Regeneration of Sensory Hair Cells Requires Localized Interactions between the Notch and Wnt Pathways

Andrés Romero-Carvajal; Joaquín Navajas Acedo; Linjia Jiang; Agne Kozlovskaja-Gumbriene; Richard Alexander; Hua Li; Tatjana Piotrowski

doi:10.1016/j.devcel.2015.05.025

Regeneration of Sensory Hair Cells Requires Localized Interactions between the Notch and Wnt Pathways

Andrés Romero-Carvajal, Joaquín Navajas Acedo, Linjia Jiang, Agne Kozlovskaja-Gumbriene, Richard Alexander, Hua Li, Tatjana Piotrowski^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

84 Scopus citations

Abstract

In vertebrates, mechano-electrical transduction of sound is accomplished by sensory hair cells. Whereas mammalian hair cells are not replaced when lost, in fish they constantly renew and regenerate after injury. In vivo tracking and cell fate analyses of all dividing cells during lateral line hair cell regeneration revealed that support and hair cell progenitors localize to distinct tissue compartments. Importantly, we find that the balance between self-renewal and differentiation in these compartments is controlled by spatially restricted Notch signaling and its inhibition of Wnt-induced proliferation. The ability to simultaneously study and manipulate individual cell behaviors and multiple pathways in vivo transforms the lateral line into a powerful paradigm to mechanistically dissect sensory organ regeneration. The striking similarities to other vertebrate stem cell compartments uniquely place zebrafish to help elucidate why mammals possess such low capacity to regenerate hair cells.

Original language	English
Pages (from-to)	267-282
Number of pages	16
Journal	Developmental Cell
Volume	34
Issue number	3
DOIs	https://doi.org/10.1016/j.devcel.2015.05.025
State	Published - 10 Aug 2015
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2015 Elsevier Inc.

Funding

We are grateful to Drs. A. Sánchez Alvarado, L. Li, M. Lush, J. Kniss, and M. Venero Galanternik for valuable comments on the manuscript and to Drs. V. Korzh, N. Lawson, T. Ishitani, H. Wada, K. Kawakami, B. Appel, and P. Kulesa for strains and reagents. We are also thankful to R. Duncan and E. Young for preliminary experiments, members of the T.P. lab, and Dr. T. Xie for insightful discussions. We would also like to thank D. Fekete for suggesting the neo-LY-neo experiment. We thank the University of Utah Zebrafish Core and the Aquatics Facility at the Stowers Institute for excellent fish care; J. Unruh and B. Rubinstein for support with the spatial analysis; J. Lange, S. McKinney, and the Microscopy Core for imaging support; and M. Miller for help with graphic design. This work was funded by an NIH (NIDCD) award RC1DC010631 (to T.P.), by the Hearing Health Foundation, and by institutional support from the Stowers Institute for Medical Research.

Funders	Funder number
National Institutes of Health
National Institute on Deafness and Other Communication Disorders	RC1DC010631
Hearing Health Foundation
Stowers Institute for Medical Research

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10.1016/j.devcel.2015.05.025

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title = "Regeneration of Sensory Hair Cells Requires Localized Interactions between the Notch and Wnt Pathways",

abstract = "In vertebrates, mechano-electrical transduction of sound is accomplished by sensory hair cells. Whereas mammalian hair cells are not replaced when lost, in fish they constantly renew and regenerate after injury. In vivo tracking and cell fate analyses of all dividing cells during lateral line hair cell regeneration revealed that support and hair cell progenitors localize to distinct tissue compartments. Importantly, we find that the balance between self-renewal and differentiation in these compartments is controlled by spatially restricted Notch signaling and its inhibition of Wnt-induced proliferation. The ability to simultaneously study and manipulate individual cell behaviors and multiple pathways in vivo transforms the lateral line into a powerful paradigm to mechanistically dissect sensory organ regeneration. The striking similarities to other vertebrate stem cell compartments uniquely place zebrafish to help elucidate why mammals possess such low capacity to regenerate hair cells.",

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AU - Kozlovskaja-Gumbriene, Agne

AU - Alexander, Richard

AU - Li, Hua

AU - Piotrowski, Tatjana

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AB - In vertebrates, mechano-electrical transduction of sound is accomplished by sensory hair cells. Whereas mammalian hair cells are not replaced when lost, in fish they constantly renew and regenerate after injury. In vivo tracking and cell fate analyses of all dividing cells during lateral line hair cell regeneration revealed that support and hair cell progenitors localize to distinct tissue compartments. Importantly, we find that the balance between self-renewal and differentiation in these compartments is controlled by spatially restricted Notch signaling and its inhibition of Wnt-induced proliferation. The ability to simultaneously study and manipulate individual cell behaviors and multiple pathways in vivo transforms the lateral line into a powerful paradigm to mechanistically dissect sensory organ regeneration. The striking similarities to other vertebrate stem cell compartments uniquely place zebrafish to help elucidate why mammals possess such low capacity to regenerate hair cells.

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Regeneration of Sensory Hair Cells Requires Localized Interactions between the Notch and Wnt Pathways

Abstract

Bibliographical note

Funding

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