Comparative analysis of human and bovine thyroglobulin structures

Journal of Analytical Science and Technology - 2022
Han-ul Kim1,2, Hyomin Jeong3, Jeong Min Chung4, Dooil Jeoung2, Jaekyung Hyun5, Hyun Suk Jung2,1
1Kangwon Center for Systems Imaging, Chuncheon, Republic of Korea
2Department of Biochemistry, College of Natural Sciences, Kangwon National University, Chuncheon, Republic of Korea
3Center for Electron Microscopy Research, Korea Basic Science Institute, Ochang, Republic of Korea
4Department of Biotechnology, The Catholic University of Korea, Bucheon-si, Republic of Korea
5Department of Convergence Medicine, School of Medicine, Pusan National University, Yangsan, Republic of Korea

Tóm tắt

AbstractIn biology, evolutionary conserved protein sequences show homologous physiological phenotypes in their structures and functions. If the protein has a vital function, its sequence is usually conserved across the species. However, in highly conserved protein there still remains small differences across the species. Upon protein–protein interaction (PPI), it is observed that the conserved proteins can have different binding partners that are considered to be caused by the small sequence variations in a specific domain. Thyroglobulin (TG) is the most commonly found protein in the thyroid gland of vertebrates and serves as the precursor of the thyroid hormones, tetraiodothyronine and triiodothyronine that are critical for growth, development and metabolism in vertebrates. In this study, we comparatively analyzed the sequences and structures of the highly conserved regions of TG from two different species in relation to their PPIs. In order to do so, we employed SIM for sequence alignment, STRING for PPI analysis and cryo-electron microscopy for 3D structural analysis. Our Cryo-EM model for TG of Bos taurus determined at 7.1 Å resolution fitted well with the previously published Cryo-EM model for Homo sapiens TG. By demonstrating overall structural homology between TGs from different species, we address that local amino acid sequence variation is sufficient to alter PPIs specific for the organism. We predict that our result will contribute to a deeper understanding in the evolutionary pattern applicable to many other proteins.

Từ khóa


Tài liệu tham khảo

Belkadi A, Jacques C, Savagner F, Malthiery Y. Phylogenetic analysis of the human thyroglobulin regions. Thyroid Res. 2012;5:3. https://doi.org/10.1186/1756-6614-5-3.

Brock K, Talley K, Coley K, Kundrotas P, Alexov E. Optimization of electrostatic interactions in protein-protein complexes. Biophys J. 2007;93:3340–52. https://doi.org/10.1529/biophysj.107.112367.

Citterio CE, Morishita Y, Dakka N, Veluswamy B, Arvan P. Relationship between the dimerization of thyroglobulin and its ability to form triiodothyronine. J Biol Chem. 2018;293:4860–9. https://doi.org/10.1074/jbc.RA118.001786.

Coscia F, Taler-Vercic A, Chang VT, Sinn L, O’Reilly FJ, Izore T, Renko M, Berger I, Rappsilber J, Turk D, Lowe J. The structure of human thyroglobulin. Nature. 2020;578:627–30. https://doi.org/10.1038/s41586-020-1995-4.

De Las RJ, Fontanillo C. Protein-protein interactions essentials: key concepts to building and analyzing interactome networks. PLoS Comput Biol. 2010;6: e1000807. https://doi.org/10.1371/journal.pcbi.1000807.

Ding Z, Kihara D. Computational identification of protein-protein interactions in model plant proteomes. Sci Rep. 2019;9:8740. https://doi.org/10.1038/s41598-019-45072-8.

Duret L, Gasteiger E, Perriere G. LALNVIEW: a graphical viewer for pairwise sequence alignments. Comput Appl Biosci. 1996;12:507–10. https://doi.org/10.1093/bioinformatics/12.6.507.

Franc JL, Venot N, Marriq C. Characterization of the two oligosaccharides present in the preferential hormonogenic domain of human thyroglobulin. Biochem Biophys Res Commun. 1990;166:937–44. https://doi.org/10.1016/0006-291x(90)90901-x.

Hishinuma A, Furudate S, Oh-Ishi M, Nagakubo N, Namatame T, Ieiri T. A novel missense mutation (G2320R) in thyroglobulin causes hypothyroidism in rdw rats. Endocrinology. 2000;141:4050–5. https://doi.org/10.1210/endo.141.11.7794.

Holzer G, Morishita Y, Fini JB, Lorin T, Gillet B, Hughes S, Tohme M, Deleage G, Demeneix B, Arvan P, Laudet V. Thyroglobulin represents a novel molecular architecture of vertebrates. J Biol Chem. 2016;291:16553–66. https://doi.org/10.1074/jbc.M116.719047.

Huang XQ, Hardison RC, Miller W. A space-efficient algorithm for local similarities. Comput Appl Biosci. 1990;6:373–81. https://doi.org/10.1093/bioinformatics/6.4.373.

Jo S, Kim T, Iyer VG, Im W. CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem. 2008;29:1859–65. https://doi.org/10.1002/jcc.20945.

Johansson-Akhe I, Mirabello C, Wallner B. Predicting protein-peptide interaction sites using distant protein complexes as structural templates. Sci Rep. 2019;9:4267. https://doi.org/10.1038/s41598-019-38498-7.

Kim PS, Ding M, Menon S, Jung CG, Cheng JM, Miyamoto T, Li B, Furudate S, Agui T. A missense mutation G2320R in the thyroglobulin gene causes non-goitrous congenital primary hypothyroidism in the WIC-rdw rat. Mol Endocrinol. 2000;14:1944–53. https://doi.org/10.1210/mend.14.12.0571.

Kim K, Kopylov M, Bobe D, Kelley K, Eng ET, Arvan P, Clarke OB. The structure of natively iodinated bovine thyroglobulin. Acta Crystallogr D Struct Biol. 2021;77:1451–9. https://doi.org/10.1107/S2059798321010056.

Kimanius D, Forsberg BO, Scheres SH, Lindahl E. Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. Elife. 2016. https://doi.org/10.7554/eLife.18722.

Knight RD, Freeland SJ, Landweber LF. A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol. 2001. https://doi.org/10.1186/gb-2001-2-4-research0010.

Kwon E, Pathak D, Kim HU, Dahal P, Ha SC, Lee SS, Jeong H, Jeoung D, Chang HW, Jung HS, Kim DY. Structural Insights into stressosome assembly. IUCrJ. 2019;6:938–47. https://doi.org/10.1107/S205225251900945X.

Lee D, Redfern O, Orengo C. Predicting protein function from sequence and structure. Nat Rev Mol Cell Biol. 2007;8:995–1005. https://doi.org/10.1038/nrm2281.

Lee J, Di Jeso B, Arvan P. The cholinesterase-like domain of thyroglobulin functions as an intramolecular chaperone. J Clin Invest. 2008;118:2950–8. https://doi.org/10.1172/JCI35164.

Li M, Luo Z, Yu S, Tang Z. Proton pump inhibitor use and risk of dementia: systematic review and meta-analysis. Medicine (baltimore). 2019;98: e14422. https://doi.org/10.1097/MD.0000000000014422.

Lipman DJ, Souvorov A, Koonin EV, Panchenko AR, Tatusova TA. The relationship of protein conservation and sequence length. BMC Evol Biol. 2002;2:20. https://doi.org/10.1186/1471-2148-2-20.

Makino T, Gojobori T. Evolution of protein-protein interaction network. Genome Dyn. 2007;3:13–29. https://doi.org/10.1159/000107601.

Malthiery Y, Lissitzky S. Primary structure of human thyroglobulin deduced from the sequence of its 8448-base complementary DNA. Eur J Biochem. 1987;165:491–8. https://doi.org/10.1111/j.1432-1033.1987.tb11466.x.

Marmur J, Falkow S, Mandel M. New approaches to bacterial taxonomy. Ann Rev Microbiol. 1963;17:329–72. https://doi.org/10.1146/annurev.mi.17.100163.001553.

Molina F, Bouanani M, Pau B, Granier C. Characterization of the type-1 repeat from thyroglobulin, a cysteine-rich module found in proteins from different families. Eur J Biochem. 1996;240:125–33. https://doi.org/10.1111/j.1432-1033.1996.0125h.x.

Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–12. https://doi.org/10.1002/jcc.20084.

Sanger F. Species differences in insulins. Nature. 1949;164:529. https://doi.org/10.1038/164529a0.

Schmitz M, Candelise N, Kanata E, Llorens F, Thune K, Villar-Pique A, da Silva Correia SM, Dafou D, Sklaviadis T, Appelhans D, Zerr I. Validation of Poly(Propylene Imine) glycodendrimers towards their anti-prion conversion efficiency. Mol Neurobiol. 2020;57:1863–74. https://doi.org/10.1007/s12035-019-01837-w.

Schwede T, Kopp J, Guex N, Peitsch MC. SWISS-MODEL: an automated protein homology-modeling server. Nucl Acids Res. 2003;31:3381–5. https://doi.org/10.1093/nar/gkg520.

Shehu A, Kavraki LE. Modeling structures and motions of loops in protein molecules. Entropy. 2012;14:252–90.

Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering CV. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucl Acids Res. 2019;47:D607–13. https://doi.org/10.1093/nar/gky1131.

UniProt C. UniProt: the universal protein knowledgebase in 2021. Nucl Acids Res. 2021;49:D480–9. https://doi.org/10.1093/nar/gkaa1100.

Yang SX, Pollock HG, Rawitch AB. Glycosylation in human thyroglobulin: location of the N-linked oligosaccharide units and comparison with bovine thyroglobulin. Arch Biochem Biophys. 1996;327:61–70. https://doi.org/10.1006/abbi.1996.0093.

Zhang K. Gctf: real-time CTF determination and correction. J Struct Biol. 2016;193:1–12. https://doi.org/10.1016/j.jsb.2015.11.003.

Thông tin
Thông tin xuất bản

Journal of Analytical Science and Technology

Thông tin tác giả