Abstract
The nucleolus is a multifunctional organelle involved in ribosomal subunit biogenesis as well as a multitude of other cellular functions. Although the mammalian nucleolus has been studied extensively and a multitude of nucleolar proteins have been identified relatively little is known about the nucleolus in lower eukaryotes and relatively few nucleolar proteins have been examined. The lower eukaryote Dictyostelium is a model system used to study several cellular processes such as growth, chemotaxis, differentiation, and development. In recent years Dictyostelium has also been used to study several human diseases such as Alzheimer’s disease and Huntington’s disease. However despite its extensive study relatively little is known about its nucleolus. It is important to examine the nucleolus of Dictyostelium and other lower eukaryotes in order to gain a better understanding of the structure and function of this fascinating multifunctional organelle. This chapter will focus on the nucleolus and nucleolar proteins in Dictyostelium and will then examine the nucleoli of other lower eukaryotes.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Altschuler M, Mascarenhas JP (1985) Transcription and translation of heat-shock and normal proteins in seedlings and developing seeds of soybean exposed to a gradual temperature increase. Plant Mol Biol 5:291–297
Annesley SJ, Fisher PR (2009) Dictyostelium discoideum – a model for many reasons. Mol Cell Biochem 329:73–91
Balbo A, Bozzaro S (2006) Cloning of Dictyostelium eIF6 (p27BBP) and mapping its nucle(ol)ar localization subdomains. Eur J Cell Biol 85:1069–1078
Barry EG, Perkins DD (1969) Position of linkage group V markers in chromosome 2 of Neurospora crassa. J Hered 60:120–125
Bartek J, Falck J, Lukas J (2001) CHK2 kinase – a busy messenger. Nat Rev Mol Cell Biol 2:877–886
Beffa T, Staib F, Lott Fischer J et al (1998) Mycological control and surveillance of biological waste and compost. Med Mycol 36(Suppl 1):137–145
Benichou J-C, Quiviger B, Ryter A (1983) Cytochemical study of the nucleolus of the slime mold Dictyostelium discoideum. J Ultrastruct Res 84:60–66
Bhabhra R, Askew DS (2005) Thermotolerance and virulence of Aspergillus fumigatus: role of the fungal nucleolus. Med Mycol 43(Supp 1):S87–S93
Bhabhra R, Miley MD, Mylonakis E et al (2004) Distribution of the Aspergillus fumigatus gene encoding nucleolar protein CgrA impairs thermotolerant growth and reduces virulence. Infect Immun 72:4731–4740
Boettner D, Huebner N, Rhodes JC, Askew DS (2001) Molecular cloning of Aspergillus fumigatus CgrA, the ortholog of a conserved fungal nucleolar protein. Med Mycol 39:517–521
Brewer BJ, Fangman WL (1980) Preferential inclusion of extrachromosomal genetic elements in yeast meiotic spores. Proc Natl Acad Sci U S A 77:5380
Burdine V, Clarke M (1995) Genetic and physiological modulation of the prestarvation response in Dictyostelium discoideum. Mol Biol Cell 6:311–325
Butler DK, Metzenberg RL (1990) Expansion and contraction of the nucleolus organizer region of Neurospora: changes originate in both proximal and distal segments. Genetics 126:325–333
Catalano A, O’Day DH (2011) Nucleolar localization and identification of nuclear/nucleolar localization signals of the calmodulin-binding protein nucleomorphin during growth and mitosis in Dictyostelium. Histochem Cell Biol 135:239–249
Catalano A, O’Day DH (2012a) Nucleoplasmic/nucleolar translocation and identification of a nuclear localization signal (NLS) in Dictyostelium BAF60a/SMARCD1 homologue Snf12. Histochem Cell Biol 138:515–530
Catalano A, O’Day DH (2012b) Rad53 homologue forkhead-associated kinase A (FhkA) and calcium-binding protein 4a (CBP4a) are nucleolar proteins that differentially redistribute during mitosis in Dictyostelium. Submitted to Cell Division
Catalano A, Poloz Y, O’Day DH (2011) Dictyostelium puromycin-sensitive aminopeptidase A is a nucleoplasmic nucleomorphin-binding protein that relocates to the cytoplasm during mitosis. Histochem Cell Biol 136:677–688
Cechetto JD, Gupta RS (2000) Immunoelectron microscopy provides evidence that tumor necrosis factor receptor-associated protein 1 (TRAP-1) is a mitochondrial protein which also localizes at specific extramitochondrial sites. Exp Cell Res 260:30–39
Cockburn AF, Newkirk MJ, Firtel RA (1976) Organization of ribosomal-RNA genes of Dictyostelium discoideum – mapping of non-transcribed spacer regions. Cell 9:605–613
Cockburn AF, Taylor WC, Firtel RA (1978) Dictyostelium rDNA consists of non-chromosomal palindromic dimers containing 5S and 36S coding regions. Chromosoma 70:19–29
Cocucci SM, Sussman M (1970) RNA in cytoplasmic and nuclear fraction so cellular slime mold amebas. J Cell Biol 45:399–407
De Backer MD, Ilyina T, Ma XJ et al (2001) Genomic profiling of the response of Candida albicans to itraconazole treatment using a DNA microarray. Antimicrob Agents Chemother 45:1660–1670
DeMaria AC, Gomes SL, Juliania MH, Mazzarella R, Klein C (1995) Cloning of a cDNA-encoding a novel heat-shock protein from Dictyostelium discoideum. Gene 163:163–164
DeMaria AC, Moerman A, Klein C, Gomes SL (1997) Cloning, structural analysis and expression of the gene encoding Hsp32 from Dictyostelium discoideum. Gene 193:173–180
Denning DW (1998) Invasive aspergillosis. Clin Infect Dis 26:781–803
Felts SJ, Owen BAL, Nguyen P, Trepel J, Donner DB, Toft DO (2000) The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J Biol Chem 275:3305–3312
Frank DJ, Roth MB (1998) ncl-1 is required for the regulation of cell size and ribosomal RNA synthesis in Caenorhabditis elegans. J Cell Biol 140:1321–1329
Fuchs J, Loidl J (2004) Behaviour of nucleolus organizing regions (NORs) and nucleoli during mitotic and meiotic divisions in budding yeast. Chromosome Res 12:427–438
Garrison RG, Mariat F, Boyd KS, Fromentin H (1979) Perithecial ultrastructure and formation of ascospores of Ceratocystis stenoceras (Robak) C Moreau. Ann Microbiol A130:3–21
Groft CM, Beckmann R, Sali A, Burley SK (2000) Crystal structure of ribosome anti-association factor IF6. Nat Struct Biol 7:1156–1164
Gross C, Watson K (1998) Transcriptional and translational regulation of major heat shock proteins and patterns of trehalose mobilization during hyperthermic recovery in repressed and derepressed Saccharomyces cerevisiae. Can J Microbiol 44:341–350
Grossman SR (2009) Occam’s dull razor. MDM2 and P/CAF keep Chk2 in check the hard way. Cell Cycle 8:515–517
Hohl HR, Hamamoto ST (1969) Ultrastructure of Acrasis rosea, a cellular slime mold, during development. J Protozool 16:333–344
Hohl HR, Ly M, Cotter DA (1970) Ultrastructural changes during formation and germination of microcysts in Polysphondylium pallidum, a cellular slime mould. J Cell Sci 7:285–305
Horwitz J, Bova MP, Ding LL, Haley DA, Stewart PL (1999) Lens alpha-crystallin: function and structure. Eye 13:403–408
Hsiao PW, Fryer CJ, Trotter KW, Wang W, Archer TK (2003) BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol 23:6210–6220
Huber RJ, O’Day DH (2011) Nucleocytoplasmic transfer of cyclin dependent kinase 5 and its binding to puromycin-sensitive aminopeptidase in Dictyostelium discoideum. Histochem Cell Biol 136:177–189
Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O’Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425:686–691
Hung CY, Wells K (1977) Behavior of nucleolus during nuclear divisions in Asci of Pyronema domesticum. Mycologia 69:685–692
Ideue T, Azad AK, Yoshida J-I, Matsusaka T, Yanagida M, Ohshima Y, Tani T (2004) The nucleolus is involved in mRNA export from the nucleus in fission yeast. J Cell Sci 117:2887–2895
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
Ishida S, Maeda Y, Takeuchi I (1974) Anucleolate mutant of cellular slime-mold Dictyostelium discoideum. J Gen Microbiol 81:491–499
Kanda F, Ochiai H, Iwabuchi M (1974) Molecular weight determinations and stoichiometric measurements of 40S and 60S ribosomal proteins of cellular slime-mold Dictyostelium discoideum. Eur J Biochem 44:469–479
Korgaonkar C, Hagen J, Tompkins V, Frazier AA, Allamargot C, Quelle FW, Quelle DE (2005) Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function. Mol Cell Biol 25:1258–1271
Kubai DF, Ris H (1969) Division in the Dinoflagellate Gyrodinium cohnii (Schiller) – a new type of nuclear reproduction. J Cell Biol 40:508–528
Kurki S, Peltonen K, Latonen L, Kiviharju TM, Ojala PM, Meek D, Laiho M (2004) Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell 5:465–475
Labhart P, Koller T (1982) Structure of the active nucleolar chromatin of Xenopus laevis oocytes. Cell 28:279–292
Labhart P, Ness P, Banz E, Parish R, Koller T (1983) Model for the structure of the active nucleolar chromatin. Cold Spring Harb Symp Quant Biol 47(Pt 1):557–564
Latge JP (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12:310–350
Latonen L (2011) Nucleolar aggresomes as counterparts of cytoplasmic aggresomes in proteotoxic stress. Bioessays 33:386–395
Latonen L, Moore HM, Bai B, Jaamaa S, Laiho M (2011) Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene 30:790–805
Lee L-W, Lee C-C, Huang C-R, Szecheng JL (2012) The nucleolus of Caenorhabditis elegans. J Biomed Biotech. doi:10.1155/2012/601274
Li S, Liu C, Li N, Hao T, Han T, Hill DE, Vidal M, Lin JD (2008) Genome-wide coactivation analysis of PGC-1α identifies BAF60a as a regulator of hepatic lipid metabolism. Cell Metab 8:105–117
Lin SJ, Schranz J, Teutsch SM (2001) Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 32:358–366
Lindquist S, Craig EA (1988) The heat-shock proteins. Ann Rev Gen 22:631–677
Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501
Loidl J (2003) Chromosomes of the budding yeast, Saccharomyces cerevisiae. Int Rev Cyt 222:141–196
Maclean N, Garside K, Bradley MC, Wood C (1984) The nucleus of axenically grown Dictyostelium discoideum studies on its division cycle isolation and conformation. Experientia (Basel) 40:1207–1214
Maeda Y, Takeuchi I (1969) Cell differentiation and fine structures in development of cellular slime molds. Dev Growth Differ 11:232–245
Maizels N (1976) Dictyostelium 17S, 25S, and 5S rDNAs lie within a 38,000 base pair repeated unit. Cell 9:341–438
Matsuyama SI, Maeda Y (1998) A mitochondrion as the structural basis of the formation of a cell-type specific organelle in Dictyostelium development. Protoplasma 201:172–179
Moerman AM, Klein C (1997) Developmental regulation of hsp32, a small heat shock protein in Dictyostelium discoideum. Exp Cell Res 237:149–157
Moerman AM, Klein C (1998) Dictyostelium discoideum Hsp32 is a resident nucleolar heat-shock protein. Chromosoma 107:145–154
Molenaar I, Sillevis-Smith WW, Rozijn TH, Tonino GM (1970) Biochemical and electron-microscopic study of isolated yeast nuclei. Exp Cell Res 60:148–156
Morimoto RI, Kline MP, Bimston DN, Cotto JJ (1997) The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 32:17–29
Morita T, Saitoh K, Maeda Y (2001) Dd-TRAP1 (Dictyostelium discoideum TNF receptor-ascociated protein 1) in the regulation of growth, cell adhesion and differentiation during Dictyostelium development. Dev Growth Differ 43:S112
Morita T, Amagai A, Maeda Y (2002) Unique behavior of Dictyostelium homologue of TRAP-1, coupling with differentiation of D. discoideum cells. Exp Cell Res 280:45–54
Morita T, Amagai A, Maeda Y (2004) Translocation of the Dictyostelium TRAP1 homologue to mitochondria induces a novel prestarvation response. J Cell Sci 117:5759–5770
Morita T, Yamaguchi H, Amagai A, Maeda Y (2005) Involvement of the TRAP-1 homologue, Dd-TRAP1, in spore differentiation during Dictyostelium development. Exp Cell Res 303:425–431
Moy TI, Boettner D, Rhodes JC, Silver PA, Askew DS (2002) Identification of a role for Saccharomyces cerevisiae Cgr1p in pre-rRNA processing and 60S ribosome subunit synthesis. Microbiology 148:1081–1090
Myre (2005) Characterization of nucleomorphin, a novel nuclear breast cancer carboxy-terminal-domain containing calmodulin-binding protein from Dictyostelium discoideum. Ph.D. dissertation, Department of Zoology, University of Toronto, Canada
Myre MA, O’Day DH (2002) Nucleomorphin: a novel, acidic, nuclear calmodulin-binding protein from Dictyostelium that regulates nuclear number. J Biol Chem 277:19735–19744
Myre MA, O’Day DH (2004a) Dictyostelium calcium-binding protein 4a interacts with nucleomorphin, a BRCT-domain protein that regulates nuclear number. Biochem Biophys Res Commun 322:665–671
Myre MA, O’Day DH (2004b) Dictyostelium nucleomorphin is a member of the BRCT-domain family of cell cycle checkpoint proteins. Biochim Biophys Acta 1675:192–197
Myre MA, O’Day DH (2005) An N-terminal nuclear localization sequence but not the calmodulin-binding domain mediates nuclear localization of nucleomorphin, a protein that regulates nuclear number in Dictyostelium. Biochem Biophys Res Commun 332:157–166
Myre MA, Lumsden AL, Thompson MN, Wasco W, MacDonald ME, Gusella JF (2011) Deficiency of Huntingtin has pleiotropic effects in the social amoeba Dictyostelium discoideum. PLoS Genet 7. doi:10.1371/journal.pgen.1002052
Ness PJ, Labhart P, Banz E, Koller T, Parish RW (1983) Chromatin structure along the ribosomal DNA of Dictyostelium – regional differences and changes accompanying cell differentiation. J Mol Biol 166:361–381
Petes TD (1979) Yeast ribosomal DNA genes are located on chromosome-XII. Proc Natl Acad Sci U S A 76:410–414
Poloz Y, Catalano A, O’Day DH (2012) Bestatin inhibits cell growth, cell division, and spore cell differentiation in Dictyostelium discoideum. Eukaryot Cell 11:545–557
Rae PMM (1970) The nature and processing of ribosomal ribonucleic acid in a Dinoflagellate. J Cell Biol 46:106–113
Reisman D, Glaros S, Thompson EA (2009) The SWI/SNF complex and cancer. Oncogene 28:1653–1668
Roos UP, Bottini F, Jenni V (1992) Morphology of the nucleolus in undifferentiated amebas of Dictyostelium discoideum. Eur J Protistol 28:94–101
Sameshima M, Fujimoto H, Imai Y, Tsukita S, Hashimoto Y (1991) Relation of nucleolar structure and position to the cytoplasmic microtubule system in Dictyostelium. Cell Motil Cytoskel 18:293–303
Sanvito F, Piatti S, Villa A, Bossi M, Lucchini G, Marchisio PC, Biffo S (1999) The beta 4 integrin interactor p27(BBP/eIF6) is an essential nuclear matrix protein involved in 60S ribosomal subunit assembly. J Cell Biol 144:828–837
Saxe CL (1999) Learning from the slime mold: Dictyostelium and human disease. Am J Human Gen 65:25–30
Schultz TW, Kennedy JR (1976) The fine structure of the digestive system of Daphnia pulex (Crustacea: Cladocera). Tissue Cell 8:479–490
Senger B, Lafontaine DLJ, Graindorge JS, Gadal O, Camasses A, Sanni A, Garnier JM, Breitenbach M, Hurt E, Fasiolo F (2001) The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol Cell 8:1363–1373
Shaw PJ, Highett MI, Beven AF, Jordan EG (1995) The nucleolar architecture of polymerase-I transcription and processing. EMBO J 14:2896–2906
Si K, Maitra U (1999) The Saccharomyces cerevisiae homologue of mammalian translation initiation factor 6 does not function as a translation initiation factor. Mol Cell Biol 19:1416–1426
Simon I, Olins DE (1994) Higher-order association of extrachromosomal ribosomal-RNA genes in Dictyostelium discoideum. Cell Biol Int 18:1091–1094
Song HY, Dunbar JD, Zhang YX, Guo DQ, Donner DB (1995) Identification of a protein with homology to Hsp90 that binds the type-1 tumor necrosis factor-receptor. J Biol Chem 270:3574–3581
Srinivasan S, Traini M, Herbert B, Sexton D, Harry J, Alexander H, Williams KL, Alexander S (2001) Proteomic analysis of a developmentally regulated secretory vesicle. Proteomics 1:1119–1127
Steen BR, Lian T, Zuyderduyn S et al (2002) Temperature-regulated transcription in the pathogenic fungus Cryptococcus neoformans. Genome Res 12:1386–4000
St-Germain G, Summerbell R (1996) Identifying filamentous fungi: a clinical laboratory handbook. Star Publishing Co, Belmont
Stracker TH, Usui T, Petrini JHJ (2009) Taking the time to make important decisions: the checkpoint effector kinases Chk1 and Chk2 and the DNA damage response. DNA Repair 8:1047–1054
Sudarsanam P, Winston F (2000) Recent advances in understanding transcriptional control by the Snf/Swi family of nucleosomes remodeling complexes. Trends Genet 16:345–351
Sun J, McFarland M, Boettner D et al (2001) Cgr1p, a novel nucleolar protein encoded by Saccharomyces cerevisiae orf YGL0292w. Curr Microbiol 42:65–69
That TCT, Turian G (1978) Ultrastructural study of microcyclic macroconidiation in Neurospora crassa. Arch Microbiol 116:279–288
van Es S, Wessels D, Soll DR, Borleis J, Devreotes PN (2001) Tortoise, a novel mitochondrial protein, is required for directional responses of Dictyostelium in chemotactic gradients. J Cell Biol 152:621–632
Williams JG (2010) Dictyostelium finds new roles to model. Genetics 185:717–726
Wood LC, Ashby MN, Grunfeld C, Feingold KR (1999) Cloning of murine translation initiation factor 6 and functional analysis of the homologues sequences YPR016c in Saccharomyces cerevisiae. J Biol Chem 274:11653–11659
Yamaguchi H, Morita T, Amagai A, Maeda Y (2005) Changes in spatial and temporal localization of Dictyostelium homologues of TRAP1 and GRP94 revealed by immunoelectron microscopy. Exp Cell Res 303:415–424
Yang CH, Lambie EJ, Hardin J, Craft J, Snyder M (1989) Higher order structure is present in the yeast nucleus: autoantibody probes demonstrate that the nucleolus lies opposite the spindle pole body. Chromosoma 98:123–128
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Catalano, A., O’Day, D.H. (2013). The Nucleolus of Dictyostelium and Other Lower Eukaryotes. In: O'Day, D., Catalano, A. (eds) Proteins of the Nucleolus. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5818-6_4
Download citation
DOI: https://doi.org/10.1007/978-94-007-5818-6_4
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-5817-9
Online ISBN: 978-94-007-5818-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)