Genetic Dissection of Photoreceptor Subtype Specification by the Zinc Finger Proteins Elbow and No ocelli

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The eyes of many animals contain groups of photoreceptor cells with different chromatic sensitivities that can be arranged in complex patterns. It is of great interest to identify the genes and pathways shaping these ‘retinal mosaics’ which include stochastically distributed groups of cells, versus highly localized ones. In many insect eyes, which are composed of large numbers of unit eyes, or ommatidia, specialized photoreceptors are found only in the dorsal periphery, where they face the sky. These ommatidia are responsible for detecting linearly polarized skylight, which serves as an important navigational cue for these animals. Here we describe how two closely related proteins called Elbow and No ocelli interact with the transcription factors Homothorax and Orthodenticle to correctly specify the polarization detectors at the dorsal rim of the retina of Drosophila melanogaster. Interestingly, all four proteins are evolutionarily conserved from worms to humans, and they appear to be involved in similar developmental processes across species. Furthermore, human homologs of Elbow and No ocelli have been identified as promoters of luminal breast cancer. The newly identified role of these two proteins within a regulatory network might therefore enable new approaches in a number of important processes.

Vyšlo v časopise: Genetic Dissection of Photoreceptor Subtype Specification by the Zinc Finger Proteins Elbow and No ocelli. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004210
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004210

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Zdroje

1. TomlinsonA (2003) Patterning the peripheral retina of the fly: decoding a gradient. Dev Cell 5(5): 799–809.

2. Wernet M.F., Labhart T., Baumann F., Mazzoni E.O., Pichaud F., et al. (2003). Homothorax switches function of Drosophila photoreceptors from color to polarized light sensors. Cell 115: 267–79.

3. XinN, BenchabaneH, TianA, NguyenK, KlofasL, et al. (2011) Erect Wing facilitates context-dependent Wnt/Wingless signaling by recruiting the cell-specific Armadillo-TCF adaptor Earthbound to chromatin. Development 138(22): 4955–67.

4. LuqueCM, MilánM (2007) Growth control in the proliferative region of the Drosophila eye-head primordium: the elbow-noc gene complex. Dev Bio 301 ((2)): 327–39.

5. PereaD, TerrienteJ, Díaz-BenjumeaFJ (2009) Temporal and spatial windows delimit activation of the outer ring of wingless in the Drosophila wing. Dev Biol 328(2): 445–55.

6. SlorachEM, ChouJ, WerbZ (2011) Zeppo1 is a novel metastasis promoter that represses E-cadherin expression and regulates p120-catenin isoform expression and localization. Genes Dev. 2011 Mar 1 25(5): 471–84.

7. ZhaoX, YangY, FitchDH, HermanMA (2002) TLP-1 is an asymmetric cell fate determinant that responds to Wnt signals and controls male tail tip morphogenesis in C. elegans. Development 129(6): 1497–508.

8. DavisT, TrenearJ, AshburnerM (1990) The molecular analysis of the el-noc complex of Drosophila melanogaster. Genetics 126(1): 105–19.

9. DavisT, AshburnerM, JohnsonG, GubbD, RooteJ (1997) Genetic and phenotypic analysis of the genes of the elbow-no-ocelli region of chromosome 2L of Drosophila melanogaster. Hereditas 126(1): 67–75.

10. DorfmanR, GlazerL, WeiheU, WernetMF, ShiloBZ (2002) Elbow and Noc define a family of zinc finger proteins controlling morphogenesis of specific tracheal branches. Development 129(15): 3585–96.

11. NakamuraM, RunkoAP, SagerströmCG (2004) A novel subfamily of zinc finger genes involved in embryonic development. J Cell Biochem 93(5): 887–95.

12. RunkoAP, SagerströmCG (2003) Nlz belongs to a family of zinc-finger-containing repressors and controls segmental gene expression in the zebrafish hindbrain. Dev Biol 262(2): 254–67.

13. NakamuraM, ChoeSK, RunkoAP, GardnerPD, SagerströmCG (2008) Nlz1/Znf703 acts as a repressor of transcription. BMC Dev Biol 8: 108.

14. Pereira-CastroI, CostaAM, OliveiraMJ, BarbosaI, RochaAS, et al. (2013) Characterization of human NLZ1/ZNF703 identifies conserved domains essential for proper subcellular localization and transcriptional repression. J Cell Biochem 114(1): 120–33.

15. MurataY, KimHG, RogersKT, UdvadiaAJ, HorowitzJM (1994) Negative regulation of Sp1 trans-activation is correlated with the binding of cellular proteins to the amino terminus of the Sp1 trans-activation domain. J Biol Chem 269(32): 20674–81.

16. SuK, RoosMD, YangX, HanI, PatersonAJ, et al. (1999) An N-terminal region of Sp1 targets its proteasome-dependent degradation in vitro. J Biol Chem 274(21): 15194–202.

17. JiSJ, PerizG, SockanathanS (2009) Nolz1 is induced by retinoid signals and controls motoneuron subtype identity through distinct repressor activities. Development 136(2): 231–40.

18. HoyleJ, TangYP, WielletteEL, WardleFC, SiveH (2004) nlz gene family is required for hindbrain patterning in the zebrafish. Dev Dyn 229(4): 835–46.

19. ChangSL, YanYT, ShiYL, LiuYC, TakahashiH, et al. (2011) Region- and cell type-selective expression of the evolutionarily conserved Nolz-1/zfp503 gene in the developing mouse hindbrain. Gene Expr Patterns 11(8): 525–32.

20. ChangCW, TsaiCW, WangHF, TsaiHC, ChenHY, et al. (2004) Identification of a developmentally regulated striatum-enriched zinc-finger gene, Nolz-1, in the mammalian brain. Proc Natl Acad Sci U S A 101(8): 2613–8.

21. UrbánN, Martín-IbáñezR, HerranzC, EsgleasM, CrespoE, et al. (2010) Nolz1 promotes striatal neurogenesis through the regulation of retinoic acid signaling. Neural Dev 24;5: 21.

22. HollandDG, BurleighA, GitA, GoldgrabenMA, Perez-ManceraPA, et al. (2011) ZNF703 is a common Luminal B breast cancer oncogene that differentially regulates luminal and basal progenitors in human mammary epithelium. EMBO Mol Med 3(3): 167–80.

23. SircoulombF, NicolasN, FerrariA, FinettiP, BekhoucheI, et al. (2011) ZNF703 gene amplification at 8p12 specifies luminal B breast cancer. EMBO Mol Med 3(3): 153–66.

24. WeiheU, DorfmanR, WernetMF, CohenSM, MilánM (2003) Proximodistal subdivision of Drosophila legs and wings: the elbow-no ocelli gene complex. Development 131(4): 767–74.

25. Wolff, T R., Ready D.F. (1993). Pattern formation in the Drosophila Retina. In The Development of Drosophila melanogaster, M. M.-A. BateA, ed. (Cold Spring Harbor, Cold Spring Harbor Laboratory Press) pp., 1277–1325.

26. Meinertzhagen I.A. and Hanson,T.E. (1993). The development of the optic lobe. In The Development of Drosophila melanogaster (eds. Bate M. andMartinez Arias, A.).Plainview, NY: Cold Spring Harbor Laboratory Press, pp. 1363–1491.

27. Mollereau B., Dominguez M., Webel R., Colley, N J., Keung B., et al. (2001). Two-step process for photoreceptor formation in Drosophila. Nature 412: 911–913.

28. CookT, PichaudF, SonnevilleR, PapatsenkoD, DesplanC (2003) Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev Cell 4(6): 853–64.

29. XieB, Charlton-PerkinsM, McDonaldE, GebeleinB, CookT (2007) Senseless functions as a molecular switch for color photoreceptor differentiation in Drosophila. Development 134(23): 4243–53.

30. MoreyM, YeeSK, HermanT, NernA, Blanco, etal (2008) Coordinate control of synaptic-layer specificity and rhodopsins in photoreceptor neurons. Nature 456(7223): 795–9.

31. Hardie R.C. (1985). Functional organization of the fly retina. In Progress in sensory physiology, H Autrum, D Ottoson, E. R Perl, R. FSchmidt, H Shimazu and W.D Willis, eds ( Berlin: Springer), pp 1–79.

32. BellML, EarlJB, BrittSG (2007) Two types of Drosophila R7 photoreceptor cells are arranged randomly: a model for stochastic cell-fate determination. J Comp Neurol 502(1): 75–85.

33. ThanawalaSU, RisterJ, GoldbergGW, ZuskovA, OlesnickyEC, et al. (2013) Regional modulation of a stochastically expressed factor determines photoreceptor subtypes in the Drosophila retina. Dev Cell 25(1): 93–105.

34. FeilerR, BjornsonR, KirschfeldK, MismerD, RubinGM, et al. (1992) Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J Neurosci 12(10): 3862–8.

35. ChouWH, HallKJ, WilsonDB, WidemanCL, TownsonSM, et al. (1996) Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron 17(6): 1101–15.

36. PapatsenkoD, ShengG, DesplanC (1997) A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development 124(9): 1665–73.

37. HuberA, SchulzS, BentropJ, GroellC, WolfrumU, et al. (1997) Molecular cloning of Drosophila Rh6 rhodopsin: the visual pigment of a subset of R8 photoreceptor cells. FEBS Lett 7 406(1-2): 6–10.

38. Chou, W H., Huber A., Bentrop J., Schulz S., Schwab K., et al. (1999). Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification. Development 126: 607–616.

39. Wernet M.F., Desplan C. (2004). Building a retinal mosaic: cell fate decisions in the fly eye. Trends Cell Biol. 14: 576–584.

40. YamaguchiS, Desplan, HeisenbergC (2010) M (2010) Contributions of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proc Natl Acad Sci U S A 107(12): 5634–9.

41. MazzoniEO, CelikA, WernetMF, VasiliauskasD, JohnstonRJ, et al. (2008) Iroquois complex genes induce co-expression of rhodopsins in Drosophila. PLoS Biol 6(4): e97.

42. Labhart T., Meyer E.P. (1999). Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc. Res. Tech. 47: 368–379.

43. Fortini, M.ERubin (1990) G.M (1990) Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev 4(3): 444–63.

44. Hardie R.C. (1984). Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. J. Comp. Physiol. A 154: 157–165.

45. WernetMF, VelezMM, ClarkDA, Baumann-KlausenerF, BrownJR, et al. (2012) Genetic dissection reveals two separate retinal substrates for polarization vision in Drosophila. Curr Biol 22(1): 12–20.

46. WeirPT, DickinsonMH (2012) Flying Drosophila orient to sky polarization. Curr Biol 22(1): 21–7.

47. RieckhofGE, CasaresF, RyooHD, Abu-ShaarM, MannRS (1997) Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. 91(2): 171–83.

48. Ladam F., Sagerström C.G. (2013). Hox regulation of transcription - more complex(es). Dev Dyn. 2013 Jun 13. doi:10.1002/dvdy.23997.

49. TahayatoA, SonnevilleR, PichaudF, WernetMF, PapatsenkoD, et al. (2003) Otd/Crx, a dual regulator for the specification of ommatidial subtypes in the Drosophila retina. Dev. Cell 5(3): 391–402.

50. JohnstonRJ, OtakeY, SoodP, VogtN, BehniaR, et al. (2011) Interlocked feedforward loops control cell-type-specific Rhodopsin expression in the Drosophila eye. 145(6): 956–68.

51. MishraM, OkeA, LebelC, McDonaldEC, PlummerZ, et al. (2010) Pph13 and orthodenticle define a dual regulatory pathway for photoreceptor cell morphogenesis and function. Development 137(17): 2895–904.

52. FinkelsteinR, SmouseD, CapaciTM, SpradlingAC, PerrimonN (1990) The orthodenticle gene encodes a novel homeo domain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev 4(9): 1516–27.

53. HouHY, HefferA, AndersonWR, LiuJ, BowlerT, et al. (2009) Stripy Ftz target genes are coordinately regulated by Ftz-F1. Dev Biol 335(2): 442–53.

54. FreundCL, Gregory-EvansCY, FurukawaT, PapaioannouM, LooserJ, et al. (1997) Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell 91(4): 543–53.

55. SwainPK, ChenS, WangQL, AffatigatoLM, CoatsCL, et al. (1997) Mutations in the cone-rod homeobox gene are associated with the cone-rod dystrophy photoreceptor degeneration. Neuron 19(6): 1329–36.

56. ReichertH (2005) A tripartite organization of the urbilaterian brain: developmental genetic evidence from Drosophila. Brain Res Bull 66(4-6): 491–4.

57. TerrellD, XieB, WorkmanM, MahatoS, ZelhofA, et al. (2012) OTX2 and CRX rescue overlapping and photoreceptor-specific functions in the Drosophila eye. Dev Dyn 241(1): 215–28.

58. LeuzingerS, HirthF, GerlichD, AcamporaD, SimeoneA, et al. (1998) Equivalence of the fly orthodenticle gene and the human OTX genes in embryonic brain development of Drosophila. Development 125(9): 1703–10.

59. AcamporaD, AvantaggiatoV, TuortoF, BaroneP, ReichertH, et al. (1998) Murine Otx1 and Drosophila otd genes share conserved genetic functions required in invertebrate and vertebrate brain development. Development 125(9): 1691–702.

60. StowersRS, SchwarzTL (1999) A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152(4): 1631–9.

61. FrankfortBJ, NoloR, ZhangZ, BellenH, MardonG (2001) senseless repression of rough is required for R8 photoreceptor differentiation in the developing Drosophila eye. Neuron 8 32(3): 403–14.

62. DomingosPM, BrownS, BarrioR, RatnakumarK, FrankfortBJ, et al. (2004) Regulation of R7 and R8 differentiation by the spalt genes. Dev Biol 273(1): 121–33.

63. Wada S. (1974). Spezielle randzonale Ommatidien der Fliegen (Diptera: Brachycera): Architektur und Verteilung in den Komplexaugen. Z. Morph. Tiere 77: 87–125.

64. van deWetering, CavalloM, DooijesR, van BeestD, van EsMJ, et al. (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88(6): 789–99.

65. FreemanM, BienzM (2000) EGF receptor/Rolled MAP kinase signalling protects cells against activated Armadillo in the Drosophila eye. EMBO Rep 2(2): 157–62.

66. Wolfe, S A., Nekludova L., & Pabo, C O. (2000). DNA recognition by Cys2His2 zinc finger proteins. Annual Review of Biophysics and Biomolecular Structure, 29: 183–212.

67. BrayerKJ, SegalDJ (2008) Keep your fingers off my DNA: protein-protein interactions mediated by C2H2 zinc finger domains. Cell Biochem Biophys 50(3): 111–31.

68. Ryoo, H D., Marty T., Casares F., Affolter M., and Mann, R S. (1999). Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex. Development 126: 5137–5148.

69. VandendriesER, JohnsonD, ReinkeR (1996) orthodenticle is required for photoreceptor cell development in the Drosophila eye. Dev Biol 173(1): 243–55.

70. HiraiH, TaniT, KikyoN (2010) Structure and functions of powerful transactivators: VP16, MyoD and FoxA. Int J Dev Biol 54(11-12): 1589–96.

71. MorganR (2006) Engrailed: complexity and economy of a multi-functional transcription factor. FEBS Lett 15 580(11): 2531–3.

72. Mikeladze-DvaliT, WernetMF, PistilloD, TelemanA, ChenYW, et al. (2005) The growth regulators Dlats and Melted interact in a bistable loop to specify opposite fates in R8 photoreceptors. Cell 122(5): 775–87.

73. JukamD, DesplanC (2011) Binary regulation of Hippo pathway by Merlin/NF2, Kibra, Lgl, and Melted specifies and maintains postmitotic neuronal fate. Dev Cell. 2011 Nov 15 21(5): 874–87.

74. BazarovAV, YaswenP (2011) Who is in the driver's seat in 8p12 amplifications? ZNF703 in luminal B breast tumors. Breast Cancer Res 25 13(3): 308.

75. KobayashiM, FujiokaM, TolkunovaEN, DekaD, Abu-ShaarM, et al. (2003) Engrailed cooperates with extradenticle and homothorax to repress target genes in Drosophila. Development 130(4): 741–51.

76. FujiokaM, GebeleinB, CoferZC, MannRS, JaynesJB (2012) Engrailed cooperates directly with Extradenticle and Homothorax on a distinct class of homeodomain binding sites to repress sloppy paired. Dev Biol 366(2): 382–92.

77. Li-KroegerD, WittLM, GrimesHL, CookTA, GebeleinB (2008) Hox and senseless antagonism functions as a molecular switch to regulate EGF secretion in the Drosophila PNS. Dev Cell 15(2): 298–308.

78. ZhaiZ, FuchsAL, LohmannI (2010) Cellular analysis of newly identified Hox downstream genes in Drosophila. Eur J Cell Biol 89(2-3): 273–8.

79. RunkoAP, SagerströmCG (2004) Isolation of nlz2 and characterization of essential domains in Nlz family proteins. J Biol Chem 279(12): 11917–25.

80. WimmerEA, JackleH, PfeifleC, CohenSM (1993) A Drosophila homologue of human Sp1 is a head-specific segmentation gene. Nature 66: 690–694.

81. AthanikarJN, SanchezHB, OsborneTF (1997) Promoter selective transcriptional synergy mediated by sterol regulatory element binding protein and Sp1: A critical role for the Btd domain of Sp1. Mol Cell Biol 17: 5193–5200.

82. McDonaldEC, XieB, WorkmanM, Charlton-PerkinsM, TerrellDA, et al. (2010) Separable transcriptional regulatory domains within Otd control photoreceptor terminal differentiation events. Dev Biol 347(1): 122–32.

83. BrownJD, DuttaS, BhartiK, BonnerRF, MunsonPJ, et al. (2009) Expression profiling during ocular development identifies 2 Nlz genes with a critical role in optic fissure closure. Proc Natl Acad Sci USA 106(5): 1462–7.

84. McGlinnE, RichmanJM, MetzisV, TownL, ButterfieldNC, et al. (2008) Expression of the NET family member Zfp503 is regulated by hedgehog and BMP signaling in the limb. Dev Dyn 237(4): 1172–82.

85. MosesK, RubinGM (1991). Glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev 5: 583–593.

86. BrandAH, PerrimonN (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.