Abstract
The social amoeba or cellular slime mould Dictyostelium discoideum is a “professional” phagocyte that has long been recognized for its value as a biomedical model organism, particularly in studying the actomyosin cytoskeleton and chemotactic motility in non-muscle cells. The complete genome sequence of D. discoideum is known, it is genetically tractable, readily grown clonally as a eukaryotic microorganism and is highly accessible for biochemical, cell biological and physiological studies. These are the properties it shares with other microbial model organisms. However, Dictyostelium combines these with a unique life style, with motile unicellular and multicellular stages, and multiple cell types that offer for study an unparalleled variety of phenotypes and associated signalling pathways. These advantages have led to its recent emergence as a valuable model organism for studying the molecular pathogenesis and treatment of human disease, including a variety of infectious diseases caused by bacterial and fungal pathogens. Perhaps surprisingly, this organism, without neurons or brain, has begun to yield novel insights into the cytopathology of mitochondrial diseases as well as other genetic and idiopathic disorders affecting the central nervous system. Dictyostelium has also contributed significantly to our understanding of NDP kinase, as it was the Dictyostelium enzyme whose structure was first determined and related to enzymatic activity. The phenotypic richness and tractability of Dictyostelium should provide a fertile arena for future exploration of NDPK’s cellular roles.
Similar content being viewed by others
References
Baldauf SL, Roger AJ, Wenk-Siefert I et al (2000) A kingdom-level phylogeny of eukaryotes based on combined protein. Science 290:972–977. doi:10.1126/science.290.5493.972
Eichinger L, Pachebat JA, Glockner G et al (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57. doi:10.1038/nature03481
Chisholm RL, Gaudet P, Just EM et al (2006) dictyBase, the model organism database for Dictyostelium discoideum. Nucleic Acids Res 34:D423–D427. doi:10.1093/nar/gkj090
Goldberg JM, Manning G, Liu A et al (2006) The Dictyostelium kinome—analysis of the protein kinases from a simple model organism. PLoS Genet 2:e38. doi:10.1371/journal.pgen.0020038
Torija P, Robles A, Escalante R (2006) Optimization of a large-scale gene disruption protocol in Dictyostelium and analysis of conserved genes of unknown function. BMC Microbiol 6:75. doi:10.1186/1471-2180-6-75
Torija P, Vicente JJ, Rodrigues TB et al (2006) Functional genomics in Dictyostelium: MidA, a novel conserved protein is required for mitochondrial function and development. J Cell Sci 119:1154–1164. doi:10.1242/jcs.02819
Calvo-Garrido J, Carilla-Latorre S, Lázaro-Diéguez F et al (2008) Vacuole membrane protein 1 is an endoplasmic reticulum protein required for organelle biogenesis, protein secretion, and development. Mol Biol Cell 19:3442–3453. doi:10.1091/mbc.E08-01-0075
Nellen W, Silan C, Firtel RA (1984) DNA-mediated transformation in Dictyostelium discoideum: regulated expression of an actin gene fusion. Mol Cell Biol 4:2890–2898
Eichinger L, Rivero F (eds) (2006) Dictyostelium discoideum protocols. Methods in molecular biology, vol 346. Humana Press, Totowo
Maniak M (2002) Conserved features of endocytosis in Dictyostelium. Int Rev Cytol 221:257–287. doi:10.1016/S0074-7696(02)21014-1
Cardelli J (2001) Phagocytosis and macropinocytosis in Dictyostelium: phosphoinositide-based processes, biochemically distinct. Traffic 2:311–320. doi:10.1034/j.1600-0854.2001.002005311.x
Maniak M (2001) Fluid-phase uptake and transit in axenic Dictyostelium cells. Biochim Biophys Acta 1525:197–204
Steinert M, Heuner K (2005) Dictyostelium as host model for pathogenesis. Cell Microbiol 7:307–314. doi:10.1111/j.1462-5822.2005.00493.x
Willard SS, Devreotes PN (2006) Signaling pathways mediating chemotaxis in the social amoeba, Dictyostelium discoideum. Eur J Cell Biol 85:897–904. doi:10.1016/j.ejcb.2006.06.003
Sasaki AT, Firtel RA (2006) Regulation of chemotaxis by the orchestrated activation of Ras, PI3K, and TOR. Eur J Cell Biol 85:873–895. doi:10.1016/j.ejcb.2006.04.007
Veltman DM, Keizer-Gunnik I, van Haastert PJM (2008) Four key signaling pathways mediating chemotaxis in Dictyostelium discoideum. J Cell Biol 180:747–753. doi:10.1083/jcb.200709180
Janetopoulos C, Firtel RA (2008) Directional sensing during chemotaxis. FEBS Lett 582:2075–2085. doi:10.1016/j.febslet.2008.04.035
Fisher PR (1997) Genetics of phototaxis in a model eukaryote, Dictyostelium discoideum. Bioessays 19:397–408. doi:10.1002/bies.950190507
Fisher PR (2001) Genetic analysis of phototaxis in Dictyostelium. In: Hader DP, Lebert M (eds) Photomovement. ESP comprehensive series in photosciences, vol 1. Elsevier Science Ltd, Amsterdam, pp 519–559
Williams JG (2006) Transcriptional regulation of Dictyostelium pattern formation. EMBO Rep 7:694–698. doi:10.1038/sj.embor.7400714
Golstein P, Aubry L, Levraud JP (2003) Cell-death alternative model organisms: why and which? Nat Rev Mol Cell Biol 4:798–807. doi:10.1038/nrm1224
Laporte C, Kosta A, Klein G et al (2007) A necrotic cell death model in a protist. Cell Death Differ 14:266–274. doi:10.1038/sj.cdd.4401994
Noegel AA, Schleicher M (2000) The actin cytoskeleton of Dictyostelium: a story told by mutants. J Cell Sci 113:759–766
Parent CA (2004) Making all the right moves: chemotaxis in neutrophils and Dictyostelium. Curr Opin Cell Biol 16:4–13. doi:10.1016/j.ceb.2003.11.008
Fisher PR, Merkl G, Gerisch G (1989) Quantitative analysis of cell motility and chemotaxis in Dictyostelium discoideum using an image processing system and a novel chemotaxis chamber providing stationary chemical gradients. J Cell Biol 108:973–984. doi:10.1083/jcb.108.3.973
Fisher PR (1990) Pseudopodium activation and inhibition signals in chemotaxis by Dictyostelium discoideum amoebae. Semin Cell Biol 1:87–97
Chung C, Firtel RA (2002) Signaling pathways at the leading edge of chemotaxing cells. J Muscle Res Cell Motil 23:773–779. doi:10.1023/A:1024479728970
Klein PS, Sun TJ, Saxe CLIII et al (1988) A chemoattractant receptor controls development in Dictyostelium discoideum. Science 241:1467–1472. doi:10.1126/science.3047871
Jin T, Xu X, Fang J, et al (2009) How human leukocytes track down and destroy pathogens: lessons learned from the model organism Dictyostelium discoideum. Immunol Res 43:118–127. doi:10.1007/s12026-008-8056-7
Jin T, Xu X, Hereld D (2008) Chemotaxis, chemokine receptors and human disease. Cytokine 44:1–8. doi:10.1016/j.cyto.2008.06.017
Brzostowski JA, Kimmel AR (2001) Signaling at zero G: G-protein independent functions for 7-TM receptors. Trends Biochem Sci 26:291–297. doi:10.1016/S0968-0004(01)01804-7
Affolter M, Weijer CJ (2005) Signaling to cytoskeletal dynamics during chemotaxis. Dev Cell 9:19–34. doi:10.1016/j.devcel.2005.06.003
von Philipsborn AC, Bastmeyer M (2007) Mechanisms of gradient detection: a comparison of axon pathfinding with eukaryotic cell migration. Int Rev Cytol 263:1–62. doi:10.1016/S0074-7696(07)63001-0
Bolourani P, Spiegelman GB, Weeks G (2006) Delineation of the roles played by RasG and RasC in cAMP-dependent signal transduction during the early development of Dictyostelium discoideum. Mol Biol Cell 17:4543–4550. doi:10.1091/mbc.E05-11-1019
Kölsch V, Charest PG, Firtel RA (2008) The regulation of cell motility and chemotaxis by phospholipid signaling. J Cell Sci 121:551–559. doi:10.1242/jcs.023333
Funamoto S, Milan K, Meili R et al (2001) Role of phosphatidylinositol 3’ kinase and a downstream pleckstrin homology domain-containing protein in controlling chemotaxis in Dictyostelium. J Cell Biol 153:795–810. doi:10.1083/jcb.153.4.795
Vlahou G, Rivero F (2006) Rho GTPase signaling in Dictyostelium discoideum: insights from the genome. Eur J Cell Biol 85:947–959. doi:10.1016/j.ejcb.2006.04.011
Chung CY, Potikyan G, Firtel RA (2001) Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. Mol Cell 7:937–947. doi:10.1016/S1097-2765(01)00247-7
Insall R, Muller-Taubenberger A, Machesky L et al (2001) Dynamics of the Dictyostelium Arp2/3 complex in endocytosis, cytokinesis, and chemotaxis. Cell Motil Cytoskeleton 50:115–128. doi:10.1002/cm.10005
Caracino D, Jones C, Compton M (2007) The N-terminus of Dictyostelium scar interacts with Abi and HSPC300 and is essential for proper regulation and function. Mol Biol Cell 18:1609–1620. doi:10.1091/mbc.E06-06-0518
Kamimura Y, Xiong Y, Iglesias PA, Hoeller O, Bolourani P, Devreotes PN (2008) PIP3-independent activation of TorC2 and PKB at the cell’s leading edge mediates chemotaxis. Curr Biol 18:1034–1043. doi:10.1016/j.cub.2008.06.068
Iijima M, Devreotes P (2002) Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109:599–610. doi:10.1016/S0092-8674(02)00745-6
Funamoto S, Meili R, Lee S, Parry L, Firtel RA (2002) Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109:611–623. doi:10.1016/S0092-8674(02)00755-9
Comer FI, Parent CA (2002) PI 3-kinases and PTEN: how opposites chemoattract. Cell 109:541–544. doi:10.1016/S0092-8674(02)00765-1
Wessels D, Lusche DF, Kuhl S et al (2007) PTEN plays a role in the suppression of lateral pseudopod formation during Dictyostelium motility and chemotaxis. J Cell Sci 120:2517–2531. doi:10.1242/jcs.010876
Yumura S, Furuya K, Takeuchi I (1996) Intracellular free calcium responses during chemotaxis of Dictyostelium cells. J Cell Sci 109:2673–2678
Nebl T, Fisher PR (1997) Intracellular Ca2+ signals in Dictyostelium chemotaxis are mediated exclusively by Ca2+ influx. J Cell Sci 110:2845–2853
Pikzack C, Prassler J, Furukawa R et al (2005) Role of calcium-dependent actin-bundling proteins: characterization of Dictyostelium mutants lacking fimbrin and the 34-kilodalton protein. Cell Motil Cytoskeleton 62:210–231. doi:10.1002/cm.20098
Traynor D, Milne JLS, Insall RH et al (2000) Ca2+ signalling is not required for chemotaxis in Dictyostelium. EMBO J 19:4846–4854. doi:10.1093/emboj/19.17.4846
Bosgraaf L, van Haastert PJM (2002) A model for cGMP signal transduction in Dictyostelium in perspective of 25 years of cGMP research. J Muscle Res Cell Motil 23:781–791. doi:10.1023/A:1024431813040
De Lozanne A, Spudich JA (1987) Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236:1086–1091. doi:10.1126/science.3576222
Knecht DA, Loomis WF (1987) Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236:1081–1086. doi:10.1126/science.3576221
Jung G, Saxe CLIII, Kimmel AR et al (1989) Dictyostelium discoideum contains a gene encoding a myosin I heavy chain. Proc Natl Acad Sci USA 86:6186–6190. doi:10.1073/pnas.86.16.6186
Kollmar M (2006) Thirteen is enough: the myosins of Dictyostelium discoideum and their light chains. BMC Genomics 7:183. doi:10.1186/1471-2164-7-183
Falk DL, Wessels D, Jenkins L et al (2003) Shared, unique and redundant functions of three members of the class I myosins (MyoA, MyoB and MyoF) in motility and chemotaxis in Dictyostelium. J Cell Sci 116:3985–3999. doi:10.1242/jcs.00696
Chen L, Iijima M, Tang M et al (2007) PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev Cell 12:603–614. doi:10.1016/j.devcel.2007.03.005
Hoeller O, Kay RR (2007) Chemotaxis in the absence of PIP3 gradients. Curr Biol 17:813–817. doi:10.1016/j.cub.2007.04.004
Duhon D, Cardelli J (2002) The regulation of phagosome maturation in Dictyostelium. J Muscle Res Cell Motil 23:803–808. doi:10.1023/A:1024435913949
Bozzaro S, Bucci C, Steinert M (2008) Phagocytosis and host-pathogen interactions in Dictyostelium with a look at macrophages. Int Rev Cell Mol Biol 271:253–300. doi:10.1016/S1937-6448(08)01206-9
Solomon JM, Isberg RR (2000) Growth of Legionella pneumophila in Dictyostelium discoideum: a novel system for genetic analysis of host-pathogen interactions. Trends Microbiol 8:478–480. doi:10.1016/S0966-842X(00)01852-7
Haegele S, Kohler R, Merkert H et al (2000) Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2:165–171. doi:10.1046/j.1462-5822.2000.00044.x
Pukatzki S, Kessin RH, Mekalanos JJ (2002) The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci USA 99:3159–3164. doi:10.1073/pnas.052704399
Steenbergen JN, Nosanchuk JD, Malliaris SD et al (2003) Cryptococcus neoformans virulence is enhanced after growth in the genetically malleable host Dictyostelium discoideum. Infect Immun 71:4862–4872. doi:10.1128/IAI.71.9.4862-4872.2003
Skriwan C, Fajardo M, Hagele S et al (2002) Various bacterial pathogens and symbionts infect the amoeba Dictyostelium discoideum. Int J Med Microbiol 291:615–624. doi:10.1078/1438-4221-00177
Pukatzki S, Ma AT, Sturtevant D et al (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 103:1528–1533. doi:10.1073/pnas.0510322103
Benghezal M, Fauvarque MO, Tournebize R et al (2006) Specific host genes required for the killing of Klebsiella bacteria by phagocytes. Cell Microbiol 8:139–148. doi:10.1111/j.1462-5822.2005.00607.x
Colucci AMR, Peracino B, Bozzaro S et al (2008) Dictyostelium discoideum as a model host for meningococcal pathogenesis. Med Sci Monit 14:BR134–BR140
Cosson P, Zulianello L, Join-Lambert O et al (2002) Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J Bacteriol 184:3027–3033. doi:10.1128/JB.184.11.3027-3033.2002
Farbrother P, Wagner C, Na J et al (2005) Dictyostelium transcriptional host cell response upon infection with Legionella. Cell Microbiol 8:438–456. doi:10.1111/j.1462-5822.2005.00633.x
Williams RSB, Boeckeler K, Gräf R (2006) Towards a molecular understanding of human diseases using Dictyostelium discoideum. Trends Mol Med 12:415–424. doi:10.1016/j.molmed.2006.07.003
Williams RSB (2005) Pharmacogenetics in model systems: defining a common mechanism of action for mood stabilisers. Prog Neuropsychopharmacol Biol Psychiatry 29:1029–1037. doi:10.1016/j.pnpbp.2005.03.020
Barth C, Le P, Fisher PR (2007) Mitochondrial biology and disease in Dictyostelium. Int Rev Cytol 263:207–252. doi:10.1016/S0074-7696(07)63005-8
Schapira AHV (2006) Mitochondrial disease. Lancet 368:70–82. doi:10.1016/S0140-6736(06)68970-8
Zeviani M, Carelli V (2007) Mitochondrial disorders. Curr Opin Neurol 20:564–571
Wilczynska Z, Barth C, Fisher PR (1997) Mitochondrial mutations impair signal transduction in Dictyostelium discoideum slugs. Biochem Biophys Res Commun 234:39–43. doi:10.1006/bbrc.1997.6574
Kotsifas M, Barth C, Lay ST et al (2002) Chaperonin 60 and mitochondrial disease in Dictyostelium. J Muscle Res Cell Motil 23:839–852. doi:10.1023/A:1024444215766
Bokko PB, Francioni L, Ahmed AU et al (2007) Diverse mitochondrial cytopathologies are caused by AMPK signalling. Mol Biol Cell 18:1874–1886. doi:10.1091/mbc.E06-09-0881
Hong SP, Leiper FC, Woods A et al (2003) Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc Natl Acad Sci USA 100:8839–8843. doi:10.1073/pnas.1533136100
Woods A, Johnstone SR, Dickerson K et al (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13:2004–2008. doi:10.1016/j.cub.2003.10.031
Hong S-P, Momcilovic M, Carlson M (2005) Function of mammalian LKB1 and Ca2+/calmodulin-dependent protein kinase kinase α as Snf1-activating kinases in yeast. J Biol Chem 280:21804–21809. doi:10.1074/jbc.M501887200
Hurley RL, Anderson KA, Franzone JM et al (2005) The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 280:29060–29066. doi:10.1074/jbc.M503824200
Momcilovic M, Hong S-P, Carlson M (2006) Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem 281:25336–25343. doi:10.1074/jbc.M604399200
Zong H, Ren JM, Young LH et al (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA 99:15983–15987. doi:10.1073/pnas.252625599
Hardie DG (2004) The AMP-activated protein kinase pathway—new players upstream and downstream. J Cell Sci 117:5479–5487. doi:10.1242/jcs.01540
Kahn BB, Alquier T, Carling D et al (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1:15–25. doi:10.1016/j.cmet.2004.12.003
Hardie DG, Sakamoto K (2006) AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology (Bethesda) 21:48–60. doi:10.1152/physiol.00044.2005
James AM, Murphy MP (2002) How mitochondrial damage affects cell function. J Biomed Sci 9:475–487. doi:10.1007/BF02254975
Rossignol R, Faustin B, Rocher C et al (2003) Mitochondrial threshold effects. Biochem J 370:751–762. doi:10.1042/BJ20021594
Maassen JA, ‘t Hart LM, Van Essen E et al (2004) Mitochondrial diabetes. Molecular mechanisms and clinical presentation. Diabetes 53:S103–S109. doi:10.2337/diabetes.53.2007.S103
McKenzie M, Liolitsa D, Hanna MG (2004) Mitochondrial disease: mutations and mechanisms. Neurochem Res 29:589–600. doi:10.1023/B:NERE.0000014829.42364.dd
Mandal S, Guptan P, Owusu-Ansah E et al (2005) Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev Cell 9:843–854. doi:10.1016/j.devcel.2005.11.006
Hayashi T, Hirshman MF, Fujii N et al (2000) Metabolic stress and altered glucose transport. Activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49:1–5. doi:10.2337/diabetes.49.4.527
Garcia-Gil M, Pesi R, Perna S et al (2003) 5′-Aminoimidazole-4-carboxamide riboside induces apoptosis in human neuroblastoma cells. Neuroscience 117:811–820. doi:10.1016/S0306-4522(02)00836-9
Ramamurthy S, Ronnett GV (2006) Developing a head for energy sensing: AMP-activated protein kinase as a multifunctional metabolic sensor in the brain. J Physiol 574:85–93. doi:10.1113/jphysiol.2006.110122
Marie S, Heron B, Bitoun P et al (2004) AICA-ribosiduria: a novel, neurologically devastating inborn error of purine biosynthesis caused by mutation of ATIC. Am J Hum Genet 74:1276–1281. doi:10.1086/421475
Chou SY, Lee YC, Chen HM et al (2005) CGS21680 attenuates symptoms of Huntington’s disease in a transgenic mouse model. J Neurochem 93:310–320. doi:10.1111/j.1471-4159.2005.03029.x
Lopez-Lopez C, Dietrich MO, Metzger F et al (2007) Disturbed cross talk between insulin-like growth factor I and AMP-activated protein kinase as a possible cause of vascular dysfunction in the amyloid precursor protein/Presenilin 2 mouse model of Alzheimer’s disease. J Neurosci 27:824–831. doi:10.1523/JNEUROSCI.4345-06.2007
Gilson PR, Yu X-C, Hereld D et al (2003) Two Dictyostelium orthologs of the prokaryotic cell division protein FtsZ localize to mitochondria and are required for the maintenance of normal mitochondrial morphology. Eukaryot Cell 2:1315–1326. doi:10.1128/EC.2.6.1315-1326.2003
Rehberg M, Kleylein-Sohn J, Faix J et al (2005) Dictyostelium LIS1 is a centrosomal protein required for microtubule/cell cortex interactions, nucleus/centrosome linkage, and actin dynamics. Mol Biol Cell 16:2759–2771. doi:10.1091/mbc.E05-01-0069
Harwood AJ, Agam G (2003) Search for a common mechanism of mood stabilizers. Biochem Pharmacol 66:179–189. doi:10.1016/S0006-2952(03)00187-4
Norman AW, Wedding RT, Black MK (1965) Detection of phosphohistidine in nucleoside diphosphokinase isolated from Jerusalem artichoke mitochondria. Biochem Biophys Res Commun 20:703–709. doi:10.1016/0006-291X(65)90073-2
Engel M, Veron M, Theisinger B et al (1995) A novel serine/threonine-specific protein phosphotransferase activity of Nm23/nucleoside-diphosphate kinase. Eur J Biochem 234:200–207. doi:10.1111/j.1432-1033.1995.200_c.x
Troll H, Winckler T, Lascu I et al (1993) Separate nuclear genes encode cytosolic and mitochondrial nucleoside diphosphate kinase in Dictyostelium discoideum. J Biol Chem 268:25469–25475
Lacombe ML, Wallet V, Troll H et al (1990) Functional cloning of a nucleoside diphosphate kinase from Dictyostelium discoideum. J Biol Chem 265:10012–10018
Dumas C, Lascu I, Morera S et al (1992) X-ray structure of nucleoside diphosphate kinase. EMBO J 11:3203–3208
Wallet V, Mutzle R, Troll H et al (1990) Dictyostelium nucleoside diphosphate kinase highly homologous to Nm23 and Awd proteins involved in mammalian tumor metastasis and Drosophila development. J Natl Cancer Inst 82:1199–1202. doi:10.1093/jnci/82.14.1199
Parks REJ, Agarwal RP (1973) Nucleoside diphosphokinases. Enzymes 8:307–334
Morera S, LeBras G, Lascu I et al (1994) Refined X-ray structure of Dictyostelium discoideum nucleoside diphosphate kinase at 1.8 Å resolution. J Mol Biol 243:873–890. doi:10.1006/jmbi.1994.1689
Bergeron R, Ren JM, Cadman KS et al (2001) Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am J Physiol Endocrinol Metab 281:E1340–E1346
Hardie DG, Hawley SA (2001) AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 23:1112–1119. doi:10.1002/bies.10009
Kantrowitz ER, Lipscomb WN (1988) Escherichia coli aspartate trancarbamylase. The relation between structure and function. Science 241:669–674. doi:10.1126/science.3041592
Nagai K, Oubridge C, Jessen TH et al (1990) Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature 348:515–520. doi:10.1038/348515a0
Adman ET, Sieker LC, Jensen LH (1973) The structure of a bacterial ferredoxin. J Biol Chem 248:3987–3996
Coll M, Guasch A, Aviles FX et al (1991) Three-dimensional structure of porcine procarboxypeptidase B: a structural basis of its inactivity. EMBO J 10:1–9
Pastore A, Saudek V, Ramponi G et al (1992) Three dimensional structure of acylphosphatase: refinement and structure analysis. J Mol Biol 224:427–440. doi:10.1016/0022-2836(92)91005-A
Karlsson A, Mesnildrey S, Xu Y et al (1996) Nucleoside diphosphate kinase. J Biol Chem 271:19928–19934. doi:10.1074/jbc.271.49.31426
Lascu I, Deville-Bonne D, Glaser P et al (1993) Equilibrium dissociation and unfolding of nucleoside diphosphate kinase from Dictyostelium discoideum. J Biol Chem 268:20268–20275
Giartosio A, Erent M, Cervoni L et al (1996) Thermal stability of hexameric and tetrameric nucleoside diphosphate kinases. J Biol Chem 271:17845–17851. doi:10.1074/jbc.271.30.17845
Tepper AD, Dammann H, Bominaar AA et al (1994) Investigation of the active site and the conformational stability of nucleoside diphosphate kinase by site-directed mutagenesis. J Biol Chem 269:32175–32180
Morera S, Lascu I, Dumas C et al (1994) Adenosine 5′-diphosphoate binding and the active site of nucleoside diphosphate kinase. Biochem 33:459–467. doi:10.1021/bi00168a010
Lecroisey A, Lascu I, Bominaar A et al (1995) Phosphorylation mechanism of nucleoside diphosphate kinase: 31P-nuclear magnetic resonance studies. Biochemistry 34:12445–12450. doi:10.1021/bi00038a043
Cherflis J, Morera S, Lascu I et al (1994) X-ray structure of nucleoside diphosphate kinase complexed with thymidine diphosphate and Mg2+ at 2-Å resolution. Biochemistry 3:9062–9069. doi:10.1021/bi00197a006
Morera S, Chiadmi M, LeBras G et al (1995) Mechanism of phosphate transfer by nucleoside diphosphate kinase: X-ray structures of the phosphohistidine intermediate of the enzymes from Drosophila and Dictyostelium. Biochemistry 34:11062–11070. doi:10.1021/bi00035a011
Sellam O, Veron M, Hildebrandt M (1995) Overexpression of wild-type and mutant NDP kinase in Dictyostelium discoideum. Mol Microbiol 16:79–85. doi:10.1111/j.1365-2958.1995.tb02393.x
MacDonald NJ, De La Rosa A, Benedict MA et al (1993) A serine phosphorylation of Nm23, and not its nucleoside diphosphate kinase activity, correlates with suppression of tumour metastatic potential. J Biol Chem 268:25780–25789
Bominaar AA, Molijn AC, Pestel M et al (1993) Activation of G-proteins by receptor-stimulated nucleoside diphosphate kinase in Dictyostelium. EMBO J 12:2275–2279
Srinivasan S, Traini M, Herbert B et al (2001) Proteomic analysis of a developmentally regulated secretory vesicle. Proteomics 1:1119–1127. doi:10.1002/1615-9861(200109)1:9<1119::AID-PROT1119>3.0.CO;2-X
Hohl H, Hamamoto S (1969) Ultrastructure of spore differentiation in Dictyostelium: the prespore vacuole. J Ultrastruct Res 26:442–453. doi:10.1016/S0022-5320(69)90050-1
Novick P, Zerial M (1997) The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol 9:496–504. doi:10.1016/S0955-0674(97)80025-7
Laurent O, Bruckert F, Adessi C et al (1998) In vitro reconstituted Dictyostelium discoideum early endosome fusion is regulated by Rab7 but proceeds in the absence of ATP-Mg2+ from the bulk solution. J Biol Chem 273:793–799. doi:10.1074/jbc.273.2.793
Van Haastert PJM, Janssens PMW, Erneux C (1991) Sensory transduction in eukaryotes. Eur J Biochem 195:289–303. doi:10.1111/j.1432-1033.1991.tb15706.x
Rosengard AM, Krutzsch HC, Shearn A et al (1989) Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosphila development. Nature 342:177–180. doi:10.1038/342177a0
Aguado-Velasco C, Veron M, Rambow JA et al (1996) NDP kinase can modulate contraction of Dictyostelium cytoskeletons. Cell Motil Cytoskeleton 34:194–205. doi:10.1002/(SICI)1097-0169(1996)34:3<194::AID-CM3>3.0.CO;2-A
Cheney RE, Mosseker MS (1992) Unconventional myosins. Curr Opin Cell Biol 4:27–35. doi:10.1016/0955-0674(92)90055-H
Amerik AU, Swaminathan S, Krantz BA et al (1997) In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. EMBO J 16:4826–4838. doi:10.1093/emboj/16.16.4826
Lindsey DF, Amerik A, Deery WJ et al (1998) A deubiquitinating enzyme that disassembles free polyubiquitin chains is required for development but not growth in Dictyostelium. J Biol Chem 273:29178–29187. doi:10.1074/jbc.273.44.29178
Wilkins A, Chubb JR, Insall RH (2000) A novel Dictyostelium RasGEF is required for normal endocytosis, cell motility and multicellular development. Curr Biol 10:1427–1437. doi:10.1016/S0960-9822(00)00797-1
Maselli A, Furukawa R, Thomson SAM et al (2003) Formation of Hirano bodies induced by expression of an actin cross-linking protein with a gain-of-function mutation. Eukaryot Cell 2:778–787. doi:10.1128/EC.2.4.778-787.2003
Davis RC, Furukawa R, Fechheimer M (2008) A cell culture model for investigation of Hirano bodies. Acta Neuropathol 115:205–217. doi:10.1007/s00401-007-0275-9
Chaumont F, Loomis WF, Chrispeels M (1997) Expression of a plant plasma membrane aquaporin in Dictyostelium results in hypo-osmotic sensitivity and developmental abnormalities. Proc Natl Acad Sci USA 94:6202–6209. doi:10.1073/pnas.94.12.6202
MacWilliams H, Doquang K, Pedrola R et al (2006) A retinoblastoma ortholog controls stalk/spore preference in Dictyostelium. Development 133:1287–1297. doi:10.1242/dev.02287
Souza GM, Lu S, Kuspa A (1998) YakA, a protein kinase required for the transition from growth to development in Dictyostelium. Development 125:2291–2302
Michaelis C, Weeks G (1992) Isolation and characterization of a cdc2 cDNA from Dictyostelium discoideum. Biochim et Biophys Acta—Gene Struct Expr 1132:35–42
Naorem A, Sadhale PP (2008) Identification and characterisation of DdRPB4, a subunit of Dictyostelium discoideum RNA polymerase II. Biochem Biophys Res Commun 377:1141–1146. doi:10.1016/j.bbrc.2008.10.124
Chida J, Yamaguchi H, Amagai A et al (2004) The necessity of mitochondrial genome DNA for normal development of Dictyostelium cells. J Cell Sci 117:3141–3152. doi:10.1242/jcs.01140
Inazu Y, Chae SC, Maeda Y (1999) Transient expression of a mitochondrial gene cluster including rps4 is essential for the phase-shift of Dictyostelium cells from growth to differentiation. Dev Genet 25:339–352. doi:10.1002/(SICI)1520-6408(1999)25:4<339::AID-DVG8>3.0.CO;2-3
Zhu Q, Hulen D, Liu T et al (1997) The cluA− mutant of Dictyostelium identifies a novel class of proteins required for dispersion of mitochondria. Proc Natl Acad Sci USA 9:7308–7313. doi:10.1073/pnas.94.14.7308
van Es S, Wessels D, Soll DR et al (2001) Tortoise, a novel mitochondrial protein, is required for directional responses of Dictyostelium in chemotactic gradients. J Cell Biol 152:621–632. doi:10.1083/jcb.152.3.621
Morita T, Yamaguchi H, Amagai A et al (2005) Involvement of the TRAP-1 homologue, Dd-TRAP1, in spore differentiation during Dictyostelium development. Exp Cell Res 303:425–431. doi:10.1016/j.yexcr.2004.10.010
Peitsch, MC (1995) Protein modeling by E-mail Bio/Technology. 13:658–660
Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723. doi:10.1002/elps.1150181505
Schwede T, Kopp J, Guex NP et al (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385. doi:10.1093/nar/gkg520
Kopp J, Schwede T (2004) The SWISS-MODEL Repository of annotated and three-dimensional protein structure homology models. Nucleic Acids Res 32:D230–D234. doi:10.1093/nar/gkh008
Meyer P, Schneider B, Sarfati S, Deville-Bonne D, Guerreiro C, Boretto J, Janin J, Veron M, Canard B (2000) Structural basis for activation of alpha-boranophosphate nucleotide analogues targeting drug-resistant reverse transcriptase. EMBO J 19:3520–3529. doi:10.1093/emboj/19.14.3520
Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28:235–242. doi:10.1093/nar/28.1.235
Acknowledgements
We thank the Thyne Reid Memorial Trusts for supporting this work. We are grateful to colleagues who allowed us to cite the unpublished data within this manuscript or who drew our attention to the examples listed in Table 1 of proteins from Dictyostelium that function correctly when expressed heterologously in other organisms or vice versa.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Annesley, S.J., Fisher, P.R. Dictyostelium discoideum—a model for many reasons. Mol Cell Biochem 329, 73–91 (2009). https://doi.org/10.1007/s11010-009-0111-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11010-009-0111-8