Contributions of mast cells and vasoactive products, leukotrienes and chymase, to dengue virus-induced vascular leakage

eLife

Volumn 2013, Issue 2, 2013, Pages

  St John, Ashley L ^a,b   Rathore, Abhay P S ^a   Raghavan, Bhuvanakantham ^a   Ng, Mah Lee ^a   Abraham, Soman N ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CHYMASE; CHYMOSTATIN; CROMOGLYCATE DISODIUM; EVANS BLUE; KETOTIFEN; MONTELUKAST; LEUKOTRIENE;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; CAPILLARY LEAK SYNDROME; CONTROLLED STUDY; DENGUE; DENGUE VIRUS; DISEASE SEVERITY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE; FEMALE; HEMATOCRIT; HEMORRHAGIC FEVER; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; MALE; MAST CELL; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; VASCULAR DISEASE; ANIMAL; CAPILLARY PERMEABILITY; PHYSIOLOGY; VALIDATION STUDY;

ANIMALS; CAPILLARY PERMEABILITY; CHYMASES; DENGUE VIRUS; LEUKOTRIENES; MAST CELLS; MICE;

EID: 84881540233     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00481     Document Type: Article

References (56)

1. Abraham SN, St John AL. 2010. Mast cell-orchestrated immunity to pathogens. Nat Rev Immunol 10:440-52. doi: 10.1038/nri2782.
2. Assuncao-Miranda I, Amaral FA, Bozza FA, Fagundes CT, Sousa LP, Souza DG, et al. 2010. Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection. FASEB J 24:218-28. doi: 10.1096/fj.09-139469.
3. Atrasheuskaya A, Petzelbauer P, Fredeking TM, Ignatyev G. 2003. Anti-TNF antibody treatment reduces mortality in experimental dengue virus infection. FEMS Immunol Med Microbiol 35:33-42. doi: 10.1111/j.1574-695X.2003.tb00646.x.
4. Bente DA, Rico-Hesse R. 2006. Models of dengue virus infection. Drug Discov Today Dis Models 3:97-103. doi: 10.1016/j.ddmod.2006.03.014.
5. Blackley S, Kou Z, Chen H, Quinn M, Rose RC, Schlesinger JJ, et al. 2007. Primary human splenic macrophages, but not T or B cells, are the principal target cells for dengue virus infection in vitro. J Virol 81:13325-34. doi: 10.1128/JVI.01568-07.
6. Bois P. 1964. Mast cells and histamine concentration in muscle and liver of dystrophic mice. Am J Physiol 206:338-40.
7. Boonpucknavig S, Vuttiviroj O, Boonpucknavig V. 1981. Infection of young adult mice with dengue virus type 2. Trans R Soc Trop Med Hyg 75:647-53. doi: 10.1016/0035-9203(81)90142-5.
8. Brett J, Gerlach H, Nawroth P, Steinberg S, Godman G, Stern D. 1989. Tumor necrosis factor/cachectin increases permeability of endothelial cell monolayers by a mechanism involving regulatory G proteins. J Exp Med 169:1977-91. doi: 10.1084/jem.169.6.1977.
9. Busse WW, McGill KA, Horwitz RJ. 1999. Leukotriene pathway inhibitors in asthma and chronic obstructive pulmonary disease. Clin Exp Allergy 29(suppl 2):110-5.
10. Chen HC, Hofman FM, Kung JT, Lin YD, Wu-Hsieh BA. 2007. Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virol 81:5518-26. doi: 10.1128/JVI.02575-06.
11. Chien LJ, Liao TL, Shu PY, Huang JH, Gubler DJ, Chang GJ. 2006. Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses. J Clin Microbiol 44:1295-304. doi: 10.1128/JCM.44.4.1295-1304.2006.
12. Dahlen SE, Bjork J, Hedqvist P, Arfors KE, Hammarstrom S, Lindgren JA, et al. 1981. Leukotrienes promote plasma leakage and leukocyte adhesion in postcapillary venules: in vivo effects with relevance to the acute inflammatory response. Proc Natl Acad Sci USA 78:3887-91. doi: 10.1073/pnas.78.6.3887.
13. Fink J, Gu F, Ling L, Tolfvenstam T, Olfat F, Chin KC, et al. 2007. Host gene expression profiling of dengue virus infection in cell lines and patients. PLoS Negl Trop Dis 1:e86. doi: 10.1371/journal.pntd.0000086.
14. Finkelman FD. 2007. Anaphylaxis: lessons from mouse models. J Allergy Clin Immunol 120:506-15. doi: 10.1016/j.jaci.2007.07.033.
15. Flower RJ, Harvey EA, Kingston WP. 1976. Inflammatory effects of prostaglandin D2 in rat and human skin. Br J Pharmacol 56:229-33. doi: 10.1111/j.1476-5381.1976.tb07446.x.
16. Frangogiannis NG, Lindsey ML, Michael LH, Youker KA, Bressler RB, Mendoza LH, et al. 1998. Resident cardiac mast cells degranulate and release preformed TNF-alpha, initiating the cytokine cascade in experimental canine myocardial ischemia/reperfusion. Circulation 98:699-710. doi: 10.1161/01.CIR.98.7.699.
17. Furuta T, Murao LA, Lan NT, Huy NT, Huong VT, Thuy TT, et al. 2012. Association of mast cell-derived VEGF and proteases in Dengue shock syndrome. PLoS Negl Trop Dis 6:e1505. doi: 10.1371/journal.pntd.0001505.
18. Gowen BB, Julander JG, London NR, Wong MH, Larson D, Morrey JD, et al. 2010. Assessing changes in vascular permeability in a hamster model of viral hemorrhagic fever. Virol J 7:240. doi: 10.1186/1743-422X-7-240.
19. Grimbaldeston MA, Chen CC, Piliponsky AM, Tsai M, Tam SY, Galli SJ. 2005. Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am J Pathol 167:835-48. doi: 10.1016/S0002-9440(10)62055-X.
20. Halstead SB. 2007. Dengue. Lancet 370:1644-52. doi: 10.1016/S0140-6736(07)61687-0.
21. He S, Walls AF. 1998. The induction of a prolonged increase in microvascular permeability by human mast cell chymase. Eur J Pharmacol 352:91-8. doi: 10.1016/S0014-2999(98)00343-4.
22. Holian A, Hamilton R, Scheule RK. 1991. Mechanistic aspects of cromolyn sodium action on the alveolar macrophage: inhibition of stimulation by soluble agonists. Agents Actions 33:318-25. doi: 10.1007/BF01986580.
23. Huang C, Wong GW, Ghildyal N, Gurish MF, Sali A, Matsumoto R, et al. 1997. The tryptase, mouse mast cell protease 7, exhibits anticoagulant activity in vivo and in vitro due to its ability to degrade fibrinogen in the presence of the diverse array of protease inhibitors in plasma. J Biol Chem 272:31885-93. doi: 10.1074/jbc.272.50.31885.
24. Huang KJ, Li SY, Chen SC, Liu HS, Lin YS, Yeh TM, et al. 2000. Manifestation of thrombocytopenia in dengue-2-virus-infected mice. J Gen Virol 81:2177-82.
25. Jessie K, Fong MY, Devi S, Lam SK, Wong KT. 2004. Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis 189:1411-8. doi: 10.1086/383043.
26. Koda W, Harada K, Tsuneyama K, Kono N, Sasaki M, Matsui O, et al. 2000. Evidence of the participation of peribiliary mast cells in regulation of the peribiliary vascular plexus along the intrahepatic biliary tree. Lab Invest 80:1007-17. doi: 10.1038/labinvest.3780106.
27. Koraka P, Murgue B, Deparis X, Setiati TE, Suharti C, van Gorp EC, et al. 2003. Elevated levels of total and dengue virus-specific immunoglobulin E in patients with varying disease severity. J Med Virol 70:91-8. doi: 10.1002/jmv.10358.
28. Kunder CA, St John AL, Abraham SN. 2011. Mast cell modulation of the vascular and lymphatic endothelium. Blood 118:5383-93. doi: 10.1182/blood-2011-07-358432.
29. Leff JA, Busse WW, Pearlman D, Bronsky EA, Kemp J, Hendeles L, et al. 1998. Montelukast, a leukotriene-receptor antagonist, for the treatment of mild asthma and exercise-induced bronchoconstriction. N Engl J Med 339:147-52. doi: 10.1056/NEJM199807163390302.
30. Low JG, Ooi EE, Tolfvenstam T, Leo YS, Hibberd ML, Ng LC, et al. 2006. Early Dengue infection and outcome study (EDEN)-study design and preliminary findings. Ann Acad Med Singapore 35:783-9.
31. Mabalirajan U, Kadhiravan T, Sharma SK, Banga A, Ghosh B. 2005. Th(2) immune response in patients with dengue during defervescence: preliminary evidence. Am J Trop Med Hyg 72:783-5.
32. Malasit P. 1987. Complement and dengue haemorrhagic fever/shock syndrome. Southeast Asian J Trop Med Public Health 18:316-20.
33. McClean SP, Arreaza EE, Lett-Brown MA, Grant JA. 1989. Refractory cholinergic urticaria successfully treated with ketotifen. J Allergy Clin Immunol 83:738-41. doi: 10.1016/0091-6749(89)90008-0.
34. McFadden ER Jnr, Gilbert IA. 1992. Asthma. N Engl J Med 327:1928-37. doi: 10.1056/NEJM199212313272708.
35. McLachlan JB, Hart JP, Pizzo SV, Shelburne CP, Staats HF, Gunn MD, et al. 2003. Mast cell-derived tumor necrosis factor induces hypertrophy of draining lymph nodes during infection. Nat Immunol 4:1199-205. doi: 10.1038/ni1005.
36. Oschatz C, Maas C, Lecher B, Jansen T, Bjorkqvist J, Tradler T, et al. 2011. Mast cells increase vascular permeability by heparin-initiated bradykinin formation in vivo. Immunity 34:258-68. doi: 10.1016/j.immuni.2011.02.008.
37. Paes MV, Pinhao AT, Barreto DF, Costa SM, Oliveira MP, Nogueira AC, et al. 2005. Liver injury and viremia in mice infected with dengue-2 virus. Virology 338:236-46. doi: 10.1016/j.virol.2005.04.042.
38. Rathore AP, Paradkar PN, Watanabe S, Tan KH, Sung C, Connolly JE, et al. 2011. Celgosivir treatment misfolds dengue virus NS1 protein, induces cellular pro-survival genes and protects against lethal challenge mouse model. Antiviral Res 92:453-60. doi: 10.1016/j.antiviral.2011.10.002.
39. Raut CG, Deolankar RP, Kolhapure RM, Goverdhan MK. 1996. Susceptibility of laboratory-bred rodents to the experimental infection with dengue virus type 2. Acta Virol 40:143-6.
40. Rosen L, Khin MM, U T. 1989. Recovery of virus from the liver of children with fatal dengue: reflections on the pathogenesis of the disease and its possible analogy with that of yellow fever. Res Virol 140:351-60. doi: 10.1016/S0923-2516(89)80115-3.
41. Sanchez LF, Hotta H, Hotta S, Homma M. 1986. Degranulation and histamine release from murine mast cells sensitized with dengue virus-immune sera. Microbiol Immunol 30:753-9.
42. Sendo T, Sumimura T, Itoh Y, Goromaru T, Aki K, Yano T, et al. 2003. Involvement of proteinase-activated receptor-2 in mast cell tryptase-induced barrier dysfunction in bovine aortic endothelial cells. Cell Signal 15:773-81. doi: 10.1016/S0898-6568(03)00014-7.
43. Shresta S, Kyle JL, Snider HM, Basavapatna M, Beatty PR, Harris E. 2004. Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T-and B-cell-dependent immunity are less critical. J Virol 78:2701-10. doi: 10.1128/JVI.78.6.2701-2710.2004.
44. St John AL, Abraham SN, Gubler DJ. 2013. Barriers to pre-clinical investigations of anti-dengue immunity and immune-pathology. Nat Rev Immunol.
45. St John AL, Rathore AP, Yap H, Ng ML, Metcalfe DD, Vasudevan SG, et al. 2011. Immune surveillance by mast cells during dengue infection promotes natural killer (NK) and NKT-cell recruitment and viral clearance. Proc Natl Acad Sci USA 108:9190-5. doi: 10.1073/pnas.1105079108.
46. Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J, Sun W, et al. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197:823-9. doi: 10.1084/jem.20021840.
47. Theoharides TC, Sieghart W, Greengard P, Douglas WW. 1980. Antiallergic drug cromolyn may inhibit histamine secretion by regulating phosphorylation of a mast cell protein. Science 207:80-2. doi: 10.1126/science.6153130.
48. Tseng CS, Lo HW, Teng HC, Lo WC, Ker CG. 2005. Elevated levels of plasma VEGF in patients with dengue hemorrhagic fever. FEMS Immunol Med Microbiol 43:99-102. doi: 10.1016/j.femsim.2004.10.004.
49. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, Suntayakorn S, et al. 2000. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181:2-9. doi: 10.1086/315215.
50. Vitarana T, de Silva H, Withana N, Gunasekera C. 1991. Elevated tumour necrosis factor in dengue fever and dengue haemorrhagic fever. Ceylon Med J 36:63-5.
51. Wang Z, Lai Y, Bernard JJ, Macleod DT, Cogen AL, Moss B, et al. 2012. Skin mast cells protect mice against vaccinia virus by triggering mast cell receptor S1PR2 and releasing antimicrobial peptides. J Immunol 188:345-57. doi: 10.4049/jimmunol.1101703.
52. Williams CM, Galli SJ. 2000. Mast cells can amplify airway reactivity and features of chronic inflammation in an asthma model in mice. J Exp Med 192:455-62. doi: 10.1084/jem.192.3.455.
53. World Health Organization. 1997. Dengue hemorrhagic fever: diagnosis, treatment, prevention, and control. 2nd ed. Geneva: World Health Organization. http://www.who.int/csr/resources/publications/dengue/Denguepublication/en.
54. Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, Putvatana R, et al. 2000. Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6:816-20. doi: 10.1038/77553.
55. Yauch LE, Shresta S. 2008. Mouse models of dengue virus infection and disease. Antiviral Res 80:87-93. doi: 10.1016/j.antiviral.2008.06.010.
56. Zellweger RM, Prestwood TR, Shresta S. 2010. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 7:128-39. doi: 10.1016/j.chom.2010.01.004.