Serum angiopoietin-2 and soluble VEGF receptor 2 are surrogate markers for plasma leakage in patients with acute dengue virus infection

Journal of Clinical Virology

Volumn 60, Issue 4, 2014, Pages 328-335

  van de Weg, Cornelia A M ^a   Pannuti, Cláudio S ^b   van den Ham, Henk Jan ^a   de Araújo, Evaldo S A ^b,c   Boas, Lucy S V ^b   Felix, Alvina C ^b   Carvalho, Karina I ^d   Levi, José E ^b   Romano, Camila M ^b   Centrone, Cristiane C ^b   Rodrigues, Celia L de Lima ^b   Luna, Expedito ^b   van Gorp, Eric C M ^a   Osterhaus, Albert D M E ^a   Kallas, Esper G ^b   Martina, Byron E E ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c HOSPITAL ANA COSTA   (Brazil)

^d HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

Author keywords

Angiopoietin 2; Dengue virus; Plasma leakage; Soluble VEGFR 2; Vascular permeability

Indexed keywords

ANGIOPOIETIN 2; ENDOGLIN; ENDOTHELIN 1; GELATINASE A; GELATINASE B; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; BIOLOGICAL MARKER; IMMUNOGLOBULIN G; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2, HUMAN; VIRUS ANTIBODY; SOLUBLE VASCULOTROPIN RECEPTOR 2; UNCLASSIFIED DRUG;

ACUTE DISEASE; ADOLESCENT; ADULT; ARTICLE; BLOOD VESSEL PERMEABILITY; BRAZIL; CASE CONTROL STUDY; CHILD; CLUSTER ANALYSIS; COMORBIDITY; CONTROLLED STUDY; DENGUE; DISEASE MARKER; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMATOLOGIC DISEASE; HUMAN; MAJOR CLINICAL STUDY; MALE; PATHOGENESIS; PHYLOGENETIC TREE; PLASMA LEAKAGE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; THROMBOCYTE COUNT; VIRUS LOAD; X RAY; ANTIBODY AFFINITY; BLOOD; CAPILLARY PERMEABILITY; DENGUE VIRUS; IMMUNOLOGY; MIDDLE AGED; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; RADIOGRAPHY; VIROLOGY; YOUNG ADULT; DISEASE ASSOCIATION; ECHOGRAPHY; PROTEIN EXPRESSION;

ADOLESCENT; ADULT; ANGIOPOIETIN-2; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; BIOLOGICAL MARKERS; BRAZIL; CAPILLARY PERMEABILITY; CASE-CONTROL STUDIES; CHILD; DENGUE VIRUS; ENDOTHELIAL CELLS; ENDOTHELIN-1; FEMALE; HUMANS; IMMUNOGLOBULIN G; MALE; MATRIX METALLOPROTEINASE 2; MIDDLE AGED; SEVERE DENGUE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; YOUNG ADULT;

EID: 84902766083     PISSN: 13866532     EISSN: 18735967     Source Type: Journal    
DOI: 10.1016/j.jcv.2014.05.001     Document Type: Article

References (47)

1. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., et al. The global distribution and burden of dengue. Nature 2013, 496:504-507.
2. Lam P.K., Tam D.T., Diet T.V., Tam C.T., Tien N.T., Kieu N.T., et al. Clinical characteristics of dengue shock syndrome in Vietnamese children; a 10-year prospective study in a single hospital. Clin Infect Dis 2013, 57(11):1577-1580.
3. Dalrymple N.A., Mackow E.R. Endothelial cells elicit immune-enhancing responses to dengue virus infection. J Virol 2012, 86:6408-6415.
4. Jessie K., Fong M.Y., Devi S., Lam S.K., Wong K.T. Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis 2004, 189:1411-1418.
5. Kelley J.F., Kaufusi P.H., Nerurkar V.R. Dengue hemorrhagic fever-associated immunomediators induced via maturation of dengue virus nonstructural 4B protein in monocytes modulate endothelial cell adhesion molecules and human microvascular endothelial cells permeability. Virology 2012, 422:326-337.
6. Dewi B.E., Takasaki T., Kurane I. Peripheral blood mononuclear cells increase the permeability of dengue virus-infected endothelial cells in association with downregulation of vascular endothelial cadherin. J Gen Virol 2008, 89:642-652.
7. Dalrymple N.A., Mackow E.R. Roles for endothelial cells in dengue virus infection. Adv Virol 2012, 2012:840654.
8. Srikiatkhachorn A., Ajariyakhajorn C., Endy T.P., Kalayanarooj S., Libraty D.H., Green S., et al. Virus-induced decline in soluble vascular endothelial growth receptor 2 is associated with plasma leakage in dengue hemorrhagic Fever. J Virol 2007, 81:1592-1600.
9. Tseng C.S., Lo H.W., Teng H.C., Lo W.C., Ker C.G. Elevated levels of plasma VEGF in patients with dengue hemorrhagic fever. FEMS Immunol Med Microbiol 2005, 43:99-102.
10. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 1999, 13:9-22.
11. Basbaum C.B., Werb Z. Focalized proteolysis: spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr Opin Cell Biol 1996, 8:731-738.
12. Taraboletti G., D'Ascenzo S., Borsotti P., Giavazzi R., Pavan A., Dolo V. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol 2002, 160:673-680.
13. Kubelka C.F., Azeredo E.L., Gandini M., Oliveira-Pinto L.M., Barbosa L.S., Damasco P.V., et al. Metalloproteinases are produced during dengue fever and MMP9 is associated with severity. J Infect 2010, 61:501-505.
14. Thurston G., Rudge J.S., Ioffe E., Zhou H., Ross L., Croll S.D., et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 2000, 6:460-463.
15. Scharpfenecker M., Fiedler U., Reiss Y., Augustin H.G. The Tie-2 ligand angiopoietin-2 destabilizes quiescent endothelium through an internal autocrine loop mechanism. J Cell Sci 2005, 118:771-780.
16. Michels M., van der Ven A.J., Djamiatun K., Fijnheer R., de Groot P.G., Griffioen A.W., et al. Imbalance of angiopoietin-1 and angiopoetin-2 in severe dengue and relationship with thrombocytopenia, endothelial activation, and vascular stability. Am J Trop Med Hyg 2012, 87:943-946.
17. Dietmann A., Helbok R., Lackner P., Fischer M., Reindl M., Lell B., et al. Endoglin in African children with Plasmodium falciparum malaria: a novel player in severe malaria pathogenesis?. J Infect Dis 2009, 200:1842-1848.
18. + channels. J Hypertens Suppl 1988, 6:S188-S191.
19. Dietmann A., Lackner P., Helbok R., Spora K., Issifou S., Lell B., et al. Opposed circulating plasma levels of endothelin-1 and C-type natriuretic peptide in children with Plasmodium falciparum malaria. Malar J 2008, 7:253.
20. Pittet J.F., Morel D.R., Hemsen A., Gunning K., Lacroix J.S., Suter P.M., et al. Elevated plasma endothelin-1 concentrations are associated with the severity of illness in patients with sepsis. Ann Surg 1991, 213:261-264.
21. Romano C.M., de Matos A.M., Araujo E.S., Villas-Boas L.S., da Silva W.C., Oliveira O.M., et al. Characterization of Dengue virus type 2: new insights on the 2010 Brazilian epidemic. PLoS One 2010, 5:e11811.
22. Romano C.M., Lauck M., Salvador F.S., Lima C.R., Villas-Boas L.S., Araujo E.S., et al. Inter- and intra-host viral diversity in a large seasonal DENV2 outbreak. PLoS One 2013, 8:e87031.
23. van de Weg C.A., Pannuti C.S., de Araujo E.S., van den Ham H.J., Andeweg A.C., Boas L.S., et al. Microbial translocation is associated with extensive immune activation in dengue virus infected patients with severe disease. PLoS Negl Trop Dis 2013, 7:e2236.
24. Felix A.C., Romano C.M., Centrone Cde C., Rodrigues C.L., Villas-Boas L., Araujo E.S., et al. Low sensitivity of NS1 protein tests evidenced during a dengue type 2 virus outbreak in Santos, Brazil, in 2010. Clin Vacc Immunol 2012, 19:1972-1976.
25. van de Weg C.A., van Gorp E.C., Supriatna M., Soemantri A., Osterhaus A.D., Martina B.E. Evaluation of the 2009 WHO dengue case classification in an Indonesian pediatric cohort. Am J Trop Med Hyg 2012, 86:166-170.
26. Dengue hemorrhagic fever: diagnosis, treatment, prevention and control (new edition) 2009, World Health Organization, Geneva.
27. de Souza V.A., Fernandes S., Araujo E.S., Tateno A.F., Oliveira O.M., Oliveira R.R., et al. Use of an immunoglobulin G avidity test to discriminate between primary and secondary dengue virus infections. J Clin Microbiol 2004, 42:1782-1784.
28. Harris E., Roberts T.G., Smith L., Selle J., Kramer L.D., Valle S., et al. Typing of dengue viruses in clinical specimens and mosquitoes by single-tube multiplex reverse transcriptase PCR. J Clin Microbiol 1998, 36:2634-2639.
29. van den Ham H.J., de Jager W., Bijlsma J.W., Prakken B.J., de Boer R.J. Differential cytokine profiles in juvenile idiopathic arthritis subtypes revealed by cluster analysis. Rheumatology 2009, 48:899-905.
30. Bernardo M.M., Fridman R. TIMP-2 (tissue inhibitor of metalloproteinase-2) regulates MMP-2 (matrix metalloproteinase-2) activity in the extracellular environment after pro-MMP-2 activation by MT1 (membrane type 1)-MMP. Biochem J 2003, 374:739-745.
31. Huy N.T., Van Giang T., Thuy D.H., Kikuchi M., Hien T.T., Zamora J., et al. Factors associated with dengue shock syndrome: a systematic review and meta-analysis. PLoS Negl Trop Dis 2013, 7:e2412.
32. Trung D.T., Thao le T.T., Dung N.M., Ngoc T.V., Hien T.T., Chau N.V., et al. Clinical features of dengue in a large Vietnamese cohort: intrinsically lower platelet counts and greater risk for bleeding in adults than children. PLoS Negl Trop Dis 2012, 6:e1679.
33. Harris E., Videa E., Perez L., Sandoval E., Tellez Y., Perez M.L., et al. Clinical, epidemiologic, and virologic features of dengue in the 1998 epidemic in Nicaragua. Am J Trop Med Hyg 2000, 63:5-11.
34. Bethell D.B., Gamble J., Pham P.L., Nguyen M.D., Tran T.H., Ha T.H., et al. Noninvasive measurement of microvascular leakage in patients with dengue hemorrhagic fever. Clin Infect Dis 2001, 32:243-253.
35. Vaughn D.W., Green S., Kalayanarooj S., Innis B.L., Nimmannitya S., Suntayakorn S., et al. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 2000, 181:2-9.
36. Khongphatthanayothin A., Suesaowalak M., Muangmingsook S., Bhattarakosol P., Pancharoen C. Hemodynamic profiles of patients with dengue hemorrhagic fever during toxic stage: an echocardiographic study. Intens Care Med 2003, 29:570-574.
37. Luplertlop N., Misse D. MMP cellular responses to dengue virus infection-induced vascular leakage. Japn J Infect Dis 2008, 61:298-301.
38. Luplertlop N., Misse D., Bray D., Deleuze V., Gonzalez J.P., Leardkamolkarn V., et al. Dengue-virus-infected dendritic cells trigger vascular leakage through metalloproteinase overproduction. EMBO Rep 2006, 7:1176-1181.
39. Furuta T., Murao L.A., Lan N.T., Huy N.T., Huong V.T., Thuy T.T., et al. Association of mast cell-derived VEGF and proteases in Dengue shock syndrome. PLoS Negl Trop Dis 2012, 6:e1505.
40. Seet R.C., Chow A.W., Quek A.M., Chan Y.H., Lim E.C. Relationship between circulating vascular endothelial growth factor and its soluble receptors in adults with dengue virus infection: a case-control study. Int J Infect Dis 2009, 13:e248-e253.
41. Rathakrishnan A., Wang S.M., Hu Y., Khan A.M., Ponnampalavanar S., Lum L.C., et al. Cytokine expression profile of dengue patients at different phases of illness. PLoS One 2012, 7:e55221.
42. Ong S.P., Ng M.L., Chu J.J. Differential regulation of angiopoietin 1 and angiopoietin 2 during dengue virus infection of human umbilical vein endothelial cells: implications for endothelial hyperpermeability. Med Microbiol Immunol 2013, 202:437-452.
43. Fiedler U., Scharpfenecker M., Koidl S., Hegen A., Grunow V., Schmidt J.M., et al. The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood 2004, 103:4150-4156.
44. Cardier J.E., Rivas B., Romano E., Rothman A.L., Perez-Perez C., Ochoa M., et al. Evidence of vascular damage in dengue disease: demonstration of high levels of soluble cell adhesion molecules and circulating endothelial cells. Endothelium 2006, 13:335-340.
45. Gavard J., Gutkind J.S. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 2006, 8:1223-1234.
46. Krishnamurti C., Kalayanarooj S., Cutting M.A., Peat R.A., Rothwell S.W., Reid T.J., et al. Mechanisms of hemorrhage in dengue without circulatory collapse. Am J Trop Med Hyg 2001, 65:840-847.
47. Nachman R.L., Rafii S. Platelets, petechiae, and preservation of the vascular wall. N Engl J Med 2008, 359:1261-1270.