TY - JOUR
T1 - A gain-of-function mutation in oma-1, a C. elegans gene required for oocyte maturation, results in delayed degradation of maternal proteins and embryonic lethality
AU - Lin, Rueyling
N1 - Funding Information:
I thank Scott Robertson, Scott Cameron, and Eric Rogers for critical reading of the manuscript. Special thanks are given to Melanie Reuben for her technical assistance and to Jim Priess in whose laboratory the zu405 mutation was initially isolated. I would also like to thank Jim Priess for the SKN-1, MEX-1, MEX-3, MEX-5, and POS- 1 antibodies, Geraldine Seydoux for the P pie-1 gfp transgenic strain, Morris Maduro and Joel Rothman for the P med-1 gfp transgenic strain, Keith Blackwell for the skn-1 clone, and Yuji Kohara for the cDNA clone yk283g8. I also thank Alan Coulson for all C. elegans cosmids used in this study. Unless mentioned otherwise, all strains used in this study were provided by the C. elegans Genome Consortium (CGC). This research was supported by a grant from NIH (to R.L.) (HD37933).
PY - 2003/6/1
Y1 - 2003/6/1
N2 - In vertebrates, oocytes undergo maturation, arrest in metaphase II, and can then be fertilized by sperm. Fertilization initiates molecular events that lead to the activation of early embryonic development. In Caenorhabditis elegans, where no delay between oocyte maturation and fertilization is apparent, oocyte maturation and fertilization must be tightly coordinated. It is not clear what coordinates the transition from an oocyte to an embryo in C. elegans, but regulated turnover of oocyte-specific proteins contributes to the process. We describe here a gain-of-function mutation (zu405) in a gene that is essential for oocyte maturation, oma-1. In wild type animals, OMA-1 protein is expressed at a high level exclusively in oocytes and newly fertilized embryos and is degraded rapidly after the first mitotic division. The zu405 mutation results in improper degradation of the OMA-1 protein in embryos. In oma-1(zu405) embryos, the C blastomere is transformed to the EMS blastomere fate, resulting in embryonic lethality. We show that degradation of several maternally supplied cell fate determinants, including SKN-1, PIE-1, MEX-3, and MEX-5, is delayed in oma-1(zu405) mutant embryos. In wild type embryos, SKN-1 functions in EMS for EMS blastomere fate specification. A decreased level of maternal SKN-1 protein in the C blastomere relative to EMS is believed to be responsible for this cell expressing the C, instead of the EMS, fate. Delayed degradation of maternal SKN-1 protein in oma-1(zu405) embryos and resultant elevated levels in C blastomere is likely responsible for the observed C-to-EMS blastomere fate transformation. These observations suggest that oma-1, in addition to its role in oocyte maturation, contributes to early embryonic development by regulating the temporal degradation of maternal proteins in early C. elegans embryos.
AB - In vertebrates, oocytes undergo maturation, arrest in metaphase II, and can then be fertilized by sperm. Fertilization initiates molecular events that lead to the activation of early embryonic development. In Caenorhabditis elegans, where no delay between oocyte maturation and fertilization is apparent, oocyte maturation and fertilization must be tightly coordinated. It is not clear what coordinates the transition from an oocyte to an embryo in C. elegans, but regulated turnover of oocyte-specific proteins contributes to the process. We describe here a gain-of-function mutation (zu405) in a gene that is essential for oocyte maturation, oma-1. In wild type animals, OMA-1 protein is expressed at a high level exclusively in oocytes and newly fertilized embryos and is degraded rapidly after the first mitotic division. The zu405 mutation results in improper degradation of the OMA-1 protein in embryos. In oma-1(zu405) embryos, the C blastomere is transformed to the EMS blastomere fate, resulting in embryonic lethality. We show that degradation of several maternally supplied cell fate determinants, including SKN-1, PIE-1, MEX-3, and MEX-5, is delayed in oma-1(zu405) mutant embryos. In wild type embryos, SKN-1 functions in EMS for EMS blastomere fate specification. A decreased level of maternal SKN-1 protein in the C blastomere relative to EMS is believed to be responsible for this cell expressing the C, instead of the EMS, fate. Delayed degradation of maternal SKN-1 protein in oma-1(zu405) embryos and resultant elevated levels in C blastomere is likely responsible for the observed C-to-EMS blastomere fate transformation. These observations suggest that oma-1, in addition to its role in oocyte maturation, contributes to early embryonic development by regulating the temporal degradation of maternal proteins in early C. elegans embryos.
KW - C. elegans
KW - Embryo
KW - Fate transformation
KW - Gain-of-function
KW - Oma-1
KW - Protein degradation
KW - SKN-1
UR - http://www.scopus.com/inward/record.url?scp=0038360791&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=0038360791&partnerID=8YFLogxK
U2 - 10.1016/S0012-1606(03)00119-2
DO - 10.1016/S0012-1606(03)00119-2
M3 - Article
C2 - 12781695
AN - SCOPUS:0038360791
SN - 0012-1606
VL - 258
SP - 226
EP - 239
JO - Developmental Biology
JF - Developmental Biology
IS - 1
ER -