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Molecular and Cellular Biology Volume 20, 2000 - Issue 13
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Gene Expression

Upf1p Control of Nonsense mRNA Translation Is Regulated by Nmd2p and Upf3p

Alan B. MaderazoDepartment of Molecular Genetics and Microbiology, University of Massachusetts Medical School, Worcester, Massachusetts01655-0122
,
Feng HeDepartment of Molecular Genetics and Microbiology, University of Massachusetts Medical School, Worcester, Massachusetts01655-0122
,
David A. MangusDepartment of Molecular Genetics and Microbiology, University of Massachusetts Medical School, Worcester, Massachusetts01655-0122
&
Allan JacobsonDepartment of Molecular Genetics and Microbiology, University of Massachusetts Medical School, Worcester, Massachusetts01655-0122Correspondence[email protected]
Pages 4591-4603 | Received 20 Oct 1999, Accepted 04 Apr 2000, Published online: 28 Mar 2023

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Feng He, Robin Ganesan & Allan Jacobson. (2013) Intra- and Intermolecular Regulatory Interactions in Upf1, the RNA Helicase Central to Nonsense-Mediated mRNA Decay in Yeast. Molecular and Cellular Biology 33:23, pages 4672-4684.
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Kim M. Keeling, Joe Salas-Marco, Lev Z. Osherovich & David M. Bedwell. (2006) Tpa1p Is Part of an mRNP Complex That Influences Translation Termination, mRNA Deadenylation, and mRNA Turnover in Saccharomyces cerevisiae. Molecular and Cellular Biology 26:14, pages 5237-5248.
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Alan B. Maderazo, Jonathan P. Belk, Feng He & Allan Jacobson. (2003) Nonsense-Containing mRNAs That Accumulate in the Absence of a Functional Nonsense-Mediated mRNA Decay Pathway Are Destabilized Rapidly upon Its Restitution. Molecular and Cellular Biology 23:3, pages 842-851.
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Bertrand Cosson, Anne Couturier, Svetlana Chabelskaya, Denis Kiktev, Sergey Inge-Vechtomov, Michel Philippe & Galina Zhouravleva. (2002) Poly(A)-Binding Protein Acts in Translation Termination via Eukaryotic Release Factor 3 Interaction and Does Not Influence [PSI+] Propagation. Molecular and Cellular Biology 22:10, pages 3301-3315.
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Andrew T. Bond, David A. Mangus, Feng He & Allan Jacobson. (2001) Absence of Dbp2p Alters Both Nonsense-Mediated mRNA Decay and rRNA Processing. Molecular and Cellular Biology 21:21, pages 7366-7379.
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Feng He & Allan Jacobson. (2001) Upf1p, Nmd2p, and Upf3p Regulate the Decapping and Exonucleolytic Degradation of both Nonsense-Containing mRNAs and Wild-Type mRNAs. Molecular and Cellular Biology 21:5, pages 1515-1530.
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Joshua T. Mendell, Susan M. Medghalchi, Ross G. Lake, Erick N. Noensie & Harry C. Dietz. (2000) Novel Upf2p Orthologues Suggest a Functional Link between Translation Initiation and Nonsense Surveillance Complexes. Molecular and Cellular Biology 20:23, pages 8944-8957.
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Articles from other publishers (74)

Caleb M. Embree, Rabab Abu-Alhasan & Guramrit Singh. (2022) Features and factors that dictate if terminating ribosomes cause or counteract nonsense-mediated mRNA decay. Journal of Biological Chemistry 298:11, pages 102592.
Crossref
Feng He & Allan Jacobson. (2022) Eukaryotic mRNA decapping factors: molecular mechanisms and activity . The FEBS Journal.
Crossref
Sze Jing Tang, Haoqing Shen, Omer An, HuiQi Hong, Jia Li, Yangyang Song, Jian Han, Daryl Jin Tai Tay, Vanessa Hui En Ng, Fernando Bellido Molias, Ka Wai Leong, Priyankaa Pitcheshwar, Henry Yang & Leilei Chen. (2020) Cis- and trans-regulations of pre-mRNA splicing by RNA editing enzymes influence cancer development. Nature Communications 11:1.
Crossref
Tatsuaki Kurosaki, Maximilian W. Popp & Lynne E. Maquat. (2019) Quality and quantity control of gene expression by nonsense-mediated mRNA decay. Nature Reviews Molecular Cell Biology 20:7, pages 406-420.
Crossref
Robin Ganesan, John Leszyk & Allan Jacobson. (2019) Selective profiling of ribosomes associated with yeast Upf proteins. Methods 155, pages 58-67.
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Roland Klassen & Raffael Schaffrath. (2018) Collaboration of tRNA modifications and elongation factor eEF1A in decoding and nonsense suppression. Scientific Reports 8:1.
Crossref
Saverio Brogna, Tina McLeod & Marija Petric. (2016) The Meaning of NMD: Translate or Perish. Trends in Genetics 32:7, pages 395-407.
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Emiliano Altamura, Monica Borgatti, Alessia Finotti, Jessica Gasparello, Roberto Gambari, Mariangela Spinelli, Rosa Castaldo & Nicola Altamura. (2016) Chemical-Induced Read-Through at Premature Termination Codons Determined by a Rapid Dual-Fluorescence System Based on S. cerevisiae. PLOS ONE 11:4, pages e0154260.
Crossref
Feng HeAllan Jacobson. (2015) Nonsense-Mediated mRNA Decay: Degradation of Defective Transcripts Is Only Part of the Story. Annual Review of Genetics 49:1, pages 339-366.
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Alper Celik, Stephanie Kervestin & Allan Jacobson. (2015) NMD: At the crossroads between translation termination and ribosome recycling. Biochimie 114, pages 2-9.
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S. P. Zadorsky, Y. V. Sopova, D. Y. Andreichuk, V. A. Startsev, V. P. Medvedeva & S. G. Inge-Vechtomov. (2015) Chromosome VIII disomy influences the nonsense suppression efficiency and transition metal tolerance of the yeast Saccharomyces cerevisiae . Yeast 32:6, pages 479-497.
Crossref
Bijoyita Roy, John D. Leszyk, David A. Mangus & Allan Jacobson. (2015) Nonsense suppression by near-cognate tRNAs employs alternative base pairing at codon positions 1 and 3. Proceedings of the National Academy of Sciences 112:10, pages 3038-3043.
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Lam Son Nguyen, Miles F. Wilkinson & Jozef Gecz. (2014) Nonsense-mediated mRNA decay: Inter-individual variability and human disease. Neuroscience & Biobehavioral Reviews 46, pages 175-186.
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Clarivel Lasalde, Andrea V. Rivera, Alfredo J. León, José A. González-Feliciano, Luis A. Estrella, Eva N. Rodríguez-Cruz, María E. Correa, Iván J. Cajigas, Dina P. Bracho, Irving E. Vega, Miles F. Wilkinson & Carlos I. González. (2014) Identification and functional analysis of novel phosphorylation sites in the RNA surveillance protein Upf1. Nucleic Acids Research 42:3, pages 1916-1929.
Crossref
Ei Ei Min, Bijoyita Roy, Nadia Amrani, Feng He & Allan Jacobson. (2013) Yeast Upf1 CH domain interacts with Rps26 of the 40S ribosomal subunit. RNA 19:8, pages 1105-1115.
Crossref
Lam S. Nguyen, Hyung-Goo Kim, Jill A. Rosenfeld, Yiping Shen, James F. Gusella, Yves Lacassie, Lawrence C. Layman, Lisa G. Shaffer & Jozef Gécz. (2013) Contribution of copy number variants involving nonsense-mediated mRNA decay pathway genes to neuro-developmental disorders. Human Molecular Genetics 22:9, pages 1816-1825.
Crossref
Stuart W. PeltzManal MorsyEllen M. WelchAllan Jacobson. (2013) Ataluren as an Agent for Therapeutic Nonsense Suppression. Annual Review of Medicine 64:1, pages 407-425.
Crossref
Stephanie Kvas, Gregory B Gloor & Christopher J Brandl. (2012) Loss of nonsense mediated decay suppresses mutations in Saccharomyces cerevisiae TRA1. BMC Genetics 13:1.
Crossref
Stephanie Kervestin & Allan Jacobson. (2012) NMD: a multifaceted response to premature translational termination. Nature Reviews Molecular Cell Biology 13:11, pages 700-712.
Crossref
Roy Parker. (2012) RNA Degradation in Saccharomyces cerevisae . Genetics 191:3, pages 671-702.
Crossref
Stephanie Kervestin, Chunfang Li, Richard Buckingham & Allan Jacobson. (2012) Testing the faux-UTR model for NMD: Analysis of Upf1p and Pab1p competition for binding to eRF3/Sup35p. Biochimie 94:7, pages 1560-1571.
Crossref
Bessie W. Kebaara, Kristian E. Baker, Krista D. Patefield & Audrey L. Atkin. (2012) Analysis of Nonsense‐Mediated mRNA Decay in Saccharomyces cerevisiae . Current Protocols in Cell Biology 54:1.
Crossref
Anton A. Nizhnikov, Zalina M. Magomedova, Alexandr A. Rubel, Alexandra M. Kondrashkina, Sergey G. Inge-Vechtomov & Alexey P. Galkin. (2012) [NSI +] determinant has a pleiotropic phenotypic manifestation that is modulated by SUP35, SUP45, and VTS1 genes. Current Genetics 58:1, pages 35-47.
Crossref
Rafael Deliz-Aguirre, Audrey L. Atkin & Bessie W. Kebaara. (2011) Copper tolerance of Saccharomyces cerevisiae nonsense-mediated mRNA decay mutants. Current Genetics 57:6, pages 421-430.
Crossref
Jungwook Hwang & Lynne E Maquat. (2011) Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. Current Opinion in Genetics & Development 21:4, pages 422-430.
Crossref
Sutapa Chakrabarti, Uma Jayachandran, Fabien Bonneau, Francesca Fiorini, Claire Basquin, Silvia Domcke, Hervé Le Hir & Elena Conti. (2011) Molecular Mechanisms for the RNA-Dependent ATPase Activity of Upf1 and Its Regulation by Upf2. Molecular Cell 41:6, pages 693-703.
Crossref
Shubhendu Ghosh, Robin Ganesan, Nadia Amrani & Allan Jacobson. (2010) Translational competence of ribosomes released from a premature termination codon is modulated by NMD factors. RNA 16:9, pages 1832-1847.
Crossref
Marcus J.O. Johansson & Allan Jacobson. (2010) Nonsense-mediated mRNA decay maintains translational fidelity by limiting magnesium uptake. Genes & Development 24:14, pages 1491-1495.
Crossref
Luis A. Estrella, Miles F. Wilkinson & Carlos I. González. (2009) The Shuttling Protein Npl3 Promotes Translation Termination Accuracy in Saccharomyces cerevisiae. Journal of Molecular Biology 394:3, pages 410-422.
Crossref
Bessie W. Kebaara & Audrey L. Atkin. (2009) Long 3′-UTRs target wild-type mRNAs for nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Nucleic Acids Research 37:9, pages 2771-2778.
Crossref
Yi-Hsiu Chen, Li-Hsin Su, Yu-Chang Huang, Yi-Ting Wang, Yu-Yun Kao & Chin-Hung Sun. (2008) UPF1, a Conserved Nonsense-Mediated mRNA Decay Factor, Regulates Cyst Wall Protein Transcripts in Giardia lamblia. PLoS ONE 3:10, pages e3609.
Crossref
Shinya Takahashi, Yasuhiro Araki, Yuriko Ohya, Takeshi Sakuno, Shin-Ichi Hoshino, Kenji Kontani, Hiroshi Nishina & Toshiaki Katada. (2008) Upf1 potentially serves as a RING-related E3 ubiquitin ligase via its association with Upf3 in yeast. RNA 14:9, pages 1950-1958.
Crossref
Feng He, Nadia Amrani, Marcus J.O. Johansson & Allan Jacobson. 2008. RNA Turnover in Eukaryotes: Analysis of Specialized and Quality Control RNA Decay Pathways. RNA Turnover in Eukaryotes: Analysis of Specialized and Quality Control RNA Decay Pathways 127 147 .
Gabriele Neu‐Yilik & Andreas E. Kulozik. 2008. 185 243 .
Yao-Fu ChangJ. Saadi ImamMiles F. Wilkinson. (2007) The Nonsense-Mediated Decay RNA Surveillance Pathway. Annual Review of Biochemistry 76:1, pages 51-74.
Crossref
Hiroyuki Kodama, Koichi Ito & Yoshikazu Nakamura. (2007) The role of N-terminal domain of translational release factor eRF3 for the control of functionality and stability in S. cerevisiae. Genes to Cells 12:5, pages 639-650.
Crossref
Ellen M. Welch, Elisabeth R. Barton, Jin Zhuo, Yuki Tomizawa, Westley J. Friesen, Panayiota Trifillis, Sergey Paushkin, Meenal Patel, Christopher R. Trotta, Seongwoo Hwang, Richard G. Wilde, Gary Karp, James Takasugi, Guangming Chen, Stephen Jones, Hongyu Ren, Young-Choon Moon, Donald Corson, Anthony A. Turpoff, Jeffrey A. Campbell, M. Morgan Conn, Atiyya Khan, Neil G. Almstead, Jean Hedrick, Anna Mollin, Nicole Risher, Marla Weetall, Shirley Yeh, Arthur A. Branstrom, Joseph M. Colacino, John Babiak, William D. Ju, Samit Hirawat, Valerie J. Northcutt, Langdon L. Miller, Phyllis Spatrick, Feng He, Masataka Kawana, Huisheng Feng, Allan Jacobson, Stuart W. Peltz & H. Lee Sweeney. (2007) PTC124 targets genetic disorders caused by nonsense mutations. Nature 447:7140, pages 87-91.
Crossref
Shuyun Dong, Chunfang Li, Daniel Zenklusen, Robert H. Singer, Allan Jacobson & Feng He. (2007) YRA1 Autoregulation Requires Nuclear Export and Cytoplasmic Edc3p-Mediated Degradation of Its Pre-mRNA. Molecular Cell 25:4, pages 559-573.
Crossref
Cheng Wu, Nadia Amrani, Allan Jacobson & Matthew S. Sachs. 2007. Translation Initiation: Extract Systems and Molecular Genetics. Translation Initiation: Extract Systems and Molecular Genetics 203 225 .
Julia Morales, Odile Mulner-Lorillon, Bertrand Cosson, Emmanuelle Morin, Robert Bellé, Cynthia A. Bradham, Wendy S. Beane & Patrick Cormier. (2006) Translational control genes in the sea urchin genome. Developmental Biology 300:1, pages 293-307.
Crossref
Nadia Amrani, Matthew S. Sachs & Allan Jacobson. (2006) Early nonsense: mRNA decay solves a translational problem. Nature Reviews Molecular Cell Biology 7:6, pages 415-425.
Crossref
Ujwal Sheth & Roy Parker. (2006) Targeting of Aberrant mRNAs to Cytoplasmic Processing Bodies. Cell 125:6, pages 1095-1109.
Crossref
Nicole K. Nesser, David O. Peterson & Diane K. Hawley. (2006) RNA polymerase II subunit Rpb9 is important for transcriptional fidelity in vivo . Proceedings of the National Academy of Sciences 103:9, pages 3268-3273.
Crossref
Amanda S. Ford, Qiaoning Guan, Eric Neeno-Eckwall & Michael R. Culbertson. (2006) Ebs1p, a Negative Regulator of Gene Expression Controlled by the Upf Proteins in the Yeast Saccharomyces cerevisiae . Eukaryotic Cell 5:2, pages 301-312.
Crossref
Rachel Taylor, Bessie Wanja Kebaara, Tara Nazarenus, Ashley Jones, Rena Yamanaka, Rachel Uhrenholdt, Jason P. Wendler & Audrey L. Atkin. (2005) Gene Set Coregulated by the Saccharomyces cerevisiae Nonsense-Mediated mRNA Decay Pathway . Eukaryotic Cell 4:12, pages 2066-2077.
Crossref
Anthony Gaba, Allan Jacobson & Matthew S. Sachs. (2005) Ribosome Occupancy of the Yeast CPA1 Upstream Open Reading Frame Termination Codon Modulates Nonsense-Mediated mRNA Decay. Molecular Cell 20:3, pages 449-460.
Crossref
MICHAEL R. CULBERTSON & ERIC NEENO-ECKWALL. (2005) Transcript selection and the recruitment of mRNA decay factors for NMD in Saccharomyces cerevisiae . RNA 11:9, pages 1333-1339.
Crossref
Marenda A. Wilson, Stacie Meaux, Roy Parker & Ambro van Hoof. (2005) Genetic interactions between [ PSI + ] and nonstop mRNA decay affect phenotypic variation . Proceedings of the National Academy of Sciences 102:29, pages 10244-10249.
Crossref
S. Rospert, M. Rakwalska & Y. Dubaquié. (2005) Polypeptide chain termination and stop codon readthrough on eukaryotic ribosomes. Reviews of Physiology, Biochemistry and Pharmacology.
Crossref
Joe Salas-Marco & David M. Bedwell. (2005) Discrimination Between Defects in Elongation Fidelity and Termination Efficiency Provides Mechanistic Insights into Translational Readthrough. Journal of Molecular Biology 348:4, pages 801-815.
Crossref
Bun-ichiro Ono, Ryohma Yoshida, Koh Kamiya & Tatsuzo Sugimoto. (2005) Suppression of termination mutations caused by defects of the NMD machinery in Saccharomyces cerevisiae. Genes & Genetic Systems 80:5, pages 311-316.
Crossref
Tara Nazarenus, Rebecca Cedarberg, Ryan Bell, Joseph Cheatle, Amanda Forch, Alexis Haifley, Ann Hou, Bessie Wanja Kebaara, Christina Shields, Kate Stoysich, Rachel Taylor & Audrey L. Atkin. (2005) Upf1p, a highly conserved protein required for nonsense-mediated mRNA decay, interacts with the nuclear pore proteins Nup100p and Nup116p. Gene 345:2, pages 199-212.
Crossref
S. Rospert, M. Rakwalska & Y. Dubaquié. 2005. Reviews of Physiology Biochemistry and Pharmacology. Reviews of Physiology Biochemistry and Pharmacology 1 30 .
Philip L. Ross, Yulin N. Huang, Jason N. Marchese, Brian Williamson, Kenneth Parker, Stephen Hattan, Nikita Khainovski, Sasi Pillai, Subhakar Dey, Scott Daniels, Subhasish Purkayastha, Peter Juhasz, Stephen Martin, Michael Bartlet-Jones, Feng He, Allan Jacobson & Darryl J. Pappin. (2004) Multiplexed Protein Quantitation in Saccharomyces cerevisiae Using Amine-reactive Isobaric Tagging Reagents. Molecular & Cellular Proteomics 3:12, pages 1154-1169.
Crossref
JASON W. HARGER & JONATHAN D. DINMAN. (2004) Evidence against a direct role for the Upf proteins in frameshifting or nonsense codon readthrough. RNA 10:11, pages 1721-1729.
Crossref
Nadia Amrani, Robin Ganesan, Stephanie Kervestin, David A. Mangus, Shubhendu Ghosh & Allan Jacobson. (2004) A faux 3′-UTR promotes aberrant termination and triggers nonsense- mediated mRNA decay. Nature 432:7013, pages 112-118.
Crossref
Kenneth C. Parker, Dale Patterson, Brian Williamson, Jason Marchese, Armin Graber, Feng He, Allan Jacobson, Peter Juhasz & Stephen Martin. (2004) Depth of Proteome Issues. Molecular & Cellular Proteomics 3:7, pages 625-659.
Crossref
Jason J. LeBlanc & Karen L. Beemon. (2004) Unspliced Rous Sarcoma Virus Genomic RNAs Are Translated and Subjected to Nonsense-Mediated mRNA Decay before Packaging. Journal of Virology 78:10, pages 5139-5146.
Crossref
KIM M. KEELING, JESSICA LANIER, MING DU, JOE SALAS-MARCO, LIN GAO, ANISA KAENJAK-ANGELETTI & DAVID M. BEDWELL. (2004) Leaky termination at premature stop codons antagonizes nonsense-mediated mRNA decay in S. cerevisiae . RNA 10:4, pages 691-703.
Crossref
B. de Pinto, R. Lippolis, R. Castaldo & N. Altamura. (2004) Overexpression of Upf1p compensates for mitochondrial splicing deficiency independently of its role in mRNA surveillance. Molecular Microbiology 51:4, pages 1129-1142.
Crossref
Ajit Nott, Hervé Le Hir & Melissa J. Moore. (2004) Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes & Development 18:2, pages 210-222.
Crossref
Feng He, Xiangrui Li, Phyllis Spatrick, Ryan Casillo, Shuyun Dong & Allan Jacobson. (2003) Genome-Wide Analysis of mRNAs Regulated by the Nonsense-Mediated and 5′ to 3′ mRNA Decay Pathways in Yeast. Molecular Cell 12:6, pages 1439-1452.
Crossref
SHANG-YI CHIU, GUILLAUME SERIN, OSAMU OHARA & LYNNE E. MAQUAT. (2003) Characterization of human Smg5/7a: A protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1 . RNA 9:1, pages 77-87.
Crossref
Joshua T. MendellColette M. J. ap RhysHarry C. Dietz. (2002) Separable Roles for rent1/hUpf1 in Altered Splicing and Decay of Nonsense Transcripts. Science 298:5592, pages 419-422.
Crossref
Eileen Wagner & Jens Lykke-Andersen. (2002) mRNA surveillance: the perfect persist. Journal of Cell Science 115:15, pages 3033-3038.
Crossref
Renee L Shirley, Amanda S Ford, M Rachel Richards, Markus Albertini & Michael R Culbertson. (2002) Nuclear Import of Upf3p Is Mediated by Importin-α/-β and Export to the Cytoplasm Is Required for a Functional Nonsense-Mediated mRNA Decay Pathway in Yeast. Genetics 161:4, pages 1465-1482.
Crossref
Olivier Namy, Isabelle Hatin, Guillaume Stahl, Hongmei Liu, Stephanie Barnay, Laure Bidou & Jean-Pierre Rousset. (2002) Gene Overexpression as a Tool for Identifying New trans -Acting Factors Involved in Translation Termination in Saccharomyces cerevisiae . Genetics 161:2, pages 585-594.
Crossref
Carlos I González, Anirban Bhattacharya, Weirong Wang & Stuart W Peltz. (2001) Nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Gene 274:1-2, pages 15-25.
Crossref
Philip Mitchell & David Tollervey. (2001) mRNA turnover. Current Opinion in Cell Biology 13:3, pages 320-325.
Crossref
Rachel Aronoff, Renee Baran & Jonathan Hodgkin. (2001) Molecular identification of smg-4 , required for mRNA surveillance in C. elegans. Gene 268:1-2, pages 153-164.
Crossref
C.I. GONZALEZ, W. WANG & S.W. PELTZ. (2001) Nonsense-mediated mRNA Decay in Saccharomyces cerevisiae: A Quality Control Mechanism That Degrades Transcripts Harboring Premature Termination Codons. Cold Spring Harbor Symposia on Quantitative Biology 66:0, pages 321-328.
Crossref
L.E. MAQUAT & G. SERIN. (2001) Nonsense-mediated mRNA Decay: Insights into Mechanism from the Cellular Abundance of Human Upf1, Upf2, Upf3, and Upf3X Proteins. Cold Spring Harbor Symposia on Quantitative Biology 66:0, pages 313-320.
Crossref
Patricia M. Clissold & Chris P. Ponting. (2000) PIN domains in nonsense-mediated mRNA decay and RNAi. Current Biology 10:24, pages R888-R890.
Crossref
Jens Lykke-Andersen, Mei-Di Shu & Joan A. Steitz. (2000) Human Upf Proteins Target an mRNA for Nonsense-Mediated Decay When Bound Downstream of a Termination Codon. Cell 103:7, pages 1121-1131.
Crossref

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