DAnkrd49 and Bdbt act via Casein kinase Iε to regulate planar polarity in Drosophila

English version

Autoři: Helen Strutt ^aff001; David Strutt ^aff001
Působiště autorů: Department of Biomedical Science, University of Sheffield, Western Bank, Sheffield, United Kingdom ^aff001
Vyšlo v časopise: DAnkrd49 and Bdbt act via Casein kinase Iε to regulate planar polarity in Drosophila. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008820
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008820

Souhrn

The core planar polarity proteins are essential mediators of tissue morphogenesis, controlling both the polarised production of cellular structures and polarised tissue movements. During development the core proteins promote planar polarisation by becoming asymmetrically localised to opposite cell edges within epithelial tissues, forming intercellular protein complexes that coordinate polarity between adjacent cells. Here we describe a novel protein complex that regulates the asymmetric localisation of the core proteins in the Drosophila pupal wing. DAnkrd49 (an ankyrin repeat protein) and Bride of Doubletime (Bdbt, a non-canonical FK506 binding protein family member) physically interact, and regulate each other’s levels in vivo. Loss of either protein results in a reduction in core protein asymmetry and disruption of the placement of trichomes at the distal edge of pupal wing cells. Post-translational modifications are thought to be important for the regulation of core protein behaviour and their sorting to opposite cell edges. Consistent with this, we find that loss of DAnkrd49 or Bdbt leads to reduced phosphorylation of the core protein Dishevelled and to decreased Dishevelled levels both at cell junctions and in the cytoplasm. Bdbt has previously been shown to regulate activity of the kinase Discs Overgrown (Dco, also known as Doubletime or Casein Kinase Iε), and Dco itself has been implicated in regulating planar polarity by phosphorylating Dsh as well as the core protein Strabismus. We demonstrate that DAnkrd49 and Bdbt act as dominant suppressors of Dco activity. These findings support a model whereby Bdbt and DAnkrd49 act together to modulate the activity of Dco during planar polarity establishment.

Klíčová slova:

Cell polarity – Cloning – Drosophila melanogaster – Phenotypes – Phosphorylation – RNA interference – Trichomes – Planar cell polarity

Zdroje

1. Goodrich LV, Strutt D. Principles of planar polarity in animal development. Development. 2011; 138:1877–1892. doi: 10.1242/dev.054080 21521735

2. Devenport D. The cell biology of planar cell polarity. J Cell Biol. 2014; 207:171–179. doi: 10.1083/jcb.201408039 25349257

3. Butler MT, Wallingford JB. Planar cell polarity in development and disease. Nat Rev Mol Cell Biol. 2017; 18:375–388. doi: 10.1038/nrm.2017.11 28293032

4. Davey CF, Moens CB. Planar cell polarity in moving cells: think globally, act locally. Development. 2017; 144:187–200. doi: 10.1242/dev.122804 28096212

5. Hale R, Strutt D. Conservation of planar polarity pathway function across the animal kingdom. Annu Rev Genet. 2015; 49:529–551. doi: 10.1146/annurev-genet-112414-055224 26360326

6. Wong LL, Adler PN. Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J Cell Biol. 1993; 123:209–221. doi: 10.1083/jcb.123.1.209 8408199

7. Aw WY, Devenport D. Planar cell polarity: global inputs establishing cellular asymmetry. Curr Opin Cell Biol. 2016; 44:110–116. doi: 10.1016/j.ceb.2016.08.002 27576155

8. Amonlirdviman K, Khare NA, Tree DR, Chen WS, Axelrod JD, Tomlin CJ. Mathematical modeling of planar cell polarity to understand domineering nonautonomy. Science. 2005; 307:423–426. doi: 10.1126/science.1105471 15662015

9. Le Garrec JF, Lopez P, Kerszberg M. Establishment and maintenance of planar epithelial cell polarity by asymmetric cadherin bridges: a computer model. Dev Dyn. 2006; 235:235–246. doi: 10.1002/dvdy.20617 16258926

10. Burak Y, Shraiman BI. Order and stochastic dynamics in Drosophila planar cell polarity. PLoS Comput Biol. 2009; 5:e1000628. doi: 10.1371/journal.pcbi.1000628 20041171

11. Schamberg S, Houston P, Monk NA, Owen MR. Modelling and analysis of planar cell polarity. Bull Math Biol. 2010; 72:645–680. doi: 10.1007/s11538-009-9464-0 20107923

12. Tree DR, Shulman JM, Rousset R, Scott MP, Gubb D, Axelrod JD. Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell. 2002; 109:371–381. doi: 10.1016/s0092-8674(02)00715-8 12015986

13. Carreira-Barbosa F, Concha ML, Takeuchi M, Ueno N, Wilson SW, Tada M. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development. 2003; 130:4037–4046. doi: 10.1242/dev.00567 12874125

14. Jenny A, Reynolds-Kenneally J, Das G, Burnett M, Mlodzik M. Diego and Prickle regulate Frizzled planar cell polarity signalling by competing for Dishevelled binding. Nat Cell Biol. 2005; 7:691–697. doi: 10.1038/ncb1271 15937478

15. Warrington SJ, Strutt H, Fisher KH, Strutt D. A dual function for Prickle in regulating Frizzled stability during feedback-dependent amplification of planar polarity. Curr Biol. 2017; 27:2784–2797. doi: 10.1016/j.cub.2017.08.016 28918952

16. Strutt H, Searle E, Thomas-Macarthur V, Brookfield R, Strutt D. A Cul-3-BTB ubiquitylation pathway regulates junctional levels and asymmetry of core planar polarity proteins. Development. 2013; 140:1693–1702. doi: 10.1242/dev.089656 23487316

17. Bastock R, Strutt H, Strutt D. Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development. 2003; 130:3007–3014. doi: 10.1242/dev.00526 12756182

18. Strutt H, Thomas-MacArthur V, Strutt D. Strabismus promotes recruitment and degradation of farnesylated Prickle in Drosophila melanogaster planar polarity specification. PLoS Genet. 2013; 9:e1003654. doi: 10.1371/journal.pgen.1003654 23874239

19. Cho B, Pierre-Louis G, Sagner A, Eaton S, Axelrod JD. Clustering and negative feedback by endocytosis in planar cell polarity signaling is modulated by ubiquitinylation of prickle. PLoS Genet. 2015; 11:e1005259. doi: 10.1371/journal.pgen.1005259 25996914

20. Narimatsu M, Bose R, Pye M, Zhang L, Miller B, Ching P, et al. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell. 2009; 137:295–307. doi: 10.1016/j.cell.2009.02.025 19379695

21. Butler MT, Wallingford JB. Control of vertebrate core planar cell polarity protein localization and dynamics by Prickle 2. Development. 2015; 142:3429–3439. doi: 10.1242/dev.121384 26293301

22. Djiane A, S. Y, Mlodzik M. The apical determinants aPKC and dPatj regulate Frizzled-dependent planar cell polarity in the Drosophila eye. Cell. 2005; 121:621–631. doi: 10.1016/j.cell.2005.03.014 15907474

23. Klein TJ, Jenny A, Djiane A, Mlodzik M. CKIepsilon/discs overgrown promotes both Wnt-Fz/beta-catenin and Fz/PCP signaling in Drosophila. Curr Biol. 2006; 16:1337–1343. doi: 10.1016/j.cub.2006.06.030 16824922

24. Strutt H, Price MA, Strutt D. Planar polarity is positively regulated by casein kinase Iepsilon in Drosophila. Curr Biol. 2006; 16:1329–1336. doi: 10.1016/j.cub.2006.04.041 16824921

25. Singh J, Yanfeng WA, Grumolato L, Aaronson SA, Mlodzik M. Abelson family kinases regulate Frizzled planar cell polarity signaling via Dsh phosphorylation. Genes Dev. 2010; 24:2157–2168. doi: 10.1101/gad.1961010 20837657

26. Gao B, Song H, Bishop K, Elliot G, Garrett L, English MA, et al. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev Cell. 2011; 20:163–176. doi: 10.1016/j.devcel.2011.01.001 21316585

27. Kelly LK, Wu J, Yanfeng WA, Mlodzik M. Frizzled-induced Van Gogh phosphorylation by CK1epsilon promotes asymmetric localization of core PCP factors in Drosophila. Cell Rep. 2016; 16:344–356. doi: 10.1016/j.celrep.2016.06.010 27346358

28. Yang W, Garrett L, Feng D, Elliott G, Liu X, Wang N, et al. Wnt-induced Vangl2 phosphorylation is dose-dependently required for planar cell polarity in mammalian development. Cell Res. 2017; 27:1466–1484. doi: 10.1038/cr.2017.127 29056748

29. Strutt H, Gamage J, Strutt D. Reciprocal action of Casein Kinase I epsilon on core planar polarity proteins regulates clustering and asymmetric localisation. Elife. 2019; 8:e45107. doi: 10.7554/eLife.45107 31090542

30. Thomas C, Strutt D. Rabaptin-5 and Rabex-5 are neoplastic tumour suppressor genes that interact to modulate Rab5 dynamics in Drosophila melanogaster. Dev Biol. 2014; 385:107–121. doi: 10.1016/j.ydbio.2013.09.029 24104056

31. Fan JY, Agyekum B, Venkatesan A, Hall DR, Keightley A, Bjes ES, et al. Noncanonical FK506-binding protein BDBT binds DBT to enhance its circadian function and forms foci at night. Neuron. 2013; 80:984–996. doi: 10.1016/j.neuron.2013.08.004 24210908

32. Venkatesan A, Fan JY, Nauman C, Price JL. A Doubletime Nuclear Localization Signal Mediates an Interaction with Bride of Doubletime to Promote Circadian Function. J Biol Rhythms. 2015; 30:302–317. doi: 10.1177/0748730415588189 26082158

33. Mintseris J, Obar RA, Celniker S, Gygi SP, VijayRaghavan K, Artavanis-Tsakonas S. DPiM: the Drosophila Protein Interaction Mapping project Personal communication to FlyBase. 2009:FBrf0209452.

34. Guruharsha KG, Rual JF, Zhai B, Mintseris J, Vaidya P, Vaidya N, et al. A protein complex network of Drosophila melanogaster. Cell. 2011; 147:690–703. doi: 10.1016/j.cell.2011.08.047 22036573

35. Huen D, Roote J. Personal communication to FlyBase. 2010:FBrf0210708.

36. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res. 2001; 11:863–874. doi: 10.1101/gr.176601 11337480

37. Kang CB, Hong Y, Dhe-Paganon S, Yoon HS. FKBP family proteins: immunophilins with versatile biological functions. Neurosignals. 2008; 16:318–325. doi: 10.1159/000123041 18635947

38. Rein T. FK506 binding protein 51 integrates pathways of adaptation: FKBP51 shapes the reactivity to environmental change. Bioessays. 2016; 38:894–902. doi: 10.1002/bies.201600050 27374865

39. Peters JM, McKay RM, McKay JP, Graff JM. Casein kinase I transduces Wnt signals. Nature. 1999; 401:345–350. doi: 10.1038/43830 10517632

40. McKay RM, Peters JM, Graff JM. The casein kinase I family in Wnt signaling. Dev Biol. 2001; 235:388–396. doi: 10.1006/dbio.2001.0308 11437445

41. Cong F, Schweizer L, Varmus H. Casein kinase Iε modulates the signaling specificities of Dishevelled. Mol Cell Biol. 2004; 24:2000–2011. doi: 10.1128/mcb.24.5.2000-2011.2004 14966280

42. Fan JY, Preuss F, Muskus MJ, Bjes ES, Price JL. Drosophila and vertebrate casein kinase Idelta exhibits evolutionary conservation of circadian function. Genetics. 2009; 181:139–152. doi: 10.1534/genetics.108.094805 18957703

43. Zilian O, Burke R, Brentrup D, Gutjahr T, Bryant P, Noll M. double-time is identical to discs overgrown, which is required for cell survival, proliferation and growth arrest in Drosophila imaginal discs. Development. 1999; 126:5409–5420. 10556065

44. Cho E, Feng Y, Rauskolb C, Maitra S, Fehon R, Irvine KD. Delineation of a Fat tumor suppressor pathway. Nat Genet. 2006; 38:1142–1150. doi: 10.1038/ng1887 16980976

45. Guan J, Li H, Rogulja A, Axelrod JD, Cadigan KM. The Drosophila casein kinase Iepsilon/delta Discs Overgrown promotes cell survival via activation of DIAP1 expression. Dev Biol. 2007; 303:16–28. doi: 10.1016/j.ydbio.2006.10.028 17134692

46. Feng Y, Irvine K. Processing and phosphorylation of the Fat receptor. Proc Natl Acad Sci USA. 2009; 106:11989–11994. doi: 10.1073/pnas.0811540106 19574458

47. Sopko R, Silva E, Clayton L, Gardano L, Barrios-Rodiles M, Wrana J, et al. Phosphorylation of the tumor suppressor Fat Is regulated by Its ligand Dachsous and the kinase Discs Overgrown. Curr Biol. 2009; 19:1112–1117. doi: 10.1016/j.cub.2009.05.049 19540118

48. Price MA. CKI, there's more than one: casein kinase I family members in Wnt/Wingless and Hedgehog signaling. Genes Dev. 2006; 20:399–410. doi: 10.1101/gad.1394306 16481469

49. Kategaya LS, Hilliard A, Zhang L, Asara JM, Ptacek LJ, Fu YH. Casein kinase 1 proteomics reveal prohibitin 2 function in molecular clock. PLoS One. 2012; 7:e31987. doi: 10.1371/journal.pone.0031987 22384121

50. Taipale M, Tucker G, Peng J, Krykbaeva I, Lin ZY, Larsen B, et al. A quantitative chaperone interaction network reveals the architecture of cellular protein homeostasis pathways. Cell. 2014; 158:434–448. doi: 10.1016/j.cell.2014.05.039 25036637

51. Huttlin EL, Bruckner RJ, Paulo JA, Cannon JR, Ting L, Baltier K, et al. Architecture of the human interactome defines protein communities and disease networks. Nature. 2017; 545:505–509. doi: 10.1038/nature22366 28514442

52. Pletscher-Frankild S, Palleja A, Tsafou K, Binder JX, Jensen LJ. DISEASES: text mining and data integration of disease-gene associations. Methods. 2015; 74:83–89. doi: 10.1016/j.ymeth.2014.11.020 25484339

53. Gao B, Yang Y. Planar cell polarity in vertebrate limb morphogenesis. Curr Opin Genet Dev. 2013; 23:438–444. doi: 10.1016/j.gde.2013.05.003 23747034

54. Sekine T, Yamaguchi T, Hamano K, Young MW, Shimoda M, Saez L. Casein kinase I epsilon does not rescue double-time function in Drosophila despite evolutionarily conserved roles in the circadian clock. J Biol Rhythms. 2008; 23:3–15. doi: 10.1177/0748730407311652 18258753

55. Strutt H, Gamage J, Strutt D. Robust asymmetric localization of planar polarity proteins is associated with organization into signalosome-like domains of variable stoichiometry. Cell Rep. 2016; 17:2660–2671. doi: 10.1016/j.celrep.2016.11.021 27926869

56. Strutt DI. Asymmetric localization of Frizzled and the establishment of cell polarity in the Drosophila wing. Mol Cell. 2001; 7:367–375. doi: 10.1016/s1097-2765(01)00184-8 11239465

57. Kloss B, Price JL, Saez L, Blau J, Rothenfluh A, Wesley CS, et al. The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iepsilon. Cell. 1998; 94:97–107. doi: 10.1016/s0092-8674(00)81225-8 9674431

58. Price JL, Blau J, Rothenfluh A, Abodeely M, Kloss B, Young MW. double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell. 1998; 94:83–95. doi: 10.1016/s0092-8674(00)81224-6 9674430

59. O'Donnell J, Mandel HC, Krauss M, Sofer W. Genetic and cytogenetic analysis of the Adh region in Drosophila melanogaster. Genetics. 1977; 86:553–566. 408228

60. Huang J, Zhou W, Watson AM, Jan YN, Hong Y. Efficient ends-out gene targeting in Drosophila. Genetics. 2008; 180:703–707. doi: 10.1534/genetics.108.090563 18757917

61. Capdevila J, Guerrero I. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 1994; 13:4459–4468. 7925288

62. Hinz U, Giebel B, Campos-Ortega JA. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell. 1994; 76:77–87. doi: 10.1016/0092-8674(94)90174-0 8287481

63. Johnson RL, Grenier JK, Scott MP. patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets. Development. 1995; 121:4161–4170. 8575316

64. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, Schwarz TL, et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell. 1999; 98:585–595. doi: 10.1016/s0092-8674(00)80046-x 10490098

65. Bastock R, Strutt D. The planar polarity pathway promotes coordinated cell migration during Drosophila oogenesis. Development. 2007; 134:3055–3064. doi: 10.1242/dev.010447 17652348

66. Aigouy B, Farhadifar R, Staple DB, Sagner A, Röper J-C, Julicher F, et al. Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell. 2010; 142:773–786. doi: 10.1016/j.cell.2010.07.042 20813263

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