Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-23T00:37:27.208Z Has data issue: false hasContentIssue false
  • English
  • Français

Cloning and sequence analysis of Bufo arenarum oviductin cDNA and detection of its orthologous gene expression in the mouse female reproductive tract

Published online by Cambridge University Press:  02 September 2010

Daniel Barrera ,
Pablo A. Valdecantos ,
E. Vanesa García  and
Dora C. Miceli
Daniel Barrera
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, 3° piso, T4000ILI, S. M. de Tucumán, Tucumán, Argentina.
Pablo A. Valdecantos
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, 3° piso, T4000ILI, S. M. de Tucumán, Tucumán, Argentina.
E. Vanesa García
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, 3° piso, T4000ILI, S. M. de Tucumán, Tucumán, Argentina.
Dora C. Miceli*
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, 3° piso, T4000ILI, S. M. de Tucumán, Tucumán, Argentina.
*
All correspondence to: Dora C. Miceli. Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, 3° piso, T4000ILI, S. M. de Tucumán, Tucumán, Argentina. Tel: +54 381 4247752, ext. 7099. Fax: +54 381 4248921. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The glycoprotein envelope surrounding the Bufo arenarum egg exists in different functional forms. Conversion between types involves proteolysis of specific envelope glycoproteins. When the egg is released from the ovary, the envelope cannot be penetrated by sperm. Conversion to a penetrable state occurs during passage through the pars recta portion of the oviduct, where oviductin, a serine protease with trypsin-like substrate specificity, hydrolyzes two kinds of envelope glycoproteins: gp84 and gp55. The nucleotide sequence of a 3203 bp B. arenarum oviductin cDNA was obtained. Deduced amino acid sequence showed a complete open reading frame encoding 980 amino acids. B. arenarum oviductin is a multi-domain protein with a protease domain at the N-terminal region followed by two CUB domains and toward the C-terminal region another protease domain, which lacked an active histidine site, and one CUB domain. Expression of ovochymase 2, the mammalian orthologous of amphibian oviductin, was assayed in mouse female reproductive tract. Ovochymase 2 mRNA was unnoticeable in the mouse oviduct but expression was remarkable in the uterus. Phylogenetic relationship between oviductin and ovochymase 2 opens the possibility to understand the role of this enzyme in mammalian reproduction.

Keywords

Bufo arenarumOviductOviductinOvochymase 2Serine protease
Type
Research Article
Information
Zygote , Volume 20 , Issue 1 , February 2012 , pp. 17 - 26
Copyright
Copyright © Cambridge University Press 2010

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

Bakos, M.A., Kurosky, A. & Hedrick, J.L. (1990). Enzymatic and envelope-converting activities of pars recta oviductal fluid from Xenopus laevis. Dev. Biol. 138, 169–76.Google Scholar
Blanc, G., Font, B., Eichenberger, D., Moreau, C., Ricard-Blum, D.J.S. & Moali, C. (2007). Insights into how CUB domains can exert specific functions while sharing a common fold: conserved and specific features of the CUB 1 domain contribute to the molecular basis of procollagen c–proteinase enhancer-1 activity. J. Biol. Chem. 282, 16924–33.Google Scholar
Bork, P. & Beckmann, G. (1993). The CUB domain. A widespread module in developmentally regulated proteins. J. Mol. Biol. 231, 539–45.Google Scholar
Cal, S., Moncada-Pazos, A. & López-Otín, C. (2007). Expanding the complexity of the human degradome: polyserases and their tandem serine protease domains. Front. Biosci. 12, 4661–9.Google Scholar
Gerton, G.L. & Hedrick, J.L. (1986). The coelomic envelope to vitelline envelope conversion in eggs of Xenopus laevis. J. Cell Biochem. 30, 341–50.CrossRefGoogle ScholarPubMed
Hardy, D.M. & Hedrick, J.L. (1992). Oviductin. Purification and properties of the oviductal protease that processes the molecular weight 43,000 glycoprotein of the Xenopus laevis egg envelope. Biochemistry 31, 4466–72.Google Scholar
Hedrick, J.L. (2008). Anuran and pig egg zona pellucida glycoproteins in fertilization and early development. Int. J. Dev. Biol. 52, 683–701.Google Scholar
Hedrick, J.L. & Hardy, D.M. (1991). Isolation of extracellular-matrix structures from Xenopus laevis oocytes, eggs, and embryos. Methods Cell Biol. 36, 231–47.Google Scholar
Hedrick, J.L. & Nishihara, T. (1991). Structure and function of the extracellular matrix of anuran eggs. J. Electron. Microsc. Tech. 17, 319–35.Google Scholar
Hedstrom, L. (2002). Serine protease mechanism and specificity. Chem. Rev. 102, 4501–24.Google Scholar
Hiyoshi, M., Takamune, K., Mita, K., Kubo, H., Sugimoto, Y. & Katagiri, Ch. (2002). Oviductin, the oviductal protease that mediates gamete interaction by affecting the vitelline coat in Bufo japonicus: its molecular cloning and analyses of expression and posttranslational activation. Dev. Biol. 243, 176–84.CrossRefGoogle ScholarPubMed
Katagiri, Ch., Yoshizaki, N., Kotani, M. & Kubo, H. (1999). Analyses of oviductal pars recta-induced fertilizability of coelomic eggs in Xenopus laevis. Dev. Biol. 210, 269–76.CrossRefGoogle ScholarPubMed
Kitamoto, Y., Yuan, X., Wu, Q., McCourt, D.W. & Sadler, J.E. (1994). Enterokinase, the initiator of intestinal digestion, is a mosaic protease composed of a distinctive assortment of domains. Proc. Natl. Acad. Sci. USA 91, 7588–92.Google Scholar
Larabell, C.A., Hardy, D.M. & Hedrick, J.L. (1989). Fibers of coelomic envelope of Xenopus laevis eggs are unbundled by an oviductal enzyme. J. Cell Biol. 109, 128a.Google Scholar
Lindsay, L.L. & Hedrick, J.L. (1998). Treatment of Xenopus laevis coelomic eggs with trypsin mimics pars recta oviductal transit by selectively hydrolyzing envelope glycoprotein gp43, increasing sperm binding to the envelope and rendering eggs fertilizable. J. Exp. Zool. 281, 132–8.3.0.CO;2-P>CrossRefGoogle Scholar
Lindsay, L.L., Matthew, J.W. & Hedrick, J.L. (1999). Oviductin, the Xenopus laevis oviductal protease that processes egg envelope glycoprotein gp43, increases sperm binding to envelopes, and is translated as part of an unusual mosaic protein composed of two protease and several CUB domains. Biol. Reprod. 60, 989–95.Google Scholar
Llanos, R.J., Barrera, D., Valz-Gianinet, J.N. & Miceli, D.C. (2006). Oviductal protease and trypsin treatment enhance sperm–envelope interaction in Bufo arenarum coelomic eggs. J. Exp. Zool. 305, 872–82.Google Scholar
Makalowski, W. & Boguski, M.S. (1998). Evolutionary parameters of the transcribed mammalian genome: an analysis of 2820 orthologous rodent and human sequences. Proc. Natl. Acad. Sci. USA 95, 9407–12.Google Scholar
Mariano, M.I., de Martin, M.G. & Pisano, A. (1984). Morphological modifications of oocyte vitelline envelope from Bufo arenarum during different functional states. Dev. Growth Differ. 26, 33–42.CrossRefGoogle ScholarPubMed
Miceli, D.C. & Cabada, M.O. (1998). Amphibian fertilization. Trends Comp. Biochem. Physiol. 5, 249–65.Google Scholar
Miceli, D.C. & Fernández, S.N. (1982). Properties of an oviducal protein involved in amphibian oocyte fertilization. J. Exp. Zool. 221, 357–64.Google Scholar
Miceli, D.C., Fernández, S.N., Raisman, J.S. & Barbieri, F.D. (1978). A trypsin like oviducal proteinase involved in Bufo arenarum fertilization. J. Embryol. Exp. Morphol. 48, 79–91.Google ScholarPubMed
Miceli, D.C., Fernández, S.N. & Morero, R.D. (1980). Effect of oviducal proteinase upon Bufo arenarum vitelline envelope. A fluorescence approach. Dev. Growth Differ. 22, 639–43.Google Scholar
Omata, S. & Katagiri, C. (1996). Involvement of carbohydrate moieties of the toad egg vitelline coat in binding with fertilizing sperm. Dev. Growth Differ. 38, 663–72.Google Scholar
Puente, X.S., Sanchez, L.M., Overall, C.M. & López-Otín, C. (2003). Human and mouse proteases: a comparative genomic approach. Nat. Rev. Genet. 4, 544–8.Google Scholar
Puente, X.S., Sánchez, L.M., Gutiérrez-Fernández, A., Velasco, G. & López-Otín, C. (2005). A genomic view of the complexity of mammalian proteolytic systems. Biochem. Soc. Trans. 33, 331–4.Google Scholar
Swanson, W.J. & Vacquier, V.D. (2002). Reproductive protein evolution. Annu. Rev. Ecol. Syst. 33, 161–79CrossRefGoogle Scholar
Takamune, K. & Katagiri, C. (1987). The properties of the oviductal pars recta protease which mediates gamete interaction by affecting the vitelline coat of toad egg. Dev. Growth Differ. 29, 193–203.Google Scholar
Takamune, K., Yoshizaki, N. & Katagiri, C. (1986). Oviducal pars recta induced degradation of vitelline coat proteins in relation to acquisition of fertilizability of a toad eggs. Gamete Res. 14, 215–24.CrossRefGoogle Scholar
Takamune, K., Lindsay, L., Hedrick, J.L. & Katagiri, C. (1987). Comparative studies of Bufo and Xenopus vitelline coat molecular transformations induced by homologous and heterologous oviducal pars recta proteases. J. Exp. Zool. 244, 145–50.CrossRefGoogle Scholar
Tao, Z., Peng, Y., Nolasco, L., Cal, S., López-Otín, C., Li, R., Moake, J.L., López, J.A. & Dong, J.F. (2005). Recombinant CUB-1 domain polypeptide inhibits the cleavage of ULVWF strings by ADAMTS13 under flow conditions. Blood 106, 4139–45.Google Scholar
Tian, J.D., Gong, H., Thomsen, G.H. & Lennarz, W.J. (1997). Gamete interactions in Xenopus laevis: identification of sperm binding glycoproteins in the egg vitelline envelope. J. Cell Biol. 136, 1099–108.Google Scholar
Varela, P.F., Romero, A., Sanz, L., Romão, M.J., Töpfer-Petersen, E. & Calvete, J.J. (1997). The 2.4 Å resolution crystal structure of boar seminal plasma PSP-I/PSP-II: a zona pellucida-binding glycoprotein heterodimer of the spermadhesin family built by a CUB domain architecture. J. Mol. Biol. 274, 635–49.CrossRefGoogle ScholarPubMed
Vo, L.H. & Hedrick, J.L. (2000). Independent and hetero-oligomeric-dependent sperm binding to egg envelope glycoprotein ZPC in Xenopus laevis. Biol. Reprod. 62, 766–74.Google Scholar
Whitacre, C.M. & Miceli, D.C. (1996). Serum antigens detected in pars recta luminal fluid and coelomic envelope surrounding Bufo arenarum eggs. Dev. Growth Differ. 38, 597–603.Google Scholar