Evidence of simian retrovirus type D by polymerase chain reaction
Christian Z.R. Hwa
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorSheung Pun Tsai
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorJoAnn L. Yee
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorKoen K. Van Rompay
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorCorresponding Author
Jeffrey A. Roberts
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Correspondence
Jeffrey A. Roberts, Pathogen Detection Laboratory, California National Primate Research Center, University of California, Davis, CA, USA
Email: [email protected]
Search for more papers by this authorChristian Z.R. Hwa
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorSheung Pun Tsai
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorJoAnn L. Yee
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorKoen K. Van Rompay
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Search for more papers by this authorCorresponding Author
Jeffrey A. Roberts
Pathogen Detection Laboratory (PDL), California National Primate Research Center (CNPRC), University of California, Davis, CA, USA
Correspondence
Jeffrey A. Roberts, Pathogen Detection Laboratory, California National Primate Research Center, University of California, Davis, CA, USA
Email: [email protected]
Search for more papers by this authorAbstract
Background
Over the past few years, there have been reports of finding Simian retrovirus type D (SRV) in macaque colonies where some animals were characterized as antibody positive but virus negative raising questions about how SRV was transmitted or whether there is a variant strain detected by antibody but not polymerase chain reaction (PCR) in current use.
Methods
We developed a three-round nested PCR assay using degenerate primers targeting the pol gene to detect for SRV serotypes 1-5 and applied this newly validated PCR assay to test macaque DNA samples collected in China from 2010 to 2015.
Results
Using the nested PCR assay validated in this study, we found 0.15% of the samples archived on FTA® cards were positive.
Conclusions
The source of SRV infection identified within domestic colonies might have originated from imported macaques. The multiplex nested PCR assay developed here may supplement the current assays for SRV.
References
- 1Marx PA, Maul DH, Osborn KG, et al. Simian AIDS: isolation of a type D retrovirus and transmission of the disease. Science. 1984; 223: 1083-1086.
- 2Marx PA, Bryant ML, Osborn KG, et al. Isolation of a new serotype of simian acquired immune deficiency syndrome type D retrovirus from celebes black macaques (Macaca nigra) with immune deficiency and retroperitoneal fibromatosis. J Virol. 1985; 56: 571-578.
- 3Lerche NW, Marx PA, Osborn KG, et al. Natural history of endemic type D retrovirus infection and acquired immune deficiency syndrome in group-house rhesus monkeys. J Natl Cancer Inst. 1987; 79: 847-854.
- 4Gardner MB, Carlos MP, Luciw P. Simian Retroviruses. In: GP Wormser, ed. AIDS and Other Manifestations of HIV Infection, 4th edn. New York: Raven Press; 2004: 191-258.
10.1016/B978-012764051-8/50012-3 Google Scholar
- 5Gardner MB, Luciw PA. Animal models of AIDS. FASEB J. 1989; 3: 2593-2606.
- 6't Hart BA, Vervoordeldonk M, Heeney JL, Tak PP. Gene therapy in nonhuman primate models of human autoimmune disease. Gene Ther 2003; 10: 890-901.
- 7Van Rompay KK. Antiretroviral drug studies in nonhuman primates: a valid animal model for innovative drug efficacy and pathogenesis experiments. AIDS Rev. 2005; 7: 67-83.
- 8Sasseville VG, Diters RW. Impact of infections and normal flora in nonhuman primates on drug development. ILAR J. 2008; 49: 179-190.
- 9Cook DJ, Tymianski M. Nonhuman primate models of stroke for translational neuroprotection research. Neurotherapeutics. 2012; 9: 371-379.
- 10Vallender EJ, Miller GM. Nonhuman primate models in the genomic era: a paradigm shift. ILAR J. 2013; 54: 154-165.
- 11Daadi MM, Barberi T, Shi Q, Lanford RE. Nonhuman primate models in translational regenerative medicine. Stem Cells Dev. 2014; 23(Suppl 1): 83-87.
- 12't Hart BA, Bogers WM, Haanstra KG, Verreck FA, Kocken CH. The translational value of non-human primates in preclinical research on infection and immunopathology. Eur J Pharmacol. 2015; 759: 69-83.
- 13Lerche NW, Osborn KG. Simian retrovirus infections: potential confounding variables in primate toxicology studies. Toxicol Pathol. 2003; 31: 103-110.
- 14Lerche NW, Marx PA, Gardner MB. Elimination of type D retrovirus infection from group-housed rhesus monkeys using serial testing and removal. Lab Anim Sci. 1991; 41: 123-127.
- 15Lerche NW, Yee JL, Jennings MB. Establishing specific retrovirus-free breeding colonies of macaques: an approach to primary screening and surveillance. Lab Anim Sci. 1994; 44: 217-221.
- 16Schroder MA, Fisk SK, Lerche NW. Eradication of simian retrovirus type D from a colony of cynomolgus, rhesus, and stump-tailed macaques by using serial testing and removal. Contemp Top Lab Anim Sci. 2000; 39: 16-23.
- 17Wolf RH, Eberle R, White GL. Generation of specific-pathogen-free baboon colony. J Am Assoc Lab Anim Sci. 2010; 49: 814-820.
- 18Lerche NW. Epidemiology and Control of Type D Retrovirus Infection in Macaques. In: S Matano, RH Tuttle, H Ishida, M Goodman, eds. Topics in Primatology, vol. 3. Tokyo: University of Tokyo Press; 1992: 439-448.
- 19Montiel NA. An updated review of simian betaretrovirus (SRV) in macaque hosts. J Med Primatol. 2010; 39: 303-314.
- 20Lerche NW, Cotterman RF, Dobson MD, Yee JL, Rosenthal AN, Heneine WM. Screening for simian type-D retrovirus infection in macaques, using nested polymerase chain reaction. Lab Anim Sci. 1997; 47: 263-268.
- 21Lowenstine LJ, Lerche NW. Retrovirus infections of nonhuman primates: a review. J Zoo Anim Med. 1988; 19: 168-187.
- 22Lerche NW, Switzer WM, Yee JL, et al. Evidence of infection with simian type D retrovirus in persons occupationally exposed to nonhuman primates. J Virol. 2001; 75: 1783-1789.
- 23Hara M, Kikuchi T, Ono F, et al. Survey of captive cynomolgus macaque colonies for SRV/D infection using polymerase chain reaction assays. Comp Med. 2005; 55: 145-149.
- 24Grant RF, Windsor SK, Malinak CJ, et al. Characterization of infectious type D retrovirus from baboons. Virology. 1995; 207: 292-296.
- 25Morton WR, Agy MB, Capuano SV, Grant RF. Specific pathogen-free macaques: definition, history, and current production. ILAR J. 2008; 49: 137-144.
- 26Chung H-K, Unangst T, Treece J, Weiss D, Markham P. Development of real-time PCR assays for quantitation of simian betaretrovirus serotype-1, -2, -3, and -5 viral DNA in Asian monkeys. J Virol Methods. 2008; 152: 91-97.
- 27White JA, Todd PA, Rosenthal AN, Yee JL, Grant R, Lerche NW. Development of a generic real-time PCR assay for simultaneous detection of proviral DNA of simian betaretrovirus serotypes 1, 2, 3, 4 and 5 and secondary uniplex assays for specific serotype identification. J Virol Methods. 2009; 162: 148-154.
- 28Khlif M, Mary C, Sellami H, et al. Evaluation of nested and real-time PCR assays in the diagnosis of candidaemia. Clin Microbiol Infect. 2009; 15: 656-661.
- 29Mosca M, Giuliano T, Curcio M, et al. Comparison of real-time PCR and nested PCR for the detection of Y chromosome sequences in the peripheral blood mononuclear cells of patients with systemic sclerosis. Ann Rheum Dis. 2009; 68: 155-156.
- 30Rajendram D, Ayenza R, Holder FM, Moran B, Long T, Shah HN. Long-term storage and safe retrieval of DNA from microorganisms for molecular analysis using FTA matrix cards. J Microbiol Methods. 2006; 67: 582-592.
- 31Becker S, Franco JR, Simarro PP, Stich A, Abel PM, Steverding D. Real-time PCR for detection of Trypanosoma brucei in human blood samples. Diag Microbiol Infect Dis. 2004; 50: 193-199.
- 32Ahmed HA, MacLeod ET, Hide G, Welburn SC, Picozzi K. The best practice for preparation of samples from FTA® cards for diagnosis of blood borne infections using African trypanosomes as a model system. Parasit Vectors. 2011; 4: 68.
- 33Voevodin AF, Marx PA. Simian Virology. Singapore: Wiley-Blackwell; 2009: 169.
10.1002/9780813809793 Google Scholar
- 34Zao C-L, Armstrong K, Tomanek L, et al. The complete genome and genetic characteristics of SRV-4 isolated from cynomolgus monkeys (Macaca fasicularis). Virology. 2010; 405: 390-396.
- 35Li B, Axthelm MK, Machida CA. Simian retrovirus serogroup 5: partial gag-prt sequence and viral RNA distribution in an infected rhesus macaque. Virus Genes. 2000; 21: 241-248.
- 36Zao C-L, Tomanek L, Cooke A, et al. A novel simian retrovirus subtype discovered in cynomolgus monkeys (Macaca fascicularis). J Gen Virol. 2016; 97: 3017-3023.
- 37 IPPL. U.S. primate import statistics for 2013. https://www.ippl.org/gibbon/blog/u-s-primate-import-statistics-2013/. Accessed January 6, 2017.