Abstract
ABSTRACT A combination of micromanipulative cell grafting and flu-orescent cell labelling techniques were used to examine the developmental fate of the cranial paraxial mesoderm of the 8.5-day early-somite-stage mouse embryo. Mesodermal cells isolated from seven regions of the cranial mesoderm, identified on the basis of their topographical association with specific brain segments were assessed for their contribution to craniofacial morphogenesis during 48 hours of in vitro development. The results demonstrate extensive cell mixing between adjacent but not alternate groups of mesodermal cells and a strict cranial-to-caudal distribution of the paraxial mesoderm to craniofacial structures. A two-segment periodicity similar to the origins of the branchial motor neurons and the distribution of the rhombencephalic neural crest cells was observed as the paraxial mesoderm migrates during formation of the first three branchial arches. The paraxial mesoderm colonises the mesenchymal core of the branchial arches, consistent with the location of the muscle plates. A dorsoventral regionalisation of cell fate similar to that of the somitic mesoderm is also found. This suggests evolution has conserved the fate of the murine cranial paraxial mesoderm as a multiprogenitor population which displays a predominantly myogenic fate. Heterotopic transplantation of cells to different regions of the cranial mesoderm revealed no discernible restriction in cell potency in the craniocaudal axis, reflecting considerable plasticity in the developmental fate of the cranial mesoderm at least at the time of experimentation. The distribution of the different groups of cranial mesoderm matches closely with that of the cranial neural crest cells suggesting the two cell populations may share a common segmental origin and similar destination.
References
58
Referenced
151
10.1016/0925-4773(93)90071-5
/ Mech. Dev / The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos by Bulfone (1993)10.1242/dev.102.4.763
/ Development / Positional signals: evidence for a possible role in muscle fibre-type patterning of the embryonic avian limb by Butler (1988)10.1242/dev.116.4.1123
/ Development / Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differently expressed during early mesodermal patterning in mouse embryos by Candia (1992)10.1016/0304-3940(86)90132-1
/ Neurosci Letters / Intraspecific chick/chick chimaeras: dystrophic somitic mesoderm transplanted to a normal host forms muscles with a dystrophic phenotype by Cauwenbergs (1986){'key': '2024121800004980900_DEVELOP_120_9_2397C5', 'first-page': '183', 'article-title': 'The histogenetic potential of neural plate cells of early-somite-stage mouse embryos', 'volume': '96', 'author': 'Chan', 'year': '1986', 'journal-title': 'J. Embryol. Exp. Morph'}
/ J. Embryol. Exp. Morph / The histogenetic potential of neural plate cells of early-somite-stage mouse embryos by Chan (1986)10.1242/dev.102.2.427
/ Development / A morphological and experimental study of the mesencephalic neural crest cells in the mouse embryo using wheat germ agglutin-gold conjugates as the cell marker by Chan (1988)10.1242/dev.111.4.945
/ Development / Expression of the mouse a1(II) collagen gene is not restricted to cartilage during development by Cheah (1991){'key': '2024121800004980900_DEVELOP_120_9_2397C8', 'first-page': '73', 'article-title': 'Role of somitic mesoderm in the development of the thorax in bird embryos. II. Origin of thoracic and appendicular musculature', 'volume': '49', 'author': 'Chevallier', 'year': '1979', 'journal-title': 'J. Embryol. Exp. Morph'}
/ J. Embryol. Exp. Morph / Role of somitic mesoderm in the development of the thorax in bird embryos. II. Origin of thoracic and appendicular musculature by Chevallier (1979)10.1007/BF00848416
/ Wilhelm Roux’ Archiv. Ent Mech. Org / On the role of the connective tissue in the patterning of the chick limb musculature by Chevallier (1982)10.1242/dev.102.4.735
/ Development / Embryonic vascular development: Immunohistochemical identification of the origin and subsequent morphogenesis of the major vessel primordia in quail embryos by Coffin (1988)10.1242/dev.114.1.1
/ Development / The developmental fate of the cephalic mesoderm in chick-quail chimaeras by Couly (1992)10.1242/dev.117.2.409
/ Development / The triple origin of the skull in higher vertebrates: a study in chick-quail chimeras by Couly (1993)10.1006/dbio.1993.1118
/ Dev. Biol / The homeobox gene S8: mesoderm- specific expression in presomite embryos and in cells cultured in vitro and modulation in differentiating pluripotent cells by de Jong (1993)10.1038/363630a0
/ Nature / Segmental organisation of the embryonic diencephalon by Figdor (1993)10.1016/0960-9822(93)90033-K
/ Curr. Biol / Segmentation moves to the fore by Fraser (1993)10.1038/344431a0
/ Nature / Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions by Fraser (1990)10.1016/0092-8674(91)90029-X
/ Cell / Deciphering the Hox code: Clues to patterning branchial regions of the head by Hunt (1991)10.1242/dev.112.1.43
/ Development / Patterning the vertebrate head: murine Hox 2 genes mark distinct subpopulations of premigratory and migrating neural crest by Hunt (1991)10.1038/353861a0
/ Nature / A distinct Hox code for the branchial region of the vertebrate head by Hunt (1991){'issue': 'Supplement', 'key': '2024121800004980900_DEVELOP_120_9_2397C20', 'article-title': 'Homeobox genes and models for patterning the hindbrain and branchial arches', 'volume': '113', 'author': 'Hunt', 'year': '1991', 'journal-title': 'Development'}
/ Development / Homeobox genes and models for patterning the hindbrain and branchial arches by Hunt (1991){'key': '2024121800004980900_DEVELOP_120_9_2397C21', 'first-page': '42', 'article-title': 'Somitomeres: Mesodermal segments in the head and trunk', 'volume': '1', 'author': 'Jacobson', 'year': '1993', 'journal-title': 'The Vertebrate Skull'}
/ The Vertebrate Skull / Somitomeres: Mesodermal segments in the head and trunk by Jacobson (1993)10.1002/ar.1092030308
/ Anat. Rec / Cephalic neurulation in the mouse embryo analyzed by SEM and morphometry by Jacobson (1982){'key': '2024121800004980900_DEVELOP_120_9_2397C23', 'first-page': '1', 'article-title': 'Somitomeres: The primordial body segments', 'volume': '118', 'author': 'Jacobson', 'year': '1986', 'journal-title': 'Somites in Developing Embryos'}
/ Somites in Developing Embryos / Somitomeres: The primordial body segments by Jacobson (1986)10.1038/310786a0
/ Nature / Segmentation in the vertebrate nervous system by Keynes (1984){'volume-title': 'The Neural Crest. Cambridge: Cambridge University Press', 'year': '1982', 'author': 'Le Douarin', 'key': '2024121800004980900_DEVELOP_120_9_2397C25'}
/ The Neural Crest. Cambridge: Cambridge University Press by Le Douarin (1982){'key': '2024121800004980900_DEVELOP_120_9_2397C26', 'first-page': '17', 'article-title': 'Participation of neural crest-derived cells in the genesis of the skull in birds', 'volume': '347', 'author': 'Le Lievre', 'year': '1978', 'journal-title': 'J. Embryol. Exp. Morph'}
/ J. Embryol. Exp. Morph / Participation of neural crest-derived cells in the genesis of the skull in birds by Le Lievre (1978)10.1016/0166-2236(90)90144-Y
/ Trends Neurosci / The cellular basis of segmentation in the developing hindbrain by Lumsden (1990)10.1038/337424a0
/ Nature / Segmental patterns of neuronal development in the chick hindbrain by Lumsden (1989)10.1242/dev.113.4.1281
/ Development / Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo by Lumsden (1991){'key': '2024121800004980900_DEVELOP_120_9_2397C30', 'first-page': '1', 'article-title': 'The spatial pattern of muscle development in the limb', 'volume-title': 'The Development and Specialisation of Muscle', 'author': 'McLachlan', 'year': '1980'}
/ The Development and Specialisation of Muscle / The spatial pattern of muscle development in the limb by McLachlan (1980){'key': '2024121800004980900_DEVELOP_120_9_2397C31', 'first-page': '73', 'article-title': 'Development of the chick mesoblast. Formation of the embryonic axis and the establishment of the metameric pattern', 'volume': '38', 'author': 'Meier', 'year': '1979', 'journal-title': 'Dev. Biol'}
/ Dev. Biol / Development of the chick mesoblast. Formation of the embryonic axis and the establishment of the metameric pattern by Meier (1979)10.1111/j.1432-0436.1982.tb01202.x
/ Differentiation / Metameric pattern development in the embryonic axis of the mouse I. Differentiation of the cranial segments by Meier (1982)10.1006/dbio.1993.1251
/ Dev. Biol / Preferential expression of alternatively spliced mRNAs encoding Type II procollagen with a cysteine- rich amino-propeptide in differentiating cartilage and non-chondrogenic tissues during early mouse development by Ng (1993)10.1242/dev.113.Supplement_2.59
/ Development / Conserved segmental expression of Krox-20 in the vertebrate hindbrain and its relationship to lineage restriction by Nieto (1991)10.1242/dev.116.4.1137
/ Development / A receptor protein tyrosine kinase implicated in the segmental patterning of the hindbrain and mesoderm by Nieto (1992)10.1016/0012-1606(78)90202-6
/ Dev. Biol / The control of avian cephalic neural crest cytodifferentiation. I. Skeletal and connective tissues by Noden (1978){'key': '2024121800004980900_DEVELOP_120_9_2397C37', 'first-page': '167', 'article-title': 'Patterns and organisation of craniofacial skeletogenic and myogenic mesenchyme: A perspective', 'volume-title': 'Factors and Mechanisms Influencing Bone Growth', 'author': 'Noden', 'year': '1982'}
/ Factors and Mechanisms Influencing Bone Growth / Patterns and organisation of craniofacial skeletogenic and myogenic mesenchyme: A perspective by Noden (1982)10.1016/0012-1606(83)90318-4
/ Dev. Biol / The role of the neural crest in patterning of the avian cranial skeletal, connective and muscle tissues by Noden (1983)10.1002/aja.1001680302
/ Amer. J. Anat / The embryonic origins of the avian cephalic and cervical muscles and associated connective tissues by Noden (1983)10.1016/0012-1606(86)90138-7
/ Dev. Biol / Patterning of avian craniofacial muscles by Noden (1986)10.1242/dev.103.Supplement.121
/ Development / Interactions and fates of avian craniofacial mesenchyme by Noden (1988)10.1006/dbio.1994.1211
/ Dev. Biol / The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos by Osumi-Yamashita (1994)10.1242/dev.111.4.1097
/ Development / Early expression of the myogenic regulatory gene, myf-5, in precursors of skeletal muscle in the mouse embryo by Ott (1991){'key': '2024121800004980900_DEVELOP_120_9_2397C44', 'first-page': '339', 'article-title': 'Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognising endothelial cells', 'volume': '100', 'author': 'Pardanaud', 'year': '1987', 'journal-title': 'Dev. Biol'}
/ Dev. Biol / Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognising endothelial cells by Pardanaud (1987)10.1073/pnas.80.10.2976
/ Proc. Nat. Acad. Sci. USA / Surface marker for hemopoeitic and endothelial cell lineages in quail that is defined by a monoclonal antibody by Peault (1983){'key': '2024121800004980900_DEVELOP_120_9_2397C46', 'first-page': '443', 'article-title': 'Developmental angiogenesis: Quail embryonic vasculature', 'volume': '2', 'author': 'Poole', 'year': '1988', 'journal-title': 'Scanning Microscopy'}
/ Scanning Microscopy / Developmental angiogenesis: Quail embryonic vasculature by Poole (1988){'key': '2024121800004980900_DEVELOP_120_9_2397C47', 'first-page': '472', 'article-title': 'Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organisation', 'volume': '16', 'author': 'Puelles', 'year': '1993', 'journal-title': 'Trends Genet'}
/ Trends Genet / Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organisation by Puelles (1993)10.1016/0925-4773(93)90016-Q
/ Mech. Dev / Characterisation and developmental expression of Tlx-1, the murine homologue of HOX11 by Raju (1993)10.1242/dev.116.2.297
/ Development / Vital dye analysis of cranial neural crest cell migration in the mouse embryo by Serbedzija (1992)10.1016/0076-6879(93)25013-R
/ Meth. Enzymol / Isolation and culture of whole postimplantation embryos and germ layer derivatives by Sturm (1993)10.1002/aja.1001640303
/ Amer. J. Anat / The establishment of a somitomeric pattern in the mesoderm of a gastrulating mouse embryo by Tam (1982)10.1242/dev.115.3.703
/ Development / The somitogenic potential of cells in the primitive streak and the tail bud of the organogenesis-stage mouse embryo by Tam (1992)10.1007/BF00190586
/ Anat. Embryol / Segmentation and specification of the paraxial mesoderm by Tam (1994){'key': '2024121800004980900_DEVELOP_120_9_2397C54', 'article-title': 'Analysis of cranial neural crest cell migration and early fates in post-implantation rat chimaeras', 'volume-title': 'J. Embryol. Exp. Morphol. 98:21-58', 'author': 'Tan', 'year': '1986'}
/ J. Embryol. Exp. Morphol. 98:21-58 / Analysis of cranial neural crest cell migration and early fates in post-implantation rat chimaeras by Tan (1986)10.1016/0960-9822(93)90075-Y
/ Current Biology / The problems of building a head by Thorogood (1993)10.1038/341405a0
/ Nature / Segmental expression of Hox-2 homeobox-containing genes in the developing mouse hindbrain by Wilkinson (1989)10.1016/0166-2236(90)90145-Z
/ Trends Neurosci / Molecular approaches to the segmentation of the hindbrain by Wilkinson (1990)10.1016/0012-1606(91)90086-I
/ Dev. Biol / The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and Drosophila twist genes by Wolf (1991)
Dates
Type | When |
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Created | 4 years, 4 months ago (April 23, 2021, 2:37 p.m.) |
Deposited | 8 months, 2 weeks ago (Dec. 17, 2024, 7:02 p.m.) |
Indexed | 3 weeks, 4 days ago (Aug. 7, 2025, 4:25 p.m.) |
Issued | 31 years ago (Sept. 1, 1994) |
Published | 31 years ago (Sept. 1, 1994) |
Published Online | 31 years ago (Sept. 1, 1994) |
Published Print | 31 years ago (Sept. 1, 1994) |
@article{Trainor_1994, title={Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos}, volume={120}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.120.9.2397}, DOI={10.1242/dev.120.9.2397}, number={9}, journal={Development}, publisher={The Company of Biologists}, author={Trainor, Paul A. and Tan, Seong-Seng and Tam, Patrick P. L.}, year={1994}, month=sep, pages={2397–2408} }