Spatial and temporal pattern of neuroblasts, proliferation, and Engrailed expression during early brain development in Tenebrio molitor L. (Coleoptera)

Arthropod Structure and Development

Volumn 32, Issue 1, 2003, Pages 125-140

  Urbach, Rolf ^a   Technau, Gerhard M ^a   Breidbach, Olaf ^b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Antennal lobe; Head segmentation; Insect; Mushroom body neuroblast; Neurogenesis; Segment polarity gene

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; EARLY DIAGNOSIS; EMBRYO; EMBRYO DEVELOPMENT; HEMISPHERE; MITOSIS; NEUROBLAST; NONHUMAN; SPATIAL AUTOCORRELATION ANALYSIS; STATISTICAL SIGNIFICANCE; TENEBRIO; TENEBRIO MOLITOR;

BASIDIOMYCOTA; COLEOPTERA; HEXAPODA; INSECTA; TENEBRIO MOLITOR;

EID: 0141858712     PISSN: 14678039     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1467-8039(03)00043-4     Document Type: Article

References (90)

1. Abrams, J.M., White, K., Fessler, L.I., Steller, H., 1993. Programmed cell death during Drosophila embryogenesis. Development 117, 29-43.
2. 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 Science in USA 96, 10224-10229.
3. Abzhanov, A., Kaufman, T.C., 2000. Evolution of distinct expression patterns for engrailed paralogues in higher crustaceans (Malacostraca). Development, Genes and Evolution 210, 493-506.
4. Bate, M., 1976. Embryogenesis of an insect nervous system. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. Journal of Embryology and Experimental Morphology 35, 107-123.
5. Bauer, A., 1904. Zur inneren Metamorphose des Zentralnervensystems der Insekten. Zoologisches Jahrbuch der Abteilung Anatomie und Ontogenie der Tiere 20, 317-330.
6. Boyan, G.S., Williams, J.L.D., 1997. Embryonic development of the pars intercerebralis/central complex of the grasshopper. Development, Genes and Evolution 207, 317-329.
7. Boyan, G.S., Williams, J.L.D., 2000. Building the antennal lobe: engrailed expression reveals a contribution from protocerebral neuroblasts in the grasshopper Schistocerca gregoria. Arthropod Structure and Development 29, 267-274.
8. Boyan, G.S., Williams, J.L.D., 2002. A single cell analysis of engrailed in the early embryonic brain of the grasshopper Schistocerca gregaria: ontogeny and identity of the secondary head spot cells. Arthropod Structure and Development 30, 207-218.
9. Boyan, G.S., Therianos, S., Williams, J.L.D., Reichert, H., 1995a. Axogenesis in the embryonic brain of the grasshopper Schistocerca gregaria: an identified cell analysis of early brain development. Development 121, 75-86.
10. Boyan, G.S., Williams, J.L.D., Reichert, H., 1995b. Morphogenetic reorganization of the brain during embryogenesis in the grasshopper. Journal of Comparative Neurology 361, 429-440.
11. Boyan, G.S., Williams, J.L.D., Posser, S., Bräunig, P., 2002. Morphological and molecular data argue for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the locust. Arthropod Structure and Development 31, 65-76.
12. Breidbach, O., Urbach, R., 1996. Embryonic and postembryonic development of serial homologous neurons in the subesophageal ganglion of Tenebrio molitor (Insecta: Coleoptera). Microscopy Research and Technique 35, 180-200.
13. Brown, S.J., Patel, N.H., Denell, R.E., 1994. Embryonic expression of the single Tribolium engrailed homolog. Developmental Genetics 15, 7-18.
14. Bullock, T.H., Horridge, G.A., 1965. Structure and function in the nervous system of invertebrates, Freeman, San Francisco.
15. Campos-Ortega, J.A., Hartenstein, V., 1985. In: Kerkut, G.A., Gilbert, L.I. (Eds.), Development of the nervous system, Comprehensive Insect Physiology, Biochemistry, and Pharmacology, vol. 5. Pergamon press, Oxford, pp. 49-84.
16. Campos-Ortega, J.A., Hartenstein, V., 1997. The embryonic development of Drosophila. melanogaster, Springer, Berlin.
17. Cayre, M., Strambi, C., Charpin, P., Augier, R., Meyer, M.R., Edwards, J.S., Strambi, A., 1996. Neurogenesis in adult insect mushroom bodies. Journal of Comparative Neurology 371, 300-310.
18. Chaudonneret, J. 1987. Evolution of the insect brain, with special reference to the so-called tritocerebrum, In: Gupta, A.P., (Ed.), Arthropod brain, Wiley, New York, pp. 3-26.
19. Cohen, S.M., Jürgens, G., 1990. Mediation of Drosophila head development by gap-like segmentation genes. Nature 346, 482-485.
20. Diederich, R.J., Pattatucci, A.M., Kaufman, T.C., 1991. Developmental and evolutionary implications of labial, Deformed and engrailed expression in the Drosophila head. Development 113, 273-281.
21. DiNardo, S., Kuner, J.M., Theis, J., O'Farrell, P.H., 1985. Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell 43, 59-69.
22. Doe, C.Q., Goodman, C.S., 1985. Early events in insect neurogenesis I. Development and segmental differences in the pattern of neuronal precursor cells. Developmental Biology 111, 193-205.
23. Dumstrei, K., Nassif, C., Abboud, G., Aryai, A., Hartenstein, V., 1998. EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head. Development 125, 3417-3426.
24. Dumstrei, K., Wang, F., Nassif, C., Hartenstein, V., 2003. Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. Journal of Comparative Neurology 455, 451-462.
25. Fleig, R., 1994. Head segmentation in the embryo of the Colorado beetle Leptinotarsa decemlineata as seen with anti-en immunostaining. Roux's Archives of Developmental Biology 203, 227-229.
26. Haas, M.S., Brown, S.J., Beeman, R.W., 2001. Pondering the procephalon: the segmental origin of the labrum. Development, Genes and Evolution 211, 89-95.
27. Hartenstein, V., Campos-Ortega, J.A., 1984. Early neurogenesis in wild-type Drosophila melanogaster. Roux's Archives of Developmental Biology 193, 308-325.
28. Hartenstein, V., Nassif, C., Lekven, A., 1998. Embryonic development of the Drosophila brain. II. Pattern of glial cells. Journal of Comparative Neurology 402, 32-47.
29. Hartmann, B., Reichert, H., 1998. The genetics of embryonic brain development in Drosophila., Molecular and Cellular Neurocience 12, 194-205.
30. Hartmannm, B., Hirth, F., Walldorf, U., Reichert, H., 2000. Expression, regulation and function of the homeobox gene empty spiracles in brain and ventral nerve cord development of Drosophila. Mechanisms of Development 90, 143-153.
31. Harzsch, S., Miller, J., Benton, J., Dawirs, R.R., Beltz, B., 1998. Neurogenesis in the thoracic neuromeres of two crustaceans with different types of metamorphic development. Journal of Experimental Biology 201, 2465-2479.
32. Harzsch, S., Miller, J., Benton, J., Beltz, B., 1999. From embryo to adult: persistent neurogenesis and apoptotic cell death shape the lobster deutocerebrum. Journal of Neuroscience 19, 3472-3485.
33. Hirth, F., Therianos, S., Loop, T., Gehring, W.J., Reichert, H., Furukubo-Tokunaga, K., 1995. Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron 15, 769-778.
34. Hirth, F., Hartmann, B., Reichert, H., 1998. Homeotic gene action in embryonic brain development of Drosophila. Development 125, 1579-1589.
35. Hirth, F., Loop, T., Egger, B., Miller, D.F., Kaufman, T.C., Reichert, H., 2001. Functional equivalence of Hox gene products in the specification of the tritocerebrum during embryonic brain development of Drosophila. Development 128, 4781-4788.
36. Ito, K., Hotta, Y., 1992. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Developmental Biology 149, 134-148.
37. Johansson, A.S., 1957. The nervous system of the milkweed bug. Oncopeltus fasciatus (Dallas) (Heteroptera, Lygaeidae). Transactions of the American Entomological Society 83, 119-183.
38. Jürgens, G., Hartenstein, V., 1993. The terminal regions of the body pattern. In: Bate, C.M., Martinez-Arias, A. (Eds.), The development of Drosophila melanogaster, Cold Spring Harbor Laboratory press, Cold Spring Harbor, pp. 687-746.
39. Kornberg, T., Siden, I., O'Farrell, P., Simon, M., 1985. The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40, 45-53.
40. Kurusu, M., Nagao, T., Walldorf, U., Flister, S., Gehring, W.J., Furukubo-Tokunaga, K., 2000. Genetic control of development of the mushroom bodies, the associative learning centers in the Drosophila brain, by the eyeless, twin of eyeless, and dachshund genes. Proceedings of the National Academy of Science in USA 97, 2140-2144.
41. Kurusu, M., Awasaki, T., Masuda-Nakagawa, L.M., Kawauchi, H., Ito, K., Furukubo-Tokunaga, K., 2002. Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of Fasciclin II. Development 129, 409-419.
42. Ludwig, P., Williams, J.L.D., Lodde, E., Reichert, H., Boyan, G.S., 1999. Neurogenesis in the median domain of the embryonic brain of the grasshopper Schistocerca gregaria. Journal of Comparative Neurology 414, 379-390.
43. Malzacher, P., 1968. Die Embryogenese des Gehirns paurometaboler Insekten. Untersuchungen an Carausius morosus und Periplaneta americana. Zeitschrift für Morphologie der Tiere 62, 103-161.
44. Nassif, C., Daniel, A., Lengyel, J.A., Hartenstein, V., 1998a. The role of morphogenetic cell death during Drosophila embryonic head development. Developmental Biology 197, 170-186.
45. Nassif, C., Noveen, A., Hartenstein, V., 1998b. Embryonic development of the Drosophila brain. I. Pattern of pioneer tracts. Journal of Comparative Neurology 402, 10-31.
46. Nassif, C., Noveen, A., Hartenstein, V., 2003. Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. Journal of Comparative Neurology 455, 417-434.
47. Noveen, A., Daniel, A., Hartenstein, V., 2000. Early development of the Drosophila mushroom body: the roles of eyeless and dachshund. Development 127, 3475-3488.
48. Panov, A.A., 1957. The structure of the brain in insects in successive stages of postembryonic development. Ent. Obozr. 36, 269-284.
49. Patel, N.H., Kornberg, T.B., Goodman, C.S., 1989a. Expression of engrailed during segmentation in grasshopper and crayfish. Development 107, 201-212.
50. Patel, N.H., Martin-Blanco, E., Coleman, K.G., Poole, S.J., Ellis, M.C., Kornberg, T.B., Goodman, C.S., 1989b. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
51. Patel, N.H., Condron, B.G., Zinn, K., 1994. Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367, 429-434.
52. Popadic, A., Panganiban, G., Rusch, D., Shear, W.A., Kaufman, T.C., 1998. Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Development, Genes and Evolution 208, 142-150.
53. Poulson, D.S., 1950. Histogenesis, organogenesis and differentiation in the embryo of Drosophila melanogaster Meigen. In: Demerec, M., (Ed.), Biology of Drosophila, Wiley, New York, pp. 168-274.
54. Prokop, A., Technau, G.M., 1991. The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111, 79-88.
55. Prokop, A., Technau, G.M., 1994. Normal function of the mushroom body defect gene of Drosophila is required for the regulation of the number and proliferation of neuroblasts. Developmental Biology 161, 321-337.
56. Prpic, N.-M., Wigand, B., Damen, W.G.M., Klingler, M., 2001. Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates seriel homologies in insect appendages. Development, Genes and Evolution 2001, 467-477.
57. Pusey, H.K., 1939. Methods of reconstruction from microscopic sections. J. R. Microsc. Sci. 59, 232-244.
58. Reichert, H., 2002. Conserved genetic mechanisms for embryonic brain patterning. International Journal of Developmental Biology 46, 81-87.
59. Reichert, H., Boyan, G.S., 1997. Building a brain: developmental insights in insects. Trends in Neurosciences 20, 258-264.
60. Rempel, J.G., 1975. The evolution of the insect head: an endless dispute. Quaestiones Entomologicae 11, 7-25.
61. Rempel, J.G., Church, N.S., 1969. The embryology of Lytta viridana Le Conte (Coleoptera): Meloidae. V. The blastoderm, germ layers and body segments. Canadian Journal of Zoology 47, 1157-1171.
62. Rempel, J.G., Church, N.S., 1971. The embryology of Lytta viridana Le Conte (Coleoptera): Meloidae. VII. Eighty-eight to 132 h: the appendages, the cephalic apodemes, and head segmentation. Canadian Journal of Zoology 49, 1571-1581.
63. Rogers, B.T., Kaufman, T.C., 1996. Structure of the insect head as revealed by the EN protein pattern in developing embryos. Development 122, 3419-3432.
64. Rogers, B.T., Kaufman,T.C., 1997. Structure of the insect head in ontogeny and phylogeny: a view from Drosophila. International Review of Cytology 174, 1-84.
65. Rudolph, K.M., Liaw, G.J., Daniel, A., Green, P., Courey, A.J., Hartenstein, V., Lengyel, J.A., 1997. Complex regulatory region mediating tailless expression in early embryonic patterning and brain development. Development 124, 4297-4308.
66. Schmidt-Ott, U., Technau, G.M., 1992. Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. Development 116, 111-125.
67. Schmidt-Ott, U., Gonzalez-Gaitan, M., Jäckle, H., Technau, G.M., 1994a. Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proceedings of the National Academy of Science in USA 91, 8363-8367.
68. Schmidt-Ott, U., Sander, K., Technau, G.M., 1994b. Expression of engrailed in embryos of a beetle and five dipteran species with special reference to the terminal regions. Roux's Archives of Developmental Biology 203, 298-303.
69. Schmidt-Ott, U., Gonzalez-Gaitan, M., Technau, G.M., 1995. Analysis of neural elements in the head-mutant Drosophila embryos suggests a segmental origin of the optic lobes. Roux's Archives of Developmental Biology 205, 31-44.
70. Scholtz, G., 1995. Head segmentation in Crustacea-an immunocytochemical study. Zoology 98, 104-114.
71. Scholtz, G., 1998. Cleavage, germ band formation and head segmentation: the ground pattern of the Euarthropoda. In: Fortey, R.A., Thomas, R.H. (Eds.), Arthropod Relationships, Chapman and Hall, London, pp. 317-332.
72. Schrader, K., 1938. Untersuchungen über die Normalentwicklung des Gehirns und Gehirnexplantationen bei der Mehlmotte Ephestia kühniella Zeller. Biologisches Zentralblatt 58, 52-90.
73. Shepherd, D., Bate, M.C., 1990. Spatial and temporal patterns of neurogenesis in the embryo of the locust (Schistocerca gregaria). Development 108, 83-96.
74. Stanley, M.S.M., Grundmann, A.W., 1970. The embryonic development of Tribolium confusum. Annals of the Entomological Society of America 63, 1248-1256.
75. Stocker, R.F., Tissot, M., Gendre, N., 1995. Morphogenesis and cellular proliferation pattern in the developing antennal lobe of Drosophila melanogaster. Roux's Archives of Developmental Biology 205, 62-72.
76. Therianos, S., Leuzinger, S., Hirth, F., Goodman, C.S., Reichert, H., 1995. Embryonic development of the Drosophila brain: formation of commissural and descending pathways. Development 121, 3849-3860.
77. Ullman, S.L., 1964. The origin and structure of the mesoderm and the formation of the coelomic sacs in Tenebrio molitor L., (Insecta, Coleoptera). Philosophical Transactions of the Royal Society (London) B 248, 245-277.
78. Ullman, S.L., 1967. The development of the nervous system and other ectodermal derivatives in Tenebrio molitor L., Insecta. Coleoptera. Philosophical Transactions of the Royal Society (London) B 252, 1-25.
79. Urbach, R., Technau, G.M., 2003a. Early steps in building the insect brain: Neuroblast formation and segmental patterning in the developing brain of different insect species. Arthropod Structure and Development in press.
80. Urbach, R., Technau, G.M., 2003b. Segment polarity and D/V patterning gene expression reveals segmental organization of the Drosophila brain. Development, 130, 3607-3620.
81. Urbach, R., Technau, G.M., 2003c. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development, 130, 3621-3637.
82. Urbach, R., Schnabel, R., Technau, G.M., 2003. The pattern of neuroblast formation, mitotic domains, and proneural gene expression during early brain development in Drosophila. Development, 130, 3589-3606.
83. Wheeler, WM., 1891. Neuroblasts in the arthropod embryo. Journal of Morphology 4, 337-343.
84. Wheeler, W.C., Whiting, M., Wheeler, Q.D., Carpenter, J.M., 2001. The phylogeny of the extant hexapod orders. Cladistics 17, 113-169.
85. Younossi-Hartenstein, A., Tepass, U., Hartenstein, V., 1993. Embryonic origin of the imaginal discs of the head of Drosophila melanogaster. Roux's Archives of Developmental Biology, 1-14.
86. Younossi-Hartenstein, A., Nassif, C., Green, P., Hartenstein, V., 1996. Early neurogenesis of the Drosophila brain. Journal of Comparative Neurology 370, 313-329.
87. Younossi-Hartenstein, A., Green, P., Liaw, G.J., Rudolph, K., Lengyel, J., Hartenstein, V., 1997. Control of early neurogenesis of the Drosophila brain by the head gap genes tll, otd, ems, and btd. Developmental Biology 182, 270-283.
88. Younossi-Hartenstein, A., Salvaterra, P.M., Hartenstein, V., 2003. Early development of the Drosophila brain: IV. Larval neuropile compartments defined by glial septa. Journal of Comparative Neurology 455, 435-450.
89. Zacharias, D., Williams, J.L.D., Meier, T., Reichert, H., 1993. Neurogenesis in the insect brain: cellular identification and molecular characterization of brain neuroblasts in the grasshopper embryo. Development 118, 941-955.
90. Zachäus, T., Breidbach, O., 1991. In: Elsner, N., Penzlin, H. (Eds.), Neuroblasts proliferate in the adult insect brain, Tenebrio molitor L., Insecta, Coleoptera, Proceedings of the 19th Göttingen Neurobiology Conference, Thieme, Stuttgart, p. 510.