Divergent and conserved roles of Dll1 signaling in development of craniofacial and trunk muscle

Developmental Biology

Volumn 395, Issue 2, 2014, Pages 307-316

  Czajkowski, Maciej T ^a   Rassek, Claudia ^a   Lenhard, Diana C ^a   Bröhl, Dominique ^a   Birchmeier, Carmen ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Craniofacial muscles; Dll1; Myogenic progenitor cells; Notch signaling; Pax7

Indexed keywords

DLL1 PROTEIN; MYOD PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR PAX7; UNCLASSIFIED DRUG; DLK1 PROTEIN, MOUSE; NOTCH RECEPTOR; PAX7 PROTEIN, MOUSE; PRIMER DNA; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL HOMING; CONTROLLED STUDY; EXTRAOCULAR MUSCLE; FACE MUSCLE; GENE MUTATION; GENE REPRESSION; MASSETER MUSCLE; MESODERM; MOUSE; MUSCLE DEVELOPMENT; MUSCLE GROWTH; MYOBLAST; MYOGENIC PROGENITOR CELL; NONHUMAN; NOTCH SIGNALING; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; STEM CELL; TIBIALIS ANTERIOR MUSCLE; TONGUE; ANIMAL; EMBRYOLOGY; FLOW CYTOMETRY; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MORPHOGENESIS; MUTANT MOUSE STRAIN; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRUNK;

ANIMALS; DNA PRIMERS; FACIAL MUSCLES; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, MUTANT STRAINS; MORPHOGENESIS; MUSCLE, SKELETAL; PAX7 TRANSCRIPTION FACTOR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NOTCH; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; TORSO;

EID: 84908121858     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.09.005     Document Type: Article

References (54)

1. Artavanis-Tsakonas S., Rand M.D., Lake R.J. Notch signaling: cell fate control and signal integration in development. Science 1999, 284:770-776.
2. Bjornson C.R., Cheung T.H., Liu L., Tripathi P.V., Steeper K.M., Rando T.A. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 2012, 30:232-242.
3. Bladt F., Riethmacher D., Isenmann S., Aguzzi A., Birchmeier C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 1995, 376:768-771.
4. Bröhl D., Vasyutina E., Czajkowski M.T., Griger J., Rassek C., Rahn H.P., Purfurst B., Wende H., Birchmeier C. Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals. Dev. Cell 2012, 23:469-481.
5. Brohmann H., Jagla K., Birchmeier C. The role of Lbx1 in migration of muscle precursor cells. Development 2000, 127:437-445.
6. Buas M.F., Kabak S., Kadesch T. Inhibition of myogenesis by Notch: evidence for multiple pathways. J. Cell Physiol. 2009, 218:84-93.
7. Buas M.F., Kadesch T. Regulation of skeletal myogenesis by Notch. Exp. Cell Res. 2010, 316:3028-3033.
8. Conboy I.M., Rando T.A. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 2002, 3:397-409.
9. Delfini M.C., Hirsinger E., Pourquie O., Duprez D. Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. Development 2000, 127:5213-5224.
10. Dietrich S., Abou-Rebyeh F., Brohmann H., Bladt F., Sonnenberg-Riethmacher E., Yamaai T., Lumsden A., Brand-Saberi B., Birchmeier C. The role of SF/HGF and c-Met in the development of skeletal muscle. Development 1999, 126:1621-1629.
11. Dong F., Sun X., Liu W., Ai D., Klysik E., Lu M.F., Hadley J., Antoni L., Chen L., Baldini A., Francis-West P., Martin J.F. Pitx2 promotes development of splanchnic mesoderm-derived branchiomeric muscle. Development 2006, 133:4891-4899.
12. Grifone R., Kelly R.G. Heartening news for head muscle development. Trends Genet. 2007, 23:365-369.
13. Gros J., Manceau M., Thome V., Marcelle C. A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 2005, 435:954-958.
14. Harel I., Nathan E., Tirosh-Finkel L., Zigdon H., Guimaraes-Camboa N., Evans S.M., Tzahor E. Distinct origins and genetic programs of head muscle satellite cells. Dev. Cell 2009, 16:822-832.
15. Hazelton R.D. A radioautographic analysis of the migration and fate of cells derived from the occipital somites in the chick embryo with specific reference to the development of the hypoglossal musculature. J. Embryol. Exp. Morphol. 1970, 24:455-466.
16. Hirsinger E., Malapert P., Dubrulle J., Delfini M.C., Duprez D., Henrique D., Ish-Horowicz D., Pourquie O. Notch signalling acts in postmitotic avian myogenic cells to control MyoD activation. Development 2001, 128:107-116.
17. Horst D., Ustanina S., Sergi C., Mikuz G., Juergens H., Braun T., Vorobyov E. Comparative expression analysis of Pax3 and Pax7 during mouse myogenesis. Int. J. Dev. Biol. 2006, 50:47-54.
18. Hrabe de Angelis M., McIntyre J., Gossler A. Maintenance of somite borders in mice requires the Delta homologue DII1. Nature 1997, 386:717-721.
19. Huang R., Zhi Q., Izpisua-Belmonte J.C., Christ B., Patel K. Origin and development of the avian tongue muscles. Anat. Embryol. (Berl) 1999, 200:137-152.
20. Jarriault S., Brou C., Logeat F., Schroeter E.H., Kopan R., Israel A. Signalling downstream of activated mammalian Notch. Nature 1995, 377:355-358.
21. Kassar-Duchossoy L., Gayraud-Morel B., Gomes D., Rocancourt D., Buckingham M., Shinin V., Tajbakhsh S. Mrf4 determines skeletal muscle identity in Myf5:myod double-mutant mice. Nature 2004, 431:466-471.
22. Kassar-Duchossoy L., Giacone E., Gayraud-Morel B., Jory A., Gomes D., Tajbakhsh S. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 2005, 19:1426-1431.
23. Kelly R.G., Jerome-Majewska L.A., Papaioannou V.E. The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum. Mol. Gen. 2004, 13:2829-2840.
24. Kimble J., Simpson P. The LIN-12/Notch signaling pathway and its regulation. Annu. Rev. Cell Dev. Biol. 1997, 13:333-361.
25. Kitamura K., Miura H., Miyagawa-Tomita S., Yanazawa M., Katoh-Fukui Y., Suzuki R., Ohuchi H., Suehiro A., Motegi Y., Nakahara Y., Kondo S., Yokoyama M. Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 1999, 126:5749-5758.
26. Kopan R., Nye J.S., Weintraub H. The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development 1994, 120:2385-2396.
27. Kuroda K., Tani S., Tamura K., Minoguchi S., Kurooka H., Honjo T. Delta-induced Notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J. Biol. Chem. 1999, 274:7238-7244.
28. Lewis J. Notch signalling and the control of cell fate choices in vertebrates. Semin. Cell Dev. Biol. 1998, 9:583-589.
29. Lin S., Shen H., Jin B., Gu Y., Chen Z., Cao C., Hu C., Keller C., Pear W.S., Wu L. Brief report: blockade of Notch signaling in muscle stem cells causes muscular dystrophic phenotype and impaired muscle regeneration. Stem Cells 2013, 31:823-828.
30. Lu J.R., Bassel-Duby R., Hawkins A., Chang P., Valdez R., Wu H., Gan L., Shelton J.M., Richardson J.A., Olson E.N. Control of facial muscle development by MyoR and capsulin. Science 2002, 298:2378-2381.
31. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
32. Mootoosamy R.C., Dietrich S. Distinct regulatory cascades for head and trunk myogenesis. Development 2002, 129:573-583.
33. Mourikis P., Gopalakrishnan S., Sambasivan R., Tajbakhsh S. Cell-autonomous Notch activity maintains the temporal specification potential of skeletal muscle stem cells. Development 2012, 139:4536-4548.
34. Mourikis P., Sambasivan R., Castel D., Rocheteau P., Bizzarro V., Tajbakhsh S. A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 2012, 30:243-252.
35. Nathan E., Monovich A., Tirosh-Finkel L., Harrelson Z., Rousso T., Rinon A., Harel I., Evans S.M., Tzahor E. The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development 2008, 135:647-657.
36. Noden D.M. The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am. J. Anat. 1983, 168:257-276.
37. Noden D.M., Francis-West P. The differentiation and morphogenesis of craniofacial muscles. Dev. Dyn. 2006, 235:1194-1218.
38. Ono Y., Boldrin L., Knopp P., Morgan J.E., Zammit P.S. Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev. Biol. 2010, 337:29-41.
39. Relaix F., Demignon J., Laclef C., Pujol J., Santolini M., Niro C., Lagha M., Rocancourt D., Buckingham M., Maire P. Six homeoproteins directly activate Myod expression in the gene regulatory networks that control early myogenesis. PLoS Genet. 2013, 9:e1003425.
40. Relaix F., Rocancourt D., Mansouri A., Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 2005, 435:948-953.
41. Rudnicki M.A., Braun T., Hinuma S., Jaenisch R. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 1992, 71:383-390.
42. Rudnicki M.A., Schnegelsberg P.N., Stead R.H., Braun T., Arnold H.H., Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 1993, 75:1351-1359.
43. Saga Y., Miyagawa-Tomita S., Takagi A., Kitajima S., Miyazaki J., Inoue T. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 1999, 126:3437-3447.
44. Sambasivan R., Gayraud-Morel B., Dumas G., Cimper C., Paisant S., Kelly R.G., Tajbakhsh S. Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev. Cell 2009, 16:810-821.
45. Sambasivan R., Kuratani S., Tajbakhsh S. An eye on the head: the development and evolution of craniofacial muscles. Development 2011, 138:2401-2415.
46. Schuster-Gossler K., Cordes R., Gossler A. Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:537-542.
47. Shawber C., Nofziger D., Hsieh J.J., Lindsell C., Bogler O., Hayward D., Weinmaster G. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 1996, 122:3765-3773.
48. Sieber M.A., Storm R., Martinez-de-la-Torre M., Muller T., Wende H., Reuter K., Vasyutina E., Birchmeier C. Lbx1 acts as a selector gene in the fate determination of somatosensory and viscerosensory relay neurons in the hindbrain. J. Neurosci. 2007, 27:4902-4909.
49. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
50. Tajbakhsh S., Rocancourt D., Cossu G., Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 1997, 89:127-138.
51. Theis S., Patel K., Valasek P., Otto A., Pu Q., Harel I., Tzahor E., Tajbakhsh S., Christ B., Huang R. The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development 2010, 137:2961-2971.
52. Tzahor E. Heart and craniofacial muscle development: a new developmental theme of distinct myogenic fields. Dev. Biol. 2009, 327:273-279.
53. Vasyutina E., Lenhard D.C., Wende H., Erdmann B., Epstein J.A., Birchmeier C. RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:4443-4448.
54. Wilkinson D.G. In Situ Hybridization: A Practical Approach 1992, Oxford University Press/IRL Press.