Skip to main content
Log in

Glia associated with central complex lineages in the embryonic brain of the grasshopper Schistocerca gregaria

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

We have investigated the pattern of glia associated with central complex lineages in the embryonic brain of the grasshopper Schistocerca gregaria. Using the glia-specific marker Repo, we identified glia associated externally with such lineages, termed lineage-extrinsic glia, and glia located internally within the lineages, termed lineage-intrinsic glia. Populations of both glial types increase up to 60 % of embryogenesis, and thereafter decrease. Extrinsic glia change their locations over time, while intrinsic ones are consistently found in the more apical part of a lineage. Apoptosis is not observed for either glial type, suggesting migration is a likely mechanism accounting for changes in glial number. Proliferative glia are present both within and without individual lineages and two glial clusters associated with the lineages, one apically and the other basally, may represent sources of glia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abrams JM, White K, Fessler LI, Steller H (1993) Programmed cell death during Drosophila embryogenesis. Development 117:29–43

    PubMed  CAS  Google Scholar 

  • Adams RR, Maiato H, Earnshaw WC, Carmena M (2001) Essential Roles of Drosophila Inner Centromere Protein (INCENP) and Aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J Cell Bio 153(4):865–879

    Article  CAS  Google Scholar 

  • Akiyama Y, Hosoya T, Poole AM, Hotta Y (1996) The gcm-motif: a novel DNA-binding motif conserved in Drosophila and mammals. Proc Natl Acad Sci USA 93:14912–14916

    Article  PubMed  CAS  Google Scholar 

  • Awasaki T, Lai S-L, Ito K, Lee T (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28:13742–13753

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Boyan G, Williams L (2011) Embryonic development of the insect central complex: insights from lineages in the grasshopper and Drosophila. Arthr Struct Dev 40(4):334–348

    Google Scholar 

  • Boyan GS, Reichert H (2011) Mechanisms for complexity in the brain: generating the insect central complex. Trends Neurosci 34(5):247–257

    Article  PubMed  CAS  Google Scholar 

  • Boyan G, Williams L, Meier T (1993) Organization of the commissural fibers in the adult brain of the locust. J Comp Neurol 332:358–377

    Article  PubMed  CAS  Google Scholar 

  • Boyan GS, Therianos S, Williams JLD, Reichert H (1995) Axogenesis in the embryonic brain of the grasshopper Schistocerca gregaria: an identified cell analysis of early brain development. Development 121:75–86

    PubMed  CAS  Google Scholar 

  • Boyan G, Richert H, Hirth F (2003) Commissure formation in the embryonic insect brain. Arthr Struct Dev 32:61–77

    Article  Google Scholar 

  • Boyan G, Herbert Z, Williams L (2010a) Cell death shapes embryonic lineages of the central complex in the grasshopper Schistocerca gregaria. J Morphol 271:949–959

    PubMed  Google Scholar 

  • Boyan GS, Williams L, Legl A, Herbert Z (2010b) Proliferative cell types in embryonic lineages of the central complex of the grasshopper Schistocerca gregaria. Cell Tissue Res 341:259–277

    Article  PubMed  Google Scholar 

  • Boyan G, Loser M, Williams L, Liu Y (2011) Astrocyte-like glia associated with the embryonic development of the central complex in the grasshopper Schistocerca gregaria. Dev Genes Evol 221:141–155

    Article  PubMed  Google Scholar 

  • Boyan G, Liu Y, Loser M (2012) A cellular network of dye-coupled glia associated with the embryonic central complex in the grasshopper Schistocerca gregaria. Dev Genes Evol 222:125–138

    Article  PubMed  CAS  Google Scholar 

  • Bravo R, Celis JE (1980) A search for differential polypeptide synthesis throughout the cell cycle of Hela cells. J Cell Biol 84:795–802

    Article  PubMed  CAS  Google Scholar 

  • Bravo R, Macdonald-Bravo H (1987) Existence of two populations of Cyclin/Proliferating Cell Nuclear Antigen during the cell cycle: association with DNA replication sites. J Cell Biol 105:1549–1554

    Article  PubMed  CAS  Google Scholar 

  • Cayre M, Strambi C, Charpin P, Augier R, Meyer MR, Edwards JS, Strambi A (1996) Neurogenesis in adult insect mushroom bodies. J Comp Neurol 371:300–310

    Article  PubMed  CAS  Google Scholar 

  • Celis JE, Celis A (1985) Cell cycle-dependent variatioins in the distribution of the nuclear protein cyclin proliferating cell nuclear antigen in cultured cells: subdivision of S phase. Proc Natl Acad Sci USA 82:3262–3266

    Article  PubMed  CAS  Google Scholar 

  • Celis JE, Madsen P, Celis A, Nielsen HV, Gesser B (1987) Cyclin (PCNA, auxiliary protein of DNA polymerase delta) is a central component of the pathway(s) leading to DNA replication and cell division. FEBS Lett 220(1):1–7

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Edwards TN, Meinertzhagen IA (2010) The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol 90:471–497

    Article  PubMed  CAS  Google Scholar 

  • Egger B, Leemans R, Loop T, Kammermeier L, Fan Y, Radimerski T, Strahm MC, Certa U, Reichert H (2002) Gliogenesis in Drosophila: genome-wide analysis of downstream genes of glial cells missing in the embryonic nervous system. Development 129:3295–3309

    PubMed  CAS  Google Scholar 

  • el Jundi B, Heinze S, Lenschow C, Kurylas A, Rohlfing T, Homberg U (2010) The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front Syst Neurosci 3:21

    PubMed  Google Scholar 

  • Fairman MP (1990) DNA polymerase delta/PCNA: actions and interactions. J Cell Sci 95:1–4

    PubMed  CAS  Google Scholar 

  • Gocht D, Wagner S, Heinrich R (2009) Recognition, presence, and survival of locust central nervous glia in situ and in vitro. Microsc Res Tech 72(5):385–397

    Article  PubMed  Google Scholar 

  • Haase A, Stern M, Wachtler K, Bicker G (2001) A tissue-specific marker of Ecdysozoa. Dev Genes Evol 211:428–433

    Article  PubMed  CAS  Google Scholar 

  • Hähnlein I, Bicker G (1997) Glial patterning during postemebryonic development of central neuropiles in the brain of the honeybee. Dev Genes Evol 207:29–41

    Article  PubMed  Google Scholar 

  • Hall PA, Levison DA, Woods AL, Yu CC-W, Kellock DB, Watkins JA, Barnes DM, Gillett CE, Camplejohn R, Dover R, Waseem NH, Lane DP (1990) Proliferating cell nuclear antigen (PCNA) immunolocalization in paraffin sections: an index of cell proliferation with evidence of deregulated expression in some neoplasms. J Pathol 162:285–294

    Article  PubMed  CAS  Google Scholar 

  • Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, Technau GM (1995) The homeobox gene repo is required for the differentiation and maintenance of glial function in the embryonic nervous system of Drosophila melanogaster. Development 121:317–322

    PubMed  CAS  Google Scholar 

  • Hartenstein V (2011) Morphological diversity and development of glia in Drosophila. Glia 59:1237–1252

    Article  PubMed  Google Scholar 

  • Hartenstein V, Nassif C, Lekven A (1998) Embryonic development of the Drosophila brain: II. Pattern of glia cells. J Comp Neurol 402:32–47

    Article  PubMed  CAS  Google Scholar 

  • Heinze S, Homberg U (2007) Maplike representation of celestial e-vector orientations in the brain of an insect. Science 315:995–997

    Article  PubMed  CAS  Google Scholar 

  • Hendzel MJ, Wei Y, Mancini MA, Hooser AV, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Izergina N, Balmer J, Bello B, Reichert H (2009) Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev 4:44

    Article  PubMed  Google Scholar 

  • Jan LY, Jan YN (1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc Natl Acad Sci USA 79:2700–2704

    Article  PubMed  CAS  Google Scholar 

  • Jiang C, Baehrecke EH, Thummel CS (1987) Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124:4673–4683

    Google Scholar 

  • Liu G, Seiler H, Wen A, Zars T, Ito K, Wolf M, Heisenberg M, Liu L (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439:551–556

    Article  PubMed  CAS  Google Scholar 

  • Naimski P, Bierzyimageski A, Fikus M (1980) Quantitative fluorescent analysis of different conformational forms of DNA bound to the dye 4′,6-diamidine-2-phenylindole, and separated by gel electrophoresis. Anal Biochem 106:471–475

    Article  PubMed  CAS  Google Scholar 

  • Neuser K, Triphan T, Mronz M, Poeck B, Strauss R (2008) Analysis of a spatial orientation memory in Drosophila. Nature 453:1244–1247

    Article  PubMed  CAS  Google Scholar 

  • Ng L, Prelich G, Anderson CW, Stillman B, Fisher PA (1990) Drosophila proliferating cell nuclear antigen. J Biol Chem 266(20):11948–11954

    Google Scholar 

  • Nordlander RH, Edwards JS (1969) Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus, L.: I. Cellular events during brain morphogenesis. Wilh Roux´Archiv 162:197–217

    Article  Google Scholar 

  • Oland LA, Tolbert LP (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2(1):10–24

    Article  PubMed  CAS  Google Scholar 

  • Paschinger K, Rendic D, Wilson IBH (2009) Revealing the anti-HRP epitope in Drosophila and Caenorhabditis. Glycoconj J 26:385–395

    Article  PubMed  CAS  Google Scholar 

  • Pereanu W, Shy D, Hartenstein V (2005) Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 283:191–203

    Article  PubMed  CAS  Google Scholar 

  • Seaver EC, Carpenter EM, Bastiani MJ (1993) Glial cells in the development of the nervous system: developmental expression and molecular characterization of REGA-1 in grasshoppers. Neurosci Abstr 19:266

    Google Scholar 

  • Shreeram S, Blow JJ (2003) The role of the replication licensing system in cell proliferation and cancer. Prog Cell cycle Res 5:287–293

    PubMed  CAS  Google Scholar 

  • Spreij THE (1971) Cell death during the development of the imaginal disks of Calliphora erythrocephala. Netherland J Zool 21(3):221–264

    Article  Google Scholar 

  • Stacey SM, Muraro NI, Peco E, Labbe A, Thomas GB, Baines RA, van Meyel DJ (2010) Drosophila glial glutamate transporter Eaat1 is regulated by fringe-mediated Notch signaling and is essential for larval locomotion. J Neuro 30(43):14446–14457

    Article  CAS  Google Scholar 

  • Stork T, Bernardos R, Freeman MR (2012) Analysis of glial cell development and function in Drosophila. Cold Spring Harb Protoc. doi:10.1101/pdb.top067587

  • Strausfeld NJ (2009) Brain organization and the origin of insects: an assessment. Proc Biol Sci 276(1664):1929–1937

    Article  PubMed  Google Scholar 

  • Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638

    Article  PubMed  CAS  Google Scholar 

  • Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters J-M (2000) Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol 151(4):749–761

    Article  PubMed  CAS  Google Scholar 

  • Takizawa T, Meshorer E (2008) Chromatin and nuclear architecture in the nervous system. Trends Neurosci 31(7):343–352

    Article  PubMed  CAS  Google Scholar 

  • Vanhems E (1985) An in vitro autoradiographic study of gliogenesis in the embryonic locust brain. Dev Brain Res 23:269–275

    Article  Google Scholar 

  • Viktorin G, Riebli N, Popkova A, Giangrande A, Reichert H (2011) Multipotent neural stem cells generate glial cells of the central complex through transit amplifying intermediate progenitors in Drosophila brain development. Dev Biol 356:553–565

    Article  PubMed  CAS  Google Scholar 

  • 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. Arthr Struct Dev 34:97–110

    Article  Google Scholar 

  • Xiong W, Okano H, Patel N, Blendy J, Montell C (1994) Repo endodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev 8:981–994

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi M, Date T, Matsukage A (1991) Distribution of PCNA in Drosophila embryo during nuclear division cycles. J Cell Sci 100:729–733

    PubMed  Google Scholar 

  • Yamaguchi M, Nishimoto Y, Hirose F, Matsukage A (1995) Distribution of PCNA during postblastoderm cell division cycles in the Drosophila melanogaster embryo: effect of a string- mutation. Cell Struc Funct 20:47–57

    Article  CAS  Google Scholar 

  • Zacharias D, Williams JLD, Meier T, Reichert H (1993) Neurogenesis in the insect brain: cellular identification and molecular characterization of brain neuro- blasts in the grasshopper embryo. Development 118:941–955

    Google Scholar 

  • Zudaire E, Simpson SJ, Illa I, Montuenga LM (2004) Dietary influences over proliferating cell nuclear antigen expression in the locust midgut. J Exp Biol 207:2255–2265

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Drs. G. Technau (Repo) and M. Wullimann (PCNA) for their gifts of antibodies, Michael Loser for critical comments, and Karin Fischer for excellent technical assistance. Grant sponsor: Deutsche Forschungsgemeinschaft (BO 1434/3-5).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu Liu.

Additional information

Communicated by: Siegfried Roth

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Y., Boyan, G. Glia associated with central complex lineages in the embryonic brain of the grasshopper Schistocerca gregaria . Dev Genes Evol 223, 213–223 (2013). https://doi.org/10.1007/s00427-013-0439-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-013-0439-7

Keywords

Navigation