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Sociodemographic effects on immune cell composition in a free-ranging non-human primate

View ORCID ProfileMitchell R. Sanchez Rosado, View ORCID ProfileNicole Marzan-Rivera, View ORCID ProfileMarina M. Watowich, Petraleigh Pantoja, Melissa A. Pavez-Fox, View ORCID ProfileErin R. Siracusa, Eve B. Cooper, Josue E. Negron-Del Valle, Daniel Phillips, View ORCID ProfileAngelina Ruiz-Lambides, Cayo Biobank Research Unit, View ORCID ProfileMelween I. Martinez, Michael J. Montague, Michael L. Platt, James P. Higham, View ORCID ProfileLauren J. N. Brent, View ORCID ProfileCarlos A. Sariol, View ORCID ProfileNoah Snyder-Mackler
doi: https://doi.org/10.1101/2021.12.06.471383
Mitchell R. Sanchez Rosado
1Department of Microbiology & Medical Zoology, University of Puerto Rico-Medical Sciences, San Juan, PR
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Nicole Marzan-Rivera
1Department of Microbiology & Medical Zoology, University of Puerto Rico-Medical Sciences, San Juan, PR
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Marina M. Watowich
2Department of Biology, University of Washington, Seattle, WA, USA
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Petraleigh Pantoja
1Department of Microbiology & Medical Zoology, University of Puerto Rico-Medical Sciences, San Juan, PR
3Unit of Comparative Medicine, Caribbean Primate Research Center and Animal Resources Center, University of Puerto Rico-Medical Sciences Campus, San Juan, PR, USA
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Melissa A. Pavez-Fox
4Centre for Research in Animal Behaviour, University of Exeter, Exeter EX4 4QG, UK
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Erin R. Siracusa
4Centre for Research in Animal Behaviour, University of Exeter, Exeter EX4 4QG, UK
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Eve B. Cooper
5Department of Anthropology, New York University, New York, NY 10003, USA
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Josue E. Negron-Del Valle
6School of Life Sciences, Arizona State University, Tempe, AZ, USA
7Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ, USA
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Daniel Phillips
6School of Life Sciences, Arizona State University, Tempe, AZ, USA
7Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ, USA
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Angelina Ruiz-Lambides
3Unit of Comparative Medicine, Caribbean Primate Research Center and Animal Resources Center, University of Puerto Rico-Medical Sciences Campus, San Juan, PR, USA
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  • ORCID record for Angelina Ruiz-Lambides
Melween I. Martinez
3Unit of Comparative Medicine, Caribbean Primate Research Center and Animal Resources Center, University of Puerto Rico-Medical Sciences Campus, San Juan, PR, USA
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Michael J. Montague
8Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA
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Michael L. Platt
8Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA
9Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA
10Department of Marketing, Wharton School, University of Pennsylvania, Philadelphia, PA 19104, USA
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James P. Higham
5Department of Anthropology, New York University, New York, NY 10003, USA
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Lauren J. N. Brent
4Centre for Research in Animal Behaviour, University of Exeter, Exeter EX4 4QG, UK
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  • ORCID record for Lauren J. N. Brent
Carlos A. Sariol
1Department of Microbiology & Medical Zoology, University of Puerto Rico-Medical Sciences, San Juan, PR
3Unit of Comparative Medicine, Caribbean Primate Research Center and Animal Resources Center, University of Puerto Rico-Medical Sciences Campus, San Juan, PR, USA
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Noah Snyder-Mackler
6School of Life Sciences, Arizona State University, Tempe, AZ, USA
7Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ, USA
11School for Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA
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  • For correspondence: nsnyderm@asu.edu
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Abstract

Aging results in declines in immune function and increases in inflammation, which underlie many age-related diseases. These immunosenescent signatures are similar to those seen in individuals exposed to social adversity, who may age more rapidly than those unexposed. Yet, it is unclear how social adversity alters immunity across demographic factors - data that are essential to identify how it might increase aging-related diseases. Here, we investigated how age, sex, and social adversity predicted immune cell proportions in 250 rhesus macaques living in a semi-naturalistic colony. As macaques aged, they exhibited signatures of immunosenescence. Older individuals had signatures of diminished antibody production and adaptive immunity, with declines in CD20+ B cells, CD20+/CD3+ cell ratio, and the CD4+/CD8+ T cell ratio. At all ages, females had higher CD20+/CD3+ and CD4+/CD8+ ratios, indicative of a stronger antibody and adaptive immune response that may facilitate pathogen clearance even with increasing age. Older individuals had signatures of inflammation, with higher proportions of CD3+/CD8+ Cytotoxic T cells, CD16+/CD3- Natural Killer cells, CD3+/CD4+/CD25+ and CD3+/CD8+/CD25+ T regulatory cells, and CD14+/CD16+/HLA-DR+ intermediate monocytes, combined with lower levels of CD14+/CD16-/HLA-DR+ classical monocytes. Notably, we found an interaction between age and social adversity, where low-status individuals had higher proportions of CD3+/CD4+/CD25+ T regulatory cells for their age, compared to higher-status individuals. Together, our study identifies immune cell types that are affected by age and sex in the premier nonhuman primate model of human biology and behavior, and demonstrate a novel link between inflammatory CD4+ T regulatory cells and social adversity.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Cayo Biobank Research Unit

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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-NC-ND 4.0 International license.
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Sociodemographic effects on immune cell composition in a free-ranging non-human primate
Mitchell R. Sanchez Rosado, Nicole Marzan-Rivera, Marina M. Watowich, Petraleigh Pantoja, Melissa A. Pavez-Fox, Erin R. Siracusa, Eve B. Cooper, Josue E. Negron-Del Valle, Daniel Phillips, Angelina Ruiz-Lambides, Cayo Biobank Research Unit, Melween I. Martinez, Michael J. Montague, Michael L. Platt, James P. Higham, Lauren J. N. Brent, Carlos A. Sariol, Noah Snyder-Mackler
bioRxiv 2021.12.06.471383; doi: https://doi.org/10.1101/2021.12.06.471383
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Sociodemographic effects on immune cell composition in a free-ranging non-human primate
Mitchell R. Sanchez Rosado, Nicole Marzan-Rivera, Marina M. Watowich, Petraleigh Pantoja, Melissa A. Pavez-Fox, Erin R. Siracusa, Eve B. Cooper, Josue E. Negron-Del Valle, Daniel Phillips, Angelina Ruiz-Lambides, Cayo Biobank Research Unit, Melween I. Martinez, Michael J. Montague, Michael L. Platt, James P. Higham, Lauren J. N. Brent, Carlos A. Sariol, Noah Snyder-Mackler
bioRxiv 2021.12.06.471383; doi: https://doi.org/10.1101/2021.12.06.471383

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