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Protein & Peptide Letters


ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

β Pore-forming Protein-based Evolutionary Divergence of Gnathostomata from Agnatha

Author(s): Bhupendra Kumar, Mohd Kashif*, Ahad Amer Alsaiari, Mohammad Imran Khan, Abul Kalam, Abrar Ahmad, Rayees Ahmad Lone, Mazen Almehmadi, Shivanand Suresh Dudhagi and Mazin A Zamzami

Volume 30, Issue 8, 2023

Published on: 17 August, 2023

Page: [679 - 689] Pages: 11

DOI: 10.2174/0929866530666230726100916

Price: $65


Introduction: The first vertebrates were jawless fish, or Agnatha, whose evolution diverged into jawed fish, or Gnathostomes, around 550 million years ago.

Methods: In this study, we investigated β PFT proteins' evolutionary divergence of lamprey immune protein from Agnatha, reportedly possessing anti-cancer activity, into Dln1 protein from Gnathostomes. Both proteins showed structural and functional divergence, and shared evolutionary origin. Primary, secondary and tertiary sequences were compared to discover functional domains and conserved motifs in order to study the evolution of these two proteins. The structural and functional information relevant to evolutionary divergence was revealed using hydrophobic cluster analysis.

Results: The findings demonstrate that two membrane proteins with only a small degree of sequence identity can have remarkably similar hydropathy profiles, pointing towards conserved and similar global structures. When facing the lipid bilayer or lining the pore lumen, the two proteins' aerolysin domains' corresponding residues displayed a similar and largely conserved pattern. Aerolysin-like proteins from different species can be identified using a fingerprint created by PIPSA analysis of the pore-forming protein.

Conclusion: We were able to fully understand the mechanism of action during pore formation through structural studies of these proteins.

Keywords: Aerolysin, gnathostome, agnatha, hydropathy, divergence, origin.

Graphical Abstract
Brazeau, M.D.; Friedman, M. The origin and early phylogenetic history of jawed vertebrates. Nature, 2015, 520(7548), 490-497.
[] [PMID: 25903631]
Conlon, J.M. Host-defense peptides of the skin with therapeutic potential: From hagfish to human. Peptides, 2015, 67, 29-38.
[] [PMID: 25794853]
Srikulnath, K.; Ahmad, S.F.; Singchat, W.; Panthum, T. Why do some vertebrates have microchromosomes? Cells, 2021, 10(9), 2182.
[] [PMID: 34571831]
Shimeld, S.M.; Donoghue, P.C.J. Evolutionary crossroads in developmental biology: Cyclostomes (lamprey and hagfish). Development, 2012, 139(12), 2091-2099.
[] [PMID: 22619386]
Donoghue, P.C.J.; Sansom, I.J.; Downs, J.P. Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development. J. Exp. Zoolog. B Mol. Dev. Evol., 2006, 306B(3), 278-294.
[] [PMID: 16555304]
Matsushita, M. The complement system of agnathans. Front. Immunol., 2018, 9, 1405.
[] [PMID: 29967624]
Nonaka, M.; Kimura, A. Genomic view of the evolution of the complement system. Immunogenetics, 2006, 58(9), 701-713.
[] [PMID: 16896831]
Abou Chakra, M.; Hall, B.K.; Stone, J.R. Using information in taxonomists’ heads to resolve hagfish and lamprey relationships and recapitulate craniate–vertebrate phylogenetic history. Hist. Biol., 2014, 26(5), 652-660.
Bally-Cuif, L.; Vernier, P. Organization and physiology of the zebrafish nervous system. Fish Physiol., 2010, 29, 25-80.
Montgomery, J.; Bodznick, D. Evolution of the cerebellar sense of self; Oxford University Press, 2016.
Zardoya, R. Phylogeny and evolution of the major intrinsic protein family. Biol. Cell, 2005, 97(6), 397-414.
[] [PMID: 15850454]
Bowen, B.W.; Collette, B.B.; Facey, D.E.; Helfman, G.S. The Diversity of Fishes: Biology, Evolution and Ecology; John Wiley & Sons, Hoboken, New Jersey, U.S., 2022.
Hall, B.K. Evolutionary developmental biology; Springer Science & Business Media, Heidelberg, Germany, 2012.
Schmitt-Ulms, G.; Ehsani, S.; Watts, J.C.; Westaway, D.; Wille, H. Evolutionary descent of prion genes from the ZIP family of metal ion transporters. PLoS One, 2009, 4(9), e7208.
[] [PMID: 19784368]
Roy, A.; Yang, J.; Zhang, Y. COFACTOR: An accurate comparative algorithm for structure-based protein function annotation. Nucleic Acids Res., 2012, 40(W1), W471-W477.
[] [PMID: 22570420]
Parmagnani, A.S.; D’Alessandro, S.; Maffei, M.E. Iron-sulfur complex assembly: Potential players of magnetic induction in plants. Plant Sci., 2022, 325, 111483.
[] [PMID: 36183809]
Kashif, M.; Bharati, A.P.; Chaturvedi, S.K.; Khan, R.H.; Ahmad, A.; Kumar, B.; Zamzami, M.A.; Ahmad, V.; Kumari, S. pH and alcohol induced structural transition in Ntf2 a nuclear transport factor of Saccharomyces cerevisiae. Int. J. Biol. Macromol., 2020, 159, 79-86.
[] [PMID: 32407943]
Samant, L.R.; Sangar, V.C.; Gulamaliwala, A.; Chowdhary, A.S. Computational modelling and functional characterization of HDAC-11. Int. J. Pharm. Sci. Res., 2015, 49, 1727-1735.
Bharati, A.P.; Kashif, M.; Chaturvedi, S.K.; Khan, R.H.; Ahmad, A. An insight into structural plasticity and conformational transitions of transcriptional co-activator Sus1. PLoS One, 2020, 15(3), e0229216.
[] [PMID: 32134955]
Kashif, M.; Asalam, M.; Al Shehri, S.S.; Kumar, B.; Singh, N.; Akhtar, M.S. Recombinant expression and biophysical characterization of Mrt4 protein that involved in mRNA turnover and ribosome assembly from Saccharomyces cerevisiae. Bioengineered, 2022, 13(4), 9103-9113.
[] [PMID: 35387555]
Jia, N.; Liu, N.; Cheng, W.; Jiang, Y.L.; Sun, H.; Chen, L.L.; Peng, J.; Zhang, Y.; Ding, Y.H.; Zhang, Z.H.; Wang, X.; Cai, G.; Wang, J.; Dong, M.Q.; Zhang, Z.; Wu, H.; Wang, H.W.; Chen, Y.; Zhou, C.Z. Structural basis for receptor recognition and pore formation of a zebrafish aerolysin-like protein. EMBO Rep., 2016, 17(2), 235-248.
[] [PMID: 26711430]
Eddie Ip, W.K.; Takahashi, K.; Alan Ezekowitz, R.; Stuart, L.M. Mannose-binding lectin and innate immunity. Immunol. Rev., 2009, 230(1), 9-21.
[] [PMID: 19594626]
Takahashi, K. Mannose-binding lectin and the balance between immune protection and complication. Expert Rev. Anti Infect. Ther., 2011, 9(12), 1179-1190.
[] [PMID: 22114968]
Wu, F.; Feng, B.; Ren, Y.; Wu, D.; Chen, Y.; Huang, S.; Chen, S.; Xu, A. A pore-forming protein implements VLR-activated complement cytotoxicity in lamprey. Cell Discov., 2017, 3(1), 17033.
[] [PMID: 28944078]
Pang, Y.; Gou, M.; Yang, K.; Lu, J.; Han, Y.; Teng, H.; Li, C.; Wang, H.; Liu, C.; Zhang, K.; Yang, Y.; Li, Q. Crystal structure of a cytocidal protein from lamprey and its mechanism of action in the selective killing of cancer cells. Cell Commun. Signal., 2019, 17(1), 54.
[] [PMID: 31133022]
Olson, R.; Gouaux, E. Vibrio cholerae cytolysin is composed of an α-hemolysin-like core. Protein Sci., 2003, 12(2), 379-383.
[] [PMID: 12538902]
Smedley, J.G., III Investigating the Molecular Mechanism of action of Clostridium perfringens enterotoxin using structure-function and oligomeric analyses. Doctoral dissertation, University of Pittsburgh, 2007.
Ogbu, C.P.; Roy, S.; Vecchio, A.J. Disruption of claudin-made tight junction barriers by Clostridium perfringens enterotoxin: Insights from structural biology. Cells, 2022, 11(5), 903.
[] [PMID: 35269525]
Yu, J.; Zhou, Y.; Engelhard, M.; Zhang, Y.; Son, J.; Liu, S.; Zhu, Z.; Yu, X.Y. In situ molecular imaging of adsorbed protein films in water indicating hydrophobicity and hydrophilicity. Sci. Rep., 2020, 10(1), 3695.
[] [PMID: 32111945]
Escribá, P.V. Membrane-lipid therapy: A historical perspective of membrane-targeted therapies — From lipid bilayer structure to the pathophysiological regulation of cells. Biochim. Biophys. Acta Biomembr., 2017, 1859(9), 1493-1506.
[] [PMID: 28577973]
Kastritis, P.L.; Visscher, K.M.; van Dijk, A.D.J.; Bonvin, A.M.J.J. Solvated protein-protein docking using Kyte-Doolittle-based water preferences. Proteins, 2013, 81(3), 510-518.
[] [PMID: 23161727]
Huang, F.; Oldfield, C.J.; Xue, B.; Hsu, W.L.; Meng, J.; Liu, X.; Shen, L.; Romero, P.; Uversky, V.N.; Dunker, A.K. Improving protein order-disorder classification using charge-hydropathy plots. BMC Bioinformatics, 2014, 15(S17), S4.
[] [PMID: 25559583]
Radivojac, P.; Vacic, V.; Haynes, C.; Cocklin, R.R.; Mohan, A.; Heyen, J.W.; Goebl, M.G.; Iakoucheva, L.M. Identification, analysis, and prediction of protein ubiquitination sites. Proteins, 2010, 78(2), 365-380.
[] [PMID: 19722269]
Phatak, M. Lipid accessibility prediction and identification of functional hotspots in transmembrane proteins; University of Cincinnati, 2010.
Shi, S.P.; Sun, X.Y.; Qiu, J.D.; Suo, S.B.; Chen, X.; Huang, S.Y.; Liang, R.P. The prediction of palmitoylation site locations using a multiple feature extraction method. J. Mol. Graph. Model., 2013, 40, 125-130.
[] [PMID: 23419766]
Gänger, S.; Schindowski, K. Tailoring formulations for intranasal nose-to-brain delivery: A review on architecture, physico-chemical characteristics and mucociliary clearance of the nasal olfactory mucosa. Pharmaceutics, 2018, 10(3), 116.
[] [PMID: 30081536]
Farheen, S.; Oanz, A.M.; Khan, N.; Umar, M.S.; Jamal, F.; Kashif, M.; Owais, M. Antimicrobial effect of nano-silver against oral streptococci: Implications in containment of bacterial biofilm on orthodontal appliances. Preprints, 2021, 2021020436.
Righetto, I.; Milani, A.; Cattoli, G.; Filippini, F. Comparative structural analysis of haemagglutinin proteins from type A influenza viruses: Conserved and variable features. BMC Bioinformatics, 2014, 15(1), 363.
[] [PMID: 25492298]
Gemayel, R.; Vinces, M.D.; Legendre, M.; Verstrepen, K.J. Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu. Rev. Genet., 2010, 44(1), 445-477.
[] [PMID: 20809801]
Bharati, A.P.; Singh, N.; Kumar, V.; Kashif, M.; Singh, A.K.; Singh, P.; Singh, S.K.; Siddiqi, M.I.; Tripathi, T.; Akhtar, M.S. The mRNA capping enzyme of Saccharomyces cerevisiae has dual specificity to interact with CTD of RNA Polymerase II. Sci. Rep., 2016, 6(1), 31294.
[] [PMID: 27503426]
Kashif, M.; Kumar, B.; Bharati, A.P.; Altayeb, H.; Asalam, M.; Akhtar, M.S.; Khan, M.I.; Ahmad, A.; Chaudhary, H.; Hosawi, S.B.; Zamzami, M.A.; Baothman, O.A. Association of peptidyl prolyl cis/trans isomerase Rrd1 with C terminal domain of RNA polymerase II. Int. J. Biol. Macromol., 2023, 242(Pt 1), 124653.
[] [PMID: 37141964]
Iacovache, I.; De Carlo, S.; Cirauqui, N.; Dal Peraro, M.; van der Goot, F.G.; Zuber, B. Cryo-EM structure of aerolysin variants reveals a novel protein fold and the pore-formation process. Nat. Commun., 2016, 7(1), 12062.
[] [PMID: 27405240]
Yilmaz, N.; Yamaji-Hasegawa, A.; Hullin-Matsuda, F.; Kobayashi, T. Molecular mechanisms of action of sphingomyelin-specific pore-forming toxin, lysenin. Semin. Cell Dev. Biol., 2018, 73, 188-198.
[] [PMID: 28751253]
Nonaka, S.; Salim, E.; Kamiya, K.; Hori, A.; Nainu, F.; Asri, R.M.; Masyita, A.; Nishiuchi, T.; Takeuchi, S.; Kodera, N.; Kuraishi, T. Molecular and functional analysis of pore-forming toxin monalysin from entomopathogenic bacterium Pseudomonas entomophila. Front. Immunol., 2020, 11, 520.
[] [PMID: 32292407]
Tong, R.; Wade, R.C.; Bruce, N.J. Comparative electrostatic analysis of adenylyl cyclase for isoform dependent regulation properties. Proteins, 2016, 84(12), 1844-1858.
[] [PMID: 27667304]
Stein, M.; Pilli, M.; Bernauer, S.; Habermann, B. H.; Zerial, M.; Wade, R. C. The interaction properties of the human RabGTPase family–A comparative analysis reveals determinants of molecular binding selectivity. PloS one, 2012, 7(4)

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