Tao Pan

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.
Functional genomics, Microbiome, epitranscriptomics, RNA modification, tRNA
  • 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
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  2. [Surgical issues and managements in cochlear reimplantation in 32 children]. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2023 Mar; 37(3):218-221. View in: PubMed

  3. Structure-informed microbial population genetics elucidate selective pressures that shape protein evolution. Sci Adv. 2023 02 22; 9(8):eabq4632. View in: PubMed

  4. Single-read tRNA-seq analysis reveals coordination of tRNA modification and aminoacylation and fragmentation. Nucleic Acids Res. 2023 02 22; 51(3):e17. View in: PubMed

  5. Validation of the Chinese Translation of the "Meaning of Life" in Patients with Hearing Loss or Tinnitus. J Am Acad Audiol. 2022 Dec 10. View in: PubMed

  6. Data analysis guidelines for single-cell RNA-seq in biomedical studies and clinical applications. Mil Med Res. 2022 12 02; 9(1):68. View in: PubMed

  7. tRNA abundance, modification and fragmentation in nasopharyngeal swabs as biomarkers for COVID-19 severity. Front Cell Dev Biol. 2022; 10:999351. View in: PubMed

  8. DKK1 as a robust predictor for adjuvant platinum chemotherapy benefit in resectable pStage II-III gastric cancer. Transl Oncol. 2022 Nov 01; 27:101577. View in: PubMed

  9. Quantitative sequencing using BID-seq uncovers abundant pseudouridines in mammalian mRNA at base resolution. Nat Biotechnol. 2023 03; 41(3):344-354. View in: PubMed

  10. Epitranscriptome profiling of spleen mRNA m6A methylation reveals pathways of host responses to malaria parasite infection. Front Immunol. 2022; 13:998756. View in: PubMed

  11. Age-related endoplasmic reticulum stress represses testosterone synthesis via attenuation of the circadian clock in Leydig cells. Theriogenology. 2022 Sep 01; 189:137-149. View in: PubMed

  12. Analysis of queuosine and 2-thio tRNA modifications by high throughput sequencing. Nucleic Acids Res. 2022 09 23; 50(17):e99. View in: PubMed

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  15. Profiling Selective Packaging of Host RNA and Viral RNA Modification in SARS-CoV-2 Viral Preparations. Front Cell Dev Biol. 2022; 10:768356. View in: PubMed

  16. Long non-coding RNA ZNF674-AS1 regulates miR-23a/E-cadherin axis to suppress the migration and invasion of non-small cell lung cancer cells. Transl Cancer Res. 2021 Sep; 10(9):4116-4124. View in: PubMed

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  18. tRNA modification dynamics from individual organisms to metaepitranscriptomics of microbiomes. Mol Cell. 2022 03 03; 82(5):891-906. View in: PubMed

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

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  95. 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

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  97. 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

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  100. 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

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  102. Reversible and rapid transfer-RNA deactivation as a mechanism of translational repression in stress. PLoS Genet. 2013 Aug; 9(8):e1003767. View in: PubMed

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  104. Mitochondrial genome of Protobothrops dabieshanensis (Squamata: Viperidae: Crotalinae). Mitochondrial DNA. 2014 Oct; 25(5):337-8. View in: PubMed

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  107. A self-defeating anabolic program leads to ?-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

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  110. Function and mode of action of cytohesins in the epidermal growth factor pathway in colorectal cancer cells. Oncol Lett. 2013 Feb; 5(2):521-526. View in: PubMed

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  112. 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

  113. 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

  114. 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

  115. 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

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  118. Misacylation of tRNA with methionine in Saccharomyces cerevisiae. Nucleic Acids Res. 2012 Nov 01; 40(20):10494-506. View in: PubMed

  119. 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

  120. Meta-analysis of randomized controlled trials on laparoscopic gastrectomy vs. open gastrectomy for distal gastric cancer. Hepatogastroenterology. 2012 Sep; 59(118):1699-705. View in: PubMed

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  122. 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

  123. Rationalization and prediction of selective decoding of pseudouridine-modified nonsense and sense codons. RNA. 2012 Mar; 18(3):355-67. View in: PubMed

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  133. 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

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  138. 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

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  144. 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

  145. Efficient chemical synthesis of AppDNA by adenylation of immobilized DNA-5'-monophosphate. Org Lett. 2009 Mar 05; 11(5):1067-70. View in: PubMed

  146. 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

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  150. Folding of a universal ribozyme: the ribonuclease P RNA. Q Rev Biophys. 2007 May; 40(2):113-61. View in: PubMed

  151. 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

  152. 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

  153. Tissue-specific differences in human transfer RNA expression. PLoS Genet. 2006 Dec; 2(12):e221. View in: PubMed

  154. Diversity of tRNA genes in eukaryotes. Nucleic Acids Res. 2006; 34(21):6137-46. View in: PubMed

  155. A systematic, ligation-based approach to study RNA modifications. RNA. 2006 Nov; 12(11):2025-33. View in: PubMed

  156. RNA folding during transcription. Annu Rev Biophys Biomol Struct. 2006; 35:161-75. View in: PubMed

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