20-Hydroxyecdysone Inhibits the Mitotic Activity of
Neuronal Precursors in the Developing Mushroom
Bodies of the Honeybee, Apis mellifera
Dagmar Malun, Ariane D. Moseleit, Bernd Gru ¨ newald
Neurobiologie, Institut fu ¨ r Biologie, Freie Universita ¨ t Berlin, Ko ¨ nigin-Luise-Str. 28-30,
14195 Berlin, Germany
Received 29 January 2003; accepted 8 April 2003
ABSTRACT: The mushroom bodies (MBs) within
the brain of the honeybee, Apis mellifera, are prominent
paired neuropil structures consisting of a lateral and a
median subunit. The intrinsic MB neurons (Kenyon
cells) of each of these subunits are generated in four
distinct proliferation centers, each associated with a ca-
lyx. Previous BrdU studies revealed that neurogenesis of
Kenyon cells starts at the first larval stage (L1) by
symmetrical cell division of Kenyon precursor cells, and
ceases abruptly at a midpupal stage (P5). In the present
work, we confirmed these results using the antiphospho
histone H3 mitosis marker to label mitotically active
cells in a cell culture system, in histological sections, and
in whole-mount brain preparations. To elucidate
whether the steroid hormone ecdysone plays a role in the
termination of Kenyon cell neurogenesis, we manipu-
lated the hormone titer by injecting 20-hydroxyecdysone
(20E) into animals of those pupal stages (P0/1, P3, P4) in
which neurogenesis of Kenyon cells was still extensive.
The effects of 20E were evaluated by determining the
number of mitotically active cells in confocal micro-
scopic images of squash preparations of the MB prolif-
eration centers. In all pupal stages studied, 20E caused a
reduction of mitotic activity, indicating its involvement
in the cessation of Kenyon cell neurogenesis. © 2003
Wiley Periodicals, Inc. J Neurobiol 57: 1–14, 2003
Keywords: insect; Kenyon cells; ecdysteroid; phospho
histone H3 mitosis marker; BrdU
INTRODUCTION
Steroid hormones play a major role throughout devel-
opment and maturation of the nervous system in both
vertebrates and invertebrates (for review see Arnold
and Gorski, 1984; Weeks and Levine, 1990; Kawata,
1995; Levine et al., 1995). In rats, neurogenesis and
apoptosis are regulated by adrenal steroids in the adult
dentate gyrus (Gould and Cameron, 1996); in the
adult canary brain gonadal steroids control neurogen-
esis (Nordeen and Nordeen, 1989). Steroids also reg-
ulate the dendritic morphology of mammalian mo-
toneurons (Kurz et al., 1986). Classical steroid
hormones in insects are ecdysone and ecdysone-like
substances, which are collectively called ecdysteroids
(Ga ¨de et al., 1997). The roles played by ecdysteroids
during ontogenesis are many and diverse, including
regulation of molting in embryos, larvae, and nymphs
(Truman, 1996), and control of neuronal cell death,
cell proliferation, cellular physiology, and structural
plasticity of neuronal arbors (for review see Weeks
and Levine, 1990). As shown for the moth Manduca
sexta, ecdysteroids control neurogenesis within the
optic lobes anlagen; proliferation can be turned on and
off depending on the ecdysteroid concentration
(Champlin and Truman, 1998a,b). Also, ecdysteroids’
involvement in neuronal death was shown for
Manduca sexta (Truman and Schwartz, 1984; Fahr-
bach and Truman, 1987; Streichert et al., 1997; Hoff-
Correspondence to: D. Malun (malun@zedat.fu-berlin.de).
Contract grant sponsor: DFG; contract grant number: SFB 515
(D.M. and B.G.).
© 2003 Wiley Periodicals, Inc.
DOI 10.1002/neu.10251
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