JY-1, an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle

*Laboratory of Mammalian Reproductive Biology and Genomics, and
Departments of ^†Animal Science and
^§Physiology, Michigan State University, East Lansing, MI 48824; and
^‡Division of Animal and Nutritional Sciences, West Virginia University, Morgantown, WV 26506

Edited by R. Michael Roberts, University of Missouri, Columbia, MO, and approved September 21, 2007 (received for review July 7, 2007)

Abstract

Oocyte-specific gene products play a key role in regulation of fertility in mammals. Here, we describe the discovery, molecular characterization, and function of JY-1, a bovine oocyte-expressed gene shown to regulate both function of ovarian granulosa cells and early embryogenesis in cattle and characteristics of JY-1 loci in other species. The JY-1 gene encodes for a secreted protein with multiple mRNA transcripts containing an identical ORF but differing lengths of 3′ UTR. JY-1 mRNA and protein are oocyte-specific and detectable throughout folliculogenesis. Recombinant JY-1 protein regulates function of follicle-stimulating hormone-treated ovarian granulosa cells, resulting in enhanced progesterone synthesis accompanied by reduced cell numbers and estradiol production. JY-1 mRNA of maternal origin is also present in early bovine embryos, temporally regulated during the window from meiotic maturation through embryonic genome activation, and is required for blastocyst development. The JY-1 gene has three exons and is located on bovine chromosome 29. JY-1-like sequences are present on syntenic chromosomes of other vertebrate species, but lack exons 1 and 2, including the protein-coding region, suggestive of species specificity in evolution and function of this oocyte-specific gene.

Footnotes

^¶To whom correspondence should be addressed. E-mail: smithge7{at}msu.edu
Author contributions: A.B., J.Y., J.J.I., and G.W.S. designed research; A.B., J.Y., A.S., Q.L., and K.-B.L. performed research; Y.K., O.V.P., and P.M.C. contributed new reagents/analytic tools; A.B., J.Y., and G.W.S. analyzed data; and A.B. and G.W.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. EF642496 and EF642497).
This article contains supporting information online at www.pnas.org/cgi/content/full/0706383104/DC1.
Abbreviations:

FSH,

follicle-stimulating hormone;

GV,

germinal vesicle;

GVO,

GV oocyte;

rJY-1,

recombinant JY-1;

MII,

metaphase II;

IVF,

in vitro fertilized;

Chr,

chromosome.