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Rhesus macaques as a tractable physiological model of human ageing

View ORCID ProfileKenneth L. Chiou, View ORCID ProfileMichael J. Montague, Elisabeth A. Goldman, Marina M. Watowich, Sierra N. Sams, Jeff Song, Julie E. Horvath, View ORCID ProfileKirstin N. Sterner, View ORCID ProfileAngelina V. Ruiz-Lambides, View ORCID ProfileMelween I. Martínez, View ORCID ProfileJames P. Higham, View ORCID ProfileLauren J. N. Brent, Michael L. Platt, View ORCID ProfileNoah Snyder-Mackler
doi: https://doi.org/10.1101/2020.06.10.143669
Kenneth L. Chiou
1Department of Psychology, University of Washington, Seattle, WA 98195, USA
2Nathan Shock Center of Excellence in the Basic Biology of Aging, Department of Pathology
5Center for Evolution and Medicine, Arizona State University, Tempe, AZ 85281, USA
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  • For correspondence: chiou@asu.edu nsnyderm@asu.edu
Michael J. Montague
7Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA
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Elisabeth A. Goldman
10Department of Anthropology, University of Oregon, Eugene, OR 97403, USA
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Marina M. Watowich
3Department of Biology
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Sierra N. Sams
1Department of Psychology, University of Washington, Seattle, WA 98195, USA
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Jeff Song
11Department of Biological and Biomedical Sciences, North Carolina Central University, Durham, NC 27707, USA
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Julie E. Horvath
11Department of Biological and Biomedical Sciences, North Carolina Central University, Durham, NC 27707, USA
12North Carolina Museum of Natural Sciences, Raleigh, NC 27601, USA
13Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA
14Department of Evolutionary Anthropology, Duke University, Durham, NC 27708, USA
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Kirstin N. Sterner
10Department of Anthropology, University of Oregon, Eugene, OR 97403, USA
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  • ORCID record for Kirstin N. Sterner
Angelina V. Ruiz-Lambides
15Caribbean Primate Research Center, Unit of Comparative Medicine, University of Puerto Rico, San Juan, PR 00936, USA
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Melween I. Martínez
15Caribbean Primate Research Center, Unit of Comparative Medicine, University of Puerto Rico, San Juan, PR 00936, USA
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James P. Higham
16Department of Anthropology, New York University, New York, NY 10003, USA
17New York Consortium in Evolutionary Primatology, New York, NY, USA
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Lauren J. N. Brent
18Centre for Research in Animal Behaviour, University of Exeter, Exeter, EX4 4QG, UK
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Michael L. Platt
7Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA
8Department of Psychology
9Department of Marketing, Wharton School of Business
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Noah Snyder-Mackler
1Department of Psychology, University of Washington, Seattle, WA 98195, USA
2Nathan Shock Center of Excellence in the Basic Biology of Aging, Department of Pathology
3Department of Biology
4Center for Studies in Demography and Ecology
5Center for Evolution and Medicine, Arizona State University, Tempe, AZ 85281, USA
6School of Life Sciences
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  • ORCID record for Noah Snyder-Mackler
  • For correspondence: chiou@asu.edu nsnyderm@asu.edu
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Abstract

Research in the basic biology of ageing is increasingly identifying mechanisms and modifiers of ageing in short-lived organisms such as worms and mice. The ultimate goal of such work is to improve human health, particularly in the growing segment of the population surviving into old age. Thus far, few interventions have robustly transcended species boundaries in the laboratory, suggesting that changes in approach are needed to avoid costly failures in translational human research. In this review, we discuss both well-established and alternative model organisms for ageing research and outline how research in nonhuman primates is sorely needed, first, to translate findings from shorter-lived organisms to humans, and second, to understand key aspects of ageing that are unique to primate biology. We focus on rhesus macaques as a particularly promising model organism for ageing research due to their social and physiological similarity to humans as well as the existence of key resources that have been developed for this species. As a case study, we compare gene regulatory signatures of ageing in the peripheral immune system between humans and rhesus macaques from a free-ranging study population in Cayo Santiago. We show that both mRNA expression and DNA methylation signatures of immune ageing are broadly shared between macaques and humans, indicating strong conservation of the trajectory of ageing in the immune system. We conclude with a review of key issues in the biology of ageing for which macaques and other nonhuman primates may uniquely contribute valuable insights, including the effects of social gradients on health and ageing. We anticipate that continuing research in rhesus macaques and other nonhuman primates will play a critical role in conjunction with model organism and human biodemographic research in ultimately improving translational outcomes and extending health and longevity in our ageing population.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Rhesus macaques as a tractable physiological model of human ageing
Kenneth L. Chiou, Michael J. Montague, Elisabeth A. Goldman, Marina M. Watowich, Sierra N. Sams, Jeff Song, Julie E. Horvath, Kirstin N. Sterner, Angelina V. Ruiz-Lambides, Melween I. Martínez, James P. Higham, Lauren J. N. Brent, Michael L. Platt, Noah Snyder-Mackler
bioRxiv 2020.06.10.143669; doi: https://doi.org/10.1101/2020.06.10.143669
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Rhesus macaques as a tractable physiological model of human ageing
Kenneth L. Chiou, Michael J. Montague, Elisabeth A. Goldman, Marina M. Watowich, Sierra N. Sams, Jeff Song, Julie E. Horvath, Kirstin N. Sterner, Angelina V. Ruiz-Lambides, Melween I. Martínez, James P. Higham, Lauren J. N. Brent, Michael L. Platt, Noah Snyder-Mackler
bioRxiv 2020.06.10.143669; doi: https://doi.org/10.1101/2020.06.10.143669

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