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Original Research

B cell lymphoma progression promotes the accumulation of circulating Ly6Clo monocytes with immunosuppressive activity

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Article: e1393599 | Received 15 Sep 2017, Accepted 13 Oct 2017, Published online: 18 Dec 2017

References

  • Sun HL, Pan YQ, He BS, Nie ZL, Lin K, Peng HX, Cho WC, Wang SK. Prognostic performance of lymphocyte-to-monocyte ratio in diffuse large B-cell lymphoma: an updated meta-analysis of eleven reports. Onco Targets Ther. 2016;9:3017–23. PMID:27284252.
  • Tadmor T, Bari A, Sacchi S, Marcheselli L, Liardo EV, Avivi I, Benyamini N, Attias D, Pozzi S, Cox MC, et al. Monocyte count at diagnosis is a prognostic parameter in diffuse large B-cell lymphoma: results from a large multicenter study involving 1191 patients in the pre- and post-rituximab era. Haematologica. 2014;99:125–30. doi:10.3324/haematol.2013.088161. PMID:23935023.
  • Li ZM, Huang JJ, Xia Y, Sun J, Huang Y, Wang Y, Zhu YJ, Li YJ, Zhao W, Wei WX, et al. Blood lymphocyte-to-monocyte ratio identifies high-risk patients in diffuse large B-cell lymphoma treated with R-CHOP. PLoS One. 2012;7:e41658. doi:10.1371/journal.pone.0041658. PMID:22911837.
  • Jaipersad AS, Lip GY, Silverman S, Shantsila E. The role of monocytes in angiogenesis and atherosclerosis. J Am Coll Cardiol. 2014;63:1–11. doi:10.1016/j.jacc.2013.09.019. PMID:24140662.
  • Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer. 2008;8:618–31. doi:10.1038/nrc2444. PMID:18633355.
  • Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA, Pollard JW. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475:222–5. doi:10.1038/nature10138. PMID:21654748.
  • Allaoui R, Bergenfelz C, Mohlin S, Hagerling C, Salari K, Werb Z, Anderson RL, Ethier SP, Jirström K, Påhlman S, et al. Cancer-associated fibroblast-secreted CXCL16 attracts monocytes to promote stroma activation in triple-negative breast cancers. Nat Commun. 2016;7:13050. doi:10.1038/ncomms13050. PMID:27725631.
  • Yin M, Li X, Tan S, Zhou HJ, Ji W, Bellone S, Xu X, Zhang H, Santin AD, Lou G, et al. Tumor-associated macrophages drive spheroid formation during early transcoelomic metastasis of ovarian cancer. J Clin Invest. 2016;126:4157–73. doi:10.1172/JCI87252. PMID:27721235.
  • Lin Y, Gustafson MP, Bulur PA, Gastineau DA, Witzig TE, Dietz AB. Immunosuppressive CD14+HLA-DR(low)/- monocytes in B-cell non-Hodgkin lymphoma. Blood. 2011;117:872–81. doi:10.1182/blood-2010-05-283820. PMID:21063024.
  • Xiu B, Lin Y, Grote DM, Ziesmer SC, Gustafson MP, Maas ML, Zhang Z, Dietz AB, Porrata LF, Novak AJ, et al. IL-10 induces the development of immunosuppressive CD14(+)HLA-DR(low/-) monocytes in B-cell non-Hodgkin lymphoma. Blood Cancer J. 2015;5:e328. doi:10.1038/bcj.2015.56. PMID:26230952.
  • Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 2007;317:666–70. doi:10.1126/science.1142883. PMID:17673663.
  • Ginhoux F, Jung S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 2014; 14:392–404. doi:10.1038/nri3671. PMID:24854589.
  • Feng AL, Zhu JK, Sun JT, Yang MX, Neckenig MR, Wang XW, Shao QQ, Song BF, Yang QF, Kong BH, et al. CD16+ monocytes in breast cancer patients: expanded by monocyte chemoattractant protein-1 and may be useful for early diagnosis. Clin Exp Immunol. 2011;164:57–65. doi:10.1111/j.1365-2249.2011.04321.x. PMID:21361908.
  • Sanford DE, Belt BA, Panni RZ, Mayer A, Deshpande AD, Carpenter D, Mitchem JB, Plambeck-Suess SM, Worley LA, Goetz BD, et al. Inflammatory monocyte mobilization decreases patient survival in pancreatic cancer: a role for targeting the CCL2/CCR2 axis. Clin Cancer Res. 2013;19:3404–15. doi:10.1158/1078-0432.CCR-13-0525. PMID:23653148.
  • Andersen MN, Abildgaard N, Maniecki MB, Moller HJ, Andersen NF. Monocyte/macrophage-derived soluble CD163: a novel biomarker in multiple myeloma. Eur J Haematol. 2014;93:41–7. doi:10.1111/ejh.12296. PMID:24612259.
  • Jones K, Vari F, Keane C, Crooks P, Nourse JP, Seymour LA, Gottlieb D, Ritchie D, Gill D, Gandhi MK. Serum CD163 and TARC as disease response biomarkers in classical Hodgkin lymphoma. Clinical cancer research : an official journal of the American Association for Cancer Research. 2013; 19:731–42. doi:10.1158/1078-0432.CCR-12-2693. PMID:23224400.
  • Fridlender ZG, Buchlis G, Kapoor V, Cheng G, Sun J, Singhal S, Crisanti MC, Wang LC, Heitjan D, Snyder LA, et al. CCL2 Blockade Augments Cancer Immunotherapy. Cancer Res. 2010;70:109–18. doi:10.1158/0008-5472.CAN-09-2326. PMID:20028856.
  • Hanna BS, McClanahan F, Yazdanparast H, Zaborsky N, Kalter V, Rossner PM, Benner A, Dürr C, Egle A, Gribben JG, et al. Depletion of CLL-associated patrolling monocytes and macrophages controls disease development and repairs immune dysfunction in vivo. Leukemia. 2016;30:570–9. doi:10.1038/leu.2015.305. PMID:26522085.
  • Hanna RN, Cekic C, Sag D, Tacke R, Thomas GD, Nowyhed H, Herrley E, Rasquinha N, McArdle S, Wu R. Patrolling monocytes control tumor metastasis to the lung. Science. 2015;350:985–90. doi:10.1126/science.aac9407. PMID:26494174.
  • Lapuc I, Bolkun L, Eljaszewicz A, Rusak M, Luksza E, Singh P, Miklasz P, Piszcz J, Ptaszynska-Kopczynska K, Jasiewicz M, et al. Circulating classical CD14++CD16- monocytes predict shorter time to initial treatment in chronic lymphocytic leukemia patients: Differential effects of immune chemotherapy on monocyte-related membrane and soluble forms of CD163. Oncol Rep. 2015;34:1269–78. doi:10.3892/or.2015.4088. PMID:26135617.
  • Weide B, Martens A, Zelba H, Stutz C, Derhovanessian E, Di Giacomo AM, Maio M, Sucker A, Schilling B, Schadendorf D, et al. Myeloid-derived suppressor cells predict survival of patients with advanced melanoma: comparison with regulatory T cells and NY-ESO-1- or melan-A-specific T cells. Clin Cancer Res 2014;20:1601–9. doi:10.1158/1078-0432.CCR-13-2508. PMID:24323899.
  • Gabitass RF, Annels NE, Stocken DD, Pandha HA, Middleton GW. Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the Th2 cytokine interleukin-13. Cancer Immunol Immunother 2011; 60:1419–30. doi:10.1007/s00262-011-1028-0. PMID:21644036.
  • Wu C, Wu X, Zhang X, Chai Y, Guo Q, Li L, Yue L, Bai J, Wang Z, Zhang L. Prognostic significance of peripheral monocytic myeloid-derived suppressor cells and monocytes in patients newly diagnosed with diffuse large b-cell lymphoma. Int J Clin Exp Med. 2015;8:15173–81. PMID:26629001.
  • Giallongo C, Parrinello NL, Tibullo D, La Cava P, Romano A, Chiarenza A, et al. Monocytic Myeloid Derived Suppressor CELLS (M-MDSC) As Prognostic Factor in Chronic Myeloid Leukemia Patients Treated with Dasatinib. Blood. 2015;126:2767.
  • Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S, Palmiter RD, Brinster RL. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 1985;318:533–8. doi:10.1038/318533a0. PMID:3906410.
  • Azzaoui I, Uhel F, Rossille D, Pangault C, Dulong J, Le Priol J, Lamy T, Houot R, Le Gouill S, Cartron G, et al. T-cell defect in diffuse large B-cell lymphomas involves expansion of myeloid-derived suppressor cells. Blood. 2016;128:1081–92. doi:10.1182/blood-2015-08-662783. PMID:27338100.
  • Jakubzick CV, Randolph GJ, Henson PM. Monocyte differentiation and antigen-presenting functions. Nat Rev Immunol 2017;17:349–62. doi:10.1038/nri.2017.28. PMID:28436425.
  • Lu C, Redd PS, Lee JR, Savage N, Liu K. The expression profiles and regulation of PD-L1 in tumor-induced myeloid-derived suppressor cells. Oncoimmunology. 2016;5:e1247135. doi:10.1080/2162402X.2016.1247135. PMID:28123883.
  • McKee SJ, Doff BL, Soon MS, Mattarollo SR. Therapeutic Efficacy of 4-1BB Costimulation Is Abrogated by PD-1 Blockade in a Model of Spontaneous B-cell Lymphoma. Cancer Immunol Res. 2017;5:191–7. doi:10.1158/2326-6066.CIR-16-0249. PMID:28115358.
  • Rios-Doria J, Durham N, Wetzel L, Rothstein R, Chesebrough J, Holoweckyj N, Zhao W, Leow CC, Hollingsworth R. Doxil synergizes with cancer immunotherapies to enhance antitumor responses in syngeneic mouse models. Neoplasia. 2015;17:661–70. doi:10.1016/j.neo.2015.08.004. PMID:26408258.
  • Kobayashi T, Doff BL, Rearden RC, Leggatt GR, Mattarollo SR. NKT cell-targeted vaccination plus anti-4-1BB antibody generates persistent CD8 T cell immunity against B cell lymphoma. Oncoimmunology. 2015;4:e990793. doi:10.4161/2162402X.2014.990793. PMID:25949907.
  • Khalifa KA, Badawy HM, Radwan WM, Shehata MA, Bassuoni MA. CD14(+) HLA-DR low/(-) monocytes as indicator of disease aggressiveness in B-cell non-Hodgkin lymphoma. Int J Lab Hematol. 2014;36:650–5. doi:10.1111/ijlh.12203. PMID:24636145.
  • Kitamura T, Qian BZ, Pollard JW. Immune cell promotion of metastasis. Nat Rev Immunol. 2015;15:73–86. doi:10.1038/nri3789. PMID:25614318.
  • Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9:162–74. doi:10.1038/nri2506. PMID:19197294.
  • De Veirman K, Van Valckenborgh E, Lahmar Q, Geeraerts X, De Bruyne E, Menu E, Van Riet I, Vanderkerken K, Van Ginderachter JA. Myeloid-derived suppressor cells as therapeutic target in hematological malignancies. Front Oncol. 2014;4:349. doi:10.3389/fonc.2014.00349. PMID:25538893.
  • Keane C, Vari F, Hertzberg M, Cao KA, Green MR, Han E, Seymour JF, Hicks RJ, Gill D, Crooks P. Ratios of T-cell immune effectors and checkpoint molecules as prognostic biomarkers in diffuse large B-cell lymphoma: a population-based study. Lancet Haematol. 2015;2:e445–55. doi:10.1016/S2352-3026(15)00150-7. PMID:26686046.
  • Marchesi F, Cirillo M, Bianchi A, Gately M, Olimpieri OM, Cerchiara E, Renzi D, Micera A, Balzamino BO, Bonini S, et al. High density of CD68+/CD163+ tumour-associated macrophages (M2-TAM) at diagnosis is significantly correlated to unfavorable prognostic factors and to poor clinical outcomes in patients with diffuse large B-cell lymphoma. Hematological oncology. 2015;33:110–2. doi:10.1002/hon.2142. PMID:24711044.
  • Harris JA, Jain S, Ren Q, Zarineh A, Liu C, Ibrahim S. CD163 versus CD68 in tumor associated macrophages of classical Hodgkin lymphoma. Diagnostic pathology. 2012;7:12. doi:10.1186/1746-1596-7-12. PMID:22289504.
  • Klein JL, Nguyen TT, Bien-Willner GA, Chen L, Foyil KV, Bartlett NL, Duncavage EJ, Hassan A, Frater JL, Kreisel F. CD163 immunohistochemistry is superior to CD68 in predicting outcome in classical Hodgkin lymphoma. Am J Clin Pathol. 2014;141:381–7. doi:10.1309/AJCP61TLMXLSLJYS. PMID:24515766.
  • Keam B, Ha H, Kim TM, Jeon YK, Lee SH, Kim DW, Kim CW, Heo DS. Neutrophil to lymphocyte ratio improves prognostic prediction of International Prognostic Index for patients with diffuse large B-cell lymphoma treated with rituximab, cyclophosphamide, doxorubicin, vincristine and prednisone. Leuk Lymphoma. 2015;56:2032–8. doi:10.3109/10428194.2014.982642. PMID:25382617.
  • Troppan K, Deutsch A, Gerger A, Stojakovic T, Beham-Schmid C, Wenzl K, Neumeister P, Pichler M. The derived neutrophil to lymphocyte ratio is an independent prognostic factor in patients with diffuse large B-cell lymphoma. Br J Cancer. 2014;110:369–74. doi:10.1038/bjc.2013.763. PMID:24357794.
  • Gamrekelashvili J, Giagnorio R, Jussofie J, Soehnlein O, Duchene J, Briseno CG, Ramasamy SK, Krishnasamy K, Limbourg A, Kapanadze T, et al. Regulation of monocyte cell fate by blood vessels mediated by Notch signalling. Nat Commun. 2016;7:12597. doi:10.1038/ncomms12597. PMID:27576369.
  • Ribatti D, Nico B, Ranieri G, Specchia G, Vacca A. The role of angiogenesis in human non-Hodgkin lymphomas. Neoplasia. 2013;15:231–8. doi:10.1593/neo.121962. PMID:23479502.
  • Suhasini AN, Wang L, Holder KN, Lin AP, Bhatnagar H, Kim SW, Moritz AW, Aguiar RCT. A phosphodiesterase 4B-dependent interplay between tumor cells and the microenvironment regulates angiogenesis in B-cell lymphoma. Leukemia. 2016;30:617–26. doi:10.1038/leu.2015.302. PMID:26503641.
  • Barrera P, Blom A, van Lent PL, van Bloois L, Beijnen JH, van Rooijen N, de Waal Malefijt MC, van de Putte LB, Storm G, van den Berg WB. Synovial macrophage depletion with clodronate-containing liposomes in rheumatoid arthritis. Arthritis Rheum. 2000;43:1951–9. doi:10.1002/1529-0131(200009)43:9%3c1951::AID-ANR5%3e3.0.CO;2-K. PMID:11014344.
  • Nakamura T, Abu-Dahab R, Menger MD, Schafer U, Vollmar B, Wada H, Lehr CM, Schäfers HJ. Depletion of alveolar macrophages by clodronate-liposomes aggravates ischemia-reperfusion injury of the lung. J Heart Lung Transplant. 2005;24:38–45. doi:10.1016/j.healun.2003.10.007. PMID:15653377.
  • Oki Y, Ewer MS, Lenihan DJ, Fisch MJ, Hagemeister FB, Fanale M, Romaguera J, Pro B, Fowler N, Younes A, et al. Pegylated liposomal doxorubicin replacing conventional doxorubicin in standard R-CHOP chemotherapy for elderly patients with diffuse large B-cell lymphoma: an open label, single arm, phase II trial. Clin Lymphoma Myeloma Leuk. 2015;15:152–8. doi:10.1016/j.clml.2014.09.001. PMID:25445468.
  • Zhou D, Li L, Bao C, Zhu J, Zhu L, Yang X, Zheng Y, Zhou M, Luo X, Xie W, et al. Replacement of conventional doxorubicin by pegylated liposomal doxorubicin in standard RCHOP chemotherapy for elderly diffuse large B-Cell lymphoma: a retrospective study in China. Int J Clin Exp Med 2015; 8:22497–502. PMID:26885233.
  • Lindemann RK, Newbold A, Whitecross KF, Cluse LA, Frew AJ, Ellis L, Williams S, Wiegmans AP, Dear AE, Scott CL, et al. Analysis of the apoptotic and therapeutic activities of histone deacetylase inhibitors by using a mouse model of B cell lymphoma. Proc Natl Acad Sci U S A. 2007;104:8071–6. doi:10.1073/pnas.0702294104. PMID:17470784.
  • Hertzberg M, Gandhi MK, Trotman J, Butcher B, Taper J, Johnston A, Gill D, Ho SJ, Cull G, Fay K, et al. Early treatment intensification with R-ICE and 90Y-ibritumomab tiuxetan (Zevalin)-BEAM stem cell transplantation in patients with high-risk diffuse large B-cell lymphoma patients and positive interim PET after 4 cycles of R-CHOP-14. Haematologica. 2017;102:356–63. doi:10.3324/haematol.2016.154039. PMID:28143954.
  • Perkins JR, Dawes JM, McMahon SB, Bennett DL, Orengo C, Kohl M. ReadqPCR and NormqPCR: R packages for the reading, quality checking and normalisation of RT-qPCR quantification cycle (Cq) data. BMC Genomics. 2012;13:296. doi:10.1186/1471-2164-13-296. PMID:22748112.
  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034. doi:10.1186/gb-2002-3-7-research0034. PMID:12184808.
  • Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106. doi:10.1186/gb-2010-11-10-r106. PMID:20979621.

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