Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 107, Issue 31, Pages 13942-13947Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.0914026107
Keywords
evolution; nuclear-receptor; stress response
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Funding
- Confederated Tribes of the Umatilla Indian Reservation
- Bonneville Power Administration
- Great Lakes Fishery Commission
- Office of Diversity and Pluralism in the College of Agriculture and Natural Resources at Michigan State University
- National Institute of Mental Health [T32MH70343]
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Corticosteroid hormones are critical for controlling metabolism, hydromineral balance, and the stress response in vertebrates. Although corticosteroid hormones have been well characterized in most vertebrate groups, the identity of the earliest vertebrate corticosteroid hormone has remained elusive. Here we provide evidence that 11-deoxycortisol is the corticosteroid hormone in the lamprey, a member of the agnathans that evolved more than 500 million years ago. We used RIA, HPLC, and mass spectrometry analysis to determine that 11-deoxycortisol is the active corticosteroid present in lamprey plasma. We also characterized an 11-deoxycortisol receptor extracted from sea lamprey gill cytosol. The receptor was highly specific for 11-deoxycortisol and exhibited corticosteroid binding characteristics, including DNA binding. Furthermore, we observed that 11-deoxycortisol was regulated by the hypothalamus-pituitary axis and responded to acute stress. 11-Deoxycortisol implants reduced sex steroid concentrations and upregulated gill Na(+), K(+)-ATPase, an enzyme critical for ion balance. We show here that 11-deoxycortisol functioned as both a glucocorticoid and a mineralocorticoid in the lamprey. Our findings indicate that a complex and highly specific corticosteroid signaling pathway evolved at least 500 million years ago with the arrival of the earliest vertebrate.
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