Plasma pentraxin-3 and coagulation and fibrinolysis variables during acute Puumala hantavirus infection and associated thrombocytopenia

Blood Coagulation and Fibrinolysis

Volumn 25, Issue 6, 2014, Pages 612-617

  Laine, Outi K ^a,b   Koskela, Sirpa M ^a   Outinen, Tuula K ^a   Joutsi Korhonen, Lotta ^c   Huhtala, Heini ^b   Vaheri, Antti ^d   Hurme, Mikko A ^a,b   Jylhävä, Juulia ^b   Mäkelä, Satu M ^a,b   Mustonen, Jukka T ^a,b  

^a TAMPERE UNIVERSITY HOSPITAL   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

cell free DNA; coagulation; hemorrhagic fever with renal syndrome; pentraxin 3; platelet; Puumala hantavirus

Indexed keywords

ADAM PROTEIN; ADAMTS13 PROTEIN, HUMAN; ANTITHROMBIN III; BIOLOGICAL MARKER; C REACTIVE PROTEIN; COMPLEMENT COMPONENT C3; COMPLEMENT MEMBRANE ATTACK COMPLEX; DNA; FIBRINOGEN; IL6 PROTEIN, HUMAN; INTERLEUKIN 6; PENTRAXIN 3; PROTEIN C; PROTEIN S; SC5B-9 PROTEIN COMPLEX; SERUM AMYLOID P; THROMBIN;

ACUTE DISEASE; ADULT; BLOOD; BLOOD CLOTTING; COMPLICATION; FEMALE; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HUMAN; MALE; METABOLISM; MIDDLE AGED; PHYSIOLOGY; PREDICTIVE VALUE; PUUMALA VIRUS; SEVERITY OF ILLNESS INDEX; THROMBOCYTOPENIA; VIROLOGY;

ACUTE DISEASE; ADAM PROTEINS; ADULT; ANTITHROMBIN III; BIOLOGICAL MARKERS; BLOOD COAGULATION; C-REACTIVE PROTEIN; COMPLEMENT C3; COMPLEMENT MEMBRANE ATTACK COMPLEX; DNA; FEMALE; FIBRINOGEN; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HUMANS; INTERLEUKIN-6; MALE; MIDDLE AGED; PREDICTIVE VALUE OF TESTS; PROTEIN C; PROTEIN S; PUUMALA VIRUS; SERUM AMYLOID P-COMPONENT; SEVERITY OF ILLNESS INDEX; THROMBIN; THROMBOCYTOPENIA;

EID: 84905819158     PISSN: 09575235     EISSN: 14735733     Source Type: Journal    
DOI: 10.1097/MBC.0000000000000117     Document Type: Article

References (47)

1. Kariwa H, Yoshimatsu K, Arikawa J. Hantavirus infection in East Asia. Comp Immunol Microbiol Inf Dis 2007; 30:341-356.
2. Vaheri A, Strandin T, Hepojoki J, Sironen T, Henttonen H, MäkeläS, et al. Uncovering the mysteries of hantavirus infections. Nat Rev Microbiol 2013; 11:539-550.
3. MäkeläS, Jaatinen P, Miettinen M, Salmi J, Ala-Houhala IO, Huhtala H, et al. Hormonal deficiencies during and after Puumala hantavirus infection. Eur J Clin Microbiol Infect Dis 2010; 29:705-713.
4. MäkeläS, Ala-Houhala I, Mustonen J, Koivisto AM, Kouri T, Turjanmaa V, et al. Renal function and blood pressure five years after puumala virus-induced nephropathy. Kidney Int 2000; 58:1711-1718.
5. Vaheri A, Henttonen H, Voutilainen L, Mustonen J, Sironen T, Vapalahti O. Hantavirus infections in Europe and their impact on public health. Rev Med Virol 2013; 23:35-49.
6. Jonsson CB, Figueiredo LT, Vapalahti O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rew 2010; 23:412-441.
7. Simpson SQ, Spikes L, Patel S, Faruqi I. Hantavirus pulmonary syndrome. Infect Dis Clin North Am 2010; 24:159-173.
8. Krüger DH, Schönrich G, Klempa B. Human pathogenic hantaviruses and prevention of infection. Hum Vaccin 2011; 7:685-693.
9. Laine O, MäkeläS, Mustonen J, Huhtala H, Szanto T, Vaheri A, et al. Enhanced thrombin formation and fibrinolysis during acute Puumala hantavirus infection. Thromb Res 2010; 126:154-158.
10. Laine O, MäkeläS, Mustonen J, Helminen M, Vaheri A, Lassila R, et al. Platelet ligands and ADAMTS13 during Puumala hantavirus infection and associated thrombocytopenia. Blood Coagul Fibrinolysis 2011; 22:468-472.
11. Laine O, Joutsi-Korhonen L, MäkeläS, Mikkelsson J, Pessi T, Tuomisto S, et al. Polymorphisms of PAI-1 and platelet GP Ia may associate with impairment of renal function and thrombocytopenia in Puumala hantavirus infection. Thromb Res 2012; 129:611-615.
12. Rasche FM, Uhel B, Krüger DH, Karges W, Czock D, Hampl W, et al. Thrombocytopenia and acute renal failure in Puumala infections. Emerg Infect Dis 2004; 10:1420-1425.
13. Wang M, Wang J, Wang T, Li J, Hui L, Ha X. Thrombocytopenia as a predictor of severe acute kidney injury in patients with Hantaan virus infections. PloS One 2013; 8:e53236.
14. Outinen TK, MäkeläS, Huhtala H, Hurme M, Meri S, Pörsti I, et al. High pentraxin-3 plasma levels associate with thrombocytopenia in acute Puumala hantavirus-induced nephropathia epidemica. Eur J Clin Microbiol Infect Dis 2011; 31:957-963.
15. Holdenrieder S, Stieber P, Bodenmuller H, Fertig G, Fürst H, Schmeller N, et al. Nucleosomes in serum as a marker for cell death. Clin Chem Lab Med 2001; 39:596-605.
16. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532-1535.
17. Outinen TK, Kuparinen T, JylhäväJ, Leppänen S, Mustonen J, MäkeläS, et al. Plasma cell-free DNA levels are elevated in acute Puumala hantavirus infection. PloS One 2015; 7:e31455.
18. Sane J, Laine O, MäkeläS, Pakkala A, Jarva H, Mustonen J, et al. Complement activation in Puumala hantavirus infection correlates with disease severity. Ann Med 2012; 44:468-475.
19. Vapalahti O, Lundkvist A, Kallio-Kokko H, Paukku K, Julkunen I, Lankinen H, et al. Antigenic properties and diagnostic potential of Puumala virus nucleocapsid protein expressed in insect cells. J Clin Microbiol 1996; 34:119-125.
20. Nauta AJ, de Haij S, Bottazzi B, Mantovani A, Borrias MC, Aten J, et al. Human renal epithelial cells produce the long pentraxin PTX3. Kidney Int 2005; 67:543-553.
21. Garlanda C, Bottazzi B, Bastone A, Mantovani A. Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu Rew Immunol 2005; 23:337-366.
22. Chen J, Matzuk MM, Zhou XJ, Lu CY. Endothelial pentraxin 3 contributes to murine ischemic acute kidney injury. Kidney Int 2012; 82:1195-1207.
23. Bottazzi B, Doni A, Garlanda C, Mantovani A. An integrated view of humoral innate immunity: Pentraxins as a paradigm. Annu Rew Immunol 2010; 28:157-183.
24. Lech M, Rommele C, Anders HJ. Pentraxins in nephrology: C-reactive protein, serum amyloid P and pentraxin-3. Nephrol Dial Transplant 2013; 28:803-811.
25. Mairuhu AT, Peri G, Setiati TE, Hack CE, Koraka P, Soemantri A, et al. Elevated plasma levels of the long pentraxin, pentraxin 3, in severe dengue virus infections. J Med Virol 2005; 76:547-552.
26. Outinen TK, MäkeläSM, Ala-Houhala IO, Huhtala H, Hurme M, Paakkala A, et al. The severity of Puumala hantavirus induced nephropathia epidemica can be better evaluated using plasma interleukin-6 than C-reactive protein determinations. BMC Infect Dis 2010; 10:132.
27. Napoleone E, di Santo A, Peri G, Mantovani A, de Gaetano G, Donati MB, et al. The long pentraxin PTX3 up-regulates tissue factor in activated monocytes: Another link between inflammation and clotting activation. J Leukoc Biol 2004; 76:203-209.
28. Nauta AJ, Bottazzi B, Mantovani A, Salvatori G, Kishore U, Schwaeble WJ, et al. Biochemical and functional characterization of the interaction between pentraxin 3 and C1q. Eur J Immunol 2003; 33:465-473.
29. Deban L, Russo RC, Sironi M, Moalli F, Scanziani M, Zambelli V, et al. Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat Immunol 2010; 11:328-334.
30. Lech M, Rommele C, Kulkarni OP, Susanti HE, Migliorini A, Garlanda C, et al. Lack of the long pentraxin PTX3 promotes autoimmune lung disease but not glomerulonephritis in murine systemic lupus erythematosus. PloS One 2011; 6:e20118.
31. Bauer KA, Rosenberg RD. Role of antithrombin III as a regulator of in vivo coagulation. Semin Hematol 1991; 28:10-18.
32. Yamashiro K, Kiryu J, Tsujikawa A, Honjo M, Nonaka A, Miyamoto K, et al. Inhibitory effects of antithrombin III against leukocyte rolling and infiltration during endotoxin-induced uveitis in rats. Invest Ophtalmol Vis Sci 2001; 42:1553-1560.
33. Okajima K. Antithrombin prevents endotoxin-induced pulmonary vascular injury by inhibiting leukocyte activation. Blood Coagul Fibrinolysis 1998; 9 (Suppl 2):S25-S37.
34. Kobayashi M, Shimada K, Ozawa T. Human recombinant interleukin-1 betaand tumor necrosis factor alpha-mediated suppression of heparin-like compounds on cultured porcine aortic endothelial cells. J Cell Physiol 1990; 144:383-390.
35. van Der Poll T, Opal SM. Host-pathogen interactions in sepsis. Lancet Infect Dis 2008; 8:32-43.
36. Maclean PS, Tait RC. Hereditary and acquired antithrombin deficiency: Epidemiology, pathogenesis and treatment options. Drugs 2007; 67:1429-1440.
37. Sundberg E, Hultdin J, Nilsson S, Ahlm C. Evidence of disseminated intravascular coagulation in a hemorrhagic fever with renal syndromescoring models and severe illness. PloS One 2011; 6:e21134.
38. Chuang YC, Lei HY, Lin YS, Liu HS,WuHL, Yeh TM. Dengue virus-induced autoantibodies bind to plasminogen and enhance its activation. J Immunol 2011; 187:6483-6490.
39. Klingstrom J, Hardestam J, Stoltz M, Zuber B, Lundkvist A, Linder S, et al. Loss of cell membrane integrity in puumala hantavirus-infected patients correlates with levels of epithelial cell apoptosis and perforin. J Virol 2006; 80:8279-8282.
40. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, et al. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15:1318-1321.
41. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci 2010; 107:15880-15885.
42. Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, et al. Extracellular histones promote thrombin generation through plateletdependent mechanisms: Involvement of platelet TLR2 and TLR4. Blood 2011; 118:1952-1961.
43. Ammollo CT, Semeraro F, Xu J, Esmon NL, Esmon CT. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation. J Thromb Haemost 2011; 9:1795-1803.
44. Lee M. Coagulopathy in patients with hemorrhagic fever with renal syndrome. J Kor Med Sci 1987; 2:201-211.
45. Amara U, Flierl MA, Rittirsch D, Klos A, Chen H, Acker B, et al. Molecular intercommunication between the complement and coagulation systems. J Immunol 2010; 185:5628-5636.
46. Paakkala A, Mustonen J, Viander M, Huhtala H, Pasternack A. Complement activation in nephropathia epidemica caused by Puumala hantavirus. Clin Nephrol 2000; 53:424-431.
47. Pettersson L, Thunberg T, Rocklov J, Klingstrom J, Evander M, Ahlm C. Viral load and humoral immune response in association with disease severity in Puumala hantavirus-infected patients-implications for treatment. Clin Microbiol Infect 2014; 20:235-241.