3,618
Views
19
CrossRef citations to date
0
Altmetric
Research Article

Tumor cell-derived IL-10 promotes cell-autonomous growth and immune escape in diffuse large B-cell lymphoma

, , , , , , , , , ORCID Icon, & show all
Article: 2003533 | Received 07 Sep 2021, Accepted 03 Nov 2021, Published online: 22 Nov 2021

References

  • Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403(6769):503–13. doi:10.1038/35000501.
  • Chapuy B, Stewart C, Dunford AJ, Kim J, Kamburov A, Redd RA, Lawrence MS, Roemer MGM, Li AJ, Ziepert M, et al. Molecular subtypes of diffuse large B cell lymphoma are associated with distinct pathogenic mechanisms and outcomes. Nature Medicine. 2018;24(5):679–690. doi:10.1038/s41591-018-0016-8.
  • Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fisher RI, Gascoyne RD, Muller-Hermelink HK, Smeland EB, and Giltnane JM , et al. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. Lymphoma/Leukemia Molecular Profiling. The New England Journal of Medicine. 2002;346(25), 1937–1947. DOI: 10.1056/NEJMoa012914.
  • Schmitz R, Wright GW, Huang DW, Johnson CA, Phelan JD, Wang JQ, Roulland S, Kasbekar M, Young RM, Shaffer AL, et al. Genetics and Pathogenesis of Diffuse Large B-Cell Lymphoma. The New England Journal of Medicine. 2018;378(15):1396–1407. doi:10.1056/NEJMoa1801445.
  • Basso K, Dalla-Favera R. Germinal centres and B cell lymphomagenesis. Nature Reviews Immunology. 2015;15(3):172–184. doi:10.1038/nri3814.
  • Pasqualucci L, Dalla-Favera R. SnapShot: diffuse large B cell lymphoma. Cancer Cell. 2014;25(132–132):e131. doi:10.1016/j.ccr.2013.12.012.
  • Pasqualucci L, Dalla-Favera R. The genetic landscape of diffuse large B-cell lymphoma. Semin Hematol. 2015;52(2):67–76. doi:10.1053/j.seminhematol.2015.01.005.
  • Coiffier B, Thieblemont C, Van Den Neste E, Lepeu G, Plantier I, Castaigne S, Lefort S, Marit G, Macro M, Sebban C, et al. Long-term outcome of patients in the LNH-98.5 trial, the first randomized study comparing rituximab-CHOP to standard CHOP chemotherapy in DLBCL patients: a study by the Groupe d’Etudes des Lymphomes de l’Adulte. Blood. 2010;116(12):2040–2045. doi:10.1182/blood-2010-03-276246.
  • Crump M, Neelapu SS, Farooq U, Van Den Neste E, Kuruvilla J, Westin J, Link BK, Hay A, Cerhan JR, Zhu L, et al. Outcomes in refractory diffuse large B-cell lymphoma: results from the international SCHOLAR-1 study. Blood. 2017;130(16):1800–1808. doi:10.1182/blood-2017-03-769620.
  • Hashwah H, Bertram K, Stirm K, Stelling A, Wu CT, Kasser S, Manz MG, Theocharides AP, Tzankov A, Muller A. The IL −6 signaling complex is a critical driver, negative prognostic factor, and therapeutic target in diffuse large B-cell lymphoma. EMBO Molecular Medicine. 2019;11(10):e10576. doi:10.15252/emmm.201910576.
  • Meier C, Hoeller S, Bourgau C, Hirschmann P, Schwaller J, Went P, Pileri SA, Reiter A, Dirnhofer S, Tzankov A. Recurrent numerical aberrations of JAK2 and deregulation of the JAK2-STAT cascade in lymphomas. Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc. 2009;22(3):476–487. doi:10.1038/modpathol.2008.207.
  • Ok CY, Chen J, Xu-Monette ZY, Tzankov A, Manyam GC, Li L, Visco C, Montes-Moreno S, Dybkaer K, Chiu A, et al. Clinical Implications of Phosphorylated STAT3 Expression in De Novo Diffuse Large B-cell Lymphoma. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research. 2014;20(19):5113–5123. doi:10.1158/1078-0432.CCR-14-0683.
  • Tzankov A, Leu N, Muenst S, Juskevicius D, Klingbiel D, Mamot C, Dirnhofer S. 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. Journal of Hematology & Oncology. 2015;8(1):70. doi:10.1186/s13045-015-0168-7.
  • Buchert M, Burns CJ, Ernst M. Targeting JAK kinase in solid tumors: emerging opportunities and challenges. Oncogene. 2016;35(8):939–951. doi:10.1038/onc.2015.150.
  • Lu L, Zhu F, Zhang M, Li Y, Drennan AC, Kimpara S, Rumball I, Selzer C, Cameron H, and Kellicut A, et al. () Gene regulation and suppression of type I interferon signaling by STAT3 in diffuse large B cell lymphoma. Proceedings of the National Academy of Sciences of the United States of America. 2018;115: E498–E505
  • Gupta M, Han JJ, Stenson M, Maurer M, Wellik L, Hu G, Ziesmer S, Dogan A, Witzig TE. Elevated serum IL-10 levels in diffuse large B-cell lymphoma: a mechanism of aberrant JAK2 activation. Blood. 2012;119(12):2844–2853. doi:10.1182/blood-2011-10-388538.
  • Beguelin W, Sawh S, Chambwe N, Chan FC, Jiang Y, Choo JW, Scott DW, Chalmers A, Geng H, Tsikitas L, et al. IL10 receptor is a novel therapeutic target in DLBCLs. Leukemia. 2015;29(8):1684–1694. doi:10.1038/leu.2015.57.
  • Ngo VN, Young RM, Schmitz R, Jhavar S, Xiao W, Lim KH, Kohlhammer H, Xu W, Yang Y, Zhao H, et al. Oncogenically active MYD88 mutations in human lymphoma. Nature. 2011;470(7332):115–119. doi:10.1038/nature09671.
  • Phelan JD, Young RM, Webster DE, Roulland S, Wright GW, Kasbekar M, Shaffer AL 3rd, Ceribelli M, Wang JQ, Schmitz R, et al. A multiprotein supercomplex controlling oncogenic signalling in lymphoma. Nature. 2018;560(7718):387–391. doi:10.1038/s41586-018-0290-0.
  • Hashwah H, Schmid CA, Kasser S, Bertram K, Stelling A, Manz MG, and Muller A. () Inactivation of CREBBP expands the germinal center B cell compartment, down-regulates MHCII expression and promotes DLBCL growth. Proceedings of the National Academy of Sciences of the United States of America. 2017;114: 9701–9706
  • Stelling A, Hashwah H, Bertram K, Manz MG, Tzankov A, Muller A. The tumor suppressive TGF-beta/SMAD1/S1PR2 signaling axis is recurrently inactivated in diffuse large B-cell lymphoma. Blood. 2018;131(20):2235–2246. doi:10.1182/blood-2017-10-810630.
  • Das R, Strowig T, Verma R, Koduru S, Hafemann A, Hopf S, Kocoglu MH, Borsotti C, Zhang L, Branagan A, et al. Microenvironment-dependent growth of preneoplastic and malignant plasma cells in humanized mice. Nature Medicine. 2016;22(11):1351–1357. doi:10.1038/nm.4202.
  • Menter T, Ernst M, Drachneris J, Dirnhofer S, Barghorn A, Went P, Tzankov A. Phenotype profiling of primary testicular diffuse large B-cell lymphomas. Hematological Oncology. 2014;32(2):72–81. doi:10.1002/hon.2090.
  • Harris AW, Pinkert CA, Crawford M, Langdon WY, Brinster RL, Adams JM. The E mu-myc transgenic mouse. A model for high-incidence spontaneous lymphoma and leukemia of early B cells. The Journal of Experimental Medicine. 1988;167(2):353–371. doi:10.1084/jem.167.2.353.
  • Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103:275–282. doi:10.1182/blood-2003-05-1545.
  • Obermann EC, Csato M, Dirnhofer S, Tzankov A. Aberrations of the MYC gene in unselected cases of diffuse large B-cell lymphoma are rare and unpredictable by morphological or immunohistochemical assessment. Journal of Clinical Pathology. 2009;62(8):754–756. doi:10.1136/jcp.2009.065227.
  • Tzankov A, Heiss S, Ebner S, Sterlacci W, Schaefer G, Augustin F, Fiegl M, Dirnhofer S. Angiogenesis in nodal B cell lymphomas: a high throughput study. Journal of Clinical Pathology. 2007;60:476–482. doi:10.1136/jcp.2006.038661.
  • Juskevicius D, Jucker D, Klingbiel D, Mamot C, Dirnhofer S, Tzankov A. Mutations of CREBBP and SOCS1 are independent prognostic factors in diffuse large B cell lymphoma: mutational analysis of the SAKK 38/07 prospective clinical trial cohort. Journal of Hematology & Oncology. 2017;10(1):70. doi:10.1186/s13045-017-0438-7.
  • Carpenter RL, Lo HW. STAT3 Target Genes Relevant to Human Cancers. Cancers. 2014;6(2):897–925. doi:10.3390/cancers6020897.
  • Snyder M, Huang XY, Zhang JJ. Identification of novel direct Stat3 target genes for control of growth and differentiation. The Journal of Biological Chemistry. 2008;283(7):3791–3798. doi:10.1074/jbc.M706976200.
  • Ouyang W, O’Garra A. IL-10 Family Cytokines IL-10 and IL-22: from Basic Science to Clinical Translation. Immunity. 2019;50(4):871–891. doi:10.1016/j.immuni.2019.03.020.
  • Menter T, Dickenmann M, Juskevicius D, Steiger J, Dirnhofer S, Tzankov A. Comprehensive phenotypic characterization of PTLD reveals potential reliance on EBV or NF-kappaB signalling instead of B-cell receptor signalling. Hematological Oncology. 2017a;35(2):187–197. doi:10.1002/hon.2280.
  • Ding BB, Yu JJ, Yu RY, Mendez LM, Shaknovich R, Zhang Y, Cattoretti G, Ye BH. Constitutively activated STAT3 promotes cell proliferation and survival in the activated B-cell subtype of diffuse large B-cell lymphomas. Blood. 2008;111(3):1515–1523. doi:10.1182/blood-2007-04-087734.
  • Rongvaux A, Willinger T, Martinek J, Strowig T, Gearty SV, Teichmann LL, Saito Y, Marches F, Halene S, Palucka AK, et al. Development and function of human innate immune cells in a humanized mouse model. Nature Biotechnology. 2014;32(4):364–372. doi:10.1038/nbt.2858.
  • Chaudhry A, Samstein RM, Treuting P, Liang Y, Pils MC, Heinrich JM, Jack RS, Wunderlich FT, Bruning JC, Muller W, et al. Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity. 2011;34(4):566–578. doi:10.1016/j.immuni.2011.03.018.
  • Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H, Kronenberg M. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nature Immunology. 2009;10(11):1178–1184. doi:10.1038/ni.1791.
  • Naing A, Infante JR, Papadopoulos KP, Chan IH, Shen C, Ratti NP, Rojo B, Autio KA, Wong DJ, Patel MR, et al. PEGylated IL-10 (Pegilodecakin) Induces Systemic Immune Activation, CD8(+) T Cell Invigoration and Polyclonal T Cell Expansion in Cancer Patients. Cancer Cell. 2018;34(775–791):e773. doi:10.1016/j.ccell.2018.10.007.
  • Menter T, Juskevicius D, Alikian M, Steiger J, Dirnhofer S, Tzankov A, and Naresh KN. Mutational landscape of B-cell post-transplant lymphoproliferative disorders. British Journal of Haematology. 2017;178:48–56.