Live Imaging of Hair Bundle Polarity Acquisition Demonstrates a Critical Timeline for Transcription Factor Emx2

Overview

Journal Elife

Specialty Biology

Date 2020 Sep 23

PMID 32965215

Citations 7

Authors

Yosuke Tona

Doris K Wu

Affiliations

Soon will be listed here.

Abstract

Directional sensitivity of hair cells (HCs) is conferred by the aymmetric apical hair bundle, comprised of a kinocilium and stereocilia staircase. The mother centriole (MC) forms the base of the kinocilium and the stereocilia develop adjacent to it. Previously, we showed that transcription factor Emx2 reverses hair bundle orientation and its expression in the mouse vestibular utricle is restricted, resulting in two regions of opposite bundle orientation (Jiang et al., 2017). Here, we investigated establishment of opposite bundle orientation in embryonic utricles by live-imaging GFP-labeled centrioles in HCs. The daughter centriole invariably migrated ahead of the MC from the center to their respective peripheral locations in HCs. Comparing HCs between utricular regions, centriole trajectories were similar but they migrated toward opposite directions, suggesting that Emx2 pre-patterned HCs prior to centriole migration. Ectopic , however, reversed centriole trajectory within hours during a critical time-window when centriole trajectory was responsive to Emx2.

Citing Articles

Emx2 is an essential regulator of ciliated cell development across embryonic tissues.

Nguyen T, Rodriguez J, Wesselman H, Wingert R iScience. 2024; 27(12):111271.

PMID: 39687012 PMC: 11647118. DOI: 10.1016/j.isci.2024.111271.

In utero adeno-associated virus (AAV)-mediated gene delivery targeting sensory and supporting cells in the embryonic mouse inner ear.

Spinola C, de Monvel J, Safieddine S, Lahlou G, Etournay R PLoS One. 2024; 19(7):e0305742.

PMID: 39028743 PMC: 11259301. DOI: 10.1371/journal.pone.0305742.

Inhibitory G proteins play multiple roles to polarize sensory hair cell morphogenesis.

Jarysta A, Tadenev A, Day M, Krawchuk B, Low B, Wiles M Elife. 2024; 12.

PMID: 38651641 PMC: 11037916. DOI: 10.7554/eLife.88186.

Function of bidirectional sensitivity in the otolith organs established by transcription factor Emx2.

Ji Y, Tona Y, Wafa T, Christman M, Tourney E, Jiang T Nat Commun. 2022; 13(1):6330.

PMID: 36280667 PMC: 9592604. DOI: 10.1038/s41467-022-33819-3.

Mutations in OSBPL2 cause hearing loss associated with primary cilia defects via sonic hedgehog signaling.

Shi H, Wang H, Zhang C, Lu Y, Yao J, Chen Z JCI Insight. 2022; 7(4).

PMID: 35041619 PMC: 8876550. DOI: 10.1172/jci.insight.149626.

References

Mardin B, Lange C, Baxter J, Hardy T, Scholz S, Fry A . Components of the Hippo pathway cooperate with Nek2 kinase to regulate centrosome disjunction. Nat Cell Biol. 2010; 12(12):1166-76. PMC: 3939356. DOI: 10.1038/ncb2120. View

Zheng J, Gao W . Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci. 2000; 3(6):580-6. DOI: 10.1038/75753. View

Madisen L, Zwingman T, Sunkin S, Oh S, Zariwala H, Gu H . A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci. 2009; 13(1):133-40. PMC: 2840225. DOI: 10.1038/nn.2467. View

Kakehata S, Nakagawa T, Takasaka T, Akaike N . Cellular mechanism of acetylcholine-induced response in dissociated outer hair cells of guinea-pig cochlea. J Physiol. 1993; 463:227-44. PMC: 1175341. DOI: 10.1113/jphysiol.1993.sp019592. View

Pelletier L, Yamashita Y . Centrosome asymmetry and inheritance during animal development. Curr Opin Cell Biol. 2012; 24(4):541-6. PMC: 3425708. DOI: 10.1016/j.ceb.2012.05.005. View

Loukil A, Tormanen K, Sutterlin C . The daughter centriole controls ciliogenesis by regulating Neurl-4 localization at the centrosome. J Cell Biol. 2017; 216(5):1287-1300. PMC: 5412565. DOI: 10.1083/jcb.201608119. View

Montcouquiol M, Rachel R, Lanford P, Copeland N, Jenkins N, Kelley M . Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature. 2003; 423(6936):173-7. DOI: 10.1038/nature01618. View

Holley M, Rhodes C, Kneebone A, Herde M, Fleming M, Steel K . Emx2 and early hair cell development in the mouse inner ear. Dev Biol. 2010; 340(2):547-56. PMC: 2877772. DOI: 10.1016/j.ydbio.2010.02.004. View

Tarchini B, Lu X . New insights into regulation and function of planar polarity in the inner ear. Neurosci Lett. 2019; 709:134373. PMC: 6732021. DOI: 10.1016/j.neulet.2019.134373. View

10.

Betleja E, Nanjundappa R, Cheng T, Mahjoub M . A novel Cep120-dependent mechanism inhibits centriole maturation in quiescent cells. Elife. 2018; 7. PMC: 5986273. DOI: 10.7554/eLife.35439. View

11.

Schneider C, Rasband W, Eliceiri K . NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012; 9(7):671-5. PMC: 5554542. DOI: 10.1038/nmeth.2089. View

12.

Miyamoto N, Yoshida M, Kuratani S, Matsuo I, Aizawa S . Defects of urogenital development in mice lacking Emx2. Development. 1997; 124(9):1653-64. DOI: 10.1242/dev.124.9.1653. View

13.

Lepelletier L, de Monvel J, Buisson J, Desdouets C, Petit C . Auditory hair cell centrioles undergo confined Brownian motion throughout the developmental migration of the kinocilium. Biophys J. 2013; 105(1):48-58. PMC: 3703712. DOI: 10.1016/j.bpj.2013.05.009. View

14.

Mogensen M, Malik A, Piel M, Bornens M . Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J Cell Sci. 2000; 113 ( Pt 17):3013-23. DOI: 10.1242/jcs.113.17.3013. View

15.

Simeone A, Gulisano M, Acampora D, Stornaiuolo A, Rambaldi M, Boncinelli E . Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 1992; 11(7):2541-50. PMC: 556729. DOI: 10.1002/j.1460-2075.1992.tb05319.x. View

16.

Wallis D, Hamblen M, Zhou Y, Venken K, Schumacher A, Grimes H . The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival. Development. 2002; 130(1):221-32. DOI: 10.1242/dev.00190. View

17.

Evsen L, Sugahara S, Uchikawa M, Kondoh H, Wu D . Progression of neurogenesis in the inner ear requires inhibition of Sox2 transcription by neurogenin1 and neurod1. J Neurosci. 2013; 33(9):3879-90. PMC: 3865497. DOI: 10.1523/JNEUROSCI.4030-12.2013. View

18.

Montcouquiol M, Sans N, Huss D, Kach J, Dickman J, Forge A . Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. J Neurosci. 2006; 26(19):5265-75. PMC: 6674235. DOI: 10.1523/JNEUROSCI.4680-05.2006. View

19.

Yang J, Adamian M, Li T . Rootletin interacts with C-Nap1 and may function as a physical linker between the pair of centrioles/basal bodies in cells. Mol Biol Cell. 2005; 17(2):1033-40. PMC: 1356609. DOI: 10.1091/mbc.e05-10-0943. View

20.

Bermingham N, Hassan B, Price S, Vollrath M, Ben-Arie N, Eatock R . Math1: an essential gene for the generation of inner ear hair cells. Science. 1999; 284(5421):1837-41. DOI: 10.1126/science.284.5421.1837. View