Bacterial Obg proteins: GTPases at the nexus of protein and DNA synthesis

Critical Reviews in Microbiology

Volumn 40, Issue 3, 2014, Pages 207-224

  Kint, Cyrielle ^a   Verstraeten, Natalie ^a   Hofkens, Johan ^a   Fauvart, Maarten ^a   Michiels, Jan ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Cell cycle; Dna replication; Ppgpp; Ribosome; Stress response

Indexed keywords

BACTERIAL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; OBG PROTEIN; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG;

BIOGENESIS; CHROMOSOME SEGREGATION; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; MATURATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; RIBOSOME; SPOROGENESIS; STRESS; TIGHT JUNCTION; ULTRAVIOLET IRRADIATION;

BACTERIA; DNA; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GTP PHOSPHOHYDROLASES; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; METABOLIC NETWORKS AND PATHWAYS; PROTEIN BIOSYNTHESIS;

EID: 84891136247     PISSN: 1040841X     EISSN: 15497828     Source Type: Journal    
DOI: 10.3109/1040841X.2013.776510     Document Type: Review

References (85)

1. Anurag M, Dash D. (2009). Unraveling the potential of intrinsically disordered proteins as drug targets: application to Mycobacterium tuberculosis. Mol Biosyst 5:1752-7.
2. Arigoni F, Talabot F, Peitsch M, et al. (1998). A genome-based approach for the identification of essential bacterial genes. Nat Biotechnol 16: 851-6. (Pubitemid 28405856)
3. Ash MR, Maher MJ, Mitchell Guss J, Jormakka M. (2012). The cationdependent G-proteins: in a class of their own. FEBS Lett 586: 2218-24.
4. Berthon J, Fujikane R, Forterre P. (2009). When DNA replication and protein synthesis come together. Trends Biochem Sci 34:429-34.
5. Blombach F, Brouns SJ, Van Der Oost J. (2011). Assembling the archaeal ribosome: roles for translation-factor-related GTPases. Biochem Soc Trans 39:45-50.
6. Braeken K, Moris M, Daniels R, et al. (2006). New horizons for (p)ppGpp in bacterial and plant physiology. Trends Microbiol 14: 45-54. (Pubitemid 43063191)
7. Britton, RA. (2009). Role of GTPases in bacterial ribosome assembly. Annu Rev Microbiol 63:155-76.
8. Brown ED. (2005). Conserved P-loop GTPases of unknown function in bacteria: an emerging and vital ensemble in bacterial physiology. Biochem Cell Biol 83:738-46.
9. Buglino J, Shen V, Hakimian P, Lima CD. (2002). Structural and biochemical analysis of the Obg GTP binding protein. Structure 10: 1581-92. (Pubitemid 35351498)
10. Caldon CE, March, PE. (2003). Function of the universally conserved bacterial GTPases. Curr Opin Microbiol 6:135-9. (Pubitemid 36628656)
11. Comartin DJ, Brown ED. (2006). Non-ribosomal factors in ribosome subunit assembly are emerging targets for new antibacterial drugs. Curr Opin Pharmacol 6:453-8. (Pubitemid 44340664)
12. Courcelle J, Khodursky A, Peter B, et al. (2001). Comparative gene expression profiles following UV exposure in wild-type and SOSdeficient Escherichia coli. Genetics 158:41-64.
13. Cox MM. (2007). Motoring along with the bacterial RecA protein. Nat Rev Mol Cell Biol 8:127-38. (Pubitemid 46432527)
14. Czyz A, Zielke R, Konopa G, Wegrzyn G. (2001). A Vibrio harveyi insertional mutant in the cgtA (obg, yhbZ) gene, whose homologues are present in diverse organisms ranging from bacteria to humans and are essential genes in many bacterial species. Microbiology 147: 183-91. (Pubitemid 32094321)
15. Datta K, Skidmore JM, Pu K, Maddock JR. (2004). The Caulobacter crescentus GTPase CgtAC is required for progression through the cell cycle and for maintaining 50S ribosomal subunit levels. Mol Microbiol 54:1379-92. (Pubitemid 39578279)
16. Davies BW, Kohanski MA, Simmons LA, et al. (2009). Hydroxyurea induces hydroxyl radical-mediated cell death in Escherichia coli. Mol Cell 36:845-60.
17. Dutkiewicz R, S?ominska M, Wegrzyn G, Czyz A. (2002). Overexpression of the cgtA (yhbZ, obgE) gene, coding for an essential GTP-binding protein, impairs the regulation of chromosomal functions in Escherichia coli. Curr Microbiol 45:440-5. (Pubitemid 36935573)
18. Feig LA, Cooper GM. (1988). Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol Cell Biol 8:3235-43.
19. Flardh K, Buttner MJ. (2009). Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
20. Foti JJ, Persky NS, Ferullo DJ, Lovett ST. (2007). Chromosome segregation control by Escherichia coli ObgE GTPase. Mol Microbiol 65:569-81. (Pubitemid 47052736)
21. Foti JJ, Schienda J, Sutera Jr VA, Lovett ST. (2005). A bacterial G protein-mediated response to replication arrest. Mol Cell 17:549-60. (Pubitemid 40269119)
22. Gasper R, Meyer S, Gotthardt K, et al. (2009). It takes two to tango: regulation of G proteins by dimerization. Nat Rev Mol Cell Biol 10: 423-9.
23. Gibbs JB, Sigal IS, Poe M, Scolnick EM. (1984). Intrinsic GTPase activity distinguishes normal and oncogenic ras p21 molecules. Proc Natl Acad Sci USA 81:5704-8. (Pubitemid 14023834)
24. Hecker M, Pane-Farre J, Volker U. (2007). SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61:215-36. (Pubitemid 350058207)
25. Higgins D, Dworkin J. (2012). Recent progress in Bacillus subtilis sporulation. FEMS Microbiol Rev 36:131-48.
26. Hwang J, Inouye, M. (2010). A bacterial GAP-like protein, YihI, regulating the GTPase of Der, an essential GTP-binding protein in Escherichia coli. J Mol Biol 399:759-72.
27. Jiang M, Datta K, Walker A, et al. (2006). The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly. J Bacteriol 188:6757-70. (Pubitemid 44497887)
28. Jiang M, Sullivan SM, Wout PK, Maddock JR. (2007). G-protein control of the ribosome-associated stress response protein SpoT. J Bacteriol 189:6140-7. (Pubitemid 47378620)
29. Karbstein K. (2007). Role of GTPases in ribosome assembly. Biopolymers 87:1-11. (Pubitemid 47401777)
30. Kataoka T, Powers S, Mcgill C, et al. (1984). Genetic analysis of yeast RAS1 and RAS2 genes. Cell, 37:437-45. (Pubitemid 14079038)
31. Katayama T, Ozaki S, Keyamura K, Fujimitsu K. (2010). Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8:163-70.
32. Kint CI, Verstraeten N, Wens I, et al. (2012). The Escherichia coli GTPase ObgE modulates hydroxyl radical levels in response to DNA replication fork arrest. FEBS J 279:3692-704.
33. Kobayashi G, Moriya S, Wada C. (2001). Deficiency of essential GTP-binding protein ObgE in Escherichia coli inhibits chromosome partition. Mol Microbiol 41:1037-51. (Pubitemid 36124701)
34. Kok J, Trach KA, Hoch JA. (1994). Effects on Bacillus subtilis of a conditional lethal mutation in the essential GTP-binding protein Obg. J Bacteriol 176:7155-60. (Pubitemid 24364040)
35. Kukimoto-Niino M, Murayama K, Inoue M, et al. (2004). Crystal structure of the GTP-binding protein Obg from Thermus thermophilus HB8. J Mol Biol 337:761-70. (Pubitemid 38326889)
36. Kuo S, Demeler B, Haldenwang WG. (2008). The growth-promoting and stress response activities of the Bacillus subtilis GTP binding protein Obg are separable by mutation. J Bacteriol 190: 6625-35.
37. Kuo S, Zhang S, Woodbury RL, Haldenwang WG. (2004). Associations between Bacillus subtilisB regulators in cell extracts. Microbiology 150:4125-36. (Pubitemid 40045341)
38. Lamb HK, Thompson P, Elliott C, et al. (2007). Functional analysis of the GTPases EngA and YhbZ encoded by Salmonella typhimurium. Protein Sci 16:2391-402. (Pubitemid 350036746)
39. Leipe DD, Wolf YI, Koonin EV, Aravind L. (2002). Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317: 41-72. (Pubitemid 34722199)
40. Lin B, Covalle KL, Maddock JR. (1999). The Caulobacter crescentus CgtA protein displays unusual guanine nucleotide binding and exchange properties. J Bacteriol 181:5825-32. (Pubitemid 29437156)
41. Lin B, Maddock JR. (2001). The N-terminal domain of the Caulobacter crescentus CgtA protein does not function as a guanine nucleotide exchange factor. FEBS Lett 489:108-11.
42. Lin B, Skidmore JM, Bhatt A, et al. (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 39:924-34. (Pubitemid 32176337)
43. Lin B, Thayer DA, Maddock JR. (2004). The Caulobacter crescentus CgtAC protein cosediments with the free 50S ribosomal subunit. J Bacteriol 186:481-9. (Pubitemid 38076439)
44. Maddock J, Bhatt A, Koch M, Skidmore J. (1997). Identification of an essential Caulobacter crescentus gene encoding a member of the Obg family of GTP-binding proteins. J Bacteriol 179: 6426-31. (Pubitemid 27443926)
45. Mccormick JR, Flardh K. (2012). Signals and regulators that govern Streptomyces development. FEMS Microbiol Rev 36:206-31.
46. Meena LS, Chopra P, Bedwal RS, Singh Y. (2008). Cloning and characterization of GTP-binding proteins of Mycobacterium tuberculosis H(37)Rv. Enzyme Microb Technol 42:138-44. (Pubitemid 350235589)
47. Michel B. (2005). Obg/CtgA, a signaling protein that controls replication, translation, and morphological development? Dev Cell 8:300-1. (Pubitemid 40309799)
48. Milon P, Tischenko E, Tomsic J, et al. (2006). The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Natl Acad Sci USA 103:13962-7. (Pubitemid 44452965)
49. Mohr D, Wintermeyer, W, Rodnina MV. (2002). GTPase activation of elongation factors Tu and G on the ribosome. Biochemistry 41: 12520-8.
50. Morimoto T, Loh PC, Hirai T, et al. (2002). Six GTP-binding proteins of the Era/Obg family are essential for cell growth in Bacillus subtilis. Microbiology 148:3539-52. (Pubitemid 35414464)
51. Okamoto S, Itoh, M, Ochi, K. (1997). Molecular cloning and characterization of the obg gene of Streptomyces griseus in relation to the onset of morphological differentiation. J Bacteriol 179:170-9. (Pubitemid 26428480)
52. Okamoto S, Ochi K. (1998). An essential GTP-binding protein functions as a regulator for differentiation in Streptomyces coelicolor. Mol Microbiol 30:107-19. (Pubitemid 28446624)
53. Paduch M, Jelen F, Otlewski J. (2001). Structure of small G proteins and their regulators. Acta Biochim Pol 48:829-50. (Pubitemid 33602340)
54. Patel BA, Moreau M, Widom J, et al. (2009). Endogenous nitric oxide regulates the recovery of the radiation-resistant bacterium Deinococcus radiodurans from exposure to UV light. Proc Natl Acad Sci USA 106:18183-8.
55. Persky NS, Ferullo DJ, Cooper DL, et al. (2009). The ObgE/CgtA GTPase influences the stringent response to amino acid starvation in Escherichia coli. Mol Microbiol 73:253-66.
56. Polakis P, McCormick F. (1993). Structural requirements for the interaction of p21ras with GAP, exchange factors, and its biological effector target. J Biol Chem 268:9157-60. (Pubitemid 23145950)
57. Polkinghorne A, Vaughan L. (2011). Chlamydia abortus YhbZ, a truncated Obg family GTPase, associates with the Escherichia coli large ribosomal subunit. Microb Pathog 50:200-6.
58. Potrykus K, Cashel M. (2008). (p)ppGpp: still magical? Annu Rev Microbiol 62:35-51.
59. Raskin DM, Judson N, Mekalanos JJ. (2007). Regulation of the stringent response is the essential function of the conserved bacterial G protein CgtA in Vibrio cholerae. Proc Natl Acad Sci USA 104:4636-41. (Pubitemid 47186277)
60. Sasindran SJ, Saikolappan S, Scofield VL, Dhandayuthapani S. (2011). Biochemical and physiological characterization of the GTP-binding protein Obg of Mycobacterium tuberculosis. BMC Microbiol 11:43.
61. Sato A, Kobayashi G, Hayashi H, et al. (2005). The GTP binding protein Obg homolog ObgE is involved in ribosome maturation. Genes Cells 10:393-408. (Pubitemid 40590358)
62. Scott JM, Haldenwang WG. (1999). Obg, an essential GTP binding protein of Bacillus subtilis, is necessary for stress activation of transcription factor B. J Bacteriol 181:4653-60. (Pubitemid 29357949)
63. Scott JM, Ju J, Mitchell T, Haldenwang WG. (2000). The Bacillus subtilis GTP binding protein Obg and regulators of theB stress response transcription factor cofractionate with ribosomes. J Bacteriol 182:2771-7. (Pubitemid 30246907)
64. Shah S, Das B, Bhadra RK. (2008). Functional analysis of the essential GTP-binding-protein-coding gene cgtA of Vibrio cholerae. J Bacteriol 190:4764-71. (Pubitemid 351898995)
65. Shajani Z, Sykes MT, Williamson JR. (2011). Assembly of bacterial ribosomes. Annu Rev Biochem 80:501-26.
66. Sigal IS, Gibbs JB, D?alonzo JS, et al. (1986). Mutant ras-encoded proteins with altered nucleotide binding exert dominant biological effects. Proc Natl Acad Sci USA 83:952-6. (Pubitemid 16086393)
67. Sikora AE, Datta K, Maddock JR. (2006a). Biochemical properties of the Vibrio harveyi CgtAV GTPase. Biochem Biophys Res Commun 339: 1165-70. (Pubitemid 41790585)
68. Sikora AE, Zielke R, Datta K, Maddock JR. (2006b). The Vibrio harveyi GTPase CgtAV is essential and is associated with the 50S ribosomal subunit. J Bacteriol 188:1205-10. (Pubitemid 43146442)
69. Sikora AE, Zielke R, Wegrzyn A, Wegrzyn G. (2006c). DNA replication defect in the Escherichia coli cgtA(ts) mutant arising from reduced DnaA levels. Arch Microbiol 185:340-7.
70. Sprang SR. (1997). G proteins, effectors and GAPs: structure and mechanism. Curr Opin Struct Biol 7:849-56. (Pubitemid 28025113)
71. Tan J, Jakob U, Bardwell JC. (2002). Overexpression of two different GTPases rescues a null mutation in a heat-induced rRNA methyltransferase. J Bacteriol 184:2692-8. (Pubitemid 34457036)
72. Trach K, Hoch JA. (1989). The Bacillus subtilis spo0B stage 0 sporulation operon encodes an essential GTP-binding protein. J Bacteriol 171:1362-71. (Pubitemid 19080773)
73. Traxler MF, Summers SM, Nguyen HT, et al. (2008). The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli. Mol Microbiol 68:1128-48. (Pubitemid 351670199)
74. Ulanowska K, Sikora A, Wegrzyn G, Czyz A. (2003). Role of the cgtA gene function in DNA replication of extrachromosomal elements in Escherichia coli. Plasmid 50:45-52. (Pubitemid 36765457)
75. Verstraeten N, Fauvart M, Versees W, Michiels J. (2011). The universally conserved prokaryotic GTPases. Microbiol Mol Biol Rev 75:507-42.
76. Vetter IR, Wittinghofer A. (2001). The guanine nucleotide-binding switch in three dimensions. Science 294:1299-304. (Pubitemid 33063089)
77. Vidwans SJ, Ireton K, Grossman AD. (1995). Possible role for the essential GTP-binding protein Obg in regulating the initiation of sporulation in Bacillus subtilis. J Bacteriol 177:3308-11.
78. Wang X, Xue J, Sun Z, et al. (2012). Study on the chaperone properties of conserved GTPases. Protein Cell 3:44-50.
79. Welsh KM, Trach KA, Folger C, Hoch JA. (1994). Biochemical characterization of the essential GTP-binding protein Obg of Bacillus subtilis. J Bacteriol 176:7161-8. (Pubitemid 24364041)
80. Wittinghofer A, Vetter IR. (2011). Structure-function relationships of the G domain, a canonical switch motif. Annu Rev Biochem 80:943-71.
81. Wout P, Pu K, Sullivan SM, et al. (2004). The Escherichia coli GTPase CgtAE cofractionates with the 50S ribosomal subunit and interacts with SpoT, a ppGpp synthetase/hydrolase. J Bacteriol 186:5249-57. (Pubitemid 39038128)
82. Yamanaka K, Hwang J, Inouye M. (2000). Characterization of GTPase activity of TrmE, a member of a novel GTPase superfamily, from Thermotoga maritima. J Bacteriol 182:7078-82. (Pubitemid 32259615)
83. Zhang, S, Haldenwang WG. (2004). Guanine nucleotides stabilize the binding of Bacillus subtilis Obg to ribosomes. Biochem Biophys Res Commun 322:565-9. (Pubitemid 39490341)
84. Zhang S, Scott JM, Haldenwang WG. (2001). Loss of ribosomal protein L11 blocks stress activation of the Bacillus subtilis transcription factor B. J Bacteriol 183:2316-21. (Pubitemid 32240402)
85. Zielke R, Sikora A, Dutkiewicz R, et al. (2003). Involvement of the cgtA gene function in stimulation of DNA repair in Escherichia coli and Vibrio harveyi. Microbiology 149:1763-70. (Pubitemid 36880735)