IL-25 dampens the growth of human germinal center-derived B-cell non Hodgkin Lymphoma by curtailing neoangiogenesis

References

• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19:1423–37. doi:10.1038/nm.3394. PMID:24202395.
   PubMed Web of Science ®Google Scholar
• Fowler NH, Cheah CY, Gascoyne RD, Gribben J, Neelapu SS, Ghia P, Bollard C, Ansell S, Curran M, Wilson WH, et al. Role of the tumor microenvironment in mature B-cell lymphoid malignancies. Haematologica. 2016;101:531–40. doi:10.3324/haematol.2015.139493. PMID:27132279.
   PubMed Web of Science ®Google Scholar
• Shaffer AL, 3rd, Young RM, Staudt LM. Pathogenesis of human B cell lymphomas. Annu Rev Immunol. 2012;30:565–610. doi:10.1146/annurev-immunol-020711-075027. PMID:22224767.
   PubMed Web of Science ®Google Scholar
• Scott DW, Gascoyne RD. The tumour microenvironment in B cell lymphomas. Nat Rev Cancer. 2014;14:517–34. doi:10.1038/nrc3774. PMID:25008267.
   PubMed Web of Science ®Google Scholar
• Ferretti E, Di Carlo E, Ognio E, Guarnotta C, Bertoni F, Corcione A, Prigione I, Fraternali-Orcioni G, Ribatti D, Ravetti JL, et al. Interleukin-17A promotes the growth of human germinal center derived non-Hodgkin B cell lymphoma. Oncoimmunology. 2015;4:e1030560. doi:10.1080/2162402X.2015.1030560. PMID:26451300.
   PubMed Web of Science ®Google Scholar
• Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity. 2008;28:454–67. doi:10.1016/j.immuni.2008.03.004. PMID:18400188.
   PubMed Web of Science ®Google Scholar
• Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y, Fujikado N, Tanahashi Y, Akitsu A, Kotaki H, et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity. 2009;30:108–19. doi:10.1016/j.immuni.2008.11.009. PMID:19144317.
   PubMed Web of Science ®Google Scholar
• Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, Menon S, Seymour B, Jackson C, Kung TT, et al. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J Immunol. 2002;169:443–53. doi:10.4049/jimmunol.169.1.443. PMID:12077275.
   PubMed Web of Science ®Google Scholar
• Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A, Hewett DR, McIlgorm A, Jolin HE, McKenzie AN. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med. 2006;203:1105–16. doi:10.1084/jem.20051615. PMID:16606668.
   PubMed Web of Science ®Google Scholar
• Angkasekwinai P, Park H, Wang YH, Wang YH, Chang SH, Corry DB, Liu YJ, Zhu Z, Dong C. Interleukin 25 promotes the initiation of proallergic type 2 responses. J Exp Med. 2007;204:1509–17. doi:10.1084/jem.20061675. PMID:17562814.
   PubMed Web of Science ®Google Scholar
• Ikeda K, Nakajima H, Suzuki K, Kagami S, Hirose K, Suto A, Saito Y, Iwamoto I. Mast cells produce interleukin-25 upon Fc epsilon RI-mediated activation. Blood. 2003;101:3594–6. doi:10.1182/blood-2002–09-2817. PMID:12511410.
   PubMed Web of Science ®Google Scholar
• Kang CM, Jang AS, Ahn MH, Shin JA, Kim JH, Choi YS, Rhim TY, Park CS. Interleukin-25 and interleukin-13 production by alveolar macrophages in response to particles. Am J Respir Cell Mol Biol. 2005;33:290–6. doi:10.1165/rcmb.2005–0003OC. PMID:15961726.
   PubMed Web of Science ®Google Scholar
• Fort MM, Cheung J, Yen D, Li J, Zurawski SM, Lo S, Menon S, Clifford T, Hunte B, Lesley R, et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity. 2001;15:985–95. doi:10.1016/S1074–7613(01)00243–6. PMID:11754819.
   PubMed Web of Science ®Google Scholar
• Kim MR, Manoukian R, Yeh R, Silbiger SM, Danilenko DM, Scully S, Sun J, DeRose ML, Stolina M, Chang D, et al. Transgenic overexpression of human IL-17E results in eosinophilia, B-lymphocyte hyperplasia, and altered antibody production. Blood. 2002;100:2330–40. doi:10.1182/blood-2002–01-0012. PMID:12239140.
   PubMed Web of Science ®Google Scholar
• Gaffen SL. An overview of IL-17 function and signaling. Cytokine. 2008;43:402–7. doi:10.1016/j.cyto.2008.07.017. PMID:18701318.
   PubMed Web of Science ®Google Scholar
• Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, Hanabuchi S, Hippe A, Corrigan CJ, Dong C, Homey B, et al. IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J Exp Med. 2007;204:1837–47. doi:10.1084/jem.20070406. PMID:17635955.
   PubMed Web of Science ®Google Scholar
• Kang Z, Swaidani S, Yin W, Wang C, Barlow JL, Gulen MF, Bulek K, Do JS, Aronica M, McKenzie AN, et al. Epithelial cell-specific Act1 adaptor mediates interleukin-25-dependent helminth expulsion through expansion of Lin(-)c-Kit(+) innate cell population. Immunity. 2012;36:821–33. doi:10.1016/j.immuni.2012.03.021. PMID:22608496.
   PubMed Web of Science ®Google Scholar
• Yao Z, Painter SL, Fanslow WC, Ulrich D, Macduff BM, Spriggs MK, Armitage RJ. Human IL-17: a novel cytokine derived from T cells. J Immunol 1995;155:5483–6. PMID:7499828.
   PubMed Web of Science ®Google Scholar
• Shi Y, Ullrich SJ, Zhang J, Connolly K, Grzegorzewski KJ, Barber MC, Wang W, Wathen K, Hodge V, Fisher CL, et al. A novel cytokine receptor-ligand pair. Identification, molecular characterization, and in vivo immunomodulatory activity. J Biol Chem. 2000;275:19167–76..
   Google Scholar
• Rickel EA, Siegel LA, Yoon BR, Rottman JB, Kugler DG, Swart DA, Anders PM, Tocker JE, Comeau MR, Budelsky AL. Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J Immunol. 2008;181:4299–310. doi:10.4049/jimmunol.181.6.4299. PMID:18768888.
   PubMed Web of Science ®Google Scholar
• Hams E, Armstrong ME, Barlow JL, Saunders SP, Schwartz C, Cooke G, Fahy RJ, Crotty TB, Hirani N, Flynn RJ, et al. IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc Natl Acad Sci U S A. 2014;111:367–72. doi:10.1073/pnas.1315854111. PMID:24344271.
   PubMed Web of Science ®Google Scholar
• Gregory LG, Jones CP, Walker SA, Sawant D, Gowers KH, Campbell GA, McKenzie AN, Lloyd CM. IL-25 drives remodelling in allergic airways disease induced by house dust mite. Thorax. 2013;68:82–90. doi:10.1136/thoraxjnl-2012–202003. PMID:23093652.
   PubMed Web of Science ®Google Scholar
• Yao X, Wang W, Li Y, Huang P, Zhang Q, Wang J, Wang W, Lv Z, An Y, Qin J, Corrigan CJ, et al. IL-25 induces airways angiogenesis and expression of multiple angiogenic factors in a murine asthma model. Respir Res. 2015;16:39. doi:10.1186/s12931–015-0197–3. PMID:25889697.
   PubMed Web of Science ®Google Scholar
• Corrigan CJ, Wang W, Meng Q, Fang C, Wu H, Reay V, Lv Z, Fan Y, An Y, Wang YH, et al. T-helper cell type 2 (Th2) memory T cell-potentiating cytokine IL-25 has the potential to promote angiogenesis in asthma. Proc Natl Acad Sci U S A. 2011;108:1579–84. doi:10.1073/pnas.1014241108. PMID:21205894.
   PubMed Web of Science ®Google Scholar
• Wang W, Fan YQ, Lv Z, Yao XJ, Wang W, Huang KW, Meng Q, Fang CL, Lee TH, Corrigan CJ, et al. Interleukin-25 promotes basic fibroblast growth factor expression by human endothelial cells through interaction with IL-17RB, but not IL-17RA. Clin Exp Allergy. 2012;42:1604–14. doi:10.1111/j.1365–2222.2012.04062.x. PMID:23106660.
   PubMed Web of Science ®Google Scholar
• Lavocat F, Ndongo-Thiam N, Miossec P. Interleukin-25 Produced by Synoviocytes Has Anti-inflammatory Effects by Acting As a Receptor Antagonist for Interleukin-17A Function. Front Immunol. 2017;8:647. doi:10.3389/fimmu.2017.00647. PMID:28620392.
   PubMed Web of Science ®Google Scholar
• Furuta S, Jeng YM, Zhou L, Huang L, Kuhn I, Bissell MJ, Lee WH. IL-25 causes apoptosis of IL-25R-expressing breast cancer cells without toxicity to nonmalignant cells. Sci Transl Med. 2011;3:78ra31. doi:10.1126/scitranslmed.3001374..
   PubMed Web of Science ®Google Scholar
• Benatar T, Cao MY, Lee Y, Lightfoot J, Feng N, Gu X, Lee V, Jin H, Wang M, Wright JA, et al. IL-17E, a proinflammatory cytokine, has antitumor efficacy against several tumor types in vivo. Cancer Immunol Immunother. 2010;59:805–17. doi:10.1007/s00262–009-0802–8. PMID:20012860.
   PubMed Web of Science ®Google Scholar
• Huang CK, Yang CY, Jeng YM, Chen CL, Wu HH, Chang YC, Ma C, Kuo WH, Chang KJ, Shew JY, et al. Autocrine/paracrine mechanism of interleukin-17B receptor promotes breast tumorigenesis through NF-kappaB-mediated antiapoptotic pathway. Oncogene. 2014;33:2968–77. doi:10.1038/onc.2013.268. PMID:23851503.
   PubMed Web of Science ®Google Scholar
• Jiang Z, Chen J, Du X, Cheng H, Wang X, Dong C. IL-25 blockade inhibits metastasis in breast cancer. Protein Cell. 2017;8:191–201. doi:10.1007/s13238–016-0345–7. PMID:27909985.
   PubMed Web of Science ®Google Scholar
• Luo Y, Yang Z, Su L, Shan J, Xu H, Xu Y, Liu L, Zhu W, Chen X, Liu C, et al. Non-CSCs nourish CSCs through interleukin-17E-mediated activation of NF-kappaB and JAK/STAT3 signaling in human hepatocellular carcinoma. Cancer Lett. 2016;375:390–9. doi:10.1016/j.canlet.2016.03.012. PMID:27000993.
   PubMed Web of Science ®Google Scholar
• Allen CD, Okada T, Cyster JG. Germinal-center organization and cellular dynamics. Immunity. 2007;27:190–202. doi:10.1016/j.immuni.2007.07.009. PMID:17723214.
   PubMed Web of Science ®Google Scholar
• Carbone A, Gloghini A, Cabras A, Elia G. The Germinal centre-derived lymphomas seen through their cellular microenvironment. Br J Haematol. 2009;145:468–80. doi:10.1111/j.1365–2141.2009.07651.x. PMID:19344401.
   PubMed Web of Science ®Google Scholar
• Campo E, Swerdlow SH, Harris NL, Pileri S, Stein H, Jaffe ES. The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood. 2011;117:5019–32. doi:10.1182/blood-2011–01-293050. PMID:21300984.
   PubMed Web of Science ®Google Scholar
• Wong CK, Cheung PF, Ip WK, Lam CW. Interleukin-25-induced chemokines and interleukin-6 release from eosinophils is mediated by p38 mitogen-activated protein kinase, c-Jun N-terminal kinase, and nuclear factor-kappaB. Am J Respir Cell Mol Biol. 2005;33:186–94. doi:10.1165/rcmb.2005–0034OC. PMID:15860795.
   PubMed Web of Science ®Google Scholar
• Johnson PW, Watt SM, Betts DR, Davies D, Jordan S, Norton AJ, Lister TA. Isolated follicular lymphoma cells are resistant to apoptosis and can be grown in vitro in the CD40/stromal cell system. Blood 1993;82:1848–57. PMID:7691240.
   PubMed Web of Science ®Google Scholar
• Ferretti E, Ponzoni M, Doglioni C, Pistoia V. IL-17 superfamily cytokines modulate normal germinal center B cell migration. J Leukoc Biol. 2016;100:913–8. doi:10.1189/jlb.1VMR0216–096RR. PMID:27566830.
   PubMed Web of Science ®Google Scholar
• Qin Z, Blankenstein T. CD4+ T cell–mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells. Immunity. 2000;12:677–86. doi:10.1016/S1074–7613(00)80218–6. PMID:10894167.
   PubMed Web of Science ®Google Scholar
• Qin Z, Schwartzkopff J, Pradera F, Kammertoens T, Seliger B, Pircher H, Blankenstein T. A critical requirement of interferon gamma-mediated angiostasis for tumor rejection by CD8+ T cells. Cancer Res. 2003;63:4095–100. PMID:12874012.
   PubMed Web of Science ®Google Scholar
• Keane MP, Belperio JA, Arenberg DA, Burdick MD, Xu ZJ, Xue YY, Strieter RM. IFN-gamma-inducible protein-10 attenuates bleomycin-induced pulmonary fibrosis via inhibition of angiogenesis. J Immunol. 1999;163:5686–92. PMID:10553099.
   PubMed Web of Science ®Google Scholar
• Cao Y, Linden P, Farnebo J, Cao R, Eriksson A, Kumar V, et al. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci U S A. 1998;95:14389–94. doi:10.1073/pnas.95.24.14389. PMID:9826710.
   PubMed Web of Science ®Google Scholar
• Claesson-Welsh L, Welsh M. VEGFA and tumour angiogenesis. J Intern Med. 2013;273:114–27. doi:10.1111/joim.12019. PMID:23216836.
   PubMed Web of Science ®Google Scholar
• Conklin D, Gilbertson D, Taft DW, Maurer MF, Whitmore TE, Smith DL, Walker KM, Chen LH, Wattler S, Nehls M, et al. Identification of a mammalian angiopoietin-related protein expressed specifically in liver. Genomics 1999;62:477–82. doi:10.1006/geno.1999.6041. PMID:10644446.
   PubMed Web of Science ®Google Scholar
• Menrad A, Speicher D, Wacker J, Herlyn M. Biochemical and functional characterization of aminopeptidase N expressed by human melanoma cells. Cancer Res. 1993;53:1450–5. PMID:8095183.
   PubMed Web of Science ®Google Scholar
• Ishii K, Usui S, Sugimura Y, Yoshida S, Hioki T, Tatematsu M, Yamamoto H, Hirano K. Aminopeptidase N regulated by zinc in human prostate participates in tumor cell invasion. Int J Cancer. 2001;92:49–54. doi:10.1002/1097–0215(200102)9999:9999%3c::AID-IJC1161%3e3.0.CO;2-S. PMID:11279605.
   PubMed Web of Science ®Google Scholar
• Hashida H, Takabayashi A, Kanai M, Adachi M, Kondo K, Kohno N, Yamaoka Y, Miyake M. Aminopeptidase N is involved in cell motility and angiogenesis: its clinical significance in human colon cancer. Gastroenterology. 2002;122:376–86. doi:10.1053/gast.2002.31095. PMID:11832452.
   PubMed Web of Science ®Google Scholar
• Petrovic N, Schacke W, Gahagan JR, O'Conor CA, Winnicka B, Conway RE, Mina-Osorio P, Shapiro LH. CD13/APN regulates endothelial invasion and filopodia formation. Blood. 2007;110:142–50. doi:10.1182/blood-2006–02-002931. PMID:17363739.
   PubMed Web of Science ®Google Scholar
• Romagnani P, Lasagni L, Annunziato F, Serio M, Romagnani S. CXC chemokines: the regulatory link between inflammation and angiogenesis. Trends Immunol. 2004;25:201–9. doi:10.1016/j.it.2004.02.006. PMID:15039047.
   PubMed Web of Science ®Google Scholar
• Gijsbers K, Gouwy M, Struyf S, Wuyts A, Proost P, Opdenakker G, Penninckx F, Ectors N, Geboes K, Van Damme J. GCP-2/CXCL6 synergizes with other endothelial cell-derived chemokines in neutrophil mobilization and is associated with angiogenesis in gastrointestinal tumors. Exp Cell Res. 2005;303:331–42. doi:10.1016/j.yexcr.2004.09.027. PMID:15652347.
   PubMed Web of Science ®Google Scholar
• Wei LH, Kuo ML, Chen CA, Chou CH, Lai KB, Lee CN, Hsieh CY. Interleukin-6 promotes cervical tumor growth by VEGF-dependent angiogenesis via a STAT3 pathway. Oncogene. 2003;22:1517–27. doi:10.1038/sj.onc.1206226. PMID:12629515.
   PubMed Web of Science ®Google Scholar
• Zhao G, Zhu G, Huang Y, Zheng W, Hua J, Yang S, Zhuang J, Ye J. IL-6 mediates the signal pathway of JAK-STAT3-VEGF-C promoting growth, invasion and lymphangiogenesis in gastric cancer. Oncol Rep. 2016;35:1787–95. doi:10.3892/or.2016.4544. PMID:26750536.
   PubMed Web of Science ®Google Scholar
• Sarma V, Wolf FW, Marks RM, Shows TB, Dixit VM. Cloning of a novel tumor necrosis factor-alpha-inducible primary response gene that is differentially expressed in development and capillary tube-like formation in vitro. J Immunol. 1992;148:3302–12. PMID:1374453.
   PubMed Web of Science ®Google Scholar
• Pezzolo A, Marimpietri D, Raffaghello L, Cocco C, Pistorio A, Gambini C, Cilli M, Horenstein A, Malavasi F, Pistoia V. Failure of anti tumor-derived endothelial cell immunotherapy depends on augmentation of tumor hypoxia. Oncotarget. 2014;5:10368–81. doi:10.18632/oncotarget.2015. PMID:25362644.
   PubMed Web of Science ®Google Scholar
• Corcione A, Ottonello L, Tortolina G, Facchetti P, Airoldi I, Guglielmino R, Dadati P, Truini M, Sozzani S, Dallegri F, et al. Stromal cell-derived factor-1 as a chemoattractant for follicular center lymphoma B cells. J Natl Cancer Inst. 2000;92:628–35. doi:10.1093/jnci/92.8.628. PMID:10772680.
   PubMed Web of Science ®Google Scholar
• Epstein AL, Kaplan HS. Feeder layer and nutritional requirements for the establishment and cloning of human malignant lymphoma cell lines. Cancer Res. 1979;39:1748–59. PMID:371794.
   PubMed Web of Science ®Google Scholar
• Kluin-Nelemans HC, Limpens J, Meerabux J, Beverstock GC, Jansen JH, de Jong D, Kluin PM. A new non-Hodgkin's B-cell line (DoHH2) with a chromosomal translocation t(14;18)(q32;q21). Leukemia. 1991;5:221–4. PMID:1849602.
   PubMed Web of Science ®Google Scholar
• Benjamin D, Magrath IT, Maguire R, Janus C, Todd HD, Parsons RG. Immunoglobulin secretion by cell lines derived from African and American undifferentiated lymphomas of Burkitt's and non-Burkitt's type. J Immunol 1982;129:1336–42. PMID:6286763.
   PubMed Web of Science ®Google Scholar
• Corcione A, Ferretti E, Bertolotto M, Fais F, Raffaghello L, Gregorio A, et al. CX3CR1 is expressed by human B lymphocytes and mediates [corrected] CX3CL1 driven chemotaxis of tonsil centrocytes. PLoS One. 2009;4:e8485. doi:10.1371/journal.pone.0008485. PMID:20041188.
   PubMed Web of Science ®Google Scholar
• Ferretti E, Di Carlo E, Cocco C, Ribatti D, Sorrentino C, Ognio E, Montagna D, Pistoia V, Airoldi I. Direct inhibition of human acute myeloid leukemia cell growth by IL-12. Immunol Lett. 2010;133:99–105. doi:10.1016/j.imlet.2010.08.002. PMID:20705102.
   PubMed Web of Science ®Google Scholar
• Ferretti E, Montagna D, Di Carlo E, Cocco C, Ribatti D, Ognio E, Sorrentino C, Lisini D, Bertaina A, Locatelli F, et al. Absence of IL-12Rbeta2 in CD33(+)CD38(+) pediatric acute myeloid leukemia cells favours progression in NOD/SCID/IL2RgammaC-deficient mice. Leukemia. 2012;26:225–35. doi:10.1038/leu.2011.213. PMID:21844875.
   PubMed Web of Science ®Google Scholar
• Ribatti D, Nico B, Vacca A, Presta M. The gelatin sponge-chorioallantoic membrane assay. Nat Protoc. 2006;1:85–91. doi:10.1038/nprot.2006.13. PMID:17406216.
   PubMed Web of Science ®Google Scholar