Peristalsis of airway smooth muscle is developmentally regulated and uncoupled from hypoplastic lung growth

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 291, Issue 4, 2006, Pages

  Jesudason, E C ^a,b   Smith, N P ^a   Connell, M G ^a   Spiller, D G ^a   White, M R H ^a   Fernig, D G ^a   Losty, P D ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b ALDER HEY CHILDREN S HOSPITAL   (United Kingdom)

Author keywords

Congenital diaphragmatic hernia; Lung branching morphogenesis

Indexed keywords

FIBROBLAST GROWTH FACTOR 10; NICOTINE; NIFEDIPINE; UO 126;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING MUSCLE; CONTROLLED STUDY; DIAPHRAGM HERNIA; FEMALE; FETUS LUNG MATURATION; GESTATIONAL AGE; LUNG HYPOPLASIA; NONHUMAN; PERISTALSIS; PRIORITY JOURNAL; SMOOTH MUSCLE; TISSUE GROWTH;

ANIMALS; EMBRYO; EMBRYONIC DEVELOPMENT; FEMALE; FIBROBLAST GROWTH FACTOR 10; HERNIA, DIAPHRAGMATIC; LUNG; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE, SMOOTH; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY SYSTEM; RESPIRATORY SYSTEM ABNORMALITIES;

EID: 33749356699     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00498.2005     Document Type: Article

References (38)

1. Acosta JM, Thebaud B, Castillo C, Mailleux A, Tefft D, Wuenschell C, Anderson KD, Bourbon J, Thiery JP, Bellusci S, and Warburton D. Novel mechanisms in murine nitrofen-induced pulmonary hypoplasia: FGF-10 rescue in culture. Am J Physiol Lung Cell Mol Physiol 281: L250-L257, 2001.
2. Alescio T. The effect of the mesenchyme on epithelial morphogenesis in the in vitro development of mouse embryonal lung. Arch Ital Anat Embriol 73: 295-319, 1968.
3. Belik J, Davidge ST, Zhang W, Pan J, and Greer JJ. Airway smooth muscle changes in the nitrofen-induced congenital diaphragmatic hernia rat model. Pediatr Res 53: 737-743, 2003.
4. Bellusci S, Grindley J, Emoto H, Itoh N, and Hogan BL. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124: 4867-4878, 1997.
5. Brusasco V and Pellegrino R. Complexity of factors modulating airway narrowing in vivo: relevance to assessment of airway hyperresponsiveness. J Appl Physiol 95: 1305-1313, 2003.
6. Cilley RE, Zgleszewski SE, Krummel TM, and Chinoy MR. Nitrofen dose-dependent gestational day-specific murine lung hypoplasia and left-sided diaphragmatic hernia. Am J Physiol Lung Cell Mol Physiol 272: L362-L371, 1997.
7. Coleman C, Zhao J, Gupta M, Buckley S, Tefft JD, Wuenschell CW, Minoo P, Anderson KD, and Warburton D. Inhibition of vascular and epithelial differentiation in murine nitrofen-induced diaphragmatic hernia. Am J Physiol Lung Cell Mol Physiol 274: L636-L646, 1998.
8. Featherstone NC, Jesudason EC, Connell MG, Fernig DG, Wray S, Losty PD, and Burdyga TV. Spontaneous propagating calcium waves underpin airway peristalsis in embryonic rat lung. Am J Respir Cell Mol Biol 33: 153-160, 2005.
9. Guilbert TW, Gebb SA, and Shannon JM. Lung hypoplasia in the nitrofen model of congenital diaphragmatic hernia occurs early in development. Am J Physiol Lung Cell Mol Physiol 279: L1159-L1171, 2000.
10. Harding R and Hooper SB. Regulation of lung expansion and lung growth before birth. J Appl Physiol 81: 209-224, 1996.
11. Holgate ST, Lackie PM, Howarth PH, Roche WR, Puddicombe SM, Richter A, Wilson SJ, Holloway JW, and Davies DE. Invited lecture: activation of the epithelial mesenchymal trophic unit in the pathogenesis of asthma. Int Arch Allergy Immunol 124: 253-258, 2001.
12. Hyatt BA, Shangguan X, and Shannon JM. BMP4 modulates fibroblast growth factor-mediated induction of proximal and distal lung differentiation in mouse embryonic tracheal epithelium in mesenchyme-free culture. Dev Dyn 225: 153-165, 2002.
13. Hyatt BA, Shangguan X, and Shannon JM. FGF-10 induces SP-C and Bmp4 and regulates proximal-distal patterning in embryonic tracheal epithelium. Am J Physiol Lung Cell Mol Physiol 287: L1116-L1126, 2004.
14. Ingber DE. Mechanical control of tissue growth: function follows form. Proc Natl Acad Sci USA 102: 11571-11572, 2005.
15. Jesudason EC. Small lungs and suspect smooth muscle: congenital diaphragmatic hernia and the smooth muscle hypothesis. J Pediatr Surg 41: 431-435, 2006.
16. Jesudason EC, Connell MG, Fernig DG, Lloyd DA, and Losty PD. Early lung malformations in congenital diaphragmatic hernia. J Pediatr Surg 35: 124-127, 2000.
17. Jesudason EC, Smith NP, Connell MG, Spiller DG, White MR, Fernig DG, and Losty PD. Developing rat lung has a sided pacemaker region for morphogenesis-related airway peristalsis. Am J Respir Cell Mol Biol 32: 118-127, 2005.
18. Kluth D, Kangah R, Reich P, Tenbrinck R, Tibboel D, and Lambrecht W. Nitrofen-induced diaphragmatic hernias in rats: an animal model. J Pediatr Surg 25: 850-854, 1990.
19. Kluth D, Tenbrinck R, von Ekesparre M, Kangah R, Reich P, Brandsma A, Tibboel D, and Lambrecht W. The natural history of congenital diaphragmatic hernia and pulmonary hypoplasia in the embryo. J Pediatr Surg 28: 456-462; discussion 462-453, 1993.
20. Leinwand MJ, Tefft JD, Zhao J, Coleman C, Anderson KD, and Warburton D. Nitrofen inhibition of pulmonary growth and development occurs in the early embryonic mouse. J Pediatr Surg 37: 1263-1268, 2002.
21. Lewis M. Spontaneous rhythmical contraction of the muscles of the bronchial tubes and air sacs of the chick embryo. Am J Physiol 68: 385-388, 1924.
22. Liu M, Tanswell AK, and Post M. Mechanical force-induced signal transduction in lung cells. Am J Physiol Lung Cell Mol Physiol 277: L667-L683, 1999.
23. Mailleux AA, Kelly R, Veltmaat JM, De Langhe SP, Zaffran S, Thiery JP, and Bellusci S. Fgf10 expression identifies parabronchial smooth muscle cell progenitors and is required for their entry into the smooth muscle cell lineage. Development 132: 2157-2166, 2005.
24. Mitzner W. Airway smooth muscle: the appendix of the lung. Am J Respir Crit Care Med 169: 787-790, 2004.
25. Moore KA, Polte T, Huang S, Shi B, Alsberg E, Sunday ME, and Ingber DE. Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn 232: 268-281, 2005.
26. Nakamura KT and McCray PB Jr. Fetal airway smooth-muscle contractility and lung development. A player in the band or just someone in the audience? Am J Respir Cell Mol Biol 23: 3-6, 2000.
27. Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, Spector AA, and Chen CS. Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci USA 102: 11594-11599, 2005.
28. Sakurai Y, Azarow K, Cutz E, Messineo A, Pearl R, and Bohn D. Pulmonary barotrauma in congenital diaphragmatic hernia: a clinicopathological correlation. J Pediatr Surg 34: 1813-1817, 1999.
29. Schittny JC, Miserocchi G, and Sparrow MP. Spontaneous peristaltic airway contractions propel lung liquid through the bronchial tree of intact and fetal lung explants. Am J Respir Cell Mol Biol 23: 11-18, 2000.
30. Schopper W. Embryonales underwachsenes Lungengewebe vom Meerschweinchen und Huhn in der Kultur mit Zeitrafferbeobachtungen an Flimmerepithel, sog. Alveolarphagocyten und von Kontraktionen der Bronchialmuskulatur. Virchows Arch 295: 623-644, 1935.
31. Schopper W. Uber das Verhalten des Lungengewebes in der Gewebekultur (Filmdemonstration). Arch Exptl Zellforsch 19: 326-328, 1937.
32. Seow CY and Fredberg JJ. Historical perspective on airway smooth muscle: the saga of a frustrated cell. J Appl Physiol 91: 938-952, 2001.
33. Skousgaard SG. Severe bronchial hyperreactivity as a sequel to congenital diaphragmatic hernia. Paediatr Anaesth 8: 503-505, 1998.
34. Smith NP, Jesudason EC, Featherstone NC, Corbett HJ, and Losty PD. Recent advances in congenital diaphragmatic hernia. Arch Dis Child 90: 426-428, 2005.
35. Sparrow MP and Lamb JP. Ontogeny of airway smooth muscle: structure, innervation, myogenesis and function in the fetal lung. Respir Physiol Neurobiol 137: 361-372, 2003.
36. Takayanagi I, Kizawa Y, and Sone H. Action of nicotine on guinea-pig isolated bronchial smooth muscle preparation. Gen Pharmacol 15: 349-352, 1984.
37. Vanamo K, Rintala R, Sovijarvi A, Jaaskelainen J, Turpeinen M, Lindahl H, and Louhimo I. Long-term pulmonary sequelae in survivors of congenital diaphragmatic defects. J Pediatr Surg 31: 1096-1099; discussion 1099-1100, 1996.
38. Yang Y, Beqaj S, Kemp P, Ariel I, and Schuger L. Stretch-induced alternative splicing of serum response factor promotes bronchial myogenesis and is defective in lung hypoplasia. J Clin Invest 106: 1321-1330, 2000.