Characterization of B and plasma cells in blood, bone marrow, and secondary lymphoid organs of rhesus macaques by multicolor flow cytometry

Journal of Leukocyte Biology

Volumn 97, Issue 1, 2015, Pages 19-30

  Neumann, Berit ^a   Klippert, Antonina ^a   Raue, Katharina ^a,d   Sopper, Sieghart ^a,b,c   Stahl Hennig, Christiane ^a  

^a GERMAN PRIMATE CENTER   (Germany)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c TYROLEAN CANCER RESEARCH INSTITUTE   (Austria)

^d UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Activation; CD20; Macaca mulatta; Nonhuman primates; Proliferation

Indexed keywords

B7 ANTIGEN; CD19 ANTIGEN; CD20 ANTIGEN; CD38 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; KI 67 ANTIGEN; SYNDECAN 1;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BONE MARROW; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; LYMPHOCYTE SUBPOPULATION; LYMPHOID ORGAN; MALE; MEMORY CELL; NONHUMAN; PLASMA CELL; PRE B LYMPHOCYTE; PRIORITY JOURNAL; RHESUS MONKEY; T LYMPHOCYTE; ANIMAL; CELL SEPARATION; CYTOLOGY; LYMPHOID TISSUE;

MACACA MULATTA; PRIMATES;

ANIMALS; B-LYMPHOCYTES; CELL SEPARATION; FLOW CYTOMETRY; LYMPHOID TISSUE; MACACA MULATTA; PLASMA CELLS;

EID: 84925283189     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1HI0514-243R     Document Type: Article

References (51)

1. Ahmed, R., Gray, D. (1996) Immunological memory and protective immunity: understanding their relation. Science 272, 54-60.
2. Liu, Y. J., Oldfield, S., MacLennan, I. C. (1988) Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones, Eur. J. Immunol. 18, 355-362.
3. Liu, Y.J., Zhang, J., Lane, P.J., Chan, E. Y., MacLennan, I. C. (1991) Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur. J. Immunol. 21, 2951-2962.
4. Smith, K. G., Hewitson, T. D., Nossal, G. J., Tarlinton, D. M. (1996) The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol. 26, 444-448.
5. Yanaba, K, Bouaziz, J. D., Matsushita. T., Magro, C. M., St Clair, E. W., Tedder, T. F. (2008) B-lymphocyte contributions to human autoimmune disease. Immunol. Rev. 223, 284-299.
6. De Rosa, G., Gobbo, M. L., De Renzo, A., Notaro, R., Garofalo, S., Grimaldi, M., Apuzzo, A., Chiurazzi, F., Picardi, M., Matarazzo, M., Rotoli, B. (1997) High prevalence of hepatitis C virus infection in patients with B-cell lymphoproliferative disorders in Italy. Am. J. Hematol. 55, 77-82.
7. Moir, S., Malaspina, A., Pickeral, O. K., Donoghue, E. T., Vasquez, J., Miller, N.J., Krishnan, S. R., Planta, M. A., Turney, J. F., Justement,J. S., Kottilil, S., Dybul, M., Mican, J. M., Kovacs, C., Chun, T.-W., Birse, C. E., Fauci, A. S. (2004) Decreased survival of B cells of HIV-viremic patients mediated by altered expression of receptors of the TNF superfamily. J. Exp. Med. 200, 587-600.
8. Moir, S., Malaspina, A., Ogwaro, K. M., Donoghue, E. T., Hallahan, C. W., Ehler, L. A., Liu, S., Adelsberger, J., Lapointe, R., Hwu, P., Baseler, M., Orenstein,J. M., Chun, T. W., Mican, J. A., Fauci, A. S. (2001) HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals, Proc. Natl. Acad. Sci. USA 98, 10362-10367.
9. Ho, J., Moir, S., Malaspina, A., Howell, M. L., Wang, W., DiPoto, A. C, O'Shea, M. A., Roby, G. A., Kwan, R., Mican, J. M., Chun, T. W., Fauci, A. S. (2006) Two overrepresented B cell populations in HIV-infected individuals undergo apoptosis by different mechanisms. Proc. Natl Acad. Sci. USA 103, 19436-19441.
10. Moir, S., Fauci, A. S. (2008) Pathogenic mechanisms of B-lymphocytc dysfunction in HIV disease. J. Allergy Clin. Immunol. 122, 12-19; quiz 20-21.
11. Moir, S., Fauci, A. S. (2009) B cells in HIV infection and disease. Nat. Rev. Immunol. 9, 235-245.
12. De Milito, A., Mōrch, C, Sónnerborg, A., Chiodi, F. (2001) Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS 15, 957-964.
13. Malaspina, A., Moir, S., Ho, J., Wang, W., Howell, M. L., O'Shea, M. A., Roby, G. A., Rehm, C. A., Mican, J. M., Chun, T. W., Fauci, A. S. (2006) Appearance of immature/transitional B cells in HIV-infected individuals with advanced disease: correlation with increased IL-7. Proc. Natl. Acad. Sci. USA 103, 2262-2267.
14. Malaspina, A., Moir, S., Chaitt, D. G., Rehm, C. A., Kottilil, S., Falloon, J., Fauci, A. S. (2007) Idiopathic CD4+ T lymphocytopenia is associated with increases in immature/transitional B cells and serum levels of IL 7. mood 109, 2086-2088.
15. Van Rompay, K. K. (2012) The use of nonhuman primate models of HIV infection for the evaluation of antiviral strategies. AIDS Res. Hum. Retroviruses 28, 16-35.
16. Peruchon, S., Chaoul, N., Burelout, C., Delache, B., Brochard, P., Laurent, P., Cognasse, F., Prévot, S., Garraud, O., Le Grand, R., Richard, Y. (2009) Tissue-specific B-cell dysfunction and generalized memory B-cell loss during acute SIV infection. PLoS ONE 4, e5966.
17. Kuhrt, D., Faith, S. A., Leone, A., Rohankedkar, M., Sodora, D. L., Picker, L. J., Cole, K. S. (2010) Evidence of early B-cell dysregulation in simian immunodeficiency vims infection: rapid depletion of naïve and memory B-cell subsets with delayed reconstitution of the naïve B-cell population. J. Virol. 84, 2466-2476.
18. Titanji, K., Velu, V., Chennareddi, L., Vijay-Kumar, M., Gewirtz, A. ľ., Freeman, G. J., Amara, R. R. (2010) Acute depletion of activated memory B cells involves the PD-1 pathway in rapidly progressing SľV-infected macaques. J. Clin. Invest. 120, 3878-3890.
19. Das, A., Veazey, R. S., Wang, X., Lackner, A. A., Xu, H., 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. Clin. Immunol. 140, 223-228.
20. Demberg, T., Brocca-Cofano, E., Xiao, P., Venzon, D., Vargas-Inchaustegui, D., Lee, E. M., Kalisz, I., Kalyanaraman, V. S., Dipasqualc, J., McKinnon, K., Robert-Guroff, M. (2012) Dynamics of memory B-cell populations in blood, lymph nodes, and bone marrow during antiretroviral therapy and envelope boosting in simian immunodeficiency virus SIVmac251-infected rhesus macaques. J. Virol. 86, 12591-12604.
21. Caraux, A., Klein. B., Paiva, B., Bret, C., Schmitz, A., Fuhler, M., Bos, N. A.,Johnsen, H. E., Orfao, A. Perez-Andres, M., Myeloma Stem Cell Network. (2010) Circulating human B and plasma cells. Age-associated changes in counts and detailed characterization of circulating normal CD 138-and CD 138+ plasma cells. Haematologìca 95, 1016-1020.
22. Medina, F., Segundo, C., Campos-Caro, A., González-García, I. Brieva, J. A. (2002) The heterogeneity shown by human plasma cells from tonsil, blood, and bone marrow reveals graded stages of increasing maturity, but local profiles of adhesion molecule expression. Blood 99, 2154-2161.
23. Mei, H. E., Yoshida, T., Simc, W., Hiepe, F., Thiele, K. Manz, R. A., Radbruch, A., Dòrner, T. (2009) Blood-borne human plasma cells in steady state are derived from mucosal immune responses. Blood 113, 2461-2469.
24. Medina, F., Segundo, C., Rodriguez, C., Brieva, J. A. (1997) Regulatory role of CD95 ligation on human B cells induced in vivo capable of spontaneous and high-rate Ig secretion. Eur. J. Immunol. 27, 700-706.
25. Sopper, S., Stahl-Hennig, C., Dcmuth, M., Johnston, I. C., Dörries, R., ter Meulen, V. (1997) Lymphocyte subsets and expression of differentiation markers in blood and lymphoid organs of rhesus monkeys. Cytometry 29, 351-362.
26. Hultin, L. E., Hausner, M. A., Hultin, P. M., Giorgi.J. V. (1993) CD20 (pan-B cell) antigen is expressed at a low level on a subpopulation of human T lymphocytes. Cytometry 14, 196-204.
27. Marie-Cardine, A., Divay, F., Dutot, I., Green, A., Perdrix, A., Boyer, O., Contentin, N., Tilly, H., Tron, F., Vannicr, J. P., Jacquot, S. (2008) Transitional B cells in humans: characterization and insight from B lymphocyte reconstitution after hematopoietic stem cell transplantation. Clin. Immunol. 127, 14-25.
28. Agematsu, K., Nagumo, H., Yang, F. C., Nakazawa, T., Fukushima, K., Ito, S., Sugita, K., Mori, T., Kobata, T., Morimoto, C., Komiyama, A. (1997) B cell subpopulations separated by CD27 and crucial collaboration of CD27+ B cells and helper T cells in immunoglobulin production. Eur., J. Immunol. 27, 2073-2079.
29. Kuhrt, D., Faith, S., Hattemer, A., Leone, A., Sodora, D., Picker, L., Borghesi, L., Cole, K. S. (2011) Naïve and memory B cells in the rhesus macaque can be differentiated by surface expression of CD27 and have differential responses to CD40 ligation. J. Immunol. Methods 363, 166-176.
30. Verheijen, R., Kuijpers, H. J., van Driel, R., Beck, J. L., van Dierendonck, J. H., Brakenhoff, G.J., Ramaekers, F. C. (1989) Ki-67 detects a nuclear matrix-associated proliferation-related antigen. II. Localization in mitotic cells and association with chromosomes. J. Cell Sci. 92, 531-540.
31. Kunkel, E. J., Butcher, E. C. (2003) Plasma-cell homing. Nat. Rev. Immunol. 3 822-829.
32. Tokoyoda, K., Zehentmeier, S., Chang, H. D., Radbruch, A. (2009) Organization and maintenance of immunological memory by stroma niches. Eur. J. Immunol. 39, 2095-2099.
33. Perez-Andres, M., Paiva, B., Nieto, W. G., Caraux, A., Schmitz, A., Almeida, J., Vogt Jr., R. F., Marti, G. E., Rawstron, A. C., Van Zelm, M. C., Van Dongen.J. J., Johnsen, H. E., Klein, B., Orfao, A., Primary Health Care Group of Salamanca for the Study of MBL. (2010) Human peripheral blood B-cell compartments: a crossroad in B-cell traffic. Cytometry B Clin. Cytom. 78 (Suppl 1), S47-S60.
34. Vugmeyster, Y., Howell. K., Bakshi, A., Flores, C., Hwang, O., McKeever, K. (2004) B-cell subsets in blood and lymphoid organs in Macaca fascicularis. Cytometry A 61, 69-75.
35. Martin, F., Kearnev, J. F. (2002) Marginal-zone B cells. Nat. Rev. Immunol. 2, 323-335.
36. Du, M. Q., Peng, H. Z., Dogan, A., Diss, T. C., Liu, H., Pan, L. X., Moseley, R. P., Briskin, M.J., Chan.J. K. Isaacson, P. G. (1997) Preferential dissemination of B-cell gastric mucosa-associated lymphoid tissue (MALT) lymphoma to the splenic marginal zone. Blood 90, 4071-4077.
37. Tangye, S. G., Liu, Y. J., Aversa, G., Phillips, J. H., de Vries, J. E. (1998) Identification of functional human splenic memory B cells by expression of CD 148 and CD27. J. Exp. Med. 188, 1691-1703.
38. Klein, U., Rajewsky, K., Küppers, 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. J. Exp. Med. 188, 1679-1689.
39. Maurer, D., Fischer, G. F., Fae, I., Majdic, O., Stuhlmeier, K., Vonjeney, N., Holter, W., Knapp, W. (1992) IgM and IgG hut not cytokine secretion is restricted to the CD27+ B lymphocyte subset. J. Immunol. 148, 3700-3705.
40. Gujer, C., Sandgren, K.J., Douagi, Ĩ., Adams, W. G., Sundling, C., Smed-Sörenscn, A., Seder, R. A., Karlsson Hedestam, G. B., Lore, K. (2011) IFN-α produced by human plasmacytoid dendritic cells enhances T cell-dependent naïve B cell differentiation. J. Leukoc. Biol. 89, 811-821.
41. Gujer, C., Sundling, C., Seder, R. A., Karlsson Hedestam, G. B., Lore, K. (2011) Human and rhesus plasmacytoid dendritic cell and B-cell responses to Toll-like receptor stimulation. Immunology 134, 257-269.
42. Nakayama, T., Hieshima, K., Izawa, D., Tatsumi, Y., Kanamaru, A., Yoshie, O. (2003) Cutting edge: profile of chemokine receptor expression on human plasma cells accounts for their efficient recruitment to target tissues. J. Immunol. 170, 1136-1140.
43. Demberg, T., Mohanram, V., Venzon, D., Robert-Guroff, M. (2014) Phenotypes and distribution of mucosal memory B-cell populations in the SIV/SHIV rhesus macaque model. Clin. Immunol, 153, 264-276.
44. Thomas, M. A., Demberg, T., Vargas-Inchaustegui, D. A., Xiao, P., Tuero, I., Venzon, D., Weiss, D., Treece, J., Robert-Guroff, M. (2014) Rhesus macaque rectal and duodenal tissues exhibit B-cell subpopulations distinct from peripheral blood that continuously secrete antigen-specific IgA in short-term explant cultures. Vaccine 32, 872-880.
45. Lenschow, D.J., Su, G. H., Zuckerman, L. A., Nabavi, N., Jellis, C. L., Gray, G. S., Miller, J., Milestone, J. A. (1993) Expression and funcdonal significance of an additional ligand for CTIA-4. Proc. Natl. Acad. Sci. USA 90, 11054-11058.
46. Azuma, M., Ito, D., Yagita, H., Okumura, K., Phillips, J. H., Lanier, L. L., Somoza, C. (1993) B70 antigen is a second ligand for CTIA-4 and CD28. Nature 366, 76-79.
47. Vallé, A., Aubry, J. P., Durand, I., Banchereau, J. (1991) IL-4 and IL-2 upregulate the expression of antigen B7, the B cell counterstructure to T cell CD28: an amplificadon mechanism for T-B cell interactions. Int. Immunol. 3, 229-235.
48. Defrance, T., Casamayor-Pallejà, M., Krammer, P. H. (2002) The life and death of a B cell. Adv. Cancer Res. 86, 195-225.
49. Rathmell, J. C., Cooke, M. P., Ho, W. Y., Grein, J., Townsend, S. E., Davis, M. M., Goodnow, C. C. (1995) CD95 (Fas)-dependent elimination of self-reactive B cells upon interaction with CD4+ T cells Nature 376, 181-184.
50. Cumont, M. C., Diop, O. Vaslin, B., Elbim, C., Viollet, L., Monceaux, V., Lay, S., Silvestri, G., Iæ Grand, R., Mūller-Trutwin, M., Hurtrel, B., Estaquier, J. (2008) Early divergence in lymphoid tissue apoptosis between pathogenic and nonpathogenic simian immunodeficiency virus infections of nonhuman primates. J. Virol. 82, 1175-1184.
51. Hong, J. J., Amancha, P. K., Rogers, K., Ansari, A. A., Villinger. F. (2012) Spatial alterations between CD4(+) T follicular helper, B. and CD8(+) T cells during simian immunodeficiency virus infection: T/B cell homeostasis, activation, and potential mechanism for viral escape. J. Immunol. 188, 3247-3256.