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cAMP signaling in Dictyostelium

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Abstract

cAMP plays a pivotal role in control of cell movement, differentiation and response to stress in all phases of the Dictyostelium life cycle. The multitudinous functions of cAMP require precise spatial and temporal control of its production, degradation and detection. Many novel proteins have recently been identified that critically modulate the cAMP signal. We focus in this review on the properties and functions of the three adenylyl cyclases and the three cAMP-phosphodiesterases that are present in Dictyostelium, and the network of proteins that regulate the activity of these enzymes. We also briefly discuss the two modes of detection of cAMP.

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References

  • Abe K and Yanagisawa K (1983) A new class of rapid developing mutants in Dictyostelium discoideum: implications for cyclic AMP metabolism and cell differentiation. Dev Biol 95: 200–210.

    Google Scholar 

  • Anjard C, Zeng CJ, Loomis WF and Nellen W (1998) Signal transduction pathways leading to spore differentiation in Dictyostelium discoideum. Dev Biol 193: 146–155.

    Google Scholar 

  • Araki T, Gamper M, Early A, Fukuzawa M, Abe T, Kawata T, Kim E, Firtel RA and Williams JG (1998) Developmentally and spatially regulated activation of a Dictyostelium STAT protein by a serpentine receptor. EMBO J 17: 4018–4028.

    Google Scholar 

  • Bear JE, Rawls JF and Saxe CL (1998) Scar, a WASP-related protein, isolated as a suppressor of receptor defects in late Dictyostelium development. J Cell Biol 142: 1325–1335.

    Google Scholar 

  • Berks M and Kay RR (1988) Cyclic AMP is an inhibitor of stalk cell differentiation in Dictyostelium discoideum. Dev Biol 126: 108–114.

    Google Scholar 

  • Bosgraaf L, Russcher H, Snippe H, Bader S, Wind I and Van Haastert PJM (2002) Identification and characterization of two unusual cGMP-stimulated phosphodiesterases in Dictyostelium. Mol Biol Cell 13: 3878–3889.

    Google Scholar 

  • Brzostowski J, Johnson C and Kimmel A (2002) Galpha-mediated inhibition of developmental signal response. Curr Biol 12: 1199–1208.

    Google Scholar 

  • Chang WT, Thomason PA, Gross JD and Newell PC (1998) Evidence that the RdeA protein is a component of a multistep phosphorelay modulating rate of development in Dictyostelium. EMBO J 17: 2809–2816.

    Google Scholar 

  • Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR and Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289: 625–628.

    Google Scholar 

  • Chen MY, Long Y and Devreotes PN (1997) A novel cytosolic regulator, pianissimo, is required for chemoattractant receptor and G protein-mediated activation of the 12 transmembrane domain adenylyl cyclase in Dictyostelium. Genes Dev 11: 3218–3231.

    Google Scholar 

  • Clarke M and Gomer RH (1995) PSF and CMF, autocrine factors that regulate gene expression during growth and early development of Dictyostelium. Experientia 51: 1124–1134.

    Google Scholar 

  • Cotter DA, Dunbar AJ, Buconjic SD and Wheldrake JF (1999) Ammonium phosphate in sori of Dictyostelium discoideum promotes spore dormancy through stimulation of the osmosensor ACG. Microbiol 145: 1891–1901.

    Google Scholar 

  • Danchin A (1993) Phylogeny of adenylyl cyclases. Adv Second Messenger Phosphoprotein Res 27: 109–162.

    Google Scholar 

  • Darmon M, Barra J and Brachet P (1978) The role of phosphodiesterase in aggregation of Dictyostelium discodeum. J Cell Sci 31: 233–243.

    Google Scholar 

  • Devreotes PN and Steck TL (1979) Cyclic 3'5' AMP relay in Dictyostelium discoideum. II Requirements for the initiation and termination of the response. J Cell Biol 80: 300–309.

    Google Scholar 

  • Dodge KL, Khouangsathiene S, Kapiloff MS, Mouton R, Hill EV, Houslay MD, Langeberg LK and Scott JD (2001) mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. Embo J 20: 1921–1930.

    Google Scholar 

  • Dormann D, Weijer G, Parent C, Devreotes P and Weijer C (2002) Visualizing PI3 kinase-mediated cell-cell signaling during Dictyostelium development. Curr Biol 12: 1178.

    Google Scholar 

  • Endl I, Konzok A and Nellen W (1996) Antagonistic effects of signal transduction by intracellular and extracellular cAMP on gene regulation in Dictyostelium. Mol Biol Cell 7: 17–24.

    Google Scholar 

  • Faure M, Franke J, Hall AL, Podgorski GJ and Kessin RH (1990) The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum contains three promoters specific for growth, aggregation, and late development. Mol Cell Biol 10: 1921–1930.

    Google Scholar 

  • Faure M, Podgorski GJ, Franke J and Kessin RH (1988) Disruption of Dictyostelium discoideum morphogenesis by overproduction of cAMP phosphodiesterase. Proc Natl Acad Sci USA 85: 8076–8080.

    Google Scholar 

  • Feliciello A, Gottesman ME and Avvedimento EV (2001) The biological functions of A-kinase anchor proteins. J Mol Biol 308: 99–114.

    Google Scholar 

  • Ferguson SSG and Caron MG (1998) G protein-coupled receptor adaptation mechanisms. Semin Cell Dev Biol 9: 119–127.

    Google Scholar 

  • Franke J and Kessin RH (1981) The cyclic nucleotide phosphodiesterase inhibitory protein of Dictyostelium discoideum. Purification and characterization. J Biol Chem 256: 7628–7637.

    Google Scholar 

  • Fukuzawa M, Hopper N and Williams J (1997) CudA: a Dictyostelium gene with pleiotropic effects on cellular differentiation and slug behaviour. Development 124: 2719–2728.

    Google Scholar 

  • Gerisch G (1976) Extracellular cyclic-AMP phosphodiesterase regulation in agar plate cultures of Dictyostelium discoideum. Cell Differ 5: 21–25.

    Google Scholar 

  • Gerisch G, Fromm H, Huesgen A and Wick U (1975) Control of cell-contact sites by cyclic AMP pulses in differentiating Dictyostelium cells. Nature 255: 547–549.

    Google Scholar 

  • Goldberg JM, Bosgraaf L, Van Haastert PJM and Smith JL (2002) Identification of four candidate cGMP targets in Dictyostelium. Proc Natl Acad Sci USA 99: 6749–6754.

    Google Scholar 

  • Hall AL, Franke J, Faure M and Kessin RH (1993) The role of the cyclic nucleotide phosphodiesterase of Dictyostelium discoideum during growth, aggregation, and morphogenesis: overexpression and localization studies with the separate promoters of the pde. Dev Biol 157: 73–84.

    Google Scholar 

  • Hamm HE (1998) The many faces of G protein signaling. J Biol Chem 273: 669–672.

    Google Scholar 

  • Harwood AJ, Hopper NA, Simon M-N, Driscoll DM, Veron M and Williams JG (1992) Culmination in Dictyostelium is regulated by the cAMP-dependent protein kinase. Cell 69: 615–624.

    Google Scholar 

  • Hopper NA, Anjard C, Reymond CD and Williams JG (1993a) Induction of terminal differentiation of Dictyostelium by cAMP-dependent protein kinase and opposing effects of intracellular and extracellular cAMP on stalk cell differentiation. Development 119: 147–154.

    Google Scholar 

  • Hopper NA, Harwood AJ, Bouzid S, Véron M and Williams JG (1993b) 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: 2459–2466.

    Google Scholar 

  • Houslay MD and Milligan G (1997) Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem Sci 22: 217–224.

    Google Scholar 

  • Hurley JH (1998) The adenylyl and guanylyl cyclase superfamily. Curr Opin Struct Biol 8: 770–777.

    Google Scholar 

  • Insall RH, Borleis J and Devreotes PN (1996) The aimless RasGEF is required for processing of chemotactic signals through G-proteincoupled receptors in Dictyostelium. Curr Biol 6: 719–729.

    Google Scholar 

  • Insall R, Kuspa A, Lilly PJ, Shaulsky G, Levin LR, Loomis WF and Devreotes P (1994) CRAC, a cytosolic protein containing a pleckstrin homology domain, is required for receptor and Gprotein-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol 126: 1537–1545.

    Google Scholar 

  • Jin T, Soede RDM, Liu JC, Kimmel AR, Devreotes PN and Schaap P (1998) Temperature-sensitive G beta mutants discriminate between G protein-dependent and-independent signaling mediated by serpentine receptors. EMBO J 17: 5076–5084.

    Google Scholar 

  • Johnson RL, Saxe III CL, Gollop R, Kimmel AR and Devreotes PN (1993) Identification and targeted gene disruption of cAR3, a cAMP receptor subtype expressed during multicellular stages of Dictyostelium development. Genes Dev 7: 273–282.

    Google Scholar 

  • Johnson RL, Van Haastert PJM, Kimmel AR, Saxe III CL, Jastorff B and Devreotes PN (1992) The cyclic nucleotide specificity of three cAMP receptors in Dictyostelium. J Biol Chem 267: 4600–4607.

    Google Scholar 

  • Kasahara M and Ohmori M (1999) Activation of a cyanobacterial adenylate cyclase, CyaC, by autophosphorylation and a subsequent phosphotransfer reaction. J Biol Chem 274: 15,167–15,172.

    Google Scholar 

  • Kay RR (1982) cAMP and spore differentiation in Dictyostelium discoideum. Proc Natl Acad Sci USA 79: 3228–3231.

    Google Scholar 

  • Kesbeke F, Snaar-Jagalska BE and Van Haastert PJM (1988) Signal transduction in Dictyostelium fgd A mutants with a defective interaction between surface cAMP receptors and a GTP-binding regulatory protein. J Cell Biol 107: 521–528.

    Google Scholar 

  • Kessin RH, Orlow SJ, Shapiro RI and Franke J (1979) Binding of inhibitor alters kinetic and physical properties of extracellular cyclic AMP phosphodiesterase from Dictyostelium discoideum. Proc Natl Acad Sci USA 76: 5450–5454.

    Google Scholar 

  • Kim JY, Borleis JA and Devreotes PN (1998b) Switching of chemoattractant receptors programs development and morphogenesis in Dictyostelium: receptor subtypes activate common responses at different agonist concentrations. Dev l Biol 197: 117–128.

    Google Scholar 

  • Kim J-Y, Caterina MJ, Milne JLS, Lin KC, Borleis JA and Devreotes PN (1997a) Random mutagenesis of the cAMP chemoattractant receptor cAR1, of Dictyostelium. J Biol Chem 272: 2060–2068.

    Google Scholar 

  • Kim HJ, Chang WT, Meima M, Gross JD and Schaap P (1998a) A novel adenylyl cyclase detected in rapidly developing mutants of Dictyostelium. J Biol Chem 273: 30,859–30,862.

    Google Scholar 

  • Kim J-Y, Soede RDM, Schaap P, Valkema R, Borleis JA, Van-Haastert PJM, Devreotes PN and Hereld D (1997b) Phosphorylation of chemoattractant receptors is not essential for chemotaxis or termination of G-protein-mediated responses. J Biol Chem 272: 27,313–27,318.

    Google Scholar 

  • Klein PS, Sun TJ, Saxe III CL, Kimmel AR, Johnson RL and Devreotes PN (1988) A chemoattractant receptor controls development in Dictyostelium discoideum. Science 241: 1467–1472.

    Google Scholar 

  • Klein P, Theibert A, Fontana D and Devreotes PN (1985) Identification and cyclic AMP-induced modification of the cyclic AMP receptor in Dictyostelium discoideum. J Biol Chem 260: 1757–1764.

    Google Scholar 

  • Konijn TM, Van De Meene JG, Bonner JT and Barkley DS (1967) The acrasin activity of adenosine-3',5'-cyclic phosphate. Proc Natl Acad Sci USA 58: 1152–1154.

    Google Scholar 

  • Kumagai A, Pupillo M, Gundersen R, Miake-Lye R, Devreotes PN and Firtel RA (1989) Regulation and function of Galpha protein subunits in Dictyostelium. Cell 57: 265–275.

    Google Scholar 

  • Kuspa A and Loomis WF (1992) Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc Natl Acad Sci USA 89: 8803–8807.

    Google Scholar 

  • Kuwayama H, Snippe H, Derks M, Roelofs J and Van Haastert PJM (2001) Identification and characterization of DdPDE3, a cGMP-selective phosphodiesterase from Dictyostelium. Biochem J 353: 635–644.

    Google Scholar 

  • Laub MT and Loomis WF (1998) A molecular network that produces spontaneous oscillations in excitable cells of Dictyostelium. Mol Biol Cell 9: 3521–3532.

    Google Scholar 

  • Lee S, Parent CA, Insall R and Firtel RA (1999) A novel Ras-interacting protein required for chemotaxis and cyclic adenosine monophosphate signal relay in Dictyostelium. Mol Biol Cell 10: 2829–2845.

    Google Scholar 

  • Lilly PJ and Devreotes PN (1994) Identification of CRAC, a cytosolic regulator required for guanine nucleotide stimulation of adenylyl cyclase in Dictyostelium. J Biol Chem 269: 14,123–14,129.

    Google Scholar 

  • Lilly P, Wu L, Welker DL and Devreotes PN (1993) A G-protein beta-subunit is essential for Dictyostelium development. Genes Dev 7: 986–995.

    Google Scholar 

  • Lim CJ, Spiegelman GB and Weeks G (2001) RasC is required for optimal activation of adenylyl cyclase and Akt/PKB during aggregation. EMBO J 20: 4490–4499.

    Google Scholar 

  • Louis JM, Ginsburg GT and Kimmel AR (1994) The cAMP receptor CAR4 regulates axial patterning and cellular differentiation during late development of Dictyostelium. Genes Dev 8: 2086–2096.

    Google Scholar 

  • Maeda M, Aubry L, Insall R, Gaskins C, Devreotes PN and Firtel RA (1996) Seven helix chemoattractant receptors transiently stimulate mitogen-activated protein kinase in Dictyostelium. J Biol Chem 271: 3351–3354.

    Google Scholar 

  • Malchow D, Nagele B, Schwartz H and Gerisch G (1972) Membrane-bound cyclic AMP phosphodiesterase in chemotactically responding cells of Dictyostelium discoideum. Eur J Biochem 28: 136–142.

    Google Scholar 

  • Mann SKO, Brown JM, Briscoe C, Parent C, Pitt G, Devreotes PN and Firtel RA (1997) Role of cAMP-dependent protein kinase in controlling aggregation and postaggregative development in Dictyostelium. Dev Biol 183: 208–221.

    Google Scholar 

  • Mann SKO and Firtel RA (1993) cAMP-dependent protein kinase differentially regulates prestalk and prespore differentiation during Dictyostelium development. Development 119: 135–146.

    Google Scholar 

  • Mann SKO, Richardson DL, Lee S, Kimmel AR and Firtel RA (1994) Expression of cAMP-dependent protein kinase in prespore cells is sufficient to induce spore cell differentiation in Dictyostelium. Proc Natl Acad Sci USA 91: 10,561–10,565.

    Google Scholar 

  • Martiel J-L and Goldbeter A (1987) A model based on receptor desensitization for cyclic AMP signaling in Dictyostelium cells. Biophys J 52: 807–828.

    Google Scholar 

  • Mehats C, Andersen CB, Filopanti M, Jin SLC and Conti M (2002) Cyclic nucleotide phosphodiesterases and their role in endocrine cell signaling. Trends Endocrinol Metab 13: 29–35.

    Google Scholar 

  • Meima ME, Biondi RM and Schaap P (2002) Identification of a novel type of cGMP phosphodiesterase that is defective in the chemotactive stmF mutants. Mol Biol Cell 13: 3870–3877.

    Google Scholar 

  • Meima ME and Schaap P (1999) Fingerprinting of adenylyl cyclase activities during Dictyostelium development indicates a dominant role for adenylyl cyclase B in terminal diffferentiation. Dev Biol 212: 182–190.

    Google Scholar 

  • Meima ME, Weening KE and Schaap P (2003) Characterization of a cAMP-stimulated cAMP phosphodiesterase in Dictyostelium discoideum. J Biol Chem (in press).

  • Milne JL and Devreotes PN (1993) The surface cyclic AMP receptors, cAR1, cAR2, and cAR3, promote Ca2+ in.ux in Dictyostelium discoideum by a Gα2-independent mechanism. Mol Biol Cell 4: 283–292.

    Google Scholar 

  • Milne JLS, Wu L, Caterina MJ and Devreotes PN (1995) Seven helix cAMP receptors stimulate Ca2+ entry in the absence of functional G proteins in Dictyostelium. J Biol Chem 270: 5926–5931.

    Google Scholar 

  • Mohanty S, Lee S, Yadava N, Dealy MJ, Johnson RS and Firtel RA (2001) Regulated protein degradation controls PKA function and cell-type differentiation in Dictyostelium. Genes Dev 15: 1435–1448.

    Google Scholar 

  • Mutzel R, Lacombe M-L, Simon M-N, De Gunzburg J and Veron M (1987) Cloning and cDNA sequence of the regulatory subunit of cAMP-dependent protein kinase from Dictyostelium discoideum. Proc Natl Acad Sci USA 84: 6–10.

    Google Scholar 

  • Nikawa J, Sass P and Wigler M (1987) Cloning and characterization of the low-a.nity cyclic AMP phosphodiesterase gene of Saccharomyces cerevisiae. Mol Cell Biol 7: 3629–3636.

    Google Scholar 

  • Ohno S (1997) The reason for as well as the consequence of the Cambrian explosion in animal evolution. J Mol Evol 44: S23-S27.

    Google Scholar 

  • Otsuka H and Van Haastert PJM (1998) A novel myb homolog initiates Dictyostelium development by induction of adenylyl cyclase expression. Genes Dev 12: 1738–1748.

    Google Scholar 

  • Ott A, Oehme F, Keller H and Schuster SC (2000) Osmotic stress response in Dictyostelium is mediated by cAMP. EMBO J 19: 5782–5792.

    Google Scholar 

  • Parent CA and Devreotes PN (1996) Constitutively active adenylyl cyclase mutant requires neither G proteins nor cytosolic regulators. J Biol Chem 271: 18,333–18,336.

    Google Scholar 

  • Pitt GS, Brandt R, Lin KC, Devreotes PN and Schaap P (1993) Extracellular cAMP is sufficient to restore developmental gene expression and morphogenesis in Dictyostelium cells lacking the aggregation adenylyl cyclase (ACA). Genes Dev 7: 2172–2180.

    Google Scholar 

  • Pitt GS, Milona N, Borleis J, Lin KC, Reed RR and Devreotes PN (1992) Structurally distinct and stage-specific adenylyl cyclase genes play different roles in Dictyostelium development. Cell 69: 305–315.

    Google Scholar 

  • Raper KB (1940) Pseudoplasmodium formation and organization in Dictyostelium discoideum. J Elisha Mitchell Scient Soc 56: 241–282.

    Google Scholar 

  • Riedel V and Gerisch G (1971) Regulation of extracellular cyclic-AMP-phosphodiesterase activity during development of Dictyostelium discoideum. Biochem Biophys Res Commun 42: 119–124.

    Google Scholar 

  • Ross FM and Newell PC (1981) Streamers: chemotactic mutants of Dictyostelium discoideum with altered cyclic GMP metabolism. J Gen Microbiol 127: 339–350.

    Google Scholar 

  • Santos JL and Shiozaki K (2001) Fungal histidine kinases. Sci STKE 2001: RE1.

  • Saxe III CL, Ginsburg GT, Louis JM, Johnson R, Devreotes PN and Kimmel AR (1993) CAR2, a prestalk cAMP receptor required for normal tip formation and late development of Dictyostelium discoideum. Genes Dev 7: 262–272.

    Google Scholar 

  • Schaap P and Van Driel R (1985) Induction of post-aggregative differentiation in Dictyostelium discoideum by cAMP. Evidence for involvement of the cell surface cAMP receptor. Exp Cell Res 159: 388–398.

    Google Scholar 

  • Schindler J and Sussman M (1977) Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. J Mol Biol 116: 161–169.

    Google Scholar 

  • Schulkes C and Schaap P (1995) cAMP-dependent protein kinase activity is essential for preaggregative gene expression in Dictyostelium. FEBS Lett 368: 381–384.

    Google Scholar 

  • Schuster SC, Noegel AA, Oehme F, Gerisch G and Simon MI (1996) The hybrid histidine kinase DokA is part of the osmotic response system of Dictyostelium. EMBO J 15: 3880–3889.

    Google Scholar 

  • Schwindinger WF and Robishaw JD (2001) Heterotrimeric G-protein γ-dimers in growth and differentiation. Oncogene 20: 1653–1660.

    Google Scholar 

  • Segall JE, Kuspa A, Shaulsky G, Ecke M, Maeda M, Gaskins C, Firtel RA and Loomis WF (1995) A MAP kinase necessary for receptor-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol 128: 405–413.

    Google Scholar 

  • Shaulsky G, Escalante R and Loomis WF (1996) Developmental signal transduction pathways uncovered by genetic suppressors. Proc Natl Acad Sci USA 93: 15,260–15,265.

    Google Scholar 

  • Shaulsky G, Fuller D and Loomis WF (1998) A cAMP-phosphodiesterase controls PKA-dependent differentiation. Development 125: 691–699.

    Google Scholar 

  • Siegert F and Weijer CJ (1992) Three-dimensional scroll waves organize Dictyostelium slugs. Proc Natl Acad Sci USA 89: 6433–6437.

    Google Scholar 

  • Simon M-N, Pelegrini O, Veron M and Kay RR (1992) Mutation of protein kinase A causes heterochronic development of Dictyostelium. Nature 356: 171–172.

    Google Scholar 

  • Singleton CK, Zinda MJ, Mykytka B and Yang P (1998) The histidine kinase DhkC regulates the choice between migrating slugs and terminal differentiation in Dictyostelium discoideum. Dev Biol 203: 345–357.

    Google Scholar 

  • Soderbom F, Anjard C, Iranfar N, Fuller D and Loomis WF (1999) An adenylyl cyclase that functions during late development of Dictyostelium. Development 126: 5463–5471.

    Google Scholar 

  • Souza GM, daSilva AM and Kuspa A (1999) Starvation promotes Dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway. Development 126: 3263–3274.

    Google Scholar 

  • Sucgang R, Weijer CJ, Siegert F, Franke J and Kessin RH (1997) Null mutations of the Dictyostelium cyclic nucleotide phosphodiesterase gene block chemotactic cell movement in developing aggregates. Dev Biol 192: 181–192.

    Google Scholar 

  • Taminato A, Bagattini R, Gorjao R, Chen G, Kuspa A and Souza GM (2002) Role for YakA, cAMP, and protein kinase A in regulation of stress responses of Dictyostelium discoideum cells. Mol Biol Cell 13: 2266–2275.

    Google Scholar 

  • Tang Y and Othmer HG (1994) AG protein-based model of adaptation in Dictyostelium discoideum. Math Biosciences 120: 25–76.

    Google Scholar 

  • Theibert A and Devreotes P (1986) Surface receptor-mediated activation of adenylate cyclase in Dictyostelium. J Biol Chem 261: 15,121–15,125.

    Google Scholar 

  • Thomason PA, Traynor D, Cavet G, Chang W-T, Harwood AJ and Kay RR (1998) An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium. EMBO J 17: 2838–2845.

    Google Scholar 

  • Thomason PA, Traynor D, Stock JB and Kay RR (1999) The RdeA-RegA system, a eukaryotic phospho-relay controlling cAMP breakdown. J Biol Chem 274: 27,379–27,384.

    Google Scholar 

  • Tsujioka M, Yokoyama M, Nishio K, Kuwayama H, Morio T, Katoh M, Urushihara H, Saito T, Ochiai H, Tanaka Y, Takeuchi I and Maeda M (2001) Spatial expression patterns of genes involved in cyclic AMP responses in Dictyostelium discoideum development. Dev Growth Differ 43: 275–283.

    Google Scholar 

  • Van Driessche N, Shaw C, Katoh M, Morio T, Sucgang R, Ibarra M, Kuwayama H, Saito T, Urushihara H, Maeda M, Takeuchi I, Ochiai H, Eaton W, Tollett J, Halter J, Kuspa A, Tanaka Y and Shaulsky G (2002) A transcriptional profile of multicellular development in Dictyostelium discoideum. Development 129: 1543–1552.

    Google Scholar 

  • Van Es S, Virdy KJ, Pitt GS, Meima M, Sands TW, Devreotes PN, Cotter DA and Schaap P (1996) Adenylyl cyclase G, an osmosensor controlling germination of Dictyostelium spores. J Biol Chem 271: 23,623–23,625.

    Google Scholar 

  • Verkerke-van Wijk I, Fukuzawa M, Devreotes PN and Schaap P (2001) Adenylyl cyclase A expression is tip-specific in Dictyostelium slugs and directs StatA nuclear translocation and CudA gene expression. Dev Biol 234: 151–160.

    Google Scholar 

  • Verkerke VanWijk I, Kim JY, Brandt R, Devreotes PN and Schaap P (1998) Functional promiscuity of gene regulation by serpentine receptors in Dictyostelium discoideum. Mol Cell Biol 18: 5744–5749.

    Google Scholar 

  • Virdy KJ, Sands TW, Kopko SH, vanEs S, Meima M, Schaap P and Cotter DA (1999) High cAMP in spores of Dictyostelium discoideum: association with spore dormancy and inhibition of germination. Microbiology 145: 1883–1890.

    Google Scholar 

  • Wang M and Schaap P (1989) Ammonia depletion and DIF trigger stalk cell differentiation in intact Dictyostelium discoideum slugs. Development 105: 569–574.

    Google Scholar 

  • Wang N, Soderbom F, Anjard C, Shaulsky G and Loomis WF (1999) SDF-2 induction of terminal differentiation in Dictyostelium discoideum is mediated by the membrane-spanning sensor kinase DhkA. Mol Cell Biol 19: 4750–4756.

    Google Scholar 

  • Wessels DJ, Zhang H, Reynolds J, Daniels K, Heid P, Lu S, Kuspa A, Shaulsky G, Loomis WF and Soll DR (2000) The internal phosphodiesterase RegA is essential for the suppression of lateral pseudopods during Dictyostelium chemotaxis. Mol Biol Cell 11: 2803–2820.

    Google Scholar 

  • Woffendin C, Chambers TC, Schaller KL, Leichtling BH and Rickenberg HV (1986) Translocation of cAMP-dependent protein kinase to the nucleus during development of Dictyostelium discoideum. Dev Biol 115: 1–8.

    Google Scholar 

  • Wu L and Franke J (1990) A developmentally regulated and cAMP-repressible gene of Dictyostelium discoideum: cloning and expression of the gene encoding cyclic nucleotide phosphodiesterase inhibitor. Gene 91: 51–56.

    Google Scholar 

  • Wu L, Valkema R, Van Haastert PJM and Devreotes PN (1995) The G protein β-subunit is essential for multiple responses to chemoattractants in Dictyostelium. J Cell Biol 129: 1667–1675.

    Google Scholar 

  • Yeh KC, Wu SH, Murphy JT and Lagarias JC (1997) A cyanobacterial phytochrome two-component light sensory system. Science 277: 1505–1508.

    Google Scholar 

  • Zinda MJ and Singleton CK (1998) The hybrid histidine kinase DhkB regulates spore germination in Dictyostelium discoideum. Dev Biol 196: 171–183.

    Google Scholar 

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  1. School of Life Sciences, University of Dundee, MSI/WTB complex, Dundee, DD1 5EH, UK

    Shweta Saran, Marcel E. Meima, Elisa Alvarez-Curto, Karin E. Weening, Daniel E. Rozen & Pauline Schaap

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  1. Shweta Saran
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  2. Marcel E. Meima
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Saran, S., Meima, M.E., Alvarez-Curto, E. et al. cAMP signaling in Dictyostelium . J Muscle Res Cell Motil 23, 793–802 (2002). https://doi.org/10.1023/A:1024483829878

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  • DOI: https://doi.org/10.1023/A:1024483829878

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