Polypyrimidine Tract-Binding Protein Regulates Enterovirus 71 Translation Through Interaction with the Internal Ribosomal Entry Site
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摘要
Enterovirus 71(EV71), a major causative agent of hand, foot, and mouth disease, has caused periodic infection outbreaks in children in the Asia–Pacific region. In order to describe the largely unknown life cycle of EV71, the molecular basis of its virus-host interactions must first be determined. The 50 untranslated region of EV71 contains a cloverleaf-like structure and internal ribosomal entry site(IRES), which play an important role in transcription and translation of viral protein. We found that polypyrimidine tract-binding protein 1(PTB) bound to the IRES of EV71. RNA recognition motifs 1 and 2 of PTB were responsible for its binding to the EV71 IRES. Moreover, PTB protein was shuttled from nucleus to cytoplasm after EV71 infection. Additionally, IRES activity and viral protein production were inhibited by PTB knockdown. These results suggest that PTB interacts with the EV71 IRES, and positively regulates viral protein translation.
Enterovirus 71(EV71), a major causative agent of hand, foot, and mouth disease, has caused periodic infection outbreaks in children in the Asia–Pacific region. In order to describe the largely unknown life cycle of EV71, the molecular basis of its virus-host interactions must first be determined. The 50 untranslated region of EV71 contains a cloverleaf-like structure and internal ribosomal entry site(IRES), which play an important role in transcription and translation of viral protein. We found that polypyrimidine tract-binding protein 1(PTB) bound to the IRES of EV71. RNA recognition motifs 1 and 2 of PTB were responsible for its binding to the EV71 IRES. Moreover, PTB protein was shuttled from nucleus to cytoplasm after EV71 infection. Additionally, IRES activity and viral protein production were inhibited by PTB knockdown. These results suggest that PTB interacts with the EV71 IRES, and positively regulates viral protein translation.
Enterovirus 71(EV71), a major causative agent of hand, foot, and mouth disease, has caused periodic infection outbreaks in children in the Asia–Pacific region. In order to describe the largely unknown life cycle of EV71, the molecular basis of its virus-host interactions must first be determined. The 50 untranslated region of EV71 contains a cloverleaf-like structure and internal ribosomal entry site(IRES), which play an important role in transcription and translation of viral protein. We found that polypyrimidine tract-binding protein 1(PTB) bound to the IRES of EV71. RNA recognition motifs 1 and 2 of PTB were responsible for its binding to the EV71 IRES. Moreover, PTB protein was shuttled from nucleus to cytoplasm after EV71 infection. Additionally, IRES activity and viral protein production were inhibited by PTB knockdown. These results suggest that PTB interacts with the EV71 IRES, and positively regulates viral protein translation.
引文
Agis-Juarez RA,Galvan I,Medina F,Daikoku T,Padmanabhan R,Ludert JE,del Angel RM(2009)Polypyrimidine tract-binding protein is relocated to the cytoplasm and is required during dengue virus infection in Vero cells.J Gen Virol 90:2893-2901
Auweter SD,Allain FH(2008)Structure-function relationships of the polypyrimidine tract binding protein.Cell Mol Life Sci65:516-527
Bellaousov S,Reuter JS,Seetin MG,Mathews DH(2013)RNAstructure:Web servers for RNA secondary structure prediction and analysis.Nucleic Acids Res 41:W471-W474
Black DL(2003)Mechanisms of alternative pre-messenger RNAsplicing.Annu Rev Biochem 72:291-336
Clery A,Blatter M,Allain FH(2008)RNA recognition motifs:boring?Not quite.Curr Opin Struct Biol 18:290-298
Deng JX,Nie XJ,Lei YF,Ma CF,Xu DL,Li B,Xu ZK,Zhang GC(2012)The highly conserved 50untranslated region as an effective target towards the inhibition of Enterovirus 71 replication by unmodified and appropriate 20-modified siRNAs.J Biomed Sci 19:73
Faye MD,Holcik M(2015)The role of IRES trans-acting factors in carcinogenesis.Biochim Biophys Acta 1849:887-897
Ghetti A,Pinol-Roma S,Michael WM,Morandi C,Dreyfuss G(1992)hnRNP 1,the polyprimidine tract-binding protein:distinct nuclear localization and association with hnRNAs.Nucleic Acids Res 20:3671-3678
Gosert R,Chang KH,Rijnbrand R,Yi M,Sangar DV,Lemon SM(2000)Transient expression of cellular polypyrimidine-tract binding protein stimulates cap-independent translation directed by both picornaviral and flaviviral internal ribosome entry sites in vivo.Mol Cell Biol 20:1583-1595
Hellen CU,Wimmer E(1995)Translation of encephalomyocarditis virus RNA by internal ribosomal entry.Curr Top Microbiol Immunol 203:31-63
Hellen CU,Witherell GW,Schmid M,Shin SH,Pestova TV,Gil A,Wimmer E(1993)A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein.Proc Natl Acad Sci U S A 90:7642-7646
Hellen CU,Pestova TV,Litterst M,Wimmer E(1994)The cellular polypeptide p57(pyrimidine tract-binding protein)binds to multiple sites in the poliovirus 50nontranslated region.J Virol68:941-950
Holcik M,Sonenberg N(2005)Translational control in stress and apoptosis.Nat Rev Mol Cell Biol 6:318-327
Hsu NY,Ilnytska O,Belov G,Santiana M,Chen YH,Takvorian PM,Pau C,van der Schaar H,Kaushik-Basu N,Balla T,Cameron CE,Ehrenfeld E,van Kuppeveld FJ,Altan-Bonnet N(2010)Viral reorganization of the secretory pathway generates distinct organelles for RNA replication.Cell 141:799-811
Huang PN,Lin JY,Locker N,Kung YA,Hung CT,Huang HI,Li ML,Shih SR(2011)Far upstream element binding protein 1 binds the internal ribosomal entry site of enterovirus 71 and enhances viral translation and viral growth.Nucleic Acids Res 39:9633-9648
Hung CT,Kung YA,Li ML,Brewer G,Lee KM,Liu ST,Shih SR(2016)Additive promotion of viral internal ribosome entry sitemediated translation by far upstream element-binding protein 1and an enterovirus 71-induced cleavage product.PLoS Pathog12:e1005959
Jackson RJ,Hellen CU,Pestova TV(2010)The mechanism of eukaryotic translation initiation and principles of its regulation.Nat Rev Mol Cell Biol 11:113-127
Kafasla P,Morgner N,Robinson CV,Jackson RJ(2010)Polypyrimidine tract-binding protein stimulates the poliovirus IRES by modulating eIF4G binding.EMBO J 29:3710-3722
Kafasla P,Lin H,Curry S,Jackson RJ(2011)Activation of picornaviral IRESs by PTB shows differential dependence on each PTB RNA-binding domain.RNA 17:1120-1131
Knoch KP,Bergert H,Borgonovo B,Saeger HD,Altkruger A,Verkade P,Solimena M(2004)Polypyrimidine tract-binding protein promotes insulin secretory granule biogenesis.Nat Cell Biol 6:207-214
Li R,Liu L,Mo Z,Wang X,Xia J,Liang Z,Zhang Y,Li Y,Mao Q,Wang J,Jiang L,Dong C,Che Y,Huang T,Jiang Z,Xie Z,Wang L,Liao Y,Liang Y,Nong Y,Liu J,Zhao H,Na R,Guo L,Pu J,Yang E,Sun L,Cui P,Shi H,Wang J,Li Q(2014)An inactivated enterovirus 71 vaccine in healthy children.New Engl J Med 370:829-837
Lin JY,Li ML,Huang PN,Chien KY,Horng JT,Shih SR(2008)Heterogeneous nuclear ribonuclear protein K interacts with the enterovirus 71 50untranslated region and participates in virus replication.J Gen Virol 89:2540-2549
Lin JY,Li ML,Shih SR(2009a)Far upstream element binding protein 2 interacts with enterovirus 71 internal ribosomal entry site and negatively regulates viral translation.Nucleic Acids Res37:47-59
Lin JY,Shih SR,Pan M,Li C,Lue CF,Stollar V,Li ML(2009b)hnRNP A1 interacts with the 50untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication.J Virol 83:6106-6114
Lu H,Li W,Noble WS,Payan D,Anderson DC(2004)Riboproteomics of the hepatitis C virus internal ribosomal entry site.J Proteome Res 3:949-957
Luo Z,Dong X,Li Y,Zhang Q,Kim C,Song Y,Kang L,Liu Y,Wu K,Wu J(2014)PolyC-Binding protein 1 interacts with 50-untranslated region of enterovirus 71 RNA in membraneassociated complex to facilitate viral replication.PLoS ONE9:e87491
McMinn P,Stratov I,Nagarajan L,Davis S(2001)Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand,foot,and mouth disease in Western Australia.Clin Infect Dis 32:236-242
Niepmann M(1996)Porcine polypyrimidine tract-binding protein stimulates translation initiation at the internal ribosome entry site of foot-and-mouth-disease virus.FEBS Lett 388:39-42
Oberstrass FC,Auweter SD,Erat M,Hargous Y,Henning A,Wenter P,Reymond L,Amir-Ahmady B,Pitsch S,Black DL,Allain FH(2005)Structure of PTB bound to RNA:specific binding and implications for splicing regulation.Science 309:2054-2057
Ooi MH,Wong SC,Lewthwaite P,Cardosa MJ,Solomon T(2010)Clinical features,diagnosis,and management of enterovirus 71.Lancet Neurol 9:1097-1105
Qiu J(2008)Enterovirus 71 infection:a new threat to global public health?Lancet Neurol 7:868-869
Rojas-Eisenring IA,Cajero-Juarez M,del Angel RM(1995)Cell proteins bind to a linear polypyrimidine-rich sequence within the50-untranslated region of rhinovirus 14 RNA.J Virol69:6819-6824
Ryu WS,Kang B,Hong J,Hwang S,Kim A,Kim J,Cheon DS(2010)Enterovirus 71 infection with central nervous system involvement,South Korea.Emerg Infect Dis 16:1764-1766
Sawicka K,Bushell M,Spriggs KA,Willis AE(2008)Polypyrimidine-tract-binding protein:a multifunctional RNA-binding protein.Biochem Soc Trans 36:641-647
Schmid M,Wimmer E(1994)IRES-controlled protein synthesis and genome replication of poliovirus.Arch Virol Suppl 9:279-289
Shimizu H,Utama A,Yoshii K,Yoshida H,Yoneyama T,Sinniah M,Yusof MA,Okuno Y,Okabe N,Shih SR,Chen HY,Wang GR,Kao CL,Chang KS,Miyamura T,Hagiwara A(1999)Enterovirus 71 from fatal and nonfatal cases of hand,foot and mouth disease epidemics in Malaysia,Japan and Taiwan in1997-1998.Jpn J Infect Dis 52:12-15
Shingler KL,Yoder JL,Carnegie MS,Ashley RE,Makhov AM,Conway JF,Hafenstein S(2013)The enterovirus 71 A-particle forms a gateway to allow genome release:a cryoEM study of picornavirus uncoating.PLoS Pathog 9:e1003240
Singh S,Poh CL,Chow VT(2002)Complete sequence analyses of enterovirus 71 strains from fatal and non-fatal cases of the hand,foot and mouth disease outbreak in Singapore(2000).Microbiol Immunol 46:801-808
Spellman R,Rideau A,Matlin A,Gooding C,Robinson F,McGlincy N,Grellscheid SN,Southby J,Wollerton M,Smith CW(2005)Regulation of alternative splicing by PTB and associated factors.Biochem Soc Trans 33:457-460
Sweeney TR,Abaeva IS,Pestova TV,Hellen CU(2014)The mechanism of translation initiation on Type 1 picornavirus IRESs.EMBO J 33:76-92
Thompson SR,Sarnow P(2003)Enterovirus 71 contains a type IIRES element that functions when eukaryotic initiation factor eIF4G is cleaved.Virology 315:259-266
Tischendorf JJ,Beger C,Korf M,Manns MP,Kruger M(2004)Polypyrimidine tract-binding protein(PTB)inhibits Hepatitis Cvirus internal ribosome entry site(HCV IRES)-mediated translation,but does not affect HCV replication.Arch Virol149:1955-1970
Tolbert M,Morgan CE,Pollum M,Crespo-Herna′ndez CE,Li ML,Brewer G,Tolbert BS(2017)HnRNP A1 Alters the structure of a conserved enterovirus IRES domain to stimulate viral translation.J Mol Biol 29:2841-2858
Venkatramana M,Ray PS,Chadda A,Das S(2003)A 25 k Da cleavage product of polypyrimidine tract binding protein(PTB)present in mouse tissues prevents PTB binding to the 50untranslated region and inhibits translation of hepatitis A virus RNA.Virus Res 98:141-149
Wang J,Du J,Wu Z,Jin Q(2013)Quinacrine impairs enterovirus 71RNA replication by preventing binding of polypyrimidine-tract binding protein with internal ribosome entry sites.PLoS ONE8:e52954
Wei J,Ian EM,Gregory NF,Eileen S-CH,Gilbert JC(2000)Fibroblast growth factor receptor-1 alpha-exon exclusion and polypyrimidine tract-binding protein in glioblastoma multiforme tumors.Cancer Res 60:1221-1224
Witherell GW,Gil A,Wimmer E(1993)Interaction of polypyrimidine tract binding protein with the encephalomyocarditis virus m RNA internal ribosomal entry site.Biochemistry32:8268-8275
Xie J,Lee JA,Kress TL,Mowry KL,Black DL(2003)Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein.Proc Natl Acad Sci U S A 100:8776-8781
Zhu FC,Meng FY,Li JX,Li XL,Mao QY,Tao H,Zhang YT,Yao X,Chu K,Chen QH,Hu YM,Wu X,Liu P,Zhu LY,Gao F,Jin H,Chen YJ,Dong YY,Liang YC,Shi NM,Ge HM,Liu L,Chen SG,Ai X,Zhang ZY,Ji YG,Luo FJ,Chen XQ,Zhang Y,Zhu LW,Liang ZL,Shen XL(2013)Efficacy,safety,and immunology of an inactivated alum-adjuvant enterovirus 71 vaccine in children in China:a multicentre,randomised,double-blind,placebo-controlled,phase 3 trial.Lancet 381:2024-2032
Zhu F,Xu W,Xia J,Liang Z,Liu Y,Zhang X,Tan X,Wang L,Mao Q,Wu J,Hu Y,Ji T,Song L,Liang Q,Zhang B,Gao Q,Li J,Wang S,Hu Y,Gu S,Zhang J,Yao G,Gu J,Wang X,Zhou Y,Chen C,Zhang M,Cao M,Wang J,Wang H,Wang N(2014)Efficacy,safety,and immunogenicity of an enterovirus 71vaccine in China.New Engl J Med 370:818-828
Auweter SD,Allain FH(2008)Structure-function relationships of the polypyrimidine tract binding protein.Cell Mol Life Sci65:516-527
Bellaousov S,Reuter JS,Seetin MG,Mathews DH(2013)RNAstructure:Web servers for RNA secondary structure prediction and analysis.Nucleic Acids Res 41:W471-W474
Black DL(2003)Mechanisms of alternative pre-messenger RNAsplicing.Annu Rev Biochem 72:291-336
Clery A,Blatter M,Allain FH(2008)RNA recognition motifs:boring?Not quite.Curr Opin Struct Biol 18:290-298
Deng JX,Nie XJ,Lei YF,Ma CF,Xu DL,Li B,Xu ZK,Zhang GC(2012)The highly conserved 50untranslated region as an effective target towards the inhibition of Enterovirus 71 replication by unmodified and appropriate 20-modified siRNAs.J Biomed Sci 19:73
Faye MD,Holcik M(2015)The role of IRES trans-acting factors in carcinogenesis.Biochim Biophys Acta 1849:887-897
Ghetti A,Pinol-Roma S,Michael WM,Morandi C,Dreyfuss G(1992)hnRNP 1,the polyprimidine tract-binding protein:distinct nuclear localization and association with hnRNAs.Nucleic Acids Res 20:3671-3678
Gosert R,Chang KH,Rijnbrand R,Yi M,Sangar DV,Lemon SM(2000)Transient expression of cellular polypyrimidine-tract binding protein stimulates cap-independent translation directed by both picornaviral and flaviviral internal ribosome entry sites in vivo.Mol Cell Biol 20:1583-1595
Hellen CU,Wimmer E(1995)Translation of encephalomyocarditis virus RNA by internal ribosomal entry.Curr Top Microbiol Immunol 203:31-63
Hellen CU,Witherell GW,Schmid M,Shin SH,Pestova TV,Gil A,Wimmer E(1993)A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein.Proc Natl Acad Sci U S A 90:7642-7646
Hellen CU,Pestova TV,Litterst M,Wimmer E(1994)The cellular polypeptide p57(pyrimidine tract-binding protein)binds to multiple sites in the poliovirus 50nontranslated region.J Virol68:941-950
Holcik M,Sonenberg N(2005)Translational control in stress and apoptosis.Nat Rev Mol Cell Biol 6:318-327
Hsu NY,Ilnytska O,Belov G,Santiana M,Chen YH,Takvorian PM,Pau C,van der Schaar H,Kaushik-Basu N,Balla T,Cameron CE,Ehrenfeld E,van Kuppeveld FJ,Altan-Bonnet N(2010)Viral reorganization of the secretory pathway generates distinct organelles for RNA replication.Cell 141:799-811
Huang PN,Lin JY,Locker N,Kung YA,Hung CT,Huang HI,Li ML,Shih SR(2011)Far upstream element binding protein 1 binds the internal ribosomal entry site of enterovirus 71 and enhances viral translation and viral growth.Nucleic Acids Res 39:9633-9648
Hung CT,Kung YA,Li ML,Brewer G,Lee KM,Liu ST,Shih SR(2016)Additive promotion of viral internal ribosome entry sitemediated translation by far upstream element-binding protein 1and an enterovirus 71-induced cleavage product.PLoS Pathog12:e1005959
Jackson RJ,Hellen CU,Pestova TV(2010)The mechanism of eukaryotic translation initiation and principles of its regulation.Nat Rev Mol Cell Biol 11:113-127
Kafasla P,Morgner N,Robinson CV,Jackson RJ(2010)Polypyrimidine tract-binding protein stimulates the poliovirus IRES by modulating eIF4G binding.EMBO J 29:3710-3722
Kafasla P,Lin H,Curry S,Jackson RJ(2011)Activation of picornaviral IRESs by PTB shows differential dependence on each PTB RNA-binding domain.RNA 17:1120-1131
Knoch KP,Bergert H,Borgonovo B,Saeger HD,Altkruger A,Verkade P,Solimena M(2004)Polypyrimidine tract-binding protein promotes insulin secretory granule biogenesis.Nat Cell Biol 6:207-214
Li R,Liu L,Mo Z,Wang X,Xia J,Liang Z,Zhang Y,Li Y,Mao Q,Wang J,Jiang L,Dong C,Che Y,Huang T,Jiang Z,Xie Z,Wang L,Liao Y,Liang Y,Nong Y,Liu J,Zhao H,Na R,Guo L,Pu J,Yang E,Sun L,Cui P,Shi H,Wang J,Li Q(2014)An inactivated enterovirus 71 vaccine in healthy children.New Engl J Med 370:829-837
Lin JY,Li ML,Huang PN,Chien KY,Horng JT,Shih SR(2008)Heterogeneous nuclear ribonuclear protein K interacts with the enterovirus 71 50untranslated region and participates in virus replication.J Gen Virol 89:2540-2549
Lin JY,Li ML,Shih SR(2009a)Far upstream element binding protein 2 interacts with enterovirus 71 internal ribosomal entry site and negatively regulates viral translation.Nucleic Acids Res37:47-59
Lin JY,Shih SR,Pan M,Li C,Lue CF,Stollar V,Li ML(2009b)hnRNP A1 interacts with the 50untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication.J Virol 83:6106-6114
Lu H,Li W,Noble WS,Payan D,Anderson DC(2004)Riboproteomics of the hepatitis C virus internal ribosomal entry site.J Proteome Res 3:949-957
Luo Z,Dong X,Li Y,Zhang Q,Kim C,Song Y,Kang L,Liu Y,Wu K,Wu J(2014)PolyC-Binding protein 1 interacts with 50-untranslated region of enterovirus 71 RNA in membraneassociated complex to facilitate viral replication.PLoS ONE9:e87491
McMinn P,Stratov I,Nagarajan L,Davis S(2001)Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand,foot,and mouth disease in Western Australia.Clin Infect Dis 32:236-242
Niepmann M(1996)Porcine polypyrimidine tract-binding protein stimulates translation initiation at the internal ribosome entry site of foot-and-mouth-disease virus.FEBS Lett 388:39-42
Oberstrass FC,Auweter SD,Erat M,Hargous Y,Henning A,Wenter P,Reymond L,Amir-Ahmady B,Pitsch S,Black DL,Allain FH(2005)Structure of PTB bound to RNA:specific binding and implications for splicing regulation.Science 309:2054-2057
Ooi MH,Wong SC,Lewthwaite P,Cardosa MJ,Solomon T(2010)Clinical features,diagnosis,and management of enterovirus 71.Lancet Neurol 9:1097-1105
Qiu J(2008)Enterovirus 71 infection:a new threat to global public health?Lancet Neurol 7:868-869
Rojas-Eisenring IA,Cajero-Juarez M,del Angel RM(1995)Cell proteins bind to a linear polypyrimidine-rich sequence within the50-untranslated region of rhinovirus 14 RNA.J Virol69:6819-6824
Ryu WS,Kang B,Hong J,Hwang S,Kim A,Kim J,Cheon DS(2010)Enterovirus 71 infection with central nervous system involvement,South Korea.Emerg Infect Dis 16:1764-1766
Sawicka K,Bushell M,Spriggs KA,Willis AE(2008)Polypyrimidine-tract-binding protein:a multifunctional RNA-binding protein.Biochem Soc Trans 36:641-647
Schmid M,Wimmer E(1994)IRES-controlled protein synthesis and genome replication of poliovirus.Arch Virol Suppl 9:279-289
Shimizu H,Utama A,Yoshii K,Yoshida H,Yoneyama T,Sinniah M,Yusof MA,Okuno Y,Okabe N,Shih SR,Chen HY,Wang GR,Kao CL,Chang KS,Miyamura T,Hagiwara A(1999)Enterovirus 71 from fatal and nonfatal cases of hand,foot and mouth disease epidemics in Malaysia,Japan and Taiwan in1997-1998.Jpn J Infect Dis 52:12-15
Shingler KL,Yoder JL,Carnegie MS,Ashley RE,Makhov AM,Conway JF,Hafenstein S(2013)The enterovirus 71 A-particle forms a gateway to allow genome release:a cryoEM study of picornavirus uncoating.PLoS Pathog 9:e1003240
Singh S,Poh CL,Chow VT(2002)Complete sequence analyses of enterovirus 71 strains from fatal and non-fatal cases of the hand,foot and mouth disease outbreak in Singapore(2000).Microbiol Immunol 46:801-808
Spellman R,Rideau A,Matlin A,Gooding C,Robinson F,McGlincy N,Grellscheid SN,Southby J,Wollerton M,Smith CW(2005)Regulation of alternative splicing by PTB and associated factors.Biochem Soc Trans 33:457-460
Sweeney TR,Abaeva IS,Pestova TV,Hellen CU(2014)The mechanism of translation initiation on Type 1 picornavirus IRESs.EMBO J 33:76-92
Thompson SR,Sarnow P(2003)Enterovirus 71 contains a type IIRES element that functions when eukaryotic initiation factor eIF4G is cleaved.Virology 315:259-266
Tischendorf JJ,Beger C,Korf M,Manns MP,Kruger M(2004)Polypyrimidine tract-binding protein(PTB)inhibits Hepatitis Cvirus internal ribosome entry site(HCV IRES)-mediated translation,but does not affect HCV replication.Arch Virol149:1955-1970
Tolbert M,Morgan CE,Pollum M,Crespo-Herna′ndez CE,Li ML,Brewer G,Tolbert BS(2017)HnRNP A1 Alters the structure of a conserved enterovirus IRES domain to stimulate viral translation.J Mol Biol 29:2841-2858
Venkatramana M,Ray PS,Chadda A,Das S(2003)A 25 k Da cleavage product of polypyrimidine tract binding protein(PTB)present in mouse tissues prevents PTB binding to the 50untranslated region and inhibits translation of hepatitis A virus RNA.Virus Res 98:141-149
Wang J,Du J,Wu Z,Jin Q(2013)Quinacrine impairs enterovirus 71RNA replication by preventing binding of polypyrimidine-tract binding protein with internal ribosome entry sites.PLoS ONE8:e52954
Wei J,Ian EM,Gregory NF,Eileen S-CH,Gilbert JC(2000)Fibroblast growth factor receptor-1 alpha-exon exclusion and polypyrimidine tract-binding protein in glioblastoma multiforme tumors.Cancer Res 60:1221-1224
Witherell GW,Gil A,Wimmer E(1993)Interaction of polypyrimidine tract binding protein with the encephalomyocarditis virus m RNA internal ribosomal entry site.Biochemistry32:8268-8275
Xie J,Lee JA,Kress TL,Mowry KL,Black DL(2003)Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein.Proc Natl Acad Sci U S A 100:8776-8781
Zhu FC,Meng FY,Li JX,Li XL,Mao QY,Tao H,Zhang YT,Yao X,Chu K,Chen QH,Hu YM,Wu X,Liu P,Zhu LY,Gao F,Jin H,Chen YJ,Dong YY,Liang YC,Shi NM,Ge HM,Liu L,Chen SG,Ai X,Zhang ZY,Ji YG,Luo FJ,Chen XQ,Zhang Y,Zhu LW,Liang ZL,Shen XL(2013)Efficacy,safety,and immunology of an inactivated alum-adjuvant enterovirus 71 vaccine in children in China:a multicentre,randomised,double-blind,placebo-controlled,phase 3 trial.Lancet 381:2024-2032
Zhu F,Xu W,Xia J,Liang Z,Liu Y,Zhang X,Tan X,Wang L,Mao Q,Wu J,Hu Y,Ji T,Song L,Liang Q,Zhang B,Gao Q,Li J,Wang S,Hu Y,Gu S,Zhang J,Yao G,Gu J,Wang X,Zhou Y,Chen C,Zhang M,Cao M,Wang J,Wang H,Wang N(2014)Efficacy,safety,and immunogenicity of an enterovirus 71vaccine in China.New Engl J Med 370:818-828
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