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Mediators of Inflammation
Volume 2014, Article ID 480941, 10 pages
http://dx.doi.org/10.1155/2014/480941
Review Article

Role of Fractalkine/CX3CL1 and Its Receptor in the Pathogenesis of Inflammatory and Malignant Diseases with Emphasis on B Cell Malignancies

Laboratory of Oncology, Istituto Giannina Gaslini, 16147 Genova, Italy

Received 20 December 2013; Revised 26 February 2014; Accepted 5 March 2014; Published 30 March 2014

Academic Editor: Teizo Yoshimura

Copyright © 2014 Elisa Ferretti et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Mantovani, “The chemokine system: redundancy for robust outputs,” Immunology Today, vol. 20, no. 6, pp. 254–257, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Baggiolini, “Chemokines and leukocyte traffic,” Nature, vol. 392, no. 6676, pp. 565–568, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Baggiolini, “Chemokines in pathology and medicine,” Journal of Internal Medicine, vol. 250, no. 2, pp. 91–104, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. R. M. Strieter, P. J. Polverini, S. L. Kunkel et al., “The functional role of the ELR motif in CXC chemokine-mediated angiogenesis,” The Journal of Biological Chemistry, vol. 270, no. 45, pp. 27348–27357, 1995. View at Publisher · View at Google Scholar · View at Scopus
  5. J. F. Bazan, K. B. Bacon, G. Hardiman et al., “A new class of membrane-bound chemokine with a CX3C motif,” Nature, vol. 385, no. 6617, pp. 640–644, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Umehara, E. Bloom, T. Okazaki, N. Domae, and T. Imai, “Fractalkine and vascular injury,” Trends in Immunology, vol. 22, no. 11, pp. 602–607, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. A. M. Fong, L. A. Robinson, D. A. Steeber et al., “Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow,” The Journal of Experimental Medicine, vol. 188, no. 8, pp. 1413–1419, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. C.-L. Tsou, C. A. Haskell, and I. F. Charo, “Tumor necrosis factor-α-converting enzyme mediates the inducible cleavage of fractalkine,” The Journal of Biological Chemistry, vol. 276, no. 48, pp. 44622–44626, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. K. J. Garton, P. J. Gough, C. P. Blobel et al., “Tumor necrosis factor-α-converting enzyme (ADAM17) mediates the cleavage and shedding of fractalkine (CX3CL1),” The Journal of Biological Chemistry, vol. 276, no. 41, pp. 37993–38001, 2001. View at Google Scholar · View at Scopus
  10. A. K. Clark, P. K. Yip, J. Grist et al., “Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 25, pp. 10655–10660, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Corcione, E. Ferretti, M. Bertolotto et al., “CX3CR1 is expressed by human B lymphocytes and meditates CX3CL1 driven chemotaxis of tonsil centrocytes,” PLoS ONE, vol. 4, no. 12, Article ID e8485, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Corcione, E. Ferretti, and V. Pistoia, “CX3CL1/fractalkine is a novel regulator of normal and malignant human B cell function,” Journal of Leukocyte Biology, vol. 92, no. 1, pp. 51–58, 2012. View at Publisher · View at Google Scholar
  13. T. Imai, K. Hieshima, C. Haskell et al., “Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion,” Cell, vol. 91, no. 4, pp. 521–530, 1997. View at Google Scholar · View at Scopus
  14. M. Nishimura, H. Umehara, T. Nakayama et al., “Dual functions of fractalkine/CX3C ligand 1 in trafficking of perforin+/granzyme B+ cytotoxic effector lymphocytes that are defined by CX3CR1 expression,” The Journal of Immunology, vol. 168, no. 12, pp. 6173–6180, 2002. View at Google Scholar · View at Scopus
  15. F. Marchesi, M. Locatelli, G. Solinas, M. Erreni, P. Allavena, and A. Mantovani, “Role of CX3CR1/CX3CL1 axis in primary and secondary involvement of the nervous system by cancer,” Journal of Neuroimmunology, vol. 224, no. 1-2, pp. 39–44, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Le, Y. Zhou, P. Iribarren, and J. Wang, “Chemokines and chemokine receptors: their manifold roles in homeostasis and disease,” Cellular & Molecular Immunology, vol. 1, no. 2, pp. 95–104, 2004. View at Google Scholar · View at Scopus
  17. J. G. D'Haese, I. E. Demir, H. Friess, and G. O. Ceyhan, “Fractalkine/CX3CR1: why a single chemokine-receptor duo bears a major and unique therapeutic potential,” Expert Opinion on Therapeutic Targets, vol. 14, no. 2, pp. 207–219, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. J. G. D'Haese, H. Friess, and G. O. Ceyhan, “Therapeutic potential of the chemokine-receptor duo fractalkine/CX3CR1: an update,” Expert Opinion on Therapeutic Targets, vol. 16, no. 6, pp. 613–618, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. A.-C. Rimaniol, S. J. Till, G. Garcia et al., “The CX3C chemokine fractalkine in allergic asthma and rhinitis,” The Journal of Allergy and Clinical Immunology, vol. 112, no. 6, pp. 1139–1146, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. A. El-Shazly, P. Berger, P.-O. Girodet et al., “Fraktalkine produced by airway smooth muscle cells contributes to mast cell recruitment in asthma,” The Journal of Immunology, vol. 176, no. 3, pp. 1860–1868, 2006. View at Google Scholar · View at Scopus
  21. C. Mionnet, V. Buatois, A. Kanda et al., “CX3CR1 is required for airway inflammation by promoting T helper cell survival and maintenance in inflamed lung,” Nature Medicine, vol. 16, no. 11, pp. 1305–1312, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Iwamoto, H. Okamoto, Y. Toyama, and S. Momohara, “Molecular aspects of rheumatoid arthritis: chemokines in the joints of patients,” The FEBS Journal, vol. 275, no. 18, pp. 4448–4455, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Murphy, N. Caplice, and M. Molloy, “Fractalkine in rheumatoid arthritis: a review to date,” Rheumatology, vol. 47, no. 10, pp. 1446–1451, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Blaschke, M. Koziolek, A. Schwarz et al., “Proinflammatory role of fractalkine (CX3CL1) in rheumatoid arthritis,” The Journal of Rheumatology, vol. 30, no. 9, pp. 1918–1927, 2003. View at Google Scholar · View at Scopus
  25. T. Nanki, T. Imai, K. Nagasaka et al., “Migration of CX3CR1-positive T cells producing type 1 cytokines and cytotoxic molecules into the synovium of patients with rheumatoid arthritis,” Arthritis and Rheumatism, vol. 46, no. 11, pp. 2878–2883, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. J. H. Ruth, M. V. Volin, G. K. Haines III et al., “Fractalkine, a novel chemokine in rheumatoid arthritis and in rat adjuvant-induced arthritis,” Arthritis & Rheumatism, vol. 44, no. 7, pp. 1568–1581, 2001. View at Publisher · View at Google Scholar
  27. T. Nanki, Y. Urasaki, T. Imai et al., “Inhibition of fractalkine ameliorates murine collagen-induced arthritis,” The Journal of Immunology, vol. 173, no. 11, pp. 7010–7016, 2004. View at Google Scholar · View at Scopus
  28. F. Suzuki, T. Nanki, T. Imai et al., “Inhibition of CX3CL1 (fractalkine) improves experimental autoimmune myositis in SJL/J mice,” The Journal of Immunology, vol. 175, no. 10, pp. 6987–6996, 2005. View at Google Scholar · View at Scopus
  29. R. Ross, “Cell biology of atherosclerosis,” Annual Review of Physiology, vol. 57, pp. 791–804, 1995. View at Google Scholar · View at Scopus
  30. G. K. Hansson and P. Libby, “The immune response in atherosclerosis: a double-edged sword,” Nature Reviews Immunology, vol. 6, no. 7, pp. 508–519, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. U. P. Fonovic, Z. Jevnikar, and J. Kos, “Cathepsin S generates soluble CX3CL1 (fractalkine) in vascular smooth muscle cells,” Biological Chemistry, vol. 394, no. 10, pp. 1349–1352, 2013. View at Google Scholar
  32. A. D. Lucas, C. Bursill, T. J. Guzik, J. Sadowski, K. M. Channon, and D. R. Greaves, “Smooth muscle cells in human atherosclerotic plaques express the fractalkine receptor CX3CR1 and undergo chemotaxis to the CX3C chemokine fractalkine (CX3CL1),” Circulation, vol. 108, no. 20, pp. 2498–2504, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Saederup, L. Chan, S. A. Lira, and I. F. Charo, “Fractalkine deficiency markedly reduces macrophage accumulation and atherosclerotic lesion formation in CCR2-/- mice: evidence for independent chemokine functions in atherogenesis,” Circulation, vol. 117, no. 13, pp. 1642–1648, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Poupel, A. Boissonnas, P. Hermand et al., “Pharmacological inhibition of the chemokine receptor, CX3CR1, reduces atherosclerosis in mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 10, pp. 2297–2305, 2013. View at Publisher · View at Google Scholar
  35. A. M. Durkan, R. T. Alexander, G.-Y. Liu, M. Rui, G. Femia, and L. A. Robinson, “Expression and targeting of CX3CL1 (fractalkine) in renal tubular epithelial cells,” Journal of the American Society of Nephrology, vol. 18, no. 1, pp. 74–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Segerer, E. Hughes, K. L. Hudkins, M. Mack, T. Goodpaster, and C. E. Alpers, “Expression of the fractalkine receptor (CX3CR1) in human kidney diseases,” Kidney International, vol. 62, no. 2, pp. 488–495, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Bourd-Boittin, L. Basset, D. Bonnier, A. L'Helgoualc'H, M. Samson, and N. Théret, “CX3CL1/fractalkine shedding by human hepatic stellate cells: contribution to chronic inflammation in the liver,” Journal of Cellular and Molecular Medicine, vol. 13, no. 8a, pp. 1526–1535, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Efsen, C. Grappone, R. M. S. DeFranco et al., “Up-regulated expression of fractalkine and its receptor CX3CR1 during liver injury in humans,” Journal of Hepatology, vol. 37, no. 1, pp. 39–47, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Kobayashi, S. Okamoto, Y. Iwakami et al., “Exclusive increase of CX3CR1+CD28CD4+ T cells in inflammatory bowel disease and their recruitment as intraepithelial lymphocytes,” Inflammatory Bowel Diseases, vol. 13, no. 7, pp. 837–846, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. O. Medina-Contreras, D. Geem, O. Laur et al., “CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice,” The Journal of Clinical Investigation, vol. 121, no. 12, pp. 4787–4795, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. M. D. Silverman, D. O. Zamora, Y. Pan et al., “Constitutive and inflammatory mediator-regulated fractalkine expression in human ocular tissues and cultured cells,” Investigative Ophthalmology & Visual Science, vol. 44, no. 4, pp. 1608–1615, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. W. Raoul, C. Auvynet, S. Camelo et al., “CCL2/CCR2 and CX3CL1/CX3CR1 chemokine axes and their possible involvement in age-related macular degeneration,” Journal of Neuroinflammation, vol. 7, article 87, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Faure, L. Meyer, D. Costagliola et al., “Rapid progression to AIDS in HIV+ individuals with a structural variant of the chemokine receptor CX3CR1,” Science, vol. 287, no. 5461, pp. 2274–2277, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Brand, K. Hofbauer, J. Dambacher et al., “Increased expression of the chemokine fractalkine in Crohn's disease and association of the fractalkine receptor T280M polymorphism with a fibrostenosing disease phenotype,” The American Journal of Gastroenterology, vol. 101, no. 1, pp. 99–106, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. D. H. McDermott, J. S. Colla, C. A. Kleeberger et al., “Genetic polymorphism in CX3CR1 and risk of HIV disease,” Science, vol. 290, no. 5499, p. 2031, 2000. View at Google Scholar · View at Scopus
  46. D. H. McDermott, A. M. Fong, Q. Yang et al., “Chemokine receptor mutant CX3CR1-M280 has impaired adhesive function and correlates with protection from cardiovascular disease in humans,” The Journal of Clinical Investigation, vol. 111, no. 8, pp. 1241–1250, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. D. H. McDermott, J. P. J. Halcox, W. H. Schenke et al., “Association between polymorphism in the chemokine receptor CX3CR1 and coronary vascular endothelial dysfunction and atherosclerosis,” Circulation Research, vol. 89, no. 5, pp. 401–407, 2001. View at Google Scholar · View at Scopus
  48. D. Moatti, S. Faure, F. Fumeron et al., “Polymorphism in the fractalkine receptor CX3CR1 as a genetic risk factor for coronary artery disease,” Blood, vol. 97, no. 7, pp. 1925–1928, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Tuo, B. C. Smith, C. M. Bojanowski et al., “The involvement of sequence variation and expression of CX3CR1 in the pathogenesis of age-related macular degeneration,” The FASEB Journal, vol. 18, no. 11, pp. 1297–1299, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Erichsen, A. L. Lopez, H. Peng et al., “Neuronal injury regulates fractalkine: relevance for HIV-1 associated dementia,” Journal of Neuroimmunology, vol. 138, no. 1-2, pp. 144–155, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. J. K. Harrison, Y. Jiang, S. Chen et al., “Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 18, pp. 10896–10901, 1998. View at Publisher · View at Google Scholar · View at Scopus
  52. J. T. Rogers, J. M. Morganti, A. D. Bachstetter et al., “CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity,” The Journal of Neuroscience, vol. 31, no. 45, pp. 16241–16250, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Lee, N. H. Varvel, M. E. Konerth et al., “CX3CR1 deficiency alters microglial activation and reduces beta-amyloid deposition in two Alzheimer's disease mouse models,” The American Journal of Pathology, vol. 177, no. 5, pp. 2549–2562, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. S.-H. Cho, B. Sun, Y. Zhou et al., “CX3CR1 protein signaling modulates microglial activation and protects against plaque-independent cognitive deficits in a mouse model of Alzheimer disease,” The Journal of Biological Chemistry, vol. 286, no. 37, pp. 32713–32722, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Bhaskar, M. Konerth, O. N. Kokiko-Cochran, A. Cardona, R. M. Ransohoff, and B. T. Lamb, “Regulation of tau pathology by the microglial fractalkine receptor,” Neuron, vol. 68, no. 1, pp. 19–31, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. S. Kim and T. H. Joh, “Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease,” Experimental & Molecular Medicine, vol. 38, no. 4, pp. 333–347, 2006. View at Google Scholar · View at Scopus
  57. K. Tieu, H. Ischiropoulos, and S. Przedborski, “Nitric oxide and reactive oxygen species in Parkinson's disease,” IUBMB Life, vol. 55, no. 6, pp. 329–335, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. J. M. Morganti, K. R. Nash, B. A. Grimmig et al., “The soluble isoform of CX3CL1 is necessary for neuroprotection in a mouse model of Parkinson's disease,” The Journal of Neuroscience, vol. 32, no. 42, pp. 14592–14601, 2012. View at Publisher · View at Google Scholar
  59. A. E. Cardona, E. P. Pioro, M. E. Sasse et al., “Control of microglial neurotoxicity by the fractalkine receptor,” Nature Neuroscience, vol. 9, no. 7, pp. 917–924, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. K. A. Lindl, D. R. Marks, D. L. Kolson, and K. L. Jordan-Sciutto, “HIV-associated neurocognitive disorder: pathogenesis and therapeutic opportunities,” Journal of Neuroimmune Pharmacology, vol. 5, no. 3, pp. 294–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. O. Meucci, A. Fatatis, A. A. Simen, and R. J. Miller, “Expression of CX3CR1 chemokine receptors on neurons and their role in neuronal survival,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 14, pp. 8075–8080, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Limatola, C. Lauro, M. Catalano et al., “Chemokine CX3CL1 protects rat hippocampal neurons against glutamate-mediated excitotoxicity,” Journal of Neuroimmunology, vol. 166, no. 1-2, pp. 19–28, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. G. A. Chapman, K. Moores, D. Harrison, C. A. Campbell, B. R. Stewart, and P. J. Strijbos, “Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage,” The Journal of Neuroscience, vol. 20, no. 15, article RC87, 2000. View at Google Scholar · View at Scopus
  64. M. Locatelli, L. Boiocchi, S. Ferrero et al., “Human glioma tumors express high levels of the chemokine receptor CX3CR1,” European Cytokine Network, vol. 21, no. 1, pp. 27–33, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Erreni, G. Solinas, P. Brescia et al., “Human glioblastoma tumours and neural cancer stem cells express the chemokine CX3CL1 and its receptor CX3CR1,” European Journal of Cancer, vol. 46, no. 18, pp. 3383–3392, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. G. Sciumé, A. Soriani, M. Piccoli, L. Frati, A. Santoni, and G. Bernardini, “CX3CR1/CX3CL1 axis negatively controls glioma cell invasion and is modulated by transforming growth factor-beta1,” Neuro-Oncology, vol. 12, no. 7, pp. 701–710, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. V. Pistoia, F. Morandi, G. Bianchi, A. Pezzolo, I. Prigione, and L. Raffaghello, “Immunosuppressive microenvironment in neuroblastoma,” Frontiers in Oncology, vol. 3, article 167, 2013. View at Google Scholar
  68. G. M. Brodeur, “Neuroblastoma: biological insights into a clinical enigma,” Nature Reviews Cancer, vol. 3, no. 3, pp. 203–216, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. I. Nevo, O. Sagi-Assif, T. Meshel et al., “The involvement of the fractalkine receptor in the transmigration of neuroblastoma cells through bone-marrow endothelial cells,” Cancer Letters, vol. 273, no. 1, pp. 127–139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. Y. Zeng, J. Jiang, N. Huebener et al., “Fractalkine gene therapy for neuroblastoma is more effective in combination with targeted IL-2,” Cancer Letters, vol. 228, no. 1-2, pp. 187–193, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. S. A. Shulby, N. G. Dolloff, M. E. Stearns, O. Meucci, and A. Fatatis, “CX3CR1-fractalkine expression regulates cellular mechanisms involved in adhesion, migration, and survival of human prostate cancer cells,” Cancer Research, vol. 64, no. 14, pp. 4693–4698, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. W. L. Jamieson, S. Shimizu, J. A. D'Ambrosio, O. Meucci, and A. Fatatis, “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 Research, vol. 68, no. 6, pp. 1715–1722, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Li, K. Xie, R. Wolff, and J. L. Abbruzzese, “Pancreatic cancer,” The Lancet, vol. 363, no. 9414, pp. 1049–1057, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. F. Marchesi, L. Piemonti, G. Fedele et al., “The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma,” Cancer Research, vol. 68, no. 21, pp. 9060–9069, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Gaudin, S. Nasreddine, A.-C. Donnadieu et al., “Identification of the chemokine CX3CL1 as a new regulator of malignant cell proliferation in epithelial ovarian cancer,” PLoS ONE, vol. 6, no. 7, Article ID e21546, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. K. M. Hart, S. P. Bak, A. Alonso, and B. Berwin, “Phenotypic and functional delineation of murine CX3CR1+ monocyte-derived cells in ovarian cancer,” Neoplasia, vol. 11, no. 6, pp. 564–573, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Kim, L. Rooper, J. Xie, A. A. Kajdacsy-Balla, and M. V. Barbolina, “Fractalkine receptor CX3CR1 is expressed in epithelial ovarian carcinoma cells and required for motility and adhesion to peritoneal mesothelial cells,” Molecular Cancer Research, vol. 10, no. 1, pp. 11–24, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. J. Lu, P. S. Steeg, J. E. Price et al., “Breast cancer metastasis: challenges and opportunities,” Cancer Research, vol. 69, no. 12, pp. 4951–4953, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. W. L. Jamieson-Gladney, Y. Zhang, A. M. Fong, O. Meucci, and A. Fatatis, “The chemokine receptor CX3CR1 is directly involved in the arrest of breast cancer cells to the skeleton,” Breast Cancer Research, vol. 13, no. 5, article R91, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. F. Andre, N. Cabioglu, H. Assi et al., “Expression of chemokine receptors predicts the site of metastatic relapse in patients with axillary node positive primary breast cancer,” Annals of Oncology, vol. 17, no. 6, pp. 945–951, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. M. H. Park, J. S. Lee, and J. H. Yoon, “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,” Journal of Surgical Oncology, vol. 106, no. 4, pp. 386–392, 2012. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Rozen, S. J. Winawer, and J. D. Waye, “Prospects for the worldwide control of colorectal cancer through screening,” Gastrointestinal Endoscopy, vol. 55, no. 6, pp. 755–759, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Ohta, F. Tanaka, H. Yamaguchi, N. Sadanaga, H. Inoue, and M. Mori, “The high expression of Fractalkine results in a better prognosis for colorectal cancer patients,” International Journal of Oncology, vol. 26, no. 1, pp. 41–47, 2005. View at Google Scholar · View at Scopus
  84. S. Vitale, B. Cambien, B. F. Karimdjee et al., “Tissue-specific differential antitumour effect of molecular forms of fractalkine in a mouse model of metastatic colon cancer,” Gut, vol. 56, no. 3, pp. 365–372, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. N. Nagasue, M. Uchida, Y. Makino et al., “Incidence and factors associated with intrahepatic recurrence following resection of hepatocellular carcinoma,” Gastroenterology, vol. 105, no. 2, pp. 488–494, 1993. View at Google Scholar · View at Scopus
  86. T. Matsubara, T. Ono, A. Yamanoi, M. Tachibana, and N. Nagasue, “Fractalkine-CX3CR1 axis regulates tumor cell cycle and deteriorates prognosis after radical resection for hepatocellular carcinoma,” Journal of Surgical Oncology, vol. 95, no. 3, pp. 241–249, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. L. Tang, H.-D. Hu, P. Hu et al., “Gene therapy with CX3CL1/Fractalkine induces antitumor immunity to regress effectively mouse hepatocellular carcinoma,” Gene Therapy, vol. 14, no. 16, pp. 1226–1234, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Hyakudomi, T. Matsubara, R. Hyakudomi et al., “Increased expression of fractalkine is correlated with a better prognosis and an increased number of both CD8+ T cells and natural killer cells in gastric adenocarcinoma,” Annals of Surgical Oncology, vol. 15, no. 6, pp. 1775–1782, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. E. Ferretti, M. Bertolotto, S. Deaglio et al., “A novel role of the CX3 CR1/CX3 CL1 system in the cross-talk between chronic lymphocytic leukemia cells and tumor microenvironment,” Leukemia, vol. 25, no. 8, pp. 1268–1277, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Carbone, A. Gloghini, A. Cabras, and G. Elia, “The Germinal centre-derived lymphomas seen through their cellular microenvironment,” British Journal of Haematology, vol. 145, no. 4, pp. 468–480, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Campo, S. H. Swerdlow, N. L. Harris, S. Pileri, H. Stein, and E. S. Jaffe, “The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications,” Blood, vol. 117, no. 19, pp. 5019–5032, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. N. J. Senff, E. M. Noordijk, Y. H. Kim et al., “European Organization for Research and Treatment of Cancer and International Society for cutaneous lymphoma Consensus recommendations for the management of cutaneous B-cell lymphomas,” Blood, vol. 112, no. 5, pp. 1600–1609, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. P. G. Isaacson and M.-Q. Du, “MALT lymphoma: from morphology to molecules,” Nature Reviews Cancer, vol. 4, no. 8, pp. 644–653, 2004. View at Google Scholar · View at Scopus
  94. U. Andréasson, S. Ek, H. Merz et al., “B cell lymphomas express CX3CR1 a non-B cell lineage adhesion molecule,” Cancer Letters, vol. 259, no. 2, pp. 138–145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. A. J. A. Deutsch, A. Aigelsreiter, E. Steinbauer et al., “Distinct signatures of B-cell homeostatic and activation-dependent chemokine receptors in the development and progression of extragastric MALT lymphomas,” The Journal of Pathology, vol. 215, no. 4, pp. 431–444, 2008. View at Publisher · View at Google Scholar · View at Scopus