The neural crest-enriched microRNA miR-452 regulates epithelial-mesenchymal signaling in the first pharyngeal arch

Development

Volumn 137, Issue 24, 2010, Pages 4307-4316

  Sheehy, Neil T ^a,b   Cordes, Kimberly R ^a,b   White, Mark P ^a,b   Ivey, Kathryn N ^a,b   Srivastava, Deepak ^a,b  

^a GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dicer (Dicer1); Epithelial mesenchymal interaction; microRNA; Mouse; Neural crest; Pharyngeal arch

Indexed keywords

DICER; FIBROBLAST GROWTH FACTOR 8; MICRORNA; MICRORNA 452; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX2; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MORPHOLOGY; EMBRYO; EPITHELIAL MESENCHYMAL SIGNALING; GENE EXPRESSION REGULATION; GENE SILENCING; HEART SEPTUM DEFECT; IN VIVO STUDY; MOUSE; NEURAL CREST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARYNX; PHARYNX ARCH; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPINAL GANGLION; THYMUS; TISSUE DIFFERENTIATION; TRANSCRIPTION REGULATION;

ANIMALS; BRANCHIAL REGION; CELL LINE; DEAD-BOX RNA HELICASES; ENDORIBONUCLEASES; FIBROBLAST GROWTH FACTOR 8; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, MUTANT STRAINS; MICRORNAS; NEURAL CREST; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; WNT PROTEINS;

MURINAE;

EID: 78650212442     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.052647     Document Type: Article

References (59)

1. Arnold, J. S., Werling, U., Braunstein, E. M., Liao, J., Nowotschin, S., Edelmann, W., Hebert, J. M. and Morrow, B. E. (2006). Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133, 977-987.
2. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
3. Cordes, K. R., Sheehy, N. T., White, M. P., Berry, E. C., Morton, S. U., Muth, A. N., Lee, T.-H., Miano, J. M., Ivey, K. N. and Srivastava, D. (2009). miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460, 705-710.
4. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. and McMahon, A. P. (1998). Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8, 1323-1326.
5. Epstein, J. A. and Parmacek, M. S. (2005). Recent advances in cardiac development with therapeutic implications for adult cardiovascular disease. Circulation 112, 592-597.
6. Garg, V., Yamagishi, C., Hu, T., Kathiriya, I. S., Yamagishi, H. and Srivastava, D. (2001). Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev. Biol. 235, 62-73.
7. Gavin, B. J., McMahon, J. A. and McMahon, A. P. (1990). Expression of multiple novel Wnt-1/int-1-related genes during fetal and adult mouse development. Genes Dev. 4, 2319-2332.
8. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
9. Goodrich, L. V., Milenkovic, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113. (Pubitemid 27371635)
10. Gordon, J., Patel, S. R., Mishina, Y. and Manley, N. R. (2010). Evidence for an early role for BMP4 signaling in thymus and parathyroid morphogenesis. Dev. Biol. 339, 141-154.
11. Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N. and Shiekhattar, R. (2004). The Microprocessor complex mediates the genesis of microRNAs. Nature 432, 235-240. (Pubitemid 39545855)
12. Harfe, B. D., McManus, M. T., Mansfield, J. H., Hornstein, E. and Tabin, C. J. (2005). The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl. Acad. Sci. USA 102, 10898-10903. (Pubitemid 41105964)
13. Harris, K. S., Zhang, Z., McManus, M. T., Harfe, B. D. and Sun, X. (2006). Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. USA 103, 2208-2213. (Pubitemid 43271648)
14. Haworth, K. E., Wilson, J. M., Grevellec, A., Cobourne, M. T., Healy, C., Helms, J. A., Sharpe, P. T. and Tucker, A. S. (2007). Sonic hedgehog in the pharyngeal endoderm controls arch pattern via regulation of Fgf8 in head ectoderm. Dev. Biol. 303, 244-258. (Pubitemid 46241102)
15. Helms, J. A. and Schneider, R. A. (2003). Cranial skeletal biology. Nature 423, 326-331.
16. High, F. A., Jain, R., Stoller, J. Z., Antonucci, N. B., Lu, M. M., Loomes, K. M., Kaestner, K. H., Pear, W. S. and Epstein, J. A. (2009). Murine Jagged1/Notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J. Clin. Invest. 119, 1986-1996.
17. Hu, T., Yamagishi, H., Maeda, J., McAnally, J., Yamagishi, C. and Srivastava, D. (2004). Tbx1 regulates fibroblast growth factors in the anterior heart field through a reinforcing autoregulatory loop involving forkhead transcription factors. Development 131, 5491-5502.
18. Jiang, X., Rowitch, D. H., Soriano, P., McMahon, A. P. and Sucov, H. M. (2000). Fate of the mammalian cardiac neural crest. Development 127, 1607-1616.
19. Kameda, Y. (2009). Hoxa3 and signaling molecules involved in aortic arch patterning and remodeling. Cell Tissue Res. 336, 165-178.
20. Kobayashi, T., Lu, J., Cobb, B. S., Rodda, S. J., McMahon, A. P., Schipani, E., Merkenschlager, M. and Kronenberg, H. M. (2008). Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc. Natl. Acad. Sci. USA 105, 1949-1954.
21. Krutzfeldt, J., Rajewsky, N., Braich, R., Rajeev, K. G., Tuschl, T., Manoharan, M. and Stoffel, M. (2005). Silencing of microRNAs in vivo with 'antagomirs'. Nature 438, 685-689.
22. Le Douarin, N. M., Creuzet, S., Couly, G. and Dupin, E. (2004). Neural crest cell plasticity and its limits. Development 131, 4637-4650.
23. Lee, H. Y., Kleber, M., Hari, L., Brault, V., Suter, U., Taketo, M. M., Kemler, R. and Sommer, L. (2004a). Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 303, 1020-1023.
24. Lee, J., Platt, K. A., Censullo, P. and Ruiz i Altaba, A. (1997). Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124, 2537-2552.
25. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J. and Carthew, R. W. (2004b). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81.
26. Li, C., Hu, L., Xiao, J., Chen, H., Li, J. T., Bellusci, S., Delanghe, S. and Minoo, P. (2005). Wnt5a regulates Shh and Fgf10 signaling during lung development. Dev. Biol. 287, 86-97.
27. Lindsay, E. A. (2001). Chromosomal microdeletions: dissecting del22q11 syndrome. Nat. Rev. Genet. 2, 858-868.
28. Lindsay, E. A., Vitelli, F., Su, H., Morishima, M., Huynh, T., Pramparo, T., Jurecic, V., Ogunrinu, G., Sutherland, H. F., Scambler, P. J. et al. (2001). Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410, 97-101. (Pubitemid 32225843)
29. Macatee, T. L., Hammond, B. P., Arenkiel, B. R., Francis, L., Frank, D. U. and Moon, A. M. (2003). Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130, 6361-6374.
30. Maurer, J., Fuchs, S., Jager, R., Kurz, B., Sommer, L. and Schorle, H. (2007). Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation 75, 580-591. (Pubitemid 47301600)
31. McLeod, M. J. (1980). Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22, 299-301.
32. Merscher, S., Funke, B., Epstein, J. A., Heyer, J., Puech, A., Lu, M. M., Xavier, R. J., Demay, M. B., Russell, R. G., Factor, S. et al. (2001). TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104, 619-629.
33. Meulemans, D. and Bronner-Fraser, M. (2004). Gene-regulatory interactions in neural crest evolution and development. Dev. Cell 7, 291-299.
34. Meyers, E. N. and Martin, G. R. (1999). Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH. Science 285, 403-406.
35. Olson, E. N. (2006). Gene regulatory networks in the evolution and development of the heart. Science 313, 1922-1927.
36. Ornitz, D. M. and Marie, P. J. (2002). FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev. 16, 1446-1465.
37. Qiu, M., Bulfone, A., Martinez, S., Meneses, J. J., Shimamura, K., Pedersen, R. A. and Rubenstein, J. L. (1995). Null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes Dev. 9, 2523-2538.
38. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
39. Satokata, I. and Maas, R. (1994). Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 6, 348-356. (Pubitemid 24190017)
40. Sauka-Spengler, T. and Bronner-Fraser, M. (2008). A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9, 557-568. (Pubitemid 351881841)
41. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
42. Srivastava, D. (2006). Making or breaking the heart: from lineage determination to morphogenesis. Cell 126, 1037-1048.
43. Stemple, D. L. and Anderson, D. J. (1992). Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973-985.
44. Thomas, B. L., Liu, J. K., Rubenstein, J. L. and Sharpe, P. T. (2000). Independent regulation of Dlx2 expression in the epithelium and mesenchyme of the first branchial arch. Development 127, 217-224.
45. Thomas, T., Kurihara, H., Yamagishi, H., Kurihara, Y., Yazaki, Y., Olson, E. N. and Srivastava, D. (1998). A signaling cascade involving endothelin-1, dHAND and msx1 regulates development of neural-crest-derived branchial arch mesenchyme. Development 125, 3005-3014.
46. Trainor, P. A., Ariza-McNaughton, L. and Krumlauf, R. (2002). Role of the isthmus and FGFs in resolving the paradox of neural crest plasticity and prepatterning. Science 295, 1288-1291.
47. Trowell, O. A. (1954). A modified technique for organ culture in vitro. Exp. Cell Res. 6, 246-248.
48. Trumpp, A., Depew, M. J., Rubenstein, J. L., Bishop, J. M. and Martin, G. R. (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.
49. van Rooij, E., Sutherland, L. B., Qi, X., Richardson, J. A., Hill, J. and Olson, E. N. (2007). Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575-579.
50. Waldo, K. L., Hutson, M. R., Stadt, H. A., Zdanowicz, M., Zdanowicz, J. and Kirby, M. L. (2005). Cardiac neural crest is necessary for normal addition of the myocardium to the arterial pole from the secondary heart field. Dev. Biol. 281, 66-77.
51. Washington Smoak, I., Byrd, N. A., Abu-Issa, R., Goddeeris, M. M., Anderson, R., Morris, J., Yamamura, K., Klingensmith, J. and Meyers, E. N. (2005). Sonic hedgehog is required for cardiac outflow tract and neural crest cell development. Dev. Biol. 283, 357-372.
52. Yamagishi, C., Yamagishi, H., Maeda, J., Tsuchihashi, T., Ivey, K., Hu, T. and Srivastava, D. (2006). Sonic hedgehog is essential for first pharyngeal arch development. Pediatr. Res. 59, 349-354.
53. Yamagishi, H., Maeda, J., Hu, T., McAnally, J., Conway, S. J., Kume, T., Meyers, E. N., Yamagishi, C. and Srivastava, D. (2003). Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev. 17, 269-281. (Pubitemid 36105898)
54. Yamaguchi, T. P., Bradley, A., McMahon, A. P. and Jones, S. (1999). A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223.
55. Yang, Y. H., Dudoit, S., Luu, P., Lin, D. M., Peng, V., Ngai, J. and Speed, T. P. (2002). Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30, e15.
56. Yi, R., Pasolli, H. A., Landthaler, M., Hafner, M., Ojo, T., Sheridan, R., Sander, C., O'Carroll, D., Stoffel, M., Tuschl, T. et al. (2009). DGCR8-dependent microRNA biogenesis is essential for skin development. Proc. Natl. Acad. Sci. USA 106, 498-502.
57. Zehir, A., Hua, L. L., Maska, E. L., Morikawa, Y. and Cserjesi, P. (2010). Dicer is required for survival of differentiating neural crest cells. Dev. Biol. 340, 459-467.
58. Zhang, Z., Cerrato, F., Xu, H., Vitelli, F., Morishima, M., Vincentz, J., Furuta, Y., Ma, L., Martin, J. F., Baldini, A. et al. (2005). Tbx1 expression in pharyngeal epithelia is necessary for pharyngeal arch artery development. Development 132, 5307-5315.
59. Zhao, Y., Ransom, J. F., Li, A., Vedantham, V., von Drehle, M., Muth, A. N., Tsuchihashi, T., McManus, M. T., Schwartz, R. J. and Srivastava, D. (2007). Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 129, 303-317.