Memory stem T cells in autoimmune disease: High frequency of circulating CD8+ memory stem cells in acquired aplastic anemia

Journal of Immunology

Volumn 196, Issue 4, 2016, Pages 1568-1578

  Hosokawa, Kohei ^a   Muranski, Pawel ^a   Feng, Xingmin ^a   Townsley, Danielle M ^a   Liu, Baoying ^b   Knickelbein, Jared ^b   Keyvanfar, Keyvan ^a   Dumitriu, Bogdan ^a   Ito, Sawa ^a   Kajigaya, Sachiko ^a   Taylor, James G ^a   Kaplan, Mariana J ^c   Nussenblatt, Robert B ^b   Barrett, A John ^a   O'Shea, John ^c   Young, Neal S ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL EYE INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; GAMMA INTERFERON; INTERLEUKIN 2;

ADULT; AGED; ANEMIA, APLASTIC; ANEMIA, SICKLE CELL; AUTOIMMUNE DISEASE; BIOSYNTHESIS; BLOOD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLASSIFICATION; FEMALE; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; PRE T LYMPHOCYTE; RECURRENT DISEASE; T LYMPHOCYTE SUBPOPULATION; TREATMENT FAILURE; UVEITIS;

ADULT; AGED; ANEMIA, APLASTIC; ANEMIA, SICKLE CELL; AUTOIMMUNE DISEASES; BIOMARKERS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; INTERLEUKIN-2; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; PRECURSOR CELLS, T-LYMPHOID; RECURRENCE; T-LYMPHOCYTE SUBSETS; TREATMENT FAILURE; UVEITIS;

EID: 84958576256     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501739     Document Type: Article

References (59)

1. Young, N. S., R. T. Calado, and P. Scheinberg. 2006. Current concepts in the pathophysiology and treatment of aplastic anemia. Blood 108: 2509-2519.
2. Scheinberg, P., and N. S. Young. 2012. How I treat acquired aplastic anemia. Blood 120: 1185-1196.
3. Risitano, A. M., H. Kook, W. Zeng, G. Chen, N. S. Young, and J. P. Maciejewski. 2002. Oligoclonal and polyclonal CD4 and CD8 lymphocytes in aplastic anemia and paroxysmal nocturnal hemoglobinuria measured by V beta CDR3 spectratyping and flow cytometry. Blood 100: 178-183.
4. Nakao, S., A. Takami, H. Takamatsu, W. Zeng, N. Sugimori, H. Yamazaki, Y. Miura, M. Ueda, S. Shiobara, T. Yoshioka, et al. 1997. Isolation of a T-cell clone showing HLA-DRB1∗0405-restricted cytotoxicity for hematopoietic cells in a patient with aplastic anemia. Blood 89: 3691-3699.
5. Sloand, E., S. Kim, J. P. Maciejewski, J. Tisdale, D. Follmann, and N. S. Young. 2002. Intracellular interferon-gamma in circulating and marrow T cells detected by flow cytometry and the response to immunosuppressive therapy in patients with aplastic anemia. Blood 100: 1185-1191.
6. Risitano, A. M., J. P. Maciejewski, S. Green, M. Plasilova, W. Zeng, and N. S. Young. 2004. In-vivo dominant immune responses in aplastic anaemia: molecular tracking of putatively pathogenetic T-cell clones by TCR beta-CDR3 sequencing. Lancet 364: 355-364.
7. Maciejewski, J. P., D. Follmann, R. Nakamura, Y. Saunthararajah, C. E. Rivera, T. Simonis, K. E. Brown, J. A. Barrett, and N. S. Young. 2001. Increased frequency of HLA-DR2 in patients with paroxysmal nocturnal hemoglobinuria and the PNH/aplastic anemia syndrome. Blood 98: 3513-3519.
8. Katagiri, T., A. Sato-Otsubo, K. Kashiwase, S. Morishima, Y. Sato, Y. Mori, M. Kato, M. Sanada, Y. Morishima, K. Hosokawa, et al; Japan Marrow Donor Program. 2011. Frequent loss of HLA alleles associated with copy numberneutral 6pLOH in acquired aplastic anemia. Blood 118: 6601-6609.
9. Scheinberg, P., O. Nunez, B. Weinstein, P. Scheinberg, A. Biancotto, C. O. Wu, and N. S. Young. 2011. Horse versus rabbit antithymocyte globulin in acquired aplastic anemia. N. Engl. J. Med. 365: 430-438.
10. Sallusto, F., D. Lenig, R. Fö rster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
11. Hu, X., Y. Gu, Y. Wang, Y. Cong, X. Qu, and C. Xu. 2009. Increased CD4+ and CD8+ effector memory T cells in patients with aplastic anemia. Haematologica 94: 428-429.
12. Gattinoni, L., E. Lugli, Y. Ji, Z. Pos, C. M. Paulos, M. F. Quigley, J. R. Almeida, E. Gostick, Z. Yu, C. Carpenito, et al. 2011. A human memory T cell subset with stem cell-like properties. Nat. Med. 17: 1290-1297.
13. Gattinoni, L. 2014. Memory T cells officially join the stem cell club. Immunity 41: 7-9.
14. 1987. Incidence of aplastic anemia: The relevance of diagnostic criteria. By the International Agranulocytosis and Aplastic Anemia Study. Blood 70: 1718-1721.
15. Camitta, B. M., E. D. Thomas, D. G. Nathan, G. Santos, E. C. Gordon-Smith, R. P. Gale, J. M. Rappeport, and R. Storb. 1976. Severe aplastic anemia: A prospective study of the effect of early marrow transplantation on acute mortality. Blood 48: 63-70.
16. Hochberg, M. C. 1997. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40: 1725.
17. Gladman, D. D., D. Ibanez, and M. B. Urowitz. 2002. Systemic lupus erythematosus disease activity index 2000. J. Rheumatol. 29: 288-291.
18. Lugli, E., L. Gattinoni, A. Roberto, D. Mavilio, D. A. Price, N. P. Restifo, and M. Roederer. 2013. Identification, isolation and in vitro expansion of human and nonhuman primate T stem cell memory cells. Nat. Protoc. 8: 33-42.
19. Legat, A., D. E. Speiser, H. Pircher, D. Zehn, and S. A. Fuertes Marraco. 2013. Inhibitory Receptor Expression Depends More Dominantly on Differentiation and Activation than "Exhaustion" of Human CD8 T Cells. Front. Immunol. 4: 455.
20. Camitta, B. M., and K. Doney. 1990. Immunosuppressive therapy for aplastic anemia: indications, agents, mechanisms, and results. Am. J. Pediatr. Hematol. Oncol. 12: 411-424.
21. Wu, H., M. Miao, G. Zhang, Y. Hu, Z. Ming, and X. Zhang. 2009. Soluble PD-1 is associated with aberrant regulation of T cells activation in aplastic anemia. Immunol. Invest. 38: 408-421.
22. Jiao, Q., C. Liu, Z. Yang, Q. Ding, M. Wang, M. Li, T. Zhu, H. Qian, W. Li, N. Tu, et al. 2014. Upregulated PD-1 Expression Is Associated with the Development of Systemic Lupus Erythematosus, but Not the PD-1.1 Allele of the PDCD1 Gene. Int. J. Genomics 2014: 950903.
23. Gianchecchi, E., D. V. Delfino, and A. Fierabracci. 2013. Recent insights into the role of the PD-1/PD-L1 pathway in immunological tolerance and autoimmunity. Autoimmun. Rev. 12: 1091-1100.
24. Adekambi, T., C. C. Ibegbu, A. S. Kalokhe, T. Yu, S. M. Ray, and J. Rengarajan. 2012. Distinct effector memory CD4+ T cell signatures in latent Mycobacterium tuberculosis infection, BCG vaccination and clinically resolved tuberculosis. PLoS One 7: e36046.
25. + memory T Cells. Nat. Commun. 5: 5407.
26. Baitsch, L., A. Legat, L. Barba, S. A. Fuertes Marraco, J. P. Rivals, P. Baumgaertner, C. Christiansen-Jucht, H. Bouzourene, D. Rimoldi, H. Pircher, et al. 2012. Extended co-expression of inhibitory receptors by human CD8 Tcells depending on differentiation, antigen-specificity and anatomical localization. PLoS One 7: e30852.
27. Riches, J. C., J. K. Davies, F. McClanahan, R. Fatah, S. Iqbal, S. Agrawal, A. G. Ramsay, and J. G. Gribben. 2013. T cells from CLL patients exhibit features of T-cell exhaustion but retain capacity for cytokine production. Blood 121: 1612-1621.
28. Lee, R. W., L. B. Nicholson, H. N. Sen, C. C. Chan, L. Wei, R. B. Nussenblatt, and A. D. Dick. 2014. Autoimmune and autoinflammatory mechanisms in uveitis. Semin. Immunopathol. 36: 581-594.
29. Gualtierotti, R., M. Biggioggero, A. E. Penatti, and P. L. Meroni. 2010. Updating on the pathogenesis of systemic lupus erythematosus. Autoimmun. Rev. 10: 3-7.
30. Van Epps, P., R. Banks, H. Aung, M. R. Betts, and D. H. Canaday. 2014. Agerelated differences in polyfunctional T cell responses. Immun. Ageing 11: 14.
31. Mateus, J., P. Lasso, P. Pavia, F. Rosas, N. Roa, C. A. Valencia-Hernández, J. M. González, C. J. Puerta, and A. Cuéllar. 2015. Low frequency of circulating CD8+ T stem cell memory cells in chronic chagasic patients with severe forms of the disease. PLoS Negl. Trop. Dis. 9: e3432.
32. Klatt, N. R., S. E. Bosinger, M. Peck, L. E. Richert-Spuhler, A. Heigele, J. P. Gile, N. Patel, J. Taaffe, B. Julg, D. Camerini, et al. 2014. Limited HIV infection of central memory and stem cell memory CD4+ T cells is associated with lack of progression in viremic individuals. PLoS Pathog. 10: e1004345.
33. Gattinoni, L., and N. P. Restifo. 2013. Moving T memory stem cells to the clinic. Blood 121: 567-568.
34. Flynn, J. K., and P. R. Gorry. 2014. Stem memory T cells (TSCM)-their role in cancer and HIV immunotherapies. Clin. Transl. Immunology 3: e20.
35. Cieri, N., G. Oliveira, R. Greco, M. Forcato, C. Taccioli, B. Cianciotti, V. Valtolina, M. Noviello, L. Vago, A. Bondanza, et al. 2015. Generation of human memory stem T cells after haploidentical T-replete hematopoietic stem cell transplantation. Blood 125: 2865-2874.
36. Roberto, A., L. Castagna, V. Zanon, S. Bramanti, R. Crocchiolo, J. E. McLaren, S. Gandolfi, P. Tentorio, B. Sarina, I. Timofeeva, et al. 2015. Role of naivederived T memory stem cells in T-cell reconstitution following allogeneic transplantation. Blood 125: 2855-2864.
37. Nagai, Y., M. Kawahara, M. Hishizawa, Y. Shimazu, N. Sugino, S. Fujii, N. Kadowaki, and A. Takaori-Kondo. 2015. T memory stem cells are the hierarchical apex of adult T-cell leukemia. Blood 125: 3527-3535.
38. Lugli, E., M. H. Dominguez, L. Gattinoni, P. K. Chattopadhyay, D. L. Bolton, K. Song, N. R. Klatt, J. M. Brenchley, M. Vaccari, E. Gostick, et al. 2013. Superior T memory stem cell persistence supports long-lived T cell memory. J. Clin. Invest. 123: 594-599.
39. Sailler, L., B. Puissant, P. Méliani, J. O. Castex, S. Saivin, D. Adoue, B. Fournie, P. Arlet, J. L. Montastruc, M. Lapeyre-Mestre, et al. 2007. Blood concentrations of hydroxychloroquine and its desethyl derivative correlate negatively with the percentage of CD45RO+ cells among CD4+ lymphocytes in hydroxychloroquine-treated lupus patients. Ann. N. Y. Acad. Sci. 1108: 41-50.
40. Kordasti, S., J. Marsh, S. Al-Khan, J. Jiang, A. Smith, A. Mohamedali, P. P. Abellan, C. Veen, B. Costantini, A. G. Kulasekararaj, et al. 2012. Functional characterization of CD4+ T cells in aplastic anemia. Blood 119: 2033-2043.
41. Solomou, E. E., K. Rezvani, S. Mielke, D. Malide, K. Keyvanfar, V. Visconte, S. Kajigaya, A. J. Barrett, and N. S. Young. 2007. Deficient CD4+ CD25+ FOXP3+ T regulatory cells in acquired aplastic anemia. Blood 110: 1603-1606.
42. de Latour, R. P., V. Visconte, T. Takaku, C. Wu, A. J. Erie, A. K. Sarcon, M. J. Desierto, P. Scheinberg, K. Keyvanfar, O. Nunez, et al. 2010. Th17 immune responses contribute to the pathophysiology of aplastic anemia. Blood 116: 4175-4184.
43. Yeh, S., Z. Li, F. Forooghian, F. S. Hwang, M. A. Cunningham, S. Pantanelli, J. C. Lew, K. K. Wroblewski, S. Vitale, and R. B. Nussenblatt. 2009. CD4+Foxp3+ T-regulatory cells in noninfectious uveitis. Arch. Ophthalmol. 127: 407-413.
44. Amadi-Obi, A., C. R. Yu, X. Liu, R. M. Mahdi, G. L. Clarke, R. B. Nussenblatt, I. Gery, Y. S. Lee, and C. E. Egwuagu. 2007. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13: 711-718.
45. Martin, J. C., D. L. Baeten, and R. Josien. 2014. Emerging role of IL-17 and Th17 cells in systemic lupus erythematosus. Clin. Immunol. 154: 1-12.
46. Mellor-Pita, S., M. J. Citores, R. Castejon, P. Tutor-Ureta, M. Yebra-Bango, J. L. Andreu, and J. A. Vargas. 2006. Decrease of regulatory T cells in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 65: 553-554.
47. Shin, M. S., N. Lee, and I. Kang. 2011. Effector T-cell subsets in systemic lupus erythematosus: update focusing on Th17 cells. Curr. Opin. Rheumatol. 23: 444-448.
48. McPherson, S. W., J. Yang, C. C. Chan, C. Dou, and D. S. Gregerson. 2003. Resting CD8 T cells recognize beta-galactosidase expressed in the immuneprivileged retina and mediate autoimmune disease when activated. Immunology 110: 386-396.
49. Calder, V. L., Z. S. Zhao, Y. Wang, K. Barton, and S. L. Lightman. 1993. Effects of CD8 depletion on retinal soluble antigen induced experimental autoimmune uveoretinitis. Immunology 79: 255-262.
50. Mak, A., and N. Y. Kow. 2014. The pathology of T cells in systemic lupus erythematosus. J. Immunol. Res. 2014: 419029.
51. Kamphorst, A. O., and R. Ahmed. 2013. Manipulating the PD-1 pathway to improve immunity. Curr. Opin. Immunol. 25: 381-388.
52. Dolff, S., D. Quandt, T. Feldkamp, C. Jun, A. Mitchell, F. Hua, C. Specker, A. Kribben, O. Witzke, and B. Wilde. 2014. Increased percentages of PD-1 on CD4+ T cells is associated with higher INF-g production and altered IL-17 production in patients with systemic lupus erythematosus. Scand. J. Rheumatol. 43: 307-313.
53. Thompson, R. H., H. Dong, C. M. Lohse, B. C. Leibovich, M. L. Blute, J. C. Cheville, and E. D. Kwon. 2007. PD-1 is expressed by tumor-infiltrating immune cells and is associated with poor outcome for patients with renal cell carcinoma. Clin. Cancer Res. 13: 1757-1761.
54. Konishi, J., K. Yamazaki, M. Azuma, I. Kinoshita, H. Dosaka-Akita, and M. Nishimura. 2004. B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clin. Cancer Res. 10: 5094-5100.
55. Gros, A., P. F. Robbins, X. Yao, Y. F. Li, S. Turcotte, E. Tran, J. R. Wunderlich, A. Mixon, S. Farid, M. E. Dudley, et al. 2014. PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors. J. Clin. Invest. 124: 2246-2259.
56. Duraiswamy, J., C. C. Ibegbu, D. Masopust, J. D. Miller, K. Araki, G. H. Doho, P. Tata, S. Gupta, M. J. Zilliox, H. I. Nakaya, et al. 2011. Phenotype, function, and gene expression profiles of programmed death-1(hi) CD8 T cells in healthy human adults. J. Immunol. 186: 4200-4212.
57. Kook, H., A. M. Risitano, W. Zeng, M. Wlodarski, C. Lottemann, R. Nakamura, J. Barrett, N. S. Young, and J. P. Maciejewski. 2002. Changes in T-cell receptor VB repertoire in aplastic anemia: effects of different immunosuppressive regimens. Blood 99: 3668-3675.
58. Fasano, R. M., G. S. Booth, M. Miles, L. Du, T. Koyama, E. R. Meier, and N. L. Luban. 2015. Red blood cell alloimmunization is influenced by recipient inflammatory state at time of transfusion in patients with sickle cell disease. Br. J. Haematol. 168: 291-300.
59. Lee, S. P., K. I. Ataga, E. P. Orringer, D. R. Phillips, and L. V. Parise. 2006. Biologically active CD40 ligand is elevated in sickle cell anemia: potential role for platelet-mediated inflammation. Arterioscler. Thromb. Vasc. Biol. 26: 1626-1631.