Lethal giant larvae 2 regulates development of the ciliated organ Kupffer’s vesicle

H. Tay, S. Schulze, J. Compagnon, F. Foley, C.-P.J. Heisenberg, H.J. Yost, S. Abdelilah Seyfried, J. Amack, Development 140 (2013) 1550–1559.


Journal Article | Published | English
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Abstract
Motile cilia perform crucial functions during embryonic development and throughout adult life. Development of organs containing motile cilia involves regulation of cilia formation (ciliogenesis) and formation of a luminal space (lumenogenesis) in which cilia generate fluid flows. Control of ciliogenesis and lumenogenesis is not yet fully understood, and it remains unclear whether these processes are coupled. In the zebrafish embryo, lethal giant larvae 2 (lgl2) is expressed prominently in ciliated organs. Lgl proteins are involved in establishing cell polarity and have been implicated in vesicle trafficking. Here, we identified a role for Lgl2 in development of ciliated epithelia in Kupffer's vesicle, which directs left-right asymmetry of the embryo; the otic vesicles, which give rise to the inner ear; and the pronephric ducts of the kidney. Using Kupffer's vesicle as a model ciliated organ, we found that depletion of Lgl2 disrupted lumen formation and reduced cilia number and length. Immunofluorescence and time-lapse imaging of Kupffer's vesicle morphogenesis in Lgl2-deficient embryos suggested cell adhesion defects and revealed loss of the adherens junction component E-cadherin at lateral membranes. Genetic interaction experiments indicate that Lgl2 interacts with Rab11a to regulate E-cadherin and mediate lumen formation that is uncoupled from cilia formation. These results uncover new roles and interactions for Lgl2 that are crucial for both lumenogenesis and ciliogenesis and indicate that these processes are genetically separable in zebrafish.
Publishing Year
Date Published
2013-04-01
Journal Title
Development
Acknowledgement
Deposited in PMC for release after 12 months. We thank members of the Amack lab for helpful discussions and Mahendra Sonawane for donating reagents.
Volume
140
Issue
7
Page
1550 - 1559
IST-REx-ID

Cite this

Tay H, Schulze S, Compagnon J, et al. Lethal giant larvae 2 regulates development of the ciliated organ Kupffer’s vesicle. Development. 2013;140(7):1550-1559. doi:10.1242/dev.087130
Tay, H., Schulze, S., Compagnon, J., Foley, F., Heisenberg, C.-P. J., Yost, H. J., … Amack, J. (2013). Lethal giant larvae 2 regulates development of the ciliated organ Kupffer’s vesicle. Development, 140(7), 1550–1559. https://doi.org/10.1242/dev.087130
Tay, Hwee, Sabrina Schulze, Julien Compagnon, Fiona Foley, Carl-Philipp J Heisenberg, H Joseph Yost, Salim Abdelilah Seyfried, and Jeffrey Amack. “Lethal Giant Larvae 2 Regulates Development of the Ciliated Organ Kupffer’s Vesicle.” Development 140, no. 7 (2013): 1550–59. https://doi.org/10.1242/dev.087130.
H. Tay et al., “Lethal giant larvae 2 regulates development of the ciliated organ Kupffer’s vesicle,” Development, vol. 140, no. 7, pp. 1550–1559, 2013.
Tay H, Schulze S, Compagnon J, Foley F, Heisenberg C-PJ, Yost HJ, Abdelilah Seyfried S, Amack J. 2013. Lethal giant larvae 2 regulates development of the ciliated organ Kupffer’s vesicle. Development. 140(7), 1550–1559.
Tay, Hwee, et al. “Lethal Giant Larvae 2 Regulates Development of the Ciliated Organ Kupffer’s Vesicle.” Development, vol. 140, no. 7, Company of Biologists, 2013, pp. 1550–59, doi:10.1242/dev.087130.

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PMID: 23482490
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