Cellular oxidative damage is more sensitive to biosynthetic rate than to metabolic rate: A test of the theoretical model on hornworms (Manduca sexta larvae).
We develop a theoretical model from an energetic viewpoint for unraveling the entangled effects of metabolic and biosynthetic rates on oxidative cellular damage accumulation during animal's growth, and test the model by experiments in hornworms. The theoretical consideration suggests that most of the cellular damages caused by the oxidative metabolism can be repaired by the efficient maintenance mechanisms, if the energy required by repair is unlimited. However, during growth a considerable amount of energy is allocated to the biosynthesis, which entails tradeoffs with the requirements of repair. Thus, the model predicts that cellular damage is more influenced by the biosynthetic rate than the metabolic rate. To test the prediction, we induced broad variations in metabolic and biosynthetic rates in hornworms, and assayed the lipid peroxidation and protein carbonyl. We found that the increase in the cellular damage was mainly caused by the increase in biosynthetic rate, and the variations in metabolic rate had negligible effect. The oxidative stress hypothesis of aging suggests that high metabolism leads to high cellular damage and short lifespan. However, some empirical studies showed that varying biosynthetic rate, rather than metabolic rate, changes animal's lifespan. The conflicts between the empirical evidence and the hypothesis are reconciled by this study.
Department of Biological Sciences, Missouri University of Science and Technology, Rolla, MO 65409, United States.
Kaushalya
K
Amunugama
Department of Biological Sciences, Missouri University of Science and Technology, Rolla, MO 65409, United States.
Lihong
L
Jiao
Department of Mathematics and Statistics, Missouri University of Science and Technology, Rolla, MO 65409, United States.
Gayla R
GR
Olbricht
Department of Biological Sciences, Missouri University of Science and Technology, Rolla, MO 65409, United States.
Chance
C
Walker
Department of Biological Sciences, Missouri University of Science and Technology, Rolla, MO 65409, United States.
Yue-Wern
YW
Huang
Department of Chemistry, Missouri University of Science and Technology, Rolla, MO 65409, United States.
Paul K
PK
Nam
Department of Biological Sciences, Missouri University of Science and Technology, Rolla, MO 65409, United States. Electronic address: houch@mst.edu.
Chen
C
Hou
D000375:Aging / Q000378:metabolism*; D000818:Animals; D031204:Caloric Restriction; D007814:Larva / Q000502:physiology*; D016014:Linear Models; D015227:Lipid Peroxidation; D018402:Manduca / Q000502:physiology*; D008962:Models, Theoretical; D018384:Oxidative Stress; D050050:Protein Carbonylation
Energy; Repair; Theoretical model; Tradeoff