Tissue Specific Roles for the Ribosome Biogenesis Factor Wdr43 in Zebrafish Development

PLoS Genetics

Volumn 10, Issue 1, 2014, Pages

  Zhao, Chengtian ^a,b   Andreeva, Viktoria ^a   Gibert, Yann ^a   LaBonty, Melissa ^a   Lattanzi, Victoria ^a   Prabhudesai, Shubhangi ^a   Zhou, Yi ^c   Zon, Leonard ^c   McCann, Kathleen L ^d   Baserga, Susan ^d   Yelick, Pamela C ^a  

^a TUFTS UNIVERSITY   (United States)

^b OCEAN UNIVERSITY OF CHINA   (China)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GENOMIC DNA; MESSENGER RNA; PROTEIN WDR43; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DEVELOPMENTAL STAGE; DNA SEQUENCE; EMBRYO DEVELOPMENT; GENE MUTATION; NEURAL CREST CELL; NONHUMAN; NUCLEOLUS; PHENOTYPE; POINT MUTATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RIBOSOME; STOP CODON; UPREGULATION; ZEBRA FISH;

ANIMALS; APOPTOSIS; CARTILAGE; CELL DIFFERENTIATION; HUMANS; MANDIBULOFACIAL DYSOSTOSIS; MICE; NEURAL CREST; NUCLEAR PROTEINS; ORGAN SPECIFICITY; PHOSPHOPROTEINS; PROTEIN INTERACTION MAPS; RIBOSOMES; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84896700408     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004074     Document Type: Article

References (65)

1. Cordero DR, Brugmann S, Chu Y, Bajpai R, Jame M, et al. (2011) Cranial neural crest cells on the move: their roles in craniofacial development. Am J Med Genet A 155A: 270-279.
2. Minoux M, Rijli FM, (2010) Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 137: 2605-2621.
3. Gorlin RJ, Cohen MM, Levin LS (1990) Syndromes of the head and neck. New York; Oxford: Oxford University Press. xxi, 977.
4. Trainor PA, (2010) Craniofacial birth defects: The role of neural crest cells in the etiology and pathogenesis of Treacher Collins syndrome and the potential for prevention. Am J Med Genet A 152A: 2984-2994.
5. Positional cloning of a gene involved in the pathogenesis of Treacher Collins syndrome. The Treacher Collins Syndrome Collaborative Group. Nat Genet 12: 130-136.
6. Wise CA, Chiang LC, Paznekas WA, Sharma M, Musy MM, et al. (1997) TCOF1 gene encodes a putative nucleolar phosphoprotein that exhibits mutations in Treacher Collins Syndrome throughout its coding region. Proc Natl Acad Sci U S A 94: 3110-3115.
7. Hayano T, Yanagida M, Yamauchi Y, Shinkawa T, Isobe T, et al. (2003) Proteomic analysis of human Nop56p-associated pre-ribosomal ribonucleoprotein complexes. Possible link between Nop56p and the nucleolar protein treacle responsible for Treacher Collins syndrome. J Biol Chem 278: 34309-34319.
8. 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.
9. Gonzales B, Henning D, So RB, Dixon J, Dixon MJ, et al. (2005) The Treacher Collins syndrome (TCOF1) gene product is involved in pre-rRNA methylation. Hum Mol Genet 14: 2035-2043.
10. 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.
11. 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.
12. Cisterna B, Biggiogera M, (2010) Ribosome biogenesis: from structure to dynamics. Int Rev Cell Mol Biol 284: 67-111.
13. Kressler D, Hurt E, Bassler J, (2010) Driving ribosome assembly. Biochim Biophys Acta 1803: 673-683.
14. 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.
15. Krogan NJ, Peng WT, Cagney G, Robinson MD, Haw R, et al. (2004) High-definition macromolecular composition of yeast RNA-processing complexes. Mol Cell 13: 225-239.
16. 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.
17. 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.
18. Wery M, Ruidant S, Schillewaert S, Lepore N, Lafontaine DL, (2009) The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 15: 406-419.
19. 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.
20. 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.
21. McCann KL, Baserga SJ, (2013) Genetics. Mysterious ribosomopathies. Science 341: 849-850.
22. 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.
23. Azuma M, Toyama R, Laver E, Dawid IB, (2006) Perturbation of rRNA synthesis in the bap28 mutation leads to apoptosis mediated by p53 in the zebrafish central nervous system. J Biol Chem 281: 13309-13316.
24. Gallenberger M, Meinel DM, Kroeber M, Wegner M, Milkereit P, et al. (2011) Lack of WDR36 leads to preimplantation embryonic lethality in mice and delays the formation of small subunit ribosomal RNA in human cells in vitro. Hum Mol Genet 20: 422-435.
25. Skarie JM, Link BA, (2008) The primary open-angle glaucoma gene WDR36 functions in ribosomal RNA processing and interacts with the p53 stress-response pathway. Hum Mol Genet 17: 2474-2485.
26. Provost E, Wehner KA, Zhong X, Ashar F, Nguyen E, et al. (2012) Ribosomal biogenesis genes play an essential and p53-independent role in zebrafish pancreas development. Development 139: 3232-3241.
27. Bugner V, Tecza A, Gessert S, Kuhl M, (2011) Peter Pan functions independently of its role in ribosome biogenesis during early eye and craniofacial cartilage development in Xenopus laevis. Development 138: 2369-2378.
28. Wang Y, Luo Y, Hong Y, Peng J, Lo L, (2012) Ribosome biogenesis factor Bms1-like is essential for liver development in zebrafish. J Genet Genomics 39: 451-462.
29. Andreeva V, Connolly MH, Stewart-Swift C, Fraher D, Burt J, et al. (2011) Identification of adult mineralized tissue zebrafish mutants. Genesis 49: 360-366.
30. Locascio A, Nieto MA, (2001) Cell movements during vertebrate development: integrated tissue behaviour versus individual cell migration. Curr Opin Genet Dev 11: 464-469.
31. Yelick PC, Schilling TF, (2002) Molecular dissection of craniofacial development using zebrafish. Crit Rev Oral Biol Med 13: 308-322.
32. Le Douarin NM, Calloni GW, Dupin E, (2008) The stem cells of the neural crest. Cell Cycle 7: 1013-1019.
33. Yan YL, Miller CT, Nissen RM, Singer A, Liu D, et al. (2002) A zebrafish sox9 gene required for cartilage morphogenesis. Development 129: 5065-5079.
34. Yan YL, Willoughby J, Liu D, Crump JG, Wilson C, et al. (2005) A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development 132: 1069-1083.
35. Luo R, An M, Arduini BL, Henion PD, (2001) Specific pan-neural crest expression of zebrafish Crestin throughout embryonic development. Dev Dyn 220: 169-174.
36. Thomas T, Kurihara H, Yamagishi H, Kurihara Y, Yazaki Y, et al. (1998) A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development 125: 3005-3014.
37. Sperber SM, Saxena V, Hatch G, Ekker M, (2008) Zebrafish dlx2a contributes to hindbrain neural crest survival, is necessary for differentiation of sensory ganglia and functions with dlx1a in maturation of the arch cartilage elements. Dev Biol 314: 59-70.
38. Lawson ND, Weinstein BM, (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248: 307-318.
39. Li YP, Busch RK, Valdez BC, Busch H, (1996) C23 interacts with B23, a putative nucleolar-localization-signal-binding protein. Eur J Biochem 237: 153-158.
40. Gallagher JE, Baserga SJ, (2004) Two-hybrid Mpp10p interaction-defective Imp4 proteins are not interaction defective in vivo but do confer specific pre-rRNA processing defects in Saccharomyces cerevisiae. Nucleic Acids Res 32: 1404-1413.
41. Beven AF, Lee R, Razaz M, Leader DJ, Brown JW, et al. (1996) The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J Cell Sci 109 (Pt 6):: 1241-1251.
42. Ma N, Matsunaga S, Takata H, Ono-Maniwa R, Uchiyama S, et al. (2007) Nucleolin functions in nucleolus formation and chromosome congression. J Cell Sci 120: 2091-2105.
43. Fumagalli S, Thomas G, (2011) The role of p53 in ribosomopathies. Semin Hematol 48: 97-105.
44. Fumagalli S, Ivanenkov VV, Teng T, Thomas G, (2012) Suprainduction of p53 by disruption of 40S and 60S ribosome biogenesis leads to the activation of a novel G2/M checkpoint. Genes Dev 26: 1028-1040.
45. Bursac S, Brdovcak MC, Pfannkuchen M, Orsolic I, Golomb L, et al. (2012) Mutual protection of ribosomal proteins L5 and L11 from degradation is essential for p53 activation upon ribosomal biogenesis stress. Proc Natl Acad Sci U S A 109: 20467-20472.
46. Suzuki A, Kogo R, Kawahara K, Sasaki M, Nishio M, et al. (2012) A new PICTure of nucleolar stress. Cancer Sci 103: 632-637.
47. Lee KC, Goh WL, Xu M, Kua N, Lunny D, et al. (2008) Detection of the p53 response in zebrafish embryos using new monoclonal antibodies. Oncogene 27: 629-640.
48. 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.
49. Uechi T, Nakajima Y, Chakraborty A, Torihara H, Higa S, et al. (2008) Deficiency of ribosomal protein S19 during early embryogenesis leads to reduction of erythrocytes in a zebrafish model of Diamond-Blackfan anemia. Hum Mol Genet 17: 3204-3211.
50. 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.
51. Danilova N, Sakamoto KM, Lin S, (2008) Ribosomal protein S19 deficiency in zebrafish leads to developmental abnormalities and defective erythropoiesis through activation of p53 protein family. Blood 112: 5228-5237.
52. Iwanami N, Higuchi T, Sasano Y, Fujiwara T, Hoa VQ, et al. (2008) WDR55 is a nucleolar modulator of ribosomal RNA synthesis, cell cycle progression, and teleost organ development. PLoS Genet 4: e1000171.
53. Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT, et al. (2004) Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2: E139.
54. Sakai D, Trainor PA, (2009) Treacher Collins syndrome: unmasking the role of Tcof1/treacle. Int J Biochem Cell Biol 41: 1229-1232.
55. 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.
56. Yung BY, Busch RK, Busch H, Mauger AB, Chan PK, (1985) Effects of actinomycin D analogs on nucleolar phosphoprotein B23 (37,000 daltons/pI 5.1). Biochem Pharmacol 34: 4059-4063.
57. Lin CI, Yeh NH, (2009) Treacle recruits RNA polymerase I complex to the nucleolus that is independent of UBF. Biochem Biophys Res Commun 386: 396-401.
58. Kong R, Zhang L, Hu L, Peng Q, Han W, et al. (2011) hALP, a novel transcriptional U three protein (t-UTP), activates RNA polymerase I transcription by binding and acetylating the upstream binding factor (UBF). J Biol Chem 286: 7139-7148.
59. Hernandez-Verdun D, Roussel P, Thiry M, Sirri V, Lafontaine DL, (2010) The nucleolus: structure/function relationship in RNA metabolism. Wiley Interdiscip Rev RNA 1: 415-431.
60. Anastassova-Kristeva M, (1977) The nucleolar cycle in man. J Cell Sci 25: 103-110.
61. Sullivan GJ, Bridger JM, Cuthbert AP, Newbold RF, Bickmore WA, et al. (2001) Human acrocentric chromosomes with transcriptionally silent nucleolar organizer regions associate with nucleoli. EMBO J 20: 2867-2874.
62. Brangwynne CP, Mitchison TJ, Hyman AA, (2011) Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proc Natl Acad Sci U S A 108: 4334-4339.
63. Chen J, Ruan H, Ng SM, Gao C, Soo HM, et al. (2005) Loss of function of def selectively up-regulates Delta113p53 expression to arrest expansion growth of digestive organs in zebrafish. Genes Dev 19: 2900-2911.
64. Keegan BR, Feldman JL, Lee DH, Koos DS, Ho RK, et al. (2002) The elongation factors Pandora/Spt6 and Foggy/Spt5 promote transcription in the zebrafish embryo. Development 129: 1623-1632.
65. Villefranc JA, Amigo J, Lawson ND, (2007) Gateway compatible vectors for analysis of gene function in the zebrafish. Dev Dyn 236: 3077-3087.