before the aggregation stage. J. Cell Biol. 110, 1947-1954.
29. Gomer, R. H. & Ammann, R. R. 1996. A cell-cycle phase-associated cell-type choice mechanism monitors the cell cycle rather than using an independent timer. Dev. Biol. 174, 82-91.
30. Gomer, R. H. & Firtel, R. A. 1987. Cell-autonomous determination of cell-type choice in Dictyostelium development by cell-cycle phase. Science 237, 758-762.
31. Gross, J. D., Bradbury, J., Kay, R. R. & Peacey, M. J. 1983. Intracellular pH and the control of cell differentiation in Dictyostelium discoideum. Nature 303, 244-245.
32. Guo, Q., Loomis, C. & Joyner, A. L. 2003. Fate map of mouse ventral limb ectoderm and the apical ectodermal ridge. Dev. Biol. 264, 166-178.
33. Hu, M., Krause, D., Greaves, M., Sharkis, S., Dexter, M., Heyworth, C. & Enver, T. 1997. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 11, 774-785.
34. Huang, E., Blagg, S. L., Keller, T., Katoh, M., Shaulsky, G. & Thompson, C. R. L. 2006. bZIP transcription factor interactions regulate DIF responses in Dictyostelium. Development 133, 449-458.
35. Huang, S., Guo, Y. P., May, G. & Enver, T. 2007. Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev. Biol. 305, 695-713.
36. Hume, D. A. 2000. Probability in transcriptional regulation and its implications for leukocyte differentiation and inducible gene expression. Blood 96, 2323-2328.
37. Inouye, K. 1988. Differences in cytoplasmic pH and the sensitivity to acid load between prespore cells and prestalk cells of Dictyostelium. J. Cell Sci. 91, 109-115.
38. Inouye, K. 1989. Regulation of cytoplasmic pH in the differentiating cell types of the cellular slime mould Dictyostelium discoideum. Biochim. Biophys. Acta 1012, 64-68.
39. Insall, R., Nayler, O. & Kay, R. R. 1992. DIF-1 induces its own breakdown in Dictyostelium. EMBO J. 11, 2849-2854.
40. Kaern, M., Elston, T. C., Blake, W. J. & Collins, J. J. 2005. Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6, 451-464.
41. Kay, R. R., Gadian, D. G. & Williams, S. R. 1986. Intracellular pH in Dictyostelium: a 31P nuclear magnetic resonance study of its regulation and possible role in controlling cell differentiation. J. Cell Sci. 83, 165-179.
42. Kay, R. R. & Thompson, C. R. L. 2009. Forming patterns in development without morphogen gradients: scattered differentiation and sorting out. Cold Spring Harb. Perspect. Biol. Dec;1(6):a001503. Epub 2009 Jul 29.
43. Keller, T. & Thompson, C. R. 2008. Cell type specificity of a diffusible inducer is determined by a GATA family transcription factor. Development 135, 1635-1645.
44. Kessin, R. H. 2001. Dictyostelium. Cambridge University Press, Cambridge, UK.
45. Kubohara, Y., Arai, A., Gokan, N. & Hosaka, K. 2007. Pharmacological evidence that stalk cell differentiation involves increases in the intracellular Ca(2+) and H(+) concentrations in Dictyostelium discoideum. Dev. Growth Differ. 49, 253-264.
46. + concentrations determine cell fate in Dictyostelium discoideum. FASEB J. 8, 869-874.
47. Leach, C. K., Ashworth, J. M. & Garrod, D. R. 1973. Cell sorting out during the differentiation of mixtures of metabolically distinct populations of Dictyostelium discoideum. J. Embryol. Exp. Morphol. 29, 647-661.
48. Lee, H. H., Molla, M. N., Cantor, C. R. & Collins, J. J. 2010. Bacterial charity work leads to population-wide resistance. Nature 467, 82-85.
49. Losick, R. & Desplan, C. 2008. Stochasticity and cell fate. Science 320, 65-68.
50. MacWilliams, H., Doquang, K., Pedrola, R., Dollman, G., Grassi, D., Peis, T., Tsang, A. & Ceccarelli, A. 2006. A retinoblastoma ortholog controls stalk/spore preference in Dictyostelium. Development 133, 1287-1297.
51. Maeda, Y. 1986. A new method for inducing synchronous growth of Dictyostelium discoideum cells using temperature shifts. J. Gen. Microbiol. 132, 1189-1196.
52. Muramoto, T. & Chubb, J. R. 2008. Live imaging of the Dictyostelium cell cycle reveals widespread S phase during development, a G2 bias in spore differentiation and a premitotic checkpoint. Development 135, 1647-1657.
53. Murry, C. E. & Keller, G. 2008. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132, 661-680.
54. Nayler, O., Insall, R. & Kay, R. R. 1992. Differentiation-inducing-factor dechlorinase, a novel cytosolic dechlorinating enzyme from Dictyostelium discoideum. Eur. J. Biochem. 208, 531-536.
55. Neumann, C. S., Walsh, C. T. & Kay, R. R. 2010. A flavin-dependent halogenase catalyzes the chlorination step in the biosynthesis of Dictyostelium differentiation-inducing factor 1. Proc. Natl Acad. Sci. USA 107, 5798-5803.
56. Noce, T. & Takeuchi, I. 1985. Prestalk/prespore differentiation tendency of Dictyostelium discoideum cells as detected by a stalk-specific monoclonal antibody. Dev. Biol. 109, 157-164.
57. Novick, A. & Weiner, M. 1957. Enzyme induction as an all-or-none phenomenon. Proc. Natl Acad. Sci. USA 43, 553-566.
58. Plusa, B., Piliszek, A., Frankenberg, S., Artus, J. & Hadjantonakis, A. K. 2008. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081-3091.
59. Raj, A., Rifkin, S. A., Andersen, E. & van Oudenaarden, A. 2010. Variability in gene expression underlies incomplete penetrance. Nature 463, 913-918.
60. Raj, A. & van Oudenaarden, A. 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226.
61. Raser, J. M. & O'Shea, E. K. 2004. Control of stochasticity in eukaryotic gene expression. Science 304, 1811-1814.
62. Ratner, D. I. 1986. Equivalence of intracellular pH of differentiating Dictyostelium cell types. Nature 321, 180-182.
63. Saito, T., Kato, A. & Kay, R. R. 2008. DIF-1 induces the basal disc of the Dictyostelium fruiting body. Dev. Biol. 317, 444-453.
64. Satre, M., Klein, G. & Martin, J. B. 1986. Intracellular pH control in Dictyostelium discoideum: a 31P-NMR analysis. Biochimie 68, 1253-1261.
65. 2+ levels mediates stalk gene induction by differentiation inducing factor in Dictyostelium. EMBO J. 15, 5177-5183.
66. Schnabel, R., Bischoff, M., Hintze, A., Schulz, A. K., Hejnol, A., Meinhardt, H. & Hutter, H. 2006. Global cell sorting in the C. elegans embryo defines a new mechanism for pattern formation. Dev. Biol. 294, 418-431.
67. Sharma, S. V., Lee, D. Y., Li, B., Quinlan, M. P., Takahashi, F., Maheswaran, S., McDermott, U., Azizian, N., Zou, L., Fischbach, M. A., Wong, K. K., Brandstetter, K., Wittner, B., Ramaswamy, S., Classon, M. & Settleman, J. 2010. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69-80.
68. Silva, J. & Smith, A. 2008. Capturing pluripotency. Cell 132, 532-536.
69. Smith, M. C., Sumner, E. R. & Avery, S. V. 2007. Glutathione and Gts1p drive beneficial variability in the cadmium resistances of individual yeast cells. Mol. Microbiol. 66, 699-712.
70. Stevense, M., Muramoto, T., Muller, I. & Chubb, J. R. 2010. Digital nature of the immediate-early transcriptional response. Development 137, 579-584.
71. Thompson, C. R. L., Fu, Q., Buhay, C., Kay, R. R. & Shaulsky, G. 2004a. A bZIP/bRLZ transcription factor required for DIF signaling in Dictyostelium. Development 131, 513-523.
72. Thompson, C. R. L. & Kay, R. R. 2000a. Cell-fate choice in Dictyostelium: intrinsic biases modulate sensitivity to DIF signaling. Dev. Biol. 227, 56-64.
73. Thompson, C. R. L. & Kay, R. R. 2000b. The role of DIF-1 signaling in Dictyostelium development. Mol. Cell 6, 1509-1514.
74. Thompson, C. R. L., Reichelt, S. & Kay, R. R. 2004b. A demonstration of pattern formation without positional information in Dictyostelium. Dev. Growth Differ. 46, 363-369.
75. Weijer, C. J., Duschl, G. & David, C. N. 1984a. A revision of the Dictyostelium discoideum cell cycle. J. Cell Sci. 70, 111-131.
76. Weijer, C. J., Duschl, G. & David, C. N. 1984b. Dependence of cell-type proportioning and sorting on cell cycle phase in Dictyostelium discoideum. J. Cell Sci. 70, 133-145.
77. Williams, J. G., Ceccarelli, A., McRobbie, S., Mahbubani, H., Kay, R. R., Farly, A., Berks, M. & Jermyn, K. A. 1987. Direct induction of Dictyostelium prestalk gene expression by DIF provides evidence that DIF is a morphogen. Cell 49, 185-192.
78. Wood, S. A., Ammann, R. R., Brock, D. A., Li, L., Spann, T. & Gomer, R. H. 1996. RtoA links initial cell type choice to the cell cycle in Dictyostelium. Development 122, 3677-3685.
79. Wu, Z., Luby-Phelps, K., Bugde, A., Molyneux, L. A., Denard, B., Li, W. H., Suel, G. M. & Garbers, D. L. 2009. Capacity for stochastic self-renewal and differentiation in mammalian spermatogonial stem cells. J. Cell Biol. 187, 513-524.
80. Yamada, Y., Kay, R. R., Bloomfield, G., Ross, S., Ivens, A. & Williams, J. G. 2010. A new Dictyostelium prestalk cell sub-type. Dev. Biol. 339, 390-397.
81. Yamanaka, Y., Lanner, F. & Rossant, J. 2010. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137, 715-724.
82. Yarger, J., Stults, K. & Soll, D. R. 1974. Observations on the growth of Dictyostelium discoideum in axenic medium: evidence for an extracellular growth inhibitor synthesized by stationary phase cells. J. Cell Sci. 14, 681-690.
83. Zada-Hames, I. M. & Ashworth, J. M. 1978. The cell cycle during the vegetative stage of Dictyostelium discoideum and its response to temperature change. J. Cell Sci. 32, 1-20.
84. Zhukovskaya, N. V., Fukuzawa, M., Yamada, Y., Araki, T. & Williams, J. G. 2006. The Dictyostelium bZIP transcription factor DimB regulates prestalk-specific gene expression. Development 133, 439-448.