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PubMed1989

Phenotypic and functional differences in NK and LAK cells in the peripheral blood of sooty mangabeys and rhesus macaques.

Greater than 75% of the sooty mangabey monkeys at the Yerkes Regional Primate Research Center are naturally infected with SIV without any apparent clinical symptomology. On the other hand, experimental infection of rhesus macaques with SIV results in a clinical syndrome similar to human AIDS. These differences with regard to SIV infection prompted us to examine the natural immunosurveillance system of peripheral blood mononuclear cells (PBMC) from SIV-infected and uninfected monkeys of these two species. Phenotypic and functional studies of precursor and effector NK and LAK cells in the PBMC from these two species were carried out using monoclonal reagents, flow microfluorometry (FMF), and the standard in vitro 51Cr release assay against prototype K562 (NK sensitive) and RAJI (NK resistant, LAK susceptible) target cell lines. Data indicate that both NK and LAK cell activities in the PBMC of sooty mangabeys were significantly (P less than 0.01) greater than those in rhesus macaques. The predominant NK effector cells and LAK cell precursors were shown to be Leu 19-CD8+ in the PBMC of sooty mangabeys and Leu19+ CD8- in the PBMC of rhesus macaques as determined by panning depletion techniques and FMF analysis. On the other hand, the predominant LAK effector cells were found to be dual marked Leu 19+ CD8+ in rhesus macaques and Leu 19- CD8+ in sooty mangabeys. These qualitative and quantitative differences were not due to SIV infection of these two species since PBMC from both SIV-seropositive and virus-positive and SIV-sero-negative and virus-negative monkeys gave similar results. Moreover, of importance is the finding that the functional NK and LAK precursor cells are CD8+ and CD8- in sooty mangabeys and rhesus macaques, respectively. These data may have implications for the natural SIV/SMM virus-positive asymptomatic state of sooty mangabeys and may provide useful tools for tracing the ontogeny and lineage derivation of NK and LAK cells.

Animals↗

PubMed2006

Reduced TCOF1 mRNA level in a rhesus macaque with Treacher Collins-like syndrome: further evidence for haploinsufficiency of treacle as the cause of disease.

Mutations in the human gene TCOF1 cause a mandibulofacial dysostosis known as Treacher Collins syndrome (TCS). An infant rhesus macaque (Macaca mulatta) that displayed the TCS phenotype was identified at the California National Primate Research Center. The TCOF1 coding region was cloned from a normal rhesus macaque and sequenced. The rhesus macaque homolog of TCOF1 is 91.6% identical in cDNA sequence and 93.8% identical in translated protein sequence compared to human TCOF1. Sequencing of TCOF1 in the TCS-affected rhesus macaque showed no mutations within the coding region or splice sites; however, real-time quantitative PCR showed an 87% reduction of spleen TCOF1 mRNA level in the TCS affected macaque when compared with normal macaque spleen.

Amino Acid Sequence↗

PubMed2002

The rhesus macaque as an animal model for pelvic organ prolapse.

OBJECTIVE: The purpose of this study was to characterize the pelvic floor of the rhesus macaque as an experimental model for human pelvic organ prolapse and to initiate an evaluation of the effects of estradiol and progesterone on the rhesus paravaginal attachment. STUDY DESIGN: Histologic specimens were prepared from the paravaginal attachment of 13 oophorectomized rhesus macaques. Three animals were treated with estradiol; 6 animals were treated with estradiol and progesterone, and 4 animals were untreated (hormone deprived). Immunocytochemistry was used to localize steroid receptors in the paravaginal attachment. RESULTS: Spontaneous pelvic organ prolapse was observed in rhesus macaques. The paravaginal attachment is comprised of dense collagen and elastic fibers that infiltrate the levator ani muscle. The fibroblasts of this attachment are estrogen and progesterone receptor positive, and the receptors are hormone responsive. CONCLUSION: The rhesus macaque has pelvic floor anatomy that is similar to women and makes an excellent experimental model for the study of prolapse. The rhesus paravaginal attachment is ligamentous and hormone sensitive. Its fibroblast activity may be modified by estrogen treatment in a manner similar to that reported in human pelvic connective tissue. The connective tissue of the paravaginal attachment interdigitates with the levator ani muscle cells, which suggests that this muscle plays a critical role in pelvic floor support.

Animals↗

PubMed2005

Genetic characterization of Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta).

Genetic differences between Indian-origin and Chinese-origin rhesus macaques are as great as those between some primate species and can influence the results of experiments in which both are used as animal models for the study of the same human diseases. Unfortunately, many breeding facilities do not know with certainty the origin of the founders of their rhesus breeding colonies. Here I summarize the most definitive of the genetic traits among the microsatellite (STR) loci and mitochondrial DNA sequences that my laboratory previously reported to characterize Indian-origin and Chinese-origin rhesus macaques and then estimate the frequencies of these traits and their reliability as indicators of country of origin. The expression of diagnostic traits at two or more of four different unlinked loci provides a nearly 100% reliability in distinguishing rhesus macaques of Indian and Chinese origin.

Animals↗

PubMed1994

Gel electrophoretic analysis of rhesus macaque major histocompatibility complex class II DR molecules.

Rhesus macaque MHC class II DR molecules were isolated from radiolabeled B-cell line extracts by immunoprecipitation with the mAbs 7.3.19.1 and B8.11.2 and subsequently analyzed by 2D-gel electrophoresis. The B-cell lines used for this study were obtained from monkeys that are homozygous for the Mamu-DR region as defined by serologic techniques. Some of these animals have been selectively bred and originate from consanguineous matings. These analyses show that monkeys with the same allotyping may express different types of DR molecules. As in humans, the number of DR molecules expressed per haplotype is not constant and varies from 1 to 3, depending on the serologically defined Mamu-DR specificity, whereas it has been shown that the number of Mamu-DRB genes present per haplotype varies from 2 to 6. Therefore the present study also demonstrates that some of the rhesus macaque DR regions contain one or more pseudogenes.

Animals↗

PubMed2000

Conserved MHC class I peptide binding motif between humans and rhesus macaques.

Since the onset of the HIV pandemic, the use of nonhuman primate models of infection has increasingly become important. An excellent model to study HIV infection and immunological responses, in particular cell-mediated immune responses, is SIV infection of rhesus macaques. CTL epitopes have been mapped using SIV-infected rhesus macaques, but, to date, a peptide binding motif has been described for only one rhesus class I MHC molecule, Mamu-A*01. Herein, we have established peptide-live cell binding assays for four rhesus MHC class I molecules: Mamu-A*11, -B*03, -B*04, and -B*17. Using such assays, peptide binding motifs have been established for all four of these rhesus MHC class I molecules. With respect to the nature and spacing of crucial anchor positions, the motifs defined for Mamu-B*04 and -B*17 present unique features not previously observed for other primate species. The motifs identified for Mamu-A*11 and -B*03 are very similar to the peptide binding motifs previously described for human HLA-B*44 and -B*27, respectively. Accordingly, naturally processed peptides derived from HLA-B*44 and HLA-B*27 specifically bind Mamu-A*11 and Mamu-B*03, respectively, indicating that conserved MHC class I binding capabilities exist between rhesus macaques and humans. The definition of four rhesus MHC class I-specific motifs expands our ability to accurately detect and quantitate immune responses to MHC class I-restricted epitopes in rhesus macaques and to rationally design peptide epitope-based model vaccine constructs destined for use in nonhuman primates.

Alleles↗

PubMed1995

Structure and diversity of the T-cell receptor alpha chain in rhesus macaque and chimpanzee.

We cloned and sequenced cDNA for the TCRAC1 of a healthy rhesus monkey and chimpanzee. TCRAC1 from both nonhuman primates show extensive conservation compared to the human sequence and to other mammals. A possible primate-specific insertion near the hinge region of the TCRAC1 region is described. Characterization of 18 rhesus macaque and eight chimpanzee TCRA chain cDNA clones derived from inverse PCR revealed 12 different TCRAV and 16 different TCRAJ regions which corresponded closely to known human counterparts. One functional rhesus macaque TCRDV-TCRAJ rearrangement was detected, suggesting a genomic organization of the macaque TCRD locus which is similar to humans. At the genomic level, a single TCRAC1 gene segment was detected in rhesus macaque and chimpanzee. The close phylogenetic relationship between primates shown here for TCRA chain components supports the use of these species as animal models of human immune-mediated disease.

Amino Acid Sequence↗

PubMed2005

A computational resource for the prediction of peptide binding to Indian rhesus macaque MHC class I molecules.

Non-human primates, in general, and Indian rhesus macaques, specifically, play an important role in the development and testing of vaccines and diagnostics destined for human use. To date, several frequently expressed macaque MHC molecules have been identified and their binding specificities characterized in detail. Here, we report the development of computational algorithms to predict peptide binding and potential T cell epitopes for the common MHC class I alleles Mamu-A*01, -A*02, -A*11, -B*01 and -B*17, which cover approximately two thirds of the captive Indian rhesus macaque populations. We validated this method utilizing an SIV derived data set encompassing 59 antigenic peptides. Of all peptides contained in the SIV proteome, the 2.4% scoring highest in the prediction contained 80% of the antigenic peptides. The method was implemented in a freely accessible and user friendly website at . Thus, we anticipate that our approach can be utilized to rapidly and efficiently identify CD8+ T cell epitopes recognized by rhesus macaques and derived from any pathogen of interest.

Algorithms↗

PubMed2006

Evaluation and comparative analysis of a technique for laparoscopic ovariectomy in rhesus macaques (Macaca mulatta).

Surgical ovariectomy is commonly performed to support studies involving the rhesus macaque (Macaca mulatta). Traditionally, these procedures have been performed via laparotomy. We developed a laparoscopic approach to reduce surgical pain, decrease convalescence times, and reduce the total number of animals necessary to obtain valuable scientific data in studies requiring repeated intra-abdominal access in conjunction with ovariectomy. We used our new technique to perform laparoscopic ovariectomy on 8 adult female rhesus macaques; 2 additional animals underwent ovariectomy via laparotomy; data for these prospective groups were compared with retrospective data from conventionally ovariectomized macaques. The surgical time (ST; mean +/- standard error) for the laparoscopic procedures was 68 +/- 3 min, with a return-to-group time (RTG) of 8 +/- 1 d. In comparison, ST for the retrospective group was 54 +/- 3 min, with a mean RTG of 33 +/- 5 d (range, 15 to 60 d). ST differed significantly between groups. ST for the laparoscopic procedure was longer (mean difference, 14 min; 95% confidence interval, 6 to 21 min), but laparotomized animals consistently had higher RTG (6 d for the prospective group [n = 2] and 25 d for the retrospective group [n = 9]). All study animals had estradiol levels of less than 5.6 pg/ml at 6 mo after surgery. We therefore conclude that laparoscopic ovariectomy of rhesus macaques is a safe and effective technique that may reduce postoperative recovery times.

Animals↗

PubMed1997

Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, an aromatase inhibitor, on sex skin colour in intact male rhesus macaques.

For defining the mechanism of control of sex skin colour in male rhesus macaques (Macaca mulatta) by hormones, a spectrocolorimeter was used to monitor skin redness after administration of testosterone, dihydrotestosterone (a non-aromatizable androgen), oestradiol or fadrozole (an aromatase inhibitor that blocks the conversion of testosterone to oestrogen). Skin blood flow was measured by laser doppler. Eight 9-14 kg, 5-9 year old intact male rhesus macaques were given hormone, fadrozole or vehicle treatments in a cross-over experimental design. Baseline blood flow and colour measurements were taken in four paired tattoo defined areas on the back and legs of each animal (one pair in non-sex skin, three pairs in sex skin). Colour and blood flow measurements were taken 3-4 days after the first dose and, thereafter, once a week for 3-6 weeks. Measurements taken after treatments were compared with baseline and intra-animal comparisons were made between treatment and vehicle for each animal. In all animals after administration of 4 mg testosterone kg-1 (long-acting), redness in the sex skin areas increased (P = 0.032) by day 3 and returned to baseline values by day 7. Administration of 1 mg oestradiol kg-1 day-1 for 4 days caused increased redness in all animals (P = 0.007) similar in magnitude to that caused by testosterone. Administration of 0.1 mg dihydrotestosterone kg-1 day-1 for 4 days resulted in a nonsignificant decrease in redness (P = 0.09) on days 3-7. Treatment with fadrozole (0.25-0.5 mg kg-1 day-1) for 3 weeks caused sex skin to become significantly less red during treatment (P = 0.014). There was no significant change in redness in non-sex skin areas during any treatment. Sex skin blood flow increased in animals treated with testosterone, correlating with increased redness (R = 0.906), while blood flow in non-sex skin was unchanged. Increased redness after treatment with testosterone and oestrogen, no change in redness with treatment with dihydrotestosterone and a decrease in redness after treatment with fadrozole support the conclusion that oestrogen controls sex skin redness, and testosterone acts indirectly through conversion to oestrogen to cause increased sex skin redness in male rhesus macaques.

Animals↗

PubMed1997

Molecular cloning and comparative analysis of the rhesus macaque costimulatory molecules CD80 (B7-1) and CD86 (B7-2).

To facilitate analysis of the role of costimulatory molecules in a nonhuman primate model, we cloned and sequenced the CD80 (B7-1) and CD86 (B7-2) costimulatory molecules from rhesus macaques. Rhesus CD80 and CD86 were highly homologous to their human counterparts, with overall amino acid homologies of greater than 90%, and were specifically recognized by murine antihuman CD80 or CD86 monoclonal antibodies. Stable cell lines expressing rhesus CD80 or CD86 induced proliferation of suboptimally activated CD4+ T cells and transcription of cytokine mRNA. Both CD80 and CD86 were able to provide costimulation for interferon-gamma and IL-2 synthesis by rhesus CD4+ T cells, but CD80 costimulation also resulted in synthesis of IL-4 and IL-10. The high degree of homology between the rhesus and the human CD80 and CD86 molecules should facilitate analysis of therapeutic interventions directed at this costimulatory pathway in nonhuman primates.

Amino Acid Sequence↗

PubMed1986

Pathogenesis of simian AIDS in rhesus macaques inoculated with the SRV-1 strain of type D retrovirus.

Type D retrovirus was isolated from rhesus macaques with simian acquired immunodeficiency syndrome (SAIDS) and transmitted to healthy rhesus macaques with tissue culture medium containing the virus. The clinical, immunologic, and lymph node morphologic changes were observed in 9 rhesus macaques for 52 weeks after inoculation. A spectrum of clinical signs developed including early death, persistent SAIDS, and apparent remission. Animals that died or developed persistent SAIDS had characteristic lymphoid depletion, persistently depressed peripheral blood mononuclear cell (PBMC) mitogenic response, and decreased serum immunoglobulins. The SAIDS retrovirus (SRV) was recovered from PBMC of 8 of the animals after inoculation. Virus could not be recovered from PBMC of one animal in remission, but this animal developed serum-neutralizing antibodies to SRV after inoculation. Seven of the animals seroconverted to SRV after inoculation, all 9 were seronegative for human T-lymphotropic virus-III, and 5 animals tested were seronegative to human T-lymphotropic virus-I. These findings support the etiologic role of the type D retrovirus in SAIDS and further define the pathogenesis of this disease.

Acquired Immunodeficiency Syndrome↗

PubMed1983

Female sexual behavior displayed by androgenized female rhesus macaques.

Adult, prenatally androgenized female rhesus macaques (female pseudohermaphrodites) that had been ovariectomized were treated with estradiol benzoate (20 micrograms/day) and paired with males at weekly intervals for 4 weeks beginning on Day 12 of injection. Their sexual behavior was compared to that of a control group of females. The sexual behavior of the males toward the two groups of genetic females (control females with normal female genitalia and hermaphrodites with well-formed male genitalia) was also observed. Females and hermaphrodites were equally receptive to male invitations to copulate. Although there were some differences in the specific components of proceptive behavior displayed by the two groups, the overall differences were negligible. Earlier studies had shown that infant and juvenile hermaphrodites resemble males in patterns of play and sexual behavior. When treated with testosterone as adults and paired with receptive females, they displayed mounting patterns typical of males--one of seven hermaphrodites achieved intromission and ejaculated. It has now been demonstrated that when treated with estrogen and paired with males, they responded as females. Hence, the capacity to behave sexually as males is not incompatible with the capacity to respond sexually as females under certain hormonal and environmental conditions.

Aggression↗

PubMed2005

Ordinal judgments and summation of nonvisible sets of food items by two chimpanzees and a rhesus macaque.

Two chimpanzees and a rhesus macaque rapidly learned the ordinal relations between 5 colors of containers (plastic eggs) when all containers of a given color contained a specific number of identical food items. All 3 animals also performed at high levels when comparing sets of containers with sets of visible food items. This indicates that the animals learned the approximate quantity of food items in containers of a given color. However, all animals failed in a summation task, in which a single container was compared with a set of 2 containers of a lesser individual quantity but a greater combined quantity. This difficulty was not overcome by sequential presentation of containers into opaque receptacles, but performance improved if the quantitative difference between sizes was very large.

Animals↗

PubMed2006

Long lasting control and lack of pathogenicity of the attenuated Rev-independent SIV in rhesus macaques.

A cohort of 22 rhesus macaques of Indian origin infected as neonates, juveniles, or adults by Rev-independent strains of SIV was monitored over several years. After the initial acute phase, virus replication was controlled and plasma virus loads were persistently below the threshold of the assay. The animals were monitored for up to 7.6 years after infection for viral loads, cellular and humoral immune responses, hematological changes, and overall health and no signs of immune dysfunction or AIDS were observed. This study represents several years of additional observation compared to the previously published results, and indicates that the Rev-independent SIV clones tested do not cause AIDS-like progressive disease within 7.6 years from infection. All the animals showed persistent humoral and cellular SIV-specific immune responses, consistent with chronic infection. Different Rev-independent SIV strains showed similar properties and lack of pathogenicity. Multicolor flow cytometric analysis demonstrated preservation of the Central Memory subset of T cells in the attenuated SIV-infected animals. This study demonstrates a potent, long-lasting control of the Rev-independent attenuated SIV in macaques independent of the age at virus exposure.

Animals↗

PubMed1993

Analysis of simian immunodeficiency virus sequence variation in tissues of rhesus macaques with simian AIDS.

One rhesus macaque displayed severe encephalomyelitis and another displayed severe enterocolitis following infection with molecularly cloned simian immunodeficiency virus (SIV) strain SIVmac239. Little or no free anti-SIV antibody developed in these two macaques, and they died relatively quickly (4 to 6 months) after infection. Manifestation of the tissue-specific disease in these macaques was associated with the emergence of variants with high replicative capacity for macrophages and primary infection of tissue macrophages. The nature of sequence variation in the central region (vif, vpr, and vpx), the env gene, and the nef long terminal repeat (LTR) region in brain, colon, and other tissues was examined to see whether specific genetic changes were associated with SIV replication in brain or gut. Sequence analysis revealed strong conservation of the intergenic central region, nef, and the LTR. However, analysis of env sequences in these two macaques and one other revealed significant, interesting patterns of sequence variation. (i) Changes in env that were found previously to contribute to the replicative ability of SIVmac for macrophages in culture were present in the tissues of these animals. (ii) The greatest variability was located in the regions between V1 and V2 and from "V3" through C3 in gp120, which are different in location from the variable regions observed previously in animals with strong antibody responses and long-term persistent infection. (iii) The predominant sequence change of D-->N at position 385 in C3 is most surprising, since this change in both SIV and human immunodeficiency virus type 1 has been associated with dramatically diminished affinity for CD4 and replication in vitro. (iv) The nature of sequence changes at some positions (146, 178, 345, 385, and "V3") suggests that viral replication in brain and gut may be facilitated by specific sequence changes in env in addition to those that impart a general ability to replicate well in macrophages. These results demonstrate that complex selective pressures, including immune responses and varying cell and tissue specificity, can influence the nature of sequence changes in env.

Amino Acid Sequence↗

PubMed2002

Administration of recombinant rhesus interleukin-12 during acute simian immunodeficiency virus (SIV) infection leads to decreased viral loads associated with prolonged survival in SIVmac251-infected rhesus macaques.

The ability of recombinant rhesus interleukin-12 (rMamu-IL-12) administration during acute simian immunodeficiency virus SIVmac251 infection to influence the quality of the antiviral immune responses was assessed in rhesus macaques. Group I (n = 4) was the virus-only control group. Group II and III received a conditioning regimen of rMamu-IL-12 (10 and 20 microg/kg, respectively, subcutaneously [s.c.]) on days -2 and 0. Thereafter, group II received 2 microg of IL-12 per kg and group III received 10 microg/kg s.c. twice a week for 8 weeks. On day 0 all animals were infected with SIVmac251 intravenously. While all four group I animals and three of four group II animals died by 8 and 10 months post infection (p.i.), all four group III animals remained alive for >20 months p.i. The higher IL-12 dose led to lower plasma viral loads and markedly lower peripheral blood mononuclear cell and lymph node proviral DNA loads. During the acute viremia phase, the high-IL-12-dose monkeys showed an increase in CD3(-) CD8 alpha/alpha(+) and CD3(+) CD8 alpha/alpha(+) cells and, unlike the control and low-IL-12-dose animals, did not demonstrate an increase in CD4(+) CD45RA(+) CD62L(+) naive cells. The high-IL-12-dose animals also demonstrated that both CD8 alpha/alpha(+) and CD8 alpha/beta(+) cells produced antiviral factors early p.i., whereas only CD8 alpha/beta(+) cells retained this function late p.i. Long-term survival correlated with sustained high levels of SIV gag/pol and SIV env cytotoxic T lymphocytes and retention of high memory responses against nominal antigens. This is the first study to demonstrate the capacity of IL-12 to significantly protect macaques from SIV-induced disease, and it provides a useful model to more precisely identify correlates of virus-specific disease-protective responses.

Animals↗

PubMed1994

Intergroup grooming relations between alpha females in a population of free-ranging rhesus macaques.

Intergroup affiliation among female rhesus macaques, Macaca mulatta, was examined in the captive free-ranging colony of Morgan Island, S.C., USA. The provisioned colony has many social groups (35) and is maintained at a relatively high population density (21 animals/ha) with a relatively low adult male to female ratio (1:8.8). Focal and ad libitum samples were collected on 32 adults (3 males and 29 females) from two groups. Although infrequent, grooming was observed between adult females from different groups, and alpha females were the main participants in these interactions. Colony records indicated that none of the intergroup grooms was between females formerly from a common group. Relations between familiar neighboring groups may be maintained by a combination of both affiliative and aggressive behavior.

Animals↗