Connecting muscle development, birth defects, and evolution: An essential role for muscle connective tissue

Abstract

Skeletal muscle powers all movement of the vertebrate body and is distributed in multiple regions that have evolved distinct functions. Axial muscles are ancestral muscles essential for support and locomotion of the whole body. The evolution of the head was accompanied by development of cranial muscles essential for eye movement, feeding, vocalization, and facial expression. With the evolution of paired fins and limbs and their associated muscles, vertebrates gained increased locomotor agility, populated the land, and acquired fine motor skills. Finally, unique muscles with specialized functions have evolved in some groups, and the diaphragm which solely evolved in mammals to increase respiratory capacity is one such example. The function of all these muscles requires their integration with the other components of the musculoskeletal system: muscle connective tissue (MCT), tendons, bones as well as nerves and vasculature. MCT is muscle’s closest anatomical and functional partner. Not only is MCT critical in the adult for muscle structure and function, but recently MCT in the embryo has been found to be crucial for muscle development. In this review, we examine the important role of the MCT in axial, head, limb, and diaphragm muscles for regulating normal muscle development, discuss how defects in MCT-muscle interactions during development underlie the etiology of a range of birth defects, and explore how changes in MCT development or communication with muscle may have led to the modification and acquisition of new muscles during vertebrate evolution.

Skeletal Muscle Extracellular Matrix – What Do We Know About Its Composition, Regulation, and Physiological Roles? A Narrative Review

“…Recent research has provided evidence that, in addition to these obvious roles, IMCT fibroblasts and the connective tissues produced by them influence both myogenesis (i.e., the formation of muscle progenitors and their differentiation into multinucleate myofibers) and muscle morphogenesis (i.e., the process in which myofibers are assembled into muscles), thus acting as important regulators of muscle development. These complex regulatory processes occurring during embryogenic development are not covered in detail here, but have been extensively reviewed elsewhere (Nassari et al, 2017;Sefton and Kardon, 2019). In brief, the IMCT guides muscle progenitors to their designated target regions, through a combination of attractive (Hepatocyte Growth Factor, Stromal Cell-Derived Factor) and repulsive signals (Ephrin) (Dietrich et al, 1999;Swartz et al, 2001).…”

Transient and lineage-restricted requirement of Ebf3 for sternum ossification

“…However, skeletal muscle tissues are complex because different types of MCT cells intercalate into muscle fibers, and these MCT cell lineages are heterogeneous (Giordani et al, 2019). Recent studies on skeletal myogenesis have focused on MCT cells, which play crucial roles in muscle development and maintenance (Sefton and Kardon, 2019). Skeletal muscle cells should colonize a region near the skeletogenic cell components, including osteogenic and chondrogenic cells together with tenocytes and MCT cells, to build the functional locomotorium during development.…”

Local retinoic acid signaling directs emergence of the extraocular muscle functional unit

“…In all body regions, muscle connective tissue plays a central role in muscle patterning [22]. Moreover, this process appears to be tightly coupled to development of tendons and tendon attachment sites [15,[70][71][72].…”

“…Much of our understanding of musculosketal development and integration into functional units comes from studies in the limb. Lateral plate mesoderm-derived muscle connective tissue cells and tendon primordia establish a pre-pattern that determines the sites of myogenic differentiation and participate in spliting of the muscle masses in the limb [20][21][22]. Tendons connect muscles to the skeleton and are formed by scleraxis (Scx)-expressing mesenchymal progenitors [23,24].…”