title: X-Linked Retinitis Pigmentosa 2 Is a Novel Maternal-Effect Gene Required for Left-Right Asymmetry in Zebrafish.
abstract: Retinitis pigmentosa 2 (RP2) gene is responsible for up to 20% of X-linked retinitis pigmentosa, a severe heterogeneous genetic disorder resulting in progressive retinal degeneration in humans. In vertebrates, several bodies of evidence have clearly established the role of Rp2 protein in cilia genesis and/or function. Unexpectedly, some observations in zebrafish have suggested the oocyte-predominant expression of the rp2 gene, a typical feature of maternal-effect genes. In the present study, we investigate the maternal inheritance of rp2 gene products in zebrafish eggs in order to address whether rp2 could be a novel maternal-effect gene required for normal development. Although both rp2 mRNA and corresponding protein are expressed during oogenesis, rp2 mRNA is maternally inherited, in contrast to Rp2 protein. A knockdown of the protein transcribed from both rp2 maternal and zygotic mRNA results in delayed epiboly and severe developmental defects, including eye malformations, that were not observed when only the protein from zygotic origin was knocked down. Moreover, the knockdown of maternal and zygotic Rp2 revealed a high incidence of left-right asymmetry establishment defects compared to only zygotic knockdown. Here we show that rp2 is a novel maternal-effect gene exclusively expressed in oocytes within the zebrafish ovary and demonstrate that maternal rp2 mRNA is essential for successful embryonic development and thus contributes to egg developmental competence. Our observations also reveal that Rp2 protein translated from maternal mRNA is important to allow normal heart loop formation, thus providing evidence of a direct maternal contribution to left-right asymmetry establishment.
authors.affiliation: INRA, UR1037 Fish Physiology and Genomics, Campus de Beaulieu, Rennes, France IFREMER, LALR, Palavas Les Flots, France.
authors.forename: Thomas
authors.initials: T
authors.lastname: Desvignes
authors.affiliation: INRA, UR1037 Fish Physiology and Genomics, Campus de Beaulieu, Rennes, France.
authors.forename: Thaovi
authors.initials: T
authors.lastname: Nguyen
authors.affiliation: CNRS, Université de Rennes 1, Rennes, France.
authors.forename: Franck
authors.initials: F
authors.lastname: Chesnel
authors.affiliation: INRA, UR1037 Fish Physiology and Genomics, Campus de Beaulieu, Rennes, France IFREMER, LALR, Palavas Les Flots, France.
authors.forename: Aurélien
authors.initials: A
authors.lastname: Bouleau
authors.affiliation: IFREMER, LALR, Palavas Les Flots, France.
authors.forename: Christian
authors.initials: C
authors.lastname: Fauvel
authors.affiliation: INRA, UR1037 Fish Physiology and Genomics, Campus de Beaulieu, Rennes, France julien.bobe@rennes.inra.fr.
authors.forename: Julien
authors.initials: J
authors.lastname: Bobe
mesh_terms: D000818:Animals; D004625:Embryo, Nonmammalian; D047108:Embryonic Development; D005124:Eye Abnormalities / Q000235:genetics; D005136:Eye Proteins / Q000235:genetics*; D005260:Female; D007839:Functional Laterality / Q000235:genetics*; D055785:Gene Knockdown Techniques; D007150:Immunohistochemistry; D008297:Male; D009865:Oocytes / Q000378:metabolism; D009866:Oogenesis; D010053:Ovary / Q000378:metabolism; D010063:Ovum / Q000502:physiology; D012333:RNA, Messenger / Q000235:genetics; D012174:Retinitis Pigmentosa / Q000235:genetics*; D015027:Zebrafish / Q000235:genetics*; D029961:Zebrafish Proteins / Q000235:genetics*; D015053:Zygote
chemical_list: D005136:Eye Proteins; D012333:RNA, Messenger; C559526:RP2 protein, zebrafish; D029961:Zebrafish Proteins
keywords: developmental biology; egg developmental competence; egg quality; fish; fish reproduction; maternal-effect gene; ndpk; nme10; oocyte; oocyte-specific; ovum; teleost; zygote