title: Two classes of gap junction channels mediate soma-germline interactions essential for germline proliferation and gametogenesis in Caenorhabditis elegans.
abstract: In all animals examined, somatic cells of the gonad control multiple biological processes essential for germline development. Gap junction channels, composed of connexins in vertebrates and innexins in invertebrates, permit direct intercellular communication between cells and frequently form between somatic gonadal cells and germ cells. Gap junctions comprise hexameric hemichannels in apposing cells that dock to form channels for the exchange of small molecules. Here we report essential roles for two classes of gap junction channels, composed of five innexin proteins, in supporting the proliferation of germline stem cells and gametogenesis in the nematode Caenorhabditis elegans. Transmission electron microscopy of freeze-fracture replicas and fluorescence microscopy show that gap junctions between somatic cells and germ cells are more extensive than previously appreciated and are found throughout the gonad. One class of gap junctions, composed of INX-8 and INX-9 in the soma and INX-14 and INX-21 in the germ line, is required for the proliferation and differentiation of germline stem cells. Genetic epistasis experiments establish a role for these gap junction channels in germline proliferation independent of the glp-1/Notch pathway. A second class of gap junctions, composed of somatic INX-8 and INX-9 and germline INX-14 and INX-22, is required for the negative regulation of oocyte meiotic maturation. Rescue of gap junction channel formation in the stem cell niche rescues germline proliferation and uncovers a later channel requirement for embryonic viability. This analysis reveals gap junctions as a central organizing feature of many soma-germline interactions in C. elegans.
authors.affiliation: Department of Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, Minnesota 55455.
authors.forename: Todd A
authors.initials: TA
authors.lastname: Starich
authors.affiliation: Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461.
authors.forename: David H
authors.initials: DH
authors.lastname: Hall
authors.affiliation: Department of Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, Minnesota 55455 green959@umn.edu.
authors.forename: David
authors.identifier: http://orcid.org/0000-0001-8189-2087
authors.initials: D
authors.lastname: Greenstein
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology* / Q000196:embryology / Q000378:metabolism* / Q000648:ultrastructure; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D016764:Cell Polarity; D049109:Cell Proliferation; D004252:DNA Mutational Analysis; D004625:Embryo, Nonmammalian / Q000378:metabolism; D004705:Endocytosis; D004843:Epistasis, Genetic; D005260:Female; D005614:Freeze Fracturing; D005718:Gametogenesis; D017629:Gap Junctions / Q000378:metabolism*; D020440:Gene Duplication; D018507:Gene Expression Regulation, Developmental; D005854:Germ Cells / Q000166:cytology* / Q000378:metabolism* / Q000648:ultrastructure; D006066:Gonads / Q000166:cytology / Q000648:ultrastructure; D057850:Hermaphroditic Organisms / Q000166:cytology / Q000378:metabolism; D008297:Male; D009154:Mutation / Q000235:genetics; D009865:Oocytes / Q000166:cytology / Q000378:metabolism; D010060:Ovulation; D021381:Protein Transport
chemical_list: D029742:Caenorhabditis elegans Proteins
keywords: gametogenesis; gap junctions; germline stem cells; oocyte meiotic maturation; soma–germline interactions