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An intramolecular switch regulates phosphoindependent FHA domain interactions in Mycobacterium tuberculosis.

Nott TJ, Kelly G, Stach L, Li J, Westcott S, Patel D, Hunt DM, Howell S, Buxton RS, O'Hare HM, Smerdon SJ
Sci Signal 2 ra12 (2009)
Cited: 50 times
EuropePMC logo PMID: 19318624

Abstract

Forkhead-associated (FHA) domains have gained considerable prominence as ubiquitous phosphothreonine-dependent binding modules; however, their precise roles in serine and threonine kinase (STK) pathways and mechanisms of regulation remain unclear. From experiments with Rv1827, an FHA domain-containing protein from Mycobacterium tuberculosis, we derived a complete molecular description of an FHA-mediated STK signaling process. First, binding of the FHA domain to each of three metabolic enzyme complexes regulated their catalytic activities but did not require priming phosphorylation. However, phosphorylation of a threonine residue within a conserved amino-terminal motif of Rv1827 triggered its intramolecular association with the FHA domain of Rv1827, thus blocking its interactions with each of the three enzymes. The solution structure of this inactivated form and further mutagenic studies showed how a previously unidentified intramolecular phosphoswitch blocked the access of the target enzymes to a common FHA interaction surface and how this shared surface accommodated three functionally related, but structurally diverse, binding partners. Thus, our data reveal an unsuspected versatility in the FHA domain that allows for the transformation of multiple kinase inputs into various downstream regulatory signals.

Reviews - 2kfu mentioned but not cited (1)

  1. Solution NMR Studies of Mycobacterium tuberculosis Proteins for Antibiotic Target Discovery. Kim DH, Kang SM, Lee BJ. Molecules 22 (2017)

Articles - 2kfu mentioned but not cited (2)

  1. Dimerization Mediated by a Divergent Forkhead-associated Domain Is Essential for the DNA Damage and Spindle Functions of Fission Yeast Mdb1. Luo S, Xin X, Du LL, Ye K, Wei Y. J Biol Chem 290 21054-21066 (2015)
  2. 3D architecture and structural flexibility revealed in the subfamily of large glutamate dehydrogenases by a mycobacterial enzyme. Lázaro M, Melero R, Huet C, López-Alonso JP, Delgado S, Dodu A, Bruch EM, Abriata LA, Alzari PM, Valle M, Lisa MN. Commun Biol 4 684 (2021)


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  1. Eukaryote-like serine/threonine kinases and phosphatases in bacteria. Pereira SF, Goss L, Dworkin J. Microbiol Mol Biol Rev 75 192-212 (2011)
  2. Division and cell envelope regulation by Ser/Thr phosphorylation: Mycobacterium shows the way. Molle V, Kremer L. Mol Microbiol 75 1064-1077 (2010)
  3. Molecular biology of drug resistance in Mycobacterium tuberculosis. Smith T, Wolff KA, Nguyen L. Curr Top Microbiol Immunol 374 53-80 (2013)
  4. Nitrogen metabolism in Mycobacterium tuberculosis physiology and virulence. Gouzy A, Poquet Y, Neyrolles O. Nat Rev Microbiol 12 729-737 (2014)
  5. Signaling mechanisms of the Mycobacterium tuberculosis receptor Ser/Thr protein kinases. Alber T. Curr Opin Struct Biol 19 650-657 (2009)
  6. Antibiotic resistance mechanisms in M. tuberculosis: an update. Nguyen L. Arch Toxicol 90 1585-1604 (2016)
  7. Regulation of transcription by eukaryotic-like serine-threonine kinases and phosphatases in Gram-positive bacterial pathogens. Wright DP, Ulijasz AT. Virulence 5 863-885 (2014)
  8. Post-translational modifications as key regulators of bacterial metabolic fluxes. Pisithkul T, Patel NM, Amador-Noguez D. Curr Opin Microbiol 24 29-37 (2015)
  9. Dbf4: the whole is greater than the sum of its parts. Matthews LA, Guarné A. Cell Cycle 12 1180-1188 (2013)
  10. FHA domains: Phosphopeptide binding and beyond. Almawi AW, Matthews LA, Guarné A. Prog Biophys Mol Biol 127 105-110 (2017)
  11. A pseudokinase debut at the mycobacterial cell wall. Warner DF, Mizrahi V. Sci Signal 5 pe3 (2012)

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  1. Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Prisic S, Dankwa S, Schwartz D, Chou MF, Locasale JW, Kang CM, Bemis G, Church GM, Steen H, Husson RN. Proc Natl Acad Sci U S A 107 7521-7526 (2010)
  2. A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Lloyd J, Chapman JR, Clapperton JA, Haire LF, Hartsuiker E, Li J, Carr AM, Jackson SP, Smerdon SJ. Cell 139 100-111 (2009)
  3. Activity-based metabolomic profiling of enzymatic function: identification of Rv1248c as a mycobacterial 2-hydroxy-3-oxoadipate synthase. de Carvalho LP, Zhao H, Dickinson CE, Arango NM, Lima CD, Fischer SM, Ouerfelli O, Nathan C, Rhee KY. Chem Biol 17 323-332 (2010)
  4. Forkhead-associated domain-containing protein Rv0019c and polyketide-associated protein PapA5, from substrates of serine/threonine protein kinase PknB to interacting proteins of Mycobacterium tuberculosis. Gupta M, Sajid A, Arora G, Tandon V, Singh Y. J Biol Chem 284 34723-34734 (2009)
  5. Effective inhibitors of the essential kinase PknB and their potential as anti-mycobacterial agents. Lougheed KE, Osborne SA, Saxty B, Whalley D, Chapman T, Bouloc N, Chugh J, Nott TJ, Patel D, Spivey VL, Kettleborough CA, Bryans JS, Taylor DL, Smerdon SJ, Buxton RS. Tuberculosis (Edinb) 91 277-286 (2011)
  6. Functional plasticity and allosteric regulation of α-ketoglutarate decarboxylase in central mycobacterial metabolism. Wagner T, Bellinzoni M, Wehenkel A, O'Hare HM, Alzari PM. Chem Biol 18 1011-1020 (2011)
  7. PknG senses amino acid availability to control metabolism and virulence of Mycobacterium tuberculosis. Rieck B, Degiacomi G, Zimmermann M, Cascioferro A, Boldrin F, Lazar-Adler NR, Bottrill AR, le Chevalier F, Frigui W, Bellinzoni M, Lisa MN, Alzari PM, Nguyen L, Brosch R, Sauer U, Manganelli R, O'Hare HM. PLoS Pathog 13 e1006399 (2017)
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  11. A biosensor for fluorescent determination of ADP with high time resolution. Kunzelmann S, Webb MR. J Biol Chem 284 33130-33138 (2009)
  12. Structural insight into the Mycobacterium tuberculosis Rv0020c protein and its interaction with the PknB kinase. Roumestand C, Leiba J, Galophe N, Margeat E, Padilla A, Bessin Y, Barthe P, Molle V, Cohen-Gonsaud M. Structure 19 1525-1534 (2011)
  13. Forkhead-associated (FHA) domain containing ABC transporter Rv1747 is positively regulated by Ser/Thr phosphorylation in Mycobacterium tuberculosis. Spivey VL, Molle V, Whalan RH, Rodgers A, Leiba J, Stach L, Walker KB, Smerdon SJ, Buxton RS. J Biol Chem 286 26198-26209 (2011)
  14. Multisystem Analysis of Mycobacterium tuberculosis Reveals Kinase-Dependent Remodeling of the Pathogen-Environment Interface. Carette X, Platig J, Young DC, Helmel M, Young AT, Wang Z, Potluri LP, Moody CS, Zeng J, Prisic S, Paulson JN, Muntel J, Madduri AVR, Velarde J, Mayfield JA, Locher C, Wang T, Quackenbush J, Rhee KY, Moody DB, Steen H, Husson RN. mBio 9 (2018)
  15. Mycobacterium tuberculosis universal stress protein Rv2623 interacts with the putative ATP binding cassette (ABC) transporter Rv1747 to regulate mycobacterial growth. Glass LN, Swapna G, Chavadi SS, Tufariello JM, Mi K, Drumm JE, Lam TT, Zhu G, Zhan C, Vilchéze C, Arcos J, Chen Y, Bi L, Mehta S, Porcelli SA, Almo SC, Yeh SR, Jacobs WR, Torrelles JB, Chan J. PLoS Pathog 13 e1006515 (2017)
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  17. Flexible nitrogen utilisation by the metabolic generalist pathogen Mycobacterium tuberculosis. Agapova A, Serafini A, Petridis M, Hunt DM, Garza-Garcia A, Sohaskey CD, de Carvalho LPS. Elife 8 (2019)
  18. Structure and interactions of the cytoplasmic domain of the Yersinia type III secretion protein YscD. Gamez A, Mukerjea R, Alayyoubi M, Ghassemian M, Ghosh P. J Bacteriol 194 5949-5958 (2012)
  19. Glutamate Dehydrogenase Is Required by Mycobacterium bovis BCG for Resistance to Cellular Stress. Gallant JL, Viljoen AJ, van Helden PD, Wiid IJ. PLoS One 11 e0147706 (2016)
  20. Influence of allosteric regulators on individual steps in the reaction catalyzed by Mycobacterium tuberculosis 2-hydroxy-3-oxoadipate synthase. Balakrishnan A, Jordan F, Nathan CF. J Biol Chem 288 21688-21702 (2013)
  21. 'AND' logic gates at work: Crystal structure of Rad53 bound to Dbf4 and Cdc7. Almawi AW, Matthews LA, Larasati, Myrox P, Boulton S, Lai C, Moraes T, Melacini G, Ghirlando R, Duncker BP, Guarné A. Sci Rep 6 34237 (2016)
  22. A novel non-canonical forkhead-associated (FHA) domain-binding interface mediates the interaction between Rad53 and Dbf4 proteins. Matthews LA, Selvaratnam R, Jones DR, Akimoto M, McConkey BJ, Melacini G, Duncker BP, Guarné A. J Biol Chem 289 2589-2599 (2014)
  23. An Aspartate-Specific Solute-Binding Protein Regulates Protein Kinase G Activity To Control Glutamate Metabolism in Mycobacteria. Bhattacharyya N, Nkumama IN, Newland-Smith Z, Lin LY, Yin W, Cullen RE, Griffiths JS, Jarvis AR, Price MJ, Chong PY, Wallis R, O'Hare HM. mBio 9 (2018)
  24. Mycobacterium tuberculosis S-adenosyl-l-homocysteine hydrolase is negatively regulated by Ser/Thr phosphorylation. Corrales RM, Leiba J, Cohen-Gonsaud M, Molle V, Kremer L. Biochem Biophys Res Commun 430 858-864 (2013)
  25. The role of glutamine oxoglutarate aminotransferase and glutamate dehydrogenase in nitrogen metabolism in Mycobacterium bovis BCG. Viljoen AJ, Kirsten CJ, Baker B, van Helden PD, Wiid IJ. PLoS One 8 e84452 (2013)
  26. Effect of lysine succinylation on the regulation of 2-oxoglutarate dehydrogenase inhibitor, OdhI, involved in glutamate production in Corynebacterium glutamicum. Komine-Abe A, Nagano-Shoji M, Kubo S, Kawasaki H, Yoshida M, Nishiyama M, Kosono S. Biosci Biotechnol Biochem 81 2130-2138 (2017)
  27. Dimerization, but not phosphothreonine binding, is conserved between the forkhead-associated domains of Drosophila MU2 and human MDC1. Luo S, Ye K. FEBS Lett 586 344-349 (2012)
  28. In vitro reconstitution and characterization of pyruvate dehydrogenase and 2-oxoglutarate dehydrogenase hybrid complex from Corynebacterium glutamicum. Kinugawa H, Kondo N, Komine-Abe A, Tomita T, Nishiyama M, Kosono S. Microbiologyopen 9 e1113 (2020)
  29. Membrane Chaperoning of a Thylakoid Protease Whose Structural Stability Is Modified by the Protonmotive Force. McKinnon LJ, Fukushima J, Endow JK, Inoue K, Theg SM. Plant Cell 32 1589-1609 (2020)
  30. Actinobacteria challenge the paradigm: A unique protein architecture for a well-known, central metabolic complex. Bruch EM, Vilela P, Yang L, Boyko A, Lexa-Sapart N, Raynal B, Alzari PM, Bellinzoni M. Proc Natl Acad Sci U S A 118 e2112107118 (2021)
  31. Structure and interactions of the archaeal motility repression module ArnA-ArnB that modulates archaellum gene expression in Sulfolobus acidocaldarius. Hoffmann L, Anders K, Bischof LF, Ye X, Reimann J, Khadouma S, Pham TK, van der Does C, Wright PC, Essen LO, Albers SV. J Biol Chem 294 7460-7471 (2019)
  32. A Tetratricopeptide Repeat Scaffold Couples Signal Detection to OdhI Phosphorylation in Metabolic Control by the Protein Kinase PknG. Lisa MN, Sogues A, Barilone N, Baumgart M, Gil M, Graña M, Durán R, Biondi RM, Bellinzoni M, Bott M, Alzari PM. mBio 12 e0171721 (2021)
  33. Cellular localization of the hybrid pyruvate/2-oxoglutarate dehydrogenase complex in the actinobacterium Corynebacterium glutamicum. Sundermeyer L, Folkerts JG, Lückel B, Mack C, Baumgart M, Bott M. Microbiol Spectr e0266823 (2023)
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  35. Probing the Highly Disparate Dual Inhibitory Mechanisms of Novel Quinazoline Derivatives against Mycobacterium tuberculosis Protein Kinases A and B. Olotu FA, Soliman ME. Molecules 25 (2020)
  36. Structure of the Mycobacterium tuberculosis cPknF and conformational changes induced in forkhead-associated regulatory domains. Cabarca S, Frazão de Souza M, Albert de Oliveira A, Vignoli Muniz GS, Lamy MT, Vinicius Dos Reis C, Takarada J, Effer B, Souza LS, Iriarte de la Torre L, Couñago R, Pinto Oliveira CL, Balan A. Curr Res Struct Biol 3 165-178 (2021)


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