Role of CX3CR1/CX3CL1 axis in primary and secondary involvement of the nervous system by cancer

Journal of Neuroimmunology

Volumn 224, Issue 1-2, 2010, Pages 39-44

  Marchesi, Federica ^a   Locatelli, Marco ^b   Solinas, Graziella ^a   Erreni, Marco ^a   Allavena, Paola ^a   Mantovani, Alberto ^a,c  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Central nervous system; Chemokines; Perineural invasion

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; CHEMOKINE RECEPTOR; CX3CL1 PROTEIN, HUMAN; CX3CR1 PROTEIN, HUMAN;

BRAIN METASTASIS; BREAST CARCINOMA; CANCER INVASION; CANCER RECURRENCE; CELL ADHESION; CELL MIGRATION; CELL TRANSPORT; DISEASE FREE SURVIVAL; ENDOTHELIUM CELL; GLIOBLASTOMA; HUMAN; NATURAL KILLER CELL; NERVE TUMOR; NEUROBLASTOMA; NONHUMAN; OVERALL SURVIVAL; PANCREAS CARCINOMA; PREDICTION; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; TUMOR CELL; ANIMAL; BIOSYNTHESIS; BRAIN TUMOR; CELL COMMUNICATION; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SECONDARY; TUMOR INVASION;

ANIMALS; BRAIN NEOPLASMS; CELL COMMUNICATION; CELL MOVEMENT; CHEMOKINE CX3CL1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM INVASIVENESS; RECEPTORS, CHEMOKINE;

EID: 77955088689     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2010.05.007     Document Type: Review

References (81)

1. Andre F., Cabioglu N., Assi H., Sabourin J.C., Delaloge S., Sahin A., Broglio K., Spano J.P., Combadiere C., Bucana C., Soria J.C., Cristofanilli M. Expression of chemokine receptors predicts the site of metastatic relapse in patients with axillary node positive primary breast cancer. Ann. Oncol. 2006, 17:945-951.
2. Ayala G.E., Wheeler T.M., Shine H.D., Schmelz M., Frolov A., Chakraborty S., Rowley D. In vitro dorsal root ganglia and human prostate cell line interaction: redefining perineural invasion in prostate cancer. Prostate 2001, 49:213-223.
3. Bailey C., Negus R., Morris A., Ziprin P., Goldin R., Allavena P., Peck D., Darzi A. Chemokine expression is associated with the accumulation of tumour associated macrophages (TAMs) and progression in human colorectal cancer. Clin. Exp. Metastasis 2007, 24:121-130.
4. Balentien E., Mufson B.E., Shattuck R.L., Derynck R., Richmond A. Oncogene 1991, 6:1115.
5. Balkwill F. Cancer and the chemokine network. Nat. Rev. Cancer 2004, 4:540-550.
6. Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin. Cancer Biol. 2004, 14:171-179.
7. Balkwill F. Tumour necrosis factor and cancer. Nat. Rev. Cancer 2009, 9:361-371.
8. Bazan J.F., Bacon K.B., Hardiman G., Wang W., Soo K., Rossi D., Greaves D.R., Zlotnik A., Schall T.J. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997, 385:640-644.
9. Boehme S.A., Lio F.M., Maciejewski-Lenoir D., Bacon K.B., Conlon P.J. The chemokine fractalkine inhibits Fas-mediated cell death of brain microglia. J. Immunol. 2000, 165:397-403.
10. Borrello M.G., Alberti L., Fischer A., Degl'innocenti D., Ferrario C., Gariboldi M., Marchesi F., Allavena P., Greco A., Collini P., Pilotti S., Cassinelli G., Bressan P., Fugazzola L., Mantovani A., Pierotti M.A. Induction of a proinflammatory program in normal human thyrocytes by the RET/PTC1 oncogene. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14825-14830.
11. Bottazzi B., Polentarutti N., Acero R., Balsari A., Boraschi D., Ghezzi P., Salmona M., Mantovani A. Regulation of the macrophage content of neoplasms by chemoattractants. Science 1983, 220:210-212.
12. Burger J.A., Kipps T.J. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006, 107:1761-1767.
13. Cabioglu N., Yazici M.S., Arun B., Broglio K.R., Hortobagyi G.N., Price J.E., Sahin A. CCR7 and CXCR4 as novel biomarkers predicting axillary lymph node metastasis in T1 breast cancer. Clin. Cancer Res. 2005, 11:5686-5693.
14. Cardona A.E., Pioro E.P., Sasse M.E., Kostenko V., Cardona S.M., Dijkstra I.M., Huang D., Kidd G., Dombrowski S., Dutta R., Lee J.C., Cook D.N., Jung S., Lira S.A., Littman D.R., Ransohoff R.M. Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 2006, 9:917-924.
15. Ceyhan G.O., et al. Lab. Invest. 2009, 89:347.
16. Chen S., Luo D., Streit W.J., Harrison J.K. TGF-beta1 upregulates CX3CR1 expression and inhibits fractalkine-stimulated signaling in rat microglia. J. Neuroimmunol. 2002, 133:46-55.
17. Cook A., Hippensteel R., Shimizu S., Nicolai J., Fatatis A., Meucci O. Interactions between chemokines: regulation of fractalkine/CX3CL1 homeostasis by SDF/CXCL12 in cortical neurons. J Biol Chem. 2010, 285(14):10563-10571.
18. D'Haese J.G., Demir I.E., Friess H., Ceyhan G.O. Fractalkine/CX3CR1: why a single chemokine-receptor duo bears a major and unique therapeutic potential. Expert Opin Ther Targets 2010, 14:207-219.
19. Dorgham K., Ghadiri A., Hermand P., Rodero M., Poupel L., Iga M., Hartley O., Gorochov G., Combadiere C., Deterre P. An engineered CX3CR1 antagonist endowed with anti-inflammatory activity. J. Leukoc. Biol. 2009, 86(4):903-911.
20. Ehtesham M., Mapara K.Y., Stevenson C.B., Thompson R.C. CXCR4 mediates the proliferation of glioblastoma progenitor cells. Cancer Lett. 2009, 274:305-312.
21. Erichsen D., et al. J. Neuroimmunol. 2003, 138:144.
22. Farrow B., Albo D., Berger D.H. J. Surg. Res. 2008, 149:319.
23. Garton K.J., et al. J. Biol. Chem. 2001, 276:37993.
24. Giavazzi R., Garofalo A., Bani M.R., Abbate M., Ghezzi P., Boraschi D., Mantovani A., Dejana E. Interleukin 1-induced augmentation of experimental metastases from a human melanoma in nude mice. Cancer Res. 1990, 50:4771-4775.
25. Gunther K., Leier J., Henning G., Dimmler A., Weissbach R., Hohenberger W., Forster R. Prediction of lymph node metastasis in colorectal carcinoma by expression of chemokine receptor CCR7. Int. J. Cancer 2005, 116:726-733.
26. Gutwein P., et al. Eur. J. Cancer 2009, 45:478.
27. Haddad R.I., Shin D.M. Recent advances in head and neck cancer. N Engl J. Med. 2008, 359:1143-1154.
28. Harnden P., Shelley M.D., Clements H., Coles B., Tyndale-Biscoe R.S., Naylor B., Mason M.D. The prognostic significance of perineural invasion in prostatic cancer biopsies: a systematic review. Cancer 2007, 109:13-24.
29. Harrison J.K., Jiang Y., Chen S., Xia Y., Maciejewski D., McNamara R.K., Streit W.J., Salafranca M.N., Adhikari S., Thompson D.A., Botti P., Bacon K.B., Feng L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl Acad. Sci. USA 1998, 95:10896-10901.
30. Hatori K., Nagai A., Heisel R., Ryu J.K., Kim S.U. Fractalkine and fractalkine receptors in human neurons and glial cells. J. Neurosci. Res. 2002, 69:418-426.
31. Hong S.K., Kwak C., Jeon H.G., Lee E., Lee S.E. Do vascular, lymphatic, and perineural invasion have prognostic implications for bladder cancer after radical cystectomy?. Urology 2005, 65:697-702.
32. Hughes P.M., Botham M.S., Frentzel S., Mir A., Perry V.H. Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, during acute and chronic inflammation in the rodent CNS. Glia 2002, 37:314-327.
33. Ketterer K., et al. Clin. Cancer Res. 2003, 9:5127.
34. Lagwinski N., Thomas A., Stephenson A.J., Campbell S., Hoschar A.P., El-Gabry E., Dreicer R., Hansel D.E. Squamous cell carcinoma of the bladder: a clinicopathologic analysis of 45 cases. Am. J. Surg. Pathol. 2007, 31:1777-1787.
35. Li A., Varney M.L., Valasek J., Godfrey M., Dave B.J., Singh R.K. Autocrine role of interleukin-8 in induction of endothelial cell proliferation, survival, migration and MMP-2 production and angiogenesis. Angiogenesis 2005, 8:63-71.
36. Liebig C., Ayala G., Wilks J.A., Berger D.H., Albo D. Perineural invasion in cancer: a review of the literature. Cancer 2009, 115:3379-3391.
37. Limatola C., Lauro C., Catalano M., Ciotti M.T., Bertollini C., Di Angelantonio S., Ragozzino D., Eusebi F. Chemokine CX3CL1 protects rat hippocampal neurons against glutamate-mediated excitotoxicity. J. Neuroimmunol. 2005, 166:19-28.
38. Liu B., Lu K.Y. Neural invasion in pancreatic carcinoma. Hepatobiliary Pancreat. Dis. Int. 2002, 1:469-476.
39. Liu C., Luo D., Streit W.J., Harrison J.K. CX3CL1 and CX3CR1 in the GL261 murine model of glioma: CX3CR1 deficiency does not impact tumor growth or infiltration of microglia and lymphocytes. J. Neuroimmunol. 2008, 198:98-105.
40. Locatelli M., Boiocchi L., Ferrero S., Martinelli Boneschi F., Zavanone M., Pesce S., Allavena P., Gaini S.M., Bello L., Mantovani A. Human glioma tumors express high levels of the chemokine receptor CX3CR1. Eur. Cytokine Netw. 2010, 21:27-33.
41. Luboshits G., Shina S., Kaplan O., Engelberg S., Nass D., Lifshitz-Mercer B., Chaitchik S., Keydar I., Ben-Baruch A. Elevated expression of the CC chemokine regulated on activation, normal T cell expressed and secreted (RANTES) in advanced breast carcinoma. Cancer Res. 1999, 59:4681-4687.
42. Maciejewski-Lenoir D., Chen S., Feng L., Maki R., Bacon K.B. Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. J. Immunol. 1999, 163:1628-1635.
43. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
44. Mantovani A., Allavena P., Sozzani S., Vecchi A., Locati M., Sica A. Chemokines in the recruitment and shaping of the leukocyte infiltrate of tumors. Semin. Cancer Biol. 2004, 14:155-160.
45. Mantovani A., Bonecchi R., Locati M. Tuning inflammation and immunity by chemokine sequestration: decoys and more. Nat. Rev. Immunol. 2006, 6:907-918.
46. Mantovani A., Savino B., Locati M., Zammataro L., Allavena P., Bonecchi R. The chemokine system in cancer biology and therapy. Cytokine Growth Factor Rev. 2010, 21(1):27-39.
47. Marchesi F., Monti P., Leone B.E., Zerbi A., Vecchi A., Piemonti L., Mantovani A., Allavena P. Increased survival, proliferation, and migration in metastatic human pancreatic tumor cells expressing functional CXCR4. Cancer Res. 2004, 64:8420-8427.
48. Marchesi F., Piemonti L., Fedele G., Destro A., Roncalli M., Albarello L., Doglioni C., Anselmo A., Doni A., Bianchi P., Laghi L., Malesci A., Cervo L., Malosio M., Reni M., Zerbi A., Di Carlo V., Mantovani A., Allavena P. The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma. Cancer Res. 2008, 68:9060-9069.
49. Marchesi F., Piemonti L., Mantovani A., Allavena P. Molecular mechanisms of perineural invasion, a forgotten pathway of dissemination and metastasis. Cytokine Growth Factor Rev. 2010, 21(1):77-82.
50. Matsubara T., Ono T., Yamanoi A., Tachibana M., Nagasue N. Fractalkine-CX3CR1 axis regulates tumor cell cycle and deteriorates prognosis after radical resection for hepatocellular carcinoma. J. Surg. Oncol. 2007, 95:241-249.
51. Mashino K., et al. Cancer Res. 2002, 62:2937.
52. Mestdagt M., Polette M., Buttice G., Noel A., Ueda A., Foidart J.M., Gilles C. Transactivation of MCP-1/CCL2 by beta-catenin/TCF-4 in human breast cancer cells. Int. J. Cancer 2006, 118:35-42.
53. Meucci O., Fatatis A., Simen A.A., Miller R.J. Expression of CX3CR1 chemokine receptors on neurons and their role in neuronal survival. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8075-8080.
54. Miller R.J., Rostene W., Apartis E., Banisadr G., Biber K., Milligan E.D., White F.A., Zhang J. Chemokine action in the nervous system. J. Neurosci. 2008, 28:11792-11795.
55. Mizuno T., Kawanokuchi J., Numata K., Suzumura A. Production and neuroprotective functions of fractalkine in the central nervous system. Brain Res. 2003, 979:65-70.
56. Moore R.J., Owens D.M., Stamp G., Arnott C., Burke F., East N., Holdsworth H., Turner L., Rollins B., Pasparakis M., Kollias G., Balkwill F. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat. Med. 1999, 5:828-831.
57. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., McClanahan T., Murphy E., Yuan W., Wagner S.N., Barrera J.L., Mohar A., Verastegui E., Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56.
58. Nevo I., Sagi-Assif O., Meshel T., Ben-Baruch A., Johrer K., Greil R., Trejo L.E., Kharenko O., Feinmesser M., Yron I., Witz I.P. The involvement of the fractalkine receptor in the transmigration of neuroblastoma cells through bone-marrow endothelial cells. Cancer Lett. 2009, 273:127-139.
59. Norgauer, Metzner B., Schraufstatter I. J. Immunol. 1996, 156:1132.
60. Ohta M., Tanaka F., Yamaguchi H., Sadanaga N., Inoue H., Mori M. The high expression of Fractalkine results in a better prognosis for colorectal cancer patients. Int. J. Oncol. 2005, 26:41-47.
61. Okada Y., et al. Int. J. Cancer 1999, 81:67.
62. Owen J.D., et al. Int. J. Cancer 1997, 73:94.
63. Pages F., Berger A., Camus M., Sanchez-Cabo F., Costes A., Molidor R., Mlecnik B., Kirilovsky A., Nilsson M., Damotte D., Meatchi T., Bruneval P., Cugnenc P.H., Trajanoski Z., Fridman W.H., Galon J. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J. Med. 2005, 353:2654-2666.
64. Pan Y., Lloyd C., Zhou H., Dolich S., Deeds J., Gonzalo J.A., Vath J., Gosselin M., Ma J., Dussault B., Woolf E., Alperin G., Culpepper J., Gutierrez-Ramos J.C., Gearing D. Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature 1997, 387:611-617.
65. Pour P.M., Bell R.H., Batra S.K. Neural invasion in the staging of pancreatic cancer. Pancreas 2003, 26:322-325.
66. Sciumè G., Soriani A., Piccoli M., Frati L., Santoni A., Bernardini G. CX3CR1/CX3CL1 axis negatively controls glioma cell invasion and is modulated by transforming growth factor-beta1. Neuro-Oncology 2010, 111:3626-3634.
67. Shirai K., et al. World J. Surg. 2008, 32:2395.
68. Shulby S.A., Dolloff N.G., Stearns M.E., Meucci O., Fatatis A. CX3CR1-fractalkine expression regulates cellular mechanisms involved in adhesion, migration, and survival of human prostate cancer cells. Cancer Res. 2004, 64:4693-4698.
69. Soucek L., et al. Nat. Med. 2007, 13:1211. (Oct, 2007).
70. Sparmann A., Bar-Sagi D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 2004, 6:447-458.
71. Strieter R.M., Burdick M.D., Mestas J., Gomperts B., Keane M.P., Belperio J.A. Cancer CXC chemokine networks and tumour angiogenesis. Eur. J. Cancer 2006, 42:768-778.
72. Takamori H., Oades Z.G., Hoch O.C., Burger M., Schraufstatter I.U. Pancreas 2000, 21:52.
73. Takeuchi H., et al. Clin. Cancer Res. 2004, 10:2351.
74. Tsou C.L., Haskell C.A., Charo I.F. J. Biol. Chem. 2001, 276:44622.
75. Ueno T., Toi M., Saji H., Muta M., Bando H., Kuroi K., Koike M., Inadera H., Matsushima K. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin. Cancer Res. 2000, 6:3282-3289.
76. Verge G.M., Milligan E.D., Maier S.F., Watkins L.R., Naeve G.S., Foster A.C. Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur. J. Neurosci. 2004, 20:1150-1160.
77. Vetrano S., Borroni E.M., Sarukhan A., Savino B., Bonecchi R., Correale C., Arena V., Fantini M., Roncalli M., Malesci A., Mantovani A., Locati M., Danese S. The lymphatic system controls intestinal inflammation and inflammation-associated colon cancer through the chemokine decoy receptor D6. Gut. 2010, 59(2):197-206.
78. Wiley H.E., Gonzalez E.B., Maki W., Wu M.T., Hwang S.T. J. Natl. Cancer Inst. 2001, 93:1638.
79. Yan W., Chen X. Identification of GRO1 as a critical determinant for mutant p53 gain of function. J. Biol. Chem. 2009, 284:12178-12187.
80. Zeng Y., Jiang J., Huebener N., Wenkel J., Gaedicke G., Xiang R., Lode H.N. Fractalkine gene therapy for neuroblastoma is more effective in combination with targeted IL-2. Cancer Lett. 2005, 228:187-193.
81. Zujovic V., Benavides J., Vige X., Carter C., Taupin V. Fractalkine modulates TNF-alpha secretion and neurotoxicity induced by microglial activation. Glia 2000, 29:305-315.