Deconvoluting lung evolution: From phenotypes to gene regulatory networks

John S. Torday, Virender K. Rehan, James W. Hicks, Tobias Wang, John Maina, Ewald R. Weibel, Connie C W Hsia, Ralf J. Sommer, Steven F. Perry

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Speakers in this symposium presented examples of respiratory regulation that broadly illustrate principles of evolution from whole organ to genes. The swim bladder and lungs of aquatic and terrestrial organisms arose independently from a common primordial "respiratory pharynx" but not from each other. Pathways of lung evolution are similar between crocodiles and birds but a low compliance of mammalian lung may have driven the development of the diaphragm to permit lung inflation during inspiration. To meet the high oxygen demands of flight, bird lungs have evolved separate gas exchange and pump components to achieve unidirectional ventilation and minimize dead space. The process of "screening" (removal of oxygen from inspired air prior to entering the terminal units) reduces effective alveolar oxygen tension and potentially explains why nonathletic large mammals possess greater pulmonary diffusing capacities than required by their oxygen consumption. The "primitive" central admixture of oxygenated and deoxygenated blood in the incompletely divided reptilian heart is actually co-regulated with other autonomic cardiopulmonary responses to provide flexible control of arterial oxygen tension independent of ventilation as well as a unique mechanism for adjusting metabolic rate. Some of the most ancient oxygen-sensing molecules, i.e., hypoxia-inducible factor-1alpha and erythropoietin, are up-regulated during mammalian lung development and growth under apparently normoxic conditions, suggesting functional evolution. Normal alveolarization requires pleiotropic growth factors acting via highly conserved cell-cell signal transduction, e.g., parathyroid hormone-related protein transducing at least partly through the Wingless/int pathway. The latter regulates morphogenesis from nematode to mammal. If there is commonality among these diverse respiratory processes, it is that all levels of organization, from molecular signaling to structure to function, co-evolve progressively, and optimize an existing gas-exchange framework.

Original languageEnglish (US)
Pages (from-to)601-609
Number of pages9
JournalIntegrative and Comparative Biology
Volume47
Issue number4
DOIs
StatePublished - Oct 2007

Fingerprint

lungs
phenotype
oxygen
pulmonary gas exchange
mammals
erythropoietin
crocodiles
normoxia
swim bladder
parathyroid hormone
pharynx
inflation
birds
diaphragm
gene regulatory networks
pumps
compliance
growth factors
oxygen consumption
morphogenesis

ASJC Scopus subject areas

  • Animal Science and Zoology

Cite this

Torday, J. S., Rehan, V. K., Hicks, J. W., Wang, T., Maina, J., Weibel, E. R., ... Perry, S. F. (2007). Deconvoluting lung evolution: From phenotypes to gene regulatory networks. Integrative and Comparative Biology, 47(4), 601-609. https://doi.org/10.1093/icb/icm069

Deconvoluting lung evolution : From phenotypes to gene regulatory networks. / Torday, John S.; Rehan, Virender K.; Hicks, James W.; Wang, Tobias; Maina, John; Weibel, Ewald R.; Hsia, Connie C W; Sommer, Ralf J.; Perry, Steven F.

In: Integrative and Comparative Biology, Vol. 47, No. 4, 10.2007, p. 601-609.

Research output: Contribution to journalArticle

Torday, JS, Rehan, VK, Hicks, JW, Wang, T, Maina, J, Weibel, ER, Hsia, CCW, Sommer, RJ & Perry, SF 2007, 'Deconvoluting lung evolution: From phenotypes to gene regulatory networks', Integrative and Comparative Biology, vol. 47, no. 4, pp. 601-609. https://doi.org/10.1093/icb/icm069
Torday, John S. ; Rehan, Virender K. ; Hicks, James W. ; Wang, Tobias ; Maina, John ; Weibel, Ewald R. ; Hsia, Connie C W ; Sommer, Ralf J. ; Perry, Steven F. / Deconvoluting lung evolution : From phenotypes to gene regulatory networks. In: Integrative and Comparative Biology. 2007 ; Vol. 47, No. 4. pp. 601-609.
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