Chronic lymphocytic leukemia cells are activated and proliferate in response to specific T helper cells

Cell Reports

Volumn 4, Issue 3, 2013, Pages 566-577

  Os, Audun ^a   Bürgler, Simone ^a,b   Ribes, AnnaParente ^a   Funderud, Ane ^a   Wang, Dong ^a   Thompson, KeithM ^a   Tjønnfjord, GeirE ^a,b   Bogen, Bjarne ^a   Munthe, LudvigA ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD40 LIGAND; LEUKEMIA ANTIGEN; PARAPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL INTERACTION; CELL PROLIFERATION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; GENE EXPRESSION; HELPER CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; STEM CELL NICHE; TH1 CELL;

ANIMALS; ANTIGEN-PRESENTING CELLS; CELL GROWTH PROCESSES; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; MICE, SCID; TH1 CELLS; TRANSCRIPTOME; TUMOR MICROENVIRONMENT;

EID: 84881613238     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.011     Document Type: Article

References (44)

1. Bagnara D., Kaufman M.S., Calissano C., Marsilio S., Patten P.E., Simone R., Chum P., Yan X.J., Allen S.L., Kolitz J.E., et al. A novel adoptive transfer model of chronic lymphocytic leukemia suggests a key role for T lymphocytes in the disease. Blood 2011, 117:5463-5472.
2. Bishop G.A., Moore C.R., Xie P., Stunz L.L., Kraus Z.J. TRAF proteins in CD40 signaling. Adv. Exp. Med. Biol. 2007, 597:131-151.
3. Burger J.A., Ghia P., Rosenwald A., Caligaris-Cappio F. The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood 2009, 114:3367-3375.
4. Buschle M., Campana D., Carding S.R., Richard C., Hoffbrand A.V., Brenner M.K. Interferon gamma inhibits apoptotic cell death in B cell chronic lymphocytic leukemia. J.Exp. Med. 1993, 177:213-218.
5. Caligaris-Cappio F. B-chronic lymphocytic leukemia: a malignancy of anti-self B cells. Blood 1996, 87:2615-2620.
6. Chiorazzi N., Efremov D.G. Chronic lymphocytic leukemia: a tale of one or two signals?. Cell Res. 2013, 23:182-185.
7. Decker T., Schneller F., Sparwasser T., Tretter T., Lipford G.B., Wagner H., Peschel C. Immunostimulatory CpG-oligonucleotides cause proliferation, cytokine production, and an immunogenic phenotype in chronic lymphocytic leukemia B cells. Blood 2000, 95:999-1006.
8. Dorfman D.M., Hwang E.S., Shahsafaei A., Glimcher L.H. T-bet, a T-cell-associated transcription factor, is expressed in a subset of B-cell lymphoproliferative disorders. Am. J. Clin. Pathol. 2004, 122:292-297.
9. Dühren-von Minden M., Übelhart R., Schneider D., Wossning T., Bach M.P., Buchner M., Hofmann D., Surova E., Follo M., Köhler F., et al. Chronic lymphocytic leukaemia is driven by antigen-independent cell-autonomous signalling. Nature 2012, 489:309-312.
10. Faris M., Gaskin F., Parsons J.T., Fu S.M. CD40 signaling pathway: anti-CD40 monoclonal antibody induces rapid dephosphorylation and phosphorylation of tyrosine-phosphorylated proteins including protein tyrosine kinase Lyn, Fyn, and Syk and the appearance of a 28-kD tyrosine phosphorylated protein. J.Exp. Med. 1994, 179:1923-1931.
11. Fu S.M., Chiorazzi N., Kunkel H.G. Differentiation capacity and other properties of the leukemic cells of chronic lymphocytic leukemia. Immunol. Rev. 1979, 48:23-44.
12. Fulcher D.A., Lyons A.B., Korn S.L., Cook M.C., Koleda C., Parish C., Fazekas de St Groth B., Basten A. The fate of self-reactive B cells depends primarily on the degree of antigen receptor engagement and availability of Tcell help. J.Exp. Med. 1996, 183:2313-2328.
13. Ghia P., Strola G., Granziero L., Geuna M., Guida G., Sallusto F., Ruffing N., Montagna L., Piccoli P., Chilosi M., Caligaris-Cappio F. Chronic lymphocytic leukemia B cells are endowed with the capacity to attract CD4+, CD40L+ Tcells by producing CCL22. Eur. J. Immunol. 2002, 32:1403-1413.
14. Gitelson E., Hammond C., Mena J., Lorenzo M., Buckstein R., Berinstein N.L., Imrie K., Spaner D.E. Chronic lymphocytic leukemia-reactive Tcells during disease progression and after autologous tumor cell vaccines. Clin. Cancer Res. 2003, 9:1656-1665.
15. Goodnow C.C., Crosbie J., Adelstein S., Lavoie T.B., Smith-Gill S.J., Brink R.A., Pritchard-Briscoe H., Wotherspoon J.S., Loblay R.H., Raphael K., et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 1988, 334:676-682.
16. Görgün G., Holderried T.A., Zahrieh D., Neuberg D., Gribben J.G. Chronic lymphocytic leukemia cells induce changes in gene expression of CD4 and CD8 Tcells. J.Clin. Invest. 2005, 115:1797-1805.
17. Grewal I.S., Flavell R.A. CD40 and CD154 in cell-mediated immunity. Annu. Rev. Immunol. 1998, 16:111-135.
18. Gutierrez A., Arendt B.K., Tschumper R.C., Kay N.E., Zent C.S., Jelinek D.F. Differentiation of chronic lymphocytic leukemia B cells into immunoglobulin secreting cells decreases LEF-1 expression. PLoS ONE 2011, 6:e26056.
19. Hall A.M., Vickers M.A., McLeod E., Barker R.N. Rh autoantigen presentation to helper Tcells in chronic lymphocytic leukemia by malignant B cells. Blood 2005, 105:2007-2015.
20. Halper J.P., Fu S.M., Gottlieb A.B., Winchester R.J., Kunkel H.G. Poor mixed lymphocyte reaction stimulatory capacity of leukemic B cells of chronic lymphocytic leukemia patients despite the presence of Ia antigens. J.Clin. Invest. 1979, 64:1141-1148.
21. Herishanu Y., Pérez-Galán P., Liu D., Biancotto A., Pittaluga S., Vire B., Gibellini F., Njuguna N., Lee E., Stennett L., et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood 2011, 117:563-574.
22. Hoogeboom R., van Kessel K.P., Hochstenbach F., Wormhoudt T.A., Reinten R.J., Wagner K., Kater A.P., Guikema J.E., Bende R.J., van Noesel C.J. A mutated B cell chronic lymphocytic leukemia subset that recognizes and responds to fungi. J.Exp. Med. 2013, 210:59-70.
23. Kokhaei P., Palma M., Hansson L., Osterborg A., Mellstedt H., Choudhury A. Telomerase (hTERT 611-626) serves as a tumor antigen in B-cell chronic lymphocytic leukemia and generates spontaneously antileukemic, cytotoxic Tcells. Exp. Hematol. 2007, 35:297-304.
24. Muzio M., Apollonio B., Scielzo C., Frenquelli M., Vandoni I., Boussiotis V., Caligaris-Cappio F., Ghia P. Constitutive activation of distinct BCR-signaling pathways in a subset of CLL patients: a molecular signature of anergy. Blood 2008, 112:188-195.
25. Patten P., Devereux S., Buggins A., Bonyhadi M., Frohlich M., Berenson R.J. Effect of CD3/CD28 bead-activated and expanded Tcells on leukemic B cells in chronic lymphocytic leukemia. J.Immunol. 2005, 174:6562-6563. author reply 6563.
26. Patten P.E., Buggins A.G., Richards J., Wotherspoon A., Salisbury J., Mufti G.J., Hamblin T.J., Devereux S. CD38 expression in chronic lymphocytic leukemia is regulated by the tumor microenvironment. Blood 2008, 111:5173-5181.
27. Pizzolo G., Chilosi M., Ambrosetti A., Semenzato G., Fiore-Donati L., Perona G. Immunohistologic study of bone marrow involvement in B-chronic lymphocytic leukemia. Blood 1983, 62:1289-1296.
28. Ramaswamy S., Tamayo P., Rifkin R., Mukherjee S., Yeang C.H., Angelo M., Ladd C., Reich M., Latulippe E., Mesirov J.P., et al. Multiclass cancer diagnosis using tumor gene expression signatures. Proc. Natl. Acad. Sci. USA 2001, 98:15149-15154.
29. Ranheim E.A., Kipps T.J. Activated Tcells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal. J.Exp. Med. 1993, 177:925-935.
30. Ren C.L., Morio T., Fu S.M., Geha R.S. Signal transduction via CD40 involves activation of lyn kinase and phosphatidylinositol-3-kinase, and phosphorylation of phospholipase C gamma 2. J.Exp. Med. 1994, 179:673-680.
31. Rezvany M.R., Jeddi-Tehrani M., Rabbani H., Rudén U., Hammarström L., Osterborg A., Wigzell H., Mellstedt H. Autologous T lymphocytes recognize the tumour-derived immunoglobulin VH-CDR3 region in patients with B-cell chronic lymphocytic leukaemia. Br. J. Haematol. 2000, 111:230-238.
32. Riches J.C., Davies J.K., McClanahan F., Fatah R., Iqbal S., Agrawal S., Ramsay A.G., Gribben J.G. T cells from CLL patients exhibit features of T-cell exhaustion but retain capacity for cytokine production. Blood 2013, 121:1612-1621.
33. Robèrt K.H. Induction of monoclonal antibody synthesis in malignant human B cells by polyclonal B cell activators. Relationship between B cell subsets and prognosis. Immunol. Rev. 1979, 48:123-143.
34. Schjetne K.W., Thompson K.M., Aarvak T., Fleckenstein B., Sollid L.M., Bogen B. A mouse C kappa-specific Tcell clone indicates that DC-SIGN is an efficient target for antibody-mediated delivery of Tcell epitopes for MHC class II presentation. Int. Immunol. 2002, 14:1423-1430.
35. Stevenson F.K., Krysov S., Davies A.J., Steele A.J., Packham G. B-cell receptor signaling in chronic lymphocytic leukemia. Blood 2011, 118:4313-4320.
36. Tibaldi E., Brunati A.M., Zonta F., Frezzato F., Gattazzo C., Zambello R., Gringeri E., Semenzato G., Pagano M.A., Trentin L. Lyn-mediated SHP-1 recruitment to CD5 contributes to resistance to apoptosis of B-cell chronic lymphocytic leukemia cells. Leukemia 2011, 25:1768-1781.
37. Tretter T., Schuler M., Schneller F., Brass U., Esswein M., Aman M.J., Huber C., Peschel C. Direct cellular interaction with activated CD4(+) Tcells overcomes hyporesponsiveness of B-cell chronic lymphocytic leukemia invitro. Cell. Immunol. 1998, 189:41-50.
38. Trojan A., Schultze J.L., Witzens M., Vonderheide R.H., Ladetto M., Donovan J.W., Gribben J.G. Immunoglobulin framework-derived peptides function as cytotoxic T-cell epitopes commonly expressed in B-cell malignancies. Nat. Med. 2000, 6:667-672.
39. Weiss S., Bogen B. MHC class II-restricted presentation of intracellular antigen. Cell 1991, 64:767-776.
40. Yarkoni Y., Getahun A., Cambier J.C. Molecular underpinning of B-cell anergy. Immunol. Rev. 2010, 237:249-263.
41. Yasukawa M., Shiroguchi T., Inatsuki A., Kobayashi Y. Antigen presentation in an HLA-DR-restricted fashion by B-cell chronic lymphocytic leukemia cells. Blood 1988, 72:102-108.
42. Ying H., Li Z., Yang L., Zhang J. Syk mediates BCR- and CD40-signaling integration during B cell activation. Immunobiology 2011, 216:566-570.
43. Zangani M.M., Frøyland M., Qiu G.Y., Meza-Zepeda L.A., Kutok J.L., Thompson K.M., Munthe L.A., Bogen B. Lymphomas can develop from B cells chronically helped by idiotype-specific Tcells. J.Exp. Med. 2007, 204:1181-1191.
44. Zikherman J., Parameswaran R., Weiss A. Endogenous antigen tunes the responsiveness of naive B cells but not Tcells. Nature 2012, 489:160-164.