Differential expression of five prosomatostatin genes in the central nervous system of the catshark Scyliorhinus canicula

Abstract

Five prosomatostatin genes (PSST1, PSST2, PSST3, PSST5, and PSST6) have been recently identified in elasmobranchs (Tostivint et al., General and Comparative Endocrinology, 2019, 279, 139–147). In order to gain insight into the contribution of each somatostatin to specific nervous systems circuits and behaviors in this important jawed vertebrate group, we studied the distribution of neurons expressing PSST mRNAs in the central nervous system (CNS) of Scyliorhinus canicula using in situ hybridization. Additionally, we combined in situ hybridization with tyrosine hydroxylase (TH) immunochemistry for better characterization of PSST1 and PSST6 expressing populations. We observed differential expression of PSST1 and PSST6, which are the most widely expressed PSST transcripts, in cell populations of many CNS regions, including the pallium, subpallium, hypothalamus, diencephalon, optic tectum, midbrain tegmentum, and rhombencephalon. Interestingly, numerous small pallial neurons express PSST1 and PSST6, although in different populations judging from the colocalization of TH immunoreactivity and PSST6 expression but not with PSST1. We observed expression of PSST1 in cerebrospinal fluid‐contacting (CSF‐c) neurons of the hypothalamic paraventricular organ and the central canal of the spinal cord. Unlike PSST1 and PSST6, PSST2, and PSST3 are only expressed in cells of the hypothalamus and in some hindbrain lateral reticular neurons, and PSST5 in cells of the region of the entopeduncular nucleus. Comparative data of brain expression of PSST genes indicate that the somatostatinergic system of sharks is the most complex reported in any fish.

Regulatory Mechanisms of Somatostatin Expression

“…The physiological significance of somatostatin 1 is well established, whereas the different expression patterns of the other somatostatin genes might indicate that the genes have individually differing roles in various species [43]. For instance, sharks and other vertebrates show differential expression of somatostatin genes in different sets of brain neurons [44]. Gene duplication is thought to be a primary source for the evolution of novel functions [45].…”

Developmental genoarchitectonics as a key tool to interpret the mature anatomy of the chondrichthyan hypothalamus according to the prosomeric model

“…The TSPa/PSPa domain contains ScOtp -expressing cells probably migrated from the TPa/PPa (present results). These cells could give rise to different peptidergic cell types that have been described near the catshark optic chiasm (Met-Enkephalin, Vallarino et al, 1994 ; Tyrotropin Releasing Hormone, Teijido et al, 2002 ; Somatostatin, Sobrido-Cameán et al, 2020 ). Of note, Growth Hormone releasing hormone (Ghrh)-positive cells described in the PSPa of mammals have presumably migrated from the PPa ( Morales-Delgado et al, 2014 ).…”

“…Similarly, the mammalian ventromedial nucleus seems to be positive for Lhx5 and abuts Dlx -expressing territories at early stages ( Sheng et al, 1997 ; Abellán et al, 2010 ), but it is negative at later stages ( Szabó et al, 2009 ; Heide et al, 2015 ; Miquelajáuregui et al, 2015 ). The catshark NLT presents several types of peptidergic cells (somatostatin, Sobrido-Cameán et al, 2020 ; met-enkephalin and leu-enkephalin, Vallarino et al, 1994 ; melanin-concentrating hormone, Vallarino et al, 1989a ; atrial natriuretic factor, Vallarino et al, 1990b ; delta sleep-inducing peptide, Vallarino et al, 1992 ; beta-endorphin, Vallarino et al, 1989b ; galanin, Vallarino et al, 1991 ; neuropeptide Y, Vallarino et al, 1988 ; corticotropin-releasing factor, Vallarino et al, 1989c ; adrenocorticotropic hormone, Vallarino and Ottonello, 1987 , Vallarino et al, 1989b ), and is thought to be associated with the hypophysis, as reported in actinopterygian fishes (reviewed in Butler and Hodos, 2005 ). The mammalian ventromedial hypothalamus is involved in feeding, fear, thermoregulation, and sexual activity ( Harding and McGinnis, 2005 ; King, 2006 ; Silva et al, 2016 ).…”

“…An attempt to establish terminological or conceptual correspondences between the defined brain territories according to the prosomeric model in the juvenile catshark and the adult brain territories named according to the reference work of Smeets et al (1983) was previously proposed by Sobrido-Cameán et al (2020) in their study of the expression of five prosomatostatin genes, but developmental gene expression patterns typically used to identify embryonic histogenetic domains in the hypothalamus were not considered in this study. Here, we present a comprehensive comparison between the morphologic interpretation of relevant gene expression data interpreted according to the prosomeric model in embryos at stage 32 (when the basic adult brain organization becomes appreciable) and the location of functional neuronal cell groups defined in adults ( Smeets et al, 1983 , and subsequent works following columnar terms).…”

Organization of the corticotropin-releasing hormone and corticotropin-releasing hormone-binding protein systems in the central nervous system of the sea lamprey Petromyzon marinus

“…In some samples, ISH for PmCRHBP was followed by immunohistochemistry against PmCRH. These experiments were performed as described in a previous study (Sobrido-Cameán et al, 2020a). Briefly, after the ISH signal was clearly visible, sections were rinsed twice in TBS and treated with 10% H 2 O 2 in TBS for 30 minutes.…”