期刊论文详细信息
BMC Developmental Biology
The dermomyotome ventrolateral lip is essential for the hypaxial myotome formation
Ruijin Huang2  Beate Brand-Saberi3  Ketan Patel5  Michael Hans1  Dieter Schwandulla1  Carsten Theiss3  Maryna Masyuk3  Aisha Abduelmula3  Qin Pu4 
[1] Institute of Physiology, Medical Faculty Bonn, Rheinish Friedrich-Wilhelms-University of Bonn, Bonn, Germany;Institute of Anatomy and Cell Biology, Department of Molecular Embryology, Medical Faculty, Albert- Ludwigs-University of Freiburg, Freiburg, Germany;Institute of Anatomy, Department of Anatomy and Molecular Embryology, Medical Faculty, Ruhr University of Bochum, Bochum, Germany;Institute of Anatomy, Department of Neuroanatomy, Medical Faculty Bonn, Rheinish Friedrich-Wilhelms-University of Bonn, Bonn, Germany;School Biological Sciences, University of Reading, Reading, UK
关键词: Chicken embryo;    Myotome;    Dermomyotome;    Somite;   
Others  :  1085432
DOI  :  10.1186/1471-213X-13-37
 received in 2013-03-22, accepted in 2013-10-11,  发布年份 2013
PDF
【 摘 要 】

Background

The myotome is the primitive skeletal muscle that forms within the embryonic metameric body wall. It can be subdivided into an epaxial and hypaxial domain. It has been shown that the formation of the epaxial myotome requires the dorsomedial lip of the dermomyotome (DML). Although the ventrolateral lip (VLL) of the dermomyotome is believed to be required for the formation of the hypaxial myotome, experimentally evidence for this statement still needs to be provided. Provision of such data would enable the resolution of a debate regarding the formation of the hypaxial dermomyotome. Two mechanisms have been proposed for this tissue. The first proposes that the intermediate dermomyotome undergoes cellular expansion thereby pushing the ventral lateral lip in a lateral direction (translocation). In contrast, the alternative view holds that the ventral lateral lip grows laterally.

Results

Using time lapse confocal microscopy, we observed that the GFP-labelled ventrolateral lip (VLL) of the dermomyotome grows rather than translocates in a lateral direction. The necessity of the VLL for lateral extension of the myotome was addressed by ablation studies. We found that the hypaxial myotome did not form after VLL ablation. In contrast, the removal of an intermediate portion of the dermomyotome had very little effect of the hypaxial myotome. These results demonstrate that the VLL is required for the formation of the hypaxial myotome.

Conclusion

Our study demonstrates that the dermomyotome ventrolateral lip is essential for the hypaxial myotome formation and supports the lip extension model. Therefore, despite being under independent signalling controls, both the dorsomedial and ventrolateral lip fulfil the same function, i.e. they extend into adjacent regions permitting the growth of the myotome.

【 授权许可】

   
2013 Pu et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150113173250658.pdf 3032KB PDF download
Figure 2. 55KB Image download
Figure 1. 134KB Image download
【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】
  • [1]Chevallier A, Kieny M, Mauger A: Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 1977, 41:245-258.
  • [2]Franz T, Kothary R, Surani MA, Halata Z, Grim M: The Splotch mutation interferes with muscle development in the limbs. Anat Embryol (Berl) 1993, 187:153-160.
  • [3]Bober E, Franz T, Arnold HH, Gruss P, Tremblay P: Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 1994, 120:603-612.
  • [4]Zhi Q, Huang R, Christ B, Brand-Saberi B: Participation of individual brachial somites in skeletal muscles of the avian distal wing. Anat Embryol (Berl) 1996, 194:327-339.
  • [5]Huang R, Zhi Q, Izpisua-Belmonte JC, Christ B, Patel K: Origin and development of the avian tongue muscles. Anat Embryol (Berl) 1999, 200:137-152.
  • [6]He L, Papoutsi M, Huang R, Tomarev SI, Christ B, Kurz H, Wilting J: Three different fates of cells migrating from somites into the limb bud. Anat Embryol (Berl) 2003, 207:29-34.
  • [7]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.
  • [8]Huang R, Zhi Q, Wilting J, Christ B: The fate of somitocoele cells in avian embryos. Anat Embryol (Berl) 1994, 190:243-250.
  • [9]Mittapalli VR, Huang R, Patel K, Christ B, Scaal M: Arthrotome: a specific joint forming compartment in the avian somite. Dev Dyn 2005, 234:48-53.
  • [10]Christ B, Huang R, Wilting J: The development of the avian vertebral column. Anat Embryol (Berl) 2000, 202:179-194.
  • [11]Huang R, Christ B: Origin of the epaxial and hypaxial myotome in avian embryos. Anat Embryol (Berl) 2000, 202:369-374.
  • [12]Brent AE, Schweitzer R, Tabin CJ: A somitic compartment of tendon progenitors. Cell 2003, 113:235-248.
  • [13]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.
  • [14]Christ B, Ordahl CP: Early stages of chick somite development. Anat Embryol (Berl) 1995, 191:381-396.
  • [15]Kaehn K, Jacob HJ, Christ B, Hinrichsen K, Poelmann RE: The onset of myotome formation in the chick. Anat Embryol (Berl) 1988, 177:191-201.
  • [16]Denetclaw WF Jr, Christ B, Ordahl CP: Location and growth of epaxial myotome precursor cells. Development 1997, 124:1601-1610.
  • [17]Denetclaw WF, Ordahl CP: The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos. Development 2000, 127:893-905.
  • [18]Venters SJ, Ordahl CP: Persistent myogenic capacity of the dermomyotome dorsomedial lip and restriction of myogenic competence. Development 2002, 129:3873-3885.
  • [19]Denetclaw WF Jr, Berdougo E, Venters SJ, Ordahl CP: Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome. Development 2001, 128:1745-1755.
  • [20]Kahane N, Cinnamon Y, Kalcheim C: The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development. Development 1998, 125:4259-4271.
  • [21]Kahane N, Kalcheim C: Identification of early postmitotic cells in distinct embryonic sites and their possible roles in morphogenesis. Cell Tissue Res 1998, 294:297-307.
  • [22]Cinnamon Y, Kahane N, Bachelet I, Kalcheim C: The sub-lip domain–a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development 2001, 128:341-351.
  • [23]Cinnamon Y, Kahane N, Kalcheim C: Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 1999, 126:4305-4315.
  • [24]Kahane N, Cinnamon Y, Kalcheim C: The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome. Development 2002, 129:2675-2687.
  • [25]Gros J, Scaal M, Marcelle C: A two-step mechanism for myotome formation in chick. Dev Cell 2004, 6:875-882.
  • [26]Ordahl CP, Berdougo E, Venters SJ, Denetclaw WF Jr: The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. Development 2001, 128:1731-1744.
  • [27]Eloy-Trinquet S, Nicolas JF: Clonal separation and regionalisation during formation of the medial and lateral myotomes in the mouse embryo. Development 2002, 129:111-122.
  • [28]Goulding MD, Chalepakis G, Deutsch U, Erselius JR, Gruss P: Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 1991, 10:1135-1147.
  • [29]Goulding M, Lumsden A, Paquette AJ: Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 1994, 120:957-971.
  • [30]Williams BA, Ordahl CP: Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 1994, 120:785-796.
  • [31]Jungel-Waas K, Christ B, Brand-Saberi B: Defect repair after somite removal in avian embryos is not true regeneration. Anat Embryol (Berl) 1998, 198:255-265.
  • [32]Aoyama H, Asamoto K: Determination of somite cells: independence of cell differentiation and morphogenesis. Development 1988, 104:15-28.
  • [33]Ordahl CP, Le Douarin NM: Two myogenic lineages within the developing somite. Development 1992, 114:339-353.
  • [34]Dietrich S, Schubert FR, Healy C, Sharpe PT, Lumsden A: Specification of the hypaxial musculature. Development 1998, 125:2235-2249.
  • [35]Marcelle C, Stark MR, Bronner-Fraser M: Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 1997, 124:3955-3963.
  • [36]Fan CM, Lee CS, Tessier-Lavigne M: A role for WNT proteins in induction of dermomyotome. Dev Biol 1997, 191:160-165.
  • [37]Gros J, Serralbo O, Marcelle C: WNT11 acts as a directional cue to organize the elongation of early muscle fibres. Nature 2009, 457:589-593.
  • [38]Pourquie O, Coltey M, Breant C, Le Douarin NM: Control of somite patterning by signals from the lateral plate. Proc Natl Acad Sci U S A 1995, 92:3219-3223.
  • [39]Pourquie O, Fan CM, Coltey M, Hirsinger E, Watanabe Y, Breant C, Francis-West P, Brickell P, Tessier-Lavigne M, Le Douarin NM: Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 1996, 84:461-471.
  • [40]Cheng L, Alvares LE, Ahmed MU, El-Hanfy AS, Dietrich S: The epaxial-hypaxial subdivision of the avian somite. Dev Biol 2004, 274:348-369.
  • [41]Hamburger V, Hamilton HL: A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 1992, 195:231-272.
  • [42]Scaal M, Gros J, Lesbros C, Marcelle C: In ovo electroporation of avian somites. Dev Dyn 2004, 229:643-650.
  • [43]Dai F, Yusuf F, Farjah GH, Brand-Saberi B: RNAi-induced targeted silencing of developmental control genes during chicken embryogenesis. Dev Biol 2005, 285:80-90.
  • [44]Valasek P, Theis S, DeLaurier A, Hinits Y, Luke GN, Otto AM, Minchin J, He L, Christ B, Brooks G, et al.: Cellular and molecular investigations into the development of the pectoral girdle. Dev Biol 2011, 357:108-116.
  • [45]Pu Q, Christ B, Huang R: Temporal sequence in the formation of midline dermis and dorsal vertebral elements in avian embryos. J Anat 2012, 221:115-120.
  • [46]Pu Q, Bai Z, Haque Z, Wang J, Huang R: Occipital somites guide motor axons of the accessory nerve in the avian embryo. Neuroscience 2013, 246:22-27.
  • [47]Nieto MA, Patel K, Wilkinson DG: In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 1996, 51:219-235.
  文献评价指标  
  下载次数:23次 浏览次数:4次