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Two crystal structures of the cytoplasmic molybdate-binding protein ModG suggest a novel cooperative binding mechanism and provide insights into ligand-binding specificity.

Delarbre L, Stevenson CE, White DJ, Mitchenall LA, Pau RN, Lawson DM
J Mol Biol 308 1063-79 (2001)
Related entries: 1h9j, 1h9k

Cited: 27 times
EuropePMC logo PMID: 11352591

Abstract

The X-ray structures of the cytoplasmic molybdate-binding protein ModG from Azotobacter vinelandii in two different crystal forms have been determined. For such a small protein it is remarkably complex. Each 14.3 kDa subunit contains two small beta-barrel domains, which display an OB-fold motif, also seen in the related structure of ModE, a molybdenum-dependent transcriptional regulator, and very recently in the Mop protein that, like ModG, has been implicated in molybdenum homeostasis within the cell. In contrast to earlier speculation, the functional unit of ModG is actually not a dimer (as in ModE), but a trimer capable of binding a total of eight molybdate molecules that are distributed between two disparate types of site. All the binding sites are located at subunit interfaces, with one type lying on a crystallographic 3-fold axis, whilst the other lies between pairs of subunits. The two types of site are linked by short hydrogen bond networks that may suggest a cooperative binding mechanism. A superposition of two subunits of the ModG trimer on the apo-ModE dimer allows the probable locations of the molybdate-binding sites of the latter to be assigned. Through structural comparisons with other oxyanion-binding proteins, including Mop and ModE, it is possible to speculate about ligand-binding affinities, selectivity and evolution.

Reviews - 1h9m mentioned but not cited (1)

  1. Biosynthesis of Nitrogenase Cofactors. Burén S, Jiménez-Vicente E, Echavarri-Erasun C, Rubio LM. Chem Rev 120 4921-4968 (2020)

Articles - 1h9m mentioned but not cited (3)

  1. Manipulation of conformational change in proteins by single-residue perturbations. Atilgan C, Gerek ZN, Ozkan SB, Atilgan AR. Biophys J 99 933-943 (2010)
  2. Docking protein domains in contact space. Lise S, Walker-Taylor A, Jones DT. BMC Bioinformatics 7 310 (2006)
  3. Relative stabilities of conserved and non-conserved structures in the OB-fold superfamily. Guardino KM, Sheftic SR, Slattery RE, Alexandrescu AT. Int J Mol Sci 10 2412-2430 (2009)


Reviews citing this publication (1)

  1. The involvement of molybdenum in life. Williams RJ, Fraústo da Silva JJ. Biochem Biophys Res Commun 292 293-299 (2002)

Articles citing this publication (22)

  1. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Gerber S, Comellas-Bigler M, Goetz BA, Locher KP. Science 321 246-250 (2008)
  2. Towards biological supramolecular chemistry: a variety of pocket-templated, individual metal oxide cluster nucleations in the cavity of a mo/w-storage protein. Schemberg J, Schneider K, Demmer U, Warkentin E, Müller A, Ermler U. Angew Chem Int Ed Engl 46 2408-2413 (2007)
  3. Essential metals for nitrogen fixation in a free-living N₂-fixing bacterium: chelation, homeostasis and high use efficiency. Bellenger JP, Wichard T, Xu Y, Kraepiel AM. Environ Microbiol 13 1395-1411 (2011)
  4. Molybdate transport and its effect on nitrogen utilization in the cyanobacterium Anabaena variabilis ATCC 29413. Zahalak M, Pratte B, Werth KJ, Thiel T. Mol Microbiol 51 539-549 (2004)
  5. A segment of cold shock protein directs the folding of a combinatorial protein. de Bono S, Riechmann L, Girard E, Williams RL, Winter G. Proc Natl Acad Sci U S A 102 1396-1401 (2005)
  6. Crystal structure of activated ModE reveals conformational changes involving both oxyanion and DNA-binding domains. Schüttelkopf AW, Boxer DH, Hunter WN. J Mol Biol 326 761-767 (2003)
  7. Molybdenum trafficking for nitrogen fixation. Hernandez JA, George SJ, Rubio LM. Biochemistry 48 9711-9721 (2009)
  8. Transport of molybdate in the cyanobacterium Anabaena variabilis ATCC 29413. Thiel T, Pratte B, Zahalak M. Arch Microbiol 179 50-56 (2002)
  9. Novel CalphaNN structural motif for protein recognition of phosphate ions. Denessiouk KA, Johnson MS, Denesyuk AI. J Mol Biol 345 611-629 (2005)
  10. Solution structure of ribosomal protein S28E from Methanobacterium thermoautotrophicum. Wu B, Yee A, Pineda-Lucena A, Semesi A, Ramelot TA, Cort JR, Jung JW, Edwards A, Lee W, Kennedy M, Arrowsmith CH. Protein Sci 12 2831-2837 (2003)
  11. Solution NMR structure of the 30S ribosomal protein S28E from Pyrococcus horikoshii. Aramini JM, Huang YJ, Cort JR, Goldsmith-Fischman S, Xiao R, Shih LY, Ho CK, Liu J, Rost B, Honig B, Kennedy MA, Acton TB, Montelione GT. Protein Sci 12 2823-2830 (2003)
  12. Azotobacter vinelandii metal storage protein: "classical" inorganic chemistry involved in Mo/W uptake and release processes. Schemberg J, Schneider K, Fenske D, Müller A. Chembiochem 9 595-602 (2008)
  13. Siderophore production in Azotobacter vinelandii in response to Fe-, Mo- and V-limitation. McRose DL, Baars O, Morel FMM, Kraepiel AML. Environ Microbiol 19 3595-3605 (2017)
  14. Repeats in S1 Proteins: Flexibility and Tendency for Intrinsic Disorder. Machulin A, Deryusheva E, Lobanov M, Galzitskaya O. Int J Mol Sci 20 E2377 (2019)
  15. Specific interactions between four molybdenum-binding proteins contribute to Mo-dependent gene regulation in Rhodobacter capsulatus. Wiethaus J, Müller A, Neumann M, Neumann S, Leimkühler S, Narberhaus F, Masepohl B. J Bacteriol 191 5205-5215 (2009)
  16. The solution structure of the C-terminal domain of NfeD reveals a novel membrane-anchored OB-fold. Kuwahara Y, Ohno A, Morii T, Yokoyama H, Matsui I, Tochio H, Shirakawa M, Hiroaki H. Protein Sci 17 1915-1924 (2008)
  17. The molybdate binding protein Mop from Haemophilus influenzae--biochemical and thermodynamic characterisation. Masters SL, Howlett GJ, Pau RN. Arch Biochem Biophys 439 105-112 (2005)
  18. Exploring dynamics of molybdate in living animal cells by a genetically encoded FRET nanosensor. Nakanishi Y, Iida S, Ueoka-Nakanishi H, Niimi T, Tomioka R, Maeshima M. PLoS One 8 e58175 (2013)
  19. Solution structural studies of molybdate-nucleotide polyanions. Hill LM, George GN, Duhme-Klair AK, Young CG. J Inorg Biochem 88 274-283 (2002)
  20. The Molybdenum Storage Protein: A soluble ATP hydrolysis-dependent molybdate pump. Poppe J, Brünle S, Hail R, Wiesemann K, Schneider K, Ermler U. FEBS J 285 4602-4616 (2018)
  21. Transcriptional analysis of the adaptation of Ustilago maydis during growth under nitrogen fixation conditions. Sánchez-Arreguin JA, Hernandez-Oñate MA, León-Ramirez CG, Ruiz-Herrera J. J Basic Microbiol 57 597-604 (2017)
  22. Crystal structure of a monomeric thiolase-like protein type 1 (TLP1) from Mycobacterium smegmatis. Janardan N, Harijan RK, Wierenga RK, Murthy MR. PLoS One 7 e41894 (2012)


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