Deconvoluting lung evolution: from phenotypes to gene regulatory networks |
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| Authors: | Torday John S; Rehan Virender K; Hicks James W; Wang Tobias; Maina John; Weibel Ewald R; Hsia Connie CW; Sommer Ralf J; Perry Steven F |
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| Institution: | *David Geffen School of Medicine at UCLA, Los Angeles, California, USA;  Department of Ecology and Evolutionary Biology, University of California, Irvine, USA;  Department of Zoophysiology, Aarhus University, Denmark;  University of Witwatersrand, Johannesburg, South Africa; ¶University of Berne, Berne, Switzerland; University of Texas Southwestern Medical Center, Dallas, Texas, USA; Max Planck Institute for Developmental Biology, Tuebingen, Germany; University of Bonn, Bonn, Germany |
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| Abstract: | Speakers in this symposium presented examples of respiratoryregulation that broadly illustrate principles of evolution fromwhole organ to genes. The swim bladder and lungs of aquaticand terrestrial organisms arose independently from a commonprimordial "respiratory pharynx" but not from each other. Pathwaysof lung evolution are similar between crocodiles and birds buta low compliance of mammalian lung may have driven the developmentof the diaphragm to permit lung inflation during inspiration.To meet the high oxygen demands of flight, bird lungs have evolvedseparate gas exchange and pump components to achieve unidirectionalventilation and minimize dead space. The process of "screening"(removal of oxygen from inspired air prior to entering the terminalunits) reduces effective alveolar oxygen tension and potentiallyexplains why nonathletic large mammals possess greater pulmonarydiffusing capacities than required by their oxygen consumption.The "primitive" central admixture of oxygenated and deoxygenatedblood in the incompletely divided reptilian heart is actuallyco-regulated with other autonomic cardiopulmonary responsesto provide flexible control of arterial oxygen tension independentof ventilation as well as a unique mechanism for adjusting metabolicrate. Some of the most ancient oxygen-sensing molecules, i.e.,hypoxia-inducible factor-1alpha and erythropoietin, are up-regulatedduring mammalian lung development and growth under apparentlynormoxic conditions, suggesting functional evolution. Normalalveolarization requires pleiotropic growth factors acting viahighly conserved cell–cell signal transduction, e.g.,parathyroid hormone-related protein transducing at least partlythrough the Wingless/int pathway. The latter regulates morphogenesisfrom nematode to mammal. If there is commonality among thesediverse respiratory processes, it is that all levels of organization,from molecular signaling to structure to function, co-evolveprogressively, and optimize an existing gas-exchange framework. |
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