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PubMed2005

Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates.

The living Malagasy lemurs constitute a spectacular radiation of >50 species that are believed to have evolved from a common ancestor that colonized Madagascar in the early Tertiary period. Yet, at least 15 additional Malagasy primate species, some of which were relative giants, succumbed to extinction within the past 2,000 years. Their existence in Madagascar is recorded predominantly in its Holocene subfossil record. To rigorously test the hypothesis that all endemic Malagasy primates constitute a monophyletic group and to determine the evolutionary relationships among living and extinct taxa, we have conducted an ancient DNA analysis of subfossil species. A total of nine subfossil individuals from the extinct genera Palaeopropithecus and Megaladapis yielded amplifiable DNA. Phylogenetic analysis of cytochrome b sequences derived from these subfossils corroborates the monophyly of endemic Malagasy primates. Our results support the close relationship of sloth lemurs to living indriids, as has been hypothesized on morphological grounds. In contrast, Megaladapis does not show a sister-group relationship with the living genus Lepilemur. Thus, the classification of the latter in the family Megaladapidae is misleading. By correlating the geographic location of subfossil specimens with relative amplification success, we reconfirm the global trend of increased success rates of ancient DNA recovery from nontropical localities.

Animals↗
PubMed2005

Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain.

Primate genomes encode a variety of innate immune strategies to defend themselves against retroviruses. One of these, TRIM5alpha, can restrict diverse retroviruses in a species-specific manner. Thus, whereas rhesus TRIM5alpha can strongly restrict HIV-1, human TRIM5alpha only has weak HIV-1 restriction. The biology of TRIM5alpha restriction suggests that it is locked in an antagonistic conflict with the proteins encoding the viral capsid. Such antagonistic interactions frequently result in rapid amino acid replacements at the protein-protein interface, as each genetic entity vies for evolutionary dominance. By analyzing its evolutionary history, we find strong evidence for ancient positive selection in the primate TRIM5alpha gene. This selection is strikingly variable with some of the strongest selection occurring in the human lineage. This history suggests that TRIM5alpha evolution has been driven by antagonistic interactions with a wide variety of viruses and endogenous retroviruses that predate the origin of primate lentiviruses. A 13-aa "patch" in the SPRY protein domain bears a dense concentration of positively selected residues, potentially implicating it as an antiviral interface. By using functional studies of chimeric TRIM5alpha genes, we show that this patch is generally essential for retroviral restriction and is responsible for most of the species-specific antiretroviral restriction activity. Our study highlights the power of evolutionary analyses, in which positive selection identifies not only the age of genetic conflict but also the interaction interface where this conflict plays out.

Amino Acid Sequence↗
PubMed2005

Primate lentiviral virion infectivity factors are substrate receptors that assemble with cullin 5-E3 ligase through a HCCH motif to suppress APOBEC3G.

Cullin-Ring E3 ubiquitin ligases target substrates for ubiquitin-dependent, proteasome-mediated degradation and regulate critical cellular processes. These cullins assemble with cellular substrate receptor proteins through specific adaptor molecules. F-box- and BC-box-containing receptors use Skp1, ElonginB, and ElonginC as adaptors to recruit Cul1/Cul7 and Cul2/Cul5, respectively. At present, the determinants of Cul2 vs. Cul5 specificity for the BC-box-containing receptors are poorly defined. Here, we demonstrate that primate lentiviral Vif (virion infectivity factor) proteins represent previously uncharacterized substrate receptor proteins that contain divergent BC-box motifs. These molecules selectively assemble with a Cul5-E3 ligase to suppress the antiviral activity of autologous cytidine deaminase APOBEC3G. A previously unrecognized Hx5Cx(17-18)Cx(3-5)H motif that is highly conserved among all primate lentiviral Vif proteins was found to be critical for the selective assembly and activity of Vif-Cul5-E3 ligase. Non-primate lentiviral Vif proteins, which lack this HCCH motif, displayed reduced interaction with Cul5. These data suggest that in addition to target protein specificity, substrate receptor proteins play important roles in cullin selection and functional assembly of cullin-Ring E3 ligases. The discovery of these viral substrate receptor molecules that recruit Cul5 through distinct mechanisms from cellular proteins may facilitate the identification of additional cellular factors that regulate cellular functions through Cul5-E3 ligase. Motifs in Vif that are absent from cellular proteins could also be targets for the development of innovative therapeutics.

APOBEC-3G Deaminase↗
PubMed2005

Dental senescence in a long-lived primate links infant survival to rainfall.

Primates tend to be long-lived, and, except for humans, most primate females are able to reproduce into old age. Although aging in most mammals is accompanied by dental senescence due to advanced wear, primates have low-crowned teeth that wear down before old age. Because tooth wear alters crown features gradually, testing whether early dental senescence causes reproductive senescence has been difficult. To identify whether and when low-crowned teeth compromise reproductive success, we used a 20-year field study of Propithecus edwardsi, a rainforest lemur from Madagascar with a maximum lifespan of >27 years. We analyzed tooth wear in three dimensions with dental topographic analysis by using Geographical Information Systems (GIS) technology. We report that tooth wear exposes compensatory shearing blades that maintain dental function for 18 years. Beyond this age, female fertility remains high; however infants survive only if lactation seasons have elevated rainfall. Therefore, low-crowned teeth accommodate wear to a point, after which reproductive success closely tracks environmental fluctuations. These results suggest a tooth wear-determined, but rainfall-mediated, onset of reproductive senescence. Additionally, our study indicates that even subtle changes in climate may affect reproductive success of rainforest species.

Aging↗
PubMed2006

Natural selection and molecular evolution in primate PAX9 gene, a major determinant of tooth development.

Large differences in relation to dental size, number, and morphology among and within modern human populations and between modern humans and other primate species have been observed. Molecular studies have demonstrated that tooth development is under strict genetic control, but, the genetic basis of primate tooth variation remains unknown. The PAX9 gene, which codes for a paired domain-containing transcription factor that plays an essential role in the development of mammal dentition, has been associated with selective tooth agenesis in humans and mice, which mainly involves the posterior teeth. To determine whether this gene is polymorphic in humans, we sequenced approximately 2.1 kb of the entire four-exon region (exons 1, 2, 3 and 4; 1,026 bp) and exon-intron (1.1 kb) boundaries of 86 individuals sampled from Asian, European, and Native American populations. We provided evidence that human PAX9 polymorphisms are limited to exon 3 only and furnished details about the distribution of a mutation there in 350 Polish subjects. To investigate the pattern of selective pressure on exon 3, we sequenced ortholog regions of this exon in four species of New World monkeys and one gorilla. In addition, orthologous sequences of PAX9 available in public databases were also analyzed. Although several differences were identified between humans and other species, our findings support the view that strong purifying selection is acting on PAX9. New World and Old World primate lineages may, however, have different degrees of restriction for changes in this DNA region.

Amino Acid Sequence↗
PubMed2006

Phylogenetic comparisons suggest that distance from the locus control region guides developmental expression of primate beta-type globin genes.

Phylogenetic inferences drawn from comparative data on mammalian beta-globin gene clusters indicate that the ancestral primate cluster contained a locus control region (LCR) and five paralogously related beta-type globin loci (5'-LCR-epsilon-gamma-psieta-delta-beta-3'), with epsilon and gamma expressed solely during embryonic life. A gamma locus tandem duplication (5'-gamma(1)-gamma(2)-3') triggered gamma's evolution toward fetal expression but by a different trajectory in platyrrhines (New World monkeys) than in catarrhines (Old World monkeys and apes, including humans). In platyrrhine (e.g., Cebus) fetuses, gamma(1) at the ancestral distance from epsilon is down-regulated, whereas gamma(2) at increased distance is up-regulated. Catarrhine gamma(1) and gamma(2) acquired longer distances from epsilon (14 and 19 kb, respectively), and both are up-regulated throughout fetal life with gamma(1)'s expression predominating over gamma(2)'s. On enlarging the platyrrhine expression data, we find Aotus gamma is embryonic, Alouatta gamma is inactive at term, and in Callithrix, gamma(1) is down-regulated fetally, whereas gamma(2) is up-regulated. Of eight mammalian taxa now represented per taxon by embryonic, fetal, and postnatal beta-type globin gene expression data, four taxa are primates, and data for three of these primates are from this laboratory. Our results support a model in which a short distance (<10 kb) between epsilon and the adjacent gamma is a plesiomorphic character that allows the LCR to drive embryonic expression of both genes, whereas a longer distance (>10 kb) impedes embryonic activation of the downstream gene.

Animals↗
PubMed2002

Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates.

We demonstrate that the nuclear topological arrangement of chromosome territories (CTs) has been conserved during primate evolution over a period of about 30 million years. Recent evidence shows that the positioning of chromatin in human lymphocyte nuclei is correlated with gene density. For example, human chromosome 19 territories, which contain mainly gene-dense and early replicating chromatin, are located toward the nuclear center, whereas chromosome 18 territories, which consist mainly of gene-poor and later replicating chromatin, is located close to the nuclear border. In this study, we subjected seven different primate species to comparative analysis of the radial distribution pattern of human chromosome 18- and 19-homologous chromatin by three-dimensional fluorescence in situ hybridization. Our data demonstrate that gene-density-correlated radial chromatin arrangements were conserved during higher-primate genome evolution, irrespective of the major karyotypic rearrangements that occurred in different phylogenetic lineages. The evolutionarily conserved positioning of homologous chromosomes or chromosome segments in related species supports evidence for a functionally relevant higher-order chromatin arrangement that is correlated with gene-density.

Animals↗
PubMed1982

Glucocorticoid hormone resistance during primate evolution: receptor-mediated mechanisms.

The concentrations of total and protein-unbound plasma cortisol of New World monkeys are higher than those of Old World primates and prosimians. The urinary free-cortisol excretion also is increased markedly. However, there is no physiologic evidence of increased cortisol effect. These findings suggest end-organ resistance to glucocorticoids. This was confirmed by showing that the hypothalamic-pituitary adrenal axis is resistant to suppression by dexamethasone. To study this phenomenon, glucocorticoid receptors were examined in circulating mononuclear leukocytes and cultured skin fibroblasts from both New and Old World species. The receptor content is the same in all species, but the New World monkeys have a markedly decreased binding affinity for dexamethasone. Thus, the resistance of these species to the action of cortisol is due to the decreased binding affinity of the glucocorticoid receptor. This presumed mutation must have occurred after the bifurcation of Old and New World primates (approximately 60 x 10(6) yr ago) and before the diversion of the New World primates from each other (approximately 15 x 10(6) yr ago).

Animals↗
PubMed1987

Primate involucrins: antigenic relatedness and detection of multiple forms.

Hominoid apes (gorilla, chimpanzee, orangutan, gibbon), Old World monkeys (rhesus, cynomolgus), New World monkeys (owl, cebus), and a prosimian (lemur) express involucrin-like proteins in cultured keratinocytes. Primate involucrins can be precipitated with trichloroacetic acid, resolubilized at pH 8, and subsequently retain aqueous solubility in 67% ethanol. Polyacrylamide gel electrophoresis of keratinocyte extracts after this rapid partial purification has revealed in each species tested one (chimpanzee, orangutan, gibbon) or two (gorilla, rhesus, owl, cebus) antigenically crossreactive proteins that migrate in the vicinity of human involucrin. In the species examined further (gorilla, chimpanzee, rhesus), poly(A)+ mRNA isolated from the cultures directed the cell-free translation of polypeptides with mobilities similar to those extracted from the cells. From five cynomolgus monkeys, three different electrophoretic profiles were obtained, suggesting the existence of different alleles. Quantitative comparisons by a sensitive enzyme-linked immunosorbent assay indicated that certain primate involucrins have a higher density of antigenic determinants than the human protein, whereas others lack some determinant(s). In contrast to those from other species, all of which showed substantial crossreactivity, the lemur protein was minimally immunoreactive by immunoblotting and not clearly detected by solid-phase assay. The electrophoretic and antigenic differences displayed throughout the primate order suggest that this protein has been subject to relatively rapid evolution.

Animals↗
PubMed1987

Evolutionary relationship between the natural anti-Gal antibody and the Gal alpha 1----3Gal epitope in primates.

Anti-Gal is a natural antibody, which constitutes as much as 1% of circulating IgG in humans and displays a distinct specificity for the structure Gal alpha 1----3Gal. This glycosidic structure has been found on various tissues of many nonprimate mammals. A comparative study of the occurrence of anti-Gal versus the expression of the Gal alpha 1----3Gal epitope was performed in primates, and a distinct evolutionary pattern was observed. Whereas anti-Gal was found to be present in Old World monkeys and apes in titers comparable to those in humans, its corresponding antigenic epitope is abundantly expressed on erythrocytes of New World monkeys. Immunostaining with anti-Gal of glycolipids from New World monkey erythrocytes indicated that the molecules to which anti-Gal binds are similar to those found in rabbit and bovine erythrocytes. These findings indicate that there is an evolutionary reciprocity between New World and Old World primates in the production of the Gal alpha 1----3Gal structure and the antibody that recognizes it. The expression of the Gal alpha 1----3Gal epitope was evolutionarily conserved in New World monkeys, but it was suppressed in ancestral lineages of Old World primates. The suppression of this epitope was accompanied by the production of anti-Gal. The observed in vivo binding of anti-Gal to human normal senescent and some pathologic erythrocytes implies that the Gal alpha 1----3Gal epitope is present in man in a cryptic form.

Animals↗
PubMed1989

Cloning and sequencing of cDNA encoding baboon liver alcohol dehydrogenase: evidence for a common ancestral lineage with the human alcohol dehydrogenase beta subunit and for class I ADH gene duplications predating primate radiation.

The baboon has at least five alcohol dehydrogenases (ADH; alcohol:NAD+ oxidoreductase, EC 1.1.1.1) and has distinct liver and kidney class I isozymes. A rat liver class I ADH partial cDNA was used to screen a baboon liver cDNA library. A cDNA clone was isolated and sequenced and found to contain the entire coding region for baboon liver ADH, 12 nucleotides of the 5' noncoding region, and 256 nucleotides of the 3' noncoding region. The amino acid sequence deduced from this cDNA most closely resembles that of human liver ADH beta subunit (ADH-beta): 363 of 374 residues were identical. This suggested that baboon liver class I ADH is of the same ancestral lineage as the human ADH-beta. In contrast to human liver, only a single ADH-beta transcript is observed in baboon liver. A comparison of human and baboon ADH 3' noncoding regions suggests that a single nucleotide change in a polyadenylylation signal consensus sequence may, in part, be responsible for the generation of ADH-beta transcripts with variable-length 3' ends in human liver. A nucleotide substitution rate of 0.5 x 10(-9) substitutions per site per year for primate class I ADH genes was deduced from the data, which suggests that the alpha-beta gamma separation of human ADH genes occurred about 60 million years ago, and that primate class I ADH gene duplications predated primate radiation.

Alcohol Dehydrogenase↗
PubMed1990

Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks.

Phylogenetic analysis of DNA sequences from primates, rodents, lagomorphs, artiodactyls, carnivores, and birds strongly suggests that the order Rodentia is an outgroup to the other four mammalian orders and that Artiodactyla and Carnivora belong to a superordinal clade. Further, there is strong evidence against the Glires concept, which unites Lagomorpha and Rodentia. The radiation among Lagomorpha, Primates, and Artiodactyla--Carnivora is very bush-like, but there is some evidence that Lagomorpha has branched off first. Thus, the branching sequence for these five orders of mammals seems to be Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora. The branching date for Rodentia could be as early as 100 million years ago. The rate of nucleotide substitution in the rodent lineage is shown to be at least 1.5 times higher than those in the other four mammalian lineages.

Animals↗
PubMed1993

Brain structures and life-span in primate species.

In haplorhine primates, when the effect of body weight is removed, brain weight is correlated with maximum recorded life-span. In this paper we have analyzed the relationships between volumes of specific brain structures and life-span. When the effect of body weight is removed, the volumes of many brain structures are significantly, positively correlated with maximum recorded life-span. However, the volumes of the medulla and most first-order sensory structures do not correlate with life-span. The cerebellum is the brain structure that best correlates with life-span. Parts of the cerebellum are particularly vulnerable to age-related loss of mass in humans. For another measure of the life cycle, female reproductive age, a similar set of brain structures is significantly, positively correlated (again with the exceptions of the medulla and most first-order sensory structures). There are some differences between the structures correlated for life-span and female reproductive age. For example, the hippocampus and lateral geniculate nucleus correlate with female reproductive age but do not correlate with life-span. In strepsirhine primates, when the effect of body weight is removed, total brain weight does not significantly correlate with either life-span or female reproductive age. However, the volumes of some brain structures in strepsirhines do correlate with these life-cycle parameters. The centromedial complex of the amygdala is the only structure to correlate with life-span in both strepsirhine and haplorhine primates. This structure participates in the regulation of blood pressure and in the stress response, which may be key factors governing life-span.

Animals↗
PubMed1998

Tarsier-like locomotor specializations in the oligocene primate afrotarsius.

Tarsiers and extinct tarsier-like primates have played a central role in views of primate phylogeny and evolution for more than a century. Because of the importance of tarsiers in so many primatological problems, there has been particular interest in questions about the origin of tarsier specializations and the biogeography of early tarsioid radiations. We report on a new fossil of rare Afrotarsius that shows near identity to modern Tarsius in unique specializations of the leg, which provides information about the locomotor behavior and clarifies the phylogenetic position of this previously controversial primate. These specializations constitute evidence that Afrotarsius is a tarsiid, closely related to extant Tarsius; hence, it is now excluded from being a generalized sister taxon to Anthropoidea.

Animals↗
PubMed1999

Constructing primate phylogenies from ancient retrovirus sequences.

The genomes of modern humans are riddled with thousands of endogenous retroviruses (HERVs), the proviral remnants of ancient viral infections of the primate lineage. Most HERVs are nonfunctional, selectively neutral loci. This fact, coupled with their sheer abundance in primate genomes, makes HERVs ideal for exploitation as phylogenetic markers. Endogenous retroviruses (ERVs) provide phylogenetic information in two ways: (i) by comparison of integration site polymorphism and (ii) by orthologous comparison of evolving, proviral, nucleotide sequence. In this study, trees are constructed with the noncoding long terminal repeats (LTRs) of several ERV loci. Because the two LTRs of an ERV are identical at the time of integration but evolve independently, each ERV locus can provide two estimates of species phylogeny based on molecular evolution of the same ancestral sequence. Moreover, tree topology is highly sensitive to conversion events, allowing for easy detection of sequences involved in recombination as well as correction for such events. Although other animal species are rich in ERV sequences, the specific use of HERVs in this study allows comparison of trees to a well established phylogenetic standard, that of the Old World primates. HERVs, and by extension the ERVs of other species, constitute a unique and plentiful resource for studying the evolutionary history of the Retroviridae and their animal hosts.

Animals↗
PubMed1996

Inactivation of a novel neuropeptide Y/peptide YY receptor gene in primate species.

Neuropeptide Y (NPY), peptide YY (PYY), and pancreatic polypeptide (PP) belong to a family of structurally related peptides which have numerous functions in both neural and endocrine signaling. By homology screening, we cloned a novel gene sharing the highest homology with the NPY Y1 receptor gene from humans, rabbits, and several other species. This novel gene of rabbit encodes a functional NPY/PYY receptor, designated Y2b, which prefers NPY13-36 rather than [Leu31,Pro34]NPY despite its higher identity with the Y1 receptor. Although, at low levels, mRNA was detected in the tissues and brain regions, including hypothalamus. Further, sequence data revealed that this gene is the orthologue of the recently cloned mouse novel NPY receptor, Y5. However, our study demonstrates that the receptor function of this gene has been inactivated in primates by a frameshift mutation occurring early in primate evolution. This novel NPY receptor represents the first neurotransmitter receptor identified that has universally lost its receptor function in primate species. Interestingly, despite its inactivation in humans, the transcripts were abundantly detected in the heart and skeletal muscle, suggesting a novel function of the human gene.

Amino Acid Sequence↗
PubMedDate not supplied

Simian retrovirus infections: potential confounding variables in primate toxicology studies.

Various species of nonhuman primates are natural hosts for 6 exogenous retroviruses, including gibbon-ape leukemia virus (GaLV), simian sarcoma virus, simian T-lymphotropic virus (STLV), simian immunodeficiency virus (SIV), simian type D retrovirus (SRV), and simian foamy virus (SFV). These viruses establish persistent infections with a broad spectrum of pathogenic potential, ranging from highly pathogenic to nonpathogenic, depending on various host, virus, and environmental factors. Latent or subclinical infections are common, and various procedures associated with experimental protocols may lead to virus reactivation and disease. Adverse effects on toxicologic research by undetected retroviral infections can occur in several ways, including loss of experimental subjects (and statistical power) due to increased morbidity and mortality. In addition, results may be confounded by virus-induced clinical abnormalities, histologic lesions, alteration of physiologic parameters and responses, and interference with in vitro assays and/or destruction of primary cell cultures. Key clinical and epidemiological features of several important retroviruses are reviewed, with emphasis on viruses infecting species of macaques most commonly used as research subjects in primate toxicology studies. Examples of actual and potential confounding of toxicologic studies by retroviruses are discussed, including altered cytokine profiles in healthy STLV carriers, and clinical and pathological abnormalities induced by SRV infection. Adequate prestudy viral screening is critical to exclude retrovirus-infected primates from toxicologic research protocols and prevent potential confounding of research results.

Animals↗
PubMed2006

Age-related effects on the biological clock and its behavioral output in a primate.

In humans, activity rhythms become fragmented and attenuated in the elderly. This suggests an alteration of the circadian system per se that could in turn affect the expression of biological rhythms. In primates, very few studies have analyzed the effect of aging on the circadian system. The mouse lemur provides a unique model of aging in non-human primates. To assess the effect of aging on the circadian system of this primate, we recorded the circadian and daily rhythms of locomotor activity of mouse lemurs of various ages. We also examined age-related changes in the daily rhythm of immunoreactivities for vasoactive intestinal polypeptide (VIP) and arginine-vasopressin (AVP) in suprachiasmatic nucleus neurons (SCN), two major peptides of the biological clock. Compared to adult animals, aged mouse lemurs showed a significant increase in daytime activity and an advanced activity onset. Moreover, when maintained in constant dim red light, aged animals exhibited a shortening of the free-running period compared to adult animals. In adults, AVP immunoreactivity (ir) peaked during the second part of the day, and VIP ir peaked during the night. In aged mouse lemurs, the peaks of AVP ir and VIP ir were significantly shifted with no change in amplitude. AVP ir was most intense at the beginning of the night; whereas, VIP ir peaked at the beginning of the daytime. A weakened oscillator could account for the rhythmic disorders often observed in the elderly. Changes in the daily rhythms of AVP ir and VIP ir may affect the ability of the SCN to transmit rhythmic information to other neural target sites, and thereby modify the expression of some biological rhythms.

Aging↗