Crystal structures of the apo and ATP bound Mycobacterium tuberculosis nitrogen regulatory PII protein

Protein Science

Volumn 19, Issue 8, 2010, Pages 1513-1524

  Shetty, Nishant D ^a   Reddy, Manchi C M ^a   Palaninathan, Satheesh K ^a   Owen, Joshua L ^a   Sacchettini, James C ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Ammonium transporter; Binary complex; Crystal structure; GlnB; GlnK; Glutamine synthetase; Homology model; Mycobacterium tuberculosis; Nitrogen regulatory protein; PII

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMTB PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; GLNK PROTEIN; MAGNESIUM ION; NITROGEN REGULATORY PROTEIN; PHOSPHATE; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; NITROGEN; PII NITROGEN REGULATORY PROTEINS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

METHANOCALDOCOCCUS JANNASCHII; MYCOBACTERIUM TUBERCULOSIS;

EID: 77955114169     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.430     Document Type: Article

References (57)

1. Ninfa AJ, Atkinson MR (2000) PII signal transduction proteins. Trends Microbiol 8:172-9.
2. Arcondeguy T, Jack R, Merrick M (2001) P(II) signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80-105. (Pubitemid 32204288)
3. Jiang P, Peliska JA, Ninfa AJ (1998) The regulation of Escherichia coli glutamine synthetase revisited: role of 2-ketoglutarate in the regulation of glutamine synthetase adenylylation state. Biochemistry 37:12802-10. (Pubitemid 28433511)
4. Engleman EG, Francis SH (1978) Cascade control of E. coli glutamine synthetase. II. Metabolite regulation of the enzymes in the cascade. Arch Biochem Biophys 191:602-12.
5. Ehlers C, Weidenbach K, Veit K, Forchhammer K, Schmitz RA (2005) Unique mechanistic features of post-translational regulation of glutamine synthetase activity in Methanosarcina mazei strain Go1 in response to nitrogen availability. Mol Microbiol 55: 1841-54. (Pubitemid 40445217)
6. II, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci U S A 83:5909-13.
7. Zhang Y, Pohlmann EL, Roberts GP (2005) GlnD is essential for NifA activation, NtrB/NtrC-regulated gene expression, and posttranslational regulation of nitrogenase activity in the photosynthetic, nitrogen-fixing bacterium Rhodospirillum rubrum. J Bacteriol 187: 1254-65. (Pubitemid 40299450)
8. van Heeswijk WC, Hoving S, Molenaar D, Stegeman B, Kahn D, Westerhoff HV (1996) An alternative PII protein in the regulation of glutamine synthetase in Escherichia coli. Mol Microbiol 21:133-46. (Pubitemid 26233088)
9. Javelle A, Merrick M (2005) Complex formation between AmtB and GlnK: an ancestral role in prokaryotic nitrogen control. Biochem Soc Trans 33:170-2. (Pubitemid 40313792)
10. Thomas G, Coutts G, Merrick M (2000) The glnKamtB operon. A conserved gene pair in prokaryotes. Trends Genet 16:11-4.
11. Khademi S, O'Connell J, 3rd, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 305:1587-94. (Pubitemid 39296348)
12. Durand A, Merrick M (2006) In vitro analysis of the Escherichia coli AmtB-GlnK complex reveals a stoichiometric interaction and sensitivity to ATP and 2-oxoglutarate. J Biol Chem 281:29558-67.
13. Strosser J, Ludke A, Schaffer S, Kramer R, Burkovski A (2004) Regulation of GlnK activity: modification, membrane sequestration and proteolysis as regulatory principles in the network of nitrogen control in Corynebacterium glutamicum. Mol Microbiol 54:132-47. (Pubitemid 39315164)
14. Read R, Pashley CA, Smith D, Parish T (2007) The role of GlnD in ammonia assimilation in Mycobacterium tuberculosis. Tuberculosis (Edinb) 87:384-90. (Pubitemid 46957538)
15. Hesketh A, Fink D, Gust B, Rexer HU, Scheel B, Chater K, Wohlleben W, Engels A (2002) The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol Microbiol 46:319-30.
16. Conroy MJ, Durand A, Lupo D, Li XD, Bullough PA, Winkler FK, Merrick M (2007) The crystal structure of the Escherichia coli AmtB-GlnK complex reveals how GlnK regulates the ammonia channel. Proc Natl Acad Sci U S A 104:1213-8.
17. Huergo LF, Merrick M, Pedrosa FO, Chubatsu LS, Araujo LM, Souza EM (2007) Ternary complex formation between AmtB, GlnZ and the nitrogenase regulatory enzyme DraG reveals a novel facet of nitrogen regulation in bacteria. Mol Microbiol 66:1523-35.
18. Huergo LF, Chubatsu LS, Souza EM, Pedrosa FO, Steffens MB, Merrick M (2006) Interactions between PII proteins and the nitrogenase regulatory enzymes DraT and DraG in Azospirillum brasilense. FEBS Lett 580: 5232-6.
19. Heinrich A, Woyda K, Brauburger K, Meiss G, Detsch C, Stulke J, Forchhammer K (2006) Interaction of the membrane-bound GlnK-AmtB complex with the master regulator of nitrogen metabolism TnrA in Bacillus subtilis. J Biol Chem 281:34909-17.
20. Jakoby M, Nolden L, Meier-Wagner J, Kramer R, Burkovski A (2000) AmtR, a global repressor in the nitrogen regulation system of Corynebacterium glutamicum. Mol Microbiol 37:964-77.
21. Wray LV, Jr., Atkinson MR, Fisher SH (1991) Identification and cloning of the glnR locus, which is required for transcription of the glnA gene in Streptomyces coelicolor A3(2). J Bacteriol 173:7351-60.
22. Fink D, Weissschuh N, Reuther J, Wohlleben W, Engels A (2002) Two transcriptional regulators GlnR and GlnRII are involved in regulation of nitrogen metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 46:331-47.
23. Tiffert Y, Supra P, Wurm R, Wohlleben W, Wagner R, Reuther J (2008) The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 67:861-80. (Pubitemid 351143689)
24. Mizuno Y, Moorhead GB, Ng KK (2007) Structural basis for the regulation of N-acetylglutamate kinase by PII in Arabidopsis thaliana. J Biol Chem 282: 35733-40. (Pubitemid 350277117)
25. Llacer JL, Contreras A, Forchhammer K, Marco-Marin C, Gil-Ortiz F, Maldonado R, Fita I, Rubio V (2007) The crystal structure of the complex of PII and acetylglutamate kinase reveals how PII controls the storage of nitrogen as arginine. Proc Natl Acad Sci U S A 104: 17644-9. (Pubitemid 350210889)
26. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-44.
27. Rengarajan J, Bloom BR, Rubin EJ (2005) Genomewide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 102:8327-32. (Pubitemid 40800088)
28. Goulding CW, Apostol M, Anderson DH, Gill HS, Smith CV, Kuo MR, Yang JK, Waldo GS, Suh SW, Chauhan R, Kale A, Bachhawat N, Mande SC, Johnston JM, Lott JS, Baker EN, Arcus VL, Leys D, McLean KJ, Munro AW, Berendzen J, Sharma V, Park MS, Eisenberg D, Sacchettini J, Alber T, Rupp B, Jacobs W Jr., Terwilliger TC (2002) The TB structural genomics consortium: providing a structural foundation for drug discovery. Curr Drug Targets Infect Disord 2: 121-41.
29. Carr PD, Cheah E, Suffolk PM, Vasudevan SG, Dixon NE, Ollis DL (1996) X-ray structure of the signal transduction protein from Escherichia coli at 1.9 Å. Acta Crystallogr D Biol Crystallogr 52:93-104.
30. Xu Y, Cheah E, Carr PD, van Heeswijk WC, Westerhoff HV, Vasudevan SG, Ollis DL (1998) GlnK, a PII-homologue: structure reveals ATP binding site and indicates how the T-loops may be involved in molecular recognition. J Mol Biol 282:149-65. (Pubitemid 28418666)
31. Cheah E, Carr PD, Suffolk PM, Vasudevan SG, Dixon NE, Ollis DL (1994) Structure of the Escherichia coli signal transducing protein PII. Structure 2:981-90.
32. Machado Benelli E, Buck M, Polikarpov I, Maltempi de Souza E, Cruz LM, Pedrosa FO (2002) Herbaspirillum seropedicae signal transduction protein PII is structurally similar to the enteric GlnK. Eur J Biochem 269: 3296-303.
33. Sakai H, Wang H, Takemoto-Hori C, Kaminishi T, Yamaguchi H, Kamewari Y, Terada T, Kuramitsu S, Shirouzu M, Yokoyama S (2005) Crystal structures of the signal transducing protein GlnK from Thermus thermophilus HB8. J Struct Biol 149:99-110. (Pubitemid 40051404)
34. Gruswitz F, O'Connell J, 3rd, Stroud RM (2007) Inhibitory complex of the transmembrane ammonia channel, AmtB, and the cytosolic regulatory protein, GlnK, at 1.96 Å. Proc Natl Acad Sci U S A 104:42-7.
35. Yildiz O, Kalthoff C, Raunser S, Kuhlbrandt W (2007) Structure of GlnK1 with bound effectors indicates regulatory mechanism for ammonia uptake. Embo J 26: 589-99.
36. Murzin AG, Lesk AM, Chothia C (1994) Principles determining the structure of beta-sheet barrels in proteins. I. A theoretical analysis. J Mol Biol 236: 1369-81.
37. Murzin AG, Lesk AM, Chothia C (1994) Principles determining the structure of beta-sheet barrels in proteins. II. The observed structures. J Mol Biol 236: 1382-400.
38. Schwarzenbacher R, von Delft F, Abdubek P, Ambing E, Biorac T, Brinen LS, Canaves JM, Cambell J, Chiu HJ, Dai X, Deacon AM, DiDonato M, Elsliger MA, Eshagi S, Floyd R, Godzik A, Grittini C, Grzechnik SK, Hampton E, Jaroszewski L, Karlak C, Klock HE, Koesema E, Kovarik JS, Kreusch A, Kuhn P, Lesley SA, Levin I, McMullan D, McPhillips TM, Miller MD, Morse A, Moy K, Ouyang J, Page R, Quijano K, Robb A, Spraggon G, Stevens RC, van den Bedem H, Velasquez J, Vincent J, Wang X, West B, Wolf G, Xu Q, Hodgson KO, Wooley J, Wilson IA (2004) Crystal structure of a putative PII-like signaling protein (TM0021) from Thermotoga maritima at 2.5 Å resolution. Proteins 54:810-3.
39. Xu Y, Carr PD, Clancy P, Garcia-Dominguez M, Forchhammer K, Florencio F, Vasudevan SG, Tandeau de Marsac N, Ollis DL (2003) The structures of the PII proteins from the cyanobacteria Synechococcus sp. PCC 7942 and Synechocystis sp. PCC 6803. Acta Crystallogr D Biol Crystallogr 59:2183-90.
40. Nichols CE, Sainsbury S, Berrow NS, Alderton D, Saunders NJ, Stammers DK, Owens RJ (2006) Structure of the PII signal transduction protein of Neisseria meningitidis at 1.85 Å resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:494-7.
41. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. Embo J 1:945-51.
42. Bandyopadhyay A, Arora A, Jain S, Laskar A, Mandal C, Ivanisenko VA, Fomin ES, Pintus SS, Kolchanov NA, Maiti S, Ramachandran S (2010) Expression and molecular characterization of the Mycobacterium tuberculosis PII protein. J Biochem 147:279-89.
43. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res 31:3381-5. (Pubitemid 37442164)
44. Mizuno Y, Berenger B, Moorhead GB, Ng KK (2007) Crystal structure of Arabidopsis PII reveals novel structural elements unique to plants. Biochemistry 46: 1477-83.
45. Bueno R, Pahel G, Magasanik B (1985) Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli. J Bacteriol 164:816-22. (Pubitemid 16191857)
46. Burkovski A (2007) Nitrogen control in Corynebacterium glutamicum: proteins, mechanisms, signals. J Microbiol Biotechnol 17:187-94.
47. Reuther J, Wohlleben W (2007) Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 12: 139-46. (Pubitemid 46011135)
48. Xu Y, Carr PD, Huber T, Vasudevan SG, Ollis DL (2001) The structure of the PII-ATP complex. Eur J Biochem 268:2028-37.
49. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-26. (Pubitemid 27085611)
50. McCoy AJ (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63:32-41.
51. Vagin AA, Steiner RA, Lebedev AA, Potterton L, McNicholas S, Long F, Murshudov GN (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr D Biol Crystallogr 60:2184-95.
52. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-3.
53. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-32.
54. McRee DE (1999) XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125:156-65.
55. Reddy V, Swanson SM, Segelke B, Kantardjieff KA, Sacchettini JC, Rupp B (2003) Effective electron-density map improvement and structure validation on a Linux multi-CPU web cluster: The TB Structural Genomics Consortium Bias Removal Web Service. Acta Crystallogr D Biol Crystallogr 59:2200-10.
56. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25:1605-12.
57. Merritt EA, Murphy ME (1994) Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr D Biol Crystallogr 50:869-73.