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

doi:10.1007/s11515-011-1160-4

Front Biol

2012, Vol. 7

Issue (1) : 73-82 https://doi.org/10.1007/s11515-011-1160-4

REVIEW

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

Aparna SHERLEKAR, Richa RIKHY(

)

Indian Institute of Science, Education and Research, Biology, 301, Central Tower, Sai Trinity Bldg, Pashan, Pune 411021, India

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Abstract

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.

Keywords morphogen gradient Drosophila syncytium embryo cellular architecture

Corresponding Author(s): RIKHY Richa,Email:richa@iiserpune.ac.in

Issue Date: 01 February 2012

Cite this article:

Aparna SHERLEKAR,Richa RIKHY. Drosophila embryo syncytial blastoderm cellular architecture and morphogen gradient dynamics: Is there a correlation?[J]. Front Biol, 2012, 7(1): 73-82.

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https://academic.hep.com.cn/fib/EN/10.1007/s11515-011-1160-4
https://academic.hep.com.cn/fib/EN/Y2012/V7/I1/73

Fig.1 The cellular architecture in the syncytial embryo during interphase of the nuclear cycles 11-13. The centrosomes are present apically. These form microtubules in the vertical direction. The endoplasmic reticulum and the Golgi complex are partitioned to each nucleus and show compartmentalization of diffusion around each nucleus. The actin cytoskeleton is present as caps beneath apical plasma membrane, which is rich in microvilli. The lateral plasma membrane, which surrounds each nucleus only partially during interphase of the syncytial cycle, contains specific transmembrane proteins such as Tl, junctional proteins such as Cadherin and Patj, cytoskeletal-remodeling proteins such as Anillin and Peanut and endocytosis proteins such as Dynamin and Clathrin (not drawn to scale).

Fig.2 Bicoid (Bcd) gradient in the syncytium. The mRNA and the Bcd protein form a gradient across the syncytial nuclei in the anterior (A). The Staufen protein is required for anchoring the mRNA at the anterior of the embryo. The Bcd protein is formed from translation of the mRNA and enters the nucleus where it activates specific downstream gene expression responsible for determining the anterior end of the embryo (B) (not drawn to scale).

Fig.3 MAP kinase (MAPK) gradient in the syncytium. The MAPK gradient is formed on the anterior and the posterior by the activation of the Torso (Tor) receptor (A). The Tor receptor gets activated by processing of the Tor-like ligand in the perivitelline space. The Tor receptor is present all over the plasma membrane and is endocytosed and degraded in lysosomes after activation (B) (not drawn to scale).

Fig.4 Dorsal (Dl) gradient in the syncytium. The Dl gradient in the syncytium is formed in response to activation of Toll (Tl) receptor by Sp?ztle (Spz) (A). The Tl receptor is activated by cleaved Spz locally formed in the perivitelline space on the ventral side. The activated Tl receptor is endocytosed and has been shown to signal from Rab5 positive early endosomes (B) (not drawn to scale).

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 Sp?tzle, the ligand for the Drosophila Toll receptor. J Biol Chem , 285(25): 19502-19509 doi: 10.1074/jbc.M109.098186
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 doi: 10.1083/jcb.122.1.113
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 doi: 10.1016/j.ydbio.2007.09.058
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 doi: 10.1038/embor.2009.128
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 doi: 10.1242/dev.010934
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	Dil?o R, Muraro D (2010). mRNA diffusion explains protein gradients in Drosophila early development. J Theor Biol , 264(3): 847-853 doi: 10.1016/j.jtbi.2010.03.012
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 doi: 10.1016/0092-8674(88)90182-1
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 doi: 10.1016/0092-8674(88)90183-3
16	Field C M (2005). Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development , 132(12): 2849-2860 doi: 10.1242/dev.01843
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 doi: 10.1083/jcb.131.1.165
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 doi: 10.1016/0092-8674(86)90666-5
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 doi: 10.1083/jcb.200601156
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 Sp?tzle. J Biol Chem , 283(21): 14629-14635 doi: 10.1074/jbc.M800112200
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 doi: 10.1242/dev.032409
25	Grimm O, Wieschaus E (2010). The Bicoid gradient is shaped independently of nuclei INTRODUCTION. Development , 2862(17): 2857-2862 doi: 10.1242/dev.052589
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 doi: 10.1242/dev.01669
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 doi: 10.1126/science.1191054
28	Huang A M, Rusch J, Levine M (1997). An anteroposterior Dorsal gradient in the Drosophila embryo. Genes Dev , 11(15): 1963-1973 doi: 10.1101/gad.11.15.1963
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 doi: 10.1073/pnas.0912395106
31	Karr T L, Alberts B M (1986). Organization of the cytoskeleton in early Drosophila embryos. J Cell Biol , 102(4): 1494-1509 doi: 10.1083/jcb.102.4.1494
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 doi: 10.1016/j.ydbio.2010.05.491
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 doi: 10.1126/science.1191184
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 doi: 10.1016/j.cub.2010.01.019
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 doi: 10.1242/jcs.01312.
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 doi: 10.1016/S1534-5807(02)00141-7
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 doi: 10.1016/S0092-8674(02)00611-6
41	L?hr U, Chung H R, Beller M, J?ckle 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 doi: 10.1073/pnas.0910225106
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 doi: 10.1073/pnas.1009157107
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 doi: 10.1016/j.devcel.2008.11.003
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 doi: 10.1083/jcb.109.2.505
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 doi: 10.1073/pnas.0409414102
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 doi: 10.1016/0092-8674(89)90130-X
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 doi: 10.1242/dev.02643
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 doi: 10.1083/jcb.200305115
51	Roth S, Lynch J A (2009). Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol , 1(2): a001891 doi: 10.1101/cshperspect.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 doi: 10.1083/jcb.200203148
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 doi: 10.1101/gad.8.11.1247
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 doi: 10.1091/mbc.E08-01-0049
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 doi: 10.1083/jcb.151.4.905
57	Sokac A M, Wieschaus E (2008). Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev Cell , 14(5): 775-786 doi: 10.1016/j.devcel.2008.02.014
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 doi: 10.1242/dev.031195
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 doi: 10.1038/338478a0
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 doi: 10.1126/science.290.5490.341
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 doi: 10.1038/emboj.2010.202
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 doi: 10.1016/0012-1606(77)90225-1
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 doi: 10.1016/j.ydbio.2010.05.002
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 doi: 10.1083/jcb.127.6.1637
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 doi: 10.1074/jbc.M700068200
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 doi: 10.1016/j.devcel.2006.06.006
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 doi: 10.1016/j.cub.2008.06.046

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