About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 101597, 15 pages
http://dx.doi.org/10.1155/2013/101597
Review Article

Development and Remodeling of the Vertebrate Blood-Gas Barrier

1Institute of Anatomy, University of Bern, Baltzerstrasse 2, 3000 Berne, Switzerland
2Department of Veterinary Anatomy & Physiology, University of Nairobi, Riverside Drive, P.O. Box 30197, Nairobi 00100, Kenya

Received 17 August 2012; Accepted 24 November 2012

Academic Editor: Richard Tucker

Copyright © 2013 Andrew Makanya et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. B. West, “Invited review: pulmonary capillary stress failure,” Journal of Applied Physiology, vol. 89, no. 6, pp. 2483–2489, 2000. View at Scopus
  2. J. B. West, “Comparative physiology of the pulmonary blood-gas barrier: the unique avian solution,” American Journal of Physiology, vol. 297, no. 6, pp. R1625–R1634, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. P. H. Burri, “Structural aspects of postnatal lung development—alveolar formation and growth,” Biology of the Neonate, vol. 89, no. 4, pp. 313–322, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. J. N. Maina, G. M. O. Maloiy, and A. N. Makanya, “Morphology and morphometry of the lungs of two East African mole rats, Tachyoryctes splendens and Heterocephalus glaber (Mammalia, Rodentia),” Zoomorphology, vol. 112, no. 3, pp. 167–179, 1992. View at Publisher · View at Google Scholar · View at Scopus
  5. J. N. Maina, “Structure, function and evolution of the gas exchangers: comparative perspectives,” Journal of Anatomy, vol. 201, no. 4, pp. 281–304, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. P. H. Burri, “Fetal and postnatal development of the lung,” Annual Review of Physiology, vol. 46, pp. 617–628, 1984. View at Scopus
  7. D. Warburton, S. Bellusci, S. De Langhe et al., “Molecular mechanisms of early lung specification and branching morphogenesis,” Pediatric Research, vol. 57, no. 5, part 2, pp. 26R–37R, 2005. View at Scopus
  8. R. Bellairs and M. Osmond, The Atlas of Chick Development, Academic Press, New York, NY, USA, 1998.
  9. A. N. Makanya and V. Djonov, “Development and spatial organization of the air conduits in the lung of the domestic fowl, gallus Gallus variant domesticus,” Microscopy Research and Technique, vol. 71, no. 9, pp. 689–702, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. J. I. Sakiyama, A. Yamagishi, and A. Kuroiwa, “Tbx4-Fgf10 system controls lung bud formation during chicken embryonic development,” Development, vol. 130, no. 7, pp. 1225–1234, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. A. N. Makanya, S. A. Tschanz, B. Haenni, and P. H. Burri, “Functional respiratory morphology in the newborn quokka wallaby (Setonix brachyurus),” Journal of Anatomy, vol. 211, no. 1, pp. 26–36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. A. N. Makanya, M. P. Sparrow, C. N. Warui, D. K. Mwangi, and P. H. Burri, “Morphological analysis of the postnatally developing marsupial lung: the quokka wallaby,” The Anatomical Record, vol. 262, no. 3, pp. 253–265, 2001.
  13. P. H. Burri, B. Haenni, S. A. Tschanz, and A. N. Makanya, “Morphometry and allometry of the postnatal marsupial lung development: an ultrastructural study,” Respiratory Physiology and Neurobiology, vol. 138, no. 2-3, pp. 309–324, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. R. R. Watson, Z. Fu, and J. B. West, “Morphometry of the extremely thin pulmonary blood-gas barrier in the chicken lung,” American Journal of Physiology, vol. 292, no. 3, pp. L769–L777, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. A. N. Makanya, R. Hlushchuk, and V. Djonov, “The pulmonary blood-gas barrier in the avian embryo: inauguration, development and refinement,” Respiratory Physiology and Neurobiology, vol. 178, no. 1, pp. 30–38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Gehr, M. Bachofen, and E. R. Weibel, “The normal human lung: ultrastructure and morphometric estimation of diffusion capacity,” Respiration Physiology, vol. 32, no. 2, pp. 121–140, 1978. View at Scopus
  17. E. R. Weibel, The Pathway for Oxygen, Havard University Press, Cambridge, Mass, USA, 1984.
  18. E. K. Birks, O. Mathieu-Costello, Z. Fu, W. S. Tyler, and J. B. West, “Comparative aspects of the strength of pulmonary capillaries in rabbit, dog, and horse,” Respiration Physiology, vol. 97, no. 2, pp. 235–246, 1994. View at Publisher · View at Google Scholar · View at Scopus
  19. J. B. West and O. Mathieu-Costello, “Structure, strength, failure, and remodeling of the pulmonary blood-gas barrier,” Annual Review of Physiology, vol. 61, pp. 543–572, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. M. N. Fernandes, A. L. da Cruz, O. T. da Costa, and S. F. Perry, “Morphometric partitioning of the respiratory surface area and diffusion capacity of the gills and swim bladder in juvenile Amazonian air-breathing fish, Arapaima gigas,” Micron, vol. 43, no. 9, pp. 961–970, 2012.
  21. C. Meban, “Thickness of the air-blood barriers in vertebrate lungs,” Journal of Anatomy, vol. 131, part 2, pp. 299–307, 1980. View at Scopus
  22. S. F. Perry, “Gas exchange strategy in the Nile crocodile: a morphometric study,” Journal of Comparative Physiology B, vol. 159, no. 6, pp. 761–769, 1990. View at Scopus
  23. J. N. Maina, S. P. Thomas, and D. M. Hyde, “A morphometric study of the lungs of different sized bats: correlations between structure and function of the chiropteran lung,” Philosophical transactions of the Royal Society of London B, vol. 333, no. 1266, pp. 31–50, 1991. View at Scopus
  24. W. G. Henk and J. T. Haldiman, “Microanatomy of the lung of the bowhead whale Balaena mysticetus,” Anatomical Record, vol. 226, no. 2, pp. 187–197, 1990. View at Scopus
  25. J. N. Maina and C. Nathaniel, “A qualitative and quantitative study of the lung of an ostrich, Struthio camelus,” Journal of Experimental Biology, vol. 204, part 13, pp. 2313–2330, 2001. View at Scopus
  26. J. N. Maina and A. S. King, “A morphometric study of the lung of a Humboldt penguin (Sphenicus humboldti),” Anatomia, Histologia, Embryologia, vol. 16, no. 4, pp. 293–297, 1987. View at Scopus
  27. J. N. Maina and A. S. King, “The lung of the emu, Dromaius novaehollandiae: a microscopic and morphometric study,” Journal of anatomy, vol. 163, pp. 67–73, 1989. View at Scopus
  28. J. C. Schittny and P. H. Burri, “Morphogenesis of the mammalian lung: aspects of structure and extracellular matrix,” in Lung Development and Regeneration, J. D. Massaro, G. Massaro, and P. Chambon, Eds., pp. 275–317, Mercel Dekker, New York, NY, USA, 2003.
  29. A. R. Mercurio and J. A. G. Rhodin, “An electron microscopic study on the type I pneumocyte in the cat: pre-natal morphogenesis,” Journal of Morphology, vol. 156, no. 2, pp. 141–155, 1978. View at Scopus
  30. P. H. Burri and E. R. Weibel, “Ultrastructure and morphometry of the developing lung,” in Development of the Lung, W. A. Hudson, Ed., pp. 215–268, Mercwel dekker, New York, NY, USA, 1977.
  31. J. C. Schittny, V. Djonov, A. Fine, and P. H. Burri, “Programmed cell death contributes to postnatal lung development,” American Journal of Respiratory Cell and Molecular Biology, vol. 18, no. 6, pp. 786–793, 1998. View at Scopus
  32. J. N. Maina and J. B. West, “Thin and strong! The bioengineering dilemma in the structural and functional design of the blood-gas barrier,” Physiological Reviews, vol. 85, no. 3, pp. 811–844, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Anderson-Berry, E. A. O'Brien, S. B. Bleyl et al., “Vasculogenesis drives pulmonary vascular growth in the developing chick embryo,” Developmental Dynamics, vol. 233, no. 1, pp. 145–153, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. A. N. Makanya, R. Hlushchuk, O. Baum, N. Velinov, M. Ochs, and V. Djonov, “Microvascular endowment in the developing chicken embryo lung,” American Journal of Physiology, vol. 292, no. 5, pp. L1136–L1146, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. N. Makanya and V. G. Djonov, “Parabronchial angioarchitecture in developing and adult chickens,” Journal of Applied Physiology, vol. 106, no. 6, pp. 1959–1969, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. A. N. Makanya, T. Koller, R. Hlushchuk, and V. Djonov, “Pre-hatch lung development in the ostrich,” Respiratory Physiology & Neurobiology, vol. 180, no. 2-3, pp. 183–192, 2012.
  37. A. N. Makanya, R. Hlushchuk, H. R. Duncker, A. Draeger, and V. Djonov, “Epithelial transformations in the establishment of the blood-gas barrier in the developing chick embryo lung,” Developmental Dynamics, vol. 235, no. 1, pp. 68–81, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. D. W. Scheuermann, E. Klika, M. H. A. De Groodt-Lasseel, I. Bazantova, and A. Switka, “The development and differentiation of the parabronchial unit in quail (Coturnix coturnix),” European Journal of Morphology, vol. 36, no. 4-5, pp. 201–215, 1998. View at Scopus
  39. J. N. Maina, “A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study on the domestic fowl, Gallus gallus variant domesticus,” Tissue and Cell, vol. 35, no. 5, pp. 375–391, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. A. P. Gesase and Y. Satoh, “Apocrine secretory mechanism: recent findings and unresolved problems,” Histology and Histopathology, vol. 18, no. 2, pp. 597–608, 2003. View at Scopus
  41. I. Deyrup-Olsen and D. L. Luchtel, “Secretion of mucous granules and other membrane-bound structures: a look beyond exocytosis,” International Review of Cytology, vol. 183, pp. 95–141, 1998. View at Scopus
  42. M. Kliewer, E. K. Fram, A. R. Brody, and S. L. Young, “Secretion of surfactant by rat alveolar type II cells: morphometric analysis and three-dimensional reconstruction,” Experimental Lung Research, vol. 9, no. 3-4, pp. 351–361, 1985. View at Scopus
  43. G. Aumüller, B. Wilhelm, and J. Seitz, “Apocrine secretion: fact or artifact?” Annals of Anatomy, vol. 181, no. 5, pp. 437–446, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Stoeckelhuber, A. Sliwa, and U. Welsch, “Histo-physiology of the scent-marking glands of the penile pad, anal pouch, and the forefoot in the aardwolf (Proteles cristatus),” The Anatomical Record, vol. 259, no. 3, pp. 312–326, 2000.
  45. M. Stoeckelhuber, B. M. Stoeckelhuber, and U. Welsch, “Human glands of Moll: histochemical and ultrastructural characterization of the glands of Moll in the human eyelid,” Journal of Investigative Dermatology, vol. 121, no. 1, pp. 28–36, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Volberg, B. Geiger, J. Kartenbeck, and W. W. Franke, “Changes in membrane-microfilament interaction in intercellular adherens junctions upon removal of extracellular Ca2+ ions,” Journal of Cell Biology, vol. 102, no. 5, pp. 1832–1842, 1986. View at Scopus
  47. D. Shook and R. Keller, “Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development,” Mechanisms of Development, vol. 120, no. 11, pp. 1351–1383, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Mačuhová, V. Tančin, and R. M. Bruckmaier, “Effects of oxytocin administration on oxytocin release and milk ejection,” Journal of Dairy Science, vol. 87, no. 5, pp. 1236–1244, 2004. View at Scopus
  49. J. B. West and O. Mathieucostello, “Pulmonary blood-gas barrier—a physiological dilemma,” News in Physiological Science, vol. 8, pp. 249–253, 1993.
  50. J. T. Berg, Z. Fu, E. C. Breen, H. C. Tran, O. Mathieu-Costello, and J. B. West, “High lung inflation increases mRNA levels of ECM components and growth factors in lung parenchyma,” Journal of Applied Physiology, vol. 83, no. 1, pp. 120–128, 1997. View at Scopus
  51. J. C. Parker, E. C. Breen, and J. B. West, “High vascular and airway pressures increase interstitial protein mRNA expression in isolated rat lungs,” Journal of Applied Physiology, vol. 83, no. 5, pp. 1697–1705, 1997. View at Scopus
  52. P. Ravikumar, D. J. Bellotto, R. L. Johnson Jr., and C. C. W. Hsia, “Permanent alveolar remodeling in canine lung induced by high-altitude residence during maturation,” Journal of Applied Physiology, vol. 107, no. 6, pp. 1911–1917, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. E. K. Birks, O. Mathieu-Costello, Z. Fu, W. S. Tyler, and J. B. West, “Very high pressures are required to cause stress failure of pulmonary capillaries in Thoroughbred racehorses,” Journal of Applied Physiology, vol. 82, no. 5, pp. 1584–1592, 1997. View at Scopus
  54. S. R. Hopkins, R. B. Schoene, W. R. Henderson, R. G. Spragg, T. R. Martin, and J. B. West, “Intense exercise impairs the integrity of the pulmonary blood-gas barrier in elite athletes,” American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 3, pp. 1090–1094, 1997. View at Scopus
  55. K. Tsukimoto, O. Mathieu-Costello, R. Prediletto, A. R. Elliott, and J. B. West, “Ultrastructural appearances of pulmonary capillaries at high transmural pressures,” Journal of Applied Physiology, vol. 71, no. 2, pp. 573–582, 1991. View at Scopus
  56. J. B. West and O. Mathieu-Costello, “Stress-induced injury of pulmonary capillaries,” Proceedings of the Association of American Physicians, vol. 110, no. 6, pp. 506–512, 1998. View at Scopus
  57. S. P. Herbert and D. Y. R. Stainier, “Molecular control of endothelial cell behaviour during blood vessel morphogenesis,” Nature Reviews Molecular Cell Biology, vol. 12, no. 9, pp. 551–564, 2011.
  58. P. Carmeliet and R. K. Jain, “Molecular mechanisms and clinical applications of angiogenesis,” Nature, vol. 473, no. 7347, pp. 298–307, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Lee, J. D. Fryer, H. Kang et al., et al., “ATXN1 protein family and CIC regulate extracellular matrix remodeling and lung alveolarization,” Developmental Cell, vol. 21, no. 4, pp. 746–757, 2011.
  60. J. N. Maina, “The morphology of the lung of the black mamba Dendroaspis polylepis (Reptilia: Ophidia: Elapidae). A scanning and transmission electron microscopic study,” Journal of Anatomy, vol. 167, pp. 31–46, 1989. View at Scopus
  61. J. N. Fleetwood and J. F. Munnell, “Morphology of the airways and lung parenchyma in hatchlings of the loggerhead sea turtle, Caretta caretta,” Journal of Morphology, vol. 227, no. 3, pp. 289–304, 1996. View at Scopus
  62. J. N. Maina, “The morphology of the lung of the East African tree frog Chiromantis petersi with observations on the skin and the buccal cavity as secondary gas exchange organs: a TEM and SEM study,” Journal of Anatomy, vol. 165, pp. 29–43, 1989.
  63. F. Demayo, P. Minoo, C. G. Plopper, L. Schuger, J. Shannon, and J. S. Torday, “Mesenchymal-epithelial interactions in lung development and repair: are modeling and remodeling the same process?” American Journal of Physiology, vol. 283, no. 3, pp. L510–L517, 2002. View at Scopus
  64. J. M. Shannon and B. A. Hyatt, “Epithelial-mesenchymal interactions in the developing lung,” Annual Review of Physiology, vol. 66, pp. 625–645, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. J. C. Schittny, G. Miserocchi, and M. P. Sparrow, “Spontaneous peristaltic airway contractions propel lung liquid through the bronchial tree of intact and fetal lung explants,” American Journal of Respiratory Cell and Molecular Biology, vol. 23, no. 1, pp. 11–18, 2000. View at Scopus
  66. J. C. Herriges, L. Yi, E. A. Hines et al., “Genome-scale study of transcription factor expression in the branching mouse lung,” Developmental Dynamics, vol. 241, no. 9, pp. 1432–1453, 2012.
  67. L. Raaberg, E. Nexo, P. E. Jorgensen, S. S. Poulsen, and M. Jakab, “Fetal effects of epidermal growth factor deficiency induced in rats by autoantibodies against epidermal growth factor,” Pediatric Research, vol. 37, no. 2, pp. 175–181, 1995. View at Scopus
  68. P. J. Miettinen, D. Warburton, D. Bu et al., “Impaired lung branching morphogenesis in the absence of functional EGF receptor,” Developmental Biology, vol. 186, no. 2, pp. 224–236, 1997. View at Publisher · View at Google Scholar · View at Scopus
  69. Z. Huang, Y. Wang, P. S. Nayak, C. E. Dammann, and J. Sanchez-Esteban, “Stretch-induced fetal type II cell differentiation is mediated via ErbB-ErbB4 interactions,” The Journal of Biological Chemistry, vol. 287, no. 22, p. 1, 2012.
  70. C. Liu, M. Ikegami, M. T. Stahlman, C. R. Dey, and J. A. Whitsett, “Inhibition of alveolarization and altered pulmonary mechanics in mice expressing GATA-6,” American Journal of Physiology, vol. 285, no. 6, pp. L1246–L1254, 2003. View at Scopus
  71. S. Bellusci, R. Henderson, G. Winnier, T. Oikawa, and B. L. M. Hogan, “Evidence from normal expression and targeted misexpression that Bone Morphogenetic Protein-4 (Bmp-4) plays a role in mouse embryonic lung morphogenesis,” Development, vol. 122, no. 6, pp. 1693–1702, 1996. View at Scopus
  72. L. Yang, A. Naltner, and C. Yan, “Overexpression of dominant negative retinoic acid receptor α causes alveolar abnormality in transgenic neonatal lungs,” Endocrinology, vol. 144, no. 7, pp. 3004–3011, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. H. Wan, S. Dingle, Y. Xu et al., “Compensatory roles of Foxal and Foxa2 during lung morphogenesis,” The Journal of Biological Chemistry, vol. 280, no. 14, pp. 13809–13816, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. H. Wan, Y. Xu, M. Ikegami et al., “Foxa2 is required for transition to air breathing at birth,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 40, pp. 14449–14454, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. Y. Maeda, V. Davé, and J. A. Whitsett, “Transcriptional control of lung morphogenesis,” Physiological Reviews, vol. 87, no. 1, pp. 219–244, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Kimura, Y. Hara, T. Pineau et al., “The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary,” Genes and Development, vol. 10, no. 1, pp. 60–69, 1996. View at Scopus
  77. K. Devriendt, C. Vanhole, G. Matthijs, and F. De Zegher, “Deletion of thyroid transcription factor-1 gene in an infant with neonatal thyroid dysfunction and respiratory failure,” The New England Journal of Medicine, vol. 338, no. 18, pp. 1317–1318, 1998. View at Publisher · View at Google Scholar · View at Scopus
  78. V. Compernolle, K. Brusselmans, T. Acker et al., “Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice,” Nature Medicine, vol. 8, no. 7, pp. 702–710, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. J. S. Guseh, S. A. Bores, B. Z. Stanger et al., “Notch signaling promotes airway mucous metaplasia and inhibits alveolar development,” Development, vol. 136, no. 10, pp. 1751–1759, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. T. P. Dang, S. Eichenberger, A. Gonzalez, S. Olson, and D. P. Carbone, “Constitutive activation of Notch3 inhibits terminal epithelial differentiation in lungs of transgenic mice,” Oncogene, vol. 22, no. 13, pp. 1988–1997, 2003. View at Publisher · View at Google Scholar · View at Scopus
  81. P. N. Tsao, F. Chen, K. I. Izvolsky et al., “γ-Secretase activation of notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung,” The Journal of Biological Chemistry, vol. 283, no. 43, pp. 29532–29544, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. T. J. Cole, N. M. Solomon, R. Van Driel et al., “Altered epithelial cell proportions in the fetal lung of glucocorticoid receptor null mice,” American Journal of Respiratory Cell and Molecular Biology, vol. 30, no. 5, pp. 613–619, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. C. Wongtrakool, S. Malpel, J. Gorenstein et al., “Down-regulation of retinoic acid receptor alpha signaling is required for sacculation and type I cell formation in the developing lung,” The Journal of Biological Chemistry, vol. 278, no. 47, pp. 46911–46918, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. R. Keijzer, M. van Tuyl, C. Meijers et al., “The transcription factor GATA6 is essential for branching morphogenesis and epithelial cell differentiation during fetal pulmonary development,” Development, vol. 128, no. 4, pp. 503–511, 2001. View at Scopus
  85. G. De Carlo Massaro, D. Massaro, and P. Chambon, “Retinoic acid receptor-α regulates pulmonary alveolus formation in mice after, but not during, perinatal period,” American Journal of Physiology, vol. 284, no. 2, pp. L431–L433, 2003. View at Scopus
  86. D. E. Metzger, M. T. Stahlman, and J. M. Shannon, “Misexpression of ELF5 disrupts lung branching and inhibits epithelial differentiation,” Developmental Biology, vol. 320, no. 1, pp. 149–160, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. M. L. Mucenski, S. E. Wert, J. M. Nation et al., “β-catenin is required for specification of proximal/distal cell fate during lung morphogenesis,” The Journal of Biological Chemistry, vol. 278, no. 41, pp. 40231–40238, 2003. View at Publisher · View at Google Scholar · View at Scopus
  88. P. M. Becker, T. S. Tran, M. J. Delannoy, C. He, J. M. Shannon, and S. McGrath-Morrow, “Semaphorin 3A contributes to distal pulmonary epithelial cell differentiation and lung morphogenesis,” PLoS One, vol. 6, no. 11, Article ID e27449, 2011.
  89. K. Nagata, K. Masumoto, G. Esumi et al., “Connexin43 plays an important role in lung development,” Journal of Pediatric Surgery, vol. 44, no. 12, pp. 2296–2301, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. G. Millien, A. Spira, A. Hinds, J. Wang, M. C. Williams, and M. I. Ramirez, “Alterations in gene expression in T1α null lung: a model of deficient alveolar sac development,” BMC Developmental Biology, vol. 6, article no. 35, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Loscertales, A. J. Mikels, J. K. H. Hu, P. K. Donahoe, and D. J. Roberts, “Chick pulmonary Wnt5a directs airway and vascular tubulogenesis,” Development, vol. 135, no. 7, pp. 1365–1376, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. R. S. Moura, J. P. Coutinho-Borges, A. P. Pacheco, P. O. daMota, and J. Correia-Pinto, “FGF signaling pathway in the developing chick lung: expression and inhibition studies,” PLoS ONE, vol. 6, no. 3, Article ID e17660, 2011. View at Publisher · View at Google Scholar · View at Scopus