The dynamic nitric oxide pattern in developing cuttlefish Sepia officinalis

Abstract

Background: Nitric oxide (NO) is implied in many important biological processes in all metazoans from porifera to chordates. In the cuttlefish Sepia officinalis NO plays a key role in the defense system and neurotransmission. Results: Here, we detected for the first time NO, NO synthase (NOS) and transcript levels during the development of S. officinalis. The spatial pattern of NO and NOS is very dynamic, it begins during organogenesis in ganglia and epithelial tissues, as well as in sensory cells. At later stages, NO and NOS appear in organs and/or structures, including Hoyle organ, gills and suckers. Temporal expression of NOS, followed by real-time PCR, changes during development reaching the maximum level of expression at stage 26. Conclusions: Overall these data suggest the involvement of NO during cuttlefish development in different fundamental processes, such as differentiation of neural and nonneural structures, ciliary beating, sensory cell maintaining, and organ functioning. Developmental Dynamics 241:390-402, 2012. V C 2012 Wiley Periodicals, Inc.

Mollusca

“…Small cardioactive peptides (ScPs) are also expressed in neural subsets of gastropod and bivalve larvae and in the juvenile and adult nervous system of gastropods and cephalopods (Barlow and Truman 1992 ;Kempf et al 1992 ;Kanda and Minakata 2006 ;Ellis and Kempf 2011 ). With antibodies against these substances available, and several other neuroactive compounds such as nitric oxide and vasopressin identifi ed Filla et al 2009 ;Bardou et al 2010 ;Mattiello et al 2012 ), potentially useful tools are at hand for future comparative evolutionary neurodevelopmental studies on mollusks.…”

The short life of the Hoyle organ of Sepia officinalis: formation, differentiation and degradation by programmed cell death

“…On the other hand, this finding together with the presence of NOS and NO in the HO at later developmental stages before hatching (Mattiello et al, 2012) could also suggest a possible involvement of NO in preventing cell death signalling (CDS). The action of NO as a cell death inhibitor has likewise been reported in the apical ganglion of the gastropod Ilyanassa obsoleta (Say, 1822), whereby this structure disappears by apoptosis at metamorphosis induction (Leise et al, 2004).…”

“…This gaseous molecule, synthesized from L-arginine by the enzyme NO synthase (NOS), plays key roles in neurotransmission, defence system and development in S. officinalis (Palumbo et al, 2000;Fiore et al, 2004;Di Cristo et al, 2007;Mattiello et al, 2010Mattiello et al, , 2012Mattiello et al, , 2013. The spatial pattern of NO and NOS is very dynamic during cuttlefish development (Mattiello et al, 2012). An initial weak NO signal and NOS immunopositivity have been detected in the HO area at embryonic stage 26 (Mattiello et al, 2012).…”

“…The spatial pattern of NO and NOS is very dynamic during cuttlefish development (Mattiello et al, 2012). An initial weak NO signal and NOS immunopositivity have been detected in the HO area at embryonic stage 26 (Mattiello et al, 2012). As development proceeds (stages 28-29), the NO signal is amplified in the anchor-shaped HO area.…”

Histamine and histidine decarboxylase in the olfactory system and brain of the common cuttlefish Sepia officinalis (Linnaeus, 1758)

“…Another important neurotransmitter in vertebrates (Arvidsson, 1997;Karalliedde & Senanayake, 1989;McGehee & Role, 1995) and other molluscs (McCormack et al, 2010;Popova & Panchin, 1999;Tsangaris et al, 2010), acetylcholine, interacts with iridophores in squid that reflect different wavelengths of light (Hanlon, Cooper, Budelmann, & Pappas, 1990) and activates both white-cap papillae and chromatophores (Gonzalez-Bellido et al, 2018). Neuromodulators like nitric oxide are well described as having a variety of roles in vertebrates (Ferrando et al, 2012) and molluscs (Biggers et al, 2012;Gelperin, Flores, Raccuia-Behling, & Cooke, 2000;Röszer et al, 2004), and are no exception in cephalopods with their involvement in a variety of functions including regulation of metabolism, blood pressure, statocyst activity, and chromatophore activity (Di Cosmo, Di Cristo, Palumbo, d'Ischia, & Messenger, 2000;Mattiello et al, 2012). Among the monoamines, serotonin is abundant in both vertebrates (Halasz & Shepherd, 1983;Yee, Yang, Böttger, Finger, & Kinnamon, 2001) and other molluscs (Alavi, Nagasawa, Takahashi, & Osada, 2017;Croll & Chiasson, 1989;Dickinson, Croll, & Voronezhskaya, 2000;Elekes & Nässel, 1990).…”