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Calcium regulates the expression of aDictyostelium discoideum asparaginyl tRNA synthetase gene

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Abstract

In a screen for calcium-regulated gene expression during growth and development ofDictyostelium discoideum we have identified an asparaginyl tRNA synthetase (ddAsnRS) gene, the second tRNA synthetase gene identified in this organism. TheddAsnRS gene shows many unique features. One, it is repressed by lowering cellular calcium, making it the first known calcium-regulated tRNA synthetase. Two, despite the calcium-dependence, its expression is unaltered during the cell cycle, making this the firstD. discoideum gene to show a calcium-dependent but cell cycle phase-independent expression. Finally, the N-terminal domain of the predicted ddAsnRS protein shows higher sequence similarity to Glutaminyl tRNA synthetases than to other Asn tRNA synthetases. These unique features of theAsnRS from this primitive eukaryote not only point to a novel mechanism regulating the components of translation machinery and gene expression by calcium, but also hint at a link between the evolution ofGlnRS andAsnRS in eukaryotes.

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Abbreviations

AARS:

Amino acyl tRNA synthetase

AsnRS:

asparaginyl tRNA synthetase

HC:

high calcium

LC:

low calcium

RAP-PCR:

RNA arbitrary primed-PCR

References

  • Altschul S F, Gish W, Miller W, Myers E W and Lipman D J 1990 Basic local alignment search tool;J. Mol. Biol. 215 403–410

    PubMed  CAS  Google Scholar 

  • Azhar M 1997Dependence of post-aggregative cell fate on early phenotypic differences with respect to cellular calcium and cell cycle phase in Dictyostelium discoideum, Ph. D. thesis, Indian Institute of Science, Bangalore, India

    Google Scholar 

  • Azhar M, Kennady P K, Pande G, Espiritu M, Holloman W, Brazill D, Gomer R H and Nanjundiah V 2001 Cell cycle phase, cellular Ca2+ and development inDictyostelium discoideum;Int. J. Dev. Biol. 45 405–414

    PubMed  CAS  Google Scholar 

  • Azhar M, Krefft M, Saran S, Weeks G and Nanjundiah V 1998 Calcium levels correlate with cell cycle phase and affect the level of the cyclin B transcript inDictyostelium discoideum;FEMS Microbiol. Lett. 161 193–199

    Article  PubMed  CAS  Google Scholar 

  • Azhar M, Manogaran P S, Kennady P K, Pande G and Nanjundiah V 1996 A Ca2+-dependent early functional heterogeneity in amoebae ofDictyostelium discoideum, revealed by flow cytometry;Exp. Cell Res. 227 344–351

    Article  PubMed  CAS  Google Scholar 

  • Bain G, Grant C E and Tsang A 1991 Isolation and characterization of cDNA clones encoding polypeptides related to aDictyostelium discoideum cyclic AMP binding protein;J. Gen. Microbiol. 137 501–508

    PubMed  CAS  Google Scholar 

  • Baskar R, Chhabra P, Mascarenhas P and Nanjundiah V 2000 A cell type-specific effect of calcium on pattern formation and differentiation inDictyostelium discoideum;Int. J. Dev. Biol. 44 491–498

    PubMed  CAS  Google Scholar 

  • Bush J, Richardson J and Cardelli J 1994 Molecular cloning and characterization of the full-length cDNA encoding the developmentally regulated lysosomal enzyme beta-glucosidase inDictyostelium discoideum;J. Biol. Chem. 269 468–1476

    Google Scholar 

  • Chomczynski P and Sacchi N 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction;Anal. Biochem. 162 156–159

    Article  PubMed  CAS  Google Scholar 

  • Commans S, Lazard M, Delort F, Blanquet S and Plateau P 1998 tRNA anticodon recognition and specification within subclass IIb aminoacyl-tRNA synthetases;J. Mol. Biol. 278 801–813

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Lazcoz Y, Aude J C, Nitschke P, Chiapello H, Landes-Devauchelle C and Risler J L 1998 Evolution of genes, evolution of species: the case of aminoacyl-tRNA synthetases;Mol. Biol. Evol. 15 1548–1561

    PubMed  CAS  Google Scholar 

  • Glöckner G, Eichinger L, Szafranski K, Pachebat J A, Bankier A T, Dear P H, Lehmann R, Baumgart C, Parra G, Abril J F, Guigo R, Kumpf K, Tunggal B, Cox E, Quail M A, Platzer M, Rosenthal A and Noegel A A 2002 Sequence and analysis of chromosome 2 ofDictyostelium discoideum;Nature (London) 418 79–85

    Article  Google Scholar 

  • Gmitter D, Brostrom C O and Brostrom M A 1996 Translational suppression by Ca2+ ionophores: reversibility and roles of Ca2+ mobilization, Ca2+ influx, and nucleotide depletion;Cell Biol. Toxicol. 12 101–113

    Article  PubMed  CAS  Google Scholar 

  • Gomer R H and Firtel R A 1987 Cell-autonomous determination of cell-type choice inDictyostelium development by cell-cycle phase;Science 237 758–762

    Article  PubMed  CAS  Google Scholar 

  • Grant C E and Tsang A 1990 Cloning and characterization of cDNAs encoding a novel cyclic AMP-binding protein inDictyostelium discoideum;Gene 96 213–218

    Article  PubMed  CAS  Google Scholar 

  • Hardingham G E and Bading H 1999 Calcium as a versatile second messenger in the control of gene expression;Micros. Res. Tech. 46 348–355

    Article  CAS  Google Scholar 

  • Higgins D G and Sharp P M 1988 CLUSTAL: a package for performing multiple sequence alignment on a microcomputer;Gene 73 237–244

    Article  PubMed  CAS  Google Scholar 

  • Hirose S, Inazu Y, Chae S and Maeda Y 2000 Suppression of the growth/differentiation transition inDictyostelium development by transient expression of a novel gene, dia1;Development 127 3263–3270

    PubMed  CAS  Google Scholar 

  • Holland I B, Jones H E, Campbell A K and Jacq A 1999 An assessment of the role of intracellular free Ca2+ inE. coli;Biochimie 81 901–907

    Article  PubMed  CAS  Google Scholar 

  • Hopper N A, Harwood A J, Bouzid S, Veron M and Williams J G 1993 Activation of the prespore and spore cell pathway ofDictyostelium differentiation by cAMP-dependent protein kinase and evidence for its upstream regulation by ammonia;EMBO J. 12 2459–2466

    PubMed  CAS  Google Scholar 

  • Huang H and Pears C 1999 Cell cycle-dependent regulation of early developmental genes;Biochim. Biophys. Acta 1452 296–302

    Article  PubMed  CAS  Google Scholar 

  • Inazu Y, Chae S C and Maeda Y 1999 Transient expression of a mitochondrial gene cluster including rps4 is essential for the phase-shift ofDictyostelium cells from growth to differentiation;Dev. Genet. 25 339–352

    Article  PubMed  CAS  Google Scholar 

  • Itoh M, Noguchi M and Maeda Y 1998 Overexpression of CAF1 encoding a novel Ca2+-binding protein stimulates the transition ofDictyostelium cells from growth to differentiation;Dev. Growth Differ. 40 677–683

    Article  PubMed  CAS  Google Scholar 

  • Jaiswal J K 2001 Calcium - how and why?;J. Biosci 26 357–363

    Article  PubMed  CAS  Google Scholar 

  • Jaiswal J K 2001Genes involved in cell type specification and morphogenesis in Dictyostelium discoideum, Ph. D. thesis, Indian Institute of Science, Bangalore, India

    Google Scholar 

  • Kumar R V, Panniers R, Wolfman A and Henshaw E C 1991 Inhibition of protein synthesis by antagonists of calmodulin in Ehrlich ascites tumor cells;Eur. J. Biochem. 195 313–319

    Article  PubMed  CAS  Google Scholar 

  • Leach C K, Ashworth J M and Garrod D R 1973 Cell sorting out during the differentiation of mixtures of metabolically distinct populations ofDictyostelium discoideum;J. Embryol. Exp. Morphol. 29 647–661

    PubMed  CAS  Google Scholar 

  • Liang P and Pardee A B 1995 Recent advances in differential display;Curr. Opin. Immunol. 7 274–280

    Article  PubMed  CAS  Google Scholar 

  • MacWilliams H, Gaudet P, Deichsel H, Bonfils C and Tsang A 2001 Biphasic expression of rnrB inDictyostelium discoideum suggests a direct relationship between cell cycle control and cell differentiation;Differentiation 67 12–24

    Article  PubMed  CAS  Google Scholar 

  • Maeda Y, Ohmori T, Abe T, Abe F and Amagai A 1989 Transition of starvingDictyostelium cells to differentiation phase at a particular position of the cell cycle;Differentiation 41 169–175

    Article  PubMed  CAS  Google Scholar 

  • Malchow D, Mutzel R and Schlatterer C 1996 On the role of calcium during chemotactic signalling and differentiation of the cellular slime mouldDictyostelium discoideum;Int. J. Dev. Biol. 40 135–139

    PubMed  CAS  Google Scholar 

  • Martinis S A, Plateau P, Cavarelli J and Florentz C 1999 Aminoacyl-tRNA synthetases: a new image for a classical family;Biochimie 81 683–700

    Article  PubMed  CAS  Google Scholar 

  • McDonald S A and Durston A J 1984 The cell cycle and sorting behaviour inDictyostelium discoideum;J. Cell Sci. 66 195204

    Google Scholar 

  • Motomura S, Fukushima K, Nishitani H, Nawata H and Nishimoto T 1996 A hamster temperature-sensitive G1 mutant, tsBN250 has a single point mutation in histidyl-tRNA synthetase that inhibits an accumulation of cyclin D1;Genes Cells 1 1101–1112

    Article  PubMed  CAS  Google Scholar 

  • Noce T and Takeuchi I 1985 Prestalk-prespore differentiation tendency ofDictyostelium discoideum as detected by a stalk-specific monoclonal antibody;Dev. Biol. 109 157–164

    Article  PubMed  CAS  Google Scholar 

  • Pelchat M and Lapointe J 1999 Aminoacyl-tRNA synthetase genes ofBacillus subtilis: organization and regulation;Biochem. Cell Biol. 77 343–347

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch E F and Maniatis T 1989Molecular cloning: A laboratory manual (New York: Cold Spring Harbour Laboratory Press)

    Google Scholar 

  • Saran S 1999 Calcium levels during cell cycle correlate with cell fateof Dictyostelium discoideum;Cell Biol. Int. 23 399–405

    Article  PubMed  CAS  Google Scholar 

  • Saran S, Azhar M, Manogaran P S, Pande G and Nanjundiah V 1994 The level of sequestered calcium in vegetative amoebae ofDictyostelium discoideum can predict post-aggregative cell fate;Differentiation 57 163–169

    Article  PubMed  CAS  Google Scholar 

  • Sen S, Zhou H, Ripmaster T, Hittelman W N, Schimmel P and White R A 1997 Expression of a gene encoding a tRNA synthetase-like protein is enhanced in tumorigenic human myeloid leukemia cells and is cell cycle stage-and differentiation-dependent;Proc. Natl. Acad. Sci. USA 94 6164–6169

    Article  PubMed  CAS  Google Scholar 

  • Shiba K, Motegi H, Yoshida M and Noda T 1998 Human asparaginyl-tRNA synthetase: molecular cloning and the inference of the evolutionary history of Asx-tRNA synthetase family;Nucleic Acids Res. 26 5045–5051

    Article  PubMed  CAS  Google Scholar 

  • Singleton C K, Manning S S and Ken R 1989 Primary structure and regulation of vegetative specific genes ofDictyostelium discoideum;Nucleic Acids Res. 17 9679–9692

    Article  PubMed  CAS  Google Scholar 

  • Sonnemann J, Drugeon G, Haenni A L and Mutzel R 1993 Elongation in aDictyostelium in vitro translation system is affected by calmodulin antagonists;FEBS Lett. 329 183–188

    Article  PubMed  CAS  Google Scholar 

  • Sonnhammer E L, Eddy S R and Durbin R 1997 Pfam: a comprehensive database of protein domain families based on seed alignments;Proteins 28 405–420

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Itakura R, Amagai A and Maeda Y 1998 The signals for starvation response are transduced through elevated [Ca2+]i inDictyostelium cells;Exp. Cell Res. 240 340–348

    Article  PubMed  CAS  Google Scholar 

  • Thompson J D, Higgins D G and Gibson T J 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice;Nucleic Acids Res. 22 4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tumbula D L, Becker H D, Chang W Z and Soll D 2000 Domain-specific recruitment of amide amino acids for protein synthesis;Nature (London) 407 106–110

    Article  CAS  Google Scholar 

  • Watts D J and Ashworth J M 1970 Growth of myxameobae of the cellular slime mouldDictyostelium discoideum in axenic culture;Biochem. J. 119 171–174

    PubMed  CAS  Google Scholar 

  • Weijer C J, Duschl G and David C N 1984a A revision of theDictyostelium discoideum cell cycle;J. Cell Sci. 70 111–131

    PubMed  CAS  Google Scholar 

  • Weijer C J, Duschl G and David C N 1984b Dependence of cell-type proportioning and sorting on cell cycle phase inDictyostelium discoideum;J. Cell Sci. 70 133–145

    PubMed  CAS  Google Scholar 

  • Weiner A M 1999 Molecular evolution: aminoacyl-tRNA synthetases on the loose;Curr. Biol. 9 R842-R844

    Article  PubMed  CAS  Google Scholar 

  • Welsh J, Chada K, Dalal S S, Cheng R, Ralph D and McClelland M 1992 Arbitrarily Primed PCR fingerprinting of RNA;Nucleic Acids Res. 20 4965–4970

    Article  PubMed  CAS  Google Scholar 

  • Woese C R, Olsen G J, Ibba M and Soll D 2000 Aminoacyl-tRNA synthetases, the genetic code and the evolutionary process;Microbiol. Mol. Biol. Rev. 64 202–236

    Article  PubMed  CAS  Google Scholar 

  • Xu A, Bellamy A R and Taylor J A 1999 Expression of translationally controlled tumour protein is regulated by calcium at both the transcriptional and post-transcriptional level;Biochem. J. 342 683–689

    Article  PubMed  CAS  Google Scholar 

  • Yuan A, Siu C H and Chia C P 2001 Calcium requirement for efficient phagocytosis byDictyostelium discoideum;Cell Calcium 29 229–238

    Article  PubMed  CAS  Google Scholar 

  • Zhou X, Richon V M, Ngo L, Rifkind R A and Marks P A 1999 Cloning of the cDNA encoding phenylalanyl tRNA synthetase regulatory alpha-subunit-like protein whose expression is down-regulated during differentiation;Gene 233 13–19

    Article  PubMed  CAS  Google Scholar 

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  1. Jyoti K. Jaiswal

    Present address: The Rockefeller University, 1230 York Avenue, Box 304, 10021, New York, NY, USA

Authors and Affiliations

  1. Department of Molecular Reproduction, Development and Genetics, Indian Institute of Science, 560 012, Bangalore, India

    Jyoti K. Jaiswal & Vidyanand Nanjundiah

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  1. Jyoti K. Jaiswal
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  2. Vidyanand Nanjundiah
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Correspondence to Jyoti K. Jaiswal.

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Jaiswal, J.K., Nanjundiah, V. Calcium regulates the expression of aDictyostelium discoideum asparaginyl tRNA synthetase gene. J Biosci 28, 697–707 (2003). https://doi.org/10.1007/BF02708430

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