Chromatin Modification of Notch Targets in Olfactory Receptor Neuron Diversification

Overview

Journal Nat Neurosci

Date 2011 Dec 27

PMID 22197833

Citations 46

Authors

Keita Endo

M Rezaul Karim

Hiroaki Taniguchi

Alena Krejci

Emi Kinameri

Matthias Siebert

Kei Ito

Sarah J Bray

Adrian W Moore

Affiliations

Soon will be listed here.

Abstract

Neuronal-class diversification is central during neurogenesis. This requirement is exemplified in the olfactory system, which utilizes a large array of olfactory receptor neuron (ORN) classes. We discovered an epigenetic mechanism in which neuron diversity is maximized via locus-specific chromatin modifications that generate context-dependent responses from a single, generally used intracellular signal. Each ORN in Drosophila acquires one of three basic identities defined by the compound outcome of three iterated Notch signaling events during neurogenesis. Hamlet, the Drosophila Evi1 and Prdm16 proto-oncogene homolog, modifies cellular responses to these iteratively used Notch signals in a context-dependent manner, and controls odorant receptor gene choice and ORN axon targeting specificity. In nascent ORNs, Hamlet erases the Notch state inherited from the parental cell, enabling a modified response in a subsequent round of Notch signaling. Hamlet directs locus-specific modifications of histone methylation and histone density and controls accessibility of the DNA-binding protein Suppressor of Hairless at the Notch target promoter.

Citing Articles

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References

Moore A, Roegiers F, Jan L, Jan Y . Conversion of neurons and glia to external-cell fates in the external sensory organs of Drosophila hamlet mutants by a cousin-cousin cell-type respecification. Genes Dev. 2004; 18(6):623-8. PMC: 387238. DOI: 10.1101/gad.1170904. View

Mukherjee A, Veraksa A, Bauer A, Rosse C, Camonis J, Artavanis-Tsakonas S . Regulation of Notch signalling by non-visual beta-arrestin. Nat Cell Biol. 2005; 7(12):1191-201. DOI: 10.1038/ncb1327. View

Vosshall L, Amrein H, Morozov P, Rzhetsky A, Axel R . A spatial map of olfactory receptor expression in the Drosophila antenna. Cell. 1999; 96(5):725-36. DOI: 10.1016/s0092-8674(00)80582-6. View

Moore A, Jan L, Jan Y . hamlet, a binary genetic switch between single- and multiple- dendrite neuron morphology. Science. 2002; 297(5585):1355-8. DOI: 10.1126/science.1072387. View

Mori K, Sakano H . How is the olfactory map formed and interpreted in the mammalian brain?. Annu Rev Neurosci. 2011; 34:467-99. DOI: 10.1146/annurev-neuro-112210-112917. View

Endo K, Aoki T, Yoda Y, Kimura K, Hama C . Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat Neurosci. 2007; 10(2):153-60. DOI: 10.1038/nn1832. View

Matsuzaki F, Koizumi K, Hama C, Yoshioka T, Nabeshima Y . Cloning of the Drosophila prospero gene and its expression in ganglion mother cells. Biochem Biophys Res Commun. 1992; 182(3):1326-32. DOI: 10.1016/0006-291x(92)91878-t. View

Komiyama T, Carlson J, Luo L . Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat Neurosci. 2004; 7(8):819-25. DOI: 10.1038/nn1284. View

Wang S, Jan L, Jan Y . Only a subset of the binary cell fate decisions mediated by Numb/Notch signaling in Drosophila sensory organ lineage requires Suppressor of Hairless. Development. 1997; 124(22):4435-46. DOI: 10.1242/dev.124.22.4435. View

10.

Andrews H, Giagtzoglou N, Yamamoto S, Schulze K, Bellen H . Sequoia regulates cell fate decisions in the external sensory organs of adult Drosophila. EMBO Rep. 2009; 10(6):636-41. PMC: 2711842. DOI: 10.1038/embor.2009.66. View

11.

Schneider R, Bannister A, Myers F, Thorne A, Crane-Robinson C, Kouzarides T . Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol. 2003; 6(1):73-7. DOI: 10.1038/ncb1076. View

12.

Izutsu K, Kurokawa M, Imai Y, Maki K, Mitani K, Hirai H . The corepressor CtBP interacts with Evi-1 to repress transforming growth factor beta signaling. Blood. 2001; 97(9):2815-22. DOI: 10.1182/blood.v97.9.2815. View

13.

Bernstein B, Humphrey E, Erlich R, Schneider R, Bouman P, Liu J . Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci U S A. 2002; 99(13):8695-700. PMC: 124361. DOI: 10.1073/pnas.082249499. View

14.

Shi Y, Sawada J, Sui G, Affar E, Whetstine J, Lan F . Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature. 2003; 422(6933):735-8. DOI: 10.1038/nature01550. View

15.

Kinameri E, Inoue T, Aruga J, Imayoshi I, Kageyama R, Shimogori T . Prdm proto-oncogene transcription factor family expression and interaction with the Notch-Hes pathway in mouse neurogenesis. PLoS One. 2008; 3(12):e3859. PMC: 2585159. DOI: 10.1371/journal.pone.0003859. View

16.

Wagh D, Rasse T, Asan E, Hofbauer A, Schwenkert I, Durrbeck H . Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron. 2006; 49(6):833-44. DOI: 10.1016/j.neuron.2006.02.008. View

17.

Ray A, van der Goes van Naters W, Shiraiwa T, Carlson J . Mechanisms of odor receptor gene choice in Drosophila. Neuron. 2007; 53(3):353-69. PMC: 1986798. DOI: 10.1016/j.neuron.2006.12.010. View

18.

Pires-daSilva A, Sommer R . The evolution of signalling pathways in animal development. Nat Rev Genet. 2003; 4(1):39-49. DOI: 10.1038/nrg977. View

19.

Kramatschek B, Campos-Ortega J . Neuroectodermal transcription of the Drosophila neurogenic genes E(spl) and HLH-m5 is regulated by proneural genes. Development. 1994; 120(4):815-26. DOI: 10.1242/dev.120.4.815. View

20.

Lim D, Huang Y, Swigut T, Mirick A, Garcia-Verdugo J, Wysocka J . Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature. 2009; 458(7237):529-33. PMC: 3800116. DOI: 10.1038/nature07726. View