Metal ion-dependent anti-termination of transcriptional regulation of ribonucleoprotein complexes

Biophysical Reviews - Tập 6 - Trang 215-226 - 2014
Penmetcha K. R. Kumar1, Hiroshi Mizuno1
1Biomedical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba City, Japan

Tóm tắt

Anti-terminator proteins are frequently used by bacteria to sense a specific metabolite signal and direct RNA polymerase to either terminate or continue transcription of the genes downstream of an operon. One such protein is HutP, which binds to upstream cis-regulatory sequences to regulate expression of the histidine utilization (hut) operon in Bacillus subtilis. HutP must be activated by L-histidine and divalent metal ions before binding to hut mRNA; binding of activated HutP prevents termination of transcription. Thus, HutP appears to regulate the hut operon in a unique fashion in this class of regulatory proteins. To understand gene (hut operon) regulation by HutP, we performed several biochemical and structural studies. These studies reveal events in the regulatory mechanism, starting with the activation of HutP and ending with the unwinding of hut terminator RNA. In this review, we describe the unique regulatory mechanisms commonly used by many Bacillus species.

Tài liệu tham khảo

Alpert CA, Siebers U (1997) The lac operon of Lactobacillus casei contains lacT, a gene coding for a protein of the Bg1G family of transcriptional antiterminators. J Bacteriol 179:1555–1562 Arnaud MD, Debarbouille M, Rapoport G, Saier MH, Reizer J (1996) In vitro reconstitution of transcriptional attenuation by the SacT and SacY proteins of Bacillus subtilis. J Biol Chem 271:18966–18972 Aymerich S, Steinmetz M (1992) Specificity determinants and structural features in the RNA target of the bacterial antiterminator proteins of the BglG/SacY family. Proc Natl Acad Sci USA 89:10410–10414 Babitzke P, Yanofsky C (1993) Reconstitution of Bacillus subtilis trp attenuation in vitro with TRAP, the trp RNA-binding attenuation protein. Proc Natl Acad Sci USA 90:133–137 Balasundaresan D, Mizuno H, Kumar PKR (2013) Alternative binding modes of L-histidine guided by metal ions for the activation of the antiterminator protein HutP of Bacillus subtilis. J Struct Biol 183:512–518 Bender RA (2012) Regulation of the histidine utilization (Hut) system in bacteria. Microbiol Mol Biol Rev 76:565–584 Chasin LA, Magasanik B (1968) Induction and repression of histidine-degrading enzymes of Bacillus subtili. J Biol Chem 243:5165–5178 Glatz E, Nilsson RP, Rutberg L, Rutberg B (1996) A dual role for the Bacillus subtilis glpD leader and the GlpP protein in the regulated expression of glpD: antitermination and control of mRNA stability. Mol Microbiol 19:319–328 Gopinath SCB, Balasundaresan D, Kumarevel T, Misono TS, Mizuno H, Kumar PKR (2008) Insight into anti-termination regulation of the hut operon in Bacillus subtilis: importance of the dual RNA-binding surfaces of HutP. Nucleic Acids Res 36:3463–3473 Houman F, Diaz-Torres MR, Wright A (1990) Transcriptional antitermination in the bgl operon of E. coli is modulated by a specific RNA binding protein. Cell 62:1153–1163 Kimmhi Y, Magasanik B (1970) Genetic basis of histidine degradation in Bacillus subtili. J Biol Chem 245:3545–3548 Kumarevel T, Fujimoto Z, Karthe P, Oda M, Mizuno H, Kumar PKR (2004a) Crystal structure of activated HutP: An RNA binding protein that regulates transcription of the hut operon in Bacillus subtili. Structure 12:1269–1280 Kumarevel T, Gopinath SCB, Nishikawa S, Mizuno H, Kumar PKR (2004b) Identification of important chemical groups of the hut mRNA for HutP interactions that regulates the hut operon in Bacillus subtili. Nucleic Acids Res 32:3904–3912 Kumarevel T, Mizuno H, Kumar PKR (2005a) Characterization of the metal ion binding site in the anti-terminator protein, HutP, of Bacillus subtili. Nucleic Acids Res 33:5494–5502 Kumarevel T, Mizuno H, Kumar PKR (2005b) Structural basis of HutP-mediated anti-termination and roles of the Mg2+ ion and L-histidine ligand. Nature 434:183–191 Lu Y, Turner RJ, Switzer RL (1996) Function of RNA secondary structures in transcriptional attenuation of the Bacillus subtilis pyr operon. Proc Natl Acad Sci USA 93:14462–14467 Oda M, Sugishita A, Furukawa K (1988) Cloning and nucleotide sequence of histidase and regulatory genes in the Bacillus subtili hut operon and positive regulatory operon. J Bacteriol 170:3199–3205 Oda M, Katagai T, Tomura D, Shoun H, Hoshino T, Furukawa T (1992) Analysis of the transcriptional activity of the hut promoter in Bacillus subtilis and identification of a cis-acting regulatory region associated with catabolite repression downstream from the site of transcription. Mol Microbiol 6:2573–2582 Oda M, Kobayashi N, Ito A, Kurusu Y, Taira K (2000) Cis-acting regulatory sequences for antitermination in the transcript of the Bacillus subtili hut operon and histidine-dependent binding of HutP to the transcript containing regulatory sequences. Mol Microbiol 35:1244–1254 Yoshida K, Sano H, Seki S, Oda M, Fujimura M, Fujita Y (1995) Cloning and sequencing of a 29 kb region of the Bacillus subtili genome containing the hut and wapA loci. Microbiology 141:337–343