Cited by 8Protein Structure and DynamicsEnzyme Structure and FunctionGenomics and Phylogenetic Studies

The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.

New β-Propellers Are Continuously Amplified From Single Blades in all Major Lineages of the β-Propeller Superfamily

Open access
Pereira, Joana, Lupas, Andrei N.·2022·Frontiers in Molecular Biosciences

Published version of a preprint

Abstract

β-Propellers are toroidal folds, in which consecutive supersecondary structure units of four anti-parallel β-strands–called blades–are arranged radially around a central axis. Uniquely among toroidal folds, blades span the full range of sequence symmetry, from near identity to complete divergence, indicating an ongoing process of amplification and differentiation. We have proposed that the major lineages of β-propellers arose through this mechanism and that therefore their last common ancestor was a single blade, not a fully formed β-propeller. Here we show that this process of amplification and differentiation is also widespread within individual lineages, yielding β-propellers with blades of more than 60% pairwise sequence identity in most major β-propeller families. In some cases, the blades are nearly identical, indicating a very recent amplification event, but even in cases where such recently amplified β-propellers have more than 80% overall sequence identity to each other, comparison of their DNA sequence shows that the amplification occurred independently.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fmolb.2022.895496

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 61

  1. Afanasieva, 2019, Structural Diversity of Oligomeric β-propellers with Different Numbers of Identical Blades, eLife, 8, 10.7554/eLife.49853 · DOI
  2. Altschul, 1997, Gapped BLAST and PSI-BLAST: a New Generation of Protein Database Search Programs, Nucleic Acids Res., 25, 3389, 10.1093/nar/25.17.3389 · DOI · Paper page
  3. Alva, 2015, A Vocabulary of Ancient Peptides at the Origin of Folded Proteins, eLife, 4, e09410, 10.7554/eLife.09410.001 · DOI
  4. Amara, 2011, Macromolecular Inhibition of Quorum Sensing: Enzymes, Antibodies, and beyond, Chem. Rev., 111, 195, 10.1021/cr100101c · DOI
  5. Andrade, 2001, Protein Repeats: Structures, Functions, and Evolution, J. Struct. Biol., 134, 117, 10.1006/jsbi.2001.4392 · DOI
  6. Beisel, 1999, Tachylectin-2: Crystal Structure of a Specific GlcNAc/GalNAc-Binding Lectin Involved in the Innate Immunity Host Defense of the Japanese Horseshoe Crab Tachypleus Tridentatus, Embo J., 18, 2313, 10.1093/emboj/18.9.2313 · DOI
  7. Bezerra, 2015, Structure of Human Dipeptidyl Peptidase 10 (DPPY): A Modulator of Neuronal Kv4 Channels, Sci. Rep., 5, 10.1038/srep08769 · DOI
  8. Biegert, 2008, De Novo identification of Highly Diverged Protein Repeats by Probabilistic Consistency, Oxf. Univ. Press, 24, 807, 10.1093/bioinformatics/btn039 · DOI
  9. Blatch, 1999, The Tetratricopeptide Repeat: A Structural Motif Mediating Protein-Protein Interactions, BioEssays, 21, 932, 10.1002/(sici)1521-1878(199911)21:11<932::aid-bies5>3.0.co;2-n · DOI
  10. Bliven, 2019, Analyzing the Symmetrical Arrangement of Structural Repeats in Proteins with CE-Symm, PLoS Comput. Biol., 15, e1006842, 10.1371/journal.pcbi.1006842 · DOI
  11. Brown, 2013, Identification of the β-Lactamase Inhibitor Protein-II (BLIP-II) Interface Residues Essential for Binding Affinity and Specificity for Class A β-Lactamases, J. Biol. Chem., 288, 17156, 10.1074/jbc.M113.463521 · DOI
  12. Capella-Gutierrez, 2009, trimAl: a Tool for Automated Alignment Trimming in Large-Scale Phylogenetic Analyses, Bioinformatics, 25, 1972, 10.1093/bioinformatics/btp348 · DOI
  13. Chaudhuri, 2008, Evolution of the β-propeller Fold, Proteins, 71, 795, 10.1002/prot.21764 · DOI
  14. Chen, 2011, The Many Blades of the β-propeller Proteins: Conserved but Versatile, Trends Biochem. Sci., 36, 553, 10.1016/j.tibs.2011.07.004 · DOI
  15. Cock, 2009, Biopython: Freely Available Python Tools for Computational Molecular Biology and Bioinformatics, Bioinformatics, 25, 1422, 10.1093/bioinformatics/btp163 · DOI · Paper page
  16. Corbett, 2004, The C-Terminal Domain of DNA Gyrase A Adopts a DNA-Bending β-pinwheel Fold, Proc. Natl. Acad. Sci. U.S.A., 101, 7293, 10.1073/pnas.0401595101 · DOI
  17. Das, 2003, Structure and Evolutionary Aspects of Matrix Metalloproteinases: A Brief Overview, Mol. Cell. Biochem., 253, 31, 10.1023/A:1026093016148 · DOI
  18. Dunin-Horkawicz, 2014, Prokaryotic Ancestry of Eukaryotic Protein Networks Mediating Innate Immunity and Apoptosis, J. Mol. Biol., 426, 1568, 10.1016/j.jmb.2013.11.030 · DOI
  19. Edgar, 2004, MUSCLE: Multiple Sequence Alignment with High Accuracy and High Throughput, Nucleic acids Res., 32, 1792, 10.1093/nar/gkh340 · DOI · Paper page
  20. Frickey, 2004, CLANS: A Java Application for Visualizing Protein Families Based on Pairwise Similarity, Bioinformatics, 20, 3702, 10.1093/bioinformatics/bth444 · DOI
  21. Fülöp, 1998, Prolyl Oligopeptidase: an Unusual Beta-Propeller Domain Regulates Proteolysis, Cell, 94, 161, 10.1016/S0092-8674(00)81416-6 · DOI
  22. Fülöp, 1999, β Propellers: Structural Rigidity and Functional Diversity, Curr. Opin. Struct. Biol., 9, 715, 10.1016/S0959-440X(99)00035-4 · DOI
  23. Ghosh, 1995, The Refined Structure of the Quinoprotein Methanol Dehydrogenase from Methylobacterium Extorquens at 1.94 Å, Structure, 3, 177, 10.1016/S0969-2126(01)00148-4 · DOI
  24. Giuseppe, 2008, The Leptospiral Antigen Lp49 Is a Two-Domain Protein with Putative Protein Binding Function, J. Struct. Biol., 163, 53, 10.1016/j.jsb.2008.04.003 · DOI
  25. Gupta, 2014, Kelch Proteins: Emerging Roles in Skeletal Muscle Development and Diseases, Skelet. Muscle, 4, 11, 10.1186/2044-5040-4-11 · DOI
  26. Guruprasad, 2004, Structural Plasticity Associated with the β-propeller Architecture, Int. J. Biol. Macromol., 34, 55, 10.1016/j.ijbiomac.2004.03.003 · DOI
  27. Hadjebi, 2008, The RCC1 Superfamily: From Genes, to Function, to Disease, Biochimica Biophysica Acta (BBA) - Mol. Cell Res., 1783, 1467, 10.1016/j.bbamcr.2008.03.015 · DOI
  28. Hernandez Alvarez, 2019, Structural Diversity of Coiled Coils in Protein Fibers of the Bacterial Cell Envelope, Int. J. Med. Microbiol., 309, 351, 10.1016/J.IJMM.2019.05.011 · DOI
  29. Hester, 1996, The Mannose-specific Bulb Lectin fromGalanthus nivalis(Snowdrop) Binds Mono- and Dimannosides at Distinct Sites. Structure Analysis of Refined Complexes at 2.3 Å and 3.0 Å Resolution, J. Mol. Biol., 262, 516, 10.1006/jmbi.1996.0532 · DOI
  30. Hiramatsu, 2003, The Structure and Function of Human Dipeptidyl Peptidase IV, Possessing a Unique Eight-Bladed β-propeller Fold, Biochem. Biophysical Res. Commun., 302, 849, 10.1016/S0006-291X(03)00258-4 · DOI
  31. Jawad, 2002, Novel Sequences Propel Familiar Folds, Structure, 10, 447, 10.1016/S0969-2126(02)00750-5 · DOI
  32. Kaus, 2019, The 1.9 Å Crystal Structure of the Extracellular Matrix Protein Bap1 from Vibrio cholerae Provides Insights into Bacterial Biofilm Adhesion, J. Biol. Chem., 294, 14499, 10.1074/jbc.RA119.008335 · DOI
  33. Kim, 2011, Crystal Structure of Escherichia coli BamB, a Lipoprotein Component of the β-Barrel Assembly Machinery Complex, J. Mol. Biol., 406, 667, 10.1016/j.jmb.2010.12.020 · DOI
  34. Kopec, 2013, β-Propeller Blades as Ancestral Peptides in Protein Evolution, PLoS ONE, 8, e77074, 10.1371/journal.pone.0077074 · DOI
  35. Levasseur, 2011, The Role of Duplications in the Evolution of Genomes Highlights the Need for Evolutionary-Based Approaches in Comparative Genomics, Biol. Direct, 6, 11, 10.1186/1745-6150-6-11 · DOI
  36. Makarova, 2019, Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts, mBio, 10, e00715, 10.1128/mBio.00715-19 · DOI
  37. Matsushima, 2005, Leucine-Rich Repeats (LRRs): Structure, Function, Evolution and Interaction with Ligands, Ddro, 2, 305, 10.2174/1567269054087613 · DOI
  38. Mirdita, 2021, ColabFold - Making Protein Folding Accessible to All, bioRxiv, 10.1101/2021.08.15.456425 · DOI · Paper page
  39. Ochiai, 2007, A Novel Structural Fold in Polysaccharide Lyases, J. Biol. Chem., 282, 37134, 10.1074/jbc.M704663200 · DOI
  40. Ochiai, 2009, Structural Determinants Responsible for Substrate Recognition and Mode of Action in Family 11 Polysaccharide Lyases, J. Biol. Chem., 284, 10181, 10.1074/jbc.M807799200 · DOI
  41. Oubrie, 1999, Structure and Mechanism of Soluble Quinoprotein Glucose Dehydrogenase, EMBO J., 18, 5187, 10.1093/emboj/18.19.5187 · DOI
  42. Park, 1998, Cloning and Heterologous Expression of the Gene for BLIP-II, a -Lactamase-Inhibitory Protein from Streptomyces Exfoliatus SMF19, Microbiology, 144, 2161, 10.1099/00221287-144-8-2161 · DOI
  43. Pei, 2014, PROMALS3D: Multiple Protein Sequence Alignment Enhanced with Evolutionary and Three-Dimensional Structural Information, Methods Mol. Biol., 1079, 263, 10.1007/978-1-62703-646-7_17 · DOI
  44. Pereira, 2021, The VCBS Superfamily Forms a Third Supercluster of β-propellers that Includes Tachylectin and Integrins, Bioinformatics, 36, 5618, 10.1093/bioinformatics/btaa1085 · DOI
  45. Polgár, 2002, The Prolyl Oligopeptidase Family, Cell. Mol. Life Sci., 59, 349, 10.1007/s00018-002-8427-5 · DOI
  46. Pons, 2003, Beta-propellers: Associated Functions and Their Role in Human Diseases, Cmc, 10, 505, 10.2174/0929867033368204 · DOI
  47. Quistgaard, 2009, Sequence and Structural Analysis of the Asp-Box Motif and Asp-Box Beta-Propellers; a Widespread Propeller-type Characteristic of the Vps10 Domain Family and Several Glycoside Hydrolase Families, BMC Struct. Biol., 9, 46, 10.1186/1472-6807-9-46 · DOI
  48. Rigden, 2004, The DxDxDG Motif for Calcium Binding: Multiple Structural Contexts and Implications for Evolution, J. Mol. Biol., 343, 971, 10.1016/j.jmb.2004.08.077 · DOI
  49. Rigden, 2011, New Structural and Functional Contexts of the Dx[DN]xDG Linear Motif: Insights into Evolution of Calcium-Binding Proteins, PLoS ONE, 6, e21507, 10.1371/journal.pone.0021507 · DOI
  50. Smock, 2016, De Novo Evolutionary Emergence of a Symmetrical Protein Is Shaped by Folding Constraints, Cell, 164, 476, 10.1016/j.cell.2015.12.024 · DOI
  51. Söding, 2003, More Than the Sum of Their Parts: on the Evolution of Proteins from Peptides, BioEssays, 25, 837, 10.1002/bies.10321 · DOI · Paper page
  52. Söding, 2005, Protein Homology Detection by HMM-HMM Comparison, Bioinformatics, 21, 951, 10.1093/bioinformatics/bti125 · DOI
  53. Stevens, 2008, RCC1-like Repeat Proteins: A Pangenomic, Structurally Diverse New Superfamily of β-propeller Domains, Proteins, 70, 378, 10.1002/prot.21521 · DOI
  54. Studer, 2020, QMEANDisCo-Distance Constraints Applied on Model Quality Estimation, Bioinformatics, 36, 1765, 10.1093/bioinformatics/btz828 · DOI
  55. Varnay, 2009, Investigations on the 100 kDa Homohexameric Protein Ph1500 by NMR Spectroscopy
  56. Vrancken, 2020, Molecular Assemblies Built with the Artificial Protein Pizza, J. Struct. Biol. X, 4, 100027, 10.1016/j.yjsbx.2020.100027 · DOI
  57. Waterhouse, 2018, SWISS-MODEL: Homology Modelling of Protein Structures and Complexes, Nucleic Acids Res., 46, W296, 10.1093/nar/gky427 · DOI
  58. Yadid, 2011, Functional β-propeller Lectins by Tandem Duplications of Repetitive Units, Narnia, 24, 185, 10.1093/protein/gzq053 · DOI
  59. Yadid, 2007, Reconstruction of Functional β-Propeller Lectins via Homo-Oligomeric Assembly of Shorter Fragments, J. Mol. Biol., 365, 10, 10.1016/j.jmb.2006.09.055 · DOI
  60. Zhu, 2016, Origin of a Folded Repeat Protein from an Intrinsically Disordered Ancestor, eLife, 5, 551, 10.7554/eLife.16761 · DOI
  61. Zimmermann, 2018, A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core, J. Mol. Biol., 430, 2237, 10.1016/j.jmb.2017.12.007 · DOI · Paper page

Metadata

Authors
Pereira, J., & Lupas, A. N.
Affiliations
Max Planck Institute for Biology (DE)
Corresponding author
  • Pereira, Joana
  • Lupas, Andrei N.
Venue
Frontiers in Molecular Biosciences
Published
2022-06-09
Volume
9
Pages
895496-895496
ISSN
2296-889X (ISSN-L)
OpenAlex
W4281991817
Cited by
8
References
2
Citations by year
2026: 2 · 2025: 2 · 2024: 4
FWCI
0.49
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Molecular Biosciences (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
Max-Planck-Gesellschaft
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
beta-propeller, protein evolution, sequence divergence, supersecondary structure, common ancestor, DNA sequence comparison

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review