NF-κB-mediated CCL20 reigns dominantly in CXCR2-driven ovarian cancer progression

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Ignacio, Rosa Mistica C ^a   Kabir, Syeda M ^a   Lee, Eun Sook ^b   Adunyah, Samuel E ^a   Son, Deok Soo ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b FLORIDA A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN KINASE B; RAF PROTEIN; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER SURVIVAL; CCL20 GENE; CONTROLLED STUDY; FEMALE; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; OMENTUM; OVARY CANCER; PELVIS; PERITONEUM METASTASIS; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURVIVAL TIME; ANIMAL; DISEASE COURSE; GENETIC TRANSFECTION; GENETICS; METABOLISM; NUDE MOUSE; OVARY TUMOR; PATHOLOGY; PERITONEAL CAVITY; REPORTER GENE; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CHEMOKINE CCL20; CHEMOKINE CXCL1; DISEASE PROGRESSION; FEMALE; GENES, REPORTER; HUMANS; MICE; MICE, NUDE; NF-KAPPA B; OVARIAN NEOPLASMS; PERITONEAL CAVITY; PROMOTER REGIONS, GENETIC; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INTERLEUKIN-8B; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS;

EID: 84991465801     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0164189     Document Type: Article

References (53)

1. Chobanian N, Dietrich CS III. Ovarian cancer. Surg Clin North Am. 2008; 88:285-299, vi. doi: 10. 1016/j. suc. 2007. 12. 002 PMID: 18381114
2. Maccio A, Madeddu C. Inflammation and ovarian cancer. Cytokine. 2012; 58:133-147. doi: 10. 1016/j. cyto. 2012. 01. 015 PMID: 22349527
3. Dobrzycka B, Terlikowski SJ, Kowalczuk O, Kinalski M. Circulating levels of TNF-αlpha and its soluble receptors in the plasma of patients with epithelial ovarian cancer. Eur Cytokine Netw. 2009; 20:131-134. doi: 10. 1684/ecn. 2009. 0161 PMID: 19825522
4. Szlosarek PW, Grimshaw MJ, Kulbe H, Wilson JL, Wilbanks GD, Burke F, et al. Expression and regulation of tumor necrosis factor alpha in normal and malignant ovarian epithelium. Mol Cancer Ther. 2006; 5:382-390. doi: 10. 1158/1535-7163. MCT-05-0303 PMID: 16505113
5. Son DS, Parl AK, Rice VM, Khabele D. Keratinocyte chemoattractant (KC)/human growth-regulated oncogene (GRO) chemokines and pro-inflammatory chemokine networks in mouse and human ovarian epithelial cancer cells. Cancer Biol Ther. 2007; 6:1302-1312. doi: 10. 4161/cbt. 6. 8. 4506 PMID: 17712227
6. Son DS, Kabir SM, Dong Y, Lee E, Adunyah SE. Characteristics of chemokine signatures elicited by EGF and TNF in ovarian cancer cells. J Inflamm (Lond). 2013; 10:25. doi: 10. 1186/1476-9255-10-25 PMID: 23800251
7. Son DS, Kabir SM, Dong YL, Lee E, Adunyah SE. Inhibitory effect of tumor suppressor p53 on proinflammatory chemokine expression in ovarian cancer cells by reducing proteasomal degradation of IkappaB. PLoS One. 2012; 7:e51116. doi: 10. 1371/journal. pone. 0051116 PMID: 23300534
8. Balkwill FR. The chemokine system and cancer. J Pathol. 2012; 226:148-157. doi: 10. 1002/path. 3029 PMID: 21989643
9. Singh R, Lillard JW Jr, Singh S. Chemokines: key players in cancer progression and metastasis. Front Biosci (Schol Ed). 2011; 3:1569-1582. doi: 10. 2741/246 PMID: 21622291
10. Olson TS, Ley K. Chemokines and chemokine receptors in leukocyte trafficking. Am J Physiol Regul Integr Comp Physiol. 2002; 283:R7-28. doi: 10. 1152/ajpregu. 00738. 2001 PMID: 12069927
11. Yang G, Rosen DG, Liu G, Yang F, Guo X, Xiao X, et al. CXCR2 promotes ovarian cancer growth through dysregulated cell cycle, diminished apoptosis, and enhanced angiogenesis. Clin Cancer Res. 2010; 16:3875-3886. doi: 10. 1158/1078-0432. CCR-10-0483 PMID: 20505188
12. Shen H, Schuster R, Lu B, Waltz SE, Lentsch AB. Critical and opposing roles of the chemokine receptors CXCR2 and CXCR3 in prostate tumor growth. Prostate. 2006; 66:1721-1728. doi: 10. 1002/pros. 20476 PMID: 16941672
13. Keane MP, Belperio JA, Xue YY, Burdick MD, Strieter RM. Depletion of CXCR2 inhibits tumor growth and angiogenesis in a murine model of lung cancer. J Immunol. 2004; 172:2853-2860. doi: 10. 4049/jimmunol. 172. 5. 2853 PMID: 14978086
14. Mestas J, Burdick MD, Reckamp K, Pantuck A, Figlin RA, Strieter RM. The role of CXCR2/CXCR2 ligand biological axis in renal cell carcinoma. J Immunol. 2005; 175:5351-5357. doi: 10. 4049/jimmunol. 175. 8. 5351 PMID: 16210641
15. Jamieson T, Clarke M, Steele CW, Samuel MS, Neumann J, Jung A, et al. Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J Clin Invest. 2012; 122:3127-3144. doi: 10. 1172/JCI61067 PMID: 22922255
16. Lee YS, Choi I, Ning Y, Kim NY, Khatchadourian V, Yang D, et al. Interleukin-8 and its receptor CXCR2 in the tumour microenvironment promote colon cancer growth, progression and metastasis. Br J Cancer. 2012; 106:1833-1841. doi: 10. 1038/bjc. 2012. 177 PMID: 22617157
17. Oladipo O, Conlon S, O'Grady A, Purcell C, Wilson C, Maxwell PJ, et al. The expression and prognostic impact of CXC-chemokines in stage II and III colorectal cancer epithelial and stromal tissue. Br J Cancer. 2011; 104:480-487. doi: 10. 1038/sj. bjc. 6606055 PMID: 21285972
18. Dong YL, Kabir SM, Lee ES, Son DS. CXCR2-driven ovarian cancer progression involves upregulation of proinflammatory chemokines by potentiating NF-kappaB activation via EGFR-transactivated Akt signaling. PLoS One. 2013; 8:e83789. doi: 10. 1371/journal. pone. 0083789 PMID: 24376747
19. Yu D, Wolf JK, Scanlon M, Price JE, Hung MC. Enhanced c-erbB-2/neu expression in human ovarian cancer cells correlates with more severe malignancy that can be suppressed by E1A. Cancer Res. 1993; 53:891-898. PMID: 8094034
20. Bobbs AS, Cole JM, Cowden Dahl KD. Emerging and Evolving Ovarian Cancer Animal Models. Cancer Growth Metastasis. 2015; 8:29-3621. doi: 10. 4137/CGM. S21221 PMID: 26380555
21. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010; 8:e1000412. doi: 10. 1371/journal. pbio. 1000412 PMID: 20613859
22. Yeung TL, Leung CS, Wong KK, Samimi G, Thompson MS, Liu J, et al. TGF-beta modulates ovarian cancer invasion by upregulating CAF-derived versican in the tumor microenvironment. Cancer Res. 2013; 73:5016-5028. doi: 10. 1158/0008-5472. CAN-13-0023 PMID: 23824740
23. Capes-Davis A, Theodosopoulos G, Atkin I, Drexler HG, Kohara A, MacLeod RA, et al. Check your cultures! A list of cross-contaminated or misidentified cell lines. Int J Cancer. 2010; 127:1-8. doi: 10. 1002/ijc. 25242 PMID: 20143388
24. Perez-Llamas C, Lopez-Bigas N. Gitools: analysis and visualisation of genomic data using interactive heat-maps. PLoS One. 2011; 6:e19541. doi: 10. 1371/journal. pone. 0019541 PMID: 21602921
25. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol. 2010; 177: 1053-1064. doi: 10. 2353/ajpath. 2010. 100105 PMID: 20651229
26. Sale S, Orsulic S. Models of ovarian cancer metastasis: Murine models. Drug Discov Today Dis Models. 2006; 3:149-154. doi: 10. 1016/j. ddmod. 2006. 05. 006 PMID: 19337569
27. Bolitho C, Hahn MA, Baxter RC, Marsh DJ. The chemokine CXCL1 induces proliferation in epithelial ovarian cancer cells by transactivation of the epidermal growth factor receptor. Endocr Relat Cancer. 2010; 17:929-940. doi: 10. 1677/ERC-10-0107 PMID: 20702723
28. Baumgarten SC, Frasor J. Minireview: Inflammation: an instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol Endocrinol. 2012; 26:360-371. doi: 10. 1210/me. 2011-1302 PMID: 22301780
29. Wiley HE, Gonzalez EB, Maki W, Wu MT, Hwang ST. Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J Natl Cancer Inst. 2001; 93:1638-1643. doi: 10. 1093/jnci/93. 21. 1638 PMID: 11698568
30. Murakami T, Maki W, Cardones AR, Fang H, Tun Kyi A, Nestle FO, et al. Expression of CXC chemokine receptor-4 enhances the pulmonary metastatic potential of murine B16 melanoma cells. Cancer Res. 2002; 62:7328-7334. PMID: 12499276
31. Murakami T, Cardones AR, Finkelstein SE, Restifo NP, Klaunberg BA, Nestle FO, et al. Immune evasion by murine melanoma mediated through CC chemokine receptor-10. J Exp Med. 2003; 198:1337-1347. doi: 10. 1084/jem. 20030593 PMID: 14581607
32. Frick VO, Rubie C, Kolsch K, Wagner M, Ghadjar P, Graeber S, et al. CCR6/CCL20 chemokine expression profile in distinct colorectal malignancies. Scand J Immunol. 2013; 78:298-305. doi: 10. 1111/sji. 12087 PMID: 23790181
33. Vicinus B, Rubie C, Stegmaier N, Frick VO, Kolsch K, Kauffels A, et al. 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. doi: 10. 3892/or. 2013. 2580 PMID: 23817679
34. Roberti MP, Arriaga JM, Bianchini M, Quinta HR, Bravo AI, Levy EA, et al. Protein expression changes during human triple negative breast cancer cell line progression to lymph node metastasis in a xenografted model in nude mice. Cancer Biol. Ther. 2012; 13:1123-1140. doi: 10. 4161/cbt. 21187 PMID: 22825326
35. Kirshberg S, Izhar U, Amir G, Demma J, Vernea F, Beider K, et al. Involvement of CCR6/CCL20/IL-17 axis in NSCLC disease progression. PLoS One. 2011; 6:e24856. doi: 10. 1371/journal. pone. 0024856 PMID: 21949768
36. Rubie C, Frick VO, Wagner M, Weber C, Kruse B, Kempf K, et al. Chemokine expression in hepatocellular carcinoma versus colorectal liver metastases. World J Gastroenterol. 2006; 12:6627-6633. doi: 10. 3748/wjg. v12. i41. 6627 PMID: 17075975
37. Rubie C, Frick VO, Ghadjar P, Wagner M, Grimm H, Vicinus B, et al. CCL20/CCR6 expression profile in pancreatic cancer. J Transl Med. 2010; 8:45. doi: 10. 1186/1479-5876-8-45 PMID: 20459729
38. Chen KJ, Lin SZ, Zhou L, Xie HY, Zhou WH, Takin-Eldin A, et al. Selective recruitment of regulatory T cell through CCR6-CCL20 in hepatocellular carcinoma fosters tumor progression and predicts poor prognosis. PLoS One. 2001; 6:e24671. doi: 10. 1371/journal. pone. 0024671 PMID: 21935436
39. Beider K, Abraham M, Begin M, Wald H, Weiss ID, Wald O, et al. Interaction between CXCR4 and CCL20 pathways regulates tumor growth. PLoS One. 2009; 4:e5125. doi: 10. 1371/journal. pone. 0005125 PMID: 19340288
40. Kim KY, Baek A, Park YS, Park MY, Kim JH, Lim JS, et al. Adipocyte culture medium stimulates invasiveness of MDA-MB-231 cell via CCL20 production. Oncol Rep. 2009; 22:1497-1504. PMID: 19885605
41. Landen CN Jr, Birrer MJ, Sood AK. Early events in the pathogenesis of epithelial ovarian cancer. J Clin Oncol. 2008; 26:995-1005. doi: 10. 1200/JCO. 2006. 07. 9970 PMID: 18195328
42. Siwak DR, Carey M, Hennessy BT, Nguyen CT, McGahren Murray MJ, Nolden L, et al. Targeting the epidermal growth factor receptor in epithelial ovarian cancer: current knowledge and future challenges. J Oncol. 2010; 2010:568938. doi: 10. 1155/2010/568938 PMID: 20037743
43. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer. 2004; 4:540-550. doi: 10. 1038/nrc1388 PMID: 15229479
44. Smale ST. Hierarchies of NF-kappaB target-gene regulation. Nat Immunol. 2011; 12:689-694. doi: 10. 1038/ni. 2070 PMID: 21772277
45. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004; 25:280-288. doi: 10. 1016/j. it. 2004. 03. 008 PMID: 15145317
46. Fujiie S, Hieshima K, Izawa D, Nakayama T, Fujisawa R, Ohyanagi H, et al. Proinflammatory cytokines induce liver and activation-regulated chemokine/macrophage inflammatory protein-3alpha/CCL20 in mucosal epithelial cells through NF-kappaB [correction of NK-kappaB]. Int Immunol. 2001; 13:1255-1263. PMID: 11581170
47. Harant H, Eldershaw SA, Lindley IJ. Human macrophage inflammatory protein-3alpha/CCL20/LARC/Exodus/SCYA20 is transcriptionally upregulated by tumor necrosis factor-alpha via a non-standard NF-kappaB site. FEBS Lett. 2001; 509:439-445. PMID: 11749970
48. Cheadle EJ, Riyad K, Subar D, Rothwell DG, Ashton G, Batha H, et al. Eotaxin-2 and colorectal cancer: a potential target for immune therapy. Clin Cancer Res. 2007; 13:5719-5728. doi: 10. 1158/1078-0432. CCR-07-1145 PMID: 17908961
49. Ben-Yehuda C, Bader R, Puxeddu I, Levi-Schaffer F, Breuer R, Berkman N. Airway eosinophil accumulation and eotaxin-2/CCL24 expression following allergen challenge in BALB/c mice. Exp Lung Res. 2008; 34:467-479. doi: 10. 1080/01902140802220625 PMID: 18850374
50. Menzies-Gow A, Ying S, Sabroe I, Stubbs VL, Soler D, Williams TJ, et al. Eotaxin (CCL11) and eotaxin-2 (CCL24) induce recruitment of eosinophils, basophils, neutrophils, and macrophages as well as features of early-and late-phase allergic reactions following cutaneous injection in human atopic and nonatopic volunteers. J Immunol. 2002; 169:2712-2718. doi: 10. 4049/jimmunol. 169. 5. 2712 PMID: 12193745
51. Anthoni M, Fyhrquist-Vanni N, Wolff H, Alenius H, Lauerma A. Transforming growth factor-beta/Smad3 signalling regulates inflammatory responses in a murine model of contact hypersensitivity. Br J Dermatol. 2008; 159:546-554. doi: 10. 1111/j. 1365-2133. 2008. 08696. x PMID: 18616786
52. Yoshida N, Aizu-Yokota E, Sonoda Y, Moriwaki Y, Kishi K, Kasahara T, et al. Production and regulation of eotaxin-2/CCL24 in a differentiated human leukemic cell line, HT93. Biol Pharm Bull. 2007; 30:1826-1832. doi: 10. 1248/bpb. 30. 1826 PMID: 17917245
53. Schaefer D, Meyer JE, Pods R, Pethe W, Hedderich J, Schmidt C, et al. Endothelial and epithelial expression of eotaxin-2 (CCL24) in nasal polyps. Int Arch Allergy Immunol. 2006; 140:205-214. doi: 10. 1159/000093206 PMID: 16682802