Memory CD8+ T cells colocalize with IL-7+ stromal cells in bone marrow and rest in terms of proliferation and transcription

European Journal of Immunology

Volumn 45, Issue 4, 2015, Pages 975-987

  Sercan Alp, Özen ^a   Durlanik, Sibel ^b   Schulz, Daniel ^a   Mcgrath, Mairi ^a   Grün, Joachim R ^c   Bardua, Marcus ^a   Ikuta, Koichi ^d   Sgouroudis, Evridiki ^a   Riedel, René ^a   Zehentmeier, Sandra ^c   Hauser, Anja E ^c   Tsuneto, Motokazu ^e   Melchers, Fritz ^e   Tokoyoda, Koji ^c   Chang, Hyun Dong ^a   Thiel, Andreas ^b   Radbruch, Andreas ^a  

^a DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c A Leibniz Institute   (Germany)

^d KYOTO UNIVERSITY   (Japan)

^e MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

Bone marrow; CD8 T cell; Gene expression; Interleukin 7; Memory cells

Indexed keywords

BROXURIDINE; CD4 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; HERMES ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 7; KI 67 ANTIGEN; LIPOPOLYSACCHARIDE; PROPIDIUM IODIDE; VASCULAR CELL ADHESION MOLECULE 1; CD137 ANTIGEN; LECTIN; LEUKOCYTE ANTIGEN; MKI67 PROTEIN, MOUSE; T LYMPHOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARENAVIRUS INFECTION; ARTICLE; BONE MARROW; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CYCLE G0 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL SURVIVAL; CYTOKINE PRODUCTION; EFFECTOR CELL; GENE EXPRESSION; HELPER CELL; IMMUNE RESPONSE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; SPLEEN CELL; STROMA CELL; ANIMAL; BIOSYNTHESIS; BONE MARROW CELL; C57BL MOUSE; CYTOLOGY; GENETIC TRANSCRIPTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD137; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; BONE MARROW CELLS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; G0 PHASE; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; INTERLEUKIN-2; INTERLEUKIN-7; KI-67 ANTIGEN; LECTINS, C-TYPE; MICE; MICE, INBRED C57BL; STROMAL CELLS; TRANSCRIPTION, GENETIC;

EID: 84926619198     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445295     Document Type: Article

References (55)

1. Tokoyoda, K., Egawa, T., Sugiyama, T., Choi, B. I. and Nagasawa, T., Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 2004. 20: 707-718.
2. Manz, R. A., Thiel, A. and Radbruch, A., Lifetime of plasma cells in the bone marrow. Nature 1997. 388: 133-134.
3. Manz, R. A. and Radbruch, A., Plasma cells for a lifetime? Eur. J. Immunol. 2002. 32: 923-927.
4. + T lymphocytes preferentially reside and rest in the bone marrow. Immunity 2009. 30: 721-730.
5. Tokoyoda, K., Hauser, A. E., Nakayama, T. and Radbruch, A., Organization of immunological memory by bone marrow stroma. Nat. Rev. Immunol. 2010. 10: 193-200.
6. Okhrimenko, A., Grun, J. R., Westendorf, K., Fang, Z., Reinke, S., vonRoth, P., Wassilew, G. et al., Human memory T cells from the bone marrow are resting and maintain long-lasting systemic memory. Proc. Natl. Acad. Sci. USA 2014. 111: 9229-9234.
7. + T cells. Immunity 2005. 22: 259-270.
8. Becker, T. C., Coley, S. M., Wherry, E. J. and Ahmed, R., Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J. Immunol. 2005. 174: 1269-1273.
9. + T cells with close contact to IL-15-producing cells. J. Immunol. 2011. 186: 6965-6971.
10. Di Rosa, F. and Pabst, R., The bone marrow: a nest for migratory memory T cells. Trends Immunol. 2005. 26: 360-366.
11. Kudernatsch, R. F., Letsch, A., Guerreiro, M., Lobel, M., Bauer, S., Volk, H. D. and Scheibenbogen, C., Human bone marrow contains a subset of quiescent early memory CD8 T cells characterized by high CD127 expression and efflux capacity. Eur. J. Immunol. 2014. 44: 3532-3542.
12. Parretta, E., Cassese, G., Barba, P., Santoni, A., Guardiola, J. and Di Rosa, F., CD8 cell division maintaining cytotoxic memory occurs predominantly in the bone marrow. J. Immunol. 2005. 174: 7654-7664.
13. Parretta, E., Cassese, G., Santoni, A., Guardiola, J., Vecchio, A. and Di Rosa, F., Kinetics of in vivo proliferation and death of memory and naive CD8 T cells: parameter estimation based on 5-bromo-2'-deoxyuridine incorporation in spleen, lymph nodes, and bone marrow. J. Immunol. 2008. 180: 7230-7239.
14. Schluns, K. S., Kieper, W. C., Jameson, S. C. and Lefrancois, L., Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat. Immunol. 2000. 1: 426-432.
15. Surh, C. D. and Sprent, J., Homeostasis of naive and memory T cells. Immunity 2008. 29: 848-862.
16. Tokoyoda, K., Zehentmeier, S., Chang, H. D. and Radbruch, A., Organization and maintenance of immunological memory by stroma niches. Eur. J. Immunol. 2009. 39: 2095-2099.
17. Chu, V. T., Frohlich, A., Steinhauser, G., Scheel, T., Roch, T., Fillatreau, S., Lee, J. J. et al., Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol. 2011. 12: 151-159.
18. Zehentmeier, S., Roth, K., Cseresnyes, Z., Sercan, O., Horn, K., Niesner, R. A., Chang, H. D. et al., Static and dynamic components synergize to form a stable survival niche for bone marrow plasma cells. Eur. J. Immunol. 2014. 44: 2306-2317.
19. Kondrack, R. M., Harbertson, J., Tan, J. T., McBreen, M. E., Surh, C. D. and Bradley, L. M., Interleukin 7 regulates the survival and generation of memory CD4 cells. J. Exp. Med. 2003. 198: 1797-1806.
20. Hara, T., Shitara, S., Imai, K., Miyachi, H., Kitano, S., Yao, H., Tani-ichi, S. et al., Identification of IL-7-producing cells in primary and secondary lymphoid organs using IL-7-GFP knock-in mice. J. Immunol. 2012. 189: 1577-1584.
21. Shinoda, K., Tokoyoda, K., Hanazawa, A., Hayashizaki, K., Zehentmeier, S., Hosokawa, H., Iwamura, C. et al., Type II membrane protein CD69 regulates the formation of resting T-helper memory. Proc. Natl. Acad. Sci. USA 2012. 109: 7409-7414.
22. Gebhardt, T., Wakim, L. M., Eidsmo, L., Reading, P. C., Heath, W. R. and Carbone, F. R., Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 2009. 10: 524-530.
23. + T(RM) cells providing global skin immunity. Nature 2012. 483: 227-231.
24. + tissue-resident memory T cells of skin. Nat. Immunol. 2013. 14: 1294-1301.
25. Mackay, L. K., Stock, A. T., Ma, J. Z., Jones, C. M., Kent, S. J., Mueller, S. N., Heath, W. R. et al., Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc. Natl. Acad. Sci. USA 2012. 109: 7037-7042.
26. Sathaliyawala, T., Kubota, M., Yudanin, N., Turner, D., Camp, P., Thome, J. J., Bickham, K. L. et al., Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 2013. 38: 187-197.
27. Casey, K. A., Fraser, K. A., Schenkel, J. M., Moran, A., Abt, M. C., Beura, L. K., Lucas, P. J. et al., Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J. Immunol. 2012. 188: 4866-4875.
28. Heffner, M. and Fearon, D. T., Loss of T cell receptor-induced Bmi-1 in the KLRG1(+) senescent CD8(+) T lymphocyte. Proc. Natl. Acad. Sci. USA 2007. 104: 13414-13419.
29. Joshi, N. S., Cui, W., Chandele, A., Lee, H. K., Urso, D. R., Hagman, J., Gapin, L. et al., Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 2007. 27: 281-295.
30. Matloubian, M., Lo, C. G., Cinamon, G., Lesneski, M. J., Xu, Y., Brinkmann, V., Allende, M. L. et al., Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 2004. 427: 355-360.
31. Bankovich, A. J., Shiow, L. R. and Cyster, J. G., CD69 suppresses sphingosine 1-phosophate receptor-1 (S1P1) function through interaction with membrane helix 4. J. Biol. Chem. 2010. 285: 22328-22337.
32. + T cells. Nat. Immunol. 2013. 14: 1285-1293.
33. Schenkel, J. M., Fraser, K. A. and Masopust, D., Cutting edge: resident memory CD8 T cells occupy frontline niches in secondary lymphoid organs. J. Immunol. 2014. 192: 2961-2964.
34. Snell, L. M., Lin, G. H. and Watts, T. H., IL-15-dependent upregulation of GITR on CD8 memory phenotype T cells in the bone marrow relative to spleen and lymph node suggests the bone marrow as a site of superior bioavailability of IL-15. J. Immunol. 2012. 188: 5915-5923.
35. Feuerer, M., Beckhove, P., Garbi, N., Mahnke, Y., Limmer, A., Hommel, M., Hammerling, G. J. et al., Bone marrow as a priming site for T cell responses to blood-borne antigen. Nat. Med. 2003. 9: 1151-1157.
36. Gerdes, J., Lemke, H., Baisch, H., Wacker, H. H., Schwab, U. and Stein, H., Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 1984. 133: 1710-1715.
37. Westendorf, K., Okhrimenko, A., Grun, J. R., Schliemann, H., Chang, H. D., Dong, J. and Radbruch, A., Unbiased transcriptomes of resting human CD4(+) CD45RO(+) T lymphocytes. Eur. J. Immunol. 2014. 44: 1866-1869.
38. Darzynkiewicz, Z., Gong, J., Juan, G., Ardelt, B. and Traganos, F., Cytometry of cyclin proteins. Cytometry 1996. 25: 1-13.
39. Murray, A. W., Recycling the cell cycle: cyclins revisited. Cell 2004. 116: 221-234.
40. Slifka, M. K., Antia, R., Whitmire, J. K. and Ahmed, R., Humoral immunity due to long-lived plasma cells. Immunity 1998. 8: 363-372.
41. Slifka, M. K., Matloubian, M. and Ahmed, R., Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol. 1995. 69: 1895-1902.
42. Manz, R. A., Lohning, M., Cassese, G., Thiel, A. and Radbruch, A., Survival of long-lived plasma cells is independent of antigen. Int. Immunol. 1998. 10: 1703-1711.
43. Hauser, A. E., Debes, G. F., Arce, S., Cassese, G., Hamann, A., Radbruch, A. and Manz, R. A., Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasma blasts during the time course of a memory immune response. J. Immunol. 2002. 169: 1277-1282.
44. Bernasconi, N. L., Traggiai, E. and Lanzavecchia, A., Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002. 298: 2199-2202.
45. Odendahl, M., Mei, H., Hoyer, B. F., Jacobi, A. M., Hansen, A., Muehlinghaus, G., Berek, C. et al., Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood 2005. 105: 1614-1621.
46. Mazzucchelli, R. I., Warming, S., Lawrence, S. M., Ishii, M., Abshari, M., Washington, A. V., Feigenbaum, L. et al., Visualization and identification of IL-7 producing cells in reporter mice. PLoS One 2009. 4: e7637.
47. Link, A., Vogt, T. K., Favre, S., Britschgi, M. R., Acha-Orbea, H., Hinz, B., Cyster, J. G. et al., Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 2007. 8: 1255-1265.
48. Repass, J. F., Laurent, M. N., Carter, C., Reizis, B., Bedford, M. T., Cardenas, K., Narang, P. et al., IL7-hCD25 and IL7-Cre BAC transgenic mouse lines: new tools for analysis of IL-7 expressing cells. Genesis 2009. 47: 281-287.
49. Shalapour, S., Deiser, K., Sercan, O., Tuckermann, J., Minnich, K., Willimsky, G., Blankenstein, T. et al., Commensal microflora and interferon-gamma promote steady-state interleukin-7 production in vivo. Eur. J. Immunol. 2010. 40: 2391-2400.
50. Nygren, J. M. and Bryder, D., A novel assay to trace proliferation history in vivo reveals that enhanced divisional kinetics accompany loss of hematopoietic stem cell self-renewal. PLoS One 2008. 3: e3710.
51. Lin, G. H., Edele, F., Mbanwi, A. N., Wortzman, M. E., Snell, L. M., Vidric, M., Roth, K. et al., Contribution of 4-1BBL on radioresistant cells in providing survival signals through 4-1BB expressed on CD8(+) memory T cells in the bone marrow. Eur. J. Immunol. 2012. 42: 2861-2874.
52. Becker, T. C., Wherry, E. J., Boone, D., Murali-Krishna, K., Antia, R., Ma, A. and Ahmed, R., Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J. Exp. Med. 2002. 195: 1541-1548.
53. Wherry, E. J., Becker, T. C., Boone, D., Kaja, M. K., Ma, A. and Ahmed, R., Homeostatic proliferation but not the generation of virus specific memory CD8 T cells is impaired in the absence of IL-15 or IL-15Ralpha. Adv. Exp. Med. Biol. 2002. 512: 165-175.
54. Schluns, K. S. and Lefrancois, L., Cytokine control of memory T cell development and survival. Nat. Rev. Immunol. 2003. 3: 269-279.
55. Kawamoto, T., Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch. Histol. Cytol. 2003. 66: 123-143.