Volume 35 Issue 6
Nov.  2014
Turn off MathJax
Article Contents
Hong-Yi ZHENG, Ming-Xu ZHANG, Lin-Tao ZHANG, Xiao-Liang ZHANG, Wei PANG, Long-Bao LYU, Yong-Tang ZHENG. Flow cytometric characterizations of leukocyte subpopulations in the peripheral blood of northern pig-tailed macaques (Macaca leonina). Zoological Research, 2014, 35(6): 465-473. doi: 10.13918/j.issn.2095-8137.2014.6.465
Citation: Hong-Yi ZHENG, Ming-Xu ZHANG, Lin-Tao ZHANG, Xiao-Liang ZHANG, Wei PANG, Long-Bao LYU, Yong-Tang ZHENG. Flow cytometric characterizations of leukocyte subpopulations in the peripheral blood of northern pig-tailed macaques (Macaca leonina). Zoological Research, 2014, 35(6): 465-473. doi: 10.13918/j.issn.2095-8137.2014.6.465

Flow cytometric characterizations of leukocyte subpopulations in the peripheral blood of northern pig-tailed macaques (Macaca leonina)

doi: 10.13918/j.issn.2095-8137.2014.6.465
Funds:  This work was supported by the National Special Science Research Program of China (2012CBA01305); the National Natural Science Foundation of China (81172876, U0832601, 81273251, U1202228); the Knowledge Innovation Program of CAS (KSCX2-EW-R-13) and the National Science and Technology Major Project (2013ZX10001-002, 2012ZX10001-007)
More Information
  • Corresponding author: Yong-Tang ZHENG
  • Received Date: 2014-05-08
  • Rev Recd Date: 2014-08-10
  • Publish Date: 2014-11-08
  • Pig-tailed macaques (Macaca nemistrina group) have been extensively used as non-human primate animal models for various human diseases in recent years, notably for AIDS research due to their sensitivity to HIV-1. Northern pig-tailed macaques (M. leonina) are distributed in China and other surrounding Southeast Asia countries. Although northern pig-tailed macaques have been bred on a large scale as experimental animals since 2012, the reference value of normal levels of leukocytes is not available. To obtain such information, 62 blood samples from male and female healthy northern pig-tailed macaques at different ages were collected. The normal range of major leukocyte subpopulations, such as T lymphocytes, B lymphocytes, natural killer (NK) cells, monocytes, and the expression levels of activation or differentiation related molecules (CD38, HLA-DR, CCR5, CD21, IgD, CD80 and CD86) on lymphocytes were analyzed by flow cytometry. The counts of B cells decreased with age, but those of CD8+ T cells and NK cells and the frequency of CD38+HLA-DR+CD4+ T cells were positively correlated with age. The counts of leukocyte subpopulations were higher in males than those in females except for CD4+ T cells. Males also showed higher expression levels of IgD and CD21 within B cells. This study provides basic data about the leukocyte subpopulations of northern pig-tailed macaques and compares this species with commonly used Chinese rhesus macaques (M. mulatta), which is meaningful for the biomedical application of northern pig-tailed macaques.
  • loading
  • [1]
    Agy MB, Frumkin LR, Corey L, Coombs RW, Wolinsky SM, Koehler J, Morton WR, Katze MG. 1992. Infection of Macaca nemestrina by human immunodeficiency virus type-1. Science, 257(5066): 103-106.
    Asquith M, Haberthur K, Brown M, Engelmann F, Murphy A, Al-Mahdi Z, Messaoudi I. 2012. Age-dependent changes in innate immune phenotype and function in rhesus macaques (Macaca mulatta). Pathobiology of Aging & Age Related Diseases, 2.
    Baroncelli S, Negri D R, Michelini Z, Cara A. 2008. Macaca mulatta, fascicularis and nemestrina in AIDS vaccine development. Expert Review of Vaccines, 7(9): 1419-1434.
    Batten CJ, De Rose R, Wilson KM, Agy MB, Chea S, Stratov I, Montefiori DC, Kent SJ. 2006. Comparative evaluation of simian, simian-human, and human immunodeficiency virus infections in the pigtail macaque (Macaca nemestrina) model. AIDS Research and Human Retroviruses, 22(6): 580-588.
    Bosch ML, Schmidt A, Chen J, Florey MJ, Agy M, Morton WR. 2000. Enhanced replication of HIV-1 in vivo in pigtailed macaques (Macaca nemestrina). Journal of Medical Primatology, 29(3-4): 107-113.
    Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, Nguyen PL, Khoruts A, Larson M, Haase AT, Douek DC. 2004. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. Journal of Experimental Medicine, 200(6): 749-759.
    Brignolo L, Spinner A, Yee JL, Lerche NW. 2004. Subsets of T cells in healthy rhesus macaques (Macaca mulatta) infected with simian T-lymphotropic virus type 1. Comparative Medicine, 54(3): 271-274.
    Choong ML, Ton SH, Cheong SK. 1995. Influence of race, age and sex on the lymphocyte subsets in peripheral blood of healthy Malaysian adults. Annals of Clinical Biochemistry, 32(Pt 6): 532-539.
    Coe CL, Ershler WB. 2001. Intrinsic and environmental influences on immune senescence in the aged monkey. Physiology & Behavior, 73(3): 379-384.
    Das A, Veazey RS, Wang XL, Lackner AA, Xu HB, Pahar B. 2011. Simian immunodeficiency virus infection in rhesus macaques induces selective tissue specific B cell defects in double positive CD21+CD27+ memory B cells. Clinical Immunology, 140(3): 223-228.
    Della Bella S, Bierti L, Presicce P, Arienti R, Valenti M, Saresella M, Vergani C, Villa ML. 2007. Peripheral blood dendritic cells and monocytes are differently regulated in the elderly. Clinical Immunology, 122(2): 220-228.
    Didier ES, Sugimoto C, Bowers LC, Khan IA, Kuroda MJ. 2012. Immune correlates of aging in outdoor-housed captive rhesus macaques (Macaca mulatta). Immunity & Ageing, 9(1): 25.
    Dykhuizen M, Ceman J, Mitchen J, Zayas M, MacDougall A, Helgeland J, Rakasz E, Pauza CD. 2000. Importance of the CD3 marker for evaluating changes in rhesus macaque CD4/CD8 T-cell ratios. Cytometry, 40(1): 69-75.
    Fagnoni FF, Vescovini R, Mazzola M, Bologna G, Nigro E, Lavagetto G, Franceschi C, Passeri M, Sansoni P. 1996. Expansion of cytotoxic CD8+ CD28- T cells in healthy ageing people, including centenarians. Immunology, 88(4): 501-507.
    Ferguson FG, Wikby A, Maxson P, Olsson J, Johansson B. 1995. Immune parameters in a longitudinal study of a very old population of Swedish people: a comparison between survivors and nonsurvivors. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 50(6): B378-B382.
    Frasca D, Landin AM, Riley RL, Blomberg BB. 2008. Mechanisms for decreased function of B cells in aged mice and humans. The Journal of Immunology, 180(5): 2741-2746.
    Gippoliti S. 2001. Notes on the taxonomy of Macaca nemestrina leonina Blyth, 1863 (Primates: Cercopithecidae). Hystrix - Italian Journal of Mammalogy, 12(1): 51-54.
    Hatziioannou T, Ambrose Z, Chung NPY, Piatak M Jr, Yuan F, Trubey CM, Coalter V, Kiser R, Schneider D, Smedley J, Pung R, Gathuka M, Estes JD, Veazey RS, KewalRamani VN, Lifson JD, Bieniasz PD. 2009. A macaque model of HIV-1 infection. Proceedings of the National Academy of Sciences of the United States of America, 106(11): 4425-4429.
    High KP. 2004. Infection as a cause of age-related morbidity and mortality. Ageing Research Reviews, 3(1): 1-14.
    Hong HS, Rajakumar PA, Billingsley JM, Reeves RK, Johnson RP. 2013. No monkey business: why studying NK cells in non-human primates pays off. Frontiers in Immunology, 4: 32.
    Jiao Y, Qiu ZF, Xie J, Li DJ, Li TS. 2009. Reference ranges and age-related changes of peripheral blood lymphocyte subsets in Chinese healthy adults. Science in China. Series C: Life Sciences, 52(7): 643-650.
    Kestens L, Vanham G, Gigase P, Young G, Hannet I, Vanlangendonck F, Hulstaert F, Bach BA. 1992. Expression of activation antigens, HLA-DR and CD38, on CD8 lymphocytes during HIV-1 infection. AIDS, 6(8): 793-797.
    Klatt NR, Canary LA, Vanderford TH, Vinton CL, Engram JC, Dunham RM, Cronise HE, Swerczek JM, Lafont BAP, Picker LJ, Silvestri G, Brenchley JM. 2012. Dynamics of simian immunodeficiency virus SIVmac239 infection in pigtail macaques. Journal of Virology, 86(2): 1203-1213.
    Klein U, Rajewsky K, Kuppers R. 1998. Human immunoglobulin (Ig) M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. Journal of Experimental Medicine, 188(9): 1679-1689.
    Kling HM, Shipley TW, Norris KA. 2011. Alterations in peripheral blood B-cell populations in SHIV89.6P-infected macaques (Macacca fascicularis). Comparative Medicine, 61(3): 269-277.
    Klose N, Coulibaly B, Tebit DM, Nauwelaers F, Spengler HP, Kynast-Wolf G, Kouyaté B, Kräusslich HG, Böhler T. 2007. Immunohematological reference values for healthy adults in Burkina Faso. Clinical and Vaccine Immunology, 14(6): 782-784.
    Koch S, Larbi A, Ozcelik D, Solana R, Gouttefangeas C, Attig S, Wikby A, Strindhall J, Franceschi C, Pawelec G. 2007. Cytomegalovirus infection: a driving force in human T cell immunosenescence. Annals of the New York Academy of Sciences, 1114: 23-35.
    Kuang YQ, Tang X, Liu FL, Jiang XL, Zhang YP, Gao GX, Zheng YT. 2009. Genotyping of TRIM5 locus in northern pig-tailed macaques (Macaca leonina), a primate species susceptible to Human Immunodeficiency Virus type 1 infection. Retrovirology, 6: 58.
    Lei AH, Pang W, Zhang GH, Zheng YT. 2013. Use and research of pigtailed macaques in nonhuman primate HIV/AIDS models. Zoological Research, 34(2): 77-88. (in Chinese)
    Ling BH, Veazey RS, Luckay A, Penedo C, Xu KY, Lifson JD, Marx PA. 2002. SIV(mac) pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. AIDS, 16(11): 1489-1496.
    Mahbub S, Brubaker AL, Kovacs EJ. 2011. Aging of the innate immune system: an update. Current Immunology Reviews, 7(1): 104-115.
    Malaivijitnond S, Arsaithamkul V, Tanaka H, Pomchote P, Jaroenporn S, Suryobroto B, Hamada Y. 2012. Boundary zone between northern and southern pig-tailed macaques and their morphological differences. Primates, 53(4): 377-389.
    Meditz AL, Haas MK, Folkvord JM, Melander K, Young R, McCarter M, MaWhinney S, Campbell TB, Lie Y, Coakley E, Levy DN, Connick E. 2011. HLA-DR+ CD38+ CD4+ T lymphocytes have elevated CCR5 expression and produce the majority of R5-tropic HIV-1 RNA in vivo. Journal of Virology, 85(19): 10189-10200.
    Messaoudi I, Estep R, Robinson B, Wong SW. 2011. Nonhuman primate models of human immunology. Antioxidants and Redox Signaling, 14(2): 261-273.
    Moir S, Fauci AS. 2008. Pathogenic mechanisms of B-lymphocyte dysfunction in HIV disease. Journal of Allergy and Clinical Immunology, 122(1): 12-19.
    Onlamoon N, Tabprasit S, Suwanagool S, Louisirirotchanakul S, Ansari AA, Pattanapanyasat K. 2005. Studies on the potential use of CD38 expression as a marker for the efficacy of anti-retroviral therapy in HIV-1-infected patients in Thailand. Virology, 341(2): 238-247.
    Pang W, Lü LB, Wang Y, Li G, Huang DT, Lei AH, Zhang GH, Zheng YT. 2013. Measurement and analysis of hematology and blood chemistry parameters in northern pig-tailed macaques (Macaca leonina). Zoological Research, 34(2): 89-96. (in Chinese)
    Patton DL, Sweeney YT, Paul KJ. 2009. A summary of preclinical topical microbicide rectal safety and efficacy evaluations in a pigtailed macaque model. Sexually Transmitted Diseases, 36(6): 350-356.
    Shaw AC, Joshi S, Greenwood H, Panda A, Lord JM. 2010. Aging of the innate immune system. Current Opinion in Immunology, 22(4): 507-513.
    Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 2004. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature, 427(6977): 848-853.
    Thippeshappa R, Polacino P, Yu Kimata MT, Siwak EB, Anderson D, Wang WM, Sherwood L, Arora R, Wen M, Zhou P, Hu SL, Kimata JT. 2011. Vif substitution enables persistent infection of pig-tailed macaques by human immunodeficiency virus type 1. Journal of Virology, 85(8): 3767-3779.
    Tollerud DJ, Clark JW, Brown LM, Neuland CY, Pankiw-Trost LK, Blattner WA, Hoover RN. 1989. The influence of age, race, and gender on peripheral blood mononuclear-cell subsets in healthy nonsmokers. Journal of Clinical Immunology, 9(3): 214-222.
    Tryphonas H, Lacroix F, Hayward S, Izaguirre C, Parenteau M, Fournier J. 1996. Cell surface marker evaluation of infant Macaca monkey leukocytes in peripheral whole blood using simultaneous dual-color immunophenotypic analysis. Journal of Medical Primatology, 25(2): 89-105.
    Uppal SS, Verma S, Dhot PS. 2003. Normal values of CD4 and CD8 lymphocyte subsets in healthy indian adults and the effects of sex, age, ethnicity, and smoking. Cytometry. Part B: Clinical Cytometry, 52(1): 32-36.
    Wiener D, Shah S, Malone J, Lowell N, Lowitt S, Rowlands DT Jr. 1990. Multiparametric analysis of peripheral blood in the normal pediatric population by flow cytometry. Journal of Clinical Laboratory Analysis, 4(3): 175-179.
    Xia HJ, Zhang GH, Wang RR, Zheng YT. 2009. The influence of age and sex on the cell counts of peripheral blood leukocyte subpopulations in Chinese rhesus macaques. Cellular & Molecular Immunology, 6(6): 433-440.
    Zandieh A, Izad M, Fakhri M, Amirifard H, Khazaeipour Z, Harirchian MH. 2013. Cytometric profiling in various clinical forms of multiple sclerosis with respect to CD21+, CD32+, and CD35+ B and T cells. Translational Neurodegeneration, 2(1): 14.
    Zhang XL, Pang W, Deng DY, Lü LB, Feng Y, Wang Y, Zheng YT. 2014. Analysis of immunoglobulin, complements and CRP levels in serum of captive northern pig-tailed macaques (Macaca leonina). Zoological Research, 35(3): 196-203.
    Zheng HY, Zhang MX, Pang W, Zheng YT. 2014. Aged Chinese rhesus macaques suffer severe phenotypic T- and B-cell aging accompanied with sex differences. Experimental Gerontology, 55: 113-119.
    Zhu L, Zhang GH, Zheng YT. 2010. Application studies of animal models in evaluating safety and efficacy of HIV-1 microbicides. Zoological Research, 31(1): 66-76. (in Chinese)
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (749) PDF downloads(1149) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint