Tao Pan

Professor
Websites
Research Summary
Our research focuses on (i) functional genomics and biology of tRNA including microbiomes and (ii) epitranscriptomics including microbiome-host interactions. tRNA biology: Translational regulation relies on the dynamic properties of tRNA that constantly change to facilitate response and adaptation to new environments and to control gene expression. We developed high throughput sequencing technologies that measure tRNA abundance, charging and modifications in one single sequencing library. We are investigating the roles of tRNA in translational control and extra-translational functions in mammalian cells. Microbiome: We also developed tRNA-seq as another approach for microbiome characterization. Standard microbiome characterizations include 16S-seq or shotgun metagenomics. Although powerful, these DNA-based methods do not directly report the microbiome activity such as dynamic gene expression which requires the studies of RNA in the microbiome. Our microbiome tRNA-seq results show extensive variations of tRNA abundance and modification patterns in microbiomes from different sources. We also show that tRNA modification dynamics in the microbiome correlates with tuning the expression of specific microbial proteins, indicating that tRNA-seq can provide new insights in microbiome biology. We are further developing this approach to explore the potentials of tRNA-seq to study microbiomes from humans and from the oceans. Epitranscriptomics: Over 100 types of post-transcriptional RNA modifications have been identified in thousands of sites in the transcriptome. They include methylation of bases and the ribose backbone, rotation and reduction of uridine, base deamination, addition of ring structures and carbohydrate moieties, and so on. mRNA modifications are involved in cell differentiation, proliferation, and many other cellular functions and human diseases. Some mRNA modifications can also be removed by cellular enzymes, resulting in the dynamic regulation of their functions. We are investigating the function and mechanisms of mRNA modifications such as N6-methyladenosine (m6A) in the regulation of gene expression. For example, we discovered that m6A modification can alter the local mRNA structure to regulate binding of mRNA binding proteins transcriptome-wide (m6A switch), resulting in changes in mRNA abundance and alternative splicing. Microbiome-host interactions through epitranscriptomics: We are working on elucidating the function of mammalian host mRNA and tRNA modifications in response to the gut microbiome. We found that microbiome reprograms the host m6A modifications transcriptome-wide in a tissue-dependent manner, suggesting that this dynamic epitranscriptomic mark is used in yet unknown ways in microbiome response. We also found that a microbiome dependent, host tRNA modification alters the cellular small RNA pool, suggesting yet another pathway of microbiome response through RNA modifications.
Keywords
Functional genomics, Microbiome, epitranscriptomics, RNA modification, tRNA
Education
  • University des Saarlands, Germany, BS/MS Chemistry 06/1986
  • Yale University, New Haven, CT, Ph.D. Biophysics/Biochemistry 08/1990
  • University of Colorado at Boulder, Boulder, CO, postdoctoral Biochemistry 12/1993
Biosciences Graduate Program Association
Awards & Honors
  • 1991 - 1993 Damon Runyon-Walter Winchell Cancer Research Fund
  • 1994 - Cancer Research Foundation, Raymond F. Zelko Young Investigator
  • 1995 - 1997 American Cancer Society, Junior Faculty Research Award
  • 2009 - 2013 NIH EUREKA award
  • 2011 - 2016 NIH Director’s Pioneer award
  • 2015 - American Association for the Advancement of Science (AAAS) Fellow
Publications
  1. Zhang W, Eckwahl M, Zhou K, Pan T. Sensitive and quantitative probing of pseudouridine modification in mRNA and long non-coding RNA. RNA. 2019 Jun 21. View in: PubMed

  2. Wang X, Li Y, Chen W, Shi H, Eren AM, Morozov A, He C, Luo GZ, Pan T. Transcriptome-wide reprogramming of N6-methyladenosine modification by the mouse microbiome. Cell Res. 2019 Feb; 29(2):167-170. View in: PubMed

  3. Schwartz MH, Wang H, Pan JN, Clark WC, Cui S, Eckwahl MJ, Pan DW, Parisien M, Owens SM, Cheng BL, Martinez K, Xu J, Chang EB, Pan T, Eren AM. Microbiome characterization by high-throughput transfer RNA sequencing and modification analysis. Nat Commun. 2018 12 17; 9(1):5353. View in: PubMed

  4. Ma H, Wang X, Cai J, Dai Q, Natchiar SK, Lv R, Chen K, Lu Z, Chen H, Shi YG, Lan F, Fan J, Klaholz BP, Pan T, Shi Y, He C. N6-Methyladenosine methyltransferase ZCCHC4 mediates ribosomal RNA methylation. Nat Chem Biol. 2019 01; 15(1):88-94. View in: PubMed

  5. Richter U, Evans ME, Clark WC, Marttinen P, Shoubridge EA, Suomalainen A, Wredenberg A, Wedell A, Pan T, Battersby BJ. RNA modification landscape of the human mitochondrial tRNALys regulates protein synthesis. Nat Commun. 2018 09 27; 9(1):3966. View in: PubMed

  6. Wang X, Matuszek Z, Huang Y, Parisien M, Dai Q, Clark W, Schwartz MH, Pan T. Queuosine modification protects cognate tRNAs against ribonuclease cleavage. RNA. 2018 10; 24(10):1305-1313. View in: PubMed

  7. Zhou KI, Clark WC, Pan DW, Eckwahl MJ, Dai Q, Pan T. Pseudouridines have context-dependent mutation and stop rates in high-throughput sequencing. RNA Biol. 2018; 15(7):892-900. View in: PubMed

  8. Zhou KI, Pan T. An additional class of m6A readers. Nat Cell Biol. 2018 03; 20(3):230-232. View in: PubMed

  9. Pan T. Modifications and functional genomics of human transfer RNA. Cell Res. 2018 Apr; 28(4):395-404. View in: PubMed

  10. Roundtree IA, Evans ME, Pan T, He C. Dynamic RNA Modifications in Gene Expression Regulation. Cell. 2017 Jun 15; 169(7):1187-1200. View in: PubMed

  11. Evans ME, Clark WC, Zheng G, Pan T. Determination of tRNA aminoacylation levels by high-throughput sequencing. Nucleic Acids Res. 2017 Aug 21; 45(14):e133. View in: PubMed

  12. Zhou KI, Liu N, Pan T. Identification of N6-methyladenosine reader proteins. Methods. 2017 08 15; 126:105-111. View in: PubMed

  13. Dai Q, Zheng G, Schwartz MH, Clark WC, Pan T. Selective Enzymatic Demethylation of N2 ,N2 -Dimethylguanosine in RNA and Its Application in High-Throughput tRNA Sequencing. Angew Chem Int Ed Engl. 2017 04 24; 56(18):5017-5020. View in: PubMed

  14. Liu N, Zhou KI, Parisien M, Dai Q, Diatchenko L, Pan T. N6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein. Nucleic Acids Res. 2017 Jun 02; 45(10):6051-6063. View in: PubMed

  15. Peterlin BM, Liu P, Wang X, Cary D, Shao W, Leoz M, Hong T, Pan T, Fujinaga K. Hili Inhibits HIV Replication in Activated T Cells. J Virol. 2017 06 01; 91(11). View in: PubMed

  16. Lewis CJ, Pan T, Kalsotra A. RNA modifications and structures cooperate to guide RNA-protein interactions. Nat Rev Mol Cell Biol. 2017 03; 18(3):202-210. View in: PubMed

  17. Schwartz MH, Pan T. Function and origin of mistranslation in distinct cellular contexts. Crit Rev Biochem Mol Biol. 2017 Apr; 52(2):205-219. View in: PubMed

  18. Schwartz MH, Pan T. tRNA Misacylation with Methionine in the Mouse Gut Microbiome in Situ. Microb Ecol. 2017 07; 74(1):10-14. View in: PubMed

  19. Liu F, Clark W, Luo G, Wang X, Fu Y, Wei J, Wang X, Hao Z, Dai Q, Zheng G, Ma H, Han D, Evans M, Klungland A, Pan T, He C. ALKBH1-Mediated tRNA Demethylation Regulates Translation. Cell. 2016 Oct 20; 167(3):816-828.e16. View in: PubMed

  20. Schwartz MH, Waldbauer JR, Zhang L, Pan T. Global tRNA misacylation induced by anaerobiosis and antibiotic exposure broadly increases stress resistance in Escherichia coli. Nucleic Acids Res. 2016 Dec 01; 44(21):10292-10303. View in: PubMed

  21. Schwartz MH, Pan T. Determining the fidelity of tRNA aminoacylation via microarrays. Methods. 2017 01 15; 113:27-33. View in: PubMed

  22. Sun L, Gomes AC, He W, Zhou H, Wang X, Pan DW, Schimmel P, Pan T, Yang XL. Evolutionary Gain of Alanine Mischarging to Noncognate tRNAs with a G4:U69 Base Pair. J Am Chem Soc. 2016 10 05; 138(39):12948-12955. View in: PubMed

  23. Clark WC, Evans ME, Dominissini D, Zheng G, Pan T. tRNA base methylation identification and quantification via high-throughput sequencing. RNA. 2016 11; 22(11):1771-1784. View in: PubMed

  24. Saikia M, Wang X, Mao Y, Wan J, Pan T, Qian SB. Codon optimality controls differential mRNA translation during amino acid starvation. RNA. 2016 11; 22(11):1719-1727. View in: PubMed

  25. Zhou KI, Pan T. Structures of the m(6)A Methyltransferase Complex: Two Subunits with Distinct but Coordinated Roles. Mol Cell. 2016 07 21; 63(2):183-185. View in: PubMed

  26. Wang X, Pan T. Stress Response and Adaptation Mediated by Amino Acid Misincorporation during Protein Synthesis. Adv Nutr. 2016 07; 7(4):773S-9S. View in: PubMed

  27. Wang X, Chow CR, Ebine K, Lee J, Rosner MR, Pan T, Munshi HG. Interaction of tRNA with MEK2 in pancreatic cancer cells. Sci Rep. 2016 06 15; 6:28260. View in: PubMed

  28. Frye M, Jaffrey SR, Pan T, Rechavi G, Suzuki T. RNA modifications: what have we learned and where are we headed? Nat Rev Genet. 2016 06; 17(6):365-72. View in: PubMed

  29. Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N, Ben-Haim MS, Dai Q, Di Segni A, Salmon-Divon M, Clark WC, Zheng G, Pan T, Solomon O, Eyal E, Hershkovitz V, Han D, Doré LC, Amariglio N, Rechavi G, He C. The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA. Nature. 2016 Feb 25; 530(7591):441-6. View in: PubMed

  30. Liu N, Pan T. N6-methyladenosine–encoded epitranscriptomics. Nat Struct Mol Biol. 2016 Feb; 23(2):98-102. View in: PubMed

  31. Wang X, Pan T. Correction: Methionine Mistranslation Bypasses the Restraint of the Genetic Code to Generate Mutant Proteins with Distinct Activities. PLoS Genet. 2016 01; 12(1):e1005832. View in: PubMed

  32. Gomes AC, Kordala AJ, Strack R, Wang X, Geslain R, Delaney K, Clark WC, Keenan R, Pan T. A dual fluorescent reporter for the investigation of methionine mistranslation in live cells. RNA. 2016 Mar; 22(3):467-76. View in: PubMed

  33. Wang X, Pan T. Methionine Mistranslation Bypasses the Restraint of the Genetic Code to Generate Mutant Proteins with Distinct Activities. PLoS Genet. 2015 Dec; 11(12):e1005745. View in: PubMed

  34. Schwartz MH, Pan T. Temperature dependent mistranslation in a hyperthermophile adapts proteins to lower temperatures. Nucleic Acids Res. 2016 Jan 08; 44(1):294-303. View in: PubMed

  35. Liu N, Pan T. Probing N6-methyladenosine (m6A) RNA Modification in Total RNA with SCARLET. Methods Mol Biol. 2016; 1358:285-92. View in: PubMed

  36. Wallace EW, Kear-Scott JL, Pilipenko EV, Schwartz MH, Laskowski PR, Rojek AE, Katanski CD, Riback JA, Dion MF, Franks AM, Airoldi EM, Pan T, Budnik BA, Drummond DA. Reversible, Specific, Active Aggregates of Endogenous Proteins Assemble upon Heat Stress. Cell. 2015 Sep 10; 162(6):1286-98. View in: PubMed

  37. Zhou KI, Parisien M, Dai Q, Liu N, Diatchenko L, Sachleben JR, Pan T. N(6)-Methyladenosine Modification in a Long Noncoding RNA Hairpin Predisposes Its Conformation to Protein Binding. J Mol Biol. 2016 Feb 27; 428(5 Pt A):822-833. View in: PubMed

  38. Liu N, Pan T. Probing RNA Modification Status at Single-Nucleotide Resolution in Total RNA. Methods Enzymol. 2015; 560:149-59. View in: PubMed

  39. Zheng G, Qin Y, Clark WC, Dai Q, Yi C, He C, Lambowitz AM, Pan T. Efficient and quantitative high-throughput tRNA sequencing. Nat Methods. 2015 Sep; 12(9):835-837. View in: PubMed

  40. Pan T. My adventure in tRNA biology, so far. RNA. 2015 Apr; 21(4):707-8. View in: PubMed

  41. Liu N, Dai Q, Zheng G, He C, Parisien M, Pan T. N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature. 2015 Feb 26; 518(7540):560-4. View in: PubMed

  42. Chen K, Lu Z, Wang X, Fu Y, Luo GZ, Liu N, Han D, Dominissini D, Dai Q, Pan T, He C. High-resolution N(6) -methyladenosine (m(6) A) map using photo-crosslinking-assisted m(6) A sequencing. Angew Chem Int Ed Engl. 2015 Jan 26; 54(5):1587-90. View in: PubMed

  43. Zaborske JM, DuMont VL, Wallace EW, Pan T, Aquadro CF, Drummond DA. A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. PLoS Biol. 2014 Dec; 12(12):e1002015. View in: PubMed

  44. Liu N, Pan T. RNA epigenetics. Transl Res. 2015 Jan; 165(1):28-35. View in: PubMed

  45. Saikia M, Jobava R, Parisien M, Putnam A, Krokowski D, Gao XH, Guan BJ, Yuan Y, Jankowsky E, Feng Z, Hu GF, Pusztai-Carey M, Gorla M, Sepuri NB, Pan T, Hatzoglou M. Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Mol Cell Biol. 2014 Jul; 34(13):2450-63. View in: PubMed

  46. Parisien M, Wang X, Pan T. Diversity of human tRNA genes from the 1000-genomes project. RNA Biol. 2013 Dec; 10(12):1853-67. View in: PubMed

  47. Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, Fu Y, Parisien M, Dai Q, Jia G, Ren B, Pan T, He C. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2014 Jan 02; 505(7481):117-20. View in: PubMed

  48. Liu N, Parisien M, Dai Q, Zheng G, He C, Pan T. Probing N6-methyladenosine RNA modification status at single nucleotide resolution in mRNA and long noncoding RNA. RNA. 2013 Dec; 19(12):1848-56. View in: PubMed

  49. Czech A, Wende S, Mörl M, Pan T, Ignatova Z. Reversible and rapid transfer-RNA deactivation as a mechanism of translational repression in stress. PLoS Genet. 2013 Aug; 9(8):e1003767. View in: PubMed

  50. Pan T. Adaptive translation as a mechanism of stress response and adaptation. Annu Rev Genet. 2013; 47:121-37. View in: PubMed

  51. Parisien M, Wang X, Perdrizet G, Lamphear C, Fierke CA, Maheshwari KC, Wilde MJ, Sosnick TR, Pan T. Discovering RNA-protein interactome by using chemical context profiling of the RNA-protein interface. Cell Rep. 2013 May 30; 3(5):1703-13. View in: PubMed

  52. Krokowski D, Han J, Saikia M, Majumder M, Yuan CL, Guan BJ, Bevilacqua E, Bussolati O, Bröer S, Arvan P, Tchórzewski M, Snider MD, Puchowicz M, Croniger CM, Kimball SR, Pan T, Koromilas AE, Kaufman RJ, Hatzoglou M. A self-defeating anabolic program leads to ß-cell apoptosis in endoplasmic reticulum stress-induced diabetes via regulation of amino acid flux. J Biol Chem. 2013 Jun 14; 288(24):17202-13. View in: PubMed

  53. Vilfan ID, Tsai YC, Clark TA, Wegener J, Dai Q, Yi C, Pan T, Turner SW, Korlach J. Analysis of RNA base modification and structural rearrangement by single-molecule real-time detection of reverse transcription. J Nanobiotechnology. 2013 Apr 03; 11:8. View in: PubMed

  54. Pavon-Eternod M, Gomes S, Rosner MR, Pan T. Overexpression of initiator methionine tRNA leads to global reprogramming of tRNA expression and increased proliferation in human epithelial cells. RNA. 2013 Apr; 19(4):461-6. View in: PubMed

  55. Pan T. N6-methyl-adenosine modification in messenger and long non-coding RNA. Trends Biochem Sci. 2013 Apr; 38(4):204-9. View in: PubMed

  56. Subramaniam AR, Pan T, Cluzel P. Environmental perturbations lift the degeneracy of the genetic code to regulate protein levels in bacteria. Proc Natl Acad Sci U S A. 2013 Feb 05; 110(6):2419-24. View in: PubMed

  57. Pavon-Eternod M, David A, Dittmar K, Berglund P, Pan T, Bennink JR, Yewdell JW. Vaccinia and influenza A viruses select rather than adjust tRNAs to optimize translation. Nucleic Acids Res. 2013 Feb 01; 41(3):1914-21. View in: PubMed

  58. Geslain R, Uddin S, Liu H, Jiang H, van Besien K, Pan T, Wickrema A. Distinct functions of erythropoietin and stem cell factor are linked to activation of mTOR kinase signaling pathway in human erythroid progenitors. Cytokine. 2013 Jan; 61(1):329-35. View in: PubMed

  59. Saikia M, Krokowski D, Guan BJ, Ivanov P, Parisien M, Hu GF, Anderson P, Pan T, Hatzoglou M. Genome-wide identification and quantitative analysis of cleaved tRNA fragments induced by cellular stress. J Biol Chem. 2012 Dec 14; 287(51):42708-25. View in: PubMed

  60. Li M, Kao E, Gao X, Sandig H, Limmer K, Pavon-Eternod M, Jones TE, Landry S, Pan T, Weitzman MD, David M. Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11. Nature. 2012 Nov 01; 491(7422):125-8. View in: PubMed

  61. Zhou DH, Lee J, Frankenberger C, Geslain R, Rosner M, Pan T. Anti-tumor effects of an engineered "killer" transfer RNA. Biochem Biophys Res Commun. 2012 Oct 12; 427(1):148-53. View in: PubMed

  62. Wiltrout E, Goodenbour JM, Fréchin M, Pan T. Misacylation of tRNA with methionine in Saccharomyces cerevisiae. Nucleic Acids Res. 2012 Nov 01; 40(20):10494-506. View in: PubMed

  63. Starck SR, Jiang V, Pavon-Eternod M, Prasad S, McCarthy B, Pan T, Shastri N. Leucine-tRNA initiates at CUG start codons for protein synthesis and presentation by MHC class I. Science. 2012 Jun 29; 336(6089):1719-23. View in: PubMed

  64. Novoa EM, Pavon-Eternod M, Pan T, Ribas de Pouplana L. A role for tRNA modifications in genome structure and codon usage. Cell. 2012 Mar 30; 149(1):202-13. View in: PubMed

  65. Perdrizet GA, Artsimovitch I, Furman R, Sosnick TR, Pan T. Transcriptional pausing coordinates folding of the aptamer domain and the expression platform of a riboswitch. Proc Natl Acad Sci U S A. 2012 Feb 28; 109(9):3323-8. View in: PubMed

  66. Parisien M, Yi C, Pan T. Rationalization and prediction of selective decoding of pseudouridine-modified nonsense and sense codons. RNA. 2012 Mar; 18(3):355-67. View in: PubMed

  67. Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, Yi C, Lindahl T, Pan T, Yang YG, He C. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol. 2011 Oct 16; 7(12):885-7. View in: PubMed

  68. Geslain R, Pan T. tRNA: Vast reservoir of RNA molecules with unexpected regulatory function. Proc Natl Acad Sci U S A. 2011 Oct 04; 108(40):16489-90. View in: PubMed

  69. Yi C, Pan T. Cellular dynamics of RNA modification. Acc Chem Res. 2011 Dec 20; 44(12):1380-8. View in: PubMed

  70. Jones TE, Alexander RW, Pan T. Misacylation of specific nonmethionyl tRNAs by a bacterial methionyl-tRNA synthetase. Proc Natl Acad Sci U S A. 2011 Apr 26; 108(17):6933-8. View in: PubMed

  71. Dai Q, Song CX, Pan T, He C. Syntheses of two 5-hydroxymethyl-2'-deoxycytidine phosphoramidites with TBDMS as the 5-hydroxymethyl protecting group and their incorporation into DNA. J Org Chem. 2011 May 20; 76(10):4182-8. View in: PubMed

  72. Reiter NJ, Osterman A, Torres-Larios A, Swinger KK, Pan T, Mondragón A. Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature. 2010 Dec 09; 468(7325):784-9. View in: PubMed

  73. Baird NJ, Ludtke SJ, Khant H, Chiu W, Pan T, Sosnick TR. Discrete structure of an RNA folding intermediate revealed by cryo-electron microscopy. J Am Chem Soc. 2010 Nov 24; 132(46):16352-3. View in: PubMed

  74. Wong TN, Pan T. RNA folding during transcription: protocols and studies. Methods Enzymol. 2009; 468:167-93. View in: PubMed

  75. Zaborske JM, Wu X, Wek RC, Pan T. Selective control of amino acid metabolism by the GCN2 eIF2 kinase pathway in Saccharomyces cerevisiae. BMC Biochem. 2010 Aug 04; 11:29. View in: PubMed

  76. Fu Y, Dai Q, Zhang W, Ren J, Pan T, He C. The AlkB domain of mammalian ABH8 catalyzes hydroxylation of 5-methoxycarbonylmethyluridine at the wobble position of tRNA. Angew Chem Int Ed Engl. 2010 Nov 15; 49(47):8885-8. View in: PubMed

  77. Zaborske J, Pan T. Genome-wide analysis of aminoacylation (charging) levels of tRNA using microarrays. J Vis Exp. 2010 Jun 18; (40). View in: PubMed

  78. Saikia M, Fu Y, Pavon-Eternod M, He C, Pan T. Genome-wide analysis of N1-methyl-adenosine modification in human tRNAs. RNA. 2010 Jul; 16(7):1317-27. View in: PubMed

  79. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, Zaborske J, Pan T, Dahan O, Furman I, Pilpel Y. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell. 2010 Apr 16; 141(2):344-54. View in: PubMed

  80. Staschke KA, Dey S, Zaborske JM, Palam LR, McClintick JN, Pan T, Edenberg HJ, Wek RC. Integration of general amino acid control and target of rapamycin (TOR) regulatory pathways in nitrogen assimilation in yeast. J Biol Chem. 2010 May 28; 285(22):16893-911. View in: PubMed

  81. Baird NJ, Gong H, Zaheer SS, Freed KF, Pan T, Sosnick TR. Extended structures in RNA folding intermediates are due to nonnative interactions rather than electrostatic repulsion. J Mol Biol. 2010 Apr 16; 397(5):1298-306. View in: PubMed

  82. Geslain R, Pan T. Functional analysis of human tRNA isodecoders. J Mol Biol. 2010 Feb 26; 396(3):821-31. View in: PubMed

  83. Pavon-Eternod M, Wei M, Pan T, Kleiman L. Profiling non-lysyl tRNAs in HIV-1. RNA. 2010 Feb; 16(2):267-73. View in: PubMed

  84. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, Schneider JR, Boone D, Eves EM, Rosner MR, Gibbs JS, Embry A, Dolan B, Das S, Hickman HD, Berglund P, Bennink JR, Yewdell JW, Pan T. Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature. 2009 Nov 26; 462(7272):522-6. View in: PubMed

  85. Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, Pan T. tRNA over-expression in breast cancer and functional consequences. Nucleic Acids Res. 2009 Nov; 37(21):7268-80. View in: PubMed

  86. Zaborske JM, Narasimhan J, Jiang L, Wek SA, Dittmar KA, Freimoser F, Pan T, Wek RC. Genome-wide analysis of tRNA charging and activation of the eIF2 kinase Gcn2p. J Biol Chem. 2009 Sep 11; 284(37):25254-67. View in: PubMed

  87. Zhou Y, Goodenbour JM, Godley LA, Wickrema A, Pan T. High levels of tRNA abundance and alteration of tRNA charging by bortezomib in multiple myeloma. Biochem Biophys Res Commun. 2009 Jul 24; 385(2):160-4. View in: PubMed

  88. Dai Q, Saikia M, Li NS, Pan T, Piccirilli JA. Efficient chemical synthesis of AppDNA by adenylation of immobilized DNA-5'-monophosphate. Org Lett. 2009 Mar 05; 11(5):1067-70. View in: PubMed

  89. Qu X, Smith GJ, Lee KT, Sosnick TR, Pan T, Scherer NF. Single-molecule nonequilibrium periodic Mg2+-concentration jump experiments reveal details of the early folding pathways of a large RNA. Proc Natl Acad Sci U S A. 2008 May 06; 105(18):6602-7. View in: PubMed

  90. Pan T. Probing RNA structure by lead cleavage. Curr Protoc Nucleic Acid Chem. 2001 May; Chapter 6:Unit 6.3. View in: PubMed

  91. Smith GJ, Lee KT, Qu X, Xie Z, Pesic J, Sosnick TR, Pan T, Scherer NF. A large collapsed-state RNA can exhibit simple exponential single-molecule dynamics. J Mol Biol. 2008 May 09; 378(4):943-53. View in: PubMed

  92. Wong TN, Sosnick TR, Pan T. Folding of noncoding RNAs during transcription facilitated by pausing-induced nonnative structures. Proc Natl Acad Sci U S A. 2007 Nov 13; 104(46):17995-8000. View in: PubMed

  93. Baird NJ, Fang XW, Srividya N, Pan T, Sosnick TR. Folding of a universal ribozyme: the ribonuclease P RNA. Q Rev Biophys. 2007 May; 40(2):113-61. View in: PubMed

  94. Dai Q, Fong R, Saikia M, Stephenson D, Yu YT, Pan T, Piccirilli JA. Identification of recognition residues for ligation-based detection and quantitation of pseudouridine and N6-methyladenosine. Nucleic Acids Res. 2007; 35(18):6322-9. View in: PubMed

  95. Song XY, Yuan XM, Chen WJ, Pan T, Xie SD, Qin C, Lou C, Jin M, Wang LB, Wu JM. Different criteria for radioactive sentinel lymph nodes has different impact on sentinel node biopsy in breast cancer patients. J Surg Oncol. 2007 Jun 15; 95(8):635-9. View in: PubMed

  96. Dittmar KA, Goodenbour JM, Pan T. Tissue-specific differences in human transfer RNA expression. PLoS Genet. 2006 Dec; 2(12):e221. View in: PubMed

  97. Goodenbour JM, Pan T. Diversity of tRNA genes in eukaryotes. Nucleic Acids Res. 2006; 34(21):6137-46. View in: PubMed

  98. Saikia M, Dai Q, Decatur WA, Fournier MJ, Piccirilli JA, Pan T. A systematic, ligation-based approach to study RNA modifications. RNA. 2006 Nov; 12(11):2025-33. View in: PubMed

  99. Pan T, Sosnick T. RNA folding during transcription. Annu Rev Biophys Biomol Struct. 2006; 35:161-75. View in: PubMed

  100. Torres-Larios A, Swinger KK, Pan T, Mondragón A. Structure of ribonuclease P--a universal ribozyme. Curr Opin Struct Biol. 2006 Jun; 16(3):327-35. View in: PubMed

  101. Baird NJ, Srividya N, Krasilnikov AS, Mondragón A, Sosnick TR, Pan T. Structural basis for altering the stability of homologous RNAs from a mesophilic and a thermophilic bacterium. RNA. 2006 Apr; 12(4):598-606. View in: PubMed

  102. 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. 2005 Sep 23; 352(3):712-22. View in: PubMed

  103. Torres-Larios A, Swinger KK, Krasilnikov AS, Pan T, Mondragón A. Crystal structure of the RNA component of bacterial ribonuclease P. Nature. 2005 Sep 22; 437(7058):584-7. View in: PubMed

  104. Le TT, Harlepp S, Guet CC, Dittmar K, Emonet T, Pan T, Cluzel P. Real-time RNA profiling within a single bacterium. Proc Natl Acad Sci U S A. 2005 Jun 28; 102(26):9160-4. View in: PubMed

  105. Wong T, Sosnick TR, Pan T. Mechanistic insights on the folding of a large ribozyme during transcription. Biochemistry. 2005 May 24; 44(20):7535-42. View in: PubMed

  106. Dittmar KA, Sørensen MA, Elf J, Ehrenberg M, Pan T. Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep. 2005 Feb; 6(2):151-7. View in: PubMed

  107. Smith GJ, Sosnick TR, Scherer NF, Pan T. Efficient fluorescence labeling of a large RNA through oligonucleotide hybridization. RNA. 2005 Feb; 11(2):234-9. View in: PubMed

  108. Krasilnikov AS, Xiao Y, Pan T, Mondragón A. Basis for structural diversity in homologous RNAs. Science. 2004 Oct 01; 306(5693):104-7. View in: PubMed

  109. Sosnick TR, Pan T. Reduced contact order and RNA folding rates. J Mol Biol. 2004 Oct 01; 342(5):1359-65. View in: PubMed

  110. Wang L, Shen J, Song X, Chen W, Pan T, Zhang W, Sun X, He C, Wu J. A study of the lengthening and contractility of the surgical margins in digestive tract cancer. Am J Surg. 2004 Mar; 187(3):452-5. View in: PubMed

  111. Dittmar KA, Mobley EM, Radek AJ, Pan T. Exploring the regulation of tRNA distribution on the genomic scale. J Mol Biol. 2004 Mar 12; 337(1):31-47. View in: PubMed

  112. Barrera A, Pan T. Interaction of the Bacillus subtilis RNase P with the 30S ribosomal subunit. RNA. 2004 Mar; 10(3):482-92. View in: PubMed

  113. Song X, Wang L, Chen W, Pan T, Zhu H, Xu J, Jin M, Finley RK, Wu J. Lymphatic mapping and sentinel node biopsy in gastric cancer. Am J Surg. 2004 Feb; 187(2):270-3. View in: PubMed

  114. Xie Z, Srividya N, Sosnick TR, Pan T, Scherer NF. Single-molecule studies highlight conformational heterogeneity in the early folding steps of a large ribozyme. Proc Natl Acad Sci U S A. 2004 Jan 13; 101(2):534-9. View in: PubMed

  115. Sosnick TR, Pan T. RNA folding: models and perspectives. Curr Opin Struct Biol. 2003 Jun; 13(3):309-16. View in: PubMed

  116. Fang XW, Srividya N, Golden BL, Sosnick TR, Pan T. Stepwise conversion of a mesophilic to a thermophilic ribozyme. J Mol Biol. 2003 Jul 04; 330(2):177-83. View in: PubMed

  117. Krasilnikov AS, Yang X, Pan T, Mondragón A. Crystal structure of the specificity domain of ribonuclease P. Nature. 2003 Feb 13; 421(6924):760-4. View in: PubMed

  118. Sosnick TR, Pan T. Getting hotter with RNA. Nat Struct Biol. 2002 Nov; 9(11):795-6. View in: PubMed

  119. Barrera A, Fang X, Jacob J, Casey E, Thiyagarajan P, Pan T. Dimeric and monomeric Bacillus subtilis RNase P holoenzyme in the absence and presence of pre-tRNA substrates. Biochemistry. 2002 Oct 29; 41(43):12986-94. View in: PubMed

  120. Wang L, Song X, Chen W, Pan T, Zhang W, Sun X, He C, Wu J. [The extensibility and retractility of surgical margins in digestive tract cancer]. Zhonghua Wai Ke Za Zhi. 2002 Apr; 40(4):271-3. View in: PubMed

  121. Fang XW, Thiyagarajan P, Sosnick TR, Pan T. The rate-limiting step in the folding of a large ribozyme without kinetic traps. Proc Natl Acad Sci U S A. 2002 Jun 25; 99(13):8518-23. View in: PubMed

  122. Qin H, Sosnick TR, Pan T. Modular construction of a tertiary RNA structure: the specificity domain of the Bacillus subtilis RNase P RNA. Biochemistry. 2001 Sep 18; 40(37):11202-10. View in: PubMed

  123. Loria A, Pan T. Modular construction for function of a ribonucleoprotein enzyme: the catalytic domain of Bacillus subtilis RNase P complexed with B. subtilis RNase P protein. Nucleic Acids Res. 2001 May 01; 29(9):1892-7. View in: PubMed

  124. Shelton VM, Sosnick TR, Pan T. Altering the intermediate in the equilibrium folding of unmodified yeast tRNAPhe with monovalent and divalent cations. Biochemistry. 2001 Mar 27; 40(12):3629-38. View in: PubMed

  125. Fang XW, Golden BL, Littrell K, Shelton V, Thiyagarajan P, Pan T, Sosnick TR. The thermodynamic origin of the stability of a thermophilic ribozyme. Proc Natl Acad Sci U S A. 2001 Apr 10; 98(8):4355-60. View in: PubMed

  126. Fang XW, Yang XJ, Littrell K, Niranjanakumari S, Thiyagarajan P, Fierke CA, Sosnick TR, Pan T. The Bacillus subtilis RNase P holoenzyme contains two RNase P RNA and two RNase P protein subunits. RNA. 2001 Feb; 7(2):233-41. View in: PubMed

  127. Loria A, Pan T. The 3' substrate determinants for the catalytic efficiency of the Bacillus subtilis RNase P holoenzyme suggest autolytic processing of the RNase P RNA in vivo. RNA. 2000 Oct; 6(10):1413-22. View in: PubMed

  128. Fang X, Littrell K, Yang XJ, Henderson SJ, Siefert S, Thiyagarajan P, Pan T, Sosnick TR. Mg2+-dependent compaction and folding of yeast tRNAPhe and the catalytic domain of the B. subtilis RNase P RNA determined by small-angle X-ray scattering. Biochemistry. 2000 Sep 12; 39(36):11107-13. View in: PubMed

  129. Pan T. Probing RNA structure and function, by circular permutation. Methods Enzymol. 2000; 317:313-30. View in: PubMed

  130. Fang X, Pan T, Sosnick TR. A thermodynamic framework and cooperativity in the tertiary folding of a Mg2+-dependent ribozyme. Biochemistry. 1999 Dec 21; 38(51):16840-6. View in: PubMed

  131. Shelton VM, Sosnick TR, Pan T. Applicability of urea in the thermodynamic analysis of secondary and tertiary RNA folding. Biochemistry. 1999 Dec 21; 38(51):16831-9. View in: PubMed

  132. Fang XW, Pan T, Sosnick TR. Mg2+-dependent folding of a large ribozyme without kinetic traps. Nat Struct Biol. 1999 Dec; 6(12):1091-5. View in: PubMed

  133. Mobley EM, Pan T. Design and isolation of ribozyme-substrate pairs using RNase P-based ribozymes containing altered substrate binding sites. Nucleic Acids Res. 1999 Nov 01; 27(21):4298-304. View in: PubMed

  134. Pan T, Artsimovitch I, Fang XW, Landick R, Sosnick TR. Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proc Natl Acad Sci U S A. 1999 Aug 17; 96(17):9545-50. View in: PubMed

  135. Loria A, Pan T. The cleavage step of ribonuclease P catalysis is determined by ribozyme-substrate interactions both distal and proximal to the cleavage site. Biochemistry. 1999 Jul 06; 38(27):8612-20. View in: PubMed

  136. Pan T, Fang X, Sosnick T. Pathway modulation, circular permutation and rapid RNA folding under kinetic control. J Mol Biol. 1999 Feb 26; 286(3):721-31. View in: PubMed

  137. Loria A, Niranjanakumari S, Fierke CA, Pan T. Recognition of a pre-tRNA substrate by the Bacillus subtilis RNase P holoenzyme. Biochemistry. 1998 Nov 03; 37(44):15466-73. View in: PubMed

  138. Odell L, Huang V, Jakacka M, Pan T. Interaction of structural modules in substrate binding by the ribozyme from Bacillus subtilis RNase P. Nucleic Acids Res. 1998 Aug 15; 26(16):3717-23. View in: PubMed

  139. Pan T. Novel and variant ribozymes obtained through in vitro selection. Curr Opin Chem Biol. 1997 Jun; 1(1):17-25. View in: PubMed

  140. Loria A, Pan T. Recognition of the 5' leader and the acceptor stem of a pre-tRNA substrate by the ribozyme from Bacillus subtilis RNase P. Biochemistry. 1998 Jul 14; 37(28):10126-33. View in: PubMed

  141. Pan T, Sosnick TR. Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nat Struct Biol. 1997 Nov; 4(11):931-8. View in: PubMed

  142. Loria A, Pan T. Recognition of the T stem-loop of a pre-tRNA substrate by the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry. 1997 May 27; 36(21):6317-25. View in: PubMed

  143. Loria A, Pan T. Domain structure of the ribozyme from eubacterial ribonuclease P. RNA. 1996 Jun; 2(6):551-63. View in: PubMed

  144. Pan T, Jakacka M. Multiple substrate binding sites in the ribozyme from Bacillus subtilis RNase P. EMBO J. 1996 May 01; 15(9):2249-55. View in: PubMed

  145. Pan T, Loria A, Zhong K. Probing of tertiary interactions in RNA: 2'-hydroxyl-base contacts between the RNase P RNA and pre-tRNA. Proc Natl Acad Sci U S A. 1995 Dec 19; 92(26):12510-4. View in: PubMed

  146. Pan T. Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry. 1995 Jan 24; 34(3):902-9. View in: PubMed

  147. Pan T. Novel RNA substrates for the ribozyme from Bacillus subtilis ribonuclease P identified by in vitro selection. Biochemistry. 1995 Jul 04; 34(26):8458-64. View in: PubMed

  148. Pan T, Zhong K. Selection of circularly permuted ribozymes from Bacillus subtilis RNAse P by substrate binding. Biochemistry. 1994 Nov 29; 33(47):14207-12. View in: PubMed