The emerging roles of ribosome biogenesis in craniofacial development

Frontiers in Physiology

Volumn 5 FEB, Issue , 2014, Pages

  Ross, Adam P ^a   Zarbalis, Konstantinos S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell cycle regulation; Craniofacial development; Neural crest; Neurocristopathies; Ribosome biogenesis; Ribosomopathies; TP53

Indexed keywords

BIOGENESIS; BLACKFAN DIAMOND ANEMIA; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CRANIOFACIAL DEVELOPMENT; HUMAN; MANDIBULOFACIAL DYSOSTOSIS; MESENCHYME; MULTIPOTENT STEM CELL; NEURAL CREST CELL; NEUROCRISTOPATHY; NEUROPATHY; NEURULATION; NONHUMAN; REVIEW; RIBOSOME;

EID: 84895462193     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00026     Document Type: Review

References (95)

1. Abu-Issa, R., Smyth, G., Smoak, I., Yamamura, K., and Meyers, E. N. (2002). Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129, 4613-4625.
2. Attie, T., Till, M., Pelet, A., Amiel, J., Edery, P., Boutrand, L., et al. (1995). Mutation of the endothelin-receptor B gene in Waardenburg-Hirschsprung disease. Hum. Mol. Genet. 4, 2407-2409. doi: 10.1093/hmg/4.12.2407.
3. Bastidas, F., De Calisto, J., and Mayor, R. (2004). Identification of neural crest competence territory: role of Wnt signaling. Dev. Dyn. 229, 109-117. doi: 10.1002/dvdy.10486.
4. Bohnsack, B. L., Lai, L., Dolle, P., and Hirschi, K. K. (2004). Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Genes Dev. 18, 1345-1358. doi: 10.1101/gad.1184904.
5. Bolande, R. P. (1997). Neurocristopathy: its growth and development in 20 years. Pediatr. Pathol. Lab. Med. 17, 1-25. doi: 10.1080/107710497174994.
6. Boultwood, J., Yip, B. H., Vuppusetty, C., Pellagatti, A., and Wainscoat, J. S. (2013). Activation of the mTOR pathway by the amino acid (L)-leucine in the 5q-syndrome and other ribosomopathies. Adv. Biol. Regul. 53, 8-17. doi: 10.1016/j.jbior.2012.09.002.
7. Britsch, S., Li, L., Kirchhoff, S., Theuring, F., Brinkmann, V., Birchmeier, C., et al. (1998). The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 12, 1825-1836. doi: 10.1101/gad.12.12.1825.
8. Butler Tjaden, N. E., and Trainor, P. A. (2013). The developmental etiology and pathogenesis of Hirschsprung disease. Transl. Res. 162, 1-15. doi: 10.1016/j.trsl.2013.03.001.
9. Cheung, M., Chaboissier, M. C., Mynett, A., Hirst, E., Schedl, A., and Briscoe, J. (2005). The transcriptional control of trunk neural crest induction, survival, and delamination. Dev. Cell 8, 179-192. doi: 10.1016/j.devcel.2004.12.010.
10. Couly, G., Creuzet, S., Bennaceur, S., Vincent, C., and Le Douarin, N. M. (2002). Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129, 1061-1073.
11. Creuzet, S., Couly, G., Vincent, C., and Le Douarin, N. M. (2002). Negative effect of Hox gene expression on the development of the neural crest-derived facial skeleton. Development 129, 4301-4313.
12. Dai, M. S., and Lu, H. (2004). Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J. Biol. Chem. 279. 44475-44482. doi: 10.1074/jbc.M403722200.
13. Daniels, R. H., and Bokoch, G. M. (1999). p21-activated protein kinase: a crucial component of morphological signaling? Trends Biochem. Sci. 24 350-355. doi: 10.1016/S0968-0004(99)01442-5.
14. Dauwerse, J. G., Dixon, J., Seland, S., Ruivenkamp, C. A., van Haeringen, A., Hoefsloot, L. H., 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.
15. Davy, A., Aubin, J., and Soriano, P. (2004). Ephrin-B1 forward and reverse signaling are required during mouse development. Genes Dev. 18, 572-583. doi: 10.1101/gad.1171704.
16. de Pontual, L., Nepote, V., Attie-Bitach, T., Al Halabiah, H., Trang, H., Elghouzzi, V., et al. (2003). Noradrenergic neuronal development is impaired by mutation of the proneural HASH-1 gene in congenital central hypoventilation syndrome (Ondine's curse). Hum. Mol. Genet. 12, 3173-3180. doi: 10.1093/hmg/ddg339.
17. Devlin, E. E., Dacosta, L., Mohandas, N., Elliott, G., and Bodine, D. M. (2010). A transgenic mouse model demonstrates a dominant negative effect of a point mutation in the RPS19 gene associated with Diamond-Blackfan anemia. Blood 116, 2826-2835. doi: 10.1182/blood-2010-03-275776.
18. Dow, E., Cross, S., Wolgemuth, D. J., Lyonnet, S., Mulligan, L. M., Mascari, M., et al. (1994). Second locus for Hirschsprung disease/Waardenburg syndrome in a large Mennonite kindred. Am. J. Med. Genet. 53, 75-80. doi: 10.1002/ajmg.1320530116.
19. Du, Y. C., and Stillman, B. (2002). Yph1p, an ORC-interacting protein: potential links between cell proliferation control, replication, DNA, and ribosome biogenesis. Cell 109, 835-848. doi: 10.1016/S0092-8674(02)00773-0.
20. Dupin, E., and Coelho-Aguiar, J. M. (2013). Isolation and differentiation properties of neural crest stem cells. Cytometry A 83, 38-47. doi: 10.1002/cyto.a.22098.
21. Dupin, E., Glavieux, C., Vaigot, P., and Le Douarin, N. M. (2000). Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glial-melanocytic progenitor. Proc. Natl. Acad. Sci. U.S.A. 97, 7882-7887. doi: 10.1073/pnas.97.14.7882.
22. Duprez, D., Leyns, L., Bonnin, M. A., Lapointe, F., Etchevers, H., De Robertis, E. M., et al. (1999). Expression of Frzb-1 during chick development. Mech. Dev. 89, 179-183. doi: 10.1016/S0925-4773(99)00206-3.
23. Dutt, S., Narla, A., Lin, K., Mullally, A., Abayasekara, N., Megerdichian, C., et al. (2011). Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood 117, 2567-2576. doi: 10.1182/blood-2010-07-295238.
24. Etchevers, H. C., Amiel, J., and Lyonnet, S. (2006). Molecular bases of human neurocristopathies. Adv. Exp. Med. Biol. 589, 213-234. doi: 10.1007/978-0-387-46954-6_14.
25. Gammill, L. S., and Bronner-Fraser, M. (2002). Genomic analysis of neural crest induction. Development 129, 5731-5741. doi: 10.1242/dev.00175.
26. Garcia-Bellido, A., and de Celis, J. F. (2009). The complex tale of the achaete-scute complex: a paradigmatic case in the analysis of gene organization and function during development. Genetics 182, 631-639. doi: 10.1534/genetics.109.104083.
27. Green, D. R., and Evan, G. I. (2002). A matter of life and death. Cancer Cell 1, 19-30. doi: 10.1016/S1535-6108(02)00024-7.
28. Guillemot, F., Caspary, T., Tilghman, S. M., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., et al. (1995). Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat. Genet. 9, 235-242. doi: 10.1038/ng0395-235.
29. Halilagic, A., Zile, M. H., and Studer, M. (2003). A novel role for retinoids in patterning the avian forebrain during presomite stages. Development 130, 2039-2050. doi: 10.1242/dev.00423.
30. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. (1997). Mdm2 promotes the rapid degradation of p53. Nature 387, 296-299. doi: 10.1038/387296a0.
31. Henras, A. K., Soudet, J., Gerus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A., 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.
32. Honda, R., Tanaka, H., and Yasuda, H. (1997). Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420, 25-27. doi: 10.1016/S0014-5793(97)01480-4.
33. Horos, R., and von Lindern, M. (2012). Molecular mechanisms of pathology and treatment in Diamond Blackfan Anaemia. Br. J. Haematol. 159, 514-527.
34. Horton, L. E., Bushell, M., Barth-Baus, D., Tilleray, V. J., Clemens, M. J., and Hensold, J. O. (2002). p53 activation results in rapid dephosphorylation of the eIF4E-binding protein 4E-BP1, inhibition of ribosomal protein S6 kinase and inhibition of translation initiation. Oncogene 21 5325-5334. doi: 10.1038/sj.onc.1205662.
35. Hosoda, K., Hammer, R. E., Richardson, J. A., Baynash, A. G., Cheung, J. C., Giaid, A., et al. (1994). Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice. Cell 79, 1267-1276. doi: 10.1016/0092-8674(94)90017-5.
36. Ito, E., Konno, Y., Toki, T., and Terui, K. (2010). Molecular pathogenesis in Diamond-Blackfan anemia. Int. J. Hematol. 92, 413-418. doi: 10.1007/s12185-010-0693-7.
37. Jensen, N. A., Rodriguez, M. L., Garvey, J. S., Miller, C. A., and Hood, L. (1993). Transgenic mouse model for neurocristopathy: Schwannomas and facial bone tumors. Proc. Natl. Acad. Sci. U.S.A. 90, 3192-3196. doi: 10.1073/pnas.90.8.3192.
38. Johnson, A. W., Lund, E., and Dahlberg, J. (2002). Nuclear export of ribosomal subunits. Trends Biochem. Sci. 27, 580-585. doi: 10.1016/S0968-0004(02)02208-9.
39. Johnson, J. E., Birren, S. J., and Anderson, D. J. (1990). Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346, 858-861. doi: 10.1038/346858a0.
40. Jones, N. C., Lynn, M. L., Gaudenz, K., Sakai, D., Aoto, K., Rey, J. P., et al. (2008). Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med. 14, 125-133. doi: 10.1038/nm1725.
41. Khanna-Gupta, A. (2011). Regulation and deregulation of mRNA translation during myeloid maturation. Exp. Hematol. 39, 133-141. doi: 10.1016/j.exphem.2010.10.011.
42. Kim, H. W., Yang, P., Qyang, Y., Lai, H., Du, H., Henkel, J. S., et al. (2001). Genetic and molecular characterization of Skb15, a highly conserved inhibitor of the fission yeast PAK, Shk1. Mol. Cell 7, 1095-1101. doi: 10.1016/S1097-2765(01)00248-9.
43. Kondrashov, N., Pusic, A., Stumpf, C. R., Shimizu, K., Hsieh, A. C., Xue, S., 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.
44. Kressler, D., Hurt, E., and Bassler, J. (2010). Driving ribosome assembly. Biochimica et biophysica acta 1803, 673-683. doi: 10.1016/j.bbamcr.2009.10.009.
45. Kruger, G. M., Mosher, J. T., Bixby, S., Joseph, N., Iwashita, T., and Morrison, S. J. (2002). Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35, 657-669. doi: 10.1016/S0896-6273(02)00827-9.
46. Kubbutat, M. H., Jones, S. N., and Vousden, K. H. (1997). Regulation of p53 stability by Mdm2. Nature 387, 299-303. doi: 10.1038/387299a0.
47. Landowski, M., O'Donohue, M. F., Buros, C., Ghazvinian, R., Montel-Lehry, N., Vlachos, A., Sieff, C. A., et al. (2013). Novel deletion of RPL15 identified by array-comparative genomic hybridization in Diamond-Blackfan anemia. Hum. Genet. 132, 1265-1274. doi: 10.1007/s00439-013-1326-z.
48. Lee, G., Kim, H., Elkabetz, Y., Al Shamy, G., Panagiotakos, G., Barberi, T., et al. (2007). Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat. Biotechnol. 25, 1468-1475. doi: 10.1038/nbt1365.
49. Le Lievre, C. S., and Le Douarin, N. M. (1975). Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J. Embryol. Exp. Morphol. 34, 125-154.
50. Lewis, J. L., Bonner, J., Modrell, M., Ragland, J. W., Moon, R. T., Dorsky, R. I., et al. (2004). Reiterated Wnt signaling during zebrafish neural crest development. Development 131, 1299-1308. doi: 10.1242/dev.01007.
51. Locascio, A., Manzanares, M., Blanco, M. J., and Nieto, M. A. (2002). Modularity and reshuffling of Snail and Slug expression during vertebrate evolution. Proc. Natl. Acad. Sci. U.S.A. 99, 16841-16846. doi: 10.1073/pnas.262525399.
52. Lohrum, M. A., Ludwig, R. L., Kubbutat, M. H., Hanlon, M., and Vousden, K. H. (2003). Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 3, 577-587. doi: 10.1016/S1535-6108(03)00134-X.
53. Michael, D., and Oren, M. (2003). The p53-Mdm2 module and the ubiquitin system. Semin. Cancer Biol. 13, 49-58. doi: 10.1016/S1044-579X(02)00099-8.
54. Momand, J., Jung, D., Wilczynski, S., and Niland, J. (1998). The MDM2 gene amplification database. Nucleic Acids Res. 26, 3453-3459. doi: 10.1093/nar/26.15.3453.
55. Monsoro-Burq, A. H., Wang, E., and Harland, R. (2005). Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev. Cell 8, 167-178. doi: 10.1016/j.devcel.2004.12.017.
56. Morgan, W. C. (1950). A new tail-short mutation in the mouse whose lethal effects are conditioned by the residual genotypes. J. Hered. 41, 208-215.
57. Morrison, K. M., Miesegaes, G. R., Lumpkin, E. A., and Maricich, S. M. (2009). Mammalian Merkel cells are descended from the epidermal lineage. Dev. Biol. 336, 76-83. doi: 10.1016/j.ydbio.2009.09.032.
58. Nakagawara, A. (2004). Neural crest development and neuroblastoma: the genetic and biological link. Prog. Brain Res. 146, 233-242. doi: 10.1016/S0079-6123(03)46015-9.
59. Norbury, C., and Nurse, P. (1992). Animal cell cycles and their control. Annu. Rev. Biochem. 61, 441-470. doi: 10.1146/annurev.bi.61.070192.002301.
60. Ong, C. C., Jubb, A. M., Zhou, W., Haverty, P. M., Harris, A. L., Belvin, M., et al. (2011). p21-activated kinase 1, PAK'ed with potential. Oncotarget 2. 491-496.
61. Parras, C. M., Galli, R., Britz, O., Soares, S., Galichet, C., Battiste, J., et al. (2004). Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23, 4495-4505. doi: 10.1038/sj.emboj.7600447.
62. Pattyn, A., Simplicio, N., van Doorninck, J. H., Goridis, C., Guillemot, F., and Brunet, J. F. (2004). Ascl1/Mash1 is required for the development of central serotonergic neurons. Nat. Neurosci. 7, 589-595. doi: 10.1038/nn1247.
63. Payne, E. M., Virgilio, M., Narla, A., Sun, H., Levine, M., Paw, B. H., et al. (2012). L-Leucine improves the anemia and developmental defects associated with Diamond-Blackfan anemia and del(5q) MDS by activating the mTOR pathway. Blood 120, 2214-2224. doi: 10.1182/blood-2011-10-382986.
64. Pingault, V., Bondurand, N., Kuhlbrodt, K., Goerich, D. E., Prehu, M. O., Puliti, A., et al. (1998). SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat. Genet. 18, 171-173. doi: 10.1038/ng0298-171.
65. Pla, P., Alberti, C., Solov'eva, O., Pasdar, M., Kunisada, T., and Larue, L. (2005). Ednrb2 orients cell migration towards the dorsolateral neural crest pathway and promotes melanocyte differentiation. Pigment Cell Res. 18, 181-187. doi: 10.1111/j.1600-0749.2005.00230.x.
66. Poswillo, D. (1975). The pathogenesis of the Treacher Collins syndrome (mandibulofacial dysostosis). Br. J. Oral Surg. 13, 1-26. doi: 10.1016/0007-117X(75)90019-0.
67. Puffenberger, E. G., Hosoda, K., Washington, S. S., Nakao, K., deWit, D., Yanagisawa, M., et al. (1994). A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung's disease. Cell 79, 1257-1266. doi: 10.1016/0092-8674(94)90016-7.
68. Qualman, S. J., Green, W. R., Brovall, C., and Leventhal, B. G. (1986). Neurofibromatosis and associated neuroectodermal tumors: a congenital neurocristopathy. Pediatr. Pathol. 5, 65-78. doi: 10.3109/15513818609068849.
69. Ramagopal, S. (1992). The Dictyostelium ribosome: biochemistry, molecular biology, and developmental regulation. Biochem. Cell Biol. 70, 738-750. doi: 10.1139/o92-113.
70. Ross, A. P., Mansilla, M. A., Choe, Y., Helminski, S., Sturm, R., Maute, R. L., et al. (2013). A mutation in mouse Pak1ip1 causes orofacial clefting while human PAK1IP1 maps to 6p24 translocation breaking points associated with orofacial clefting. PLoS ONE 8:e69333. doi: 10.1371/journal.pone.0069333.
71. Ruhin, B., Creuzet, S., Vincent, C., Benouaiche, L., Le Douarin, N. M., and Couly, G. (2003). Patterning of the hyoid cartilage depends upon signals arising from the ventral foregut endoderm. Dev. Dyn. 228, 239-246. doi: 10.1002/dvdy.10380.
72. Ruvinsky, I., and Meyuhas, O. (2006). Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem. Sci. 31, 342-348. doi: 10.1016/j.tibs.2006.04.003.
73. Sakai, D., and Trainor, P. A. (2009). Treacher Collins syndrome: unmasking the role of Tcof1/treacle. Int. J. Biochem. Cell Biol. 41, 1229-1232. doi: 10.1016/j.biocel.2008.10.026.
74. Sanchez-Martin, M., Rodriguez-Garcia, A., Perez-Losada, J., Sagrera, A., Read, A. P., and Sanchez-Garcia, I. (2002). SLUG (SNAI2) deletions in patients with Waardenburg disease. Hum. Mol. Genet. 11, 3231-3236. doi: 10.1093/hmg/11.25.3231.
75. Sauka-Spengler, T., and Bronner-Fraser, M. (2008). A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9, 557-568. doi: 10.1038/nrm2428.
76. Saveanu, C., Namane, A., Gleizes, P. E., Lebreton, A., Rousselle, J. C., Noaillac-Depeyre, J., et al. (2003). Sequential protein association with nascent 60S ribosomal particles. Mol. Cell. Biol. 23, 4449-4460. doi: 10.1128/MCB.23.13.4449-4460.2003.
77. Saveanu, C., Rousselle, J. C., Lenormand, P., Namane, A., Jacquier, A., and Fromont-Racine, M. (2007). The p21-activated protein kinase inhibitor Skb15 and its budding yeast homologue are 60S ribosome assembly factors. Mol. Cell. Biol. 27, 2897-2909. doi: 10.1128/MCB.00064-07.
78. Schneider, R. A., and Helms, J. A. (2003). The cellular and molecular origins of beak morphology. Science 299, 565-568. doi: 10.1126/science.1077827.
79. Schneider, R. A., Hu, D., Rubenstein, J. L., Maden, M., and Helms, J. A. (2001). Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 128, 2755-2767.
80. Sengupta, S., Peterson, T. R., and Sabatini, D. M. (2010). Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40, 310-322. doi: 10.1016/j.molcel.2010.09.026.
81. Stone, J. G., Spirling, L. I., and Richardson, M. K. (1997). The neural crest population responding to endothelin-3 in vitro includes multipotent cells. J. Cell Sci. 110 (Pt 14), 1673-1682.
82. Szeder, V., Grim, M., Halata, Z., and Sieber-Blum, M. (2003). Neural crest origin of mammalian Merkel cells. Dev. Biol. 253, 258-263. doi: 10.1016/S0012-1606(02)00015-5.
83. Toledo, F., and Wahl, G. M. (2006). Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat. Rev. Cancer 6, 909-923. doi: 10.1038/nrc2012.
84. Trainor, P. A. (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. doi: 10.1002/ajmg.a.33454.
85. Trainor, P. A., Dixon, J., and Dixon, M. J. (2009). Treacher Collins syndrome: etiology, pathogenesis and prevention. Eur. J. Hum. Genet. 17, 275-283. doi: 10.1038/ejhg.2008.221.
86. Uechi, T., Nakajima, Y., Chakraborty, A., Torihara, H., Higa, S., and Kenmochi, N. (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. doi: 10.1093/hmg/ddn216.
87. Venema, J., and Tollervey, D. (1999). Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33, 261-311. doi: 10.1146/annurev.genet.33.1.261.
88. Vogelstein, B., Lane, D., and Levine, A. J. (2000). Surfing the p53 network. Nature 408, 307-310. doi: 10.1038/35042675.
89. Vousden, K. H. (2002). Activation of the p53 tumor suppressor protein. Biochim. Biophys. Acta 1602, 47-59. doi: 10.1016/S0304-419X(02)00035-5.
90. Wakahashi, S., Sudo, T., Oka, N., Ueno, S., Yamaguchi, S., Fujiwara, K., et al. (2013). VAV1 represses E-cadherin expression through the transactivation of Snail and Slug: a potential mechanism for aberrant epithelial to mesenchymal transition in human epithelial ovarian cancer. Transl. Res. 162, 181-190. doi: 10.1016/j.trsl.2013.06.005.
91. Watanabe, A., Takeda, K., Ploplis, B., and Tachibana, M. (1998). Epistatic relationship between Waardenburg syndrome genes MITF and PAX3. Nat. Genet. 18, 283-286. doi: 10.1038/ng0398-283.
92. Yu, W., Qiu, Z., Gao, N., Wang, L., Cui, H., Qian, Y., et al. (2011). PAK1IP1, a ribosomal stress-induced nucleolar protein, regulates cell proliferation via the p53-MDM2 loop. Nucleic Acids Res. 39, 2234-2248. doi: 10.1093/nar/gkq1117.
93. Zarbalis, K., May, S. R., Shen, Y., Ekker, M., Rubenstein, J. L., and Peterson, A. S. (2004). A focused and efficient genetic screening strategy in the mouse: identification of mutations that disrupt cortical development. PLoS Biol. 2:E219. doi: 10.1371/journal.pbio.0020219.
94. Zhang, Y., Wolf, G. W., Bhat, K., Jin, A., Allio, T., Burkhart, W. A., et al. (2003). Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol. Cell. Biol. 23, 8902-8912. doi: 10.1128/MCB.23.23.8902-8912.2003.
95. Zhu, L., Lee, H. O., Jordan, C. S., Cantrell, V. A., Southard-Smith, E. M., and Shin, M. K. (2004). Spatiotemporal regulation of endothelin receptor-B by SOX10 in neural crest-derived enteric neuron precursors. Nat. Genet. 36, 732-737. doi: 10.1038/ng1371.