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Selectively frequent expression of CXCR5 enhances resistance to apoptosis in CD8+CD34+ T cells from patients with T-cell-lineage acute lymphocytic leukemia

A Retraction to this article was published on 16 June 2011

Abstract

We investigated CD4+CD34+, CD8+CD34+, CD4+CD34, and CD8+CD34 T cells from cord blood and from typical patients with T-cell-lineage acute lymphocytic leukemia and T-cell-lineage chronic lymphocytic leukemia in terms of expression and functions of CXCR5/CXCL13. We found that CXCR5 was selectively frequently expressed on T-cell-lineage acute (chronic) lymphocytic leukemia (T-ALL) CD8+CD34+ T cells, but not on T-ALL CD4+CD34+, CD4+CD34, and CD8+CD34 T cells. CXCR5 was rarely expressed on all types of CD34+ and CD34 CB or T-CLL T cells. CXCL13/B cells attracting chemokine 1 induced significant resistance to TNF-α-mediated apoptosis in T-ALL CD8+CD34+ T cells, instead of induction of chemotactic and adhesive responsiveness. A proliferation-inducing ligand expression in T-ALL CD8+CD34+ T cells was upregulated by CXCL13/BCA-1 (B-cell attracting chemokine 1). The CXCR5/CXCL13 pair by means of activation of APRIL (A proliferation-inducing ligand) induced resistance to apoptosis in T-ALL CD8+CD34+ T cells in livin-dependent manner. In this process, cell–cell contact in culture was necessary. Based on our findings, we suggested that there were differential functions of CXCR5/CXCL13 in distinct types of cells. Normal lymphocytes, especially naïve B and T cells, utilized CXCR5/CXCL13 for migration, homing, maturation, and cell homeostasis, as well as secondary lymphoid tissue organogenesis. Meanwhile, certain malignant cells took advantages of CXCR5/CXCL13 for infiltration, resistance to apoptosis, and inappropriate proliferation.

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Abbreviations

APRIL:

A proliferation-inducing ligand

BCA-1:

B-cell attracting chemokine 1

BCMA:

B-cell maturation antigen

C.I.:

chemotactic index

CXCL (CC):

CXC (CC) chemokine ligand

CXCR (CC):

CXC (CC) chemokine receptor

T-ALL (T-CLL):

T-cell-lineage acute (chronic) lymphocytic leukemia

References

  • Algeciras-Schimnich A, Vlahakis SR, Villasis-Keever A, Gomez T, Heppelmann CJ, Bou G and Paya CV . (2002). AIDS, 16, 1467–1478.

  • Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R, Sedgwick JD, Browning JL, Lipp M and Cyster JG . (2000). Nature, 406, 309–314.

  • Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR and Sultan C . (1981). Br. J. Haematol., 47, 553–558.

  • Bennett JM, Catovsky D, Daniel M-T, Flandrin G, Galton DA, Gralnick HR and Sultan C . (1989). J. Clin. Pathol., 42, 567–584.

  • Berndt C, Mopps B, Angermuller S, Gierschik P and Krammer PH . (1998). Proc. Natl. Acad. Sci. USA, 95, 12556–12561.

  • Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F, Lipp M and Forster R . (2000). J. Exp. Med., 192, 1545–1552.

  • Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES, Shi Y and Dataa P . (2001). Cell, 104, 769–780.

  • Cheson BD, Bennett JM, Grever M, Kay N, Keating MJ, O'Brien S and Rai KR . (1996). Blood, 87, 4990–4997.

  • Duckett CS, Nava VE, Gedrich RW, Clem RJ, Van Dongen JL, Gilfillan MC, Shiels H, Hardwick JM and Thompson CB . (1996). EMBO J., 15, 2685–2694.

  • Finke D, Acha-Orbea H, Mattis A, Lipp M and Kraehenbuhl J . (2002). Immunity, 17, 363–373.

  • Förster R, Emrich T, Kremmer E and Lipp M . (1994). Blood, 84, 830–840.

  • Förster R, Mattis AE, Kremmer E, Wolf E, Brem G and Lipp M . (1996). Cell, 87, 1037–1047.

  • Gunn MD, Ngo VN, Ansel KM, Ekland EH, Cyster JG and Williams LT . (1998). Nature, 391, 799–803.

  • Hahne M, Kataoka T, Schroter M, Hofmann K, Irmler M, Bodmer JL, Schneider P, Bornand T, Holler N, French LE, Sordat B, Rimoldi D and Tschopp J . (1998). J. Exp. Med., 188, 1185–1190.

  • Han ZC, Lu M, Li J, Defard M, Boval B, Schlegel N and Caen JP . (1997). Blood, 89, 2328–2335.

  • Hargreaves DC, Hyman PL, Lu TT, Ngo VN, Bidgol A, Suzuki G, Zou YR, Littman DR and Cyster JG . (2001). J. Exp. Med., 194, 45–56.

  • Jinquan T, Jacobi HH, Jing C, Millner A, Sten E, Hviid L, Anting L, Ryder LP, Glue C, Skov PS, Jarman E, Lamberth K, Malling HJ and Poulsen LK . (2003). J. Immunol., 171, 1722–1731.

  • Jinquan T, Quan S, Jacobi HH, Jing C, Millner A, Jensen B, Madsen HO, Ryder LP, Svejgaard A, Malling HJ, Skov PS and Poulsen LK . (2000). Blood, 96, 1230–1238.

  • Jonuleit H, Schmitt E, Schuler G, Knop J and Enk AH . (2000). J. Exp. Med., 192, 1213–1222.

  • Kanbe K, Shimizu N, Soda Y, Takagishi K and Hoshino H . (1999). Virology, 265, 264–273.

  • Kasof GM and Gomes BC . (2001). J. Biol. Chem., 276, 3238–3246.

  • Kelly K, Manos E, Jensen G, Nadauld L and Jones DA . (2000). Cancer Res., 60, 1021–1027.

  • Kern C, Cornuel JF, Billard C, Tang R, Rouillard D, Stenou V, Defrance T, Ajchenbaum-Cymbalista F, Simonin PY, Feldblum S and Kolb JP . (2004). Blood, 103, 679–688.

  • Kim CH, Rott LS, Clark-Lewis I, Campbell DJ, Wu L and Butcher EC . (2001). J. Exp. Med., 193, 1373–1382.

  • Kruse N, Pette M, Toyka K and Rieckmann P . (1997). J. Immunol. Methods, 210, 195–203.

  • Lin JH, Deng G, Huang Q and Morser J . (2000). Biochem. Biophys. Res. Commun., 279, 820–831.

  • Lopez-Fraga M, Fernandez R, Albar JP and Hahne M . (2001). EMBO Rep., 2, 945–951.

  • Luther SA, Lopez T, Bai W, Hanahan D and Cyster JG . (2000). Immunity, 12, 471–481.

  • Massari P, Ho Y and Wetzler LM . (2000). Proc. Natl. Acad. Sci. USA, 97, 9070–9075.

  • Mazzucchelli L, Blaser A, Kappeler A, Scharli P, Laissue JA, Baggiolini M and Uguccioni M . (1999). J. Clin. Invest., 104, R49–R54.

  • Medema JP, Planelles-Carazo L, Hardenberg G and Hahne M . (2003). Cell Death Diff., 10, 1121–1125.

  • Miller LK . (1999). Trends Cell. Biol., 9, 323–328.

  • Muller G, Hopken UE and Lipp M . (2003). Immunol. Rev., 195, 117–135.

  • Ohl L, Henning G, Krautwald S, Lipp M, Hardtke S, Bernhardt G, Pabst O and Forster R . (2003). J. Exp. Med., 197, 1199–1204.

  • Okada T, Ngo VN, Ekland EH, Forster R, Lipp M, Littman DR and Cyster JG . (2002). J. Exp. Med., 196, 65–75.

  • Pradet-Balade B, Medema JP, Lopez-Fraga M, Lozano JC, Kolfschoten GM, Picard A, Martinez-A C, Garcia-Sanz JA and Hahne M . (2002). EMBO J., 21, 5711–5720.

  • Qiuping Z, Qun L, Chunsong H, Xiaolian Z, Baojun H, Mingzhen Y, Chengming L, Jinshen H, Qingping G, Kejian Z, Zhimin S, Xuejun Z, Junyan L and Jinquan T . (2003). Cancer Res., 63, 6469–6477.

  • Reif K, Ekland EH, Ohl L, Nakano H, Lipp M, Forster R and Cyster JG . (2002). Nature, 416, 94–99.

  • Rennert P, Schneider P, Cachero TG, Thompson J, Trabach L, Hertig S, Holler N, Qian F, Mullen C, Strauch K, Browning JL, Ambrose C and Tschopp J . (2000). J. Exp. Med., 192, 1677–1684.

  • Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, Liddington RC and Salvesen GS . (2001). Cell, 104, 791–800.

  • Roth W, Wagenknecht B, Klumpp A, Naumann U, Hahne M, Tschopp J and Weller M . (2001). Cell Death Differ., 8, 403–410.

  • Saeki H, Wu MT, Olasz E and Hwang ST . (2000). Eur. J. Immunol., 30, 2808–2814.

  • Sanna MG, da Silva Correia J, Ducrey O, Lee J, Nomoto K, Schrantz N, Deveraux QL and Ulevitch RJ . (2002). Mol. Cell. Biol., 22, 1754–1766.

  • Scheuerer B, Ernst M, Durrbaum-Landmann I, Fleischer J, Grage-Griebenow E, Brandt E, Flad HD and Petersen F . (2000). Blood, 95, 1158–1166.

  • Schmollinger JC, Vonderheide RH, Hoar KM, Maecker B, Schultze JL, Hodi FS, Soiffer RJ, Jung K, Kuroda MJ, Letvin NL, Greenfield EA, Mihm M, Kutok JL and Dranoff G . (2003). Proc. Natl. Acad. Sci. USA, 100, 3398–3403.

  • Sica A, Saccani A, Borsatti A, Power CA, Wells TN, Luini W, Polentarutti N, Sozzani S and Mantovani A . (1997). J. Exp. Med., 185, 969–974.

  • Siegel RM and Lenardo MJ . (2001). Nat. Immunol., 2, 577–578.

  • Smith JR, Braziel RM, Paoletti S, Lipp M, Uguccioni M and Rosenbaum JT . (2003). Blood, 101, 815–821.

  • Stein JV, Lopez-Fraga M, Elustondo FA, Carvalho-Pinto CE, Rodriguez D, Gomez-Caro R, De Jong J, Martinez-A C, Medema JP and Hahne M . (2002). J. Clin. Invest., 109, 1587–1598.

  • Thornberry NA and Lazebnik Y . (1998). Science, 281, 1312–1316.

  • Till KJ, Lin K, Zuzel M and Cawley JC . (2002). Blood, 99, 2977–2984.

  • Voigt I, Camacho SA, de Boer BA, Lipp M, Forster R and Berek C . (2000). Eur. J. Immunol., 30, 560–567.

  • Vucic D, Stennicke HR, Pisabarro MT, Salvesen GS and Dixit VM . (2000). Curr. Biol., 10, 1359–1366.

  • Wu MT and Hwang ST . (2002). J. Immunol., 168, 5096–5102.

  • Youn BS, Kim YJ, Mantel C, Yu KY and Broxmeyer HE . (2001). Blood, 98, 925–933.

  • Youn BS, Yu KY, Oh J, Lee J, Lee TH and Broxmeyer HE . (2002). Apoptosis, 7, 271–276.

  • Yu G, Boone T, Delaney J, Hawkins N, Kelley M, Ramakrishnan M, McCabe S, Qiu WR, Kornuc M, Xia XZ, Guo J, Stolina M, Boyle WJ, Sarosi I, Hsu H, Senaldi G and Theill LE . (2000). Nat. Immunol., 1, 252–256.

  • Yu P, Wang Y, Chin RK, Martinez-Pomares L, Gordon S, Kosco-Vibois M H, Cyster J and Fu YX . (2002). J. Immunol., 168, 5117–5123.

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Acknowledgements

This work was supported by the National Science Foundation of China (no. 39870674), Science Foundation of Anhui Province, China (no. 98436630), and Education and Research Foundation of Anhui Province, China (no. 98JL063), and Research Foundation from Health Department of Hubei Provincial Gvernment, China (no. 301140344).

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Correspondence to Tan Jinquan.

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Qiuping, Z., Jie, X., Youxin, J. et al. Selectively frequent expression of CXCR5 enhances resistance to apoptosis in CD8+CD34+ T cells from patients with T-cell-lineage acute lymphocytic leukemia. Oncogene 24, 573–584 (2005). https://doi.org/10.1038/sj.onc.1208184

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