The POU gene ceh-18 promotes gonadal sheath cell differentiation and function required for meiotic maturation and ovulation in Caenorhabditis elegans

Kimberly L. Rose, Virginia P. Winfrey, Loren H. Hoffman, David H. Hall, Tokiko Furuta, David Greenstein

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67 Scopus citations

Abstract

In Caenorhabditis elegans, specialized contractile myoepithelial cells of the somatic gonad, the gonadal sheath cells, are closely apposed to oocytes and are required for normal meiotic maturation and ovulation. Previously we found that mutations in the ceh-18 gene, which encodes a POU- class homeoprotein expressed in sheath cells, result in oocyte defects. To determine the basis for these oocyte defects, we have used time-lapse video Nomarski microscopy to observe meiotic maturation, ovulation, and early embryogenesis in ceh-18 mutants. In ceh-18 mutants sheath cell contractions are weaker, less frequent, and uncoordinated throughout the sequence of ovulation events, and ovulation is defective. Defective ovulation can result in the formation of endomitotic oocytes in the gonad, the formation of haploid embryos, and reversals in embryonic polarity. ceh-18 mutant oocytes exhibit defects prior to nuclear envelope breakdown, suggesting that they are physiologically different from the wild type. We observed delays in meiotic maturation, as well as maturation out of the normal spatial and temporal sequence, suggesting that proximal sheath cells directly or indirectly promote and spatially restrict meiotic maturation. Analysis of sheath cell differentiation in ceh-18 mutants using antibodies to proteins of the contractile apparatus reveals that although contractile proteins are expressed, the sheath cells appear disorganized. Transmission electron microscopy reveals that ceh-18 mutant sheath cells are morphologically irregular and only loosely cover oocytes. Taken together, these observations indicate that ceh-18 is a crucial determinant of sheath cell differentiation, a function required for normal meiotic maturation and ovulation.

Original languageEnglish (US)
Pages (from-to)59-77
Number of pages19
JournalDevelopmental Biology
Volume192
Issue number1
DOIs
StatePublished - Dec 1 1997

Bibliographical note

Funding Information:
We thank Jim McCarter and Tim Schedl for helpful discussions, for sharing their video recording protocol, and for comments on the manuscript. We thank Guy Benian for generously providing antibodies to UNC-89, Peg McMorris for sending antibodies to yolk proteins, David Miller for his gift of anti-MHC A (5.6) and FITC-labeled anti-MHCB (5.8), and Theresa Stiernagle for sending strains. The authors are grateful to David Miller and Brigid Hogan for helpful comments, advice, and encouragement. Some strains used in this study were provided by the Caenorhabditis Genetics Center, which is supported by the National Institutes of Health's National Center for Research Resources. This work was supported by grants to D.G. from the American Cancer Society (DB-149 and JFRA-630), the Markey Charitable Trust, and the Joe C. Davis Foundation. Core facilities for electron microscopy were provided through NIH Center Grant HD05797.

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