Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Webb, Alexis B ^a,b,f   Lengyel, Iván M ^c   Jörg, David J ^d   Valentin, Guillaume ^a,b,g   Jülicher, Frank ^d   Morelli, Luis G ^c   Oates, Andrew C ^a,b,e,f  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^d MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^g GenOway   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CIRCADIAN RHYTHM; EMBRYO SEGMENTATION; GENE EXPRESSION ASSAY; IMMUNOCYTOCHEMISTRY; NONHUMAN; OSCILLATION; ZEBRA FISH; ANIMAL; BIOLOGICAL RHYTHM; BIOSYNTHESIS; CELL CULTURE; CELL FUNCTION; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENE FUSION; PHYSIOLOGY; REPORTER GENE; TRANSGENIC ANIMAL;

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HER1 PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARTIFICIAL GENE FUSION; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOLOGICAL CLOCKS; CELL PHYSIOLOGICAL PHENOMENA; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENES, REPORTER; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84961967589     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08438     Document Type: Article

References (68)

1. Albeck JG, Mills GB, Brugge JS. 2013. Frequency-modulated pulses of ERK activity transmit quantitative proliferation signals. Molecular Cell 49:249-261. doi: 10.1016/j.molcel.2012.11.002
2. Aoki K, Kumagai Y, Sakurai A, Komatsu N, Fujita Y, Shionyu C, Matsuda M. 2013. Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density-dependent proliferation. Molecular Cell 52: 529-540. doi: 10.1016/j.molcel.2013.09.015
3. Ay a, Holland J, Sperlea a, Devakanmalai GS, Knierer S, Sangervasi S, Stevenson a, Ozbudak EM. 2014. Spatial gradients of protein-level time delays set the pace of the traveling segmentation clock waves. Development 141:4158-4167. doi: 10.1242/dev.111930
4. Barral J, Dierkes K, Lindner B, Julicher F, Martin P. 2010. Coupling a sensory hair-cell bundle to cyber clones enhances nonlinear amplification. Proceedings of the National Academy of Sciences of the United States of America 107:8079-8084. doi: 10.1073/pnas.0913657107
5. Chang HH, Hemberg M, Barahona M, Ingber DE, Huang S. 2008. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453:544-547. doi: 10.1038/nature06965
6. Cooke J, Zeeman EC. 1976. A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. Journal of Theoretical Biology 58:455-476.
7. Danino T, Mondragón-Palomino O, Tsimring L, Hasty J. 2010. A synchronized quorum of genetic clocks. Nature 463:326-330. doi: 10.1038/nature08753
8. 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. Developmental Cell 23:995-1005. doi: 10.1016/j.devcel.2012.09.009
9. Dequéant M-L, Glynn E, Gaudenz K, Wahl M, Chen J, Mushegian A, Pourquié O. 2006. A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314:1595-1598. doi: 10.1126/science.1133141
10. Diz-Muñoz A, Krieg M, Bergert M, Ibarlucea-Benitez I, Muller DJ, Paluch E, Heisenberg C-P. 2010. Control of directed cell migration in vivo by membrane-to-cortex attachment. PLoS Biology 8:e1000544. doi: 10.1371/journal.pbio.1000544
11. Dubrulle J, McGrew MJ, Pourquié O. 2001. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal hox gene activation. Cell 106:219-232. doi: 10.1016/S0092-8674(01)00437-8
12. Garcia-Ojalvo J, Elowitz MB, Strogatz SH. 2004. Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing. Proceedings of the National Academy of Sciences of the United States of America 101: 10955-10960. doi: 10.1073/pnas.0307095101
13. Giudicelli F, Ozbudak EM, Wright GJ, Lewis J. 2007. Setting the tempo in development: an investigation of the zebrafish somite clock mechanism. PLoS Biology 5:e150. doi: 10.1371/journal.pbio.0050150
14. Goldbeter A, Pourquié O. 2008. Modeling the segmentation clock as a network of coupled oscillations in the notch, wnt and FGF signaling pathways. Journal of Theoretical Biology 252:574-585. doi: 10.1016/j.jtbi.2008.01.006
15. Gonze D, Bernard S, Waltermann C, Kramer A, Herzel H. 2005. Spontaneous synchronization of coupled circadian oscillators. Biophysical Journal 89:120-129. doi: 10.1529/biophysj.104.058388
16. Gregor T, Fujimoto K, Masaki N, Sawai S. 2010. The onset of collective behavior in social amoebae. Science 328: 1021-1025. doi: 10.1126/science.1183415
17. Herrgen L, Ares S, Morelli LG, Schroter C, Julicher F, Oates AC. 2010. Intercellular coupling regulates the period of the segmentation clock. Current Biology 20:1244-1253. doi: 10.1016/j.cub.2010.06.034
18. Herzog ED, Aton SJ, Numano R, Sakaki Y, Tei H. 2004. Temporal precision in the mammalian circadian system: a reliable clock from less reliable neurons. Journal of Biological Rhythms 19:35-46. doi: 10.1177/0748730403260776
19. Hirata H, Yoshiura S, Ohtsuka T, Bessho Y, Harada T, Yoshikawa K, Kageyama R. 2002. Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 298:840-843. doi: 10.1126/science.1074560
20. 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 & Development 14:1678-1690.
21. Holley SA, Julich D, Rauch G-J, Geisler R, Nusslein-Volhard C. 2002. Her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development 129:1175-1183.
22. Horikawa K, Ishimatsu K, Yoshimoto E, Kondo S, Takeda H. 2006. Noise-resistant and synchronized oscillation of the segmentation clock. Nature 441:719-723. doi: 10.1038/nature04861
23. Huang S. 2009. Non-genetic heterogeneity of cells in development: more than just noise. Development 136: 3853-3862. doi: 10.1242/dev.035139
24. Huang H, Lindgren A, Wu X, Liu N-A, Lin S. 2012. High-throughput screening for bioactive molecules using primary cell culture of transgenic zebrafish embryos. Cell Reports 2:695-704. doi: 10.1016/j.celrep.2012.08.015
25. Imayoshi I, Isomura A, Harima Y, Kawaguchi K, Kori H, Miyachi H, Fujiwara T, Ishidate F, Kageyama R. 2013. Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342: 1203-1208. doi: 10.1126/science.1242366
26. Ishimatsu K, Takamatsu A, Takeda H. 2010. Emergence of traveling waves in the zebrafish segmentation clock. Development 137:1595-1599. doi: 10.1242/dev.046888
27. Jiang YJ, Aerne BL, Smithers L, Haddon C, Ish-Horowicz D, Lewis J. 2000. Notch signalling and the synchronization of the somite segmentation clock. Nature 408:475-479. doi: 10.1038/35044091
28. Krol AJ, Roellig D, Dequéant M-L, Tassy O, Glynn E, Hattem G, Mushegian A, Oates AC, Pourquié O. 2011. Evolutionary plasticity of segmentation clock networks. Development 138:2783-2792. doi: 10.1242/dev.063834
29. Langenberg T, Brand M, Cooper MS. 2003. Imaging brain development and organogenesis in zebrafish using immobilized embryonic explants. Developmental Dynamics 228:464-474. doi: 10.1002/dvdy.10395
30. Lauschke VM, Tsiairis CD, François P, Aulehla A. 2012. Scaling of embryonic patterning based on phase-gradient encoding. Nature 493:101-105. doi: 10.1038/nature11804
31. Leise TL, Wang CW, Gitis PJ, Welsh DK. 2012. Persistent cell-autonomous circadian oscillations in fibroblasts revealed by six-week single-cell imaging of PER2::LUC bioluminescence. PloS One 7:e33334-e33334. doi: 10.1371/journal.pone.0033334
32. Lewis J. 2003. Autoinhibition with transcriptional delay. Current Biology 13:1398-1408. doi: 10.1016/S0960-9822(03)00534-7
33. Maroto M, Dale JK, Dequéant M-L, Petit A-C, Pourquié O. 2005. Synchronised cycling gene oscillations in presomitic mesoderm cells require cell-cell contact. The International Journal of Developmental Biology 49: 309-315. doi: 10.1387/ijdb.041958mm
34. Martin BL, Kimelman D. 2010. Brachyury establishes the embryonic mesodermal progenitor niche. Genes & Development 24:2778-2783. doi: 10.1101/gad.1962910
35. Martin BL, Kimelman D. 2012. Canonical wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Developmental Cell 22:223-232. doi: 10.1016/j.devcel.2011.11.001
36. Masamizu Y, Ohtsuka T, Takashima Y, Nagahara H, Takenaka Y, Yoshikawa K, Okamura H, Kageyama R. 2006. Real-time imaging of the somite segmentation clock: revelation of unstable oscillators in the individual presomitic mesoderm cells. Proceedings of the National Academy of Sciences of the United States of America 103:1313-1318. doi: 10.1073/pnas.0508658103
37. Matsuda M, Koga M, Woltjen K, Nishida E, Ebisuya M. 2015. Synthetic lateral inhibition governs cell-type bifurcation with robust ratios. Nature Communications 6:6195. doi: 10.1038/ncomms7195
38. Maître J-L, Berthoumieux H, Krens SFG, Salbreux G, Julicher F, Paluch E, Heisenberg C-P. 2012. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338:253-256. doi: 10.1126/science.1225399
39. Meinhardt H. 1986. Hierarchical inductions of cell states: a model for segmentation in drosophila. Journal of Cell Science 1986:357-381. doi: 10.1242/jcs.1986.Supplement_4.20
40. Meinhardt HH, Gierer AA. 2000. Pattern formation by local self-activation and lateral inhibition. BioEssays 22: 753-760. doi: 10.1002/1521-1878(200008)22:8<753::AID-BIES9>3.0.CO;2-Z
41. Monk NAM. 2003. Oscillatory expression of Hes1, p53, and NF-kB driven by transcriptional time delays. Current Biology 13:1409-1413. doi: 10.1016/S0960-9822(03)00494-9
42. Morelli L, Julicher F. 2007. Precision of genetic oscillators and clocks. Physical Review Letters 98:1-4. doi: 10.1103/PhysRevLett.98.228101
43. Morelli LG, Ares S, Herrgen L, Schroter C, Julicher F, Oates AC. 2009. Delayed coupling theory of vertebrate segmentation. HFSP Journal 3:55-66. doi: 10.2976/1.3027088
44. Niwa Y, Masamizu Y, Liu T, Nakayama R, Deng CX, Kageyama R. 2007. The initiation and propagation of Hes7 oscillation are cooperatively regulated by fgf and notch signaling in the somite segmentation clock. Developmental Cell 13:298-304. doi: 10.1016/j.devcel.2007.07.013
45. 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 129:2929-2946.
46. Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O. 1997. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639-648. doi: 10.1016/S0092-8674(00)80451-1
47. Palmeirim I, Dubrulle J, Henrique D, Ish-Horowicz D, Pourquié O. 1998. Uncoupling segmentation and somitogenesis in the chick presomitic mesoderm. Developmental Genetics 23:77-85. doi: 10.1002/(SICI)1520- 6408(1998)23:1<77::AID-DVG8>3.0.CO;2-3
48. Riedel-Kruse IH, Muller C, Oates AC. 2007. Synchrony dynamics during initiation, failure, and rescue of the segmentation clock. Science 317:1911-1915. doi: 10.1126/science.1142538
49. Ruprecht V, Wieser S, Callan-Jones A, Smutny M, Morita H, Sako K, Barone V, Ritsch-Marte M, Sixt M, Voituriez R, Heisenberg C-P. 2015. Cortical contractility triggers a stochastic switch to fast amoeboid cell motility. Cell 160:673-685. doi: 10.1016/j.cell.2015.01.008
50. Sawada A, Shinya M, Jiang YJ, Kawakami A, Kuroiwa A, Takeda H. 2001. Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. Development 128:4873-4880.
51. Schroter C, Herrgen L, Cardona A, Brouhard GJ, Feldman B, Oates AC. 2008. Dynamics of zebrafish somitogenesis. Developmental Dynamics 237:545-553. doi: 10.1002/dvdy.21458
52. Schroter C, Ares S, Morelli LG, Isakova A, Hens K, Soroldoni D, Gajewski M, Julicher F, Maerkl SJ, Deplancke B, Oates AC. 2012. Topology and dynamics of the zebrafish segmentation clock core circuit. PLoS Biology 10: e1001364. doi: 10.1371/journal.pbio.1001364
53. Shih NP, Francois P, Delaune E, Amacher SL. 2015. Dynamics of the slowing segmentation clock reveal alternating two-segment periodicity. Development 142:1785-1793. doi: 10.1242/dev.119057
54. Sigal A, Milo R, Cohen A, Geva-Zatorsky N, Klein Y, Liron Y, Rosenfeld N, Danon T, Perzov N, Alon U. 2006. Variability and memory of protein levels in human cells. Nature 444:643-646. doi: 10.1038/nature05316
55. Soroldoni D, Jorg DJ, Morelli LG, Richmond DL, Schindelin J, Julicher F, Oates AC. 2014. A doppler effect in embryonic pattern formation. Science 345:222-225. doi: 10.1126/science.1253089
56. Sprinzak D, Lakhanpal A, Lebon L, Santat LA, Fontes ME, Anderson GA, Garcia-Ojalvo J, Elowitz MB. 2010. Cis- interactions between notch and delta generate mutually exclusive signalling states. Nature 465:86-90. doi: 10.1038/nature08959
57. Strogatz SH. 1994. Nonlinear Dynamics and Chaos.
58. Suel GM, Garcia-Ojalvo J, Liberman LM, Elowitz MB. 2006. An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440:545-550. doi: 10.1038/nature04588
59. Trofka A, Schwendinger-Schreck J, Brend T, Pontius W, Emonet T, Holley SA. 2012. The Her7 node modulates the network topology of the zebrafish segmentation clock via sequestration of the Hes6 hub. Development 18. doi: 10.1242/dev.073544
60. Uriu K, Morishita Y, Iwasa Y. 2009. Traveling wave formation in vertebrate segmentation. Journal of Theoretical Biology 257:385-396. doi: 10.1016/j.jtbi.2009.01.003
61. Verdugo A, Rand R. 2008a. Hopf bifurcation in a DDE model of gene expression. Communications in Nonlinear Science and Numerical Simulation 13:235-242. doi: 10.1016/j.cnsns.2006.05.001
62. Verdugo A, Rand R. 2008b. Center manifold analysis of a DDE model of gene expression. Communications in Nonlinear Science and Numerical Simulation 13:1112-1120. doi: 10.1016/j.cnsns.2006.09.011
63. Webb AB, Angelo N, Huettner JE, Herzog ED, Takahashi, Intrinsic JS. 2009. Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proceedings of the National Academy of Sciences of the United States of America 106:16493-16498. doi: 10.1073/pnas.0902768106
64. Webb AB, Soroldoni D, Oswald A, Schindelin J, Oates AC. 2014. Generation of dispersed presomitic mesoderm cell cultures for imaging of the zebrafish segmentation clock in single cells. Journal of Visualized Experiments: 1-8. doi: 10.3791/50307
65. Welsh DK, Logothetis DE, Meister M, Reppert SM. 1995. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697-706. doi: 10.1016/0896-6273(95)90214-7
66. Westerfield M. 2000. The Zebrafish Book. a Guide for the Laboratory Use of Zebrafish (Danio Rerio). 4th edition Eugene: University of Oregon Press.
67. Wu XP, Eshete M. 2011. Bifurcation analysis for a model of gene expression with delays. Communications in Nonlinear Science and Numerical Simulation 16:1073-1088. doi: 10.1016/j.cnsns.2010.05.010
68. Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J, Castiglioni A, Price E, Liu M, Barton ER, Kahn CR, Wagers AJ, Zon LI. 2013. A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155:909-921. doi: 10.1016/j.cell.2013.10.023