The Ribosome Biogenesis Factor Nol11 Is Required for Optimal rDNA Transcription and Craniofacial Development in Xenopus

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Griffin, John N ^a   Sondalle, Samuel B ^a   del Viso, Florencia ^a   Baserga, Susan J ^a   Khokha, Mustafa K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN; PROTEIN NOL11; PROTEIN P53; RIBOSOME DNA; RIBOSOME PROTEIN; RIBOSOME RNA; UNCLASSIFIED DRUG; MESSENGER RNA; NOL11 PROTEIN, HUMAN;

AMPHIBIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOGENESIS; CARTILAGE; CELL SURVIVAL; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; DNA TRANSCRIPTION; EMBRYO; GENETIC CONSERVATION; MAMMAL; MOLECULAR MECHANICS; MOUSE; NEURAL CREST CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA PROCESSING; RNA TRANSCRIPTION; VERTEBRATE; XENOPUS TROPICALIS; ANIMAL; ANTIBODY SPECIFICITY; EMBRYOLOGY; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MANDIBULOFACIAL DYSOSTOSIS; METABOLISM; NEURAL CREST; PATHOLOGY; RIBOSOME; SKULL; XENOPUS;

AMPHIBIA; ANURA; MAMMALIA; VERTEBRATA;

ANIMALS; CELL SURVIVAL; DNA, RIBOSOMAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; MANDIBULOFACIAL DYSOSTOSIS; MICE; NEURAL CREST; NUCLEAR PROTEINS; ORGAN SPECIFICITY; RIBOSOMES; RNA, MESSENGER; SKULL; TRANSCRIPTION, GENETIC; XENOPUS;

EID: 84926150308     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005018     Document Type: Article

References (75)

1. McCann KL, Baserga SJ, (2013) Genetics. Mysterious ribosomopathies. Science 341: 849–850. doi: 10.1126/science.1244156 23970686
2. Bolze A, Mahlaoui N, Byun M, Turner B, Trede N, et al. (2013) Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia. Science 340: 976–978. doi: 10.1126/science.1234864 23579497
3. Butterfield RJ, Stevenson TJ, Xing L, Newcomb TM, Nelson B, et al. (2014) Congenital lethal motor neuron disease with a novel defect in ribosome biogenesis. Neurology.
4. Chagnon P, Michaud J, Mitchell G, Mercier J, Marion JF, et al. (2002) A missense mutation (R565W) in cirhin (FLJ14728) in North American Indian childhood cirrhosis. Am J Hum Genet 71: 1443–1449. 12417987
5. Dauwerse JG, Dixon J, Seland S, Ruivenkamp CA, van Haeringen A, et al. (2011) Mutations in genes encoding subunits of RNA polymerases I and III cause Treacher Collins syndrome. Nat Genet 43: 20–22. doi: 10.1038/ng.724 21131976
6. Dixon J, Jones NC, Sandell LL, Jayasinghe SM, Crane J, et al. (2006) Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proc Natl Acad Sci U S A 103: 13403–13408. 16938878
7. Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, et al. (1999) The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet 21: 169–175. 9988267
8. Ebert BL, Pretz J, Bosco J, Chang CY, Tamayo P, et al. (2008) Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. Nature 451: 335–339. doi: 10.1038/nature06494 18202658
9. Freed EF, Baserga SJ, (2010) The C-terminus of Utp4, mutated in childhood cirrhosis, is essential for ribosome biogenesis. Nucleic Acids Res 38: 4798–4806. doi: 10.1093/nar/gkq185 20385600
10. Freed EF, Bleichert F, Dutca LM, Baserga SJ, (2010) When ribosomes go bad: diseases of ribosome biogenesis. Mol Biosyst 6: 481–493. doi: 10.1039/b919670f 20174677
11. Gazda HT, Sheen MR, Vlachos A, Choesmel V, O'Donohue MF, et al. (2008) Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. Am J Hum Genet 83: 769–780. doi: 10.1016/j.ajhg.2008.11.004 19061985
12. Hannan KM, Sanij E, Rothblum LI, Hannan RD, Pearson RB, (2013) Dysregulation of RNA polymerase I transcription during disease. Biochim Biophys Acta 1829: 342–360. doi: 10.1016/j.bbagrm.2012.10.014 23153826
13. Narla A, Ebert BL, (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood 115: 3196–3205. doi: 10.1182/blood-2009-10-178129 20194897
14. Teng T, Thomas G, Mercer CA, (2013) Growth control and ribosomopathies. Curr Opin Genet Dev 23: 63–71. doi: 10.1016/j.gde.2013.02.001 23490481
15. Trainor PA, Merrill AE, (2014) Ribosome biogenesis in skeletal development and the pathogenesis of skeletal disorders. Biochim Biophys Acta 1842: 769–778. doi: 10.1016/j.bbadis.2013.11.010 24252615
16. Valdez BC, Henning D, So RB, Dixon J, Dixon MJ, (2004) The Treacher Collins syndrome (TCOF1) gene product is involved in ribosomal DNA gene transcription by interacting with upstream binding factor. Proc Natl Acad Sci U S A 101: 10709–10714. 15249688
17. Trainor PA, Andrews BT, (2013) Facial dysostoses: Etiology, pathogenesis and management. Am J Med Genet C Semin Med Genet 163: 283–294.
18. Chai Y, Jiang X, Ito Y, Bringas P, Jr.Han J, et al. (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127: 1671–1679. 10725243
19. Dupin E, Creuzet S, Le Douarin NM, (2006) The contribution of the neural crest to the vertebrate body. Adv Exp Med Biol 589: 96–119. 17076277
20. Inman KE, Purcell P, Kume T, Trainor PA, (2013) Interaction between Foxc1 and Fgf8 during mammalian jaw patterning and in the pathogenesis of syngnathia. PLoS Genet 9: e1003949. doi: 10.1371/journal.pgen.1003949 24385915
21. Jones NC, Lynn ML, Gaudenz K, Sakai D, Aoto K, et al. (2008) Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat Med 14: 125–133. doi: 10.1038/nm1725 18246078
22. Le Lievre CS, Le Douarin NM, (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morphol 34: 125–154. 1185098
23. Noden DM, (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96: 144–165. 6825950
24. Olsson L, Falck P, Lopez K, Cobb J, Hanken J, (2001) Cranial neural crest cells contribute to connective tissue in cranial muscles in the anuran amphibian, Bombina orientalis. Dev Biol 237: 354–367. 11543620
25. Depew MJ, Lufkin T, Rubenstein JL, (2002) Specification of jaw subdivisions by Dlx genes. Science 298: 381–385. 12193642
26. Griffin JN, Compagnucci C, Hu D, Fish J, Klein O, et al. (2013) Fgf8 dosage determines midfacial integration and polarity within the nasal and optic capsules. Dev Biol 374: 185–197. doi: 10.1016/j.ydbio.2012.11.014 23201021
27. Rijli FM, Mark M, Lakkaraju S, Dierich A, Dolle P, et al. (1993) A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 75: 1333–1349. 7903601
28. Trumpp A, Depew MJ, Rubenstein JL, Bishop JM, Martin GR, (1999) Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev 13: 3136–3148. 10601039
29. Basch ML, Bronner-Fraser M, (2006) Neural crest inducing signals. Adv Exp Med Biol 589: 24–31. 17076273
30. Pegoraro C, Monsoro-Burq AH, (2013) Signaling and transcriptional regulation in neural crest specification and migration: lessons from xenopus embryos. Wiley Interdiscip Rev Dev Biol 2: 247–259. doi: 10.1002/wdev.76 24009035
31. Aybar MJ, Nieto MA, Mayor R, (2003) Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development 130: 483–494. 12490555
32. Bhatt S, Diaz R, Trainor PA, (2013) Signals and switches in Mammalian neural crest cell differentiation. Cold Spring Harb Perspect Biol 5.
33. Garcia-Castro M, Bronner-Fraser M, (1999) Induction and differentiation of the neural crest. Curr Opin Cell Biol 11: 695–698. 10600707
34. Garcia-Castro MI, Marcelle C, Bronner-Fraser M, (2002) Ectodermal Wnt function as a neural crest inducer. Science 297: 848–851. 12161657
35. Henras AK, Soudet J, Gerus M, Lebaron S, Caizergues-Ferrer M, et al. (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65: 2334–2359. doi: 10.1007/s00018-008-8027-0 18408888
36. Kressler D, Hurt E, Bassler J, (2010) Driving ribosome assembly. Biochim Biophys Acta 1803: 673–683. doi: 10.1016/j.bbamcr.2009.10.009 19879902
37. Lempiainen H, Shore D, (2009) Growth control and ribosome biogenesis. Curr Opin Cell Biol 21: 855–863. doi: 10.1016/j.ceb.2009.09.002 19796927
38. Woolford JL, Jr.Baserga SJ, (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195: 643–681. doi: 10.1534/genetics.113.153197 24190922
39. Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, et al. (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417: 967–970. 12068309
40. Prieto JL, McStay B, (2007) Recruitment of factors linking transcription and processing of pre-rRNA to NOR chromatin is UBF-dependent and occurs independent of transcription in human cells. Genes Dev 21: 2041–2054. 17699751
41. Sloan KE, Bohnsack MT, Schneider C, Watkins NJ, (2014) The roles of SSU processome components and surveillance factors in the initial processing of human ribosomal RNA. RNA 20: 540–550. doi: 10.1261/rna.043471.113 24550520
42. Gallagher JE, Dunbar DA, Granneman S, Mitchell BM, Osheim Y, et al. (2004) RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev 18: 2506–2517. 15489292
43. Zhao C, Andreeva V, Gibert Y, LaBonty M, Lattanzi V, et al. (2014) Tissue specific roles for the ribosome biogenesis factor Wdr43 in zebrafish development. PLoS Genet 10: e1004074. doi: 10.1371/journal.pgen.1004074 24497835
44. Freed EF, Prieto JL, McCann KL, McStay B, Baserga SJ, (2012) NOL11, implicated in the pathogenesis of North American Indian childhood cirrhosis, is required for pre-rRNA transcription and processing. PLoS Genet 8: e1002892. doi: 10.1371/journal.pgen.1002892 22916032
45. Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, et al. (2002) Functional proteomic analysis of human nucleolus. Mol Biol Cell 13: 4100–4109. 12429849
46. Wood HB, Episkopou V, (1999) Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86: 197–201. 10446282
47. Rowitch DH, Kispert A, McMahon AP, (1999) Pax-2 regulatory sequences that direct transgene expression in the developing neural plate and external granule cell layer of the cerebellum. Brain Res Dev Brain Res 117: 99–108. 10536237
48. Hopwood ND, Pluck A, Gurdon JB, (1989) MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO J 8: 3409–3417. 2555164
49. Carl TF, Dufton C, Hanken J, Klymkowsky MW, (1999) Inhibition of neural crest migration in Xenopus using antisense slug RNA. Dev Biol 213: 101–115. 10452849
50. Hong CS, Devotta A, Lee YH, Park BY, Saint-Jeannet JP, (2014) Transcription factor AP2 epsilon (Tfap2e) regulates neural crest specification in Xenopus. Dev Neurobiol.
51. Soo K, O'Rourke MP, Khoo PL, Steiner KA, Wong N, et al. (2002) Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev Biol 247: 251–270. 12086465
52. Blum M, Beyer T, Weber T, Vick P, Andre P, et al. (2009) Xenopus, an ideal model system to study vertebrate left-right asymmetry. Dev Dyn 238: 1215–1225. doi: 10.1002/dvdy.21855 19208433
53. Chen CY, Croissant J, Majesky M, Topouzis S, McQuinn T, et al. (1996) Activation of the cardiac alpha-actin promoter depends upon serum response factor, Tinman homologue, Nkx-2.5, and intact serum response elements. Dev Genet 19: 119–130. 8900044
54. Patterson KD, Drysdale TA, Krieg PA, (2000) Embryonic origins of spleen asymmetry. Development 127: 167–175. 10654610
55. Takebayashi-Suzuki K, Funami J, Tokumori D, Saito A, Watabe T, et al. (2003) Interplay between the tumor suppressor p53 and TGF beta signaling shapes embryonic body axes in Xenopus. Development 130: 3929–3939. 12874116
56. Wallingford JB, Seufert DW, Virta VC, Vize PD, (1997) p53 activity is essential for normal development in Xenopus. Curr Biol 7: 747–757. 9368757
57. Yadav GV, Chakraborty A, Uechi T, Kenmochi N, (2014) Ribosomal protein deficiency causes Tp53-independent erythropoiesis failure in zebrafish. Int J Biochem Cell Biol 49: 1–7. doi: 10.1016/j.biocel.2014.01.006 24417973
58. Holmberg Olausson K, Nister M, Lindstrom MS, (2012) p53-Dependent and-Independent Nucleolar Stress Responses. Cells 1: 774–798. doi: 10.3390/cells1040774 24710530
59. Tafforeau L, Zorbas C, Langhendries JL, Mullineux ST, Stamatopoulou V, et al. (2013) The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol Cell 51: 539–551. doi: 10.1016/j.molcel.2013.08.011 23973377
60. Wang M, Anikin L, Pestov DG, (2014) Two orthogonal cleavages separate subunit RNAs in mouse ribosome biogenesis. Nucleic Acids Res 42: 11180–11191. doi: 10.1093/nar/gku787 25190460
61. Holzel M, Orban M, Hochstatter J, Rohrmoser M, Harasim T, et al. (2010) Defects in 18 S or 28 S rRNA processing activate the p53 pathway. J Biol Chem 285: 6364–6370. doi: 10.1074/jbc.M109.054734 20056613
62. Zhang Y, Lu H, (2009) Signaling to p53: ribosomal proteins find their way. Cancer Cell 16: 369–377. doi: 10.1016/j.ccr.2009.09.024 19878869
63. Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI, (2010) The nucleolus under stress. Mol Cell 40: 216–227. doi: 10.1016/j.molcel.2010.09.024 20965417
64. Sondalle SB, Baserga SJ, (2014) Human diseases of the SSU processome. Biochim Biophys Acta 1842: 758–764. doi: 10.1016/j.bbadis.2013.11.004 24240090
65. Ellis SR, (2014) Nucleolar stress in Diamond Blackfan anemia pathophysiology. Biochim Biophys Acta 1842: 765–768. doi: 10.1016/j.bbadis.2013.12.013 24412987
66. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, et al. (2011) Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145: 383–397. doi: 10.1016/j.cell.2011.03.028 21529712
67. Boglev Y, Badrock AP, Trotter AJ, Du Q, Richardson EJ, et al. (2013) Autophagy induction is a Tor- and Tp53-independent cell survival response in a zebrafish model of disrupted ribosome biogenesis. PLoS Genet 9: e1003279. doi: 10.1371/journal.pgen.1003279 23408911
68. Khokha MK, Chung C, Bustamante EL, Gaw LW, Trott KA, et al. (2002) Techniques and probes for the study of Xenopus tropicalis development. Dev Dyn 225: 499–510. 12454926
69. Hensey C, Gautier J, (1998) Programmed cell death during Xenopus development: a spatio-temporal analysis. Dev Biol 203: 36–48. 9806771
70. Pestov DG, Lapik YR, Lau LF, (2008) Assays for ribosomal RNA processing and ribosome assembly. Curr Protoc Cell Biol Chapter 22: Unit 22 11.
71. Borovjagin AV, Gerbi SA, (1999) U3 small nucleolar RNA is essential for cleavage at sites 1, 2 and 3 in pre-rRNA and determines which rRNA processing pathway is taken in Xenopus oocytes. J Mol Biol 286: 1347–1363. 10064702
72. Borovjagin AV, Gerbi SA, (2001) Xenopus U3 snoRNA GAC-Box A' and Box A sequences play distinct functional roles in rRNA processing. Mol Cell Biol 21: 6210–6221. 11509664
73. Mougey EB, Pape LK, Sollner-Webb B, (1993) A U3 small nuclear ribonucleoprotein-requiring processing event in the 5' external transcribed spacer of Xenopus precursor rRNA. Mol Cell Biol 13: 5990–5998. 8413202
74. Peculis BA, Steitz JA, (1993) Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73: 1233–1245. 8513505
75. Savino R, Gerbi SA, (1990) In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J 9: 2299–2308. 2357971