CX3CR1 reduces kidney fibrosis by inhibiting local proliferation of profibrotic macrophages

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1628-1638

  Engel, Daniel R ^a,b   Krause, Torsten A ^a   Snelgrove, Sarah L ^c   Thiebes, Stephanie ^a   Hickey, Michael J ^c   Boor, Peter ^d   Kitching, A Richard ^c   Kurts, Christian ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

^c MONASH UNIVERSITY   (Australia)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; TRANSFORMING GROWTH FACTOR BETA; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELL TRANSFER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE SEVERITY; FLOW CYTOMETRY; KIDNEY FIBROSIS; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PHAGOCYTE; ANIMAL; C57BL MOUSE; DISEASE MODEL; FIBROSIS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; KIDNEY; METABOLISM; MUTANT MOUSE STRAIN; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FIBROSIS; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; KIDNEY; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CHEMOKINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84922567687     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402149     Document Type: Article

References (80)

1. Nelson, P. J., A. J. Rees, M. D. Griffin, J. Hughes, C. Kurts, and J. Duffield. 2012. The renal mononuclear phagocytic system. J. Am. Soc. Nephrol. 23: 194-203.
2. Kurts, C., U. Panzer, H. J. Anders, and A. J. Rees. 2013. The immune system and kidney disease: basic concepts and clinical implications. Nat. Rev. Immunol. 13: 738-753.
3. Hochheiser, K., C. Heuser, T. A. Krause, S. Teteris, A. Ilias, C. Weisheit, F. Hoss, A. P. Tittel, P. A. Knolle, U. Panzer, et al. 2013. Exclusive CX3CR1 dependence of kidney DCs impacts glomerulonephritis progression. J. Clin. Invest. 123: 4242-4254.
4. Schiwon, M., C. Weisheit, L. Franken, S. Gutweiler, A. Dixit, C. Meyer-Schwesinger, J. M. Pohl, N. J. Maurice, S. Thiebes, K. Lorenz, et al. 2014. Crosstalk between sentinel and helper macrophages permits neutrophil migration into infected uroepithelium. Cell 156: 456-468.
5. Geissmann, F., S. Gordon, D. A. Hume, A. M. Mowat, and G. J. Randolph. 2010. Unravelling mononuclear phagocyte heterogeneity. Nat. Rev. Immunol. 10: 453-460.
6. Leibund Gut-Landmann, S., O. Gross, M. J. Robinson, F. Osorio, E. C. Slack, S. V. Tsoni, E. Schweighoffer, V. Tybulewicz, G. D. Brown, J. Ruland, and C. Reis e Sousa. 2007. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8: 630-638.
7. Krüger, T., D. Benke, F. Eitner, A. Lang, M. Wirtz, E. E. Hamilton-Williams, D. Engel, B. Giese, G. Müller-Newen, J. Floege, and C. Kurts. 2004. Identification and functional characterization of dendritic cells in the healthy murine kidney and in experimental glomerulonephritis. J. Am. Soc. Nephrol. 15: 613-621.
8. Miller, J. C., B. D. Brown, T. Shay, E. L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K. G. Elpek, J. Helft, et al. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13: 888-899.
9. Gautier, E. L., T. Shay, J. Miller, M. Greter, C. Jakubzick, S. Ivanov, J. Helft, A. Chow, K. G. Elpek, S. Gordonov, et al. 2012. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13: 1118-1128.
10. Tittel, A. P., C. Heuser, C. Ohliger, P. A. Knolle, D. R. Engel, and C. Kurts. 2011. Kidney dendritic cells induce innate immunity against bacterial pyelonephritis. J. Am. Soc. Nephrol. 22: 1435-1441.
11. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964.
12. Murray, P. J., and T. A. Wynn. 2011. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11: 723-737.
13. Vernon, M. A., K. J. Mylonas, and J. Hughes. 2010. Macrophages and renal fibrosis. Semin. Nephrol. 30: 302-317.
14. Wynn, T. A., and L. Barron. 2010. Macrophages: master regulators of inflammation and fibrosis. Semin. Liver Dis. 30: 245-257.
15. Persy, V. P., A. Verhulst, D. K. Ysebaert, K. E. De Greef, and M. E. De Broe. 2003. Reduced postischemic macrophage infiltration and interstitial fibrosis in osteopontin knockout mice. Kidney Int. 63: 543-553.
16. Kitagawa, K., T. Wada, K. Furuichi, H. Hashimoto, Y. Ishiwata, M. Asano, M. Takeya, W. A. Kuziel, K. Matsushima, N. Mukaida, and H. Yokoyama. 2004. Blockade of CCR2 ameliorates progressive fibrosis in kidney. Am. J. Pathol. 165: 237-246.
17. Kitamoto, K., Y. Machida, J. Uchida, Y. Izumi, M. Shiota, T. Nakao, H. Iwao, T. Yukimura, T. Nakatani, and K. Miura. 2009. Effects of liposome clodronate on renal leukocyte populations and renal fibrosis in murine obstructive nephropathy. J. Pharmacol. Sci. 111: 285-292.
18. Snelgrove, S. L., J. Y. Kausman, C. Lo, C. Lo, J. D. Ooi, P. T. Coates, M. J. Hickey, S. R. Holdsworth, C. Kurts, D. R. Engel, and A. R. Kitching. 2012. Renal dendritic cells adopt a pro-inflammatory phenotype in obstructive urop-athy to activate T cells but do not directly contribute to fibrosis. Am. J. Pathol. 180: 91-103.
19. Wynn, T. A. 2008. Cellular and molecular mechanisms of fibrosis. J. Pathol. 214: 199-210.
20. Duffield, J. S., M. Lupher, V. J. Thannickal, and T. A. Wynn. 2013. Host responses in tissue repair and fibrosis. Annu. Rev. Pathol. 8: 241-276.
21. Ginhoux, F., F. Tacke, V. Angeli, M. Bogunovic, M. Loubeau, X. M. Dai, E. R. Stanley, G. J. Randolph, and M. Merad. 2006. Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7: 265-273.
22. Schulz, C., E. Gomez Perdiguero, L. Chorro, H. Szabo-Rogers, N. Cagnard, K. Kierdorf, M. Prinz, B. Wu, S. E. Jacobsen, J. W. Pollard, et al. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336: 86-90.
23. Shi, C., and E. G. Pamer. 2011. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11: 762-774.
24. Ginhoux, F., M. Greter, M. Leboeuf, S. Nandi, P. See, S. Gokhan, M. F. Mehler, S. J. Conway, L. G. Ng, E. R. Stanley, et al. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330: 841-845.
25. Schraml, B. U., J. van Blijswijk, S. Zelenay, P. G. Whitney, A. Filby, S. E. Acton, N. C. Rogers, N. Moncaut, J. J. Carvajal, and C. Reis e Sousa. 2013. Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 154: 843-858.
26. Kezic, J., and P. G. McMenamin. 2010. The monocyte chemokine receptor CX3CR1 does not play a significant role in the pathogenesis of experimental autoimmune uveoretinitis. Invest. Ophthalmol. Vis. Sci. 51: 5121-5127.
27. + common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 206: 595-606.
28. Medina-Contreras, O., D. Geem, O. Laur, I. R. Williams, S. A. Lira, A. Nusrat, C. A. Parkos, and T. L. Denning. 2011. CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice. J. Clin. Invest. 121: 4787-4795.
29. Farache, J., E. Zigmond, G. Shakhar, and S. Jung. 2013. Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense. Immunol. Cell Biol. 91: 232-239.
30. Kostadinova, F. I., T. Baba, Y. Ishida, T. Kondo, B. K. Popivanova, and N. Mukaida. 2010. Crucial involvement of the CX3CR1-CX3CL1 axis in dextran sulfate sodium-mediated acute colitis in mice. J. Leukoc. Biol. 88: 133-143.
31. Landsman, L., C. Varol, and S. Jung. 2007. Distinct differentiation potential of blood monocyte subsets in the lung. J. Immunol. 178: 2000-2007.
32. - pulmonary dendritic cell populations. J. Immunol. 180: 3019-3027.
33. Fuhrmann, M., T. Bittner, C. K. Jung, S. Burgold, R. M. Page, G. Mitteregger, C. Haass, F. M. LaFerla, H. Kretzschmar, and J. Herms. 2010. Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat. Neurosci. 13: 411-413.
34. Kim, K. W., A. Vallon-Eberhard, E. Zigmond, J. Farache, E. Shezen, G. Shakhar, A. Ludwig, S. A. Lira, and S. Jung. 2011. In vivo structure/function and expression analysis of the CX3C chemokine fractalkine. Blood 118: e156-e167.
35. Durkan, A. M., R. T. Alexander, G. Y. Liu, M. Rui, G. Femia, and L. A. Robinson. 2007. Expression and targeting of CX3CL1 (fractalkine) in renal tubular epithelial cells. J. Am. Soc. Nephrol. 18: 74-83.
36. Serbina, N. V., and E. G. Pamer. 2006. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7: 311-317.
37. Jia, T., N. V. Serbina, K. Brandl, M. X. Zhong, I. M. Leiner, I. F. Charo, and E. G. Pamer. 2008. Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J. Immunol. 180: 6846-6853.
38. high monocytes from the bone marrow, but is dispensable for bladder infiltration in bacterial urinary tract infection. J. Immunol. 181: 5579-5586.
39. Landsman, L., and S. Jung. 2007. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J. Immunol. 179: 3488-3494.
40. high monocytes are selectively recruited to injured kidney and differentiate into functionally distinct populations. J. Immunol. 183: 6733-6743.
41. Krause, T. A., A. F. Alex, D. R. Engel, C. Kurts, and N. Eter. 2014. VEGF-production by CCR2-dependent macrophages contributes to laser-induced cho-roidal neovascularization. PLoS One 9: e94313.
42. Schmidt, M., G. Sun, M. A. Stacey, L. Mori, and S. Mattoli. 2003. Identification of circulating fibrocytes as precursors of bronchial myofibroblasts in asthma. J. Immunol. 171: 380-389.
43. Pérez de Lema, G., H. Maier, T. J. Franz, M. Escribese, S. Chilla, S. Segerer, N. Camarasa, H. Schmid, B. Banas, S. Kalaydjiev, et al. 2005. Chemokine receptor Ccr2 deficiency reduces renal disease and prolongs survival in MRL/lpr lupus-prone mice. J. Am. Soc. Nephrol. 16: 3592-3601.
44. Li, L., L. Huang, S. S. Sung, A. L. Vergis, D. L. Rosin, C. E. Rose, Jr., P. I. Lobo, and M. D. Okusa. 2008. The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury. Kidney Int. 74: 1526-1537.
45. Tacke, F., D. Alvarez, T. J. Kaplan, C. Jakubzick, R. Spanbroek, J. Llodra, A. Garin, J. Liu, M. Mack, N. van Rooijen, et al. 2007. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117: 185-194.
46. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670.
47. Combadière, C., C. Feumi, W. Raoul, N. Keller, M. Rodéro, A. Pézard, S. Lavalette, M. Houssier, L. Jonet, E. Picard, et al. 2007. CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J. Clin. Invest. 117: 2920-2928.
48. Clover, A. J., A. H. Kumar, and N. M. Caplice. 2011. Deficiency of CX3CR1 delays burn wound healing and is associated with reduced myeloid cell recruitment and decreased sub-dermal angiogenesis. Burns 37: 1386-1393.
49. Furuichi, K., J. L. Gao, and P. M. Murphy. 2006. Chemokine receptor CX3CR1 regulates renal interstitial fibrosis after ischemia-reperfusion injury. Am. J. Pathol. 169: 372-387.
50. 3CR1 protects against liver fibrosis by controlling differentiation and survival of infiltrating hepatic monocytes. Hepatology 52: 1769-1782.
51. Aoyama, T., S. Inokuchi, D. A. Brenner, and E. Seki. 2010. CX3CL1-CX3CR1 interaction prevents carbon tetrachloride-induced liver inflammation and fibrosis in mice. Hepatology 52: 1390-1400.
52. Arai, M., Y. Ikawa, S. Chujo, Y. Hamaguchi, W. Ishida, F. Shirasaki, M. Hasegawa, N. Mukaida, M. Fujimoto, and K. Takehara. 2013. Chemokine receptors CCR2 and CX3CR1 regulate skin fibrosis in the mouse model of cytokine-induced systemic sclerosis. J. Dermatol. Sci. 69: 250-258.
53. Zhang, J., and J. M. Patel. 2010. Role of the CX3CL1-CX3CR1 axis in chronic inflammatory lung diseases. Int. J. Clin. Exp. Med. 3: 233-244.
54. Shimizu, K., K. Furuichi, N. Sakai, K. Kitagawa, K. Matsushima, N. Mukaida, S. Kaneko, and T. Wada. 2011. Fractalkine and its receptor, CX3CR1, promote hypertensive interstitial fibrosis in the kidney. Hypertens. Res. 34: 747-752.
55. Ishida, Y., J. L. Gao, and P. M. Murphy. 2008. Chemokine receptor CX3CR1 mediates skin wound healing by promoting macrophage and fibroblast accumulation and function. J. Immunol. 180: 569-579.
56. + interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int. 70: 591-596.
57. Feng, L., S. Chen, G. E. Garcia, Y. Xia, M. A. Siani, P. Botti, C. B. Wilson, J. K. Harrison, and K. B. Bacon. 1999. Prevention of crescentic glomerulone-phritis by immunoneutralization of the fractalkine receptor CX3CR1 rapid communication. Kidney Int. 56: 612-620.
58. Lionakis, M. S., M. Swamydas, B. G. Fischer, T. S. Plantinga, M. D. Johnson, M. Jaeger, N. M. Green, A. Masedunskas, R. Weigert, C. Mikelis, et al. 2013. CX3CR1-dependent renal macrophage survival promotes Candida control and host survival. J. Clin. Invest. 123: 5035-5051.
59. Koziolek, M. J., H. Schmid, C. D. Cohen, S. Blaschke, B. Hemmerlein, A. Zapf, G. A. Müller, and F. Strutz. 2007. Potential role of fractalkine receptor expression in human renal fibrogenesis. Kidney Int. 72: 599-607.
60. Lindquist, R. L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M. L. Dustin, and M. C. Nussenzweig. 2004. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5: 1243-1250.
61. Jung, S., J. Aliberti, P. Graemmel, M. J. Sunshine, G. W. Kreutzberg, A. Sher, and D. R. Littman. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20: 4106-4114.
62. Kuligowski, M. P., A. R. Kitching, and M. J. Hickey. 2006. Leukocyte recruitment to the inflamed glomerulus: a critical role for platelet-derived P-selectin in the absence of rolling. J. Immunol. 176: 6991-6999.
63. Devi, S., A. Li, C. L. Westhorpe, C. Y. Lo, L. D. Abeynaike, S. L. Snelgrove, P. Hall, J. D. Ooi, C. G. Sobey, A. R. Kitching, and M. J. Hickey. 2013. Multiphoton imaging reveals a new leukocyte recruitment paradigm in the glomer-ulus. Nat. Med. 19: 107-112.
64. Boor, P., A. Konieczny, L. Villa, A. L. Schult, E. Bücher, S. Rong, U. Kunter, C. R. van Roeyen, T. Polakowski, H. Hawlisch, et al. 2007. Complement C5 mediates experimental tubulointerstitial fibrosis. J. Am. Soc. Nephrol. 18: 1508-1515.
65. Inoue, A., H. Hasegawa, M. Kohno, M. R. Ito, M. Terada, T. Imai, O. Yoshie, M. Nose, and S. Fujita. 2005. Antagonist of fractalkine (CX3CL1) delays the initiation and ameliorates the progression of lupus nephritis in MRL/lpr mice. Arthritis Rheum. 52: 1522-1533.
66. Machida, Y., K. Kitamoto, Y. Izumi, M. Shiota, J. Uchida, Y. Kira, T. Nakatani, and K. Miura. 2010. Renal fibrosis in murine obstructive nephropathy is attenuated by depletion of monocyte lineage, not dendritic cells. J. Pharmacol. Sci. 114: 464-473.
67. Hammad, H., and B. N. Lambrecht. 2008. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat. Rev. Immunol. 8: 193-204.
68. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82.
69. Yanagita, M. 2012. Inhibitors/antagonists of TGF-β system in kidney fibrosis. Nephrol. Dial. Transplant. 27: 3686-3691.
70. Martinez-Pomares, L., D. M. Reid, G. D. Brown, P. R. Taylor, R. J. Stillion, S. A. Linehan, S. Zamze, S. Gordon, and S. Y. Wong. 2003. Analysis of mannose receptor regulation by IL-4, IL-10, and proteolytic processing using novel monoclonal antibodies. J. Leukoc. Biol. 73: 604-613.
71. Xue, J., S. V. Schmidt, J. Sander, A. Draffehn, W. Krebs, I. Quester, D. De Nardo, T. D. Gohel, M. Emde, L. Schmidleithner, et al. 2014. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 40: 274-288.
72. Jenkins, S. J., D. Ruckerl, P. C. Cook, L. H. Jones, F. D. Finkelman, N. van Rooijen, A. S. MacDonald, and J. E. Allen. 2011. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332: 1284-1288.
73. Jenkins, S. J., D. Ruckerl, G. D. Thomas, J. P. Hewitson, S. Duncan, F. Brombacher, R. M. Maizels, D. A. Hume, and J. E. Allen. 2013. IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J. Exp. Med. 210: 2477-2491.
74. Landsman, L., L. Bar-On, A. Zernecke, K. W. Kim, R. Krauthgamer, E. Shagdarsuren, S. A. Lira, I. L. Weissman, C. Weber, and S. Jung. 2009. CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood 113: 963-972.
75. Mionnet, C., V. Buatois, A. Kanda, V. Milcent, S. Fleury, D. Lair, M. Langelot, Y. Lacoeuille, E. Hessel, R. Coffman, et al. 2010. CX3CR1 is required for airway inflammation by promoting T helper cell survival and maintenance in inflamed lung. Nat. Med. 16: 1305-1312.
76. -/- mice reveals a role for fractalkine in atherogenesis. J. Clin. Invest. 111: 333-340.
77. Dong, X., S. Swaminathan, L. A. Bachman, A. J. Croatt, K. A. Nath, and M. D. Griffin. 2007. Resident dendritic cells are the predominant TNF-secreting cell in early renal ischemia-reperfusion injury. Kidney Int. 71: 619-628.
78. Lech, M., A. Avila-Ferrufino, R. Allam, S. Segerer, A. Khandoga, F. Krombach, C. Garlanda, A. Mantovani, and H. J. Anders. 2009. Resident dendritic cells prevent postischemic acute renal failure by help of single Ig IL-1 receptor-related protein. J. Immunol. 183: 4109-4118.
79. Tittel, A. P., C. Heuser, C. Ohliger, C. Llanto, S. Yona, G. J. Hämmerling, D. R. Engel, N. Garbi, and C. Kurts. 2012. Functionally relevant neutrophilia in CD11c diphtheria toxin receptor transgenic mice. Nat. Methods 9: 385-390.
80. Chorro, L., A. Sarde, M. Li, K. J. Woollard, P. Chambon, B. Malissen, A. Kissenpfennig, J. B. Barbaroux, R. Groves, and F. Geissmann. 2009. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J. Exp. Med. 206: 3089-3100.