Neopterin as a Tool for Primate Ecoimmunology: Current Knowledge, Practical Application, and New Directions From Captivity to the Wild
ABSTRACTNeopterin is a well‐established biomarker of interferon‐gamma‐mediated macrophage activation that indicates cell‐mediated immune system responses in humans. Because it is readily quantifiable in urine, it is increasingly used in nonhuman primates to study cell‐mediated immune functioning in relation to infectious diseases, but also environmental and individual factors, in both captive and wild primates. This review synthesizes our current knowledge on these topics with a focus on nonhuman primates. We cover the influence of various methodological factors during sampling and analysis on the reliability of neopterin measurements and give practical advice on how these factors can be mitigated. Furthermore, we address the advantages and disadvantages of different biological matrices in which neopterin can be measured and propose best practice guidelines for handling and storage of samples that consider challenges encountered during fieldwork. We conclude this review with an outlook on topics within primatology where neopterin, as a marker of cell‐mediated immune functioning, could become a valuable tool to answer applied questions and test evolutionary hypotheses about immune functioning in primates.
- Research Article
65
- 10.1098/rspb.1998.0418
- Jul 7, 1998
- Proceedings of the Royal Society of London. Series B: Biological Sciences
The effects of reproductive condition and exogenous melatonin on immune function were investigated in castrated European starlings, Sturnus vulgaris. Photorefractory and photostimulated starlings exposed to long days were implanted with melatonin or with blank capsules. Photostimulated starlings with blank capsules exhibited reduced splenocyte proliferation in response to the T-cell mitogen, concanavalin A, compared with the other long-day birds. Exogenous melatonin prevented the suppression of immune function by photostimulation. Photorefractory starlings, with or without melatonin implants, exhibited enhanced immune function compared with photostimulated starlings implanted with blanks. This enhancement was not mediated by endogenous melatonin, but appeared to be related to changes in reproductive state. In addition to the traditional costs of reproduction in birds (e.g. raising of young), there may be a cost of the reproductive state of starlings (i.e. whether they are photorefractory or photostimulated). These data are, we believe, the first to indicate a direct effect of reproductive state on immune function that is independent of both photoperiod (i.e., changes in the duration of melatonin secretion) and gonadal steroids.
- Research Article
365
- 10.1002/(sici)1096-8644(1997)25+<201::aid-ajpa8>3.0.co;2-6
- Jan 1, 1997
- American Journal of Physical Anthropology
The last decade has seen a resurgence of interest in laterality of function in primates, especially in hand use as it links to handedness and language in Homo sapiens. Manual lateralization of behavior in humans reflects asymmetry in cerebral structure, which must have evolved from nonhuman progenitors. To what extent is hand function lateralized in our nearest living relations? First, we address current issues of theory and methodology: statistics, measurement, variables, setting, sensory modality, and sample size. Specific topics include preference vs. performance, posture, bimanuality, inheritance, and arm asymmetry. We categorize the published literature in a descriptive, classificatory framework of five levels that range from Level 1, ambilaterality, to Level 5, human-like handedness. In a meta-analysis we put 241 published data-sets to a methodological test of seven criteria and code the 48 survivors onto the levels framework, by taxonomic grouping (prosimian, New World monkey, Old World monkey, ape, chimpanzee). Primates at Level 1 are mostly wild or naturalistic populations performing spontaneous species-typical behavior patterns. Most primates are at Levels 2 and 3, that is, individually lateralized to either side, especially on complex, demanding or practiced tasks, usually as devised in captive settings. Only chimpanzees show signs of population-level bias (Levels 4 and 5) to the right, but only in captivity and only incompletely. We conclude that nonhu- man primate hand function has not been shown to be lateralized at the species level—it is not the norm for any species, task, or setting, and so offers no easy model for the evolution of human handedness. Yrbk Phys Anthropol 40:201- 232, 1997. r 1997 Wiley-Liss, Inc.
- Research Article
2
- 10.1128/msystems.00478-22
- Jul 25, 2022
- mSystems
ABSTRACTPrimate hair and skin are substrates upon which social interactions occur and are host-pathogen interfaces. While human hair and skin microbiomes display body site specificity and immunological significance, little is known about the nonhuman primate (NHP) hair microbiome. Here, we collected hair samples (n = 158) from 8 body sites across 12 NHP species housed at three zoological institutions in the United States to examine the following: (1) the diversity and composition of the primate hair microbiome and (2) the factors predicting primate hair microbiome diversity and composition. If both environmental and evolutionary factors shape the microbiome, then we expect significant differences in microbiome diversity across host body sites, sexes, institutions, and species. We found our samples contained high abundances of gut-, respiratory-, and environment-associated microbiota. In addition, multiple factors predicted microbiome diversity and composition, although host species identity outweighed sex, body site, and institution as the strongest predictor. Our results suggest that hair microbial communities are affected by both evolutionary and environmental factors and are relatively similar across nonhuman primate body sites, which differs from the human condition. These findings have important implications for understanding the biology and conservation of wild and captive primates and the uniqueness of the human microbiome.IMPORTANCE We created the most comprehensive primate hair and skin data set to date, including data from 12 nonhuman primate species sampled from 8 body regions each. We find that the nonhuman primate hair microbiome is distinct from the human hair and skin microbiomes in that it is relatively uniform—as opposed to distinct—across body regions and is most abundant in gut-, environment-, and respiratory-associated microbiota rather than human skin-associated microbiota. Furthermore, we found that the nonhuman primate hair microbiome varies with host species identity, host sex, host environment, and host body site, with host species identity being the strongest predictor. This result demonstrates that nonhuman primate hair microbiome diversity varies with both evolutionary and environmental factors and within and across primate species. These findings have important implications for understanding the biology and conservation of wild and captive primates and the uniqueness of the human microbiome.
- Research Article
38
- 10.1007/s10764-014-9752-x
- Feb 22, 2014
- International Journal of Primatology
The endocrine system serves as a mediator by which the body integrates environmental cues to organize physiological alterations, including changes in immunocompetence. Hormones are central mechanisms that contribute to the onset and timing of key life history events, the allocation of time and energy between competing functions, and in general modulate phenotypic development and variation. Here we provide a very brief review of testosterone and immunity, which highlights the physiological costs that elevated testosterone levels can incur as a result of reproductive investments. We focus primarily on nonhuman primates where possible. Although there is substantial evidence that testosterone exerts some influences on immune responses, results from in vivo studies involving human and nonhuman primates have yielded equivocal results regarding such immunomodulatory actions. There may be several reasons for this, including variation in study design, immunological measures used, levels of other hormones present, host energy status, and even social conditions. We therefore review some of these potential methodological issues, concluding that increased care must be taken to analyze seasonal variability in energy budgets, to collect an adequate number of samples from known individuals, to account for status in the dominance hierarchy when applicable, and to use multiple measures of immunity. We must also seek to understand the collaborative effects of multiple hormones (particularly dehydroepiandrosterone and estradiol) with relation to their downstream immunological effects, assessing both individual and multiplicative actions in both males and females. Such efforts would benefit from the development of additional noninvasive immune measures for primates.
- Research Article
- 10.19227/jzar.v2i3.46
- Jul 31, 2014
- Journal of Zoo and Aquarium Research
Considerable variability in dietary and digestive strategies exists across primate taxa. Differences in wild primate diet are strongly reflected along the frugivory-folivory continuum, whereby the selection of fruits or leaves as primary diet is strongly linked to different digestive systems that optimizes the extraction of nutrients from these different food types to meet nutritional goals. Successful maintenance of wild primates in captivity require appropriate dietary husbandry to meet the different needs of these primate species. We examined the diet of six species of captive primates with primarily frugivorous or folivorous dietary management and how their nutritional intake corresponded to their provided diet of fruits/vegetables and leaves. Folivorous primates obtained major components of their diet (protein and carbohydrate) from their leave diet while frugivores obtained relatively equal proportions of these components from both food types. Folivorous primates obtained higher protein and fiber - Neutral Detergent Fiber (NDF) and Acid Detergent fiber (ADF) intake from their leave diets; and higher Non-Structural Carbohydrate (NSC) intake from their fruit diets. Frugivorous primates obtained higher NSC and lower fiber (ADF and NDF) intake from their fruit/vegetable diets. Higher fiber intake resulted in longer Transit Time (TT) for frugivores and longer Mean Retention Time (MRT) for folivores. Overall dietary NSC levels for folivores were close to the recommended upper limits for foregut fermenters; and dietary fiber levels were relatively high for frugivores. These results suggests that appropriate adjustments to the diet provided to these primates should be considered to reduce general intake of easily digestible carbohydrates by folivorous and evaluate the possible implications of high fiber diets for frugivores. Dietary husbandry for captive primates according to their dietary specializations should be considered whenever possible, within constrains of practical captive management.
- Research Article
88
- 10.1152/ajpregu.2000.278.6.r1401
- Jun 1, 2000
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
Energetic demands are high while energy availability is minimum during winter. To cope with this energetic bottleneck, animals exhibit numerous energy-conserving adaptations during winter, including changes in immune and reproductive functions. A majority of individual rodents within a population inhibits reproductive function (responders) as winter approaches. A substantial proportion of small rodents within a species, however, fails to inhibit reproduction (nonresponders) during winter in the field or in the laboratory when maintained in winter-simulated day lengths. In contrast, immune function is bolstered by short day lengths in some species. The specific mechanisms that link reproductive and immune functions remain unspecified. Leptin is a hormone produced by adipose tissue, and several studies suggest that leptin modulates reproductive and immune functions. The present study sought to determine if photoperiodic alterations in reproductive function and leptin concentrations are linked to photoperiod-modulated changes in immune function. Siberian hamsters (Phodopus sungorus) were housed in either long (LD 16:8) or short (LD 8:16) day lengths for 9 wk. After 9 wk, blood samples were collected during the middle of the light and dark phase to assess leptin concentrations. One week later, animals were injected with keyhole limpet hemocyanin to evaluate humoral immunity. Body mass, body fat content, and serum leptin concentrations were correlated with reproductive responsiveness to photoperiod; short-day animals with regressed gonads exhibited a reduction in these measures, whereas short-day nonresponders resembled long-day animals. In contrast, immune function was influenced by photoperiod but not reproductive status. Taken together, these data suggest that humoral immune function in Siberian hamsters is independent of photoperiod-mediated changes in leptin concentrations.
- Research Article
4
- 10.1046/j.1523-1747.2001.00014.x
- Nov 1, 2001
- Journal of Investigative Dermatology Symposium Proceedings
Immunologic characterization of HIV-specific DNA vaccine.
- Research Article
251
- 10.1371/journal.pone.0013963
- Nov 12, 2010
- PLoS ONE
BackgroundHost-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys.Methodology/Principal FindingsWe analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny.Conclusion/SignificanceOur analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in addition to dietary influences. These results contribute to the limited body of primate microbiome studies and provide a framework for comparative microbiome analysis between human and non-human primates as well as a comparative evolutionary understanding of the human microbiome.
- Research Article
- 10.3760/cma.j.issn.1673-4394.2019.02.008
- Mar 5, 2019
Objective To investigate the changes of cellular immunity and humoral immune function in children with bronchopneumonia and to analyze the clinical significance. Methods From April 2016 to September 2018, 60 patients with bronchial pneumonia in Heze City Hospital were recruited as observation group, and 60 healthy children were enrolled as control group.Immunoglobulin M(IgM), IgA and IgG were detected by immune rate turbidimetric method.Six-color flow cytometry was used to detect CD3+ , CD4+ /CD8+ , CD3+ /CD4+ and CD3+ /CD8+ in all subjects, the changes of indicators before treatment, during treatment and after treatment in the observation group and the control group were compared.At the same time, the levels of interleukin 10(IL-10), interleukin 6(IL-6) and tumor necrosis factor α(TNF-α)in two groups were compared too. Results Before treatment, during treatment and after treatment, IgM, IgG of the patients in the observation group was lower than that of the control group, the difference was statistically significant(all P<0.05). As the treatment progresses, IgM , IgA and IgG of the patients in the observation group increased, while the levels of the cells with CD3+ , CD4+ /CD8+ and CD3+ /CD4+ in the observation group were significantly lower than those in the control group, the difference was statistically significant(P<0.05), the CD3+ /CD8+ index in the observation group was significantly higher than that in the control group (P<0.05). The level of IL-10, IL-6 and TNF-αin the observation group were significantly higher than those in the control group(all P<0.05). Conclusion Children with bronchopneumonia showed different degrees of imbalance of cellular immunity and humoral immune.Detection of children's immune function index may be used to evaluate the therapeutic effect and the prognosis of children with bronchial pneumonia. Key words: Cellular immunity; Humoral immunity; Children with bronchopneumonia; Clinical significance
- Discussion
19
- 10.3201/eid2207.151837
- Jul 1, 2016
- Emerging Infectious Diseases
Naturally Circulating Hepatitis A Virus in Olive Baboons, Uganda
- Research Article
23
- 10.1097/01.mnh.0000232876.04975.33
- Jul 1, 2006
- Current Opinion in Nephrology & Hypertension
The majority of uric acid nephrolithiasis in humans occurs in the absence of frank hyperuricosuria and is primarily a disease of excessively low urinary pH. Uric acid is substantially less soluble than urate salts so in low urine pH urate is protonated, thus favoring precipitation even under what is considered physiologic concentrations of total urinary uric acid/urate. This commentary examines the rationales behind the existence of uric acid in urine and body fluids in vertebrate evolution. The purpose of uric acid in arthropod, avian and reptilian species is to enable nitrogen excretion in solid state without loss of water. The re-emergence of uric acid in higher primates as an end product of metabolism is intriguing since urea functions perfectly well as a nitrogenous waste. Uric acid must purvey important physiologic functions in primate biology. Numerous roles of uric acid as an antioxidant, immune signaling molecule, and a defender of circulatory integrity have recently been proposed. There is little doubt that uric acid serves multiple important functions in higher primates. It is also conceivable, however, that this important molecule when present in the wrong concentration or context can lead to undesirable phenotypes.
- Research Article
10
- 10.3892/ol.2017.7631
- Dec 15, 2017
- Oncology Letters
This study aims to comparatively analyze the impact of laparoscopic myomectomy (LM) and transcervical resection of myoma (TCRM) on ovarian function, immune function and quality of sexual life of patients with hysteromyoma. Two hundred and forty patients with hysteromyoma admitted into the Second Affiliated Hospital of Zhengzhou University from June 2014 to June 2016 were divided into laparoscopic myomectomy group (LM group, n=120) and transcervical resection of myoma group (TCRM group, n=120) according to random figure table. The difference between the two surgical methods were compared among hysteromyoma patients of different age in the following aspects: perioperative indicators, ovarian function, immune function and quality of sexual life before treatment and after operation. 1) there was no significant difference in age structure between LM and TCRM group (P>0.05). 2) There were no significant differences in the amount of bleeding, operative time, analgesics usage rate between the groups (P>0.05), but the anal exhaust time, postoperative ambulation time, hospitalization time and hospitalization costs in TCRM group were significantly less than that in LM group, the difference was statistically significant (P<0.01). 3) Before treatment and in the 3rd, and 6th month after operation, there was no significant difference on follicle stimulating hormone (FSH), luteinizing hormone (LH) or estradiol (E2) level between the two groups (P>0.05); but in the 3rd month after operation, the level of E2 decreased remarkably, with FSH and LH level increased significantly compared with the 6th month after operation and before treatment (P<0.05). 4) Compared with the preoperative status, there was no significant decrease in humoral immunity (IgG, IgA, IgM) and cellular immune function (CD4+, CD8+) in TCRM group at the 3rd and 6th month after operation (P>0.05). While at the 3rd month after operation, the levels of CD4+, CD8+ were decreased significantly in comparison to those at the 6th month after operation (P<0.05), but the levels of IgG, IgA and IgM were not decreased significantly (P>0.05). 5) There was no significant difference in the quality of sexual life between the two groups before operation or at the 3rd and 6th month after operation (P>0.05). In recent years, endoscopic treatment has become the main treatment evolution of hysteromyoma, patients of all ages are paying attention to the preservation of the uterus. This study showed that TCRM is approaching through the natural cavity, which has the features of less damage to body, faster recovery and lower cost of hospitalization than LM. The two surgical methods have no obvious influence on ovarian function, immune function and quality of sexual life.
- Research Article
34
- 10.1093/beheco/arm099
- Oct 22, 2007
- Behavioral Ecology
Male ornaments may advertise genetic benefits to females choosing mates. These benefits may come in the form of genes for resistance to parasites and disease. Thus, females that prefer more ornamented males as mates may receive genes for enhanced immune system function for their offspring. The common yellowthroat (Geothlypis trichas) is the only species to date in which a male plumage ornament (size of the black facial mask) is known to be related to extrapair mating, and extrapair young are more immunocompetent than their within-pair half-sibs (at least in colder years). To investigate whether male mask size signals superior immune function, we examined male ornaments (mask and bib size and color) in relation to measures of overall health (hematocrit) and immune system function (plasma immunoglobulin G [IgG] concentration and cutaneous immune activity). We also investigated the role that testosterone may play in mediating the relationship between ornaments and immunity. Male mask size was correlated positively with IgG level, suggesting that male mask size may indicate humoral immunity. However, mask size was correlated negatively with hematocrit and cutaneous immune activity (our measure of nestling immunocompetence). Bib size and color were not related to these indices of immune function or health. Plasma testosterone level was neither related to immune function or health nor to the expression of male ornaments. These results suggest that there might be a trade-off between immune system components, as well as between immunity and the production or advertisement of male ornaments.
- Research Article
88
- 10.1371/journal.pntd.0002140
- Mar 28, 2013
- PLoS Neglected Tropical Diseases
Balantidiasis is considered a neglected zoonotic disease with pigs serving as reservoir hosts. However, Balantidium coli has been recorded in many other mammalian species, including primates. Here, we evaluated the genetic diversity of B. coli in non-human primates using two gene markers (SSrDNA and ITS1-5.8SDNA-ITS2). We analyzed 49 isolates of ciliates from fecal samples originating from 11 species of captive and wild primates, domestic pigs and wild boar. The phylogenetic trees were computed using Bayesian inference and Maximum likelihood. Balantidium entozoon from edible frog and Buxtonella sulcata from cattle were included in the analyses as the closest relatives of B. coli, as well as reference sequences of vestibuliferids. The SSrDNA tree showed the same phylogenetic diversification of B. coli at genus level as the tree constructed based on the ITS region. Based on the polymorphism of SSrDNA sequences, the type species of the genus, namely B. entozoon, appeared to be phylogenetically distinct from B. coli. Thus, we propose a new genus Neobalantidium for the homeothermic clade. Moreover, several isolates from both captive and wild primates (excluding great apes) clustered with B. sulcata with high support, suggesting the existence of a new species within this genus. The cysts of Buxtonella and Neobalantidium are morphologically indistinguishable and the presence of Buxtonella-like ciliates in primates opens the question about possible occurrence of these pathogens in humans.
- Research Article
44
- 10.1016/j.zool.2016.01.001
- Feb 2, 2016
- Zoology
Sources of variation in hair cortisol in wild and captive non-human primates
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