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is a Long Non-coding RNA in JNK Signaling in Epithelial Shape Changes during Drosophila Dorsal Closure


Changes in cell shape affect many critical cellular and bodily processes, like wound healing and developmental events, and when gone awry, metastatic processes in cancer. Evolutionarily conserved signaling pathways govern regulation of these cellular changes. The Jun-N-terminal kinase pathway regulates cell stretching during wound healing and normal development. An extensively studied developmental process is embryonic dorsal closure in fruit flies, a well-established model for the regulation and manner of this cell shape changes. Here we describe and characterize a processed, long non-coding RNA locus, acal, that adds a new layer of complexity to the Jun-N-terminal kinase signaling, acting as a negative regulator of the pathway. acal modulates the expression of two key genes in the pathway: the scaffold protein Cka, and the transcription factor Aop. Together, they enable the proper level of Jun-N-terminal kinase pathway activation to occur to allow cell stretching and closure.


Vyšlo v časopise: is a Long Non-coding RNA in JNK Signaling in Epithelial Shape Changes during Drosophila Dorsal Closure. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004927
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004927

Souhrn

Changes in cell shape affect many critical cellular and bodily processes, like wound healing and developmental events, and when gone awry, metastatic processes in cancer. Evolutionarily conserved signaling pathways govern regulation of these cellular changes. The Jun-N-terminal kinase pathway regulates cell stretching during wound healing and normal development. An extensively studied developmental process is embryonic dorsal closure in fruit flies, a well-established model for the regulation and manner of this cell shape changes. Here we describe and characterize a processed, long non-coding RNA locus, acal, that adds a new layer of complexity to the Jun-N-terminal kinase signaling, acting as a negative regulator of the pathway. acal modulates the expression of two key genes in the pathway: the scaffold protein Cka, and the transcription factor Aop. Together, they enable the proper level of Jun-N-terminal kinase pathway activation to occur to allow cell stretching and closure.


Zdroje

1. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10: 155–159. 19188922

2. Fatica A, Bozzoni I (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15: 7–21. doi: 10.1038/nrg3606 24296535

3. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99–110. 21245828

4. Okamura K, Ishizuka A, Siomi H, Siomi MC (2004) Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev 18: 1655–1666. 15231716

5. Batista PJ, Chang HY (2013) Long noncoding RNAs: cellular address codes in development and disease. Cell 152: 1298–1307. doi: 10.1016/j.cell.2013.02.012 23498938

6. Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81: 145–166. 22663078

7. Li Z, Liu M, Zhang L, Zhang W, Gao G, et al. (2009) Detection of intergenic non-coding RNAs expressed in the main developmental stages in Drosophila melanogaster. Nucleic Acids Res 37: 4308–4314. doi: 10.1093/nar/gkp334 19451167

8. Ilott NE, Ponting CP (2013) Predicting long non-coding RNAs using RNA sequencing. Methods 63: 50–59. 23541739

9. Young RS, Marques AC, Tibbit C, Haerty W, Bassett AR, et al. (2012) Identification and properties of 1,119 candidate lincRNA loci in the Drosophila melanogaster genome. Genome Biol Evol 4: 427–442. doi: 10.1093/gbe/evs020 22403033

10. Gummalla M, Maeda RK, Castro Alvarez JJ, Gyurkovics H, Singari S, et al. (2012) abd-A regulation by the iab-8 noncoding RNA. PLoS Genet 8: e1002720. 22654672

11. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Berlin; New York: Springer. xvii, 405 p. p.

12. Riesgo-Escovar JR, Jenni M, Fritz A, Hafen E (1996) The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev 10: 2759–2768. 8946916

13. Rios-Barrera LD, Riesgo-Escovar JR (2013) Regulating cell morphogenesis: the Drosophila Jun N-terminal kinase pathway. Genesis 51: 147–162.

14. Homsy JG, Jasper H, Peralta XG, Wu H, Kiehart DP, et al. (2006) JNK signaling coordinates integrin and actin functions during Drosophila embryogenesis. Dev Dyn 235: 427–434. 16317725

15. Riesgo-Escovar JR, Hafen E (1997) Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes Dev 11: 1717–1727. 9224720

16. Wada A, Kato K, Uwo MF, Yonemura S, Hayashi S (2007) Specialized extraembryonic cells connect embryonic and extraembryonic epidermis in response to Dpp during dorsal closure in Drosophila. Dev Biol 301: 340–349. 17034783

17. Bates KL, Higley M, Letsou A (2008) Raw mediates antagonism of AP-1 activity in Drosophila. Genetics 178: 1989–2002. doi: 10.1534/genetics.107.086298 18430930

18. Marts KL, Higley M, Letsou A (2008) Raw mediates antagonism of A98) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12: 557–570. 9472024

19. Reed BH, Wilk R, Lipshitz HD (2001) Downregulation of Jun kinase signaling in the amnioserosa is essential for dorsal closure of the Drosophila embryo. Curr Biol 11: 1098–1108. 11509232

20. Chen HW, Marinissen MJ, Oh SW, Chen X, Melnick M, et al. (2002) CKA, a novel multidomain protein, regulates the JUN N-terminal kinase signal transduction pathway in Drosophila. Mol Cell Biol 22: 1792–1803. 11865058

21. Giniger E, Tietje K, Jan LY, Jan YN (1994) lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development 120: 1385–1398. 8050351

22. Grillo M, Furriols M, Casanova J, Luschnig S (2011) Control of germline torso expression by the BTB/POZ domain protein pipsqueak is required for embryonic terminal patterning in Drosophila. Genetics 187: 513–521. doi: 10.1534/genetics.110.121624 21098720

23. St Pierre SE, Ponting L, Stefancsik R, McQuilton P, FlyBase C (2014) FlyBase 102--advanced approaches to interrogating FlyBase. Nucleic Acids Res 42: D780–788. doi: 10.1093/nar/gkt1092 24234449

24. Wilk R, Pickup AT, Hamilton JK, Reed BH, Lipshitz HD (2004) Dose-sensitive autosomal modifiers identify candidate genes for tissue autonomous and tissue nonautonomous regulation by the Drosophila nuclear zinc-finger protein, hindsight. Genetics 168: 281–300. 15454543

25. Retelska D, Iseli C, Bucher P, Jongeneel CV, Naef F (2006) Similarities and differences of polyadenylation signals in human and fly. BMC Genomics 7: 176. 16836751

26. Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, et al. (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297: 2270–2275. 12351791

27. Celniker SE, Dillon LA, Gerstein MB, Gunsalus KC, Henikoff S, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927–930. 19536255

28. Kondo T, Hashimoto Y, Kato K, Inagaki S, Hayashi S, et al. (2007) Small peptide regulators of actin-based cell morphogenesis encoded by a polycistronic mRNA. Nat Cell Biol 9: 660–665. 17486114

29. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, et al. (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35: W345–349. 17631615

30. Galindo MI, Pueyo JI, Fouix S, Bishop SA, Couso JP (2007) Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol 5: e106. 17439302

31. Tupy JL, Bailey AM, Dailey G, Evans-Holm M, Siebel CW, et al. (2005) Identification of putative noncoding polyadenylated transcripts in Drosophila melanogaster. Proc Natl Acad Sci U S A 102: 5495–5500. 15809421

32. Berezikov E, Robine N, Samsonova A, Westholm JO, Naqvi A, et al. (2011) Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Res 21: 203–215. doi: 10.1101/gr.116657.110 21177969

33. Chatterjee N, Bohmann D (2012) A versatile PhiC31 based reporter system for measuring AP-1 and Nrf2 signaling in Drosophila and in tissue culture. PLoS One 7: e34063. doi: 10.1371/journal.pone.0034063 22509270

34. Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149: 471–490. 10769037

35. Jemc JC, Milutinovich AB, Weyers JJ, Takeda Y, Van Doren M (2012) raw functions through JNK signaling and cadherin-based adhesion to regulate Drosophila gonad morphogenesis. Dev Biol 367: 114–125. doi: 10.1016/j.ydbio.2012.04.027 22575490

36. Zeitlinger J, Bohmann D (1999) Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development 126: 3947–3956. 10433922

37. Riesgo-Escovar JR, Hafen E (1997) Common and distinct roles of DFos and DJun during Drosophila development. Science 278: 669–672. 9381174

38. Glise B, Bourbon H, Noselli S (1995) hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83: 451–461. 8521475

39. Biswas R, Stein D, Stanley ER (2006) Drosophila Dok is required for embryonic dorsal closure. Development 133: 217–227. 16339186

40. Peswas R, Stein D, Stanley ER (2006) Drosophila Dok is required for embryonic dorsal closure. Development 133: 217–227. cell sheet movement. Cell 83: 451–461.1050.

41. Li M, Wen S, Guo X, Bai B, Gong Z, et al. (2012) The novel long non-coding RNA CRG regulates Drosophila locomotor behavior. Nucleic Acids Res 40: 11714–11727. doi: 10.1093/nar/gks943 23074190

42. Ferres-Marco D, Gutierrez-Garcia I, Vallejo D, Bolivar J, Gutierrez-Aviing RNA CRG regulates Drosophilailencers and Notch collaborate to promote malignant tumours by Rb silencing. Nature 439: 430–436. 16437107

43. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146: 353–358. doi: 10.1016/j.cell.2011.07.014 21802130

44. Tay Y, Karreth FA, Pandolfi PP (2014) Aberrant ceRNA activity drives lung cancer. Cell Res 24: 259–260. doi: 10.1038/cr.2014.21 24525785

45. Schwartz YB, Pirrotta V (2013) A new world of Polycombs: unexpected partnerships and emerging functions. Nat Rev Genet 14: 853–864. doi: 10.1038/nrg3603 24217316

46. Gutierrez L, Zurita M, Kennison JA, Vazquez M (2003) The Drosophila trithorax group gene tonalli (tna) interacts genetically with the Brahma remodeling complex and encodes an SP-RING finger protein. Development 130: 343–354. 12466201

47. Grote P, Wittler L, Hendrix D, Koch F, Wahrisch S, et al. (2013) The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell 24: 206–214. doi: 10.1016/j.devcel.2012.12.012 23369715

48. Ladoukakis E, Pereira V, Magny EG, Eyre-Walker A, Couso JP (2011) Hundreds of putatively functional small open reading frames in Drosophila. Genome Biol 12: R118. doi: 10.1186/gb-2011-12-11-r118 22118156

49. Xu B, Zhou Y, O K, Choy PC, Pierce GN, et al. (2010) Regulation of stress-associated scaffold proteins JIP1 and JIP3 on the c-Jun NH2-terminal kinase in ischemia-reperfusion. Can J Physiol Pharmacol 88: 1084–1092. doi: 10.1139/y10-088 21076496

50. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, et al. (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689–693. 20616235

51. Jones RS, Gelbart WM (1990) Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics 126: 185–199. 1977656

52. Lagarou A, Mohd-Sarip A, Moshkin YM, Chalkley GE, Bezstarosti K, et al. (2008) dKDM2 couples histone H2A ubiquitylation to histone H3 demethylation during Polycomb group silencing. Genes Dev 22: 2799–2810. doi: 10.1101/gad.484208 18923078

53. Herz HM, Madden LD, Chen Z, Bolduc C, Buff E, et al. (2010) The H3K27me3 demethylase dUTX is a suppressor of Notch—and Rb-dependent tumors in Drosophila. Mol Cell Biol 30: 2485–2497. doi: 10.1128/MCB.01633-09 20212086

54. Nerz HM, Madden LD, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795–801. 6776413

55. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory. 545 p.

56. Marygold SJ, Leyland PC, Seal RL, Goodman JL, Thurmond J, et al. (2013) FlyBase: improvements to the bibliography. Nucleic Acids Res 41: D751–757. doi: 10.1093/nar/gks1024 23125371

57. Loevenich SN, Brunner E, King NL, Deutsch EW, Stein SE, et al. (2009) The Drosophila melanogaster PeptideAtlas facilitates the use of peptide data for improved fly proteomics and genome annotation. BMC Bioinformatics 10: 59. doi: 10.1186/1471-2105-10-59 19210778

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Genetika Reprodukčná medicína

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