6,475
Views
35
CrossRef citations to date
0
Altmetric
Reviews

The significance of FOXP1 in diffuse large B-cell lymphoma

&
Pages 1037-1051 | Received 17 Jul 2016, Accepted 21 Aug 2016, Published online: 27 Sep 2016

References

  • Li C, Tucker PW. DNA-binding properties and secondary structural model of the hepatocyte nuclear factor 3/fork head domain. Proc Natl Acad Sci USA. 1993;90:11583–11587.
  • Banham AH, Beasley N, Campo E, et al. The FOXP1 winged helix transcription factor is a novel candidate tumor suppressor gene on chromosome 3p. Cancer Res. 2001;61:8820–8829.
  • Wang B, Lin D, Li C, et al. Multiple domains define the expression and regulatory properties of Foxp1 forkhead transcriptional repressors. J Biol Chem. 2003;278:24259–24268.
  • Sin C, Li H, Crawford DA. Transcriptional regulation by FOXP1, FOXP2, and FOXP4 dimerization. J Mol Neurosci. 2015;55:437–448.
  • Koon HB, Ippolito GC, Banham AH, et al. FOXP1: a potential therapeutic target in cancer. Expert Opin Ther Targets. 2007;11:955–965.
  • Campo E, Swerdlow SH, Harris NL, et al. The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood. 2011;117:5019–5032.
  • Coiffier B, Pfreundschuh M, Stahel R, et al. Aggressive lymphoma: improving treatment outcome with rituximab. Anticancer Drugs. 2002;13:S43–S50.
  • Sehn LH, Gascoyne RD. Diffuse large B-cell lymphoma: optimizing outcome in the context of clinical and biologic heterogeneity. Blood. 2015;125:22–32.
  • Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403:503–511.
  • Rosenwald A, Wright G, Chan WC, et al. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med. 2002;346:1937–1947.
  • Shaffer AL, Rosenwald A, Staudt LM. Lymphoid malignancies: the dark side of B-cell differentiation. Nat Rev Immunol. 2002;2:920–932.
  • Davis RE, Brown KD, Siebenlist U, et al. Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med. 2001;194:1861–1874.
  • Shipp MA, Ross KN, Tamayo P, et al. Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat Med. 2002;8:68–74.
  • Davis RE, Ngo VN, Lenz G, et al. Chronic active B-cell-receptor signaling in diffuse large B-cell lymphoma. Nature. 2010;463:88–92.
  • Young RM, Shaffer AL, III, Phelan JD, et al. B-cell receptor signaling in diffuse large B-cell lymphoma. Semin Hematol. 2015;52:77–85.
  • Pasqualucci L, Compagno M, Houldsworth J, et al. Inactivation of the PRDM1/BLIMP1 gene in diffuse large B cell lymphoma. J Exp Med. 2006;203:311–317.
  • Jones M, Gerring D, Ott G, et al. The differential expression of proteins in diffuse large B cell lymphoma. Blood. 2001;98:332a.
  • Banham A, Brown P, Baldry C, et al. Expression of the FOXP1 transcription factor is stronger in activated B-like diffuse large B cell lymphomas. J Clin Pathol. 2002;55:28.
  • Wright G, Tan B, Rosenwald A, et al. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc Natl Acad Sci USA. 2003;100:9991–9996.
  • Blenk S, Engelmann J, Weniger M, et al. Germinal center B cell-like (GCB) and activated B cell-like (ABC) type of diffuse large B cell lymphoma (DLBCL): analysis of molecular predictors, signatures, cell cycle state and patient survival. Cancer Inform. 2007;3:399–420.
  • Jais JP, Haioun C, Molina TJ, et al. The expression of 16 genes related to the cell of origin and immune response predicts survival in elderly patients with diffuse large B-cell lymphoma treated with CHOP and rituximab. Leukemia. 2008;22:1917–1924.
  • Hans CP, Weisenburger DD, Greiner TC, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103:275–282.
  • Copie-Bergman C, Gaulard P, Leroy K, et al. Immuno-fluorescence in situ hybridization index predicts survival in patients with diffuse large B-cell lymphoma treated with R-CHOP: a GELA study. J Clin Oncol. 2009;27:5573–5579.
  • He M, Gao L, Zhang S, et al. Prognostic significance of miR-34a and its target proteins of FOXP1, p53, and BCL2 in gastric MALT lymphoma and DLBCL. Gastric Cancer. 2014;17:431–441.
  • Meyer PN, Fu K, Greiner TC, et al. Immunohistochemical methods for predicting cell of origin and survival in patients with diffuse large B-cell lymphoma treated with rituximab. J Clin Oncol. 2011;29:200–207.
  • Nyman H, Jerkeman M, Karjalainen-Lindsberg ML, et al. Bcl-2 but not FOXP1, is an adverse risk factor in immunochemotherapy-treated non-germinal center diffuse large B-cell lymphomas. Eur J Haematol. 2009;82:364–372.
  • Visco C, Li Y, Xu-Monette ZY, et al. Comprehensive gene expression profiling and immunohistochemical studies support application of immunophenotypic algorithm for molecular subtype classification in diffuse large B-cell lymphoma: a report from the International DLBCL Rituximab-CHOP Consortium Program Study. Leukemia. 2012;26:2103–2113.
  • Wong KK, Gascoyne DM, Brown PJ, et al. Reciprocal expression of the endocytic protein HIP1R and its repressor FOXP1 predicts outcome in R-CHOP-treated diffuse large B-cell lymphoma patients. Leukemia. 2014;28:362–372.
  • Choi WW, Weisenburger DD, Greiner TC, et al. A new immunostain algorithm classifies diffuse large B-cell lymphoma into molecular subtypes with high accuracy. Clin Cancer Res. 2009;15:5494–5502.
  • Brown P,J, Banham AH, Connors JM. Expression of the FOXP1 transcription factor is strongly associated with inferior survival in patients with diffuse large B-cell lymphoma. Blood. 2003;102:102a.
  • Banham AH, Connors JM, Brown PJ, et al. Expression of the FOXP1 transcription factor is strongly associated with inferior survival in patients with diffuse large B-cell lymphoma. Clin Cancer Res. 2005;11:1065–1072.
  • Barrans SL, Fenton JA, Banham A, et al. Strong expression of FOXP1 identifies a distinct subset of diffuse large B-cell lymphoma (DLBCL) patients with poor outcome. Blood. 2004;104:2933–2935.
  • Hans CP, Weisenburger DD, Greiner TC, et al. Expression of PKC-beta or cyclin D2 predicts for inferior survival in diffuse large B-cell lymphoma. Mod Pathol. 2005;18:1377–1384.
  • Rubenstein JL, Fridlyand J, Abrey L, et al. Phase I study of intraventricular administration of rituximab in patients with recurrent CNS and intraocular lymphoma. J Clin Oncol. 2007;25:1350–1356.
  • Nyman H, Jerkeman M, Karjalainen-Lindsberg ML, et al. Prognostic impact of activated B-cell focused classification in diffuse large B-cell lymphoma patients treated with R-CHOP. Mod Pathol. 2009;22:1094–1101.
  • Thieblemont C, Briere J, Mounier N, et al. The germinal center/activated B-cell subclassification has a prognostic impact for response to salvage therapy in relapsed/refractory diffuse large B-cell lymphoma: a bio-CORAL study. J Clin Oncol. 2011;29:4079–4087.
  • de Jong D, Rosenwald A, Chhanabhai M, et al. Immunohistochemical prognostic markers in diffuse large B-cell lymphoma: validation of tissue microarray as a prerequisite for broad clinical applications–a study from the Lunenburg Lymphoma Biomarker Consortium. J Clin Oncol. 2007;25:805–812.
  • Coutinho R, Clear AJ, Owen A, et al. Poor concordance among nine immunohistochemistry classifiers of cell-of-origin for diffuse large B-cell lymphoma: implications for therapeutic strategies. Clin Cancer Res. 2013;19:6686–6695.
  • Lawrie CH, Ballabio E, Soilleux E, et al. Inter- and intra-observational variability in immunohistochemistry: a multicentre analysis of diffuse large B-cell lymphoma staining. Histopathology. 2012;61:18–25.
  • Hoeller S, Schneider A, Haralambieva E, et al. FOXP1 protein overexpression is associated with inferior outcome in nodal diffuse large B-cell lymphomas with non-germinal center phenotype, independent of gains and structural aberrations at 3p14.1. Histopathology. 2010;57:73–80.
  • Bellas C, Garcia D, Vicente Y, et al. Immunohistochemical and molecular characteristics with prognostic significance in diffuse large B-cell lymphoma. PLoS One. 2014;9:e98169.
  • Tzankov A, Leu N, Muenst S, et al. Multiparameter analysis of homogeneously R-CHOP-treated diffuse large B cell lymphomas identifies CD5 and FOXP1 as relevant prognostic biomarkers: report of the prospective SAKK 38/07 study. J Hematol Oncol. 2015;8:70.
  • Dekker JD, Park D, Shaffer AL. 3rd, et al. Subtype-specific addiction of the activated B-cell subset of diffuse large B-cell lymphoma to FOXP1. Proc Natl Acad Sci USA. 2016;113:E577–E586.
  • Craig VJ, Cogliatti SB, Imig J, et al. Myc-mediated repression of microRNA-34a promotes high-grade transformation of B-cell lymphoma by dysregulation of FoxP1. Blood. 2011;117:6227–6236.
  • Dunleavy K. Aggressive B cell lymphoma: optimal therapy for MYC-positive, double-hit, and triple-hit DLBCL. Curr Treat Options Oncol. 2015;16:58.
  • Wang W, Hu S, Lu X, et al. Triple-hit B-cell lymphoma with MYC, BCL2, and BCL6 translocations/rearrangements: clinicopathologic features of 11 cases. Am J Surg Pathol. 2015;39:1132–1139.
  • Streubel B, Vinatzer U, Lamprecht A, et al. T(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma. Leukemia. 2005;19:652–658.
  • Sagaert X, de Paepe P, Libbrecht L, et al. Forkhead box protein P1 expression in mucosa-associated lymphoid tissue lymphomas predicts poor prognosis and transformation to diffuse large B-cell lymphoma. J Clin Oncol. 2006;24:2490–2497.
  • Wlodarska I, Veyt E, De Paepe P, et al. FOXP1, a gene highly expressed in a subset of diffuse large B-cell lymphoma, is recurrently targeted by genomic aberrations. Leukemia. 2005;19:1299–1305.
  • Fenton JA, Schuuring E, Barrans SL, et al. t(3;14)(p14;q32) results in aberrant expression of FOXP1 in a case of diffuse large B-cell lymphoma. Gene Chromosome Canc. 2006;45:164–168.
  • Haralambieva E, Adam P, Ventura R, et al. Genetic rearrangement of FOXP1 is predominantly detected in a subset of diffuse large B-cell lymphomas with extranodal presentation. Leukemia. 2006;20:1300–1303.
  • Barrans SL, Fenton JA, Ventura R, et al. Deregulated over expression of FOXP1 protein in diffuse large B-cell lymphoma does not occur as a result of gene rearrangement. Haematologica. 2007;92:863–864.
  • Bea S, Zettl A, Wright G, et al. Diffuse large B-cell lymphoma subgroups have distinct genetic profiles that influence tumor biology and improve gene-expression-based survival prediction. Blood. 2005;106:3183–3190.
  • Lenz G, Wright GW, Emre NC, et al. Molecular subtypes of diffuse large B-cell lymphoma arise by distinct genetic pathways. Proc Natl Acad Sci USA. 2008;105:13520–13525.
  • Fox SB, Brown P, Han C, et al. Expression of the forkhead transcription factor FOXP1 is associated with estrogen receptor alpha and improved survival in primary human breast carcinomas. Clin Cancer Res. 2004;10:3521–3527.
  • Brown PJ, Ashe SL, Leich E, et al. Potentially oncogenic B-cell activation-induced smaller isoforms of FOXP1 are highly expressed in the activated B cell-like subtype of DLBCL. Blood. 2008;111:2816–2824.
  • Pajer P, Pecenka V, Kralova J, et al. Identification of potential human oncogenes by mapping the common viral integration sites in avian nephroblastoma. Cancer Res. 2006;66:78–86.
  • Brown PJ, Gascoyne DM, Lyne L, et al. N-terminally truncated FOXP1 protein expression and alternate internal FOXP1 promoter usage in normal and malignant B cells. Haematologica. 2016;101:861–871.
  • Goatly A, Bacon CM, Nakamura S, et al. FOXP1 abnormalities in lymphoma: translocation breakpoint mapping reveals insights into deregulated transcriptional control. Mod Pathol. 2008;21:902–911.
  • Rouhigharabaei L, Finalet Ferreiro J, Tousseyn T, et al. Non-IG aberrations of FOXP1 in B-cell malignancies lead to an aberrant expression of N-truncated isoforms of FOXP1. PLoS One. 2014;9:e85851.
  • Mullighan CG, Goorha S, Radtke I, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukemia. Nature. 2007;446:758–764.
  • Ernst T, Score J, Deininger M, et al. Identification of FOXP1 and SNX2 as novel ABL1 fusion partners in acute lymphoblastic leukemia. Br J Haematol. 2011;153:43–46.
  • Sugimoto Y, Sada A, Shimokariya Y, et al. A novel FOXP1-PDGFRA fusion gene in myeloproliferative neoplasm with eosinophilia. Cancer Genet. 2015;208:508–512.
  • Twa DD, Mottok A, Chan FC, et al. Recurrent genomic rearrangements in primary testicular lymphoma. J Pathol. 2015;236:136–141.
  • Green MR, Gandhi MK, Courtney MJ, et al. Relative abundance of full-length and truncated FOXP1 isoforms is associated with differential NFkappaB activity in follicular lymphoma. Leuk Res. 2009;33:1699–1702.
  • Banham AH, Boddy J, Launchbury R, et al. Expression of the forkhead transcription factor FOXP1 is associated both with hypoxia inducible factors (HIFs) and the androgen receptor in prostate cancer but is not directly regulated by androgens or hypoxia. Prostate. 2007;67:1091–1098.
  • Bates GJ, Fox SB, Han C, et al. Expression of the forkhead transcription factor FOXP1 is associated with that of estrogen receptor-beta in primary invasive breast carcinomas. Breast Cancer Res Treat. 2008;111:453–459.
  • Wong KK, Ch'ng ES, Loo SK, et al. Low HIP1R mRNA and protein expression are associated with worse survival in diffuse large B-cell lymphoma patients treated with R-CHOP. Exp Mol Pathol. 2015;99:537–545.
  • Tan LP, Wang M, Robertus JL, et al. miRNA profiling of B-cell subsets: specific miRNA profile for germinal center B cells with variation between centroblasts and centrocytes. Lab Invest. 2009;89:708–716.
  • Mraz M, Chen L, Rassenti LZ, et al. miR-150 influences B-cell receptor signaling in chronic lymphocytic leukemia by regulating expression of GAB1 and FOXP1. Blood. 2014;124:84–95.
  • Caramuta S, Lee L, Ozata DM, et al. Role of microRNAs and microRNA machinery in the pathogenesis of diffuse large B-cell lymphoma. Blood Cancer J. 2013;3:e152.
  • Hu H, Wang B, Borde M, et al. Foxp1 is an essential transcriptional regulator of B cell development. Nat Immunol. 2006;7:819–826.
  • Rao DS, O'Connell RM, Chaudhuri AA, et al. MicroRNA-34a perturbs B lymphocyte development by repressing the forkhead box transcription factor Foxp1. Immunity. 2010;33:48–59.
  • Sun GX, Cao XS, Li Q, et al. [Significance of miR-155, miR-34a and miR-30a expression in diffuse large B-cell lymphoma]. Zhonghua Yi Xue Yi Chuan Xue Za Zhi. 2013;30:79–83.
  • Fang C, Zhu DX, Dong HJ, et al. Serum microRNAs are promising novel biomarkers for diffuse large B cell lymphoma. Ann Hematol. 2012;91:553–559.
  • Alencar AJ, Malumbres R, Kozloski GA, et al. MicroRNAs are independent predictors of outcome in diffuse large B-cell lymphoma patients treated with R-CHOP. Clin Cancer Res. 2011;17:4125–4135.
  • Sagardoy A, Martinez-Ferrandis JI, Roa S, et al. Downregulation of FOXP1 is required during germinal center B-cell function. Blood. 2013;121:4311–4320.
  • van Keimpema M, Gruneberg LJ, Mokry M, et al. FOXP1 directly represses transcription of proapoptotic genes and cooperates with NF-kappaB to promote survival of human B cells. Blood. 2014;124:3431–3440.
  • Walker MP, Stopford CM, Cederlund M, et al. FOXP1 potentiates Wnt/beta-catenin signaling in diffuse large B cell lymphoma. Sci Signal. 2015;8:ra12.
  • Brown PJ, Campbell AJ, Lyne L, et al. Expression of the FOXP1 transcription factor is post-transcriptionally silenced in normal and malignant CD138+ plasma cells. TO Leukemia J. 2009;2:32–39.
  • Hunter ZR, Xu L, Yang G, et al. The genomic landscape of Waldenstrom macroglobulinemia is characterized by highly recurring MYD88 and WHIM-like CXCR4 mutations, and small somatic deletions associated with B-cell lymphomagenesis. Blood. 2014;123:1637–1646.
  • van Keimpema M, Gruneberg LJ, Mokry M, et al. The forkhead transcription factor FOXP1 represses human plasma cell differentiation. Blood. 2015;126:2098–2109.
  • Tsai DY, Hung KH, Lin IY, et al. Uncovering microRNA regulatory hubs that modulate plasma cell differentiation. Sci Rep. 2015;5:17957.
  • Wilkinson ST, Vanpatten KA, Fernandez DR, et al. Partial plasma cell differentiation as a mechanism of lost major histocompatibility complex class II expression in diffuse large B-cell lymphoma. Blood. 2012;119:1459–1467.
  • Brown PJ, Wong KK, Felce SL, et al. FOXP1 suppresses immune response signatures and MHC class II expression in activated B-cell-like diffuse large B-cell lymphomas. Leukemia. 2016;30:605–616.
  • Flori M, Schmid CA, Sumrall ET, et al. The hematopoietic oncoprotein FOXP1 promotes tumor cell survival in diffuse large B-cell lymphoma by repressing S1PR2 signaling. Blood. 2016;127:1438–1448.
  • Muppidi JR, Schmitz R, Green JA, et al. Loss of signaling via Galpha13 in germinal center B-cell-derived lymphoma. Nature. 2014;516:254–258.
  • Wong KK, Gascoyne DM, Soilleux EJ, et al. FOXP2-positive diffuse large B-cell lymphomas exhibit a poor response to R-CHOP therapy and distinct biological signatures. Oncotarget. 2016. [Epub ahead of print]. doi: 10.18632/oncotarget.9507.
  • Ackermann S, Kocak H, Hero B, et al. FOXP1 inhibits cell growth and attenuates tumorigenicity of neuroblastoma. BMC Cancer. 2014;14:840.
  • Takayama K, Suzuki T, Tsutsumi S, et al. Integrative analysis of FOXP1 function reveals a tumor-suppressive effect in prostate cancer. Mol Endocrinol. 2014;28:2012–2024.
  • Choi EJ, Seo EJ, Kim DK, et al. FOXP1 functions as an oncogene in promoting cancer stem cell-like characteristics in ovarian cancer cells. Oncotarget. 2016;7:3506–3519.
  • van Boxtel R, Gomez-Puerto C, Mokry M, et al. FOXP1 acts through a negative feedback loop to suppress FOXO-induced apoptosis. Cell Death Differ. 2013;20:1219–1229.
  • Bacon CM, Du MQ, Dogan A. Mucosa-associated lymphoid tissue (MALT) lymphoma: a practical guide for pathologists. J Clin Pathol. 2007;60:361–372.
  • Stephen TL, Rutkowski MR, Allegrezza MJ, et al. Transforming growth factor beta-mediated suppression of antitumor T cells requires FoxP1 transcription factor expression. Immunity. 2014;41:427–439.
  • Grundmann S, Lindmayer C, Hans FP, et al. FoxP1 stimulates angiogenesis by repressing the inhibitory guidance protein semaphorin 5B in endothelial cells. PLoS One. 2013;8:e70873.
  • Kodama K, Massone C, Chott A, et al. Primary cutaneous large B-cell lymphomas: clinicopathologic features, classification, and prognostic factors in a large series of patients. Blood. 2005;106:2491–2497.
  • Adams H, Tzankov A, Lugli A, et al. New time-dependent approach to analyze the prognostic significance of immunohistochemical biomarkers in colon cancer and diffuse large B-cell lymphoma. J Clin Pathol. 2009;62:986–997.
  • Cheng J, Tu P, Shi QL, et al. [Primary diffuse large B-cell lymphoma of central nervous system belongs to activated B-cell-like subgroup: a study of 47 cases]. Zhonghua Bing Li Xue Za Zhi. 2008;37:384–389.
  • Chadburn A, Chiu A, Lee JY, et al. Immunophenotypic analysis of AIDS-related diffuse large B-cell lymphoma and clinical implications in patients from AIDS Malignancies Consortium clinical trials 010 and 034. J Clin Oncol. 2009;27:5039–5048.
  • Yu B, Zhou X, Li B, et al. FOXP1 expression and its clinicopathologic significance in nodal and extranodal diffuse large B-cell lymphoma. Ann Hematol. 2011;90:701–708.
  • Hu CR, Wang JH, Wang R, et al. Both FOXP1 and p65 expression are adverse risk factors in diffuse large B-cell lymphoma: a retrospective study in China. Acta Histochem. 2013;115:137–143.
  • Shen L, Chen BB, Chen Z, et al. [Expression of FOXP1 and cyclinE in primary central nervous system lymphoma and its significance]. Zhonghua Xue Ye Xue Za Zhi. 2012;33:648–652.
  • Chen BB, Xu XP, Shen L, et al. Prognostic value of clinical characteristics and immunophenotypic biomarkers in 115 patients with primary central nervous system lymphoma. Chin Med J (Engl). 2013;126:482–487.
  • Culpin RE, Sieniawski M, Angus B, et al. Prognostic significance of immunohistochemistry-based markers and algorithms in immunochemotherapy-treated diffuse large B cell lymphoma patients. Histopathology. 2013;63:788–801.
  • Horn H, Ziepert M, Wartenberg M, et al. Different biological risk factors in young poor-prognosis and elderly patients with diffuse large B-cell lymphoma. Leukemia. 2015;29:1564–1570.
  • Deng L, Xu-Monette ZY, Loghavi S, et al. Primary testicular diffuse large B-cell lymphoma displays distinct clinical and biological features for treatment failure in rituximab era: a report from the International PTL Consortium. Leukemia. 2016;30:361–372.