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Immune competence and spleen size scale with colony status in the naked mole-rat

Valérie Bégay, Branko Cirovic, Alison J. Barker, Robert Klopfleisch, Daniel W. Hart, Nigel C. Bennett, Gary R. Lewin
doi: https://doi.org/10.1101/2021.08.15.456351
Valérie Bégay
1Department of Neuroscience, Max Delbrück Center for Molecular Medicine, Robert-Rössle Straße 10, D-13092 Berlin, Germany
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  • For correspondence: vbegay@mdc-berlin.de glewin@mdc-berlin.de
Branko Cirovic
2Division of Cellular Immunology, German Cancer Research Center, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany
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Alison J. Barker
1Department of Neuroscience, Max Delbrück Center for Molecular Medicine, Robert-Rössle Straße 10, D-13092 Berlin, Germany
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Robert Klopfleisch
3Institute of Veterinary Pathology, Free University Berlin, Robert von Ostertag strasse 15, 14163 Berlin, Germany
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Daniel W. Hart
4Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria, Republic of South Africa
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Nigel C. Bennett
4Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria, Republic of South Africa
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Gary R. Lewin
1Department of Neuroscience, Max Delbrück Center for Molecular Medicine, Robert-Rössle Straße 10, D-13092 Berlin, Germany
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  • For correspondence: vbegay@mdc-berlin.de glewin@mdc-berlin.de
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Abstract

Naked mole-rats (NM-R; Heterocephalus glaber) live in multi-generational colonies with a social hierarchy, show low cancer incidence and long life-spans. Here we asked if such extreme physiology might have an immune component. The spleen is the largest lymphoid organ and plays an essential role in response to immunological insults and may participate in combating cancer and slowing ageing. We investigated the anatomy, molecular composition and function of the NM-R spleen using RNA-sequencing and histological analysis in healthy animals. We found that spleen size in healthy NM-Rs varies considerably. We therefore classified NM-Rs according to spleen size as NM-Rs with small spleens or enlarged spleens. Animals with enlarged spleens showed potentially better anti-microbial profiles and were much more likely to have a high rank within the colony. Splenomegaly was associated with infection in sick NM-Rs, but not in NM-Rs with enlarged spleens. In all healthy NM-Rs splenic erythropoiesis, megakaryopoiesis and myelopoiesis were increased, but B lymphopoiesis was reduced and splenic marginal zone showed markedly altered morphology when compared to other rodents. However, in NM-Rs lymphocytes were found in secondary sites such as lymph nodes, gut lymphoid nodules and thymus. Thus, the NM-R spleen is a major site of adult hematopoiesis under normal physiological conditions. Overall, the NM-R immune system seems to rely mainly on innate immune responses with a more restricted adaptive immune response. We propose that the anatomical plasticity of the spleen might be regulated by social interaction and gives immunological advantage to increase the life-span of higher ranked animals.

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-NC-ND 4.0 International license.
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Posted August 15, 2021.
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Immune competence and spleen size scale with colony status in the naked mole-rat
Valérie Bégay, Branko Cirovic, Alison J. Barker, Robert Klopfleisch, Daniel W. Hart, Nigel C. Bennett, Gary R. Lewin
bioRxiv 2021.08.15.456351; doi: https://doi.org/10.1101/2021.08.15.456351
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Immune competence and spleen size scale with colony status in the naked mole-rat
Valérie Bégay, Branko Cirovic, Alison J. Barker, Robert Klopfleisch, Daniel W. Hart, Nigel C. Bennett, Gary R. Lewin
bioRxiv 2021.08.15.456351; doi: https://doi.org/10.1101/2021.08.15.456351

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