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Sheath Cell Invasion and Trans-differentiation Repair Mechanical Damage Caused by Loss of Caveolae in the Zebrafish Notochord.

Publication ,  Journal Article
Garcia, J; Bagwell, J; Njaine, B; Norman, J; Levic, DS; Wopat, S; Miller, SE; Liu, X; Locasale, JW; Stainier, DYR; Bagnat, M
Published in: Curr Biol
July 10, 2017

The notochord, a conserved axial structure required for embryonic axis elongation and spine development, consists of giant vacuolated cells surrounded by an epithelial sheath [1-3]. During morphogenesis, vacuolated cells maintain their structural integrity despite being under constant mechanical stress [4]. We hypothesized that the high density of caveolae present in vacuolated cells [5, 6] could buffer mechanical tension. Caveolae are 50- to 80-nm membrane invaginations lined by cage-like polygonal structures [7, 8] formed by caveolin 1 (Cav1) or Cav3 and one of the cavin proteins [6, 9-11]. Recent in vitro work has shown that plasma membrane caveolae constitute a membrane reservoir that can buffer mechanical stresses such as stretching or osmotic swelling [12]. Moreover, mechanical integrity of vascular and muscle cells is partly dependent on caveolae [13-15]. However, the in vivo mechano-protective roles of caveolae have only begun to be explored. Using zebrafish mutants for cav1, cav3, and cavin1b, we show that caveolae are essential for notochord integrity. Upon loss of caveola function, vacuolated cells collapse at discrete positions under the mechanical strain of locomotion. Then, sheath cells invade the inner notochord and differentiate into vacuolated cells, thereby restoring notochord function and allowing normal spine development. Our data further indicate that nucleotides released by dying vacuolated cells promote sheath cell vacuolization and trans-differentiation. This work reveals a novel structural role for caveolae in vertebrates and provides unique insights into the mechanisms that safeguard notochord and spine development.

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Published In

Curr Biol

DOI

EISSN

1879-0445

Publication Date

July 10, 2017

Volume

27

Issue

13

Start / End Page

1982 / 1989.e3

Location

England

Related Subject Headings

  • Zebrafish
  • Stress, Mechanical
  • Notochord
  • Mutation
  • Developmental Biology
  • Cell Differentiation
  • Caveolae
  • Biomechanical Phenomena
  • Animals
  • 52 Psychology
 

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Garcia, J., Bagwell, J., Njaine, B., Norman, J., Levic, D. S., Wopat, S., … Bagnat, M. (2017). Sheath Cell Invasion and Trans-differentiation Repair Mechanical Damage Caused by Loss of Caveolae in the Zebrafish Notochord. Curr Biol, 27(13), 1982-1989.e3. https://doi.org/10.1016/j.cub.2017.05.035
Garcia, Jamie, Jennifer Bagwell, Brian Njaine, James Norman, Daniel S. Levic, Susan Wopat, Sara E. Miller, et al. “Sheath Cell Invasion and Trans-differentiation Repair Mechanical Damage Caused by Loss of Caveolae in the Zebrafish Notochord.Curr Biol 27, no. 13 (July 10, 2017): 1982-1989.e3. https://doi.org/10.1016/j.cub.2017.05.035.
Garcia J, Bagwell J, Njaine B, Norman J, Levic DS, Wopat S, et al. Sheath Cell Invasion and Trans-differentiation Repair Mechanical Damage Caused by Loss of Caveolae in the Zebrafish Notochord. Curr Biol. 2017 Jul 10;27(13):1982-1989.e3.
Garcia, Jamie, et al. “Sheath Cell Invasion and Trans-differentiation Repair Mechanical Damage Caused by Loss of Caveolae in the Zebrafish Notochord.Curr Biol, vol. 27, no. 13, July 2017, pp. 1982-1989.e3. Pubmed, doi:10.1016/j.cub.2017.05.035.
Garcia J, Bagwell J, Njaine B, Norman J, Levic DS, Wopat S, Miller SE, Liu X, Locasale JW, Stainier DYR, Bagnat M. Sheath Cell Invasion and Trans-differentiation Repair Mechanical Damage Caused by Loss of Caveolae in the Zebrafish Notochord. Curr Biol. 2017 Jul 10;27(13):1982-1989.e3.
Journal cover image

Published In

Curr Biol

DOI

EISSN

1879-0445

Publication Date

July 10, 2017

Volume

27

Issue

13

Start / End Page

1982 / 1989.e3

Location

England

Related Subject Headings

  • Zebrafish
  • Stress, Mechanical
  • Notochord
  • Mutation
  • Developmental Biology
  • Cell Differentiation
  • Caveolae
  • Biomechanical Phenomena
  • Animals
  • 52 Psychology