Cell-Mediated Immune Ontogeny Is Affected by Sex but Not Environmental Context in a Long-Lived Primate Species

Behringer, Verena; Deimel, Caroline; Stevens, Jeroen M. G.; Lee, Sean M.; Hohmann, Gottfried; Fruth, Barbara; Heistermann, Michael

doi:10.3389/fevo.2021.629094

Cited by 8 publications

(14 citation statements)

References 112 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Previous studies have found a large degree of variability in baseline neopterin in humans ( 53 ) and primates [barbary macaques, ( 24 ); chimpanzees, ( 18 , 19 , 21 , 22 ); bonobos, ( 23 ); emperor tamarins, ( 26 ); saddle-back tamarins, ( 26 )], making it difficult to determine “normal”, baseline neopterin values for primate species. Importantly, there is overlap between baseline neopterin and neopterin after immune activation.…”

Section: Discussionmentioning

confidence: 99%

“…Difference in neopterin between wild and captive individuals may depend on degree of anthropogenic degradation in the wild environment. Individuals living in more “pristine” environments [i.e., bonobos; ( 23 )] may show little difference in immune activation from captive individuals because of the shared evolutionary history with common pathogens in their environment ( 23 ). Further, glucocorticoids are known to affect immune system activation ( 58 ) and may differ between wild and captive populations.…”

Section: Discussionmentioning

confidence: 99%

“…In line with previous research, we found that both creatinine and specific gravity (SG) were tightly correlated (36,37) suggesting that either can be used to standardize urinary neopterin. Some wild primate urinary neopterin studies used SG to control for urine dilution, most likely because it is a more field-friendly and economical method to control for sample concentration than creatinine assays (18,19,(21)(22)(23)(24)26). We now know SG is a sufficient method to control for urine dilution for neopterin analysis in capuchin monkeys.…”

Section: Discussionmentioning

confidence: 99%

“…Given this, we predicted that neopterin would be elevated in wild compared to captive individuals. Lastly, a common pattern among primates, and humans, is that neopterin changes with age, specifically, it is high in infants, decreases through juvenile and early adulthood, and then increases again with advanced age ( 18 , 21 , 23 , 44 – 46 ). Thus, we predicted a similar pattern in both our wild and captive populations.…”

Section: Introductionmentioning

confidence: 99%

“…Neopterin has been used in clinical applications to monitor disease progression in humans (14) and has been found to increase in urine after HIV infection in macaque species (15)(16)(17) and respiratory infection in bonobos and chimpanzees (18,19). Urinary neopterin has been validated and integrated into health monitoring studies in a number of primate species (Pan troglodytes [chimpanzees; (18)(19)(20)(21)(22)], Pan paniscus [bonobos; (18,23)], Macaca sylvanus [barbary macaques; (24)] and has been shown to vary with age (18,23,24), differ between environments [captivity vs. wild; (20)], and respond to infection (18,19).…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Validating Urinary Neopterin as a Biomarker of Immune Response in Captive and Wild Capuchin Monkeys

et al. 2022

View full text Add to dashboard Cite

Non-invasive health monitoring is advantageous for wild and captive primate populations because it reduces the need for traditional invasive techniques (i.e., anesthetization) that can be stressful and potentially harmful for individuals. The biomarker neopterin is an emerging tool in primatology to measure immune activation and immunosenescence, however, most neopterin studies have focused on catarrhine species with little comparative work examining neopterin and health in platyrrhines. To address this gap, we validated a commercially available enzyme-linked immunosorbent assay (ELISA) to measure urinary neopterin in two types of capuchin monkeys, a wild population of white-faced capuchins (Cebus imitator) and a socially housed captive colony of tufted capuchins (Sapajus apella). We analytically validated methods for measuring urinary neopterin in two capuchin populations and demonstrated that two commonly-used methods to control for urine concentration—creatinine and specific gravity (SG)—produced highly concordant results. We also biologically validated these methods by examining variation in neopterin levels based on environment (captive and wild) and age, and changes in levels associated with immune-response. We found that neopterin increased after immune perturbation (rabies vaccine booster), varied by environmental condition, and mirrored expected trends in immune system ontogeny. Our results improve understanding of the innate immune system in platyrrhine species and suggest neopterin may be useful for non-invasive health monitoring in both captive and wild primates.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Validating Urinary Neopterin as a Biomarker of Immune Response in Captive and Wild Capuchin Monkeys

et al. 2022

View full text Add to dashboard Cite

show abstract

Urinary cytokine measurements do not reflect surgery‐induced inflammation in rhesus macaques

Higham

Cooper

Whalen

et al. 2023

American J Primatol

Self Cite

View full text Add to dashboard Cite

Measurement of the health and disease status of free-ranging primates is often limited by a lack of available biomarkers of immune activation and inflammation that can be applied noninvasively via the measurement of urine or fecal samples. Here, we evaluate the potential usefulness of noninvasive urinary measurements of a number of cytokines, chemokines, and other markers of inflammation and infection.We took advantage of surgery-associated inflammation in seven captive rhesus macaques, collecting urine samples before and after the medical interventions. We measured these urine samples for 33 different markers of inflammation and immune activation that are known to be responsive to inflammation and infection in rhesus macaque blood samples, via the Luminex platform. We also measured all samples for concentrations of the soluble urokinase plasminogen activator receptor (suPAR), which we had validated in a prior study as an effective biomarker of inflammation. Despite urine samples being collected in captivity under ideal conditions (clean, no contamination with feces or soil, frozen quickly), 13/33 biomarkers measured via Luminex were found at concentrations below detection limits in >50% of samples. Of the remaining 20 markers, only 2 showed significant increases in response to surgery-IL18 and MPO (myeloperoxidase). However, suPAR measurements of the same samples show a consistent marked increase in response to surgery that is absent from the patterns of IL18 and MPO measurement.Given that our samples were collected under conditions that are greatly preferable to those usually encountered in the field, urinary cytokine measurements via the Luminex platform seem overall unpromising for primate field studies.

show abstract

In vivo deciduous dental eruption in LuiKotale bonobos and Gombe chimpanzees

Lee

Sutherland

Fruth

et al. 2021

American J Phys Anthropol

Self Cite

View full text Add to dashboard Cite

Objectives: Existing data on bonobo and chimpanzee dental eruption timing are derived predominantly from captive individuals or deceased wild individuals. However, recent advances in noninvasive photographic monitoring of living, wild apes have enabled researchers to characterize dental eruption in relatively healthy individuals under naturalistic conditions. At present, such data are available for only one population of wild chimpanzees. We report data for an additional population of wild chimpanzees and the first dental eruption data for wild bonobos. Materials and Methods: We collected photographs and video footage of teeth from the open mouths of wild bonobos and East African chimpanzees of known age from LuiKotale, Democratic Republic of the Congo, and Gombe National Park, Tanzania, respectively. We scored the presence and absence of deciduous teeth from photographs and video footage to characterize deciduous dental eruption timing in these two populations.Results: Deciduous dental eruption ages in our sample fall within the range of variation previously documented for captive chimpanzees, but eruption ages are later in wild than in captive contexts. We found substantial variation in deciduous canine eruption timing, particularly among bonobos. One bonobo had a deciduous canine present by 227 days old while another did not have a deciduous canine present at 477 days old.

show abstract

Cell-Mediated Immune Ontogeny Is Affected by Sex but Not Environmental Context in a Long-Lived Primate Species

Cited by 8 publications

References 112 publications

Validating Urinary Neopterin as a Biomarker of Immune Response in Captive and Wild Capuchin Monkeys

Validating Urinary Neopterin as a Biomarker of Immune Response in Captive and Wild Capuchin Monkeys

Urinary cytokine measurements do not reflect surgery‐induced inflammation in rhesus macaques

In vivo deciduous dental eruption in LuiKotale bonobos and Gombe chimpanzees

Contact Info

Product

Resources

About