Downregulation of angiotensin-converting enzyme 2 by the neuraminidase protein of influenza A (H1N1) virus

Virus Research

Volumn 185, Issue , 2014, Pages 64-71

  Liu, Xin ^a   Yang, Ning ^b   Tang, Jun ^c   Liu, Song ^c   Luo, Deyan ^a   Duan, Qing ^a   Wang, Xiliang ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

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

^c INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

ACE2; Downregulation; Influenza; Neuraminidase

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; DIPEPTIDYL CARBOXYPEPTIDASE; NA PROTEIN, INFLUENZA A VIRUS; SIALIDASE; VIRUS PROTEIN;

DOWN REGULATION; ENZYMOLOGY; GENETICS; HUMAN; INFLUENZA; INFLUENZA VIRUS A H1N1; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; VIROLOGY; VIRUS REPLICATION;

DOWN-REGULATION; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; NEURAMINIDASE; PEPTIDYL-DIPEPTIDASE A; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84898645626     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.03.010     Document Type: Article

References (30)

1. Carmona F., Carlotti A.P., Ramalho L.N., Costa R.S., Ramalho F.S. Evidence of renal infection in Fatal Cases of 2009 Pandemic Influenza A (H1N1). Am. J. Clin. Pathol. 2011, 136(3):416-423.
2. Chen G., Gharib T.G., Huang C.C., Taylor J.M., Misek D.E., Kardia S.L., Giordano T.J., Iannettoni M.D., Orringer M.B., Hanash S.M., Beer D.G. Discordant protein and mRNA expression in lung adenocarcinomas. Mol. Cell. Proteomics 2002, 1(4):304-313.
3. Clarke N.E., Turner A.J. Angiotensin-converting enzyme 2: the first decade. Int. J. Hypertens. 2012, 2012:307315.
4. Ehlers M.R., Riordan J.F. Membrane proteins with soluble counterparts: role of proteolysis in the release of transmembrane proteins. Biochemistry 1991, 30(42):10065-10074.
5. Glezen W.P. Serious morbidity and mortality associated with influenza epidemics. Epidemiol. Rev. 1982, 4:25-44.
6. Glowacka I., Bertram S., Herzog P., Pfefferle S., Steffen I., Muench M.O., Simmons G., Hofmann H., Kuri T., Weber F., Eichler J., Drosten C., Pohlmann S. Differential downregulation of ACE2 by the spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus NL63. J. Virol. 2010, 84(2):1198-1205.
7. Haga S., Yamamoto N., Nakai-Murakami C., Osawa Y., Tokunaga K., Sata T., Sasazuki T., Ishizaka Y. Modulation of TNF-alpha-converting enzyme by the spike protein of SARS-CoV and ACE2 induces TNF-alpha production and facilitates viral entry. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(22):7809-7814.
8. Hamming I., Cooper M.E., Haagmans B.L., Hooper N.M., Korstanje R., Osterhaus A.D., Timens W., Turner A.J., Navis G., van Goor H. The emerging role of ACE2 in physiology and disease. J. Pathol. 2007, 212(1):1-11.
9. Hamming I., Timens W., Bulthuis M.L., Lely A.T., Navis G., van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 2004, 203(2):631-637.
10. He X., Han B., Mura M., Xia S., Wang S., Ma T., Liu M., Liu Z. Angiotensin-converting enzyme inhibitor captopril prevents oleic acid-induced severe acute lung injury in rats. Shock 2007, 28(1):106-111.
11. Hooper N.M., Karran E.H., Turner A.J. Membrane protein secretases. Biochem. J. 1997, 321(Pt 2):265-279.
12. Imai Y., Kuba K., Rao S., Huan Y., Guo F., Guan B., Yang P., Sarao R., Wada T., Leong-Poi H., Crackower M.A., Fukamizu A., Hui C.C., Hein L., Uhlig S., Slutsky A.S., Jiang C., Penninger J.M. Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 2005, 436(7047):112-116.
13. Jerng J.S., Hsu Y.C., Wu H.D., Pan H.Z., Wang H.C., Shun C.T., Yu C.J., Yang P.C. Role of the renin-angiotensin system in ventilator-induced lung injury: an in vivo study in a rat model. Thorax 2007, 62(6):527-535.
14. Jia H.P., Look D.C., Tan P., Shi L., Hickey M., Gakhar L., Chappell M.C., Wohlford-Lenane C., McCray P.B. Ectodomain shedding of angiotensin converting enzyme 2 in human airway epithelia. Am. J. Physiol. Lung Cell Mol. Physiol. 2009, 297(1):L84-L96.
15. Kasowski E.J., Garten R.J., Bridges C.B. Influenza pandemic epidemiologic and virologic diversity: reminding ourselves of the possibilities. Clin. Infect. Dis. 2011, 52(Suppl. 1):S44L 49.
16. Keidar S., Kaplan M., Gamliel-Lazarovich A. ACE2 of the heart: from angiotensin I to angiotensin (1-7). Cardiovasc. Res. 2007, 73(3):463-469.
17. Kuba K., Imai Y., Penninger J.M. Angiotensin-converting enzyme 2 in lung diseases. Curr. Opin. Pharmacol. 2006, 6(3):271-276.
18. Lambert D.W., Yarski M., Warner F.J., Thornhill P., Parkin E.T., Smith A.I., Hooper N.M., Turner A.J. Tumor necrosis factor-alpha convertase (ADAM17) mediates regulated ectodomain shedding of the severe-acute respiratory syndrome-coronavirus (SARS-CoV) receptor, angiotensin-converting enzyme-2 (ACE2). J. Biol. Chem. 2005, 280(34):30113-30119.
19. Lee D.H., Goldberg A.L. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 1998, 8(10):397-403.
20. Li W., Greenough T.C., Moore M.J., Vasilieva N., Somasundaran M., Sullivan J.L., Farzan M., Choe H. Efficient replication of severe acute respiratory syndrome coronavirus in mouse cells is limited by murine angiotensin-converting enzyme 2. J. Virol. 2004, 78(20):11429-11433.
21. Li W., Moore M.J., Vasilieva N., Sui J., Wong S.K., Berne M.A., Somasundaran M., Sullivan J.L., Luzuriaga K., Greenough T.C., Choe H., Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003, 426(6965):450-454.
22. Li W., Zhang C., Sui J., Kuhn J.H., Moore M.J., Luo S., Wong S.K., Huang I.C., Xu K., Vasilieva N., Murakami A., He Y., Marasco W.A., Guan Y., Choe H., Farzan M. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 2005, 24(8):1634-1643.
23. Li X., Molina-Molina M., Abdul-Hafez A., Uhal V., Xaubet A., Uhal B. Angiotensin converting enzyme-2 is protective but downregulated in human and experimental lung fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295(1):L178-L185.
24. Li X., Molina-Molina M., Abdul-Hafez A., Uhal V., Xaubet A., Uhal B.D. Angiotensin converting enzyme-2 is protective but downregulated in human and experimental lung fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol. 2008, 295(1):L178-L185.
25. Marshall R.P., Gohlke P., Chambers R.C., Howell D.C., Bottoms S.E., Unger T., McAnulty R.J., Laurent G.J. Angiotensin II and the fibroproliferative response to acute lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 2004, 286(1):L156-L164.
26. Mitnaul L.J., Castrucci M.R., Murti K.G., Kawaoka Y. The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. J. Virol. 1996, 70(2):873-879.
27. Reed L., Muench H. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 1938, 27(3):493-497.
28. Suttajit M., Winzler R.J. Effect of modification of N-acetylneuraminic acid on the binding of glycoproteins to influenza virus and on susceptibility to cleavage by neuraminidase. J. Biol. Chem. 1971, 246(10):3398-3404.
29. Tobita K., Sugiura A., Enomote C., Furuyama M. Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med. Microbiol. Immunol. 1975, 162(1):9-14.
30. Yang N., Hong X., Yang P., Ju X., Wang Y., Tang J., Li C., Fan Q., Zhang F., Chen Z., Xing L., Zhao Z., Gao X., Liao G., Li Q., Wang X., Li D., Jiang C. The 2009 pandemic A/Wenshan/01/2009 H1N1 induces apoptotic cell death in human airway epithelial cells. J. Mol. Cell Biol. 2011, 3(4):221-229.