於果蠅胚胎背部閉鎖時期，上皮細胞中的微管配置會大幅度地由巢狀構造重新排列違反向平行的配置。除了在背部頂端細胞中促進偽足形成的功能之外(Jankovics and Brunner, 2006)，微管也被指出參與了含有黏著帶蛋白分子的胞內體於側邊上皮細胞之間的移動(Li et al., 2015)。然而，其間的運作機制仍幾乎為未知。透過活體影像與免疫組織染色，合成中的微管與乙醯化的微管皆被發現能經由類似孔隙的結構穿過在黏著帶的細胞膜。結合了位於黏著帶與間壁帶的訊號所形成的綠色螢光蛋白區帶，揭露了於側邊上皮細胞的細胞膜上有著一新型黏著帶附著孔隙的存在，且此孔隙能容許細胞間傳遞胞內體。利用以可激發綠色螢光蛋白進行的細胞質連通分析與細胞系譜標定實驗，發現了側邊上皮細胞可透過與環橋及系譜無關的方式連通其它相鄰細胞之細胞質。以光遺傳二聚法連接微管驅動蛋白與位於黏著帶之免疫球蛋白黏著分子的實驗結果中，也支持了微管於細胞間胞內體運輸一事扮演著軌道的角色。穿透式電子顯微鏡影像結果，暗示了於背部閉鎖期間，與微管的架皆可能導致黏著帶細胞膜的不穩定；此外也得到了內有貼覆著許多胞內體的微管、可能為黏著帶附著孔隙之結構。與在哺乳類細胞得到之成果一致，支撐與重新排列微管配置需要鈣黏著分子複合體與許多微管相連蛋白。這些蛋白也因而被認為是「捕捉者」，用來抓住並穩定在細胞邊緣近黏著帶的微管。
根據結果，我們提出了一個假說模型：於閉鎖時期，微管被重新配置到黏著帶一層。此一與黏著帶之相互作用造成了局部脂質的不穩定，進而有助於初生孔隙的形成。經過後續的擴張與穩固之後，穩定的乙醯化微管可成為新型成為管之生長軌道，有意於成長與穿越細胞膜上的孔隙、不被黏著帶複合體抓住。這同時也只能相鄰細胞能夠連通細胞質，並容許細胞間胞內體穿越其中。

Microtubule (MT) arrays are dramatically reorganized from nest‐like structures into anti‐parallel ones during dorsal closure (DC) in Drosophila embryos. In addition to its function in dorsal most epithelial (DME) cells for promoting fillopodia formation (Jankovics and Brunner, 2006), MTs are reported to be involved in the intercellular transport (IT) of adherens junction (AJ) protein-containing intercellular endosomes (IEs) in those lateral epithelial (LE) cells (Li et al., 2015); however, the underlying mechanism is poorly understood. By live imaging and immuno-histochemical (IHC) staining, both the synthesizing MTs (EB1) and acetylated MTs (Ac-MTs) were found to be able to pierce through "pore-like" structures on plasma membrane (PM) at AJs. The "GFP belt" resulted from signal combination from AJ and SJ markers revealed the existence of novel AJ-associated pores on the PM of LE cells, which allowed the IT. Analysis with photo-activatable GFP (C3PA-GFP) and cell lineages labeling experiments suggested cytoplasmic connections among neighboring LE cells that were independent of ring canals or cell lineages. Optogenetic dimerization between the Kinesin and Echinoid (Ed) suggested the role of MTs as tracks in the transport of IEs. TEM images implied the instability of AJ membrane during DC upon conjugating with MTs and also the possible structure for AJ-associated pores with vesicle-decorated MTs in the lumen. Consistent with what have been suggested in mammalian cells, cadherin complexes and several MT‐associated proteins were also required for the embracement and rearrangement of MT arrays, and therefore were concerned as the “capturers” for MTs by stabilizing them at the cell cortex near AJs.
According to the results, we suggested a hypothetic model for the AJ-associated pores and the MT-dependent IT : MT arrays are rearranged and relocated to the AJs during DC. The association among MTs and AJs leads to local lipid instability, which might benefit the formation of nascent AJ-associated pores. After further expansion and stabilization, acetylated MT arrays may act as the tracks for the synthesizing MTs to grow along and across the "pores" without being captured, and thereby allow the IT of IEs and the cytoplasmic connections.

Introduction 1
Cell-cell communication 1
Dorsal closure during late embryogenesis of Drosophila Melanogaster 4
Microtubules during embryogenesis of Drosophila Melanogaster 6
Intercellular transport through adherens junctions between epithelial cells 7
Materials and Methods 8
Cloning of fusion protein 8
Fly strains 10
Sample preparation 12
Immunohistochemical staining (IHC staining) 12
Live imaging 14
Transmission electron microscope -- heptane-independent fixation 15
Optogenetic dimerization 17
By using LSM780 17
By using LLSM 17
Limited-cytoplasmic connection 18
Microinjection with dyes 19
Live imaging for PM or MTs 19
IHC staining for PM 19
Results 20
- The 1st part - The appearance of the epithelial cells and the AJ-associating MTs during DC 22
Comparison of labeling ability of different PM markers at AJs 22
Lipid dyes 23
PM-associating proteins 25
Rearrangement of cell shape and MT arrays of epithelial cells during DC 27
Bi-directional organization of MT arrays and movement of AJ protein-containing vesicles with preferences for the orientation along D-V axis during DC 29
- The 2nd part - A novel PM-piercing behavior of MTs at AJs 31
Acetylated MT bundles pierce through the PM at AJs during DC 33
Uneven association with MT bundles leads to local disturbance of AJ membranes during DC 35
MT bundles pierce through the PM at AJs without lipids covered surround 36
Novel AJ-associated pores: MT-based structures other than somatic ring canals that bridge neighboring cells 38
Hypothetic model for the AJ-associated pores 38
Somatic ring canal-independent AJ-associated pores 39
Possible structures of AJ-associated pores revealed by TEM images 41
MTs grow and pierce across the PM at AJs 42
- The 3rd part - Demonstration for the role of MT-dependent movement in IT 44
Demonstration of MT-based mechanism by the optogenetic dimerization system 44
Control experiments for efficacy of the optogenetic dimerization system (LSM780) 46
Demonstration with optogenetic dimerization system (LSM780) 48
Control experiments for the requirement of laser intensity (LLSM) 49
Demonstration with optogenetic dimerization system (LLSM) 50
- The 4th part - IEs moved across the novel AJ-associated pore on PM at AJs 51
The MT-based mechanism underling IT through AJ-associated pores on PM at AJs 51
Manifesting of AJ-associated pores by "GFP belts" 52
IEs moved across the AJ-associated pores on PM at AJs 53
- The 5th part - Limited cytoplasmic connections among LE cells 54
The independency on somatic ring canal and the limited configuration of cytoplasmic connections among LEs 54
The independency on cell lineages and the limited configuration of cytoplasmic connections among LEs 58
- The 6th part - The hypothetic model for the AJ-associated pores and the MT-based mechanism underlying IT 60
Hypothetic model 60
IT of signaling components at AJs 61
Discussions 62
- The 1st part - The model for AJ-associated pores and the MT-dependent IT 64
Evidences from super resolution microscopy, SR-SIM and LLSM 64
Evidences from TEM 65
- The 2nd part - The possible physiological functions of the AJ-associated pores 67
Exchange signaling components 67
Replenishment of PM 69
- The 3rd part - The possible mechanisms underlying the formation of AJ-associated pores 70
Proteins involved in MT orientation and positioning in LE cells during DC 70
Hypothesis for the formation of AJ-associated pores and the traversing MTs 71
- The 4th part - Similar sub-cellular structures or mechanisms found in other model organisms or tissues 73
Anti-paralleled MT arrays and PCP establishment 73
Fusion of plasma membrane 76
Figures 77
Figure 1. The alteration in cell shape and the orientation of MT arrays of Drosophila epithelial cells during DC. (LSM510) 77
Figure 2. Acetylated MTs pierced through the PM at AJs. (SR-SIM) (LSM780) 79
Figure 3. MTs pierced through the PM at AJs without lipids covered surround. (LSM780) 81
Figure 4. Hypothetic models for the novel AJ-associated pores: the size-dependent structures as closed circles or open circles. 83
Figure 5. TEM serial images of the MT-based pore-liked structures in various sizes. (TEM) 84
Figure 6. MTs pierced through the PM at AJs as continuous filaments. (LLSM) 86
Figure 7. Demonstration of MT-based mechanism underlying the intercellular movements. (LSM780) (LLSM) 88
Figure 8. AJ protein-containing vesicles move through a pore-liked structure on PM. (LSM780) (LLSM) 90
Figure 9. Limited ring canal-independent cytoplasmic connections among epithelial cells. (LSM510-META-NLO) 92
Figure 10. Cells from different cell lineages could exchange vesicles with their neighboring cells. (LSM780) 94
Figure 11. Model of the MT-based intercellular transport through the pore on PM. 96
Figure 12. Physiological function of the MT-based intercellular transport through the pore on PM. (LSM780) 97
Supplementary figures 98
Figure S1. Comparison of PM-labeling abilities among DEcad and other different markers at AJs. (LSM780) 98
Figure S2. Comparison of PM-labeling abilities among DEcad and lipid dyes at AJs. (LSM780) 100
Figure S3. Co-localization between DEcad and FM4-64 at AJs. (LSM780) 101
Figure S4. MT arrays were organized bi-directionally in a preference to aligned along the D-V axis. (LSM780) 102
Figure S5. Strategy for TEM sampling 104
Figure S6. Uneven association with MT bundles led to local disturbance of AJ membranes during DC. (TEM) 105
Figure S7. MT-based protrusions at the AJs with membrane proteins covered surround. (LSM780) (SR-SIM) 107
Figure S8. Somatic ring canals in epithelial cells during DC. (LSM780) (TEM) 108
Figure S9. Intercellular movements along different MT bundles. (LSM780) 109
Figure S10. Induction of optogenetical dimerization with blue light. (LSM780) 111
Figure S11. Induction of optogenetical dimerization with blue light. (LLSM) 113
Figure S12. LE cells were post-mitotic cells that stay in G1 phase after the post-blastoderm mitosis. (LSM780) 115
Figure S13. DEcad is required for the organization of MT arrays along the D-V axis. (LSM780) 116
Figure S14. RNAi screening for proteins involved in MT positioning at AJs. (LSM780) 117
Figure S15. Hypothetic model for the novel MT behavior during DC. 118
Videos and 3D structures 119
Videos 119
Video 6B. MTs pierced through the PM at AJs as continuous filaments. (LLSM) 119
Video 6C. MTs pierced through the PM at AJs as continuous filaments. -- partial enlargement (LLSM) 119
Video 7B. Demonstration of MT-based mechanism underlying the intercellular movements. (LSM780) 119
Video 7C. Demonstration of MT-based mechanism underlying the intercellular movements. (LLSM) 119
Video 8B. AJ protein-containing vesicles move through a pore-liked structure on PM. (LLSM) 119
Video 9A. Cytoplasmic connections between LE cells without any ring canal on the interface. (LSM510-META-NLO) 120
Video 12A. Tkv-containing vesicles undergo cell-to-cell transport. (LSM780) 120
Video S4A. Orientation of MT arrays in LE cells of a stage 12embryo. (LSM780) 120
Video S4A'. Orientation of MT arrays in LE cells of a stage 14 embryo. (LSM780) 120
Video S4C. Bi-directional orientation of MT arrays in LE cells of a stage 14 embryo. (LSM780) 120
Video S4D. Bi-directional movements of Ed-containing vesicles along a MT bundle in LE cells of a stage 14 embryo. (LSM780) 120
Video S9. Intercellular movements along different MT bundles. (LSM780) 121
Video S10A. Control group for the efficacy of the optogenetical dimerization system. (LSM780) 121
Video S10D. Control group for the efficacy of the optogenetical dimerization system. (LSM780) 121
Video S11. Induction of optogenetical dimerization with blue light. (LLSM) 121
3D structures 122
3D Structure 2A. Acetylated MTs pierced through the PM at AJs -- The open circle structure (SR-SIM) 122
3D Structure 2B. Acetylated MTs pierced through the PM at AJs -- The closed circle structure (SR-SIM) 122
3D Structure 3A. MTs pierced through the PM at AJs without lipids covered surround -- live imaging (LSM780) 122
3D Structure 3A''. MTs pierced through the PM at AJs without lipids covered surround -- live imaging -- partial enlargement (LSM780) 122
3D Structure 3B. MTs pierced through the PM at AJs without lipids covered surround -- IHC staining (LSM780) 122
3D structure 8A. Pore-liked structures on the PM at AJs. -- live imaging (LSM780) 122
3D structure 8B. AJ protein-containing vesicles move through a pore-liked structure on PM. -- live imaging (LLSM) 123

3D Structure S7B. MT-based protrusions at the AJs with membrane proteins covered surround. (SR-SIM) 123
3D Structure S11. Formation of Ed-Khc doublets after induction of optogenetic dimerization. -- 70% 488 nm laser -- live imaging (LLSM) 123
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