Центральный регуляторный контур системы морфогенеза механорецепторов дрозофилы: эффекты мутаций

Центральный регуляторный контур системы морфогенеза механорецепторов дрозофилы: эффекты мутаций

Фурман Д. П., Бухарина Т. А., Голубятников В. П.
Сибирский журнал индустриальной математики, 26, 3(95), 142-153 (2023)
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УДК 517.958:539.3 
DOI: 10.33048/SIBJIM.2023.26.311

Аннотация:

Описана математическая модель функционирования центрального регуляторного контура генных сетей морфогенеза механорецепторов дрозофилы с учётом мутаций входящих в него генов. Проведены вычислительные эксперименты, показывающие наличие иерархии эффектов мутаций генов ЦРК на продукцию белков ASC.

Литература:
  1. Chasman D., Fotuhi Siahpirani A., Roy S. Network-based approaches for analysis of complex biological systems.Curr. Opin. Biotechnol., 2016. Vol. 39, pp. 157–166; DOI: 10.1016/j.copbio.2016.04.007  
     
  2. Emmert-Streib F., Dehmer M. Networks for systems biology: conceptual connection of data and function. IET Syst. Biol., 2011, Vol. 5, No. 3, pp. 185–207; DOI: 10.1049/iet-syb.2010.0025  
     
  3. Emmert-Streib F., Glazko G. V. Network biology: a direct approach to study biological function. Wiley Interdiscip. Rev. Syst. Biol. Med., 2011, Vol. 3, No. 4, pp. 379–91; DOI: 10.1002/wsbm.134  
     
  4. Schlitt T., Palin K., Rung J., Dietmann S., Lappe M., Ukkonen E., Brazma A. From gene networks to gene function. Genome Res., 2003, Vol. 13, No. 12, pp. 2568–2576; DOI: 10.1101/gr.1111403  
     
  5. Zhu X., Gerstein M., Snyder M. Getting connected: analysis and principles of biological networks. Genes Dev., 2007, Vol. 21, No. 9, pp. 1010–1024. DOI: 10.1101/gad.1528707  
     
  6. Akinshin A. A., Bukharina T. A., Golubyatnikov V. P., Furman D. P. Mathematical modeling of the interaction of two cells in the proneural cluster of the wing imaginal disk D.melanogaster [Matematicheskoe modelirovanie vzaimozheistviya dvukh kletok v proneiral’nom klastere krylovogo imaginal’nogo diska D.melanogaster]. Sib. Zh. Chist. Prikl. Mat., 2014, Vol. 14, No. 4, pp. 3–10 (in Russian).  
     
  7. Bukharina T. A., Furman D. P., Golubyatnikov V. P. A model study of the morphogenesis of D. melanogaster mechanoreceptors: The central regulatory circuit. J. Bioinformat. Comput. Biology, 2015, Vol. 13, No. 1, pp. 1540006-1–1540006-15; DOI: 10.1142/S0219720015400065  
     
  8. Ayupova N. B., Golubyatnikov V. P. A Three-cell Model of the Initial Stage of Development of a Proneural Cluster. J. Appl. Ind. Math., 2017. Vol. 11, No. 2, pp. 168–173; DOI: 10.1134/S1990478917020028  
     
  9. Buharina T. A., Akin’shin A. A., Golubjatnikov V. P., Furman D. P. Matematicheskaya i chislennaya modeli central’nogo regulyatornogo kontura sistemy morfogeneza mekhanoreceptorov drozofily. [Mathematical and numerical models of the Central Regulatory Circuit of the mechanoreceptors morphogenesis system of Drosophila]. Sib. Zhurn. Indust. Mat., 2020, Vol. 23, No. 2, pp. 41–50 (in Russian); DOI: 10.33048/SIBJIM.2020.23.203  
     
  10. Bukharina T. A., Golubyatnikov V. P., Furman D. P. Gene Network Controlling the Morphogenesis of D. melanogaster Macrochaetes: An Expanded Model of the Central Regulatory Circuit. Russian Journal of Developmental Biology, 2016, Vol. 47, No. 5, pp. 288–293; DOI: 10.1134/S1062360416050040  
     
  11. Yamasaki Y., Lim Y. M., Niwa N., Hayashi S., Tsuda L. Robust specification of sensory neurons by dual functions of charlatan, a Drosophila NRSF/REST-like repressor of extramacrochaetae and hairy. Genes Cells, 2011, Vol. 16, No. 8,. pp. 896–909; DOI: 10.1111/j.1365-2443.2011.01537.x   
     
  12. Garía-Bellido A., de Celis J. F. The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics, 2009, Vol. 182, No. 3, pp. 631–639; https://doi.org/10.1534/genetics.109.104083 
     
  13. Ghysen A., Thomas R. The formation of sense organs in Drosophila: a logical approach. BioEssays, 2003, Vol. 25, pp. 802–807; DOI: 10.1002/bies.10311 
     
  14. Sistemnaja komp’juternaja biologija [System computer biology]. Novosibirsk: Izd-vo SB RAN, 2008 (in Russian).  
     
  15. Golubyatnikov V. P., Kazantsev M. V., Kirillova N. E., Bukharina T. A., Furman D. P. Mathematical and numerical models of two asymmetric gene networks. Sib. Electron. Math. Reports, 2018, Vol. 15, pp. 1271– 1283; DOI: 10.17377/semi.2018.15.103 
     
  16. Akinshin A. A., Ayupova N. B., Golubyatnikov V. P., Kirillova N. E., Podkolodnaya O. A., Podkolodnyy N. L. On a numerical model of a circadian oscillator. Numer. Anal. Appl., 2022, Vol. 15, No. 3, pp. 187–196; DOI: 10.1134/S199542392203001 
     
  17. Golubyatnikov V. P., Akinshin A. A., Ayupova N. B., Minushkina L. S. Stratifications and foliations in phase portraits of gene network models. Vavilov J. Genetics and Breeding, 2022, Vol. 26, No. 8, pp. 758– 764; DOI: 10.18699/VJGB-22-91 
     
  18. Chang P. J., Hsiao Y. L., Tien A. C., Li Y. C., Pi H. Negative-feedback regulation of proneural proteins controls the timing of neural precursor division. Development, 2008, Vol. 135, No. 18, pp. 302–3030; DOI: 10.1242/dev.021923 
     
  19. Anikonov Yu. E., Gölgeleyen $\dot{I}$., Yildiz M. Identification problems for systems of nonlinear evolution equations and functional equations. Adv. Differ. Equ., 2016, Vol. 1, article 152; DOI: 10.1186/s13662-016-0877-4
     
  20. Moscoso del Prado J., García-Bellido A. Genetic regulation of the achaete-scute complex of Drosophila melanogaster. Wilehm Roux Arch. Dev. Biology, 1984, Vol. 193, No. 4, pp. 242–245; DOI: 10.1007/BF01260345 
     
  21. Escudero L. M., Caminero E., Schulze K. L., Bellen H. J., Modolell J. Charlatan, a Zn-finger transcription factor, establishes a novel level of regulation of the proneural achaete/scute genes of Drosophila. Development, 2005, Vol. 132, No. 6, pp. 1211–1222; DOI: 10.1242/dev.01691
     
  22. Nolo R., Abbott L. A., Bellen H. J. Senseless, a Zn-finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell, 2000, Vol. 102, No. 3, pp.349–362; DOI: 10.1016/s0092-8674(00)00040-4
     
  23. Roark M., Sturtevant M. A., Emery J., Vaessin H., Grell E., Bier E. scratch, a pan-neural gene encoding a zinc finger protein related to snail, promotes neuronal development. Genes Dev., 1995, Vol. 9, No. 19, pp. 2384–2398; DOI: 10.1101/gad.9.19.2384
     
  24. Agol I. J. Step Allelomorphism in D. melanogaster. Genetics, 1931, Vol. 16, No. 3, pp. 254–266.
     
  25. Dubinin N. P. Step-allelomorphism in D. melanogaster. The allelomorphs achaete2-scute10, achaete1-scute11 and achaete3-scute13. J. Genet., 1932, Vol. 25, No. 2, pp. 163–181; https://doi.org/10.1007/BF02983250  
     
  26. García-Bellido A., de Celis J. F. The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics, 2009, Vol. 182, No. 3, pp. 631–639; https://doi.org/10.1534/genetics.109.104083
     
  27. Ghysen A., Dambly-Chaudière C. From DNA to form: the achaete-scute complex. Genes Dev., 1988, Vol. 2, No. 5, pp. 495–501; DOI: 10.1101/gad.2.5.495
     
  28. Usui K., Goldstone C., Gibert J. M., Simpson P. Redundant mechanisms mediate bristle patterning on the Drosophila thorax. Proc. Natl. Acad. Sci. USA, 2008, Vol. 105, No. 51, pp. 20112–20117; DOI: 10.1073/pnas.0804282105
     
  29. Cabrera C. V., Alonso M. C., Huikeshoven H. Regulation of scute function by extramacrochaete in vitro and in vivo. Development, 1994, Vol. 120, No. 12, pp. 3595–603; DOI: 10.1242/dev.120.12.3595
     
  30. Acar M., Jafar-Nejad H., Giagtzoglou N., Yallampalli S., David G., He Y., Delidakis C., Bellen H. J. Senseless physically interacts with proneural proteins and functions as a transcriptional co-activator. Development, 2006, Vol. 133, No. 10, pp. 1979–1989; DOI: 10.1242/dev.02372
     
  31. Pi H., Wu H. J., Chien C. T. A dual function of phyllopod in Drosophila external sensory organ development: cell fate specification of sensory organ precursor and its progeny. Development, 2001, Vol. 128, No. 14, pp. 2699–2710; DOI: 10.1242/dev.128.14.2699
     
  32. Ramat A., Audibert A., Louvet-Vallèe S., Simon F., Fichelson P., Gho M. Escargot and Scratch regulate neural commitment by antagonizing Notch activity in Drosophila sensory organs. Development, 2016, Vol. 143, No. 16, pp. 3024–3034; DOI: 10.1242/dev.134387

Работа выполнена в рамках государственного задания ИЦиГ СО РАН (проект FWNR-2022-0020) и государственного задания ИМ СО РАН (проект FWNF-2022-0009).

Д. П. Фурман
  1. Федеральный научно-исследовательский центр Институт цитологии и генетики СО РАН, 
    просп. Лаврентьева, 10, г. Новосибирск 630090, Россия
  2. Новосибирский государственный университет, 
    ул. Пирогова, 1, г. Новосибирск 630090, Россия

E-mail: furman@bionet.nsc.ru

Т. А. Бухарина
  1. Федеральный научно-исследовательский центр Институт цитологии и генетики СО РАН, 
    просп. Лаврентьева, 10, г. Новосибирск 630090, Россия
  2. Новосибирский государственный университет, 
    ул. Пирогова, 1, г. Новосибирск 630090, Россия

E-mail: bukharina@bionet.nsc.ru

В. П. Голубятников
  1. Институт математики им. С. Л. Соболева СО РАН, 
    просп. Акад. Коптюга, 4, г. Новосибирск 630090, Россия

E-mail: vladimir.golubyatnikov1@fulbrightmail.org

Статья поступила 09.02.2023 г.
После доработки — 29.03.2023 г.
Принята к публикации 27.04.2023 г.

Abstract:

A mathematical model of the functioning of the central regulatory circuit of gene networks of morphogenesis of drosophila mechanoreceptors is described, taking into account mutations of its genes. Computational experiments have been carried out showing the presence of a hierarchy of effects of CRK gene mutations on the production of ASC proteins.

References:
  1. Chasman D., Fotuhi Siahpirani A., Roy S. Network-based approaches for analysis of complex biological systems.Curr. Opin. Biotechnol., 2016. Vol. 39, pp. 157–166; DOI: 10.1016/j.copbio.2016.04.007
     
  2. Emmert-Streib F., Dehmer M. Networks for systems biology: conceptual connection of data and function. IET Syst. Biol., 2011, Vol. 5, No. 3, pp. 185–207; DOI: 10.1049/iet-syb.2010.0025
     
  3. Emmert-Streib F., Glazko G. V. Network biology: a direct approach to study biological function. Wiley Interdiscip. Rev. Syst. Biol. Med., 2011, Vol. 3, No. 4, pp. 379–91; DOI: 10.1002/wsbm.134
     
  4. Schlitt T., Palin K., Rung J., Dietmann S., Lappe M., Ukkonen E., Brazma A. From gene networks to gene function. Genome Res., 2003, Vol. 13, No. 12, pp. 2568–2576; DOI: 10.1101/gr.1111403
     
  5. Zhu X., Gerstein M., Snyder M. Getting connected: analysis and principles of biological networks. Genes Dev., 2007, Vol. 21, No. 9, pp. 1010–1024. DOI: 10.1101/gad.1528707
     
  6. Akinshin A. A., Bukharina T. A., Golubyatnikov V. P., Furman D. P. Mathematical modeling of the interaction of two cells in the proneural cluster of the wing imaginal disk D.melanogaster [Matematicheskoe modelirovanie vzaimozheistviya dvukh kletok v proneiral’nom klastere krylovogo imaginal’nogo diska D.melanogaster]. Sib. Zh. Chist. Prikl. Mat., 2014, Vol. 14, No. 4, pp. 3–10 (in Russian).
     
  7. Bukharina T. A., Furman D. P., Golubyatnikov V. P. A model study of the morphogenesis of D. melanogaster mechanoreceptors: The central regulatory circuit. J. Bioinformat. Comput. Biology, 2015, Vol. 13, No. 1, pp. 1540006-1–1540006-15; DOI: 10.1142/S0219720015400065
     
  8. Ayupova N. B., Golubyatnikov V. P. A Three-cell Model of the Initial Stage of Development of a Proneural Cluster. J. Appl. Ind. Math., 2017. Vol. 11, No. 2, pp. 168–173; DOI: 10.1134/S1990478917020028
     
  9. Buharina T. A., Akin’shin A. A., Golubjatnikov V. P., Furman D. P. Matematicheskaya i chislennaya modeli central’nogo regulyatornogo kontura sistemy morfogeneza mekhanoreceptorov drozofily. [Mathematical and numerical models of the Central Regulatory Circuit of the mechanoreceptors morphogenesis system of Drosophila]. Sib. Zhurn. Indust. Mat., 2020, Vol. 23, No. 2, pp. 41–50 (in Russian); DOI: 10.33048/SIBJIM.2020.23.203
     
  10. Bukharina T. A., Golubyatnikov V. P., Furman D. P. Gene Network Controlling the Morphogenesis of D. melanogaster Macrochaetes: An Expanded Model of the Central Regulatory Circuit. Russian Journal of Developmental Biology, 2016, Vol. 47, No. 5, pp. 288–293; DOI: 10.1134/S1062360416050040
     
  11. Yamasaki Y., Lim Y. M., Niwa N., Hayashi S., Tsuda L. Robust specification of sensory neurons by dual functions of charlatan, a Drosophila NRSF/REST-like repressor of extramacrochaetae and hairy. Genes Cells, 2011, Vol. 16, No. 8,. pp. 896–909; DOI: 10.1111/j.1365-2443.2011.01537.x
     
  12. García-Bellido A., de Celis J.F. The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics, 2009, Vol. 182, No. 3, pp. 631–639; https://doi.org/10.1534/genetics.109.104083
     
  13. Ghysen A., Thomas R. The formation of sense organs in Drosophila: a logical approach. BioEssays, 2003, Vol. 25, pp. 802–807; DOI: 10.1002/bies.10311
     
  14. Sistemnaja komp’juternaja biologija [System computer biology]. Novosibirsk: Izd-vo SB RAN, 2008 (in Russian). 
     
  15. Golubyatnikov V. P., Kazantsev M. V., Kirillova N. E., Bukharina T. A., Furman D. P. Mathematical and numerical models of two asymmetric gene networks. Sib. Electron. Math. Reports, 2018, Vol. 15, pp. 1271– 1283; DOI: 10.17377/semi.2018.15.103
     
  16. Akinshin A. A., Ayupova N. B., Golubyatnikov V. P., Kirillova N. E., Podkolodnaya O. A., Podkolodnyy N. L. On a numerical model of a circadian oscillator. Numer. Anal. Appl., 2022, Vol. 15, No. 3, pp. 187–196; DOI: 10.1134/S199542392203001
     
  17. Golubyatnikov V. P., Akinshin A. A., Ayupova N. B., Minushkina L. S. Stratifications and foliations in phase portraits of gene network models. Vavilov J. Genetics and Breeding, 2022, Vol. 26, No. 8, pp. 758– 764; DOI: 10.18699/VJGB-22-91
     
  18. Chang P. J., Hsiao Y. L., Tien A. C., Li Y. C., Pi H. Negative-feedback regulation of proneural proteins controls the timing of neural precursor division. Development, 2008, Vol. 135, No. 18, pp. 302–3030; DOI: 10.1242/dev.021923
     
  19. Anikonov Yu. E., Gölgeleyen $\dot{I}$., Yildiz M. Identification problems for systems of nonlinear evolution equations and functional equations. Adv. Differ. Equ., 2016, Vol. 1, article 152; DOI: 10.1186/s13662-016-0877-4
     
  20. Moscoso del Prado J., García-Bellido A. Genetic regulation of the achaete-scute complex of Drosophila melanogaster. Wilehm Roux Arch. Dev. Biology, 1984, Vol. 193, No. 4, pp. 242–245; DOI: 10.1007/BF01260345 
     
  21. Escudero L. M., Caminero E., Schulze K. L., Bellen H. J., Modolell J. Charlatan, a Zn-finger transcription factor, establishes a novel level of regulation of the proneural achaete/scute genes of Drosophila. Development, 2005, Vol. 132, No. 6, pp. 1211–1222; DOI: 10.1242/dev.01691
     
  22. Nolo R., Abbott L. A., Bellen H. J. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell, 2000, Vol. 102, No. 3, pp.349–362; DOI: 10.1016/s0092-8674(00)00040-4
     
  23. Roark M., Sturtevant M. A., Emery J., Vaessin H., Grell E., Bier E. scratch, a pan-neural gene encoding a zinc finger protein related to snail, promotes neuronal development. Genes Dev., 1995, Vol. 9, No. 19, pp. 2384–2398; DOI: 10.1101/gad.9.19.2384
     
  24. Agol I. J. Step Allelomorphism in D. melanogaster. Genetics, 1931, Vol. 16, No. 3, pp. 254–266.
     
  25. Dubinin N. P. Step-allelomorphism in D. melanogaster. The allelomorphs achaete2-scute10, achaete1-scute11 and achaete3-scute13. J. Genet., 1932, Vol. 25, No. 2, pp. 163–181; https://doi.org/10.1007/BF02983250
     
  26. García-Bellido A., de Celis J. F. The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics, 2009, Vol. 182, No. 3, pp. 631–639; https://doi.org/10.1534/genetics.109.104083
     
  27. Ghysen A., Dambly-Chaudière C. From DNA to form: the achaete-scute complex. Genes Dev., 1988, Vol. 2, No. 5, pp. 495–501; DOI: 10.1101/gad.2.5.495
     
  28. Usui K., Goldstone C., Gibert J. M., Simpson P. Redundant mechanisms mediate bristle patterning on the Drosophila thorax. Proc. Natl. Acad. Sci. USA, 2008, Vol. 105, No. 51, pp. 20112–20117; DOI: 10.1073/pnas.0804282105
     
  29. Cabrera C. V., Alonso M. C., Huikeshoven H. Regulation of scute function by extramacrochaete in vitro and in vivo. Development, 1994, Vol. 120, No. 12, pp. 3595–603; DOI: 10.1242/dev.120.12.3595
     
  30. Acar M., Jafar-Nejad H., Giagtzoglou N., Yallampalli S., David G., He Y., Delidakis C., Bellen H. J. Senseless physically interacts with proneural proteins and functions as a transcriptional co-activator. Development, 2006, Vol. 133, No. 10, pp. 1979–1989; DOI: 10.1242/dev.02372
     
  31. Pi H., Wu H. J., Chien C. T. A dual function of phyllopod in Drosophila external sensory organ development: cell fate specification of sensory organ precursor and its progeny. Development, 2001, Vol. 128, No. 14, pp. 2699–2710; DOI: 10.1242/dev.128.14.2699
     
  32. Ramat A., Audibert A., Louvet-Vallèe S., Simon F., Fichelson P., Gho M. Escargot and Scratch regulate neural commitment by antagonizing Notch activity in Drosophila sensory organs. Development, 2016, Vol. 143, No. 16, pp. 3024–3034; DOI: 10.1242/dev.134387