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Zitao XIONG, Jiazhe YANG, Shun ZHANG, Yajun WANG, Shanliang XU, Chunyang GUO, Danli WANG. Expression and localization of vitellogenin genes (VTG) and receptor (VGR) in the gonad development of silver pomfret Pampus argenteus[J]. Journal of Oceanology and Limnology, 2023, 41(4): 1575-1592

Expression and localization of vitellogenin genes (VTG) and receptor (VGR) in the gonad development of silver pomfret Pampus argenteus

Zitao XIONG1, Jiazhe YANG1, Shun ZHANG1, Yajun WANG1, Shanliang XU1,2, Chunyang GUO1, Danli WANG1
1 School of Marine Sciences, Ningbo University, Ningbo 315211, China;
2 Key Laboratory of Applied Marine Biotechnology, Ningbo University, Chinese Ministry of Education, Ningbo 315211, China
Vitellogenesis is the main event of oocyte growth in oviparous animals, which is mainly manifested by the accumulation of vitellogenin (VTG). The accumulation of vitellogenin depends mainly on the absorption of exogenous vitellogenin, which enters oocyte through endocytosis mediated by its receptor (VGR). We investigated the expression and localization of VTG and VGR during gonad development of Pampus argenteus. The qPCR results show that vtgs were not expressed in male fish, but in the ovary and liver of female fish; the expression levels went up at first and then down. The expression levels of vgr in the testis were low and only 1%–3% of that in ovary. ELISA results show that during the ovarian development of P. argenteus, VTG in liver, serum, and ovary all showed a trend from increasing to decreasing. However, VTG in liver peaked in Stage Ⅳ, and in serum and ovary peaked in Stage V, reflecting changes in the characteristics of VTG in the liver (synthesis), blood (transport), and ovaries (accumulation). During gonad development, VGR in the ovaries first increased and then decreased, reaching a peak in Stage V, in contrast to vgr mRNA expression. The VGR content in the testis was extremely low and stable, consistent with vgr mRNA. Immunohistochemistry results show that the location and intensity of VTG and VGR positive signals were synchronized with the changes of their protein content, which revealed that VTG was mainly synthesized in the liver cytoplasm, secreted into the blood, and transported to ovary in Stage Ⅲ. VGR is highly expressed in oocytes in Stage Ⅱ. In Stage Ⅲ, a large amount of VTG reaches the ovary, when VGR begins to translate and is subsequently transported to the plasma membrane of the oocyte. Therefore, the positive signal of VGR was stronger near the plasma membrane of oocytes in Stages Ⅰ and Ⅱ. By using qPCR, ELISA, and immunohistochemistry, the synthesis, transport, and accumulation of vitellogenin were elucidated and the mechanism of its endocytosis on egg membrane mediated by VTG during the development of P. argenteus was revealed preliminarily.
Key words:    Pampus argenteus|vitellogenin (VTG)|vitellogenin receptor (VGR)|vitellogenesis   
Received: 2022-01-12   Revised:
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Avarre J C, Michelis R, Tietz A et al. 2003. Relationship between vitellogenin and vitellin in a marine shrimp(Penaeus semisulcatus) and molecular characterization of vitellogenin complementary DNAs1. Biology of Reproduction, 69(1): 355-364,
Chen J S, Sappington T W, Raikhel A S. 1997. Extensive sequence conservation among insect, nematode, and vertebrate vitellogenins reveals ancient common ancestry.Journal of Molecular Evolution, 44(4): 440-451,
Finn R N, Kristoffersen B A. 2007. Vertebrate vitellogenin gene duplication in relation to the “3R hypothesis”:correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One, 2(1): e169,
Hara A, Hiramatsu N, Fujita T. 2016. Vitellogenesis and choriogenesis in fishes. Fisheries Science, 82(2): 187-202,
Hiramatsu N, Chapman R W, Lindzey J K et al. 2004.Molecular characterization and expression of vitellogenin receptor from white perch (Morone americana). Biology of Reproduction, 70(6): 1720-1730,
Hiramatsu N, Cheek A O, Sullivan C V et al. 2005.Vitellogenesis and endocrine disruption. Biochemistry and Molecular Biology of Fishes, 6: 431-471,
Hiramatsu N, Ichikawa N, Fukada H et al. 2002a.Identification and characterization of proteases involved in specific proteolysis of vitellogenin and yolk proteins in salmonids. Journal of Experimental Zoology, 292(1):11-25,
Hiramatsu N, Matsubara T, Fujita T et al. 2006. Multiple piscine vitellogenins: biomarkers of fish exposure to estrogenic endocrine disruptors in aquatic environments.Marine Biology, 149(1): 35-47,
Hiramatsu N, Matsubara T, Weber G M et al. 2002b.Vitellogenesis in aquatic animals. Fisheries Science, 68(sup1): 694-699,
Lan W Q, Che X, Xu Q L et al. 2018. Sensory and chemical assessment of silver pomfret (Pampus argenteus) treated with Ginkgo biloba leaf extract treatment during storage in ice. Aquaculture and Fisheries, 3(1): 30-37,
Li A K, Sadasivam M, Ding J L. 2003. Receptor-ligand interaction between vitellogenin receptor (VtgR) and vitellogenin (Vtg), implications on low density lipoprotein receptor and apolipoprotein B/E. The first three ligand-binding repeats of VtgR interact with the amino-terminal region of Vtg. Journal of Biological Chemistry, 278(5): 2799-2806,
Little D C, Coward K, Bhujel R C et al. 2000. Effect of broodfish exchange strategy on the spawning performance and sex steroid hormone levels of Oreochromis niloticus broodfish in hapas. Aquaculture, 186(1-2): 77-88, 00368-3.
Liu C, Li K, Wang F et al. 2011. The full length cDNA cloning and expression profile of vitellogenin C(Vg C) gene from swordtail fish Xiphophorus helleri. Journal of Fisheries of China, 35(10): 1441-1449,
Lubzens E, Bobe J, Young G et al. 2017. Maternal investment in fish oocytes and eggs: the molecular cargo and its contributions to fertility and early development. Aquaculture, 472: 107-143,
Lubzens E, Young G, Bobe J et al. 2010.Oogenesis in teleosts: how fish eggs are formed. General and Comparative Endocrinology, 165(3): 367-389,
Luckenbach J A, Iliev D B, Goetz F W et al. 2008.Identification of differentially expressed ovarian genes during primary and early secondary oocyte growth in coho salmon, Oncorhynchus kisutch. Reproductive Biology and Endocrinology, 6: 2,
Luo M K, Zhao J L, Jeerawat T et al. 2015. Changes in sex steroid hormones, vitellogenin content, and Vtg mRNA expression during ovarian development in Oreochromis niloticus. Journal of Fishery Sciences of China, 22(6):1123-1132. (in Chinese with English abstract)
Matsubara T, Nagae M, Ohkubo N et al. 2003. Multiple vitellogenins and their unique roles in marine teleosts.Fish Physiology and Biochemistry, 28(1-4): 295-299,
Matsubara T, Ohkubo N, Andoh T et al. 1999. Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost that spawns pelagic eggs. Developmental Biology, 213(1):18-32,
Mizuta H, Luo W S, Ito Y et al. 2013. Ovarian expression and localization of a vitellogenin receptor with eight ligand binding repeats in the cutthroat trout (Oncorhynchus clarki). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 166(1): 81-90,
Okumura T, Yamano K, Sakiyama K. 2007. Vitellogenin gene expression and hemolymph vitellogenin during vitellogenesis, final maturation, and oviposition in female kuruma prawn, Marsupenaeus japonicus.Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 147(4): 1028-1037,
Patiño R, Sullivan C V. 2002. Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiology and Biochemistry, 26(1): 57-70,
Perazzolo L M, Coward K, Davail B et al. 1999. Expression and localization of messenger ribonucleic acid for the vitellogenin receptor in ovarian follicles throughout oogenesis in the rainbow trout, Oncorhynchus mykiss.Biology of Reproduction, 60(5): 1057-1068,
Pousis C, Santamaria N, Zupa R et al. 2012. Expression of vitellogenin receptor gene in the ovary of wild and captive Atlantic bluefin tuna (Thunnus thynnus). Animal Reproduction Science, 132(1-2): 101-110,
Reading B J, Hiramatsu N, Sawaguchi S et al. 2009.Conserved and variant molecular and functional features of multiple egg yolk precursor proteins (vitellogenins) in white perch (Morone americana) and other teleosts.Marine Biotechnology, 11(2): 169-187,
Sawaguchi S, Kagawa H, Ohkubo N et al. 2006. Molecular characterization of three forms of vitellogenin and their yolk protein products during oocyte growth and maturation in red seabream (Pagrus major), a marine teleost spawning pelagic eggs. Molecular Reproduction and Development, 73(6): 719-736,
Tarrant A M, Atkinson S, Atkinson M J. 1999. Estrone and estradiol-17β concentration in tissue of the scleractinian coral, Montipora verrucosa. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 122(1): 85-92,
Tsutsui N, Saido-Sakanaka H, Yang W J et al. 2004.Molecular characterization of a cDNA encoding vitellogenin in the coonstriped shrimp, Pandalus hypsinotus and site of vitellogenin mRNA expression.Journal of Experimental Zoology Part A: Comparative Experimental Biology, 301A(10): 802-814,
Tyler C R, Lancaster P. 1993. Isolation and characterization of the receptor for vitellogenin from follicles of the rainbow trout, Oncorhynchus mykiss. Journal of Comparative Physiology B, 163(3): 225-233,
Wallace R A. 1985. Vitellogenesis and oocyte growth in nonmammalian vertebrates. In: Browder L W ed.Oogenesis. Springer, New York. p.127-177,
Wang T F, Zhang D Y, Guo C Y et al. 2017. The gonadal development and changes of serum steroid levels of cultured Pampus argenteus. Journal of Fisheries of China, 41(2): 198-211. (in Chinese with English abstract)
Williams V N, Reading B J, Amano H et al. 2014.Proportional accumulation of yolk proteins derived from multiple vitellogenins is precisely regulated during vitellogenesis in striped bass (Morone saxatilis). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 321(6): 301-315,
Wu L T, Hui J H L, Chu K H. 2013. Origin and evolution of yolk proteins: expansion and functional diversification of large lipid transfer protein superfamily. Biology of Reproduction, 88(4): 102,
Xue R, Wang X Y, Xu S H et al. 2018. Expression profile and localization of vitellogenin mRNA and protein during ovarian development in turbot (Scophthalmus maximus).Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology, 226: 53-63,
Yilmaz O, Prat F, Ibánez A J et al. 2016. Multiple vitellogenins and product yolk proteins in European sea bass (Dicentrarchus labrax): molecular characterization, quantification in plasma, liver and ovary, and maturational proteolysis. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 194-195:71-86,
Zmora N, Trant J, Chan S M et al. 2007. Vitellogenin and its messenger RNA during ovarian development in the female blue crab, Callinectes sapidus: gene expression, synthesis, transport, and cleavage. Biology of Reproduction, 77(1):138-146,
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