Drosophila embryo syncytial blastoderm cellular architecture and morphogen gradient dynamics: Is there a correlation?

Frontiers in Biology - Tập 7 - Trang 73-82 - 2012
Aparna Sherlekar1, Richa Rikhy1
1Indian Institute of Science, Education and Research, Biology, Pune, India

Tóm tắt

During embryo development in many metazoan animals, the first differentiated cell type to form is an epithelial cell. This epithelial layer is modified by developmental cues of body axes formation to give rise to various tissues. The cells that arise are mesenchymal in nature and are a source of other tissue types. This epithelial to mesenchymal transition is used for tissue type formation and also seen in diseases such as cancer. Here we discuss recent findings on the cellular architecture formation in the Drosophila embryo and how it affects the developmental program of body axes formation. In particular these studies suggest the presence of compartments around each nucleus in a common syncytium. Despite the absence of plasma membrane boundaries, each nucleus not only has its own endoplasmic reticulum and Golgi complex but also its own compartmentalized plasma membrane domain above it. This architecture is potentially essential for morphogen gradient restriction in the syncytial Drosophila embryo. We discuss various properties of the dorso-ventral and the antero-posterior morphogen gradients in the Drosophila syncytium, which are likely to depend on the syncytial architecture of the embryo.

Tài liệu tham khảo

Acloque H, Adams M S, Fishwick K, Bronner-fraser M, Nieto M A (2009). Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest, 119(6): 1438–1449 Afshar K, Stuart B, Wasserman S A (2000). Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development, 127: 1887–1897 Arnot C J, Gay N J, Gangloff M (2010). Molecular mechanism that induces activation of Spätzle, the ligand for the Drosophila Toll receptor. J Biol Chem, 285(25): 19502–19509 Baker J, Theurkauf W E, Schubiger G (1993). Dynamic changes in microtubule configuration correlate with nuclear migration in the preblastoderm Drosophila embryo. J Cell Biol, 122(1): 113–121 Berleth T, Burri M, Thoma G, Bopp D, Richstein S, Frigerio G, Noll M, Nüsslein-Volhard C (1988). The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J, 7: 1749–1756 Bownes M (1975). A photographic study of development in the living embryo of Drosophila melanogaster. J Embryol Exp Morphol, 33: 789–801 Coppey M, Berezhkovskii A M, Kim Y, Boettiger A N, Shvartsman S Y (2007). Modeling the bicoid gradient: diffusion and reversible nuclear trapping of a stable protein. Dev Biol, 312(2): 623–630 Coppey M, Boettiger A N, Berezhkovskii A M, Shvartsman S Y (2008). Nuclear trapping shapes the terminal gradient in the Drosophila embryo. Curr Biol, 18(12): 915–919 de Las Heras J M, Martinho R G, Lehmann R, Casanova J (2009). A functional antagonism between the pgc germline repressor and torso in the development of somatic cells. EMBO Rep, 10(9): 1059–1065 DeLotto R, DeLotto Y, Steward R, Lippincott-Schwartz J (2007). Nucleocytoplasmic shuttling mediates the dynamic maintenance of nuclear Dorsal levels during Drosophila embryogenesis. Development, 134(23): 4233–4241 Deng J, Wang W, Lu L J, Ma J (2010). A two-dimensional simulation model of the Bicoid Gradient in Drosophila. system, PLoS ONE, 5(4): e10275 Dilão R, Muraro D (2010). mRNA diffusion explains protein gradients in Drosophila early development. J Theor Biol, 264(3): 847–853 Dornan S, Jackson A P, Gay N J (1997). Alpha-adaptin, a marker for endocytosis, is expressed in complex patterns during Drosophila development. Mol Biol Cell, 8: 1391–1403 Driever W, Nüsslein-Volhard C (1988a). A gradient of bicoid protein in Drosophila embryos. Cell, 54(1): 83–93 Driever W, Nüsslein-Volhard C (1988b). The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell, 54(1): 95–104 Field C M (2005). Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development, 132(12): 2849–2860 Field C M, Alberts B M (1995). Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol, 131(1): 165–178 Foe V E, Alberts B M (1983). Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci, 61: 31–70 Freeman M, Nüsslein-Volhard C, Glover D M (1986). The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila. Cell, 46(3): 457–468 Frescas D, Mavrakis M, Lorenz H, Delotto R, Lippincott-Schwartz J (2006). The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei. J Cell Biol, 173(2): 219–230 Gangloff M, Murali A, Xiong J, Arnot C J, Weber A N, Sandercock A M, Robinson C V, Sarisky R, Holzenburg A, Kao C, Gay N J (2008). Structural insight into the mechanism of activation of the Toll receptor by the dimeric ligand Spätzle. J Biol Chem, 283(21): 14629–14635 Gillespie S K, Wasserman S A (1994). Dorsal, a Drosophila Rel-like protein, is phosphorylated upon activation of the transmembrane protein Toll. Mol Cell Biol, 14: 3559–3568 Gregor T, Tank D W, Wieschaus E F, Bialek W (2007). Probing the limits to positional information. Cell, 130(1): 153–164 Grimm O, Coppey M, Wieschaus E (2010). Modelling the Bicoid gradient. Development, 137(14): 2253–2264 Grimm O, Wieschaus E (2010). The Bicoid gradient is shaped independently of nuclei INTRODUCTION. Development, 2862(17): 2857–2862 Grosshans J, Wenzl C, Herz H M, Bartoszewski S, Schnorrer F, Vogt N, Schwarz H, Müller H A (2005). RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development, 132(5): 1009–1020 Hu Q, Milenkovic L, Jin H, Scott M P, Nachury M V, Spiliotis E T, Nelson W J (2010). A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science, 329(5990): 436–439 Huang A M, Rusch J, Levine M (1997). An anteroposterior Dorsal gradient in the Drosophila embryo. Genes Dev, 11(15): 1963–1973 Huang H R, Chen Z J, Kunes S, Chang G D, Maniatis T (2010). Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc Natl Acad Sci U S A, 107(18): 8322–8327 Kanodia J S, Rikhy R, Kim Y, Lund V K, DeLotto R, Lippincott-Schwartz J, Shvartsman S Y (2009). Dynamics of the Dorsal morphogen gradient. Proc Natl Acad Sci USA, 106(51): 21707–21712 Karr T L, Alberts B M (1986). Organization of the cytoskeleton in early Drosophila embryos. J Cell Biol, 102(4): 1494–1509 Kavousanakis M E, Kanodia J S, Kim Y, Kevrekidis I G, Shvartsman S Y (2010). A compartmental model for the bicoid gradient. Dev Biol, 345(1): 12–17 Keith F J, Gay N J (1990). The Drosophila membrane receptor Toll promote cellular adhesion function to. EMBO J, 9: 4299–4306 Kim S K, Shindo A, Park T J, Oh E C, Ghosh S, Gray R S, Lewis R A, Johnson C A, Attie-Bittach T, Katsanis N, Wallingford J B (2010). Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science, 329(5997): 1337–1340 Kim Y, Coppey M, Grossman R, Ajuria L, Jiménez G, Paroush Z, Shvartsman S Y (2010). MAPK substrate competition integrates patterning signals in the Drosophila embryo. Curr Biol, 20(5): 446–451 Kim Y K, Furic L, Desgroseillers L, Maquat L E, York N (2005). Mammalian Staufen1 recruits Upf1 to specific mRNA 3’UTRs so as to elicit mRNA decay. Cell, 120(2): 195–208 Lecuit T (2004). Junctions and vesicular trafficking during Drosophila cellularization. J Cell Sci, 117(16): 3427–3433. Lecuit T, Samanta R, Wieschaus E (2002). slam encodes a developmental regulator of polarized membrane growth during cleavage of the Drosophila embryo. Dev Cell, 2(4): 425–436 Lipshitz H D (2009). Follow the mRNA: a new model for Bicoid gradient formation. Nat Rev Mol Cell Biol, 10: 509–512 Lloyd T E, Atkinson R, Wu M N, Zhou Y, Pennetta G, Bellen H J (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell, 108(2): 261–269 Löhr U, Chung H R, Beller M, Jäckle H (2009). Antagonistic action of Bicoid and the repressor Capicua determines the spatial limits of Drosophila head gene expression domains. Proc Natl Acad Sci USA, 106(51): 21695–21700 Lund V K, DeLotto Y, DeLotto R (2010). Endocytosis is required for Toll signaling and shaping of the Dorsal/NF-κB morphogen gradient during Drosophila embryogenesis. Proc Natl Acad Sci USA, 107(42): 18028–18033 Mavrakis M, Rikhy R, Lippincott-Schwartz J (2009). Plasma membrane polarity and compartmentalization are established before cellularization in the fly embryo. Dev Cell, 16(1): 93–104 Minden J S, Agard D (1989). Direct cell lineage analysis in Drosophila melanogaster by time-lapse, three-dimensional optical microscopy of living embryos. J Cell Biol, 109(2): 505–516 Moussian B, Roth S (2005). Dorsoventral axis formation in the Drosophila embryo-shaping and transducing a morphogen gradient. Curr Biol, 15: 887–899 Papatsenko D (2005). Quantitative analysis of binding motifs mediating diverse spatial readouts of the Dorsal gradient in the Drosophila embryo. Proc Natl Acad Sci USA, 102(14): 4966–4971 Postner MA, Wieschaus E F (1994). The nullo protein is a component of the actin-myosin network that mediates cellularization in Drosophila melanogaster embryos. J Cell Sci, 107(Pt 7): 1863–1873 Raff J W, Glover D M (1989). Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell, 57(4): 611–619 Ratnaparkhi G S, Jia S, Courey A J (2006). Uncoupling dorsal-mediated activation from dorsal-mediated repression in the Drosophila embryo. Development, 4414(22): 4409–4414 Riggs B, Rothwell W, Mische S, Hickson G R X, Matheson J, Hays T S, Gould G W (2003). Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J Cell Biol, 163(1): 143–154 Roth S, Lynch J A (2009). Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol, 1(2): a001891 Royou A, Sullivan W (2002). Cortical recruitment of nonmuscle myosin II in early syncytial Drosophila embryos: its role in nuclear axial expansion and its regulation by Cdc2 activity. J Cell Biol, 158(1): 127–137 Rusch J, Levine M (1994). Regulation of the dorsal morphogen by the Toll and torso signaling pathways: a receptor tyrosine kinase selectively masks transcriptional repression. Genes Dev, 8(11): 1247–1257 Silverman-Gavrila R V, Hales K G, Wilde A (2008). Anillin-mediated targeting of peanut to pseudocleavage furrows is regulated by the GTPase Ran. Mol Biol Cell, 19(9): 3735–3744 Simpson L, Wieschaus E (1990). Zygotic activity of the nullo locus is required to stabilize the actin-myosin network during cellularization in Drosophila. Development, 110: 851–863 Sisson J C, Field C, Ventura R, Royou A, Sullivan W (2000). Lava lamp, a novel peripheral Golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol, 151(4): 905–918 Sokac A M, Wieschaus E (2008). Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev Cell, 14(5): 775–786 Sonnenblick B P (1948). Synchronous mitoses in Drosophila, their intensely rapid rate, and the sudden appearance of the nucleolus. Genetics, 33: 125 Spirov A, Fahmy K, Schneider M, Frei E, Noll M, Baumgartner S (2009). Formation of the bicoid morphogen gradient: an mRNA gradient dictates the protein gradient. Development, 614(4): 605–614 Sprenger F, Stevens L M, Nüsslein-Volhard C (1989). The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature, 338(6215): 478–483 Stevenson V, Hudson A, Cooley L, Theurkauf W E (2002). Arp2/3-dependent pseudocleavage furrow assembly in syncytial Drosophila embryos. Curr Biol, 12: 705–711 Takizawa P A, DeRisi J L, Wilhelm J E, Vale R D (2000). Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science, 290(5490): 341–344 Tipping M, Kim Y, Kyriakakis P, Tong M, Shvartsman S Y, Veraksa A (2010). β-arrestin Kurtz inhibits MAPK and Toll signalling in Drosophila development. EMBO J, 29(19): 3222–3235 Turner F R, Mahowald A P (1977). Scanning electron microscopy of Drosophila melanogaster embryogenesis. II. Gastrulation and segmentation. Dev Biol, 57(2): 403–416 Ventura G, Furriols M, Martín N, Barbosa V, Casanova J (2010). closca, a new gene required for both Torso RTK activation and vitelline membrane integrity. Germline proteins contribute to Drosophila eggshell composition. Dev Biol, 344(1): 224–232 von Dassow G, Schubiger G (1994). How an actin network might cause fountain streaming and nuclear migration in the syncytial Drosophila embryo. J Cell Biol, 127(6): 1637–1653 Weber A N R, Gangloff M, Moncrieffe M C, Hyvert Y, Imler J L, Gay N J (2007). Role of the Spatzle Pro-domain in the generation of an active toll receptor ligand. J Biol Chem, 282(18): 13522–13531 Weil T T, Forrest K M, Gavis E R (2006). Localization of bicoid mRNA in late oocytes is maintained by continual active transport. Dev Cell, 11(2): 251–262 Weil T T, Parton R, Davis I, Gavis E R (2008). Report changes in bicoid mRNA anchoring highlight conserved mechanisms during the oocyte-to-embryo transition. Curr Biol, 18(14): 1055–1061