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RESEARCH ARTICLE
Ontogenesis of the tear drainage system requires Prickle1-driven polarized basement membrane deposition
Dianlei Guo, Jiali Ru, Fuxiang Mao, Hong Ouyang, Rong Ju, Kaili Wu, Yizhi Liu, Chunqiao Liu
Development 2020 147: dev191726 doi: 10.1242/dev.191726 Published 30 November 2020
Dianlei Guo
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Jiali Ru
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Fuxiang Mao
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Hong Ouyang
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Rong Ju
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Kaili Wu
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Yizhi Liu
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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Chunqiao Liu
State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China
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  • ORCID record for Chunqiao Liu
  • For correspondence: liuchunq3@mail.sysu.edu.cn

Handling Editor: Liz Robertson

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ABSTRACT

In terrestrial animals, the lacrimal drainage apparatus evolved to serve as conduits for tear flow; however, little is known about the ontogenesis of this system. Here, we define the anatomy of the fully formed tear duct in mice, characterize crucial morphogenetic events for the development of tear duct components and identify the site for primordial tear duct (PTD) initiation. We report that the PTD originates from the orbital lacrimal lamina, a junction formed by the epithelia of the maxillary and lateral nasal processes. We demonstrate that Prickle1, a key component of planar cell polarity signaling, is expressed in progenitors of the PTD and throughout tear duct morphogenesis. Disruption of Prickle1 stalls tear duct elongation; in particular, the loss of basement membrane deposition and aberrant cytoplasmic accumulation of laminin are salient. Altered cell adhesion, cytoskeletal transport systems, vesicular transport systems and cell axis orientation in Prickle1 mutants support the role of Prickle1 in planar cell polarity. Taken together, our results highlight a crucial role of Prickle1-mediated polarized basement membrane secretion and deposition in PTD elongation.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Formal analysis: R.J.; Investigation: D.G., J.R., F.M., C.L.; Resources: H.O., Y.L.; Data curation: D.G., J.R., K.W., C.L.; Writing - original draft: D.G., J.R., C.L.; Writing - review & editing: C.L.; Supervision: Y.L.; Project administration: F.M.; Funding acquisition: H.O., C.L.

  • Funding

    This work was supported by grants from the National Natural Science Foundation of China (NSFC: 31571077; Beijing, China), the Guangzhou Science and Technology Innovation Center (201707020009; Guangzhou, Guangdong Province, China), ‘100 People Plan’ from Sun Yat-sen University (8300-18821104; Guangzhou, Guangdong Province, China) and research funding from State Key Laboratory of Ophthalmology at Zhongshan Ophthalmic Center (303060202400339; Guangzhou, Guangdong Province, China) to C.L.; and from the National Natural Science Foundation of China (NSFC: 81622012; Beijing, China) to H.O.

  • Supplementary information

    Supplementary information available online at https://dev.biologists.org/lookup/doi/10.1242/dev.191726.supplemental

  • Received April 17, 2020.
  • Accepted October 23, 2020.
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Keywords

  • Basement membrane
  • Ontogenesis
  • Planar cell polarity
  • Polarized deposition
  • Prickle1
  • Tear duct

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RESEARCH ARTICLE
Ontogenesis of the tear drainage system requires Prickle1-driven polarized basement membrane deposition
Dianlei Guo, Jiali Ru, Fuxiang Mao, Hong Ouyang, Rong Ju, Kaili Wu, Yizhi Liu, Chunqiao Liu
Development 2020 147: dev191726 doi: 10.1242/dev.191726 Published 30 November 2020
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RESEARCH ARTICLE
Ontogenesis of the tear drainage system requires Prickle1-driven polarized basement membrane deposition
Dianlei Guo, Jiali Ru, Fuxiang Mao, Hong Ouyang, Rong Ju, Kaili Wu, Yizhi Liu, Chunqiao Liu
Development 2020 147: dev191726 doi: 10.1242/dev.191726 Published 30 November 2020

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