Endothelial Cell Permeability during Hantavirus Infection Involves Factor XII-Dependent Increased Activation of the Kallikrein-Kinin System

PLoS Pathogens

Volumn 9, Issue 7, 2013, Pages

  Taylor, Shannon L ^a   Wahl Jensen, Victoria ^b   Copeland, Anna Maria ^a   Jahrling, Peter B ^b   Schmaljohn, Connie S ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTEPLASE; BLOOD CLOTTING FACTOR 12; BRADYKININ; COLLAGEN TYPE 18; HIGH MOLECULAR WEIGHT KININOGEN; ICATIBANT; PREKALLIKREIN; SMOOTH MUSCLE ACTIN; TRYPSIN INHIBITOR; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; VON WILLEBRAND FACTOR;

ANIMAL CELL; ARTICLE; BLOOD VESSEL PERMEABILITY; CAPILLARY; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DENSITOMETRY; DISEASE TRANSMISSION; ENZYME ACTIVITY; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; HANTAVIRUS INFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; KALLIKREIN KININ SYSTEM; NONHUMAN; SCANNING ELECTRON MICROSCOPY; SMOOTH MUSCLE FIBER; UMBILICAL VEIN ENDOTHELIAL CELL; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; WESTERN BLOTTING;

EID: 84884777032     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003470     Document Type: Article

References (53)

1. Khaiboullina SF, Morzunov SP, St Jeor SC, (2005) Hantaviruses: molecular biology, evolution and pathogenesis. Curr Mol Med 5: 773-790.
2. Muranyi W, Bahr U, Zeier M, van der Woude FJ, (2005) Hantavirus infection. J Am Soc Nephrol 16: 3669-3679.
3. Macneil A, Nichol ST, Spiropoulou CF, (2011) Hantavirus pulmonary syndrome. Virus Res 162: 138-147.
4. Cosgriff TM, (1991) Mechanisms of disease in Hantavirus infection: pathophysiology of hemorrhagic fever with renal syndrome. Rev Infect Dis 13: 97-107.
5. Zaki SR, Greer PW, Coffield LM, Goldsmith CS, Nolte KB, et al. (1995) Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am J Pathol 146: 552-579.
6. Kanerva M, Mustonen J, Vaheri A, (1998) Pathogenesis of puumala and other hantavirus infections. Rev Med Virol 8: 67-86.
7. Terajima M, Ennis FA, (2011) T cells and pathogenesis of hantavirus cardiopulmonary syndrome and hemorrhagic fever with renal syndrome. Viruses 3: 1059-1073.
8. Hammerbeck CD, Hooper JW, (2011) T cells are not required for pathogenesis in the Syrian hamster model of hantavirus pulmonary syndrome. J Virol 85: 9929-9944.
9. Gavrilovskaya IN, Gorbunova EE, Mackow NA, Mackow ER, (2008) Hantaviruses direct endothelial cell permeability by sensitizing cells to the vascular permeability factor VEGF, while angiopoietin 1 and sphingosine 1-phosphate inhibit hantavirus-directed permeability. J Virol 82: 5797-5806.
10. Gorbunova E, Gavrilovskaya IN, Mackow ER, (2010) Pathogenic hantaviruses Andes virus and Hantaan virus induce adherens junction disassembly by directing vascular endothelial cadherin internalization in human endothelial cells. J Virol 84: 7405-7411.
11. Li Y, Wang W, Wang JP, Pan L, Zhang Y, et al. (2012) Elevated vascular endothelial growth factor levels induce hyperpermeability of endothelial cells in hantavirus infection. J Int Med Res 40: 1812-1821.
12. Shrivastava-Ranjan P, Rollin PE, Spiropoulou CF, (2010) Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J Virol 84: 11227-11234.
13. Vestweber D, (2008) VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol 28: 223-232.
14. Safronetz D, Zivcec M, Lacasse R, Feldmann F, Rosenke R, et al. (2011) Pathogenesis and host response in Syrian hamsters following intranasal infection with Andes virus. PLoS Pathog 7: e1002426.
15. Schmaier AH, (2008) Assembly, activation, and physiologic influence of the plasma kallikrein/kinin system. Int Immunopharmacol 8: 161-165.
16. Harris MB, Ju H, Venema VJ, Blackstone M, Venema RC, (2000) Role of heat shock protein 90 in bradykinin-stimulated endothelial nitric oxide release. Gen Pharmacol 35: 165-170.
17. Joseph K, Tholanikunnel BG, Kaplan AP, (2002) Heat shock protein 90 catalyzes activation of the prekallikrein-kininogen complex in the absence of factor XII. Proc Natl Acad Sci U S A 99: 896-900.
18. Kaplan AP, Silverberg M, (1987) The coagulation-kinin pathway of human plasma. Blood 70: 1-15.
19. Golias C, Charalabopoulos A, Stagikas D, Charalabopoulos K, Batistatou A, (2007) The kinin system-bradykinin: biological effects and clinical implications. Multiple role of the kinin system-bradykinin. Hippokratia 11: 124-128.
20. Giles TD, Sander GE, Nossaman BD, Kadowitz PJ, (2012) Impaired vasodilation in the pathogenesis of hypertension: focus on nitric oxide, endothelial-derived hyperpolarizing factors, and prostaglandins. J Clin Hypertens (Greenwich) 14: 198-205.
21. Mehta D, Malik AB, (2006) Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279-367.
22. Fuller RW, Dixon CM, Cuss FM, Barnes PJ, (1987) Bradykinin-induced bronchoconstriction in humans. Mode of action. Am Rev Respir Dis 135: 176-180.
23. Granger J, Remick D, (2005) Acute pancreatitis: models, markers, and mediators. Shock 24 (Suppl 1):: 45-51.
24. Kaplan AP, Joseph K, (2010) The bradykinin-forming cascade and its role in hereditary angioedema. Ann Allergy Asthma Immunol 104: 193-204.
25. Wuillemin WA, Fijnvandraat K, Derkx BH, Peters M, Vreede W, et al. (1995) Activation of the intrinsic pathway of coagulation in children with meningococcal septic shock. Thromb Haemost 74: 1436-1441.
26. Antonen J, Leppanen I, Tenhunen J, Arvola P, Makela S, et al. (2013) A severe case of Puumala hantavirus infection successfully treated with bradykinin receptor antagonist icatibant. Scand J Infect Dis 45: 494-6.
27. Evensen L, Micklem DR, Blois A, Berge SV, Aarsaether N, et al. (2009) Mural cell associated VEGF is required for organotypic vessel formation. PLoS One 4: e5798.
28. Crosby CV, Fleming PA, Argraves WS, Corada M, Zanetta L, et al. (2005) VE-cadherin is not required for the formation of nascent blood vessels but acts to prevent their disassembly. Blood 105: 2771-2776.
29. Zhang JC, Claffey K, Sakthivel R, Darzynkiewicz Z, Shaw DE, et al. (2000) Two-chain high molecular weight kininogen induces endothelial cell apoptosis and inhibits angiogenesis: partial activity within domain 5. FASEB J 14: 2589-2600.
30. Maurer M, Bader M, Bas M, Bossi F, Cicardi M, et al. (2011) New topics in bradykinin research. Allergy 66: 1397-1406.
31. Riethmuller C, Jungmann P, Wegener J, Oberleithner H, (2006) Bradykinin shifts endothelial fluid passage from para- to transcellular routes. Pflugers Arch 453: 157-165.
32. Shariat-Madar Z, Mahdi F, Schmaier AH, (2002) Assembly and activation of the plasma kallikrein/kinin system: a new interpretation. Int Immunopharmacol 2: 1841-1849.
33. Triggle CR, Samuel SM, Ravishankar S, Marei I, Arunachalam G, et al. (2012) The endothelium: influencing vascular smooth muscle in many ways. Can J Physiol Pharmacol 90: 713-738.
34. Kimura H, Esumi H, (2003) Reciprocal regulation between nitric oxide and vascular endothelial growth factor in angiogenesis. Acta Biochim Pol 50: 49-59.
35. Sriskandan S, Cohen J, (2000) Kallikrein-kinin system activation in streptococcal toxic shock syndrome. Clin Infect Dis 30: 961-962.
36. Nickel KF, Renne T, (2012) Crosstalk of the plasma contact system with bacteria. Thromb Res 130 (Suppl 1):: S78-83.
37. Kannemeier C, Shibamiya A, Nakazawa F, Trusheim H, Ruppert C, et al. (2007) Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci U S A 104: 6388-6393.
38. Maas C, Govers-Riemslag JW, Bouma B, Schiks B, Hazenberg BP, et al. (2008) Misfolded proteins activate factor XII in humans, leading to kallikrein formation without initiating coagulation. J Clin Invest 118: 3208-3218.
39. Renne T, Schuh K, Muller-Esterl W, (2005) Local bradykinin formation is controlled by glycosaminoglycans. J Immunol 175: 3377-3385.
40. Gershom ES, Sutherland MR, Lollar P, Pryzdial EL, (2010) Involvement of the contact phase and intrinsic pathway in herpes simplex virus-initiated plasma coagulation. J Thromb Haemost 8: 1037-1043.
41. Longhurst H, Cicardi M, (2012) Hereditary angio-oedema. Lancet 379: 474-481.
42. Caballero T, (2012) Efficacy Assessments in Randomized Controlled Studies of Acute Therapy for Hereditary Angioedema. J Clin Immunol 32: 1204-12.
43. Kaplan AP, Ghebrehiwet B, (2010) The plasma bradykinin-forming pathways and its interrelationships with complement. Mol Immunol 47: 2161-2169.
44. Joseph K, Shibayama Y, Ghebrehiwet B, Kaplan AP, (2001) Factor XII-dependent contact activation on endothelial cells and binding proteins gC1qR and cytokeratin 1. Thromb Haemost 85: 119-124.
45. Stavrou E, Schmaier AH, (2010) Factor XII: what does it contribute to our understanding of the physiology and pathophysiology of hemostasis & thrombosis. Thromb Res 125: 210-215.
46. Mahdi F, Madar ZS, Figueroa CD, Schmaier AH, (2002) Factor XII interacts with the multiprotein assembly of urokinase plasminogen activator receptor, gC1qR, and cytokeratin 1 on endothelial cell membranes. Blood 99: 3585-3596.
47. Sidel'nikov Iu N, Obukhova GG, (1990) [The role of biologically active substances in permeability changes in the blood vessels of patients with hemorrhagic fever with renal syndrome]. Ter Arkh 62: 66-68.
48. Fedorchenko Iu L, Sirotin BZ, Rozhkovskaia EN, (1990) [Vascular permeability, microcirculation and biologically active substances in patients with hemorrhagic fever with renal syndrome]. Ter Arkh 62: 71-74.
49. Aasen AO, Erichsen NS, Gallimore MJ, Amundsen E, (1980) Studies on components of the plasma kallikrein-kinin system in plasma samples from normal individuals and patients with septic shock. Adv Shock Res 4: 1-10.
50. Castillo C, Naranjo J, Sepulveda A, Ossa G, Levy H, (2001) Hantavirus pulmonary syndrome due to Andes virus in Temuco, Chile: clinical experience with 16 adults. Chest 120: 548-554.
51. Safronetz D, Ebihara H, Feldmann H, Hooper JW, (2012) The Syrian hamster model of hantavirus pulmonary syndrome. Antiviral Res 95: 282-292.
52. Wahl-Jensen V, Chapman J, Asher L, Fisher R, Zimmerman M, et al. (2007) Temporal analysis of Andes virus and Sin Nombre virus infections of Syrian hamsters. J Virol 81: 7449-7462.
53. Lee HW, Lee PW, Johnson KM, (1978) Isolation of the etiologic agent of Korean Hemorrhagic fever. J Infect Dis 137: 298-308.