CCL20 mediates RANK/RANKL-induced epithelial-mesenchymal transition in endometrial cancer cells

Oncotarget

Volumn 7, Issue 18, 2016, Pages 25328-25339

  Liu, Yao ^a   Wang, Jing ^a   Ni, Ting ^a   Wang, Lihua ^a   Wang, Yudong ^a   Sun, Xiao ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

CCL20; Endometrial cancer; Epithelial mesenchymal transition; RANK; RANKL

Indexed keywords

MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; OSTEOCLAST DIFFERENTIATION FACTOR; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; CCL20 PROTEIN, HUMAN; TNFRSF11A PROTEIN, HUMAN; TNFSF11 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER STAGING; CELL INVASION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOMETRIAL CANCER CELL LINE; ENDOMETRIUM CANCER; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEIN SECRETION; TISSUE LEVEL; ANIMAL; ENDOMETRIUM TUMOR; FEMALE; GENE EXPRESSION REGULATION; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CHEMOKINE CCL20; ENDOMETRIAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; MICE; MICE, NUDE; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B;

EID: 84967316114     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8291     Document Type: Article

References (41)

1. Siegel R, Miller K, Jemal A. Cancer statistics. CA Cancer J Clin. 2015; 65:5-29.
2. Di Cristofano A, Ellenson LH. Endometrial carcinoma. Annu Rev Pathol. 2007; 2:57-85.
3. Hill EK, Dizon DS. Medical therapy of endometrial cancer: current status and promising novel treatments. Drugs. 2012; 72:705-713.
4. Oza AM, Elit L, Tsao MS, Kamel-Reid S, Biagi J, Provencher DM, Gotlieb WH, Hoskins PJ, Ghatage P, Tonkin KS, Mackay HJ, Mazurka J, Sederias J, et al. Phase II study of temsirolimus in women with recurrent or metastatic endometrial cancer: a trial of the NCIC Clinical Trials Group. J Clin Oncol. 2011; 29:3278-3285.
5. Leonardi GC, Candido S, Cervello M, Nicolosi D, Raiti F, Travali S, Spandidos DA, Libra M. The tumor microenvironment in hepatocellular carcinoma (review). Int J Oncol. 2012; 40:1733-1747.
6. O'Hayre M, Salanga CL, Handel TM, Allen SJ. Chemokines and cancer: Migration, intracellular signalling and intercellular communication in the microenvironment. Biochem J. 2008; 409:635-649.
7. Tan W, Zhang W, Strasner A, Grivennikov S, Cheng JQ, Hoffman RM, Karin M. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signalling. Nature. 2011; 470:548-553.
8. Santini D, Perrone G, Roato I, Godio L, Pantano F, Grasso D, Russo A, Vincenzi B, Fratto ME, Sabbatini R, Della Pepa C, Porta C, Del Conte A, et al. Expression pattern of receptor activator of NFκB (RANK) in a series of primary solid tumors and related bone metastases. J Cell Physiol. 2011; 226:780-784.
9. Jones DH, Nakashima T, Sanchez OH, Kozieradzki I, Komarova SV, Sarosi I, Morony S, Rubin E, Sarao R, Hojilla CV, Komnenovic V, Kong YY, Schreiber M, et al. Regulation of cancer cell migration and bone metastasis by RANKL. Nature. 2006; 440:692-696.
10. Palafox M, Ferrer I, Pellegrini P, Vila S, Hernandez-OrtegaS, Urruticoechea A, Climent F, Soler MT, Muñoz P, Viñals F, Tometsko M, Branstetter D, Dougall WC, et al. RANK induces epithelial-mesenchymal transition and stemness in human mammary epithelial cells and promotes tumorigenesis and metastasis. Cancer Res. 2012; 72:2879-2888.
11. Wang J, Sun X, Zhang H, Wang Y, Li Y. MPA influences tumor cell proliferation, migration, and invasion induced by RANKL through PRB involving the MAPK pathway in endometrial cancer. Oncol Rep. 2015; 33:799-809.
12. Wang J, Liu Y, Wang L, Sun X, Wang Y. Clinical prognostic significance and pro-metastatic activity of RANK/RANKL via the AKT pathway in endometrial cancer. Oncotarget. 2015. doi: 10.18632/oncotarget.6795.
13. Giuliani N, Lisignoli G, Colla S, Lazzaretti M, StortiP, Mancini C, Bonomini S, Manferdini C, Codeluppi K, Facchini A, Rizzoli V, et al. CC-chemokine ligand 20/macrophage inflammatory protein-3a and CC-chemokine receptor 6 are overexpressed in myeloma microenvironment related to osteolytic bone lesions. Cancer Res. 2008; 68:6840-6850.
14. Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 2003; 14:409-426.
15. Yoshimura T, Matsushima K, Tanaka S, Robinson EA, Appella E, Oppenheim JJ, Leonard EJ. Purification of a human monocyte-derived neutrophil chemotactic factor that has peptide sequence similarity to other host defense cytokines. Proc Natl Acad Sci USA. 1987; 84:9233-9237.
16. Marsigliante S, Vetrugno C, Muscella A. CCL20 induces migration and proliferation on breast epithelial cells. J Cell Physiol. 2013; 228:1873-1883.
17. Vicinus B, Rubie C, Stegmaier N, Frick VO, Kölsch K, Kauffels A, Ghadjar P, Wagner M, Glanemann M. miR-21 and its target gene CCL20 are both highly overexpressed in the microenvironment of colorectal tumors: significance of their regulation. Oncol Rep. 2013; 30:1285-1292.
18. Biswas S, Sengupta S, Roy Chowdhury S, Jana S, Mandal G, Mandal PK, Saha N, Malhotra V, Gupta A, Kuprash DV, Bhattacharyya A. CXCL13-CXCR5 co-expression regulates epithelial to mesenchymal transition of breast cancer cells during lymph node metastasis. Breast Cancer Res Treat. 2014; 143:265-276.
19. Li X, Ma Q, Xu Q, Liu H, Lei J, Duan W, Bhat K, Wang F, Wu E, Wang Z. SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial-mesenchymal transition in vitro through non-canonical activation of Hedgehog pathway. Cancer Lett. 2012; 322:169-176.
20. Matsushita K, Toiyama Y, Tanaka K, Saigusa S, HiroJ, Uchida K, Inoue Y, Kusunoki M. Soluble CXCL16 in preoperative serum is a novel prognostic marker and predicts recurrence of liver metastases in colorectal cancer patients. Ann Surg Oncol. 2012; 19:S518-S527.
21. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell. 2008; 14:818-829.
22. Liao Y, He X, Qiu H, Che Q, Wang F, Lu W, Chen Z, Qiu M, Wang J, Wang H, Wan X. Suppression of the epithelial-mesenchymal transition by SHARP1 is linked to the NOTCH1 signaling pathway in metastasis of endometrial cancer. BMC Cancer. 2014; 487.
23. Beleut M, Rajaram RD, Caikovski M, Ayyanan A, Germano D, Choi Y, Schneider P, Brisken C. Two distinct mechanisms underlie progesterone-induced proliferation in the mammary gland. Proc Natl Acad Sci USA. 2010; 107:2989-2994.
24. Shimamura M, Nakagami H, Osako MK, KurinamiH, Koriyama H, Zhengda P, Tomioka H, Tenma A, Wakayama K, Morishita R. OPG/RANKL/RANK axis is a critical inflammatory signaling system in ischemic brain in mice. Proc Natl Acad Sci USA. 2014; 111:8191-8196.
25. Nieto MA. Epithelial plasticity: a common theme in embryonic and cancer cells. Science. 2013; 342:1234850.
26. Tan EJ, Kahata K, Idås O, Thuault S, Heldin CH, MoustakasA. The high mobility group A2 protein epigenetically silences the Cdh1 gene during epithelial-to-mesenchymal transition. Nucleic Acids Res. 2015; 43:162-178.
27. Zhang J, Wei J, Lu J, Tong Z, Liao B, Yu B, ZhengF, Huang X, Chen Z, Fang Y, Li B, Chen W, Xie D, et al. Overexpression of Rab25 contributes to metastasis of bladder cancer through induction of epithelial-mesenchymal transition and activation of Akt/GSK-3beta/Snail signaling. Carcinogenesis. 2013; 34:2401-2408.
28. Tanaka Y, Terai Y, Kawaguchi H, Fujiwara S, Yoo S, Tsunetoh S, Takai M, Kanemura M, Tanabe A, Ohmichi M. Prognostic impact of EMT (epithelial-mesenchymal-transition)-related protein expression in endometrial cancer. Cancer Biol Ther. 2013; 14:13-19.
29. Pirus Ghadjar, Claudia Rubie, Daniel M. Aebersold, Ulrich Keilholz. The chemokine CCL20 and its receptor CCR6 in human malignancy with focus on colorectal cancer. Int J Cancer. 2009; 125:741-745.
30. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, WagnerSN, Barrera JL, Mohar A, Verástegui E, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature. 2001; 410:50-56.
31. Ding Y, Shimada Y, Maeda M, Kawabe A, KaganoiJ, Komoto I, Hashimoto Y, Miyake M, Hashida H, Imamura M. Association of CC chemokine receptor 7 with lymph node metastasis of esophageal squamous cell carcinoma. Clin Cancer Res. 2003; 9:3406-3412.
32. Wiley HE, Gonzales EB, Maki W, Wu MT, Hwang ST. Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16murine melanoma. J Natl Cancer Inst. 2001; 93:1638-1643.
33. Taichman RS, Cooper C, Keller ET, Pienta KJ, TaichmanNS, McCauley LK. Use of the stromal cell-derived Factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res. 2002; 62:1832-187.
34. Murakami T, Maki W, Cardones AR, Fang H, TunKyi A, Nestle FO, Hwang ST. Expression of CXC chemokine receptor-4 enhances the pulmonary metastatic potential of murine B16melanoma cells. Cancer Res. 2002; 62:7328-7334.
35. Letsch A, Keilholz U, Schadendorf D, Assfalg G, Asemissen AM, Thiel E, Scheibenbogen C. Functional CCR9 expression is associated with small intestinal metastasis. J Invest Dermatol. 2004; 122:685-690.
36. Mashino K, Sadanaga N, Yamaguchi H, Tanaka F, Ohta M, Shibuta K, Inoue H, Mori M. Expression of chemokine receptor CCR7 is associated with lymph node metastasis of gastric carcinoma. Cancer Res. 2002; 62:2937-2941.
37. Zeelenberg IS, Ruuls-Van Stalle L, Roos E. The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res. 2003; 63:3833-3839.
38. Boon T, Van den Eynde B. Tumour immunology. Curr Opin Immunol. 2003; 15:129-130.
39. Wilson J, Balkwill F. The role of cytokines in the epithelial cancer microenvironment. Semin Cancer Biol. 2002; 12:113-120.
40. Creasman W. Revised FIGO staging for carcinoma of the endometrium. Int J Gynaecol Obstet. 2009; 105:109.
41. Remmele W, Stegner HE. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe. 1987; 8:138-140.