The fractalkine-receptor axis improves human colorectal cancer prognosis by limiting tumor metastatic dissemination

Journal of Immunology

Volumn 196, Issue 2, 2016, Pages 902-914

  Erreni, Marco ^a   Siddiqui, Imran ^a   Marelli, Giulia ^a   Grizzi, Fabio ^a   Bianchi, Paolo ^a   Morone, Diego ^a,b   Marchesi, Federica ^a   Celesti, Giuseppe ^a   Pesce, Samantha ^a   Doni, Andrea ^a   Rumio, Cristiano ^b   Roncalli, Massimo G ^a,c   Laghi, Luigi ^a   Mantovani, Alberto ^a,c   Allavena, Paola ^a  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c HUMANITAS UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

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

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PROGNOSIS; CANCER STAGING; CD3+ T LYMPHOCYTE; CELL AGGREGATION; CELL MIGRATION; CHEMOTAXIS ASSAY; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DISEASE SPECIFIC SURVIVAL; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; MACROPHAGE; MALE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SPLEEN CANCER; UPREGULATION; ANIMAL; BIOSYNTHESIS; COLORECTAL TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; KAPLAN MEIER METHOD; METABOLISM; MORTALITY; NUDE MOUSE; PATHOLOGY; POLYMERASE CHAIN REACTION; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR INVASION;

ANIMALS; CHEMOKINE CX3CL1; COLORECTAL NEOPLASMS; DISEASE-FREE SURVIVAL; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; POLYMERASE CHAIN REACTION; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; RECEPTORS, CHEMOKINE; TRANSCRIPTOME;

EID: 84954124515     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501335     Document Type: Article

References (59)

1. Sadanandam, A., C. A. Lyssiotis, K. Homicsko, E. A. Collisson, W. J. Gibb, S. Wullschleger, L. C. Ostos, W. A. Lannon, C. Grotzinger, M. Del Rio, et al. 2013. A colorectal cancer classification system that associates cellular phenotype and responses to therapy. Nat. Med. 19: 619-625.
2. Celesti, G., G. Di Caro, P. Bianchi, F. Grizzi, G. Basso, F. Marchesi, A. Doni, G. Marra, M. Roncalli, A. Mantovani, A. Malesci, and L. Laghi. 2013. Presence of Twist1-positive neoplastic cells in the stroma of chromosome-unstable colorectal tumors. Gastroenterology 145: 647-657.e15.doi:10.1053/j.gastro.2013.05.011
3. Grivennikov, S. I., K. Wang, D. Mucida, C. A. Stewart, B. Schnabl, D. Jauch, K. Taniguchi, G. Y. Yu, C. H. Osterreicher, K. E. Hung, et al. 2012. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491: 254-258.
4. Jobin, C. 2013. Colorectal cancer: looking for answers in the microbiota. Cancer Discov. 3: 384-387.
5. Zambetti, L. P., and A. Mortellaro. 2014. NLRPs, microbiota, and gut homeo-stasis: unravelling the connection. J. Pathol. 233: 321-330.
6. Coussens, L. M., and Z. Werb. 2002. Inflammation and cancer. Nature 420: 860-867.
7. Mantovani, A., P. Allavena, A. Sica, and F. Balkwill. 2008. Cancer-related inflammation. Nature 454: 436-444.
8. Thun, M. J., E. J. Jacobs, and C. Patrono. 2012. The role of aspirin in cancer prevention. Nat. Rev. Clin. Oncol. 9: 259-267.
9. Grivennikov, S., E. Karin, J. Terzic, D. Mucida, G. Y. Yu, S. Vallabhapurapu, J. Scheller, S. Rose-John, H. Cheroutre, L. Eckmann, and M. Karin. 2009. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15: 103-113.
10. Zaki, M. H., P. Vogel, R. K. Malireddi, M. Body-Malapel, P. K. Anand, J. Bertin, D. R. Green, M. Lamkanfi, and T. D. Kanneganti. 2011. The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell 20: 649-660.
11. Canna, K., P. A. McArdle, D. C. McMillan, A. M. McNicol, G. W. Smith, R. F. McKee, and C. S. McArdle. 2005. The relationship between tumour T-lymphocyte infiltration, the systemic inflammatory response and survival in patients undergoing curative resection for colorectal cancer. Br. J. Cancer 92: 651-654.
12. Laghi, L., P. Bianchi, E. Miranda, E. Balladore, V. Pacetti, F. Grizzi, P. Allavena, V. Torri, A. Repici, A. Santoro, et al. 2009. CD3+ cells at the invasive margin of deeply invading (pT3-T4) colorectal cancer and risk of post-surgical metastasis: a longitudinal study. Lancet Oncol. 10: 877-884.
13. Nosho, K., Y. Baba, N. Tanaka, K. Shima, M. Hayashi, J. A. Meyerhardt, E. Giovannucci, G. Dranoff, C. S. Fuchs, and S. Ogino. 2010. Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J. Pathol. 222: 350-366.
14. Bindea, G., B. Mlecnik, M. Tosolini, A. Kirilovsky, M. Waldner, A. C. Obenauf, H. Angell, T. Fredriksen, L. Lafontaine, A. Berger, et al. 2013. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 39: 782-795.
15. Erreni, M., P. Bianchi, L. Laghi, M. Mirolo, M. Fabbri, M. Locati, A. Mantovani, and P. Allavena. 2009. Expression of chemokines and chemokine receptors in human colon cancer. Methods Enzymol. 460: 105-121.
16. Bazan, J. F., K. B. Bacon, G. Hardiman, W. Wang, K. Soo, D. Rossi, D. R. Greaves, A. Zlotnik, and T. J. Schall. 1997. A new class of membrane-bound chemokine with a CX3C motif. Nature 385: 640-644.
17. Garton, K. J., P. J. Gough, C. P. Blobel, G. Murphy, D. R. Greaves, P. J. Dempsey, and E. W. Raines. 2001. Tumor necrosis factor-alpha-converting enzyme (ADAM17) mediates the cleavage and shedding of fractalkine (CX3CL1). J. Biol. Chem. 276: 37993-38001.
18. Muehlhoefer, A., L. J. Saubermann, X. Gu, K. Luedtke-Heckenkamp, R. Xavier, R. S. Blumberg, D. K. Podolsky, R. P. MacDermott, and H. C. Reinecker. 2000. Fractalkine is an epithelial and endothelial cell-derived chemoattractant for intraepithelial lymphocytes in the small intestinal mucosa. J. Immunol. 164: 3368-3376.
19. D'Haese, J. G., I. E. Demir, H. Friess, and G. O. Ceyhan. 2010. Fractalkine/CX3CR1: why a single chemokine-receptor duo bears a major and unique therapeutic potential. Expert Opin. Ther. Targets 14: 207-219.
20. Jamieson, W. L., S. Shimizu, J. A. D'Ambrosio, O. Meucci, and A. Fatatis. 2008. CX3CR1 is expressed by prostate epithelial cells and androgens regulate the levels of CX3CL1/fractalkine in the bone marrow: potential role in prostate cancer bone tropism. Cancer Res. 68: 1715-1722.
21. Marchesi, F., L. Piemonti, G. Fedele, A. Destro, M. Roncalli, L. Albarello, C. Doglioni, A. Anselmo, A. Doni, P. Bianchi, et al. 2008. The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma. Cancer Res. 68: 9060-9069.
22. Erreni, M., G. Solinas, P. Brescia, D. Osti, F. Zunino, P. Colombo, A. Destro, M. Roncalli, A. Mantovani, R. Draghi, et al. 2010. Human glioblastoma tumours and neural cancer stem cells express the chemokine CX3CL1 and its receptor CX3CR1. Eur. J. Cancer 46: 3383-3392.
23. Celesti, G., G. Di Caro, P. Bianchi, F. Grizzi, F. Marchesi, G. Basso, D. Rahal, G. Delconte, M. Catalano, P. Cappello, et al. 2013. Early expression of the fractalkine receptor CX3CR1 in pancreatic carcinogenesis. Br. J. Cancer 109: 2424-2433.
24. Wei, L. M., S. Cao, W. D. Yu, Y. L. Liu, and J. T. Wang. 2015. Overexpression of CX3CR1 is associated with cellular metastasis, proliferation and survival in gastric cancer. Oncol. Rep. 33: 615-624.
25. Lavergne, E., B. Combadière, O. Bonduelle, M. Iga, J. L. Gao, M. Maho, A. Boissonnas, P. M. Murphy, P. Debré, and C. Combadière. 2003. Fractalkine mediates natural killer-dependent antitumor responses in vivo. Cancer Res. 63: 7468-7474.
26. Ohta, M., F. Tanaka, H. Yamaguchi, N. Sadanaga, H. Inoue, and M. Mori. 2005. The high expression of Fractalkine results in a better prognosis for colorectal cancer patients. Int. J. Oncol. 26: 41-47.
27. Sciumè, G., A. Soriani, M. Piccoli, L. Frati, A. Santoni, and G. Bernardini. 2010. CX3CR1/CX3CL1 axis negatively controls glioma cell invasion and is modulated by transforming growth factor-b1. Neuro-oncol. 12: 701-710.
28. Galon, J., A. Costes, F. Sanchez-Cabo, A. Kirilovsky, B. Mlecnik, C. Lagorce-Pagès, M. Tosolini, M. Camus, A. Berger, P. Wind, et al. 2006. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964.
29. Ladoire, S., F. Martin, and F. Ghiringhelli. 2011. Prognostic role of FOXP3+ regulatory T cells infiltrating human carcinomas: the paradox of colorectal cancer. Cancer Immunol. Immunother. 60: 909-918.
30. Goda, S., T. Imai, O. Yoshie, O. Yoneda, H. Inoue, Y. Nagano, T. Okazaki, H. Imai, E. T. Bloom, N. Domae, and H. Umehara. 2000. CX3C-chemokine, fractalkine-enhanced adhesion of THP-1 cells to endothelial cells through integrin-dependent and-independent mechanisms. J. Immunol. 164: 4313-4320.
31. Lauro, C., M. Catalano, F. Trettel, F. Mainiero, M. T. Ciotti, F. Eusebi, and C. Limatola. 2006. The chemokine CX3CL1 reduces migration and increases adhesion of neurons with mechanisms dependent on the beta1 integrin subunit. J. Immunol. 177: 7599-7606.
32. Tardáguila, M., E. Mira, M. A. García-Cabezas, A. M. Feijoo, M. Quintela-Fandino, I. Azcoitia, S. A. Lira, and S. Man-es. 2013. CX3CL1 promotes breast cancer via transactivation of the EGF pathway. Cancer Res. 73: 4461-4473.
33. Digman, M. A., V. R. Caiolfa, M. Zamai, and E. Gratton. 2008. The phasor approach to fluorescence lifetime imaging analysis. Biophys. J. 94: L14-L16.
34. Lucas, A. D., N. Chadwick, B. F. Warren, D. P. Jewell, S. Gordon, F. Powrie, and D. R. Greaves. 2001. The transmembrane form of the CX3CL1 chemokine fractalkine is expressed predominantly by epithelial cells in vivo. Am. J. Pathol. 158: 855-866.
35. Shang, L., N. Thirunarayanan, A. Viejo-Borbolla, A. P. Martin, M. Bogunovic, F. Marchesi, J. C. Unkeless, Y. Ho, G. C. Furtado, A. Alcami, et al. 2009. Expression of the chemokine binding protein M3 promotes marked changes in the accumulation of specific leukocytes subsets within the intestine. Gastroenter-ology 137: 1006-1018, 1018.e1-3. doi:10.1053/j.gastro.2009.05.055
36. Trinchieri, G. 2014. Critical role for CX3CR1? mononuclear phagocytes in intestinal homeostasis. J. Exp. Med. 211: 1500-1501.
37. Tsou, C. L., C. A. Haskell, and I. F. Charo. 2001. Tumor necrosis factor-alpha-converting enzyme mediates the inducible cleavage of fractalkine. J. Biol. Chem. 276: 44622-44626.
38. Calon, A., E. Espinet, S. Palomo-Ponce, D. V. Tauriello, M. Iglesias, M. V. Céspedes, M. Sevillano, C. Nadal, P. Jung, X. H. Zhang, et al. 2012. Dependency of colorectal cancer on a TGF-b-driven program in stromal cells for metastasis initiation. Cancer Cell 22: 571-584.
39. McCulloch, D. R., M. Harvey, and A. C. Herington. 2000. The expression of the ADAMs proteases in prostate cancer cell lines and their regulation by dihy-drotestosterone. Mol. Cell. Endocrinol. 167: 11-21.
40. Vitale, S., B. Cambien, B. F. Karimdjee, R. Barthel, P. Staccini, C. Luci, V. Breittmayer, F. Anjuère, A. Schmid-Alliana, and H. Schmid-Antomarchi. 2007. Tissue-specific differential antitumour effect of molecular forms of frac-talkine in a mouse model of metastatic colon cancer. Gut 56: 365-372.
41. Ostuni, M. A., J. Guellec, P. Hermand, P. Durand, C. Combadière, F. Pincet, and P. Deterre. 2014. CX3CL1, a chemokine finely tuned to adhesion: critical roles of the stalk glycosylation and the membrane domain. Biol. Open 3: 1173-1182.
42. Hyakudomi, M., T. Matsubara, R. Hyakudomi, T. Yamamoto, S. Kinugasa, A. Yamanoi, R. Maruyama, and T. Tanaka. 2008. Increased expression of frac-talkine is correlated with a better prognosis and an increased number of both CD8+ T cells and natural killer cells in gastric adenocarcinoma. Ann. Surg. Oncol. 15: 1775-1782.
43. Park, M. H., J. S. Lee, and J. H. Yoon. 2012. High expression of CX3CL1 by tumor cells correlates with a good prognosis and increased tumor-infiltrating CD8+ T cells, natural killer cells, and dendritic cells in breast carcinoma. J. Surg. Oncol. 106: 386-392.
44. Mlecnik, B., M. Tosolini, P. Charoentong, A. Kirilovsky, G. Bindea, A. Berger, M. Camus, M. Gillard, P. Bruneval, W. H. Fridman, et al. 2010. Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology 138: 1429-1440.
45. Halama, N., S. Michel, M. Kloor, I. Zoernig, A. Benner, A. Spille, T. Pommerencke, D. M. von Knebel, G. Folprecht, B. Luber, et al. 2011. Localization and density of immune cells in the invasive margin of human colo-rectal cancer liver metastases are prognostic for response to chemotherapy. Cancer Res. 71: 5670-5677.
46. Zheng, J., M. Yang, J. Shao, Y. Miao, J. Han, and J. Du. 2013. Chemokine receptor CX3CR1 contributes to macrophage survival in tumor metastasis. Mol. Cancer 12: 141.
47. Xiao, L. J., Y. Y. Chen, P. Lin, H. F. Zou, F. Lin, L. N. Zhao, D. Li, L. Guo, J. B. Tang, X. L. Zheng, and X. G. Yu. 2012. Hypoxia increases CX3CR1 expression via HIF-1 and NF-kB in androgen-independent prostate cancer cells. Int. J. Oncol. 41: 1827-1836.
48. Zhao, T., S. Gao, X. Wang, J. Liu, Y. Duan, Z. Yuan, J. Sheng, S. Li, F. Wang, M. Yu, et al. 2012. Hypoxia-inducible factor-1a regulates chemotactic migration of pancreatic ductal adenocarcinoma cells through directly transactivating the CX3CR1 gene. PLoS One 7: e43399.
49. Matsubara, T., T. Ono, A. Yamanoi, M. Tachibana, and N. Nagasue. 2007. Fractalkine-CX3CR1 axis regulates tumor cell cycle and deteriorates prognosis after radical resection for hepatocellular carcinoma. J. Surg. Oncol. 95: 241-249.
50. Jamieson-Gladney, W. L., Y. Zhang, A. M. Fong, O. Meucci, and A. Fatatis. 2011. The chemokine receptor CX3CR1 is directly involved in the arrest of breast cancer cells to the skeleton. Breast Cancer Res. 13: R91.
51. Nevo, I., O. Sagi-Assif, T. Meshel, A. Ben-Baruch, K. Jöhrer, R. Greil, L. E. Trejo, O. Kharenko, M. Feinmesser, I. Yron, and I. P. Witz. 2009. The involvement of the fractalkine receptor in the transmigration of neuroblastoma cells through bone-marrow endothelial cells. Cancer Lett. 273: 127-139.
52. Ferretti, E., V. Pistoia, and A. Corcione. 2014. Role of fractalkine/CX3CL1 and its receptor in the pathogenesis of inflammatory and malignant diseases with emphasis on B cell malignancies. Mediators Inflamm. DOI: 10.1155/2014/480941.
53. Kehlen, A., T. Greither, S. Wach, E. Nolte, M. Kappler, M. Bache, H. J. Holzhausen, C. Lautenschläger, S. Göbel, P. Würl, et al. 2014. High coexpression of CCL2 and CX3CL1 is gender-specifically associated with good prognosis in soft tissue sarcoma patients. Int. J. Cancer 135: 2096-2106.
54. Tardáguila, M., and S. Mañes. The complex role of chemokines in cancer: the case of the CX3CL1/CX3CR1 axis. Oncology Theory & Practice
55. Balkwill, F. 2004. Cancer and the chemokine network. Nat. Rev. Cancer 4: 540-550.
56. Mantovani, A., B. Savino, M. Locati, L. Zammataro, P. Allavena, and R. Bonecchi. 2010. The chemokine system in cancer biology and therapy. Cy-tokine Growth Factor Rev. 21: 27-39.
57. Zlotnik, A., A. M. Burkhardt, and B. Homey. 2011. Homeostatic chemokine receptors and organ-specific metastasis. Nat. Rev. Immunol. 11: 597-606.
58. Halkias, J., H. J. Melichar, K. T. Taylor, J. O. Ross, B. Yen, S. B. Cooper, A. Winoto, and E. A. Robey. 2013. Opposing chemokine gradients control human thymocyte migration in situ. J. Clin. Invest. 123: 2131-2142.
59. Chen, H. J., R. Edwards, S. Tucci, P. Bu, J. Milsom, S. Lee, W. Edelmann, Z. H. Gümüs, X. Shen, and S. Lipkin. 2012. Chemokine 25-induced signaling suppresses colon cancer invasion and metastasis. J. Clin. Invest. 122: 3184-3196.