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Research Article

Shorter telomeres with high telomerase activity are associated with raised allostatic load and impoverished psychosocial resources

Argita Zalli, Livia A. Carvalho, Jue Lin, Mark Hamer, Jorge D. Erusalimsky, Elizabeth H. Blackburn, and Andrew Steptoe
PNAS first published March 10, 2014; https://doi.org/10.1073/pnas.1322145111
Argita Zalli
aDepartment of Epidemiology and Public Health, University College London, London WC1E 6BT, United Kingdom;
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Livia A. Carvalho
aDepartment of Epidemiology and Public Health, University College London, London WC1E 6BT, United Kingdom;
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Jue Lin
bDepartment of Biochemistry and Biophysics, University of California, San Francisco, CA 94158-2517; and
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Mark Hamer
aDepartment of Epidemiology and Public Health, University College London, London WC1E 6BT, United Kingdom;
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Jorge D. Erusalimsky
cCellular Senescence and Vascular Biology Group, Cardiff School of Health Sciences, Cardiff Metropolitan University, Cardiff CF5 2YB, Wales, United Kingdom
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Elizabeth H. Blackburn
bDepartment of Biochemistry and Biophysics, University of California, San Francisco, CA 94158-2517; and
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Andrew Steptoe
aDepartment of Epidemiology and Public Health, University College London, London WC1E 6BT, United Kingdom;
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  • For correspondence: a.steptoe@ucl.ac.uk
  1. Edited by Bruce S. McEwen, The Rockefeller University, New York, NY, and approved February 14, 2014 (received for review November 26, 2013)

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Significance

These findings indicate that the combination of shorter leukocyte telomeres with high telomerase activity is associated with stress-related impairment of function at both the biological and psychological levels. Slow poststress recovery in cardiovascular activity in inflammatory responses and reduced stress responsivity in blood pressure and cortisol are indicative of a state of heightened allostatic load. Older men with the shorter telomere/high telomerase phenotype also show impoverished resources for dealing with stress, including low levels of social support and optimism and higher levels of hostility. The integrated approach taken in this study advances our understanding of the cellular substrate of stress-related processes and documents the dynamic interplay between social environmental exposures and the mechanisms underlying chromosomal integrity.

Abstract

Recent work has linked psychological stress with premature cellular aging as indexed by reduced leukocyte telomere length. The combination of shorter telomeres with high telomerase activity (TA) may be indicative of active cell stress. We hypothesized that older individuals characterized by shorter telomeres with high TA in unstimulated leukocytes would show signs of high allostatic load and low levels of protective psychosocial resources. We studied 333 healthy men and women aged 54–76 y who underwent laboratory testing in which we measured cardiovascular, neuroendocrine, and inflammatory responses to standardized mental stress tasks. The tasks elicited prompt increases in blood pressure (BP), heart rate, cortisol, and mediators of inflammation and reductions in heart rate variability, returning toward baseline levels following stress. However, men having shorter telomeres with high TA showed blunted poststress recovery in systolic BP, heart rate variability, and monocyte chemoattractant protein-1, together with reduced responsivity in diastolic BP, heart rate, and cortisol, in comparison to men with longer telomeres or men with shorter telomeres and low TA. Shorter telomeres with high TA were also associated with reduced social support, lower optimism, higher hostility, and greater early life adversity. These effects were independent of age, socioeconomic status, and body mass index. We did not observe differences among older women. Our findings suggest that active cell stress is associated with impaired physiological stress responses and impoverished psychosocial resources, reflecting an integration of cellular, systemic, and psychological stress processes potentially relevant to health in older men.

  • cellular senescence
  • allostasis
  • psychological distress

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: a.steptoe{at}ucl.ac.uk.
  • Author contributions: A.S. designed research; J.L., M.H., J.D.E., and A.S. performed research; A.Z., J.L., and A.S. analyzed data; and A.Z., L.A.C., M.H., J.D.E., E.H.B., and A.S. wrote the paper.

  • Conflict of interest statement: J.L. and E.H.B. are cofounders of Telome Health, a diagnostic company measuring telomere biology. All other authors report no biomedical financial interests or potential conflicts of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1322145111/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Telomeres, stress, and allostatic load
Argita Zalli, Livia A. Carvalho, Jue Lin, Mark Hamer, Jorge D. Erusalimsky, Elizabeth H. Blackburn, Andrew Steptoe
Proceedings of the National Academy of Sciences Mar 2014, 201322145; DOI: 10.1073/pnas.1322145111

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Telomeres, stress, and allostatic load
Argita Zalli, Livia A. Carvalho, Jue Lin, Mark Hamer, Jorge D. Erusalimsky, Elizabeth H. Blackburn, Andrew Steptoe
Proceedings of the National Academy of Sciences Mar 2014, 201322145; DOI: 10.1073/pnas.1322145111
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