Interference with the Host Haemostatic System by Schistosomes
Schistosomes, parasitic flatworms that cause the tropical disease schistosomiasis, are still a threat. They are responsible for 200 million infections worldwide and an estimated 280,000 deaths annually in sub-Saharan Africa alone. The adult parasites reside as pairs in the mesenteric or perivesicular veins of their human host, where they can survive for up to 30 years. The parasite is a potential activator of blood coagulation according to Virchow's triad, because it is expected to alter blood flow and endothelial function, leading to hypercoagulability. In contrast, hepatosplenic schistosomiasis patients are in a hypocoagulable and hyperfibrinolytic state, indicating that schistosomes interfere with the haemostatic system of their host. In this review, the interactions of schistosomes with primary haemostasis, secondary haemostasis, fibrinolysis, and the vascular tone will be discussed to provide insight into the reduction in coagulation observed in schistosomiasis patients.
Interference with the haemostatic system by pathogens is a common mechanism and has been described for other parasitic worms, bacteria, and fungi as a mechanism to support survival and spread or enhance virulence. Insight into the mechanisms used by schistosomes to interfere with the haemostatic system will provide important insight into the maintenance of the parasitic life cycle within the host. This knowledge may reveal new potential anti-schistosome drug and vaccine targets. In addition, some of the survival mechanisms employed by schistosomes might be used by other pathogens, and therefore, these mechanisms that interfere with host haemostasis might be a broad target for drug development against blood-dwelling pathogens. Also, schistosome antithrombotic or thrombolytic molecules could form potential new drugs in the treatment of haemostatic disorders.
Vyšlo v časopise:
Interference with the Host Haemostatic System by Schistosomes. PLoS Pathog 9(12): e32767. doi:10.1371/journal.ppat.1003781
Kategorie:
Review
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003781
Souhrn
Schistosomes, parasitic flatworms that cause the tropical disease schistosomiasis, are still a threat. They are responsible for 200 million infections worldwide and an estimated 280,000 deaths annually in sub-Saharan Africa alone. The adult parasites reside as pairs in the mesenteric or perivesicular veins of their human host, where they can survive for up to 30 years. The parasite is a potential activator of blood coagulation according to Virchow's triad, because it is expected to alter blood flow and endothelial function, leading to hypercoagulability. In contrast, hepatosplenic schistosomiasis patients are in a hypocoagulable and hyperfibrinolytic state, indicating that schistosomes interfere with the haemostatic system of their host. In this review, the interactions of schistosomes with primary haemostasis, secondary haemostasis, fibrinolysis, and the vascular tone will be discussed to provide insight into the reduction in coagulation observed in schistosomiasis patients.
Interference with the haemostatic system by pathogens is a common mechanism and has been described for other parasitic worms, bacteria, and fungi as a mechanism to support survival and spread or enhance virulence. Insight into the mechanisms used by schistosomes to interfere with the haemostatic system will provide important insight into the maintenance of the parasitic life cycle within the host. This knowledge may reveal new potential anti-schistosome drug and vaccine targets. In addition, some of the survival mechanisms employed by schistosomes might be used by other pathogens, and therefore, these mechanisms that interfere with host haemostasis might be a broad target for drug development against blood-dwelling pathogens. Also, schistosome antithrombotic or thrombolytic molecules could form potential new drugs in the treatment of haemostatic disorders.
Zdroje
1. KlingerMH, JelkmannW (2002) Role of blood platelets in infection and inflammation. J Interferon Cytokine Res 22: 913–922.
2. Hoffbrand AV, Pettit JE, Moss PAH (2003) Essential haematology. Hoboken: Blackwell Science. 349 p.
3. OpalSM (2003) Interactions between coagulation and inflammation. Scand J Infect Dis 35: 545–554.
4. LoweGD (2003) Virchow's triad revisited: Abnormal flow. Pathophysiol Haemost Thromb 33: 455–457.
5. BagotCN, AryaR (2008) Virchow and his triad: A question of attribution. Br J Haematol 143: 180–190.
6. WolbergAS, AlemanMM, LeidermanK, MachlusKR (2012) Procoagulant activity in hemostasis and thrombosis: Virchow's triad revisited. Anesth Analg 114: 275–285.
7. GryseelsB, PolmanK, ClerinxJ, KestensL (2006) Human schistosomiasis. Lancet 368: 1106–1118.
8. FileS (1995) Interaction of schistosome eggs with vascular endothelium. J Parasitol 81: 234–238.
9. SilvaCL, MorelN, NoelF (1998) Portal veins of mice infected with Schistosoma mansoni exhibit an increased reactivity to 5-hydroxytryptamine. Mem Inst Oswaldo Cruz 93 (Suppl 1) 153–155.
10. ColleyDG, SecorWE (2007) A schistosomiasis research agenda. PLoS Negl Trop Dis 1: e32 doi: 10.1371/journal.pntd.0000032
11. SteinPD, SabbahHN (1974) Measured turbulence and its effect on thrombus formation. Circ Res 35: 608–614.
12. JohnsonBD, MatherKJ, WallaceJP (2011) Mechanotransduction of shear in the endothelium: Basic studies and clinical implications. Vasc Med 16: 365–377.
13. DiamondSL, EskinSG, McIntireLV (1989) Fluid flow stimulates tissue plasminogen activator secretion by cultured human endothelial cells. Science 243: 1483–1485.
14. GalbuseraM, ZojaC, DonadelliR, ParisS, MorigiM, et al. (1997) Fluid shear stress modulates von willebrand factor release from human vascular endothelium. Blood 90: 1558–1564.
15. SunRJ, MullerS, WangX, ZhuangFY, StoltzJF (2000) Regulation of von willebrand factor of human endothelial cells exposed to laminar flows: An in vitro study. Clin Hemorheol Microcirc 23: 1–11.
16. MazzolaiL, SilacciP, BouzoureneK, DanielF, BrunnerH, et al. (2002) Tissue factor activity is upregulated in human endothelial cells exposed to oscillatory shear stress. Thromb Haemost 87: 1062–1068.
17. JinZG, UebaH, TanimotoT, LunguAO, FrameMD, et al. (2003) Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ Res 93: 354–363.
18. WalsheTE, FergusonG, ConnellP, O'BrienC, CahillPA (2005) Pulsatile flow increases the expression of eNOS, ET-1, and prostacyclin in a novel in vitro coculture model of the retinal vasculature. Invest Ophthalmol Vis Sci 46: 375–382.
19. SilvaCL, LenziHL, SilvaVF, PauloFO, NoelF (2003) Cellular mechanisms involved in the increased contraction of portal veins from Schistosoma mansoni-infected mice. Parasitol Res 89: 16–22.
20. Da'daraA, SkellyPJ (2011) Manipulation of vascular function by blood flukes? Blood Rev 25: 175–179.
21. OliveiraSD, QuintasLE, AmaralLS, NoelF, FarskySH, et al. (2011) Increased endothelial cell-leukocyte interaction in murine schistosomiasis: Possible priming of endothelial cells by the disease. PLoS One 6: e23547 doi: 10.1371/journal.pone.0023547
22. EsterreP, RaobelisonA, RamarokotoCE, RavaoalimalalaVE, BoisierP, et al. (1998) Serum concentrations of sICAM-1, sE-, sP- and sL-selectins in patients with Schistosoma mansoni infection and association with disease severity. Parasite Immunol 20: 369–376.
23. SteinPC, LumsdenRD (1973) Schistosoma mansoni: Topochemical features of cercariae, schistosomula, and adults. Exp Parasitol 33: 499–514.
24. TanabeM (2003) Haemostatic abnormalities in hepatosplenic schistosomiasis mansoni. Parasitol Int 52: 351–359.
25. OmranSA, el-BassiouniNE, HusseinNA, AklMM, HusseinAT, et al. (1995) Disseminated intravascular coagulation in endemic hepatosplenic schistosomiasis. Haemostasis 25: 218–228.
26. CarvalhoMG, MelloRT, SoaresAL, BicalhoRS, Lima e SilvaFC, et al. (2005) Murine schistosomiasis mansoni: Process of blood coagulation at pre-patent, acute and chronic phases, and consequence of chemotherapeutic cure on the reversion of changes. Blood Coagul Fibrinolysis 16: 469–475.
27. AminHM, OmranSA, el-BassuoniNE, el-KalioubyAH, el-AshmawySA (1994) Assessment of factors II, VII, IX, X, and protein C in hepatosplenic schistosomiasis. Haemostasis 24: 22–26.
28. El-BassiouniNE, El BassiounyAE, HusseinNA, El-SayedHH, IbrahimIM, et al. (1998) The coagulation profile in hepatosplenic schistosomiasis. Blood Coagul Fibrinolysis 9: 189–194.
29. El-BassiouniNE, el BassiounyAE, el-KhayatHR, AklMM, OmranSA (1996) Hyperfibrinolysis in hepatosplenic schistosomiasis. J Clin Pathol 49: 990–993.
30. WuYP, LentingPJ, TielensAGM, de GrootPG, van HellemondJJ (2007) Differential platelet adhesion to distinct life-cycle stages of the parasitic helminth Schistosoma mansoni. J Thromb Haemost 5: 2146–2148.
31. SunH (2006) The interaction between pathogens and the host coagulation system. Physiology (Bethesda) 21: 281–288.
32. HerrmannM, HartleibJ, KehrelB, MontgomeryRR, SixmaJJ, et al. (1997) Interaction of von willebrand factor with Staphylococcus aureus. J Infect Dis 176: 984–991.
33. NgaizaJR, DoenhoffMJ (1987) Schistosoma mansoni-induced thrombocytopenia in mice. Trans R Soc Trop Med Hyg 81: 655–656.
34. CorreiaMC, DominguesAL, LacerdaHR, SantosEM, MachadoCG, et al. (2009) Platelet function and the von willebrand factor antigen in the hepatosplenic form of schistosomiasis mansoni. Trans R Soc Trop Med Hyg 103: 1053–1058.
35. KaczmarekE, KoziakK, SevignyJ, SiegelJB, AnratherJ, et al. (1996) Identification and characterization of CD39/vascular ATP diphosphohydrolase. J Biol Chem 271: 33116–33122.
36. SevignyJ, SundbergC, BraunN, GuckelbergerO, CsizmadiaE, et al. (2002) Differential catalytic properties and vascular topography of murine nucleoside triphosphate diphosphohydrolase 1 (NTPDase1) and NTPDase2 have implications for thromboregulation. Blood 99: 2801–2809.
37. BornGV (1962) Aggregation of blood platelets by adenosine diphosphate and its reversal. Nature 194: 927–929.
38. BornGV, CrossMJ (1963) The aggregation of blood platelets. J Physiol 168: 178–195.
39. BhardwajR, SkellyPJ (2009) Purinergic signaling and immune modulation at the schistosome surface? Trends Parasitol 25: 256–260.
40. CesariIM, SimpsonAJ, EvansWH (1981) Properties of a series of tegumental membrane-bound phosphohydrolase activities of Schistosoma mansoni. Biochem J 198: 467–473.
41. Araujo-MontoyaBO, RofattoHK, TararamCA, FariasLP, OliveiraKC, et al. (2011) Schistosoma mansoni: Molecular characterization of alkaline phosphatase and expression patterns across life cycle stages. Exp Parasitol 129: 284–291.
42. MillanJL (2006) Alkaline phosphatases: Structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2: 335–341.
43. BogitshBJ, KrupaPL (1971) Schistosoma mansoni and Haematoloechus medioplexus: Nuclosidediphosphatase localization in tegument. Exp Parasitol 30: 418–425.
44. VasconcelosEG, NascimentoPS, MeirellesMN, Verjovski-AlmeidaS, FerreiraST (1993) Characterization and localization of an ATP-diphosphohydrolase on the external surface of the tegument of Schistosoma mansoni. Mol Biochem Parasitol 58: 205–214.
45. DeMarcoR, KowaltowskiAT, MortaraRA, Verjovski-AlmeidaS (2003) Molecular characterization and immunolocalization of Schistosoma mansoni ATP-diphosphohydrolase. Biochem Biophys Res Commun 307: 831–838.
46. CarvalhoWS, LopesCT, JulianoL, CoelhoPM, Cunha-MeloJR, et al. (1998) Purification and partial characterization of kininogenase activity from Schistosoma mansoni adult worms. Parasitology 117: 311–319.
47. CocudeC, PierrotC, CetreC, FontaineJ, GodinC, et al. (1999) Identification of a developmentally regulated Schistosoma mansoni serine protease homologous to mouse plasma kallikrein and human factor I. Parasitology 118: 389–396.
48. MaurerM, BaderM, BasM, BossiF, CicardiM, et al. (2011) New topics in bradykinin research. Allergy 66: 1397–1406.
49. NorrisLA (2003) Blood coagulation. Best Pract Res Clin Obstet Gynaecol 17: 369–383.
50. NawrothPP, SternDM (1986) Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J Exp Med 163: 740–745.
51. WilnerGD, NosselHL, LeRoyEC (1968) Activation of hageman factor by collagen. J Clin Invest 47: 2608–2615.
52. EspanaF, RatnoffOD (1983) Activation of hageman factor (factor XII) by sulfatides and other agents in the absence of plasma proteases. J Lab Clin Med 102: 31–45.
53. RenneT, SchmaierAH, NickelKF, BlombackM, MaasC (2012) In vivo roles of factor XII. Blood 120: 4296–4303.
54. AmerA, AmerME (2002) Enhanced monocyte tissue factor expression in hepatosplenic schistosomiasis. Blood Coagul Fibrinolysis 13: 43–47.
55. TsangVC, HubbardWJ, DamianRT (1977) Coagulation factor XIIa (activated hageman factor) inhibitor from adult Schistosoma mansoni. Am J Trop Med Hyg 26: 243–247.
56. TsangVC, DamianRT (1977) Demonstration and mode of action of an inhibitor for activated hageman factor (factor XIIa) of the intrinsic blood coagulation pathway from Schistosoma mansoni. Blood 49: 619–633.
57. FosterCB, FlaniganTP, DeStigterKK, BlantonR, DumencoLL, et al. (1992) Inhibition of the activation of hageman factor (factor XII) by extracts of Schistosoma mansoni. J Lab Clin Med 120: 735–739.
58. LinYL, HeS (2006) Sm22.6 antigen is an inhibitor to human thrombin. Mol Biochem Parasitol 147: 95–100.
59. SteinLD, DavidJR (1986) Cloning of a developmentally regulated tegument antigen of Schistosoma mansoni. Mol Biochem Parasitol 20: 253–264.
60. RenneT, PozgajovaM, GrunerS, SchuhK, PauerHU, et al. (2005) Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med 202: 271–281.
61. Beck WS (1985) Hematology. Cambridge: The MIT Press. 496 p.
62. GhebrehiwetB, SilverbergM, KaplanAP (1981) Activation of the classical pathway of complement by hageman factor fragment. J Exp Med 153: 665–676.
63. RobertsonNP, CainGD (1985) Isolation and characterization of glycosaminoglycans from Schistosoma mansoni. Comp Biochem Physiol B 82: 299–306.
64. EvansDL, McGroganM, ScottRW, CarrellRW (1991) Protease specificity and heparin binding and activation of recombinant protease nexin I. J Biol Chem 266: 22307–22312.
65. BlantonRE, LicateLS, AmanRA (1994) Characterization of a native and recombinant Schistosoma haematobium serine protease inhibitor gene product. Mol Biochem Parasitol 63: 1–11.
66. MannKG, Brummel-ZiedinsK, OrfeoT, ButenasS (2006) Models of blood coagulation. Blood Cells Mol Dis 36: 108–117.
67. MilesLA, GreengardJS, GriffinJH (1983) A comparison of the abilities of plasma kallikrein, beta-factor XIIa, factor XIa and urokinase to activate plasminogen. Thromb Res 29: 407–417.
68. Ramajo-HernandezA, Perez-SanchezR, Ramajo-MartinV, OleagaA (2007) Schistosoma bovis: Plasminogen binding in adults and the identification of plasminogen-binding proteins from the worm tegument. Exp Parasitol 115: 83–91.
69. de la Torre-EscuderoE, Manzano-RomanR, Perez-SanchezR, Siles-LucasM, OleagaA (2010) Cloning and characterization of a plasminogen-binding surface-associated enolase from schistosoma bovis. Vet Parasitol 173: 76–84.
70. de la Torre-EscuderoE, Manzano-RomanR, Siles-LucasM, Perez-SanchezR, MoyanoJC, et al. (2012) Molecular and functional characterization of a Schistosoma bovis annexin: Fibrinolytic and anticoagulant activity. Vet Parasitol 184: 25–36.
71. SkellyPJ, Alan WilsonR (2006) Making sense of the schistosome surface. Adv Parasitol 63: 185–284.
72. YangJ, QiuC, XiaY, YaoL, FuZ, et al. (2010) Molecular cloning and functional characterization of Schistosoma japonicum enolase which is highly expressed at the schistosomulum stage. Parasitol Res 107: 667–677.
73. Angles-CanoE (1994) Overview on fibrinolysis: Plasminogen activation pathways on fibrin and cell surfaces. Chem Phys Lipids 67–68: 353–362.
74. FloodEC, HajjarKA (2011) The annexin A2 system and vascular homeostasis. Vascul Pharmacol 54: 59–67.
75. PellegrinoJ, CoelhoPM (1978) Schistosoma mansoni: Wandering capacity of a worm couple. J Parasitol 64: 181–182.
76. SalafskyB, FuscoAC (1987) Schistosoma mansoni: A comparison of secreted vs nonsecreted eicosanoids in developing schistosomulae and adults. Exp Parasitol 64: 361–367.
77. AngeliV, FaveeuwC, RoyeO, FontaineJ, TeissierE, et al. (2001) Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal langerhans cell migration during schistosomiasis infection. J Exp Med 193: 1135–1147.
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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