The atypical chemokine receptor CCX-CKR regulates metastasis of mammary carcinoma via an effect on EMT

Immunology and Cell Biology

Volumn 92, Issue 10, 2014, Pages 815-824

  Harata Lee, Yuka ^a   Turvey, Michelle E ^a   Brazzatti, Julie A ^a,e   Gregor, Carly E ^a   Brown, Michael P ^b   Smyth, Mark J ^c,d   Comerford, Iain ^a   McColl, Shaun R ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b An alliance between SA Pathology and the University of South Australia   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCX CKR; MESSENGER RNA; PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; CCRL1 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CCR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL MODEL; ANOIKIS; ARTICLE; AUTOCRINE EFFECT; BREAST CARCINOMA; BREAST METASTASIS; CARCINOGENICITY; CARCINOMA CELL; CELL ADHESION; CELL GROWTH; CELL INVASION; CELL MOTILITY; CONTROLLED STUDY; CORRELATIONAL STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FEMALE; GROWTH INHIBITION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; CARCINOMA; EXPERIMENTAL MAMMARY NEOPLASM; GENETICS; HOMEOSTASIS; METABOLISM; METASTASIS; PATHOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; CARCINOMA; CHEMOKINES; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HOMEOSTASIS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; NEOPLASM METASTASIS; RECEPTORS, CCR; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84927570596     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2014.58     Document Type: Article

References (55)

1. Gale LM, McColl SR. Chemokines: extracellular messengers for all occasions? Bioessays 1999; 21: 17-28.
2. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000; 18: 217-242.
3. Thelen M. Dancing to the tune of chemokines. Nat Immunol 2001; 2: 129-134.
4. Balkwill FR. The chemokine system and cancer. J Pathol 2012; 226: 148-157.
5. 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.
6. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001; 410: 50-56.
7. Kochetkova M, Kumar S, McColl SR. Chemokine receptors CXCR4 and CCR7 promote metastasis by preventing anoikis in cancer cells. Cell Death Differ 2009; 16: 664-673.
8. Correale P, Rotundo MS, Botta C, Del Vecchio MT, Ginanneschi C, Licchetta A et al. Tumor infiltration by T lymphocytes expressing chemokine receptor 7 (CCR7) is predictive of favorable outcome in patients with advanced colorectal carcinoma. Clin Cancer Res 2012; 18: 850-857.
9. Middel P, Brauneck S, Meyer W, Radzun HJ. Chemokine-mediated distribution of dendritic cell subsets in renal cell carcinoma. BMC Cancer 2010; 10: 578.
10. Kirk CJ, Hartigan-O'Connor D, Nickoloff BJ, Chamberlain JS, Giedlin M, Aukerman L et al. T cell-dependent antitumor immunity mediated by secondary lymphoid tissue chemokine: augmentation of dendritic cell-based immunotherapy. Cancer Res 2001; 61: 2062-2070.
11. Sharma S, Stolina M, Luo J, Strieter RM, Burdick M, Zhu LX et al. Secondary lymphoid tissue chemokine mediates T cell-dependent antitumor responses in vivo. J Immunol 2000; 164: 4558-4563.
12. Hillinger S, Yang SC, Zhu L, Huang M, Duckett R, Atianzar K et al. EBV-induced molecule 1 ligand chemokine (ELC/CCL19) promotes IFN-gamma-dependent antitumor responses in a lung cancer model. J Immunol 2003; 171: 6457-6465.
13. Comerford I, Litchfield W, Harata-Lee Y, Nibbs RJ, McColl SR. Regulation of chemotactic networks by 'atypical' receptors. Bioessays 2007; 29: 237-247.
14. Gosling J, Dairaghi DJ, Wang Y, Hanley M, Talbot D, Miao Z et al. Cutting edge: identification of a novel chemokine receptor that binds dendritic cell-and T cell-active chemokines including ELC, SLC, and TECK. J Immunol 2000; 164: 2851-2856.
15. Townson JR, Nibbs RJ. Characterization of mouse CCX-CKR, a receptor for the lymphocyte-attracting chemokines TECK/mCCL25, SLC/mCCL21 and MIP-3beta/mCCL19: comparison to human CCX-CKR. Eur J Immunol 2002; 32: 1230-1241.
16. Comerford I, Milasta S, Morrow V, Milligan G, Nibbs R. The chemokine receptor CCX-CKR mediates effective scavenging of CCL19 in vitro. Eur J Immunol 2006; 36: 1904-1916.
17. Bunting MD, Comerford I, Seach N, Hammett MV, Asquith DL, Körner H et al. CCX-CKR deficiency alters thymic stroma impairing thymocyte development and promoting autoimmunity. Blood 2013; 121: 118-128.
18. Comerford I, Nibbs RJ, Litchfield W, Bunting M, Harata-Lee Y, Haylock-Jacobs S et al. The atypical chemokine receptor CCX-CKR scavenges homeostatic chemokines in circulation and tissues and suppresses Th17 responses. Blood 2010; 116: 4130-4140.
19. Feng LY, Ou ZL, Wu FY, Shen ZZ, Shao ZM. Involvement of a novel chemokine decoy receptor CCX-CKR in breast cancer growth, metastasis and patient survival. Clin Cancer Res 2009; 15: 2962-2970.
20. Oft M, Heider KH, Beug H. TGFbeta signaling is necessary for carcinoma cell invasiveness and metastasis. Curr Biol 1998; 8: 1243-1252.
21. Derynck R, Akhurst RJ. Differentiation plasticity regulated by TGF-beta family proteins in development and disease. Nat Cell Biol 2007; 9: 1000-1004.
22. Tian F, Byfield SD, Parks WT, Stuelten CH, Nemani D, Zhang YE et al. Smad-binding defective mutant of transforming growth factor beta type I receptor enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res 2004; 64: 4523-4530.
23. Tian F, DaCosta Byfield S, Parks WT, Yoo S, Felici A, Tang B et al. Reduction in Smad2/3 signaling enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res 2003; 63: 8284-8292.
24. Kasai H, Allen JT, Mason RM, Kamimura T, Zhang Z. TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res 2005; 6: 56.
25. Nawshad A, Lagamba D, Polad A, Hay ED. Transforming growth factor-beta signaling during epithelial-mesenchymal transformation: implications for embryogenesis and tumor metastasis. Cells Tissues Organs 2005; 179: 11-23.
26. Williams SA, Harata-Lee Y, Comerford I, Anderson RL, Smyth MJ, McColl SR. Multiple functions of CXCL12 in a syngeneic model of breast cancer. Mol Cancer 2010; 9: 250.
27. Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, Denoyer D et al. Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci USA 2010; 107: 1547-1552.
28. Campbell SE, Katwa LC. Angiotensin II stimulated expression of transforming growth factor-beta1 in cardiac fibroblasts and myofibroblasts. J Mol Cell Cardiol 1997; 29: 1947-1958.
29. Kagami S, Border WA, Miller DE, Noble NA. Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest 1994; 93: 2431-2437.
30. Habashi JP, Doyle JJ, Holm TM, Aziz H, Schoenhoff F, Bedja D et al. Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science 2011; 332: 361-365.
31. Hunyady L, Catt KJ. Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol Endocrinol 2006; 20: 953-970.
32. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 2007; 292: C82-C97.
33. Lindsay ME, Dietz HC. Lessons on the pathogenesis of aneurysm from heritable conditions. Nature 2011; 473: 308-316.
34. Heinzel K, Benz C, Bleul CC. A silent chemokine receptor regulates steady-state leukocyte homing in vivo. Proc Natl Acad Sci USA 2007; 104: 8421-8426.
35. Watts AO, Verkaar F, van der Lee MM, Timmerman CA, Kuijer M, van Offenbeek J et al. beta-Arrestin recruitment and G protein signaling by the atypical human chemokine decoy receptor CCX-CKR. J Biol Chem 2013; 288: 7169-7181.
36. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S et al. Control of chemokine-guided cell migration by ligand sequestration. Cell 2008; 132: 463-473.
37. Burns JM, Summers BC, Wang Y, Melikian A, Berahovich R, Miao Z et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 2006; 203: 2201-2213.
38. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009; 113: 6085-6093.
39. Wang J, Shiozawa Y, Wang J, Wang Y, Jung Y, Pienta KJ et al. The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem 2008; 283: 4283-4294.
40. Rajagopal S, Kim J, Ahn S, Craig S, Lam CM, Gerard NP et al. Beta-arrestin-but not G protein-mediated signaling by the 'decoy' receptor CXCR7. Proc Natl Acad Sci USA 2010; 107: 628-632.
41. Akekawatchai C, Holland JD, Kochetkova M, Wallace JC, McColl SR. Transactivation of CXCR4 by the insulin-like growth factor-1 receptor (IGF-1R) in human MDA-MB-231 breast cancer epithelial cells. J Biol Chem 2005; 280: 39701-39708.
42. Connolly EC, Freimuth J, Akhurst RJ. Complexities of TGF-beta targeted cancer therapy. Int J Biol Sci 2012; 8: 964-978.
43. Massague J. TGFbeta in Cancer. Cell 2008; 134: 215-230.
44. Chen CR, Kang Y, Siegel PM, Massague J. E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 2002; 110: 19-32.
45. Gomis RR, Alarcon C, Nadal C, Van Poznak C, Massague J. C/EBPbeta at the core of the TGFbeta cytostatic response and its evasion in metastatic breast cancer cells. Cancer Cell 2006; 10: 203-214.
46. Sorrentino A, Thakur N, Grimsby S, Marcusson A, von Bulow V, Schuster N et al. The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinaseindependent manner. Nat Cell Biol 2008; 10: 1199-1207.
47. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE. TRAF6 mediates Smadindependent activation of JNK and p38 by TGF-beta. Mol Cell 2008; 31: 918-924.
48. Tremain R, Marko M, Kinnimulki V, Ueno H, Bottinger E, Glick A. Defects in TGF-beta signaling overcome senescence of mouse keratinocytes expressing v-Ha-ras. Oncogene 2000; 19: 1698-1709.
49. Vijayachandra K, Lee J, Glick AB. Smad3 regulates senescence and malignant conversion in a mouse multistage skin carcinogenesis model. Cancer Res 2003; 63: 3447-3452.
50. Boulanger CA, Wagner KU, Smith GH. Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression. Oncogene 2005; 24: 552-560.
51. Han G, Lu SL, Li AG, He W, Corless CL, Kulesz-Martin M et al. Distinct mechanisms of TGF-beta1-mediated epithelial-to-mesenchymal transition and metastasis during skin carcinogenesis. J Clin Invest 2005; 115: 1714-1723.
52. Muraoka RS, Koh Y, Roebuck LR, Sanders ME, Brantley-Sieders D, Gorska AE et al. Increased malignancy of Neu-induced mammary tumors overexpressing active transforming growth factor beta1. Mol Cell Biol 2003; 23: 8691-8703.
53. Weeks BH, He W, Olson KL, Wang XJ. Inducible expression of transforming growth factor beta1 in papillomas causes rapid metastasis. Cancer Res 2001; 61: 7435-7443.
54. Lelekakis M, Moseley JM, Martin TJ, Hards D, Williams E, Ho P et al. A novel orthotopic model of breast cancer metastasis to bone. Clin Exp Metastasis 1999; 17: 163-170.
55. Brazzatti JA, Klingler-Hoffmann M, Haylock-Jacobs S, Harata-Lee Y, Niu M, Higgins MD et al. Differential roles for the p101 and p84 regulatory subunits of PI3Kgamma in tumor growth and metastasis. Oncogene 2012; 31: 2350-2361.