Multipotent neuroblasts generate a biochemical neuroarchitecture in the central complex of the grasshopper Schistocerca gregaria

Cell and Tissue Research

Volumn 340, Issue 1, 2010, Pages 13-28

  Boyan, George ^a   Williams, Leslie ^a   Herbert, Zsofia ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Brain; Lineages; Neuroblasts; Schistocerca gregaria (Insecta); Transmitters

Indexed keywords

ALLATOSTATIN; CELL PROTEIN; LEUCOKININ 1; LOCUSTATCHYKININ; SEROTONIN; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; INSECT PROTEIN; LOCUSTATACHYKININ I PROTEIN, LOCUSTA MIGRATORIA; NEUROPEPTIDE; TACHYKININ;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LINEAGE; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GRASSHOPPER; MULTIPOTENT STEM CELL; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SCHISTOCERA GREGARIA; ANIMAL; BRAIN LEVEL; BRAIN MAPPING; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PRENATAL DEVELOPMENT; SPECIES DIFFERENCE; TIME;

INSECTA; SCHISTOCERCA GREGARIA;

ANIMALS; BRAIN CHEMISTRY; BRAIN MAPPING; CELL DIFFERENTIATION; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GRASSHOPPERS; IMMUNOHISTOCHEMISTRY; INSECT PROTEINS; MICROSCOPY, CONFOCAL; MULTIPOTENT STEM CELLS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS; ORGAN CULTURE TECHNIQUES; SEROTONIN; SPECIES SPECIFICITY; TACHYKININS; TIME FACTORS;

EID: 77953464580     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-009-0922-7     Document Type: Article

References (82)

1. Antle MC, LeSauter J, Silver R (2005) Neurogenesis and ontogeny of specific cell phenotypes within the hamster suprachiasmatic nucleus. Dev Brain Res 157:8-18
2. Bentley D, Keshishian H, Shankland M, Torian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47-74
3. Bossing T, Udolph G, Doe CQ, Technau GM (1996) The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev Biol 179:41-61
4. Boyan GS, Williams JDL (1997) Embryonic development of the pars intercerebralis/central complex of the grasshopper. Dev Genes Evol 207:317-329
5. Boyan GS, Williams JL, Herbert Z (2008) An ontogenetic analysis of locustatachykinin-like expression in the central complex of the grasshopper Schistocerca gregaria. Arthropod Struct Dev 37:480-491
6. Condron BG (1999) Serotonergic neurons transiently require a midline-derived FGF signal. Neuron 24:531-540
7. Doe CQ, Goodman CS (1985a) Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111:193-205
8. Doe CQ, Goodman CS (1985b) Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev Biol 111:206-219
9. Duve H, Audsley N, Weaver RJ, Thorpe A (2000) Triple colocalisation of two types of allatostatin and an allatotropin in the frontal ganglion of the lepidopteran Lacanobia oleracea (Noctuidae): innervation and action on the foregut. Cell Tissue Res 300:153-163
10. Farris SM, Strausfeld NJ (2001) Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation. J Comp Neurol 439:331-351
11. Filla A, Hiripi L, Elekes K (2008) Role of aminergic (serotonin and dopamine) systems in the embryogenesis and different embryonic behaviors of the pond snail, Lymnaea stagnalis. Comp Biochem Physiol [C] 149:73-82
12. Gammie SC, Truman JW (1997) Neuropeptide hierarchies and the activation of sequential motor behaviors in the hawkmoth Manduca sexta. J Neurosci 17:4389-4397
13. Gaspar P, Cases O, Maroteaux L (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4:1002-1012
14. Goodman CS, Spitzer NC (1979) Embryonic development of identified neurones: differentiation from neuroblast to neurone. Nature 280:208-214
15. Goodman CS, Spitzer NC (1980) Embryonic development of neurotransmitter receptors in grasshoppers. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North-Holland Biomedical, Amsterdam, pp 195-207
16. Goodman CS, O'Shea M, McCaman R, Spitzer NC (1979) Embryonic development of identified neurons: temporal pattern of morphological and biochemical differentiation. Science 204:1219-1222
17. Goodman CS, Pearson KG, Spitzer NC (1980) Electrical excitability: a spectrum of properties in the progeny of a single embryonic neuroblast. Proc Nat Acad Sci USA 77:1676-1680
18. Heinze S, Homberg U (2008) Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511:454-478
19. Herbert Z, Rauser S, Williams L, Kapan N, Güntner, M, Walch A, Boyan G (2009) Developmental expression of neuroactive substances in the central complex of the grasshopper Schistocerca gregaria. J Comp Neurol (in press)
20. Hiripi L, S-Rozsa K (1984) Octopamine- and dopamine-sensitive adenylate cylase in the brain of Locusta migratoria during its development. Cell Mol Neurobiol 4:199-206
21. Hiripi L, S-Rozsa K, Miller TA (1979) The effect of proctolin on the adenylate and guanylate cyclases in the Locusta brain at various developmental stages. Experientia 35:1287-1288
22. Hoffmann K, Wirmer A, Kunst M, Gocht D, Heinrich R (2007) Muscarinic excitation in grasshopper song control circuits is limited by acetylcholinesterase activity. Zool Sci 24:1028-1035
23. Homberg U (1987) Structure and functions of the central complex in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and functions. Wiley, New York, pp 347-367
24. Homberg U (1991) Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303:245-254
25. Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189-209
26. Homberg U, Vitzthum H, Müller M, Binkle U (1999) Immunocyto-chemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409:495-507
27. Huber F (1960) Untersuchungen über die Funktion des Zentralner-vensystems und insbesondere des Gehirnes bei der Fortbewegung und der Lauterzeugung der Grillen. Z Vgl Physiol 44:60-132
28. Ito K, Awasaki T (2008) Clonal unit architecture of the adult fly brain. In: Technau GM (ed) Brain development in Drosophila melanogaster. Springer, New York, pp 137-158
29. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761-771
30. Jia XX, Siegler MVS (2002) Midline lineages in grasshopper produce neuronal siblings with asymmetric expression of engrailed. Development 129:5181-5193
31. Keshishian H, O'Shea M (1985) The acquisition and expression of a peptidergic phenotype in the grasshopper embryo. J Neurosci 5:1005-1015
32. Kim MY, Lee BH, Kwon D, Kang H, Nässel DR (1998) Distribution of tachykinin-related neuropeptide in the developing central nervous system of the moth Spodoptera litura. Cell Tissue Res 294:351-365
33. Kurylas A, Ott SR, Schachtner J, Elphick MR, Williams L, Homberg U (2005) Localization of nitric oxid synthase in the central complex and surrounding midbrain neuropils of the locust Schistocerca gregaria. J Comp Neurol 484:206-223
34. Lai SL, Awasaki T, Ito K, Lee T (2008) Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 135:2883-2893
35. Legl A (2009) Dynamik mitotischer und absterbender Zellen in den W-, X-, Y- und Z-Lineages des Zentralkomplexes bei Schistocerca gregaria. Ludwig-Maximilians-Universität München, Diplomarbeit
36. Ludwig P, Williams JLD, Nässel D, Reichert H, Boyan GS (2001) The primary commissure pioneers in the brain of the grasshopper Schistocerca gregaria: development ultrastructure and peptide expression. J Comp Neurol 430:118-130
37. Marder E (1999) Neural signalling: does colocalisation imply cotransmission? Curr Biol 9:809-811
38. Martin JR, Raabe T, Heisenberg M (1999) Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. J Comp Physiol [A] 185:277-288
39. Muren JE, Lundquist CT, Nässel DR (1993) Quantitative determination of myotropic neuropeptide in the nervous system of the cockroach Leucophaea maderae: distribution and release of leucokinins. J Exp Biol 179:289-300
40. Nässel DR (1993) Insect myotropic peptides: differential distribution of locustatachykinin and leucokinin-like immunoreactive neurons in the locust brain. Cell Tissue Res 274:27-40
41. Nässel DR (1994) Neuropeptides, multifunctional messengers in the nervous system of insects. Verh Deutsch Zool Ges 87:59-81
42. Nässel DR (1999) Tachykinin-related peptides in invertebrates: a review. Peptides 20:141-158
43. Nässel DR (2002) Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neuro-hormones. Prog Neurobiol 68:1-84
44. Nässel DR, Cantera R, Karlsson A (1992) Neurons in the cockroach nervous system reacting with antisera to the neuropeptide leucocinin I. J Comp Neurol 322:45-67
45. Pearson BJ, Doe CQ (2003) Regulation of neuroblast competence in Drosophila. Nature 425:624-628
46. Pereanu W, Hartenstein V (2006) Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J Neurosci 26:5534-5553
47. Persico AM, Di Pino G, Levitt P (2006) Multiple receptors mediate the trophic effects of serotonin on ventroposterior thalamic neurons in vitro. Brain Res 1095:17-25
48. Pflüger HJ, Stevenson PA (2005) Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34:379-396
49. Reichert H, Boyan GS (1997) Building a brain: insights from insects. Trends Neurosci 20:258-264
50. Renn SCN, Armstrong JD, Yang M, Wang Z, An X, Kaiser K, Taghert PH (1999) Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J Neurobiol 41:189-207
51. Roeder T (2002) Biochemistry and molecular biology of receptors for biogenic amines in locusts. Microsc Res Tech 56:237-247
52. Romeuf M, Rémy C (1984) Early immunohistochemical detection of somatostatin-like and methionine-enkephalin-like neuropeptides in the brain of the migratory locust embryo. Cell Tissue Res 236:289-292
53. Schoofs L, Veelaert D, Vanden Broeck J, De Loof A (1997) Peptides in the locusts, Locusta migratoria and Schistocerca gregaria. Peptides 18:145-156
54. Seeger M, Tear G, Ferres-Marco D, Goodman CS (1993) Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409-426
55. Seidel C, Bicker G (1996) The developmental expression of serotonin-immunoreactivity in the brain of the pupal honeybee. Tissue Cell 28:663-672
56. Seidel C, Bicker G (2002) Developmental expression of nitric oxide/cyclic GMP signaling pathways in the brain of the embryonic grasshopper. Dev Brain Res 138:71-79
57. Siegl T, Schachtner J, Holstein GR, Homberg U (2009) NO/cGMP signalling: L-citrulline and cGMP immunostaining in the central complex of the desert locust Schistocerca gregaria. Cell Tissue Res 337:327-340
58. Stern M, Knipp S, Bicker G (2007) Embryonic differentiation of serotonin-containing neurons in the enteric nervous system of the locust (Locusta migratoria). J Comp Neurol 501:38-51
59. Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
60. Strausfeld NJ (1996) Ancient structures in modern brains: insect phylogeny from the nervous system. Proceedings of the XX International Congress of Entomology, Florence, p 197
61. Strausfeld NJ (1998) Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol 52:186-206
62. Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633-638
63. Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852-1861
64. Sykes PA, Condron BG (2005) Development and sensitivity to serotonin of Drosophila serotonergic varicosities in the central nervous system. Dev Biol 286:207-216
65. Taghert PH, Goodman CS (1984) Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. J Neurosci 4:989-1000
66. Taghert PH, Truman JW (1982a) The distribution and molecular characeristics of the tanning hormone, bursicon, in the tobacco hornmoth, Manduca sexta. J Exp Biol 98:373-383
67. Taghert PH, Truman JW (1982b) Identification of the bursicon-containing neurons in abdominal ganglia of the tobacco horn-worm moth, Manduca sexta. J Exp Biol 98:385-401
68. Thompson KSJ, Rayne RC, Gibbon CR, May ST, Patel M, Coast GM, Bacon JP (1995) Cellular colocalization of diuretic peptides in locusts: a potent control mechanism. Peptides 16:95-104
69. Turlejski K (1996) Evolutionary ancient roles of serotonin: long-lasting regulation of activity and development. Acta Neurobiol Exp 56:619-636
70. Udolph G, Prokop A, Bossing T, Techanu GM (1993) A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants. Development 118:765-775
71. Vitalis T, Cases O, Passemard S, Callebert J, Parnavelas JG (2007) Embryonic depletion of serotonin affects cortical development. Eur J Neurosci 26:331-344
72. Vitzthum H, Homberg U (1998) Immunocytochemical demonstration of locustatachykinin-related peptides in the central complex of the locust brain. J Comp Neurol 390:455-469
73. Vitzthum H, Homberg U, Agricola H (1996) Distribution of Dip-allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. J Comp Neurol 369:419-437
74. Wegerhoff R, Breidbach O (1992) Structure and development of the larval central complex in a holometabolous insect, the beetle Tenebrio molitor. Cell Tissue Res 268:341-358
75. Wegerhoff R, Breidbach O, Lobemeier M (1996) Development of locustatachykinin immunopositive neurons in the central complex of the beetle Tenebrio molitor. J Comp Neurol 375:157-166
76. Weinrich A, Kunst M, Wirmer A, Holstein GR, Heinrich R (2008) Suppression of grasshopper sound production by nitric oxide-releasing neurons of the central complex. J Comp Physiol [A] 194:763-776
77. Wenzel B, Kunst M, Günther C, Ganter GK, Lakes-Harlan R, Elsner N, Heinrich R (2005) Nitric oxide/cyclic guanosine monophosphate signalling in the central complex of the grasshopper brain inhibits singing behavior. J Comp Neurol 488:129-139
78. Whitaker-Azmitia PM (2001) Serotonin and brain development: role in human developmental diseases. Brain Res Bull 56:479-485
79. Williams JLD (1975) Anatomical studies of the insect central nervous system: a ground-plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool Lond 176:67-86
80. Williams JLD, Guentner M, Boyan GS (2005) Building the central complex of the grasshopper Schistocerca gregaria: temporal topology organizes the neuroarchitecture of the w, x, y, z tracts. Arthropod Struct Dev 34:97-110
81. Winther AM, Acebes A, Ferrus A (2006) Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31:399-406
82. Zacharias D, Williams JLD, 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