The Drosophila actin nucleator DAAM is essential for left-right asymmetry

English version

Autoři: Anil Chougule ^aff001; François Lapraz ^aff001; István Földi ^aff002; Delphine Cerezo ^aff001; József Mihály ^aff002; Stéphane Noselli ^aff001
Působiště autorů: Université Côte D’Azur, CNRS, Inserm, iBV, Nice, France ^aff001; Biological Research Centre, Hungarian Academy of Sciences, Institute of Genetics, Hungary ^aff002; Biological Research Centre, Hungarian Academy of Sciences, Institute of Genetics,Hungary ^aff002
Vyšlo v časopise: The Drosophila actin nucleator DAAM is essential for left-right asymmetry. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008758
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008758

Souhrn

Left-Right (LR) asymmetry is essential for organ positioning, shape and function. Myosin 1D (Myo1D) has emerged as an evolutionary conserved chirality determinant in both Drosophila and vertebrates. However, the molecular interplay between Myo1D and the actin cytoskeleton underlying symmetry breaking remains poorly understood. To address this question, we performed a dual genetic screen to identify new cytoskeletal factors involved in LR asymmetry. We identified the conserved actin nucleator DAAM as an essential factor required for both dextral and sinistral development. In the absence of DAAM, organs lose their LR asymmetry, while its overexpression enhances Myo1D-induced de novo LR asymmetry. These results show that DAAM is a limiting, LR-specific actin nucleator connecting up Myo1D with a dedicated F-actin network important for symmetry breaking.

Klíčová slova:

Actins – Cytoskeleton – Drosophila melanogaster – Genetic screens – Genital anatomy – Phenotypes – Protein domains – RNA interference

Zdroje

1. Blum M, Feistel K, Thumberger T, Schweickert A. The evolution and conservation of left-right patterning mechanisms. Development. 2014;141 : 1603–13. doi: 10.1242/dev.100560 24715452

2. Coutelis J-B, González-Morales N, Géminard C, Noselli S. Diversity and convergence in the mechanisms establishing L/R asymmetry in metazoa. EMBO Rep. 2014;15 : 926–37. doi: 10.15252/embr.201438972 25150102

3. Nakamura T, Hamada H. Left-right patterning: conserved and divergent mechanisms. Development. 2012;139 : 3257–3262. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=22912409&retmode=ref&cmd=prlinks doi: 10.1242/dev.061606 22912409

4. Spéder P, Adám G, Noselli S. Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature. 2006;440 : 803–7. doi: 10.1038/nature04623 16598259

5. Hozumi S, Maeda R, Taniguchi K, Kanai M, Shirakabe S, Sasamura T, et al. An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature. 2006;440 : 798–802. doi: 10.1038/nature04625 16598258

6. Petzoldt AG, Coutelis J-B, Geminard C, Speder P, Suzanne M, Cerezo D, et al. DE-Cadherin regulates unconventional Myosin ID and Myosin IC in Drosophila left-right asymmetry establishment. Development. 2012;139 : 1874–1884. doi: 10.1242/dev.047589 22491943

7. Taniguchi K, Maeda R, Ando T, Okumura T, Nakazawa N, Hatori R, et al. Chirality in planar cell shape contributes to left-right asymmetric epithelial morphogenesis. Science (80-). 2011;333 : 339–341. Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=21764746&retmode=ref&cmd=prlinks doi: 10.1126/science.1200940 21764746

8. Coutelis J-B, Géminard C, Spéder P, Suzanne M, Petzoldt AG, Noselli S. Drosophila Left/Right Asymmetry Establishment Is Controlled by the Hox Gene Abdominal-B. Dev Cell. 2013;24 : 89–97. Available: doi: 10.1016/j.devcel.2012.11.013 23328400

9. González-Morales N, Géminard C, Lebreton G, Cerezo D, Coutelis JB, Noselli S. The Atypical Cadherin Dachsous Controls Left-Right Asymmetry in Drosophila. Dev Cell. 2015;33 : 675–689. doi: 10.1016/j.devcel.2015.04.026 26073018

10. Suzanne M, Petzoldt AG, Spéder P, Coutelis J-B, Steller H, Noselli S. Coupling of Apoptosis and L/R Patterning Controls Stepwise Organ Looping. Curr Biol. 2010;20 : 1773–1778. doi: 10.1016/j.cub.2010.08.056 20832313

11. Coutelis JB, Petzoldt AG, Speder P, Suzanne M, Noselli S. Left–right asymmetry in Drosophila. Semin Cell Dev Biol. 2008;19 : 252–262. Available: http://linkinghub.elsevier.com/retrieve/pii/S1084952108000086 doi: 10.1016/j.semcdb.2008.01.006 18328746

12. Geminard C, Gonzalez-Morales N, Coutelis J-BB, Noselli SS, Géminard C, González-Morales N, et al. The myosin ID pathway and left-right asymmetry in Drosophila. Genesis. 2014;52 : 471–80. doi: 10.1002/dvg.22763 24585718

13. Lebreton G, Géminard C, Lapraz F, Pyrpassopoulos S, Cerezo D, Spéder P, et al. Molecular to organismal chirality is induced by the conserved myosin 1D. Science (80-). 2018;362 : 949–952. doi: 10.1126/science.aat8642 30467170

14. Juan T, Géminard C, Coutelis JB, Cerezo D, Polès S, Noselli S, et al. Myosin1D is an evolutionarily conserved regulator of animal left-right asymmetry. Nat Commun. 2018;9 : 1942. doi: 10.1038/s41467-018-04284-8 29769531

15. Tingler M, Kurz S, Maerker M, Ott T, Fuhl F, Schweickert A, et al. A Conserved Role of the Unconventional Myosin 1d in Laterality Determination. Curr Biol. 2018;28 : 810–816.e3. doi: 10.1016/j.cub.2018.01.075 29478852

16. Noël ES, Verhoeven M, Lagendijk AK, Tessadori F, Smith K, Choorapoikayil S, et al. A Nodal-independent and tissue-intrinsic mechanism controls heart-looping chirality. Nat Commun. 2013;4. doi: 10.1038/ncomms3754 24212328

17. Kuroda R, Fujikura K, Abe M, Hosoiri Y, Asakawa S, Shimizu M, et al. Diaphanous gene mutation affects spiral cleavage and chirality in snails. Sci Rep. 2016;6 : 34809. doi: 10.1038/srep34809 27708420

18. Davison A, McDowell GSS, Holden JMM, Johnson HFF, Koutsovoulos GDD, Liu MMM, et al. Formin Is Associated with Left-Right Asymmetry in the Pond Snail and the Frog. Curr Biol. 2016;26 : 1–7. doi: 10.1016/j.cub.2015.11.020

19. Abe M, Kuroda R. The development of CRISPR for a mollusc establishes the formin Lsdia1 as the long-sought gene for snail dextral/sinistral coiling. Development. 2019;146: dev175976. doi: 10.1242/dev.175976 31088796

20. Paul AS, Pollard T. Review of the mechanism of processive actin filament elongation by formins. Cell Motil Cytoskeleton. 2009;66 : 606–617. doi: 10.1002/cm.20379 19459187

21. Grikscheit K, Grosse R. Formins at the Junction. Trends Biochem Sci. 2015;xx: 148–159. doi: 10.1016/j.tibs.2015.12.002 26732401

22. Higashi T, Ikeda T, Murakami T, Shirakawa R, Kawato M, Okawa K, et al. Flightless-I (Fli-I) regulates the actin assembly activity of diaphanous-related formins (DRFs) Daam1 and mDia1 in cooperation with active Rho GTPase. J Biol Chem. 2010. doi: 10.1074/jbc.M109.079236 20223827

23. Barko S, Bugyi B, Carlier MF, Gombos R, Matusek T, Mihályand J, et al. Characterization of the biochemical properties and biological function of the formin homology domains of Drosophila DAAM. J Biol Chem. 2010;285 : 13154–13169. doi: 10.1074/jbc.M109.093914 20177055

24. Matusek T, Djiane A, Jankovics F, Brunner D, Mlodzik M, Mihály J. The Drosophila formin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton. Development. 2006;133 : 957–66. doi: 10.1242/dev.02266 16469972

25. Hu Y, Comjean A, Perkins LA, Perrimon N, Mohr SE. GLAD: an Online Database of G ene L ist A nnotation for D rosophila. J Genomics. 2015;3 : 75–81. doi: 10.7150/jgen.12863 26157507

26. Perkins AD, Lee MJJ, Tanentzapf G. The systematic identification of cytoskeletal genes required for Drosophila melanogaster muscle maintenance. Sci data. 2014;1 : 140002. doi: 10.1038/sdata.2014.2 25977760

27. Molnár I, Migh E, Szikora S, Kalmár T, Végh AG, Deák F, et al. DAAM Is Required for Thin Filament Formation and Sarcomerogenesis during Muscle Development in Drosophila. PLoS Genet. 2014;10: e1004166. doi: 10.1371/journal.pgen.1004166 24586196

28. McGuire SE. Spatiotemporal Rescue of Memory Dysfunction in Drosophila. Science (80-). 2003;302 : 1765–1768. doi: 10.1126/science.1089035 14657498

29. Matusek T, Gombos R, Szécsényi A, Sánchez-Soriano N, Czibula A, Pataki C, et al. Formin proteins of the DAAM subfamily play a role during axon growth. J Neurosci. 2008;28 : 13310–13319. doi: 10.1523/JNEUROSCI.2727-08.2008 19052223

30. Tay HG, Schulze SK, Compagnon J, Foley FC, Heisenberg C-PC-P, Yost HJ, et al. Lethal giant larvae 2 regulates development of the ciliated organ Kupffer’s vesicle. Development. 2013;140 : 1550–9. doi: 10.1242/dev.087130 23482490

31. Sato K, Hiraiwa T, Maekawa E, Isomura A, Shibata T, Kuranaga E. Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis. Nat Commun. 2015;6 : 10074. doi: 10.1038/ncomms10074 26656655

32. Fraichard S, Bougé AL, Kendall T, Chauvel I, Bouhin H, Bunch TA. Tenectin is a novel αPS2βPS integrin ligand required for wing morphogenesis and male genital looping in Drosophila. Dev Biol. 2010. doi: 10.1016/j.ydbio.2010.02.008 20152825

33. García-Castro MI, Vielmetter E, Bronner-Fraser M. N-cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. Science (80-). 2000. doi: 10.1126/science.288.5468.1047 10807574

34. Kurpios NA, Ibañes M, Davis NM, Lui W, Katz T, Martin JF, et al. The direction of gut looping is established by changes in the extracellular matrix and in cell:cell adhesion. Proc Natl Acad Sci. 2008;105 : 8499–8506. doi: 10.1073/pnas.0803578105 18574143

35. Welsh IC, Thomsen M, Gludish DW, Alfonso-Parra C, Bai Y, Martin JF, et al. Integration of left-right Pitx2 transcription and Wnt signaling drives asymmetric gut morphogenesis via Daam2. Dev Cell. 2013;26 : 629–644. doi: 10.1016/j.devcel.2013.07.019 24091014

36. Juan T, Géminard C, Coutelis J-B, Cerezo D, Polès S, Noselli S, et al. Myosin1D is an evolutionarily conserved determinant of animal Left/Right asymmetry. bioRxiv. 2018;in press. doi: 10.1101/267146

37. Miller RK, De La Torre Canny SG, Jang CW, Cho K, Ji H, Wagner DS, et al. Pronephric tubulogenesis requires Daam1-mediated planar cell polarity signaling. J Am Soc Nephrol. 2011;22 : 1654–1667. doi: 10.1681/ASN.2010101086 21804089

38. Tee YH, Shemesh T, Thiagarajan V, Hariadi RF, Anderson KL, Page C, et al. Cellular chirality arising from the self-organization of the actin cytoskeleton. Nat Cell Biol. 2015;17 : 445–457. doi: 10.1038/ncb3137 25799062

39. Jalal S, Shi S, Acharya V, Huang RY-J, Viasnoff V, Bershadsky AD, et al. Actin cytoskeleton self-organization in single epithelial cells and fibroblasts under isotropic confinement. J Cell Sci. 2019;132: jcs220780. doi: 10.1242/jcs.220780 30787030

40. de Navas L, Foronda D, Suzanne M, Sánchez-Herrero E. A simple and efficient method to identify replacements of P-lacZ by P-Gal4 lines allows obtaining Gal4 insertions in the bithorax complex of Drosophila. Mech Dev. 2006. doi: 10.1016/j.mod.2006.07.010 16971094

41. Iwaki DD, Lengyel JA. A Delta-Notch signaling border regulated by Engrailed/Invected repression specifies boundary cells in the Drosophila hindgut. Mech Dev. 2002. doi: 10.1016/S0925-4773(02)00061-8

42. Sudarsan V, Pasalodos-Sanchez S, Wan S, Gampel A, Skaer H. A genetic hierarchy establishes mitogenic signalling and mitotic competence in the renal tubules of Drosophila. Development. 2002.

43. Couturier L, Mazouni K, Bernard F, Besson C, Reynaud E, Schweisguth F. Regulation of cortical stability by RhoGEF3 in mitotic Sensory Organ Precursor cells in Drosophila. Biol Open. 2017. doi: 10.1242/bio.026641 29101098

44. Gombos R, Migh E, Antal O, Mukherjee A, Jenny A, Mihaly J. The Formin DAAM Functions as Molecular Effector of the Planar Cell Polarity Pathway during Axonal Development in Drosophila. J Neurosci. 2015;35 : 10154–10167. doi: 10.1523/JNEUROSCI.3708-14.2015 26180192

Článek Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis

Článek The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana

Článek High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements

Článek XPF-ERCC1 protects liver, kidney and blood homeostasis outside the canonical excision repair pathways

Článek Technical and social issues influencing the adoption of preprints in the life sciences

Článek The nanophthalmos protein TMEM98 inhibits MYRF self-cleavage and is required for eye size specification

Článek Is imprinting the result of “friendly fire” by the host defense system?

Článek XPF–ERCC1: Linchpin of DNA crosslink repair

Článek A missense variant in Mitochondrial Amidoxime Reducing Component 1 gene and protection against liver disease

Článek Deconstructing cerebellar development cell by cell

Článek The genomic landscape of undifferentiated embryonal sarcoma of the liver is typified by C19MC structural rearrangement and overexpression combined with TP53 mutation or loss

Článek Variants encoding a restricted carboxy-terminal domain of SLC12A2 cause hereditary hearing loss in humans