Otoc1: A novel otoconin‐90 ortholog required for otolith mineralization in zebrafish

Within the vestibular system of virtually all vertebrate species, gravity and linear acceleration are detected via coupling of calcified masses to the cilia of mechanosensory hair cells. The mammalian ear contains thousands of minute biomineralized particles called otoconia, whereas the inner ear of teleost fish contains three large ear stones called otoliths that serve a similar function. Otoconia and otoliths are composed of calcium carbonate crystals condensed on a core protein lattice. Otoconin‐90 (Oc90) is the major matrix protein of mammalian and avian otoconia, while otolith matrix protein (OMP) is the most abundant matrix protein found in the otoliths of teleost fish. We have identified a novel gene, otoc1, which encodes the zebrafish ortholog of Oc90. Expression of otoc1 was detected in the ear between 15 hpf and 72 hpf, and was restricted primarily to the macula and the developing epithelial pillars of the semicircular canals. Expression of otoc1 was also detected in epiphysis, optic stalk, midbrain, diencephalon, flexural organ, and spinal cord. During embryogenesis, expression of otoc1 mRNA preceded the appearance of omp‐1 transcripts. Knockdown of otoc1 mRNA translation with antisense morpholinos produced a variety of aberrant otolith phenotypes. Our results suggest that Otoc1 may serve to nucleate calcium carbonate mineralization of aragonitic otoliths. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2008

[1]  E. Yamoah,et al.  Gene targeting reveals the role of Oc90 as the essential organizer of the otoconial organic matrix. , 2007, Developmental biology.

[2]  B. Riley,et al.  Zebrafish atoh1 genes: classic proneural activity in the inner ear and regulation by Fgf and Notch , 2007, Development.

[3]  J. Dickman,et al.  Separate Na,K-ATPase genes are required for otolith formation and semicircular canal development in zebrafish. , 2006, Developmental biology.

[4]  B. Thisse,et al.  Neuronal calcium sensor-1 gene ncs-1a is essential for semicircular canal formation in zebrafish inner ear. , 2005, Journal of neurobiology.

[5]  Herwig Baier,et al.  A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection , 2005, Development.

[6]  H. Takeda,et al.  Otolith matrix proteins OMP-1 and Otolin-1 are necessary for normal otolith growth and their correct anchoring onto the sensory maculae , 2005, Mechanisms of Development.

[7]  R. Geisler,et al.  Mutated otopetrin 1 affects the genesis of otoliths and the localization of Starmaker in zebrafish , 2004, Development Genes and Evolution.

[8]  H. Tsai,et al.  Na,K-ATPase is essential for embryonic heart development in the zebrafish , 2003, Development.

[9]  M. Burghammer,et al.  Control of Crystal Size and Lattice Formation by Starmaker in Otolith Biomineralization , 2003, Science.

[10]  A. Folarin,et al.  Hedgehog signalling is required for correct anteroposterior patterning of the zebrafish otic vesicle , 2003, Development.

[11]  B. Kachar,et al.  Development and Maintenance of Otoconia , 2001 .

[12]  A. Meiniel,et al.  SCO‐spondin, a glycoprotein of the subcommissural organ/reissner's fiber complex: Evidence of a potent activity on neuronal development in primary cell cultures , 2001, Microscopy research and technique.

[13]  A. Herbet,et al.  SCO‐spondin and RF‐GlyI: Two designations for the same glycoprotein secreted by the subcommissural organ , 2000, Journal of neuroscience research.

[14]  H. Nagasawa,et al.  Molecular cloning and expression of an otolith matrix protein cDNA from the rainbow trout, Oncorhynchus mykiss. , 2000, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[15]  B. Riley,et al.  The deltaA gene of zebrafish mediates lateral inhibition of hair cells in the inner ear and is regulated by pax2.1. , 1999, Development.

[16]  W. Naumann,et al.  Reissner’s substance expressed as a transient pattern in vertebrate floor plate , 1999, Anatomy and Embryology.

[17]  C. Petit,et al.  Characterization of otoconin-95, the major protein of murine otoconia, provides insights into the formation of these inner ear biominerals. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Mager,et al.  Otoconin-90, the mammalian otoconial matrix protein, contains two domains of homology to secretory phospholipase A2. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  E. Rodríguez,et al.  Partial sequencing of Reissner’s fiber glycoprotein I (RF-Gly I) , 1998, Cell and Tissue Research.

[20]  C. Janetopoulos,et al.  A critical period of ear development controlled by distinct populations of ciliated cells in the zebrafish. , 1997, Developmental biology.

[21]  B. Dastugue,et al.  SCO-spondin: a new member of the thrombospondin family secreted by the subcommissural organ is a candidate in the modulation of neuronal aggregation. , 1996, Journal of cell science.

[22]  H. Michel,et al.  Otoconin-22, the major protein of aragonitic frog otoconia, is a homolog of phospholipase A2. , 1993, Biochemistry.

[23]  S. Ekker,et al.  Differential DNA sequence recognition is a determinant of specificity in homeotic gene action. , 1992, The EMBO journal.

[24]  M. Westerfield,et al.  Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos , 1992, Neuron.

[25]  E. Rodríguez,et al.  Identification and partial characterization of the secretory glycoproteins of the bovine subcommissural organ-Reissner's fiber complex. Evidence for the existence of two precursor forms. , 1991, Brain research. Molecular brain research.

[26]  A. Meiniel,et al.  Glycoprotein synthesis in the subcommissural organ of the chick embryo , 1990, Journal of Neural Transmission / General Section JNT.

[27]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[28]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[29]  D. Lim.  Morphogenesis and malformation of otoconia: a review. , 1980, Birth defects original article series.

[30]  M. Ross,et al.  The Nature and Crystal Growth of Otoconia in the Rat , 1975, The Annals of otology, rhinology, and laryngology.

[31]  G. Pannella.  Fish Otoliths: Daily Growth Layers and Periodical Patterns , 1971, Science.

[32]  J. R. Wait.  Electromagnetics of the sea. , 1970, Science.

[33]  R. Haedrich,et al.  Molecular structure and composition of fish otoliths , 1969 .

[34]  W. Fitch,et al.  Construction of phylogenetic trees. , 1967, Science.

[35]  B. Thisse,et al.  High-resolution in situ hybridization to whole-mount zebrafish embryos , 2007, Nature Protocols.

[36]  W. Naumann,et al.  Axon pathfinding and the floor plate factor Reissner's substance in wildtype, cyclops and one-eyed pinhead mutants of Danio rerio. , 2005, Brain research. Developmental brain research.

[37]  J. Felsenstein.  Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

[38]  E. Rodríguez,et al.  Secretory glycoproteins of the rat subcommissural organ are N-linked complex-type glycoproteins. Demonstration by combined use of lectins and specific glycosidases, and by the administration of tunicamycin , 2004, Histochemistry.

[39]  M. Greene,et al.  Fish otolith contains a unique structural protein, otolin-1. , 2002, European journal of biochemistry.

[40]  W. Naumann,et al.  Multiple forms of glycoproteins in the secretory product of the bovine subcommissural organ--an ancient glial structure. , 2001, Acta histochemica.

[41]  B. Kachar,et al.  Development and maintenance of otoconia: biochemical considerations. , 2001, Annals of the New York Academy of Sciences.

[42]  M. Ross,et al.  Each otoconia polymorph has a protein unique to that polymorph. , 1991, Comparative biochemistry and physiology. B, Comparative biochemistry.

[43]  G. Panella,et al.  Fish otoliths: daily growth layers and periodical patterns. , 1971, Science.