The CD14CD16 Inflammatory Monocyte Subset Displays Increased Mitochondrial Activity and Effector Function During Acute Malaria

English version České info

Malaria, caused by a protozoa parasite, Plasmodium, affects more than 200 million people per year. The infection triggers an acute febrile illness, the paroxysms, occurring every 48 or 72 hours depending on the species. Plasmodium vivax, in most cases, does not cause severe malaria, but it is the most geographically widespread parasite responsible for human disease and causes substantial costs to individuals and governments. Once the parasite reaches the blood stream, they infect reticulocytes that can be destroyed by phagocytes. Our goal was to assess the importance of monocyte subsets during malaria. We found that P. vivax infection causes an increase in frequency of circulating monocytes, which were defined as classical, inflammatory, and patrolling, based on the expression of membrane molecules. Classical and inflammatory monocytes produced higher levels of pro-inflammatory cytokines and were distinguished from patrolling monocytes by displaying larger and more active mitochondria. Importantly, inflammatory monocytes were more efficient phagocytes; produced high levels of intracellular reactive oxygen species and TNF and consequently control better Plasmodium vivax infection. Hence, our results support the hypothesis that CD14+CD16+ monocytes display effector functions involved in parasite control during malaria.

Vyšlo v časopise: The CD14CD16 Inflammatory Monocyte Subset Displays Increased Mitochondrial Activity and Effector Function During Acute Malaria. PLoS Pathog 10(9): e32767. doi:10.1371/journal.ppat.1004393
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004393

Souhrn

Zdroje

1. GethingPW, ElyazarIR, MoyesCL, SmithDL, BattleKE, et al. (2012) A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis 6: e1814.

2. LanghorneJ, NdunguFM, SponaasAM, MarshK (2008) Immunity to malaria: more questions than answers. Nat Immunol 9: 725–732.

3. SpencePJ, LanghorneJ (2012) T cell control of malaria pathogenesis. Curr Opin Immunol 24: 444–448.

4. MuellerI, GalinskiMR, BairdJK, CarltonJM, KocharDK, et al. (2009) Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555–566.

5. LeorattiFM, TrevelinSC, CunhaFQ, RochaBC, CostaPA, et al. (2012) Neutrophil paralysis in Plasmodium vivax malaria. PLoS Negl Trop Dis 6: e1710.

6. GazzinelliRT, DenkersEY (2006) Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat Rev Immunol 6: 895–906.

7. TakeuchiO, AkiraS (2010) Pattern recognition receptors and inflammation. Cell 140: 805–820.

8. FranklinBS, ParrocheP, AtaideMA, LauwF, RopertC, et al. (2009) Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Natl Acad Sci U S A 106: 5789–5794.

9. ParrocheP, LauwFN, GoutagnyN, LatzE, MonksBG, et al. (2007) Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci U S A 104: 1919–1924.

10. SharmaS, DeOliveiraRB, KalantariP, ParrocheP, GoutagnyN, et al. (2011) Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity 35: 194–207.

11. KwiatkowskiD, HillAV, SambouI, TwumasiP, CastracaneJ, et al. (1990) TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336: 1201–1204.

12. McCallMB, NeteaMG, HermsenCC, JansenT, JacobsL, et al. (2007) Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. J Immunol 179: 162–171.

13. AntonelliLR, Gigliotti RothfuchsA, GoncalvesR, RoffeE, CheeverAW, et al. (2010) Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J Clin Invest 120: 1674–1682.

14. GoncalvesR, ZhangX, CohenH, DebrabantA, MosserDM (2011) Platelet activation attracts a subpopulation of effector monocytes to sites of Leishmania major infection. J Exp Med 208: 1253–1265.

15. SerbinaNV, ChernyM, ShiC, BleauSA, CollinsNH, et al. (2009) Distinct responses of human monocyte subsets to Aspergillus fumigatus conidia. J Immunol 183: 2678–2687.

16. PasslickB, FliegerD, Ziegler-HeitbrockHW (1989) Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 74: 2527–2534.

17. GordonS, TaylorPR (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953–964.

18. CrosJ, CagnardN, WoollardK, PateyN, ZhangSY, et al. (2010) Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33: 375–386.

19. ZawadaAM, RogacevKS, RotterB, WinterP, MarellRR, et al. (2011) SuperSAGE evidence for CD14++CD16+ monocytes as a third monocyte subset. Blood 118: e50–61.

20. KanekoO, KimuraM, KawamotoF, FerreiraMU, TanabeK (1997) Plasmodium falciparum: allelic variation in the merozoite surface protein 1 gene in wild isolates from southern Vietnam. Exp Parasitol 86: 45–57.

21. IhalamullaRL, MendisKN (1987) Plasmodium vivax: isolation of mature asexual stages and gametocytes from infected human blood by colloidal silica (Percoll) gradient centrifugation. Trans R Soc Trop Med Hyg 81: 25–28.

22. CarvalhoBO, LopesSC, NogueiraPA, OrlandiPP, BargieriDY, et al. (2010) On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J Infect Dis 202: 638–647.

23. Chiarini-GarciaH, HornickJR, GriswoldMD, RussellLD (2001) Distribution of type A spermatogonia in the mouse is not random. Biol Reprod 65: 1179–1185.

24. Chiarini-GarciaH, RussellLD (2002) Characterization of mouse spermatogonia by transmission electron microscopy. Reproduction 123: 567–577.

25. GeissGK, BumgarnerRE, BirdittB, DahlT, DowidarN, et al. (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26: 317–325.

26. DixitE, BoulantS, ZhangY, LeeAS, OdendallC, et al. (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141: 668–681.

27. GripO, BredbergA, LindgrenS, HenrikssonG (2007) Increased subpopulations of CD16(+) and CD56(+) blood monocytes in patients with active Crohn's disease. Inflamm Bowel Dis 13: 566–572.

28. 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.

29. LambethJD (2004) Nox enzymes and the biology of reactive oxygen. Nature Reviews Immunology 4: 181–189.

30. BalabanRS, NemotoS, FinkelT (2005) Mitochondria, oxidants, and aging. Cell 120: 483–495.

31. ChanceB, SiesH, BoverisA (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527–605.

32. BalabanRS, NemotoS, FinkelT (2005) Mitochondria, oxidants, and aging. Cell 120: 483–495.

33. HightonJ, CarlisleB, PalmerDG (1995) Changes in the phenotype of monocytes/macrophages and expression of cytokine mRNA in peripheral blood and synovial fluid of patients with rheumatoid arthritis. Clin Exp Immunol 102: 541–546.

34. PhillipsRJ, LutzM, PremackB (2005) Differential signaling mechanisms regulate expression of CC chemokine receptor-2 during monocyte maturation. J Inflamm (Lond) 2: 14.

35. TrialJ, BirdsallHH, HallumJA, CraneML, Rodriguez-BarradasMC, et al. (1995) Phenotypic and functional changes in peripheral blood monocytes during progression of human immunodeficiency virus infection. Effects of soluble immune complexes, cytokines, subcellular particulates from apoptotic cells, and HIV-1-encoded proteins on monocytes phagocytic function, oxidative burst, transendothelial migration, and cell surface phenotype. J Clin Invest 95: 1690–1701.

36. TurriniF, GinsburgH, BussolinoF, PescarmonaGP, SerraMV, et al. (1992) Phagocytosis of Plasmodium-Falciparum-Infected Human Red-Blood-Cells by Human Monocytes - Involvement of Immune and Nonimmune Determinants and Dependence on Parasite Developmental Stage. Blood 80: 801–808.

37. BuluaAC, SimonA, MaddipatiR, PelletierM, ParkH, et al. (2011) Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). Journal of Experimental Medicine 208: 519–533.

38. HancockJT, JonesOTG (1987) The Inhibition by Diphenyleneiodonium and Its Analogs of Superoxide Generation by Macrophages. Biochemical Journal 242: 103–107.

39. StuehrDJ, FasehunOA, KwonNS, GrossSS, GonzalezJA, et al. (1991) Inhibition of Macrophage and Endothelial-Cell Nitric-Oxide Synthase by Diphenyleneiodonium and Its Analogs. Faseb Journal 5: 98–103.

40. OthoroC, LalAA, NahlenB, KoechD, OragoAS, et al. (1999) A low interleukin-10 tumor necrosis factor-alpha ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J Infect Dis 179: 279–282.

41. KurtzhalsJA, AdabayeriV, GokaBQ, AkanmoriBD, Oliver-CommeyJO, et al. (1998) Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet 351: 1768–1772.

42. AndradeBB, Reis-FilhoA, Souza-NetoSM, ClarencioJ, CamargoLM, et al. (2010) Severe Plasmodium vivax malaria exhibits marked inflammatory imbalance. Malar J 9: 13.

43. SkorokhodOA, AlessioM, MordmullerB, AreseP, SchwarzerE (2004) Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. J Immunol 173: 4066–4074.

44. Ziegler-HeitbrockL, AncutaP, CroweS, DalodM, GrauV, et al. (2010) Nomenclature of monocytes and dendritic cells in blood. Blood 116: e74–80.

45. FadiniGP, CappellariR, MazzucatoM, AgostiniC, Vigili de KreutzenbergS, et al. (2013) Monocyte-macrophage polarization balance in pre-diabetic individuals. Acta Diabetol 50: 977–982.

46. MantovaniA, GarlandaC, LocatiM (2009) Macrophage diversity and polarization in atherosclerosis: a question of balance. Arterioscler Thromb Vasc Biol 29: 1419–1423.

47. SponaasAM, Freitas do RosarioAP, VoisineC, MastelicB, ThompsonJ, et al. (2009) Migrating monocytes recruited to the spleen play an important role in control of blood stage malaria. Blood 114: 5522–5531.

48. FernandesAA, CarvalhoLJ, ZaniniGM, VenturaAM, SouzaJM, et al. (2008) Similar cytokine responses and degrees of anemia in patients with Plasmodium falciparum and Plasmodium vivax infections in the Brazilian Amazon region. Clin Vaccine Immunol 15: 650–658.

49. NylenS, MauryaR, EidsmoL, Das ManandharK, SundarS, et al. (2007) Splenic accumulation of IL-10 mRNA in T cells distinct from CD4(+) CD25(+) (Foxp3) regulatory T cells in human visceral leishmaniasis. Journal of Experimental Medicine 204: 805–817.

50. AndersonCF, OukkaM, KuchrooVJ, SacksD (2007) CD4(+)CD25(−)Foxp3(−) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. Journal of Experimental Medicine 204: 285–297.

51. RoffeE, RothfuchsAG, SantiagoHC, MarinoAPMP, Ribeiro-GomesFL, et al. (2012) IL-10 Limits Parasite Burden and Protects against Fatal Myocarditis in a Mouse Model of Trypanosoma cruzi Infection. Journal of Immunology 188: 649–660.

52. JankovicD, KullbergMC, FengCG, GoldszmidRS, CollazoCM, et al. (2007) Conventional T-bet(+)Foxp3(−) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. Journal of Experimental Medicine 204: 273–283.

53. GraingerJR, WohlfertEA, FussIJ, BouladouxN, AskenaseMH, et al. (2013) Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nature Medicine 19: 713–+.

54. NewboldC, WarnP, BlackG, BerendtA, CraigA, et al. (1997) Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am J Trop Med Hyg 57: 389–398.

55. RoweJA, ClaessensA, CorriganRA, ArmanM (2009) Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 11: e16.

56. UdomsangpetchR, ReinhardtPH, SchollaardtT, ElliottJF, KubesP, et al. (1997) Promiscuity of clinical Plasmodium falciparum isolates for multiple adhesion molecules under flow conditions. J Immunol 158: 4358–4364.

57. AyiK, PatelSN, SerghidesL, SmithTG, KainKC (2005) Nonopsonic phagocytosis of erythrocytes infected with ring-stage Plasmodium falciparum. Infect Immun 73: 2559–2563.

58. McGilvrayID, SerghidesL, KapusA, RotsteinOD, KainKC (2000) Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 96: 3231–3240.

59. ChimmaP, RoussilhonC, SratongnoP, RuangveerayuthR, PattanapanyasatK, et al. (2009) A distinct peripheral blood monocyte phenotype is associated with parasite inhibitory activity in acute uncomplicated Plasmodium falciparum malaria. PLoS Pathog 5: e1000631.

60. JaworowskiA, KamwendoDD, ElleryP, SonzaS, MwapasaV, et al. (2007) CD16+ monocyte subset preferentially harbors HIV-1 and is expanded in pregnant Malawian women with Plasmodium falciparum malaria and HIV-1 infection. J Infect Dis 196: 38–42.

61. NimmerjahnF, RavetchJV (2011) FcgammaRs in health and disease. Curr Top Microbiol Immunol 350: 105–125.

62. Skrzeczynska-MoncznikJ, BzowskaM, LosekeS, Grage-GriebenowE, ZembalaM, et al. (2008) Peripheral blood CD14high CD16+ monocytes are main producers of IL-10. Scand J Immunol 67: 152–159.

63. SchwarzerE, TurriniF, UlliersD, GiribaldiG, GinsburgH, et al. (1992) Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. Journal of Experimental Medicine 176: 1033–1041.

64. SkorokhodOA, AlessioM, MordmullerB, AreseP, SchwarzerE (2004) Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. Journal of Immunology 173: 4066–4074.

65. ScorzaT, MagezS, BrysL, De BaetselierP (1999) Hemozoin is a key factor in the induction of malaria-associated immunosuppression. Parasite Immunol 21: 545–554.

66. SchwarzerE, AlessioM, UlliersD, AreseP (1998) Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infect Immun 66: 1601–1606.

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

68. KumarS, ChristophidesGK, CanteraR, CharlesB, HanYS, et al. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci U S A 100: 14139–14144.

69. MatsumotoA, BesshoH, UehiraK, SudaT (1991) Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J Electron Microsc (Tokyo) 40: 356–363.

70. SinaiAP, WebsterP, JoinerKA (1997) Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci 110 (Pt 17): 2117–2128.

71. WestAP, BrodskyIE, RahnerC, WooDK, Erdjument-BromageH, et al. (2011) TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472: 476–480.

72. OgondaLA, OragoAS, OtienoMF, AdhiamboC, OtienoW, et al. (2010) The levels of CD16/Fc gamma receptor IIIA on CD14+ CD16+ monocytes are higher in children with severe Plasmodium falciparum anemia than in children with cerebral or uncomplicated malaria. Infect Immun 78: 2173–2181.

73. AlexandreMA, FerreiraCO, SiqueiraAM, MagalhaesBL, MouraoMP, et al. (2010) Severe Plasmodium vivax malaria, Brazilian Amazon. Emerg Infect Dis 16: 1611–1614.

74. DouglasNM, AnsteyNM, BuffetPA, PoespoprodjoJR, YeoTW, et al. (2012) The anaemia of Plasmodium vivax malaria. Malar J 11: 135.

75. Rodriguez-MoralesAJ, SanchezE, VargasM, PiccoloC, ColinaR, et al. (2006) Anemia and thrombocytopenia in children with Plasmodium vivax malaria. J Trop Pediatr 52: 49–51.

76. Lewis SM, Bain BJ, Bates I (2006) Dacie and Lewis Practical Haematology. Philadelphia: Churchill Livingstone Elsevier. 736 p.

77. AncutaP, RaoR, MosesA, MehleA, ShawSK, et al. (2003) Fractalkine preferentially mediates arrest and migration of CD16+ monocytes. J Exp Med 197: 1701–1707.