The avidin-theophylline complex: A structural and computational study.
avidin complex
binding constant
crystal structure
free-energy
xanthine
Journal
Proteins
ISSN: 1097-0134
Titre abrégé: Proteins
Pays: United States
ID NLM: 8700181
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
revised:
12
05
2023
received:
04
04
2023
accepted:
30
05
2023
medline:
20
9
2023
pubmed:
15
6
2023
entrez:
15
6
2023
Statut:
ppublish
Résumé
The interaction between avidin and its counterpart biotin is one of central importance in biology and has been reproposed and studied at length. However, the binding pocket of avidin is prone to promiscuous binding, able to accommodate even non-biotinylated ligands. Comprehending the factors that distinguish the extremely strong interaction with biotin to other ligands is an important step to fully picture the thermodynamics of these low-affinity complexes. Here, we present the complex between chicken white egg avidin and theophylline (TEP), the xanthine derivative used in the therapy of asthma. In the crystal structure, TEP lies in the biotin-binding pocket with the same orientation and planarity of the aromatic ring of 8-oxodeoxyguanosine. Indeed, its affinity for avidin measured by isothermal titration calorimetry is in the same μM range as those obtained for the previously characterized nucleoside derivatives. By the use of molecular dynamic simulations, we have investigated the most important intermolecular interactions occurring in the avidin-TEP binding pocket and compared them with those obtained for the avidin 8-oxodeoxyguanosine and avidin-biotin complexes. These results testify the capability of avidin to complex purely aromatic molecules.
Substances chimiques
Avidin
1405-69-2
Biotin
6SO6U10H04
Theophylline
C137DTR5RG
Ligands
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1437-1443Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Hama Y, Urano Y, Koyama Y, et al. In vivo spectral fluorescence imaging of submillimeter peritoneal cancer implants using a lectin-targeted optical agent. Neoplasia. 2006;8(7):607-612.
Rosano C, Arosio P, Bolognesi M. The X-ray three-dimensional structure of avidin. Biomol Eng. 1999;16(1-4):5-12.
Ellison D, Hinton J, Hubbard SJ, Beynon RJ. Limited proteolysis of native proteins: the interaction between avidin and proteinase K. Protein Sci. 1995;4(7):1337-1345.
González M, Argaraña CE, Fidelio GD. Extremely high thermal stability of streptavidin and avidin upon biotin binding. Biomol Eng. 1999;16:67-72.
Green NM. Avidin.4. Stability at extremes of pH and dissociation into subunits by guanidine hydrochloride. Biochem J. 1964;89:609-620.
Ostrowska M, Bartoszewicz Z, Bednarczuk T, Walczak K, Zgliczyński W, Glinicki P. The effect of biotin interference on the results of blood hormone assays. Endokrynol Pol. 2019;70(1):102-121.
Huynh V, Wylie RG. Competitive affinity release for long-term delivery of antibodies from hydrogels. Angew Chem Int Ed Engl. 2018;57(13):3406-3410.
Ahrens L, Vonwil D, Arya N, Forget A, Shastri VP. Biotin-Avidin-mediated capture of microspheres on polymer fibers. Molecules. 2019;24(11):2036.
Shah MA, Ullah R, De March M, et al. Overexpression and characterization of the 100K protein of fowl adenovirus-4 as an antiviral target. Virus Res. 2017;238:218-225.
Neimair J, D'Ercole C, De March M, Elsner M, Seidel M, de Marco A. Macroporous epoxy-based monoliths functionalized with anti-CD63 nanobodies for effective isolation of extracellular vesicles in urine. Int J Mol Sci. 2023;24:6131-6144.
Hajdu P, Chimote AA, Thompson TH, Koo Y, Yun Y, Conforti L. Functionalized liposomes loaded with siRNAs targeting ion channels in effector memory T cells as a potential therapy for autoimmunity. Biomaterials. 2013;34(38):10249-10257.
Säälik P, Elmquist A, Hansen M, et al. Protein cargo delivery properties of cell-penetrating peptides. A comparative study. Bioconjug Chem. 2004;15(6):1246-1253.
Weir C, Hudson AL, Moon E, et al. Streptavidin: a novel immunostimulant for the selection and delivery of autologous and syngeneic tumor vaccines. Cancer Immunol Res. 2014;2(5):469-479.
Pardridge WM. Blood-brain barrier drug delivery of IgG fusion proteins with a transferrin receptor monoclonal antibody. Expert Opin Drug Deliv. 2015;12(2):207-222.
Galli F, Rapisarda AS, Stabile H, et al. In vivo imaging of natural killer cell trafficking in tumors. J NuclMed. 2015;56(10):1575-1580.
Barbet J, Bardiès M, Bourgeois M, et al. Radiolabeled antibodies for cancer imaging and therapy. Methods Mol Biol. 2012;907:681-697.
Pan JF, Liu NH, Shu LY, Sun H. Application of avidin-biotin technology to improve cell adhesion on nanofibrous matrices. J Nanobiotechnol. 2015;13:37.
Bodey B, Bodey B Jr, Siegel SE, Kaiser HE. Immunocytochemical detection of leukocyte-associated and apoptosis-related antigen expression in childhood brain tumors. Crit Rev Oncol Hematol. 2001;39(1-2):3-16.
Dixon RW, Radmer RJ, Kuhn B, et al. Theoretical and experimental studies of biotin analogues that bind almost as tightly to streptavidin as biotin. J Org Chem. 2002;67(6):1827-1837.
Yamamoto T, Aoki K, Sugiyama A, et al. Design and synthesis of biotin analogues reversibly binding with streptavidin. Chem Asian J. 2015;10(4):1071-1078.
Strzelczyk P, Plażuk D, Zakrzewski J, Bujacz G. Structural characterization of the avidin interactions with fluorescent pyrene-conjugates: 1-biotinylpyrene and 1-desthiobiotinylpyrene. Molecules. 2016;21(10):1270.
Pazy Y, Kulik T, Bayer EA, Wilchek M, Livnah O. Ligand exchange between proteins. Exchange of biotin and biotin derivatives between avidin and streptavidin. J Biol Chem. 2002;277(34):30892-30900.
Burt AJ, Ahmadvand P, Opp LK, Ryan AT, Kang C, Mancini RJ. A ligand-directed nitrophenol carbonate for transient in situ bioconjugation and drug delivery. ChemMedChem. 2020;15:2004-2009.
Conners R, Hooley E, Clarke AR, Thomas S, Brady RL. Recognition of oxidatively modified bases within the biotin-binding site of avidin. J Mol Biol. 2006;357(1):263-274.
Powell HR, Battye TGG, Kontogiannis L, Johnson O, Leslie AGW. Integrating macromolecular X-ray diffraction data with the graphical user interface iMosflm. Nat Protoc. 2017;12(7):1310-1325.
Winn MD, Ballard CC, Cowtan KD, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011;67(Pt 4):235-242.
Vagin A, Teplyakov A. Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr. 2010;66(Pt 1):22-25.
Pugliese L, Coda A, Malcovati M, Bolognesi M. Three-dimensional structure of the tetragonal crystal form of egg-white avidin in its functional complex with biotin at 2.7 Å resolution. J Mol Biol. 1993;231(3):698-710.
Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of coot. Acta Crystallogr D Biol Crystallogr. 2010;66(Pt 4):486-501.
Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997;53(Pt 3):240-255.
De March M, Di Rocco G, Hickey N, Geremia S. High-resolution crystal structure of the recombinant diheme cytochrome c from Shewanella baltica (OS155). J Biomol Struct Dyn. 2015;33(2):395-403.
DeLano WL. The PyMOL Molecular Graphics System. Delano Scientific; 2002.
Scheuermann TH, Brautigam CA. High-precision, automated integration of multiple isothermal titration calorimetric thermograms: new features of NITPIC. Methods. 2015;76:87-98.
Zhao H, Piszczek G, Schuck P. SEDPHAT-a platform for global ITC analysis and global multi-method analysis of molecular interactions. Methods. 2015;76:137-148.
Spinello A, Borišek J, Malcovati L, Magistrato A. Investigating the molecular mechanism of H3B-8800: a splicing modulator inducing preferential lethality in spliceosome-mutant cancers. Int J Mol Sci. 2021;22(20):11222.
Anandakrishnan R, Aguilar B, Onufriev AV. H++ 3.0: automating pK prediction and the preparation of biomolecular structures for atomistic molecular modeling and simulations. Nucleic Acids Res. 2012;40:W537-W541.
Lindorff-Larsen K, Piana S, Palmo K, et al. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins. 2010;78(8):1950-1958.
Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA. Development and testing of a general amber force field. J Comput Chem. 2004;25(9):1157-1174.
Wang J, Wang W, Kollman PA, Case DA. Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model. 2006;25(2):247-260.
Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ. GROMACS: fast, flexible, and free. J Comput Chem. 2005;26(16):1701-1718.
Bussi G, Donadio D, Parrinello M. Canonical sampling through velocity rescaling. J Chem Phys. 2007;126(1):014101.
Miller BR 3rd, McGee TD Jr, Swails JM, Homeyer N, Gohlke H, Roitberg AE. MMPBSA.py: an efficient program for end-state free energy calculations. J Chem Theory Comput. 2012;8(9):3314-3321.
Nguyen H, Roe DR, Simmerling C. Improved generalized born solvent model parameters for protein simulations. J Chem Theory Comput. 2013;9(4):2020-2034.
Borišek J, Saltalamacchia A, Spinello A, Magistrato A. Exploiting Cryo-EM structural information and all-atom simulations to decrypt the molecular mechanism of splicing modulators. J Chem Inf Model. 2020;60(5):2510-2521.
Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph. 1996;14(1):33-38.
Ayoub AT, Craddock TJA, Klobukowski M, Tuszynski J. Analysis of the strength of interfacial hydrogen bonds between tubulin dimers using quantum theory of atoms in molecules. Biophys J. 2014;107(3):740-750.
Hytönen VP, Hörhä J, Airenne TT, et al. Controlling quaternary structure assembly: subunit interface engineering and crystal structure of dual chain avidin. J Mol Biol. 2006;359(5):1352-1363.
Freitag S, Le Trong I, Klumb L, Stayton PS, Stenkamp RE. Structural studies of the streptavidin binding loop. Protein Sci. 1997;6(6):1157-1166.
Izrailev S, Stepaniants S, Balsera M, Oono Y, Schulten K. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys J. 1997;72(4):1568-1581.
Błauż A, Rychlik B, Makal A, et al. Ferrocene-biotin conjugates: synthesis, structure, cytotoxic activity and interaction with avidin. ChemPlusChem. 2016;81(11):1191-1201.
Barker KD, Eckermann AL, Sazinsky MH, et al. Protein binding and the electronic properties of iron(II) complexes: an electrochemical and optical investigation of outer sphere effects. Bioconjug Chem. 2009;20(10):1930-1939.
Plażuk P, Zakrzewski J, Salmain M, et al. Ferrocene−biotin conjugates targeting cancer cells: synthesis, interaction with avidin, cytotoxic properties and the crystal structure of the complex of avidin with a biotin−linker−ferrocene conjugate. Organometallics. 2013;32(20):5774-5783.
Tong Y, Mei Y, Li YL, Ji CG, Zhang JZ. Electrostatic polarization makes a substantial contribution to the free energy of avidin-biotin binding. J Am Chem Soc. 2010;132(14):5137-5142.