Genetic study of motor functions in Drosophila melanogaster



Cite item

Full Text

Abstract

To investigate molecular mechanisms of central pattern generators (CPG s) functioning, we carried out a screening of collection of Drosophila P-insertional mutants for strong deviations in locomotion and courtship song. In 21 mutants, the site of the P-insertion was localized by sequencing of the fragments of genomic DNA flanking the P-element. Bioinformational analysis revealed a list of candidate genes, potential players in development and functioning of CPG s. Possible involvement of certain identified genes in rhythmic motor activity is suggested for the first time (CG15630, Map205).

About the authors

Sergey A Fedotov

I.P. Pavlov Institute of Physiology, RAS, Saint-Petersburg, RF

Email: serg900@yandex.ru

Julia V Bragina

I.P. Pavlov Institute of Physiology, RAS, Saint-Petersburg, RF

Email: julia_bragina@mail.ru

Nataliya G Besedina

I.P. Pavlov Institute of Physiology, RAS, Saint-Petersburg, RF

Email: molotova@pavlov.infran.ru

Larisa V Danilenkova

I.P. Pavlov Institute of Physiology, RAS, Saint-Petersburg, RF

Email: nkam@pavlov.infran.ru

Elena A Kamysheva

I.P. Pavlov Institute of Physiology, RAS, Saint-Petersburg, RF

Email: nkam@pavlov.infran.ru

Nikolay G Kamyshev

I.P. Pavlov Institute of Physiology, RAS, Saint-Petersburg, RF

Email: nkam@pavlov.infran.ru; nkamster@gmail.com

References

  1. Камышев Н. Г., 2011. Дрозофила как модельный объект для вскрытия молекулярных механизмов моторных и когнитивных дисфункций и поиска фармакологических способов их коррекции: количественный подход к оценке изменений локомоторного поведения//Международная научная конференция «Измерительные и информационные технологии в охране здоровья (МЕТРОМЕД-2011)», Сборник научных трудов, Санкт-Петербург, С. 152-160.
  2. Попов А. В., Савватеева-Попова Е. В., Камышев Н. Г., 2000. Особенности акустической коммуникации у плодовых мушек Drosophila melanogaster//Сенсорные системы. Т. 14. № 1. С. 60-74.
  3. Abdelilah-Seyfried S., Chan Y. M., Zeng C. et al., 2000. A gain-of-function screen for genes that affect the development of the Drosophila adult external sensor y organ//Genetics. Vol. 155. P. 733-752.
  4. Archambault V., D'Avino P. P., Deery M. J. et al., 2008. Sequestration of Polo kinase to microtubules by phosphopriming-independent binding to Map205 is relieved by phosphorylation at a CDK site in mitosis//Genes Dev. Vol. 22. P. 2707-2720.
  5. Baker P. W., Tanaka K. K., Klitgord N., Cripps R. M., 2005. Adult myogenesis in Drosophila melanogaster can proceed independently of myocyte enhancer factor-2//Genetics. Vol. 170. P. 1747-1759.
  6. Banerjee S., Lee J., Venkatesh K. et al., 2004. Loss of flight and associated neuronal rhythmicity in inositol 1,4,5-trisphosphate receptor mutants of Drosophila//J. Neurosci. Vol. 24. P. 7869-7878.
  7. Blanchard F. J., Collins B., Cyran S. A. et al., 2010. The transcription factor Mef2 is required for normal circadian behavior in Drosophila//J. Neurosci. Vol. 30. P. 5855-5865.
  8. Boube M., Benassayag C., Seroude L., Cribbs D. L., 1997. Ras1-mediated modulation of Drosophila homeotic function in cell and segment identity//Genetics. Vol. 146. P. 619-628.
  9. Boukhelifa M., Hwang S. J., 9. Valtschanoff J. G. et al., 2003. A critical role for palladin in astrocyte morphology and response to injury//Mol. Cell Neurosci. Vol. 23. P. 661-668.
  10. Cheah P. Y., Chia W., Yang X, 2000. Jumeaux, a novel Drosophila winged-helix family protein, is required for generating asymmetric sibling neuronal cell fates//Development. Vol. 127. P. 3325-3335.
  11. Chien S., Reiter L.T., Bier E., Gribskov M., 2002. Homophila: human disease gene cognates in Drosophila//Nucleic Acids Research. Vol. 30. P. 149-151.
  12. Chintapalli V.R., Wang J., Dow J. A. T., 2007. Using FlyAtlas to identify better Drosophila models of human disease//Nature Genetics. Vol. 39. P. 715-720.
  13. Clyne J. D., Miesenböck G., 2008. Sex-specific control and tuning of the pattern generator for courtship song in Drosophila//Cell. Vol. 133. P. 354-363.
  14. Cooley L., Kelley R., Spradling A., 1988. Insertional mutagenesis of the Drosophila genome with single P elements//Science. Vol. 4. P. 1121-1128.
  15. Crowner D., Madden K., Goeke S., Giniger E., 2002. Lola regulates midline crossing of CNS axons in Drosophila//Development. Vol. 129. P. 1317-1325.
  16. Edgington E. S., 1995. Randomization tests (3rd ed.). New York: Marcel Dekker.
  17. Fradkin L. G., Dura J. M., Noordermeer J. N., 2010. Ryks: new partners for Wnts in the developing and regenerating nervous system//Trends in Neurosciences. Vol. 33. P. 84-92.
  18. Friedman A., Perrimon N., 2006. A functional RNAi screen for regulators of receptor tyrosine kinase and ERK signaling//Nature. Vol. 444. P. 230-234.
  19. Gajewski K. M., Schulz R. A., 2010. CF2 represses Actin 88F gene expression and maintains filament balance during indirect flight muscle development in Drosophila//PLoS ONE. Vol. 5. P. e10713.
  20. Girardot F., Monnier V., Tricoire H., 2004. Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster//BMC Genomics. Vol. 5. P. 74.
  21. Gordon I. T., Whelan P. J., 2006. Deciphering the organization and modulation of spinal locomotor central pattern generators//J. Exp. Biol. Vol. 209. P. 2007-2014.
  22. Goulding M., Pfaff S. L., 2005. Development of circuits that generate simple rhythmic behaviors in vertebrates//Curr. Opin. Neurobiol. Vol. 15. P. 14-20.
  23. Graveley B. R., Brooks A. N., Carlson J. W. et al., 2011. The developmental transcriptome of Drosophila melanogaster//Nature. Vol. 471. P. 473-479.
  24. Greene J. C., Whitworth A. J., Andrews et al., 2005. Genetic and genomic studies of Drosophila parkin mutants implicate oxidative stress and innate immune responses in pathogenesis//Hum. Mol. Genet. Vol. 14. P. 799-811.
  25. Gruenewald C., Botella J. A., Bayersdorfer F. et al., 2009. Hyperoxia-induced neurodegeneration as a tool to identify neuroprotective genes in Drosophila melanogaster//Free Radical Biol. Med. Vol. 46. P. 1668-1676.
  26. Huang A. M., Rubin G. M., 2000. A misexpression screen identifies genes that can modulate RAS1 pathway signaling in Drosophila melanogaster//Genetics. Vol. 156. P. 1219-1230.
  27. Hunter S., Apweiler R., Attwood T. K. et al., 2009. InterPro: the integrative protein signature database//Nucleic Acids Res. Vol. 37. P. D211-D215
  28. Jordan K. W., Morgan T. J., Mackay T. F., 2006. Quantitative trait loci for locomotor behavior in Drosophila melanogaster//Genetics. Vol. 174. P. 271-284.
  29. Kiehn O., Butt S. J. B., 2003. Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord//Progress in Neurobiology. Vol. 70. P. 347-361.
  30. Kurusu M., Cording A., Taniguchi M. et al., 2008. A screen of cell-surface molecules identifies leucinerich repeat proteins as key mediators of synaptic target selection//Neuron. Vol. 59. P. 972-985.
  31. Landis G. N., Bhole D., Lu L., Tower J., 2001. Highfrequency generation of conditional mutations affecting Drosophila melanogaster development and life span//Genetics. Vol. 158. P. 1167-1176.
  32. Landis G. N., Bhole D., Tower J., 2003. A search for doxycycline-dependent mutations that increase Drosophila melanogaster life span identifies the VhaSFD, Sugar baby, filamin, fwd and Cctl genes//Genome Biol. Vol. 4. P. R8.
  33. Liebl F. L., Wu Y., Featherstone D. E. et al., 2008. Derailed regulates development of the Drosophila neuromuscular junction//Dev. Neurobiol. Vol. 68. P. 152-165.
  34. Lorenzetti D., Bohlega S., Zoghbi H. Y., 1997. The expansion of the CAG repeat in ataxin-2 is a frequent cause of autosomal dominant spinocerebellar ataxia//Neurology. Vol. 49. P. 1009-1013.
  35. Luo H., Liu X., Wang F. et al., 2005. Disruption of palladin results in neural tube closure defects in mice//Mol. Cell. Neurosci. Vol. 29. P. 507-515.
  36. Marder E., Bucher D., 2001. Central pattern generators and the control of rhythmic movements//Curr. Biol. Vol. 11. P. R986-R996. Генетика поведени я ` экологическая генетика том X № 1 2012 ISSN 1811-0932 60
  37. Martin J. R., 37. Ernst R., Heisenberg M., 1998. Mushroom bodies suppress locomotor activity in Drosophila melanogaster//Learn. Mem. Vol. 5. P. 179-191.
  38. McCormick C., Duncan G., Goutsos K. T., Tufaro F., 2000. The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate//Proc. Natl. Acad. Sci. USA. Vol. 97. P. 668-673.
  39. Moran C. N., Kyriacou C. P., 2009. Functional neurogenomics of the courtship song of male Drosophila melanogaster//Cortex. Vol. 45. P. 18-34.
  40. Moreau-Fauvarque C., Taillebourg E., Boissoneau E. et al., 1998. The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies//Mech. Dev. Vol. 78. P. 47-61.
  41. Otey C. A., Rachlin A., Moza M. et al., 2005. The palladin/myotilin/myopalladin family of actinassociated scaffolds//Int. Rev. Cytol. Vol. 246. P. 31-58.
  42. Pearson K. G., 2000. Neural adaptation in the generation of rhythmic behavior//Annu. Rev. Physiol. Vol. 62. P. 723-753.
  43. Pearson K. C., Wolf H., 1987. Comparison of motor patterns in the intact and deafferented flight system of the locust. I. Electromyographic analysis//J. Comp. Physiol. A. Vol. 160. P. 259-268.
  44. Pena-Rangel M. T., Rodriguez I., Riesgo-Escovar J. R., 2002. A misexpression study examining dorsal thorax formation in Drosophila melanogaster//Genetics. Vol. 160. P. 1035-1050.
  45. Redl B., 2000. Human tear lipocalin//Biochim. Biophys. Acta. Vol. 1482. P. 241-248.
  46. Sakurai M., Aoki T., Yoshikawa S. et al., 2009. Differentially expressed Drl and Drl-2 play opposing roles in Wnt5 signaling during Drosophila olfactory system development//J. Neurosci. Vol. 29. P. 4972-4980.
  47. Sawamoto K., Taguchi A., Hirota Y. et al., 1998. Argos induces programmed cell death in the developing Drosophila eye by inhibition of the Ras pathway//Cell Death Differ. Vol. 5. P. 262-270.
  48. Schlichet F., Hall J. C, 1979. Neural topography of courtship song in sex mosaics of Drosophila melanogaster//J. Comp. Physiol. A. Vol. 129. P. 85-95.
  49. Schulz C., Kiger A. A., Tazuke S. I. et al., 2004. A misexpression screen reveals effects of bag-ofmarbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage//Genetics. Vol. 167. P. 707-723.
  50. Senju S., Iyama K., Kudo H. et al., 2000. Immunocytochemical analyses and targeted gene disruption of GTPBP1//Mol. Cell. Biol. Vol. 20. P. 6195-6200.
  51. Sonnenfeld M.J., Barazesh N., Sedaghat Y., Fan C., 2004. The jing and ras1 pathways are functionally related during CNS midline and tracheal development//Mech. Dev. Vol. 121. P. 1531-1547.
  52. Stark C., Breitkreutz B.J., Chatr-Aryamontri A. et al., 2011. The BioGRID interaction database: 2011 update//Nucleic Acids Res. Vol. 39. P. D698-D704.
  53. Strauss R., 2002. The central complex and the genetic dissection of locomotor behavior//Curr. Opin. Neurobiol. Vol. 12. P. 633-638.
  54. Strauss R., Heisenberg M., 1990. Coordination of legs during straight walking and turning in Drosophila melanogaster//J. Comp. Physiol. A. Vol. 167. P. 403-412.
  55. Suster M. L., Bate M., 2002. Embryonic assembly of a central pattern generator without sensory input//Nature. Vol. 416. P. 174-178.
  56. Suster M. L., Martin J. R., Sung C., Robinow S., 2003. Targeted expression of tetanus toxin reveals sets of neurons involved in lar val locomotion in Drosophila//J. Neurobiol. Vol. 55. P. 233-246.
  57. Takei Y., Ozawa Y., Sato M. et al., 2004. Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans//Development. Vol. 131. P. 73-82.
  58. Tanaka K. K., Bryantsev A. L., Cripps R. M., 2008. Myocyte enhancer factor 2 and chorion factor 2 collaborate in activation of the myogenic program in Drosophila//Mol. Cell. Biol. Vol. 28. P. 1616-1629.
  59. Venken K. J., Bellen H. J., 2007. Transgenesis upgrades for Drosophila melanogaster//Development. Vol. 134. P. 3571-3584.
  60. Yao Y., Wu Y., Yin C. et al., 2007. Antagonistic roles of Wnt5 and the Drl receptor in patterning the Drosophila antennal lobe//Nat. Neurosci. Vol. 10. P. 1423-1432.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2012 Fedotov S.A., Bragina J.V., Besedina N.G., Danilenkova L.V., Kamysheva E.A., Kamyshev N.G.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 65617 от 04.05.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies