Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 46, 2012, Pages

  Ramachandran, Prakash ^a   Pellicoro, Antonella ^a   Vernon, Madeleine A ^a   Boulter, Luke ^a   Aucott, Rebecca L ^a   Ali, Aysha ^a   Hartland, Stephen N ^a   Snowdon, Victoria K ^a   Cappon, Andrea ^a,b   Gordon Walker, Timothy T ^a   Williams, Mike J ^a   Dunbar, Donald R ^c   Manning, Jonathan R ^c   Van Rooijen, Nico ^d   Fallowfield, Jonathan A ^a   Forbes, Stuart J ^a   Iredale, John P ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Collagen; Degradation; Kupffer cell; Myofibroblast; Proliferation

Indexed keywords

CARBON TETRACHLORIDE; CD11B ANTIGEN; CELL SURFACE PROTEIN; GELATINASE B; GLYCOPROTEIN; LY 6C PROTEIN; MACROPHAGE ELASTASE; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; LIVER FIBROSIS; MACROPHAGE; MALE; MICROARRAY ANALYSIS; MONOCYTE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, LY; CARBON TETRACHLORIDE; CARBON TETRACHLORIDE POISONING; GENE EXPRESSION REGULATION; INSULIN-LIKE GROWTH FACTOR I; LIVER CIRRHOSIS; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 12; MATRIX METALLOPROTEINASE 9; MICE; MICE, TRANSGENIC; MONOCYTES;

MURINAE; MUS MUSCULUS;

EID: 84869208905     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1119964109     Document Type: Article

References (60)

1. Hayden T (2011) Scarred by disease. Nat Med 17(1):18-20.
2. Wynn TA (2008) Cellular and molecular mechanisms of fibrosis. J Pathol 214(2):199-210.
3. Ramachandran P, Iredale JP (2009) Reversibility of liver fibrosis. Ann Hepatol 8(4):283-291.
4. Eddy AA (2005) Can renal fibrosis be reversed? Pediatr Nephrol 20(10):1369-1375.
5. Pickrell JA, Diel JH, Slauson DO, Halliwell WH, Mauderly JL (1983) Radiation-induced pulmonary fibrosis resolves spontaneously if dense scars are not formed. Exp Mol Pathol 38(1):22-32.
6. Gibbons MA, et al. (2011) Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis. Am J Respir Crit Care Med 184(5):569-581.
7. Tyralla K, et al. (2011) High-dose enalapril treatment reverses myocardial fibrosis in experimental uremic cardiomyopathy. PLoS One 6(1):e15287.
8. Wynn TA, Barron L (2010) Macrophages: Master regulators of inflammation and fibrosis. Semin Liver Dis 30(3):245-257.
9. Vernon MA, Mylonas KJ, Hughes J (2010) Macrophages and renal fibrosis. Semin Nephrol 30(3):302-317.
10. Hardie WD, Glasser SW, Hagood JS (2009) Emerging concepts in the pathogenesis of lung fibrosis. Am J Pathol 175(1):3-16.
11. Duffield JS, et al. (2005) Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest 115(1):56-65.
12. Fallowfield JA, et al. (2007) Scar-associated macrophages are a major source of hepatic matrix metalloproteinase-13 and facilitate the resolution of murine hepatic fibrosis. J Immunol 178(8):5288-5295.
13. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8(12):958-969.
14. Mantovani A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12):677-686.
15. Gordon S, Taylor PR (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5(12):953-964.
16. Ingersoll MA, et al. (2010) Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 115(3):e10-e19.
17. Lin SL, Castaño AP, Nowlin BT, Lupher ML, Jr., Duffield JS (2009) Bone marrow Ly6Chigh monocytes are selectively recruited to injured kidney and differentiate into functionally distinct populations. J Immunol 183(10):6733-6743.
18. Nahrendorf M, et al. (2007) The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 204(12):3037-3047.
19. Arnold L, et al. (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204(5):1057-1069.
20. Movahedi K, et al. (2010) Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 70(14):5728-5739.
21. Karlmark KR, et al. (2009) Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50(1):261-274.
22. Holt MP, Cheng L, Ju C (2008) Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J Leukoc Biol 84(6):1410-1421.
23. Cortez-Retamozo V, et al. (2008) Real-time assessment of inflammation and treatment response in a mouse model of allergic airway inflammation. J Clin Invest 118(12):4058-4066.
24. Sunderkötter C, et al. (2004) Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 172(7):4410-4417.
25. Bamboat ZM, et al. (2010) Conventional DCs reduce liver ischemia/reperfusion injury in mice via IL-10 secretion. J Clin Invest 120(2):559-569.
26. Jiao J, et al. (2012) Dendritic cell regulation of carbon tetrachloride-induced murine liver fibrosis regression. Hepatology 55(1):244-255.
27. Hume DA (2008) Macrophages as APC and the dendritic cell myth. J Immunol 181(9): 5829-5835.
28. Phythian-Adams AT, et al. (2010) CD11c depletion severely disrupts Th2 induction and development in vivo. J Exp Med 207(10):2089-2096.
29. Tacke F, et al. (2006) Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J Exp Med 203(3):583-597.
30. Tacke F, et al. (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 117(1):185-194.
31. Jenkins SJ, et al. (2011) Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332(6035):1284-1288.
32. 3CR1 protects against liver fibrosis by controlling differentiation and survival of infiltrating hepatic monocytes. Hepatology 52(5):1769-1782.
33. Heinrichs D, et al. (2011) Macrophage migration inhibitory factor (MIF) exerts antifibrotic effects in experimental liver fibrosis via CD74. Proc Natl Acad Sci USA 108(42):17444-17449.
34. Breitkopf K, et al. (2005) Thrombospondin 1 acts as a strong promoter of transforming growth factor beta effects via two distinct mechanisms in hepatic stellate cells. Gut 54(5):673-681.
35. Sobrevals L, et al. (2010) Insulin-like growth factor I gene transfer to cirrhotic liver induces fibrolysis and reduces fibrogenesis leading to cirrhosis reversion in rats. Hepatology 51(3):912-921.
36. Dennis G, Jr., et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4(5):3.
37. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.
38. Anstee QM, Wright M, Goldin R, Thursz MR (2009) Parenchymal extinction: Coagulation and hepatic fibrogenesis. Clin Liver Dis 13(1):117-126.
39. Sahin H, Trautwein C, Wasmuth HE (2010) Functional role of chemokines in liver disease models. Nat Rev Gastroenterol Hepatol 7(12):682-690.
40. Lawrence T, Natoli G (2011) Transcriptional regulation of macrophage polarization: Enabling diversity with identity. Nat Rev Immunol 11(11):750-761.
41. Martinez FO, Gordon S, Locati M, Mantovani A (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: New molecules and patterns of gene expression. J Immunol 177(10):7303-7311.
42. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: Clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2(12):965-975.
43. Henson PM, Bratton DL, Fadok VA (2001) Apoptotic cell removal. Curr Biol 11(19):R795-R805.
44. Newman SL, Henson JE, Henson PM (1982) Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages. J Exp Med 156(2):430-442.
45. Marim FM, Silveira TN, Lima DS, Jr., Zamboni DS (2010) A method for generation of bone marrow-derived macrophages from cryopreserved mouse bone marrow cells. PLoS One 5(12):e15263.
46. Ferenbach DA, et al. (2010) Macrophages expressing heme oxygenase-1 improve renal function in ischemia/reperfusion injury. Mol Ther 18(9):1706-1713.
47. Kurosaka K, Takahashi M, Kobayashi Y (2003) Activation of extracellular signal-regulated kinase 1/2 is involved in production of CXC-chemokine by macrophages during phagocytosis of late apoptotic cells. Biochem Biophys Res Commun 306(4):1070-1074.
48. Chung EY, et al. (2007) Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity 27(6):952-964.
49. Raza SL, Nehring LC, Shapiro SD, Cornelius LA (2000) Proteinase-activated receptor-1 regulation of macrophage elastase (MMP-12) secretion by serine proteinases. J Biol Chem 275(52):41243-41250.
50. Valledor AF, Comalada M, Xaus J, Celada A (2000) The differential time-course of extracellular-regulated kinase activity correlates with the macrophage response toward proliferation or activation. J Biol Chem 275(10):7403-7409.
51. Chi H, et al. (2006) Dynamic regulation of pro- and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc Natl Acad Sci USA 103(7):2274-2279.
52. Perry DG, Martin WJ, 2nd (1995) Fluorescent liposomes as quantitative markers of phagocytosis by alveolar macrophages. J Immunol Methods 181(2):269-285.
53. Ma HM, Wu Z, Nakanishi H (2011) Phosphatidylserine-containing liposomes suppress inflammatory bone loss by ameliorating the cytokine imbalance provoked by infiltrated macrophages. Lab Invest 91(6):921-931.
54. Harel-Adar T, et al. (2011) Modulation of cardiac macrophages by phosphatidylserine-presenting liposomes improves infarct repair. Proc Natl Acad Sci USA 108(5):1827-1832.
55. Friedman SL (2005) Mac the knife? Macrophages - the double-edged sword of hepatic fibrosis. J Clin Invest 115(1):29-32.
56. Wynn TA (2011) Integrating mechanisms of pulmonary fibrosis. J Exp Med 208(7):1339-1350.
57. Vielhauer V, Kulkarni O, Reichel CA, Anders HJ (2010) Targeting the recruitment of monocytes and macrophages in renal disease. Semin Nephrol 30(3):318-333.
58. Mitchell C, et al. (2009) Dual role of CCR2 in the constitution and the resolution of liver fibrosis in mice. Am J Pathol 174(5):1766-1775.
59. O'Connor RA, Leech MD, Suffner J, Hämmerling GJ, Anderton SM (2010) Myelin-reactive, TGF-β-induced regulatory T cells can be programmed to develop Th1-like effector function but remain less proinflammatory than myelin-reactive Th1 effectors and can suppress pathogenic T cell clonal expansion in vivo. J Immunol 185(12):7235-7243.
60. Van Rooijen N, Sanders A (1994) Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applications. J Immunol Methods 174(1-2):83-93.