Somitogenesis

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Introduction

Human embryo (week 4, Carnegie stage 11) Somites

The term used to describe the process of segmentation of the paraxial mesoderm within the trilaminar embryo body to form pairs of somites, or balls of mesoderm. In humans, the first somite pair appears at day 20 and adds caudally at 1 somite pair/90 minutes until on average 44 pairs eventually form.


A somite is added either side of the notochord (axial mesoderm) to form a somite pair. The segmentation does not occur in the head region, and begins cranially (head end) and extends caudally (tailward) adding a somite pair at regular time intervals. The process is sequential and therefore used to stage the age of many different species embryos based upon the number visible somite pairs.


A mesenchymal to epithelial transition defines the outer cellular "shell" of the developing somite, with the core cells remain as a mesenchymal organisation. During early somite development a transient fluid-filled space, the somitocoel, can be identified in each somite and is later lost by cell proliferation. Neural crest cells also enter and mix with the somatic cells.


Somites give rise to many different connective tissues including: cartilage, bone, muscle and tendon.

Mesoderm Links: Endoderm | Mesoderm | Ectoderm | Lecture - Mesoderm | Lecture - Musculoskeletal | 2016 Lecture | Notochord | Notochord Movie | Somitogenesis | Musculoskeletal | Sonic hedgehog | Category:Mesoderm
Historic Embryology  
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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Historic Papers: 1883 | 1910 Chick Somites | 1933 | 1935 Rabbit Somites

Historic Textbooks: 1892 Primitive Segments | 1907 Somites | 1910 Skeleton | 1914 Somite | 1920 Chick Mesoderm | 1921 Connective Tissue | 1951 Frog Mesoderm

Musculoskeletal Links: Introduction | Mesoderm | Somitogenesis | Limb | Cartilage | Bone | Bone Timeline | Axial Skeleton | Skull | Joint | Muscle | Muscle Timeline | Tendon | Diaphragm | Lecture - Musculoskeletal Development | Lecture Movie | Abnormalities | Limb Abnormalities | Cartilage Histology | Bone Histology | Skeletal Muscle Histology | Category:Musculoskeletal
Historic Musculoskeletal Embryology  
1902 - Pubo-femoral Region | Spinal Column and Back | Body Segmentation | Cranium | Body Wall, Ribs, and Sternum | Limbs | 1901 - Limbs | 1902 - Arm Development | 1906 Human Embryo Ossification | 1906 Lower limb Nerves and Muscle | 1907 - Muscular System | Skeleton and Limbs | 1909 Mandible | 1910 - Skeleton and Connective Tissues | Muscular System | Coelom and Diaphragm | 1913 Clavicle | 1920 Clavicle | 1921 - External body form | Connective tissues and skeletal | Muscular | Diaphragm | 1929 Rat Somite | 1932 Pelvis | 1940 Synovial Joints | 1943 Human Embryonic, Fetal and Circumnatal Skeleton | 1949 Cartilage and Bone | 1957 Chondrification Hands and Feet

Some Recent Findings

Mouse somitogenesis genes[1]
  • Developmental dynamics of occipital and cervical somites[2] "Development of somites leading to somite compartments, sclerotome, dermomyotome and myotome, has been intensely investigated. Most knowledge on somite development, including the commonly used somite maturation stages, is based on data from somites at thoracic and lumbar levels. Potential regional differences in somite maturation dynamics have been indicated by a number of studies, but have not yet been comprehensively examined. Here, we present an overview on the developmental dynamics of somites at occipital and cervical levels in the chicken embryo. We show that in these regions, the onset of sclerotomal and myotomal compartment formation is later than at thoracolumbar levels, and is initiated simultaneously in multiple somites, which is in contrast to the serial cranial- to- caudal progression of somite maturation in the trunk."
  • Mesogenin 1 is a master regulator of paraxial presomitic mesoderm differentiation[3] "Neuromesodermal (NM) stem cells generate neural and paraxial presomitic mesoderm (PSM) cells, which are the respective progenitors of the spinal cord and musculoskeleton of the trunk and tail. The Wnt-regulated basic helix-loop-helix (bHLH) transcription factor mesogenin 1 (Msgn1) has been implicated as a cooperative regulator working in concert with T-box genes to control PSM formation in zebrafish, although the mechanism is unknown. We show here that, in mice, Msgn1 alone controls PSM differentiation by directly activating the transcriptional programs that define PSM identity, epithelial-mesenchymal transition, motility and segmentation. Forced expression of Msgn1 in NM stem cells in vivo reduced the contribution of their progeny to the neural tube, and dramatically expanded the unsegmented mesenchymal PSM while blocking somitogenesis and notochord differentiation. Expression of Msgn1 was sufficient to partially rescue PSM differentiation in Wnt3a(-/-) embryos, demonstrating that Msgn1 functions downstream of Wnt3a as the master regulator of PSM differentiation."
  • The precise timeline of transcriptional regulation reveals causation in mouse somitogenesis network[1] "In vertebrate development, the segmental pattern of the body axis is established as somites, masses of mesoderm distributed along the two sides of the neural tube, are formed sequentially in the anterior-posterior axis. This mechanism depends on waves of gene expression associated with the Notch, Fgf and Wnt pathways."
  • From dynamic expression patterns to boundary formation in the presomitic mesoderm[4] "The segmentation of the vertebrate body is laid down during early embryogenesis. The formation of signaling gradients, the periodic expression of genes of the Notch-, Fgf- and Wnt-pathways and their interplay in the unsegmented presomitic mesoderm (PSM) precedes the rhythmic budding of nascent somites at its anterior end, which later develops into epithelialized structures, the somites. Although many in silico models describing partial aspects of somitogenesis already exist, simulations of a complete causal chain from gene expression in the growth zone via the interaction of multiple cells to segmentation are rare. Here, we present an enhanced gene regulatory network (GRN) for mice in a simulation program that models the growing PSM by many virtual cells and integrates WNT3A and FGF8 gradient formation, periodic gene expression and Delta/Notch signaling. Assuming Hes7 as core of the somitogenesis clock and LFNG as modulator, we postulate a negative feedback of HES7 on Dll1 leading to an oscillating Dll1 expression as seen in vivo. "
  • FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis[5] "Somites form along the embryonic axis by sequential segmentation from the presomitic mesoderm (PSM) and differentiate into the segmented vertebral column as well as other unsegmented tissues. Somites are thought to form via the intersection of two activities known as the clock and the wavefront. ...Significantly, markers of nascent somite cell fate expand throughout the PSM, demonstrating the premature differentiation of this entire tissue, a highly unusual phenotype indicative of the loss of wavefront activity. When WNT signaling is restored in mutants, PSM progenitor markers are partially restored but premature differentiation of the PSM still occurs, demonstrating that FGF signaling operates independently of WNT signaling. This study provides genetic evidence that FGFs are the wavefront signal and identifies the specific FGF ligands that encode this activity. Furthermore, these data show that FGF action maintains WNT signaling, and that both signaling pathways are required in parallel to maintain PSM progenitor tissue."
More recent papers  
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This table shows an automated computer PubMed search using the listed sub-heading term.

  • Therefore the list of references do not reflect any editorial selection of material based on content or relevance.
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References listed on the rest of the content page and the associated discussion page (listed under the publication year sub-headings) do include some editorial selection based upon both relevance and availability.

Links: References | Discussion Page | Pubmed Most Recent | Journal Searches


Search term: Somitogenesis

Paul Bardot, Stéphane D Vincent, Marjorie Fournier, Alexis Hubaud, Mathilde Joint, László Tora, Olivier Pourquié The TAF10-containing TFIID and SAGA transcriptional complexes are dispensable for early somitogenesis in the mouse embryo. Development: 2017; PubMed 28893950

Harika Nagandla, M David Stewart Quantification of Embryonic Myofiber Development by Immunofluorescence. Methods Mol. Biol.: 2017, 1668;167-176 PubMed 28842909

Cindy Xu, Mariana B Grizante, Kenro Kusumi Somitogenesis and Axial Development in Reptiles. Methods Mol. Biol.: 2017, 1650;335-353 PubMed 28809033

Alexander J Hale, Eline Ter Steege, Jeroen den Hertog Recent advances in understanding the role of protein-tyrosine phosphatases in development and disease. Dev. Biol.: 2017, 428(2);283-292 PubMed 28728679

Presomitic Mesoderm

Model for Sprouty4 and FGF in mesoderm segmentation
  • Within the mesodermal layer either side of the notochord (axial mesoderm) lie the paraxial mesoderm strips.
  • Below the unsegmented cranial paraxial mesoderm region the region that will later segment is described as presomitic mesoderm (PSM).
  • This PSM is being "patterned" by two two molecular activities described as the "clock" and the "wavefront" (reviewed[6])
  • Many different molecular factors are involved in this patterning effect.
    • Hes7, FGF, Sprouty4, Notch, Shh
  • notochord influences somite formation, notochord removal increases the period of molecular clock oscillations.[7]
Somitogenesis 01 icon.jpg
 ‎‎Somitogenesis
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Human First Somites

Stage9 dorsal.jpg Stage9 bf3.jpg Stage 9 SEM1.jpg

Human embryo first somite pairs (week 4, Carnegie stage 9)

Somite Number

Week 4 to 5 (GA 6 to 7) covers the main period of human somitogenesis.

Human Embryo Somite Number
Week Days Carnegie Stage Somite Number (pairs)
Week 3 19 - 21 9 1 - 3
Week 4 22 - 23 10 4 - 12
Week 4 23 - 26 11 13 - 20
Week 4 26 - 30 12 21 - 29
Week 4 28 - 32 13 30

Seel also Other species Somitogenesis

Mesoderm to Somite

Human embryo first somite pair (week 4, Carnegie stage 9)

Mesoderm means the "middle layer" and it is from this layer that nearly all the bodies connective tissues are derived. In early mesoderm development a number of transient structures will form and then be lost as tissue structure is patterned and organised. Humans are vertebrates, with a "backbone", and the first mesoderm structure we will see form after the notochord will be somites.

  • During segmentation the outer cell layer forms an epithelial layer over a still mesenchymal organization of cells at the core.
  • The early forming somite has a cavity at its core called a "somitocoel" that later fills with proliferating mesoderm cells.


Mesoderm cartoon.gif

Mesoderm-cartoon1.jpgMesoderm-cartoon2.jpgMesoderm-cartoon3.jpgMesoderm-cartoon4.jpg

Human embryo (week 4, Carnegie stage 11) Somites

Somite to Sclerotome and Dermomyotome

  Sclerotome   Dermatome
  • sclerotome later becomes subdivided
    • rostral and caudal halves separated laterally by von Ebner's fissure
  • half somites contribute to a single vertebral level body
  • other half intervertebral disc
  • therefore final vertebral segmentation “shifts”
  • connective tissue underlying epidermis
  • begins as a dorsal thickening
  • spreads throughout the body
  Myotome
  • Body - epaxial and hypaxial muscles
  • Limbs - flexor and extensor muscles


Somite initially forms 2 main regional components

  • ventromedial region - sclerotome forms vertebral body and intervertebral disc
  • dorsolateral region - dermomyotome forms dermis and skeletal muscle

Somite 001 icon.jpg

Sclerotome

Somite regions
  • The left and right sclerotomes from the same segmental level engulf the notochord.
  • Each segmental level is then resegmented in a rostrocaudal direction.

Dermomyotome

  • The dermomyotome is divided into a dorsal and ventral half.
    • Dorsal - dermatome.
    • Ventral - myotome, this will also divide into a dorsal and ventral half that contribute the epaxial and hypaxial skeletal muscle groups respectively.
  • hypaxial - muscles of the ventrolateral body wall, girdle, limb and tongue.[8]
    • Muscle cells of the limb, tongue and lateral shoulder girdle muscles - derived from somite migrating myogenic precursor cells.
    • Muscle cells of the ventrolateral body wall muscles (intercostal and abdominal muscles) and the medial shoulder girdle muscles - derived from the myotome.


Part of the shoulder girdle muscles (trapezius and sternocleidomastoideus) - derived from the lateral plate mesoderm.

Molecular

Pax

Mesoderm Development and Pax cartoon

Mesoderm Development and Pax[9]


Links: Developmental Signals - Pax

Mesogenin 1

A master regulator of paraxial presomitic mesoderm differentiation.'[3]

Other Species

Animal Species - Average Somite Pair Number
Species Somites Number
Human 44
Mouse 65
Chicken 55
Lizard (anole) 72-73
Xenopus 42
Zebrafish 32

Chicken

Chicken Somitogenesis
HH Stages
Age
Somite Number
7
23-26 hr 1 somite
7 to 8-
ca. 23-26 hr 1-3
8
26-29 hr 4
9
29-33 hr 7
9+ to 10-
ca. 33 hr 8-9
10
33-38 hr 10
11
40-45 hr 13
12
45-49 hr 16
13
48-52 hr 19
13+ to 14-
ca. 50-52 hr 20-21
14
50-53 hr 22
14+ to 15-
ca. 50-54 hr 23
15
50-55 hr 24-27
16
51-56 hr 26-28
17
52-64 hr 29-32
18
3 da 30-36
19
3.0-3.5 da 37- 40 extending into tail
20
3.0-3.5 da 40-43
21
3.5 da 43-44
22
3.5-4.0 da Somites extend to tip of tail
Hamburger Hamilton Stages | Chicken Development
Chicken Somitogenesis  
HH Stages
Age
Somite Number
7
23-26 hr 1 somite
7 to 8-
ca. 23-26 hr 1-3
8
26-29 hr 4
9
29-33 hr 7
9+ to 10-
ca. 33 hr 8-9
10
33-38 hr 10
11
40-45 hr 13
12
45-49 hr 16
13
48-52 hr 19
13+ to 14-
ca. 50-52 hr 20-21
14
50-53 hr 22
14+ to 15-
ca. 50-54 hr 23
15
50-55 hr 24-27
16
51-56 hr 26-28
17
52-64 hr 29-32
18
3 da 30-36
19
3.0-3.5 da 37- 40 extending into tail
20
3.0-3.5 da 40-43
21
3.5 da 43-44
22
3.5-4.0 da Somites extend to tip of tail
Hamburger Hamilton Stages | Chicken Development

Mouse

Mouse Somitogenesis
Theiler Stages
Age E
(range dpc)
Somite
Number
Rat Witschi
Stage
Human Stage
12 8 1 - 7 14-15 9
13 8.5 (8 - 9.25) 8 - 12 15 10
14 9 (8.5 - 9.75) 13 - 20 16 11
15 9.5 (9 - 10.25) 21 - 29 17 - 19 12
16 10 (9.5 - 10.75) 30 - 34 20 - 21 13 - 15
17 10.5 (10 - 11.25) 35 - 39 24 - 25 13 - 15
18 11 (10.5 - 11.25) 40 - 44 25 - 26 13 - 15
19 11.5 (11 - 12.25) 45 - 47 26 - 27 16
20 12 (11.5 - 13) 48 - 51 28 17
21 13 (12.5-14) 52 - 55 29 - 30 18 - 19
22 14 (13.5-15) 56 - 60 31 20 - 23
23 15 60 + 32 Fetal period
Mouse Somitogenesis  
Theiler
Stages
Age E
(range dpc)
Somite
Number
Rat Witschi
Stage
Human Stage
12 8 1 - 7 14-15 9
13 8.5 (8 - 9.25) 8 - 12 15 10
14 9 (8.5 - 9.75) 13 - 20 16 11
15 9.5 (9 - 10.25) 21 - 29 17 - 19 12
16 10 (9.5 - 10.75) 30 - 34 20 - 21 13 - 15
17 10.5 (10 - 11.25) 35 - 39 24 - 25 13 - 15
18 11 (10.5 - 11.25) 40 - 44 25 - 26 13 - 15
19 11.5 (11 - 12.25) 45 - 47 26 - 27 16
20 12 (11.5 - 13) 48 - 51 28 17
21 13 (12.5-14) 52 - 55 29 - 30 18 - 19
22 14 (13.5-15) 56 - 60 31 20 - 23
23 15 60 + 32 Fetal period

Rat

Table III - Showing Means And Variation For Each Rat Age
Maximum Variation
Age
Days-Hrs.
Number of
Litters
Number of
Embryos
Counted
Means All Embryos One Litter Standard
Deviation
Coefficient of
Variation %
10-12 1 4 8.7 6-11 6-11 2.8 32
10-13 1 6 1 0. 2 8-13 8-13 1.9 19
10-16 2 12 12.4 6-26 6-26 5.8 47
10-17 6 48 12.9 4-26 7-26 3 .3 26
10-18 4 23 14.1 6-18 9-18 3.1 22
10-19 1 6 14 .3 12-17 12-17 1.2 8
10-22 3 16 13.1 6-19 6-14 3.9 30
10-23 3 17 15.2 8-18 8-18 2.4 16
11-00 2 0 14.6 10-17 10-17 1.9 13
11-02 2 15 20 . 9 17-22 17-22 1. 3 6
11-04 1 10 25. 3 23-26 23-26 1.2 5
11-06 1 2 18.0 18-18 18-18 .0 0
11-08 1 8 25 0 23-28 23-28 1.9 8
11-09 1 3 22 .0 20-25 20-25 2 . 2 10
11-10 2 18 26.2 21-31 21-31 2.9 11
11-11 3 26 25.6 14-29 14-27 3.2 12
11-12 1 3 26. 7 25-28 25-28 1.2 4
11-14 1 3 21.3 21-22 21-22 .6 2
11-15 1 8 23.1 17-28 17-28 4 . 0 17
11-16 1 7 26.7 24-28 24-28 1.3 5
11-17 1 7 26.1 25-28 25-28 1.1 4
11-18 3 25 25 .4 19-28 19-28 1.9 7
11-20 2 16 27.2 25-29 25-29 1.2 4
23 Ages 44 292 Av 2.2 Av 13%
Reference: Landacre FL. and Amstutz MM. Data on the number of somites compared with age in the white rat. (1929) Ohio J. Science. 29(6): 253-259.
Table III Showing Means And Variation For Each Age 
Table III - Showing Means And Variation For Each Rat Age
Maximum Variation
Age
Days-Hrs.
Number of
Litters
Number of
Embryos
Counted
Means All Embryos One Litter Standard
Deviation
Coefficient of
Variation %
10-12 1 4 8.7 6-11 6-11 2.8 32
10-13 1 6 1 0. 2 8-13 8-13 1.9 19
10-16 2 12 12.4 6-26 6-26 5.8 47
10-17 6 48 12.9 4-26 7-26 3 .3 26
10-18 4 23 14.1 6-18 9-18 3.1 22
10-19 1 6 14 .3 12-17 12-17 1.2 8
10-22 3 16 13.1 6-19 6-14 3.9 30
10-23 3 17 15.2 8-18 8-18 2.4 16
11-00 2 0 14.6 10-17 10-17 1.9 13
11-02 2 15 20 . 9 17-22 17-22 1. 3 6
11-04 1 10 25. 3 23-26 23-26 1.2 5
11-06 1 2 18.0 18-18 18-18 .0 0
11-08 1 8 25 0 23-28 23-28 1.9 8
11-09 1 3 22 .0 20-25 20-25 2 . 2 10
11-10 2 18 26.2 21-31 21-31 2.9 11
11-11 3 26 25.6 14-29 14-27 3.2 12
11-12 1 3 26. 7 25-28 25-28 1.2 4
11-14 1 3 21.3 21-22 21-22 .6 2
11-15 1 8 23.1 17-28 17-28 4 . 0 17
11-16 1 7 26.7 24-28 24-28 1.3 5
11-17 1 7 26.1 25-28 25-28 1.1 4
11-18 3 25 25 .4 19-28 19-28 1.9 7
11-20 2 16 27.2 25-29 25-29 1.2 4
23 Ages 44 292 Av 2.2 Av 13%
Reference: Landacre FL. and Amstutz MM. Data on the number of somites compared with age in the white rat. (1929) Ohio J. Science. 29(6): 253-259.
Reference: Landacre FL. and Amstutz MM. Data on the number of somites compared with age in the white rat. (1929) Ohio J. Science. 29(6): 253-259.

Additional Images

References

  1. 1.0 1.1 Bernard Fongang, Andrzej Kudlicki The precise timeline of transcriptional regulation reveals causation in mouse somitogenesis network. BMC Dev. Biol.: 2013, 13;42 PubMed 24304493 | BMC Dev Biol.
  2. Anja Maschner, Stefanie Krück, Margarethe Draga, Felicitas Pröls, Martin Scaal Developmental dynamics of occipital and cervical somites. J. Anat.: 2016; PubMed 27380812
  3. 3.0 3.1 Ravindra B Chalamalasetty, Robert J Garriock, William C Dunty, Mark W Kennedy, Parthav Jailwala, Han Si, Terry P Yamaguchi Mesogenin 1 is a master regulator of paraxial presomitic mesoderm differentiation. Development: 2014, 141(22);4285-97 PubMed 25371364
  4. Hendrik B Tiedemann, Elida Schneltzer, Stefan Zeiser, Bastian Hoesel, Johannes Beckers, Gerhard K H Przemeck, Martin Hrabě de Angelis From dynamic expression patterns to boundary formation in the presomitic mesoderm. PLoS Comput. Biol.: 2012, 8(6);e1002586 PubMed 22761566 | PLoS Comput Biol.
  5. L A Naiche, Nakisha Holder, Mark Lewandoski FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis. Proc. Natl. Acad. Sci. U.S.A.: 2011, 108(10);4018-23 PubMed 21368122
  6. Alexander Aulehla, Olivier Pourquié On periodicity and directionality of somitogenesis. Anat. Embryol.: 2006, 211 Suppl 1;3-8 PubMed 17024300
  7. Tatiana P Resende, Mónica Ferreira, Marie-Aimée Teillet, Ana Teresa Tavares, Raquel P Andrade, Isabel Palmeirim Sonic hedgehog in temporal control of somite formation. Proc. Natl. Acad. Sci. U.S.A.: 2010, 107(29);12907-12 PubMed 20615943
  8. Qin Pu, Aisha Abduelmula, Maryna Masyuk, Carsten Theiss, Dieter Schwandulla, Michael Hans, Ketan Patel, Beate Brand-Saberi, Ruijin Huang The dermomyotome ventrolateral lip is essential for the hypaxial myotome formation. BMC Dev. Biol.: 2013, 13;37 PubMed 24138189
  9. Judith A Blake, Melanie R Ziman Pax genes: regulators of lineage specification and progenitor cell maintenance. Development: 2014, 141(4);737-51 PubMed 24496612 | Development

Reviews

Yoshiko Takahashi, Yuki Sato Somitogenesis as a model to study the formation of morphological boundaries and cell epithelialization. Dev. Growth Differ.: 2008, 50 Suppl 1;S149-55 PubMed 18482400

Peter D Turnpenny Defective somitogenesis and abnormal vertebral segmentation in man. Adv. Exp. Med. Biol.: 2008, 638;164-89 PubMed 21038776

Kenro Kusumi, William Sewell, Megan L O'Brien Mouse mutations disrupting somitogenesis and vertebral patterning. Adv. Exp. Med. Biol.: 2008, 638;140-63 PubMed 21038775

Andrew Mara, Scott A Holley Oscillators and the emergence of tissue organization during zebrafish somitogenesis. Trends Cell Biol.: 2007, 17(12);593-9 PubMed 17988868

Olivier Cinquin Understanding the somitogenesis clock: what's missing? Mech. Dev.: 2007, 124(7-8);501-17 PubMed 17643270

Emily T Shifley, Susan E Cole The vertebrate segmentation clock and its role in skeletal birth defects. Birth Defects Res. C Embryo Today: 2007, 81(2);121-33 PubMed 17600784

Alexander Aulehla, Olivier Pourquié On periodicity and directionality of somitogenesis. Anat. Embryol.: 2006, 211 Suppl 1;3-8 PubMed 17024300

Ava E Brent Somite formation: where left meets right. Curr. Biol.: 2005, 15(12);R468-70 PubMed 15964269

Bodo Christ, Ruijin Huang, Martin Scaal Formation and differentiation of the avian sclerotome. Anat. Embryol.: 2004, 208(5);333-50 PubMed 15309628

Martin Scaal, Bodo Christ Formation and differentiation of the avian dermomyotome. Anat. Embryol.: 2004, 208(6);411-24 PubMed 15338303


Articles

R O'Rahilly, F Müller Somites, spinal Ganglia, and centra. Enumeration and interrelationships in staged human embryos, and implications for neural tube defects. Cells Tissues Organs (Print): 2003, 173(2);75-92 PubMed 12649586

| Cells Tissues Organs

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