Accumulation of 4-1BBL+ B cells in the elderly induces the generation of granzyme-B+ CD8+ T cells with potential antitumor activity

Blood

Volumn 124, Issue 9, 2014, Pages 1450-1459

  Lee Chang, Catalina ^a   Bodogai, Monica ^a   Moritoh, Kanako ^a   Olkhanud, Purevdorj B ^a   Chan, Andrew C ^b   Croft, Michael ^c   Mattison, Julie A ^d   Holst, Peter Johannes ^e   Gress, Ronald E ^f   Ferrucci, Luigi ^d   Hakim, Fran ^f   Biragyn, Arya ^a  

^a Laboratory of Molecular Biology and Immunology   (United States)

^b GENENTECH INC   (United States)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^d NATIONAL INSTITUTE ON AGING   (United States)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD137 LIGAND; GLYCOPROTEIN GP 100; GRANZYME B; CD137 ANTIGEN; GRANZYME; GZMB PROTEIN, HUMAN; GZMB PROTEIN, MOUSE; TNFSF9 PROTEIN, HUMAN; TNFSF9 PROTEIN, MOUSE;

AGE DISTRIBUTION; AGED; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; B LYMPHOCYTE; CANCER GROWTH; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHEMOTHERAPY; CLINICAL ARTICLE; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; HYPOTHESIS; IMMUNE RECONSTITUTION; IMMUNOLOGICAL PARAMETERS; MELANOMA B16; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; RHESUS MONKEY; STEM CELL EXPANSION; VERY ELDERLY; ADULT; AGING; ANIMAL; C57BL MOUSE; CYTOLOGY; DEFICIENCY; ENZYMOLOGY; EXPERIMENTAL MELANOMA; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

4-1BB LIGAND; ADULT; AGED; AGED, 80 AND OVER; AGING; ANIMALS; ANTIGENS, CD137; B-LYMPHOCYTE SUBSETS; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; GRANZYMES; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; MACACA MULATTA; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MIDDLE AGED; SIGNAL TRANSDUCTION;

EID: 84907320066     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-03-563940     Document Type: Article

References (50)

1. Roeder I, Horn K, Sieburg HB, Cho R, Muller-Sieburg C, Loeffler M. Characterization and quantification of clonal heterogeneity among hematopoietic stem cells: a model-based approach. Blood. 2008;112(13):4874-4883.
2. Cho RH, Sieburg HB, Muller-Sieburg CE. A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells. Blood. 2008;111(12):5553-5561.
3. Kuranda K, Vargaftig J, de la Rochere P, et al. Age-related changes in human hematopoietic stem/progenitor cells. Aging Cell. 2011;10(3): 542-546.
4. Guerrettaz LM, Johnson SA, Cambier JC. Acquired hematopoietic stem cell defects determine B-cell repertoire changes associated with aging. Proc Natl Acad Sci USA. 2008; 105(33):11898-11902.
5. Cancro MP, Allman DM. Connecting the dots: revealing the interactions of lymphocyte development and homeostasis in the immunobiology of aging. Semin Immunol. 2005; 17(5):319-320.
6. Rubtsov AV, Rubtsova K, Fischer A, et al. Toll-like receptor 7 (TLR7)-driven accumulation of a novel CD11c+ B-cell population is important for the development of autoimmunity. Blood. 2011; 118(5):1305-1315.
7. Hao Y, O'Neill P, Naradikian MS, Scholz JL, Cancro MP. A B-cell subset uniquely responsive to innate stimuli accumulates in aged mice. Blood. 2011;118(5):1294-1304.
8. Ratliff M, Alter S, Frasca D, Blomberg BB, Riley RL. In senescence, age-associated B cells secrete TNFα and inhibit survival of B-cell precursors. Aging Cell. 2013;12(2):303-311.
9. Tomihara K, Shin T, Hurez VJ, et al. Aging-associated B7-DC+ B cells enhance anti-tumor immunity via Th1 and Th17 induction. Aging Cell. 2012;11(1):128-138.
10. Koch S, Larbi A, Derhovanessian E, Ozcelik D, Naumova E, Pawelec G. Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun Ageing. 2008;5:6.
11. Lerner A, Yamada T, Miller RA. Pgp-1hi T lymphocytes accumulate with age in mice and respond poorly to concanavalin A. Eur J Immunol. 1989;19(6):977-982.
12. Park W, Weyand CM, Schmidt D, Goronzy JJ. Co-stimulatory pathways controlling activation and peripheral tolerance of human CD4+CD28-T cells. Eur J Immunol. 1997;27(5):1082-1090.
13. Weyand CM, Brandes JC, Schmidt D, Fulbright JW, Goronzy JJ. Functional properties of CD4+ CD28- T cells in the aging immune system. Mech Ageing Dev. 1998;102(2-3):131-147.
14. Effros RB, Boucher N, Porter V, et al. Decline in CD28+ T cells in centenarians and in long-term T cell cultures: a possible cause for both in vivo and in vitro immunosenescence. Exp Gerontol. 1994;29(6):601-609.
15. Fann M, Chiu WK, Wood WH 3rd, Levine BL, Becker KG, Weng NP. Gene expression characteristics of CD28null memory phenotype CD8+ T cells and its implication in T-cell aging. Immunol Rev. 2005;205:190-206.
16. Strioga M, Pasukoniene V, Characiejus D. CD8+ CD28- and CD8+ CD57+ T cells and their role in health and disease. Immunology. 2011;134(1): 17-32.
17. Mikulkova Z, Praksova P, Stourac P, et al. Numerical defects in CD8+CD28- T-suppressor lymphocyte population in patients with type 1 diabetes mellitus and multiple sclerosis. Cell Immunol. 2010;262(2):75-79.
18. Morgan MD, Pachnio A, Begum J, et al. CD4+CD28- T cell expansion in granulomatosis with polyangiitis (Wegener's) is driven by latent cytomegalovirus infection and is associated withan increased risk of infection and mortality. Arthritis Rheum. 2011;63(7):2127-2137.
19. Goronzy JJ, Weyand CM. Immune aging and autoimmunity. Cell Mol Life Sci. 2012;69(10):1615-1623.
20. Sportès C, Steinberg SM, Liewehr DJ, et al. Strategies to improve long-term outcome in stage IIIB inflammatory breast cancer: multimodality treatment including dose-intensive induction and high-dose chemotherapy. Biol Blood Marrow Transplant. 2009;15(8):963-970.
21. Bodogai M, Lee Chang C, Wejksza K, et al.Anti-CD20 antibody promotes cancer escape via enrichment of tumor-evoked regulatory B cells expressing low levels of CD20 and CD137L. Cancer Res. 2013;73(7):2127-2138.
22. Cooper D, Bansal-Pakala P, Croft M. 4-1BB (CD137) controls the clonal expansion and survival of CD8 T cells in vivo but does not contribute to the development of cytotoxicity. Eur J Immunol. 2002;32(2):521-529.
23. Watts TH, DeBenedette MA. T cell co-stimulatory molecules other than CD28. Curr Opin Immunol. 1999;11(3):286-293.
24. Vinay DS, Kwon BS. 4-1BB signaling beyond T cells. Cell Mol Immunol. 2011;8(4):281-284.
25. Bouaziz JD, Yanaba K, Venturi GM, et al.Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc Natl Acad Sci USA. 2007;104(52):20878-20883.
26. Townsend MJ, Monroe JG, Chan AC. B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol Rev. 2010;237(1):264-283.
27. Denduluri N, Ershler WB. Aging biology and cancer. Semin Oncol. 2004;31(2):137-148.
28. Ershler WB, Socinski MA, Greene CJ. Bronchogenic cancer, metastases, and aging. J Am Geriatr Soc. 1983;31(11):673-676.
29. Weedon-Fekjaer H, Lindqvist BH, Vatten LJ, Aalen OO, Tretli S. Breast cancer tumor growth estimated through mammography screening data. Breast Cancer Res. 2008;10(3):R41.
30. Leibovici J, Itzhaki O, Kaptzan T, et al. Designing ageing conditions in tumour microenvironmenta new possible modality for cancer treatment. Mech Ageing Dev. 2009;130(1-2):76-85.
31. Overwijk WW, Theoret MR, Finkelstein SE, et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med. 2003;198(4):569-580.
32. Zhao Y, Croft M. Dispensable role for 4-1BB and 4-1BBL in development of vaccinia virus-specific CD8 T cells. Immunol Lett. 2012;141(2):220-226.
33. Zhao S, Zhang H, Xing Y, Natkunam Y. CD137 ligand is expressed in primary and secondary lymphoid follicles and in B-cell lymphomas: diagnostic and therapeutic implications. Am J Surg Pathol. 2013;37(2):250-258.
34. Vallejo AN. CD28 extinction in human T cells: altered functions and the program of T-cell senescence. Immunol Rev. 2005;205:158-169.
35. Ortiz-Suárez A, Miller RA. A subset of CD8 memory T cells from old mice have high levels of CD28 and produce IFN-gamma. Clin Immunol. 2002;104(3):282-292.
36. Keren Z, Naor S, Nussbaum S, et al. B-cell depletion reactivates B lymphopoiesis in the BM and rejuvenates the B lineage in aging. Blood. 2011;117(11):3104-3112.
37. Ershler WB, Stewart JA, Hacker MP, Moore AL, Tindle BH. B16 murine melanoma and aging: slower growth and longer survival in old mice. J Natl Cancer Inst. 1984;72(1):161-164.
38. Donin N, Sinai J, Michowitz M, Hiss J, Nordenberg J, Leibovici J. Role of immune response as determinant of tumor progression in function of host age in the B16 melanoma. Mech Ageing Dev. 1995;80(2):121-137.
39. Pagès F, Berger A, Camus M, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med. 2005;353(25): 2654-2666.
40. Lindstrom TM, Robinson WH. Rheumatoid arthritis: a role for immunosenescence? J Am Geriatr Soc. 2010;58(8):1565-1575.
41. Dauby N, Kummert C, Lecomte S, et al. Primary human cytomegalovirus infection induces the expansion of virus-specific activated and atypical memory B cells. J Infect Dis. 2014;jiu255. [Epub ahead of print]
42. Williams KM, Hakim FT, Gress RE. T cell immune reconstitution following lymphodepletion. Semin Immunol. 2007;19(5):318-330.
43. Rivera A, Chen CC, Ron N, Dougherty JP, Ron Y. Role of B cells as antigen-presenting cells in vivo revisited: antigen-specific B cells are essential for T cell expansion in lymph nodes and for systemic T cell responses to low antigen concentrations. Int Immunol. 2001;13(12):1583-1593.
44. von Bergwelt-Baildon MS, Vonderheide RH, Maecker B, et al. Human primary and memory cytotoxic T lymphocyte responses are efficiently induced by means of CD40-activated B cells as antigen-presenting cells: potential for clinical application. Blood. 2002;99(9):3319-3325.
45. Skelsey ME, Mayhew E, Niederkorn JY. Splenic B cells act as antigen presenting cells for the induction of anterior chamber-associated immune deviation. Invest Ophthalmol Vis Sci. 2003;44(12): 5242-5251.
46. Ceeraz S, Hall C, Choy EH, Spencer J, Corrigall VM. Defective CD8+CD28+ regulatory T cell suppressor function in rheumatoid arthritis is restored by tumour necrosis factor inhibitor therapy. Clin Exp Immunol. 2013;174(1):18-26.
47. Labalette M, Salez F, Pruvot FR, Noel C, Dessaint JP. CD8 lymphocytosis in primary cytomegalovirus (CMV) infection of allograft recipients: expansion of an uncommon CD8+ CD57- subset and its progressive replacement by CD8+CD57+ T cells. Clin Exp Immunol. 1994; 95(3):465-471.
48. Wallace DL, Masters JE, De Lara CM, et al. Human cytomegalovirus-specific CD8(+) T-cell expansions contain long-lived cells that retain functional capacity in both young and elderly subjects. Immunology. 2011;132(1):27-38.
49. Petrova M, Muhtarova M, Nikolova M, et al. Chronic Epstein-Barr virus-related hepatitis in immunocompetent patients. World J Gastroenterol. 2006;12(35):5711-5716.
50. Wikby A, Maxson P, Olsson J, Johansson B, Ferguson FG. Changes in CD8 and CD4 lymphocyte subsets, T cell proliferation responses and non-survival in the very old: the Swedish longitudinal OCTO-immune study. Mech Ageing Dev. 1998;102(2-3):187-198.