Human bone marrow: A reservoir for "enhanced effector memory" CD8+ T cells with potent recall function

Journal of Immunology

Volumn 177, Issue 10, 2006, Pages 6730-6737

  Zhang, Xiaoyu ^a   Dong, Haidong ^b   Lin, Wei ^a   Voss, Stephen ^c   Hinkley, Lucinda ^c   Westergren, Melissa ^c   Tian, Guoliang ^d   Berry, Daniel ^c   Lewellen, David ^c   Vile, Richard G ^c   Chen, Lieping ^e   Farber, Donna L ^a   Strome, Scott E ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c Mayo Clinic   (United States)

^d UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^e JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD38 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR; GRANZYME B; HLA DR ANTIGEN; PERFORIN; T LYMPHOCYTE RECEPTOR; VIRUS ANTIGEN; VIRUS VACCINE;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CYTOTOXICITY; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; JOINT PROSTHESIS; LYMPHOCYTE FUNCTION; MALE; MEMORY T LYMPHOCYTE; OSTEOARTHRITIS; PRIORITY JOURNAL; RECEPTOR UPREGULATION;

EID: 33750825269     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.10.6730     Document Type: Article

References (57)

1. + T cells to antigen stimulation in vivo. Nat. Immunol. 1: 47-53.
2. + T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2: 415-422.
3. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262.
4. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 402: 708-712.
5. Masopust, D., V. Vezys, A. L. Marzo, and L. Lefrancois. 2001. Preferential localization of effector memory cells in noniymphoid tissue. Science 291: 2413-2417.
6. Khazaie, K., S. Prifti, P. Beckhove, A. Griesbach, S. Russell, M. Collins, and V. Schirrmacher. 1994. Persistence of dormant tumor cells in the bone marrow of tumor cell-vaccinated mice correlates with long-term immunological protection. Proc. Natl. Acad. Sci. USA 91: 7430-7434.
7. + immune T cells. Cancer Res. 58: 5439-5446.
8. Feuerer, M., P. Beckhove, L. Bai, E.-F. Solomayer, G. Bastert, I. J. Diel, C. Pedain, M. Oberniedermayr, V. Schirrmacher, and V. Umansky. 2001. Therapy of human tumors in NOD/SCID mice with patient-derived reactivated memory T cells from bone marrow. Nat. Med. 7: 452.
9. Bai, L., P. Beckhove, M. Feuerer, V. Umansky, C. Choi, F. Schutz Erich-Franz Solomayer, I. Diel, and V. Schirrmacher. 2003. Cognate interactions between memory T cell and tumor antigen-presenting dendritic cells from bone marrow of breast cancer patients: bidirectional cell stimulation, survival and antitumor activity in vivo. Int. J. Cancer 103: 73-83.
10. Beckhove, P., M, Feuerer, M. Dolenc, F. Schuetz, C. Choi, N. Sommerfeldt, J. Schwendemann, K. Ehlert, P. Altevogt, G. Basiert, et al. 2004. Specifically activated memory T cell subsets from cancer patients recognize and reject xenotransplanted autologous tumors. J. Clin. Invest. 114: 67-76.
11. Schmitz-Winnenthai, F. H., C. Volk, K. Z'Graggen, L. Galindo, D. Nummer, Y. Ziouta, M. Bucur, J. Weitz, V. Schirrmacher, M. W. Buchler, and P. Beckhove. 2005. High frequencies of functional tumor-reactive T cells in bone marrow and blood of pancreatic cancer patients. Cancer Res. 65: 10079-10087.
12. Choi, C., M. Witzens, M. Bucur, M. Feuerer, N. Sommerfeldt, A. Trojan, A. Ho, V. Schirrmacher, H. Goldschmidt, and P. Beckhove. 2005. Enrichment of functional CD8 memory T cells specific for MUC1 in bone marrow of patients with multiple myeloma. Blood 105: 2132-2134.
13. + memory T cells. Cancer Res. 63: 5582-5586.
14. Slifka, M. K., J. K. Whitmire, and R. Ahmed. 1997. Bone marrow contains virus-specific cytotoxic T lymphocytes. Blood 90: 2103-2108.
15. Grassland, K. D., V. K. Lee, W. Chen, S. R. Riddell, P. D. Greenberg, and M. A. Cheever. 1991. T cells from tumor-immune mice nonspecifically expanded in vitro with anti-CD3 plus IL-2 retain specific function in vitro and can eradicate disseminated leukemia in vivo. J. Immunol. 146: 4414-4420.
16. Currier, J. R., E. G. Kuta, E. Turk, L. B. Earhart, L. Loomis-Price, S. Janetzki, G. Ferrari, D. L. Birx, and J. H. Cox. 2002. A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J. Immunol. Methods 260: 157-172.
17. + T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78.
18. + central and effector memory T cell subsets are largely distinct. Immunity 18: 193-204.
19. Wherry, E. J., V. Teichgraber, T. C. Becker, D. Masopust, S. M. Kaech, R. Antia, U. H. von Andrian, and R. Ahmed. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4: 225-234.
20. + T cells play a prominent role in recall responses to secondary viral infection in the lung. J. Immunol. 172: 6533-6537.
21. Campbell, D. J., C. H. Kim, and E. C. Butcher. 2003. Chemokines in the systemic organization of immunity. Immunol. Rev. 195: 58-71.
22. Bleul, C. C., R. C. Fuhlbrigge, J. M. Casasnovas, A. Aiuti, and T. A. Springer. 1996. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J. Exp. Med. 184: 1101-1109.
23. + cells on vascular endothelium under shear flow. J. Clin. Invest. 104: 1199-1211.
24. Brouty-Boyé, D., C. Doucet, D. Clay, M. C Le Bousse-Kerdiles, T. J. Lampidis, and B. Azzarone. 1998. Phenotypic diversity in human fibroblasts from myelometaplasic and non-myelometaplasic hematopoietic tissues. Int. J. Cancer 76: 767-773.
25. Lee, S.-K., and C. D. Surh. 2005. Role of interleukin-7 in bone and T-cell homeostasis. Immunol. Rev. 208: 169-180.
26. + memory T cells by opposing cytokines. Science 288: 675-678.
27. Schluns, K. S., K. Williams, A. Ma, X. X. Zheng, and L. Lefrancois. 2002. Cutting edge: requirement for IL-15 in the generation of primary and memory antigen-specific CD8 T cells. J. Immunol. 168: 4827-4831.
28. Maraskovsky, E., M. Teepe, P. J. Morrissey, S. Braddy, R. E. Miller, D. H. Lynch, and J. J. Peschon. 1996. Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J. Immunol. 157: 5315-5323.
29. Schluns, K. S., W. C. Kieper, S. C. Jameson, and L. Lefrancois. 2000. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat. Immunol. 1: 426.
30. Feuerer, M., M. Rocha, L. Bai, V. Umansky, E. F. Solomayer, G. Basiert, I. J. Diel, and V. Schirrmacher. 2001. Enrichment of memory T cells and other profound immunological changes in the bone marrow from untreated breast cancer patients. Int. J. Cancer 92: 96-105.
31. Feuerer, M., P. Beckhove, N. Garbi, Y. Mahnke, A. Limmer, M. Hommel, G. J. Hammerling, B. Kyewski, A. Hamann, V. Umansky, and V. Schirrmacher. 2003. Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat. Med. 9: 1151-1157.
32. Sallusto, F., J. Geginat, and A. Lanzavecchja. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
33. + T cells. J. Exp. Med. 186: 1407-1418.
34. Dudley, M. E., J. R. Wunderlich, P. F. Robbins, J. C. Yang, P. Hwu, D. J. Schwartzentruber, S. L. Topalian, R. Sherry, N. P. Restifo, A. M. Hubicki, et al. 2002. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854.
35. + tumor-reactive effector memory T cells in humans after adoptive transfer therapy. Blood 105: 241-250.
36. + cytotoxic T lymphocytes in HIV infected patients. J. Exp. Med. 200: 1407-1417.
37. Mills, K. C., T. G. Gross, M. L. Varney, D. G. Heimann, E. C. Reed, A. Kessinger, and J. E. Talmadge. 1996. Immunologic phenotype and function in human bone marrow, blood stem cells and umbilical cord blood. Bone Marrow Transplant. 18:53-61.
38. Di Rosa, F., and A. Santoni. 2002. Bone marrow CD8 T cells are in a different activation state than those in the lymphoid periphery. Eur. J. Immunol. 32: 1873-1880.
39. Wright, D. E., E. P. Bowman, A. J. Wagers, E. C. Butcher, and I. L. Weissman. 2002. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J. Exp. Med. 195: 1145-1154.
40. Peled, A., I. Petit, O. Kollet, M. Magid, T. Ponomaryov, T. Byk, A. Nagler, H. Ben-Hur, A. Many, L. Shultz, et al. 1999. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283: 845-848.
41. Pruijt, J. F. M., P. Verzaal, R. van Os, E.-J. F. M. de Kruijf, M. L. J. van Schie, A. Mantovani, A. Vecchi, I. J. D. Lindley, R. Willemze, S. Starckx, et al. 2002. Neutrophils are indispensable for hematopoietic stem cell mobilization induced by interleukin-8 in mice. Proc. Natl. Acad. Sci. USA 99: 6228-6233.
42. Schluns, K, S., and L. Lefrancois. 2003. Cytokine control of memory T-cell development and survival. Nat. Rev. Immunol. 3: 269-279.
43. Gutierrez-Ramos, J., C. Olsson, and R. Palacios. 1992. Interleukin (IL1 to IL7) gene expression in fetal liver and bone marrow stromal clones: cytokine-mediated positive and negative regulation. Exp. Hematol. 20: 986-990.
44. Giuliani, N., S. Colla, R. Sala, M. Moroni, M. Lazzaretti, S. La Monica, S. Bonomini, M. Hojden, G. Sammarelli, S. Barille, et al. 2002. Human myeloma cells stimulate the receptor activator of nuclear factor-κB ligand (RANKL) in T lymphocytes: a potential role in multiple myeloma bone disease. Blood 100: 4615-4621.
45. + T cells is dispensable for T cell memory. Proc. Natl. Acad. Sci. USA 100: 4724-4729.
46. + bone marrow-derived cells. Blood 103: 988-994.
47. Sandau, M. M., K. S. Schluns, L. Lefrancois, and S. C. Jameson. 2004. Cutting edge: transpresentation of IL-15 by bone marrow-derived cells necessitates expression of IL-15 and IL-15Rα by the same cells. J. Immunol. 173: 6537-6541.
48. + T cell homeostasis. J. Exp. Med. 200: 825-834.
49. Sakata, M., K. Masuko-Hongo, H. Nakamura, H. Onuma, J. Tsuruha, H. Aoki, K. Nishioka, and T. Kato. 2003. Osteoarthritic articular chondrocytes stimulate autologous T cell responses in vitro. Clin. Exp. Rheumatol. 21: 704-710.
50. Benito, M. J., D. J. Veale, O. FitzGerald, W. B. van den Berg, and B. Bresnihan. 2005. Synovial tissue inflammation in early and late osteoarthritis. Ann. Rheum. Dis. 64: 1263-1267.
51. Sakkas, L. I., C. Scanzello, N. Johanson, J. Burkholder, A. Mitra, P. Salgame, C. D. Katsetos, and C. D. Platsoucas. 1998. T cells and T-cell cytokine transcripts in the synovial membrane in patients with osteoarthritis. Clin. Diagn. Lab. Immunol. 5: 430-437.
52. Liossis, S.-N. C., and G. C. Tsokos. 1998. Cellular immunity in osteoarthritis: novel concepts for an old disease. Clin. Diagn. Lab. Immunol. 5: 427-429.
53. Chen, T., and D. Hudnall. 2006. Anatomical mapping of human herpesvirus reservoirs of infection. Mod. Pathol. 19: 726-737.
54. + T cells. Immunity 22: 259-270.
55. + T cells. Mech. Ageing Dev. 125: 615.
56. + T cells. J. Exp. Med. 194: 953-966.
57. Jacob, J., and D. Baltimore. 1999. Modelling T-cell memory by genetic marking of memory T cells in vivo. Nature 399: 593-597.