Atypical laminin spots and pull-generated microtubule-actin projections mediate Drosophila wing adhesion

• Published in: Cell reports (Cambridge) Vol. 36; no. 10; p. 109667
• Main Authors: Sun, Tianhui, Song, Yuzhao, Teng, Dequn, Chen, Yanan, Dai, Jianli, Ma, Mengqi, Zhang, Wei, Pastor-Pareja, José C.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 07.09.2021
• Subjects: Actins - metabolism; Animals; basement membrane; Basement Membrane - metabolism; Butterflies - metabolism; cytoskeleton; Drosophila - metabolism; Drosophila Proteins - metabolism; extracellular matrix; integrins; Laminin - metabolism; metamorphosis; Metamorphosis, Biological - physiology; Microtubule-Associated Proteins - metabolism; Microtubules - metabolism; Morphogenesis - physiology; serum response factor; wing morphogenesis; Wings, Animal - metabolism; wing morphogenesis; integrins; basement membrane; cytoskeleton; serum response factor; metamorphosis; extracellular matrix
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2021.109667

During Drosophila metamorphosis, dorsal and ventral wing surfaces adhere, separate, and reappose in a paradoxical process involving cell-matrix adhesion, matrix production and degradation, and long cellular projections. The identity of the intervening matrix, the logic behind the adhesion-reapposition cycle, and the role of projections are unknown. We find that laminin matrix spots devoid of other main basement membrane components mediate wing adhesion. Through live imaging, we show that long microtubule-actin cables grow from those adhesion spots because of hydrostatic pressure that pushes wing surfaces apart. Formation of cables resistant to pressure requires spectraplakin, Patronin, septins, and Sdb, a SAXO1/2 microtubule stabilizer expressed under control of wing intervein-selector SRF. Silkworms and dead-leaf butterflies display similar dorso-ventral projections and expression of Sdb in intervein SRF-like patterns. Our study supports the morphogenetic importance of atypical basement-membrane-related matrices and dissects matrix-cytoskeleton coordination in a process of great evolutionary significance. [Display omitted] •Laminin spots devoid of other basement-membrane components adhere Drosophila wings•Cytoskeleton cables grow symmetrically from laminin spots because of hydrostatic pressure•Cables contain spectraplakin, septins, and SRF-dependent microtubule stabilizer Sdb•Lepidopteran wings display similar cables and expression of Sdb in SRF-like patterns Sun et al. find that dorsoventral adhesion in the Drosophila wing during metamorphosis depends on laminin spots and associated cytoskeleton cables. Correct formation of cables requires, among other factors, wing-specific microtubule stabilizer Sdb.