The many roles of Notch signaling during vertebrate somitogenesis

Seminars in Cell and Developmental Biology

Volumn 49, Issue , 2016, Pages 68-75

  Wahi, Kanu ^a   Bochter, Matthew S ^a   Cole, Susan E ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Notch pathway; Segmentation clock; Somitogenesis

Indexed keywords

NOTCH RECEPTOR;

EMBRYO SEGMENTATION; MESODERM; MOLECULAR CLOCK; MOLECULAR MODEL; NONHUMAN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SOMITE; SOMITOGENESIS; VERTEBRATE; ANIMAL; EMBRYO DEVELOPMENT; EMBRYOLOGY; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; MORPHOGENESIS; PHYSIOLOGY;

ANIMALS; BODY PATTERNING; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; SOMITES;

EID: 84958117778     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.11.010     Document Type: Review

References (108)

1. Christ B., Huang R., Scaal M. Amniote somite derivatives. Dev Dyn 2007, 236:2382-2396.
2. Eckalbar W.L., Fisher R.E., Rawls A., Kusumi K. Scoliosis and segmentation defects of the vertebrae. Wiley Interdiscip Rev Dev Biol 2012, 1:401-423.
3. Turnpenny P.D., Alman B., Cornier A.S., Giampietro P.F., Offiah A., Tassy O., et al. Abnormal vertebral segmentation and the notch signaling pathway in man. Dev Dyn 2007, 236:1456-1474.
4. Pourquie O. Vertebrate segmentation: from cyclic gene networks to scoliosis. Cell 2011, 145:650-663.
5. Gomez C., Pourquie O. Developmental control of segment numbers in vertebrates. J Exp Zool B: Mol Dev Evol 2009, 312:533-544.
6. Christ B., Schmidt C., Huang R., Wilting J., Brand-Saberi B. Segmentation of the vertebrate body. Anat Embryol 1998, 197:1-8.
7. Gossler A., Hrabe de Angelis M. Somitogenesis. Curr Top Dev Biol 1998, 38:225-287.
8. Tam P.P. The control of somitogenesis in mouse embryos. J Embryol Exp Morphol 1981, 65:103-128.
9. Palmeirim I., Henrique D., Ish-Horowicz D., Pourquie O. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 1997, 91:639-648.
10. Schroter C., Herrgen L., Cardona A., Brouhard G.J., Feldman B., Oates A.C. Dynamics of zebrafish somitogenesis. Dev Dyn 2008, 237:545-553.
11. William D.A., Saitta B., Gibson J.D., Traas J., Markov V., Gonzalez D.M., et al. Identification of oscillatory genes in somitogenesis from functional genomic analysis of a human mesenchymal stem cell model. Dev Biol 2007, 305:172-186.
12. Saga Y. The mechanism of somite formation in mice. Curr Opin Genet Dev 2012, 22:331-338.
13. Yusuf F., Brand-Saberi B. The eventful somite: patterning, fate determination and cell division in the somite. Anat Embryol (Berl) 2006, 211(Suppl. 1):21-30.
14. Cooke J. Control of somite number during morphogenesis of a vertebrate Xenopus laevis. Nature 1975, 254:196-199.
15. Cooke J., Zeeman E.C. A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J Theor Biol 1976, 58:455-476.
16. Kusumi K., May C.M., Eckalbar W.L. A large-scale view of the evolution of amniote development: insights from somitogenesis in reptiles. Curr Opin Genet Dev 2013, 23:491-497.
17. Maroto M., Dale J.K., Dequeant M.L., Petit A.C., Pourquie O. Synchronised cycling gene oscillations in presomitic mesoderm cells require cell-cell contact. Int J Dev Biol 2005, 49:309-315.
18. Masamizu Y., Ohtsuka T., Takashima Y., Nagahara H., Takenaka Y., Yoshikawa K., et al. Real-time imaging of the somite segmentation clock: revelation of unstable oscillators in the individual presomitic mesoderm cells. Proc Natl Acad Sci USA 2006, 103:1313-1318.
19. Jiang Y.J., Aerne B.L., Smithers L., Haddon C., Ish-Horowicz D., Lewis J. Notch signalling and the synchronization of the somite segmentation clock. Nature 2000, 408:475-479.
20. Lewis J. Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 2003, 13:1398-1408.
21. Riedel-Kruse I.H., Muller C., Oates A.C. Synchrony dynamics during initiation, failure, and rescue of the segmentation clock. Science 2007, 317:1911-1915.
22. Herrgen L., Ares S., Morelli L.G., Schroter C., Julicher F., Oates A.C. Intercellular coupling regulates the period of the segmentation clock. Curr Biol 2010, 20:1244-1253.
23. Horikawa K., Ishimatsu K., Yoshimoto E., Kondo S., Takeda H. Noise-resistant and synchronized oscillation of the segmentation clock. Nature 2006, 441:719-723.
24. Hori K., Sen A., Artavanis-Tsakonas S. Notch signaling at a glance. J Cell Sci 2013, 126:2135-2140.
25. Guruharsha K.G., Kankel M.W., Artavanis-Tsakonas S. The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat Rev Genet 2012, 13:654-666.
26. Penton A.L., Leonard L.D., Spinner N.B. Notch signaling in human development and disease. Semin Cell Dev Biol 2012, 23:450-457.
27. Logeat F., Bessia C., Brou C., LeBail O., Jarriault S., Seidah N.G., et al. The Notch1 receptor is cleaved constitutively by a furin-like convertase. Proc Natl Acad Sci USA 1998, 95:8108-8112.
28. Struhl G., Greenwald I. Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 1999, 398:522-525.
29. Brou C., Logeat F., Gupta N., Bessia C., LeBail O., Doedens J.R., et al. A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Mol Cell 2000, 5:207-216.
30. Kopan R., Ilagan M.X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009, 137:216-233.
31. Bray S., Bernard F. Notch targets and their regulation. Curr Top Dev Biol 2010, 92:253-275.
32. Luther K.B., Haltiwanger R.S. Role of unusual O-glycans in intercellular signaling. Int J Biochem Cell Biol 2009, 41:1011-1024.
33. Takeuchi H., Haltiwanger R.S. Significance of glycosylation in Notch signaling. Biochem Biophys Res Commun 2014, 453:235-242.
34. Moloney D.J., Panin V.M., Johnston S.H., Chen J., Shao L., Wilson R., et al. Fringe is a glycosyltransferase that modifies Notch. Nature 2000, 406:369-375.
35. Yang L.T., Nichols J.T., Yao C., Manilay J.O., Robey E.A., Weinmaster G. Fringe glycosyltransferases differentially modulate Notch1 proteolysis induced by Delta1 and Jagged1. Mol Biol Cell 2005, 16:927-942.
36. Hicks C., Johnston S.H., diSibio G., Collazo A., Vogt T.F., Weinmaster G. Fringe differentially modulates Jagged1 and Delta1 signalling through Notch1 and Notch2. Nat Cell Biol 2000, 2:515-520.
37. Panin V.M., Shao L., Lei L., Moloney D.J., Irvine K.D., Haltiwanger R.S. Notch ligands are substrates for protein O-fucosyltransferase-and Fringe. J Biol Chem 2002, 277:29945-29952.
38. Muller J., Rana N.A., Serth K., Kakuda S., Haltiwanger R.S., Gossler A. O-fucosylation of the notch ligand mDLL1 by POFUT1 is dispensable for ligand function. PLoS ONE 2014, 9:88571.
39. Conlon R.A., Reaume A.G., Rossant J. Notch1 is required for the coordinate segmentation of somites. Development 1995, 121:1533-1545.
40. Bessho Y., Sakata R., Komatsu S., Shiota K., Yamada S., Kageyama R. Dynamic expression and essential functions of Hes7 in somite segmentation. Genes Dev 2001, 15:2642-2647.
41. Evrard Y.A., Lun Y., Aulehla A., Gan L., Johnson R.L. Lunatic fringe is an essential mediator of somite segmentation and patterning. Nature 1998, 394:377-381.
42. Kusumi K., Sun E.S., Kerrebrock A.W., Bronson R.T., Chi D.C., Bulotsky M.S., et al. The mouse pudgy mutation disrupts Delta homologue Dll3 and initiation of early somite boundaries. Nat Genet 1998, 19:274-278.
43. Shifley E.T., Vanhorn K.M., Perez-Balaguer A., Franklin J.D., Weinstein M., Cole S.E. Oscillatory lunatic fringe activity is crucial for segmentation of the anterior but not posterior skeleton. Development 2008, 135:899-908.
44. Sparrow D.B., Chapman G., Wouters M.A., Whittock N.V., Ellard S., Fatkin D., et al. Mutation of the LUNATIC FRINGE gene in humans causes spondylocostal dysostosis with a severe vertebral phenotype. Am J Hum Genet 2006, 78:28-37.
45. Bulman M.P., Kusumi K., Frayling T.M., McKeown C., Garrett C., Lander E.S., et al. Mutations in the human delta homologue, DLL3, cause axial skeletal defects in spondylocostal dysostosis. Nat Genet 2000, 24:438-441.
46. Sparrow D.B., Guillen-Navarro E., Fatkin D., Dunwoodie S.L. Mutation of hairy-and-enhancer-of-split-in humans causes spondylocostal dysostosis. Hum Mol Genet 2008, 17:3761-3766.
47. Holley S.A., Julich D., Rauch G.J., Geisler R., Nusslein-Volhard C. her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development 2002, 129:1175-1183.
48. Henry C.A., Urban M.K., Dill K.K., Merlie J.P., Page M.F., Kimmel C.B., et al. Two linked hairy/Enhancer of split-related zebrafish genes, her1 and her7, function together to refine alternating somite boundaries. Development 2002, 129:3693-3704.
49. Giudicelli F., Ozbudak E.M., Wright G.J., Lewis J. Setting the tempo in development: an investigation of the zebrafish somite clock mechanism. PLoS Biol 2007, 5:e150.
50. Bessho Y., Hirata H., Masamizu Y., Kageyama R. Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock. Genes Dev 2003, 17:1451-1456.
51. Chen J., Kang L., Zhang N. Negative feedback loop formed by Lunatic fringe and Hes7 controls their oscillatory expression during somitogenesis. Genesis 2005, 43:196-204.
52. Mara A., Schroeder J., Chalouni C., Holley S.A. Priming, initiation and synchronization of the segmentation clock by deltaD and deltaC. Nat Cell Biol 2007, 9:523-530.
53. Holley S.A., Geisler R., Nusslein-Volhard C. Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity. Genes Dev 2000, 14:1678-1690.
54. Wright G.J., Giudicelli F., Soza-Ried C., Hanisch A., Ariza-McNaughton L., Lewis J. DeltaC and DeltaD interact as Notch ligands in the zebrafish segmentation clock. Development 2011, 138:2947-2956.
55. Soza-Ried C., Ozturk E., Ish-Horowicz D., Lewis J. Pulses of Notch activation synchronise oscillating somite cells and entrain the zebrafish segmentation clock. Development 2014, 141:1780-1788.
56. Delaune E.A., Francois P., Shih N.P., Amacher S.L. Single-cell-resolution imaging of the impact of Notch signaling and mitosis on segmentation clock dynamics. Dev Cell 2012, 23:995-1005.
57. Huppert S.S., Ilagan M.X., De Strooper B., Kopan R. Analysis of Notch function in presomitic mesoderm suggests a gamma-secretase-independent role for presenilins in somite differentiation. Dev Cell 2005, 8:677-688.
58. Morimoto M., Takahashi Y., Endo M., Saga Y. The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity. Nature 2005, 435:354-359.
59. Niwa Y., Masamizu Y., Liu T., Nakayama R., Deng C.X., Kageyama R. The initiation and propagation of Hes7 oscillation are cooperatively regulated by Fgf and notch signaling in the somite segmentation clock. Dev Cell 2007, 13:298-304.
60. Feller J., Schneider A., Schuster-Gossler K., Gossler A. Noncyclic Notch activity in the presomitic mesoderm demonstrates uncoupling of somite compartmentalization and boundary formation. Genes Dev 2008, 22:2166-2171.
61. Maruhashi M., Putte V.D., Huylebroeck D., Kondoh H., Higashi Y. Involvement of SIP1 in positioning of somite boundaries in the mouse embryo. Dev Dyn 2005, 234:332-338.
62. Zhang N., Gridley T. Defects in somite formation in lunatic fringe-deficient mice. Nature 1998, 394:374-377.
63. Serth K., Schuster-Gossler K., Cordes R., Gossler A. Transcriptional oscillation of lunatic fringe is essential for somitogenesis. Genes Dev 2003, 17:912-925.
64. Dale J.K., Maroto M., Dequeant M.L., Malapert P., McGrew M., Pourquie O. Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 2003, 421:275-278.
65. Cole S.E., Levorse J.M., Tilghman S.M., Vogt T.F. Clock regulatory elements control cyclic expression of Lunatic fringe during somitogenesis. Dev Cell 2002, 3:75-84.
66. Morales A.V., Yasuda Y., Ish-Horowicz D. Periodic Lunatic fringe expression is controlled during segmentation by a cyclic transcriptional enhancer responsive to notch signaling. Dev Cell 2002, 3:63-74.
67. Aulehla A., Johnson R.L. Dynamic expression of lunatic fringe suggests a link between notch signaling and an autonomous cellular oscillator driving somite segmentation. Dev Biol 1999, 207:49-61.
68. Oginuma M., Takahashi Y., Kitajima S., Kiso M., Kanno J., Kimura A., et al. The oscillation of Notch activation, but not its boundary, is required for somite border formation and rostral-caudal patterning within a somite. Development 2010, 137:1515-1522.
69. Okubo Y., Sugawara T., Abe-Koduka N., Kanno J., Kimura A., Saga Y. Lfng regulates the synchronized oscillation of the mouse segmentation clock via trans-repression of Notch signalling. Nat Commun 2012, 3:1141.
70. Niwa Y., Shimojo H., Isomura A., Gonzalez A., Miyachi H., Kageyama R. Different types of oscillations in Notch and Fgf signaling regulate the spatiotemporal periodicity of somitogenesis. Genes Dev 2011, 25:1115-1120.
71. Ferjentsik Z., Hayashi S., Dale J.K., Bessho Y., Herreman A., De Strooper B., et al. Notch is a critical component of the mouse somitogenesis oscillator and is essential for the formation of the somites. PLoS Genetics 2009, 5:e1000662.
72. Williams D.R., Shifley E.T., Lather J.D., Cole S.E. Posterior skeletal development and the segmentation clock period are sensitive to Lfng dosage during somitogenesis. Dev Biol 2014, 388:159-169.
73. Dequeant M.L., Glynn E., Gaudenz K., Wahl M., Chen J., Mushegian A., et al. A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 2006, 314:1595-1598.
74. Stauber M., Laclef C., Vezzaro A., Page M.E., Ish-Horowicz D. Modifying transcript lengths of cycling mouse segmentation genes. Mech Dev 2012, 129:61-72.
75. Fujimuro T., Matsui T., Nitanda Y., Matta T., Sakumura Y., Saito M., et al. Hes7 3'UTR is required for somite segmentation function. Sci Rep 2014, 4:6462.
76. Hoyle N.P., Ish-Horowicz D. Transcript processing and export kinetics are rate-limiting steps in expressing vertebrate segmentation clock genes. Proc Natl Acad Sci USA 2013, 110:E4316-E4324.
77. Harima Y., Takashima Y., Ueda Y., Ohtsuka T., Kageyama R. Accelerating the tempo of the segmentation clock by reducing the number of introns in the hes7 gene. Cell Rep 2013, 3:1-7.
78. Takashima Y., Ohtsuka T., Gonzalez A., Miyachi H., Kageyama R. Intronic delay is essential for oscillatory expression in the segmentation clock. Proc Natl Acad Sci USA 2011, 108:3300-3305.
79. Feng P., Navaratna M. Modelling periodic oscillations during somitogenesis. Math Biosci Eng 2007, 4:661-673.
80. Nitanda Y., Matsui T., Matta T., Higami A., Kohno K., Nakahata Y., et al. 3'-UTR-dependent regulation of mRNA turnover is critical for differential distribution patterns of cyclic gene mRNAs. FEBS J 2014, 281:146-156.
81. Riley M.F., Bochter M.S., Wahi K., Nuovo G.J., Cole S.E. Mir-125a-5p-mediated regulation of Lfng is essential for the avian segmentation clock. Dev Cell 2013, 24:554-561.
82. Hirata H., Bessho Y., Kokubu H., Masamizu Y., Yamada S., Lewis J., et al. Instability of Hes7 protein is crucial for the somite segmentation clock. Nat Genet 2004, 36:750-754.
83. Oates A.C., Morelli L.G., Ares S. Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development 2012, 139:625-639.
84. Aulehla A., Wehrle C., Brand-Saberi B., Kemler R., Gossler A., Kanzler B., et al. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 2003, 4:395-406.
85. Dubrulle J., Pourquie O. fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 2004, 427:419-422.
86. Delfini M.C., Dubrulle J., Malapert P., Chal J., Pourquie O. Control of the segmentation process by graded MAPK/ERK activation in the chick embryo. Proc Natl Acad Sci USA 2005, 102:11343-11348.
87. Diez del Corral R., Olivera-Martinez I., Goriely A., Gale E., Maden M., Storey K., et al. FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 2003, 40:65-79.
88. Aulehla A., Wiegraebe W., Baubet V., Wahl M.B., Deng C., Taketo M., et al. A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat Cell Biol 2008, 10:186-193.
89. Dunty W.C., Biris K.K., Chalamalasetty R.B., Taketo M.M., Lewandoski M., Yamaguchi T.P. Wnt3a/-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 2008, 135:85-94.
90. Takada S., Stark K.L., Shea M.J., Vassileva G., McMahon J.A., McMahon A.P. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 1994, 8:174-189.
91. Dubrulle J., McGrew M.J., Pourquie O. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 2001, 106:219-232.
92. Naiche L.A., Holder N., Lewandoski M. FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis. Proc Natl Acad Sci USA 2011, 108:4018-4023.
93. Kawamura A., Koshida S., Hijikata H., Sakaguchi T., Kondoh H., Takada S. Zebrafish hairy/enhancer of split protein links FGF signaling to cyclic gene expression in the periodic segmentation of somites. Genes Dev 2005, 19:1156-1161.
94. Schroter C., Ares S., Morelli L.G., Isakova A., Hens K., Soroldoni D., et al. Topology and dynamics of the zebrafish segmentation clock core circuit. PLoS Biol 2012, 10:e1001364.
95. Schwendinger-Schreck J., Kang Y., Holley S.A. Modeling the zebrafish segmentation clock's gene regulatory network constrained by expression data suggests evolutionary transitions between oscillating and nonoscillating transcription. Genetics 2014, 197:725-738.
96. Schroter C., Oates A.C. Segment number and axial identity in a segmentation clock period mutant. Curr Biol 2010, 20:1254-1258.
97. Saga Y., Kitajima S., Miyagawa-Tomita S. Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc Med 2000, 10:345-352.
98. Takahashi Y., Koizumi K., Takagi A., Kitajima S., Inoue T., Koseki H., et al. Mesp2 initiates somite segmentation through the Notch signalling pathway. Nat Genet 2000, 25:390-396.
99. Yasuhiko Y., Haraguchi S., Kitajima S., Takahashi Y., Kanno J., Saga Y. Tbx6-mediated Notch signaling controls somite-specific Mesp2 expression. Proc Natl Acad Sci USA 2006, 103:3651-3656.
100. Yasuhiko Y., Kitajima S., Takahashi Y., Oginuma M., Kagiwada H., Kanno J., et al. Functional importance of evolutionally conserved Tbx6 binding sites in the presomitic mesoderm-specific enhancer of Mesp2. Development 2008, 135:3511-3519.
101. Oginuma M., Niwa Y., Chapman D.L., Saga Y. Mesp2 and Tbx6 cooperatively create periodic patterns coupled with the clock machinery during mouse somitogenesis. Development 2008, 135:2555-2562.
102. Morimoto M., Sasaki N., Oginuma M., Kiso M., Igarashi K., Aizaki K., et al. The negative regulation of Mesp2 by mouse Ripply2 is required to establish the rostro-caudal patterning within a somite. Development 2007, 134:1561-1569.
103. Takahashi J., Ohbayashi A., Oginuma M., Saito D., Mochizuki A., Saga Y., et al. Analysis of Ripply1/2-deficient mouse embryos reveals a mechanism underlying the rostro-caudal patterning within a somite. Dev Biol 2010, 342:134-145.
104. Lauschke V.M., Tsiairis C.D., Francois P., Aulehla A. Scaling of embryonic patterning based on phase-gradient encoding. Nature 2013, 493:101-105.
105. Koizumi K., Nakajima M., Yuasa S., Saga Y., Sakai T., Kuriyama T., et al. The role of presenilin 1 during somite segmentation. Development 2001, 128:1391-1402.
106. Sasaki N., Kiso M., Kitagawa M., Saga Y. The repression of Notch signaling occurs via the destabilization of mastermind-like 1 by Mesp2 and is essential for somitogenesis. Development 2011, 138:55-64.
107. White P.H., Chapman D.L. Dll1 is a downstream target of Tbx6 in the paraxial mesoderm. Genesis 2005, 42:193-202.
108. Lopez T.P., Fan C.M. Dynamic CREB family activity drives segmentation and posterior polarity specification in mammalian somitogenesis. Proc Natl Acad Sci USA 2013, 110:E2019-E2027.