Implications of dealing with airborne substances and reactive oxygen species: What mammalian lungs, animals, and plants have to say

Oliveira, Elisabeth Spinelli; Hermes-Lima, Marcelo; Filho, Danilo Wilhem; Spinelli de Oliveira, Elisabeth; Hancock, John T.; Isola, Daniel A.; Wilhelm Filho, Danilo; Ochs, Matthias; Yu, Jerry

Abstract

A gas-exchange structure interacts with the environment and is constantly challenged by contaminants that may elicit defense responses, thus compromising its primary function. It is also exposed to high concentrations of O2 that can generate reactive oxygen species (ROS). Revisiting the lung of mammals, an integrative picture emerges, indicating that this bronchi-alveolar structure deals with inflammation in a special way, which minimizes compromising the gas-exchange role. Depending on the challenge, pro-inflammatory or antiinflammatory responses are elicited by conserved molecules, such as surfactant proteins A and D. An even broader picture points to the participation of airway sensors, responsive to inflammatory mediators, in a loop linking the immunological and nervous systems and expanding the role played by respiratory organs in functions other than gas-exchange. A byproduct of exposure to high concentration of O2 is the formation of superoxide (), hydrogen peroxide (H2O2), hydroxyl radical (HO•), and other ROS, which are known to be toxic to different types of cells, including the lung epithelium. A balance between antioxidants and oxidants exists; in pulmonary epithelial cells high intracellular and extracellular levels of antioxidants are found. Antioxidant adaptations related to plant and animal life-styles involve a broad range of overlapping strategies based on well-conserved molecules. Glutathione (GSH) is an abundant and ubiquitous thiol-tripeptide antioxidant, also present in lungs, whose role in providing information on the intracellular redox state of animals and plants is well established. In these organisms, GSH influences gene expression associated with stress, maximizing defense responses. Several enzymatic antioxidants, such as glutathione peroxidase (GPx), glutathione reductase, glutathione S-transferase, and glucose 6-phosphate dehydrogenase participate in the redox system; in animals that are stress-tolerant GPx is a key element against oxidative assaults. Most importantly, alternative roles of ROS as signaling molecules have been found in all plants and animals. For example, alveolar macrophages produce that act as second messengers, in addition to having a bactericidal role. The nonradical ROS H2O2 signals inflammation in mammalian lungs, apoptosis in different animal tissues, and is also involved in stomatal closure, root development, gene expression, and defense responses of plants. Antioxidant adaptations in some water-breathing animals involve the excretion of H2O2 by diffusion through gas-exchange structures. The fine balance among a multitude of factors and cells makes the difference between damage and protection in animals and plants. Knowledge about the mechanisms and consequences of these molecular interactions is now starting to be integrated.

Citation

Filho, D. W., Hermes-Lima, M., Oliveira, E. S., Spinelli de Oliveira, E., Hancock, J. T., Isola, D. A., …Wilhelm Filho, D. (2007). Implications of dealing with airborne substances and reactive oxygen species: What mammalian lungs, animals, and plants have to say. Integrative and Comparative Biology, 47(4), 578-591. https://doi.org/10.1093/icb/icm078

• Journal Article Type: Article
• Publication Date: Oct 1, 2007
• Journal: Integrative and Comparative Biology
• Print ISSN: 1540-7063
• Electronic ISSN: 1557-7023
• Publisher: Oxford University Press (OUP)
• Peer Reviewed: Peer Reviewed
• Volume: 47
• Issue: 4
• Pages: 578-591
• DOI: https://doi.org/10.1093/icb/icm078
• Public URL: https://uwe-repository.worktribe.com/output/1034555
• Publisher URL: http://dx.doi.org/10.1093/icb/icm078