Adult neurogenesis and cell cycle regulation in the crustacean olfactory pathway: from glial precursors to differentiated neurons

Abstract

Adult neurogenesis is a characteristic feature of the olfactory pathways of decapod crustaceans. In crayfish and clawed lobsters, adult-born neurons are the progeny of precursor cells with glial characteristics located in a neurogenic niche on the ventral surface of the brain. The daughters of these precursor cells migrate during S and G 2 stages of the cell cycle along glial fibers to lateral (cluster 10) and medial (cluster 9) proliferation zones. Here, they divide (M phase) producing offspring that differentiate into olfactory interneurons. The complete lineage of cells producing neurons in these animals, therefore, is arranged along the migratory stream according to cell cycle stage. We have exploited this model to examine the influence of environmental and endogenous factors on adult neurogenesis. We find that increased levels of serotonin upregulate neuronal production, as does maintaining animals in an enriched (versus deprived) environment or augmenting their diet with omega-3 fatty acids; increased levels of nitric oxide, on the other hand, decrease the rate of neurogenesis. The features of the neurogenic niche and migratory streams, and the fact that these continue to function in vitro, provide opportunities unavailable in other organisms to explore the sequence of cellular and molecular events leading to the production of new neurons in adult brains.

Distribution of serotonin and dopamine in the central nervous system of the female mud crab, Scylla olivacea (Herbst)

“…5-HT has been shown to stimulate gonad maturation in other crab species (Kulkarni and Fingerman, 1992;Richardson et al, 1991;Sainath and Reddy, 2011). Moreover, serotonin could be involved in neurogenesis in proliferation zones of clusters 9 and 10 in the brain that are involved in reproduction in crustaceans (Beltz et al, 2011;Sandeman et al, 2009;Sullivan et al, 2007). In the SEG and TG, 5-HT is most likely involved not only in reproduction but also in the innervation of appendage muscles, especially by the large neurons (Beltz, 1999).…”

Cytoarchitecture and ultrastructure of neural stem cell niches and neurogenic complexes maintaining adult neurogenesis in the olfactory midbrain of spiny lobsters, Panulirus argus

“…In P. clarkii , CFCs were identified as glial cells mainly because they were labeled by anti-GS (Sullivan et al, 2007a,b). Anti-GS is a marker for astrocytes in the mammalian brain (Norenberg, 1979), and it selectively labels a class of glial cells in the brain of decapod crustaceans (Linser et al 1997; Sullivan et al, 2007a; Harzsch and Hansson, 2008).…”

“…In the olfactory deutocerebrum of adult P. argus and P. clarkii , each aNB is closely associated with a morphologically unique clump of cells that has been interpreted as a putative stem cell niche (Fig. 1; Schmidt, 2007a,b; Sullivan et al, 2007a,b; Song et al, 2009). Similar clumps of cells were originally identified as “deutocerebral organs” in brains of several other species of decapod crustaceans by Bazin (1970) suggesting that they are a common component associated with adult neurogenesis in the olfactory deutocerebrum (Schmidt, 2007b).…”

Adult neurogenesis in the crayfish brain: Proliferation, migration, and possible origin of precursor cells

“…Adult-born neurons in the crustacean brain differentiate into olfactory interneurons (Schmidt, 1997; Sullivan and Beltz, 2005), as do those in mammals (Gheusi and Lledo, 2007) and fish (Kaslin et al, 2008). The lineage of cells producing adult-born neurons in crayfish and clawed lobsters has been identified, is accessible on the ventral surface of the brain, and can be maintained in short-term culture (Sullivan et al, 2007a, b; Benton and Beltz, 2008). The goal of our present work was to examine in detail the proliferation and migration of neuronal precursor cells in this system.…”