Differences in the Virulence of Plasmodium Knowlesi for Macaca Irus (Fascicularis) of Philippine and Malayan Origins *

Lh, Schmidt; Fradkin, Rochelle; Harrison, Janet; Rn, Rossan

doi:10.4269/ajtmh.1977.26.612

Cited by 41 publications

(30 citation statements)

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“…Thus, viral dynamics in cynomolgus macaques may have resulted in reduced virally induced cytopathicity giving rise to better preservation of immune responses and, ultimately, an attenuation of disease course compared to that seen in Indian rhesus macaques. In- deed, there is evidence that pathogenicity of other viral, bacterial, and parasitic microbes is also attenuated in cynomolgus macaques (5,6,18).…”

Section: Discussionmentioning

confidence: 99%

Pathogenicity of Simian-Human Immunodeficiency Virus SHIV-89.6P and SIVmac Is Attenuated in Cynomolgus Macaques and Associated with Early T-Lymphocyte Responses

Reimann

Parker

Seaman

et al. 2005

J Virol

119

115

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Because most studies of AIDS pathogenesis in nonhuman primates have been performed in Indian-origin rhesus macaques (Macaca mulatta), little is known about lentiviral pathogenicity and control of virus replication following infection of alternative macaque species. Here, we report the consequences of simian-human immunodeficiency virus SHIV-89.6P and SIVmac251 infection in cynomolgus (Macaca fascicularis) and rhesus macaques of Chinese origin. Compared to the pathogenicity of the same viruses in Indian rhesus macaques, both cynomolgus and Chinese rhesus macaques showed lower levels of plasma virus. By 9 to 10 months after infection, both viruses became undetectable in plasma more frequently in cynomolgus than in either Chinese or Indian rhesus macaques. Furthermore, after SHIV-89.6P infection, CD4؉ T-cell numbers declined less and survival was longer in cynomolgus and Chinese rhesus macaques than in Indian rhesus macaques. This attenuated pathogenicity was associated with gamma interferon ELISPOT responses to Gag and Env that were generated earlier and of higher frequency in cynomolgus than in Indian rhesus macaques. Cynomolgus macaques also developed higher titer neutralizing antibodies against SHIV-89.6 at 10 and 20 weeks postinoculation than Indian rhesus macaques. These studies demonstrate that the pathogenicity of nonhuman primate lentiviruses varies markedly based on the species or geographic origin of the macaques infected and suggest that the cellular immune responses may contribute to the control of pathogenicity in cynomolgus macaques. While cynomolgus and Chinese rhesus macaques provide alternative animal models of lentiviral infection, the lower levels of viremia in cynomolgus macaques limit the usefulness of infection of this species for vaccine trials that utilize viral load as an experimental endpoint.Nonhuman primates infected with naturally occurring or genetically engineered lentiviruses serve as important animal models for evaluating the efficacy of candidate AIDS vaccines (9,14). Studies in which macaques are immunized with new vaccine prototypes and subsequently challenged with pathogenic lentiviruses help to determine which vaccine products are best advanced to human clinical trials. The vast majority of AIDS vaccine/challenge data has been generated in rhesus macaques of Indian origin. An extensive knowledge of the genetics of Indian rhesus macaques has allowed detailed characterizations of major histocompatibility complex (MHC)-restricted immune responses elicited during vaccination and challenge (1, 17). However, infection of alternative macaque species such as cynomolgus or rhesus macaques from different geographic origins could provide information on comparative pathogenicity and provide an opportunity to examine diverse responses to viral infections.Rhesus macaques of Chinese origin, both wild and captive, are more plentiful than Indian origin rhesus macaques. Preliminary observations suggest that important genetic differences may exist between regional populations of rhesus macaques ...

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Section: Discussionmentioning

confidence: 99%

Pathogenicity of Simian-Human Immunodeficiency Virus SHIV-89.6P and SIVmac Is Attenuated in Cynomolgus Macaques and Associated with Early T-Lymphocyte Responses

Reimann

Parker

Seaman

et al. 2005

J Virol

119

115

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“…Although all macaques share a common ancestor up to 5 Ma, the sinica and fascicularis groups diverged from each other around 3 Ma (Tosi et al 2003; Perelman et al 2011). It is already known that different species (subspecies) of macaque react differently and show different levels of pathogenesis to human infectious diseases such as AIDS (Ling et al 2002) and malaria (Schmidt et al 1977). Therefore, it is highly desirable to fully assess the genetic backgrounds of the different macaque species.…”

Section: Introductionmentioning

confidence: 99%

Whole-Genome Sequencing of Tibetan Macaque (Macaca thibetana) Provides New Insight into the Macaque Evolutionary History

Fan

Zhao

et al. 2014

Molecular Biology and Evolution

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Macaques are the most widely distributed nonhuman primates and used as animal models in biomedical research. The availability of full-genome sequences from them would be essential to both biomedical and primate evolutionary studies. Previous studies have reported whole-genome sequences from rhesus macaque (Macaca mulatta) and cynomolgus macaque (M. fascicularis, CE), both of which belong to the fascicularis group. Here, we present a 37-fold coverage genome sequence of the Tibetan macaque (M. thibetana; TM). TM is an endemic species to China belonging to the sinica group. On the basis of mapping to the rhesus macaque genome, we identified approximately 11.9 million single-nucleotide variants), of which 3.9 million were TM specific, as assessed by comparison two Chinese rhesus macaques (CR) and two CE genomes. Some genes carried TM-specific homozygous nonsynonymous variants (TSHNVs), which were scored as deleterious in human by both PolyPhen-2 and SIFT (Sorting Tolerant From Intolerant) and were enriched in the eye disease genes. In total, 273 immune response and disease-related genes carried at least one TSHNV. The heterozygosity rates of two CRs (0.002617 and 0.002612) and two CEs (0.003004 and 0.003179) were approximately three times higher than that of TM (0.000898). Polymerase chain reaction resequencing of 18 TM individuals showed that 29 TSHNVs exhibited high allele frequencies, thus confirming their low heterozygosity. Genome-wide genetic divergence analysis demonstrated that TM was more closely related to CR than to CE. We further detected unusual low divergence regions between TM and CR. In addition, after applying statistical criteria to detect putative introgression regions (PIRs) in the TM genome, up to 239,620 kb PIRs (8.84% of the genome) were identified. Given that TM and CR have overlapping geographical distributions, had the same refuge during the Middle Pleistocene, and show similar mating behaviors, it is highly likely that there was an ancient introgression event between them. Moreover, demographic inferences revealed that TM exhibited a similar demographic history as other macaques until 0.5 Ma, but then it maintained a lower effective population size until present time. Our study has provided new insight into the macaque evolutionary history, confirming hybridization events between macaque species groups based on genome-wide data.

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“…In monkeys, results from early experimental studies (Butcher et al 2010;Schmidt et al 1977) have strongly suggested that some macaque species, for example, Macaca fascicularis (the crab-eating macaque) and possibly Macaca nemestrina (the pig-tailed macaque) and Macaca nigra (Celebes crested macaque), who are natural hosts for P. knowlesi, are able to control infection by P. knowlesi and turn it into a chronic infection. These macaque species are either wholly or partially distributed across the Southeast Asian islands where P. knowlesi is also distributed.…”

Section: Introductionmentioning

confidence: 99%

“…In contrast, other macaque species, with geographic distributions outside the range of P. knowlesi, for example, Macaca mulatta in mainland India and China, show virtually no ability to control infection to P. knowlesi and usually display a fulminant infection that quickly leads to death (Butcher 1996;Butcher et al 2010). Interestingly, in contrast to island population of M. fascicularis, mainland populations of M. fascicularis apparently have little to no ability to control infection by P. knowlesi and are similar to M. mulatta in this respect (Butcher et al 2010;Fooden 1994;Schmidt et al 1977). The possible molecular basis accounting for the differential susceptibility to P. knowlesi in different macaque species is unknown.…”

Section: Introductionmentioning

confidence: 99%

Molecular evolution of a malaria resistance gene (DARC) in primates

et al. 2012

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Genes involved in host-pathogen interactions are often strongly affected by positive natural selection. The Duffy antigen, coded by the Duffy antigen receptor for chemokines (DARC) gene, serves as a receptor for Plasmodium vivax in humans and for Plasmodium knowlesi in some nonhuman primates. In the majority of sub-Saharan Africans, a nucleic acid variant in GATA-1 of the gene promoter is responsible for the nonexpression of the Duffy antigen on red blood cells and consequently resistance to invasion by P. vivax. The Duffy antigen also acts as a receptor for chemokines and is expressed in red blood cells and many other tissues of the body. Because of this dual role, we sequenced a ~3,000-bp region encompassing the entire DARC gene as well as part of its 5' and 3' flanking regions in a phylogenetic sample of primates and used statistical methods to evaluate the nature of selection pressures acting on the gene during its evolution. We analyzed both coding and regulatory regions of the DARC gene. The regulatory analysis showed accelerated rates of substitution at several sites near known motifs. Our tests of positive selection in the coding region using maximum likelihood by branch sites and maximum likelihood by codon sites did not yield statistically significant evidence for the action of positive selection. However, the maximum likelihood test in which the gene was subdivided into different structural regions showed that the known binding region for P. vivax/P. knowlesi is under very different selective pressures than the remainder of the gene. In fact, most of the gene appears to be under strong purifying selection, but this is not evident in the binding region. We suggest that the binding region is under the influence of two opposing selective pressures, positive selection possibly exerted by the parasite and purifying selection exerted by chemokines.

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Differences in the Virulence of Plasmodium Knowlesi for Macaca Irus (Fascicularis) of Philippine and Malayan Origins *

Cited by 41 publications

References 0 publications

Pathogenicity of Simian-Human Immunodeficiency Virus SHIV-89.6P and SIVmac Is Attenuated in Cynomolgus Macaques and Associated with Early T-Lymphocyte Responses

Pathogenicity of Simian-Human Immunodeficiency Virus SHIV-89.6P and SIVmac Is Attenuated in Cynomolgus Macaques and Associated with Early T-Lymphocyte Responses

Whole-Genome Sequencing of Tibetan Macaque (Macaca thibetana) Provides New Insight into the Macaque Evolutionary History

Molecular evolution of a malaria resistance gene (DARC) in primates

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