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Biology of Reproduction 64, 1090-1099 (2001)
© 2001 Society for the Study of Reproduction, Inc.


Regular Article

Molecular Characterization and High Expression During Oocyte Development of a Shrimp Ovarian Cortical Rod Protein Homologous to Insect Intestinal Peritrophins1

Morad Khayata,b, Patrick J. Babinc, Bruria Funkensteinb, Marei Sammarb, Hiromichi Nagasawad, Aliza Tietza, and Esther Lubzens2,,c

a Department of Neurobiochemistry, Tel Aviv University, Tel Aviv 66978, Israel b Israel Oceanographic and Limnological Research, 81080 Haifa, Israel c Génomique et Physiologie des Poissons, USC INRA, Université Bordeaux I, 33405 Talence cedex, France d Department of Applied Biological Chemistry, The University of Tokyo, Bunkyo-ku, Tokyo 113, Japan

ABSTRACT

Penaeoid shrimp oocytes nearing the completion of oogenesis are enveloped in an acellular vitelline envelope and possess extracellular cortical rods (CRs) that extended into the cortical cytoplasm. These cortical specializations are precursors of the jelly layer (JL) of the egg. In searching for highly expressed mRNAs during oogenesis in the marine shrimp (Penaeus semisulcatus), two related cDNAs have been isolated that encode a mature protein of 250 amino acid residues. The deduced amino acid sequences revealed the presence of repeated cysteine-rich domains that are related to the chitin-binding domains of insect intestinal peritrophins. Similar cysteine-rich domains were reported in insect intestinal mucin, crustacean tachycitin, and invertebrate chitinases. The shrimp ovarian peritrophin (SOP) is glycosylated and can bind chitin when extracted from CRs. Its apparent molecular mass in SDS-PAGE is 29–35 kDa and 33–36 kDa, under nonreducing or reducing conditions, respectively. SOP is a major protein of CRs and the JL, and was immunodetected in ovaries; purified CRs; fertilized eggs that were surrounded by a JL matrix; and in the cloudy, whitish flocculent material appearing in sea water immediately after spawning. Immunolocalization in tissue sections determined that SOP was present in oocyte cytoplasm and in extraoocytic CRs. Shrimp expressed SOP mRNA in ovaries at all oocyte developmental stages, whereas expression in the hepatopancreas was restricted to vitellogenic stages. SOP mRNA was abundant in the shrimp ovary and was detected before the presence of the corresponding protein. This is the first demonstration that a protein with similar features to insect intestinal peritrophins is a component of CRs and is therefore a main precursor of the JL of spawned shrimp eggs.

FOOTNOTES

First decision: 11 August 2000.

1 This work was supported by grant 93-0083/1 from the Binational Science Foundation and grant 8938-1-97 from the Israel Ministry of Science. The nucleotide sequences reported in this paper have been submitted to the GenBank/EBI databank with accession numbers AF095580 for SOP1 and AF095581 for SOP2 cDNA sequences.

2 Correspondence: Esther Lubzens, Israel Oceanographic and Limnological Research, Tel-Shikmona, P.O. Box 8030, Haifa 31080, Israel. FAX: 972 4 8511911; esther{at}ocean.org.il




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K. Yamano, G.-F. Qiu, and T. Unuma
Molecular Cloning and Ovarian Expression Profiles of Thrombospondin,a Major Component of Cortical Rods in Mature Oocytes of Penaeid Shrimp,Marsupenaeus japonicus
Biol Reprod, June 1, 2004; 70(6): 1670 - 1678.
[Abstract] [Full Text] [PDF]




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