Musculoskeletal System - Shoulder Development

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Stage20-23 limbs b.jpg

Introduction

Adult shoulder skeleton
Adult appendicular skeleton
Limb bud geometry and patterning[1]

The skeletal shoulder consists of: the clavicle (collarbone), the scapula (shoulder blade), and the humerus. Development of his region occurs through both forms of ossification processes.

The mesoderm forms nearly all the connective tissues of the musculoskeletal system. Each tissue (cartilage, bone, and muscle) goes through many different mechanisms of differentiation.

The musculoskeletal system consists of skeletal muscle, bone, and cartilage and is mainly mesoderm in origin with some neural crest contribution.

The intraembryonic mesoderm can be broken into paraxial, intermediate and lateral mesoderm relative to its midline position. During the 3rd week the paraxial mesoderm forms into "balls" of mesoderm paired either side of the neural groove, called somites.

Somites appear bilaterally as pairs at the same time and form earliest at the cranial (rostral,brain) end of the neural groove and add sequentially at the caudal end. This addition occurs so regularly that embryos are staged according to the number of somites that are present. Different regions of the somite differentiate into dermomyotome (dermal and muscle component) and sclerotome (forms vertebral column). An example of a specialized musculoskeletal structure can be seen in the development of the limbs.

Skeletal muscle forms by fusion of mononucleated myoblasts to form mutinucleated myotubes. Bone is formed through a lengthy process involving ossification of a cartilage formed from mesenchyme. Two main forms of ossification occur in different bones, intramembranous (eg skull) and endochondrial (eg limb long bones) ossification. Ossification continues postnatally, through puberty until mid 20s. Early ossification occurs at the ends of long bones.

Musculoskeletal and limb abnormalities are one of the largest groups of congenital abnormalities.


Historic Embryology: 1902 Shoulder Girdle
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 | 1908 Vertebra | 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 | 1947 Joints | 1949 Cartilage and Bone | 1957 Chondrification Hands and Feet | 1968 Knee

Some Recent Findings

  • Scapula development is governed by genetic interactions of Pbx1 with its family members and with Emx2 via their cooperative control of Alx1[2] "The genetic pathways underlying shoulder blade development are largely unknown, as gene networks controlling limb morphogenesis have limited influence on scapula formation. Analysis of mouse mutants for Pbx and Emx2 genes has suggested their potential roles in girdle development. In this study, by generating compound mutant mice, we examined the genetic control of scapula development by Pbx genes and their functional relationship with Emx2. Analyses of Pbx and Pbx1;Emx2 compound mutants revealed that Pbx genes share overlapping functions in shoulder development and that Pbx1 genetically interacts with Emx2 in this process. Here, we provide a biochemical basis for Pbx1;Emx2 genetic interaction by showing that Pbx1 and Emx2 can bind specific DNA sequences as heterodimers. Moreover, the expression of genes crucial for scapula development is altered in these mutants, indicating that Pbx genes act upstream of essential pathways for scapula formation. In particular, expression of Alx1, an effector of scapula blade patterning, is absent in all compound mutants. We demonstrate that Pbx1 and Emx2 bind in vivo to a conserved sequence upstream of Alx1 and cooperatively activate its transcription via this potential regulatory element. Our results establish an essential role for Pbx1 in genetic interactions with its family members and with Emx2 and delineate novel regulatory networks in shoulder girdle development."
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.
  • References appear in this list based upon the date of the actual page viewing.

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.

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Search term: Shoulder Development

Juliane Diedrich, William Heymann, Samuel Leweke, Stephen Hunt, Robert Todd, Christian Kunert, Will Johnson, Eric von Lieres Multi-state steric mass action model and case study on complex high loading behavior of mAb on ion exchange tentacle resin. J Chromatogr A: 2017; PubMed 29055527

Kees H Woldendorp, Anne M Boonstra, J Hans Arendzen, Michiel F Reneman Variation in occupational exposure associated with musculoskeletal complaints: a cross-sectional study among professional bassists. Int Arch Occup Environ Health: 2017; PubMed 29052757

Cristina Simon-Martinez, Ellen Jaspers, Lisa Mailleux, Kaat Desloovere, Jos Vanrenterghem, Els Ortibus, Guy Molenaers, Hilde Feys, Katrijn Klingels Negative Influence of Motor Impairments on Upper Limb Movement Patterns in Children with Unilateral Cerebral Palsy. A Statistical Parametric Mapping Study. Front Hum Neurosci: 2017, 11;482 PubMed 29051729

Michael G Saper, Lauren A Pierpoint, Wei Liu, R Dawn Comstock, John D Polousky, James R Andrews Epidemiology of Shoulder and Elbow Injuries Among United States High School Baseball Players: School Years 2005-2006 Through 2014-2015. Am J Sports Med: 2017;363546517734172 PubMed 29048928

Patricia V G Figueira, Cinira A S Haddad, Samantha K L de Almeida Rizzi, Gil Facina, Afonso C P Nazario Diagnosis of Axillary Web Syndrome in Patients After Breast Cancer Surgery: Epidemiology, Risk Factors, and Clinical Aspects: A Prospective Study. Am. J. Clin. Oncol.: 2017; PubMed 29045263

Textbooks

  • The Developing Human: Clinically Oriented Embryology (8th Edition) by Keith L. Moore and T.V.N Persaud - Moore & Persaud Chapter 15 the skeletal system
  • Larsen’s Human Embryology by GC. Schoenwolf, SB. Bleyl, PR. Brauer and PH. Francis-West - Chapter 11 Limb Dev (bone not well covered in this textbook)
  • Before we Are Born (5th ed.) Moore and Persaud Chapter 16,17: p379-397, 399-405
  • Essentials of Human Embryology Larson Chapter 11 p207-228

Embryonic Shoulder

Human embryonic shoulder girdle 01.jpg Drawing of a model of the right shoulder girdle of the 17mm. (Robinson) embryo, viewed from behind.Human embryonic shoulder girdle (17mm CRL) [3]

The sternal segment (S.S.) has been cut coronally to expose the interior, and the acromial segment has been cut horizontally for the same purpose.

The black area in each is bone, the dotted area surrounding the bone is precartilage, and the area surrounding this is perichondrium.

Above the junction of the two segments, two circles and a black dot are seen; the circles represent supraclavicular nerves, the black dot represents the cephalic vein.

The scapula has been purposely shortened.

Legend

  • Ac. pr. - acromion process
  • A. S. - acromial segment of clavicle
  • C. Al. - clei-do-mastoid
  • C. Cl. I. - coraco-clavicular ligament
  • C. pr. - coracoid process
  • T. - trapezius muscle
  • P.M. - pectoralis major
  • St. MI. - sterno-miastoid
  • S. S. - sternal segment of clavicle
Human embryonic shoulder girdle (17mm CRL) [3] 17mm CRL (Robinson) embryo
  • Week 7 - difficult to estimate the amount of shrinkage in this historic material.
  • Stage 18 CRL 13 - 17 (Somites 44 - 48)
  • Stage 19 CRL 16 - 18 (Somites 48 - 51)

Myogenesis

  • Early myogenic progenitor cells in the dermomyotome can be initially identified by the transcription factor Pax3.
  • Subsequent myogenic program development then depends on the myogenic determination factors (Myf5, MyoD, and MRF4), both Myf5 and MyoD are expressed in the limbs.
  • Final differentiation of these cells into post-mitotic muscle fibers in the limb bud is regulated by another myogenic determination factor, Myogenin.

Some text modified from[4]

Links: Muscle Development

Limb Bone

Limb sox9 and Wnt6 expression[5]
Chicken- limb bud chondrogenesis

Bone formation within the limb occurs by endochondral ossification of a pre-existing cartilage template. Ossification then replaces the existing cartilage except in the regions of articulation, where cartilage remains on the surface of the bone within the joint. Therefore bone development in the limb is initially about cartilage development or chondrogenesis.

In addition, there are two quite separate aspects to this development.

  1. Pattern - where the specific regions will commence to form cartilage, which will be different for each cartilage element.
  2. Chondrogenesis - the differentiation of mesoderm to form cartilage, which will be essentially the same program for all cartilage templates.

A recent study has identified that the overlying limb surface ectoderm potentially inhibits limb early chondrogenesis through Wnt6 signaling.[5]


Links: Cartilage Development | Bone Development

Clavicle Development

(collarbone)

Postnatal Growth

A recent paper has characterised the postnatal growth of male and female clavicles (data shown below).[6]

  • 18 years of age the mean clavicle length +/-SD for females was 149+/-12 mm and for males it was 161+/-11 mm.
  • statistically significant difference (P=0.049) was noted between the length of right and left clavicles it was not clinically significant (0.036 mm).
  • A steady growth rate was noted for both genders from birth to the age of 12 years (8.4 mm/y).
  • Above the age of 12 years there were significant differences in the growth of the clavicles of girls (2.6 mm/y) versus boys (5.4 mm/y) (P<0.001).
  • Females achieve 80% of their clavicle length by 9 years of age and boys by 12 years of age.

Scapula Development

(shoulder blade)

Humerus Development

Pelvis

Hip bone

The skeletal pelvis consists of: the sacrum and coccyx (axial skeleton), and pelvic girdle formed by a pair of hip bones (appendicular skeleton). Before puberty, he pelvic girdle also consists of three unfused bones: the ilium, ischium, and pubis. In chicken, the entire pelvic girdle originates from the somatopleure mesoderm (somite levels 26 to 35) and the ilium, but not of the pubis and ischium, depends on somitic and ectodermal signals.[7]


Links: Pelvis Development

Molecular

Fibroblast Growth Factors

  • Fgf8 - morphogen gradient forms by a source-sink mechanism with freely diffusing molecules.[8]

T-box Transcription Factors

References

  1. Anna Kicheva, James Briscoe Limbs made to measure. PLoS Biol.: 2010, 8(7);e1000421 PubMed 20644713 | PMC2903596 | PLoS
  2. Terence D Capellini, Giulia Vaccari, Elisabetta Ferretti, Sebastian Fantini, Mu He, Massimo Pellegrini, Laura Quintana, Giuseppina Di Giacomo, James Sharpe, Licia Selleri, Vincenzo Zappavigna Scapula development is governed by genetic interactions of Pbx1 with its family members and with Emx2 via their cooperative control of Alx1. Development: 2010, 137(15);2559-69 PubMed 20627960
  3. 3.0 3.1 Fawcett The Development and Ossification of the Human Clavicle. J Anat Physiol: 1913, 47(Pt 2);225-34 PubMed 17232952 | PMC1289013
  4. Julien Giordani, Lola Bajard, Josiane Demignon, Philippe Daubas, Margaret Buckingham, Pascal Maire Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs. Proc. Natl. Acad. Sci. U.S.A.: 2007, 104(27);11310-5 PubMed 17592144
  5. 5.0 5.1 Poongodi Geetha-Loganathan, Suresh Nimmagadda, Bodo Christ, Ruijin Huang, Martin Scaal Ectodermal Wnt6 is an early negative regulator of limb chondrogenesis in the chicken embryo. BMC Dev. Biol.: 2010, 10;32 PubMed 20334703
  6. Molly A McGraw, Charles T Mehlman, Christopher J Lindsell, Cassie L Kirby Postnatal growth of the clavicle: birth to 18 years of age. J Pediatr Orthop: 2009, 29(8);937-43 PubMed 19934713
  7. Yegor Malashichev, Bodo Christ, Felicitas Pröls Avian pelvis originates from lateral plate mesoderm and its development requires signals from both ectoderm and paraxial mesoderm. Cell Tissue Res.: 2008, 331(3);595-604 PubMed 18087724
  8. Shuizi Rachel Yu, Markus Burkhardt, Matthias Nowak, Jonas Ries, Zdenek Petrásek, Steffen Scholpp, Petra Schwille, Michael Brand Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature: 2009, 461(7263);533-6 PubMed 19741606


Reviews

Ruijin Huang, Bodo Christ, Ketan Patel Regulation of scapula development. Anat. Embryol.: 2006, 211 Suppl 1;65-71 PubMed 17006658

B K Hall Development of the clavicles in birds and mammals. J. Exp. Zool.: 2001, 289(3);153-61 PubMed 11170011

M Klima Early development of the shoulder girdle and sternum in marsupials (Mammalia: Metatheria). Adv Anat Embryol Cell Biol: 1987, 109;1-91 PubMed 3324657


Articles

Guido Currarino, John A Herring Congenital pseudarthrosis of the clavicle. Pediatr Radiol: 2009, 39(12);1343-9 PubMed 19763557

K F Kreitner, F Schweden, H H Schild, T Riepert, B Nafe [Computerized tomography of the epiphyseal union of the medial clavicle: an auxiliary method of age determination during adolescence and the 3d decade of life?]. [Die computertomographisch bestimmte Ausreifung der medialen Klavikulaepiphyse--eine additive Methode zur Altersbestimmung im Adoleszentenalter und in der dritten Lebensdekade?] Rofo: 1997, 166(6);481-6 PubMed 9272998

J A Ogden, G J Conlogue, M L Bronson Radiology of postnatal skeletal development. III. The clavicle. Skeletal Radiol.: 1979, 4(4);196-203 PubMed 531584


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Search Pubmed: Shoulder Development | Clavicle Development | Scapula Development

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Cite this page: Hill, M.A. 2017 Embryology Musculoskeletal System - Shoulder Development. Retrieved October 24, 2017, from https://embryology.med.unsw.edu.au/embryology/index.php/Musculoskeletal_System_-_Shoulder_Development

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