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Published online 9 August 2004. doi:10.1083/jcb.200402054
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 166, Number 4, 591-600
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Article

 Esophageal muscle physiology and morphogenesis require assembly of a collagen XIX–rich basement membrane zone

Hideaki Sumiyoshi1,2, Niv Mor1, Sui Y. Lee1, Stephen Doty1, Scott Henderson3, Shizuko Tanaka1, Hidekatsu Yoshioka2, Satish Rattan4, and Francesco Ramirez1

1 Research Division of the Hospital for Special Surgery and Department of Physiology and Biophysics at the Weill College of Medicine of Cornell University, New York, NY 10019
2 Department of Anatomy, Biology, and Medicine, Oita Medical University, Oita 879-5593, Japan
3 Department of Molecular, Cellular, and Developmental Biology, Mount Sinai School of Medicine, New York, NY 10029
4 Department of Medicine, Jefferson Medical College of Thomas Jefferson University, Philadelphia, PA 19107

Address correspondence to Francesco Ramirez, Laboratory of Genetics and Organogenesis, Hospital for Special Surgery at the Weill College of Medicine of Cornell University, 535 East 70th St., New York, NY 10021. Tel.: (212) 7874-7554. Fax: (212) 774-7864. email: ramirezf{at}hss.edu

Collagen XIX is an extremely rare extracellular matrix component that localizes to basement membrane zones and is transiently expressed by differentiating muscle cells. Characterization of mice harboring null and structural mutations of the collagen XIX (Col19a1) gene has revealed the critical contribution of this matrix protein to muscle physiology and differentiation. The phenotype includes smooth muscle motor dysfunction and hypertensive sphincter resulting from impaired swallowing-induced, nitric oxide–dependent relaxation of the sphincteric muscle. Muscle dysfunction was correlated with a disorganized matrix and a normal complement of enteric neurons and interstitial cells of Cajal. Mice without collagen XIX exhibit an additional defect, namely impaired smooth-to-skeletal muscle cell conversion in the abdominal segment of the esophagus. This developmental abnormality was accounted for by failed activation of myogenic regulatory factors that normally drive esophageal muscle transdifferentiation. Therefore, these findings identify collagen XIX as the first structural determinant of sphincteric muscle function, and as the first extrinsic factor of skeletal myogenesis in the murine esophagus.

Key Words: achalasia; basement membrane; collagen; muscle transdifferentiation; nitrergic neurotransmission

Abbreviations used in this paper: BM, basement membrane; EFS, electrical field stimulation; ES, embryonic stem; ICC-IM, intramuscular interstitial cells of Cajal; LES, lower esophageal sphincter; MRF, myogenic regulatory factor; NANC, nonadrenergic noncholinergic; NC, noncollagenous; NO, nitric oxide; NOS, nitric oxide synthase; SMC, smooth muscle cell.


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