NMR study of the structure and dynamics of the BRCT domain from the kinetochore protein KKT4.
BRCT
Hydrogen–deuterium exchange
KKT4
Kinetochore
Kinetoplastid
NMR resonance assignments
Phosphopeptide-binding
Trypanosomes
Journal
Biomolecular NMR assignments
ISSN: 1874-270X
Titre abrégé: Biomol NMR Assign
Pays: Netherlands
ID NLM: 101472371
Informations de publication
Date de publication:
07 Mar 2024
07 Mar 2024
Historique:
received:
04
09
2023
accepted:
18
01
2024
medline:
8
3
2024
pubmed:
8
3
2024
entrez:
7
3
2024
Statut:
aheadofprint
Résumé
KKT4 is a multi-domain kinetochore protein specific to kinetoplastids, such as Trypanosoma brucei. It lacks significant sequence similarity to known kinetochore proteins in other eukaryotes. Our recent X-ray structure of the C-terminal region of KKT4 shows that it has a tandem BRCT (BRCA1 C Terminus) domain fold with a sulfate ion bound in a typical binding site for a phosphorylated serine or threonine. Here we present the
Identifiants
pubmed: 38453826
doi: 10.1007/s12104-024-10163-9
pii: 10.1007/s12104-024-10163-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Wellcome Trust
ID : 210622/Z/18/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 210622/Z/18/Z
Pays : United Kingdom
Informations de copyright
© 2024. The Author(s).
Références
Akiyoshi B, Gull K (2014) Discovery of unconventional kinetochores in kinetoplastids. Cell 156(6):1247–1258
doi: 10.1016/j.cell.2014.01.049
Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Bohme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A, Davies RM, Doggett J, Djikeng A, Feldblyum T, Field MC, Fraser A, Goodhead I, Hance Z, Harper D, Harris BR, Hauser H, Hostetler J, Ivens A, Jagels K, Johnson D, Johnson J, Jones K, Kerhornou AX, Koo H, Larke N, Landfear S, Larkin C, Leech V, Line A, Lord A, Macleod A, Mooney PJ, Moule S, Martin DM, Morgan GW, Mungall K, Norbertczak H, Ormond D, Pai G, Peacock CS, Peterson J, Quail MA, Rabbinowitsch E, Rajandream MA, Reitter C, Salzberg SL, Sanders M, Schobel S, Sharp S, Simmonds M, Simpson AJ, Tallon L, Turner CM, Tait A, Tivey AR, Van Aken S, Walker D, Wanless D, Wang S, White B, White O, Whitehead S, Woodward J, Wortman J, Adams MD, Embley TM, Gull K, Ullu E, Barry JD, Fairlamb AH, Opperdoes F, Barrell BG, Donelson JE, Hall N, Fraser CM, Melville SE, El-Sayed NM (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309(5733):416–422
doi: 10.1126/science.1112642
Biggins S (2013) The composition, functions, and regulation of the budding yeast kinetochore. Genetics 194(4):817–846
doi: 10.1534/genetics.112.145276
Brinkley BR, Stubblefield E (1966) The fine structure of the kinetochore of a mammalian cell in vitro. Chromosoma 19(1):28–43
doi: 10.1007/BF00332792
Brun R, Schonenberger M (1979) Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium Short communication. Acta Trop 36(3):289–292
Brünger AT (1992) X-PLOR, Version 3.1 : a system for X-ray crystallography and NMR. Yale University Press, New Haven
Brusini L, D’archivio S, Mcdonald J, Wickstead B (2021) Trypanosome KKIP1 dynamically links the inner kinetochore to a kinetoplastid outer kinetochore complex. Front Cell Infect Microbiol 11:641174
doi: 10.3389/fcimb.2021.641174
Cheeseman IM (2014) The kinetochore. Cold Spring Harb Perspect Biol 6(7):a015826
doi: 10.1101/cshperspect.a015826
Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9(1):33–46
doi: 10.1038/nrm2310
Cornilescu G, Marquardt JL, Ottiger M, Bax A (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120(27):6836–7683
doi: 10.1021/ja9812610
Cowtan K (2006) The buccaneer software for automated model building.1. Tracing protein chains. Acta Crystallogr Sec D: Biol Crystallogr 62(9):1002–1011
doi: 10.1107/S0907444906022116
D’archivio S, Wickstead B (2017) Trypanosome outer kinetochore proteins suggest conservation of chromosome segregation machinery across eukaryotes. J Cell Biol 216(2):379–391
doi: 10.1083/jcb.201608043
Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6(3):277–293
doi: 10.1007/BF00197809
Delano WL (2002) Pymol: an open-source molecular graphics tool. CCP4 Newsl. Protein Crystallogr 40:82–92
Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486–501
doi: 10.1107/S0907444910007493
Gileadi O, Burgess-Brown NA, Colebrook SM, Berridge G, Savitsky P, Smee CEA, Loppnau P, Johansson C, Salah E, Pantic NH (2008) High throughput production of recombinant human proteins for crystallography. Methods Mol Biol (clifton, N.J.) 426:221–246
doi: 10.1007/978-1-60327-058-8_14
Hyberts SG, Milbradt AG, Wagner AB, Arthanari H, Wagner G (2012) Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional poisson gap scheduling. J Biomol NMR 52(4):315–327
doi: 10.1007/s10858-012-9611-z
Lescop E, Schanda P, Brutscher B (2007) A set of BEST triple-resonance experiments for time-optimized protein resonance assignment. J Magn Reson 187(1):163–169
doi: 10.1016/j.jmr.2007.04.002
Liebschner D, Afonine PV, Baker ML, Bunkoczi G, Chen VB, Croll TI, Hintze B, Hung LW, Jain S, Mccoy AJ, Moriarty NW, Oeffner RD, Poon BK, Prisant MG, Read RJ, Richardson JS, Richardson DC, Sammito MD, Sobolev OV, Stockwell DH, Terwilliger TC, Urzhumtsev AG, Videau LL, Williams CJ, Adams PD (2019) Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr D Struct Biol 75(Pt 10):861–877
doi: 10.1107/S2059798319011471
Llauro A, Hayashi H, Bailey ME, Wilson A, Ludzia P, Asbury CL, Akiyoshi B (2018) The kinetoplastid kinetochore protein KKT4 is an unconventional microtubule tip-coupling protein. J Cell Biol 217(11):3886–3900
doi: 10.1083/jcb.201711181
Ludzia P, Lowe ED, Marciano G, Mohammed S, Redfield C, Akiyoshi B (2021) Structural characterization of KKT4, an unconventional microtubule-binding kinetochore protein. Structure 29(9):1014–1028
doi: 10.1016/j.str.2021.04.004
Mccoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr. https://doi.org/10.1107/S0021889807021206
doi: 10.1107/S0021889807021206
Mcintosh JR (2016) Mitosis. Cold Spring Harb Perspect Biol 8(9):a023218
doi: 10.1101/cshperspect.a023218
Meraldi P, Mcainsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7(3):R23
doi: 10.1186/gb-2006-7-3-r23
Metzler WJ, Constantine KL, Friedrichs MS, Bell AJ, Ernst EG, Lavoie TB, Mueller L (1993) Characterization of the 3-dimensional solution structure of human profilin - H-1, C-13, and N-15 Nmr assignments and global folding pattern. Biochemistry 32(50):13818–13829
doi: 10.1021/bi00213a010
Musacchio A, Desai A (2017) A molecular view of kinetochore assembly and function. Biology (basel) 6(1):5
Nerusheva OO, Akiyoshi B (2016) Divergent polo box domains underpin the unique kinetoplastid kinetochore. Open Biol 6(3):150206
doi: 10.1098/rsob.150206
Nerusheva OO, Ludzia P, Akiyoshi B (2019) Identification of four unconventional kinetoplastid kinetochore proteins KKT22-25 in Trypanosoma brucei. Open Biol 9(12):190236
doi: 10.1098/rsob.190236
Poon SK, Peacock L, Gibson W, Gull K, Kelly S (2012) A modular and optimized single marker system for generating Trypanosoma brucei cell lines expressing T7 RNA polymerase and the tetracycline repressor. Open Biol 2(2):110037
doi: 10.1098/rsob.110037
Redfield C (2015) Assignment of protein NMR spectra using heteronuclear NMR—A tutorial. Biol Magn Reson 32:1–42
doi: 10.1007/978-1-4899-7621-5_1
Rückert M, Otting G (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J Am Chem Soc 122(32):7793–7797
doi: 10.1021/ja001068h
Santaguida S, Musacchio A (2009) The life and miracles of kinetochores. EMBO J 28:2511–2531
doi: 10.1038/emboj.2009.173
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to imageJ: 25 years of image analysis. Nat Methods 9(7):671–675
doi: 10.1038/nmeth.2089
Schulte-Herbruggen T, Sorensen OW (2000) Clean TROSY: compensation for relaxation-induced artifacts. J Magn Reson 144(1):123–128
doi: 10.1006/jmre.2000.2020
Shen Y, Bax A (2013) Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J Biomol NMR 56(3):227–241
doi: 10.1007/s10858-013-9741-y
Spera S, Bax A (1991) Empirical correlation between protein backbone conformation and C-alpha and C-beta C-13 nuclear-magnetic-resonance chemical-shifts. J Amer Chem Soc 113(14):5490–5492
doi: 10.1021/ja00014a071
Strong M, Sawaya MR, Wang S, Phillips M, Cascio D, Eisenberg D (2006) Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103(21):8060–8065
doi: 10.1073/pnas.0602606103
Van Hooff JJ, Tromer E, Van Wijk LM, Snel B, Kops GJ (2017) Evolutionary dynamics of the kinetochore network in eukaryotes as revealed by comparative genomics. EMBO Rep 18(9):1559–1571
doi: 10.15252/embr.201744102
Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, Ulrich EL, Markley JL, Ionides J, Laue ED (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59(4):687–696
doi: 10.1002/prot.20449
Zhu G, Xia Y, Nicholson LK, Sze KH (2000) Protein dynamics measurements by TROSY-based NMR experiments. J Magn Reson 143(2):423–426
doi: 10.1006/jmre.2000.2022