Ecological geneticsEcological geneticsЭкологическая генетика1811-09322411-9202Eco-Vector69984010.17816/ecogen699840Genetic basis of ecosystems evolutionГенетические основы эволюции экосистемDifferences in the intron-retaining fragment of the shortened isoform of the NXF1 protein in different representatives of RodentiaРазличия соответствующего интрону фрагмента укороченной изоформы белка NXF1 у различных представителей Rodentiahttps://orcid.org/0000-0003-0265-57598162-8441BondarukDmitrii D.БондарукДмитрий Денисович
Russian Federation

Applican, Department of Genetics and Biotechnology.

Соискатель, младший научный сотрудник кафедры генетики и биотехнологии.

D.D.Bondaruk@yandex.ruhttps://orcid.org/0000-0002-9528-57607386-1230GolubkovaElena V.ГолубковаЕлена Валерьевна
Russian Federation

Cand. Sci. (Biology)

Кандидат биологических наук

e.golubkova@spbu.ruhttps://orcid.org/0000-0001-5338-07037780-6907MamonLudmila A.МамонЛюдмила Андреевна
Russian Federation

Doctor of Sci. (Biology)

Доктор биологических наук

lmamon46@mail.ruhttps://orcid.org/0009-0002-0025-66316211-7251PelleDaria I.ПеллеДарья Ивановна
Russian Federation

Bachelor

Бакалавр, студент-магистрант.

kaisa23@ya.ruFederal State Budgetary Educational Institution of Higher Education "Saint-Petersburg State University"Федеральное государственное бюджетное образовательное учреждение высшего образования «Санкт-Петербургский государственный университет»ITMO University, Saint Petersburg, RussiaФедеральное государственное автономное образовательное учреждение высшего образования «Национальный исследовательский университет ИТМО»050520262422812202518032026Copyright ©; , Eco-VectorCopyright ©; , Эко-ВекторEco-VectorЭко-Векторhttps://eco-vector.com/for_authors.php#07https://journals.eco-vector.com/ecolgenet/article/view/699840

AIM:

The aim of this study was to analyze the species specificity of the sequence of the C-terminal fragment of the sNXF1 protein translated from the intron.

METHODS:

The study was performed using in silico methods, using the sequences of the Nxf1 gene of thirty-three representatives of the order Rodentia as materials, obtained from publicly available databases and NCBI data.

RESULTS:

The analysis revealed that the C-terminal fragments of the sNXF1 of some representatives of the Rodentia order are of increased length. It was found that the cause of these extended fragments in all cases was the deletion of cytosine nucleotide. In all identified cases, regardless of the systematic position of the species, the extended fragment contains a sequence of conserved 13 a.a.

CONCLUSION:

The obtained results indicate that the analyzed sequence fragment does not influence the conformation of the protein sNxf1 in general. However, since the fragment has a specific folding pattern, it might define a set of RNP-complex partners.

Цель

Проанализировать видоспецифичность последовательности C-концевого фрагмента белка sNXF1, транслируемого с интрона.

Методы

Вся работа проводилась методами in silico, в качестве материала использовались последовательности гена Nxf1 тридцати трёх представителей отряда Rodentia, полученные из общедоступных баз, данных NCBI.

Результаты

В результате анализа выявлено, что C-терминальные фрагменты sNXF1 у некоторых представителей отряда Rodentia имеют увеличенную длину. Установлено, что причиной появления этих удлиненных фрагментов во всех случаях выступала делеция цитозина в интроне гена Nxf1. Во всех выявленных случаях, независимо от систематического положения вида, удлиненный фрагмент содержит последовательность из консервативных 13 а.о.

Выводы

Полученные результаты свидетельствуют о том, что анализируемый фрагмент последовательности не изменяет конформацию белка sNxf1 в целом. Однако, поскольку исследуемый фрагмент имеет специфический паттерн укладки, он потенциально может повлиять на взаимодействие с белками-партнёрами для образования РНП-комплексов.

RodentiaNucleocytoplasmic Transport ProteinsRNA-Binding ProteinsSequence AlignmentSequence Analysis.RodentiaNucleocytoplasmic Transport ProteinsRNA-Binding ProteinsSequence AlignmentSequence Analysis.SPbUСПбГУ124032000041-1Исследование выполнено при финансовой поддержке гранта СПбГУ “Изучение генетических основ внутривидовой изменчивости, надорганизменных взаимодействий и таксономического разнообразия с использованием биоресурсных коллекций” (шифр проекта 124032000041-1). Россия.1. Herold A, Suyama M, Rodrigues JP, Braun IC, Kutay U, Carmo-Fonseca M, Bork P, Izaurralde E. TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol Cell Biol. 2000 Dec;20(23):8996-9008. doi: 10.1128/MCB.20.23.8996-9008.2000. PMID: 11073998; PMCID: PMC86553.2. Herold A, Klymenko T, Izaurralde E. NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila. RNA. 2001 Dec;7(12):1768-80. PMID: 11780633; PMCID: PMC1370216.3. Tan W, Zolotukhin AS, Bear J, Patenaude DJ, Felber BK. The mRNA export in Caenorhabditis elegans is mediated by Ce-NXF-1, an ortholog of human TAP/NXF and Saccharomyces cerevisiae Mex67p. RNA. 2000 Dec;6(12):1762-72. doi: 10.1017/s1355838200000832. PMID: 11142376; PMCID: PMC1370046.4. Segref A, Sharma K, Doye V, Hellwig A, Huber J, Lührmann R, Hurt E. Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J. 1997 Jun 2;16(11):3256-71. doi: 10.1093/emboj/16.11.3256. PMID: 9214641; PMCID: PMC1169942.5. Thakurta AG, Gopal G, Yoon JH, Saha T, Dhar R. Conserved nuclear export sequences in Schizosaccharomyces pombe Mex67 and human TAP function in mRNA export by direct nuclear pore interactions. J Biol Chem. 2004 Apr 23;279(17):17434-42. doi: 10.1074/jbc.M309731200. Epub 2004 Feb 12. PMID: 14963046.6. Katahira J, Strässer K, Podtelejnikov A, Mann M, Jung JU, Hurt E. The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. EMBO J. 1999 May 4;18(9):2593-609. doi: 10.1093/emboj/18.9.2593. PMID: 10228171; PMCID: PMC1171339.7. Dostalova A, Käser S, Cristodero M, Schimanski B. The nuclear mRNA export receptor Mex67-Mtr2 of Trypanosoma brucei contains a unique and essential zinc finger motif. Mol Microbiol. 2013 May;88(4):728-39. doi: 10.1111/mmi.12217. Epub 2013 Apr 8. PMID: 23560737.8. Hegedűsová E, Kulkarni S, Burgman B, Alfonzo JD, Paris Z. The general mRNA exporters Mex67 and Mtr2 play distinct roles in nuclear export of tRNAs in Trypanosoma brucei. Nucleic Acids Res. 2019 Sep 19;47(16):8620-8631. doi: 10.1093/nar/gkz671. PMID: 31392978; PMCID: PMC6794378.9. Al Jewari C, Baldauf SL. An excavate root for the eukaryote tree of life. Sci Adv. 2023 Apr 28;9(17):eade4973. doi: 10.1126/sciadv.ade4973. Epub 2023 Apr 28. PMID: 37115919; PMCID: PMC10146883.10. Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, Cárdenas P, Čepička I, Chistyakova L, Del Campo J, Dunthorn M, Edvardsen B, Eglit Y, Guillou L, Hampl V, Heiss AA, Hoppenrath M, James TY, Karnkowska A, Karpov S, Kim E, Kolisko M, Kudryavtsev A, Lahr DJG, Lara E, Le Gall L, Lynn DH, Mann DG, Massana R, Mitchell EAD, Morrow C, Park JS, Pawlowski JW, Powell MJ, Richter DJ, Rueckert S, Shadwick L, Shimano S, Spiegel FW, Torruella G, Youssef N, Zlatogursky V, Zhang Q. Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes. J Eukaryot Microbiol. 2019 Jan;66(1):4-119. doi: 10.1111/jeu.12691. PMID: 30257078; PMCID: PMC6492006.11. Grüter P, Tabernero C, von Kobbe C, Schmitt C, Saavedra C, Bachi A, Wilm M, Felber BK, Izaurralde E. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell. 1998 Apr;1(5):649-59. doi: 10.1016/s1097-2765(00)80065-9. PMID: 9660949.12. Kang Y, Cullen BR. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 1999 May 1;13(9):1126-39. doi: 10.1101/gad.13.9.1126. PMID: 10323864; PMCID: PMC316956.Kang Y, Cullen BR. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 1999 May 1;13(9):1126-39. doi: 10.1101/gad.13.9.1126. PMID: 10323864; PMCID: PMC316956.13. Li Y, Bor YC, Misawa Y, Xue Y, Rekosh D, Hammarskjöld ML. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature. 2006 Sep 14;443(7108):234-7. doi: 10.1038/nature05107. PMID: 16971948.14. Ivankova N, Tretyakova I, Lyozin GT, Avanesyan E, Zolotukhin A, Zatsepina OG, Evgen'ev MB, Mamon LA. Alternative transcripts expressed by small bristles, the Drosophila melanogaster nxf1 gene. Gene. 2010 Jun 15;458(1-2):11-9. doi: 10.1016/j.gene.2010.02.013. Epub 201015. Мамон Л.А., Кливер С.Ф., Просовская А.О., Гинанова В.Р., Голубкова Е.В. Интрон-содержащий транскрипт — эволюционно-консервативная особенность генов-ортологов nxf1 (nuclear export factor) // Экологическая генетика. - 2013. - Т. 11. - №3. - C. 3-13. doi: 10.17816/ecogen1133-1316. Li Y, Bor YC, Fitzgerald MP, Lee KS, Rekosh D, Hammarskjold ML. An NXF1 mRNA with a retained intron is expressed in hippocampal and neocortical neurons and is translated into a protein that functions as an Nxf1 cofactor. Mol Biol Cell. 2016 Dec 1;27(24):3903-3912. doi: 10.1091/mbc.E16-07-0515. Epub 2016 Oct 5. PMID: 27708137; PMCID: PMC5170612.17. Aibara S, Katahira J, Valkov E, Stewart M. The principal mRNA nuclear export factor NXF1:NXT1 forms a symmetric binding platform that facilitates export of retroviral CTE-RNA. Nucleic Acids Res. 2015 Feb 18;43(3):1883-93. doi: 10.1093/nar/gkv032. Epub 2015 Jan 27. PMID: 25628361; PMCID: PMC4330390.18. Yakimova AO, Pugacheva OM, Golubkova EV, Mamon LA. Cytoplasmic localization of SBR (Dm NXF1) protein and its zonal distribution in the ganglia of Drosophila melanogaster larvae. Invert Neurosci. 2016 Sep;16(3):9. doi: 10.1007/s10158-016-0192-5. Epub 2016 Jul 7. PMID: 27389771.19. Gene [Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; 2004 – [cited 2023 05 26]. Available from: https://www.ncbi.nlm.nih.gov/gene/20. Hall, T.A. (1999). BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT.21. Kumar S., Stecher G., Li M., et al. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms // Mol Biol EVol. 2018. Vol. 35, No. 6. P. 1547–1549. DOI: 10.1093/molbev/msy09622. Edgar R.C. MUSCLE: multiple sequence alignment with high ac-curacy and high throughput // Nucleic Acids Res. 2004. Vol. 32, No. 5. P. 1792–1797. DOI: 10.1093/nar/gkh34023. Michener C.D., Sokal R.R. A quantitative approach to a problem in classification // Evolution. 1957. Vol. 11, No. 2. P. 130–162. DOI: 10.1111/j.1558-5646.1957.tb02884.x24. Okonechnikov K, Golosova O, Fursov M; UGENE team. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. 2012;28(8):1166-1167. doi:10.1093/bioinformatics/bts09125. Waterhouse A., Bertoni M, Bienert S, et al,, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Research, Volume 46, Issue W1, 2 July 2018, Pages W296–W303, doi.org/10.1093/nar/gky42726. Maddison, W. P. and D.R. Maddison. 2021. Mesquite: a modular system for evolutionary analysis. Version 3.70 http://www.mesquiteproject.org27. Huelsenbeck, J. P. and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754-755. Ronquist, F. and J. P. Huelsenbeck. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.28. Rambaut, A. FigTree v1.3.1. [Internet] Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. 2006– . [cited 2025 June 29] Available from: http://tree.bio.ed.ac.uk/software/figtree/29. Rodríguez F, Oliver JL, Marín A, Medina JR. The general stochastic model of nucleotide substitution. J Theor Biol. 1990;142(4):485-501. doi:10.1016/s0022-5193(05)80104-330. Lanave, C., Preparata, G., Sacone, C. et al. A new method for calculating evolutionary substitution rates. J Mol Evol 20, 86–93 (1984). https://doi.org/10.1007/BF0210199031. X Gu, Y X Fu, W H Li, Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites., Molecular Biology and Evolution, Volume 12, Issue 4, July 1995, Pages 546–557, https://doi.org/10.1093/oxfordjournals.molbev.a04023532. Doronina, L., Matzke, A., Churakov, G. et al. The Beaver’s Phylogenetic Lineage Illuminated by Retroposon Reads. Sci Rep 7, 43562 (2017). https://doi.org/10.1038/srep4356233. Churakov G, Sadasivuni MK, Rosenbloom KR, Huchon D, Brosius J, Schmitz J. Rodent evolution: back to the root. Mol Biol Evol. 2010 Jun;27(6):1315-26. doi: 10.1093/molbev/msq019. Epub 2010 Jan 25. PMID: 20100942.34. Steppan SJ, Schenk JJ. Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS One. 2017 Aug 16;12(8):e0183070. doi: 10.1371/journal.pone.0183070. PMID: 28813483; PMCID: PMC5559066.35. Gupta RS, Suggett C. Conserved Signatures in Protein Sequences Reliably Demarcate Different Clades of Rodents/Glires Species and Consolidate Their Evolutionary Relationships. Genes (Basel). 2022 Feb 1;13(2):288. doi: 10.3390/genes13020288. PMID: 35205335; PMCID: PMC8871558.36. Blanga-Kanfi S, Miranda H, Penn O, Pupko T, DeBry RW, Huchon D. Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol Biol. 2009 Apr 2;9:71. doi: 10.1186/1471-2148-9-71. PMID: 19341461; PMCID: PMC2674048.37. Fabre PH, Hautier L, Dimitrov D, Douzery EJ. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol Biol. 2012 Jun 14;12:88. doi: 10.1186/1471-2148-12-88. PMID: 22697210; PMCID: PMC3532383.38. Swanson MT, Oliveros CH, Esselstyn JA. A phylogenomic rodent tree reveals the repeated evolution of masseter architectures. Proc Biol Sci. 2019 May 15;286(1902):20190672. doi: 10.1098/rspb.2019.0672. PMID: 31064307; PMCID: PMC6532498.39. Guillermo D’Elía, Pierre-Henri Fabre, Enrique P Lessa, Rodent systematics in an age of discovery: recent advances and prospects, Journal of Mammalogy, Volume 100, Issue 3, 23 May 2019, Pages 852–871, https://doi.org/10.1093/jmammal/gyy17940. Gupta RS, Suggett C. Conserved Signatures in Protein Sequences Reliably Demarcate Different Clades of Rodents/Glires Species and Consolidate Their Evolutionary Relationships. Genes (Basel). 2022 Feb 1;13(2):288. doi: 10.3390/genes13020288. PMID: 35205335; PMCID: PMC8871558.41. Stanyon R, Stone G, Garcia M, Froenicke L. Reciprocal chromosome painting shows that squirrels, unlike murid rodents, have a highly conserved genome organization. Genomics. 2003 Aug;82(2):245-9. doi: 10.1016/s0888-7543(03)00109-5. PMID: 1283727442. Gossmann TI, Shanmugasundram A, Börno S, Duvaux L, Lemaire C, Kuhl H, Klages S, Roberts LD, Schade S, Gostner JM, Hildebrand F, Vowinckel J, Bichet C, Mülleder M, Calvani E, Zelezniak A, Griffin JL, Bork P, Allaine D, Cohas A, Welch JJ, Timmermann B, Ralser M. Ice-Age Climate Adaptations Trap the Alpine Marmot in a State of Low Genetic Diversity. Curr Biol. 2019 May 20;29(10):1712-1720.e7. doi: 10.1016/j.cub.2019.04.020. Epub 2019 May 9. PMID: 31080084; PMCID: PMC6538971.43. Katahira J, Dimitrova L, Imai Y, Hurt E. NTF2-like domain of Tap plays a critical role in cargo mRNA recognition and export. Nucleic Acids Res. 2015 Feb 18;43(3):1894-904. doi: 10.1093/nar/gkv039. Epub 2015 Jan 27. PMID: 25628355; PMCID: PMC4330393.44. Bachi A, Braun IC, Rodrigues JP, Panté N, Ribbeck K, von Kobbe C, Kutay U, Wilm M, Görlich D, Carmo-Fonseca M, Izaurralde E. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA. 2000 Jan;6(1):136-58. doi: 10.1017/s1355838200991994. PMID: 10668806; PMCID: PMC1369901.