The Caulobacter crescentus GTPase CgtAc is required for progression through the cell cycle and for maintaining 50S ribosomal subunit levels

Molecular Microbiology

Volumn 54, Issue 5, 2004, Pages 1379-1392

  Datta, Kaustuv ^a   Skidmore, Jennifer M ^a   Pu, Kun ^a   Maddock, Janine R ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; GUANINE NUCLEOTIDE ACTIVATING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; PROTEIN CGTA C; PROTEIN OBG; RAS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BINDING AFFINITY; BINDING SITE; CAULOBACTER CRESCENTUS; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; DNA REPLICATION; FLOW CYTOMETRY; GENE MUTATION; NONHUMAN; OBG GENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN STABILITY; RIBOSOME; TEMPERATURE;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; CELL CYCLE; DNA REPLICATION; GENES, BACTERIAL; GENES, ESSENTIAL; GUANOSINE TRIPHOSPHATE; MONOMERIC GTP-BINDING PROTEINS; MUTATION; PROTEIN BINDING; RIBOSOMES; TEMPERATURE;

BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES; NEGIBACTERIA;

EID: 9644260815     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04354.x     Document Type: Article

References (52)

1. Alfoldi, L., Stent, G.S., and Clowes, R.C. (1962) The chromosomal site for the RNA control (R.C.) locus in E. coll. J Mol Biol 5: 348-355.
2. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
3. Buglino, J., Shen, V., Hakimian, P., and Lima, C.D. (2002) Structural and biochemical analysis of the Obg GTP-binding protein. Structure 10: 1581-1592.
4. Caldas, T., Binet, E., Bouloc, P., Costa, A., Desgres, J., and Richarme, G. (2000) The FtsJ/RrmJ heat shock protein of Escherichia coli is a 23 S ribosomal RNA methyltransferase. J Biol Chem 275: 16414-16419.
5. Caldon, C.E., and March, P.E. (2003) Function of the universally conserved bacterial GTPases. Curr Opin Microbiol 6: 135-139.
6. Chiaramello, A.E., and Zyskind, J.W. (1990) Coupling of DNA replication to growth rate in Escherichia coli: a possible role for guanosine tetraphosphate. J Bacteriol 172: 2013-2019.
7. Chiaverotti, T.A., Parker, G., Gallant, J., and Agabian, N. (1981) Conditions that trigger guanosine tetraphophate accumulation in Caulobacter crescentus. J Bacteriol 145: 1463-1465.
8. Cool, R.H., Schmidt, G., Lenzen, C.U., Prinz, H., Vogt, D., and Wittinghofer, A. (1999) The Ras mutant D119N is both dominant negative and activated. Mol Cell Biol 19: 6297-6305.
9. Dabbs, E.R. (1982) A spontaneous mutant of Escherichia coli with protein L24 lacking from the ribosome. Mol Gen Genet 187: 453-458.
10. Daigle, D.M., Rossi, L., Berghuis, A.M., Aravind, L., Koonin, E.V., and Brown, E.D. (2002) YjeQ, an essential, conserved, uncharacterized protein from Escherichia coli, is an unusual GTPase with circularly permuted G-Motifs and marked burst kinetics. Biochemistry 41: 11109-11117.
11. Degnen, ST., and Newton, A. (1972) Chromosome replication during development in Caulobacter crescentus. J Mol Biol 64: 671-680.
12. Ely, B. (1979) Transfer of drug resistance factors to the dimorphic bacterium Caulobacter crescentus. Genetics 91: 371-380.
13. Evinger, M., and Agabian, N. (1977) Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol 132: 294-301.
14. Farnsworth, C.L., and Feig, L.A. (1991) Dominant inhibitory mutations in the Mg(2+)-binding site of RasH prevent its activation by GTP. Mol Cell Biol 11: 4822-4829.
15. Franceschi, F.J., and Nierhaus, K.H. (1990) Ribosomal proteins L15 and L16 are mere late assembly proteins of the large ribosomal subunit. Analysis of an Escherichia coli mutant lacking L15. J Biol Chem 265: 16676-16682.
16. Gentry, D., and Cashel, M. (1995) Cellular location of the Escherichia coli SpoT protein. J Bacteriol 177: 3890-3893.
17. Gibbs, J.B., Schaber, M.D., Allard, W.J., Sigal, I.S., and Scolnick, E.M. (1988) Purification of ras GTPase activating protein from bovine brain. Proc Natl Acad Sci USA 85: 5026-5030.
18. Haseltine, W.A., and Bock, R. (1973) Synthesis of guanosine tetra and pentaphosphate requires the presence of a codon-specific uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc Natl Acad Sci USA 70: 1564-1568.
19. Hernandez, V.J., and Bremer, H. (1991) Escherichia coli ppGpp synthetase II activity requires spoT. J Biol Chem 266: 5991-5999.
20. Herald, M., Nowotny, V., Dabbs, E.R., and Nierhaus, K.H. (1986) Assembly analysis of ribosomes from a mutant lacking the assembly-initiator protein L24: lack of L24 induces temperature sensitivity. Mol Gen Genet 203: 281-287.
21. Hwang, J., and Inouye, M. (2001) An essential GTPase, der, containing double GTP-binding domains from Escherichia coli and Thermotoga maritima. J Biol Chem 17: 31415-31421.
22. Jensen, B.C., Wang, Q., Kifer, C.T., and Parsons, M. (2003) The NOG1 GTP-binding protein is required for biogenesis of the 60S ribosomal subunit. J Biol Chem 278: 32204-32211.
23. John, J., Rensland, H., Schlichting, I., Vetter, I., Borasio, G.D., Goody, R.S., and Wittinghofer, A. (1993) Kinetic and structural analysis of the Mg(2+)-binding site of the guanine nucleotide-binding protein p21H-ras. J Biol Chem 268: 923-929.
24. Kallstrom, G., Hedges, J., and Johnson, A. (2003) The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol Cell Biol 23: 4344-4355.
25. E in Escherichia coli inhibits chromosome partition. Mol Microbiol 41: 1037-1051.
26. Kok, J., Trach, K.A., and Hoch, J.A. (1994) Effects on Bacillus subtilis of a conditional lethal mutation in the essential GTP-binding protein Obg. J Bacteriol 176: 7155-7160.
27. Kukimoto-Niino, M., Murayama, K., Inoue, M., Terada, T., Tame, J.R., Kuramitsu, S., et al. (2004) Crystal structure of the GTP-binding protein Obg from Thermus thermophilus HB8. J Mol Biol 337: 761-770.
28. Lehoux, I.E., Mazzulla, M.J., Baker, A., and Petit, C.M. (2003) Purification and characterization of YihA, an essential GTP-binding protein from Escherichia coli. Protein Expr Purif 30: 203-209.
29. Leipe, D.D., Wolf, Y.I., Koonin, E.V., and Aravind, L. (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317: 41-72.
30. Lin, B., and Maddock, J.R. (2001) The N-terminal domain of the Caulobacter crescentus CgtA protein does not function as a guanine nucleotide exchange factor. FEBS Lett 489: 108-111.
31. Lin, B., Covalle, K.L., and Maddock, J.R. (1999) The Caulobacter crescentus CgtA protein displays unusual guanine nucleotide binding and exchange properties. J Bacteriol 181: 5825-5832.
32. Lin, B., Skidmore, J.M., Bhatt, A., Pfeffer, S.M., Pawloski, L., and Maddock, J.R. (2001) Alanine scan mutagenesis of the switch I domain of the Caulobacter crescentus CgtA protein reveals critical amino acids required for in vivo function. Mol Microbiol 39: 924-934.
33. c protein cosediments with the free 50S ribosomal subunit. J Bacteriol 186: 481-489.
34. Maddock, J., Bhatt, A., Koch, M., and Skidmore, J. (1997) Identification of an essential Caulobacter crescentus gene encoding a member of the Obg family of GTP-binding proteins. J Bacteriol 179: 6426-6431.
35. Marczynski, G.T., Lentine, K., and Shapiro, L. (1995) A developmentally regulated chromosomal origin of replication uses essential transcription elements. Genes Dev 9: 1543-1557.
36. Marvaldi, J., Pichon, J., and Marchis-Mouren, G. (1979) On the control of ribosomal protein biosynthesis in E. coli. IV. Studies on a temperature-sensitive mutant defective in the assembly of 50S subunits. Mol Gen Genet 171: 317-325.
37. Okamoto, S., and Ochi, K. (1998) An essential GTP-binding protein functions as a regulator of differentiation in Streptomyces coelicolor. Mol Microbiol 30: 107-119.
38. Orr, E., Fairweather, N.F., Holland, I.B., and Pritchard, R.H. (1979) Isolation and characterisation of a strain carrying a conditional lethal mutation in the cou gene of Escherichia coli K12. Mol Gen Genet 177: 102-112.
39. Poindexter, J.S. (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28: 231-295.
40. Ramagopal, S., and Davis, B.D. (1974) Localization of the stringent protein of Escherichia coli on the 50S ribosomal subunit. Proc Natl Acad Sci 71: 820-824.
41. Richter, D. (1980) Uncharged tRNA inhibits guanosine 3′,5′- bis (diphosphate) 3′-pyrophosphohydrolase [ppGppase], the spoT gene product, from Escherichia coli. Mol Gen Genet 178: 325-327.
42. B. J Bacteriol 181: 4653-4660.
43. B stress response transcription factor cofractionate with ribosomes. J Bacteriol 182: 2771-2777.
44. Stephens, C., Mohr, C., Boyd, C., Maddock, J., Gober, J., and Shapiro, L. (1997) Identification of the flil and fliJ components of the Caulobacter flagellar type III protein secretion system. J Bacteriol 179: 5355-5366.
45. Sullivan, S.M., Mishra, R., Neubig, R.R., and Maddock, J.R. (2000) Analysis of guanine nucleotide binding and exchange kinetics of the Escherichia coli GTPase Era. J Bacteriol 182: 3460-3466.
46. Tan, J., Jakob, U., and Bardwell, J.C. (2002) Overexpression of two different GTPases rescues a null mutation in a heat-induced rRNA methyltransferase. J Bacteriol 184: 2692-2698.
47. Trach, K., and Hoch, J.A. (1989) The Bacillus subtilis spoOB stage 0 sporulation operon encodes an essential GTP-binding protein. J Bacteriol 171: 1362-1371.
48. Ulanowska, K., Sikora, A., Wegrzyn, G., and Czyz, A. (2003) Role of the cgtA gene function in DNA replication of extrachromosomal elements in Escherichia coli. Plasmid 50: 45-52.
49. Welsh, K.M., Trach, K.A., Folger, C., and Hoch, J.A. (1994) Biochemical characterization of the essential GTP-binding protein Obg of Bacillus subtilis. J Bacteriol 176: 7161-7168.
50. Wolf, Y.I., Aravind, L., Grishin, N.V., and Koonin, E.V. (1999) Evolution of aminoacyl-tRNA synthetases - analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res 9: 689-710.
51. E, cofractionates with the 50S ribosomal subunit and interacts with SpoT, a ppGpp synthetase/hydrolase. J Bacteriol 186: 5249-5257.
52. Wower, I.K., Wower, J., and Zimmermann, R.A. (1998) Ribosomal protein L27 participates in both 50 S subunit assembly and the peptidyl transferase reaction. J Biol Chem 273: 19847-19852.