Neurogenesis in the spider: New insights from comparative analysis of morphological processes and gene expression patterns

Arthropod Structure and Development

Volumn 32, Issue 1, 2003, Pages 5-16

  Stollewerk, Angelika ^a   Tautz, Diethard ^a   Weller, Mathias ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cupiennius salei; Helicerate; Neural identity; Neurogenesis; Pan neural genes; Proneural genes

Indexed keywords

ARTICLE; CELL SPECIFICITY; COMPARATIVE ANATOMY; CONTROLLED STUDY; CRUSTACEA; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; FLY; FUNCTIONAL ASSESSMENT; GENE CONTROL; GENE EXPRESSION REGULATION; INSECT DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROECTODERM; NONHUMAN; SIGNAL TRANSDUCTION; SPIDER; STEM CELL; STEREOTYPY;

ARACHNIDA; ARANEAE; CHELICERATA; CRUSTACEA; CUPIENNIUS SALEI; DIPTERA; DROSOPHILA MELANOGASTER; DROSOPHILIDAE; GASTROPODA; HEXAPODA; INSECTA; MELANOGASTER; MUSCOMORPHA;

EID: 0141524068     PISSN: 14678039     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1467-8039(03)00041-0     Document Type: Article

References (77)

1. Abzhanov, A., Kaufman, T.C., 1999. Homeotic genes and the arthropod head: expression patterns of the labial, proboscipedia, and Deformed genes in crustaceans and insects. Proceedings of the National Academy of Sciences USA 96, 10224-10229.
2. Abzhanov, A., Kaufman, T.C., 2000. Crustacean (malacostracan) Hox genes and the evolution of the arthropod trunk. Development 127, 2239-2249.
3. Abzhanov, A., Popadic, A., Kaufman, T.C., 1999. Chelicerate Hox genes and the homology of arthropod segments. Evolution and Development 2, 77-89.
4. Agricola, H.-J., Bräunig, P., 1995. Comparative aspects of peptidergic signalling pathways in the nervous systems of arthropods. In: Breidbach, O., Kutsch, W. (Eds.), The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach, pp. 303-328.
5. Akam, M., 2000. Arthropods: developmental diversity within a (super) phylum. Proceedings of the National Academy of Sciences USA 97, 4438-4441.
6. Akam, M., Dawson, I., Tear, G., 1988. Homeotic genes and the control of segment diversity. Development 104, 123-133.
7. Anderson, D., 1973. Embryology and Phylogeny in Annelids and Arthropods, Pergamon Press, Oxford.
8. Barth, F.G., 2001. Sinne und Verhalten-Aus dem Leben einer Spinne, Springer, Berlin.
9. Bate, C.M., 1976. Embryogenesis of an insect nervous system. I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. Journal of Embryology and Experimental Morphology 35, 107-123.
10. Bate, C.M., Grunewald, E.B., 1981. Embryogenesis of an insect nervous system II: A class of neuron precursor cells and the origin of the intersegmental connectives. Journal of Embryology and Experimental Morphology 61, 317-330.
11. Brand, M., Jarman, A.P., Jan, L.Y., Jan, Y.N., 1993. asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development 119, 1-17.
12. Brody, T., Odenwald, W.F., 2002. Cellular diversity in the developing nervous system: temporal view from Drosophila. Development 129, 3763-3770.
13. Buescher, M., Hing, F.S., Chia, W., 2002. Formation of neuroblasts in the embryonic central nervous system of Drosophila melanogaster is controlled by SoxNeuro. Development 129, 4193-4203.
14. Cabrera, C.V., Martinez A., Bate, M., 1987. The expression of three members of the achaete-scute gene complex correlates with neuroblast segregation in Drosophila. Cell 50, 425-433.
15. Campos-Ortega J.A., 1993. Early neurogenesis in Drosophila melanogaster. In: Bate, M., Martinez-Arias, A. (Eds.), The Development of Drosophila melanogaster, Cold Spring Harbor Laboratory, Cold Spring Harbor, pp. 1091-1129.
16. Campos-Ortega, J.A., Haenlin, M., 1992. Regulatory signals and signal molecules in early neurogenesis. Roux's Archiv of Developmental Biology 201, 1-11.
17. Chitnis A.B., 1995. The role of Notch in lateral inhibition and cell fate specification. Molecular and Cellular Neuroscience 6, 311-321.
18. Chu-LaGraff, Q., Doe, C.Q., 1993. Neuroblast specification and formation regulated by wingless in the Drosophila CNS. Science 261, 1594-1597.
19. Collier, J.R., Monk, N.A.M., Maini, P.K., Lewis, J.H., 1996. Pattern formation by lateral inhibition with feedback: a mathematical model of delta-notch intercellular signalling. Journal of Theoretical Biology 183, 429-446.
20. Cubas, P., de Cells, J.F., Campuzano, S., Modollel, J., 1991. Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes and Development 5, 996-1008.
21. 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.
22. Damen, W.G.M., Tautz, D., 1998. A Hox class 3 orthologue from the spider Cupiennius salei is expressed in a Hox-gene-like fashion. Development Genes and Evolution 208, 586-590.
23. Damen, W.G.M., Hausdorf, M., Seyfarth, E-A., Tautz, D., 1998. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proceedings of the National Academy of Sciences USA 95, 1065-10670.
24. Damen, W.G.M., Tautz, D., 1999. Abdominal-B expression in a spider suggests a general role for Abdominal-B in specifying the genital structure. Journal of Experimental Zoology 1999 Apr 15:285(1), 85-91.
25. Damen, W.G.M., Weller, M., 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. Proceedings of the National Academy of Sciences USA 97, 4515-4519.
26. Doe, C.Q., Skeath, J., 1996. Neurogenesis in the insect central nervous system. Current Opinions in Neurobiology 6, 18-24.
27. Doe, C.Q., Hiromi, Y., Gehring, W.J., Goodman, C.S., 1988. Expression and function of the segmentation gene fushi-tarazu during Drosophila neurogenesis. Science 239, 170-175.
28. Dohle, W., Scholtz, G., 1988. Clonal analysis of the crustacean segment: the disaccordance between genealogical and segmental borders. Development 104(Suppl.), 147-160.
29. Foelix, R.F., 1996. Biology of Spiders. In: Foelix, (Ed.), Oxford University Press, Oxford.
30. Fuse, N., Hirose, S., Hayashi, S., 1996. Determination of wing cell fate by escargot and snail genes in Drosophila. Development 122, 1059-1067.
31. Ghysen, A., Dambly-Chaudière, C., Jan, I.Y., Jan, Y.N., 1993. Cell interactions and gene interactions in peripheral neurogenesis. Genes and Development 7, 723-733.
32. Goodman, C.S., Doe, C.Q., 1993. Embryonic development of the Drosophila central nervous system. In: Bate, M., Martinez-Arias, A. (Eds.), The Development of Drosophila melanogaster, Cold Spring Harbor Laboratory Press, New York, pp. 1131-1206.
33. Groβhans, J., Wieschaus, E., 2000. A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101, 523-531.
34. Haase, A., Stern, M., Wachtler, K., Bicker, G., 2002. A tissue-specific marker of Ecdysozoa. Development Genes and Evolution 211, 428-433.
35. Hartenstein, V., Campos-Ortega, J.A., 1984. Early neurogenesis in wildtype Drosophila melanogaster. Roux's Archiv of Developmental Biology 193, 308-325.
36. Hartenstein, V., Rudloff, E., Campos-Ortega, J.A., 1987. The pattern of proliferation of the neuroblasts in the wild-type embryo of Drosophila melanogaster. Roux's Archiv of Developmental Biology 196, 473-485.
37. Heitzler, P., Simpson, P., 1991. The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083-1092.
38. Ip, Y.T., Levine, M., Bier, E., 1994. Neurogenic expression of snail is controlled by separable CNS and PNS promotor elements. Development 120, 199-207.
39. Isshiki, T., Pearson, B., Holbrook, S., Doe, C.Q., 2001. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511-521.
40. Jan, L.Y., Jan, Y.N., 1982. Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proceedings of the National Academy of Sciences USA 79, 2700-2704.
41. Jiménez, F., Campos-Ortega, J.A., 1990. Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of D. melanogaster. Neuron 5, 81-89.
42. Lehmann, R., Dietrich, F., Jiménez, F., Campos-Ortega, J.A., 1981. Mutations of early neurogenesis in Drosophila. Roux's Archiv of Developmental Biology 190, 226-229.
43. Lehmann, R., Jiménez, F., Dietrich, U., Campos-Ortega, J.A. 1983. On the phenotype and development of of mutants of early neurogenesis in Drosophila melanogaster. Roux's Archiv of Developmental Biology 192, 62-74.
44. Ligoxygakis, P., Yu, S.Y., Delidakis, C., Baker, N.E., 1998. A subset of Notch functions during Drosophila eye development require Su(H) and the E(spl) gene complex. Development 125, 2893-2900.
45. Martin-Bermudo, M.D., Martinez, C., Rodriguez, A., Jimenez, F., 1991. Distirbution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development 113, 445-454.
46. Mathew, A.P., 1956. Embryology of Heterometrus scaber (Thorell), Arachnida, Scorpionidae. Zool. Mem. Univ. Travancore 1, 1-96.
47. Meier, T., Reichert, H., 1990. Embryonic developement and evolutionary origin of the Orthopteran auditory organs. Journal of Neurobiology 21, 592-610.
48. Muskavitch, M.A.T., 1994. Delta-Notch signaling and Drosophila cell fate choice. Developmental Biology 166, 415-430.
49. Nakao, K., Campos-Ortega, J.A., 1996. Persistent expression of genes of the Enhancer of split complex suppresses neural development in Drosophila. Neuron 16, 275-286.
50. Overton. P.M., Meadows, L.A., Urban, J., Russell, S., 2002. Evidence for differential and redundant function of the Sox genes Dichaete and SoxN during CNS development in Drosophila. Development 129, 4219-4228.
51. Pasakony, J.W., 1994. Nature versus nurture: asymmetric cell divisions in Drosophila bristle development. Cell 76, 477-491.
52. Patel, N.H., Martin-Blanco, E., Coleman, K.G., Poole, S.J., Ellis, M.C., Kornberg, T.B., Goodman, C.S., 1989a. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
53. Patel, N.H., Kornberg, T.B., Goodman, C.S., 1989b. Expression of engrailed during segmentation in grasshopper and crayfish. Development 107, 201-212.
54. Retzlaff, M., 1996. Vergleichende Analyse von Entwicklungsgenen bei verschiedenen Arthropoden unter besonderer Berücksichtigung von Cupiennius salei (Araneae: Ctenidas), Shaker, Aachen.
55. Roark, M., Sturtevant, M.A., Emery, J., Vaessin, H., Grell, E., Bier, E., 1995. Scratch, a pan-neural gene encoding a zinc finger protein related to snail promotes neuronal development. Genes and Development 9, 2384-2398.
56. Romani, S., Campuzano, S., Macagno, E.R., Modollel, J., 1989. Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development. Genes and Development 3, 997-1007.
57. Romani, S., Jiménez, F., Hoch, M., Patel, N.H., Taubert, H., Jäckle, H., 1996. Krüppel, a Drosophila segmentation gene, participates in the specification of neurons and glial cells. Mechanisms of Development 60, 95-107.
58. Sander, K., 1988. Studies in insect segmentation: from teratology to phenogenetics. Development 104 (Supplement), 112-121.
59. Scholtz, G., 1990. The formation, differentiation and segmentation of the post-naupliar germ band of the amphipod Gammarus pulex L. (Crustacea, Malacostraca. Peracarida). Proceedings of the Royal Society of London B 239, 163-211.
60. Scholtz, G., 1992. Cell lineage studies in the crayfish Cherax destructor (Crustacea, Decapoda): germ band formation, segmentation and early neurogenesis. Roux's Archiv of Developmental Bioliology 202, 36-484.
61. Seitz, K.A., 1966. Normale Entwicklung des Arachniden-Embryos Cupiennius salei KEYSERLING und seine Regulationsbefähigung nach Rö ntgenbestrahlung. Zoologisches Jahrbuch der Anatomie Band 83, 327-447.
62. Skeath, J.B., 1999. At the nexus between pattern formation and cell-type specification: the generation of individual neuroblast fates in the Drosophila embryonic central nervous system. BioEssays 21, 922-931.
63. Skeath, J.B., Carroll, S.B., 1992. Regulation of proneural gene expression and cell fate during neuroblast seggrgation in the Drosophila embryo. Development 114, 939-946.
64. Skeath, J.B., Zhang, Y., Holmgren, R., Carroll, S.B., Doe, C.Q., 1995. Specification of neuroblast identity in the Drosophila embryonic central nervous system by gooseberry-distal. Nature 376, 427-430.
65. Sommer, R.J., Retzlaff. M., Goerlich, K., Sander, K., Tautz, D., 1992. Evolutionary conservation pattern of zinc finger domains of Drosophila segmentation genes. Proceedings of the National Academy of Sciences USA 89, 10782-10786.
66. Sternberg, P.W., 1993. Falling off the knife edge. Current Biology 3, 763-765.
67. Stollewerk, A., 2000. Changes in cell shape in the ventral neuroectoderm of Drosophila melanogaster depend on the activity of the achaete-scute complex genes. Development Genes and Evolution 210, 190-199.
68. Stollewerk, A., 2002. Recruitment of cell groups through Delta/Notch signalling during spider neurogenesis. Development 129, 5339-5348.
69. Stollewerk, A., Weller, M., Tautz, D., 2001. Neurogenesis in the spider Cupiennius salei. Development 128, 2673-2688.
70. Telford, M.J., Thomas, R.H., 1998. Expression of homeobox genes shows chelicerate arthropods retain their deuterocerebral segment. Proceedings of the National Academy of Sciences USA 95, 10671-10675.
71. Wegerhoff, R., Breidbach, O., 1995. Comparative aspects of the chelicerate nervous systems. In: Breidbach, O., Kutsch, W. (Eds.), The Nervous Systems of Invertebrates: an Evolutionary and Comparative Approach, pp. 159-179.
72. Weygoldt, P., 1985. Ontogeny of the Arachnid central nervous system. In: Barth, F.G., (Ed.), Neurobiology of Arachnids, Springer, Berlin, pp. 20-37.
73. Whitington, P.M., Meier, T., King, P., 1991. Segmentation, neurogenesis and formation of early axonal pathways in the centipede, Ethmostigmus rubrides (Brandt). Roux's Archiv of Developmental Biology 199, 349-363.
74. Wolf, H., Harzsch, S., 2002a. Evolution of the arthropod neuromuscular system. 1. Arrangement of muscles and innervation in the walking legs of a scorpion: Vaejovis spinigerus (Wood, 1863) Vaejovidae, Scorpiones, Arachnida. Arthropod, Structure and Development 31, 185-202.
75. Wolf, H., Harzsch, S., 2002b. Evolution of the arthropod neuromuscular system. 2. Inhibitory innervation ofn the walking legs of a scorpion: Vaejovis spinigerus (Wood, 1863) Vaejovidae, Scorpiones, Arachnida. Arthropod, Structure and Development 31, 185-202.
76. Yoshikura, M., 1955. Embryological studies on the liphistiid spider, Heptathela kimurai, part II. Kumamoto Journal of Science B 2, 1-86.
77. Zhao, G., Skeath, J.B., 2002. The Sox-domain containing gene Dichaete/fish-hook acts in concert with vnd and ind to regulate cell fate in the Drosophila neuroectoderm. Development 129, 1165-1174.