Caveolae-mediated albumin transcytosis is enhanced in dengue-infected human endothelial cells: A model of vascular leakage in dengue hemorrhagic fever

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Chanthick, Chanettee ^a   Kanlaya, Rattiyaporn ^a,b   Kiatbumrung, Rattanaporn ^a,b   Pattanakitsakul, Sa Nga ^a   Thongboonkerd, Visith ^a,b  

^a MAHIDOL UNIVERSITY   (Thailand)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN SERUM ALBUMIN; NYSTATIN;

BIOLOGICAL MODEL; CAPILLARY PERMEABILITY; CAVEOLA; CELL LINE; CYTOLOGY; DENGUE VIRUS; DRUG EFFECT; ENDOTHELIUM CELL; HUMAN; METABOLISM; PHYSIOLOGY; SEVERE DENGUE; TRANSCYTOSIS; VIROLOGY;

CAPILLARY PERMEABILITY; CAVEOLAE; CELL LINE; DENGUE VIRUS; ENDOTHELIAL CELLS; HUMANS; MODELS, BIOLOGICAL; NYSTATIN; SERUM ALBUMIN, HUMAN; SEVERE DENGUE; TRANSCYTOSIS;

EID: 84983362279     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep31855     Document Type: Article

References (44)

1. Mackenzie, J. S., Gubler, D. J. & Petersen, L. R. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 10, S98-109 (2004).
2. Nimmannitya, S. Clinical spectrum and management of dengue haemorrhagic fever. Southeast Asian J Trop. Med. Public Health 18, 392-397 (1987).
3. Srikiatkhachorn, A. Plasma leakage in dengue haemorrhagic fever. Thromb. Haemost. 102, 1042-1049 (2009).
4. Srikiatkhachorn, A. & Green, S. Markers of dengue disease severity. Curr. Top. Microbiol. Immunol. 338, 67-82 (2010).
5. Potts, J. A. et al. Prediction of dengue disease severity among pediatric Thai patients using early clinical laboratory indicators. PLoS. Negl. Trop. Dis. 4, e769 (2010).
6. Mehta, D. & Malik, A. B. Signaling mechanisms regulating endothelial permeability. Physiol Rev. 86, 279-367 (2006).
7. Komarova, Y. & Malik, A. B. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu. Rev. Physiol 72, 463-493 (2010).
8. Beatty, P. R. et al. Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci Transl. Med 7, 304ra141 (2015).
9. Hoh, B. P. et al. Common variants of chemokine receptor gene CXCR3 and its ligands CXCL10 and CXCL11 associated with vascular permeability of dengue infection in peninsular Malaysia. Hum. Immunol. 76, 421-426 (2015).
10. Yacoub, S., Wertheim, H., Simmons, C. P., Screaton, G. & Wills, B. Microvascular and endothelial function for risk prediction in dengue: an observational study. Lancet 385 Suppl 1, S102 (2015).
11. Halstead, S. B. Dengue Antibody-Dependent Enhancement: Knowns and Unknowns. Microbiol. Spectr. 2 (2014).
12. Predescu, D., Vogel, S. M. & Malik, A. B. Functional and morphological studies of protein transcytosis in continuous endothelia. Am. J Physiol Lung Cell Mol. Physiol 287, L895-L901 (2004).
13. Simionescu, M., Popov, D. & Sima, A. Endothelial transcytosis in health and disease. Cell Tissue Res. 335, 27-40 (2009).
14. Minshall, R. D. & Malik, A. B. Transport across the endothelium: regulation of endothelial permeability. Handb. Exp. Pharmacol. 107-144 (2006).
15. Hu, G., Place, A. T. & Minshall, R. D. Regulation of endothelial permeability by Src kinase signaling: vascular leakage versus transcellular transport of drugs and macromolecules. Chem. Biol. Interact. 171, 177-189 (2008).
16. Hu, G., Vogel, S. M., Schwartz, D. E., Malik, A. B. & Minshall, R. D. Intercellular adhesion molecule-1-dependent neutrophil adhesion to endothelial cells induces caveolae-mediated pulmonary vascular hyperpermeability. Circ. Res. 102, e120-e131 (2008).
17. Tuma, P. & Hubbard, A. L. Transcytosis: crossing cellular barriers. Physiol Rev. 83, 871-932 (2003).
18. Ziegler, U. & Groscurth, P. Morphological features of cell death. News Physiol Sci 19, 124-128 (2004).
19. Suwanik, R. et al. Plasma volume and other fluid case studies in Thai Hemorrhagic Fever. J Med Assoc Thai 50, 48-66 (1967).
20. Wang, C. C. et al. Chest radiographic presentation in patients with dengue hemorrhagic Fever. Am. J Trop. Med Hyg. 77, 291-296 (2007).
21. Venkata Sai, P. M., Dev, B. & Krishnan, R. Role of ultrasound in dengue fever. Br. J Radiol. 78, 416-418 (2005).
22. Rojanakarin, P., Sriraksa, K., Vasanawatthana, S. & Suesirisawad, C. Serial ultrasonography for early detection of plasma leakage in dendue hemorrhagic fever. Khon Kaen Hosp Med J 33, 19-27 (2009).
23. Vasanawatthana, S., Rojanakarin, P., Suesirisawad, C. & Malasit, P. Serial ultrasonography for early detection of plasma leakage in dendue hemorrhagic fever. Khon Kaen Hosp Med J 36, 16-23 (2012).
24. Nagy, J. A., Dvorak, A. M. & Dvorak, H. F. Vascular hyperpermeability, angiogenesis, and stroma generation. Cold Spring Harb. Perspect. Med 2, a006544 (2012).
25. Nagy, J. A., Benjamin, L., Zeng, H., Dvorak, A. M. & Dvorak, H. F. Vascular permeability, vascular hyperpermeability and angiogenesis. Angiogenesis. 11, 109-119 (2008).
26. Dvorak, H. F. Vascular permeability to plasma, plasma proteins, and cells: an update. Curr. Opin. Hematol. 17, 225-229 (2010).
27. Mehta, D., Bhattacharya, J., Matthay, M. A. & Malik, A. B. Integrated control of lung fluid balance. Am. J Physiol Lung Cell Mol. Physiol 287, L1081-L1090 (2004).
28. Simionescu, M. & Antohe, F. Functional ultrastructure of the vascular endothelium: changes in various pathologies. Handb. Exp. Pharmacol. 41-69 (2006).
29. Simionescu, M., Gafencu, A. & Antohe, F. Transcytosis of plasma macromolecules in endothelial cells: a cell biological survey. Microsc. Res. Tech. 57, 269-288 (2002).
30. Ghitescu, L., Fixman, A., Simionescu, M. & Simionescu, N. Specific binding sites for albumin restricted to plasmalemmal vesicles of continuous capillary endothelium: receptor-mediated transcytosis. J Cell Biol. 102, 1304-1311 (1986).
31. Ghitescu, L. & Bendayan, M. Transendothelial transport of serum albumin: a quantitative immunocytochemical study. J Cell Biol. 117, 745-755 (1992).
32. Hankins, J. The role of albumin in fluid and electrolyte balance. J Infus. Nurs. 29, 260-265 (2006).
33. Muro, S., Koval, M. & Muzykantov, V. Endothelial endocytic pathways: gates for vascular drug delivery. Curr. Vasc. Pharmacol. 2, 281-299 (2004).
34. Ivanov, A. I. Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? Methods Mol. Biol. 440, 15-33 (2008).
35. Sahaphong, S., Riengrojpitak, S., Bhamarapravati, N. & Chirachariyavej, T. Electron microscopic study of the vascular endothelial cell in dengue hemorrhagic fever. Southeast Asian J Trop. Med Public Health 11, 194-204 (1980).
36. Schnitzer, J. E. & Oh, P. Albondin-mediated capillary permeability to albumin. Differential role of receptors in endothelial transcytosis and endocytosis of native and modified albumins. J Biol. Chem. 269, 6072-6082 (1994).
37. Tiruppathi, C., Finnegan, A. & Malik, A. B. Isolation and characterization of a cell surface albumin-binding protein from vascular endothelial cells. Proc Natl Acad Sci USA 93, 250-254 (1996).
38. Shajahan, A. N. et al. Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells. J Biol. Chem. 279, 20392-20400 (2004).
39. Tiruppathi, C., Song, W., Bergenfeldt, M., Sass, P. & Malik, A. B. Gp60 activation mediates albumin transcytosis in endothelial cells by tyrosine kinase-dependent pathway. J Biol. Chem. 272, 25968-25975 (1997).
40. Minshall, R. D. et al. Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol. 150, 1057-1070 (2000).
41. Sun, Y., Hu, G., Zhang, X. & Minshall, R. D. Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ. Res. 105, 676-85, 15 (2009).
42. Hu, G. et al. Isoflurane, but not sevoflurane, increases transendothelial albumin permeability in the isolated rat lung: role for enhanced phosphorylation of caveolin-1. Anesthesiology 104, 777-785 (2006).
43. Pattanakitsakul, S. N. et al. Association of Alix with late endosomal lysobisphosphatidic acid is important for dengue virus infection in human endothelial cells. J Proteome. Res. 9, 4640-4648 (2010).
44. Kanlaya, R., Pattanakitsakul, S. N., Sinchaikul, S., Chen, S. T. & Thongboonkerd, V. Alterations in actin cytoskeletal assembly and junctional protein complexes in human endothelial cells induced by dengue virus infection and mimicry of leukocyte transendothelial migration. J Proteome. Res. 8, 2551-2562 (2009).