Skip to main content
SpringerLink
Log in

Cloning of a quail homologue of hatching enzyme: its conserved function and additional function in egg envelope digestion

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

The aim of the present study was to reveal molecular entities participating in the digestion of the egg envelope in the Japanese quail, Coturnix japonica. We isolated a 1,510-bp cDNA from extraembryonic tissues of developing embryos and designated it quail hatching enzyme (QHE) cDNA. The QHE cDNA was found to code a protein molecule comprising an astacin protease domain in the N-terminal half and a complement subcomponents C1r/C1s, Uegf, Bmp1 (CUB) domain in the C-terminal half. A phylogenetic analysis showed that QHE belonged to the hatching enzyme group and was distinct from other proteases in the astacin family. Northern blotting and in situ hybridization demonstrated that expression of the QHE mRNA occurred twice during the development: first in ectodermal cells of the yolk sac on days 0–5, then in those of the albumen sac on days 8–13. Zymography revealed that proteolytic activity in extracts of days 3–4 and 9–12 embryos appeared at the position of 40 kDa. Immunoblotting tests showed that anti-QHE antiserum stained a 40-kDa molecule in extracts of day 3 area vitellina. Anti-QHE antibody stained the ectodermal cells of the area opaca on days 0–1, those of the area vitellina of the yolk sac on days 2–5, and those of the albumen sac on days 9–12. The temporal and spatial expression pattern of QHE mRNA was closely associated with digestion of the vitelline membrane occurring on days 1–4, and with that of the egg white on days 9–12.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Bond JS, Beynon RJ (1995) The astacin family of metalloendopeptidase. Protein Sci 4:1247–1261

    Article  PubMed  CAS  Google Scholar 

  • Bork P, Beckmann G (1993) The CUB domain, a widespread molecule in developmentally regulated proteins. J Mol Biol 231:539–545

    Article  PubMed  CAS  Google Scholar 

  • Carroll EJ Jr, Hedrick JL (1974) Hatching in the toad Xenopus laevis: morphological events and evidence for a hatching enzyme. Dev Biol 38:1–13

    Article  PubMed  CAS  Google Scholar 

  • Elaroussi MA, DeLuca HF (1994) A new member to the astasin family of metalloendopeptidases. Biochim Biophys Acta 1217:1–8

    PubMed  CAS  Google Scholar 

  • Fan T, Katagiri C (1997) The mode of action on the vitelline envelope of Xenopus hatching enzyme as studied by its two molecular forms. Zool Sci 14:101–104

    Article  CAS  Google Scholar 

  • Ghiglione C, Emily-Fenouil F, Lhomond G, Gache C (1997) Organization of the proximal promoter of the hatching-enzyme gene, the earliest zygotic gene expressed in the sea urchin embryo. Eur J Biochem 250:502–513

    Article  PubMed  CAS  Google Scholar 

  • Heussen C, Dowdle EB (1980) Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal Biochem 102:196–202

    Article  PubMed  CAS  Google Scholar 

  • Inohaya K, Yasumasu S, Ishimaru M, Ohyama A, Iuchi I, Yamagami K (1995) Temporal and spatial patterns of gene expression for the hatching enzyme in the teleost embryo, Oryzias latipes. Dev Biol 171:374–385

    Article  PubMed  CAS  Google Scholar 

  • Inohaya K, Yasumasu S, Araki K, Naruse K, Yamazaki K, Yasumasu I, Iuchi I, Yamagami K (1997) Species-dependent migration of fish hatching gland cells that express astacin-like proteases in common. Dev Growth Differ 39:191–197

    Article  PubMed  CAS  Google Scholar 

  • Johnston PM, Comar CL (1955) Distribution and contribution of calcium from the albumen, yolk and shell to the developing chick embryo. Am J Physiol 183:365–370

    PubMed  CAS  Google Scholar 

  • Kamihira M, Oguchi S, Tachibana A, Kitagawa Y, Iijima S (1998) Improved hatching for in vitro quail embryo culture using surrogate eggshell and artificial vessel. Dev Growth Differ 40:449–455

    Article  PubMed  CAS  Google Scholar 

  • Kanamori A, Naruse K, Mitani H, Shima A, Hori H (2003) Genomic organization of ZP domain containing egg envelope genes in medaka (Oryzias latipes). Gene 305:35–45

    Article  PubMed  CAS  Google Scholar 

  • Katagiri C, Maeda R, Yamashika C, Mita K, Sargent TD, Yasumasu S (1997) Molecular cloning of Xenopus hatching enzyme and its specific expression in hatching gland cells. Int J Dev Biol 41:19–25

    PubMed  CAS  Google Scholar 

  • Kitamura Y, Katagiri C (1998) Characterization of the hatching enzyme from embryos of an anuran amphibian, Rana pipiens. Biochem Biophys Acta 1387:153–164

    PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • LePage T, Gache C (1989) Purification and characterization of the sea urchin hatching enzyme. J Biol Chem 264:4787–4796

    PubMed  CAS  Google Scholar 

  • LePage T, Gache C (1990) Early expression of a collagenase-like hatching enzyme gene in the sea urchin embryo. EMBO J 9:3003–3012

    PubMed  CAS  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, Oxford

    Google Scholar 

  • Nomura K, Tanaka H, Kikkawa Y, Yamaguchi M, Suzuki N (1991) The specificity of sea urchin hatching enzyme (Envelysin) places it in the mammalian matrix metalloproteinase family. Biochemistry 30:6115–6123

    Article  PubMed  CAS  Google Scholar 

  • Nomura K, Shimizu T, Kinoh H, Sendai Y, Inomata M, Suzuki N (1997) Sea urchin hatching enzyme (Envelysin): cDNA cloning and deprivation of protein substrate specificity by autolytic degradation. Biochemistry 36:7225–7238

    Article  PubMed  CAS  Google Scholar 

  • Ono T, Wakasugi N (1984) Mineral content of quail embryos cultured in mineral-rich and mineral-free conditions. Poult Sci 63:159–166

    PubMed  CAS  Google Scholar 

  • Perona RM, Wassarman PM (1986) Mouse blastocysts hatch in vitro by using a trypsin-like protease associated with cells of mural trophectoderm. Dev Biol 114:42–52

    Article  PubMed  CAS  Google Scholar 

  • Sasaki H, Hogan BL (1993) Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118:47–59

    PubMed  CAS  Google Scholar 

  • Sawada H, Yamazaki K, Hoshi M (1990) Trypsin-like hatching protease from mouse embryos: evidence for the presence in culture medium and its enzymatic properties. J Exp Zool 254:83–87

    Article  PubMed  CAS  Google Scholar 

  • Schoots AFM, Opstelten RJG, Denuce JM (1982) Hatching in the pike Esox lucius L.: evidence for a single hatching enzyme and its immunocytochemical localization in specialized hatching gland cells. Dev Biol 89:48–55

    Article  PubMed  CAS  Google Scholar 

  • Simkiss K (1961) Calcium metabolism and avian reproduction. Biol Rev 36:321–367

    Article  CAS  Google Scholar 

  • Simkiss K (1980) Water and ionic fluxes inside the egg. Am Zool 20:385–393

    CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Titani K, Torff HJ, Hormel S, Kumar S, Walsh KA, Rodl J, Neurath H, Zwilling R (1987) Amino acid sequence of a unique protease from the crayfish Astacus fluviatilis. Biochemistry 26:222–226

    Article  PubMed  CAS  Google Scholar 

  • Urch UA, Hedrick JL (1981) The hatching enzyme from Xenopus laevis: limited proteolysis of the fertilization envelope. J Supramol Struct Cell Biochem 15:111–117

    Article  PubMed  CAS  Google Scholar 

  • Yamagami K (1996) Studies on the hatching enzyme (choriolysin) and its substrate, egg envelope, constructed of the precursors (choriogenins) in Oryzias latipes: a sequel of the information in 1991/1992. Zool Sci 13:331–340

    Article  PubMed  CAS  Google Scholar 

  • Yamagami K, Hamazaki TS, Yasumasu S, Masuda K, Iuchi I (1992) Molecular and cellular basis of formation, hardening, and breakdown of the egg envelope in fish. Int Rev Cytol 136:51–92

    Article  PubMed  CAS  Google Scholar 

  • Yasumasu S, Yamada K, Akasaka K, Mitsunaga K, Iuchi I, Shimada H, Yamagami K (1992) Isolation of cDNAs for LCE and HCE, two constituent proteases of the hatching enzyme of Oryzias latipes, and concurrent expression of their mRNAs during development. Dev Biol 153:250–258

    Article  PubMed  CAS  Google Scholar 

  • Yasumasu S, Iuchi I, Yamagami K (1994) cDNAs and the genes of HCE and LCE, two constituents of the medaka hatching enzyme. Dev Growth Differ 36:241–250

    Article  CAS  Google Scholar 

  • Yoshizaki N (1991) Changes in surface ultrastructure and proteolytic activity of hatching gland cells during development of Xenopus embryo. Zool Sci 8:295–302

    Google Scholar 

  • Yoshizaki N, Katagiri C (1975) Cellular basis for the production and secretion of the hatching enzyme by frog embryos. J Exp Zool 192:203–212

    Article  Google Scholar 

  • Yoshizaki N, Saito H (2002) Changes in shell membranes during the development of quail embryos. Poult Sci 81:246–251

    PubMed  CAS  Google Scholar 

  • Yoshizaki N, Yamasaki H (1991) Morphological and biochemical changes in the fertilization coat of Xenopus laevis during the hatching process. Zool Sci 8:303–308

    Google Scholar 

  • Yoshizaki N, Yamaguchi W, Ito S, Katagiri C (2000) On the hatching mechanism of quail embryos: participation of ectodermal secretions in the escape of embryos from the vitelline membrane. Zool Sci 17:751–758

    Article  Google Scholar 

  • Yoshizaki N, Ito Y, Hori H, Saito H, Iwasawa A (2002) Absorption, transportation and digestion of egg white in quail embryos. Dev Growth Differ 44:11–22

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Life Science Institute, Sophia University, 102-8554, Tokyo, Japan

    Shigeki Yasumasu

  2. Department of Agricultural Science, Faculty of Applied Biological Science, Gifu University, 501-1193, Gifu, Japan

    Kun Ming Mao, Fowzia Sultana, Hiromi Sakaguchi & Norio Yoshizaki

Authors
  1. Shigeki Yasumasu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kun Ming Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fowzia Sultana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiromi Sakaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Norio Yoshizaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Norio Yoshizaki.

Additional information

Communicated by B.G. Herrmann

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yasumasu, S., Mao, K.M., Sultana, F. et al. Cloning of a quail homologue of hatching enzyme: its conserved function and additional function in egg envelope digestion. Dev Genes Evol 215, 489–498 (2005). https://doi.org/10.1007/s00427-005-0007-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-005-0007-x

Keywords

Search

Navigation