The Impact of Terminal Peptide Extensions of Retinal Inosine 5´Monophosphate Dehydrogenase 1 Isoforms on their DNA-binding Activities.
Bateman domain
Canonical isoform
Retinitis pigmentosa type 10
Rhodopsin
Journal
The protein journal
ISSN: 1875-8355
Titre abrégé: Protein J
Pays: Netherlands
ID NLM: 101212092
Informations de publication
Date de publication:
11 May 2024
11 May 2024
Historique:
accepted:
30
04
2024
medline:
11
5
2024
pubmed:
11
5
2024
entrez:
11
5
2024
Statut:
aheadofprint
Résumé
The main structural difference between the mutation-susceptible retinal isoforms of inosine 5´-monophosphate dehydrogenase-1 (IMPDH-1) with the canonical form resides in the C- and N-terminal peptide extensions with unknown structural/functional impacts. In this report, we aimed to experimentally evaluate the functional impact of these extensions on the specific/non-specific single-stranded DNA (ssDNA)-binding activities relative to those of the canonical form. Our in silico findings indicated the possible contribution of the C-terminal segment to the reduced flexibility of the Bateman domain of the enzyme. In addition, the in silico data indicated that the N-terminal tail acts by altering the distance between the tetramers in the concave octamer complex (the native form) of the enzyme. The overall impact of these predicted structural variations became evident, first, through higher K
Identifiants
pubmed: 38733555
doi: 10.1007/s10930-024-10202-3
pii: 10.1007/s10930-024-10202-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Bowne SJ, Sullivan LS, Blanton SH, Cepko CL, Blackshaw S, Birch DG, Hughbanks-Wheaton D, Heckenlively JR, Daiger SP (2002) Mutations in the inosine monophosphate dehydrogenase 1 gene (IMPDH1) cause the RP10 form of autosomal dominant retinitis pigmentosa. Hum Mol Genet 11(5):559–568
doi: 10.1093/hmg/11.5.559
pubmed: 11875050
Burrell AL, Nie C, Said M, Simonet JC, Fernández-Justel D, Johnson MC, Quispe J, Buey RM, Peterson JR, Kollman JM (2022) IMPDH1 retinal variants control filament architecture to tune allosteric regulation. Nat Struct Mol Biol 29(1):47–58
doi: 10.1038/s41594-021-00706-2
pubmed: 35013599
pmcid: 9044917
Plana-Bonamaisó A, López-Begines S, Fernández-Justel D, Junza A, Soler-Tapia A, Andilla J, Loza-Alvarez P, Rosa JL, Miralles E, Casals I (2020) Post-translational regulation of retinal IMPDH1 in vivo to adjust GTP synthesis to illumination conditions. elife 9:e56418
doi: 10.7554/eLife.56418
pubmed: 32254022
pmcid: 7176436
Bateman A (1997) The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem Sci 22(1):12–13
doi: 10.1016/S0968-0004(96)30046-7
pubmed: 9020585
Colby TD, Vanderveen K, Strickler MD, Markham GD, Goldstein BM (1999) Crystal structure of human type II inosine monophosphate dehydrogenase: implications for ligand binding and drug design. Proc Natl Acad Sci 96(7):3531-3536
Buey RM, Ledesma-Amaro R, Velázquez-Campoy A, Balsera M, Chagoyen M, De Pereda JM, Revuelta JL (2015) Guanine nucleotide binding to the Bateman domain mediates the allosteric inhibition of eukaryotic IMP dehydrogenases. Nat Commun 6(1):1–11
doi: 10.1038/ncomms9923
Labesse G, Alexandre T, Vaupré L, Salard-Arnaud I, Him JLK, Raynal B, Bron P, Munier-Lehmann H (2013) MgATP regulates allostery and fiber formation in IMPDHs. Structure 21(6):975–985
doi: 10.1016/j.str.2013.03.011
pubmed: 23643948
Bowne SJ, Liu Q, Sullivan LS, Zhu J, Spellicy CJ, Rickman CB, Pierce EA, Daiger SP (2006) Why do mutations in the ubiquitously expressed housekeeping gene IMPDH1 cause retina-specific photoreceptor degeneration? Invest Ophthalmol Vis Sci 47(9):3754–3765
doi: 10.1167/iovs.06-0207
pubmed: 16936083
Gunter JH, Thomas EC, Lengefeld N, Kruger SJ, Worton L, Gardiner EM, Jones A, Barnett NL, Whitehead JP (2008) Characterisation of inosine monophosphate dehydrogenase expression during retinal development: differences between variants and isoforms. Int J Biochem Cell Biol 40(9):1716–1728
doi: 10.1016/j.biocel.2007.12.018
pubmed: 18295529
Spellicy CJ, Daiger SP, Sullivan LS, Zhu J, Liu Q, Pierce EA, Bowne SJ (2007) Characterization of retinal inosine monophosphate dehydrogenase 1 in several mammalian species. Mol Vis 13:1866–1872
pubmed: 17960124
Cornuel J-F, Moraillon A, Guéron M (2002) Participation of yeast inosine 5′-monophosphate dehydrogenase in an in vitro complex with a fragment of the C-rich telomeric strand. Biochimie 84(4):279–289
doi: 10.1016/S0300-9084(02)01400-1
pubmed: 12106905
McLean JE, Hamaguchi N, Belenky P, Mortimer SE, Stanton M, Hedstrom L (2004) Inosine 5′-monophosphate dehydrogenase binds nucleic acids in vitro and in vivo. Biochem J 379(2):243–251
doi: 10.1042/bj20031585
pubmed: 14766016
pmcid: 1224093
Mortimer SE, Hedstrom L (2005) Autosomal dominant retinitis pigmentosa mutations in inosine 5′-monophosphate dehydrogenase type I disrupt nucleic acid binding. Biochem J 390(1):41–47
doi: 10.1042/BJ20042051
pubmed: 15882147
pmcid: 1184561
Mortimer SE, Xu D, McGrew D, Hamaguchi N, Lim HC, Bowne SJ, Daiger SP, Hedstrom L (2008) IMP dehydrogenase type 1 associates with polyribosomes translating rhodopsin mRNA. J Biol Chem 283(52):36354–36360
doi: 10.1074/jbc.M806143200
pubmed: 18974094
pmcid: 2605994
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12(1):7–8
doi: 10.1038/nmeth.3213
pubmed: 25549265
pmcid: 4428668
Yang J, Zhang Y (2015) I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res 43(W1):W174–W181
doi: 10.1093/nar/gkv342
pubmed: 25883148
pmcid: 4489253
Xu D, Zhang Y (2011) Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophys J 101(10):2525–2534
doi: 10.1016/j.bpj.2011.10.024
pubmed: 22098752
pmcid: 3218324
Lovell SC, Davis IW, Arendall WB III, De Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC (2003) Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins: Struct Funct Bioinformatics 50(3):437–450
doi: 10.1002/prot.10286
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612
doi: 10.1002/jcc.20084
pubmed: 15264254
Sintchak MD, Fleming MA, Futer O, Raybuck SA, Chambers SP, Caron PR, Murcko MA, Wilson KP (1996) Structure and mechanism of inosine monophosphate dehydrogenase in complex with the immunosuppressant mycophenolic acid. Cell 85(6):921–930
doi: 10.1016/S0092-8674(00)81275-1
pubmed: 8681386
Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455–461
doi: 10.1002/jcc.21334
pubmed: 19499576
pmcid: 3041641
Van Zundert G, Rodrigues J, Trellet M, Schmitz C, Kastritis P, Karaca E, Melquiond A, van Dijk M, De Vries S, Bonvin A (2016) The HADDOCK2. 2 web server: user-friendly integrative modeling of biomolecular complexes. J Mol Biol 428(4):720–725
doi: 10.1016/j.jmb.2015.09.014
pubmed: 26410586
Wassenaar TA, Van Dijk M, Loureiro-Ferreira N, Van Der Schot G, De Vries SJ, Schmitz C, Van Der Zwan J, Boelens R, Giachetti A, Ferella L (2012) WeNMR: structural biology on the grid. J Grid Comput 10(4):743–767
doi: 10.1007/s10723-012-9246-z
De Vries SJ, Van Dijk M, Bonvin AM (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5(5):883–897
doi: 10.1038/nprot.2010.32
pubmed: 20431534
Moreira IS, Fernandes PA, Ramos MJ (2010) Protein–protein docking dealing with the unknown. J Comput Chem 31(2):317–342
doi: 10.1002/jcc.21276
pubmed: 19462412
Risal D, Strickler M, Goldstein B (2003) Crystal structure of the human type I inosine monophosphate dehydrogenase and implications for isoform specificity
Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ (2005) GROMACS: fast, flexible, and free. J Comput Chem 26(16):1701–1718
doi: 10.1002/jcc.20291
pubmed: 16211538
Porollo AA, Adamczak R, Meller J (2004) POLYVIEW: a flexible visualization tool for structural and functional annotations of proteins. Bioinformatics 20(15):2460–2462
doi: 10.1093/bioinformatics/bth248
pubmed: 15073023
Andashti B, Yazdanparast R, Barzegari E, Galehdari H (2020) The functional impact of the C/N-terminal extensions of the mouse retinal IMPDH1 isoforms: a kinetic evaluation. Mol Cell Biochem 465:155–164
doi: 10.1007/s11010-019-03675-9
pubmed: 31838626
Andashti B, Yazdanparast R, Motahar M, Barzegari E, Galehdari H (2021) Terminal peptide extensions augment the retinal IMPDH1 catalytic activity and attenuate the ATP-induced fibrillation events. Cell Biochem Biophys 79:221–229
doi: 10.1007/s12013-021-00973-2
pubmed: 33733369
Andashti B, Yazdanparast R, Barzegari E, Galehdari H (2020) The functional impact of the C/N-terminal extensions of the mouse retinal IMPDH1 isoforms: a kinetic evaluation. Mol Cell Biochem 465(1):155–164
doi: 10.1007/s11010-019-03675-9
pubmed: 31838626
Waterborg J (2002) The protein protocols handbook. The Lowry method for protein quantization 2ed Totowa
Chodosh LA (1996) UV crosslinking of proteins to nucleic acids. Curr Prot Mol Biol 36(1):12.15. 11–12.15. 18
Xu D, Cobb G, Spellicy CJ, Bowne SJ, Daiger SP, Hedstrom L (2008) Retinal isoforms of inosine 5′-monophosphate dehydrogenase type 1 are poor nucleic acid binding proteins. Arch Biochem Biophys 472(2):100–104
doi: 10.1016/j.abb.2008.02.012
pubmed: 18295591
pmcid: 2366119
Heffler MA, Walters RD, Kugel JF (2012) Using electrophoretic mobility shift assays to measure equilibrium dissociation constants: GAL4-p53 binding DNA as a model system. Biochem Mol Biol Educ 40(6):383–387
doi: 10.1002/bmb.20649
pubmed: 23166026
Nimmesgern E, Black J, Futer O, Fulghum JR, Chambers SP, Brummel CL, Raybuck SA, Sintchak MD (1999) Biochemical analysis of the modular enzyme inosine 5′-monophosphate dehydrogenase. Protein Expr Purif 17(2):282–289
doi: 10.1006/prep.1999.1136
pubmed: 10545277