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研究生： 楊雯婷
Yang, Wen-Ting
論文名稱： 研究位於果蠅胚胎背部閉鎖時期之上皮細胞黏著帶一新型孔隙之經由微管進行細胞間胞內體運輸之機制與區域限定細胞質連通現象
A Microtubule-based Mechanism of Intercellular Transport of Endosomes and Limited Cytoplasmic connections through the Novel Adherens Junctions-associated Pores in Epithelial cells of Drosophila embryos during dorsal closure
指導教授： 徐瑞洲
Hsu, Jui-Chou
口試委員: 桑自剛
Sang, Tzu-Kang
孫以瀚
Sun, Y. Henry
簡正鼎
Chien, Cheng-Ting
白麗美
Pai, Li-Mei
學位類別： 博士
Doctor
系所名稱： 生命科學暨醫學院 - 分子醫學研究所
Institute of Molecular Medicine
論文出版年： 2018
畢業學年度： 107
語文別： 英文
論文頁數： 130
中文關鍵詞： 細胞間溝通 、細胞間胞內體 、黏著帶附著孔隙 、背部閉鎖 、微管 、黏著帶 、鈣黏著分子 、免疫球蛋白黏著分子
外文關鍵詞： Intercellular communication, Intercellular endosomes, Adherens junctions-associated pores, Dorsal closure, Microtubules, Adherens junctions, DE-cadherin, Echinoid
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    • 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 References (listed in the order of alphabets) 124

    1. Balabanian, L., Berger, C. L. and Hendrick, A. G. (2017) Acetylated Microtubules Are Preferentially Bundled Leading to Enhanced Kinesin-1 Motility. Biophysical Journal, Vol.113, 1551-1560
    2. Bate, M. (1990) The embryonic development of larval muscles in Drosophila. Development, Vol.110, 791-804
    3. Bauer,R., Löer, B., Ostrowski, K., Martini, J., Weimbs, A., Lechner, H. and Hoch, M. (2005) Intercellular Communication: the Drosophila Innexin Multiprotein Family of Gap Junction Proteins. Chemistry and Biology, Vol.12, 515-526
    4. Betschinger, J., Mechtler, K. and Knoblich, J. A. (2003) The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature, Vol.422, 326-330
    5. Bilder, D., Li, M. and Perrimon, N. (2000) Cooperative Regulation of Cell Polarity and Growth by Drosophila Tumor Suppressors. Science, Vol.289, 113-116
    6. Blomberg, N. and Nilges, M. (1997) Functional diversity of PH domains: an exhaustive modelling study. Folding & Design, Vol.2, 343-355
    7. Bosch, J.A., Tran, N.H. and Hariharan, I.K. (2015) CoinFLP: a system for efficient mosaic screening and for visualizing clonal boundaries in Drosophila. Development, Vol. 142, 597-606
    8. Brown, E. H. and King, R. C. (1964) Studies on the events resulting in the formation of an egg chamber in Drosophila melanogaster. Growth, Vol.28, 41-81
    9. Burgos, M. H. and Fawcett, D. W. (1955) Studies on the fine structure of the mammalian testis. The Journal of Biophysical and Biochemical Cytology, Vol.1, 287-300
    10. Buss, J. E., Kamps, M. P., Gould, K. and Sefton, B. M. (1986) The absence of myristic acid decreases membrane binding of p60src but does not affect tyrosine protein kinase activity. Journal of Virology, Vol.58, 468-474
    11. Buszczak, M., Paterno, S., Lighthouse, D., Bachman, J., Planck, J., Owen, S., Skora, A.D., Nystul, T.G., Ohlstein, B., Allen, A., Wilhelm, J.E., Murphy, T.D., Levis, R.W., Matunis, E., Srivali, N., Hoskins, R.A. and Spradling, A.C. (2007) The Carnegie Protein Trap Library: A Versatile Tool for Drosophila Developmental Studies. Genetics, Vol.175, 1505-1531
    12. Chen, B.C., Legant,W.R., Wang, K., Shao, L., Milkie, D.E., Davidson, M.W., Janetopoulos, C., Wu, X.S., Hammer III, J.A., Liu,Z., English, B.P., Mimori-Kiyosue, Y., Romero, D.P., Ritter, A.T., Lippincott-Schwartz, J., Fritz-Laylin, L., Mullins, R.D., Mitchell, D.M., Bembenek, J.N., Reymann, A.C., Böhme, R., Grill, S.W., Wang, J.T., Seydoux, G., Tulu, U.S., Kiehart, D.P. and Betzig, E. (2014) Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution. Science, Vol.346, 1257998
    13. Conde, C. and Cáceres, A. (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nature Reviews Neuroscience, Vol.10, 319-332
    14. Coquelle, F.M., Vitre, B. and Arnal, I. (2009) Structural basis of EB1 effects on microtubule dynamics. Biochemical Society Transactions, Vol.37, 997-1001
    15. Edgar, B. A. and O'Farrell, P. H.(1990) The Three Postblastoderm Cell Cycles of Drosophila Embryogenesis Are Regulated in G2 by string. Cell, Vol.62, 469-460
    16. Fededa, J.P. and Gerlich, D.W. (2012) Molecular control of animal cell cytokinesis. Nature Cell Biology, Vol.14, 440-447
    17. Gerhart, J. (1999) 1998 Warkany Lecture: Signaling Pathways in Development.Teratology, Vol.60, 226-239
    18. Gibralter, D. and Turner, D. C. (1985) Dual Adhesion Systems of Chick Myoblasts. Developmental Biology, Vol.112, 292-307
    19. Giorgi, F. (1978). Intercellular bridges in ovarian follicle cells of Drosophila melanogaster. Cell Tissue Research, Vol.186, 413-422
    20. Gorfinkiel, N. and Arias, A.M. (2007) Requirements for adherens junction components in the interaction between epithelial tissues during dorsal closure in Drosophila. Journal of Cell Science, Vol.120, 3289-3298
    21. Greenbaum, M.P., Iwamori, T., Buchold, G.M. and Matzuk, M.M. (2011) Germ Cell Intercellular Bridges. Cold Spring Harbor Perspective Biology, Vol.3, a005850
    22. Groth, A.C., M. Fish, R. Nusse, and M.P. Calos. (2004) Construction of Transgenic Drosophila by Using the Site-Specific Integrase From Phage φC31. Genetics, Vol.166, 1775-1782.
    23. Guillot, C. and Lecuit, T. (2013) Adhesion Disengagement Uncouples Intrinsic and Extrinsic Forces to Drive Cytokinesis in Epithelial Tissues. Developmental Cell, Vol.24, 227-241
    24. Haglund, K., Nezis, I.P. and Stenmark, H. (2011) Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development. Communicative and Integrative Biology, Vol.4, 1-9
    25. Hancock, J. F., Cadwallader, K., Paterson, H. and Marshall, C. J. (1991) A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins.The EMBO Journal, Vol.10, 4033-4039
    26. Harumoto, T., Ito, M., Shimada, Y., Kobayashi, T.J., Ueda, H.R., Lu, B. and Uemura, T. (2010) Atypical Cadherins Dachsous and Fat Control Dynamics of Noncentrosomal Microtubules in Planar Cell Polarity. Developmental Cell, Vol.19, 389-401
    27. Hennig, K. M., Colombani, J. and Neufeld, T. P. (2006) TOR coordinates bulk and targeted endocytosis in the Drosophila melanogaster fat body to regulate cell growth. The Journal of Cell Biology, Vol.173, 963-974
    28. Herszterg, S., Leibfried, A., Bosveld, F., Martin, C. and Bellaiche, Y. (2013) Interplay between the Dividing Cell and Its Neighbors Regulates Adherens Junction Formation during Cytokinesis in Epithelial Tissue. Developmental Cell, Vol.24, 256-270
    29. Hervé, J. and Derangeon, M. (2013) Gap-junction-mediated cell-to-cell communication. Cell Tissue Reviews, Vol.352, 21-31
    30. Hsiung, F., Ramirez-Weber F. A., Iwaki D. D. and Kornberg, T. B. (2005) Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic. Nature, Vol. 437, 560-563
    31. Inaba, M., Buszczak, M. and Yamashita Y. M. (2015) Nanotubes mediate niche-stem-cell signalling in the Drosophila testis. Nature, Vol.523,329-332
    32. Indra, I., Hong, S., Troyanovsky, R., Kormos, B. and Troyanovsky, S. (2013) The Adherens Junction: A Mosaic of Cadherin and Nectin Clusters Bundled by Actin Filaments. Journal of Investigative Dermatology, Vol.133, 2546-2554
    33. Jacinto, A., Woolner, S. and Martin, P. (2002) Dynamic Analysis of Dorsal Closure in Drosophila: From Genetics to Cell Biology. Developmental Cell, Vol.3, 9-19
    34. Jankovics, F. and Brunner, D. (2006) Transiently Reorganized Microtubules Are Essential for Zippering during Dorsal Closure in Drosophila melanogaster. Developmental Cell, Vol.11, 375-385
    35. Kakihara, K., Shinmyozu, K., Kato, K., Wada, H. and Hayashi, S. (2008) Conversion of plasma membrane topology during epithelial tube connection requires Arf-like 3 small GTPase in Drosophila. Mechanisms of Development, Vol.125, 325-336
    36. Kaltschmidt, J.A., Lawrence, N., Morel, V., Balayo, T., Fernández, B.G., Pelissier, A., Jacinto, A. and Arias A.M. (2002) Planar polarity and actin dynamics in the epidermis of Drosophila. Nature Cell Biology, Vol.4, 937-944
    37. Karpova, N., Bobinnec, Y., Fouix, S., Huitorel, P. and Debec, A. (2006) Jupiter, a New Drosophila Protein Associated With Microtubules. Cell Motility and the Cytoskeleton, Vol.63, 301-312
    38. Kelso, R.J., Buszczak, M., Quiñones, A.T., Castiblanco, C., Mazzalupo, S. and Cooley, L. (2004) Flytrap, a database documenting a GFP protein‐trap insertion screen in Drosophila melanogaster. Nucleic Acids Research, Vol.32, D418-D420
    39. Kondo, T. and Hayashi, S. (2013) Mitotic cell rounding accelerates epithelial invagination. Nature, Vol. 494, 125-129
    40. Kornberg, T.B. and Roy, S. (2014) Cytonemes as specialized signaling filopodia. Development, Vol.141, 729-736
    41. Lee, T. and Luo, L. (1999) Mosaic Analysis with a Repressible Cell Marker for Studies of Gene Function in Neuronal Morphogenesis. Neuron, Vol.22, 451-461
    42. Li, Y.C., Yang, W.T., Cheng, L.C., Lin, C.M., Ho, Y.H., Lin, P.Y., Chen, B.C., Rickoll, W.L. and Hsu, J.C. (2015) Novel transport function of adherens junction revealed by live imaging in Drosophila. Biochemical and Biophysical Research Communications, Vol. 463, 686-692
    43. Mahowald, A. P. and Strassheim, J. M. (1970). Intercellular migration of centrioles in the germarium of Drosophila melanogaster: An electron microscopic study. Journal of Cell Biology, Vol.45, 306-320
    44. Marcinkevicius, E. and Zallen, J.A. (2013) Regulation of cytoskeletal organization and junctional remodeling by the atypical cadherin Fat. Development, Vol.140, 433-443
    45. Margaritis L. H., Kafatos, F. C. and Petri, W. H. (1980) The eggshell of Drosophila melanogaster. I. Fine structure of the layers and regions of the wild-type eggshell. The Journal of Cell Science, Vol. 43, 1-35
    46. Matsumoto, E., Hirosawa, K., Takagawa, K. and Hotta, Y. (1988) Structure of retinular cells in a Drosophila melanogaster visual mutant, rdgA, at early stages of degeneration. Cell and Tissue Research, Vol.252, 293-300
    47. McDonald, K.L., Sharp, D.J. and Rickoll, W. (2012) Transmission Electron Microscopy of Thin Sections of Drosophila: Preparation of Embryos Using n-Heptane and Glutaraldehyde. Cold Spring Harbor Protocol, CSHL Press, Cold Spring Harbor, NY, USA
    48. McLean, P. F. and Cooley, L. (2013) Protein Equilibration Through Somatic Ring Canals in Drosophila. Science, Vol.340, 1445-1447
    49. Minestrini, G., Mathe, E. and Glover, D. M. (2002) Domains of the Pavarotti kinesin-like protein that direct its subcellular distribution: effects of mislocalisation on the tubulin and actin cytoskeleton during Drosophila oogenesis. Journal of Cell Science, Vol.115, 725-736
    50. Minestrini, G., Harley, A.S. and Glover, D.M. (2003) Localization of Pavarotti-KLP in Living Drosophila Embryos Suggests Roles in Reorganizing the Cortical Cytoskeleton during the Mitotic Cycle. Molecular Biology of the Cell, Vol.14, 4028-4038
    51. Morais-de-Sa´, E. and Sunkel, C. (2013) Adherens junctions determine the apical position of the midbody during follicular epithelial cell division. EMBO reports, Vol.14, 696-703
    52. Morrison, E. E., Moncur, P. M. and Askham J. M. (2002) EB1 identifies sites of microtubule polymerisation during neurite development. Molecular Brain Research, Vol.98, 145-152
    53. Nakazawa, N., Taniguchi, K., Okumura, T., Maeda, R. and Matsuno, K. (2012) A novel Cre/loxP system for mosaic gene expression in the Drosophila embryo. Developmental Dynamics, Vol. 241, 965-974
    54. Podbilewicz, B. and White, J. G. (1994) Cell Fusions in the Drosophila Epithelia of C. elegans. Developmental Biology, Vol.161, 408-424
    55. Poodry, C. A. and Schneiderman, H. A. (1970) The ultrastructure of the developing leg of Drosophila melanogaster. Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen, Vol.166, 1-44
    56. Reed, N. A., Cai, D., Blasius, T. L., Jih, G. T., Meyhofer, E., Gaertig, J. and Verhey, K. J. (2006) Microtubule Acetylation Promotes Kinesin-1 Binding and Transport. Current Biology, Vol.16, 2166-2172
    57. Revelo, N. H., Kamin, D., Truckenbrodt, S., Wong, A. B., Reuter-Jessen, K., Reisinger, E., Moser, T. and Rizzoli, S. O. (2014) A new probe for super-resolution imaging of membranes elucidates trafficking pathways. The Journal of Cell Biology, Vol.205, 591–606
    58. Robinson, D. N., Cant, K. and Cooley, L. (1994) Morphogenesis of Drosophila ovarian ring canals. Development, Vol.120, 2015-2025
    59. Rabinowitz, M. (1941) Studies on the cytology and early embryology of the egg of Drosophila melanogaster. Journal of Morphology, Vol.69, 1-49
    60. Rogers, S.L., Rogers, G.C., David J. Sharp, D.J. and Vale, R.D. (2002) Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. The Journal of Cell Biology, Vol.158, 873-884
    61. Roy, S., Huang, H., Liu, S., Kornberg, T.B. (2014) Cytoneme-Mediated Contact-Dependent Transport of the Drosophila Decapentaplegic Signaling Protein. Science, Vol.343, 1244624
    62. Rustom, A., Saffrich, R. and Markovic, I. (2004) Nanotubular Highways for Intercellular Organelle Transport. Science, Vol.303, 1007-1010
    63. Ruta, V., Datta, S. R., Vasconcelos, M. L., Freeland, J., Looger, L. L. and Axel, R. (2010) A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature, Vol.468, 686-689
    64. Schermelleh, L., Heintzmann, R. and Leonhardt, H. (2010) A guide to super-resolution fluorescence microscopy. J. Cell Biol., Vol.190, 165-175
    65. Schuyler, S.C. and Pellman, D. (2001) Microtubule “Plus-End-Tracking Proteins”: The End Is Just the Beginning. Cell, Vol.105, 421-424
    66. Shahbazi, M.N. and Perez-Moreno, M. (2014) Microtubules CLASP to Adherens Junctions in epidermal progenitor cells. Bio Architecture, Vol.4, 25-30
    67. Shimada, Y., Yonemura, S.,Ohkura, H., Strutt, D. and Uemura, T. (2006) Polarized Transport of Frizzled along the Planar Microtubule Arrays in Drosophila Wing Epithelium. Developmental Cell, Vol.10, 209-222
    68. Strickland, D., Lin, Y., Wagner, E., Hope, C. M., Zayner, J., Antoniou, C., Sosnick, T. R., Weiss, E. L. and Glotzer, M. (2012) TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nature Methods, Vol.9, 379-384
    69. Su, L. K., Burrell, M., Hill, D. E., Gyuris, J., Brent, R., Wiltshire, R., Trent, J., Vogelstein, B. and Kinzler, K.W. (1995) APC Binds to the Novel Protein EB1. Cancer Research, Vol.55, 2972-2977
    70. van Bergeijk, P., Adrian, M., Hoogenraad, C.C. and Kapitein, L.C. (2015) Optogenetic control of organelle transport and positioning. Nature, Vol. 518, 111-114
    71. Vida, T. A. and Erm S. D. (1995) A New Vital Stain for Visualizing Vacuolar Membrane Dynamics and Endocytosis in Yeast. The Journal of Cell Biology, Vol.128, 779-792
    72. Wei, S.Y., Escudero, L.M., Yu, F., Chang, L.H., Chen, L.Y., Ho, Y.H., Lin, C.M., Chou, C.S., Chia, W., Modolell, D. and Hsu, J.C. (2005) Echinoid Is a Component of Adherens Junctions That Cooperates with DE-Cadherin to Mediate Cell Adhesion. Developmental Cell, Vol.8, 493-504
    73. Wirtz-Peitz, F., Nishimura, T. and Knoblich, J.A. (2008) Linking Cell Cycle to Asymmetric Division: Aurora-A Phosphorylates the Par Complex to Regulate Numb Localization. Cell, Vol. 135, 161–173
    74. Wolf, N., Regan, C.L. and Fuller, M.T. (1988) Temporal and spatial pattern of differences in microtubule behavior during Drosophila embryogenesis revealed by distribution of a tubulin isoform. Development, Vol.102, 311-324
    75. Xue, F. and Cooley, L. (1993) kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell, Vol.72, 681-693
    76. Yamanaka, N., Rewitz, K. F. and and O’Connor, M. B. (2012) Ecdysone Control of Developmental Transitions: Lessons from Drosophila Research. The Annual Review of Entomology, Vol.58, 497–516
    77. Ye, B., Zhang, Y., Song, W., Younger, S. H., Jan, L. Y. and Jan, Y. N. (2007) Growing Dendrites and Axons Differ in Their Reliance on the Secretory Pathway. Cell, Vol.130, 717-729
    78. Yue, L. and Spradling, A. (1992) hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Development, Vol.6, 2443-2454
    79. Zhao, T., Graham, O. S., Raposo, A. and St Johnston, D. (2012) Growing Microtubules Push the Oocyte Nucleus to Polarize the Drosophila Dorsal-Ventral Axis. Science, Vol. 336, 999-1003
    80. Zielke, N., Korzelius, J., van Straaten, M., Bender, K., Schuhknecht, G. F. P., Dutta, D., Xiang, J. and Edgar, B. A. (2014) Fly-FUCCI: A Versatile Tool for Studying Cell Proliferation in Complex Tissues. Cell Reports, Vol.7, 588-598
    81. Zuber, M. X., Strittmatter, S. M. and Fishman M. C. (1989) A membrane-targeting signal in the amino terminus of the neuronal protein GAP-43. Nature, Vol.341, 345-348

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