Influenza virus and endothelial cells: A species specific relationship

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Short, Kirsty R ^a,b   Veldhuis Kroeze, Edwin J B ^a   Reperant, Leslie A ^a   Richard, Mathilde ^a   Kuiken, Thijs ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Endothelial cells; Highly pathogenic avian influenza; Influenza virus; Poultry; Zoonotic infection

Indexed keywords

CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; PADGEM PROTEIN; TRYPSIN; TUMOR NECROSIS FACTOR ALPHA;

CAT; CELL MEMBRANE PERMEABILITY; CHARADRIIFORMES; DISSEMINATED INTRAVASCULAR CLOTTING; ENDOTHELIUM CELL; GALLIFORMES; HUMAN; INFLAMMATION; INFLUENZA VIRUS A H5N1; INTESTINE; LUNG ALVEOLUS CELL TYPE 2; MICROTHROMBUS; MORTALITY; NECROSIS; NONHUMAN; POULTRY; PROTEIN EXPRESSION; RESPIRATORY SYSTEM; REVIEW; THROMBOCYTOPENIA; VIRAL TROPISM; VIRUS INFECTION; VIRUS RELEASE; WATERFOWL;

ANATIDAE; AVES; GALLUS GALLUS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 84920663663     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00653     Document Type: Review

References (65)

1. Armstrong, S. M., Darwish, I., and Lee, W. L. (2013). Endothelial activation and dysfunction in the pathogenesis of influenza A virus infection. Virulence 4, 6. doi: 10.4161/viru.25779
2. Armstrong, S. M., Wang, C., Tigdi, J., Si, X., Dumpit, C., Charles, S., et al. (2012). Influenza infects lung microvascular endothelium leading to microvascular leak: role of apoptosis and claudin-5. PLoS ONE 7:e47323. doi: 10.1371/journal.pone.0047323
3. Babinska, A., Kedees, M. H., Athar, H., Ahmed, T., Batuman, O., Ehrlich, Y. H., et al. (2002). F11-receptor (F11R/JAM) mediates platelet adhesion to endothelial cells: role in inflammatory thrombosis. Thromb. Haemost. 88, 843-850. doi: 10.1267/th02110843
4. Becker, W. (1966). The isolation and classification of tern virus: influenza virus A/tern/South Africa/1961. J. Hyg. 64, 309-320. doi: 10.1017/S0022172400040596
5. Bertran, K., Dolz, R., Busquets, N., Gamino, V., Vergara-Alert, J., Chaves, A. J., et al. (2013). Pathobiology and transmission of highly and low pathogenic avian influenza viruses in European quail (Coturnix c. coturnix). Vet. Res. 44:23. doi: 10.1186/1297-9716-44-23
6. Bertran, K., Perez-Ramirez, E., Busquets, N., Dolz, R., Ramis, A., Darji, A., et al. (2011). Pathogenesis and transmissibility of highly (H7N1) and low (H7N9) pathogenic avian influenza virus infection in red-legged partridge (Alectoris rufa). Vet. Res. 42:24. doi: 10.1186/1297-9716-42-24
7. Bröjer, C., Ågren, E. O., Uhlhorn, H., Bernodt, K., Mörner, T., Jansson, S., et al. (2009). Pathology of natural highly pathogenic avian influenza H5N1 infection in wild tufted ducks (Aythya fuligula). J. Vet. Diagn. Invest. 21, 579-587. doi: 10.1177/104063870902100501
8. Brown, C., Olander, H., and Senne, D. (1992). A pathogenesis study of highly pathogenic avian influenza virus H5N2 in chickens, using immunohistochemistry. J. Comp. Pathol. 107, 341-348. doi: 10.1016/0021-9975(92)90009-J
9. Brown, J. D., Stallknecht, D. E., Beck, J. R., Suarez, D. L., and Swayne, D. E. (2006). Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerg. Infect. Dis. 12, 1663-1670. doi: 10.3201/eid1211.060652
10. Brown, J. D., Stallknecht, D. E., and Swayne, D. E. (2008a). Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerg. Infect. Dis. 14, 136-142. doi: 10.3201/eid1401.070740
11. Brown, J. D., Stallknecht, D. E., and Swayne, D. E. (2008b). Experimental infections of herring gulls (Larus argentatus) with H5N1 highly pathogenic avian influenza viruses by intranasal inoculation of virus and ingestion of virus-infected chicken meat. Avian Pathol. 37, 393-397. doi: 10.1080/03079450802216595
12. Bunce, P. E., High, S. M., Nadjafi, M., Stanley, K., Liles, W. C., and Christian, M. D. (2011). Pandemic H1N1 influenza infection and vascular thrombosis. Clin. Infect. Dis. 52, e14-e17. doi: 10.1093/cid/ciq125
13. Chan, M., Chan, R., Yu, W., Ho, C., Chui, W., Lo, C., et al. (2009). Influenza H5N1 virus infection of polarized human alveolar epithelial cells and lung microvascular endothelial cells. Respir. Res. 10:102. doi: 10.1186/1465-9921-10-102
14. Daoust, P.-Y., Kibenge, F. S., Fouchier, R. A., Van De Bildt, M. W., Van Riel, D., and Kuiken, T. (2011). Replication of low pathogenic avian influenza virus in naturally infected mallard ducks (Anas platyrhynchos) causes no morphologic lesions. J. Wildl. Dis. 47, 401-409. doi: 10.7589/0090-3558-47.2.401
15. Ellis, T. M., Bousfield, R. B., Bissett, L. A., Dyrting, K. C., Luk, G. S., Tsim, S. T., et al. (2004). Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathol. 33, 492-505. doi: 10.1080/03079450400003601
16. Feldmann, A., Schäfer, M. K.-H., Garten, W., and Klenk, H.-D. (2000). Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos. J. Virol. 74, 8018-8027. doi: 10.1128/JVI.74.17.8018-8027.2000
17. Gorin, A. B., and Stewart, P. A. (1979). Differential permeability of endothelial and epithelial barriers to albumin flux. J. Appl. Physiol. 47, 1315-1324.
18. Gu, J., Xie, Z., Gao, Z., Liu, J., Korteweg, C., Ye, J., et al. (2007). H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 370, 1137-1145. doi: 10.1016/S0140-6736(07)61515-3
19. Hooper, P., and Selleck, P. (2003). Pathology of low and high virulent influenza virus infections. Avian Dis. 47, 134-141.
20. Ito, T., Kobayashi, Y., Morita, T., Horimoto, T., and Kawaoka, Y. (2002). Virulent influenza A viruses induce apoptosis in chickens. Virus Res. 84, 27-35. doi: 10.1016/S0168-1702(01)00414-2
21. Jones, Y. L., and Swayne, D. E. (2004). Comparative pathobiology of low and high pathogenicity H7N3 Chilean avian influenza viruses in chickens. Avian Dis. 48, 119-128. doi: 10.1637/7080
22. Kalthoff, D., Breithaupt, A., Teifke, J. P., Globig, A., Harder, T., Mettenleiter, T. C., et al. (2008). Highly pathogenic avian influenza virus (H5N1) in experimentally infected adult mute swans. Emerg. Infect. Dis. 14, 1267-1270. doi: 10.3201/eid1408.080078
23. Kuiken, T., Van Den Brand, J., Van Riel, D., Pantin-Jackwood, M., and Swayne, D. (2010). Comparative pathology of select agent influenza a virus infections. Vet. Pathol. 47, 893-914. doi: 10.1177/0300985810378651
24. Kwon, Y.-K., Joh, S.-J., Kim, M.-C., Sung, H.-W., Lee, Y.-J., Choi, J.-G., et al. (2005). Highly pathogenic avian influenza (H5N1) in the commercial domestic ducks of South Korea. Avian Pathol. 34, 367-370. doi: 10.1080/03079450500181257
25. Kwon, Y. K., Thomas, C., and Swayne, D. E. (2010). Variability in pathobiology of South Korean H5N1 high-pathogenicity avian influenza virus infection for 5 species of migratory waterfowl. Vet. Pathol. 47, 495-506. doi: 10.1177/0300985809359602
26. Lee, C. W., Suarez, D. L., Tumpey, T. M., Sung, H. W., Kwon, Y. K., Lee, Y. J., et al. (2005). Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J. Virol. 79, 3692-3702. doi: 10.1128/JVI.79.6.3692-3702.2005
27. Londt, B. Z., Nunez, A., Banks, J., Nili, H., Johnson, L. K., and Alexander, D. J. (2008). Pathogenesis of highly pathogenic avian influenza A/turkey/Turkey/1/2005 H5N1 in Pekin ducks (Anas platyrhynchos) infected experimentally. Avian Pathol. 37, 619-627. doi: 10.1080/03079450802499126
28. Muramoto, Y., Ozaki, H., Takada, A., Park, C. H., Sunden, Y., Umemura, T., et al. (2006). Highly pathogenic H5N1 influenza virus causes coagulopathy in chickens. Microbiol. Immunol. 50, 73-81. doi: 10.1111/j.1348-0421.2006.tb03764.x
29. Mutinelli, F., Capua, I., Terregino, C., and Cattoli, G. (2003). Clinical, gross, and microscopic findings in different avian species naturally infected during the H7N1 low- and high-pathogenicity avian influenza epidemics in Italy during 1999 and 2000. Avian Dis. 47, 844-848. doi: 10.1637/0005-2086-47.s3.844
30. Nakamura, K., Imada, T., Imai, K., Yamamoto, Y., Tanimura, N., Yamada, M., et al. (2008). Pathology of specific-pathogen-free chickens inoculated with H5N1 avian influenza viruses isolated in Japan in 2004. Avian Dis. 52, 8-13. doi: 10.1637/8027-060607-Reg
31. Nakatani, H., Nakamura, K., Yamamoto, Y., Yamada, M., and Yamamoto, Y. (2005). Epidemiology, pathology, and immunohistochemistry of layer hens naturally affected with H5N1 highly pathogenic avian influenza in Japan. Avian Dis. 49, 436-441. doi: 10.1637/7304-110504R1.1
32. Neufeld, J. L., Embury-Hyatt, C., Berhane, Y., Manning, L., Ganske, S., and Pasick, J. (2009). Pathology of highly pathogenic avian influenza virus (H5N1) infection in Canada geese (Branta canadensis): preliminary studies. Vet. Pathol. 46, 966-970. doi: 10.1354/vp.08-VP-0168-E-FL
33. Noymer, A., and Garenne, M. (2000). The 1918 influenza epidemic's effects on sex differentials in mortality in the United States. Popul. Dev. Rev. 26, 565-581. doi: 10.1111/j.1728-4457.2000.00565.x
34. Ocaña-Macchi, M., Bel, M., Guzylack-Piriou, L., Ruggli, N., Liniger, M., McCullough, K. C., et al. (2009). Hemagglutinin-dependent tropism of H5N1 avian influenza virus for human endothelial cells. J. Virol. 83, 12947-12955. doi: 10.1128/JVI.00468-09
35. Ogiwara, H., Yasui, F., Munekata, K., Takagi-Kamiya, A., Munakata, T., Nomura, N., et al. (2014). Histopathological evaluation of the diversity of cells susceptible to H5N1 virulent avian influenza virus. Am. J. Pathol. 184, 171-183. doi: 10.1016/j.ajpath.2013.10.004
36. Pantin-Jackwood, M. J., and Swayne, D. E. (2007). Pathobiology of Asian highly pathogenic avian influenza H5N1 virus infections in ducks. Avian Dis. 51, 250-259. doi: 10.1637/7710-090606R.1
37. Pantin-Jackwood, M., and Swayne, D. (2009). Pathogenesis and pathobiology of avian influenza virus infection in birds. Rev. Sci. Tech. 28, 113-136.
38. Pasick, J., Berhane, Y., Embury-Hyatt, C., Copps, J., Kehler, H., Handel, K., et al. (2007). Susceptibility of Canada Geese (Branta canadensis) to highly pathogenic avian influenza virus (H5N1). Emerg. Infect. Dis. 13, 1821-1827. doi: 10.3201/eid1312.070502
39. Perkins, L. E., and Swayne, D. E. (2001). Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Vet. Pathol. 38, 149-164. doi: 10.1354/vp.38-2-149
40. Perkins, L. E., and Swayne, D. E. (2002a). Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons. Avian Dis. 46, 53-63. doi: 10.1637/0005-2086(2002)046[0053:POAHKO]2.0.CO;2
41. Perkins, L. E., and Swayne, D. E. (2002b). Susceptibility of laughing gulls (Larus atricilla) to H5N1 and H5N3 highly pathogenic avian influenza viruses. Avian Dis. 46, 877-885. doi: 10.1637/0005-2086(2002)046[0877:SOLGLA]2.0.CO;2
42. Perkins, L. E., and Swayne, D. E. (2003). Comparative susceptibility of selected avian and mammalian species to a Hong Kong-origin H5N1 high-pathogenicity avian influenza virus. Avian Dis. 47, 956-967. doi: 10.1637/0005-2086-47.s3.956
43. Perrone, L. A., Plowden, J. K., García-Sastre, A., Katz, J. M., and Tumpey, T. M. (2008). H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4:e1000115. doi: 10.1371/journal.ppat.1000115
44. Piantadosi, C. A., and Schwartz, D. A. (2004). The acute respiratory distress syndrome. Ann. Intern. Med. 141, 460-470. doi: 10.7326/0003-4819-141-6-200409210-00012
45. Reperant, L. A., Van De Bildt, M. W., Van Amerongen, G., Leijten, L. M., Watson, S., Palser, A., et al. (2012). Marked endotheliotropism of highly pathogenic avian influenza virus H5N1 following intestinal inoculation in cats. J. Virol. 86, 1158-1165. doi: 10.1128/JVI.06375-11
46. Rimmelzwaan, G. F., Van Riel, D., Baars, M., Bestebroer, T. M., Van Amerongen, G., Fouchier, R. A., et al. (2006). Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am. J. Pathol. 168, 176-183. doi: 10.2353/ajpath.2006.050466
47. Schat, K. A., Bingham, J., Butler, J. M., Chen, L.-M., Lowther, S., Crowley, T. M., et al. (2012). Role of position 627 of PB2 and the multibasic cleavage site of the hemagglutinin in the virulence of H5N1 avian influenza virus in chickens and ducks. PLoS ONE 7:e30960. doi: 10.1371/journal.pone.0030960
48. Shieh, W.-J., Blau, D. M., Denison, A. M., Deleon-Carnes, M., Adem, P., Bhatnagar, J., et al. (2010). 2009 pandemic influenza A (H1N1): pathology and pathogenesis of 100 fatal cases in the United States. Am. J. Pathol. 177, 166-175. doi: 10.2353/ajpath.2010.100115
49. Shinya, K., Ebina, M., Yamada, S., Ono, M., Kasai, N., and Kawaoka, Y. (2006). Avian flu: influenza virus receptors in the human airway. Nature 440, 435-436. doi: 10.1038/440435a
50. Suarez, D. L., Perdue, M. L., Cox, N., Rowe, T., Bender, C., Huang, J., et al. (1998). Comparisons of highly virulent H5N1 influenza A viruses isolated from humans and chickens from Hong Kong. J. Virol. 72, 6678-6688.
51. Suzuki, K., Okada, H., Itoh, T., Tada, T., Mase, M., Nakamura, K., et al. (2009). Association of increased pathogenicity of Asian H5N1 highly pathogenic avian influenza viruses in chickens with highly efficient viral replication accompanied by early destruction of innate immune responses. J. Virol. 83, 7475-7486. doi: 10.1128/JVI.01434-08
52. Swayne, D. E. (2007). Understanding the complex pathobiology of high pathogenicity avian influenza viruses in birds. Avian Dis. 51, 242-249. doi: 10.1637/7763-110706-REGR.1
53. Teifke, J. P., Klopfleisch, R., Globig, A., Starick, E., Hoffmann, B., Wolf, P. U., et al. (2007). Pathology of natural infections by H5N1 highly pathogenic avian influenza virus in mute (Cygnus olor) and whooper (Cygnus cygnus) swans. Vet. Pathol. 44, 137-143. doi: 10.1354/vp.44-2-137
54. Teijaro, J. R., Walsh, K. B., Cahalan, S., Fremgen, D. M., Roberts, E., Scott, F., et al. (2011). Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell 146, 980-991. doi: 10.1016/j.cell.2011.08.015
55. van Riel, D., Den Bakker, M. A., Leijten, L. M., Chutinimitkul, S., Munster, V. J., De Wit, E., et al. (2010). Seasonal and pandemic human influenza viruses attach better to human upper respiratory tract epithelium than avian influenza viruses. Am. J. Pathol. 176, 1614-1618. doi: 10.2353/ajpath.2010.090949
56. van Riel, D., Munster, V., De Wit, E., Rimmelzwaan, G., Fouchier, R., Osterhaus, A., et al. (2007a). Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171, 1215. doi: 10.2353/ajpath.2007.070248
57. van Riel, D., Munster, V. J., De Wit, E., Rimmelzwaan, G. F., Fouchier, R. A., Osterhaus, A. D., et al. (2006). H5N1 virus attachment to lower respiratory tract. Science 312, 399-399. doi: 10.1126/science.1125548
58. van Riel, D., Munster, V. J., De Wit, E., Rimmelzwaan, G. F., Fouchier, R. A., Osterhaus, A. D., et al. (2007b). Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171, 1215-1223. doi: 10.2353/ajpath.2007.070248
59. van Riel, D., van den Brand, J., Munster, V., Besteboer, T., Fouchier, R., Osterhaus, A., et al. (2009). Pathology and virus distribution in chickens naturally infected with highly pathogenic avian influenza A virus (H7N7) during the 2003 outbreak in The Netherlands. Vet. Pathol. Online 46, 971-976. doi: 10.1354/vp.08-VP-0215-K-BC
60. Wang, S., Le, T. Q., Kurihara, N., Chida, J., Cisse, Y., Yano, M., et al. (2010). Influenza Virus-cytokine-protease cycle in the pathogenesis of vascular hyperpermeability in severe influenza. J. Infect. Dis. 202, 991-1001. doi: 10.1086/656044
61. Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., and Kawaoka, Y. (1992). Evolution and ecology of influenza A viruses. Microbiol. Rev. 56, 152-179.
62. Wibawa, H., Bingham, J., Nuradji, H., Lowther, S., Payne, J., Harper, J., et al. (2013). The pathobiology of two Indonesian H5N1 avian influenza viruses representing different clade 2.1 sublineages in chickens and ducks. Comp. Immunol. Microbiol. Infect. Dis. 36, 175-191. doi: 10.1016/j.cimid.2012.12.001
63. Yamamoto, Y., Nakamura, K., Kitagawa, K., Ikenaga, N., Yamada, M., Mase, M., et al. (2007). Severe nonpurulent encephalitis with mortality and feather lesions in call ducks (Anas platyrhyncha var. domestica) inoculated intravenously with H5N1 highly pathogenic avian influenza virus. Avian Dis. 51, 52-57. doi: 10.1637/0005-2086(2007)051[0052:SNEWMA]2.0.CO;2
64. Zeng, H., Pappas, C., Belser, J. A., Houser, K. V., Zhong, W., Wadford, D. A., et al. (2012). Human pulmonary microvascular endothelial cells support productive replication of highly pathogenic avian influenza viruses: possible involvement in the pathogenesis of human H5N1 virus infection. J. Virol. 86, 667-678. doi: 10.1128/JVI.06348-11
65. Zhou, J. Y., Shen, H. G., Chen, H. X., Tong, G. Z., Liao, M., Yang, H. C., et al. (2006). Characterization of a highly pathogenic H5N1 influenza virus derived from bar-headed geese in China. J. Gen. Virol. 87, 1823-1833. doi: 10.1099/vir.0.81800-0