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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2013

Open Access 01-12-2013 | Research

Cloning and characterization of a novel oocyte-specific gene encoding an F-Box protein in rainbow trout (Oncorhynchus mykiss)

Authors: Lei Wang, Swamy K Tripurani, Warapond Wanna, Caird E Rexroad III, Jianbo Yao

Published in: Reproductive Biology and Endocrinology | Issue 1/2013

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Abstract

Background

Oocyte-specific genes play critical roles in oogenesis, folliculogenesis and early embryonic development. The objectives of this study were to characterize the expression of a novel oocyte-specific gene encoding an F-box protein during ovarian development in rainbow trout, and identify its potential interacting partners in rainbow trout oocytes.

Methods

Through analysis of expressed sequence tags (ESTs) from a rainbow trout oocyte cDNA library, a novel transcript represented by ESTs only from the oocyte library was identified. The complete cDNA sequence for the novel gene (named fbxoo) was obtained by assembling sequences from an EST clone and a 5′RACE product. The expression and localization of fbxoo mRNA and protein in ovaries of different developmental stages were analyzed by quantitative real time PCR, immunoblotting, in situ hybridization and immunohistochemistry. Identification of Fbxoo binding proteins was performed by yeast two-hybrid screening.

Results

fbxoo mRNA is specifically expressed in mature oocytes as revealed by tissue distribution analysis. The fbxoo cDNA sequence is 1,996 bp in length containing an open reading frame, which encodes a predicted protein of 514 amino acids. The novel protein sequence does not match any known protein sequences in the NCBI database. However, a search of the Pfam protein database revealed that the protein contains an F-box motif at the N-terminus, indicating that Fbxoo is a new member of the F-box protein family. The expression of fbxoo mRNA and protein is high in ovaries at early pre-vitellogenesis stage, and both fbxoo mRNA and protein are predominantly expressed in early pre-vitellogenic oocytes. Several proteins including tissue inhibitor of metalloproteinase 2 (Timp2) were identified as potential Fbxoo protein binding partners.

Conclusions

Results suggest that the novel oocyte-specific F-box protein may play an important role in early oocyte development by regulating other critical proteins involved in oogenesis in rainbow trout.
Appendix
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Literature
1.
Sun Q, Liu K, Kikuchi K: Oocyte-Specific Knockout: A Novel In Vivo Approach for Studying Gene Functions During Folliculogenesis, Oocyte Maturation, Fertilization, and Embryogenesis. Biol Reprod. 2008, 79: 1014-1020. 10.1095/biolreprod.108.070409.CrossRefPubMed
2.
Zheng P, Dean J: Oocyte-specific genes affect folliculogenesis, fertilization, and early development. Semin Reprod Med. 2007, 25: 243-251. 10.1055/s-2007-980218.CrossRefPubMed
3.
Rajkovic APS, Ballow D, Suzumori N, Matzuk MM: NOBOX Deficiency Disrupts Early Folliculogenesis and Oocyte-Specific Gene Expression. Science. 2004, 305: 1157-1159. 10.1126/science.1099755.CrossRefPubMed
4.
Soyal SM, Amleh A, Dean J: FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development. 2000, 127: 4645-4654.PubMed
5.
Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM: Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996, 383: 531-535. 10.1038/383531a0.CrossRefPubMed
6.
Xu Y, Lei Y, Liu Q, Liu Y, Liu S, Cheng H, Deng F: Cloning, characterization and expression of zvep, a novel vitelline envelope-specific gene in the zebrafish ovary. Mol Reprod Dev. 2009, 76: 593-600. 10.1002/mrd.20985.CrossRefPubMed
7.
Dai L, Ma W, Li J, Xu Y, Li W, Zhao Y, Deng F: Cloning and characterization of a novel oocyte-specific gene zorg in zebrafish. Theriogenology. 2009, 71: 441-449. 10.1016/j.theriogenology.2008.07.028.CrossRefPubMed
8.
Ramachandra RK, Lankford SE, Weber GM, Rexroad CE, Yao J: Identification of OORP-T, a novel oocyte-specific gene encoding a protein with a conserved oxysterol binding protein domain in rainbow trout. Mol Reprod Dev. 2007, 74: 502-511. 10.1002/mrd.20628.CrossRefPubMed
9.
Qiu GF, Weber GM, Rexroad CE, Yao J: Identification of RtGST-1, a novel germ cell-specific mRNA-like transcript predominantly expressed in early previtellogenic oocytes in rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev. 2008, 75: 723-730. 10.1002/mrd.20827.CrossRefPubMed
10.
Kishi T, Ikeda A, Koyama N, Fukada J, Nagao R: A refined two-hybrid system reveals that SCFCdc4-dependent degradation of Swi5 contributes to the regulatory mechanism of S-phase entry. Proc Natl Acad Sci U S A. 2008, 105: 14497-14502. 10.1073/pnas.0806253105.PubMedCentralCrossRefPubMed
11.
Varshavsky A: The ubiquitin system. Trends Biochem Sci. 1997, 22: 383-387. 10.1016/S0968-0004(97)01122-5.CrossRefPubMed
12.
Jin J, Ang XL, Shirogane T, Wade Harper J: Indentification of substrates for F-box proteins. Methods Enzymol. 2005, 399: 287-309.CrossRefPubMed
13.
Craig KL, Tyers M: The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol. 1999, 72: 299-328. 10.1016/S0079-6107(99)00010-3.CrossRefPubMed
14.
Cenciarelli C, Chiaur DS, Guardavaccaro D, Parks W, Vidal M, Pagano M: Identification of a family of human F-box proteins. Curr Biol. 1999, 9: 1177-1179. 10.1016/S0960-9822(00)80020-2.CrossRefPubMed
15.
Tyler CR, Nagler JJ, Pottinger TG, Turner MA: Effects of unilateral ovariectomy on recruitment and growth of follicles in the rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem. 1994, 13: 309-316. 10.1007/BF00003435.CrossRefPubMed
16.
De La Chesnaye E, Kerr B, Paredes A, Merchant-Larios H, Méndez JP, Ojeda SR: Fbxw15/Fbxo12J is an F-box protein-encoding gene selectively expressed in oocytes of the mouse ovary. Biol Reprod. 2008, 78: 714-725. 10.1095/biolreprod.107.063826.CrossRefPubMed
17.
Paillisson A, Dade S, Callebaut I, Bontoux M, Dalbies-Tran R, Vaiman D, Monget P: Identification, characterization and metagenome analysis of oocyte-specific genes organized in clusters in the mouse genome. BMC Genomics. 2005, 6: 76-10.1186/1471-2164-6-76.PubMedCentralCrossRefPubMed
18.
Gebauer F, Xu W, Cooper GM, Richter JD: Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 1994, 13: 5712-5720.PubMedCentralPubMed
19.
Tay J, Hodgman R, Richter JD: The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol. 2000, 221: 1-9. 10.1006/dbio.2000.9669.CrossRefPubMed
20.
Sheets MD, Fox CA, Hunt T, Vande Woude G, Wickens M: The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 1994, 8: 926-938. 10.1101/gad.8.8.926.CrossRefPubMed
21.
Paynton BV, Bachvarova R: Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol Reprod Dev. 1994, 37: 172-180. 10.1002/mrd.1080370208.CrossRefPubMed
22.
Johnson ES: Protein modification by SUMO. Annu Rev Biochem. 2004, 73: 355-382. 10.1146/annurev.biochem.73.011303.074118.CrossRefPubMed
23.
Zhang Z, Liao B, Xu M, Jin Y: Post-translational modification of POU domain transcription factor Oct-4 by SUMO-1. FASEB J. 2007, 21: 3042-3051. 10.1096/fj.06-6914com.CrossRefPubMed
24.
Wei F, Scholer HR, Atchison ML: Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J Biol Chem. 2007, 282: 21551-21560. 10.1074/jbc.M611041200.CrossRefPubMed
25.
Kipreos ET, Pagano M: The F-box protein family. Genome Biol. 2000, 1 (5): reviews3002.1–3002.7
26.
Spaich S, Will RD, Just S, Kuhn C, Frank D, Berger IM, Wiemann S, Korn B, Koegl M, Backs J, et al: F-box and leucine-rich repeat protein 22 is a cardiac-enriched F-box protein that regulates sarcomeric protein turnover and is essential for maintenance of contractile function in vivo. Circ Res. 2012, 111: 1504-1516. 10.1161/CIRCRESAHA.112.271007.CrossRefPubMed
27.
Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL: Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA. 2001, 98: 14440-14445. 10.1073/pnas.251541198.PubMedCentralCrossRefPubMed
28.
Erhardt JA, Hynicka W, DiBenedetto A, Shen N, Stone N, Paulson H, Pittman RN: A novel F box protein, NFB42, is highly enriched in neurons and induces growth arrest. J Biol Chem. 1998, 273: 35222-35227. 10.1074/jbc.273.52.35222.CrossRefPubMed
29.
Seiliez I, Panserat S, Skiba-Cassy S, Fricot A, Vachot C, Kaushik S, Tesseraud S: Feeding status regulates the polyubiquitination step of the ubiquitin-proteasome-dependent proteolysis in rainbow trout (Oncorhynchus mykiss) muscle. J Nutr. 2008, 138: 487-491.PubMed
30.
Smith G, McCrone S, Petersen S, Smith M: Expression of messenger ribonucleic acid encoding tissue inhibitor of metalloproteinases-2 within ovine follicles and corpora lutea. Endocrinology. 1995, 136: 570-576. 10.1210/en.136.2.570.PubMed
31.
Tsukamoto H, Yokoyama Y, Suzuki T, Mizuta S, Yoshinaka R: Expression and distribution of fugu TIMP-2s (fgTIMP-2a and fgTIMP-2b) mRNAs in tissues and embryos. Comp Biochem Physiol B Biochem Mol Biol. 2007, 148: 225-230. 10.1016/j.cbpb.2007.02.016.CrossRefPubMed
32.
Xu XY, Shen YB, Yang XM, Li JL: Cloning and characterization of TIMP-2b gene in grass carp. Comp Biochem Physiol B Biochem Mol Biol. 2011, 159: 115-121. 10.1016/j.cbpb.2011.02.008.CrossRefPubMed
33.
Brenner C, Adler R, Rappolee D, Pedersen R, Werb Z: Genes for extracellular-matrix-degrading metalloproteinases and their inhibitor, TIMP, are expressed during early mammalian development. Genes Dev. 1989, 3: 848-859. 10.1101/gad.3.6.848.CrossRefPubMed
34.
McIntush EW, Smith MF: Matrix metalloproteinases and tissue inhibitors of metalloproteinases in ovarian function. Reproduction. 1998, 3: 23-30. 10.1530/ror.0.0030023.CrossRef
Metadata
Title
Cloning and characterization of a novel oocyte-specific gene encoding an F-Box protein in rainbow trout (Oncorhynchus mykiss)
Authors
Lei Wang
Swamy K Tripurani
Warapond Wanna
Caird E Rexroad III
Jianbo Yao
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2013
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-11-86

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