Early patterning of the spider embryo: A cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells

Development

Volumn 130, Issue 9, 2003, Pages 1735-1747

  Akiyama Oda, Yasuko ^a   Oda, Hiroki ^a  

^a JT Biohistory Research Hall ^*  (Japan)

Author keywords

Body axis formation; cad cdx; Chelicerate; Cumulus; dpp DMP2 BMP4; Embryogenesis; Fork head HNF3; Mad Smad; otd otx; Spider

Indexed keywords

MORPHOGEN; PHOSPHOPROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANTERIOR POSTERIOR AXIS; CELL ACTIVITY; CELL INTERACTION; CELL MIGRATION; CELL NUCLEUS; CELL STRUCTURE; CELLULAR DISTRIBUTION; CLUSTER ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DROSOPHILA; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GERM CELL; IN SITU HYBRIDIZATION; MALE; MESENCHYME CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPIDER;

AMINO ACID SEQUENCE; ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EPITHELIUM; FORKHEAD TRANSCRIPTION FACTORS; GERM CELLS; HOMEODOMAIN PROTEINS; MESODERM; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; REPRESSOR PROTEINS; SPIDERS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

ACHAEARANEA TEPIDARIORUM; ARANEAE; INVERTEBRATA;

EID: 0037621689     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00390     Document Type: Review

References (78)

1. Abzhanov, A., Popadic, A. and Kaufman, T. C. (2000). Chelicerate Hox genes and the homology of arthropod segments. Evol. Dev. 1, 77-89.
2. Angerer, L. M., Oleksyn, D. W., Logan, C. Y., McClay, D. R., Dale, L. and Angerer, R. C. (2000). A BMP pathway regulates cell fate allocation along the sea urchin animal-vegetal embryonic axis. Development 127, 1105-1114.
3. Ashe, H. L. and Levine, M. (1999). Local inhibition and long-range enhancement of Dpp signal transduction by Sog. Nature 398, 427-431.
4. Ashe, H. L., Mannervik, M. and Levine, M. (2000). Dpp signaling thresholds in the dorsal ectoderm of the Drosophila embryo. Development 127, 3305-3312.
5. Chasan, R. and Anderson, K. V. (1993). Maternal control of dorsal-ventral polarity and pattern in the embryo. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 387-424. New York: Cold Spring Harbor Laboratory Press.
6. Cohen, S. M. and Jürgens, G. (1990). Mediation of Drosophila head development by gap-like segmentation genes. Nature 346, 482-485.
7. Cook, C. E., Smith, M. L., Telford, M. J., Bastianello, A. and Akam, M. (2001). Hox genes and the phylogeny of the arthropods. Curr. Biol. 11, 759-763.
8. Damen, W. G. M. (2002). Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129, 1239-1250.
9. Damen, W. G. M., Hausdorf, M., Seyfarth, E.-A. and Tautz, D. (1998). A conserved mode of head segmentaton in arthropods revealed by the expression pattern of Hox genes in a spider. Proc. Natl. Acad. Sci. USA 95, 10665-10670.
10. Damen, W. G. M. and Tautz, D. (1998). A Hox class 3 orthologue from the spider Cupiennius salei is expressed in a Hox-gene-like fashion. Dev. Genes Evol. 208, 586-590.
11. Damen, W. G. M., Weller, M. and Tautz, D. (2000). Expression patterns of hairy, even-skipped, and runt in the spider Cupiennius salei imply that these genes were segmentation genes in a basal arthropod. Proc. Natl. Acad. Sci. USA 97, 4515-4519.
12. Darras, S. and Nishida, H. (2001). The BMP/CHORDIN antagonism controls sensory pigment cell specification and differentiation in the ascidian embryo. Dev. Biol. 236, 271-288.
13. De Robertis, E. M. and Sasai, Y. (1996). A common plan for dorsoventral patterning in Bilateria. Nature 380, 37-40.
14. Dearden, P. K. and Akam, M. (2001). Early embryo patterning in the grasshopper, Schistocerca gregaria: wingless, dacapentaplegic and caudal expression. Development 128, 3435-3444.
15. Dearden, P. K., Donly, C. and Grbic, M. (2002). Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae. Development 129, 5461-5472.
16. Dorfman, R. and Shilo, B.-Z. (2001). Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region. Development 128, 965-972.
17. Driever, W. (1993). Maternal control of anterior development in the Drosophila embryo. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 301-324. New York: Cold Spring Harbor Laboratory Press.
18. Ferguson, E. L. (1996). Conservation of dorsal-ventral patterning in arthropods and chordates. Curr. Opin. Genet. Dev. 6, 424-431.
19. Ferguson, E. L. and Anderson, K. V. (1992a). decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451-461.
20. Ferguson, E. L. and Anderson, K. V. (1992b). Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114, 583-597.
21. Finkelstein, R. and Perrimon, N. (1990). The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346, 485-488.
22. Finkelstein, R., Smouse, D., Capaci, T. M., Spradling, A. C. and Perrimon, N. (1990). The orthodenticle gene encodes a novel homeo domain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev. 4, 1516-1527.
23. François, V., Solloway, M., O'Neill, J. W., Emery, J. and Bier, E. (1994). Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev. 8, 2602-2616.
24. Friedrich, M. and Tautz, D. (1995). Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376, 165-167.
25. Gerberding, M., Browne, W. E. and Patel, N. H. (2002). Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129, 5789-5801.
26. Giribet, G., Edgecombe, G. D. and Wheeler, W. C. (2001). Arthropod phylogeny based on eight molecular loci and morphology. Nature 413, 157-161.
27. Hayward, D. C., Samuel, G., Pontynen, P. C., Catmull, J., Saint, R., Miller, D. J. and Ball, E. E. (2002). Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc. Natl. Acad. Sci. USA 99, 8106-8111.
28. Heymons, R. (1901). Die Entwicklungsgeschichte der Scolopender. Zoologica (Stuttg.) 13, 1-244.
29. Holley, S. A. and Ferguson, E. L. (1997). Fish are like flies are like frogs: conservation of dorsal-venrtal patterning mechanisms. BioEssays 19, 281-284.
30. Holley, S. A., Jackson, P. D., Sasai, Y., Lu, B., de Robertis, E. M., Hoffman, F. M. and Ferguson, E. L. (1995). A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249-253.
31. Holm, Å. (1940). Studien über die Entwicklung und Entwicklungsbiologie der Spinnen. Zool. BiDr Uppsala 19, 1-214.
32. Holm, Å. (1952). Experimentelle Untersuchungen über die Entwicklung und Entwicklungsphysiologie des Spinnenembryos. Zool. BiDr Uppsala 29, 293-424.
33. Hwang, U. W., Friedrich, M., Tautz, D., Park, C. J. and Kim, W. (2001). Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413, 154-157.
34. Irish, V. F. and Gelbart, W. M. (1987). The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev. 1, 868-879.
35. Itow, T., Kenmochi, S. and Mochizuki, T. (1991). Induction of secondary embryos by intra- and interspecific grafts of center cells under the blastopore in horseshoe crabs. Dev. Growth Differ. 33, 251-258.
36. Kokubo, H., Takiya, S., Mach, V. and Suzuki, Y. (1996). Spatial and temporal expression pattern of Bombyx fork head/SGF-1 gene in embryogenesis. Dev. Genes Evol. 206, 80-85.
37. Lai, E., Prezioso, V. R., Tao, W., Chen, W. S. and Darnell Jr, J. E. (1991). Hepatocyte nuclear factor 3α belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 5, 416-427.
38. Lehmann, R. and Tautz, D. (1994). In situ hybridization to RNA. In Drosophila melanogaster: Practical Uses in Cell and Molecular Biology (ed. L. S. B. Goldstein and E. A. Fyrberg), pp. 575-598. San Diego: Academic Press.
39. Macdonald, P. M. and Struhl, G. (1986). A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324, 537-545.
40. Marqués, G., Musacchio, M., Shimell, M. J., Wünnenberg-Stapleton, K., Cho, K. W. Y. and O'Connor, M. B. (1997). Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91, 417-426.
41. Miya, T., Morita, K., Suzuki, A., Ueno, N. and Satoh, N. (1997). Functional analysis of an ascidian homologue of vertebrate Bmp-2/Bmp-4 suggests its role in the inhibition of neural fate specification. Development 124, 5149-5159.
42. Mlodzik, M., Fjose, A. and Gehring, W. J. (1985). Isolation of caudal, a Drosophila homeo box-containing gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J. 4, 2961-2969.
43. Mlodzik, M. and Gehring, W. J. (1987). Expression of the caudal gene in the germ line of Drosophila: Formation of an RNA and protein gradient during early embryogenesis. Cell 48, 465-478.
44. Montgomery, T. H., Jr (1909). The development of Theridium, an Aranead, up to the stage of reversion. J. Morphol. 20, 297-352.
45. Morata, G. and Basler, K. (1999). Cells in search of a signal. Nat. Cell Biol. 1, E60-E61.
46. Nederbragt, A. J., van Loon, A. E. and Dictus, W. J. A. G. (2002). Expression of Patella vulgata orthorogs of engrailed and dpp-BMP2/4 in adjacent domains during molluscan shell development suggests a conserved compartment boundary mechanism. Dev. Biol. 246, 341-355.
47. Niwa, N., Inoue, Y., Nozawa, A., Saito, M., Misumi, Y., Ohuchi, H., Yoshioka, H. and Noji, S. (2000). Correlation of diversity of leg morphology in Gryllus bimaculatus (cricket) with divergence in dpp expression pattern during leg development. Development 127, 4373-4381.
48. Orii, H., Kato, K., Agata, K. and Watanabe, K. (1998). Molecular cloning of Bone Morphogenetic Protein (BMP) gene from the planarian Dugesia japonica. Zool. Sci. 15, 871-877.
49. Padgett, R. W., St Johnston, R. D. and Gelbart, W. M. (1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 325, 81-84.
50. Panganiban, G. E. F., Rashka, K. E., Neitzel, M. D. and Hoffmann, F. M. (1990). Biochemical characterization of the Drosophila dpp protein, a member of the transforming growth factor β family of growth factors. Mol. Cell. Biol. 10, 2669-2677.
51. Panopoulou, G. D., Clark, M. D., Holland, L. Z., Lehrach, H. and Holland, N. D. (1998). AmpihBMP2/4, an amphioxus bone morphogenetic protein closely related to Drosophila decapentaplegic and vertebrate BMP2 and BMP4: Insights into evolution of dorsoventral axis specification. Dev. Dyn. 213, 130-139.
52. Persson, U., Izumi, H., Souchelnytskyi, S., Itoh, S., Grimsby, S., Engström, U., Heldin, C.-H., Funa, K. and ten Dijke, P. (1998). The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434, 83-87.
53. Raftery, L. A. and Sutherland, D. J. (1999). TGF-β family signal transduction in Drosophila development: From Mad to Smads. Dev. Biol. 210, 251-268.
54. Ramírez-Weber, F.-A. and Kornberg, T. B. (1999). Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97, 599-607.
55. Ramírez-Weber, F.-A. and Kornberg, T. B. (2000). Signaling reaches to new dimensions in Drosophila imaginal discs. Cell 103, 189-192.
56. Rusch, J. and Levine, M. (1996). Threshold responses to the dorsal regulatory gradient and the subdivision of primary tissue territories in the Drosophila embryo. Curr. Opin. Genet. Dev. 6, 416-423.
57. Rushlow, C., Colosimo, P. F., Lin, M.-c., Xu, M. and Kirov, N. (2001). Transcriptional regulation of the Drosophila gene zen by competing Smad and Brinker inputs. Genes Dev. 15, 340-351.
58. Saitou, N. and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
59. Sakuma, M. and Machida, R. (2002). Germ band formation of a centipede Scolopocrytops rubiginosus L. Koch (Chilopoda: Scolopendromorpha). Proc. Arthropod. Embryol. Soc. Jpn. 37, 19-23.
60. Sanchez-Salazar, J., Pletcher, M. T., Bennett, R. L., Brown, S. J., Dandamudi, T. J., Denell, R. E. and Doctor, J. S. (1996). The Tribolium decapentaplegic gene is similar in sequence, structure, and expression to the Drosophila dpp gene. Dev. Genes Evol. 206, 237-246.
61. Sander, K. (1976). Specification of the basic body pattern in insect embryogenesis. Adv. Insect Physiol. 12, 125-238.
62. Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L. K. and de Robertis, E. M. (1994). Xenopus chordin: A novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79, 779-790.
63. Schröder, R., Eckert, C., Wolff, C. and Tautz, D. (2000). Conserved and divergent aspects of terminal patterning in the beetle Tribolium castaneum. Proc. Natl. Acad. Sci. USA 97, 6591-6596.
64. Seitz, V. K.-A. (1966). Normale Entwicklung des Arachniden-Embryos Cupiennius salei Keyserling und seine Regulationsbefähigung nach Röntgenbestrahlungen. Zool. Jb. Anat. Bd. 83, 327-447.
65. Seitz, V. K.-A. (1970). Embryonale Defekt- und Doppelbildungen im Ei der Spinne Cupiennius Salei (Ctenidae). Zool. Jb. Anat. Bd. 87, 588-639.
66. Sekiguchi, K. (1957). Reduplication in spider eggs produced by centrifugation. Sci. Rep. Tokyo kyoiku Daigaku, Sec. B 8, 227-280.
67. Sekiguchi, K. (1973). A normal plate of the development of the Japanese horse-shoe crab, Tachypleus tridentatus. Sci. Rep. Tokyo Kyoiku Daigaku, sec. B 15, 153-162.
68. St Johnston, D. and Nüsslein-Volhard, C. (1992). The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201-219.
69. St Johnston, R. D. and Gelbart, W. M. (1987). Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J. 6, 2785-2791.
70. Stathopoulos, A. and Levine, M. (2002). Dorsal gradient networks in the Drosophila embryo. Dev. Biol. 246, 57-67.
71. Stollewerk, A., Weller, M. and Tautz, D. (2001). Neurogenesis in the spider Cupiennius salei. Development 128, 2673-2688.
72. Suzuki, H. and Kondo, A. (1995). Early embryonic development, including germ-disk stage, in the theridiid spider Achaearanea japonica (Bös. et Str.). J. Morphol. 224, 147-157.
73. Tanimoto, H., Itoh, S., ten Dijke, P. and Tabata, T. (2000). Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell 5, 59-71.
74. Telford, M. J. and Thomas, R. H. (1998a). Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc. Natl. Acad. Sci. USA 95, 10671-10675.
75. Telford, M. J. and Thomas, R. H. (1998b). Of mites and zen: expression studies in a chelicerate arthropod confirm zen is a divergent Hox gene. Dev. Genes Evol. 208, 591-594.
76. Weigel, D., Jürgens, G., Küttner, F., Seifert, E. and Jäckle, H. (1989). The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645-658.
77. Wolff, C. and Scholtz, G. (2002). Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev. Biol. 250, 44-58.
78. Wu, L. H. and Lengyel, J. A. (1998). Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125, 2433-2442.