Affiliation:
1. Department of Biological Sciences, Northern Illinois University,DeKalb, IL 60115, USA
Abstract
SUMMARY
Redox signaling provides a quick and efficient mechanism for clonal or colonial organisms to adapt their growth and development to aspects of the environment, e.g. the food supply. A `signature' of mitochondrial redox signaling, particularly as mediated by reactive oxygen species (ROS), can be elucidated by experimental manipulation of the electron transport chain. The major sites of ROS formation are found at NADH dehydrogenase of complex I and at the interface between coenzyme Q and complex III. Inhibitors of complex III should thus upregulate ROS from both sites; inhibitors of complex I should upregulate ROS from the first but not the second site, while uncouplers of oxidative phosphorylation should downregulate ROS from both sites. To investigate the possibility of such redox signaling, perturbations of colony growth and development were carried out using the hydroid Podocoryna carnea. Oxygen uptake of colonies was measured to determine comparable physiological doses of antimycin A1 (an inhibitor of complex III),rotenone (an inhibitor of complex I) and carbonyl cyanide m-chlorophenylhydrazone (CCCP; an uncoupler of oxidative phosphorylation). Using these doses, clear effects on colony growth and development were obtained. Treatment with antimycin A1 results in `runner-like'colony growth, with widely spaced polyps and stolon branches, while treatment with CCCP results in `sheet-like' growth, with closely spaced polyps and stolon branches. Parallel results have been obtained previously with azide, an inhibitor of complex IV, and dinitrophenol, another uncoupler of oxidative phosphorylation. Perhaps surprisingly, rotenone produced effects on colony development similar to those of CCCP. Assays of peroxides using 2′,7′-dichlorofluorescin diacetate and fluorescent microscopy suggest a moderate difference in ROS formation between the antimycin and rotenone treatments. The second site of ROS formation (the interface between coenzyme Q and complex III) may thus predominate in the signaling that regulates colony development. The fat-rich, brine shrimp diet of these hydroids may be relevant in this context. Acyl CoA dehydrogenase, which catalyzes the first step in the mitochondrial β-oxidation of fatty acids,carries electrons to coenzyme Q, thus bypassing complex I. These results support a role for redox signaling, mediated by ROS, in colony development. Nevertheless, other redox sensors between complexes I and III may yet be found.
Publisher
The Company of Biologists
Subject
Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics
Reference23 articles.
1. Allen, J. F. (1993). Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J. Theor. Biol.165,609-631.
2. Blackstone, N. W. (1999). Redox control in development and evolution: evidence from colonial hydroids. J. Exp. Biol.202,3541-3553.
3. Blackstone, N. W. (2001). Redox state, reactive oxygen species, and adaptive growth in colonial hydroids. J. Exp. Biol.204,1845-1853.
4. Blackstone, N. W. and Kirkwood, T. B. L. (in press). Mitochondria and programmed cell death: “slave revolt” or community homeostasis? In Genetic and Cultural Evolution of Cooperation. Dahlem Workshop Report (ed. P. Hammerstein). Cambridge, MA: MIT Press.
5. Brownlee, M. (2001). Biochemistry and molecular cell biology of diabetic complications. Nature414,813-820.
Cited by
35 articles.
订阅此论文施引文献
订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献