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tRNA-seq and applications

  • Katanski, C.D., H. Alshammary, C.P. Watkins, S-H. Huang, A. Gonzales-Reiche, E.M. Sordillo, H. van Bakel, Mount Sinai PSP study group, K. Lolans, V. Simon*, Tao Pan*: tRNA abundance, modification and fragmentation in nasopharyngeal swabs as biomarkers for COVID-19 severity, Frontiers in Cell & Dev. Biology 10, 999351 (2022).
  • Katanski, C.D., C.P. Watkins, W. Zhang, M. Reyer, S. Miller, Tao Pan*: Analysis of queuosine and 2-thio tRNA modifications by high throughput sequencing, Nucl. Acids Res. 50, e99 (2022).
  • Watkins, C.P., W. Zhang, A.C. Wylder, C.D. Katanski*, Tao Pan*: A multiplex platform for small RNA sequencing elucidates multifaceted tRNA stress response and translational regulation, Nature Communications 13, 2491 (2022).
  • Wang, Y.U., C.D. Katanski, C. Watkins, J.N. Pan, Q. Dai, Z-X. Jiang, Tao Pan*: A High-throughput Screening Method for Evolving a Demethylase Enzyme with Improved and New Functionalities, Nucl. Acids Res. 49, e30 (2021).
  • Richter, U., M.E. Evans, W.C. Clark, P. Marttinen, E. Shoubridge, A. Suomalainen, A. Wredenberg, A. Wedell, Tao Pan* & B. Battersby*: RNA modification landscape of the human mitochondrial tRNALys regulates protein synthesis, Nature Communications 9, 3966, p.1-11 (2018).
  • Evans, M.E., W.C. Clark, G-Q. Zheng & Tao Pan*: Determination of tRNA aminoacylation levels by high throughput sequencing, Nucl. Acids Res. 45, e133, p.1-8 (2017).
  • Dai, Q., G-Q. Zheng, M.H. Schwartz, W.C. Clark & Tao Pan*: Selective enzymatic demethylation of N2,N2-dimethylguanosine in RNA and its application in high-throughput tRNA sequencing, Angewandte Chemie (Int) 56, 5017-5020 (2017).

mRNA and viral RNA modifications

  • Dai, Q., L-S. Zhang, H-L. Sun, K. Pajdzik, L. Yang, C. Ye, C-W. Ju, S. Liu, Y. Wang, Z. Zheng, L. Zhang, B.T. Harada, X. Dou, I. Irkliyenko, X. Feng, W. Zhang, Tao Pan, Chuan He: Quantitative sequencing using BID-seq uncovers abundant pseudouridines in mammalian mRNA at base resolution, Nature Biotech., in press (2022).
  • Pena, N., W. Zhang, C. Watkins, M. Halucha, H. Alshammary, M.M. Hernandez0, W-C. Liu, R.A. Albrecht, A. Garcia-Sastre, V. Simon, C.D. Katanski*, Tao Pan*: Profiling selective packaging of host RNA and viral RNA modification inSARS-CoV-2 viral preparations, Frontiers in Cell & Dev. Biology 10, 768356 (2022).
  • Huang, S. W. Zhang, C.D. Katanski, D. Dersh, Q. Dai, K. Lolans, J. Yewdell, A.M. Eren, Tao Pan*: Interferon inducible pseudouridine modification in human mRNA by quantitative nanopore profiling, Genome Biology 22, 330 (2021).
  • Eckwahl, M., R-Y. Xu, J. Michalkiewicz, W. Zhang, P. Patel, Z. Cai, Tao Pan*: 5-methylcytosine RNA modifications promote retrovirus replication in an ALYREF reader protein-dependent manner, J. Virology 94, e00544-20 (2020).
  • Jurczyszak, D., W. Zhang, S.N. Terry, T. Kehrer, M.C.B. González, E. McGregor, L.C.F. Mulder, M.J. Eckwahl, Tao Pan*, V. Simon*: HIV protease cleaves the antiviral m6A reader protein YTHDF3 in the viral particle, PLoS Pathogens 16, e1008305 (2020).
  • Zhou, K.I., H-L. Shi, R.T. Lyu, A.C. Wylder, Z. Matuszek, J.N. Pan, C. He, M. Parisien*, Tao Pan*: Regulation of co-transcriptional pre-mRNA splicing by m6A through the low-complexity protein hnRNPG, Mol. Cell 76, 70-81 (2019).
  • Liu, N., K.I. Zhou, M. Parisien, Q. Dai, L. Diatchenko & Tao Pan*: N6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein, Nucl. Acids Res. 45, 6051-6063 (2017).
  • Zhou, K.I., N. Liu & Tao Pan*: Identification of N6-methyladenosine reader proteins, Methods 126, 105-111 (2017).

Other RNA modifications

  • Wang, L., J. Wu, R. Liu, W. Chen, Z. Pang, F. Zhou, L. Xia, J. Huang, Tao Pan, X. Su, X-Y. Wang: Epitranscriptome profiling of spleen mRNA m6A methylation reveals pathways of host responses to malaria parasite infection, Frontiers in Immunology 13: 998756 (2022).
  • Zhang, L-S., Q. Xiong, S. Peña Perez, C. Liu, J.B. Wei, C. Le, L. Zhang, B.T. Harada, Q. Dai, X. Feng, Z. Hao, Y. Wang, X. Dong, L. Hu, E. Wang, Tao Pan, A. Klungland, R. Liu, C. He: ALKBH7-mediated demethylation regulates mitochondrial polycistronic RNA processing, Nature Cell. Biol. 23, 684-691 (2021).
  • Blaze, J., A. Navickas, H. L. Phillips, S. Heissel, A. Plaza-Jennings, S. Miglani, H. Asgharian, M. Foo, C. D. Katanski, C. P. Watkins, Z. T. Pennington, B. Javidfar, S. Espeso-Gil, B. Rostandy, H. Alwaseem, C. G. Hahn, H. Molina, D. J. Cai, Tao Pan, W. D. Yao, H. Goodarzi, F. Haghighi, S. Akbarian: Neuronal Nsun2 deficiency produces tRNA epitranscriptomic alterations and proteomic shifts impacting synaptic signaling and behavior, Nature Communications 12, 4913 (2021).
  • Zhang, W. & Tao Pan*: Pseudouridine RNA modification detection and quantification by RT-PCR, Methods S1046-2023(21)00136-5 (2021).
  • Zhang, W. & Tao Pan*: Quantitative Probing of Glycosylated Queuosine Modifications in tRNA, Methods in Enzymology 658, 73-82 (2021).
  • Matuszek, Z.* & Tao Pan*: Quantification of Queuosine Modification Levels in tRNA from Human Cells Using APB Gel and Northern Blot, Bio-protocol 9, e3191 (2019).
  • Zhang, W., M.J. Eckwahl, K.I. Zhou, Tao Pan*: Sensitive and quantitative probing of pseudouridine modification in mRNA and long non-coding RNA, RNA 25, 1218-1225 (2019).
  • Ma, H.H., X.Y. Wang, J.B. Cai, Q. Dai, S. K. Natchiar, R. Lv, K. Chen, Z.K. Lu2, H. Chen, Y.J.G. Shi, F. Lan, J. Fan, B.P. Klaholz, Tao Pan*, Y. Shi*, C. He*: N6-methyladenosine methyltransferase ZCCHC4 mediates ribosomal RNA methylation, Nature Chem. Biol. 15, 88–94 (2019).
  • Zhou, K.I., W.C. Clark, D.W. Pan, M.J. Eckwahl, Q. Dai & Tao Pan*: Pseudouridines have context-dependent mutation and stop rates in high-throughput sequencing, RNA Biol. 15, 892-900 (2018).

Microbiome and microbiome-host interactions

  • Huang, J., W.J. Chen, F. Zhou, Z.C. Pang, L.L. Wang, Tao Pan, X.Y. Wang: Tissue-specific reprogramming of host tRNA transcriptome by the microbiome, Genome Res. 31, 947–957 (2021).
  • Zhang, W., R-Y. Xu, Z. Matuszek, Z. Cai, Tao Pan*: Detection and quantification of glycosylated queuosine modified tRNAs by acid denaturing and APB gels, RNA 26, 1291-1298 (2020).
  • Zhang, J., Lu, R., Zhang, Y., Matuszek, Z., Zhang, W., Xia, Y., Tao Pan, J. Sun: tRNA queuosine modification enzyme modulates the growth and microbiome recruitment to breast tumors, Cancer 12, 628 (2020).
  • Wang*, X.Y., Y. Li, W-J. Chen, H-L. Shi, A.M. Eren, A. Morozov, C. He, G-Z. Luo*, Tao Pan*: Transcriptome-wide reprogramming of N6-methyladenosine modification by the mouse microbiome, Cell Res. 29, 167–170 (2019).
  • Schwartz, M.H., H.P. Wang, J.N. Pan, W.C. Clark, S. Cui, M.J. Eckwahl, D.W. Pan, M. Parisien, S.M. Owens, B.L. Cheng, K. Martinez, J.B. Xu, E.B. Chang, Tao Pan*, A.M. Eren*: Microbiome characterization by high-throughput transfer RNA sequencing and modification analysis, Nature Communications 9:5353, p.1-13 (2018).
  • Wang*, X-W., Z. Matuszek, Y. Huang, M. Parisien, Q. Dai, W.C. Clark, M.H. Schwartz, Tao Pan*: Queuosine modification protects cognate tRNAs against ribonuclease cleavage, RNA 24, 1305-1313 (2018).

Adaptive mistranslation

  • Schwartz*, M.H., Tao Pan*: Determining the fidelity of tRNA aminoacylation via microarrays, Methods 113, 27-33 (2017).
  • Schwartz*, M.H. & Tao Pan*: tRNA misacylation with methionine in the mouse gut microbiome in situ, Microbial Ecology 74, 10-14 (2017).

tRNA and tRNA synthetase

  • Sun, L.T., N. Wei, B. Kuhle, D. Blocque, S. Novick, Z. Matuszek, H.H. Zhou, W.W, He, J.J. Zhang, T. Weber, R. Horvath, P. Latour, Tao Pan, P. Schimmel, P. Griffin, X-L. Yang: CMT2N-causing aminoacylation domain mutants enable Nrp1 interaction with AlaRS, Proc. Natl. Acad. Sci. USA 118, e2012898118 (2021).
  • Chen, M-R. B. Kuhle, J. Diedrich, Z. Liu, J.J. Moresco, J.R. Yates III, Tao Pan, X-L. Yang: Trans-editing activity of a tRNA synthetase allows vertebrates to abundantly express mischargeable tRNA without causing mistranslation, Nucl. Acids Res. 48, 6445–6457 (2020).
  • Blocquel, D. L. Sun, Z. Matuszek, S. Li, T. Weber, B. Kuhle, G. Kooi, N. Wei, J. Baets, Tao Pan, P. Schimmel, X-L. Yang: CMT disease severity correlates with mutation-induced open conformation of His-tRNA synthetase, not aminoacylation loss in patient cells, Proc. Natl. Acad. Sci. USA 116, 19440-19448 (2019).
  • Peterlin, B.M., P-Y. Liu, X-Y. Wang, D. Cary, W. Shao, T. Hong, Tao Pan, K. Fujinaga: Hili inhibits HIV replication in activated T cells, J. Virology 91, e00237-17, p. 1-14 (2017).

Reviews and commentaries

  • Zhang, W., M. Foo, A.M. Eren, Tao Pan*: tRNA modification dynamics from individual organisms to metaepitranscriptomics of microbiomes, Mol. Cell 82 891-906 (2021). [Review]
  • Zhang, W., Tao Pan*: A dual function PUS enzyme, Nature Chem. Biol. 16, 107-108 (2020). [Commentary]
  • Tao Pan: Modifications and functional genomics of human transfer RNA, Cell Res. 28, 395–404 (2018). [Review]
  • Zhou, K.I., Tao Pan*: An additional class of N6-methyladenosine readers, Nature Cell Biol. 20, 230–232 (2018). [Commentary]
  • Roundtree, I.A., M.E. Evans, Tao Pan*, C. He*: Dynamic RNA modifications in gene expression regulation, Cell 169, 1187-1200 (2017). [Review]
  • Schwartz*, M.H., Tao Pan*: Function and origin of mistranslation in distinct cellular contexts, Crit. Rev. Biochem. Mol. Biol. 52, 205-219 (2017). [Review]
  • Lewis, C.J.T., Tao Pan* & A. Kalsotra*: RNA Modifications and Structures Cooperate to Guide RNA-protein Interactions, Nature Rev. Mol. Cell Biol. 18, 202-210 (2017). [Review]
  • Liu, N. & Tao Pan*: RNA epigenetics (epitranscriptomics). In "Translating epigenetics to the clinic" ed. Laurence, J. & Van Beusekom, M., Academic Press, Elsevier, pp.19-36 (2017). [Review]

Selected older publications

  • Schwartz, M.H., J.R. Waldbauer, L-C. Zhang, Tao Pan*: Global tRNA misacylation induced by anaerobiosis and antibiotic exposure broadly increases stress resistance in Escherichia coli, Nucl. Acids Res. 44, 10292-10303 (2016).
  • Gomes, A.C., A.J. Kordala, R. Strack, X-Y. Wang, R. Geslain, K. Delaney, W.C. Clark, R. Keenan, Tao Pan*: A dual fluorescent reporter for the investigation of methionine mistranslation in live cells, RNA 22, 467-76. (2016).
  • Schwartz, M.H. & Tao Pan*: Temperature dependent mistranslation in a hyperthermophile adapts proteins to lower temperatures, Nucl. Acids Res. 44, 294-303 (2016).
  • Clark, W.C., M.E. Evans, D. Dominissini, G-Q. Zheng, Tao Pan*: tRNA base methylation identification and quantification via high throughput sequencing, RNA 22, 1771-1784 (2016).
  • Liu, F., W. Clark, G-Z. Luo, X-Y. Wang, Y. Fu, J-B. Wei, X. Wang, Z-Y. Hao, Q. Dai, G-Q. Zheng, H-H. Ma, D. Han, M. Evans, A. Klungland, Tao Pan* & C. He*: ALKBH1-Mediated tRNA Demethylation Regulates Translation, Cell 167, 816-828 (2016).
  • Zhou, K.I., M. Parisien, Q. Dai, N. Liu, L. Diatchenko, J.R. Sachleben & Tao Pan*: N6-methyladenosine modification in a long non-coding RNA hairpin predisposes its conformation to protein binding, J. Mol. Biol. 428, 822-33 (2016).
  • Zheng, G.Q., Y. Qin, W.C. Clark, Q. Dai, C.Q. Yi, C. He, A. M. Lambowitz*, Tao Pan*: Efficient and quantitative high-throughput transfer RNA sequencing, Nature Methods 12, 835-837 (2015).
  • Liu, N., Q. Dai, GQ. Zheng, C. He, M. Parisien*, Tao Pan*: N6-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions, Nature 518, 560-564 (2015).
  • Liu, N. & Tao Pan: RNA epigenetics, Translational Research 165 165, 28-35 (2015). [review]
  • Zaborske, J.M., V. L. DuMont, E. W. J. Wallace, Tao Pan, C. F. Aquadro & D. A. Drummond: A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus, PLoS Biology 13, e1002015, p.1-13 (2014).
  • Parisien, M., X. Wang, Tao Pan*: Diversity of human tRNA genes from the 1,000-genomes project, RNA Biology 10, 1853-1867 (2013).
  • Liu, N., M. Parisien, Q. Dai, G-Q. Zheng, C. He & Tao Pan*: Probing N6-methyladenosine RNA modification status at single nucleotide resolution in mRNA and long non-coding RNA, RNA 19, 1848-1856 (2013).
  • Tao Pan: Adaptive translation as a mechanism of stress response and adaptation, Ann. Rev. Genetics 47, 139-155 (2013). [review]
  • Parisien, M., X-Y. Wang, G. Perdrizet II, C. Lamphear, C.A. Fierke, K.C. Maheshwari, M.J. Wilde, T.R. Sosnick*, Tao Pan*: Discovering RNA-protein interactome using chemical context profiling of the RNA-protein interface, Cell Reports, 3, 1703-13 (2013).
  • Pavon-Eternod, M., S. Gomes, M.R. Rosner* & Tao Pan*: Overexpression of Initiator Methionine tRNA Leads to Global Reprogramming of tRNA Expression and Increased Proliferation in Human Epithelial Cells, RNA 19, 461-6 (2013).
  • Tao Pan: N6-methyl-Adenosine modification in messenger and long non-coding RNA, Trends in Biochem. Sci. 38, 204-9 (2013). [review]
  • Perdrizet, G.A., I. Artsimovitch, R. Furman, T. R. Sosnick*, Tao Pan*: Transcriptional pausing coordinates folding of the aptamer domain and the expression platform of a riboswitch, Proc. Natl. Acad. Sci. USA 109, 3323-3328 (2012).
  • Zhou, D-H, J-Y. Lee, C. Frankenberger, R. Geslain*, M. Rosner*, Tao Pan*: Anti-tumor effects of an engineered "killer" transfer RNA, Biochem. Biophys. Res. Comm. 427, 148-153 (2012).
  • Jones, T.E., R.W. Alexander, Tao Pan*: Misacylation of specific non-methionyl-tRNAs by a bacterial methionyl-tRNA synthetases, Proc. Natl. Acad. Sci. USA, 108, 6933-6938 (2011).
  • Fu, Y., Q. Dai, W. Zhang, J. Ren, Tao Pan* & C. He*: The AlkB domain of mammalian ABH8 catalyzes hydroxylation of 5-methoxycarbonylmethyluridine at the anticodon wobble base in tRNA, Angewandte Chemie (Int) 49, 8885-8888 (2010).
  • Zaborske, J.M., X-C. Wu, R. C. Wek, Tao Pan*: Selective control of amino acid metabolism by the GCN2 eIF2 kinase pathway in Saccharomyces cerevisiae, BMC Biochemistry 11:e29 (2010).
  • Saikia, M., Y. Fu, M. Pavon-Eternod, C. He & Tao Pan*: Genome-wide analysis of N1-methyl-adenosine modification in human tRNAs, RNA, RNA 16, 1317-1327 (2010).
  • Geslain, R. & Tao Pan*: Functional analysis of human tRNA isodecoders, J. Mol. Biol. 396, 821-831 (2010).
  • Pavon-Eternod, M., M. Wei, Tao Pan* & Lawrence Kleiman*: Profiling non-lysyl tRNAs in HIV-1, RNA 16, 267-273 (2010).
  • Netzer, N., J.M. Goodenbour, A. David, K.A. Dittmar, R.B. Jones, J.R. Schneider, D. Boone, E.M. Eves, M.R. Rosner, J.S. Gibbs, A. Embry, B. Dolan, S. Das, H. Hickman, P. Berglund, J.R. Bennink, J.W. Yewdell*, Tao Pan*: Innate Immune and Chemically Triggered Oxidative Stress Modifies Translational Fidelity, Nature 462, 522-526 (2009).
  • Pavon-Eternod, M., S. Gomes, R. Geslain, Q. Dai, M. R. Rosner* & Tao Pan*: tRNA Over-expression in Breast Cancer and Functional Consequences, Nucl. Acids Res. 37, 7268-7280 (2009).
  • Zaborske, J.M., J. Narasimhan, L. Jiang, S.A. Wek, K.A. Dittmar, F. Freimoser, Tao Pan* & R.C. Wek*: Genome-wide analysis of tRNA charging and activation of the eIF2 kinase Gcn2p, J. Biol. Chem. 284, 25254-25267 (2009).
  • Wong, T., T.R. Sosnick* & Tao Pan*: Folding of non-coding RNAs during transcription facilitated by pausing-induced non-native structures, Proc. Natl. Acad. Sci. USA 104, 17995-18000 (2007).
  • Dittmar, K.A., J.M. Goodenbour & Tao Pan*: Tissue specific differences in human transfer RNA expression. PLoS Genetics 2, 2107-2115 (e221, 2006).
  • Saikia, M., Q. Dai, W.A. Decatur, M.J. Fournier, J.A. Piccirilli* & Tao Pan*: A systematic, ligation based approach to study RNA modifications, RNA 12, 2025-2033 (2006).
  • Goodenbour, J.M. & Tao Pan*: Diversity of tRNA genes in eukaryotes. Nucl. Acids Res. 34, 6137-46 (2006).
  • Tao Pan & T.R. Sosnick: RNA folding during transcription. Ann. Rev. Biophysics and Biomol. Dynamics 35, 161-175 (2006) [Review].
  • Baird NJ, Westhof E, Qin H, Pan T*, Sosnick TR*. Structure of a folding intermediate reveals the interplay between core and peripheral elements in RNA folding. J Mol Biol. 352:712-22 (2005).
  • Dittmar KA, Sorensen MA, Elf J, Ehrenberg M, Tao Pan*. Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep. 6:151-7 (2005).
  • Dittmar KA, Mobley EM, Radek AJ, Tao Pan*. Exploring the regulation of tRNA distribution on the genomic scale. J Mol Biol. 337:31-47 (2004).
  • Fang, X-W., P. Thiyagarajan, T.R. Sosnick* & Tao Pan*: The rate-limiting step in the folding of a large ribozyme without kinetic traps. Proc. Natl. Acad. Sci. USA 99, 8518-8523 (2002).
  • Fang, X-W., B.L. Golden, K. Littrell, V. Shelton, P. Thiyagarajan, Tao Pan* & T.R. Sosnick*: The thermodynamic origin of the stability of a thermophilic ribozyme. Proc. Natl. Acad. Sci. USA 98, 4355-4360 (2001).
  • Tao Pan*, I. Artsimovitch, X-W. Fang, R. Landick & T.R. Sosnick*: Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proc. Natl. Acad. Sci. USA 96, 9545-9550 (1999).
  • Loria, A. & Tao Pan*: Domain structure of the ribozyme from eubacterial ribonuclease P. RNA 2, 551-563 (1996).

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