Transcript processing and export kinetics are rate-limiting steps in expressing vertebrate segmentation clock genes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 46, 2013, Pages

  Hoyle, Nathaniel P ^a,b   Ish Horowicz, David ^b  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

mRNA processing; RNA export; RNA splicing; Somites; Transcriptional delays

Indexed keywords

LUNATIC FRINGE; NOTCH REGULATED ANKYRIN REPEAT PROTEIN; TRANSCRIPTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL KINETICS; CHICK; CONTROLLED STUDY; EMBRYO; EMBRYO SEGMENTATION; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN VIVO STUDY; INTRON; MESSENGER RNA SYNTHESIS; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; OSCILLATOR; PRIORITY JOURNAL; RNA SPLICING; RNA TRANSPORT; SEGMENTATION CLOCK GENE; SPECIES COMPARISON; TRANSCRIPTION ELONGATION; ZEBRA FISH;

MRNA PROCESSING; RNA EXPORT; RNA SPLICING; SOMITES; TRANSCRIPTIONAL DELAYS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOLOGICAL CLOCKS; BODY PATTERNING; CELL LINE; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOSYLTRANSFERASES; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MODELS, BIOLOGICAL; PROTEINS; RNA SPLICING; SPECIES SPECIFICITY; TIME FACTORS; ZEBRAFISH;

EID: 84887466041     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1308811110     Document Type: Article

References (55)

1. Cooke J, Zeeman EC (1976) A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J Theor Biol 58(2):455-476.
2. Oates AC, Morelli LG, Ares S (2012) Patterning embryos with oscillations: Structure, function and dynamics of the vertebrate segmentation clock. Development 139(4):625-639.
3. Palmeirim I, Henrique D, Ish-Horowicz D, Pourquié O (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91(5):639-648. (Pubitemid 27513655)
4. Pourquié O (2011) Vertebrate segmentation: From cyclic gene networks to scoliosis. Cell 145(5):650-663.
5. Jiang YJ, et al. (2000) Notch signalling and the synchronization of the somite segmentation clock. Nature 408(6811):475-479.
6. Masamizu Y, et al. (2006) Real-time imaging of the somite segmentation clock: Revelation of unstable oscillators in the individual presomitic mesoderm cells. Proc Natl Acad Sci USA 103(5):1313-1318. (Pubitemid 43191162)
7. Delaune EA, François P, Shih NP, Amacher SL (2012) Single-cell-resolution imaging of the impact of Notch signaling and mitosis on segmentation clock dynamics. Dev Cell 23(5):995-1005.
8. Lewis J (2003) Autoinhibition with transcriptional delay: A simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 13(16):1398-1408.
9. Giudicelli F, Özbudak EM, Wright GJ, Lewis J (2007) Setting the tempo in development: An investigation of the zebrafish somite clock mechanism. PLoS Biol 5(6):e150.
10. Bessho Y, Hirata H, Masamizu Y, Kageyama R (2003) Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock. Genes Dev 17(12):1451-1456. (Pubitemid 36734701)
11. Morimoto M, Takahashi Y, Endo M, Saga Y (2005) The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity. Nature 435(7040):354-359. (Pubitemid 40745545)
12. Saga Y, Hata N, Koseki H, Taketo MM (1997) Mesp2: A novel mouse gene expressed in the presegmented mesoderm and essential for segmentation initiation. Genes Dev 11(14):1827-1839. (Pubitemid 27315212)
13. Chen J, Kang L, Zhang N (2005) Negative feedback loop formed by Lunatic fringe and Hes7 controls their oscillatory expression during somitogenesis. Genesis 43(4):196-204. (Pubitemid 43117836)
14. Dale JK, et al. (2003) Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421(6920):275-278. (Pubitemid 36139132)
15. Ferjentsik Z, et al. (2009) Notch is a critical component of the mouse somitogenesis oscillator and is essential for the formation of the somites. PLoS Genet 5(9):e1000662.
16. Krol AJ, et al. (2011) Evolutionary plasticity of segmentation clock networks. Development 138(13):2783-2792.
17. Oates AC, Gorfinkiel N, González-Gaitán M, Heisenberg C-P (2009) Quantitative approaches in developmental biology. Nat Rev Genet 10(8):517-530.
18. Ingolia NT, Lareau LF, Weissman JS (2011) Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147(4):789-802.
19. Siwiak M, Zielenkiewicz P (2010) A comprehensive, quantitative, and genome-wide model of translation. PLOS Comput Biol 6(7):e1000865.
20. Swinburne IA, Silver PA (2008) Intron delays and transcriptional timing during development. Dev Cell 14(3):324-330.
21. Ben-Ari Y, et al. (2010) The life of an mRNA in space and time. J Cell Sci 123(Pt 10):1761-1774.
22. Darzacq X, et al. (2007) In vivo dynamics of RNA polymerase II transcription. Nat Struct Mol Biol 14(9):796-806. (Pubitemid 47373828)
23. Lionnet T, et al. (2011) A transgenic mouse for in vivo detection of endogenous labeled mRNA. Nat Methods 8(2):165-170.
24. Singh J, Padgett RA (2009) Rates of in situ transcription and splicing in large human genes. Nat Struct Mol Biol 16(11):1128-1133.
25. Wada Y, et al. (2009) A wave of nascent transcription on activated human genes. Proc Natl Acad Sci USA 106(43):18357-18361.
26. Hanisch A, et al. (2013) The elongation rate of RNA polymerase II in zebrafish and its significance in the somite segmentation clock. Development 140(2):444-453.
27. Mor A, Shav-Tal Y (2010) Dynamics and kinetics of nucleo-cytoplasmic mRNA export. Wiley Interdiscip Rev RNA 1(3):388-401.
28. Shav-Tal Y, et al. (2004) Dynamics of single mRNPs in nuclei of living cells. Science 304(5678):1797-1800. (Pubitemid 38787895)
29. Hirata H, et al. (2002) Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 298(5594):840-843. (Pubitemid 35231539)
30. Swinburne IA, Miguez DG, Landgraf D, Silver PA (2008) Intron length increases oscillatory periods of gene expression in animal cells. Genes Dev 22(17):2342-2346.
31. Takashima Y, Ohtsuka T, González A, Miyachi H, Kageyama R (2011) Intronic delay is essential for oscillatory expression in the segmentation clock. Proc Natl Acad Sci USA 108(8):3300-3305.
32. Chao LC, Jamil A, Kim SJ, Huang L, Martinson HG (1999) Assembly of the cleavage and polyadenylation apparatus requires about 10 seconds in vivo and is faster for strong than for weak poly(A) sites. Mol Cell Biol 19(8):5588-5600. (Pubitemid 29339916)
33. Salditt-Georgieff M, Harpold M, Sawicki S, Nevins J, Darnell JE, Jr. (1980) Addition of poly(A) to nuclear RNA occurs soon after RNA synthesis. J Cell Biol 86(3):844-848.
34. Morales AV, Yasuda Y, Ish-Horowicz D (2002) Periodic Lunatic fringe expression is controlled during segmentation by a cyclic transcriptional enhancer responsive to notch signaling. Dev Cell 3(1):63-74. (Pubitemid 34778396)
35. Rabani M, et al. (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotechnol 29(5):436-442.
36. Lei H, Dias AP, Reed R (2011) Export and stability of naturally intronless mRNAs require specific coding region sequences and the TREX mRNA export complex. Proc Natl Acad Sci USA 108(44):17985-17990.
37. Rodríguez-Navarro S, Hurt E (2011) Linking gene regulation to mRNA production and export. Curr Opin Cell Biol 23(3):302-309.
38. Wright D, et al. (2009) Cyclic Nrarp mRNA expression is regulated by the somitic oscillator but Nrarp protein levels do not oscillate. Dev Dyn 238(12):3043-3055.
39. Tam PP (1981) The control of somitogenesis in mouse embryos. J Embryol Exp Morphol 65(Suppl):103-128.
40. William DA, et al. (2007) Identification of oscillatory genes in somitogenesis from functional genomic analysis of a human mesenchymal stem cell model. Dev Biol 305(1):172-186. (Pubitemid 46589415)
41. Forsberg H, Crozet F, Brown NA (1998) Waves of mouse Lunatic fringe expression, in four-hour cycles at two-hour intervals, precede somite boundary formation. Curr Biol 8(18):1027-1030. (Pubitemid 28448076)
42. McGrew MJ, Dale JK, Fraboulet S, Pourquié O (1998) The lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos. Curr Biol 8(17):979-982. (Pubitemid 28447950)
43. Bhatt DM, et al. (2012) Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 150(2):279-290.
44. Stauber M, Laclef C, Vezzaro A, Page ME, Ish-Horowicz D (2012) Modifying transcript lengths of cycling mouse segmentation genes. Mech Dev 129(1-4):61-72.
45. Harima Y, Takashima Y, Ueda Y, Ohtsuka T, Kageyama R (2013) Accelerating the tempo of the segmentation clock by reducing the number of introns in the Hes7 gene. Cell Rep 3(1):1-7.
46. Audibert A, Weil D, Dautry F (2002) In vivo kinetics of mRNA splicing and transport in mammalian cells. Mol Cell Biol 22(19):6706-6718.
47. Pandya-Jones A, Black DL (2009) Co-transcriptional splicing of constitutive and alternative exons. RNA 15(10):1896-1908.
48. Grünwald D, Singer RH (2010) In vivo imaging of labelled endogenous β-actin mRNA during nucleocytoplasmic transport. Nature 467(7315):604-607.
49. Mor A, et al. (2010) Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat Cell Biol 12(6):543-552.
50. Siebrasse JP, Kaminski T, Kubitscheck U (2012) Nuclear export of single native mRNA molecules observed by light sheet fluorescence microscopy. Proc Natl Acad Sci USA 109(24):9426-9431.
51. Hirata H, et al. (2004) Instability of Hes7 protein is crucial for the somite segmentation clock. Nat Genet 36(7):750-754. (Pubitemid 38886638)
52. Moore MJ, Proudfoot NJ (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136(4):688-700.
53. Bass J (2012) Circadian topology of metabolism. Nature 491(7424):348-356.
54. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG (2005) Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33(4):e36.
55. Henrique D, et al. (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 375(6534):787-790.