Patterning of development in Dictyostelium discoideum: factors regulating growth, differentiation, spore dormancy, and germination.

Cellular communication dictates all stages of growth and development in the cellular slime molds. Dictyostelium discoideum utilizes a number of signal molecules for cell-to-cell communication, including growth and density factors, cAMP, ammonia, differentiation-inducing factor, discadenine, and spore autoactivator. A source and sink model is presented in which the assimilation of ammonia plays a major role in determining cell fate and pattern formation. This model emphasizes a recycling of ammonia by prespore cells, the accumulation of free hydrophilic and neutral amino acids, and their incorporation into proteins associated with sporulation and (or) germination. If spore cAMP signalling is regulated by the relative concentrations of discadenine and autoactivator, and its disruption triggers the initiation of the spore germination cascade, then the accumulation of intracellular cAMP may be necessary for both sporulation and dormancy maintenance.

[1]  R. Kay,et al.  Mutation of protein kinase A causes heterochronic development of Dictyostelium , 1992, Nature.

[2]  D. Cotter,et al.  Spore germination in Dictyostelium discoideum. II. Effects of dimethyl sulfoxide on post-activation lag as evidence for the multistate model of activation. , 1966, Archives of Microbiology.

[3]  M. Montminy,et al.  The CREB family of transcription activators. , 1992 .

[4]  M. Khosla,et al.  Ras-related genes in Dictyostelium discoideum. , 1991, Developmental genetics.

[5]  Yoshimasa Tanaka,et al.  Purification and some properties of discadenine synthase from Dictyostelium discoideum , 1986 .

[6]  A. Tsang,et al.  Translocation of an unusual cAMP receptor to the nucleus during development of Dictyostelium discoideum. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[7]  A. Kuspa,et al.  Physical mapping of genes to specific chromosomes in Dictyostelium discoideum. , 1992, Genomics.

[8]  J. Ståhlberg,et al.  A binding-site-deficient, catalytically active, core protein of endoglucanase III from the culture filtrate of Trichoderma reesei. , 1988, European journal of biochemistry.

[9]  M. B. Coukell,et al.  The precocious appearance and activation of an adenylate cyclase in a rapid developing mutant of Dictyostelium discoideum , 1980, FEBS letters.

[10]  G. Weeks,et al.  The effect of ammonia on stalk cell formation in submerged monolayers of Dictyostelium discoideum. , 1983, Cell differentiation.

[11]  R. Firtel,et al.  A role for cAMP-dependent protein kinase A in early Dictyostelium development. , 1990, Genes & development.

[12]  J. Williams,et al.  A Dictyostelium prespore-specific gene is transcriptionally repressed by DIF in vitro. , 1988, Development.

[13]  Complementary effects of ammonia and cAMP on aggregation territory size in the cellular slime mold Dictyostelium mucoroides. , 1977 .

[14]  R. Doolittle,et al.  A simple method for displaying the hydropathic character of a protein. , 1982, Journal of molecular biology.

[15]  J. Lonski.  The effect of ammonia on fruiting body size and microcyst formation in the cellular slime molds. , 1976, Developmental biology.

[16]  K. C. Lee.  Permeability of Dictyostelium discoideum towards amino acids and inulin: a possible relationship between initiation of differentiation and loss of "pool" metabolites. , 1972, Journal of general microbiology.

[17]  K. Yanagisawa,et al.  A new class of rapidly developing mutants in Dictyostelium discoideum: implications for cyclic AMP metabolism and cell differentiation. , 1983, Developmental biology.

[18]  P. Rosness.  Cellulolytic Enzymes During Morphogenesis in Dictyostelium discoideum , 1968, Journal of bacteriology.

[19]  F. Marin.  Regulation of development in Dictyostelium discoideum: II. Regulation of early cell differentiation by amino acid starvation and intercellular interaction. , 1977, Developmental biology.

[20]  R. Giorda,et al.  Organization of a gene family developmentally regulated during Dictyostelium discoideum spore germination. , 1989, Journal of molecular biology.

[21]  R. Kay,et al.  Two distinct classes of prestalk-enriched mRNA sequences in Dictyostelium discoideum. , 1987, Development.

[22]  R. Kessin,et al.  A defined minimal medium for axenic strains of Dictyostelium discoideum. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Gooley,et al.  Glycoproteins that exhibit extensive size polymorphisms in Dictyostelium discoideum. , 1989, Genetics.

[24]  G. Weeks,et al.  Studies on the accumulation of the differentiation-inducing factor (DIF) in high-cell-density monolayers of Dictyostelium discoideum. , 1989, Developmental biology.

[25]  G. Weeks,et al.  A possible role for DIF-2 in the formation of stalk cells during Dictyostelium development. , 1991, Developmental biology.

[26]  C. Town,et al.  Relationships between extracellular pH, intracellular pH, and gene expression in Dictyostelium discoideum. , 1987, Developmental biology.

[27]  D. Ratner,et al.  Induction and modulation of cell-type-specific gene expression in dictyostelium , 1983, Cell.

[28]  J C Wootton,et al.  The Q-linker: a class of interdomain sequences found in bacterial multidomain regulatory proteins. , 1989, Protein engineering.

[29]  D. Gadian,et al.  Intracellular pH in Dictyostelium: a 31P nuclear magnetic resonance study of its regulation and possible role in controlling cell differentiation. , 1986, Journal of cell science.

[30]  P. Newell,et al.  Inositol phosphates, G-proteins and ras genes involved in chemotactic signal transduction of Dictyostelium. , 1988, Journal of cell science.

[31]  R. Kay,et al.  Direct induction of dictyostelium prestalk gene expression by DIF provides evidence that DIF is a morphogen , 1987, Cell.

[32]  D. Cotter,et al.  Spore germination in Dictyostelium discoideum: trehalase and the requirement for protein synthesis. , 1970, Developmental biology.

[33]  G. Gerisch,et al.  Regulation of extracellular cyclic-AMP-phosphodiesterase activity during development of Dictyostelium discoideum. , 1971, Biochemical and biophysical research communications.

[34]  B. Haribabu,et al.  Pharmacological characterization of cyclic AMP receptors mediating gene regulation in Dictyostelium discoideum , 1986, Molecular and cellular biology.

[35]  M. Clarke,et al.  Induction of gene expression in Dictyostelium by prestarvation factor, a factor secreted by growing cells. , 1991, Developmental genetics.

[36]  Robert D. Taylor,et al.  A cyclic AMP dependent protein kinase in Dictyosteliumdiscoideum , 1982 .

[37]  D. Peters,et al.  Control of cAMP-induced gene expression by divergent signal transduction pathways. , 1991, Developmental genetics.

[38]  R. Firtel,et al.  cAMP signal transduction pathways regulating development of Dictyostelium discoideum. , 1991, Current opinion in genetics & development.

[39]  J. Williams,et al.  An analysis of culmination in Dictyostelium using prestalk and stalk-specific cell autonomous markers. , 1991, Development.

[40]  Cell surface binding of adenosine to Dictyostelium and inhibition of pulsatile signalling , 1982 .

[41]  R. Firtel,et al.  cAMP and cell sorting control the spatial expression of a developmentally essential cell-type-specific ras gene in Dictyostelium. , 1991, Genes & development.

[42]  M. Rennie,et al.  Inhibition of protein breakdown by glutamine in perfused rat skeletal muscle , 1988, FEBS letters.

[43]  R. Gomer,et al.  Regulation and processing of a secreted protein that mediates sensing of cell density in Dictyostelium. , 1991, Development.

[44]  A. Tsang,et al.  Cloning and characterization of cDNAs encoding a novel cyclic AMP-binding protein in Dictyostelium discoideum. , 1990, Gene.

[45]  D. Cotter,et al.  The characterization and secretion pattern of the lysosomal trehalases ofDictyostelium discoideum , 1986 .

[46]  R. Kamboj,et al.  Cell-cell adhesion and morphogenesis in Dictyostelium discoideum. , 1990, Developmental genetics.

[47]  Yoshimasa Tanaka,et al.  Structure of discadenine, a spore germination inhibitor from the cellular slime mold, dictyostelium discoideum , 1976 .

[48]  R. Kay,et al.  Diffusible signal molecules controlling cell differentiation and patterning in Dictyostelium. , 1991, Development (Cambridge, England). Supplement.

[49]  R. Gomer,et al.  Cell-autonomous determination of cell-type choice in Dictyostelium development by cell-cycle phase. , 1987, Science.

[50]  K. Inouye.  Induction by acid load of the maturation of prestalk cells in Dictyostelium discoideum , 1988 .

[51]  W. Nellen,et al.  Structure, expression, and inactivation by gene disruption of the Dictyostelium discoideum prespore gene EB4. , 1991, Developmental genetics.

[52]  D. Ebert,et al.  Biochemical and genetic analysis of the biosynthesis, sorting, and secretion of Dictyostelium lysosomal enzymes. , 1990, Developmental genetics.

[53]  D. L. Richardson,et al.  A prespore gene, Dd31, expressed during culmination of Dictyostelium discoideum. , 1991, Developmental biology.

[54]  B. Riley,et al.  Conditions that elevate intracellular cyclic AMP levels promote spore formation in Dictyostelium. , 1989, Differentiation; research in biological diversity.

[55]  L. Tisa,et al.  Expression of glycosidase activities during germination of Dictyostelium discoideum spores , 1980, Journal of bacteriology.

[56]  K. Raper,et al.  ENCYSTMENT STAGES OF DICTYOSTELIUM , 1957 .

[57]  T. Lam,et al.  Synthesis of stage-specific glycoproteins in Dictyostelium discoideum during development. , 1981, Developmental biology.

[58]  D. Cotter,et al.  Analysis of Dictyostelium mucoroides Macrocysts by Using a Simple Breakage and Fractionation Procedure , 1991, Applied and Environmental Microbiology.

[59]  C. Weijer,et al.  Influence of cyclic AMP and hydrolysis products on cell type regulation in Dictyostelium discoideum. , 1985, Journal of embryology and experimental morphology.

[60]  M. Clarke,et al.  Density-dependent induction of discoidin-I synthesis in exponentially growing cells of Dictyostelium discoideum. , 1987, Differentiation; research in biological diversity.

[61]  Y. Maeda,et al.  CELL DIFFERENTIATION AND FINE STRUCTURES IN THE DEVELOPMENT OF THE CELLULAR SLIME MOLDS 1 , 1969 .

[62]  Harry K. MacWilliams,et al.  Pattern Formation in Dictyostelium , 1984 .

[63]  R. B. Sollitto,et al.  Ammonia is the gas used for the spacing of fruiting bodies in the cellular slime mold, Dictyostelium discoideum , 1987 .

[64]  W. Loomis.  Cell-cell adhesion in Dictyostelium discoideum. , 1988, Developmental genetics.

[65]  P. Schaap.  Regulation of size and pattern in the cellular slime molds , 1986 .

[66]  H. Lodish,et al.  Regulation of dictyostelium discoideum mRNAs specific for prespore or prestalk cells , 1983, Cell.

[67]  J. Bonner,et al.  Regulation of the anterior-like cell state by ammonia in Dictyostelium discoideum. , 1990, Developmental genetics.

[68]  J. Vandekerckhove,et al.  Vegetative Dictyostelium cells containing 17 actin genes express a single major actin , 1980, Nature.

[69]  K. Inouye.  Control of cell type proportions by a secreted factor in Dictyostelium discoideum. , 1989, Development.

[70]  I. Takeuchi,et al.  Vital staining of autophagic vacuoles in differentiating cells of Dictyostelium discoideum , 1983 .

[71]  J. Ashworth,et al.  Cell sorting out during the differentiation of mixtures of metabolically distinct populations of Dictyostelium discoideum. , 1973, Journal of embryology and experimental morphology.

[72]  H. Lodish,et al.  Transcriptional control of gene expression during development of Dictyostelium discoideum , 1982, Molecular and cellular biology.

[73]  G. Gustafson,et al.  Purification and characterization of a proteinase from Dictyostelium discoideum. , 1979, The Journal of biological chemistry.

[74]  D. Cotter,et al.  The timing of ribonucleic acid synthesis during the germination of heat-activated Dictyostelium discoideum spores. , 1983, Canadian journal of microbiology.

[75]  M. Clarke,et al.  Analysis of the prestarvation response in growing cells of Dictyostelium discoideum. , 1988, Developmental genetics.

[76]  J. Williams,et al.  Multiple copies of a G-rich element upstream of a cAMP-inducible Dictyostelium gene are necessary but not sufficient for efficient gene expression. , 1988, Nucleic acids research.

[77]  A. Jacobson,et al.  mRNA decay rates in late-developing Dictyostelium discoideum cells are heterogeneous, and cyclic AMP does not act directly to stabilize cell-type-specific mRNAs , 1988, Molecular and cellular biology.

[78]  J. Segall,et al.  cDNA sequence of cyclophilin from Dictyostelium discoideum. , 1991, Developmental genetics.

[79]  D. Shaw,et al.  Characterization of genes that are developmentally regulated during Dictyostelium discoideum spore germination. , 1988, Developmental genetics.

[80]  B. Hames,et al.  Developmental expression and characterization of the gene encoding spore coat protein SP60 in Dictyostelium discoideum , 1990, Molecular microbiology.

[81]  C. N. David,et al.  Ammonia plus another factor are necessary for differentiation in submerged clumps of Dictyostelium. , 1979, Journal of cell science.

[82]  R. Delude,et al.  Structure, expression, and regulation of members of the developmentally controlled V and H gene classes from Dictyostelium. , 1991, Developmental genetics.

[83]  M. Sussman,et al.  Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. , 1977, Journal of molecular biology.

[84]  R. Kay,et al.  Combinatorial control of cell differentiation by cAMP and DIF-1 during development of Dictyostelium discoideum. , 1990, Development.

[85]  A. Gooley,et al.  Immunodominant carbohydrate determinants in the multicellular stages of Dictyostelium discoideum. , 1991, Journal of general microbiology.

[86]  J. Williams,et al.  Structural and functional characterization of genes encoding Dictyostelium prestalk and prespore cell-specific proteins. , 1988, Developmental genetics.

[87]  B. Hames,et al.  The metabolism of macromolecules during the differentiation of Myxamoebae of the cellular slime mould Dictyostelium discoideum containing different amounts of glycogen. , 1974, The Biochemical journal.

[88]  J. Bonner,et al.  Timing of the formation of the prestalk and prespore zones in Dictyostelium discoideum , 1990 .

[89]  A. Noegel,et al.  Heterodimeric capping proteins constitute a highly conserved group of actin-binding proteins. , 1990, Developmental genetics.

[90]  J. Wheldrake,et al.  The NAD-dependent glutamate dehydrogenase from Dictyostelium discoideum: purification and properties. , 1991, Archives of biochemistry and biophysics.

[91]  R. Kay,et al.  A possible morphogen controlling differentiation in Dictyostelium , 1983, Nature.

[92]  D. Cotter,et al.  Spore Germination in Strains of Dictyostelium discoideum and Other Members of the Dictyosteliaceae , 1968, Journal of bacteriology.

[93]  J. Williams,et al.  Cytoplasmic acidification facilitates but does not mediate DIF-induced prestalk gene expression in Dictyostelium discoideum. , 1990, Developmental biology.

[94]  G. Weeks,et al.  The requirement for DIF for prestalk and stalk cell formation in Dictyostelium discoideum: a comparison of in vivo and in vitro differentiation conditions. , 1988, Developmental biology.

[95]  R. Kay,et al.  Dictyostelium mutants lacking DIF, a putative morphogen , 1983, Cell.

[96]  J. Spudich,et al.  Developmentally regulated protein-tyrosine kinase genes in Dictyostelium discoideum , 1990, Molecular and cellular biology.

[97]  H. Ennis,et al.  Ribosomal protein synthesis during spore germination and vegetative growth in Dictyostelium discoideum. , 1982, The Journal of biological chemistry.

[98]  E. Cox,et al.  The regulation of cellular slime mold development: a factor causing development of Polysphondylium violaceum aggregation-defective mutants. , 1978, Developmental biology.

[99]  W. Loomis,et al.  Sequence of the Dictyostelium discoideum spore coat gene SP96. , 1989, Nucleic acids research.

[100]  C. Weijer,et al.  Dependence of cell-type proportioning and sorting on cell cycle phase in Dictyostelium discoideum. , 1984, Journal of cell science.

[101]  W. Loomis,et al.  Spore coat proteins of Dictyostelium discoideum are packaged in prespore vesicles. , 1983, Developmental biology.

[102]  R. Kay,et al.  Nature and distribution of the morphogen DIF in the Dictyostelium slug. , 1987, Development.

[103]  I. Takeuchi,et al.  Role of cell sorting in pattern formation in Dictyostelium discoideum. , 1981, Differentiation; research in biological diversity.

[104]  M. Simon,et al.  cAMP-dependent protein kinase from Dictyostelium discoideum. , 1988, Developmental genetics.

[105]  B. Wright,et al.  Protein and amino acid turnover during differentiation in the slime mold. I. Utilization of endogenous amino acids and proteins. , 1960, Biochimica et biophysica acta.

[106]  David P. Lane,et al.  Origins of the prestalk-prespore pattern in Dictyostelium development , 1989, Cell.

[107]  R. Kessin,et al.  Isolation of Germination Mutants of Dictyostelium discoideum , 1974, Journal of bacteriology.

[108]  R. Kay,et al.  Cyclic AMP is an inhibitor of stalk cell differentiation in Dictyostelium discoideum. , 1988, Developmental biology.

[109]  M. Sussman,et al.  Mutants of Dictyostelium discoideum defective in spore germination , 1975, Journal of bacteriology.

[110]  R. Firtel,et al.  A spatial gradient of expression of a cAMP-regulated prespore cell-type-specific gene in Dictyostelium. , 1990, Genes & development.

[111]  D. Blumberg,et al.  Ca++ antagonists distinguish different requirements for cAMP-mediated gene expression in the cellular slime mold, Dictyostelium discoideum. , 1989, Differentiation; research in biological diversity.

[112]  R. Firtel,et al.  A developmentally regulated trans-acting factor recognizes dissimilar G/C-rich elements controlling a class of cAMP-inducible Dictyostelium genes. , 1990, Genes & development.

[113]  R. Kessin,et al.  Detection and developmental regulation of the mRNA for the regulatory subunit of the cAMP‐dependent protein kinase of D. discoideum by cell‐free translation. , 1986, The EMBO journal.

[114]  S. Emr,et al.  The fungal vacuole: composition, function, and biogenesis. , 1990, Microbiological reviews.

[115]  C N David,et al.  Fate and regulation of anterior-like cells in Dictyostelium slugs. , 1982, Developmental biology.

[116]  M. Brenner.  Cyclic AMP gradient in migrating pseudoplasmodia of the cellular slime mold Dictyostelium discoideum. , 1977, The Journal of biological chemistry.

[117]  A. Noegel,et al.  Dictyostelium annexin VII (synexin). cDNA sequence and isolation of a gene disruption mutant. , 1991, The Journal of biological chemistry.

[118]  J. Bonner,et al.  Patterns of glucose utilization and protein synthesis in the development of Dictyostelium discoideum , 1984 .

[119]  W. Loomis,et al.  The timing of cell-type-specific differentiation in Dictyostelium discoideum. , 1984, Developmental biology.

[120]  William F. Loomis,et al.  Dictyostelium discoideum: A Developmental System , 1977 .

[121]  M. Maeda.  Efficient Induction of Sporulation of Dictyostelium Prespore Cells by 8‐Bromocyclic AMP under Both Submerged‐ and Shaken‐Culture Conditions and Involvement of Protein Kinase(s) in Its Action , 1992, Development, growth & differentiation.

[122]  R. Firtel,et al.  Identification of the sequences controlling cyclic AMP regulation and cell-type-specific expression of a prestalk-specific gene in Dictyostelium discoideum. , 1987, Molecular and cellular biology.

[123]  J. Bonner,et al.  A histochemical study of differentiation in the cellular slime molds , 1955 .

[124]  D. Cotter,et al.  Germination of Dictyotelium discoideum spores. A sup 31 P NMR analysis , 1988 .

[125]  W. Loomis.  Role of the surface sheath in the control of morphogenesis in Dictyostelium discoideum. , 1972, Nature: New biology.

[126]  F. Siegert,et al.  Analysis of optical density wave propagation and cell movement in the cellular slime mould Dictyostelium discoideum , 1991 .

[127]  Y. Maeda.  Pattern Formation in a Cell‐Cycle Dependent Manner during the Development of Dictyostelium discoideum , 1993, Development, growth & differentiation.

[128]  W. Loomis.  The Development of Dictyostelium Discoideum , 1982 .

[129]  T. H. Jones,et al.  Cellulases released during the germination of Dictyostelium discoideum spores , 1979, Journal of bacteriology.

[130]  K. Inouye.  Measurements of intracellular pH and its relevance to cell differentiation in Dictyostelium discoideum. , 1985, Journal of cell science.

[131]  R. Kay,et al.  A specific DIF binding protein in Dictyostelium. , 1990, The EMBO journal.

[132]  K. Williams,et al.  Movement of the Dictyostelium discoideum slug: models, musings, and images. , 1988, Developmental genetics.

[133]  J. Bonner,et al.  Immunofluorescence evidence for the distribution of cyclic AMP in cells and cell masses of the cellular slime molds. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[134]  P. Newell,et al.  Genetic Analysis of the Slug Stage of Dictyostelium discoideum , 1982 .

[135]  J. Williams,et al.  Multiple roles for cAMP-dependent protein kinase during Dictyostelium development. , 1992, Developmental biology.

[136]  B. Wright,et al.  Glutamate oxidation in the differentiating slime mold. II. Studies in vitro. , 1963, Biochimica et biophysica acta.

[137]  Jeffrey G. Williams,et al.  Regulation of cellular differentiation during Dictyostelium morphogenesis. , 1991, Current opinion in genetics & development.

[138]  E. Katz,et al.  Evidence for the presence of a growth factor in Dictyostelium discoideum. , 1991, Developmental genetics.

[139]  D. O’Day,et al.  Ammonia and the induction of microcyst differentiation in wild-type and mutant strains of the cellular slime mold Polysphondylium pallidum. , 1982, Developmental biology.

[140]  M. Sussman,et al.  Synchrony of enzyme accumulation in a population of differentiating slime mold cells. , 1969, Biochimica et biophysica acta.

[141]  D. Cotter,et al.  Dictyostelium discoideum spore germination: increases in proteinase activity are not directly coupled to the emergence of myxamoebae , 1990 .

[142]  S A McDonald,et al.  Cell-cycle regulation of center initiation in Dictyostelium discoideum. , 1986, Developmental biology.

[143]  P. V. Haastert,et al.  Sensory transduction in eukaryotes , 1991 .

[144]  J. Milne,et al.  A Ca2+ transport system associated with the plasma membrane of Dictyostelium discoideum is activated by different chemoattractant receptors , 1991, The Journal of cell biology.

[145]  R. Kay,et al.  Developmental regulation of a stalk cell differentiation-inducing factor in Dictyostelium discoideum. , 1982, Developmental biology.

[146]  E. L. Coe,et al.  Conversion of aspartic acid to glucose during culmination of Dictyostelium discoideum. , 1969, Biochimica et Biophysica Acta.

[147]  G. Gerisch,et al.  Cyclic AMP phosphodiesterase and its inhibitor in slime mould development. , 1972, Nature: New biology.

[148]  G. Weeks,et al.  The effect of cAMP on differentiation inducing factor (DIF)‐mediated formation of stalk cells in low‐cell‐density monolayers of Dictyostelium discoideum , 1988 .

[149]  H. Padh,et al.  Characterization of a vacuolar proton ATPase in Dictyostelium discoideum. , 1989, Biochimica et biophysica acta.

[150]  Fiona M. Ross,et al.  Inhibition by Adenosine of Aggregation Centre Initiation and Cyclic AMP Binding in Dictyostelium , 1982 .

[151]  M. Oyama,et al.  Interaction of cAMP with the cell-surface receptor induces cell-type-specific mRNA accumulation in Dictyostelium discoideum. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[152]  D. E. Hemmes,et al.  Structural and enzymatic analysis of the spore wall layers in Dictyostelium discoideum. , 1972, Journal of Ultrastructure Research.

[153]  D. Cotter,et al.  Spore-activating agents influence the temporal and quantitative activity of β-glucosidase and trehalase during Dictyostelium discoideum germination , 1982 .

[154]  M. Véron,et al.  A cAMP‐dependent protein kinase is present in differentiating Dictyostelium discoideum cells , 1982, The EMBO journal.

[155]  R. Gomer,et al.  A secreted 80 x 10(3) Mr protein mediates sensing of cell density and the onset of development in Dictyostelium. , 1991, Development.

[156]  J. Williams,et al.  Structural and functional characterization of a Dictyostelium gene encoding a DIF inducible, prestalk-enriched mRNA sequence. , 1987, Nucleic acids research.

[157]  C. Singleton,et al.  Primary structure and regulation of vegetative specific genes of Dictyostelium discoideum. , 1989, Nucleic acids research.

[158]  M. Sussman,et al.  Inhibition by ammonia of intracellular cAMP accumulation in dictyostelium discoideum: Its significance for the regulation of morphogenesis , 1979 .

[159]  C. Rutherford,et al.  A stalk-specific localization of trehalase activity in Dictyostelium discoideum. , 1976, Experimental cell research.

[160]  R. Kay,et al.  Overexpression of Dd PK2 protein kinase causes rapid development and affects the intracellular cAMP pathway of Dictyostelium discoideum. , 1992, Development.

[161]  D. Fong,et al.  Protease activity during cell differentiation of the cellular slime mold Dictyostelium discoideum , 1978, Journal of bacteriology.

[162]  T. Ozaki,et al.  Protein binding and DNase-I-hypersensitive sites in the cis-acting regulatory region of the spore-coat SP96 gene of Dictyostelium , 1992, Mechanisms of Development.

[163]  R. Pisoni,et al.  The transport systems of mammalian lysosomes. , 1991, Biochimica et biophysica acta.

[164]  W. Loomis,et al.  Effector controlling accumulation of N-acetylglucosaminidase during development of Dictyostelium discoideum. , 1978, Developmental biology.

[165]  D. Shaw,et al.  A shared internal threonine-glutamic acid-threonine-proline repeat defines a family of Dictyostelium discoideum spore germination specific proteins. , 1990, Biochemistry.

[166]  P. Schaap,et al.  Cyclic AMP-phosphodiesterase induces dedifferentiation of prespore cells in Dictyostelium discoideum slugs: evidence that cyclic AMP is the morphogenetic signal for prespore differentiation , 1988 .

[167]  R. Klein.  Determination of the stereoconfiguration of natural pterins by chiral high-performance liquid chromatography. , 1992, Analytical biochemistry.

[168]  M. Darmon,et al.  A differentiation stimulating factor induces cell sensitivity to 3':5'-cyclic AMP pulses in dictyostelium discoideum. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[169]  H. Lodish,et al.  The effects of cell density and starvation on early developmental events in Dictyostelium discoideum. , 1980, Developmental biology.

[170]  M. Sussman,et al.  A Possible Mechanism of Morphogenetic Regulation in Dictyostelium discoideum , 1978 .

[171]  J. Gross,et al.  Plasma membrane proton pump inhibition and stalk cell differentiation in Dictyostelium discoideum. , 1988, Differentiation; research in biological diversity.

[172]  J. Blume,et al.  Dictyostelium discoideum gene family contains a long internal amino acid repeat. , 1991, Developmental genetics.

[173]  S. Free,et al.  Developing Dictyostelium cells contain the lysosomal enzyme alpha- mannosidase in a secretory granule , 1989, The Journal of cell biology.

[174]  R. Gomer,et al.  Developmental regulation of a dictyostelium gene encoding a protein homologous to mammalian ras protein , 1984, Cell.

[175]  B. Riley,et al.  Inhibitors of intracellular cyclic AMP accumulation affect differentiation of sporogenous mutants of Dictyostelium discoideum , 1986 .

[176]  J. Williams,et al.  A new anatomy of the prestalk zone in Dictyostelium , 1989, Nature.

[177]  I. Majerfeld,et al.  Identification of the regulatory subunit of a cAMP-dependent protein kinase in Dictyostelium discoideum. , 1982, Biochemical and biophysical research communications.

[178]  R. Kay,et al.  Signals controlling cell differentiation and pattern formation in Dictyostelium. , 1988, Developmental genetics.

[179]  D. Cotter,et al.  Utilization of trehalose during Dictyostelium discoideum spore germination. , 1982, Developmental biology.

[180]  G. Klein,et al.  Intracellular pH control in Dictyostelium discoideum: a 31P-NMR analysis. , 1986, Biochimie.

[181]  J. Williams,et al.  Identification of sequences regulating the transcription of a Dictyostelium gene selectively expressed in prespore cells. , 1989, Nucleic acids research.

[182]  K. Williams,et al.  Evidence that positional information is used to establish the prestalk‐prespore pattern in Dictyostelium discoideum aggregates , 1984, The EMBO journal.

[183]  R. Gomer,et al.  cAMP induction of prespore and prestalk gene expression in Dictyostelium is mediated by the cell-surface cAMP receptor. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[184]  J. Gross,et al.  The effect of ammonia on cell-type-specific enzyme accumulation in Dictyostelium discoideum. , 1989, Cell differentiation and development : the official journal of the International Society of Developmental Biologists.

[185]  R. Firtel,et al.  An 80-bp cis-acting regulatory region controls cAMP and development regulation of a prestalk gene in Dictyostelium. , 1988, Genes & development.

[186]  H. Lodish,et al.  Cyclic AMP stabilizes a class of developmentally regulated Dictyostelium discoideum mRNAs , 1983, Nature.

[187]  R. Kessin,et al.  The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum utilizes alternate promoters and splicing for the synthesis of multiple mRNAs , 1989, Molecular and cellular biology.

[188]  J. Williams,et al.  Structural characterization of Dictyostelium discoideum prespore-specific gene D19 and of its product, cell surface glycoprotein PsA , 1988, Molecular and cellular biology.

[189]  J. Williams,et al.  A developmentally regulated cysteine proteinase in Dictyostelium discoideum. , 1985, The EMBO journal.

[190]  L. Tisa.  The expression of acid and alkaline phosphatase activities during germination of Dictyostelium discoideum spores , 1979 .

[191]  J. Bonner,et al.  Characterization of the genome of the cellular slime mold Dictyostelium discoideum. , 1972, Journal of molecular biology.

[192]  B. Wright,et al.  Effect of intracellular carbohydrates on heat resistance of Dictyostelium discoideum spores , 1979, Journal of bacteriology.

[193]  P. Devreotes.  Dictyostelium discoideum: a model system for cell-cell interactions in development. , 1989, Science.

[194]  M. North,et al.  Multiple acid proteinases in the cellular slime mould Dictyostelium discoideum. , 1979, Biochimica et biophysica acta.

[195]  G. Weeks,et al.  The membrane-bound alkaline phosphatase and 5'-nucleotidase activities of vegetative cells of Dictyostelium discoideum. , 1985, Archives of biochemistry and biophysics.

[196]  J. Mora,et al.  Glutamine metabolism and cycling in Neurospora crassa , 1990, Microbiological reviews.

[197]  R. Firtel,et al.  Partial characterization of several protein and amino acid metabolizing enzymes in the cellular slime mold Dictyostelium discoideum. , 1972, Developmental biology.

[198]  T. Iijima,et al.  Transient increase of the intracellular Ca2+ concentration during chemotactic signal transduction in Dictyostelium discoideum cells. , 1988, Differentiation; research in biological diversity.

[199]  D. Cotter,et al.  Autoactivation of spore germination in mutant and wild type strains of Dictyostelium discoideum. , 1978, Microbios.

[200]  G. Rose,et al.  Hydrophobicity of amino acid residues in globular proteins. , 1985, Science.

[201]  I. Majerfeld,et al.  A cytosolic cyclic AMP-dependent protein kinase in Dictyostelium discoideum. II. Developmental regulation. , 1984, The Journal of biological chemistry.

[202]  J. Wheldrake,et al.  The effect of AMP on the NAD-dependent glutamate dehydrogenase during activation and morphogenesis in the cellular slime moulds. , 1992, Journal of general microbiology.

[203]  B. Henrissat,et al.  Domains in microbial beta-1, 4-glycanases: sequence conservation, function, and enzyme families. , 1991, Microbiological reviews.

[204]  R. J. Aerts.  Changes in cytoplasmic pH are involved in the cell type regulation of Dictyostelium. , 1988, Cell differentiation.

[205]  M. Watford.  Does glutamine regulate skeletal muscle protein turnover , 1989 .

[206]  D. Cotter,et al.  The physiological effects of restrictive environmental conditions on Dictyostelium discoideum spore germination. , 1979, Canadian journal of microbiology.

[207]  I. Takeuchi,et al.  Proportion regulation without pattern formation in Dictyostelium discoideum. , 1983, Journal of embryology and experimental morphology.

[208]  R. Dimond,et al.  Major changes in gene expression occur during at least four stages of development of Dictyostelium discoideum. , 1985, Developmental biology.

[209]  W. Loomis.  Essential Genes for Development of Dictyostelium , 1990 .

[210]  M. Murphy,et al.  Effects of amino acids on cell differentiation of D. discoideum. , 1979, Cell differentiation.

[211]  S. Robbins,et al.  A Dictyostelium morphogen that is essential for stalk cell formation is generated by a subpopulation of prestalk cells. , 1990, Development.

[212]  M. Oyama,et al.  Cyclic AMP and NH3/NH4+ both regulate cell-type-specific mRNA accumulation in the cellular slime mold, Dictyostelium discoideum. , 1986, Developmental biology.

[213]  D. Fontana,et al.  Cell-cell contact elicits cAMP secretion and alters cAMP signaling in Dictyostelium discoideum , 1989 .

[214]  D. Wilkinson,et al.  Spore coat protein synthesis during development of Dictyostelium discoideum requires a low-molecular-weight inducer and continued multicellularity. , 1985, Developmental biology.

[215]  H. Ennis.  Isolation And Properties Of Dictyostelium Discoideum Mutants Temperature-Sensitive For Spore Germination , 1983 .

[216]  Peter N. Devreotes,et al.  Structurally distinct and stage-specific adenylyl cyclase genes play different roles in dictyostelium development , 1992, Cell.

[217]  R. Kay,et al.  Cell patterning in Dictyostelium. , 1981, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[218]  J. Williams,et al.  Overproduction of the regulatory subunit of the cAMP‐dependent protein kinase blocks the differentiation of Dictyostelium discoideum. , 1989, The EMBO journal.

[219]  H. Lodish,et al.  Mechanism of sequential induction of cell-type specific mRNAs in Dictyostelium differentiation , 1984, Nature.

[220]  A. Cohen.  The Effect of Ammonia on Morphogenesis in the Acrasieae. , 1953, Proceedings of the National Academy of Sciences of the United States of America.

[221]  G. Weeks,et al.  The effects of presumptive morphogens on prestalk and prespore cell gene expression in monolayers of Dictyostelium discoideum , 1990 .

[222]  J. H. Gregg,et al.  Morphogenesis and ultrastructure in Dictyostelium. , 1970, Developmental biology.

[223]  D. Cotter,et al.  ENVIRONMENTAL PARAMETERS LIMITING SPORE GERMINATION IN A SPONTANEOUSLY GERMINATING MUTANT OF DICTYOSTELIUM DISCOIDEUM , 1989 .

[224]  R. Firtel,et al.  Regulation of actin gene expression during spore germination in Dictyostelium discoideum. , 1980, Developmental biology.

[225]  I. N. Feit.  Ammonia can stimulate or inhibit aggregate density in Dictyostelium mucoroides: a quantitative test of the hypothesis that ammonia is the aggregation-suppressing gas. , 1988, Developmental genetics.

[226]  P. Devreotes,et al.  Multiple genes for cell surface cAMP receptors in Dictyostelium discoideum. , 1991, Developmental genetics.

[227]  W. Loomis,et al.  Plasma membrane proteins of Dictyostelium: the spore coat proteins. , 1979, Developmental biology.

[228]  D. Cotter,et al.  Regulation of cysteine proteinases during different pathways of differentiation in cellular slime molds. , 1991, Developmental genetics.

[229]  T. Ohmori,et al.  Transition of starving Dictyostelium cells to differentiation phase at a particular position of the cell cycle. , 1989, Differentiation; research in biological diversity.

[230]  G. Weeks,et al.  The induction of stalk cell differentiation in submerged monolayers of Dictyostelium discoideum , 1984 .

[231]  A. Amagai,et al.  The Possible Involvement of Cyclic AMP and Volatile Substance (s) in the Development of a Macrocyst‐Forming Strain of Dictyostelium mucoroides , 1984, Development, growth & differentiation.

[232]  W. Loomis,et al.  Spore coat genes SP60 and SP70 of Dictyostelium discoideum , 1989, Molecular and cellular biology.

[233]  J. Gross,et al.  Potential morphogens involved in pattern formation during Dictyostelium differentiation. , 1991, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[234]  R. Kay.  Evidence that elevated intracellular cyclic AMP maturation in Dictyostelium , 1989 .

[235]  C. Ceccarini,et al.  Purification and new biological properties of the slime mold germination inhibitor , 1975 .

[236]  A. Cameron,et al.  Effects of suboptimal levels of extracellular calcium on the regulation of the cyclic AMP phosphodiesterase-inhibitor system and membrane differentiation in Dictyostelium discoideum. , 1988, Journal of cell science.

[237]  R. Dimond,et al.  Secretion of Lysosomal enzymes in the cellular slime mold, Dictyostelium discoideum. , 1981, The Journal of biological chemistry.

[238]  A. Tsang,et al.  Characterization of an unusual cAMP receptor and its related polypeptides in Dictyostelium discoideum. , 1988, Developmental genetics.

[239]  H. Padh,et al.  Endosomes are acidified by association with discrete proton-pumping vacuoles in Dictyostelium. , 1991, The Journal of biological chemistry.

[240]  U. Müller,et al.  Pattern Formation in Dictyostelium discoideum: Temporal and Spatial Distribution of Prespore Vacuoles , 1973 .

[241]  B. Wright.  ENDOGENOUS ACTIVITY AND SPORULATION IN SLIME MOLDS , 1963, Annals of the New York Academy of Sciences.

[242]  A. Tsang,et al.  The regulation of cyclic AMP-phosphodiesterase and its specific inhibitor by cyclic AMP in dictyostelium , 1977 .

[243]  Güunther Gerisch,et al.  Chapter 6 Cell Aggregation and Differentiation in Dictyostelium , 1968 .

[244]  R. Firtel,et al.  Organization of the actin multigene family of Dictyostelium discoideum and analysis of variability in the protein coding regions. , 1985, Journal of molecular biology.

[245]  R. Kay,et al.  Intracellular pH and the control of cell differentiation in Dictyostelium discoideum , 1983, Nature.

[246]  P. Sharp,et al.  Codon usage and gene expression level in Dictyostelium discoideum: highly expressed genes do 'prefer' optimal codons. , 1989, Nucleic acids research.

[247]  A. Tsang,et al.  Identification of multiple cyclic AMP-binding proteins in developing Dictyostelium discoideum cells. , 1986, Journal of Biological Chemistry.

[248]  D. Cotter,et al.  Differential secretion of Dictyostelium discoideum proteinases , 1990 .

[249]  R. Delude,et al.  Characterization of genes which are deactivated upon the onset of development in Dictyostelium discoideum. , 1987, Developmental biology.

[250]  J. Bonner,et al.  The prestalk-prespore pattern in cellular slime molds. , 1979, Differentiation; research in biological diversity.

[251]  D. Cotter,et al.  A natural-abundance 13C-NMR study of Dictyostelium discoideum metabolism. Monitoring of the spore germination process. , 1990, European journal of biochemistry.

[252]  D. Armant,et al.  Properties of a 5'-AMP specific nucleotidase which accumulates in one cell type during development of Dictyostelium discoideum. , 1982, Archives of biochemistry and biophysics.

[253]  D. Armant,et al.  Copurification of alkaline phosphatase and 5'-AMP specific nucleotidase in Dictyostelium discoideum. , 1981, The Journal of biological chemistry.

[254]  K. Okamoto,et al.  Role of cyclic AMP and ammonia in induction and maintenance of post-aggregative differentiation in a suspension culture of Dictyostelium discoideum. , 1988, Differentiation; research in biological diversity.

[255]  K. Williams,et al.  A polymorphic, prespore-specific cell surface glycoprotein is present in the extracellular matrix of Dictyostelium discoideum , 1985, Molecular and cellular biology.

[256]  R. Kessin,et al.  Cyclic nucleotide phosphodiesterase of Dictyostelium discoideum and its glycoprotein inhibitor: structure and expression of their genes. , 1991, Developmental genetics.

[257]  L. Wu,et al.  A developmentally regulated and cAMP-repressible gene of Dictyostelium discoideum: cloning and expression of the gene encoding cyclic nucleotide phosphodiesterase inhibitor. , 1990, Gene.

[258]  A. Kimmel.  Different molecular mechanisms for cAMP regulation of gene expression during Dictyostelium development. , 1987, Developmental biology.

[259]  H. Ennis.  Changes in free amino acid levels during cellular slime mold spore and microcyst germination. , 1981, Archives of biochemistry and biophysics.

[260]  R. Kay,et al.  The DIF-1 signaling system in Dictyostelium. Metabolism of the signal. , 1991, Journal of Biological Chemistry.

[261]  A. Malkinson,et al.  Adenosine 3':5'-cyclic monophosphate concentrations and phosphodiesterase activities during axenic growth and differentiation of cells of the cellular slime mould Dictyostelium discoideum. , 1973, The Biochemical journal.

[262]  A. Durston,et al.  The cell cycle and sorting behaviour in Dictyostelium discoideum. , 1984, Journal of cell science.

[263]  B. Haribabu,et al.  Homology cloning of protein kinase and phosphoprotein phosphatase sequences of Dictyostelium discoideum. , 1991, Developmental genetics.

[264]  A. Tsang,et al.  Sequence and expression of annexin VII of Dictyostelium discoideum. , 1991, Biochimica et biophysica acta.

[265]  G. Weeks,et al.  Stalk cell formation in monolayers from isolated prestalk and prespore cells of Dictyostelium discoideum: evidence for two populations of prestalk cells. , 1988, Development.

[266]  P. Schaap,et al.  Multiple effects of differentiation-inducing factor on prespore differentiation and cyclic-AMP signal transduction in Dictyostelium , 1986 .

[267]  C. Ceccarini,et al.  Carbohydrate content during development of the slime mold, Dictyostelium discoideum. , 1965, Journal of cellular physiology.

[268]  J. Williams,et al.  Characterization of two highly diverged but developmentally co-regulated cysteine proteinase genes in Dictyostelium discoideum. , 1985, Nucleic acids research.

[269]  D. Wilkinson,et al.  Characterisation of the spore coat proteins of Dictyostelium discoideum. , 2005, European journal of biochemistry.

[270]  R. Firtel,et al.  Developmental and spatial regulation of a Dictyostelium prespore gene: cis-acting elements and a cAMP-induced, developmentally regulated DNA binding activity. , 1991, Development.

[271]  D. Cotter,et al.  Factors Affecting the Rate of Heat-induced Spore Germination in Dictyostelium discoideum , 1968, Journal of bacteriology.

[272]  Y. Anraku,et al.  Mutants of Saccharomyces cerevisiae with defective vacuolar function , 1988, Journal of bacteriology.

[273]  A. Durston,et al.  Cytoplasmic pH at the onset of development in Dictyostelium. , 1987, Journal of cell science.

[274]  S. Hamamoto,et al.  Ultrastructure of spore differentiation in Dictyostelium: the prespore vacuole. , 1969, Journal of ultrastructure research.

[275]  H. M. Snyder,et al.  Interspecific Spore Inhibition in the Cellular Slime Moulds , 1966, Nature.

[276]  D. Cotter,et al.  Germination of Dictyostelium discoideum spores : inhibition of the autoactivation pathway by vanadate , 1990 .

[277]  W. Loomis,et al.  Coordinate regulation of the spore coat genes in Dictyostelium discoideum. , 1991, Developmental genetics.

[278]  D. Francis,et al.  Mating types in cellular slime molds. , 1973, Biochemical and biophysical research communications.

[279]  P. Devreotes,et al.  Structure and expression of the cAMP cell-surface receptor. , 1988, Developmental genetics.

[280]  C. McPherson,et al.  V4, a gene required for the transition from growth to development in Dictyostelium discoideum. , 1992, Developmental biology.

[281]  M. Darmon,et al.  Effects of amino acids and glucose on adenylate cyclase and cell differentiation of Dictyostelium discoideum. , 1978, Developmental biology.

[282]  K. G. Higinbotham,et al.  A Ca2+-dependent signal transduction system participates in coupling expression of some cAMP-dependent prespore genes to the cell surface receptor. , 1988, Developmental genetics.

[283]  M. Brenner,et al.  Caffeine blocks activation of cyclic AMP synthesis in Dictyostelium discoideum. , 1984, Developmental biology.