A New Type II CHH Neuropeptide Involves Ovarian Development in the Peppermint Shrimp, Lysmata Vittata

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2024 Aug 1

PMID 39088423

Authors

Huiling Lan

Fang Liu

Li Lu

An Liu

Haihui Ye

Affiliations

Soon will be listed here.

Abstract

Type II crustacean hyperglycemic hormone (CHH) neuropeptides play diverse roles in crustaceans. In the hermaphrodite shrimp Lysmata vittata, two transcripts of type II CHHs (molt-inhibiting hormone/gonad-inhibiting hormone, MIH/GIH1 and MIH/GIH2) were identified by transcriptome sequencing, and MIH/GIH1 was later named Lvit-GIH1 for its inhibitory effect on ovarian development. Based on the high similarity of MIH/GIH2 to Lvit-GIH1, we named tentatively MIH/GIH2 as Lvit-GIH2 and explored the role of Lvit-GIH2 in ovarian development. The open reading frame (ORF) of Lvit-GIH2 was 333 bp in length, encoding a precursor consisted of a 32-aa signal peptide and a 78-aa mature peptide, which shared high sequence similarity with the type II subfamily peptides in crustaceans. Notably, Lvit-GIH2 was widely expressed in multiple tissues. The qRT-PCR findings indicated a rising trend in the expression of Lvit-GIH2 from the male phase to the euhermaphrodite phase. Both RNA interference and addition of GIH2 recombinant proteins (rGIH2) experiments showed that Lvit-GIH2 suppressed Lvit-Vg expression in hepatopancreas and Lvit-VgR expression in ovary. To further investigate the role of Lvit-GIH2 in ovarian development, the RNA-sequence analysis was performed to examine the changes in ovary after addition of rGIH2. The results showed that the pathways (Cysteine and methionine metabolism, Apoptosis-multiple species, etc.) and the genes (17bHSD8, IGFR, CHH, etc.) related to ovarian development were negatively regulated by rGIH2. In brief, Lvit-GIH2 might inhibit the ovarian development in L. vittata.

References

Webster S, Keller R, Dircksen H . The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. Gen Comp Endocrinol. 2011; 175(2):217-33. DOI: 10.1016/j.ygcen.2011.11.035. View

Shi W, Liu F, Liu A, Huang H, Lin Q, Zeng C . Roles of gonad-inhibiting hormone in the protandric simultaneous hermaphrodite peppermint shrimp†. Biol Reprod. 2020; 103(4):817-827. DOI: 10.1093/biolre/ioaa111. View

Liu F, Shi W, Ye H, Zeng C, Zhu Z . Insulin-like androgenic gland hormone 1 (IAG1) regulates sexual differentiation in a hermaphrodite shrimp through feedback to neuroendocrine factors. Gen Comp Endocrinol. 2020; 303:113706. DOI: 10.1016/j.ygcen.2020.113706. View

Yano I, Hoshino R . Effects of 17 beta-estradiol on the vitellogenin synthesis and oocyte development in the ovary of kuruma prawn (Marsupenaeus japonicus). Comp Biochem Physiol A Mol Integr Physiol. 2006; 144(1):18-23. DOI: 10.1016/j.cbpa.2006.01.026. View

Funk C . Prostaglandins and leukotrienes: advances in eicosanoid biology. Science. 2001; 294(5548):1871-5. DOI: 10.1126/science.294.5548.1871. View

Yang W, Rao K . Cloning of precursors for two MIH/VIH-related peptides in the prawn, Macrobrachium rosenbergii. Biochem Biophys Res Commun. 2001; 289(2):407-13. DOI: 10.1006/bbrc.2001.6019. View

Simon C, Truong H, Habilay N, Hines B . Feeding Behaviour and Bioavailability of Essential Amino Acids in Shrimp Fed Fresh and Leached Fishmeal and Fishmeal-Free Diets. Animals (Basel). 2021; 11(3). PMC: 8002457. DOI: 10.3390/ani11030847. View

Galikova M, Dircksen H, Nassel D . The thirsty fly: Ion transport peptide (ITP) is a novel endocrine regulator of water homeostasis in Drosophila. PLoS Genet. 2018; 14(8):e1007618. PMC: 6124785. DOI: 10.1371/journal.pgen.1007618. View

Chen D, Liu F, Zhu Z, Lin Q, Zeng C, Ye H . Ontogenetic development of gonads and external sexual characters of the protandric simultaneous hermaphrodite peppermint shrimp, Lysmata vittata (Caridea: Hippolytidae). PLoS One. 2019; 14(4):e0215406. PMC: 6474713. DOI: 10.1371/journal.pone.0215406. View

10.

Laphyai P, Kruangkum T, Chotwiwatthanakun C, Semchuchot W, Thaijongrak P, Sobhon P . Suppression of a Novel Vitellogenesis-Inhibiting Hormone Significantly Increases Ovarian Vitellogenesis in the Black Tiger Shrimp, . Front Endocrinol (Lausanne). 2021; 12:760538. PMC: 8634883. DOI: 10.3389/fendo.2021.760538. View

11.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S . MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013; 30(12):2725-9. PMC: 3840312. DOI: 10.1093/molbev/mst197. View

12.

Gu P, Chu K, Chan S . Bacterial expression of the shrimp molt-inhibiting hormone (MIH): antibody production, immunocytochemical study and biological assay. Cell Tissue Res. 2001; 303(1):129-36. DOI: 10.1007/s004410000299. View

13.

Shi L, Li B, Zhou T, Wang W, Chan S . Functional and evolutionary implications from the molecular characterization of five spermatophore CHH/MIH/GIH genes in the shrimp Fenneropenaeus merguiensis. PLoS One. 2018; 13(3):e0193375. PMC: 5858750. DOI: 10.1371/journal.pone.0193375. View

14.

Feijo R, Braga A, Lanes C, Figueiredo M, Romano L, Klosterhoff M . Silencing of Gonad-Inhibiting Hormone Transcripts in Litopenaeus vannamei Females by use of the RNA Interference Technology. Mar Biotechnol (NY). 2015; 18(1):117-23. DOI: 10.1007/s10126-015-9676-2. View

15.

Schattenberg J, Schuchmann M . Diabetes and apoptosis: liver. Apoptosis. 2009; 14(12):1459-71. DOI: 10.1007/s10495-009-0366-2. View

16.

Lafont R, Mathieu M . Steroids in aquatic invertebrates. Ecotoxicology. 2007; 16(1):109-30. DOI: 10.1007/s10646-006-0113-1. View

17.

Liang X, Luo X, Lin H, Han F, Qin J, Chen L . Effects and Mechanism of Different Phospholipid Diets on Ovary Development in Female Broodstock Pacific White Shrimp, . Front Nutr. 2022; 9:830934. PMC: 8894211. DOI: 10.3389/fnut.2022.830934. View

18.

de Kleijn D, Sleutels F, Martens G, Van Herp F . Cloning and expression of mRNA encoding prepro-gonad-inhibiting hormone (GIH) in the lobster Homarus americanus. FEBS Lett. 1994; 353(3):255-8. DOI: 10.1016/0014-5793(94)01055-2. View

19.

Galikova M, Klepsatel P . Ion transport peptide regulates energy intake, expenditure, and metabolic homeostasis in Drosophila. Genetics. 2022; 222(4). PMC: 9713441. DOI: 10.1093/genetics/iyac150. View

20.

Bao C, Liu F, Yang Y, Lin Q, Ye H . Identification of Peptides and Their GPCRs in the Peppermint Shrimp , a Protandric Simultaneous Hermaphrodite Species. Front Endocrinol (Lausanne). 2020; 11:226. PMC: 7212414. DOI: 10.3389/fendo.2020.00226. View