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Paraxial and Intermediate Mesoderm

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Paraxial and Intermediate Mesoderm 12 Paraxial and Intermediate Mesoderm CHAPTERS 10 AND 11 FOLLOWED THE FORMATION of various tissues from the ver- Of physiology from top to tebrate ectoderm. In this chapter and the next, we will follow the development of the toe I sing, mesodermal and endodermal germ layers. We will see that the endoderm forms the epithelial cell lining of the digestive and respiratory tubes, with their associated organs. Not physiognomy alone or The mesoderm generates almost all of the organs between the ectodermal wall and the brain alone endodermal tissues. These include the musculoskeletal tissues, the cardiovascular tis- is worthy for the Muse, sues, and the urogenital tissues, as well as the mesenchymal cells that associate with the I say the form complete is ectodermal and endodermal epithelia, helping them to form their own tissues. The trunk mesoderm of a neurula-stage embryo can be subdivided into four regions worthier far, (FIGURE 12.1A): The Female equally with 1. The central region of trunk mesoderm is the chordamesoderm. This tissue forms the Male I sing. the notochord, a transient organ whose major functions include inducing and pat- WT AL WHITMAN (1867) terning the neural tube and establishing the anterior-posterior body axis. The for- mation of the notochord on the future dorsal side of the embryo was discussed in Built of 206 bones, the Chapters 8 and 9. skeleton is a living cathe- 2. Flanking the notochord on both sides is the paraxial, or somitic, mesoderm. The dral of ivory vaults, ribs, tissues developing from this region will be located in the back of the embryo, sur- rounding the spinal cord. The cells in this region will form somites—blocks of and buttresses—a struc- mesodermal cells on either side of the neural tube—which will produce muscle and ture at once light and many of the connective tissues of the back (dermis, muscle, and skeletal elements strong. such as the vertebrae and ribs). The anteriormost paraxial mesoderm does not seg- NAI TAL E ANGIER (1994) ment; it becomes the head mesoderm, which (along with the neural crest) forms the skeleton, muscles, and connective tissue of the face and skull. 3. The intermediate mesoderm forms the urogenital system, consisting of the kid- neys, the gonads, and their associated ducts. The outer (cortical) portion of the adrenal gland also derives from this region. 4. Farthest away from the notochord, the lateral plate mesoderm gives rise to the heart, blood vessels, and blood cells of the circulatory system, as well as to the lin- ing of the body cavities. It gives rise to the pelvic and limb skeleton (but not the limb muscles, which are somitic in origin). Lateral plate mesoderm also helps form a series of extraembryonic membranes that are important for transporting nutrients to the embryo. These four subdivisions are thought to be specified along the mediolateral (center-to-side) axis by increasing amounts of BMPs (Pourquié et al. 1996; Tonegawa et al. 1997). The more lateral mesoderm of the chick embryo expresses higher levels of BMP4 than do the midline areas, and one can change the identity of the mesodermal tissue by altering BMP expres- sion. While it is not known how this patterning is accomplished, it is thought that the dif- ferent BMP concentrations may cause differential expression of the Forkhead (Fox) family of transcription factors. Foxf1 is transcribed in those regions that will become the lateral uncorrected page proofs © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 416 Chapter 12 (A) (B) Neural tube Paraxial Intermediate Chorda- (somitic) Lateral plate mesoderm mesoderm mesoderm mesoderm Notochord Splanchnic Somatic Extra- (circulatory (body cavity, embryonic Kidney Gonads Head Somite system) pelvis, limb bones) Sclerotome Myotome Dermatome (cartilage) (skeletal (dermis, skeletal muscle) muscle) Syndotome Endothelial FIGURE 12.1 Major lineages of the amniote mesoderm. (A) Sche- (tendons) cells matic of the mesodermal compartments of the amniote embryo. (B) Staining for the medial mesodermal compartments in the trunk of a 12-somite chick embryo (about 33 hours). In situ hybridization plate and extraembryonic mesoderm, whereas Foxc1 and Foxc2 was performed with probes binding to Chordin mRNA (blue) in the notochord, Paraxis mRNA (green) in the somites, and Pax2 mRNA are expressed in the paraxial mesoderm that will form the (red) in the intermediate mesoderm. (B from Denkers et al. 2004, somites (Wilm et al. 2004). If Foxc1 and Foxc2 are both deleted courtesy of T. J. Mauch.) from the mouse genome, the paraxial mesoderm is respecified as intermediate mesoderm and initiates the expression of Pax2, which encodes a major transcription factor of the intermediate These bands of paraxial mesoderm are referred to as the pre- mesoderm (FIGURE 12.1B). somitic mesoderm. As the primitive streak regresses and the Anterior to the trunk mesoderm is a fifth mesodermal neural folds begin to gather at the center of the embryo, the region, the head mesoderm, consisting of the unsegmented cells of the presomitic mesoderm will form somites. paraxial mesoderm and prechordal mesoderm. This region The paraxial mesoderm appears to be specified by the provides the head mesenchyme that forms much of the con- antagonism of BMP signaling by the Noggin protein. Nog- nective tissues and musculature of the head (Evans and gin is usually synthesized by the early presomitic mesoderm, GilbertNoden 2006). The muscles derived from the head mesoderm and if Noggin-expressing cells are placed into presumptive Developmentalform differently Biology than 10e, Sinauerthose formedAssociates from the somites. Not lateral plate mesoderm, the lateral plate tissue will be respeci- GIL10e_12.01 Date 04-02-13 only do they have their own set of transcription factors, but fied into somite-forming paraxial mesoderm (FIGURE 12.3; the head and trunk muscles are affected by different types of Tonegawa and Takahashi 1998; Gerhart et al. 2011). muscular dystrophies (Emery 2002; Bothe and Dietrich 2006; Mature somites contain three major compartments: the Harel et al. 2009). sclerotome, which forms the vertebrae and rib cartilage; the myotome, which forms the musculature of the back, rib cage, and ventral body wall; and the dermamyotome, which also PARAXIAL MESODERM: THE contains skeletal muscle progenitor cells (including muscle SOMITES AND THEIR DERIVATIVES progenitors that migrate into the limbs), as well as the cells that generate the dermis of the back. Additional, smaller One of the major tasks of gastrulation is to create a mesoder- compartments are formed from these three. The syndetome mal layer between the endoderm and the ectoderm. As seen arising from the most dorsal sclerotome cells generates the in FIGURE 12.2, the formation of mesodermal and endoder- tendons, while the most internal cells of the sclerotome mal tissues is not subsequent to neural tube formation but (sometimes called the arthrotome) become the vertebral joints, occurs synchronously. The notochord extends beneath the the outer portion of the intervertebral discs, and the proximal neural tube, from the base of the head into the tail. On either portion of the ribs (Mittapalli et al. 2005; Christ et al. 2007). side of the neural tube lie thick bands of mesodermal cells. Moreover, an as-yet unnamed group of cells in the posterior uncorrected page proofs © 2013 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. Paraxial and Intermediate Mesoderm 417 (A) Primitive streak Epiblast FIGURE 12.2 Gastrulation and neurulation in the chick embryo, focus- ing on the mesodermal component. Endoderm Migrating mesodermal cells (A) Primitive streak region, showing migrating mesodermal and endodermal (B) Epidermis Neural plate precursors. (B) Formation of the noto- chord and paraxial mesoderm. (C,D) Differentiation of the somites, coelom, and the two aortae (which will eventu- Endoderm Paraxial mesoderm Notochord Lateral mesoderm ally fuse). A–C, 24-hour embryos; D, 48-hour embryo. (C) Neural tube Somatic mesoderm Splanchnic Epidermis mesoderm Intermediate mesoderm Somite Coelom (D) Sclerotome of somite Myotome Dermatome of somite of somite Notochord Intraembryonic coelom Extraembryonic coelom Dorsal aortae sclerotome generates vascular cells of the dorsal aorta and intervertebral blood vessels (T ablE 12.1; Pardanaud et al. 1996; Sato et al. 2008; Ohata et al. 2009). ●● See VADE MECUM Mesoderm in the vertebrate embryo Gilbert Formation of the Somites Developmental Biology 10e, Sinauer Associates The important components of somite formation, or somito- GIL10e_12.02 Date 04-02-13 genesis, are (1) fissure formation (separation of the somites), (2) periodicity, (3) epithelialization, (4) specification, and (5) differentiation. The first somites appear in the anterior por- tion of the trunk, and new somites “bud off” from the rostral end of the presomitic mesoderm at regular intervals (FIG- URE 12.4). The anterior mesoderm arises from cells that have migrated through the primitive streak. The posterior of amni- ote embryos (as we saw in Chapter 10) contains a precursor population whose cells become either central neural tube (Sox2-expressing) or paraxial mesoderm (Tbx6-expressing). The nascent paraxial mesoderm cells are released from this FIGURE 12.3 Specification of somites. Placing Noggin-secreting cells into a prospective
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