CD5 Binds to Interleukin-6 and Induces a Feed-Forward Loop with the Transcription Factor STAT3 in B Cells to Promote Cancer

Immunity

Volumn 44, Issue 4, 2016, Pages 913-923

  Zhang, Chunyan ^a   Xin, Hong ^a   Zhang, Wang ^a   Yazaki, Paul J ^a   Zhang, Zhifang ^a   Le, Keith ^a   Li, Wenzhao ^a   Lee, Heehyoung ^a   Kwak, Larry ^a   Forman, Stephen ^a   Jove, Richard ^b   Yu, Hua ^a,c  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b NOVA SOUTHEASTERN UNIVERSITY   (United States)

^c Center for Translational Medicine   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD5 ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR ALPHA; JANUS KINASE 2; STAT3 PROTEIN; CD5 PROTEIN, MOUSE; GLYCOPROTEIN GP 130; IL6ST PROTEIN, MOUSE; INTERLEUKIN 6 RECEPTOR; INTERLEUKIN-6 RECEPTOR ALPHA; JAK2 PROTEIN, MOUSE; PROTEIN BINDING; STAT3 PROTEIN, MOUSE;

ANIMAL CELL; ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BLADDER TUMOR; CANCER GROWTH; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTERFERON INDUCTION; LUNG CANCER; MALE; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; OVARY CANCER; PERITONEAL CAVITY; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; SPLEEN; SPLEEN CELL; SURFACE PLASMON RESONANCE; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; UPREGULATION; 3T3 CELL LINE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; EXPERIMENTAL MELANOMA; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TRANSCRIPTION INITIATION; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD5; B-LYMPHOCYTES; CELL LINE, TUMOR; CYTOKINE RECEPTOR GP130; HUMANS; INTERLEUKIN-6; JANUS KINASE 2; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NIH 3T3 CELLS; PROTEIN BINDING; RECEPTORS, INTERLEUKIN-6; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION;

EID: 84964374893     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.04.003     Document Type: Article

References (54)

1. Ammirante M., Luo J.L., Grivennikov S., Nedospasov S., Karin M. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010, 464:302-305.
2. Andreu P., Johansson M., Affara N.I., Pucci F., Tan T., Junankar S., Korets L., Lam J., Tawfik D., DeNardo D.G., et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010, 17:121-134.
3. Baumgarth N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 2011, 11:34-46.
4. Berland R., Wortis H.H. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 2002, 20:253-300.
5. Bollrath J., Phesse T.J., von Burstin V.A., Putoczki T., Bennecke M., Bateman T., Nebelsiek T., Lundgren-May T., Canli O., Schwitalla S., et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 2009, 15:91-102.
6. Catlett-Falcone R., Landowski T.H., Oshiro M.M., Turkson J., Levitzki A., Savino R., Ciliberto G., Moscinski L., Fernández-Luna J.L., Nuñez G., et al. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999, 10:105-115.
7. de Visser K.E., Korets L.V., Coussens L.M. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005, 7:411-423.
8. de Wit J., Souwer Y., van Beelen A.J., de Groot R., Muller F.J., Klaasse Bos H., Jorritsma T., Kapsenberg M.L., de Jong E.C., van Ham S.M. CD5 costimulation induces stable Th17 development by promoting IL-23R expression and sustained STAT3 activation. Blood 2011, 118:6107-6114.
9. Deng J., Liu Y., Lee H., Herrmann A., Zhang W., Zhang C., Shen S., Priceman S.J., Kujawski M., Pal S.K., et al. S1PR1-STAT3 signaling is crucial for myeloid cell colonization at future metastatic sites. Cancer Cell 2012, 21:642-654.
10. + T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice. J. Immunol. 2010, 184:4006-4016.
11. Dong H.Y., Gorczyca W., Liu Z., Tsang P., Wu C.D., Cohen P., Weisberger J. B-cell lymphomas with coexpression of CD5 and CD10. Am. J. Clin. Pathol. 2003, 119:218-230.
12. Donnelly R.P., Dickensheets H., Finbloom D.S. The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J. Interferon Cytokine Res. 1999, 19:563-573.
13. Grivennikov S.I., Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev. 2010, 21:11-19.
14. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
15. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
16. Hedvat M., Huszar D., Herrmann A., Gozgit J.M., Schroeder A., Sheehy A., Buettner R., Proia D., Kowolik C.M., Xin H., et al. The JAK2 inhibitor AZD1480 potently blocks Stat3 signaling and oncogenesis in solid tumors. Cancer Cell 2009, 16:487-497.
17. Heinrich P.C., Behrmann I., Müller-Newen G., Schaper F., Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 1998, 334:297-314.
18. Heinrich P.C., Behrmann I., Haan S., Hermanns H.M., Müller-Newen G., Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 2003, 374:1-20.
19. Herrmann A., Cherryholmes G., Schroeder A., Phallen J., Alizadeh D., Xin H., Wang T., Lee H., Lahtz C., Swiderski P., et al. TLR9 is critical for glioma stem cell maintenance and targeting. Cancer Res. 2014, 74:5218-5228.
20. Hoge J., Yan I., Jänner N., Schumacher V., Chalaris A., Steinmetz O.M., Engel D.R., Scheller J., Rose-John S., Mittrücker H.W. IL-6 controls the innate immune response against Listeria monocytogenes via classical IL-6 signaling. J. Immunol. 2013, 190:703-711.
21. Ieguchi K., Fujita M., Ma Z., Davari P., Taniguchi Y., Sekiguchi K., Wang B., Takada Y.K., Takada Y. Direct binding of the EGF-like domain of neuregulin-1 to integrins (alphavbeta3 and alpha6beta4) is involved in neuregulin-1/ErbB signaling. J. Biol. Chem. 2010, 285:31388-31398.
22. Jones S.A., Scheller J., Rose-John S. Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J. Clin. Invest. 2011, 121:3375-3383.
23. Kortylewski M., Kujawski M., Wang T., Wei S., Zhang S., Pilon-Thomas S., Niu G., Kay H., Mulé J., Kerr W.G., et al. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat. Med. 2005, 11:1314-1321.
24. Kortylewski M., Xin H., Kujawski M., Lee H., Liu Y., Harris T., Drake C., Pardoll D., Yu H. Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell 2009, 15:114-123.
25. Krempler A., Qi Y., Triplett A.A., Zhu J., Rui H., Wagner K.U. Generation of a conditional knockout allele for the Janus kinase 2 (Jak2) gene in mice. Genesis 2004, 40:52-57.
26. Kujawski M., Kortylewski M., Lee H., Herrmann A., Kay H., Yu H. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J. Clin. Invest. 2008, 118:3367-3377.
27. Lamprecht B., Kreher S., Anagnostopoulos I., Jöhrens K., Monteleone G., Jundt F., Stein H., Janz M., Dörken B., Mathas S. Aberrant expression of the Th2 cytokine IL-21 in Hodgkin lymphoma cells regulates STAT3 signaling and attracts Treg cells via regulation of MIP-3alpha. Blood 2008, 112:3339-3347.
28. Lee H., Herrmann A., Deng J.H., Kujawski M., Niu G., Li Z., Forman S., Jove R., Pardoll D.M., Yu H. Persistently activated Stat3 maintains constitutive NF-kappaB activity in tumors. Cancer Cell 2009, 15:283-293.
29. Lee H., Deng J., Kujawski M., Yang C., Liu Y., Herrmann A., Kortylewski M., Horne D., Somlo G., Forman S., et al. STAT3-induced S1PR1 expression is crucial for persistent STAT3 activation in tumors. Nat. Med. 2010, 16:1421-1428.
30. Li Q., Teitz-Tennenbaum S., Donald E.J., Li M., Chang A.E. In vivo sensitized and in vitro activated B cells mediate tumor regression in cancer adoptive immunotherapy. J. Immunol. 2009, 183:3195-3203.
31. Mantovani A. B cells and macrophages in cancer: yin and yang. Nat. Med. 2011, 17:285-286.
32. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
33. Matsushita T., Yanaba K., Bouaziz J.D., Fujimoto M., Tedder T.F. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 2008, 118:3420-3430.
34. Neurath M.F., Finotto S. IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev. 2011, 22:83-89.
35. Nishimoto N., Ogata A., Shima Y., Tani Y., Ogawa H., Nakagawa M., Sugiyama H., Yoshizaki K., Kishimoto T. Oncostatin M, leukemia inhibitory factor, and interleukin 6 induce the proliferation of human plasmacytoma cells via the common signal transducer, gp130. J. Exp. Med. 1994, 179:1343-1347.
36. Putoczki T., Ernst M. More than a sidekick: the IL-6 family cytokine IL-11 links inflammation to cancer. J. Leukoc. Biol. 2010, 88:1109-1117.
37. Rose-John S. IL-6 trans-signaling via the soluble IL-6 receptor: importance for the pro-inflammatory activities of IL-6. Int. J. Biol. Sci. 2012, 8:1237-1247.
38. Rose-John S., Neurath M.F. IL-6 trans-signaling: the heat is on. Immunity 2004, 20:2-4.
39. Stout B.A., Bates M.E., Liu L.Y., Farrington N.N., Bertics P.J. IL-5 and granulocyte-macrophage colony-stimulating factor activate STAT3 and STAT5 and promote Pim-1 and cyclin D3 protein expression in human eosinophils. J. Immunol. 2004, 173:6409-6417.
40. Taga T., Kishimoto T. Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 1997, 15:797-819.
41. Trinchieri G. Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu. Rev. Immunol. 2012, 30:677-706.
42. Vera J., Fenutría R., Cañadas O., Figueras M., Mota R., Sarrias M.R., Williams D.L., Casals C., Yelamos J., Lozano F. The CD5 ectodomain interacts with conserved fungal cell wall components and protects from zymosan-induced septic shock-like syndrome. Proc. Natl. Acad. Sci. USA 2009, 106:1506-1511.
43. Wang L., Yi T., Kortylewski M., Pardoll D.M., Zeng D., Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J. Exp. Med. 2009, 206:1457-1464.
44. Woo J.R., Liss M.A., Muldong M.T., Palazzi K., Strasner A., Ammirante M., Varki N., Shabaik A., Howell S., Kane C.J., et al. Tumor infiltrating B-cells are increased in prostate cancer tissue. J. Transl. Med. 2014, 12:30.
45. Xin H., Lu R., Lee H., Zhang W., Zhang C., Deng J., Liu Y., Shen S., Wagner K.U., Forman S., et al. G-protein-coupled receptor agonist BV8/prokineticin-2 and STAT3 protein form a feed-forward loop in both normal and malignant myeloid cells. J. Biol. Chem. 2013, 288:13842-13849.
46. Xing C., Ma N., Xiao H., Wang X., Zheng M., Han G., Chen G., Hou C., Shen B., Li Y., Wang R. Critical role for thymic CD19+CD5+CD1dhiIL-10+ regulatory B cells in immune homeostasis. J. Leukoc. Biol. 2015, 97:547-556.
47. + phenotype controls T cell-dependent inflammatory responses. Immunity 2008, 28:639-650.
48. Yang C., Lee H., Jove V., Deng J., Zhang W., Liu X., Forman S., Dellinger T.H., Wakabayashi M., Yu H., Pal S. Prognostic significance of B-cells and pSTAT3 in patients with ovarian cancer. PLoS ONE 2013, 8:e54029.
49. Yang C., Lee H., Pal S., Jove V., Deng J., Zhang W., Hoon D.S., Wakabayashi M., Forman S., Yu H. B cells promote tumor progression via STAT3 regulated-angiogenesis. PLoS ONE 2013, 8:e64159.
50. Yoshizaki A., Miyagaki T., DiLillo D.J., Matsushita T., Horikawa M., Kountikov E.I., Spolski R., Poe J.C., Leonard W.J., Tedder T.F. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 2012, 491:264-268.
51. Yu H., Jove R. The STATs of cancer--new molecular targets come of age. Nat. Rev. Cancer 2004, 4:97-105.
52. Yu H., Kortylewski M., Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol. 2007, 7:41-51.
53. Yu H., Pardoll D., Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 2009, 9:798-809.
54. Zheng Z., Venkatapathy S., Rao G., Harrington C.A. Expression profiling of B cell chronic lymphocytic leukemia suggests deficient CD1-mediated immunity, polarized cytokine response, altered adhesion and increased intracellular protein transport and processing of leukemic cells. Leukemia 2002, 16:2429-2437.