Nitric oxide in the crustacean brain: Regulation of neurogenesis and morphogenesis in the developing olfactory pathway

Abstract

Nitric oxide (NO) plays major roles during development and in adult organisms. We examined the temporal and spatial patterns of nitric oxide synthase (NOS) appearance in the embryonic lobster brain to localize sources of NO activity; potential NO targets were identified by defining the distribution of NO-induced cGMP. Staining patterns are compared with NOS and cyclic 3,5 guanosine monophosphate (cGMP) distribution in adult lobster brains. Manipulation of NO levels influences olfactory glomerular formation and stabilization, as well as levels of neurogenesis among the olfactory projection neurons. In the first 2 days following ablation of the lateral antennular flagella in juvenile lobsters, a wave of increased NOS immunoreactivity and a reduction in neurogenesis occur. These studies implicate nitric oxide as a developmental architect and also support a role for this molecule in the neural response to injury in the olfactory pathway. Developmental Dynamics 236:3047-3060, 2007.

Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects

“…Interestingly, enhanced neurogenesis in the cricket Nematobius sylvestris infected with the nematomorph Paragordius tricuspidatus has been reported Biron et al, 2005). Given the implication of the serotonergic, dopaminergic and possibly nitrergic systems in behavioural manipulation of several amphipods (Table1), the reported bidirectional interaction between the nitrergic and serotonergic systems in the modulation of neurogenesis in lobster (Benton et al, 2007) is worth considering in other crustacean and insect models.…”

“…The gaseous messenger NO acts as a major signal molecule in the olfactory system and in the immune defence of major invertebrate phyla (Benton et al, 2007;Colasanti et al, 2010). The increased level of NO synthase immunoreactivity and the numerous astrocyte-like glial cells around cysts of Microphallus papillorobustus in the brain of infected Gammarus insensibilis provided evidence for a chronic neuroinflammatory response triggered by mature cysts of the trematode in its intermediate host (Helluy and Thomas, 2010).…”

“…Many behaviours, in particular anti-predatory ones, are based on previous experience and hence connected to neuronal plasticity. Life-long neurogenesis occurs in the main integrative centres in insects (mushroom body) and in the olfactory pathway of crustaceans and vertebrates (see Harzsch et al, 1999;Beltz and Sandeman, 2003;Benton et al, 2007). Interestingly, enhanced neurogenesis in the cricket Nematobius sylvestris infected with the nematomorph Paragordius tricuspidatus has been reported Biron et al, 2005).…”

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

“…Whether proliferation of aNBs is influenced by signaling molecules has not yet been studied, but, since serotonin and nitric oxide modulate cell divisions in the proliferation zones (Benton et al, 2007;2008;Sandeman et al, 2009), it is possible that they might also affect the aNB.…”

Regulation of enteric neuron migration by the gaseous messenger molecules CO and NO

“…A HO gene is expressed in the honeybee brain (Watanabe et al, 2007) and the catalytic properties of a recombinant Drosophila HO protein have been analyzed (Zhang et al, 2004). Unlike for NO signaling in arthropods, which could be linked to discrete developmental processes such as cell proliferation (Kuzin et al, 1996;Champlin and Truman, 2000;Benton et al, 2007), neurite outgrowth (Seidel and Bicker, 2000), patterning of synaptic connectivity (Ball and Truman, 1998;Gibbs and Truman, 1998;Wright et al, 1998) and axonal regeneration (Stern and Bicker, 2008), no neurodevelopmental functions of CO have so far emerged.…”