SAXS reveals highly flexible interdomain linkers of tandem acyl carrier protein-thioesterase domains from a fungal nonreducing polyketide synthase.


Journal

FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157

Informations de publication

Date de publication:
01 2021
Historique:
received: 28 05 2020
revised: 01 10 2020
accepted: 05 10 2020
pubmed: 13 10 2020
medline: 8 7 2021
entrez: 12 10 2020
Statut: ppublish

Résumé

Menisporopsin A is a fungal bioactive macrocyclic polylactone, the biosynthesis of which requires only reducing (R) and nonreducing (NR) polyketide synthases (PKSs) to guide a series of esterification and cyclolactonization reactions. There is no structural information pertaining to these PKSs. Here, we report the solution characterization of singlet and doublet acyl carrier protein (ACP

Identifiants

pubmed: 33043457
doi: 10.1002/1873-3468.13954
doi:

Substances chimiques

Acyl Carrier Protein 0
Macrolides 0
menisporopsin A 0
Polyketide Synthases 79956-01-7
Thiolester Hydrolases EC 3.1.2.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

133-144

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L01386X/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/T001968/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/OS/GC/000004
Pays : United Kingdom

Informations de copyright

© 2020 Federation of European Biochemical Societies.

Références

Chinworrungsee M, Kittakoop P, Isaka M, Maithip P, Supothina S and Thebtaranonth Y (2004) Isolation and structure elucidation of a novel antimalarial macrocyclic polylactone, menisporopsin A, from the fungus Menisporopsis theobromae. J Nat Prod 67, 689-692.
Wattana-amorn P, Juthaphan P, Sirikamonsil M, Sriboonlert A, Simpson TJ and Kongkathip N (2013) Biosynthetic origins of menisporopsin A. J Nat Prod 76, 1235-1237.
Bunnak W, Wonnapinij P, Sriboonlert A, Lazarus CM and Wattana-Amorn P (2019) Heterologous biosynthesis of a fungal macrocyclic polylactone requires only two iterative polyketide synthases. Org Biomol Chem 17, 374-379.
Takano Y, Kubo Y, Shimizu K, Mise K, Okuno T and Furusawa I (1995) Structural analysis of PKS1, a polyketide synthase gene involved in melanin biosynthesis in Colletotrichum lagenarium. Mol Gen Genet 249, 162-167.
Mayorga ME and Timberlake WE (1992) The developmentally regulated Aspergillus nidulans wA gene encodes a polypeptide homologous to polyketide and fatty acid synthases. Mol Gen Genet 235, 205-212.
Yu JH and Leonard TJ (1995) Sterigmatocystin biosynthesis in Aspergillus nidulans requires a novel type I polyketide synthase. J Bacteriol 177, 4792-4800.
Crawford JM, Korman TP, Labonte JW, Vagstad AL, Hill EA, Kamari-Bidkorpeh O, Tsai SC and Townsend CA (2009) Structural basis for biosynthetic programming of fungal aromatic polyketide cyclization. Nature 461, 1139-1143.
Wattana-amorn P, Williams C, Ploskon E, Cox RJ, Simpson TJ, Crosby J and Crump MP (2010) Solution structure of an acyl carrier protein domain from a fungal type I polyketide synthase. Biochemistry 49, 2186-2193.
Korman TP, Crawford JM, Labonte JW, Newman AG, Wong J, Townsend CA and Tsai SC (2010) Structure and function of an iterative polyketide synthase thioesterase domain catalyzing Claisen cyclization in aflatoxin biosynthesis. Proc Natl Acad Sci U S A 107, 6246-6251.
Edwards AL, Matsui T, Weiss TM and Khosla C (2014) Architectures of whole-module and bimodular proteins from the 6-deoxyerythronolide B synthase. J Mol Biol 426, 2229-2245.
Davison J, Dorival J, Rabeharindranto H, Mazon H, Chagot B, Gruez A and Weissman KJ (2014) Insights into the function of trans-acyl transferase polyketide synthases from the SAXS structure of a complete module. Chem Sci 5, 3081-3095.
Frueh DP, Arthanari H, Koglin A, Vosburg DA, Bennett AE, Walsh CT and Wagner G (2008) Dynamic thiolation-thioesterase structure of a non-ribosomal peptide synthetase. Nature 454, 903-906.
Drake EJ, Miller BR, Shi C, Tarrasch JT, Sundlov JA, Allen CL, Skiniotis G, Aldrich CC and Gulick AM (2016) Structures of two distinct conformations of holo-non-ribosomal peptide synthetases. Nature 529, 235-238.
Berrow NS, Alderton D, Sainsbury S, Nettleship J, Assenberg R, Rahman N, Stuart DI and Owens RJ (2007) A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic Acids Res 35, e45.
Lobley A, Whitmore L and Wallace BA (2002) DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18, 211-212.
Whitmore L and Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32, W668-W673.
Whitmore L and Wallace BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89, 392-400.
Provencher SW and Glockner J (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20, 33-37.
van Stokkum IH, Spoelder HJ, Bloemendal M, van Grondelle R and Groen FC (1990) Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal Biochem 191, 110-118.
Lees JG, Miles AJ, Wien F and Wallace BA (2006) A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 22, 1955-1962.
Micsonai A, Wien F, Kernya L, Lee YH, Goto Y, Refregiers M and Kardos J (2015) Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy. Proc Natl Acad Sci U S A 112, E3095-E3103.
Micsonai A, Wien F, Bulyaki E, Kun J, Moussong E, Lee YH, Goto Y, Refregiers M and Kardos J (2018) BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra. Nucleic Acids Res 46, W315-W322.
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinform 9, 40.
Roy A, Kucukural A and Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5, 725-738.
Yang J, Yan R, Roy A, Xu D, Poisson J and Zhang Y (2015) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12, 7-8.
Zhou X, Hu J, Zhang C, Zhang G and Zhang Y (2019) Assembling multidomain protein structures through analogous global structural alignments. Proc Natl Acad Sci U S A 116, 15930-15938.
Slabinski L, Jaroszewski L, Rychlewski L, Wilson IA, Lesley SA and Godzik A (2007) XtalPred: a web server for prediction of protein crystallizability. Bioinformatics 23, 3403-3405.
Wootton JC and Federhen S (1993) Statistics of local complexity in amino acid sequences and sequence databases. Comput Chem 17, 149-163.
Emsley P, Lohkamp B, Scott WG and Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66, 486-501.
Trewhella J, Duff AP, Durand D, Gabel F, Guss JM, Hendrickson WA, Hura GL, Jacques DA, Kirby NM, Kwan AH et al, (2017) 2017 publication guidelines for structural modelling of small-angle scattering data from biomolecules in solution: an update. Acta Crystallogr D Struct Biol 73, 710-728.
https://bl1231.als.lbl.gov/scatter/.
Petoukhov MV, Franke D, Shkumatov AV, Tria G, Kikhney AG, Gajda M, Gorba C, Mertens HD, Konarev PV and Svergun DI (2012) New developments in the ATSAS program package for small-angle scattering data analysis. J Appl Crystallogr 45, 342-350.
Franke D and Svergun DI (2009) DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J Appl Crystallogr 42, 342-346.
Volkov VV and Svergun DI (2003) Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 36, 860-864.
Svergun DI (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76, 2879-2886.
Kozin MB and Svergun DI (2001) Automated matching of high- and low-resolution structural models. J Appl Cryst 34, 33-41.
Bernado P, Mylonas E, Petoukhov MV, Blackledge M and Svergun DI (2007) Structural characterization of flexible proteins using small-angle X-ray scattering. J Am Chem Soc 129, 5656-5664.
Tria G, Mertens HDT, Kachala M and Svergun DI (2015) Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering. Iucrj 2, 207-217.
Ferrer M, Chernikova TN, Yakimov MM, Golyshin PN and Timmis KN (2003) Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21, 1266-1267.
Quadri LE, Weinreb PH, Lei M, Nakano MM, Zuber P and Walsh CT (1998) Characterization of Sfp, a Bacillus subtilis phosphopantetheinyl transferase for peptidyl carrier protein domains in peptide synthetases. Biochemistry 37, 1585-1595.
Mootz HD, Finking R and Marahiel MA (2001) 4'-phosphopantetheine transfer in primary and secondary metabolism of Bacillus subtilis. J Biol Chem 276, 37289-37298.
Geoghegan KF, Dixon HB, Rosner PJ, Hoth LR, Lanzetti AJ, Borzilleri KA, Marr ES, Pezzullo LH, Martin LB, LeMotte PK et al, (1999) Spontaneous alpha-N-6-phosphogluconoylation of a "His tag" in Escherichia coli: the cause of extra mass of 258 or 178 Da in fusion proteins. Anal Biochem 267, 169-184.
Crosby J, Sherman DH, Bibb MJ, Revill WP, Hopwood DA and Simpson TJ (1995) Polyketide synthase acyl carrier proteins from Streptomyces: expression in Escherichia coli, purification and partial characterisation. Biochim Biophys Acta 1251, 32-42.
Crump MP, Crosby J, Dempsey CE, Parkinson JA, Murray M, Hopwood DA and Simpson TJ (1997) Solution structure of the actinorhodin polyketide synthase acyl carrier protein from Streptomyces coelicolor A3(2). Biochemistry 36, 6000-6008.
Xu GY, Tam A, Lin L, Hixon J, Fritz CC and Powers R (2001) Solution structure of B. subtilis acyl carrier protein. Structure. 9, 277-287.
Wong HC, Liu G, Zhang YM, Rock CO and Zheng J (2002) The solution structure of acyl carrier protein from Mycobacterium tuberculosis. J Biol Chem 277, 15874-15880.
Kim Y, Kovrigin EL and Eletr Z (2006) NMR studies of Escherichia coli acyl carrier protein: dynamic and structural differences of the apo- and holo-forms. Biochem Biophys Res Commun 341, 776-783.
Evans SE, Williams C, Arthur CJ, Burston SG, Simpson TJ, Crosby J and Crump MP (2008) An ACP structural switch: conformational differences between the apo and holo forms of the actinorhodin polyketide synthase acyl carrier protein. ChemBioChem 9, 2424-2432.
Piiadov V, Ares de Araujo E, Oliveira Neto M, Craievich AF and Polikarpov I (2019) SAXSMoW 2.0: Online calculator of the molecular weight of proteins in dilute solution from experimental SAXS data measured on a relative scale. Protein Sci 28, 454-463.
Franke D, Petoukhov MV, Konarev PV, Panjkovich A, Tuukkanen A, Mertens HDT, Kikhney AG, Hajizadeh NR, Franklin JM, Jeffries CM and et al, (2017) ATSAS 2.8: a comprehensive data analysis suite for small-angle scattering from macromolecular solutions. J Appl Crystallogr 50, 1212-1225.
Wang Z, Bagde SR, Zavala G, Matsui T, Chen X and Kim CY (2018) De novo design and implementation of a tandem acyl carrier protein domain in a type I modular polyketide synthase. ACS Chem Biol 13, 3072-3077.
Kikhney AG and Svergun DI (2015) A practical guide to small angle X-ray scattering (SAXS) of flexible and intrinsically disordered proteins. FEBS Lett 589, 2570-2577.
Tran L, Broadhurst RW, Tosin M, Cavalli A and Weissman KJ (2010) Insights into protein-protein and enzyme-substrate interactions in modular polyketide synthases. Chem Biol 17, 705-716.
Nguyen C, Haushalter RW, Lee DJ, Markwick PRL, Bruegger J, Caldara-Festin G, Finzel K, Jackson DR, Ishikawa F, O'Dowd B et al. (2014) Trapping the dynamic acyl carrier protein in fatty acid biosynthesis. Nature 505, 427-431.
Barajas JF, Finzel K, Valentic TR, Shakya G, Gamarra N, Martinez D, Meier JL, Vagstad AL, Newman AG, Townsend CA et al. (2016) Structural and biochemical analysis of protein-protein interactions between the acyl-carrier protein and product template domain. Angew Chem Int Edit 55, 13005-13009.
Thiele GAR, Friedman CP, Tsai KJS, Beld J, Londergan CH and Charkoudian LK (2017) Acyl carrier protein cyanylation delivers a ketoacyl synthase-carrier protein cross-link. Biochemistry 56, 2533-2536.

Auteurs

Waraporn Bunnak (W)

Department of Chemistry, Special Research Unit for Advanced Magnetic Resonance, Center of Excellence for Innovation in Chemistry, Faculty of Science, Kasetsart University, Bangkok, Thailand.

Ashley J Winter (AJ)

School of Chemistry, University of Bristol, UK.

Colin M Lazarus (CM)

School of Biological Sciences, University of Bristol, UK.

Matthew P Crump (MP)

School of Chemistry, University of Bristol, UK.

Paul R Race (PR)

School of Biochemistry, University of Bristol, UK.
BrisSynBio Synthetic Biology Research Centre, University of Bristol, UK.

Pakorn Wattana-Amorn (P)

Department of Chemistry, Special Research Unit for Advanced Magnetic Resonance, Center of Excellence for Innovation in Chemistry, Faculty of Science, Kasetsart University, Bangkok, Thailand.

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