Flu DRiPs in MHC Class Ⅰ Immunosurveillance
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摘要
Since the publication of the DRiP(defective ribosomal product) hypothesis in 1996, numerous studies have addressed the contribution of DRiPs to generating viral antigenic peptides for CD8~+T cell immunosurveillance. Here, we review studies characterizing the generation of antigenic peptides from influenza A virus encoded DRiPs, discuss the many remaining mysteries regarding the nature of their co-translational generation, and speculate on where the future might lead.
Since the publication of the DRiP(defective ribosomal product) hypothesis in 1996, numerous studies have addressed the contribution of DRiPs to generating viral antigenic peptides for CD8~+T cell immunosurveillance. Here, we review studies characterizing the generation of antigenic peptides from influenza A virus encoded DRiPs, discuss the many remaining mysteries regarding the nature of their co-translational generation, and speculate on where the future might lead.
Since the publication of the DRiP(defective ribosomal product) hypothesis in 1996, numerous studies have addressed the contribution of DRiPs to generating viral antigenic peptides for CD8~+T cell immunosurveillance. Here, we review studies characterizing the generation of antigenic peptides from influenza A virus encoded DRiPs, discuss the many remaining mysteries regarding the nature of their co-translational generation, and speculate on where the future might lead.
引文
Al-Jubran K,Wen J,Abdullahi A,Roy Chaudhury S,Li M,Ramanathan P,Matina A,De S,Piechocki K,Rugjee KN,Brogna S(2013)Visualization of the joining of ribosomal subunits reveals the presence of 80S ribosomes in the nucleus.RNA 19:1669-1683
Amorim MJ,Read EK,Dalton RM,Medcalf L,Digard P(2007)Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity.Traffic 8:1-11
Anton LC,Yewdell JW(2014)Translating DRiPs:MHC class Iimmunosurveillance of pathogens and tumors.J Leukoc Biol95:551-562
Apanius V,Penn D,Slev PR,Ruff LR,Potts WK(2017)The nature of selection on the major histocompatibility complex.Crit Rev Immunol 37:75-120
Apcher S,Millot G,Daskalogianni C,Scherl A,Manoury B,Fahraeus R(2013)Translation of pre-spliced RNAs in the nuclear compartment generates peptides for the MHC class I pathway.Proc Natl Acad Sci USA 110:17951-17956
Berglund P,Finzi D,Bennink JR,Yewdell JW(2007)Viral alteration of cellular translational machinery increases defective ribosomal products.J Virol 81:7220-7229
Berkers CR,de Jong A,Schuurman KG,Linnemann C,Meiring HD,Janssen L,Neefjes JJ,Schumacher TN,Rodenko B,Ovaa H(2015)Definition of proteasomal peptide splicing rules for highefficiency spliced peptide presentation by MHC class Imolecules.J Immunol 195:4085-4095
Bourdetsky D,Schmelzer CE,Admon A(2014)The nature and extent of contributions by defective ribosome products to the HLApeptidome.Proc Natl Acad Sci USA 111:E1591-1599
Bullock TN,Eisenlohr LC(1996)Ribosomal scanning past the primary initiation codon as a mechanism for expression of CTLepitopes encoded in alternative reading frames.J Exp Med184:1319-1329
Clarke SR,Barnden M,Kurts C,Carbone FR,Miller JF,Heath WR(2000)Characterization of the ovalbumin-specific TCR transgenic line OT-I:MHC elements for positive and negative selection.Immunol Cell Biol 78:110-117
Clifford M,Twigg J,Upton C(2009)Evidence for a novel gene associated with human influenza A viruses.Virol J 6:198
Croft NP,Smith SA,Wong YC,Tan CT,Dudek NL,Flesch IE,Lin LC,Tscharke DC,Purcell AW(2013)Kinetics of antigen expression and epitope presentation during virus infection.PLoSPathog 9:e1003129
Dahlberg J,Lund E(2012)Nuclear translation or nuclear peptidyl transferase?Nucleus 3:320-321
Dahlberg JE,Lund E,Goodwin EB(2003)Nuclear translation:what is the evidence?RNA 9:1-8
David A,Dolan BP,Hickman HD,Knowlton JJ,Clavarino G,Pierre P,Bennink JR,Yewdell JW(2012)Nuclear translation visualized by ribosome-bound nascent chain puromycylation.J Cell Biol 197:45-57
Dolan BP,Knowlton JJ,David A,Bennink JR,Yewdell JW(2010a)RNA polymerase II inhibitors dissociate antigenic peptide generation from normal viral protein synthesis:a role for nuclear translation in defective ribosomal product synthesis?J Immunol185:6728-6733
Dolan BP,Li L,Takeda K,Bennink JR,Yewdell JW(2010b)Defective ribosomal products are the major source of antigenic peptides endogenously generated from influenza A virus neuraminidase.J Immunol 184:1419-1424
Dolan BP,Sharma AA,Gibbs JS,Cunningham TJ,Bennink JR,Yewdell JW(2012)MHC class I antigen processing distinguishes endogenous antigens based on their translation from cellular versus viral m RNA.Proc Natl Acad Sci USA109:7025-7030
Elliott T,Bodmer H,Townsend A(1996)Recognition of out-of-frame major histocompatibility complex class I-restricted epitopes in vivo.Eur J Immunol 26:1175-1179
Esquivel F,Yewdell JW,Bennink JR(1992)RMA/S cells present endogenously synthesized cytosolic proteins to class I-restricted cytotoxic T lymphocytes.J Exp Med 175:163-168
Fetten JV,Roy N,Gilboa E(1991)A frameshift mutation at the NH2terminus of the nucleoprotein gene does not affect generation of cytotoxic T lymphocyte epitopes.J Immunol 147:2697-2705
Genuth NR,Barna M(2018)The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life.Mol Cell 71:364-374
Hanada K,Yewdell JW,Yang JC(2004)Immune recognition of a human renal cancer antigen through post-translational protein splicing.Nature 427:252-256
Hickman HD,Mays JW,Gibbs J,Kosik I,Magadan JG,Takeda K,Das S,Reynoso GV,Ngudiankama BF,Wei J,Shannon JP,McManus D,Yewdell JW(2018)Influenza A virus negative strand RNA is translated for CD8(?)T cell immunosurveillance.J Immunol.https://doi.org/10.4049/jimmunol.1800586
Iborra FJ,Jackson DA,Cook PR(2004)The case for nuclear translation 1.J Cell Sci 117:5713-5720
Ingolia NT,Lareau LF,Weissman JS(2011)Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes.Cell 147:789-802
Ingolia NT,Brar GA,Stern-Ginossar N,Harris MS,Talhouarne GJ,Jackson SE,Wills MR,Weissman JS(2014)Ribosome profiling reveals pervasive translation outside of annotated protein-coding genes.Cell Rep 8:1365-1379
Jenkins MR,Webby R,Doherty PC,Turner SJ(2006)Addition of a prominent epitope affects influenza A virus-specific CD8?T cell immunodominance hierarchies when antigen is limiting.J Immunol 177:2917-2925
Karttunen J,Sanderson S,Shastri N(1992)Detection of rare antigenpresenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens.Proc Natl Acad Sci USA 89:6020-6024
Kim TS,Sun J,Braciale TJ(2011)T cell responses during influenza infection:getting and keeping control.Trends Immunol32:225-231
Lev A,Princiotta MF,Zanker D,Takeda K,Gibbs JS,Kumagai C,Waffarn E,Dolan BP,Burgevin A,Van Endert P,Chen W,Bennink JR,Yewdell JW(2010)Compartmentalized MHC class I antigen processing enhances immunosurveillance by circumventing the law of mass action.Proc Natl Acad Sci USA107:6964-6969
Liepe J,Marino F,Sidney J,Jeko A,Bunting DE,Sette A,Kloetzel PM,Stumpf MPH,Heck AJR,Mishto M(2016)A large fraction of HLA class I ligands are proteasome-generated spliced peptides.Science 354:354-358
McAllister AK(2014)Major histocompatibility complex I in brain development and schizophrenia.Biol Psychiatry 75:262-268
McGlincy NJ,Ingolia NT(2017)Transcriptome-wide measurement of translation by ribosome profiling.Methods 126:112-129
McMichael AJ,Gotch FM,Noble GR,Beare PA(1983)Cytotoxic T-cell immunity to influenza.N Engl J Med 309:13-17
Porgador A,Yewdell JW,Deng Y,Bennink JR,Germain RN(1997)Localization,quantitation,and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody.Immunity 6:715-726
Princiotta MF,Finzi D,Qian SB,Gibbs J,Schuchmann S,Buttgereit F,Bennink JR,Yewdell JW(2003)Quantitating protein synthesis,degradation,and endogenous antigen processing.Immunity 18:343-354
Reid DW,Nicchitta CV(2012)The enduring enigma of nuclear translation.J Cell Biol 197:7-9
Schubert U,Anton LC,Gibbs J,Norbury CC,Yewdell JW,Bennink JR(2000)Rapid degradation of a large fraction of newly synthesized proteins by proteasomes.Nature 404:770-774
Schuren AB,Costa AI,Wiertz EJ(2016)Recent advances in viral evasion of the MHC Class I processing pathway.Curr Opin Immunol 40:43-50
Schwanha¨usser B,Busse D,Li N,Dittmar G,Schuchhardt J,Wolf J,Chen W,Selbach M(2011)Global quantification of mammalian gene expression control.Nature 473:337-342
Shi Z,Fujii K,Kovary KM,Genuth NR,Rost HL,Teruel MN,Barna M(2017)Heterogeneous ribosomes preferentially translate distinct subpools of mRNAs genome-wide.Mol Cell67(71-83):e77
Slavov N,Semrau S,Airoldi E,Budnik B,van Oudenaarden A(2015)Differential stoichiometry among core ribosomal proteins.Cell Rep 13:865-873
Souquette A,Thomas PG(2018)Past life and future effects-how heterologous infections alter immunity to influenza viruses.Front Immunol 9:1071
Starck SR,Jiang V,Pavon-Eternod M,Prasad S,McCarthy B,Pan T,Shastri N(2012)Leucine-tRNA initiates at CUG start codons for protein synthesis and presentation by MHC class I.Science336:1719-1723
Starck SR,Tsai JC,Chen K,Shodiya M,Wang L,Yahiro K,MartinsGreen M,Shastri N,Walter P(2016)Translation from the 5'untranslated region shapes the integrated stress response.Science 351:aad3867
Townsend ARM,Gotch FM,Davey J(1985)Cytotoxic T cells recognize fragments of the influenza nucleoprotein.Cell42:457-467
Townsend ARM,Bastin J,Gould K,Brownlee GG(1986)Cytotoxic T lymphocytes recognize influenza hemagglutinin that lacks a signal sequence.Nature 324:575-577
Vigneron N,Stroobant V,Chapiro J,Ooms A,Degiovanni G,Morel S,van der Bruggen P,Boon T,Van den Eynde BJ(2004)An antigenic peptide produced by peptide splicing in the proteasome.Science 304:587-590
Wang F,Durfee Larissa A,Huibregtse Jon M(2013)A cotranslational ubiquitination pathway for quality control of misfolded proteins.Mol Cell 50:378-389
Warren EH,Vigneron NJ,Gavin MA,Coulie PG,Stroobant V,Dalet A,Tykodi SS,Xuereb SM,Mito JK,Riddell SR,Van den Eynde BJ(2006)An antigen produced by splicing of noncontiguous peptides in the reverse order.Science 313:1444-1447
Webby RJ,Andreansky S,Stambas J,Rehg JE,Webster RG,Doherty PC,Turner SJ(2003)Protection and compensation in the influenza virus-specific CD8?T cell response.Proc Natl Acad Sci USA 100:7235-7240
Wei J,Yewdell JW(2018)Immunoribosomes:Where's there's fire,there's fire.Mol Immunol.https://doi.org/10.1016/j.molimm.2017.12.026
Wheatley DN,Giddings MR,Inglis MS(1980)Kinetics of degradation of‘‘short-''and‘‘long-lived''proteins in cultured mammalian cells.Cell Biol Int Rep 4:1081-1090
Wu T(2017)Antigen presentation during influenza virus infection.Dissertation,Monash University
Yang N,Gibbs JS,Hickman HD,Reynoso GV,Ghosh AK,Bennink JR,Yewdell JW(2016)Defining viral defective ribosomal products:standard and alternative translation initiation events generate a common peptide from Influenza A virus M2 and M1mRNAs.J Immunol 196:3608-3617
Yewdell JW(2001)Not such a dismal science:the economics of protein synthesis,folding,degradation and antigen processing.Trends Cell Biol 11:294-297
Yewdell JW(2003)Immunology.Hide and seek in the peptidome.Science 301:1334-1335
Yewdell JW(2011)DRiPs solidify:progress in understanding endogenous MHC class I antigen processing.Trends Immunol32:548-558
Yewdell JW,Nicchitta CV(2006)The DRiP hypothesis decennial:support,controversy,refinement and extension.Trends Immunol27:368-373
Yewdell JW,Anton LC,Bennink JR(1996)Defective ribosomal products(DRiPs):a major source of antigenic peptides for MHCclass I molecules?J Immunol 157:1823-1826
Zanker D,Waithman J,Yewdell JW,Chen W(2013)Mixed proteasomes function to increase viral peptide diversity and broaden antiviral CD8?T cell responses.J Immunol 191:52-59
Zhirnov OP,Poyarkov SV,Vorob'eva IV,Safonova OA,Malyshev NA,Klenk HD(2007)Segment NS of influenza a virus contains an additional gene NSP in positive-sense orientation.Doklady Biochem Biophys 414:127-133
Zinkernagel RM,Doherty PC(1974)Restriction of in vitro T cellmediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system.Nature 248:701-702
Zook MB,Howard MT,Sinnathamby G,Atkins JF,Eisenlohr LC(2006)Epitopes derived by incidental translational frame shifting give rise to a protective CTL response.J Immunol176:6928-6934
Amorim MJ,Read EK,Dalton RM,Medcalf L,Digard P(2007)Nuclear export of influenza A virus mRNAs requires ongoing RNA polymerase II activity.Traffic 8:1-11
Anton LC,Yewdell JW(2014)Translating DRiPs:MHC class Iimmunosurveillance of pathogens and tumors.J Leukoc Biol95:551-562
Apanius V,Penn D,Slev PR,Ruff LR,Potts WK(2017)The nature of selection on the major histocompatibility complex.Crit Rev Immunol 37:75-120
Apcher S,Millot G,Daskalogianni C,Scherl A,Manoury B,Fahraeus R(2013)Translation of pre-spliced RNAs in the nuclear compartment generates peptides for the MHC class I pathway.Proc Natl Acad Sci USA 110:17951-17956
Berglund P,Finzi D,Bennink JR,Yewdell JW(2007)Viral alteration of cellular translational machinery increases defective ribosomal products.J Virol 81:7220-7229
Berkers CR,de Jong A,Schuurman KG,Linnemann C,Meiring HD,Janssen L,Neefjes JJ,Schumacher TN,Rodenko B,Ovaa H(2015)Definition of proteasomal peptide splicing rules for highefficiency spliced peptide presentation by MHC class Imolecules.J Immunol 195:4085-4095
Bourdetsky D,Schmelzer CE,Admon A(2014)The nature and extent of contributions by defective ribosome products to the HLApeptidome.Proc Natl Acad Sci USA 111:E1591-1599
Bullock TN,Eisenlohr LC(1996)Ribosomal scanning past the primary initiation codon as a mechanism for expression of CTLepitopes encoded in alternative reading frames.J Exp Med184:1319-1329
Clarke SR,Barnden M,Kurts C,Carbone FR,Miller JF,Heath WR(2000)Characterization of the ovalbumin-specific TCR transgenic line OT-I:MHC elements for positive and negative selection.Immunol Cell Biol 78:110-117
Clifford M,Twigg J,Upton C(2009)Evidence for a novel gene associated with human influenza A viruses.Virol J 6:198
Croft NP,Smith SA,Wong YC,Tan CT,Dudek NL,Flesch IE,Lin LC,Tscharke DC,Purcell AW(2013)Kinetics of antigen expression and epitope presentation during virus infection.PLoSPathog 9:e1003129
Dahlberg J,Lund E(2012)Nuclear translation or nuclear peptidyl transferase?Nucleus 3:320-321
Dahlberg JE,Lund E,Goodwin EB(2003)Nuclear translation:what is the evidence?RNA 9:1-8
David A,Dolan BP,Hickman HD,Knowlton JJ,Clavarino G,Pierre P,Bennink JR,Yewdell JW(2012)Nuclear translation visualized by ribosome-bound nascent chain puromycylation.J Cell Biol 197:45-57
Dolan BP,Knowlton JJ,David A,Bennink JR,Yewdell JW(2010a)RNA polymerase II inhibitors dissociate antigenic peptide generation from normal viral protein synthesis:a role for nuclear translation in defective ribosomal product synthesis?J Immunol185:6728-6733
Dolan BP,Li L,Takeda K,Bennink JR,Yewdell JW(2010b)Defective ribosomal products are the major source of antigenic peptides endogenously generated from influenza A virus neuraminidase.J Immunol 184:1419-1424
Dolan BP,Sharma AA,Gibbs JS,Cunningham TJ,Bennink JR,Yewdell JW(2012)MHC class I antigen processing distinguishes endogenous antigens based on their translation from cellular versus viral m RNA.Proc Natl Acad Sci USA109:7025-7030
Elliott T,Bodmer H,Townsend A(1996)Recognition of out-of-frame major histocompatibility complex class I-restricted epitopes in vivo.Eur J Immunol 26:1175-1179
Esquivel F,Yewdell JW,Bennink JR(1992)RMA/S cells present endogenously synthesized cytosolic proteins to class I-restricted cytotoxic T lymphocytes.J Exp Med 175:163-168
Fetten JV,Roy N,Gilboa E(1991)A frameshift mutation at the NH2terminus of the nucleoprotein gene does not affect generation of cytotoxic T lymphocyte epitopes.J Immunol 147:2697-2705
Genuth NR,Barna M(2018)The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life.Mol Cell 71:364-374
Hanada K,Yewdell JW,Yang JC(2004)Immune recognition of a human renal cancer antigen through post-translational protein splicing.Nature 427:252-256
Hickman HD,Mays JW,Gibbs J,Kosik I,Magadan JG,Takeda K,Das S,Reynoso GV,Ngudiankama BF,Wei J,Shannon JP,McManus D,Yewdell JW(2018)Influenza A virus negative strand RNA is translated for CD8(?)T cell immunosurveillance.J Immunol.https://doi.org/10.4049/jimmunol.1800586
Iborra FJ,Jackson DA,Cook PR(2004)The case for nuclear translation 1.J Cell Sci 117:5713-5720
Ingolia NT,Lareau LF,Weissman JS(2011)Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes.Cell 147:789-802
Ingolia NT,Brar GA,Stern-Ginossar N,Harris MS,Talhouarne GJ,Jackson SE,Wills MR,Weissman JS(2014)Ribosome profiling reveals pervasive translation outside of annotated protein-coding genes.Cell Rep 8:1365-1379
Jenkins MR,Webby R,Doherty PC,Turner SJ(2006)Addition of a prominent epitope affects influenza A virus-specific CD8?T cell immunodominance hierarchies when antigen is limiting.J Immunol 177:2917-2925
Karttunen J,Sanderson S,Shastri N(1992)Detection of rare antigenpresenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens.Proc Natl Acad Sci USA 89:6020-6024
Kim TS,Sun J,Braciale TJ(2011)T cell responses during influenza infection:getting and keeping control.Trends Immunol32:225-231
Lev A,Princiotta MF,Zanker D,Takeda K,Gibbs JS,Kumagai C,Waffarn E,Dolan BP,Burgevin A,Van Endert P,Chen W,Bennink JR,Yewdell JW(2010)Compartmentalized MHC class I antigen processing enhances immunosurveillance by circumventing the law of mass action.Proc Natl Acad Sci USA107:6964-6969
Liepe J,Marino F,Sidney J,Jeko A,Bunting DE,Sette A,Kloetzel PM,Stumpf MPH,Heck AJR,Mishto M(2016)A large fraction of HLA class I ligands are proteasome-generated spliced peptides.Science 354:354-358
McAllister AK(2014)Major histocompatibility complex I in brain development and schizophrenia.Biol Psychiatry 75:262-268
McGlincy NJ,Ingolia NT(2017)Transcriptome-wide measurement of translation by ribosome profiling.Methods 126:112-129
McMichael AJ,Gotch FM,Noble GR,Beare PA(1983)Cytotoxic T-cell immunity to influenza.N Engl J Med 309:13-17
Porgador A,Yewdell JW,Deng Y,Bennink JR,Germain RN(1997)Localization,quantitation,and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody.Immunity 6:715-726
Princiotta MF,Finzi D,Qian SB,Gibbs J,Schuchmann S,Buttgereit F,Bennink JR,Yewdell JW(2003)Quantitating protein synthesis,degradation,and endogenous antigen processing.Immunity 18:343-354
Reid DW,Nicchitta CV(2012)The enduring enigma of nuclear translation.J Cell Biol 197:7-9
Schubert U,Anton LC,Gibbs J,Norbury CC,Yewdell JW,Bennink JR(2000)Rapid degradation of a large fraction of newly synthesized proteins by proteasomes.Nature 404:770-774
Schuren AB,Costa AI,Wiertz EJ(2016)Recent advances in viral evasion of the MHC Class I processing pathway.Curr Opin Immunol 40:43-50
Schwanha¨usser B,Busse D,Li N,Dittmar G,Schuchhardt J,Wolf J,Chen W,Selbach M(2011)Global quantification of mammalian gene expression control.Nature 473:337-342
Shi Z,Fujii K,Kovary KM,Genuth NR,Rost HL,Teruel MN,Barna M(2017)Heterogeneous ribosomes preferentially translate distinct subpools of mRNAs genome-wide.Mol Cell67(71-83):e77
Slavov N,Semrau S,Airoldi E,Budnik B,van Oudenaarden A(2015)Differential stoichiometry among core ribosomal proteins.Cell Rep 13:865-873
Souquette A,Thomas PG(2018)Past life and future effects-how heterologous infections alter immunity to influenza viruses.Front Immunol 9:1071
Starck SR,Jiang V,Pavon-Eternod M,Prasad S,McCarthy B,Pan T,Shastri N(2012)Leucine-tRNA initiates at CUG start codons for protein synthesis and presentation by MHC class I.Science336:1719-1723
Starck SR,Tsai JC,Chen K,Shodiya M,Wang L,Yahiro K,MartinsGreen M,Shastri N,Walter P(2016)Translation from the 5'untranslated region shapes the integrated stress response.Science 351:aad3867
Townsend ARM,Gotch FM,Davey J(1985)Cytotoxic T cells recognize fragments of the influenza nucleoprotein.Cell42:457-467
Townsend ARM,Bastin J,Gould K,Brownlee GG(1986)Cytotoxic T lymphocytes recognize influenza hemagglutinin that lacks a signal sequence.Nature 324:575-577
Vigneron N,Stroobant V,Chapiro J,Ooms A,Degiovanni G,Morel S,van der Bruggen P,Boon T,Van den Eynde BJ(2004)An antigenic peptide produced by peptide splicing in the proteasome.Science 304:587-590
Wang F,Durfee Larissa A,Huibregtse Jon M(2013)A cotranslational ubiquitination pathway for quality control of misfolded proteins.Mol Cell 50:378-389
Warren EH,Vigneron NJ,Gavin MA,Coulie PG,Stroobant V,Dalet A,Tykodi SS,Xuereb SM,Mito JK,Riddell SR,Van den Eynde BJ(2006)An antigen produced by splicing of noncontiguous peptides in the reverse order.Science 313:1444-1447
Webby RJ,Andreansky S,Stambas J,Rehg JE,Webster RG,Doherty PC,Turner SJ(2003)Protection and compensation in the influenza virus-specific CD8?T cell response.Proc Natl Acad Sci USA 100:7235-7240
Wei J,Yewdell JW(2018)Immunoribosomes:Where's there's fire,there's fire.Mol Immunol.https://doi.org/10.1016/j.molimm.2017.12.026
Wheatley DN,Giddings MR,Inglis MS(1980)Kinetics of degradation of‘‘short-''and‘‘long-lived''proteins in cultured mammalian cells.Cell Biol Int Rep 4:1081-1090
Wu T(2017)Antigen presentation during influenza virus infection.Dissertation,Monash University
Yang N,Gibbs JS,Hickman HD,Reynoso GV,Ghosh AK,Bennink JR,Yewdell JW(2016)Defining viral defective ribosomal products:standard and alternative translation initiation events generate a common peptide from Influenza A virus M2 and M1mRNAs.J Immunol 196:3608-3617
Yewdell JW(2001)Not such a dismal science:the economics of protein synthesis,folding,degradation and antigen processing.Trends Cell Biol 11:294-297
Yewdell JW(2003)Immunology.Hide and seek in the peptidome.Science 301:1334-1335
Yewdell JW(2011)DRiPs solidify:progress in understanding endogenous MHC class I antigen processing.Trends Immunol32:548-558
Yewdell JW,Nicchitta CV(2006)The DRiP hypothesis decennial:support,controversy,refinement and extension.Trends Immunol27:368-373
Yewdell JW,Anton LC,Bennink JR(1996)Defective ribosomal products(DRiPs):a major source of antigenic peptides for MHCclass I molecules?J Immunol 157:1823-1826
Zanker D,Waithman J,Yewdell JW,Chen W(2013)Mixed proteasomes function to increase viral peptide diversity and broaden antiviral CD8?T cell responses.J Immunol 191:52-59
Zhirnov OP,Poyarkov SV,Vorob'eva IV,Safonova OA,Malyshev NA,Klenk HD(2007)Segment NS of influenza a virus contains an additional gene NSP in positive-sense orientation.Doklady Biochem Biophys 414:127-133
Zinkernagel RM,Doherty PC(1974)Restriction of in vitro T cellmediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system.Nature 248:701-702
Zook MB,Howard MT,Sinnathamby G,Atkins JF,Eisenlohr LC(2006)Epitopes derived by incidental translational frame shifting give rise to a protective CTL response.J Immunol176:6928-6934