Somitogenesis clock-wave initiation requires differential decay and multiple binding sites for clock protein

PLoS Computational Biology

Volumn 6, Issue 4, 2010, Pages

  Campanelli, Mark ^a   Gedeon, Tomáš ^b  

^a SOUTHWEST MINNESOTA STATE UNIVERSITY   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; CELL CULTURE; CELL PROLIFERATION; CLOCKS; DECAY (ORGANIC); DIMERS; TRANSCRIPTION;

CLOCK GENES; CLOCK WAVES; CONTROL MECHANISM; DECAY RATE; DIFFERENTIAL DECAYS; GENES EXPRESSION; MULTIPLE BINDING SITES; PRESOMITIC MESODERM; SOMITOGENESIS; WAVE INITIATION;

PROTEINS;

TRANSCRIPTION FACTOR CLOCK; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA BINDING PROTEIN; HER1 PROTEIN, ZEBRAFISH; HER7 PROTEIN, ZEBRAFISH; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

ANTERIOR POSTERIOR AXIS; ARTICLE; BINDING SITE; CELL HETEROGENEITY; COMPUTER SIMULATION; CONTROLLED STUDY; DIMERIZATION; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENETIC REGULATION; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; SIGNAL TRANSDUCTION; SOMITOGENESIS; ZEBRA FISH; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; REPRODUCIBILITY; SOMITE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CLOCK PROTEINS; DNA-BINDING PROTEINS; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; MODELS, BIOLOGICAL; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; SOMITES; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77954612561     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000728     Document Type: Article

References (56)

1. Dequéant ML, Pourquié O (2008) Segmental patterning of the vertebrate embryonic axis. Nat Rev Genet 9: 370-82.
2. Holley SA (2007) The genetics and embryology of zebrafish metamerism. Dev Dyn 236: 1422-49.
3. Saga Y, Takeda H (2001) The making of the somite: molecular events in vertebrate segmentation. Nat Rev Genet 2: 835-45.
4. Kanki JP, Ho RK (1997) The development of the posterior body in zebrafish. Development 124: 881-93.
5. 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: 455-76.
6. Primmett DR, Norris WE, Carlson GJ, Keynes RJ, Stern CD (1989) Periodic segmental anomalies induced by heat shock in the chick embryo are associated with the cell cycle. Development 105: 119-30.
7. 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: 639-48.
8. Dequéant ML, Glynn E, Gaudenz K, Wahl M, Chen J, et al. (2006) A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314: 1595-8.
9. Dubrulle J, Pourquié O (2004) fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427: 419-22.
10. Goldbeter A, Gonze D, Pourquié O (2007) Sharp developmental thresholds defined through bistability by antagonistic gradients of retinoic acid and FGF signaling. Dev Dyn 236: 1495-508.
11. Aulehla A, Wiegraebe W, Baubet V, Wahl MB, Deng C, et al. (2008) A betacatenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat Cell Biol 10: 186-93.
12. Aulehla A, Herrmann BG (2004) Segmentation in vertebrates: clock and gradient finally joined. Genes Dev 18: 2060-7.
13. Giudicelli F, Lewis J (2004) The vertebrate segmentation clock. Curr Opin Genet Dev 14: 407-14.
14. Baker RE, Schnell S, Maini PK (2008) Mathematical models for somite formation. Curr Top Dev Biol 81: 183-203.
15. Kulesa PM, Schnell S, Rudloff S, Baker RE, Maini PK (2007) From segment to somite: segmentation to epithelialization analyzed within quantitative frameworks. Dev Dyn 236: 1392-402.
16. Baker RE, Schnell S, Maini PK (2003) Formation of vertebral precursors: past models and future predictions. J Theor Med 5: 23-35.
17. Dale KJ, Pourquie O (2000) A clock-work somite. Bioessays 22: 72-83.
18. Baker RE, Schnell S (2009) How can mathematics help us explore vertebrate segmentation? HFSP J 3: 1-5.
19. Lewis J (2003) Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 13: 1398-408.
20. Monk NAM (2003) Oscillatory expression of Hes1, p53, and NF-kappaB driven by transcriptional time delays. Curr Biol 13: 1409-13.
21. Jensen MH, Sneppen K, Tiana G (2003) Sustained oscillations and time delays in gene expression of protein Hes1. FEBS Lett 541: 176-7.
22. Jiang YJ, Aerne BL, Smithers L, Haddon C, Ish-Horowicz D, et al. (2000) Notch signalling and the synchronization of the somite segmentation clock. Nature 408: 475-9.
23. Horikawa K, Ishimatsu K, Yoshimoto E, Kondo S, Takeda H (2006) Noiseresistant and synchronized oscillation of the segmentation clock. Nature 441: 719-23.
24. 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: e150.
25. Özbudak EM, Lewis J (2008) Notch signalling synchronizes the zebrafish segmentation clock but is not needed to create somite boundaries. PLoS Genet 4: e15.
26. Kawamura A, Koshida S, Hijikata H, Sakaguchi T, Kondoh H, et al. (2005) Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites. Genes Dev 19: 1156-61.
27. Sieger D, Ackermann B, Winkler C, Tautz D, Gajewski M (2006) her1 and her13.2 are jointly required for somitic border specification along the entire axis of the fish embryo. Dev Biol 293: 242-51.
28. Cinquin O (2007) Repressor dimerization in the zebrafish somitogenesis clock. PLoS Comput Biol 3: e32.
29. Buchler NE, Gerland U, Hwa T (2005) Nonlinear protein degradation and the function of genetic circuits. Proc Natl Acad Sci U S A 102: 9559-64.
30. Brend T, Holley SA (2009) Expression of the oscillating gene her1 is directly regulated by Hairy/Enhancer of Split, T-box, and Suppressor of Hairless proteins in the zebrafish segmentation clock. Dev Dyn 238: 2745-59.
31. Zeiser S, Liebscher HV, Tiedemann H, Rubio-Aliaga I, Przemeck GKH, et al. (2006) Number of active transcription factor binding sites is essential for the Hes7 oscillator. Theor Biol Med Model 3: 11.
32. Gajewski M, Sieger D, Alt B, Leve C, Hans S, et al. (2003) Anterior and posterior waves of cyclic her1 gene expression are differentially regulated in the presomitic mesoderm of zebrafish. Development 130: 4269-78.
33. Tiedemann HB, Schneltzer E, Zeiser S, Rubio-Aliaga I, Wurst W, et al. (2007) Cell-based simulation of dynamic expression patterns in the presomitic mesoderm. J Theor Biol 248: 120-9.
34. Zeiser S, Rivera O, Kuttler C, Hense B, Lasser R, et al. (2008) Oscillations of Hes7 caused by negative autoregulation and ubiquitination. Comput Biol Chem 32: 47-51.
35. Wong WW, Tsai TY, Liao JC (2007) Single-cell zeroth-order protein degradation enhances the robustness of synthetic oscillator. Mol Syst Biol 3: 130.
36. Henry CA, Urban MK, Dill KK, Merlie JP, Page MF, et al. (2002) Two linked hairy/Enhancer of split-related zebrafish genes, her1 and her7, function together to refine alternating somite boundaries. Development 129: 3693-704.
37. Oates AC, Ho RK (2002) Hairy/E(spl)-related (Her) genes are central components of the segmentation oscillator and display redundancy with the Delta/Notch signaling pathway in the formation of anterior segmental boundaries in the zebrafish. Development 129: 2929-46.
38. Leimeister C, Dale K, Fischer A, Klamt B, de Angelis MH, et al. (2000) Oscillating expression of c-Hey2 in the presomitic mesoderm suggests that the segmentation clock may use combinatorial signaling through multiple interacting bHLH factors. Dev Biol 227: 91-103.
39. Mara A, Schroeder J, Chalouni C, Holley SA (2007) Priming, initiation and synchronization of the segmentation clock by deltaD and deltaC. Nat Cell Biol 9: 523-30.
40. Oates AC, Mueller C, Ho RK (2005) Cooperative function of deltac and her7 in anterior segment formation. Dev Biol 280: 133-49.
41. Muller-Hill B (1996) The lac operon de Gruyter.
42. Ptashne M (2004) A Genetic Switch. Cold Spring Harbor Press.
43. Holley SA, Geisler R, Nusslein-Volhard C (2000) Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity. Genes Dev 14: 1678-90.
44. Sawada A, Shinya M, Jiang YJ, Kawakami A, Kuroiwa A, et al. (2001) Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. Development 128: 4873-80.
45. Shea MA, Ackers GK (1985) The OR control system of bacteriophage lambda. A physical-chemical model for gene regulation. J Mol Biol 181: 211-30.
46. Morelli LG, Ares S, Herrgen L, Schroter C, Julicher F, et al. (2009) Delayed coupling theory of vertebrate segmentation. HFSP J 3: 55-66.
47. Buchler NE, Gerland U, Hwa T (2003) On schemes of combinatorial transcription logic. Proc Natl Acad Sci U S A 100: 5136-41.
48. Santillán M, Mackey MC (2004) Why the lysogenic state of phage lambda is so stable: a mathematical modeling approach. Biophys J 86: 75-84.
49. Golding I, Cox EC (2006) Eukaryotic transcription: what does it mean for a gene to be 'on'? Curr Biol 16: R371-3.
50. Mara A, Holley SA (2007) Oscillators and the emergence of tissue organization during zebrafish somitogenesis. Trends Cell Biol 17: 593-9.
51. Rida PCG, Minh NL, Jiang YJ (2004) A Notch feeling of somite segmentation and beyond. Dev Biol 265: 2-22.
52. Masamizu Y, Ohtsuka T, Takashima Y, Nagahara H, Takenaka 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 U S A 103: 1313-8.
53. Schroter C, Herrgen L, Cardona A, Brouhard GJ, Feldman B, et al. (2008) Dynamics of zebrafish somitogenesis. Dev Dyn 237: 545-53.
54. Baker RE, Maini PK (2007) Travelling gradients in interacting morphogen systems. Math Biosci 209: 30-50.
55. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, et al. (2002) Molecular Biology of the Cell, Garland Science, chapter 7. Fourth edition.
56. Kierzenka J, Shampine LF, Thompson S (2008) dde23 and ddesd. In: MATLAB & Simulink, R2008b. Natick, MA USA: The MathWorks, Inc, Www.mathworks.com.