The Caenorhabditis elegans spe-49 gene is required for fertilization and encodes a sperm-specific transmembrane protein homologous to SPE-42

Mol Reprod Dev. 2018 Jul;85(7):563-578. doi: 10.1002/mrd.22992. Epub 2018 May 23.

Abstract

Fertilization, the fusion of sperm and oocyte to form a zygote, is the first and arguably the most important cell-cell interaction event in an organism's life. Forward and reverse genetic approaches in the nematode Caenorhabditis elegans have identified many genes that are required for gametogenesis and fertilization and thus are beginning to elucidate the molecular pathways that underlie these processes. We identified an allele of the spe-49 gene in a second filial generation (F2 ) mutagenesis screen for spermatogenesis-defective (spe) mutants. Mutant worms for spe-49 produce sperm that have normal morphology, activate to form ameboid spermatozoa, and can migrate to and maintain their position in the hermaphrodite reproductive tract but fail to fertilize oocytes. This phenotype puts spe-49 in the spe-9 class of late-acting genes that function in sperm at the time of fertilization. We cloned the spe-49 gene through a combination of deficiency mapping, transgenic rescue, and genomic sequencing. spe-49 messenger RNA (mRNA) is enriched in male germ cells, and the complementary DNA (cDNA) encodes a predicted 772-amino-acid six-pass transmembrane protein that is homologous to SPE-42. Indeed, SPE-49 and SPE-42 have identical predicted membrane topology and domain structure, including a large extracellular domain with six conserved cysteine residues, a DC-STAMP domain, and a C-terminal cytoplasmic domain containing a C4-C4 RING finger motif. The presence of two SPE-42 homologs in animal genomes from worms to humans suggests that these proteins are highly conserved components of the molecular apparatus required for the sperm-oocyte recognition, binding, and fusion.

Keywords: DC-STAMP; RING finger; fertilization; gamete interactions.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acid Sequence / genetics
  • Animals
  • Base Sequence
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans Proteins / genetics*
  • Cloning, Molecular
  • Fertilization / genetics*
  • Male
  • Membrane Proteins / genetics*
  • RNA, Messenger / genetics
  • Sequence Analysis, DNA
  • Spermatozoa / metabolism*

Substances

  • Caenorhabditis elegans Proteins
  • Membrane Proteins
  • RNA, Messenger
  • spe-42 protein, c elegans
  • spe-49 protein, C elegans