Drosophila embryo syncytial blastoderm cellular architecture and morphogen gradient dynamics: Is there a correlation?
Received date: 10 May 2011
Accepted date: 13 Jul 2011
Published date: 01 Feb 2012
Copyright
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.
Key words: morphogen gradient; Drosophila; syncytium; embryo; cellular architecture
Aparna SHERLEKAR , Richa RIKHY . Drosophila embryo syncytial blastoderm cellular architecture and morphogen gradient dynamics: Is there a correlation?[J]. Frontiers in Biology, 2012 , 7(1) : 73 -82 . DOI: 10.1007/s11515-011-1160-4
1 |
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
|
2 |
Afshar K, Stuart B, Wasserman S A (2000). Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development, 127: 1887-1897
|
3 |
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
|
4 |
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
|
5 |
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
|
6 |
Bownes M (1975). A photographic study of development in the living embryo of Drosophila melanogaster. J Embryol Exp Morphol, 33: 789-801
|
7 |
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
|
8 |
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
|
9 |
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
|
10 |
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
|
11 |
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
|
12 |
Dilão R, Muraro D (2010). mRNA diffusion explains protein gradients in Drosophila early development. J Theor Biol, 264(3): 847-853
|
13 |
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
|
14 |
Driever W, Nüsslein-Volhard C (1988a). A gradient of bicoid protein in Drosophila embryos. Cell, 54(1): 83-93
|
15 |
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
|
16 |
Field C M (2005). Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development, 132(12): 2849-2860
|
17 |
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
|
18 |
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
|
19 |
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
|
20 |
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
|
21 |
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
|
22 |
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
|
23 |
Gregor T, Tank D W, Wieschaus E F, Bialek W (2007). Probing the limits to positional information. Cell, 130(1): 153-164
|
24 |
Grimm O, Coppey M, Wieschaus E (2010). Modelling the Bicoid gradient. Development, 137(14): 2253-2264
|
25 |
Grimm O, Wieschaus E (2010). The Bicoid gradient is shaped independently of nuclei INTRODUCTION. Development, 2862(17): 2857-2862
|
26 |
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
|
27 |
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
|
28 |
Huang A M, Rusch J, Levine M (1997). An anteroposterior Dorsal gradient in the Drosophila embryo. Genes Dev, 11(15): 1963-1973
|
29 |
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
|
30 |
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
|
31 |
Karr T L, Alberts B M (1986). Organization of the cytoskeleton in early Drosophila embryos. J Cell Biol, 102(4): 1494-1509
|
32 |
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
|
33 |
Keith F J, Gay N J (1990). The Drosophila membrane receptor Toll promote cellular adhesion function to. EMBO J, 9: 4299-4306
|
34 |
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
|
35 |
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
|
36 |
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
|
37 |
Lecuit T (2004). Junctions and vesicular trafficking during Drosophila cellularization. J Cell Sci, 117(16): 3427-3433
|
38 |
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
|
39 |
Lipshitz H D (2009). Follow the mRNA: a new model for Bicoid gradient formation. Nat Rev Mol Cell Biol, 10: 509-512
|
40 |
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
|
41 |
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
|
42 |
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
|
43 |
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
|
44 |
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
|
45 |
Moussian B, Roth S (2005). Dorsoventral axis formation in the Drosophila embryo-shaping and transducing a morphogen gradient. Curr Biol, 15: 887-899
|
46 |
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
|
47 |
Postner M A, 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
|
48 |
Raff J W, Glover D M (1989). Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell, 57(4): 611-619
|
49 |
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
|
50 |
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
|
51 |
Roth S, Lynch J A (2009). Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol, 1(2): a001891
|
52 |
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
|
53 |
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
|
54 |
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
|
55 |
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
|
56 |
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
|
57 |
Sokac A M, Wieschaus E (2008). Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev Cell, 14(5): 775-786
|
58 |
Sonnenblick B P (1948). Synchronous mitoses in Drosophila, their intensely rapid rate, and the sudden appearance of the nucleolus. Genetics, 33: 125
|
59 |
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
|
60 |
Sprenger F, Stevens L M, Nüsslein-Volhard C (1989). The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature, 338(6215): 478-483
|
61 |
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
|
62 |
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
|
63 |
Tipping M, Kim Y, Kyriakakis P, Tong M, Shvartsman S Y, Veraksa A (2010). b-arrestin Kurtz inhibits MAPK and Toll signalling in Drosophila development. EMBO J, 29(19): 3222-3235
|
64 |
Turner F R, Mahowald A P (1977). Scanning electron microscopy of Drosophila melanogaster embryogenesis. II. Gastrulation and segmentation. Dev Biol, 57(2): 403-416
|
65 |
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
|
66 |
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
|
67 |
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
|
68 |
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
|
69 |
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
|
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|
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