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On the Surprising Weakness of Pancreatic Beta-Cell Antioxidant Defences: An Evolutionary Perspective

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Evolutionary Biology

Abstract

Pancreatic beta-cells are unique among other cells in possessing an extremely weak antioxidant defence system. Furthermore, beta-cell defences against oxidative stress in both mice and humans are weaker in females than in males. These observations need an evolutionary explanation given that oxidative stress in beta-cells has an important contribution to the pathogenesis of type 2 diabetes. It turns out that a satisfactory explanation is feasible only by a systems-level approach to the glucose homeostatic system and beta-cell physiology. The connection between physiology and ecology is particularly important in major transitions in the evolutionary history of beta-cells. We have proposed that beta-cells evolved weak antioxidant protection to allow for reactive oxygen species (ROS) to exert a regulatory function directly linked with reproductive fitness of the organism. By down-regulating insulin synthesis and secretion, ROS in beta-cells cooperate with the stress-induced whole-body insulin resistance to divert glucose from insulin-dependent organs to an important insulin-independent structure: the evolving brain. Mammalian evolution provoked further reduction of beta-cell antioxidant defences in females in order to provide the fetus (through the insulin-independent placenta) with a reliable energy supply in pregnancy. The stress response has driven, within physiological constraints, the co-evolution of beta-cells, the brain and placenta and shaped their current status. We review the hypothesis and explore its implications.

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Acknowledgments

AR is supported by a Dorothy Hodgkin Postgraduate Award. TBLK and DPS are supported by the BBSRC Centre for Integrated Systems Biology of Ageing and Nutrition (CISBAN). Part of this work was supported by and carried out within the EU-funded Network of Excellence LifeSpan (FP6 036894).

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  1. Centre for Integrated Systems Biology of Ageing and Nutrition, Institute for Ageing and Health, Newcastle University, Newcastle upon Tyne, UK

    Armin Rashidi, Thomas B. L. Kirkwood & Daryl P. Shanley

  2. Institute for Ageing and Health, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, NE4 5PL, UK

    Armin Rashidi

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  1. Armin Rashidi
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  2. Thomas B. L. Kirkwood
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Correspondence to Armin Rashidi .

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  1. CNRS UMR 6632, Université d'Aix-Marseille, place Victor Hugo 3, Marseille CX 03, 13331, France

    Pierre Pontarotti

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Rashidi, A., Kirkwood, T.B.L., Shanley, D.P. (2009). On the Surprising Weakness of Pancreatic Beta-Cell Antioxidant Defences: An Evolutionary Perspective. In: Pontarotti, P. (eds) Evolutionary Biology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00952-5_6

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