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Вавиловский журнал генетики и селекции

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Становление щетиночного узора у Drosophila melanogaster: предструктура и комплекс генов achaete-scute

https://doi.org/10.18699/VJ18.449

Полный текст:

Аннотация

Внешние механорецепторы дрозофилы, локализованные на голове и теле имаго, представлены щетинками разного размера – макро- и микрохетами. Макрохеты образуют устойчивую структурную композицию, так называемый щетиночный узор, специфичный для каждого вида дрозофилы, в котором каждая из макрохет занимает строго определенное положение. Формирование щетиночного узора начинается с формирования его прообраза в имагинальном диске. Специфичность позиций будущих механорецепторов определяется локальной экспрессией двух пронейральных генов – achaete (ac) и scute (sc), входящих в комплекс AS-C, в ответ на действие неких факторов, за которыми закрепилось название «факторы предструктуры», гетерогенно распределенных в эктодерме имагинальных дисков. Топография их совокупного распределения и создает прообраз (предструктуру) щетиночного узора. Таким образом, полноценный щетиночный узор является результатом взаимодействия двух систем: предструктуры и системы ответа на предструктуру – генов achaete и scute. К настоящему времени накоплено значительное число разрозненных экспериментальных данных, касающихся различных аспектов формирования щетиночного узора, однако формализованное представление полного спектра молекулярно-генетических взаимодействий факторов предструктуры как между собой, так и с генами комплекса AS-C, в литературе отсутствует. В обзоре систематизированы данные о закономерностях этих взаимодействий. Показано, что экспрессия пронейральных генов achaete-scute детерминируется иерархически организованной двухуровневой системой управления, содержащей как прямые, так и непрямые регуляторы их активности. Предложена обобщенная схема системы, включающая функциональные взаимодействия ее компонентов.

Об авторах

Д. П. Фурман
Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Новосибирский национальный исследовательский государственный университет
Россия
Новосибирск


Т. А. Бухарина
Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук
Россия
Новосибирск


Список литературы

1. Aegerter-Wilmsen T., Aegerter C.M., Hafen E., Basler K. Model for the regulation of size in the wing imaginal disc of Drosophila. Mech. Dev. 2007;124(4):318-326. DOI 10.1016/j.mod.2006.12.005.

2. Affolter M., Basler K. The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat. Rev. Genet. 2007;8(9): 663-674. DOI 10.1038/nrg2166.

3. Aldaz S., Escudero L.M. Imaginal discs. Curr. Biol. 2010;20(10):R429- R431. DOI 10.1016/j.cub.2010.03.010.

4. Aldaz S., Morata G., Azpiazu N. The Pax-homeobox gene eyegone is involved in the subdivision of the thorax of Drosophila. Development. 2003;130:4473-4482. DOI 10.1242/dev.00643.

5. Ayyar S., Negre B., Simpson P., Stollewerk A. An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian. BMC Biol. 2010;24:127. DOI 10.1186/1741-7007-8-127.

6. Ayyar S., Pistillo D., Calleja M., Brookfeld A., Gittins K., Goldstone C., Simpson P. NF-kB/Rel-mediated regulation of the neural fate in Drosophila. PLoS One. 2007;2:e1178. DOI 10.1371/journal.pone.0001178.

7. Barrios N., Campuzano S. Expanding the Iroquois genes repertoire: a non-transcriptional function in cell cycle progression. Fly (Austin). 2015;9(3):126-131. DOI 10.1080/19336934.2016.1139654.

8. Barrios N., González-Pérez E., Hernández R., Campuzano S. The homeodomain Iroquois proteins control cell cycle progression and regulate the size of developmental felds. PLoS Genet. 2015;11(8): e1005463. DOI 10.1371/journal.pgen.1005463.

9. Bate M., Martinez-Arias A. The embryonic origin of imaginal discs in Drosophila. Development. 1991;112(3):755-761.

10. Beira J.V., Paro R. The legacy of Drosophila imaginal discs. Chromosoma. 2016;125:573-592. DOI 10.1007/s00412-016-0595-4.

11. Biryukova I., Heitzler P. The Drosophila LIM-homeo domain protein Islet antagonizes pro-neural cell specifcation in the peripheral nervous system. Dev. Biol. 2005;288:559-570. DOI 10.1016/j.ydbio.2005.09.033.

12. Blair S.S. Compartments and appendage development in Drosophila. BioEssays. 1995;17(4):299-309. DOI 10.1002/bies.950170406.

13. Bronstein R., Levkovitz L., Yosef N., Yanku M., Ruppin E., Sharan R., Westphal H., Oliver B., Segal D. Transcriptional regulation by CHIP/LDB complexes. PLoS Genetics. 2010;6:e1001063. DOI 10.1371/journal.pgen.1001063.

14. Brook W.J. Hedgehog signaling and the axial patterning of Drosophila wings. Biochem. Cell Biol. 2000;78(5):585-591. DOI 10.1139/o00-072.

15. Bukharina T.A., Furman D.P. The mechanisms determining bristle pattern in Drosophila melanogaster. Rus. J. Dev. Biol. 2015;46:99-110. DOI 10.1134/S1062360415030029.

16. Calleja M., Renaud O., Usui K., Pistillo D., Morata G., Simpson P. How to pattern an epithelium: lessons from achaete-scute regulation on the notum of Drosophila. Gene. 2002;292:1-12. DOI 10.1016/S0378-1119(02)00628-5.

17. Campuzano S., Modolell J. Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 1992;8:202- 206. DOI 10.1016/0168-9525(92)90234-U.

18. Cavodeassi F., Modolell J., Gomez-Skarmeta J.L. The Iroquois family of genes: from body building to neural patterning. Development. 2001;128:2847-2855.

19. Chen L., Segal D., Hukriede N.A., Podtelejnikov A.V., Bayarsaihan D., Kennison J.A., Ogryzko V.V., Dawid I.B., Westphal H. Ssdp proteins interact with the LIM-domain-binding protein Ldb1 to regulate development. Proc. Natl. Acad. Sci. USA. 2002;99(22):14320-14325. DOI 10.1073/pnas.212532399.

20. Costa M., Calleja M., Alonso C.R., Simpson P. The bristle patterning genes hairy and extramacrochaetae regulate the development of structures required for flight in Diptera. Dev. Biol. 2014;388(2):205- 215. DOI 10.1016/j.ydbio.2013.12.032.

21. Cubadda Y., Heitzler P., Ray R.P., Bourouis M., Ramain P., Gelbart W., Simpson P., Haenlin M. u-shaped encodes a zinc fnger protein that regulates the proneural genes achaete and scute during the formation of bristles in Drosophila. Genes Dev. 1997;11:3085-3095. DOI 10.1101/gad.11.22.3083.

22. Culi J., Martin-Blanco E., Modolell J. The EGF receptor and N signalling pathways act antagonistically in Drosophila mesothorax bristle patterning. Development. 2001;128:299-308.

23. Dahmann C., Basler K. Opposing transcriptional outputs of Hedgehog signaling and engrailed control compartmental cell sorting at the Drosophila A/P boundary. Cell. 2000;100(4):411-422.

24. de Celis J.F., Barrio R. Function of the spalt/spalt-related gene complex in positioning the veins in the Drosophila wing. Mech. Dev. 2000; 91:31-41. DOI 10.1016/S0925-4773(99)00261-0.

25. de Celis J.F., Barrio R., Kafatos F.C. Regulation of the spalt/spalt-related gene complex and its function during sensory organ development in the Drosophila thorax. Development. 1999;126:2653-2662.

26. de Navascués J., Modolell J. tailup, a LIM-HD gene, and Iro-C cooperate in Drosophila dorsal mesothorax specifcation. Development. 2007;134:1779-1788. DOI 10.1242/dev.02844.

27. de Navascués J., Modolell J. The pronotum LIM-HD gene tailup is both a positive and a negative regulator of the proneural genes achaete and scute of Drosophila. Mech. Dev. 2010;127:393-406. DOI 10.1016/j.mod.2010.05.001.

28. Delanoue R., Zider A., Cossard R., Dutriaux A., Silber J. Interaction between apterous and early expression of vestigial in formation of the dorso-ventral compartments in the Drosophila wing disc. Genes Cells. 2002;7:1255-1266. DOI 10.1046/j.1365-2443.2002.00600.x.

29. Diez del Corral R., Aroca P., Gomez-Skarmeta J.L., Cavodeassi F., Modolell J. The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila. Genes Dev. 1999;13:1754-1761.

30. Dubinin N.P. Step-allelomorphism and the theory of centres of the gene achaete-scute. J. Genet. 1932;26:37-58.

31. Foronda D., Pérez-Garijo A., Martín F.A. Dpp of posterior origin patterns the proximal region of the wing. Mech. Dev. 2009;126(3-4): 99-106. DOI 10.1016/j.mod.2008.12.002.

32. Fromental-Ramain C., Taquet N., Ramain P. Transcriptional interactions between the pannier isoforms and the cofactor U-shaped during neural development in Drosophila. Mech. Dev. 2010;127:442- 457. DOI 10.1016/j.mod.2010.08.002.

33. Fromental-Ramain C., Vanolst L., Delaporte C., Ramain P. pannier encodes two structurally related isoforms that are differentially expressed during Drosophila development and display distinct functions during thorax patterning. Mech. Dev. 2008;125(1-2):43-57. DOI 10.1016/j.mod.2007.10.008.

34. Furman D.P., Bukharina T.A. How Drosophila melanogaster forms its mechanoreceptors. Curr. Genomics. 2008;9(5):312-323. DOI 10.2174/138920208785133271.

35. Furman D.P., Bukharina T.A. Analysis of the Neurogenesis:Prepattern Gene Network Controlling First Stage of Bristle Pattern Development in Drosophila melanogaster. Russ. J. Genet. Appl. Res. 2017; 7(5):550-557. DOI 10.1134/S2079059717050069.

36. Garcia-Bellido A. The cellular and genetic bases of organ size and shape in Drosophila. Int. J. Dev. Biol. 2009;53:1291-1303. DOI 10.1387/ijdb.072459ag.

37. 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;182:631-639. DOI 10.1534/genetics.109.104083.

38. Garcia-Garcia M.J., Ramain P., Simpson P., Modolell J. Different contributions of pannier and wingless to the patterning of the dorsal mesothorax of Drosophila. Development. 1999;126:3523-3532.

39. Giagtzoglou N., Alifragis P., Koumbanakis K.A., Delidakis C. Two modes of recruitment of E(spl) repressors onto target genes. Development. 2003;130:259-270. DOI 10.1242/dev.00206.

40. Gómez-Skarmeta J.L., Campuzano S., Modolell J. Half a century of neural prepatterning: the story of a few bristles and many genes. Nat. Rev. Neurosci. 2003;4:587-598. DOI 10.1038/nrn1142.

41. Gómez-Skarmeta J.L., Rodriguez I., Martinez C., Culi J., FerresMarco D., Beamonte D., Modolell J. Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs. Genes Dev. 1995;9:2598-2608. DOI 10.1101/gad.9.15.1869.

42. Hainaut M., Sagnier T., Berenger H., Pradel J., Graba Y., Miotto B. The MYST-containing protein Chameau is required for proper sensory organ specifcation during Drosophila thorax morphogenesis. PLoS One. 2012;7:e32882. DOI 10.1371/journal.pone.0032882.

43. Heitzler P., Vanolst L., Biryukova I., Ramain P. Enhancer-promoter communication mediated by Chip during Pannier-driven proneural patterning is regulated by Osa. Genes Dev. 2003;17:591-596. DOI 10.1101/gad.255703.

44. Held L.I., Jr. Imaginal Discs: The Genetic and Cellular Logic of Pattern Formation. Cambridge: Cambridge Univ. Press, 2002.

45. Higashijima S., Kojima T., Michiue T., Ishimaru S., Emori Y., Saigo K. Dual Bar homeo box genes of Drosophila required in two photoreceptor cells, R1 and R6, and primary pigment cells for normal eye development. Genes Dev. 1992;6:50-60.

46. Hooper J.E., Scott M.P. Communicating with Hedgehogs. Nat. Rev. Mol. Cell. Biol. 2005;6(4):306-317. DOI 10.1038/nrm1622.

47. Ikmi A., Netter S., Coen D. Prepatterning the Drosophila notum: the three genes of the iroquois complex play intrinsically distinct roles. Dev. Biol. 2008;317:634-648. DOI 10.1016/j.ydbio.2007.12.034.

48. Ingham P.W., Pinchin S.M., Howard K.R., Ish-Horowicz D. Genetic analysis of the hairy locus in Drosophila melanogaster. Genetics. 1985;111(3):463-486.

49. Jafar-Nejad H., Acar M., Nolo R., Lacin H., Pan H., Parkhurst S.M., Bellen H.J. Senseless acts as a binary switch during sensory organ precursor selection. Genes Dev. 2003;17:2966-2978. DOI 10.1101/gad.1122403.

50. Kehl B.T., Cho K.O., Choi K.W. mirror, a Drosophila homeobox gene in the Iroquois complex, is required for sensory organ and alula formation. Development. 1998;125:1217-1227.

51. Letizia A., Barrio R., Campuzano S. Antagonistic and cooperative actions of the EGFR and Dpp pathways on the iroquois genes regulate Drosophila mesothorax specifcation and patterning. Development. 2007;134:1337-1346. DOI 10.1242/dev.02823.

52. Martín F.A., Pérez-Garijo A., Moreno E., Morata G. The brinker gradient controls wing growth in Drosophila. Development. 2004;131: 4921-4930. DOI 10.1242/dev.01385.

53. Matthews J.M., Visvader J.E. LIM-domain-binding protein 1: a multifunctional cofactor that interacts with diverse proteins. EMBO Rep. 2003;4:1132-1137. DOI 10.1038/sj.embor.7400030.

54. Michel M., Dahmann C. Regulating mechanical tension at compartment boundaries in Drosophila. Fly. 2016;10(4):204-209. DOI 10.1080/19336934.2016.1207028.

55. Modolell J. Patterning of the adult peripheral nervous system of Drosophila. Perspect. Dev. Neurobiol. 1997;4(4):285-296.

56. Modolell J., Campuzano S. The achaete-scute complex as an integrating device. Int. J. Dev. Biol. 1998;42:275-282.

57. Nellen D., Burke R., Struhl G., Basler K. Direct and long-range action of a DPP morphogen gradient. Cell. 1996;85:357-368.

58. Nienhaus U., Aegerter-Wilmsen T., Aegerter C.M. In-vivo imaging of the Drosophila wing imaginal disc over time: novel insights on growth and boundary formation. PLoS One. 2012;7(10):e47594. DOI 10.1371/journal.pone.0047594.

59. Ohsako S., Hyer J.. Panganiban G., Oliver I., Caudy M. hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev. 1994;8:2743-2755.

60. Potter C.J., Xu T. Mechanisms of size control. Curr. Opin. Genet. Dev. 2001;11(3):279-286.

61. Ramain P., Heitzler P., Haenlin M., Simpson P. pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc fnger protein with homology to the vertebrate transcription factor GATA-1. Development. 1993;119:1277-1291.

62. Ramain P., Khechumian R., Khechumian K., Arbogast N., Ackermann C., Heitzler P. Interactions between Chip and the achaete/ scute-daughterless heterodimers are required for Pannier-driven proneural patterning. Mol. Cell. 2000;6:781-790. DOI 10.1016/S1097-2765(05)00079-1.

63. Reeves N., Posakony J.W. Genetic programs activated by proneural proteins in the developing Drosophila PNS. Dev. Cell. 2005;8:413- 425. DOI 10.1016/j.devcel.2005.01.020.

64. Restrepo S., Zartman J.J., Konrad B. Coordination of patterning and growth by the morphogen DPP. Curr. Biol. 2014;24(6):R245-R255. DOI 10.1016/j.cub.2014.01.055.

65. Rodríguez I., Hernández R., Modolell J., Ruiz-Gómez M. Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordial. EMBO J. 1990;9:3583-3592.

66. Rushlow C.A., Hogan A., Pinchin S.M., Howe K.M., Lardelli M., IshHorowicz D. The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J. 1989;8:3095-3103.

67. Sato M., Kojima T., Michiue T., Saigo K. Bar homeobox genes are latitudinal prepattern genes in the developing Drosophila notum whose expression is regulated by the concerted functions of decapentaplegic and wingless. Development. 1999;126:1457-1466.

68. Sato M., Saigo K. Involvement of pannier and u-shaped in regulation of decapentaplegic-dependent wingless expression in developing Drosophila notum. Mech. Dev. 2000;93:127-138. DOI 10.1016/S0925-4773(00)00282-3.

69. Schwank G., Restrepo S., Basler K. Growth regulation by Dpp: an essential role for Brinker and a non-essential role for graded signaling levels. Development. 2008;135:4003-4013. DOI 10.1242/dev.025635.

70. Serebrovsky A.S. Untersuchungen iiber Treppenallelomorphism. IV. Transgenation scute-6 und ein Fall des “Nicht-Allelomorphiss” von Gliedem einer Allelomorphenreihe bei Drosophila melanogaster. Wilhelm Roux’ Arch. 1930;122:88-104.

71. Skeath J.B., Carroll S.B. Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 1991;5:984-995.

72. Stern C. Two or three bristles. Am. Sci. 1954;42:213-247.

73. Stern C. Genetic Mosaics and Other Essays. Harvard Univ. Press, Cambridge, Massachusetts. 1968.

74. Stern M.D., Aihara H., Roccaro G.A., Cheung L., Zhang H., Negeri D., Nibu Y. CtBP is required for proper development of peripheral nervous system in Drosophila. Mech. Dev. 2009;126:68-79. DOI 10.1016/j.mod.2008.10.003.

75. Sweetman D., Münsterberg A. The vertebrate spalt genes in development and disease. Dev. Biol. 2006;293:285-293. DOI 10.1016/j.ydbio.2006.02.009.

76. Tomoyasu Y., Nakamura M., Ueno N. Role of Dpp signalling in prepattern formation of the dorsocentral mechanosensory organ in Drosophila melanogaster. Development. 1998;125:4215-4224.

77. Troost T., Schneider M., Klein T. A re-examination of the selection of the sensory organ precursor of the bristle sensilla of Drosophila melanogaster. PLoS Genet. 2015;11(1):e1004911. DOI 10.1371/journal.pgen.1004911.

78. van Meyel D.J., O’Keefe D.D., Jurata L.W., Thor S., Gill G.N., Thomas J.B. Chip and Apterous physically interact to form a functional complex during Drosophila development. Mol. Cell. 1999;4:259- 265. DOI 10.1016/S1097-2765(00)80373-1.

79. Vanolst L., Fromental-Ramain C., Ramain P. Toutatis, a TIP5-related protein, positively regulates Pannier function during Drosophila neural development. Development. 2005;132:4327-4338. DOI 10.1242/dev.02014.

80. Villa¬Cuesta E., González¬Pérez E., Modolell J. Apposition of iroquois expressing and non-expressing cells leads to cell sorting and fold formation in the Drosophila imaginal wing disc. BMC Dev. Biol. 2007;7:106. DOI 10.1186/1471-213X-7-106.

81. Wainwright S.M., Ish-Horowicz D. Point mutations in the Drosophila hairy gene demonstrate in vivo requirements for basic, helix-loophelix, and WRPW domains. Mol. Cell Biol. 1992;12(6):2475- 2483.

82. Wang S.H., Simcox A., Campbell G. Dual role for Drosophila epidermal growth factor receptor signaling in early wing disc development. Genes Dev. 2000;14:2271-2276. DOI 10.1101/gad.827000.

83. Yang M., Hatton-Ellis E., Simpson P. The kinase Sgg modulates temporal development of macrochaetes in Drosophila by phosphorylation of Scute and Pannier. Development. 2012;139:325-334. DOI 10.1242/dev.074260.

84. Zecca M., Basler K., Struhl G. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development. 1995;121:2265-2278.

85. Zecca M., Struhl G. Subdivision of the Drosophila wing imaginal disc by EGFR-mediated signaling. Development. 2002;129:1357-1368.

86. Zenvirt S., Nevo-Caspi Y., Rencus-Lazar S., Segal D. Drosophila LIM-only is a positive regulator of transcription during thoracic bristle development. Genetics. 2008;179(4):1989-1999. DOI 10.1534/genetics.108.090076.


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