Notch Controls Cell Adhesion in the Drosophila Eye
Sporadic evidence suggests Notch is involved in cell adhesion. However, the underlying mechanism is unknown. Here I have investigated an epithelial remodeling process in the Drosophila eye in which two primary pigment cells (PPCs) with a characteristic ‘kidney’ shape enwrap and eventually isolate a group of cone cells from inter-ommatidial cells (IOCs). This paper shows that in the developing Drosophila eye the ligand Delta was transcribed in cone cells and Notch was activated in the adjacent PPC precursors. In the absence of Notch, emerging PPCs failed to enwrap cone cells, and hibris (hbs) and sns, two genes coding for adhesion molecules of the Nephrin group that mediate preferential adhesion, were not transcribed in PPC precursors. Conversely, activation of Notch in single IOCs led to ectopic expression of hbs and sns. By contrast, in a single IOC that normally transcribes rst, a gene coding for an adhesion molecule of the Neph1 group that binds Hbs and Sns, activation of Notch led to a loss of rst transcription. In addition, in a Notch mutant where two emerging PPCs failed to enwrap cone cells, expression of hbs in PPC precursors restored the ability of these cells to surround cone cells. Further, expression of hbs or rst in a single rst- or hbs-expressing cell, respectively, led to removal of the counterpart from the membrane within the same cell through cis-interaction and forced expression of Rst in all hbs-expressing PPCs strongly disrupted the remodeling process. Finally, a loss of both hbs and sns in single PPC precursors led to constriction of the apical surface that compromised the ‘kidney’ shape of PPCs. Taken together, these results indicate that cone cells utilize Notch signaling to instruct neighboring PPC precursors to surround them and Notch controls the remodeling process by differentially regulating four adhesion genes.
Vyšlo v časopise:
Notch Controls Cell Adhesion in the Drosophila Eye. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004087
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004087
Souhrn
Sporadic evidence suggests Notch is involved in cell adhesion. However, the underlying mechanism is unknown. Here I have investigated an epithelial remodeling process in the Drosophila eye in which two primary pigment cells (PPCs) with a characteristic ‘kidney’ shape enwrap and eventually isolate a group of cone cells from inter-ommatidial cells (IOCs). This paper shows that in the developing Drosophila eye the ligand Delta was transcribed in cone cells and Notch was activated in the adjacent PPC precursors. In the absence of Notch, emerging PPCs failed to enwrap cone cells, and hibris (hbs) and sns, two genes coding for adhesion molecules of the Nephrin group that mediate preferential adhesion, were not transcribed in PPC precursors. Conversely, activation of Notch in single IOCs led to ectopic expression of hbs and sns. By contrast, in a single IOC that normally transcribes rst, a gene coding for an adhesion molecule of the Neph1 group that binds Hbs and Sns, activation of Notch led to a loss of rst transcription. In addition, in a Notch mutant where two emerging PPCs failed to enwrap cone cells, expression of hbs in PPC precursors restored the ability of these cells to surround cone cells. Further, expression of hbs or rst in a single rst- or hbs-expressing cell, respectively, led to removal of the counterpart from the membrane within the same cell through cis-interaction and forced expression of Rst in all hbs-expressing PPCs strongly disrupted the remodeling process. Finally, a loss of both hbs and sns in single PPC precursors led to constriction of the apical surface that compromised the ‘kidney’ shape of PPCs. Taken together, these results indicate that cone cells utilize Notch signaling to instruct neighboring PPC precursors to surround them and Notch controls the remodeling process by differentially regulating four adhesion genes.
Zdroje
1. BaroloS, PosakonyJW (2002) Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 16: 1167–1181.
2. DahmannC, BaslerK (1999) Compartment boundaries: at the edge of development. Trends Genet 15: 320–326.
3. IrvineKD, VogtTF (1997) Dorsal-ventral signaling in limb development. Curr Opin Cell Biol 9: 867–876.
4. CaganRL, ReadyDF (1989) Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev 3: 1099–1112.
5. HoppePE, GreenspanRJ (1986) Local function of the Notch gene for embryonic ectodermal pathway choice in Drosophila. Cell 46: 773–783.
6. HoltfreterJ (1939) Gewebeaffinität, ein Mittel der embryonal Formbildung. Arch Exptl Zellforsch Gewebezucht 23: 169–209.
7. HoltfreterJ (1944) A study of the mechanics of gastrulation: Part II. J Exp Zool 95: 171–212.
8. SteinbergMS (1963) Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science 141: 401–408.
9. SteinbergMS (1970) Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J Exp Zool 173: 395–433.
10. GodtD, TepassU (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395: 387–391.
11. Gonzalez-ReyesA, St JohnstonD (1998) The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte. Development 125: 3635–3644.
12. HayashiT, CarthewRW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431: 647–652.
13. PriceSR, De Marco GarciaNV, RanschtB, JessellTM (2002) Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109: 205–216.
14. BaoS, CaganR (2005) Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell 8: 925–935.
15. FischbachKF, LinneweberGA, AndlauerTF, HertensteinA, BonengelB, et al. (2009) The irre cell recognition module (IRM) proteins. J Neurogenet 23: 48–67.
16. Garcia-BellidoA, MerriamJR (1969) Cell lineage of the imaginal discs in Drosophila gynandromorphs. J Exp Zool 170: 61–75.
17. ShellenbargerDL, MohlerJD (1975) Temperature-sensitive mutations of the notch locus in Drosophila melanogaster. Genetics 81: 143–162.
18. LarsonDE, LibermanZ, CaganRL (2008) Cellular behavior in the developing Drosophila pupal retina. Mech Dev 125: 223–232.
19. FehonRG, JohansenK, RebayI, Artavanis-TsakonasS (1991) Complex cellular and subcellular regulation of notch expression during embryonic and imaginal development of Drosophila: implications for notch function. J Cell Biol 113: 657–669.
20. KoohPJ, FehonRG, MuskavitchMA (1993) Implications of dynamic patterns of Delta and Notch expression for cellular interactions during Drosophila development. Development 117: 493–507.
21. ParksAL, TurnerFR, MuskavitchMA (1995) Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development. Mech Dev 50: 201–216.
22. FurriolsM, BrayS (2001) A model Notch response element detects Suppressor of Hairless-dependent molecular switch. Curr Biol 11: 60–64.
23. BaoS, FischbachKF, CorbinV, CaganRL (2010) Preferential adhesion maintains separation of ommatidia in the Drosophila eye. Dev Biol 344: 948–956.
24. StruhlG, FitzgeraldK, GreenwaldI (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74: 331–345.
25. FuW, NollM (1997) The Pax2 homolog sparkling is required for development of cone and pigment cells in the Drosophila eye. Genes Dev 11: 2066–2078.
26. Artavanis-TsakonasS, RandMD, LakeRJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284: 770–776.
27. JacobsenTL, BrennanK, AriasAM, MuskavitchMA (1998) Cis-interactions between Delta and Notch modulate neurogenic signalling in Drosophila. Development 125: 4531–4540.
28. MillerAC, LyonsEL, HermanTG (2009) cis-Inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr Biol 19: 1378–1383.
29. NagarajR, BanerjeeU (2007) Combinatorial signaling in the specification of primary pigment cells in the Drosophila eye. Development 134: 825–831.
30. SinghJ, MlodzikM (2012) Hibris, a Drosophila nephrin homolog, is required for presenilin-mediated Notch and APP-like cleavages. Dev Cell 23: 82–96.
31. ApitzH, KambacheldM, HohneM, RamosRG, StraubeA, et al. (2004) Identification of regulatory modules mediating specific expression of the roughest gene in Drosophila melanogaster. Dev Genes Evol 214: 453–459.
32. LeeT, LuoL (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451–461.
33. SchneiderT, ReiterC, EuleE, BaderB, LichteB, et al. (1995) Restricted expression of the irreC-rst protein is required for normal axonal projections of columnar visual neurons. Neuron 15: 259–271.
34. BourBA, ChakravartiM, WestJM, AbmayrSM (2000) Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev 14: 1498–1511.
35. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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