Transcriptomic Analysis of the Kuruma Prawn Marsupenaeus japonicus Reveals Possible Peripheral Regulation of the Ovary

Abstract

Crustacean reproduction has been hypothesized to be under complex endocrinological regulation by peptide hormones. To further improve our understanding of the mechanisms underlying this complex regulation, knowledge is needed regarding the hormones not only of the central nervous system (CNS) such as the X-organ/sinus gland (XOSG), brain, and thoracic ganglia, but also the peripheral gonadal tissues. For example, in vertebrates, some gonadal peptide hormones including activin, inhibin, follistatin, and relaxin are known to be involved in the reproductive physiology. Therefore, it is highly likely that some peptide factors from the ovary are serving as the signals among peripheral tissues and central nervous tissues in crustaceans. In this work, we sought to find gonadal peptide hormones and peptide hormone receptors by analyzing the transcriptome of the ovary of the kuruma prawn Marsupenaeus japonicus. The generated ovarian transcriptome data led to the identification of five possible peptide hormones, including bursicon-α and-β, the crustacean hyperglycemic hormone (CHH)-like peptide, insulin-like peptide (ILP), and neuroparsin-like peptide (NPLP). Dominant gene expressions for the bursicons were observed in the thoracic ganglia and the ovary, in the CNS for the CHH-like peptide, in the heart for NPLP, and in the ovary for ILP. Since the gene expressions of CHH-like peptide and NPLP were affected by a CHH (Penaeus japonicus sinus gland peptide-I) from XOSG, we produced recombinant peptides for CHH-like peptide and NPLP using Escherichia coli expression system to examine their possible peripheral regulation. As a result, we found that the recombinant NPLP increased vitellogenin gene expression in incubated ovarian tissue fragments. Moreover, contigs encoding putative receptors for insulin-like androgenic gland factor, insulin, neuroparsin, and neuropeptide Y/F, as well as several contigs encoding orphan G-protein coupled receptors and receptor-type guanylyl cyclases were also identified in the ovarian transcriptome. These results suggest that reproductive physiology in crustaceans is regulated by various gonadal peptide hormones, akin to vertebrates.

Signaling Pathways That Regulate the Crustacean Molting Gland

“…GPCRs are characterized by seven transmembrane domains, an external N-terminal domain, and a C-terminal cytosolic domain (25). These are divided among three large classes: rhodopsin-like (Class A), which represents the largest number of GPCRs; secretinlike (Class B); and metabotropic glutamate (Class C) (25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44).…”

“…Dilp8 is one of eight insulin-like peptides (ILPs) in D. melanogaster (74)(75)(76)(77)(78). The ILP superfamily consists of insulin, insulin-like growth factors (IGFs), and relaxin-like peptides (38,71). Dilp 1 to 6 are in the insulin/IGF clade and bind to receptor tyrosine kinase receptors; Dilp 7 and 8 are in the relaxin-like clade and bind to leucine-rich repeat GPCRs (71,74,75).…”

“…In some ILPs, the C chain is not completely removed, producing a polypeptide, in which part of the C chain is retained (77). ILPs have been identified in decapod crustacean transcriptomes (28,32,33,38,83,(110)(111)(112)(113)(114). One of the best characterized ILP is the insulin-like androgenic gland hormone (IAG); it is expressed primarily in the androgenic gland and determines adult male characteristics (42,83,108,109,115,116).…”

Recent advances in neuropeptide-related omics and gene editing: Spotlight on NPY and somatostatin and their roles in growth and food intake of fish

“…Orexin is involved in the regulation of the reproductive system through the hypothalamic-pituitary-ovarian axis ( 79 ), and the transcriptome profile of the endometrium during early pregnancy in pigs has revealed that orexin affected the expression of a large number of genes differentially ( 79 ) while transcriptome of myometrial explants during the early implantation period suggested that orexin influenced the process involved in quiescence, proliferartion, remodeling and angiogenesis in myometrial explants during the peri-implantation period in the pig ( 80 ). NPY has also been found to be involved in gonadal development in crustaceans ( 31 ) and mammals ( 32 ). CCK receptor (CCKAR and CCKBR) deletion leads to abnormal cortical development, and using comparative transcriptomic analysis, transcripts of CXCL12, BMP7 are downregulated and may be target genes for abnormal cortical development ( 86 ).…”

Neuroparsin 1 (MrNP1) and Neuroparsin 2 (MrNP2) Are Involved in the Regulation of Vitellogenesis in the Shrimp Macrobrachium rosenbergii

“…For example, in the shrimp M. ensis, in vivo gene silencing of neuroparsins could cause a significant decrease in vitellogenin transcript level in the hepatopancreas and ovary (Yang et al, 2014). In Marsupenaeus japonicus, in vivo injection of recombinant neuroparsin could increase the expression of MjVg (Tsutsui et al, 2020).…”