Abstract
The eyestalk of crustaceans is a vital neuroendocrine organ complex that regulates various important physiological processes, especially molting and reproduction. The mandibular organ-inhibiting hormone (MOIH), an important member of the crustacean hyperglycemic hormone (CHH) neuropeptide family, mediates vitellogenesis and reproduction. In this study, EsMOIH was isolated from the eyestalk of Eriocheir sinensis. Sequence analysis suggested that EsMOIH belongs to CHH subfamily II and contains a conserved CHH/molt-/vitellogenesis-inhibiting hormone (MIH/VIH) domain and six conserved cysteines forming three disulfide bonds. The findings corroborated the results of phylogenetic analysis. Quantitative polymerase chain reaction (qPCR) analysis suggested that EsMOIH was ubiquitously expressed in all the examined tissues, but was highly specifically expressed in the hepatopancreas. The hepatopancreatic transcription of EsMOIH decreased significantly at stages III and IV, but increased thereafter and was highest at stage V. EsMOIH transcription was strongly negatively correlated with the hepatopancreatic expression of vitellogenin (EsVg), suggesting that EsMOIH could partake in inhibiting vitellogenesis in the hepatopancreas of E. sinensis. The RNA interference (RNAi)-mediated specific knockdown of EsMOIH significantly reduced EsMOIH expression in vitro and in vivo, but markedly increased EsVg expression in the ovary and hepatopancreas. Altogether, the results suggested that EsMOIH partakes in inhibiting vitellogenesis in E. sinensis.
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Amankwah BK, Wang C, Zhou T, Liu J, Shi L, Wang W, Chan S (2019) Eyestalk ablation, a prerequisite for Crustacean reproduction: a review. Isr J Aquacult- Bamid 71
Chang ES (1993) Comparative endocrinology of molting and reproduction: insects and crustaceans. Annu Rev Entomol 38:161–180. https://doi.org/10.1146/annurev.en.38.010193.001113
Chen DW, Zhang M, Shrestha S (2007) Compositional characteristics and nutritional quality of Chinese mitten crab (Eriocheir sinensis). Food Chem 103:1343–1349. https://doi.org/10.1016/j.foodchem.2006.10.047
Chen T, Zhang LP, Wong NK, Zhong M, Ren CH, Hu CQ (2014) Pacific white shrimp (Litopenaeus vannamei) Vitellogenesis-Inhibiting Hormone (VIH) is predominantly expressed in the brain and negatively regulates Hepatopancreatic Vitellogenin (VTG) gene expression. Biol Reprod. https://doi.org/10.1095/biolreprod.113.115030
Chen T, Ren CH, Jiang X, Zhang LP, Li HM, Huang W, Hu CQ (2015) Mechanisms for type-II vitellogenesis-inhibiting hormone suppression of vitellogenin transcription in shrimp hepatopancreas: crosstalk of GC/cGMP pathway with different MAPK-dependent cascades. Plos One. https://doi.org/10.1371/journal.pone.0194459
Chen HY, Toullec JY, Lee CY (2020) The Crustacean hyperglycemic hormone superfamily: progress made in the past decade. Front Endocrinol. https://doi.org/10.3389/fendo.2020.578958
Christie AE, Yu A, Pascual MG, Roncalli V, Cieslak MC, Warner AN, Lameyer TJ, Stanhope ME, Dickinson PS, Hull JJ (2018) Circadian signaling in Homarus americanus: Region-specific de novo assembled transcriptomes show that both the brain and eyestalk ganglia possess the molecular components of a putative clock system. Mar Genom 40:25–44. https://doi.org/10.1016/j.margen.2018.03.002
Chung JS, Christie A, Flynn E (2020) Molecular cloning of crustacean hyperglycemic hormone (CHH) family members (CHH, molt-inhibiting hormone and mandibular organ-inhibiting hormone) and their expression levels in the Jonah crab, Cancer borealis. Gen Comp Endocr. https://doi.org/10.1016/j.ygcen.2020.113522
Cohen S, Ilouz O, Manor R, Sagi A, Khalaila I (2021) Transcriptional silencing of vitellogenesis-inhibiting and molt-inhibiting hormones in the giant freshwater prawn, Macrobrachium rosenbergii, and evaluation of the associated effects on ovarian development. Aquac 538:736540. https://doi.org/10.1016/j.aquaculture.2021.736540
De Kleijn DP, Van Herp F (1995) Molecular biology of neurohormone precursors in the eyestalk of Crustacea. Comp Biochem Physiol B Biochem Mol Biol 112:573–579. https://doi.org/10.1016/0305-0491(95)00126-3
Devaraj H, Saravanakumar M, Thiyagu M (2012) Induction of ovarian maturation in Penaeus monodon by molecular signal interventional approach. J Exp Zool Part B 318:572–585. https://doi.org/10.1002/jez.b.22462
Duangprom S, Saetan J, Phanaksri T, Songkoomkrong S, Surinlert P, Tamtin M, Sobhon P, Kornthong N (2022) Acceleration of ovarian maturation in the female mud crab with RNA interference of the Vitellogenesis-Inhibiting Hormone (VIH). Front Mar Sci 9:880235. https://doi.org/10.3389/fmars.2022.880235
Fisheries and Fisheries Administration of the Ministry of Agriculture (2022) China fishery statistical yearbook. China Agricultural Press, Beijing
Gonzalez M, Betancourt JL, Rodriguez-Ramos T, Estrada MP, Carpio Y, Ramos L (2020) Induction of spawning in Pacific white shrimp Litopenaeus vannamei (Boone, 1931) by injection of its molt inhibiting hormone isoform II produced in E. coli. Aquac Res 51:3100–3108. https://doi.org/10.1111/are.14644
Green S, Bachvaroff T, Sook Chung J (2022) Eyestalk neuropeptide identification in the female red deep-sea crab, Chaceon quinquedens. Gen Comp Endocr 330:114128. https://doi.org/10.1016/j.ygcen.2022.114128
Han ZB, Li XD, Li X, Xu WB, Li YD (2019) Circadian rhythms of melatonin in haemolymph and optic lobes of Chinese mitten crab (Eriocheir sinensis) and Chinese grass shrimp (Palaemonetes sinensis). Biol Rhythm Res 50:400–407. https://doi.org/10.1080/09291016.2018.1452592
Hopkins PM (2012) The eyes have it: a brief history of crustacean neuroendocrinology. Gen Comp Endocr 175:357–366. https://doi.org/10.1016/j.ygcen.2011.12.002
Hsu YWA, Messinger DI, Chung JS, Webster SG, de la Iglesia HO, Christie AE (2006) Members of the crustacean hyperglycemic hormone (CHH) peptide family are differentially distributed both between and within the neuroendocrine organs of cancer crabs: implications for differential release and pleiotropic function. J Exp Biol 209:3241–3256. https://doi.org/10.1242/jeb.02372
Huang HY, Fu CR, Chen XL, Gong J, Huang XS, Ye HH (2015) Molt-inhibiting hormone (MIH) gene from the green mud crab Scylla paramamosain and its expression during the molting and ovarian cycle. Aquac Res 46:2665–2675. https://doi.org/10.1111/are.12421
Kang BJ, Okutsu T, Tsutsui N, Shinji J, Bae SH, Wilder MN (2014) Dynamics of vitellogenin and vitellogenesis-inhibiting hormone levels in adult and subadult whiteleg shrimp, Litopenaeus vannamei: relation to molting and eyestalk ablation. Biol Reprod 90:1. https://doi.org/10.1095/biolreprod.113.112243
Katayama H (2016) Structure-activity relationship of Crustacean peptide hormones. Biosci Biotech Bioch 80(4):633–641. https://doi.org/10.1080/09168451.2015.1116932
Lacombe C, Greve P, Martin G (1999) Overview on the sub-grouping of the crustacean hyperglycemic hormone family. Neuropeptides 33:71–80. https://doi.org/10.1054/npep.1999.0016
Li K, Chen LQ, Zhou ZL, Li EC, Zhao XQ, Guo H (2006) The site of vitellogenin synthesis in Chinese mitten-handed crab Eriocheir sinensis. Comp Biochem Physiol B Biochem Mol Biol 143:453–458. https://doi.org/10.1016/j.cbpb.2005.12.019
Li GL, Chen HP, Deng SP, Ye M, Jiang S, Chan SF, Zhu CH (2015) In vivo and in vitro inhibitory action of 17 beta-estradiol and environmental estrogen 4-nonylphenol on gonad-inhibiting hormone (GIH) expression in the eyestalks of Litopenaeus vannamei. Genet Mol Res 14(4):14056–14065. https://doi.org/10.4238/2015.October.29.25
Li X, Chen T, Han Y, Huang M, Jiang H, Huang J, Tao M, Xu R, Xie Q, Su S (2021) Potential role of Methoprene-tolerant (Met) in methyl farnesoate-mediated vitellogenesis in the Chinese mitten crab (Eriocheir sinensis). Comp Biochem Physiol B Biochem Mol Biol. https://doi.org/10.1016/j.cbpb.2020.110524
Liu L, Laufer H, Gogarten PJ, Wang M (1997) cDNA cloning of a mandibular organ inhibiting hormone from the spider crab Libinia emarginata. Invert Neurosci IN 3:199–204. https://doi.org/10.1007/BF02480375
Liu ZQ, Jiang XH, Xiong LW, Qiu GF (2016) A novel SoxB2 gene is required for maturation of sperm nucleus during spermiogenesis in the Chinese mitten crab, Eriocheir sinensis. Sci Rep 6. https://doi.org/10.10138/srep32139
Liu JH, Zhou TT, Wang CG, Wang W, Chan SM (2020) Comparative transcriptomics reveals eyestalk ablation induced responses of the neuroendocrine-immune system in the Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immun 106:823–832. https://doi.org/10.1016/j.fsi.2020.08.029
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Nagaraju GPC (2011) Reproductive regulators in decapod crustaceans: an overview. J Exp Biol 214:3–16. https://doi.org/10.1242/jeb.047183
Okumura T, Aida K (2001) Effects of bilateral eyestalk ablation on molting and ovarian development in the giant freshwater prawn, Macrobrachium rosenbergii. Fish Sci 67:1125–1135. https://doi.org/10.1046/j.1444-2906.2001.00370.x
Sathapondecha P, Panyim S, Udomkit A (2017) In vitro study of a putative role of gonad-inhibiting hormone in oocyte growth stimulation in Penaeus monodon. Aquac Res 48:5846–5853. https://doi.org/10.1111/are.13407
Song JA, Kho KH, Park YS, Choi JY, Choi CY (2021) Comparison of the effect of red light exposure and eyestalk ablation for inducing sexual maturation and improving egg quality in the cleaner shrimp Lysmata amboinensis. Crustaceana 94:551–571. https://doi.org/10.1163/15685403-bja10111
Subramoniam T (2011) Mechanisms and control of vitellogenesis in crustaceans. Fish Sci 77:1–21. https://doi.org/10.1007/s12562-010-0301-z
Tao T, Xie X, Liu M, Jiang Q, Zhu D (2017) Cloning of two carboxylesterase cDNAs from the swimming crab Portunus trituberculatus: molecular evidences for their putative roles in methyl farnesotae degradation. Comp Biochem Physiol B Biochem Mol Biol 203:100–107. https://doi.org/10.1016/j.cbpb.2016.10.001
Treerattrakool S, Panyim S, Udomkit A (2011) Induction of ovarian maturation and spawning in Penaeus monodon Broodstock by double-stranded RNA. Mar Biotechnol 13:163–169. https://doi.org/10.1007/s10126-010-9276-0
Treerattrakool S, Boonchoy C, Urtgam S, Panyim S, Udomkit A (2014) Functional characterization of recombinant gonad-inhibiting hormone (GIH) and implication of antibody neutralization on induction of ovarian maturation in marine shrimp. Aquaculture 428:166–173. https://doi.org/10.1016/j.aquaculture.2014.03.009
Verghese B, Radhakrishnan EV, Padhi A (2008) Effect of moulting, eyestalk ablation, starvation and transportation on the immune response of the Indian spiny lobster, Panulirus homarus. Aquac Res 39:1009–1013. https://doi.org/10.1111/j.1365-2109.2008.01949.x
Vrinda S, Jasmin C, Philip R, Singh ISB (2018) Thioredoxin fused CHH1 protein as antigen for polyclonal antisera: application to regulate glycemia in Penaeus monodon. Indian J Exp Biol 56(2):83–92
Wainwright G, Webster SG, Wilkinson MC, Chung JS, Rees HH (1996) Structure and significance of mandibular organ-inhibiting hormone in the crab, Cancer pagurus: involvement in multihormonal regulation of growth and reproduction. J Biol Chem 271:12749–12574. https://doi.org/10.1074/JBC.271.22.12749
Wang ZK, Luan S, Meng XH, Cao BX, Luo K, Kong J (2019) Comparative transcriptomic characterization of the eyestalk in Pacific white shrimp (Litopenaeus vannamei) during ovarian maturation. Gen Comp Endocr 274:60–72. https://doi.org/10.1016/j.ygcen.2019.01.002
Wang M, Ye HH, Miao LW, Li XR (2022) Role of short neuropeptide F in regulating eyestalk neuroendocrine systems in the mud crab Scylla paramamosain. Aquac. https://doi.org/10.1016/j.aquaculture.2022.738493
Webster SG, Keller R, Dircksen H (2012) The CHH-Superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. Gen Comp Endocr 175(2):217–233. https://doi.org/10.1016/j.ygcen.2011.11.035
Wu X, Liu MM, Pan J, Chen H, Zeng CS, Cheng YX (2017) The ovarian development pattern of pond-reared Chinese mitten crab, Eriocheir sinensis H. Milne-edwards, 1853. Crustaceana 90:449–470. https://doi.org/10.1163/15685403-00003662
Wu HR, Ge MT, Zhou XH, Jiang ST, Lin L, Lu JF (2019) Nutritional qualities of normal and precocious adult male Chinese mitten crabs (Eriocheir sinensis). Aquac Res 50:2267–2275. https://doi.org/10.1111/are.14107
Wu HR, Ge MT, Chen HF, Jiang ST, Lin L, Lu JF (2020) Comparison between the nutritional qualities of wild-caught and rice-field male Chinese mitten crabs (Eriocheir sinensis). LWT-Food Sci Technol. https://doi.org/10.1016/j.lwt.2019.108663
Yang ZB, Zhao YL, Li N, Yang J (2008) Effect of waterborne copper on the microstructures and ultrastructure of the X-organ sinus gland complex in Eriocheir sinensis. B Environ Contam Tox 80:68–73. https://doi.org/10.1007/s00128-007-9318-0
Zhang X, Shi JL, Sun YL, Wang YL, Zhang ZP (2022a) The potential role of eyestalk in the immunity of Litopenaeus vannamei to vibrio infection. Fish Shellfish Immun 121:62–73. https://doi.org/10.1016/j.fsi.2021.12.057
Zhang X, Shi JL, Sun YL, Wang YL, Zhang ZP (2022b) The potential role of eyestalk in the immunity of Litopenaeus vannamei to vibrio parahaemolyticus infection II. from the perspective of long non-coding RNA. Fish Shellfish Immun 124:300–312. https://doi.org/10.1016/j.fsi.2022.04.007
Zhou MC, Jia XW, Wan HF, Wang SH, Zhang X, Zhang ZP, Wang YL (2019) miR-34 regulates reproduction by inhibiting the expression of MIH, CHH, EcR, and FAMeT genes in mud crab Scylla paramamosain. Mol Reprod Dev 86:122–131. https://doi.org/10.1002/mrd.23063
Acknowledgements
This research was supported by Open Funding Project of the Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture and Rural Affairs [K2022-04], Anhui Provincial College Students Innovation and Entrepreneurship Project [S202110364022], Key R and D Program of Chuzhou [2020ZN005], and Fishery Industrial System of Anhui Province, China [[2021]711]. Thanks to Xuancheng Jinxin crab seed professional cooperative for providing experimental animals.
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Open Funding Project of the Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture and Rural Affairs K2022-04, Xilei Li, Anhui Provincial College Students Innovation and Entrepreneurship Project [S202110364022], Xilei Li, Key R and D Program of Chuzhou [2020ZN005], Xilei Li, and Fishery Industrial System of Anhui Province, China, China [[2021]711], Xilei Li.
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Ding, S., Huang, M., Sheng, N. et al. RNAi-mediated knockdown of the mandibular organ-inhibiting hormone (MOIH) gene stimulates vitellogenesis in the Chinese mitten crab Eriocheir sinensis. Fish Sci 89, 399–408 (2023). https://doi.org/10.1007/s12562-023-01680-y
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DOI: https://doi.org/10.1007/s12562-023-01680-y