Is allostery a fuzzy concept?
KNF model
MWC model
allostery
arginine repressor
phosphoglycerate dehydrogenase
uracil phosphoribosyltransferase
Journal
FEBS open bio
ISSN: 2211-5463
Titre abrégé: FEBS Open Bio
Pays: England
ID NLM: 101580716
Informations de publication
Date de publication:
23 May 2024
23 May 2024
Historique:
revised:
30
01
2024
received:
17
11
2023
accepted:
11
03
2024
medline:
24
5
2024
pubmed:
24
5
2024
entrez:
24
5
2024
Statut:
aheadofprint
Résumé
Allostery is an important property of biological macromolecules which regulates diverse biological functions such as catalysis, signal transduction, transport, and molecular recognition. However, the concept was expressed using two different definitions by J. Monod and, over time, more have been added by different authors, making it fuzzy. Here, we reviewed the different meanings of allostery in the current literature and found that it has been used to indicate that the function of a protein is regulated by heterotropic ligands, and/or that the binding of ligands and substrates presents homotropic positive or negative cooperativity, whatever the hypothesized or demonstrated reaction mechanism might be. Thus, proteins defined to be allosteric include not only those that obey the two-state concerted model, but also those that obey different reaction mechanisms such as ligand-induced fit, possibly coupled to sequential structure changes, and ligand-linked dissociation-association. Since each reaction mechanism requires its own mathematical description and is defined by it, there are many possible 'allosteries'. This lack of clarity is made even fuzzier by the fact that the reaction mechanism is often assigned imprecisely and/or implicitly in the absence of the necessary experimental evidence. In this review, we examine a list of proteins that have been defined to be allosteric and attempt to assign a reaction mechanism to as many as possible.
Identifiants
pubmed: 38783588
doi: 10.1002/2211-5463.13794
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ministero dell'Istruzione e del Merito
ID : 2017483NH8_05
Organisme : Regione Lazio
ID : A0375-2020-365
Informations de copyright
© 2024 The Authors. FEBS Open Bio published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Monod J, Changeux JP and Jacob F (1963) Allosteric proteins and cellular control systems. J Mol Biol 6, 306–329.
Monod J, Wyman J and Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12, 88–118.
Minton AP and Imai K (1974) The three‐state model: a minimal allosteric description of homotropic and heterotropic effects in the binding of ligands to hemoglobin. Proc Natl Acad Sci USA 71, 1418–1421.
Szabo A and Karplus M (1972) A mathematical model for structure‐function relations in hemoglobin. J Mol Biol 72, 163–197.
Di Cera E, Robert CH and Gill SJ (1987) Allosteric interpretation of the oxygen‐binding reaction of human hemoglobin tetramers. Biochemistry 26, 4003–4008.
Gill SJ, Robert CH, Coletta M, Di Cera E and Brunori M (1986) Cooperative free energies for nested allosteric models as applied to human hemoglobin. Biophys J 50, 747–752.
Ackers GK, Doyle ML, Myers D and Daugherty MA (1992) Molecular code for cooperativity in hemoglobin. Science 255, 54–63.
Viappiani C, Abbruzzetti S, Ronda L, Bettati S, Henry ER, Mozzarelli A and Eaton WA (2014) Experimental basis for a new allosteric model for multisubunit proteins. Proc Natl Acad Sci USA 111, 12758–12763.
Yonetani T, Park SI, Tsuneshige A, Imai K and Kanaori K (2002) Global allostery model of hemoglobin. Modulation of O2 affinity, cooperativity, and Bohr effect by heterotropic allosteric effectors. J Biol Chem 277, 34508–34520.
Pauling L (1935) The oxygen equilibrium of hemoglobin and its structural interpretation. Proc Natl Acad Sci USA 21, 186–191.
Koshland DE Jr, Némethy G and Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365–385.
Saccoccia F and Bellelli A (2020) Ligand‐linked association‐dissociation in transport proteins and hormone receptors. Curr Protein Pept Sci 21, 993–1010.
Morea V, Angelucci F, Tame JRH, Di Cera E and Bellelli A (2022) Structural basis of sequential and concerted cooperativity. Biomolecules 12, 1651.
Daily MD and Gray JJ (2009) Allosteric communication occurs via networks of tertiary and quaternary motions in proteins. PLoS Comput Biol 5, e1000293.
Bellelli A (2010) Hemoglobin and cooperativity: experiments and theories. Curr Protein Pept Sci 11, 2–36.
Horjales E, Altamirano MM, Calcagno ML, Garratt RC and Oliva G (1999) The allosteric transition of glucosamine‐6‐phosphate deaminase: the structure of the T state at 2.3 a resolution. Structure 7, 527–537.
Oliva G, Fontes MR, Garratt RC, Altamirano MM, Calcagno ML and Horjales E (1995) Structure and catalytic mechanism of glucosamine 6‐phosphate deaminase from Escherichia coli at 2.1 a resolution. Structure 3, 1323–1332.
Strater N, Hakansson K, Schnappauf G, Braus G and Lipscomb WN (1996) Crystal structure of the T state of allosteric yeast chorismate mutase and comparison with the R state. Proc Natl Acad Sci USA 93, 3330–3334.
Spraggon G, Kim C, Nguyen‐Huu X, Yee MC, Yanofsky C and Mills SE (2001) The structures of anthranilate synthase of Serratia marcescens crystallized in the presence of (i) its substrates, chorismate and glutamine, and a product, glutamate, and (ii) its end‐product inhibitor, L‐tryptophan. Proc Natl Acad Sci USA 98, 6021–6026.
Tao X, Yang Z and Tong L (2003) Crystal structures of substrate complexes of malic enzyme and insights into the catalytic mechanism. Structure 11, 1141–1150.
Sauer LA (1973) Mitochondrial NAD‐dependent malic enzyme: a new regulatory enzyme. FEBS Lett 33, 251–255.
Xu Y, Bhargava G, Wu H, Loeber G and Tong L (1999) Crystal structure of human mitochondrial NAD(P)+‐dependent malic enzyme: a new class of oxidative decarboxylases. Structure 7, 877–889.
Arai K, Ishimitsu T, Fushinobu S, Uchikoba H, Matsuzawa H and Taguchi H (2010) Active and inactive state structures of unliganded Lactobacillus casei allosteric L‐lactate dehydrogenase. Proteins 78, 681–694.
Park S, Meyer M, Jones AD, Yennawar HP, Yennawar NH and Nixon BT (2002) Two‐component signaling in the AAA + ATPase DctD: binding Mg2+ and BeF3− selects between alternate dimeric states of the receiver domain. FASEB J 16, 1964–1966.
Schuller DJ, Grant GA and Banaszak LJ (1995) The allosteric ligand site in the Vmax‐type cooperative enzyme phosphoglycerate dehydrogenase. Nat Struct Biol 2, 69–76.
Thompson JR, Bell JK, Bratt J, Grant GA and Banaszak LJ (2005) Vmax regulation through domain and subunit changes. The active form of phosphoglycerate dehydrogenase. Biochemistry 44, 5763–5773.
Van Duyne GD, Ghosh G, Maas WK and Sigler PB (1996) Structure of the oligomerization and L‐arginine binding domain of the arginine repressor of Escherichia coli. J Mol Biol 256, 377–391.
Jin L, Xue WF, Fukayama JW, Yetter J, Pickering M and Carey J (2005) Asymmetric allosteric activation of the symmetric ArgR hexamer. J Mol Biol 346, 43–56.
Furukawa N, Miyanaga A, Nakajima M and Taguchi H (2018) Structural basis of sequential allosteric transitions in tetrameric d‐lactate dehydrogenases from three gram‐negative bacteria. Biochemistry 57, 5388–5406.
Jensen KF, Arent S, Larsen S and Schack L (2005) Allosteric properties of the GTP activated and CTP inhibited uracil phosphoribosyltransferase from the thermoacidophilic archaeon Sulfolobus solfataricus. FEBS J 272, 1440–1453.
Arent S, Harris P, Jensen KF and Larsen S (2005) Allosteric regulation and communication between subunits in uracil phosphoribosyltransferase from Sulfolobus solfataricus. Biochemistry 44, 883–892.
Staub M and Dénes G (1969) Purification and properties of the 3‐deoxy‐D‐arabino‐ heptulosonate‐7‐phosphate synthase (phenylalanine sensitive) of Escherichia coli K12. I. Purification of enzyme and some of its catalytic properties. Biochim Biophys Acta 178, 588–598.
Staub M and Dénes G (1969) Purification and properties of the 3‐deoxy‐D‐arabino‐ heptulosonate‐7‐phosphate synthase (phenylalanine sensitive) of Escherichia coli K12. II. Inhibition of activity of the enzyme with phenylalanine and functional group‐specific reagents. Biochim Biophys Acta 178, 599–608.
Shumilin IA, Zhao C, Bauerle R and Kretsinger RH (2002) Allosteric inhibition of 3‐deoxy‐D‐arabino‐heptulosonate‐7‐phosphate synthase alters the coordination of both substrates. J Mol Biol 320, 1147–1156.
Rafferty JB, Somers WS, Saint‐Girons I and Phillips SE (1989) Three‐dimensional crystal structures of Escherichia coli met repressor with and without corepressor. Nature 341, 705–710.
Anderson AC, O'Neil RH, DeLano WL and Stroud RM (1999) The structural mechanism for half‐the‐sites reactivity in an enzyme, thymidylate synthase, involves a relay of changes between subunits. Biochemistry 38, 13829–13836.
Schumacher MA, Choi KY, Lu F, Zalkin H and Brennan RG (1995) Mechanism of corepressor‐mediated specific DNA binding by the purine repressor. Cell 83, 147–155.
Schumacher MA, Glasfeld A, Zalkin H and Brennan RG (1997) The X‐ray structure of the PurR‐guanine‐purF operator complex reveals the contributions of complementary electrostatic surfaces and a water‐mediated hydrogen bond to corepressor specificity and binding affinity. J Biol Chem 272, 22648–22653.
Hinrichs W, Kisker C, Düvel M, Müller A, Tovar K, Hillen W and Saenger W (1994) Structure of the Tet repressor‐tetracycline complex and regulation of antibiotic resistance. Science 264, 418–420.
Choe JY, Fromm HJ and Honzatko RB (2000) Crystal structures of fructose 1,6‐bisphosphatase: mechanism of catalysis and allosteric inhibition revealed in product complexes. Biochemistry 39, 8565–8574.
Amor JC, Harrison DH, Kahn RA and Ringe D (1994) Structure of the human ADP‐ribosylation factor 1 complexed with GDP. Nature 372, 704–708.
Maita N, Hatakeyama K, Okada K and Hakoshima T (2004) Structural basis of biopterin‐induced inhibition of GTP cyclohydrolase I by GFRP, its feedback regulatory protein. J Biol Chem 279, 51534–51540.
Sixma TK, Pronk SE, Kalk KH, van Zanten BA, Berghuis AM and Hol WG (1992) Lactose binding to heat‐labile enterotoxin revealed by X‐ray crystallography. Nature 355, 561–564.
Matković‐Calogović D, Loregian A, D'Acunto MR, Battistutta R, Tossi A, Palù G and Zanotti G (1999) Crystal structure of the B subunit of Escherichia coli heat‐labile enterotoxin carrying peptides with anti‐herpes simplex virus type 1 activity. J Biol Chem 274, 8764–8769.
MacRae IJ, Segel IH and Fisher AJ (2002) Allosteric inhibition via R‐state destabilization in ATP sulfurylase from Penicillium chrysogenum. Nat Struct Biol 9, 945–949.
Soisson SM, MacDougall‐Shackleton B, Schleif R and Wolberger C (1997) Structural basis for ligand‐regulated oligomerization of AraC. Science 276, 421–425.
Weldon JE, Rodgers ME, Larkin C and Schleif RF (2007) Structure and properties of a truly apo form of AraC dimerization domain. Proteins 66, 646–654.
Pasqualato S, Senic‐Matuglia F, Renault L, Goud B, Salamero J and Cherfils J (2004) The structural GDP/GTP cycle of Rab11 reveals a novel interface involved in the dynamics of recycling endosomes. J Biol Chem 279, 11480–11488.
Munshi S, Hall DL, Kornienko M, Darke PL and Kuo LC (2003) Structure of apo, unactivated insulin‐like growth factor‐1 receptor kinase at 1.5 a resolution. Acta Crystallogr D Biol Crystallogr 59, 1725–1730.
Favelyukis S, Till JH, Hubbard SR and Miller WT (2001) Structure and autoregulation of the insulin‐like growth factor 1 receptor kinase. Nat Struct Biol 8, 1058–1063.
Weaver LH, Kwon K, Beckett D and Matthews BW (2001) Corepressor‐induced organization and assembly of the biotin repressor: a model for allosteric activation of a transcriptional regulator. Proc Natl Acad Sci USA 98, 6045–6050.
Wilson KP, Shewchuk LM, Brennan RG, Otsuka AJ and Matthews BW (1992) Escherichia coli biotin holoenzyme synthetase/bio repressor crystal structure delineates the biotin‐ and DNA‐binding domains. Proc Natl Acad Sci USA 89, 9257–9261.
Hubbard SR, Wei L, Ellis L and Hendrickson WA (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372, 746–754.
Cho Y, Sharma V and Sacchettini JC (2003) Crystal structure of ATP phosphoribosyltransferase from Mycobacterium tuberculosis. J Biol Chem 278, 8333–8339.
Friedman AM, Fischmann TO and Steitz TA (1995) Crystal structure of lac repressor core tetramer and its implications for DNA looping. Science 268, 1721–1727.
Bell CE and Lewis M (2000) A closer view of the conformation of the lac repressor bound to operator. Nat Struct Biol 7, 209–214.
Birck C, Mourey L, Gouet P, Fabry B, Schumacher J, Rousseau P, Kahn D and Samama JP (1999) Conformational changes induced by phosphorylation of the FixJ receiver domain. Structure 7, 1505–1515.
Gouet P, Fabry B, Guillet V, Birck C, Mourey L, Kahn D and Samama JP (1999) Structural transitions in the FixJ receiver domain. Structure 7, 1517–1526.
Choi H, Kim S, Mukhopadhyay P, Cho S, Woo J, Storz G and Ryu SE (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105, 103–113.
Volz K and Matsumura P (1991) Crystal structure of Escherichia coli CheY refined at 1.7‐a resolution. J Biol Chem 266, 15511–15519.
Yang J, Cron P, Thompson V, Good VM, Hess D, Hemmings BA and Barford D (2002) Molecular mechanism for the regulation of protein kinase B/Akt by hydrophobic motif phosphorylation. Mol Cell 9, 1227–1240.
Seavers PR, Lewis RJ, Brannigan JA, Verschueren KH, Murshudov GN and Wilkinson AJ (2001) Structure of the Bacillus cell fate determinant SpoIIAA in phosphorylated and unphosphorylated forms. Structure 9, 605–614.
Hardy JA, Lam J, Nguyen JT, O'Brien T and Wells JA (2004) Discovery of an allosteric site in the caspases. Proc Natl Acad Sci USA 101, 12461–12466.
Zhang F, Strand A, Robbins D, Cobb MH and Goldsmith EJ (1994) Atomic structure of the MAP kinase ERK2 at 2.3 a resolution. Nature 367, 704–711.
Canagarajah BJ, Khokhlatchev A, Cobb MH and Goldsmith EJ (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90, 859–869.
Vetter IR, Arndt A, Kutay U, Görlich D and Wittinghofer A (1999) Structural view of the ran‐importin beta interaction at 2.3 a resolution. Cell 97, 635–646.
Milburn MV, Tong L, deVos AM, Brünger A, Yamaizumi Z, Nishimura S and Kim SH (1990) Molecular switch for signal transduction: structural differences between active and inactive forms of protooncogenic ras proteins. Science 247, 939–945.
Garrard SM, Capaldo CT, Gao L, Rosen MK, Macara IG and Tomchick DR (2003) Structure of Cdc42 in a complex with the GTPase‐binding domain of the cell polarity protein, Par6. EMBO J 22, 1125–1133.
Grizot S, Fauré J, Fieschi F, Vignais PV, Dagher MC and Pebay‐Peyroula E (2001) Crystal structure of the Rac1‐RhoGDI complex involved in NADPH oxidase activation. Biochemistry 40, 10007–10013.
Puius YA, Zhao Y, Sullivan M, Lawrence DS, Almo SC and Zhang ZY (1997) Identification of a second aryl phosphate‐binding site in protein‐tyrosine phosphatase 1B: a paradigm for inhibitor design. Proc Natl Acad Sci USA 94, 13420–13425.
Wiesmann C, Barr KJ, Kung J, Zhu J, Erlanson DA, Shen W, Fahr BJ, Zhong M, Taylor L, Randal M et al. (2004) Allosteric inhibition of protein tyrosine phosphatase 1B. Nat Struct Mol Biol 11, 730–737.
Stroupe C and Brunger AT (2000) Crystal structures of a Rab protein in its inactive and active conformations. J Mol Biol 304, 585–598.
Yu Y, Li S, Xu X, Li Y, Guan K, Arnold E and Ding J (2005) Structural basis for the unique biological function of small GTPase RHEB. J Biol Chem 280, 17093–17100.
Kjeldgaard M, Nissen P, Thirup S and Nyborg J (1993) The crystal structure of elongation factor EF‐Tu from Thermus aquaticus in the GTP conformation. Structure 1, 35–50.
Polekhina G, Thirup S, Kjeldgaard M, Nissen P, Lippmann C and Nyborg J (1996) Helix unwinding in the effector region of elongation factor EF‐Tu‐GDP. Structure 4, 1141–1151.
Constantinescu AT, Rak A, Alexandrov K, Esters H, Goody RS and Scheidig AJ (2002) Rab‐subfamily‐specific regions of Ypt7p are structurally different from other RabGTPases. Structure 10, 569–579.
Cherfils J, Ménétrey J, Le Bras G, Janoueix‐Lerosey I, de Gunzburg J, Garel JR and Auzat I (1997) Crystal structures of the small G protein Rap2A in complex with its substrate GTP, with GDP and with GTPgammaS. EMBO J 16, 5582–5591.
Ruzheinikov SN, Das SK, Sedelnikova SE, Baker PJ, Artymiuk PJ, García‐Lara J, Foster SJ and Rice DW (2004) Analysis of the open and closed conformations of the GTP‐binding protein YsxC from Bacillus subtilis. J Mol Biol 339, 265–278.
Pasqualato S, Ménétrey J, Franco M and Cherfils J (2001) The structural GDP/GTP cycle of human Arf6. EMBO Rep 2, 234–238.
Lambright DG, Noel JP, Hamm HE and Sigler PB (1994) Structural determinants for activation of the alpha‐subunit of a heterotrimeric G protein. Nature 369, 621–628.
Noel JP, Hamm HE and Sigler PB (1993) The 2.2 a crystal structure of transducin‐alpha complexed with GTP gamma S. Nature 366, 654–663.
Rak A, Pylypenko O, Niculae A, Pyatkov K, Goody RS and Alexandrov K (2004) Structure of the Rab7:REP‐1 complex: insights into the mechanism of Rab prenylation and choroideremia disease. Cell 117, 749–760.
Wei Y, Zhang Y, Derewenda U, Liu X, Minor W, Nakamoto RK, Somlyo AV, Somlyo AP and Derewenda ZS (1997) Crystal structure of RhoA‐GDP and its functional implications. Nat Struct Biol 4, 699–703.
Ihara K, Muraguchi S, Kato M, Shimizu T, Shirakawa M, Kuroda S, Kaibuchi K and Hakoshima T (1998) Crystal structure of human RhoA in a dominantly active form complexed with a GTP analogue. J Biol Chem 273, 9656–9666.
Coleman DE, Lee E, Mixon MB, Linder ME, Berghuis AM, Gilman AG and Sprang SR (1994) Crystallization and preliminary crystallographic studies of Gi alpha 1 and mutants of Gi alpha 1 in the GTP and GDP‐bound states. J Mol Biol 238, 630–634.
Mixon MB, Lee E, Coleman DE, Berghuis AM, Gilman AG and Sprang SR (1995) Tertiary and quaternary structural changes in Gi alpha 1 induced by GTP hydrolysis. Science 270, 954–960.
Wyman J (1948) Heme proteins. Adv Protein Chem 4, 407–531.
Wyman J (1964) Linked functions and reciprocal effects in hemoglobin: a second look. Adv Protein Chem 19, 223–286.
Bellelli A and Carey J (2018) Reversible Ligand Binding: Theory and Experiment. Wiley, Oxford, UK.
Bellelli A and Brunori M (1994) Optical measurements of quaternary structural changes in hemoglobin. Methods Enzymol 232, 56–71.
Schirmer T and Evans PR (1990) Structural basis of the allosteric behaviour of phosphofructokinase. Nature 343, 140–145.
Winicov I and Pizer LI (1974) The mechanism of end product inhibition of serine biosynthesis. IV. Subunit structure of phosphoglycerate dehydrogenase and steady state kinetic studies of phosphoglycerate oxidation. J Biol Chem 249, 1348–1355.
Grant GA, Xu XL, Hu Z and Purvis AR (1999) Phosphate ion partially relieves the cooperativity of effector binding in D‐3‐phosphoglycerate dehydrogenase without altering the cooperativity of inhibition. Biochemistry 38, 16548–16552.
Changeux JP (2012) Allostery and the Monod‐Wyman‐Changeux model after 50 years. Annu Rev Biophys 41, 103–133.
Ansari A, Berendzen J, Bowne SF, Frauenfelder H, Iben IE, Sauke TB, Shyamsunder E and Young RD (1985) Protein states and proteinquakes. Proc Natl Acad Sci USA 82, 5000–5004.
Chi CN, Bach A, Engstrom A, Wang H, Strømgaard K, Gianni S and Jemth P (2009) A sequential binding mechanism in a PDZ domain. Biochemistry 48, 7089–7097.
Hammes GG, Chang YC and Oas TG (2009) Conformational selection or induced fit: a flux description of reaction mechanism. Proc Natl Acad Sci USA 106, 13737–13741.
Changeux JP and Edelstein SJ (2011) Conformational selection or induced fit? 50 years of debate resolved. F1000 Biol Rep 3, 19.
Cui Q and Karplus M (2008) Allostery and cooperativity revised. Protein Sci 17, 1295–1307.
Hilser VJ, Wrabl OJ and Motlagh HN (2012) Structural and energetic basis of Allostery. Annu Rev Biophys 41, 585–609.
Gunasekaran K, Ma B and Nussinov R (2004) Allostery is an intrinsic property of all dynamic proteins. Proteins 57, 433–443.