hikaru genki


DEVELOPMENTAL BIOLOGY

Embryonic

Messenger RNA is detected in 8-16 hour embryos and is abundant at 16-24 hours. Expression is first detected in the head region of stage 10 embryos. Expression is observed in several cylindrical cells, some segregating from the surface in the procephalic neurogenic region. In stage 14 embryos, transcripts accumulate in several clusters of cells in each of the hemispheres of the brain and persist until later stages. In the ventral cord, expression starts at stage 11. In stage 13 embryos, a pair of cells on both sides of the midline in each segment and an additional pair on the lateral-most edge contain HIG mRNA. Slightly older embryos begin expressing mRNA in another pair of cells in each segment, located posterior to the early expressing cells. Anterior expressing cells along the midline are located ventrally and between the anterior and posterior commissures; posterior cells are behind the posterior fascicles. Based on its position relative to the fascicles, the anterior cell along the midline is one of the RP cells and the posterior cell is pCC. (See Chris Doe's Hyper-Neuroblast map site for information on identity of specific neuroblasts.) Expression does not take place in aCCs that are siblings of pCCs produced from the same precursors. At a later stage, positive cells increase in number, and by stages 16 and 17 more than 40 cells express hig in each neuromere (Hoshino, 1993).

Hikaru genki (Hig) is a putative secreted protein of Drosophila that belongs to immunoglobulin and complement-binding protein superfamilies. Previous studies have reported that, during pupal and adult stages, Hig protein is synthesized in subsets of neurons and appears to be secreted to the synaptic clefts of neuron-neuron synapses in the central nervous system (CNS). Reported here are the analyses of distribution patterns of Hig protein at embryonic and larval stages. In embryos, Hig is mainly observed in subsets of neurons of the CNS that include pCC interneurons and RP5 motorneurons. Hig is possibly localized in cholinergic neurons (e.g. many neurons in the optic lobes of the adult brain) and in histaminergic neurons (e.g. pCC neuron). Thus Hig expression is detected in various types of neurons and does not correlate with any neuronal markers examined to date (Hoshinom, 1999).

Larval and Pupal stages

mRNA levels decrease in first instar larvae and are low throughout the early pupal stage. In late pupae, it increases again (Hoshino, 1993).

In the peripheral nervous system of the third instar larva, axons containing Hig run around a body wall muscle, muscle 8, in each hemisegment. Axons innervating muscle 8 route via the transverse nerve (TN) that runs along the posterior edge of the muscle and via the SNa branch of the segmental nerve. A few axons in SNa appear to cross muscle 8 at the ventrolateral side and merge with TN vertically from the anterior side. Hig protein is found along both nerve tracts; for TN, the immunoreactivity can be traced along the nerve from muscle 7 toward muscle 8, but a strong staining associated with many varicosities is confined in a portion abutting the posterior edge of muscle 8. For SNa, staining is only found around muscle 8 but not in the region more proximal to the CNS. In addition, a lateral bipolar dendrite cell (LBD), which is located on the posterior edge of muscle 8 and sends two projections in opposite directions along TN, exhibits Hig staining in the cell body and processes. The LBD processes could not be distinguised from other axonal processes in most regions of the transvese nerve, but it is possible that LBD partly contributes to the staining of TN (Hoshino, 1999).

In the CNS of the third instar larva, cells expressing Hig were found both in the brain and ventral cord. In the brain hemispheres, a subset of cells stain for Hig. In the ventral cord, cells expressing Hig are arranged metamerically along the midline and in the lateral cortex (Hoshino, 1999).

Immunoelectron microscopic analyses have revealed the sub-cellular localization of Hig in the peripheral nervous system. In the third instar larvae, a couple of processes in or associated with TN contain numerous Hig-positive vesicles and frequently bulge with the vesicles to make varicosities along the posterior ridge of muscle 8. A few axons appear to make many NMJs on muscle 8, but only a subset of presynaptic terminals are found to be filled with vesicles heavily labelled with Hig staining. These terminals do not have widely spread subsynaptic reticulum characteristic for the type I NMJ and their morphology is rather similar to type III terminals. It should be noted that the immunoreactivity is not clearly detected in the synaptic cleft even in the NMJ stained for Hig. This staining pattern shows a striking contrast to the pattern found in the adult brain, where Hig is clearly localized in the synaptic clefts of neuron-neuron synapses but is not detected inside the synaptic terminals (Hoshino, 1999).

The localization of Hig protein was also observed in the specialized cells under the electron microscope. For instance, the LBD cell in the third instar larva, which may be a neurosecretory cell, exhibits Hig staining in a number of small dots that represent vesicles. In the ventral ganglion of adult flies, characteristic cells are occasionally observed that have a large number of dense core vesicles as well as clear vesicles in their cell bodies: subsets of the vesicles are immunoreactive to Hig antibody. The cells are morphologically different from the surrounding neurons, where a much smaller number of vesicles are present and Hig is predominantly associated with the nuclear membrane and endoplasmic reticulum/Golgi apparatus. Therefore, the vesicle-rich cells in the adult ventral ganglion seem to be specialized for neurosecretion. Hig protein thus appears to be produced by neurosecretory cells as well as neurons (Hoshino, 1999).

Adult

In adults, transcripts are most abundant in the head and absent in bodies. In the adult CNS, the optic lobes have very high levels, and weaker activity is found in cells of the central brain and ventral ganglion (Hoshino, 1993). In the brain, the laminar cells in the optic lobe and some cells in the central brain show strong protein staining. HIG protein is found both in neuropils in the internal region of the brain (in which a multitude of synapses are formed), and in the cellular cortical regions. In the ventral ganglion, stain is observed in a dotted pattern along nerves that run on the surface of the ganglion and extend to the peripheral tissues. Staining is detected along motor nerves and boutons of specific central muscles (Hoshino, 1996).

Effects of mutation or deletion

The hikaru genki locus was identified as a P element insertion, isolated using an enhancer trap screen. Homozygous mutant adults have reduced activity levels for locomotion as well as lower fertility and reduced longevity. Mutant flies remain motionless most of the time, moving only occasionally and then only slowly. Although adults die within 1-4 days after eclosion, more than half of the mutant embryos develop and survive to the adult stage. Females lay no eggs. Mutants rarely fly and never jump, but they do show grooming behavior. When placed under a strong light or in the presence of a chemical odorant, they quickly respond and move vigorously. This phenotype gives its name to the gene: in Japanese, hikaru genki means "light activated." Upon hatching, wild-type larvae elongate a significant amount during the process of escaping from the egg shell, but mutant larvae do not elongate. Mutant larvae have uncoordinated locomotion. Mutant larvae rarely move in a straight line and frequently move backward in response to stimuli that normally causes forward locomotion. Their movements are characterized by muscle contractions that are both laterally and vertically abnormal (Hoshino, 1993).

On occasion, mutant flies exhibit body and wing tremors while either standing or walking. Neural circuits of mutants show unusually frequent bursting activity, rarely observed in wild-type flies. The bursting is observed simultaneously in muscles located at both sides (Hoshino, 1996).


REFERENCES

Hoshino, M., Matsuzaki, F., Nabeshima, Y. and Hama, C. (1993). hikaru genki, a CNS-specific gene identified by abnormal locomotion in Drosophila, encodes a novel type of protein. Neuron 10: 395-407.

Hoshino, M., et al. (1996). Hikaru genki protein is secreted into synaptic clefts from an early stage of synapse formation in Drosophila. Development 122: 589-597

Hoshinom, M., et al. (1999). Neural expression of hikaru genki protein during embryonic and larval development of Drosophila melanogaster. Dev. Genes Evol. 209(1): 1-9.


hikaru genki: Biological Overview | Developmental Biology | Effects of Mutation

date revised: 1 FEB 97 

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