Hepatic localization of macrophage phenotypes during fibrogenesis and resolution of fibrosis in mice and humans

Frontiers in Immunology

Volumn 5, Issue SEP, 2014, Pages

  Beljaars, Leonie ^a   Schippers, Marlies ^a   Reker Smit, Catharina ^a   Martinez, Fernando O ^b   Helming, Laura ^c   Poelstra, Klaas ^a   Melgert, Barbro N ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cirrhosis; Fibrosis; IL 12; IRF 5; M1; M2; Resolution; TGM 2

Indexed keywords

EOSINOPHIL CHEMOTACTIC FACTOR; GELATINASE B; INTERFERON REGULATORY FACTOR 5; INTERLEUKIN 12; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MANNOSE RECEPTOR; MATRIX METALLOPROTEINASE; MESSENGER RNA; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FIBROGENESIS; FLOW CYTOMETRY; GENETIC ANALYSIS; HUMAN; HUMAN TISSUE; IMMUNITY; IMMUNOHISTOCHEMISTRY; LIVER FIBROSIS; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MALE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TISSUE PREPARATION; WESTERN BLOTTING;

EID: 84919461055     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00430     Document Type: Article

References (48)

1. Pinzani M, Rombouts K, Colagrande S. Fibrosis in chronic liver diseases: diagnosis and management. J Hepatol (2005) 42(Suppl 1):S22-36. doi:10.1016/j.jhep.2004.12.008
2. Friedman SL. Evolving challenges in hepatic fibrosis. Nat Rev Gastroenterol Hepatol (2010) 7(8):425-36. doi:10.1038/nrgastro.2010.97
3. Ramachandran P, Iredale JP. Macrophages: central regulators of hepatic fibrogenesis and fibrosis resolution. J Hepatol (2012) 56(6):1417-9. doi:10.1016/j.jhep.2011.10.026
4. Heymann F, Trautwein C, Tacke F. Monocytes and macrophages as cellular targets in liver fibrosis. Inflamm Allergy Drug Targets (2009) 8(4):307-18. doi:10.2174/187152809789352230
5. Wynn TA, Barron L. Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis (2010) 30(3):245-57. doi:10.1055/s-0030-1255354
6. Ramachandran P, Pellicoro A, Vernon MA, Boulter L, Aucott RL, Ali A, et al. Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis. Proc Natl Acad Sci U S A (2012) 109(46):E3186-95. doi:10.1073/pnas.1119964109
7. Sica A, Invernizzi P, Mantovani A. Macrophage plasticity and polarization in liver homeostasis and pathology. Hepatology (2014) 59(5):2034-42. doi:10.1002/hep.26754
8. Duffield JS, Forbes SJ, Constandinou CM, Clay S, Partolina M, Vuthoori S, et al. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest (2005) 115(1):56-65. doi:10.1172/JCI22675
9. Fallowfield JA, Mizuno M, Kendall TJ, Constandinou CM, Benyon RC, Duffield JS, et al. Scar-associated macrophages are a major source of hepatic matrix metalloproteinase-13 and facilitate the resolution of murine hepatic fibrosis. J Immunol (2007) 178(8):5288-95. doi:10.4049/jimmunol.178.8.5288
10. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity (2010) 32(5):593-604. doi:10.1016/j.immuni.2010.05.007
11. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol (2004) 25(12):677-86. doi:10.1016/j.it.2004.09.015
12. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci (2008) 13:453-61. doi:10.2741/2692
13. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol (2008) 8(12):958-69. doi:10.1038/nri2448
14. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol (2013) 229(2):176-85. doi:10.1002/path.4133
15. Mills CD, Ley K. M1 and M2 macrophages: the chicken and the egg of immunity. J Innate Immun (2014). doi:10.1159/000364945
16. Huang WC, Sala-Newby GB, Susana A, Johnson JL, Newby AC. Classical macrophage activation up-regulates several matrix metalloproteinases through mitogen activated protein kinases and nuclear factor-kappaB. PLoS One (2012) 7(8):e42507. doi:10.1371/journal.pone.0042507
17. Song E, Ouyang N, Horbelt M, Antus B, Wang M, Exton MS. Influence of alternatively and classically activated macrophages on fibrogenic activities of human fibroblasts. Cell Immunol (2000) 204(1):19-28. doi:10.1006/cimm.2000.1687
18. Lopez-Navarrete G, Ramos-Martinez E, Suarez-Alvarez K, Aguirre-Garcia J, Ledezma-Soto Y, Leon-Cabrera S, et al. Th2-associated alternative Kupffer cell activation promotes liver fibrosis without inducing local inflammation. Int J Biol Sci (2011) 7(9):1273-86. doi:10.7150/ijbs.7.1273
19. Gibbons M, MacKinnon A, Ramachandran P, Dhaliwal K, Duffin R, Phythian-Adams A, et al. Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis. Am J Respir Crit Care Med (2011) 184(5):569-81. doi:10.1164/rccm.201010-1719OC
20. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med (2012) 18(7):1028-40. doi:10.1038/nm.2807
21. Boorsma CE, Draijer C, Melgert BN. Macrophage heterogeneity in respiratory diseases. Mediators Inflamm (2013) 769214:19. doi:10.1155/2013/769214
22. Lopez-Guisa JM, Cai X, Collins SJ, Yamaguchi I, Okamura DM, Bugge TH, et al. Mannose receptor 2 attenuates renal fibrosis. J Am Soc Nephrol (2012) 23(2):236-51. doi:10.1681/ASN.2011030310
23. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, et al. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog (2009) 5(4):e1000371. doi:10.1371/journal.ppat.1000371
24. Louvet A, Teixeira-Clerc F, Chobert MN, Deveaux V, Pavoine C, Zimmer A, et al. Cannabinoid CB2 receptors protect against alcoholic liver disease by regulating Kupffer cell polarization in mice. Hepatology (2011) 54(4):1217-26. doi:10.1002/hep.24524
25. Randolph GJ. Proliferating macrophages prevail in atherosclerosis. Nat Med (2013) 19(9):1094-5. doi:10.1038/nm.3316
26. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, et al. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol (2011) 12(3):231-8. doi:10.1038/ni.1990
27. Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, et al. Towards a knowledge-based human protein atlas. Nat Biotechnol (2010) 28(12):1248-50. doi:10.1038/nbt1210-1248
28. Vos TA, Van Goor H, Tuyt L, De Jager-Krikken A, Leuvenink R, Kuipers F, et al. Expression of inducible nitric oxide synthase in endotoxemic rat hepatocytes is dependent on the cellular glutathione status. Hepatology (1999) 29(2):421-6. doi:10.1002/hep.510290231
29. Raes G, Van den Bergh R, De Baetselier P, Ghassabeh GH, Scotton C, Locati M, et al. Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells. J Immunol (2005) 174(11):6561. doi:10.4049/jimmunol.174.11.6561
30. Raes G, De Baetselier P, Noel W, Beschin A, Brombacher F, Hassanzadeh Gh G. Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol (2002) 71(4):597-602.
31. Van Gorp H, Delputte PL, Nauwynck HJ. Scavenger receptor CD163, a Jack-of-all-trades and potential target for cell-directed therapy. Mol Immunol (2010) 47(7-8):1650-60. doi:10.1016/j.molimm.2010.02.008
32. Melgert BN, ten Hacken NH, Rutgers B, Timens W, Postma DS, Hylkema MN. More alternative activation of macrophages in lungs of asthmatic patients. J Allergy Clin Immunol (2011) 127(3):831-3. doi:10.1016/j.jaci.2010.10.045
33. Martinez FO, Helming L, Milde R, Varin A, Melgert BN, Draijer C, et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood (2013) 121(9):e57-69. doi:10.1182/blood-2012-06-436212
34. Beljaars L, Molema G, Weert B, Bonnema H, Olinga P, Groothuis GM, et al. Albumin modified with mannose 6-phosphate: a potential carrier for selective delivery of antifibrotic drugs to rat and human hepatic stellate cells. Hepatology (1999) 29(5):1486-93. doi:10.1002/hep.510290526
35. Iredale JP. Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J Clin Invest (2007) 117(3):539-48. doi:10.1172/JCI30542
36. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol (2011) 11(11):723-37. doi:10.1038/nri3073
37. Hanania R, Sun HS, Xu K, Pustylnik S, Jeganathan S, Harrison RE. Classically activated macrophages use stable microtubules for matrix metalloproteinase-9 (MMP-9) secretion. J Biol Chem (2012) 287(11):8468-83. doi:10.1074/jbc.M111.290676
38. Belkin AM. Extracellular TG2: emerging functions and regulation. FEBS J (2011) 278(24):4704-16. doi:10.1111/j.1742-4658.2011.08346.x
39. Fesus L, Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci (2002) 27(10):534-9. doi:10.1016/S0968-0004(02)02182-5
40. Fesus L, Szondy Z. Transglutaminase 2 in the balance of cell death and survival. FEBS Lett (2005) 579(15):3297-302. doi:10.1016/j.febslet.2005.03.063
41. Popov Y, Sverdlov DY, Sharma AK, Bhaskar KR, Li S, Freitag TL, et al. Tissue transglutaminase does not affect fibrotic matrix stability or regression of liver fibrosis in mice. Gastroenterology (2011) 140(5):1642-52. doi:10.1053/j.gastro.2011.01.040
42. Guilliams M, Ginhoux F, Jakubzick C, Naik SH, Onai N, Schraml BU, et al. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol (2014) 14(8):571-8. doi:10.1038/nri3712
43. Liaskou E, Zimmermann HW, Li KK, Oo YH, Suresh S, Stamataki Z, et al. Monocyte subsets in human liver disease show distinct phenotypic and functional characteristics. Hepatology (2013) 57(1):385-98. doi:10.1002/hep.26016
44. Tacke F, Zimmermann HW. Macrophage heterogeneity in liver injury and fibrosis. J Hepatol (2014) 60(5):1090-6. doi:10.1016/j.jhep.2013.12.025
45. Nelson MP, Christmann BS, Dunaway CW, Morris A, Steele C. Experimental pneumocystis lung infection promotes M2a alveolar macrophage-derived MMP12 production. Am J Physiol Lung Cell Mol Physiol (2012) 303(5):L469-75. doi:10.1152/ajplung.00158.2012
46. Madala SK, Pesce JT, Ramalingam TR, Wilson MS, Minnicozzi S, Cheever AW, et al. Matrix metalloproteinase 12-deficiency augments extracellular matrix degrading metalloproteinases and attenuates IL-13-dependent fibrosis. J Immunol (2010) 184(7):3955-63. doi:10.4049/jimmunol.0903008
47. Dalli J, Serhan CN. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood (2012) 120(15):e60-72. doi:10.1182/blood-2012-04-423525
48. Morimoto K, Janssen WJ, Terada M. Defective efferocytosis by alveolar macrophages in IPF patients. Respir Med (2012) 106(12):1800-3. doi:10.1016/j.rmed.2012.08.020