The cellular dynamics and epithelial morphogenesis in Drosophila wing development
Date
2024-07-08
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Abstract
Epiteliaalsed rakud mängivad üliolulist rolli loomade organite ja 3D koestruktuuride arengus. Kudede morfogenees sõltub suuresti muutustest, mis toimuvad üksikute rakkude tasandil. Selle protsessi jälgimiseks oleme loonud süsteemi, mis võimaldab uurida rakkude detailset ehitust reaalajas. Käesolev töö keskendub raku struktuuri muutuste tuvastamisele ja kirjeldab, kuidas need muutused koordineerivad Drosophila melanogaster’i tiiva 3D-morfogeneesi kahes etapis: inflatsiooni ja teise apositsiooni ajal.
Uurimise käigus kirjeldasime üksikasjalikult erilist võrgustikku, mis tekib nukutiiva inflatsioonifaasis. See võrgustik (IPAN - Interplanar Amida Network), tekib selja- ja ventraalsete rakkude vahel ning on väga oluline tiiva koordineeritud kasvu jaoks. IPAN koosneb mikrotuubulitest ja mikrofilamentidest ning meie uuring viitab sellele, et IPAN-i kaudu toimub aktiivne transport, et koordineerida mitoosi kahe füüsiliselt eraldatud epiteelikihi vahel. Tiiva arengu hilisemates etappides IPAN võrgustik lagundatakse, millega kaasnevad rakukuju muutused ja mikrotuubulite organiseerimiskeskuste ümberlülitamine mittetsentrosomaalsetelt tsentrosomaalsetele organiseerimiskeskustele. Lisaks sellele leidsime, et α-spektriin mängib üliolulist rolli apikaalse lõdvestuse reguleerimisel aktomüosiinivõrkude kaudu, mis on samuti vajalik terve kolmemõõtmelise koe morfogeneesiks. Viimasena uurisime, kuidas raku kuju muutused ja luu morfogeneetilise valgu (Bone Morphogenetic Protein, BMP) signaaliülekande raja koostoime mõjutavad tagumise ristveeni morfogeneesi. Tulemused viitavad sellele, et apikaalne ahenemine täpsustab BMP signaale, diferentseerides rakud veenideks või veenide vahelisteks rakkudeks.
Kokkuvõtvalt käsitlevad doktoritöö artiklid küsimusi, kuidas rakukuju muutused koordineerivad 3D koe morfogeneesi, kuidas IPAN aitab sünkroniseerida selgmise ja kõhtmise tiivaepiteeli rakkude jagunemist läbi rakk-rakk kontaktide kaotamise, kuidas α-spektriin on seotud tiiva epiteeliraku apikaalse osa “lõdvestusega” ning kuidas raku apikaalse osa ahenemine ja raku kuju muutus vahendavad BMP arengusignaali konkurentsi, mis suunab tagumise tiivasoone morfogeneesi.
Epithelial cells are crucial in developing animal organs and 3D tissue structures. However, we still do not fully understand how changes in cellular structure affect tissue morphogenesis. To gain insight into this process, we need a system that allows us to observe real-time changes in cell shape. This thesis investigates how changes in cell shape coordinate 3D morphogenesis during two stages of Drosophila melanogaster wing development: inflation and second apposition. Our study discovered the intercellular connection Interplanar Amida Network (IPAN) during the inflation stage of pupal wing development. IPAN is a 3D meshwork structure that consists of dorsal and ventral cells with microtubule protrusions and microfilament extensions. It is critical for coordinated growth between two separated epitheliums. Changes in cell shape lead to a transition from non-centrosomal to centrosomal microtubule-organizing centers. IPAN provides a unique framework for 3D morphogenesis. In addition, the study also focuses on cell shape changes during microtubule protrusion disassembly. We found that α-Spectrin plays a crucial role in regulating apical relaxation via actomyosin networks, which is necessary for 3D tissue morphogenesis. Finally, the study investigated how cell shape alteration and Bone Morphogenetic Protein (BMP) signaling relate to posterior crossvein (PCV) morphogenesis in the Drosophila pupal wing. The results suggest that apical constriction refines BMP signals, differentiating cells into veins or intervein cells. In summary, the study discussed in the doctoral thesis shed light on the questions of how cell shape changes coordinate 3D tissue morphogenesis, how IPAN helps to synchronize the division of dorsal and ventral wing epithelial cells through the loss of cell-cell contacts, the relationship between α-spectrin and the "relaxation" of the apical part of the wing epithelial cell, and how apical cell constriction and cell shape change mediate competition for the BMP developmental signal that directs hindwing vein morphogenesis.
Epithelial cells are crucial in developing animal organs and 3D tissue structures. However, we still do not fully understand how changes in cellular structure affect tissue morphogenesis. To gain insight into this process, we need a system that allows us to observe real-time changes in cell shape. This thesis investigates how changes in cell shape coordinate 3D morphogenesis during two stages of Drosophila melanogaster wing development: inflation and second apposition. Our study discovered the intercellular connection Interplanar Amida Network (IPAN) during the inflation stage of pupal wing development. IPAN is a 3D meshwork structure that consists of dorsal and ventral cells with microtubule protrusions and microfilament extensions. It is critical for coordinated growth between two separated epitheliums. Changes in cell shape lead to a transition from non-centrosomal to centrosomal microtubule-organizing centers. IPAN provides a unique framework for 3D morphogenesis. In addition, the study also focuses on cell shape changes during microtubule protrusion disassembly. We found that α-Spectrin plays a crucial role in regulating apical relaxation via actomyosin networks, which is necessary for 3D tissue morphogenesis. Finally, the study investigated how cell shape alteration and Bone Morphogenetic Protein (BMP) signaling relate to posterior crossvein (PCV) morphogenesis in the Drosophila pupal wing. The results suggest that apical constriction refines BMP signals, differentiating cells into veins or intervein cells. In summary, the study discussed in the doctoral thesis shed light on the questions of how cell shape changes coordinate 3D tissue morphogenesis, how IPAN helps to synchronize the division of dorsal and ventral wing epithelial cells through the loss of cell-cell contacts, the relationship between α-spectrin and the "relaxation" of the apical part of the wing epithelial cell, and how apical cell constriction and cell shape change mediate competition for the BMP developmental signal that directs hindwing vein morphogenesis.
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