Ly6C Monocyte Recruitment Is Responsible for Th2 Associated Host-Protective Macrophage Accumulation in Liver Inflammation due to Schistosomiasis

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Schistosomiasis is an important neglected tropical disease caused by parasitic worms of the genus Schistosoma. During infection with S. mansoni, parasite eggs become trapped in the liver and elicit granulomatous inflammation characterized by accumulations of immune cells intermixed with liver cells around the eggs. This inflammation is responsible for disease symptoms, but also plays an important role in protecting the host against liver damage that can be caused by egg products. Granulomas, by definition, contain a significant number of macrophages (phagocytic cells of the immune system). Recent work has emphasized that macrophage numbers in inflammation can increase due either to recruitment of precursor cells (called monocytes) from the blood, or as a result of proliferation of tissue-resident macrophages. Local proliferation has been noted in other worm infections, during which the immune response is Th2-like and IL-4 produced by Th2 cells promotes macrophages to become “alternatively (or M2) activated”. We examined the origin of the increased numbers of macrophages in liver inflammation due to schistosomiasis, in which there is also a prominent Th2 response. We found that the cells mostly originated from monocytes recruited into the tissue from the blood. This response was critical for host survival during infection.

Vyšlo v časopise: Ly6C Monocyte Recruitment Is Responsible for Th2 Associated Host-Protective Macrophage Accumulation in Liver Inflammation due to Schistosomiasis. PLoS Pathog 10(8): e32767. doi:10.1371/journal.ppat.1004282
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004282

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Zdroje

1. FairfaxK, NascimentoM, HuangSC, EvertsB, PearceEJ (2012) Th2 responses in schistosomiasis. Semin Immunopathol 34 : 863–871.

2. AuffrayC, SiewekeMH, GeissmannF (2009) Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol 27 : 669–692.

3. SerbinaNV, JiaT, HohlTM, PamerEG (2008) Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26 : 421–452.

4. SerbinaNV, ShiC, PamerEG (2012) Monocyte-mediated immune defense against murine Listeria monocytogenes infection. Adv Immunol 113 : 119–134.

5. JenkinsSJ, RuckerlD, CookPC, JonesLH, FinkelmanFD, et al. (2011) Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332 : 1284–1288.

6. JenkinsSJ, RuckerlD, ThomasGD, HewitsonJP, DuncanS, et al. (2013) IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J Exp Med 210 : 2477–2491.

7. MartinezFO, HelmingL, GordonS (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27 : 451–483.

8. ChawlaA, NguyenKD, GohYP (2011) Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 11 : 738–749.

9. AllenJE, WynnTA (2011) Evolution of Th2 immunity: a rapid repair response to tissue destructive pathogens. PLoS Pathog 7: e1002003.

10. BrunetLR, FinkelmanFD, CheeverAW, KopfMA, PearceEJ (1997) IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. J Immunol 159 : 777–785.

11. FallonPG, RichardsonEJ, McKenzieGJ, McKenzieAN (2000) Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J Immunol 164 : 2585–2591.

12. HerbertDR, HolscherC, MohrsM, ArendseB, SchwegmannA, et al. (2004) Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20 : 623–635.

13. NairMG, DuY, PerrigoueJG, ZaphC, TaylorJJ, et al. (2009) Alternatively activated macrophage-derived RELM-{alpha} is a negative regulator of type 2 inflammation in the lung. J Exp Med 206 : 937–952.

14. PesceJT, RamalingamTR, Mentink-KaneMM, WilsonMS, El KasmiKC, et al. (2009) Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog 5: e1000371.

15. PesceJT, RamalingamTR, WilsonMS, Mentink-KaneMM, ThompsonRW, et al. (2009) Retnla (relmalpha/fizz1) suppresses helminth-induced Th2-type immunity. PLoS Pathog 5: e1000393.

16. GeissmannF, JungS, LittmanDR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19 : 71–82.

17. PearceEJ, MacDonaldAS (2002) The immunobiology of schistosomiasis. Nat Rev Immunol 2 : 499–511.

18. CheeverAW, HoffmannKF, WynnTA (2000) Immunopathology of schistosomiasis mansoni in mice and men. Immunol Today 21 : 465–466.

19. GautierEL, ShayT, MillerJ, GreterM, JakubzickC, 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.

20. SungSS, FuSM, RoseCEJr, GaskinF, JuST, et al. (2006) A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol 176 : 2161–2172.

21. SwirskiFK, NahrendorfM, EtzrodtM, WildgruberM, Cortez-RetamozoV, et al. (2009) Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325 : 612–616.

22. JungS, AlibertiJ, GraemmelP, SunshineMJ, KreutzbergGW, et al. (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.

23. BroadhurstMJ, LeungJM, LimKC, GirgisNM, GundraUM, et al. (2012) Upregulation of retinal dehydrogenase 2 in alternatively activated macrophages during retinoid-dependent type-2 immunity to helminth infection in mice. PLoS Pathog 8: e1002883.

24. TsouCL, PetersW, SiY, SlaymakerS, AslanianAM, et al. (2007) Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117 : 902–909.

25. HohlTM, RiveraA, LipumaL, GallegosA, ShiC, et al. (2009) Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 6 : 470–481.

26. FairfaxKC, AmielE, KingIL, FreitasTC, MohrsM, et al. (2012) IL-10R blockade during chronic schistosomiasis mansoni results in the loss of B cells from the liver and the development of severe pulmonary disease. PLoS Pathog 8: e1002490.

27. DewalsBG, MarillierRG, HovingJC, LeetoM, SchwegmannA, et al. (2010) IL-4Ralpha-independent expression of mannose receptor and Ym1 by macrophages depends on their IL-10 responsiveness. PLoS Negl Trop Dis 4: e689.

28. BarronL, WynnTA (2011) Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. Eur J Immunol 41 : 2509–2514.

29. ChensueSW, WarmingtonKS, LukacsNW, LincolnPM, BurdickMD, et al. (1995) Monocyte chemotactic protein expression during schistosome egg granuloma formation. Sequence of production, localization, contribution, and regulation. Am J Pathol 146 : 130–138.

30. WarmingtonKS, BoringL, RuthJH, SonsteinJ, HogaboamCM, et al. (1999) Effect of C-C chemokine receptor 2 (CCR2) knockout on type-2 (schistosomal antigen-elicited) pulmonary granuloma formation: analysis of cellular recruitment and cytokine responses. Am J Pathol 154 : 1407–1416.

31. LuB, RutledgeBJ, GuL, FiorilloJ, LukacsNW, et al. (1998) Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J Exp Med 187 : 601–608.

32. RameshM, PaciorkowskiN, DashY, ShultzL, RajanTV (2007) Acute but not chronic macrophage recruitment in filarial infections in mice is dependent on C-C chemokine ligand 2. Parasite Immunol 29 : 395–404.

33. SchwartzRH (2003) T cell anergy. Annu Rev Immunol 21 : 305–334.

34. RobbenPM, LaReginaM, KuzielWA, SibleyLD (2005) Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J Exp Med 201 : 1761–1769.

35. CheongC, MatosI, ChoiJH, DandamudiDB, ShresthaE, et al. (2010) Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 143 : 416–429.

36. AuffrayC, FoggD, GarfaM, ElainG, Join-LambertO, et al. (2007) Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317 : 666–670.

37. EgawaM, MukaiK, YoshikawaS, IkiM, MukaidaN, et al. (2013) Inflammatory Monocytes Recruited to Allergic Skin Acquire an Anti-inflammatory M2 Phenotype via Basophil-Derived Interleukin-4. Immunity 38 (3) 570–80.

38. SchulzC, Gomez PerdigueroE, ChorroL, Szabo-RogersH, CagnardN, et al. (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336 : 86–90.

39. MurrayPJ, WynnTA (2011) Obstacles and opportunities for understanding macrophage polarization. J Leukoc Biol 89 : 557–563.

40. LinehanSA, CoulsonPS, WilsonRA, MountfordAP, BrombacherF, et al. (2003) IL-4 receptor signaling is required for mannose receptor expression by macrophages recruited to granulomata but not resident cells in mice infected with Schistosoma mansoni. Lab Invest 83 : 1223–1231.

41. ThomasGD, RuckerlD, MaskreyBH, WhitfieldPD, BlaxterML, et al. (2012) The biology of nematode -⁠ and IL4Ralpha-dependent murine macrophage polarization in vivo as defined by RNA-Seq and targeted lipidomics. Blood 120: e93–e104.

42. PearceEJ, CasparP, GrzychJM, LewisFA, SherA (1991) Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med 173 : 159–166.