Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T07:19:22.606Z Has data issue: false hasContentIssue false

Characterization of oocyte-expressed GDF9 gene in buffalo and mapping of its TSS and putative regulatory elements

Published online by Cambridge University Press:  10 January 2012

B. Roy
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal, India.
S. Rajput
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal, India.
S. Raghav
Affiliation:
Amity Institute of Biotechnology, Amity University, UP, India.
P. Kumar
Affiliation:
Division of Hematology and Transfusion Medicine, Lund University, Sweden.
A. Verma
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal, India.
A. Jain
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal, India.
T. Jain
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal, India.
D. Singh
Affiliation:
Molecular Endocrinology Laboratory, National Dairy Research Institute, Karnal, India.
S. De
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal, India.
S.L. Goswami
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal, India.
T.K. Datta*
Affiliation:
Animal Genomics Laboratory, National Dairy Research Institute, Karnal 132001, Haryana, India.
*
All correspondences to: T.K. Datta. Animal Genomics Laboratory, National Dairy Research Institute, Karnal 132001, Haryana, India. Tel: +91 184 2259506. Fax: +91 184 2250042. e-mail: tirthadatta@gmail.com

Summary

In spite of emerging evidence about the vital role of GDF9 in determination of oocyte competence, there is insufficient information about its regulation of oocyte-specific expression, particularly in livestock animals. Because of the distinct prominence of buffalo as a dairy animal, the present study was undertaken to isolate and characterize GDF9 cDNA using orthologous primers based on the bovine GDF9 sequence. GDF9 transcripts were found to be expressed in oocytes irrespective of their follicular origin, and shared a single transcription start site (TSS) at –57 base pairs (bp) upstream of ATG. Assignment of the TSS is consistent with the presence of a TATA element at –23 of the TSS mapped in this study. Localization of a buffalo-specific minimal promoter within 320 bp upstream of ATG was consolidated by identification of an E-box element at –113bp. Presence of putative transcription factor binding sites and other cis regulatory elements were analyzed at ~5 kb upstream of TSS. Various germ cell-specific cis-acting regulatory elements (BNCF, BRNF, NR2F, SORY, Foxh1, OCT1, LHXF etc.) have been identified in the 5′ flanking region of the buffalo GDF9 gene, including NOBOX DNA binding elements and consensuses E-boxes (CANNTG). Presence of two conserved E-boxes found on buffalo sequence at –520 and –718 positions deserves attention in view of its sequence deviation from other species. Two NOBOX binding elements (NBE) were detected at the –3471 and –203 positions. The fall of the NBE within the putative minimal promoter territory of buffalo GDF9 and its unique non-core binding sequence could have a possible role in the control of the core promoter activity.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aaltonen, J., Laitinen, M.P., Vuojolainen, K., Jaatinen, R., Horelli-Kuitunen, N., Seppa, L., Louhio, H., Tuuri, T., Sjoberg, J., Butzow, R., Hovata, O., Dale, L. & Ritvos, O. (1999). Human growth differentiation factor 9 (GDF- 9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab. 84, 2744–50.Google ScholarPubMed
Avsian-Kretchmer, O. & Hsueh, A.J. (2004). Comparative genomic analysis of the eight-membered ring cystine knot-containing bone morphogenetic protein antagonists. Mol. Endocrinol. 18, 112.CrossRefGoogle ScholarPubMed
Baker, D., Dave, V., Reed, T., Misra, S. & Periasamy, M. (1998). A novel Ebox/ATrich element is required for the muscle-specific expression of the sarcoplasmic reticulum Ca2+ ATPase (SERCA2) gene. Nucl. Acids Res. 26, 1092–8.CrossRefGoogle Scholar
Bodensteiner, K.J., Clay, C.M., Moeller, C.L. & Sawyer, H.R. (1999). Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod. 60, 381–6.CrossRefGoogle ScholarPubMed
Choi, Y. & Rajkovic, A. (2006). Characterization of NOBOX DNA binding specificity and its regulation of GDF9 and Pou5f1 promoters. J. Biol. Chem. 281, 35747–56.CrossRefGoogle ScholarPubMed
Drost, M. (2007). Advanced reproductive technology in the water buffalo. Theriogenology 68, 450–3.CrossRefGoogle ScholarPubMed
Gasparrini, B. (2002). In vitro embryo production in buffalo species: state of the art. Theriogenology 57, 237–56.CrossRefGoogle ScholarPubMed
Gasparrini, B., Boccia, L., Marchandise, J., Di Palo, R., George, F., Donnay, I. & Zicarelli, L. (2006). Enrichment of in vitro maturation medium for buffalo (Bubalus bubalis) oocytes with thiol compounds: effects of cystine on glutathione synthesis and embryo development. Theriogenology 65, 275–87.CrossRefGoogle ScholarPubMed
Hayashi, M., Mcgee, E.A., Min, G., Klein, C., Rose, U.M., Duin, M.V. & Hsueh, A.J.W. (1999). Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236–44.CrossRefGoogle ScholarPubMed
Incerti, B., Dong, J., Borsani, G. & Matzuk, M.M. (1994). Structure of the mouse growth/differentiation factor-9 gene. Biochim. Biophys. Acta 1222, 125–8.CrossRefGoogle ScholarPubMed
Knijin, H.M., Wrenzycki, C., Hendriksen, P.J.M., Vos, P.L.A.M., Hermann, D., Vander, W., Niemann, H. & Dielemen, J.J. (2002). Effects of oocyte maturation regimen on the relative abundance of gene transcript in bovine blastocysts derived in vitro or in vivo. Reproduction 124, 365–75.CrossRefGoogle Scholar
Liang, L.F., Soyal, S., & Dean, J. (1997). FIGa, a germ cell-specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 124, 4939–47.CrossRefGoogle Scholar
Matzuk, M.M., Burns, K.H., Vivieros, M.M. & Eppig, J.J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178–80.CrossRefGoogle ScholarPubMed
McGrath, S.A., Esquela, A.F. & Lee, S.J. (1995). Oocyte specific expression of growth/differentiation factor-9. Mol. Endocrinol. 9, 131–6.Google ScholarPubMed
McPherron, A.C. & Lee, S.J. (1993). GDF-3 and GDF-9: Two new members of the transforming growth factor-β superfamily containing a novel pattern of cysteines. J. Biol. Chem. 268, 3444–9.CrossRefGoogle ScholarPubMed
Nandi, S., Raghu, H.M., Ravindranatha, B.M. & Chauhan, M.S. (2002). Production of buffalo (Bubalus bubalis) embryos in vitro: premises and promises. Reprod. Domest. Anim. 37, 6574.CrossRefGoogle ScholarPubMed
Quandt, K., Frech, K., Karas, H., Wingender, E. & Werner, T. (1995). Matlnd and MatInspector: New fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res. 23, 4878–84.CrossRefGoogle ScholarPubMed
Sambrook, J. & Russell, D. (2001). Molecular Cloning. A Laboratory Manual, 3rd edn, Cold Spring Harbor Press, Cold Spring Harbor New York.Google Scholar
Sendai, Y., Itoh, T., Yamashita, S. & Hoshi, H. (2001). Molecular cloning of a cDNA encoding a bovine growth differentiation factor-9 (GDF-9) and expression of GDF-9 in bovine ovarian oocytes and in vitro-produced embryos. Cloning 3, 310.CrossRefGoogle ScholarPubMed
Shimizu, T., Miyahayashi, Y., Yokoo, M., Hoshino, Y., Sasada, H. & Sato, E. (2004). Molecular cloning of porcine growth differentiation factor 9 (GDF-9) cDNA and its role in early folliculogenesis: direct ovarian injection of GDF-9 gene fragments promotes early folliculogenesis. Reproduction 128, 537–43.CrossRefGoogle ScholarPubMed
Sirard, M.A., Richard, F., Blondin, P. & Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–36.CrossRefGoogle ScholarPubMed
Tsunemoto, K., Anzai, M., Matsuoka, T., Tokoro, M., Shin, S.W., Amano, T., Mitani, T., Kato, H., Hosoi, Y. & Saeki, K. (2008). Cis-acting elements (E-box and NBE) in the promoter region of three maternal genes (histone H1oo, nucleoplasmin 2, and zygote arrest 1) are required for oocyte-specific gene expression in the mouse. Mol. Reprod. Dev. 75, 1104–8.CrossRefGoogle ScholarPubMed
Weiner, J.A., Chen, A. & Davis, B.H. (2000). Platelet-derived growth factor is a principal inductive factor modulating mannose 6-phosphate/insulin-like growth factor-II receptor gene expression via a distal E-box in activated hepatic stellate cells. Biochem. J. 345, 225–31.CrossRefGoogle Scholar
Weintraub, H., Genetta, T. & Kadesch, T. (1994). Tissue-specific gene activation by MyoD: determination of specificity by cis-acting repression elements. Genes Dev. 8, 2203–11.CrossRefGoogle ScholarPubMed
Yan, C., Elvin, J.A., Lin, Y.N., Hadsell, L.A., Wang, J., DeMayo, F.J. & Matzuk, M.M. (2006). Regulation of growth differentiation factor 9 expression in oocytes in vivo: a key role of the E-box. Biol. Reprod. 74, 9991006.CrossRefGoogle ScholarPubMed