Elsevier

Neuroscience

Volume 161, Issue 1, 16 June 2009, Pages 46-52
Neuroscience

Cellular Neuroscience
Research Paper
Bunched specifically regulates α/β mushroom body neuronal cell proliferation during metamorphosis

https://doi.org/10.1016/j.neuroscience.2009.03.054Get rights and content

Abstract

In Drosophila, mushroom bodies are centers for higher order behavior. Mushroom body neurons consist of three distinct types of neuronal cells, α, α′/β′, and α/β, which are all generated by the same neuroblasts. The mechanism by which a single neuroblast generates three different types of mushroom body neurons is a compelling area of research. Here, we report that bunched (bun) is expressed only in α/β-type mushroom body neurons and that mutation of the bun gene only affects the development of α/β neurons. Reduced bun expression causes decreased and premature arrest of neuroblast cell division, which results in reduced numbers of α/β neurons and thin axon bundled formation. We propose that bun acts as a specific factor in regulating neuroblast mitotic activity during the development of α/β neurons.

Section snippets

Fly strains

Strain P11459, a starter for P element mobilization, was obtained from the Bloomington stock center (Indiana University, Indiana, USA). P11459 has one P {EP} element (Rorth, 1996) inserted in the 18D11-12 region. w1118 Was used as a wild-type control. BL854 was used as an OK107-Gal4 driver.

Generation of mutant pools by P element–mediated mutagenesis

A P element line (P11459) that has the P element (Cooley et al., 1988) inserted in the X chromosome was used as a starter for P element mobilization. P elements were exposed to the P[Δ 2–3]99 B transposase

Isolation of a bun mutant by P element-induced mutagenesis

As climbing defects and reduced lifespan are commonly observed in fly mutants showing degeneration of adult neurons (Strauss and Heisenberg 1993, Cha et al 2005), these phenotypes are useful in identifying mutants with neuronal defects. To identify novel genes whose products function in the adult brain, we generated mutant pools and screened for locomotor defects and reduced lifespans (described in Experimental Procedures). Two mutant strains showed 30%–50% reductions in both locomotor activity

Discussion

MB neurons are all generated from four neuroblasts. The generation of each of the three types of neurons is characterized by their sequential, non-overlapping formation (Lee et al., 1999). The mechanism by which a single neuroblast generates three different types of MB neurons is a very interesting question. So far, most of the genes that have been identified as functioning in the MB are involved with all three types of neurons. bun is a unique gene, known to regulate neuroblast proliferation,

Acknowledgments

This work was supported by grant M10412000086-04N1200-08610 from the Korea Ministry of Science and Technology and R01-2006-000-10783 from the Korea Science and Engineering Foundation to J.K.-H.

References (33)

  • J.B. Connolly et al.

    Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies

    Science

    (1996)
  • L. Cooley et al.

    Insertional mutagenesis of the Drosophila genome with single P elements

    Science

    (1988)
  • J.R. Crittenden et al.

    Tripartite mushroom body architecture revealed by antigenic markers

    Learn Mem

    (1998)
  • B. Dalby et al.

    An inverse PCR screen for the detection of P element insertions in cloned genomic intervals in Drosophila melanogaster

    Genetics

    (1995)
  • G. Dietzl et al.

    A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila

    Nature

    (2007)
  • L.L. Dobens et al.

    Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary

    Development

    (2000)
  • Cited by (8)

    • Development of the Drosophila melanogaster embryonic CNS

      2020, Patterning and Cell Type Specification in the Developing CNS and PNS: Comprehensive Developmental Neuroscience, Second Edition
    • DGIPC is required for the locomotive activity and longevity in Drosophila

      2010, Biochemical and Biophysical Research Communications
      Citation Excerpt :

      In an effort to identify novel genes whose products are important for adult brain function, we performed P element mediated mutagenesis screening and isolated two mutant strains that showed about 30–50% reductions in both locomotor activity and lifespan in repeated tests. We previously reported characterization of one mutant, bunched [13]. We present the other mutant, M262, in this paper (Fig. 1A).

    • Regulating neural proliferation in the Drosophila CNS

      2010, Current Opinion in Neurobiology
      Citation Excerpt :

      MB neuroblasts generate 5-fold more neurons than most type-ID neuroblasts and do not express Pros nor require it for termination but, intriguingly, they do not appear to undergo apoptosis either [62]. These neuroblasts are also atypical in that they require the orphan nuclear receptor Tailless (Tll) and the leucine-zipper protein Bunched to maintain divisions at late stages [62,63]. Although more studies are needed, it seems that MB neuroblasts may utilise yet a third category of termination mechanism: Pros-independent cell-cycle exit.

    View all citing articles on Scopus
    1

    Two authors contributed equally.

    View full text