Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion

TY - JOUR

T1 - Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion

AU - Minchin, James E. N.

AU - Williams, Victoria C.

AU - Hinits, Yaniv

AU - Low, SiewHui

AU - Tandon, Panna

AU - Fan, Chen-Ming

AU - Rawls, John F.

AU - Hughes, Simon M.

PY - 2013/7/15

Y1 - 2013/7/15

N2 - Striated muscles that enable mouth opening and swallowing during feeding are essential for efficient energy acquisition, and are likely to have played a fundamental role in the success of early jawed vertebrates. The developmental origins and genetic requirements of these muscles are uncertain. Here, we determine by indelible lineage tracing in mouse that fibres of sternohyoid muscle (SHM), which is essential for mouth opening during feeding, and oesophageal striated muscle (OSM), which is crucial for voluntary swallowing, arise from Pax3-expressing somite cells. In vivo Kaede lineage tracing in zebrafish reveals the migratory route of cells from the anteriormost somites to OSM and SHM destinations. Expression of pax3b, a zebrafish duplicate of Pax3, is restricted to the hypaxial region of anterior somites that generate migratory muscle precursors (MMPs), suggesting that Pax3b plays a role in generating OSM and SHM. Indeed, loss of pax3b function led to defective MMP migration and OSM formation, disorganised SHM differentiation, and inefficient ingestion and swallowing of microspheres. Together, our data demonstrate Pax3-expressing somite cells as a source of OSM and SHM fibres, and highlight a conserved role of Pax3 genes in the genesis of these feeding muscles of vertebrates.

AB - Striated muscles that enable mouth opening and swallowing during feeding are essential for efficient energy acquisition, and are likely to have played a fundamental role in the success of early jawed vertebrates. The developmental origins and genetic requirements of these muscles are uncertain. Here, we determine by indelible lineage tracing in mouse that fibres of sternohyoid muscle (SHM), which is essential for mouth opening during feeding, and oesophageal striated muscle (OSM), which is crucial for voluntary swallowing, arise from Pax3-expressing somite cells. In vivo Kaede lineage tracing in zebrafish reveals the migratory route of cells from the anteriormost somites to OSM and SHM destinations. Expression of pax3b, a zebrafish duplicate of Pax3, is restricted to the hypaxial region of anterior somites that generate migratory muscle precursors (MMPs), suggesting that Pax3b plays a role in generating OSM and SHM. Indeed, loss of pax3b function led to defective MMP migration and OSM formation, disorganised SHM differentiation, and inefficient ingestion and swallowing of microspheres. Together, our data demonstrate Pax3-expressing somite cells as a source of OSM and SHM fibres, and highlight a conserved role of Pax3 genes in the genesis of these feeding muscles of vertebrates.

KW - Hypaxial muscle

KW - Zebrafish

KW - Mouse

KW - Pax3

KW - In vivo lineage tracing

KW - MYOGENIC PRECURSOR CELLS

KW - ZEBRAFISH DANIO-RERIO

KW - WHITE ADIPOSE-TISSUE

KW - C-MET RECEPTOR

KW - SKELETAL-MUSCLE

KW - NEURAL CREST

KW - DIGESTIVE-TRACT

KW - MOUSE ESOPHAGUS

KW - ULTRASTRUCTURAL ANALYSIS

KW - HYPAXIAL MUSCULATURE

U2 - 10.1242/dev.090050

DO - 10.1242/dev.090050

M3 - Article

SN - 0950-1991

VL - 140

SP - 2972

EP - 2984

JO - Development

JF - Development

IS - 14

ER -