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Volume 39 Issue 9
Sep.  2012
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Ribosome Biogenesis Factor Bms1-like Is Essential for Liver Development in Zebrafish

doi: 10.1016/j.jgg.2012.07.007
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  • Corresponding author: E-mail address: dbshyh@nus.edu.sg (Yunhan Hong); E-mail address: pengjr@zju.edu.cn (Jinrong Peng); E-mail address: g0403022@zju.edu.cn (Lijan Lo)
  • Received Date: 2012-05-06
  • Accepted Date: 2012-07-12
  • Rev Recd Date: 2012-07-11
  • Available Online: 2012-08-11
  • Publish Date: 2012-09-20
  • Ribosome biogenesis in the nucleolus requires numerous nucleolar proteins and small non-coding RNAs. Among them is ribosome biogenesis factor Bms1, which is highly conserved from yeast to human. In yeast, Bms1 initiates ribosome biogenesis through recruiting Rcl1 to pre-ribosomes. However, little is known about the biological function of Bms1 in vertebrates. Here we report that Bms1 plays an essential role in zebrafish liver development. We identified a zebrafishbms1l mutant which carries a T to A mutation in the gene bms1-like (bms1l). This mutation results in L152 to Q152 substitution in a GTPase motif in Bms1l. Surprisingly, bms1l mutation confers hypoplasia specifically in the liver, exocrine pancreas and intestine after 3 days post-fertilization (dpf). Consistent with the bms1l mutant phenotypes, whole-mount in situ hybridization (WISH) on wild type embryos showed that bms1l transcripts are abundant in the entire digestive tract and its accessory organs. Immunostaining for phospho-Histone 3 (P-H3) and TUNEL assay revealed that impairment of hepatoblast proliferation rather than cell apoptosis is one of the consequences of bms1l giving rise to an under-developed liver. Therefore, our findings demonstrate that Bms1l is necessary for zebrafish liver development.
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  • [1]
    Allende, M.L., Amsterdam, A., Becker, T. et al. Insertional mutagenesis in zebrafish identifies two novel genes, pescadillo and dead eye, essential for embryonic development Genes Dev., 10 (1996),pp. 3141-3155
    [2]
    Azuma, M., Toyama, R., Laver, E. et al. J. Biol. Chem., 281 (2006),pp. 13309-13316
    [3]
    Ben-Shem, A., Garreau de, L.N., Melnikov, S. et al. The structure of the eukaryotic ribosome at 3.0 A resolution Science, 334 (2011),pp. 1524-1529
    [4]
    Billy, E., Wegierski, T., Nasr, F. et al. Rcl1p, the yeast protein similar to the RNA 3′-phosphate cyclase, associates with U3 snoRNP and is required for 18S rRNA biogenesis EMBO J., 19 (2000),pp. 2115-2126
    [5]
    Bortoluzzi, S., d'Alessi, F., Romualdi, C. et al. Differential expression of genes coding for ribosomal proteins in different human tissues Bioinformatics, 17 (2001),pp. 1152-1157
    [6]
    Bourne, H.R., Sanders, D.A., McCormick, F. The GTPase superfamily: conserved structure and molecular mechanism Nature, 349 (1991),pp. 117-127
    [7]
    Chen, J., Ruan, H., Ng, S.M. et al. Loss of function of def selectively up-regulates Delta113p53 expression to arrest expansion growth of digestive organs in zebrafish Genes Dev., 19 (2005),pp. 2900-2911
    [8]
    Cheng, W., Guo, L., Zhang, Z. et al. HNF factors form a network to regulate liver-enriched genes in zebrafish Dev. Biol., 294 (2006),pp. 482-496
    [9]
    Duncan, S.A. Mechanisms controlling early development of the liver Mech. Dev., 120 (2003),pp. 19-33
    [10]
    Field, H.A., Ober, E.A., Roeser, T. et al. Formation of the digestive system in zebrafish. I. Liver morphogenesis Dev. Biol., 253 (2003),pp. 279-290
    [11]
    Fromont-Racine, M., Senger, B., Saveanu, C. et al. Ribosome assembly in eukaryotes Gene, 313 (2003),pp. 17-42
    [12]
    Holtzinger, A., Evans, T. Gata4 regulates the formation of multiple organs Development, 132 (2005),pp. 4005-4014
    [13]
    Huang, H., Ruan, H., Aw, M.Y. et al. Mypt1-mediated spatial positioning of Bmp2-producing cells is essential for liver organogenesis Development, 135 (2008),pp. 3209-3218
    [14]
    Karbstein, K., Doudna, J.A. GTP-dependent formation of a ribonucleoprotein subcomplex required for ribosome biogenesis J. Mol. Biol., 356 (2006),pp. 432-443
    [15]
    Karbstein, K., Jonas, S., Doudna, J.A. An essential GTPase promotes assembly of preribosomal RNA processing complexes Mol. Cell, 20 (2005),pp. 633-643
    [16]
    Kressler, D., Linder, P., de La, C.J. Mol. Cell. Biol., 19 (1999),pp. 7897-7912
    [17]
    Lambertsson, A. Adv. Genet., 38 (1998),pp. 69-134
    [18]
    Lee, C.S., Sund, N.J., Behr, R. et al. Foxa2 is required for the differentiation of pancreatic alpha-cells Dev. Biol., 278 (2005),pp. 484-495
    [19]
    Lohrum, M.A.E., Ludwig, R.L., Kubbutat, M.H.G. et al. Regulation of HDM2 activity by the ribosomal protein L11 Cancer Cell, 3 (2003),pp. 577-587
    [20]
    MacInnes, A.W., Amsterdam, A., Whittaker, C.A. et al. Loss of p53 synthesis in zebrafish tumors with ribosomal protein gene mutations Proc. Natl. Acad. Sci. USA, 105 (2008),pp. 10408-10413
    [21]
    Mayer, A.N., Fishman, M.C. Nil per os encodes a conserved RNA recognition motif protein required for morphogenesis and cytodifferentiation of digestive organs in zebrafish Development, 130 (2003),pp. 3917-3928
    [22]
    Ober, E.A., Field, H.A., Stainier, D.Y. From endoderm formation to liver and pancreas development in zebrafish Mech. Dev., 120 (2003),pp. 5-18
    [23]
    Ober, E.A., Verkade, H., Field, H.A. et al. Mesodermal Wnt2b signalling positively regulates liver specification Nature, 442 (2006),pp. 688-691
    [24]
    Opferman, J.T., Zambetti, G.P. Translational research? Ribosome integrity and a new p53 tumor suppressor checkpoint Cell Death Differ., 13 (2006),pp. 898-901
    [25]
    Sadler, K.C., Krahn, K.N., Gaur, N.A. et al. Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1 Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 1570-1575
    [26]
    Sanchez, R., Sali, A. Proc. Natl. Acad. Sci. USA, 95 (1998),pp. 13597-13602
    [27]
    Shimoda, N., Knapik, E.W., Ziniti, J. et al. Zebrafish genetic map with 2000 microsatellite markers Genomics, 58 (1999),pp. 219-232
    [28]
    Shin, D., Shin, C.H., Tucker, J. et al. Bmp and Fgf signaling are essential for liver specification in zebrafish Development, 134 (2007),pp. 2041-2050
    [29]
    Soulet, F., Al, S.T., Roga, S. et al. Fibroblast growth factor-2 interacts with free ribosomal protein S19 Biochem. Biophys. Res. Commun., 289 (2001),pp. 591-596
    [30]
    Stafford, D., Prince, V.E. Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development Curr. Biol., 12 (2002),pp. 1215-1220
    [31]
    Tao, T., Peng, J. J. Genet. Genomics, 36 (2009),pp. 325-334
    [32]
    Volarevic, S., Stewart, M.J., Ledermann, B. et al. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6 Science, 288 (2000),pp. 2045-2047
    [33]
    Wegierski, T., Billy, E., Nasr, F. et al. Bms1p, a G-domain-containing protein, associates with Rcl1p and is required for 18S rRNA biogenesis in yeast RNA, 7 (2001),pp. 1254-1267
    [34]
    Wen, C., Zhang, Z., Ma, W. et al. Genome-wide identification of female-enriched genes in zebrafish Dev. Dyn., 232 (2005),pp. 171-179
    [35]
    Wool, I.G. Extraribosomal functions of ribosomal proteins Trends Biochem. Sci., 21 (1996),pp. 164-165
    [36]
    Zaret, K.S. Regulatory phases of early liver development: paradigms of organogenesis Nat. Rev. Genet., 3 (2002),pp. 499-512
    [37]
    Zhao, R., Watt, A.J., Li, J. et al. GATA6 is essential for embryonic development of the liver but dispensable for early heart formation Mol. Cell. Biol., 25 (2005),pp. 2622-2631
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