Enhanced enteroviral infectivity via viral proteasemediated cleavage of Grb2-associated binder 1

FASEB Journal

Volumn 29, Issue 11, 2015, Pages 4523-4531

  Deng, Haoyu ^a   Fung, Gabriel ^a   Shi, Junyan ^a   Xu, Suowen ^b   Wang, Chen ^a   Yin, Meimei ^b   Hou, Jun ^a   Zhang, Jingchun ^a   Jin, Zheng Gen ^b   Luo, Honglin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Coxsackievirus B3; ERK1 2; Signal transduction; Viral protease 2apro

Indexed keywords

CASPASE; DOCKING PROTEIN; GRB2 ASSOCIATED BINDER 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEINASE; UNCLASSIFIED DRUG; GAB1 PROTEIN, HUMAN; MAPK1 PROTEIN, HUMAN; PEPTIDE HYDROLASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VIRAL PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; COXSACKIEVIRUS B3; ENTEROVIRUS INFECTION; ENZYME ACTIVATION; GENETIC CODE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIROGENESIS; VIRUS REPLICATION; COXSACKIE VIRUS INFECTION; ENTEROVIRUS B; GENETICS; HELA CELL LINE; METABOLISM; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CASPASES; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; ENZYME ACTIVATION; HELA CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PEPTIDE HYDROLASES; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84948844487     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-274829     Document Type: Article

References (32)

1. Esfandiarei, M., and McManus, B. M. (2008)Molecular biology and pathogenesis of viral myocarditis. Annu. Rev. Pathol. 3, 127-155.
2. Jensen, K. J., Garmaroudi, F. S., Zhang, J., Lin, J., Boroomand, S., Zhang, M., Luo, Z., Yang, D., Luo, H., McManus, B. M., and Janes, K. A. (2013)An ERK-p38 subnetwork coordinates host cell apoptosis and necrosis during coxsackievirus B3 infection. Cell Host Microbe 13, 67-76.
3. Luo, H., Wong, J., and Wong, B. (2010) Protein degradation systems in viral myocarditis leading to dilated cardiomyopathy. Cardiovasc. Res. 85, 347-356.
4. Marchant, D., Si, X., Luo, H., McManus, B., and Yang, D. (2008) The impact of CVB3 infection on host cell biology. Curr. Top. Microbiol. Immunol. 323, 177-198.
5. Luo, H., Yanagawa, B., Zhang, J., Luo, Z., Zhang, M., Esfandiarei, M., Carthy, C., Wilson, J. E., Yang, D., and McManus, B. M. (2002) Coxsackievirus B3 replication is reduced by inhibition of the extracellular signal-regulated kinase (ERK) signaling pathway. J. Virol. 76, 3365-3373.
6. Wang, W., Xu, S., Yin, M., and Jin, Z. G. (2015) Essential roles ofGab1 tyrosine phosphorylation in growth factor-mediated signaling and angiogenesis. Int. J. Cardiol. 181, 180-184.
7. Wohrle, F. U., Daly, R. J., and Brummer, T. (2009) Function, regulation and pathological roles of theGab/DOS docking proteins. Cell Commun. Signal. 7, 22.
8. Itoh, M., Yoshida, Y., Nishida, K., Narimatsu, M., Hibi, M., and Hirano, T. (2000) Role of Gab1 in heart, placenta, and skin development and growth factor- And cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol. Cell. Biol. 20, 3695-3704.
9. Nakaoka, Y., and Komuro, I. (2013) Gab docking proteins in cardiovascular disease, cancer, and inflammation. Int. J. Inflamm. 2013, 141068.
10. Nishida, K., and Hirano, T. (2003)The role ofGab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci. 94, 1029-1033.
11. Maroun, C. R., Holgado-Madruga, M., Royal, I., Naujokas, M. A., Fournier, T. M., Wong, A. J., and Park, M. (1999) The Gab1 PH domain is required for localization ofGab1 at sites of cell-cell contact and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol. Cell. Biol. 19, 1784-1799.
12. Weidner, K.M., Di Cesare, S., Sachs, M., Brinkmann, V., Behrens, J., and Birchmeier, W. (1996) Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelialmorphogenesis. Nature 384, 173-176.
13. Gu, H., and Neel, B. G. (2003) The "Gab" in signal transduction. Trends Cell Biol. 13, 122-130.
14. Liu, Y., and Rohrschneider, L. R. (2002) The gift of Gab. FEBS Lett. 515, 1-7.
15. Wong, J., Si, X., Angeles, A., Zhang, J., Shi, J., Fung, G., Jagdeo, J., Wang, T., Zhong, Z., Jan, E., and Luo, H. (2013) Cytoplasmic redistribution and cleavage of AUF1 during coxsackievirus infection enhance the stability of its viral genome. FASEB J. 27, 2777-2787.
16. Yuan, J., Zhang, J., Wong, B.W., Si, X., Wong, J., Yang, D., andLuo, H. (2005) Inhibition of glycogen synthase kinase 3beta suppresses coxsackievirus-induced cytopathic effect and apoptosis via stabilization of beta-catenin. Cell Death Differ. 12, 1097-1106.
17. Krebs, J. F., Armstrong, R. C., Srinivasan, A., Aja, T., Wong, A. M., Aboy, A., Sayers, R., Pham, B., Vu, T., Hoang, K., Karanewsky, D. S., Leist, C., Schmitz, A., Wu, J.C., Tomaselli, K. J., and Fritz, L.C. (1999) Activation of membrane-associated procaspase-3 is regulated by Bcl-2. J. Cell Biol. 144, 915-926.
18. Wong, J., Zhang, J., Yanagawa, B., Luo, Z., Yang, X., Chang, J., McManus, B., and Luo, H. (2012) Cleavage of serumresponse factor mediated by enteroviral protease 2A contributes to impaired cardiac function. Cell Res. 22, 360-371.
19. Shi, J., Fung, G., Piesik, P., Zhang, J., and Luo, H. (2014) Dominantnegative functionof theC-terminal fragments ofNBR1 andSQSTM1 generated during enteroviral infection. Cell Death Differ. 21, 1432-1441.
20. Shi, J., Wong, J., Piesik, P., Fung, G., Zhang, J., Jagdeo, J., Li, X., Jan, E., and Luo, H. (2013) Cleavage of sequestosome 1/p62 by an enteroviral protease results in disrupted selective autophagy and impaired NFKB signaling. Autophagy 9, 1591-1603.
21. Fung, G., Ng, C. S., Zhang, J., Shi, J., Wong, J., Piesik, P., Han, L., Chu, F., Jagdeo, J., Jan, E., Fujita, T., and Luo, H. (2013) Production of a dominant-negative fragment due toG3BP1 cleavage contributes to the disruption ofmitochondria-associated protective stress granules during CVB3 infection. PLoS One 8, e79546.
22. Eulenfeld, R., and Schaper, F. (2009) A new mechanism for the regulation of Gab1 recruitment to the plasma membrane. J. Cell Sci. 122, 55-64.
23. Knowlton, K. U. (2008) CVB infection and mechanisms of viral cardiomyopathy. Curr. Top. Microbiol. Immunol. 323, 315-335.
24. Lim, B. K., Peter, A. K., Xiong, D., Narezkina, A., Yung, A., Dalton, N.D., Hwang, K. K., Yajima, T., Chen, J., andKnowlton, K.U. (2013) Inhibition ofCoxsackievirus-associated dystrophin cleavage prevents cardiomyopathy. J. Clin. Invest. 123, 5146-5151.
25. Lamphear, B. J., Yan, R., Yang, F., Waters, D., Liebig, H. D., Klump, H., Kuechler, E., Skern, T., and Rhoads, R. E. (1993) Mapping the cleavage site in protein synthesis initiation factor eIF-4 gamma of the 2A proteases from human Coxsackievirus and rhinovirus. J. Biol. Chem. 268, 19200-19203.
26. Kerekatte, V., Keiper, B. D., Badorff, C., Cai, A., Knowlton, K.U., and Rhoads, R. E. (1999) Cleavage of Poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: Another mechanism for host protein synthesis shutoff? J. Virol. 73, 709-717.
27. Feng, Q., Langereis, M. A., Lork, M., Nguyen, M., Hato, S. V., Lanke, K., Emdad, L., Bhoopathi, P., Fisher, P. B., Lloyd, R. E., and van Kuppeveld, F. J. (2014) Enterovirus 2Apro targets MDA5 and MAVS in infected cells. J. Virol. 88, 3369-3378.
28. Wang, J. P., Cerny, A., Asher, D. R., Kurt-Jones, E. A., Bronson, R. T., and Finberg, R. W. (2010) MDA5 and MAVS mediate type I interferon responses to coxsackie B virus. J. Virol. 84, 254-260.
29. Jones, N., and Dumont, D. J. (1999) Recruitment of Dok-R to the EGF receptor through its PTB domain is required for attenuation of Erk MAP kinase activation. Curr. Biol. 9, 1057-1060.
30. Schroder, W. A., Buck, M., Cloonan, N., Hancock, J. F., Suhrbier, A., Sculley, T., andBushell, G. (2007)HumanSin1 containsRas-binding andpleckstrinhomologydomains and suppressesRas signalling. Cell. Signal. 19, 1279-1289.
31. Cunnick, J. M., Dorsey, J. F., Munoz-Antonia, T., Mei, L., and Wu, J. (2000) Requirement of SHP2 binding to Grb2-associated binder-1 for mitogen-activated protein kinase activation in response to lysophosphatidic acid and epidermal growth factor. J. Biol. Chem. 275, 13842-13848.
32. Kim, S.O., Loesch, K., Wang, X., Jiang, J., Mei, L., Cunnick, J.M., Wu, J., and Frank, S. J. (2002) A role for Grb2-associated binder-1 in growth hormone signaling. Endocrinology 143, 4856-4867.