Lin28 proteins are required for germ layer specification in Xenopus

Development (Cambridge)

Volumn 140, Issue 5, 2013, Pages 976-986

  Faas, Laura ^a   Warrander, Fiona C ^a   Maguire, Richard ^a   Ramsbottom, Simon A ^a   Quinn, Diana ^a   Genever, Paul ^a   Isaacs, Harry V ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Activin; FGF; Germ layer; Let 7; Lin28a; Lin28b; Mesoderm; miRNA; Nodal; Pluripotency; Xenopus

Indexed keywords

ACTIVIN; FIBROBLAST GROWTH FACTOR; MICRORNA; MICRORNA LET 7; RNA BINDING PROTEIN; RNA BINDING PROTEIN LIN 28; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION; GENE FUNCTION; GENOME; GERM LAYER; LIN28A GENE; LIN28B GENE; MESODERM; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; WESTERN BLOTTING; XENOPUS TROPICALIS; ZYGOTE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CLONING, MOLECULAR; EMBRYO, NONMAMMALIAN; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GERM LAYERS; MORPHOLINOS; PROTEIN ISOFORMS; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; XENOPUS; XENOPUS PROTEINS;

EID: 84873706905     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.089797     Document Type: Article

References (64)

1. Amaya, E., Stein, P. A., Musci, T. J. and Kirschner, M. W. (1993). FGF signaling in the early specification of mesoderm in Xenopus. Development 118, 477-487.
2. Ambros, V. and Horvitz, H. R. (1984). Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409-416.
3. Baker, J. C. and Harland, R. M. (1996). A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev. 10, 1880-1889.
4. Balzer, E., Heine, C., Jiang, Q., Lee, V. M. and Moss, E. G. (2010). LIN28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro. Development 137, 891-900.
5. Bobbs, A. S., Saarela, A. V., Yatskievych, T. A. and Antin, P. B. (2012). FGF Signaling during gastrulation negatively modulates the abundance of microRNAs that regulate proteins required for cell migration and embryo patterning. J. Biol. Chem. 287, 38505-38514.
6. Bourillot, P. Y., Garrett, N. and Gurdon, J. B. (2002). A changing morphogen gradient is interpreted by continuous transduction flow. Development 129, 2167-2180.
7. Bouvet, P. and Wolffe, A. P. (1994). A role for transcription and FRGY2 in masking maternal mRNA within Xenopus oocytes. Cell 77, 931-941.
8. Boyerinas, B., Park, S. M., Hau, A., Murmann, A. E. and Peter, M. E. (2010). The role of let-7 in cell differentiation and cancer. Endocr. Relat. Cancer 17, F19-F36.
9. Branney, P. A., Faas, L., Steane, S. E., Pownall, M. E. and Isaacs, H. V. (2009). Characterisation of the fibroblast growth factor dependent transcriptome in early development. PLoS ONE 4, e4951.
10. Christen, B. and Slack, J. M. (1999). Spatial response to fibroblast growth factor signalling in Xenopus embryos. Development 126, 119-125.
11. Darr, H. and Benvenisty, N. (2008). Genetic analysis of the role of the reprogramming gene LIN-28 in human embryonic stem cells. Stem Cells 27, 352-362.
12. De Robertis, E. M. (2006). Spemann's organizer and self-regulation in amphibian embryos. Nat. Rev. Mol. Cell Biol. 7, 296-302.
13. Dorey, K. and Amaya, E. (2010). FGF signalling: diverse roles during early vertebrate embryogenesis. Development 137, 3731-3742.
14. Hagan, J. P., Piskounova, E. and Gregory, R. I. (2009). Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 16, 1021-1025.
15. Harland, R. M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695.
16. Hartge, P. (2009). Genetics of reproductive lifespan. Nat. Genet. 41, 637-638.
17. Heasman, J. (2006). Patterning the early Xenopus embryo. Development 133, 1205-1217.
18. Heo, I., Joo, C., Cho, J., Ha, M., Han, J. and Kim, V. N. (2008). Lin28 mediates the terminal uridylation of let-7 precursor microRNA. Mol. Cell 32, 276-284.
19. Heo, I., Joo, C., Kim, Y. K., Ha, M., Yoon, M. J., Cho, J., Yeom, K. H., Han, J. and Kim, V. N. (2009). TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138, 696-708.
20. Holley, S. A., Jackson, P. D., Sasai, Y., Lu, B., De Robertis, E. M., Hoffmann, F. M. and Ferguson, E. L. (1995). A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249-253.
21. Hongo, I., Kengaku, M. and Okamoto, H. (1999). FGF signaling and the anterior neural induction in Xenopus. Dev. Biol. 216, 561-581.
22. Hopwood, N. D., Pluck, A., Gurdon, J. B. and Dilworth, S. M. (1992). Expression of XMyoD protein in early Xenopus laevis embryos. Development 114, 31-38.
23. Isaacs, H. V. (1997). New perspectives on the role of the fibroblast growth factor family in amphibian development. Cell. Mol. Life Sci. 53, 350-361.
24. Isaacs, H. V., Tannahill, D. and Slack, J. M. W. (1992). Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification. Development 114, 711-720.
25. Isaacs, H. V., Pownall, M. E. and Slack, J. M. (1994). eFGF regulates Xbra expression during Xenopus gastrulation. EMBO J. 13, 4469-4481.
26. Jin, J., Jing, W., Lei, X. X., Feng, C., Peng, S., Boris-Lawrie, K. and Huang, Y. (2011). Evidence that Lin28 stimulates translation by recruiting RNA helicase A to polysomes. Nucleic Acids Res. 39, 3724-3734.
27. Khokha, M. K., Yeh, J., Grammer, T. C. and Harland, R. M. (2005). Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev. Cell 8, 401-411.
28. Kloosterman, W. P., Wienholds, E., Ketting, R. F. and Plasterk, R. H. (2004). Substrate requirements for let-7 function in the developing zebrafish embryo. Nucleic Acids Res. 32, 6284-6291.
29. Kunath, T., Saba-El-Leil, M. K., Almousailleakh, M., Wray, J., Meloche, S. and Smith, A. (2007). FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134, 2895-2902.
30. Lei, X. X., Xu, J., Ma, W., Qiao, C., Newman, M. A., Hammond, S. M. and Huang, Y. (2012). Determinants of mRNA recognition and translation regulation by Lin28. Nucleic Acids Res. 40, 3574-3584.
31. Lettre, G., Jackson, A. U., Gieger, C., Schumacher, F. R., Berndt, S. I., Sanna, S., Eyheramendy, S., Voight, B. F., Butler, J. L., Guiducci, C. et al. (2008). Identification of ten loci associated with height highlights new biological pathways in human growth. Nat. Genet. 40, 584-591.
32. Lightfoot, H. L., Bugaut, A., Armisen, J., Lehrbach, N. J., Miska, E. A. and Balasubramanian, S. (2011). A LIN28-dependent structural change of pre-let-7g directly inhibits Dicer processing. Biochemistry 50, 7514-7521
33. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
34. Matsumoto, K. and Wolffe, A. P. (1998). Gene regulation by Y-box proteins: coupling control of transcription and translation. Trends Cell Biol. 8, 318-323.
35. Moss, E. G. and Tang, L. (2003). Conservation of the heterochronic regulator Lin-28, its developmental expression and microRNA complementary sites. Dev. Biol. 258, 432-442.
36. Moss, E. G., Lee, R. C. and Ambros, V. (1997). The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 88, 637-646.
37. Nam, Y., Chen, C., Gregory, R. I., Chou, J. J. and Sliz, P. (2011). Molecular basis for interaction of let-7 microRNAs with Lin28. Cell 147, 1080-1091.
38. Nieuwkoop, P. D. and Faber, J. (1994). Normal Table of Xenopus laevis (Daudin). New York, USA: Garland Publishing.
39. Peng, S., Chen, L. L., Lei, X. X., Yang, L., Lin, H., Carmichael, G. G. and Huang, Y. (2011). Genome-wide studies reveal that Lin28 enhances the translation of genes important for growth and survival of human embryonic stem cells. Stem Cells 29, 496-504.
40. Piskounova, E., Viswanathan, S. R., Janas, M., LaPierre, R. J., Daley, G. Q., Sliz, P. and Gregory, R. I. (2008). Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28. J. Biol. Chem. 283, 21310-21314.
41. Piskounova, E., Polytarchou, C., Thornton, J. E., LaPierre, R. J., Pothoulakis, C., Hagan, J. P., Iliopoulos, D. and Gregory, R. I. (2011). Lin28A and Lin28B inhibit let-7 microRNA biogenesis by distinct mechanisms. Cell 147, 1066-1079.
42. Polesskaya, A., Cuvellier, S., Naguibneva, I., Duquet, A., Moss, E. G. and Harel-Bellan, A. (2007). Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes Dev. 21, 1125-1138.
43. Pownall, M. E. and Isaacs, H. V. (2010) FGF Signalling in Vertebrate Development. San Rafael, CA: Morgan & Claypool Life Sciences.
44. Qiu, C., Ma, Y., Wang, J., Peng, S. and Huang, Y. (2010). Lin28-mediated posttranscriptional regulation of Oct4 expression in human embryonic stem cells. Nucleic Acids Res. 38, 1240-1248.
45. Reece-Hoyes, John S., Keenan, Iain D. and Isaacs, Harry V. (2002). Cloning and expression of the Cdx family from the frog Xenopus tropicalis. Dev. Dyn. 223, 134-140.
46. Roth, M., Bonev, B., Lindsay, J., Lea, R., Panagiotaki, N., Houart, C. and Papalopulu, N. (2010). FoxG1 and TLE2 act cooperatively to regulate ventral telencephalon formation. Development 137, 1553-1562.
47. Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L. K. and De Robertis, E. M. (1994). Xenopus chordin: a novel dorsalizing factor activated by organizerspecific homeobox genes. Cell 79, 779-790.
48. Scerbo, P., Girardot, F., Vivien, C., Markov, G. V., Luxardi, G., Demeneix, B., Kodjabachian, L. and Coen, L. (2012). Ventx factors function as Nanog-like guardians of developmental potential in Xenopus. PLoS ONE 7, e36855.
49. Schulte-Merker, S. and Smith, J. C. (1995). Mesoderm formation in response to Brachyury requires FGF signalling, Curr. Biol. 5, 62-67.
50. Slack, J. M., Darlington, B. G., Heath, J. K. and Godsave, S. F. (1987). Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature 326, 197-200.
51. Smith, J. C., Price, B. M., Green, J. B., Weigel, D. and Herrmann, B. G. (1991). Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79-87.
52. ten Dijke, P. and Hill, C. S. (2004). New insights into TGF-beta-Smad signalling. Trends Biochem. Sci. 29, 265-273.
53. Umbhauer, M., Marshall, C. J., Mason, C. S., Old, R. W. and Smith, J. C. (1995). Mesoderm induction in Xenopus caused by activation of MAP kinase. Nature 376, 58-62.
54. Vadla, B., Kemper, K., Alaimo, J., Heine, C. and Moss, E. G. (2012). lin-28 controls the succession of cell fate choices via two distinct activities. PLoS Genet. 8, e1002588.
55. Viswanathan, S. R. and Daley, G. Q. (2010). Lin28: A microRNA regulator with a macro role. Cell 140, 445-449.
56. Viswanathan, S. R., Daley, G. Q. and Gregory, R. I. (2008). Selective blockade of microRNA processing by Lin28. Science 320, 97-100.
57. Wang, J., Cao, N., Yuan, M., Cui, H., Tang, Y., Qin, L., Huang, X., Shen, N. and Yang, H. T. (2012). MicroRNA-125b/Lin28 pathway contributes to the mesendodermal fate decision of embryonic stem cells. Stem Cells Dev. 21, 1524-1537.
58. West, J. A., Viswanathan, S. R., Yabuuchi, A., Cunniff, K., Takeuchi, A., Park, I. H., Sero, J. E., Zhu, H., Perez-Atayde, A., Frazier, A. L. et al. (2009.) A role for Lin28 in primordial germ-cell development and germ-cell malignancy. Nature 460, 909-913.
59. Winterbottom, E. F., Illes, J. C., Faas, L. and Isaacs, H. V. (2010). Conserved and novel roles for the Gsh2 transcription factor in primary neurogenesis. Development 137, 2623-2631.
60. Xu, B. and Huang, Y. (2009). Histone H2a mRNA interacts with Lin28 and contains a Lin28-dependent posttranscriptional regulatory element. Nucleic Acids Res. 37, 4256-4263.
61. Yang, D. H. and Moss, E. G. (2003). Temporally regulated expression of Lin-28 in diverse tissues of the developing mouse. Gene Expr. Patterns 3, 719-726.
62. Yokoyama, S., Hashimoto, M., Shimizu, H., Ueno-Kudoh, H., Uchibe, K., Kimura, I. and Asahara, H. (2008). Dynamic gene expression of Lin-28 during embryonic development in mouse and chicken. Gene Expr. Patterns 8, 155-160.
63. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R. et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920.
64. Zhu, H., Shah, S., Shyh-Chang, N., Shinoda, G., Einhorn, W. S., Viswanathan, S. R., Takeuchi, A., Grasemann, C., Rinn, J. L., Lopez, M. F. et al. (2010). Lin28a transgenic mice manifest size and puberty phenotypes identified in human genetic association studies. Nat. Genet. 42, 626-630.