Productive Entry of Foot-and-Mouth Disease Virus via Macropinocytosis Independent of Phosphatidylinositol 3-Kinase

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Han, Shi Chong ^a   Guo, Hui Chen ^a   Sun, Shi Qi ^a   Jin, Ye ^a   Wei, Yan Quan ^a   Feng, Xia ^a   Yao, Xue Ping ^b   Cao, Sui Zhong ^b   Xiang Liu, Ding ^a,c   Liu, Xiang Tao ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b SICHUAN AGRICULTURAL UNIVERSITY   (China)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CAVEOLIN; CHOLESTEROL; MEMBRANE LIPID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE;

ANIMAL; CELL LINE; FOOT AND MOUTH DISEASE VIRUS; METABOLISM; PHYSIOLOGY; PINOCYTOSIS; VIRUS ENTRY; VIRUS REPLICATION;

ACTINS; ANIMALS; CAVEOLINS; CELL LINE; CHOLESTEROL; FOOT-AND-MOUTH DISEASE VIRUS; MEMBRANE LIPIDS; PHOSPHATIDYLINOSITOL 3-KINASES; PINOCYTOSIS; RECEPTOR PROTEIN-TYROSINE KINASES; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84955285305     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19294     Document Type: Article

References (71)

1. Domingo, E., Baranowski, E., Escarmis, C. & Sobrino, F. Foot-and-mouth disease virus. Comparative immunology, microbiology and infectious diseases 25, 297-308 (2002)
2. Mason, P. W., Grubman, M. J. & Baxt, B. Molecular basis of pathogenesis of FMDV. Virus Res 91, 9-32 (2003)
3. Grubman, M. J. & Baxt, B. Foot-and-mouth disease. Clinical microbiology reviews 17, 465-493 (2004)
4. Jamal, S. M. & Belsham, G. J. Foot-and-mouth disease: past, present and future. Veterinary research 44, 116 (2013)
5. Nicola, A. V., Aguilar, H. C., Mercer, J., Ryckman, B. & Wiethoff, C. M. Virus entry by endocytosis. Advances in virology 2013, 469-538 (2013)
6. Yamauchi, Y. & Helenius, A. Virus entry at a glance. Journal of cell science 126, 1289-1295 (2013)
7. Doherty, G. J. & McMahon, H. T. Mechanisms of endocytosis. Annual review of biochemistry 78, 857-902 (2009)
8. Mercer, J., Schelhaas, M. & Helenius, A. Virus entry by endocytosis. Annual review of biochemistry 79, 803-833 (2010)
9. Helenius, A., Kartenbeck, J., Simons, K. & Fries, E. On the entry of Semliki forest virus into BHK-21 cells. The Journal of cell biology 84, 404-420 (1980)
10. Cureton, D. K., Massol, R. H., Saffarian, S., Kirchhausen, T. L. & Whelan, S. P. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS pathogens 5, e1000394 (2009)
11. Pelkmans, L., Kartenbeck, J. & Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nature cell biology 3, 473-483 (2001)
12. Engel, S. et al. Role of endosomes in simian virus 40 entry and infection. J Virol 85, 4198-4211 (2011)
13. Mercer, J. & Helenius, A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320, 531-535 (2008)
14. Kerr, M. C. & Teasdale, R. D. Defining macropinocytosis. Traffic 10, 364-371 (2009)
15. Mercer, J. & Helenius, A. Virus entry by macropinocytosis. Nature cell biology 11, 510-520 (2009)
16. Mercer, J. & Helenius, A. Gulping rather than sipping: macropinocytosis as a way of virus entry. Current opinion in microbiology 15, 490-499 (2012)
17. Kalin, S. et al. Macropinocytotic uptake and infection of human epithelial cells with species B2 adenovirus type 35. J Virol 84, 5336-5350 (2010)
18. Mercer, J. et al. Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proceedings of the National Academy of Sciences of the United States of America 107, 9346-9351 (2010)
19. Nanbo, A. et al. Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoprotein-dependent manner. PLoS pathogens 6, e1001121 (2010)
20. Saeed, M. F., Kolokoltsov, A. A., Albrecht, T. & Davey, R. A. Cellular entry of ebola virus involves uptake by a macropinocytosis-like mechanism and subsequent trafficking through early and late endosomes. PLoS pathogens 6, e1001110 (2010)
21. de Vries, E. et al. Dissection of the influenza A virus endocytic routes reveals macropinocytosis as an alternative entry pathway. PLoS pathogens 7, e1001329 (2011)
22. Rossman, J. S., Leser, G. P. & Lamb, R. A. Filamentous influenza virus enters cells via macropinocytosis. J Virol 86, 10950-10960 (2012)
23. Krieger, S. E., Kim, C., Zhang, L., Marjomaki, V. & Bergelson, J. M. Echovirus 1 entry into polarized Caco-2 cells depends on dynamin, cholesterol, and cellular factors associated with macropinocytosis. J Virol 87, 8884-8895 (2013)
24. Coyne, C. B., Shen, L., Turner, J. R. & Bergelson, J. M. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell host & microbe 2, 181-192 (2007)
25. Khan, A. G. et al. Human rhinovirus 14 enters rhabdomyosarcoma cells expressing icam-1 by a clathrin-, caveolin-, and flotillinindependent pathway. J Virol 84, 3984-3992 (2010)
26. Khan, A. G. et al. Entry of a heparan sulphate-binding HRV8 variant strictly depends on dynamin but not on clathrin, caveolin, and flotillin. Virology 412, 55-67 (2011)
27. Neff, S. et al. Foot-and-mouth disease virus virulent for cattle utilizes the integrin alpha(v)beta3 as its receptor. J Virol 72, 3587-3594 (1998)
28. Jackson, T., Sheppard, D., Denyer, M., Blakemore, W. & King, A. M. The epithelial integrin alphavbeta6 is a receptor for foot-andmouth disease virus. J Virol 74, 4949-4956 (2000)
29. Jackson, T., Mould, A. P., Sheppard, D. & King, A. M. Integrin alphavbeta1 is a receptor for foot-and-mouth disease virus. J Virol 76, 935-941 (2002)
30. Jackson, T. et al. Integrin alphavbeta8 functions as a receptor for foot-and-mouth disease virus: role of the beta-chain cytodomain in integrin-mediated infection. J Virol 78, 4533-4540 (2004)
31. ODonnell, V., Larocco, M. & Baxt, B. Heparan sulfate-binding foot-and-mouth disease virus enters cells via caveola-mediated endocytosis. J Virol 82, 9075-9085 (2008)
32. Berryman, S. et al. Positively charged residues at the five-fold symmetry axis of cell culture-adapted foot-and-mouth disease virus permit novel receptor interactions. J Virol 87, 8735-8744 (2013)
33. Wang, L. H., Rothberg, K. G. & Anderson, R. G. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. The Journal of cell biology 123, 1107-1117 (1993)
34. Fujinaga, Y. et al. Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulm. Molecular biology of the cell 14, 4783-4793 (2003)
35. Pietiainen, V. et al. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Molecular biology of the cell 15, 4911-4925 (2004)
36. Anderson, H. A., Chen, Y. & Norkin, L. C. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Molecular biology of the cell 7, 1825-1834 (1996)
37. Martin-Acebes, M. A., Gonzalez-Magaldi, M., Sandvig, K., Sobrino, F. & Armas-Portela, R. Productive entry of type C foot-andmouth disease virus into susceptible cultured cells requires clathrin and is dependent on the presence of plasma membrane cholesterol. Virology 369, 105-118 (2007)
38. Bubb, M. R., Spector, I., Beyer, B. B. & Fosen, K. M. Effects of jasplakinolide on the kinetics of actin polymerization. An explanation for certain in vivo observations. The Journal of biological chemistry 275, 5163-5170 (2000)
39. Koivusalo, M. et al. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. The Journal of cell biology 188, 547-563 (2010)
40. Norbury, C. C. Drinking a lot is good for dendritic cells. Immunology 117, 443-451 (2006)
41. Sanchez, E. G. et al. African swine fever virus uses macropinocytosis to enter host cells. PLoS pathogens 8, e1002754 (2012)
42. Krzyzaniak, M. A., Zumstein, M. T., Gerez, J. A., Picotti, P. & Helenius, A. Host cell entry of respiratory syncytial virus involves macropinocytosis followed by proteolytic activation of the F protein. PLoS pathogens 9, e1003309 (2013)
43. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. & Hall, A. The small GTP-binding protein rac regulates growth factorinduced membrane ruffling. Cell 70, 401-410 (1992)
44. Burridge, K. & Wennerberg, K. Rho and Rac take center stage. Cell 116, 167-179 (2004)
45. Schlunck, G. et al. Modulation of Rac localization and function by dynamin. Molecular biology of the cell 15, 256-267 (2004)
46. Macia, E. et al. Dynasore, a cell-permeable inhibitor of dynamin. Developmental cell 10, 839-850 (2006)
47. Dharmawardhane, S. et al. Regulation of macropinocytosis by p21-activated kinase-1. Molecular biology of the cell 11, 3341-3352 (2000)
48. Liberali, P. et al. The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. The EMBO journal 27, 970-981 (2008)
49. Zenke, F. T., King, C. C., Bohl, B. P. & Bokoch, G. M. Identification of a central phosphorylation site in p21-activated kinase regulating autoinhibition and kinase activity. The Journal of biological chemistry 274, 32565-32573 (1999)
50. Deacon, S. W. et al. An isoform-selective, small-molecule inhibitor targets the autoregulatory mechanism of p21-activated kinase. Chemistry & biology 15, 322-331 (2008)
51. Amyere, M. et al. Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C. Molecular biology of the cell 11, 3453-3467 (2000)
52. Araki, N., Hatae, T., Furukawa, A. & Swanson, J. A. Phosphoinositide-3-kinase-independent contractile activities associated with Fcgamma-receptor-mediated phagocytosis and macropinocytosis in macrophages. Journal of cell science 116, 247-257 (2003)
53. Even-Faitelson, L., Rosenberg, M. & Ravid, S. PAK1 regulates myosin II-B phosphorylation, filament assembly, localization and cell chemotaxis. Cellular signalling 17, 1137-1148 (2005)
54. Berryman, S., Clark, S., Monaghan, P. & Jackson, T. Early events in integrin alphavbeta6-mediated cell entry of foot-and-mouth disease virus. J Virol 79, 8519-8534 (2005)
55. ODonnell, V., LaRocco, M., Duque, H. & Baxt, B. Analysis of foot-and-mouth disease virus internalization events in cultured cells. J Virol 79, 8506-8518 (2005)
56. Johns, H. L., Berryman, S., Monaghan, P., Belsham, G. J. & Jackson, T. A dominant-negative mutant of rab5 inhibits infection of cells by foot-and-mouth disease virus: implications for virus entry. J Virol 83, 6247-6256 (2009)
57. Racoosin, E. L. & Swanson, J. A. Macropinosome maturation and fusion with tubular lysosomes in macrophages. The Journal of cell biology 121, 1011-1020 (1993)
58. Rupper, A., Lee, K., Knecht, D. & Cardelli, J. Sequential activities of phosphoinositide 3-kinase, PKB/Aakt, and Rab7 during macropinosome formation in Dictyostelium. Molecular biology of the cell 12, 2813-2824 (2001)
59. Baranowski, E. et al. Cell recognition by foot-and-mouth disease virus that lacks the RGD integrin-binding motif: flexibility in aphthovirus receptor usage. J Virol 74, 1641-1647 (2000)
60. Zhao, Q., Pacheco, J. M. & Mason, P. W. Evaluation of genetically engineered derivatives of a Chinese strain of foot-and-mouth disease virus reveals a novel cell-binding site which functions in cell culture and in animals. J Virol 77, 3269-3280 (2003)
61. Karjalainen, M. et al. A Raft-derived, Pak1-regulated entry participates in alpha2beta1 integrin-dependent sorting to caveosomes. Molecular biology of the cell 19, 2857-2869 (2008)
62. Huttunen, M., Waris, M., Kajander, R., Hyypia, T. & Marjomaki, V. Coxsackievirus A9 infects cells via nonacidic multivesicular bodies. J Virol 88, 5138-5151 (2014)
63. Praefcke, G. J. & McMahon, H. T. The dynamin superfamily: universal membrane tubulation and fission molecules ? Nature reviews. Molecular cell biology 5, 133-147 (2004)
64. Grimmer, S., van Deurs, B. & Sandvig, K. Membrane ruffling and macropinocytosis in A431 cells require cholesterol. Journal of cell science 115, 2953-2962 (2002)
65. Urs, N. M. et al. A requirement for membrane cholesterol in the beta-arrestin- and clathrin-dependent endocytosis of LPA1 lysophosphatidic acid receptors. Journal of cell science 118, 5291-5304 (2005)
66. Eierhoff, T., Hrincius, E. R., Rescher, U., Ludwig, S. & Ehrhardt, C. The epidermal growth factor receptor (EGFR) promotes uptake of influenza A viruses (IAV) into host cells. PLoS pathogens 6, e1001099 (2010)
67. Berryman, S. et al. Foot-and-mouth disease virus induces autophagosomes during cell entry via a class III phosphatidylinositol 3-kinase-independent pathway. J Virol 86, 12940-12953 (2012)
68. Martin-Acebes, M. A., Gonzalez-Magaldi, M., Vazquez-Calvo, A., Armas-Portela, R. & Sobrino, F. Internalization of swine vesicular disease virus into cultured cells: a comparative study with foot-and-mouth disease virus. J Virol 83, 4216-4226 (2009)
69. Gladue, D. P. et al. Foot-and-mouth disease virus nonstructural protein 2C interacts with Beclin1, modulating virus replication. J Virol 86, 12080-12090 (2012)
70. Curry, S. et al. Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J Virol 69, 430-438 (1995)
71. Curry, S. et al. Crystallization and preliminary X-ray analysis of three serotypes of foot-and-mouth disease virus. Journal of molecular biology 228, 1263-1268 (1992)