Transport of influenza virus neuraminidase (NA) to host cell surface is regulated by ARHGAP21 and Cdc42 proteins

Journal of Biological Chemistry

Volumn 287, Issue 13, 2012, Pages 9804-9816

  Wang, Song ^a   Li, Hua ^a,b   Chen, Yuhai ^a   Wei, Haitao ^a   Gao, George F ^a   Liu, Hongqiang ^a   Huang, Shile ^c   Chen, Ji Long ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDNA MICROARRAY ANALYSIS; CELL SURFACES; CONSTITUTIVELY ACTIVES; HOST CELLS; INACTIVE MUTANTS; INFLUENZA A VIRUS; INFLUENZA VIRUS; NEURAMINIDASE; RHO FAMILY GTPASES; VIRUS ASSEMBLY; VIRUS REPLICATION;

VIRUSES;

CELL MEMBRANES;

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SHORT HAIRPIN RNA; VIRUS SIALIDASE;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; DNA MICROARRAY; GENE OVEREXPRESSION; INFLUENZA VIRUS A; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS REPLICATION;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CHICKENS; DOGS; GTPASE-ACTIVATING PROTEINS; HELA CELLS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; NEURAMINIDASE; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; VIRAL PROTEINS; VIRUS REPLICATION;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 84858980804     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.312959     Document Type: Article

References (48)

1. Wiley, D. C., and Skehel, J. J. (1987) The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Ann. Rev. Biochem. 56, 365-394
2. Weis, W., Brown, J. H., Cusack, S., Paulson, J. C., Skehel, J. J., and Wiley, D. C. (1988) Structure of the influenza virus hemagglutinin complexed with its receptor, sialic acid. Nature 333, 426-431
3. Gubareva, L. V. (2004) Molecular mechanisms of influenza virus resistance to neuraminidase inhibitors. Virus Res. 103, 199-203
4. Liu, C., Eichelberger, M. C., Compans, R. W., and Air, G. M. (1995) Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. J. Virol. 69, 1099-1106
5. Ohuchi, M., Asaoka, N., Sakai, T., and Ohuchi, R. (2006) Roles of neuraminidase in the initial stage of influenza virus infection. Microbes Infect. 8, 1287-1293 (Pubitemid 43831693)
6. Li, Q., Qi, J., Zhang, W., Vavricka, C. J., Shi, Y., Wei, J., Feng, E., Shen, J., Chen, J., Liu, D., He, J., Yan, J., Liu, H., Jiang, H., Teng, M., Li, X., and Gao, G. F. (2010) The 2009 pandemic H1N1 neuraminidase N1 lacks the 150-cavity in its active site. Nat. Struct. Mol. Biol. 17, 1266-1268
7. Liu, D., Liu, X., Yan, J., Liu, W. J., and Gao, G. F. (2009) Interspecies transmission and host restriction of avian H5N1 influenza virus. Sci. China C Life Sci. 52, 428-438
8. Whittaker, G. R. (2001) Intracellular trafficking of influenza virus: clinical implications for molecular medicine. Expert Rev. Mol. Med. 3, 1-13
9. Brass, A. L., Huang, I. C., Benita, Y., John, S. P., Krishnan, M. N., Feeley, E. M., Ryan, B. J., Weyer, J. L., van der Weyden, L., and Fikrig, E. (2009) The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139, 1243-1254
10. Barman, S., Adhikary, L., Chakrabarti, A. K., Bernas, C., Kawaoka, Y., and Nayak, D. P. (2004) Role of transmembrane domain and cytoplasmic tail amino acid sequences of influenza a virus neuraminidase in raft association and virus budding. J. Virol. 78, 5258-5269 (Pubitemid 38581477)
11. Chen, B. J., Leser, G. P., Morita, E., and Lamb, R. A. (2007) Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J. Virol. 81, 7111-7123 (Pubitemid 46986647)
12. Nayak, D. P., Balogun, R. A., Yamada, H., Zhou, Z. H., and Barman, S. (2009) Influenza virus morphogenesis and budding. Virus Res. 143, 147-161
13. Barman, S., and Nayak, D. P. (2000) Analysis of the transmembrane domain of influenza virus neuraminidase, a type II transmembrane glycoprotein, for apical sorting and raft association. J. Virol. 74, 6538-6545 (Pubitemid 30429822)
14. Cerione, R. A. (2004) Cdc42. New roads to travel. Trends Cell Biol 14, 127-132
15. Harris, K. P., and Tepass, U. (2010) Cdc42 and vesicle trafficking in polarized cells. Traffic 11, 1272-1279
16. Melendez, J., Grogg, M., and Zheng, Y. (2011) Signaling role of Cdc42 in regulating mammalian physiology. J. Biol. Chem. 286, 2375-2381
17. Calvo, F., Sanz-Moreno, V., Agudo-Ibáñez, L., Wallberg, F., Sahai, E., Marshall, C. J., and Crespo, P. (2011) RasGRF suppresses Cdc42-mediated tumorcell movement, cytoskeletal dynamics and transformation. Nat. Cell Biol. 13, 819-826
18. Stamnes, M. (2002) Regulating the actin cytoskeleton during vesicular transport. Curr. Opin. Cell Biol. 14, 428-433
19. Fucini, R. V., Chen, J. L., Sharma, C., Kessels, M. M., and Stamnes, M. (2002) Golgi vesicle proteins are linked to the assembly of an actin complex defined by mAbp1. Mol. Biol. Cell 13, 621-631 (Pubitemid 34165088)
20. Chen, J. L., Lacomis, L., Erdjument-Bromage, H., Tempst, P., and Stamnes, M. (2004) Cytosol-derived proteins are sufficient for Arp2/3 recruitment and ARF/coatomer-dependent actin polymerization on Golgi membranes. FEBS Lett. 566, 281-286 (Pubitemid 38625972)
21. Balklava, Z., Pant, S., Fares, H., and Grant, B. D. (2007) Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9, 1066-1073 (Pubitemid 47338145)
22. Luna, A., Matas, O. B., Martínez-Menárguez, J. A., Mato, E., Durán, J. M., Ballesta, J., Way, M., and Egea, G. (2002) Regulation of protein transport from the Golgi complex to the endoplasmic reticulum by CDC42 and N-WASP. Mol. Biol. Cell 13, 866-879 (Pubitemid 34250352)
23. Etienne-Manneville, S., and Hall, A. (2002) Rho GTPases in cell biology. Nature 420, 629-635 (Pubitemid 36764489)
24. Sabharanjak, S., Sharma, P., Parton, R. G., and Mayor, S. (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2, 411-423 (Pubitemid 34436571)
25. Malyukova, I., Murray, K. F., Zhu, C., Boedeker, E., Kane, A., Patterson, K., Peterson, J. R., Donowitz, M., and Kovbasnjuk, O. (2009) Macropinocytosis in Shiga toxin 1 uptake by human intestinal epithelial cells and transcellular transcytosis. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G78-G92
26. Hall, A. (2005) Rho GTPases and the control of cell behavior. Biochem. Soc. Trans. 33, 891-895
27. Osmani, N., Peglion, F., Chavrier, P., and Etienne-Manneville, S. (2010) Cdc42 localization and cell polarity depend on membrane traffic. J. Cell Biol. 191, 1261-1269
28. Slaughter, B. D., Das, A., Schwartz, J. W., Rubinstein, B., and Li, R. (2009) Dual modes of cdc42 recycling fine-tune polarized morphogenesis. Dev. Cell 17, 823-835
29. Chen, J. L., Fucini, R. V., Lacomis, L., Erdjument-Bromage, H., Tempst, P., and Stamnes, M. (2005) Coatomer-bound Cdc42 regulates dynein recruitment to COPI vesicles. J. Cell Biol. 169, 383-389 (Pubitemid 40686688)
30. Hehnly, H., Longhini, K. M., Chen, J. L., and Stamnes, M. (2009) Retrograde Shiga toxin trafficking is regulated by ARHGAP21 and Cdc42. Mol. Biol. Cell 20, 4303-4312
31. Hehnly, H., Xu, W., Chen, J. L., and Stamnes, M. (2010) Cdc42 regulates microtubule-dependent Golgi positioning. Traffic 11, 1067-1078
32. Wu, W. J., Erickson, J. W., Lin, R., and Cerione, R. A. (2000) The γ-subunit of the coatomer complex binds Cdc42 to mediate transformation. Nature 405, 800-804 (Pubitemid 30407853)
33. Matas, O. B., Fritz, S., Luna, A., and Egea, G. (2005) Membrane trafficking at the ER/Golgi interface. Functional implications of RhoA and Rac1. Eur. J. Cell Biol. 84, 699-707 (Pubitemid 41149293)
34. Guo, G., Qiu, X., Wang, S., Chen, Y., Rothman, P. B., Wang, Z., Chen, Y., Wang, G., and Chen, J. L. (2010) Oncogenic E17K mutation in the pleckstrin homology domain of AKT1 promotes v-Abl-mediated pre-B-cell transformation and survival of Pim-deficient cells. Oncogene 29, 3845-3853
35. Li, Z., Nie, F., Wang, S., and Li, L. (2011) Histone H4 Lys-20 monomethylation by histone methylase SET8 mediates Wnt target gene activation. Proc. Natl. Acad. Sci. U.S.A. 108, 3116-3123
36. Bloom, J. D., Gong, L. I., and Baltimore, D. (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328, 1272-1275
37. Liu, S., Li, R., Zhang, R., Chan, C. C., Xi, B., Zhu, Z., Yang, J., Poon, V. K., Zhou, J., and Chen, M. (2011) CL-385319 inhibits H5N1 avian influenza A virus infection by blocking viral entry. Eur. J. Pharmacol. 660, 460-467
38. + exchanger 3 (NHE3) activity by increasing its exocytosis by an NHE3 kinase A regulatory protein-dependent mechanism. J. Biol. Chem. 278, 16494-16501
39. Collins, P. J., Haire, L. F., Lin, Y. P., Liu, J., Russell, R. J., Walker, P. A., Skehel, J. J., Martin, S. R., Hay, A. J., and Gamblin, S. J. (2008) Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 453, 1258-1261 (Pubitemid 351913590)
40. Aktories, K., and Just, I. (1995) Monoglucosylation of low molecular mass GTP-binding Rho proteins by clostridial cytotoxins. Trends Cell Biol. 5, 441-443
41. Wilkins, T. D., and Lyerly, D. M. (1996) Clostridium difficile toxins attack Rho. Trends Microbiol. 4, 49-51 (Pubitemid 26077279)
42. Aktories, K., Schmidt, G., and Just, I. (2000) Rho GTPases as targets of bacterial protein toxins. Biol. Chem. 381, 421-426 (Pubitemid 30453818)
43. Aktories, K., and Just, I. (1995) In vitro ADP-ribosylation of Rho by bacterial ADP-ribosyltransferases. Methods Enzymol. 256, 184-195
44. Ridley, A. J. (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16, 522-529
45. Dubois, T., Paléotti, O., Mironov, A. A., Fraisier, V., Stradal, T. E., De Matteis, M. A., Franco, M., and Chavrier, P. (2005) Golgi-localized GAP for Cdc42 functions downstream of ARF1 to control Arp2/3 complex and F-actin dynamics. Nat. Cell Biol. 7, 353-364 (Pubitemid 40533124)
46. Ménétrey, J., Perderiset, M., Cicolari, J., Dubois, T., Elkhatib, N., El Khadali, F., Franco, M., Chavrier, P., and Houdusse, A. (2007) Structural basis for ARF1-mediated recruitment of ARHGAP21 to Golgi membranes. EMBO J. 26, 1953-1962 (Pubitemid 46624047)
47. Kumari, S., and Mayor, S. (2008) ARF1 is directly involved in dynaminin-dependent endocytosis. Nat. Cell Biol. 10, 30-41
48. Valderrama, F., Luna, A., Babía, T., Martinez-Menárguez, J. A., Ballesta, J., Barth, H., Chaponnier, C., Renau-Piqueras, J., and Egea, G. (2000) The golgi-associated COPI-coated buds and vesicles contain β/γ-actin. Proc. Natl. Acad. Sci. U.S.A. 97, 1560-1565 (Pubitemid 30118481)