CXCL9 induces chemotaxis, chemorepulsion and endothelial barrier disruption through CXCR3-mediated activation of melanoma cells

British Journal of Cancer

Volumn 104, Issue 3, 2011, Pages 469-479

  Amatschek, S ^a   Lucas, R ^b,c   Eger, A ^b   Pflueger, M ^b   Hundsberger, H ^b   Knoll, C ^b   Grosse Kracht, S ^b   Schuett, W ^b   Koszik, F ^a   Maurer, D ^a   Wiesner, C ^a,b  

^a Universitatsklinik fur Dermatologie   (Austria)

^b IMC UNIVERSITY OF APPLIED SCIENCES KREMS   (Austria)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

CXCL9; endothelial monolayer breakdown; fugetaxis; transendothelial migration

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CXCL9 CHEMOKINE;

ARTICLE; CANCER INFILTRATION; CELL CONTACT; CELL CULTURE; CELL DISRUPTION; CELL ISOLATION; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MELANOMA CELL; METASTASIS; PRIORITY JOURNAL;

CHEMOKINE CXCL9; CHEMOTAXIS; HUMANS; MELANOMA; RECEPTORS, CXCR3; SKIN NEOPLASMS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 79551585240     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6606056     Document Type: Article

References (45)

1. Aznavoorian S, Stracke ML, Krutzsch H, Schiffmann E, Liotta LA (1990) Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells. J Cell Biol 110: 1427-1438
2. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 357: 539-545
3. Bissell MJ, Radisky D (2001) Putting tumours in context. Nat Rev Cancer 1: 46-54
4. Charbonnier AS, Kohrgruber N, Kriehuber E, Stingl G, Rot A, Maurer D (1999) Macrophage inflammatory protein 3alpha is involved in the constitutive trafficking of epidermal langerhans cells. J Exp Med 190: 1755-1768
5. Clinton SK, Canto E, O'Donnell MA (2000) Interleukin-12. Opportunities for the treatment of bladder cancer. Urol Clin North Am 27: 147-155.
6. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 7: 57-70.
7. Hashizume H, Baluk P, Morikawa S, McLean JW, Thurston G, Roberge S, Jain RK, McDonald DM (2000) Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 156: 1363-1380
8. Heyder C, Gloria-Maercker E, Entschladen F, Hatzmann W, Niggemann B, Zänker KS, Dittmar T (2002) Realtime visualization of tumor cell/ endothelial cell interactions during transmigration across the endothelial barrier. J Cancer Res Clin Oncol 128: 533-538
9. Kakinuma T, Hwang ST (2006) Chemokines, chemokine receptors, and cancer metastasis. J Leukoc Biol 79: 639-651.
10. Kanegane C, Sgadari C, Kanegane H, Teruya-Feldstein J, Yao L, Gupta G, Farber JM, Liao F, Liu L, Tosato G (1998) Contribution of the CXC chemokines IP-10 and Mig to the antitumor effects of IL-12. J Leukoc Biol 64: 384-392
11. Kawada K, Sonoshita M, Sakashita H, Takabayashi A, Yamaoka Y, Manabe T, Inaba K, Minato N, Oshima M, Taketo MM (2004) Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes. Cancer Res 64: 4010-4017
12. Keeley EC, Mehrad B, Strieter RM (2008) Chemokines as mediators of neovascularization. Arterioscler Thromb Vasc Biol 28: 1928-1936
13. Keilholz U, Eggermont AM (2000) The emerging role of cytokines in the treatment of advanced melanoma. For the EORTC Melanoma Cooperative Group. Oncology 58: 89-95
14. Kriehuber E, Breiteneder-Geleff S, Groeger M, Soleiman A, Schoppmann SF, Stingl G, Kerjaschki D, Maurer D (2001) Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 194: 797-808
15. Kunz M, Toksoy A, Goebeler M, Engelhardt E, Bröcker E, Gillitzer R (1999) Strong expression of the lymphoattractant C-X-C chemokine Mig is associated with heavy infiltration of T cells in human malignant melanoma. J Pathol 189: 552-558
16. Lasagni L, Francalanci M, Annunziato F, Lazzeri E, Giannini S, Cosmi L, Sagrinati C, Mazzinghi B, Orlando C, Maggi E, Marra F, Romagnani S, Serio M, Romagnani P (2003) An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J Exp Med 197: 1537-1549
17. Li A, Varney ML, Singh RK (2001) Expression of interleukin 8 and its receptors in human colon carcinoma cells with different metastatic potentials. Clin Cancer Res 7: 3298-3304
18. Li YH, Zhu C (1999) A modified Boyden chamber assay for tumor cell transendothelial migration in vitro. Clin Exp Metastasis 17: 423-429
19. Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, Clark-Lewis I, Baggiolini M, Moser B (1996) Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J Exp Med 184: 963-969
20. Mehrad B, Keane MP, Strieter RM (2007) Chemokines as mediators of angiogenesis. Thromb Haemost 97: 755-762.
21. Mierke CT, Zitterbart DP, Kollmannsberger P, Raupach C, Schlötzer-Schrehardt U, Goecke TW, Behrens J, Fabry B (2008) Breakdown of the endothelial barrier function in tumor cell transmigration. Biophys J 94: 2832-2846
22. Müller 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 (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410: 50-56
23. Ohtani H (1998) Stromal reaction in cancer tissue: pathophysiologic significance of the expression of matrix-degrading enzymes in relation to matrix turnover and immune/inflammatory reactions. Pathol Int 48: 1-9
24. Payne AS, Cornelius LA (2002) The role of chemokines in melanoma tumor growth and metastasis. J Invest Dermatol 118: 915-922
25. Qi J, Chen N, Wang J, Siu CH (2005) Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the beta-catenin signaling pathway. Mol Biol Cell 16: 4386-4397
26. Raman D, Baugher PJ, Thu YM, Richmond A (2007) Role of chemokines in tumor growth. Cancer Lett 256: 137-165
27. Ramjeesingh R, Leung R, Siu CH (2003) Interleukin-8 secreted by endothelial cells induces chemotaxis of melanoma cells through the chemokine receptor CXCR1. FASEB J 17: 1292-1294
28. Robledo MM, Bartolome RA, Longo N, Rodríguez-Frade JM, Mellado M, Longo I, van Muijen GN, Sánchez-Mateos P, Teixidó J (2001) Expression of functional chemokine receptors CXCR3 and CXCR4 on human melanoma cells. J Biol Chem 276: 45098-45105
29. Rodolfo M, Colombo MP (1999) Interleukin-12 as an adjuvant for cancer immunotherapy. Methods 19: 114-120.
30. Rollins BJ (1997) Chemokines. Blood 90: 909-928
31. Romagnani P, Annunziato F, Lazzeri E, Cosmi L, Beltrame C, Lasagni L, Galli G, Francalanci M, Manetti R, Marra F, Vanini V, Maggi E, Romangnani S (2001a) Cell cycle-dependent expression of CXC chemokine receptor 3 by endothelial cells mediates angiostatic activity. J Clin Invest 107: 53-63
32. Romagnani P, Annunziato F, Lasagni L, Lazzeri E, Beltrame C, Francalanci M, Uguccioni M, Galli G, Cosmi L, Maurenzig L, Baggiolini M, Maggi E, Romagnani S, Serio M (2001b) Interferon-inducible protein 10, monokine induced by interferon gamma, and interferon-inducible T-cell alpha chemoattractant are produced by thymic epithelial cells and attract T-cell receptor (TCR) alphabeta+ CD8+ single-positive T cells, TCRgammadelta+. Blood 97: 601-607
33. Sandig M, Voura EB, Kalnins VI, Siu CH (1997) Role of cadherins in the transendothelial migration of melanoma cells in culture. Cell Motil Cytoskeleton 38: 351-364
34. Sgadari C, Farber JM, Angiolillo AL, Liao F, Teruya-Feldstein J, Burd PR, Yao L, Gupta G, Kanegane C, Tosato G (1997) Mig, the monokine induced by interferon-gamma, promotes tumor necrosis in vivo. Blood 89: 2635-2643
35. Shepherd J, Milne R (2000) Interferon alfa in the treatment of metastatic melanoma. Annu Meet Int Soc Tech Assess Health Care Meet 16: 073
36. Simiantonaki N, Jayasinghe C, Kirkpatrick CJ (2002) Effect of proinflammatory stimuli on tumor cell-mediated induction of endothelial cell adhesion molecules in vitro. Exp Mol Pathol 73: 46-53
37. Stewart PA, Hayakawa K, Farrell CL, Del Maestro RF (1987) Quantitative study of microvessel ultrastructure in human peritumoral brain tissue. Evidence for a blood-brain barrier defect. J Neurosurg 67: 697-705
38. Vianello F, Olszak IT, Poznansky MC (2005) Fugetaxis: active movement of leukocytes away from a chemokinetic agent. J Mol Med 83: 752-763
39. Vianello F, Papeta N, Chen T, Kraft P, White N, Hart WK, Kircher MF, Swart E, Rhee S, Palù G, Irimia D, Toner M, Weissleder R, Poznansky MC (2006) Murine B16 melanomas expressing high levels of the chemokine stromal-derived factor-1/CXCL12 induce tumor-specific T cell chemorepulsion and escape from immune control. J Immunol 176: 2902-2914
40. Voura EB, Ramjeesingh RA, Montgomery AM, Siu CH (2001) Involvement of integrin alpha(v)beta(3) and cell adhesion molecule L1 in transendothelial migration of melanoma cells. Mol Biol Cell 12: 2699-2710
41. Voura EB, Sandig M, Siu C-H (1998) Cell-cell interactions during transendothelial migration of tumor cells. Microsc Res Tech 43: 265-275.
42. Wang JM, Deng X, Gong W, Su S (1998) Chemokines and their role in tumor growth and metastasis. J Immunol Methods 220: 1-17
43. Wegener J, Keese CR, Giaever I (2000) Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp Cell Res 259: 158-166
44. Weis S, Cui J, Barnes L, Cheresh D (2004) Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J Cell Biol 25: 223-229
45. Wiley HE, Gonzalez EB, Maki W, Wu MT, Hwang ST (2001) Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J Natl Cancer Inst 93: 1638-1643