Systemic neutralization of IL-17A significantly reduces breast cancer associated metastasis in arthritic mice by reducing CXCL12/SDF-1 expression in the metastatic niches

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Roy, Lopamudra D ^a   Sahraei, Mahnaz ^b   Schettini, Jorge L ^c   Gruber, Helen E ^d   Besmer, Dahlia M ^a   Mukherjee, Pinku ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CARIS LIFE SCIENCES   (United States)

^d CAROLINAS MEDICAL CENTER   (United States)

Author keywords

Autoimmune arthritis; Bone metastasis; Breast cancer; CXCR4 CXCL12; IL 17A; Lung metastasis; SDF 1

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; COLONY STIMULATING FACTOR 1; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 6; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTHRITIS; ARTICLE; AUTOIMMUNE ARTHRITIS; BONE METASTASIS; BREAST CANCER; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DRUG EFFECT; DRUG MECHANISM; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG METASTASIS; METASTASIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SYSTEMIC THERAPY; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS; BONE NEOPLASMS; CELL LINE, TUMOR; CHEMOKINE CXCL12; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; INTERLEUKIN-17; INTERLEUKIN-6; LUNG NEOPLASMS; MACROPHAGE COLONY-STIMULATING FACTOR; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; RECEPTORS, CXCR4;

EID: 84899102412     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-225     Document Type: Article

References (49)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012, 62(1):10-29. 10.3322/caac.20138, 22237781.
2. de Visser KE, Coussens LM. The inflammatory tumor microenvironment and its impact on cancer development. Contrib Microbiol 2006, 13:118-137.
3. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436(7050):518-524. 10.1038/nature03799, 1283098, 16049480.
4. Majithia V, Geraci SA. Rheumatoid arthritis: diagnosis and management. Am J Med 2007, 120(11):936-939. 10.1016/j.amjmed.2007.04.005, 17976416.
5. Ji J, Liu X, Sundquist K, Sundquist J. Survival of cancer in patients with rheumatoid arthritis: a follow-up study in Sweden of patients hospitalized with rheumatoid arthritis 1 year before diagnosis of cancer. Rheumatology (Oxford) 2011, 50(8):1513-1518. doi:10.1093/rheumatology/ker143. Epub 2011 Apr 15, 10.1093/rheumatology/ker143, 21498553.
6. Das Roy L, Pathangey L, Tinder T, Schettini J, Gruber H, Mukherjee P. Breast cancer-associated metastasis is significantly increased in a model of autoimmune arthritis. Breast Cancer Res 2009, 11(4):R56. 10.1186/bcr2345, 2750117, 19643025.
7. Das Roy L, Ghosh S, Pathangey LB, Tinder TL, Gruber HE, Mukherjee P. Collagen induced arthritis increases secondary metastasis in MMTV-PyV MT mouse model of mammary cancer. BMC Cancer 2011, 11(1):365. 10.1186/1471-2407-11-365, 3224388, 21859454.
8. Roy LD, Curry JM, Sahraei M, Besmer DM, Kidiyoor A, Gruber HE, Mukherjee P. Arthritis augments breast cancer metastasis: role of mast cells and SCF/c-Kit signaling. Breast Cancer Res 2013, 15(2):R32. 10.1186/bcr3412, 3672823, 23577751.
9. Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, Maat C, Pin JJ, Garrone P, Garcia E, Saeland S, Blanchard D, Gaillard C, Das Mahapatra B, Rouvier E, Golstein P, Banchereau J, Lebecque S. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 1996, 183(6):2593-2603. 10.1084/jem.183.6.2593, 2192621, 8676080.
10. Zhu X, Mulcahy L, Mohammed R, Lee A, Franks H, Kilpatrick L, Yilmazer A, Paish E, Ellis I, Patel P, Jackson A. IL-17 expression by breast-cancer-associated macrophages: IL-17 promotes invasiveness of breast cancer cell lines. Breast Cancer Res 2008, 10:R95. 10.1186/bcr2195, 2656888, 19014637.
11. Hsu EL, Chen N, Westbrook A, Wang F, Zhang R, Taylor RT, Hankinson O. Modulation of CXCR4, CXCL12, and tumor cell invasion potential in vitro by phytochemicals. J Oncol 2009, 2009:491985. 2659867, 19325924.
12. Hinton CV, Avraham S, Avraham HK. Role of the CXCR4/CXCL12 signaling axis in breast cancer metastasis to the brain. Clin Exp Metastasis 2010, 27(2):97-105. 10.1007/s10585-008-9210-2, 18814042.
13. Burger JA, Peled A. CXCR4 antagonists: targeting the microenvironment in leukemia and other cancers. Leukemia 2009, 23(1):43-52. 10.1038/leu.2008.299, 18987663.
14. Tao K, Fang M, Alroy J, Sahagian GG. Imagable 4 T1 model for the study of late stage breast cancer. BMC Cancer 2008, 8:228. 10.1186/1471-2407-8-228, 2529338, 18691423.
15. Nakamori M, Fu X, Rousseau R, Chen SY, Zhang X. Destruction of nonimmunogenic mammary tumor cells by a fusogenic oncolytic herpes simplex virus induces potent antitumor immunity. Mol Ther 2004, 9(5):658-665. 10.1016/j.ymthe.2004.02.019, 15120326.
16. Li H, Dutuor A, Fu X, Zhang X. Induction of strong antitumor immunity by an HSV-2-based oncolytic virus in a murine mammary tumor model. J Gene Med 2007, 9(3):161-169. 10.1002/jgm.1005, 17266169.
17. Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, Sakihama T, Matsutani T, Negishi I, Nakatsuru S, Sakaguchi S. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 2003, 426:454-460. 10.1038/nature02119, 14647385.
18. Yoshitomi H, Sakaguchi N, Kobayashi K, Brown GD, Tagami T, Sakihama T, Hirota K, Tanaka S, Nomura T, Miki I, Gordon S, Akira S, Nakamura T, Sakaguchi S. A role for fungal {beta}-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med 2005, 201:949-960. 10.1084/jem.20041758, 2213107, 15781585.
19. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992, 12(3):954-961. 369527, 1312220.
20. Mukherjee P, Madsen CS, Ginardi AR, Tinder TL, Jacobs F, Parker J, Agrawal B, Longenecker BM, Gendler SJ. Mucin 1-specific immunotherapy in a mouse model of spontaneous breast cancer. J Immunother 2003, 26(1):47-62. 10.1097/00002371-200301000-00006, 12514429.
21. Basu GD, Tinder TL, Bradley JM, Tu T, Hattrup CL, Pockaj BA, Mukherjee P. Cyclooxygenase-2 inhibitor enhances the efficacy of a breast cancer vaccine: role of IDO. J Immunol 2006, 177(4):2391-2402.
22. Basu G, Pathangey L, Tinder T, LaGioia M, Gendler S, Mukherjee P. COX-2 inhibitor induces apoptosis in breast cancer cells in an in vivo model of spontaneous metastatic breast cancer. Mol Cancer Res 2004, 2:632-642.
23. Chen D, Xia J, Tanaka Y, Chen H, Koido S, Wernet O, Mukherjee P, Gendler SJ, Kufe D, Gong J. Immunotherapy of spontaneous mammary carcinoma with fusions of dendritic cells and mucin 1-positive carcinoma cells. Immunology 2003, 109(2):300-307. 10.1046/j.1365-2567.2003.01656.x, 1782954, 12757626.
24. Brand DD, Latham KA, Rosloniec EF. Collagen-induced arthritis. Nat Protoc 2007, 2(5):1269-1275. 10.1038/nprot.2007.173, 17546023.
25. Rosloniec EF, Cremer M, Kang AH, Myers LK, Brand DD. Collagen-induced arthritis. Curr Protoc Immunol 2010, Chapter 15(Unit 15.5):1-25. doi:10.1002/0471142735.im1505s89; PMID:20376842.
26. Roy LD, Sahraei M, Subramani DB, Besmer D, Nath S, Tinder TL, Bajaj E, Shanmugam K, Lee YY, Hwang SI, Gendler SJ, Mukherjee P. MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 2011, 30(12):1449-1459. 10.1038/onc.2010.526, 3063863, 21102519.
27. Besmer DM, Curry JM, Roy LD, Tinder TL, Sahraei M, Schettini J, Hwang SI, Lee YY, Gendler SJ, Mukherjee P. Pancreatic ductal adenocarcinoma mice lacking mucin 1 have a profound defect in tumor growth and metastasis. Cancer Res 2011, 71(13):4432-4442. 10.1158/0008-5472.CAN-10-4439, 3129481, 21558393.
28. Woo M, Nordal R. Commissioning and evaluation of a new commercial small rodent x-ray irradiator. Biomed Imaging Interv J 2006, 2(1):e10. 3097609, 21614214.
29. Meads MB, Hazlehurst LA, Dalton WS. The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin Cancer Res 2008, 14(9):2519-2526. 10.1158/1078-0432.CCR-07-2223, 18451212.
30. Kryczek I, Wei S, Keller E, Liu R, Zou W. Stroma-derived factor (SDF-1/CXCL12) and human tumor pathogenesis. Am J Physiol Cell Physiol 2007, 292(3):C987-C995.
31. Holland JD, Gyorffy B, Vogel R, Eckert K, Valenti G, Fang L, Lohneis P, Elezkurtaj S, Ziebold U, Birchmeier W. Combined Wnt/β-catenin, Met, and CXCL12/CXCR4 signals characterize basal breast cancer and predict disease outcome. Cell Rep 2013, 5(5):1214-27. doi:10.1016/j.celrep.2013.11.001; PMID:24290754, 10.1016/j.celrep.2013.11.001, 24290754.
32. Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res 2010, 16(11):2927-2931. 10.1158/1078-0432.CCR-09-2329, 20484021.
33. Petit I, Jin D, Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol 2007, 28(7):299-307. 10.1016/j.it.2007.05.007, 2952492, 17560169.
34. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verástegui E, Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410(6824):50-56. 10.1038/35065016, 11242036.
35. Chabaud M, Fossiez F, Taupin JL, Miossec P. Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. J Immunol 1998, 161(1):409-414.
36. Campbell IK, Rich MJ, Bischof RJ, Hamilton JA. The colony-stimulating factors and collagen-induced arthritis: exacerbation of disease by M-CSF and G-CSF and requirement for endogenous M-CSF. J Leukoc Biol 2000, 68(1):144-150.
37. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, Suda T. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 1999, 103(9):1345-1352. 10.1172/JCI5703, 408356, 10225978.
38. Arun B, Goss P. The role of COX-2 inhibition in breast cancer treatment and prevention. Semin Oncol 2004, 31(2 Suppl 7):22-29.
39. Ziegler J. Cancer and arthritis share underlying processes. J Natl Cancer Inst 1998, 90:802-803. 10.1093/jnci/90.11.802, 9625164.
40. Coussens L, Werb Z. Inflammation and cancer. Nature 2002, 420:860-867. 10.1038/nature01322, 2803035, 12490959.
41. Philip M, Rowley D, Schreiber H. Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 2004, 14:433-439. 10.1016/j.semcancer.2004.06.006, 15489136.
42. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995, 1(1):27-31. 10.1038/nm0195-27, 7584949.
43. Seki M, Uzuki M, Ohmoto H, Yoshino K, Maeda S, Kokubun S, Sakurai M, Sawai T. Matrix metalloproteinase (MMP-9) in patients with rheumatoid arthritis. Ryumachi 1995, 35(5):792-801.
44. Ziolkowska M, Koc A, Luszczykiewicz G, Ksiezopolska-Pietrzak K, Klimczak E, Chwalinska-Sadowska H, Maslinski W. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J Immunol 2000, 164(5):2832-2838.
45. Tilg H, Kaser A. IL-6 and arthritis: a detrimental or beneficial mediator?. IDrugs 1998, 1(8):890-895.
46. Ben-Baruch A. Inflammation-associated immune suppression in cancer: the roles played by cytokines, chemokines and additional mediators. Semin Cancer Biol 2006, 16:38-52. 10.1016/j.semcancer.2005.07.006, 16139507.
47. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, Ceccarelli C, Santini D, Paterini P, Marcu K, Chieco P, Bonafe M. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 2007, 117:3988-4002. 10.1172/JCI32533, 2096439, 18060036.
48. Nam J, Terabe M, Kang M, Chae H, Voong N, Yang Y, Laurence A, Michalowska A, Mamura M, Lonning S, Berzofsky JA, Wakefield LM. Transforming growth factor beta subverts the immune system into directly promoting tumor growth through interleukin-17. Cancer Res 2008, 68:3915-3923. 10.1158/0008-5472.CAN-08-0206, 2586596, 18483277.
49. van den Berg WB, Miossec P. IL-17 as a future therapeutic target for rheumatoid arthritis. Nat Rev Rheumatol 2009, 5(10):549-553. 10.1038/nrrheum.2009.179, 19798029.