Is Required for the Expression of Principal Recognition Molecules That Control Axon Targeting in the Retina

English version České info

Establishing neural circuits during brain development relies on the ability for neurons to find their appropriate targets, a task that depends on recognition molecules whose expression must be tightly controlled. Very little is known of the factors that control the expression of these molecules. Here we have used the genetically amenable fly retina to address this issue. We identify Orthodenticle, a protein involved in mammalian brain development, as a main component of a new genetic cascade controlling the expression of recognition molecules that govern the wiring of the fly retina. Our work raises the issue that Orthodenticle might play a similar role in mammals. It also sheds new light on the genetic basis for wiring a model neural circuit during development.

Vyšlo v časopise: Is Required for the Expression of Principal Recognition Molecules That Control Axon Targeting in the Retina. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005303
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005303

Souhrn

Zdroje

1. O'Tousa JE, Baehr W, Martin RL, Hirsh J, Pak WL, et al. (1985) The Drosophila ninaE gene encodes an opsin. Cell 40 : 839–850. 2985266

2. Meinertzhagen IA, Hanson, T.E. (1993) The development ofthe optic lobe: Bate, Martinez Arias.

3. Clandinin TR, Zipursky SL (2000) Afferent growth cone interactions control synaptic specificity in the Drosophila visual system. Neuron 28 : 427–436. 11144353

4. Montell C, Jones K, Zuker C, Rubin G (1987) A second opsin gene expressed in the ultraviolet-sensitive R7 photoreceptor cells of Drosophila melanogaster. The Journal of neuroscience: the official journal of the Society for Neuroscience 7 : 1558–1566.

5. Chou WH, Hall KJ, Wilson DB, Wideman CL, Townson SM, et al. (1996) Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron 17 : 1101–1115. 8982159

6. Papatsenko D, Sheng G, Desplan C (1997) A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development 124 : 1665–1673. 9165115

7. Senti KA, Usui T, Boucke K, Greber U, Uemura T, et al. (2003) Flamingo regulates R8 axon-axon and axon-target interactions in the Drosophila visual system. Current biology: CB 13 : 828–832. 12747830

8. Shinza-Kameda M, Takasu E, Sakurai K, Hayashi S, Nose A (2006) Regulation of layer-specific targeting by reciprocal expression of a cell adhesion molecule, capricious. Neuron 49 : 205–213. 16423695

9. Ting CY, Yonekura S, Chung P, Hsu SN, Robertson HM, et al. (2005) Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents. Development 132 : 953–963. 15673571

10. Hadjieconomou D, Timofeev K, Salecker I (2011) A step-by-step guide to visual circuit assembly in Drosophila. Curr Opin Neurobiol 21 : 76–84. doi: 10.1016/j.conb.2010.07.012 20800474

11. Astigarraga S, Hofmeyer K, Treisman JE (2010) Missed connections: photoreceptor axon seeks target neuron for synaptogenesis. Curr Opin Genet Dev 20 : 400–407. doi: 10.1016/j.gde.2010.04.001 20434326

12. Lee RC, Clandinin TR, Lee CH, Chen PL, Meinertzhagen IA, et al. (2003) The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nature neuroscience 6 : 557–563. 12754514

13. Hein I, Suzuki T, Grunwald Kadow IC (2013) Gogo receptor contributes to retinotopic map formation and prevents R1-6 photoreceptor axon bundling. PloS one 8: e66868. doi: 10.1371/journal.pone.0066868 23826162

14. Lee CH, Herman T, Clandinin TR, Lee R, Zipursky SL (2001) N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30 : 437–450. 11395005

15. Clandinin TR, Lee CH, Herman T, Lee RC, Yang AY, et al. (2001) Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 32 : 237–248. 11683994

16. Tomasi T, Hakeda-Suzuki S, Ohler S, Schleiffer A, Suzuki T (2008) The transmembrane protein Golden goal regulates R8 photoreceptor axon-axon and axon-target interactions. Neuron 57 : 691–704. doi: 10.1016/j.neuron.2008.01.012 18341990

17. Hakeda-Suzuki S, Berger-Muller S, Tomasi T, Usui T, Horiuchi SY, et al. (2011) Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system. Nature neuroscience 14 : 314–323. doi: 10.1038/nn.2756 21317905

18. Song J, Wu L, Chen Z, Kohanski RA, Pick L (2003) Axons guided by insulin receptor in Drosophila visual system. Science 300 : 502–505. 12702880

19. Petrovic M, Hummel T (2008) Temporal identity in axonal target layer recognition. Nature 456 : 800–803. doi: 10.1038/nature07407 18978776

20. Morey M, Yee SK, Herman T, Nern A, Blanco E, et al. (2008) Coordinate control of synaptic-layer specificity and rhodopsins in photoreceptor neurons. Nature 456 : 795–799. doi: 10.1038/nature07419 18978774

21. Vandendries ER, Johnson D, Reinke R (1996) orthodenticle is required for photoreceptor cell development in the Drosophila eye. Developmental biology 173 : 243–255. 8575625

22. Fichelson P, Brigui A, Pichaud F (2012) Orthodenticle and Kruppel homolog 1 regulate Drosophila photoreceptor maturation. Proceedings of the National Academy of Sciences of the United States of America 109 : 7893–7898. doi: 10.1073/pnas.1120276109 22547825

23. Tahayato A, Sonneville R, Pichaud F, Wernet MF, Papatsenko D, et al. (2003) Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina. Developmental cell 5 : 391–402. 12967559

24. McDonald EC, Xie B, Workman M, Charlton-Perkins M, Terrell DA, et al. (2010) Separable transcriptional regulatory domains within Otd control photoreceptor terminal differentiation events. Developmental biology 347 : 122–132. doi: 10.1016/j.ydbio.2010.08.016 20732315

25. Weimann JM, Zhang YA, Levin ME, Devine WP, Brulet P, et al. (1999) Cortical neurons require Otx1 for the refinement of exuberant axonal projections to subcortical targets. Neuron 24 : 819–831. 10624946

26. Morrow EM, Furukawa T, Raviola E, Cepko CL (2005) Synaptogenesis and outer segment formation are perturbed in the neural retina of Crx mutant mice. BMC neuroscience 6 : 5. 15676071

27. Velez MM, Gohl D, Clandinin TR, Wernet MF (2014) Differences in neural circuitry guiding behavioral responses to polarized light presented to either the dorsal or ventral retina in Drosophila. Journal of neurogenetics: 1–30.

28. Schwabe T, Borycz JA, Meinertzhagen IA, Clandinin TR (2014) Differential adhesion determines the organization of synaptic fascicles in the Drosophila visual system. Current biology: CB 24 : 1304–1313. doi: 10.1016/j.cub.2014.04.047 24881879

29. Chen PL, Clandinin TR (2008) The cadherin Flamingo mediates level-dependent interactions that guide photoreceptor target choice in Drosophila. Neuron 58 : 26–33. doi: 10.1016/j.neuron.2008.01.007 18400160

30. Finkelstein R, Smouse D, Capaci TM, Spradling AC, Perrimon N (1990) The orthodenticle gene encodes a novel homeo domain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes & development 4 : 1516–1527.

31. Wu JS, Luo L (2006) A protocol for mosaic analysis with a repressible cell marker (MARCM) in Drosophila. Nature protocols 1 : 2583–2589. 17406512

32. Kittel RJ, Wichmann C, Rasse TM, Fouquet W, Schmidt M, et al. (2006) Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312 : 1051–1054. 16614170

33. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49 : 833–844. 16543132

34. Frankfort BJ, Mardon G (2002) R8 development in the Drosophila eye: a paradigm for neural selection and differentiation. Development 129 : 1295–1306. 11880339

35. Kimura H, Usui T, Tsubouchi A, Uemura T (2006) Potential dual molecular interaction of the Drosophila 7-pass transmembrane cadherin Flamingo in dendritic morphogenesis. Journal of cell science 119 : 1118–1129. 16507587

36. Schwabe T, Neuert H, Clandinin TR (2013) A network of cadherin-mediated interactions polarizes growth cones to determine targeting specificity. Cell 154 : 351–364. doi: 10.1016/j.cell.2013.06.011 23870124

37. Xie B, Charlton-Perkins M, McDonald E, Gebelein B, Cook T (2007) Senseless functions as a molecular switch for color photoreceptor differentiation in Drosophila. Development 134 : 4243–4253. 17978002

38. Berger-Muller S, Sugie A, Takahashi F, Tavosanis G, Hakeda-Suzuki S, et al. (2013) Assessing the role of cell-surface molecules in central synaptogenesis in the Drosophila visual system. PloS one 8: e83732. doi: 10.1371/journal.pone.0083732 24386266

39. Rhinn M, Brand M (2001) The midbrain—hindbrain boundary organizer. Current opinion in neurobiology 11 : 34–42. 11179870

40. Tossell K, Andreae LC, Cudmore C, Lang E, Muthukrishnan U, et al. (2011) Lrrn1 is required for formation of the midbrain-hindbrain boundary and organiser through regulation of affinity differences between midbrain and hindbrain cells in chick. Developmental biology 352 : 341–352. doi: 10.1016/j.ydbio.2011.02.002 21315708

41. Edwards TN, Meinertzhagen IA (2009) Photoreceptor neurons find new synaptic targets when misdirected by overexpressing runt in Drosophila. The Journal of neuroscience: the official journal of the Society for Neuroscience 29 : 828–841.

42. Pinal N, Goberdhan DC, Collinson L, Fujita Y, Cox IM, et al. (2006) Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Current biology: CB 16 : 140–149. 16431366

43. Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87 : 651–660. 8929534

44. Miller AC, Seymour H, King C, Herman TG (2008) Loss of seven-up from Drosophila R1/R6 photoreceptors reveals a stochastic fate choice that is normally biased by Notch. Development 135 : 707–715. doi: 10.1242/dev.016386 18199577

45. Pichaud F, Desplan C (2001) A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia. Development 128 : 815–826. 11222137