Developmental expression of cell recognition molecules in the mushroom body and antennal lobe of the locust Locusta migratoria

Abstract

We examined the development of olfactory neuropils in the hemimetabolous insect Locusta migratoria with an emphasis on the mushroom bodies, protocerebral integration centers implicated in memory formation. Using a marker of the cyclic adenosine monophosphate (cAMP) signaling cascade and lipophilic dye labeling, we obtained new insights into mushroom body organization by resolving previously unrecognized accessory lobelets arising from Class III Kenyon cells. We utilized antibodies against axonal guidance cues, such as the cell surface glycoproteins Semaphorin 1a (Sema 1a) and Fasciclin I (Fas I), as embryonic markers to compile a comprehensive atlas of mushroom body development. During embryogenesis, all neuropils of the olfactory pathway transiently expressed Sema 1a. The immunoreactivity was particularly strong in developing mushroom bodies. During late embryonic stages, Sema 1a expression in the mushroom bodies became restricted to a subset of Kenyon cells in the core region of the peduncle. Sema 1a was differentially sorted to the Kenyon cell axons and absent in the dendrites. In contrast to Drosophila, locust mushroom bodies and antennal lobes expressed Fas I, but not Fas II. While Fas I immunoreactivity was widely distributed in the midbrain during embryogenesis, labeling persisted into adulthood only in the mushroom bodies and antennal lobes. Kenyon cells proliferated throughout the larval stages. Their neurites retained the embryonic expression pattern of Sema 1a and Fas I, suggesting a role for these molecules in developmental mushroom body plasticity. Our study serves as an initial step toward functional analyses of Sema 1a and Fas I expression during locust mushroom body formation.

Scanning Laser Optical Tomography Resolves Structural Plasticity during Regeneration in an Insect Brain

“…Moreover, Neurobiotin labeling of axotomized olfactory fibers could clearly ascribe the recovery of antennal lobe volume to regenerated axons. Intriguingly, regenerating olfactory receptor axons express embryonic cell surface molecules indicative of reacquisition of a developmental mode [37], [13]. The observed time course of degeneration and subsequent regeneration is comparable to what has been shown in other insect sensory systems such as deafferented cercal fibers in the cockroach and auditory afferents in the grasshopper [38]–[40].…”

Disruption of Aedes aegypti Olfactory System Development through Chitosan/siRNA Nanoparticle Targeting of semaphorin-1a

“…aegypti . The antibody, which was recently used to detect Sema1a expression in grasshoppers [17], was found to specifically recognize Aae Sema1a in the developing brain, as assayed by the lack of brain staining assessed in Ae. aegypti sema1a knockdown animals (see below).…”

“…Furthermore, graded Sema1a expression in the antennal lobe is required for the proper targeting of projection neuron dendrites into the antennal lobe [13]. Although Sema1a expression has been detected in the developing Locusta migratoria olfactory system [17], the function of Sema1a during pupal olfactory development has not yet been assessed in insects other than D. melanogaster . Our recent studies have revealed differences between D. melanogaster and Ae.…”

Characterization of plexinA and two distinct semaphorin1a transcripts in the developing and adult cricket Gryllus bimaculatus

“…The expression of many guidance molecules tends to decrease after development, though expression appears to be maintained in select areas. In particular, areas with high levels of plasticity, such as the hippocampus in mammals (Giger et al, 1998;Pascual, Pozas, & Soriano, 2005;Sahay et al, 2005) or the MBs in invertebrates (Eickhoff & Bicker, 2012;Maynard et al, 2007), continue to express developmental guidance molecules, including the Sema proteins, into adulthood. Experiments in mammals indicate that these developmental guidance proteins are important regulators of adult neuroplasticity, pruning axons, eliminating synapses, and reducing spine density and size in order to constrain plasticity in more mature circuits (Boggio et al, 2019;Lee et al, 2012;Riccomagno & Kolodkin, 2015;Tran et al, 2009).…”

“…The expression patterns of the Semas and Plexins have been described most thoroughly during development, but both continue to be expressed in some CNS regions into adulthood. Semas can be found in the adult CNS in both vertebrates (Duan et al, ; Giger, Pasterkamp, Heijnen, Holtmaat, & Verhaagen, ) and invertebrates (Maynard, McCarthy, Sheldon, & Horch, ), typically in areas of high plasticity such as the hippocampus (Sahay et al, ) and the mushroom bodies (Eickhoff & Bicker, ; Maynard et al, ). Plexins have also been described in the adult CNS in vertebrates (Gutekunst, Stewart, & Gross, ; Saha, Ypsilanti, Boutin, Cremer, & Chedotal, ; Usui, Taniguchi, Yokomizo, & Shimizu, ), and invertebrates (Yoo, ) though less is known about Plexin distribution at this stage.…”