The Roles of the Kisspeptin System in the Reproductive Physiology of the Lined Seahorse (Hippocampus erectus), an Ovoviviparous Fish With Male Pregnancy

Abstract

The kisspeptin/GPR54 system plays a crucial role in the regulation of the reproductive axis in vertebrates. Male pregnancy and ovoviviparity are special reproductive phenomena among vertebrates. To better understand the neuroendocrine mechanisms of male pregnancy, cDNAs encoding kiss2 and GPR54 were cloned and functionally characterized from the lined seahorse, Hippocampus erectus, an ovoviviparous teleost with male pregnancy. The core mature peptide of seahorse Kiss2 is high conserved among seahorses, but unique among vertebrate Kiss orthologs. In the phylogenic analysis, the seahorse Kiss clustered with the teleost Kiss2 clade. The kiss2 transcripts were shown to be widely expressed in various tissues, notably in the brain and gonad of the seahorse, while GPR54-2 mRNA was expressed exclusively in the brain. In addition, kiss2 mRNA found in male seahorse brain tissue increased significantly at the early pubertal stage, and decreased significantly during pregnancy. Intraperitoneal administration of seahorse Kiss2-10 to sexual mature male seahorses demonstrated to stimulate lutropin β (LHβ) and follitropin β (FSHβ) release and increased serum testosterone levels. In summary, we first identified the kisspeptin/GPR54 system in an ovoviviparous fish with male pregnancy, which might be involved in the regulation of the reproductive functions of pubertal onset, gonadal development, and male pregnancy via regulating the synthesis of both gonadotropic hormone (GTH) and testosterone.

Origin and Evolution of the Neuroendocrine Control of Reproduction in Vertebrates, With Special Focus on Genome and Gene Duplications

“…In vivo stimulatory [goldfish (413), sea bass (185), seahorse Hippocampus erectus (911)] or no [goldfish (524)] action of kisspeptins on gonadotropins have been described in teleosts. In the striped bass, kisspeptin action depends on the stage of development, as intramuscular injection of Kp1 has no effect on LH at the pubertal stage, while both Kp1 and Kp2 increase LH levels at gonadal recrudescence (919).…”

Testicular development and spermatogenesis in fish: insights into molecular aspects and regulation of gene expression by different exogenous factors

“…Kisspeptin is encoded by kiss1 gene in higher animals (Lee et al 1996), and however, two paralogous genes, kiss1 and kiss2, have been characterized in fish (Lee et al 2009). Studies suggest that kisspeptin is linked with the GnRH and plays an essential role in the onset of puberty in fish (Martinez-Chavez et al 2008;Elizur 2009;Zhang et al 2018). Kiss protein control HPG axis via melatonin signalling by controlling kiss1 expression and steroid feedback mechanism (Grieves et al 2008;Akazome et al 2010).…”

“…2008; Elizur 2009; Zhang et al . 2018). Kiss protein control HPG axis via melatonin signalling by controlling kiss1 expression and steroid feedback mechanism (Grieves et al .…”

A mini-review on kisspeptin hormone as an inducing agent in fish breeding

“…Administration of thyroid hormone significantly increases kiss2 and gnrh1 mRNAs in the sexually mature males of Nile tilapia (Ogawa et al, 2013) [42] . The kiss2 mRNA in male seahorse brain increased significantly at the early pubertal stage, and decreased significantly during pregnancy (Zhang et al, 2018) [81] . Both kiss2 and kissr are highly expressed in the brain regions of sexually mature black porgy (Ma et al, 2019) [31] .…”

“…Surprisingly, the study found that primary structure of the functional peptide might be species-specific even within species of the family Scombridae, and demonstrated five types of putative mature Kiss1 peptides from sixteen scombridae species (Table 1). In contrast to Kiss1, dibasic residues (RR) have been found two positions upstream to Kiss2-10 region in zebrafish (Kitahashi et al, 2009 ) [26] , medaka (Kitahashi et al, 2009) [26] , European seabass (Felip et al, 2009) [12] , orange spotted grouper (Shi et al, 2010) [68] , chub mackerel (Selvaraj et al, 2010) [58] , red seabream (Shimizu et al, 2012) [69] , Atlantic cod (Cowan et al, 2012) [7] , striped bass (Zmora et al, 2012) [83] , Nile tilapia (Ogawa et al, 2013) [42] , grass pufferfish (Shahjahan et al, 2010) [66] , catla (Rather et al, 2016) [55] , rohu (Saha et al, 2016) [56] , pejerrey (Bohórquez et al, 2017) [5] , golden mahseer (Shahi et al, 2017) [64] , seahorse (Zhang et al, 2018) [81] and black porgy (Ma et al, 2019) [31] , suggesting Kiss2 dodecapeptide as mature form in these species. However, in the salmon immunoaffinity purification and mass spectrometric analysis have indicated mature peptide of kiss2 gene as tridecapeptide (Osugi et al, 2013) [50] (Table 2).…”