Molecular mechanism for cyclic generation of somites: Lessons from mice and zebrafish

Development Growth and Differentiation

Volumn 58, Issue 1, 2016, Pages 31-42

  Yabe, Taijiro ^a,b   Takada, Shinji ^a,b  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

Mesp; Mouse; Segmentation clock; Somitogenesis; Zebrafish

Indexed keywords

ADULT; ANIMAL EXPERIMENT; CHICK; DISEASE MODEL; EMBRYO DEVELOPMENT; FEMALE; GENETIC ANALYSIS; MESODERM; MODEL; MORPHOGENESIS; MOUSE; MUSCLE; NONHUMAN; PRECURSOR; SOMITE; VERTEBRA; ZEBRA FISH; ANIMAL; EMBRYOLOGY; MAMMALIAN EMBRYO; NONMAMMALIAN EMBRYO; PHYSIOLOGY;

ANIMALS; EMBRYO, MAMMALIAN; EMBRYO, NONMAMMALIAN; MICE; MORPHOGENESIS; SOMITES; ZEBRAFISH;

EID: 84955601247     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12249     Document Type: Review

References (87)

1. Akiyama, R., Masuda, M., Tsuge, S., Bessho, Y. & Matsui, T. 2014. An anterior limit of FGF/Erk signal activity marks the earliest future somite boundary in zebrafish. Development 141, 1104-1109.
2. Aulehla, A., Wehrle, C., Brand-Saberi, B., Kemler, R., Gossler, A., Kanzler, B. & Herrmann, B. G. 2003. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev. Cell 4, 395-406.
3. Aulehla, A., Wiegraebe, W., Baubet, V., Wahl, M. B., Deng, C., Taketo, M., Lewandoski, M. & Pourquié, O. 2008. A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat. Cell Biol. 10, 186-193.
4. Bajard, L., Morelli, L. G., Ares, S., Pécréaux, J., Jülicher, F. & Oates, A. C. 2014. Wnt-regulated dynamics of positional information in zebrafish somitogenesis. Development 141, 1381-1391.
5. Barrantes, I. B., Elia, A. J., Wünsch, K., Hrabe de Angelis, M. H., Mak, T. W., Rossant, J., Conlon, R. A., Gossler, A. & de la Pompa, J. L. 1999. Interaction between Notch signalling and Lunatic fringe during somite boundary formation in the mouse. Curr. Biol. 9, 470-480.
6. Barrios, A., Poole, R. J., Durbin, L., Brennan, C., Holder, N. & Wilson, S. W. 2003. Eph/Ephrin signaling regulates the mesenchymal-to-epithelial transition of the paraxial mesoderm during somite morphogenesis. Curr. Biol. 13, 1571-1582.
7. Bénazéraf, B. & Pourquié, O. 2013. Formation and segmentation of the vertebrate body axis. Annu. Rev. Cell Dev. Biol. 29, 1-26.
8. Bessho, Y., Miyoshi, G., Sakata, R. & Kageyama, R. 2001a. Hes7: a bHLH-type repressor gene regulated by Notch and expressed in the presomitic mesoderm. Genes Cells 6, 175-185.
9. Bessho, Y., Sakata, R., Komatsu, S., Shiota, K., Yamada, S. & Kageyama, R. 2001b. Dynamic expression and essential functions of Hes7 in somite segmentation. Genes Dev. 15, 2642-2647.
10. Bone, R. A., Bailey, C. S., Wiedermann, G., Ferjentsik, Z., Appleton, P. L., Murray, P. J., Maroto, M. & Dale, J. K. 2014. Spatiotemporal oscillations of Notch1, Dll1 and NICD are coordinated across the mouse PSM. Development 141, 4806-4816.
11. Chan, T., Kondow, A., Hosoya, A., Hitachi, K., Yukita, A., Okabayashi, K., Nakamura, H., Ozawa, H., Kiyonari, H., Michiue, T., Ito, Y. & Asashima, M. 2007. Ripply2 is essential for precise somite formation during mouse early development. FEBS Lett. 581, 2691-2696.
12. Chen, J., Kang, L. & Zhang, N. 2005. Negative feedback loop formed by Lunatic fringe and Hes7 controls their oscillatory expression during somitogenesis. Genesis 43, 196-204.
13. Cooke, J. & Zeeman, E. C. 1976. A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J. Theor. Biol. 58, 455-476.
14. Cutty, S. J., Fior, R., Henriques, P. M., Saúde, L. & Wardle, F. C. 2012. Identification and expression analysis of two novel members of the Mesp family in zebrafish. Int. J. Dev. Biol. 56, 285-294.
15. Dale, J. K., Maroto, M., Dequeant, M. L., Malapert, P., Mcgrew, M. & Pourquie, O. 2003. Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421, 275-278.
16. Delaune, E. A., François, P., Shih, N. P. & Amacher, S. L. 2012. Single-cell-resolution imaging of the impact of Notch signaling and mitosis on segmentation clock dynamics. Dev. Cell 23, 995-1005.
17. 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.
18. Dubrulle, J., Mcgrew, M. J. & Pourquié, O. 2001. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106, 219-232.
19. Dunty, W. C., Biris, K. K., Chalamalasetty, R. B., Taketo, M. M., Lewandoski, M. & Yamaguchi, T. P. 2008. Wnt3a/beta-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 135, 85-94.
20. Durbin, L., Sordino, P., Barrios, A., Gering, M., Thisse, C., Thisse, B., Brennan, C., Green, A., Wilson, S. & Holder, N. 2000. Anteroposterior patterning is required within segments for somite boundary formation in developing zebrafish. Development 127, 1703-1713.
21. Gajewski, M., Sieger, D., Alt, B., Leve, C., Hans, S., Wolff, C., Rohr, K. B. & Tautz, D. 2003. Anterior and posterior waves of cyclic her1 gene expression are differentially regulated in the presomitic mesoderm of zebrafish. Development 130, 4269-4278.
22. Giudicelli, F., Ozbudak, E. M., Wright, G. J. & Lewis, J. 2007. Setting the tempo in development: an investigation of the zebrafish somite clock mechanism. PLoS Biol. 5, e150.
23. 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, 1-7.
24. Henry, C. A., Urban, M. K., Dill, K. K., Merlie, J. P., Page, M. F., Kimmel, C. B. & Amacher, S. L. 2002. Two linked hairy/Enhancer of split-related zebrafish genes, her1 and her7, function together to refine alternating somite boundaries. Development 129, 3693-3704.
25. 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.
26. Hirata, H., Bessho, Y., Kokubu, H., Masamizu, Y., Yamada, S., Lewis, J. & Kageyama, R. 2004. Instability of Hes7 protein is crucial for the somite segmentation clock. Nat. Genet. 36, 750-754.
27. Holley, S. A., Jülich, D., Rauch, G. J., Geisler, R. & Nüsslein-Volhard, C. 2002. her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development 129, 1175-1183.
28. Hollway, G. E., Bryson-Richardson, R. J., Berger, S., Cole, N. J., Hall, T. E. & Currie, P. D. 2007. Whole-somite rotation generates muscle progenitor cell compartments in the developing zebrafish embryo. Dev. Cell, 12, 207-219.
29. Horikawa, K., Ishimatsu, K., Yoshimoto, E., Kondo, S. & Takeda, H. 2006. Noise-resistant and synchronized oscillation of the segmentation clock. Nature 441, 719-723.
30. Hubaud, A. & Pourquié, O. 2014. Signalling dynamics in vertebrate segmentation. Nat. Rev. Mol. Cell Biol. 15, 709-721.
31. Jiang, Y. J., Aerne, B. L., Smithers, L., Haddon, C., Ish-Horowicz, D. & Lewis, J. 2000. Notch signalling and the synchronization of the somite segmentation clock. Nature 408, 475-479.
32. Jülich, D., Geisler, R., Holley, S.A. & Consortium, T.S. 2005a. Integrinalpha5 and delta/notch signaling have complementary spatiotemporal requirements during zebrafish somitogenesis. Dev. Cell 8, 575-586.
33. Jülich, D., Hwee Lim, C., Round, J., Nicolaije, C., Schroeder, J., Davies, A., Geisler, R., Lewis, J., Jiang, Y. J., Holley, S. A. & Tübingen 2000 Screen Consortium 2005b. beamter/deltaC and the role of Notch ligands in the zebrafish somite segmentation, hindbrain neurogenesis and hypochord differentiation. Dev. Biol. 286, 391-404.
34. Jülich, D., Mould, A. P., Koper, E. & Holley, S. A. 2009. Control of extracellular matrix assembly along tissue boundaries via Integrin and Eph/Ephrin signaling. Development 136, 2913-2921.
35. Jülich, D., Cobb, G., Melo, A. M., McMillen, P., Lawton, A. K., Mochrie, S. G., Rhoades, E. & Holley, S. A. 2015. Cross-Scale Integrin Regulation Organizes ECM and Tissue Topology. Dev. Cell 34, 33-44.
36. Kawamura, A., Koshida, S., Hijikata, H., Ohbayashi, A., Kondoh, H. & Takada, S. 2005a. Groucho-associated transcriptional repressor ripply1 is required for proper transition from the presomitic mesoderm to somites. Dev. Cell 9, 735-744.
37. Kawamura, A., Koshida, S., Hijikata, H., Sakaguchi, T., Kondoh, H. & Takada, S. 2005b. Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites. Genes Dev. 19, 1156-1161.
38. Kawamura, A., Koshida, S. & Takada, S. 2008. Activator-to-repressor conversion of T-box transcription factors by the Ripply family of Groucho/TLE-associated mediators. Mol. Cell. Biol. 28, 3236-3244.
39. Kim, S. H., Jen, W. C., De Robertis, E. M. & Kintner, C. 2000. The protocadherin PAPC establishes segmental boundaries during somitogenesis in xenopus embryos. Curr. Biol. 10, 821-830.
40. Koshida, S., Kishimoto, Y., Ustumi, H., Shimizu, T., Furutani-Seiki, M., Kondoh, H. & Takada, S. 2005. Integrinalpha5-dependent fibronectin accumulation for maintenance of somite boundaries in zebrafish embryos. Dev. Cell 8, 587-598.
41. Krebs, L. T., Bradley, C. K., Norton, C. R., Xu, J., Oram, K. F., Starling, C., Deftos, M. L., Bevan, M. J. & Gridley, T. 2012. The Notch-regulated ankyrin repeat protein is required for proper anterior-posterior somite patterning in mice. Genesis 50, 366-374.
42. Krol, A. J., Roellig, D., Dequéant, M. L., Tassy, O., Glynn, E., Hattem, G., Mushegian, A., Oates, A. C. & Pourquié, O. 2011. Evolutionary plasticity of segmentation clock networks. Development 138, 2783-2792.
43. Mara, A., Schroeder, J., Chalouni, C. & Holley, S. A. 2007. Priming, initiation and synchronization of the segmentation clock by deltaD and deltaC. Nat. Cell Biol. 9, 523-530.
44. 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. Proc. Natl Acad. Sci. USA 103, 1313-1318.
45. Morimoto, M., Takahashi, Y., Endo, M. & Saga, Y. 2005. The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity. Nature 435, 354-359.
46. Morimoto, M., Sasaki, N., Oginuma, M., Kiso, M., Igarashi, K., Aizaki, K., Kanno, J. & Saga, Y. 2007. The negative regulation of Mesp2 by mouse Ripply2 is required to establish the rostro-caudal patterning within a somite. Development 134, 1561-1569.
47. Naiche, L. A., Holder, N. & Lewandoski, M. 2011. FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis. Proc. Natl Acad. Sci. USA 108, 4018-4023.
48. Nakajima, Y., Morimoto, M., Takahashi, Y., Koseki, H. & Saga, Y. 2006. Identification of Epha4 enhancer required for segmental expression and the regulation by Mesp2. Development 133, 2517-2525.
49. Nikaido, M., Kawakami, A., Sawada, A., Furutani-Seiki, M., Takeda, H. & Araki, K. 2002. Tbx24, encoding a T-box protein, is mutated in the zebrafish somite-segmentation mutant fused somites. Nat. Genet. 31, 195-199.
50. Niwa, Y., Masamizu, Y., Liu, T., Nakayama, R., Deng, C. X. & Kageyama, R. 2007. The initiation and propagation of Hes7 oscillation are cooperatively regulated by Fgf and notch signaling in the somite segmentation clock. Dev. Cell 13, 298-304.
51. Niwa, Y., Shimojo, H., Isomura, A., González, A., Miyachi, H. & Kageyama, R. 2011. Different types of oscillations in Notch and Fgf signaling regulate the spatiotemporal periodicity of somitogenesis. Genes Dev. 25, 1115-1120.
52. Nomura-Kitabayashi, A., Takahashi, Y., Kitajima, S., Inoue, T., Takeda, H. & Saga, Y. 2002. Hypomorphic Mesp allele distinguishes establishment of rostrocaudal polarity and segment border formation in somitogenesis. Development 129, 2473-2481.
53. Oates, A. C. & Ho, R. K. 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.
54. Oates, A. C., Morelli, L. G. & Ares, S. 2012. Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development 139, 625-639.
55. Oginuma, M., Niwa, Y., Chapman, D. L. & Saga, Y. 2008. Mesp2 and Tbx6 cooperatively create periodic patterns coupled with the clock machinery during mouse somitogenesis. Development 135, 2555-2562.
56. Oginuma, M., Takahashi, Y., Kitajima, S., Kiso, M., Kanno, J., Kimura, A. & Saga, Y. 2010. The oscillation of Notch activation, but not its boundary, is required for somite border formation and rostral-caudal patterning within a somite. Development 137, 1515-1522.
57. Okubo, Y., Sugawara, T., Abe-Koduka, N., Kanno, J., Kimura, A. & Saga, Y. 2012. Lfng regulates the synchronized oscillation of the mouse segmentation clock via trans-repression of Notch signalling. Nat. Commun. 3, 1141.
58. Ozbudak, E. M. & Lewis, J. 2008. Notch signalling synchronizes the zebrafish segmentation clock but is not needed to create somite boundaries. PLoS Genet. 4, e15.
59. 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, 639-648.
60. Prince, V. E., Holley, S. A., Bally-Cuif, L., Prabhakaran, B., Oates, A. C., Ho, R. K. & Vogt, T. F. 2001. Zebrafish lunatic fringe demarcates segmental boundaries. Mech. Dev. 105, 175-180.
61. Rhee, J., Takahashi, Y., Saga, Y., Wilson-Rawls, J. & Rawls, A. 2003. The protocadherin papc is involved in the organization of the epithelium along the segmental border during mouse somitogenesis. Dev. Biol. 254, 248-261.
62. Riedel-Kruse, I. H., Müller, C. & Oates, A. C. 2007. Synchrony dynamics during initiation, failure, and rescue of the segmentation clock. Science 317, 1911-1915.
63. Saga, Y. 2012a. The mechanism of somite formation in mice. Curr. Opin. Genet. Dev. 22, 331-338.
64. Saga, Y. 2012b. The synchrony and cyclicity of developmental events. Cold Spring Harb. Perspect. Biol. 4, a008201.
65. Saga, Y., Hata, N., Koseki, H. & Taketo, M. M. 1997. Mesp2: a novel mouse gene expressed in the presegmented mesoderm and essential for segmentation initiation. Genes Dev. 11, 1827-1839.
66. Sasaki, N., Kiso, M., Kitagawa, M. & Saga, Y. 2011. The repression of Notch signaling occurs via the destabilization of mastermind-like 1 by Mesp2 and is essential for somitogenesis. Development 138, 55-64.
67. Sawada, A., Fritz, A., Jiang, Y. J., Yamamoto, A., Yamasu, K., Kuroiwa, A., Saga, Y. & Takeda, H. 2000. Zebrafish Mesp family genes, mesp-a and mesp-b are segmentally expressed in the presomitic mesoderm, and Mesp-b confers the anterior identity to the developing somites. Development 127, 1691-1702.
68. Sawada, A., Shinya, M., Jiang, Y. J., Kawakami, A., Kuroiwa, A. & Takeda, H. 2001. Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. Development 128, 4873-4880.
69. Schröter, C. & Oates, A. C. 2010. Segment number and axial identity in a segmentation clock period mutant. Curr. Biol. 20, 1254-1258.
70. Schröter, C., Ares, S., Morelli, L. G., Isakova, A., Hens, K., Soroldoni, D., Gajewski, M., Jülicher, F., Maerkl, S. J., Deplancke, B. & Oates, A. C. 2012. Topology and dynamics of the zebrafish segmentation clock core circuit. PLoS Biol. 10, e1001364.
71. Shih, N. P., François, P., Delaune, E. A. & Amacher, S. L. 2015. Dynamics of the slowing segmentation clock reveal alternating two-segment periodicity. Development 142, 1785-1793.
72. Stellabotte, F. & Devoto, S. H. 2007. The teleost dermomyotome. Dev. Dyn. 236, 2432-2443.
73. Stellabotte, F., Dobbs-Mcauliffe, B., Fernández, D. A., Feng, X. & Devoto, S. H. 2007. Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development 134, 1253-1257.
74. Takahashi, Y., Koizumi, K., Takagi, A., Kitajima, S., Inoue, T., Koseki, H. & Saga, Y. 2000. Mesp2 initiates somite segmentation through the Notch signalling pathway. Nat. Genet. 25, 390-396.
75. Takahashi, Y., Inoue, T., Gossler, A. & Saga, Y. 2003. Feedback loops comprising Dll1, Dll3 and Mesp2, and differential involvement of Psen1 are essential for rostrocaudal patterning of somites. Development 130, 4259-4268.
76. Takahashi, J., Ohbayashi, A., Oginuma, M., Saito, D., Mochizuki, A. & Saga, Y. 2010. Analysis of Ripply1/2-deficient mouse embryos reveals a mechanism underlying the rostro-caudal patterning within a somite. Dev. Biol. 342, 134-145.
77. Topczewska, J. M., Topczewski, J., Szostak, A., Solnica-Krezel, L. & Hogan, B. L. 2003. Developmentally regulated expression of two members of the Nrarp family in zebrafish. Gene Expr. Patterns 3, 169-171.
78. Trofka, A., Schwendinger-Schreck, J., Brend, T., Pontius, W., Emonet, T. & Holley, S. A. 2012. The Her7 node modulates the network topology of the zebrafish segmentation clock via sequestration of the Hes6 hub. Development 139, 940-947.
79. Van Eeden, F. J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A., Kelsh, R. N., Mullins, M. C., Odenthal, J., Warga, R. M., Allende, M. L., Weinberg, E. S. & Nüsslein-Volhard, C. 1996. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123, 153-164.
80. Wahl, M. B., Deng, C., Lewandoski, M. & Pourquié, O. 2007. FGF signaling acts upstream of the NOTCH and WNT signaling pathways to control segmentation clock oscillations in mouse somitogenesis. Development 134, 4033-4041.
81. Wanglar, C., Takahashi, J., Yabe, T. & Takada, S. 2014. Tbx protein level critical for clock-mediated somite positioning is regulated through interaction between Tbx and Ripply. PLoS ONE 9, e107928.
82. Watanabe, T., Sato, Y., Saito, D., Tadokoro, R. & Takahashi, Y. 2009. EphrinB2 coordinates the formation of a morphological boundary and cell epithelialization during somite segmentation. Proc. Natl Acad. Sci. USA 106, 7467-7472.
83. Windner, S. E., Doris, R. A., Ferguson, C. M., Nelson, A. C., Valentin, G., Tan, H., Oates, A. C., Wardle, F. C. & Devoto, S. H. 2015. Tbx6, Mesp-b and Ripply1 regulate the onset of skeletal myogenesis in zebrafish. Development 142, 1159-1168.
84. Yamamoto, A., Kemp, C., Bachiller, D., Geissert, D. & De Robertis, E. M. 2000. Mouse paraxial protocadherin is expressed in trunk mesoderm and is not essential for mouse development. Genesis 27, 49-57.
85. Yasuhiko, Y., Haraguchi, S., Kitajima, S., Takahashi, Y., Kanno, J. & Saga, Y. 2006. Tbx6-mediated Notch signaling controls somite-specific Mesp2 expression. Proc. Natl Acad. Sci. USA 103, 3651-3656.
86. Yasuhiko, Y., Kitajima, S., Takahashi, Y., Oginuma, M., Kagiwada, H., Kanno, J. & Saga, Y. 2008. Functional importance of evolutionally conserved Tbx6 binding sites in the presomitic mesoderm-specific enhancer of Mesp2. Development 135, 3511-3519.
87. Zhao, W., Ajima, R., Ninomiya, Y. & Saga, Y. 2015. Segmental border is defined by Ripply2-mediated Tbx6 repression independent of Mesp2. Dev. Biol. 400, 105-117.