Ovarian yolk formation in fishes: Molecular mechanisms underlying formation of lipid droplets and vitellogenin-derived yolk proteins

General and Comparative Endocrinology

Volumn 221, Issue , 2015, Pages 9-15

  Hiramatsu, Naoshi ^a   Todo, Takashi ^a   Sullivan, Craig V ^b   Schilling, Justin ^c   Reading, Benjamin J ^c   Matsubara, Takahiro ^d   Ryu, Yong Woon ^a,d   Mizuta, Hiroko ^a   Luo, Wenshu ^a,e   Nishimiya, Osamu ^a   Wu, Meiqin ^a   Mushirobira, Yuji ^a   Yilmaz, Ozlem ^f   Hara, Akihiko ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b Carolina AquaGyn   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d EHIME UNIVERSITY   (Japan)

^e GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^f Natl Sch of Agronomic Res (ENSA)   (France)

Author keywords

Fish; Lipoprotein receptors; Lipoproteins; Oocyte; Vitellogenins; Yolk

Indexed keywords

FAT DROPLET; VITELLOGENIN; YOLK PROTEIN; EGG PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL ASSAY; CELL FATE; CONTROLLED STUDY; EGG YOLK; FEMALE; FISH; GROWTH RATE; MOLECULAR DYNAMICS; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPECIES COMPARISON; VITELLOGENESIS; ANIMAL; METABOLISM; OVARY;

ANIMALS; EGG PROTEINS; EGG YOLK; FEMALE; FISHES; LIPID DROPLETS; OVARY; VITELLOGENINS;

EID: 84947037492     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2015.01.025     Document Type: Article

References (45)

1. Amano H., Fujita T., Hiramatsu N., Kagawa H., Matsubara T., Sullivan C.V., Hara A. Multiple vitellogenin-derived yolk proteins in grey mullet (Mugil cephalus): disparate proteolytic patterns associated with ovarian follicle maturation. Mol. Reprod. Dev. 2008, 75(8):1307-1317.
2. Amano H., Mochizuki M., Fujita T., Hiramatsu N., Todo T., Hara A. Purification and characterization of a novel incomplete-type vitellogenin protein (VtgC) in Sakhalin taimen (Hucho perryi). Comp. Biochem. Physiol. 2010, 157(1):41-48.
3. Buisine N., Trichet V., Wolff J. Complex evolution of vitellogenin genes in salmonid fishes. Mol. Genet. Genomic 2002, 268(4):535-542.
4. Bujo H., Lindstedt K.A., Hermann M., Dalmau L.M., Nimpf J., Schneider W.J. Chicken oocytes and somatic cells express different splice variants of a multifunctional receptor. J. Biol. Chem. 1995, 270:23546-23551.
5. Damsteegt E.L., Mizuta H., Hiramatsu N., Lokman P.M. How do eggs get fat? Insights into triacylglyceride uptake in the oocytes of the shortfinned eel, Anguilla australis. Gen. Comp. Endocrinol. 2015, [this volume].
6. Davail B., Pakdel F., Bujo H., Perazzolo L.M., Waclawek M., Schneider W.J., Le Menn F. Evolution of oogenesis: the receptor for vitellogenin from the rainbow trout. J. Lipid Res. 1998, 39:1929-1937.
7. Divers S.L., McQuillan H.J., Matsubara T., Todo T., Lokman P.M. Effects of reproductive stage and 11-ketotestosterone on LPL mRNA levels in the ovary of the shortfinned eel. J. Lipid Res. 2010, 51(11):3250-3258.
8. Dominguez G.A., Quattro J.M., Denslow N.D., Kroll K.J., Prucha M.S., Porak W.F., Grier H.J., Sabo-Attwood T.L. Identification and transcriptional modulation of the largemouth bass Micropterus salmoides, vitellogenin receptor during oocyte development by insulin and sex steroids. Biol. Reprod. 2012, 87(3):67. [1-12].
9. Endo T., Todo T., Lokman P.M., Kudo H., Ijiri S., Adachi S., Yamauchi K. Androgens and very low density lipoprotein are essential for the growth of previtellogenic oocytes from Japanese eel, Anguilla japonica, in vitro. Biol. Reprod. 2011, 84(4):816-825.
10. Finn R.N., Kristoffersen B.A. Vertebrate vitellogenin gene duplication in relation to the "3R hypothesis": correlation to the pelagic egg and the oceanic radiation of teleosts. PLoS One 2007, 2(1):e169.
11. Finn R.N., Wamboldt M., Fyhn H.J. Differential processing of yolk proteins during oocyte hydration in marine fishes (Labridae) that spawn benthic and pelagic eggs. Mar. Ecol. Prog. Ser. 2002, 237:217-226.
12. Goldstein J.L., Brown M.S., Anderson R.G.W., Russel D.W., Schneider W.J. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Ann. Rev. Cell Biol. 1985, 1:1-39.
13. Hiramatsu N., Matsubara T., Hara A., Donato D.M., Hiramatsu K., Denslow N.D., Sullivan C.V. Identification, purification and classification of multiple forms of vitellogenin from white perch (Morone americana). Fish Physiol. Biochem. 2002, 26(4):355-370.
14. Hiramatsu N., Matsubara T., Weber G.M., Sullivan C.V., Hara A. Vitellogenesis in aquatic animals. Fish. Sci. 2002, 68(Suppl. I):694-699.
15. Hiramatsu N., Cheek A.O., Sullivan C.V., Matsubara T., Hara A. Vitellogenesis and endocrine disruption. Biochemistry and Molecular Biology of Fishes 2005, 431-471. Elsevier, Amsterdam. sixth ed. T.P. Mommsen, T.W. Moon (Eds.).
16. Hiramatsu N., Matsubara T., Fujita T., Sullivan C.V., Hara A. Multiple piscine vitellogenins: biomarkers of fish exposure to endocrine disruptors in aquatic animals. Mar. Biol. 2006, 149(1):35-47.
17. Hiramatsu N., Luo W., Reading B.J., Sullivan C.V., Mizuta H., Ryu Y.-W., Nishimiya O., Todo T., Hara A. Ovarian lipoprotein receptors in teleosts. Fish Physiol. Biochem. 2013, 39(1):29-32.
18. Hussain M.M., Strickland D.K., Bakillah A. The mammalian low-density lipoprotein receptor family. Annu. Rev. Nutr. 1999, 19:141-172.
19. Ibanez A.J., Peinado-Onsurbe J., Sanchez E., Cerda-Reverter J.M., Prat F. Lipoprotein lipase (LPL) is highly expressed and active in the ovary of European sea bass (Dicentrarchus labrax L.), during gonadal development. Comp. Biochem. Physiol. A 2008, 150(3):347-354.
20. Kolarevic J., Nerland A., Nilsen F., Finn R.N. Goldsinny wrasse (Ctenolabrusrupestris) is an extreme vtgAa-type pelagophil teleost. Mol. Reprod. Dev. 2008, 75(6):1011-1020.
21. Kwon J.Y., Prat F., Randall C., Tyler C.R. Molecular characterization of putative yolk processing enzymes and their expression during oogenesis and embryogenesis in rainbow trout Oncorhynchus mykiss. Biol. Reprod. 2001, 65(6):1701-1709.
22. Lancaster P.M., Tyler C.R. Developmental expression and modulation of the vitellogenin receptor in ovarian follicles of the rainbow-trout, Oncorhynchus mykiss. J. Exp. Zool. 1994, 269(5):458-466.
23. Luckenbach J.A., Goetz F.W., Swanson P. Expressed sequence tags (ESTs) of follicle/interstitial cell enriched ovarian tissue from previtellogenic coho salmon. CYBIUM 2008, 32(2):142-144.
24. Luo W., Ito Y., Mizuta H., Massaki K., Hiramatsu N., Todo T., Reading B.J., Sullivan C.V., Hara A. Molecular cloning and partial characterization of an ovarian receptor with seven ligand binding repeats, an orthologue of low-density lipoprotein receptor, in the cutthroat trout (Oncorhynchus clarki). Comp. Biochem. Physiol. A 2013, 166(2):263-271.
25. Mahley R.W., Ji Zhong-Sheng Remnant lipoprotein metabolism: key pathways involving cell-surface heparin sulfate proteoglycans and apolipoprotein E. J. Lipid Res. 1999, 40:1-16.
26. Matsubara T., Ohkubo N., Andoh T., Sullivan C.V., Hara A. 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. Dev. Biol. 1999, 213(1):18-32.
27. Mizuta H., Luo W., Ito Y., Mushirobira Y., Todo T., Hara A., Reading B.J., Sullivan C.V., Hiramatsu N. Ovarian expression and localization of a vitellogenin receptor with eight ligand binding repeats in the cutthroat trout (Oncorhynchus clarki). Comp. Biochem. Physiol. B 2013, 166(1):81-90.
28. Mushirobira Y., Mizuta H., Luo W., Morita Y., Sawaguchi S., Matsubara T., Hiramatsu N., Todo T., Hara A. Changes in levels of dual vitellogenin transcripts and proteins in cutthroat trout Oncorhynchus clarki during ovarian development. Nippon Suisan Gakkaishi 2013.
29. Mushirobira, Y., Mizuta, H., Luo, W., Todo, T., Hara, A., Reading, B.J., Sullivan, C.V., Hiramatsu, N., 2014. Ligand binding properties of ovarian lipoprotein receptors in the cutthroat trout. In: Abstract Book of 10th International Symposium on Reproductive Physiology of Fish, "Expanding the knowledge base of reproductive success from genes to the environment", Olhao, Portugal, 25-30 May, p. 173. Available online: http://ccmar.ualg.pt/10ISRPF/.
30. Polzonetti-Maguni A.M., Mosconi G., Soverchia L., Kikuyama S., Carnevali O. Multihormonal control of vitellogenesis in lower vertebrates. Int. Rev. Cytol. 2004, 239:1-46.
31. Reading B.J., Hiramatsu N., Sawaguchi S., Matsubara T., Hara A., Lively M.O., Sullivan C.V. Conserved and variant molecular and functional features of multiple egg yolk precursor proteins (vitellogenins) in white perch (Morone americana) and other teleosts. Mar. Biotechnol. 2009, 11(2):169-187.
32. Reading B.J., Hiramatsu N., Sullivan C.V. Disparate binding of three types of vitellogenin to multiple forms of vitellogenin receptor in white perch. Biol. Reprod. 2011, 84(2):392-399.
33. Reading, B.J., Hiramatsu, N., Schilling, J., Molloy, K.T., Glassbrook, N., Mizuta, H., Luo, W., Baltzegar, D.A., Williams, V.N., Hara, A., Sullivan, C.V., 2014. Lrp13 is a novel vertebrate lipoprotein receptor that binds vitellogenins in teleost fishes. (Chapter 257, 2272 p.).
34. Reading B.J., Sullivan C.V. Vitellogenesis in fishes. Encyclopedia in Fish Physiology: From Genome to Environment. The Reproductive Organs and Processes 2011, 635-646. Elsevier, Maryland Heights, Missouri. A.P. Ferrel (Ed.).
35. Ryu Y.-W., Tanaka R., Kasahara A., Ito Y., Hiramatsu N., Todo T., Sullivan C.V., Hara A. Molecular cloning and transcript expression of genes encoding two types of lipoprotein lipase in the ovary of cutthroat trout, Oncorhynchus clarki. Zool. Sci. 2013, 30(3):224-237.
36. Ryu, Y-W., Todo, T., Hiramatsu, N., Matsubara, T., Sullivan, C.V., Hara, A., 2014. Very low-density lipoprotein is primary carrier of neutral lipids to ooplasm lipid droplets in teleosts. In: Abstract Book of 10th International Symposium on Reproductive Physiology of Fish, "Expanding the knowledge base of reproductive success from genes to the environment", Olhao, Portugal, 25-30 May, p. 70. Available online: http://ccmar.ualg.pt/10ISRPF/.
37. Sawaguchi S., Kagawa H., Ohkubo N., Hiramatsu N., Sullivan C.V., Matsubara T. 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. Mol. Reprod. Dev. 2006, 73(6):719-736.
38. Sawaguchi S., Ohkubo N., Amano H., Hiramatsu N., Hara A., Sullivan C.V., Matsubara T. Controlled accumulation of multiple vitellogenins into oocytes during vitellogenesis in the barfin flounder, Verasper moseri. CYBIUM 2008, 32(2):262.
39. Schilling J., Nepomuceno A., Muddiman D.C., Schaff J.E., Daniels H.V., Reading B.J. Compartment proteomics analysis of white perch (Morone americana) ovary using support vector machines. J. Proteome Res. 2014, 13(3):1515-1526.
40. Stifani S., Le Menn F., Rodriguez J.N., Schneider W.J. Regulation of oogenesis: the piscine receptor for vitellogenin. Biochem. Biophys. Acta 1990, 1045(3):271-279.
41. Tyler C.R., Lubberink K. Identification of four ovarian receptor proteins that bind vitellogenin but not other homologous plasma lipoproteins in the rainbow trout, Oncorhynchus mykiss. J. Comp. Physiol. B 1996, 166(1):11-20.
42. Williams D.L., Connelly M.A., Temel R.E., Swarnakar S., Phillips M.C., de la Llera-Moya M., Rothblat G.H. Scavenger receptor BI and cholesterol trafficking. Curr. Opin. Lipidol. 1999, 10:329-339.
43. Williams V.N., Reading B.J., Hiramatsu N., Amano H., Grassbrook N., Hara A., Sullivan C.V. Multiple vitellogenins and product yolk proteins in striped bass, Morone saxatilis: molecular characterization and processing during oocyte growth and maturation. Fish Physiol. Biochem. 2014, 40(2):395-415.
44. Williams V.N., Reading B.J., Amano H., Hiramatsu N., Schilling J., Islam Williams T., Gross K., Sullivan C.V. Proportional accumulation of yolk proteins derived from multiple vitellogenins is precisely regulated during vitellogenesis in striped bass (Morone saxatilis). J. Exp. Zool. A 2014, 321(6):301-315.
45. Yilmaz O., Prat F., Ibáñez A.J., Amano H., Koksoy S., Sullivan C.V. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: status and perspectives on multiplicity and functioning of vitellogenins. Gen. Comp. Endocrinol. 2015, 221:16-22.