the laboratory of adp-ribosylation and rna biology...

Anthony K. L. Leung’s CV of 18

SUMMARY ABOUT DR. ANTHONY K. L. LEUNG Dr. Anthony Leung – a scientist and an inventor – is an expert in the area of RNA, ADP-ribosylation and proteomics. Dr. Leung completed his four-year Master in Biochemistry degree at the Exeter College, University of Oxford. Funded by the Croucher Scholarship from Hong Kong and Overseas Research Scheme from United Kingdom, Dr. Leung earned his Ph.D. in Biochemistry from the University of Dundee under the guidance of Dr. Angus I. Lamond. Using quantitative proteomes and imaging approaches, Dr. Leung characterized the nucleolar proteome dynamics and discovered a novel nucleolar localization pathway during his Ph.D. In 2004, Dr. Leung was awarded the Human Frontier Science Program Long-term Fellowship and, subsequently in 2007, a Special Fellowship from The Leukemia & Lymphoma Society to perform postdoctoral research on microRNAs under the mentorship of Nobel Laureate Dr. Phillip A. Sharp at MIT. In 2010, Dr. Leung hold a secondary postdoctoral appointment with Dr. Paul Chang at MIT on investigating a therapeutically important protein modification called ADP-ribosylation. Dysregulation of ADP-ribosylation metabolism results in neurodegenerative disorders, virus infection and cancer susceptibility. In 2011, Dr. Leung started his lab as an Assistant Professor in the Department of Biochemistry and Molecular Biology at Johns Hopkins University. Funded by the Idea Award from the Department of Defense Breast Cancer Research Program, Dr. Leung developed a novel non-biased technique to identify the sites of ADP-ribosylation – a technical breakthrough of the field. He was since then recognized with numerous accolades: Top 5 Agilent Early Career Professor (2013), the Inaugural Johns Hopkins Catalyst Award (2015), Research Scholar Award from the American Cancer Society (2016), and Top 10 Finalist for the American Society of Cell Biology–Gibco Emerging Leader Prize (2016). Dr. Leung has authored over 40 peer-reviewed publications, invited book chapters and review articles. Because of his expertise, Dr. Leung has been frequently invited to review for many scientific journals, serve on editorial boards, chair scientific sessions and speak at international meetings. Dr. Leung is highly collaborative on multidisciplinary projects and grants with experts in virology (Dr. Diane Griffin), oncology (Dr. Ken Pienta, Dr. Marikki Laiho, Dr. Sandra Gabelli and Dr. Sonia Franco), proteomics (Dr. Shao-En Ong and Dr. Akhilesh Pandey) and single molecule diagnostics (Dr. Al Celedon; Scanogen Inc.). In addition, Dr. Leung actively involves in patient education by initiating direct conversations between basic scientists and cancer survivors.

RESEARCH CONTRIBUTIONS BY DR. ANTHONY K. L. LEUNG 1. Created the first map of the dynamic proteome of the human nucleolus (2002–2006)

Dr. Leung’s graduate work focused on proteomic analyses of nucleolus. As part of an international team co-led by Dr. Angus Lamond, his mentor, and Dr. Matthias Mann, Dr. Leung aimed to understand how nucleolar proteome changes upon stress. This international team not only developed the first proteome map of nucleolus, but also analyzed how proteins move in and out of the nucleolus under stress. This was the first-of-its-kind proteomics study to measure the fluxes of ~500 proteins in a single experiment (a Nature top 10 article, 2005). Given the high complexity of resultant datasets, Dr. Leung led the informatics effort to analyze the compositional changes in the nucleolus. This and other informatics efforts culminated in a database, which has been continually updated and widely used in the scientific community to date (current version: http://www.peptracker.com). In addition, through characterization of the nucleolar proteome, Dr. Leung also discovered a novel nucleolar targeting pathway (a Cover


Story in Journal of Cell Biology, 2002) and analyzed how these non-membraneous RNA granules are broken down and re-formed during mitosis.

2. Defined endogenous localizations and targets of microRNA activities (2006–2011)

MicroRNAs are a large group of ~22 nucleotide-short, non-coding RNAs that regulate fundamental biological processes, including proliferation, differentiation, cell death and stress responses. As a postdoctoral fellow with Dr. Phillip Sharp, Dr. Leung discovered that, in contrary to the popular belief then, that majority of microRNA activities are in the diffuse cytoplasm, rather than in a specific class of non-membranous RNA granules called P-bodies. In addition, Dr. Leung identified a change in microRNA localization and activities upon stress conditions, leading to the discovery of novel roles of ADP-ribosylation in the cytoplasm (see section 3 below). Though thousands of human microRNAs had been identified and their gene targets predicted at that time, there were no established methods to identify bona fide targets inside cells. To tackle this challenge, Dr. Leung used biochemical methods together with next-generation sequencing to purify microRNA targets. Using mouse embryonic stem cells as a model, Dr. Leung employed informatics analyses to narrow down a highly validated set of ~300 microRNA targets, where 17 out of 18 targets were verified positive (an Article of the Month in Nature Structural and Molecular Biology, 2011). 3. Discover novel roles of ADP-ribosylation in RNA biology (2011–) ADP-ribosylation is regulated by 17 poly(ADP-ribose) polymerases (PARPs). Since its discovery in 1963, ADP-ribosylation has been implicated in regulating fundamental DNA metabolic processes, including DNA repair, transcription and maintaining chromatin structures in the nucleus. However, relatively little is known about the role of ADP-ribosylation in RNA metabolism or in the cytoplasm. Of note, ADP-ribosylation is therapeutically important as evidenced by multiple Phase III clinical trials for cancer patients on drugs that inhibit the catalytic activity of PARP-1, including two recently approved by FDA. However, many of these PARP inhibitors can cross-react with cytoplasmic PARPs. To date, functions of most human PARPs remain unclear, thus identifying their functions represents a major priority and could have strong therapeutic implications. While investigating the role of microRNAs in stress during postdoc, Dr. Leung found that the core microRNA-binding protein Argonaute is ADP-ribosylated and such ADP-ribosylation reduces microRNA activities. In addition, Dr. Leung is the first to note that ADP-ribosylation, 5 PARPs along with its degradative enzymatic counterparts are enriched in non-membranous RNA granules in the cytoplasm called stress granules (a Cover Story in Molecular Cell, 2011) . Establishing his lab at Johns Hopkins University, Dr. Leung used informatics analyses to further show that RNA granule proteins enriched for low complexity regions, which aid self-assembly, are preferentially ADP-ribosylated, indicating how ADP-ribosylation could direct cellular organization. Recently, Dr. Leung also found that a subset of RNA viruses encodes a macrodomain that removes (hydrolyzes) ADP-ribosylation. Mutants abrogating such ADP-ribosylhydrolase activity are not viable whereas mutants reducing the activity have slower replication in mammalian cells and reduced virulence in mice. The current study on RNA virus will provide an outstanding biological context to investigate the role of ADP-ribosylation in the cytoplasm. 4. Develop novel proteomics approaches to profile ADP-ribosylated proteome (2014–) Though ADP-ribosylation has been discovered for over 50 years, it has been challenging to answer mechanistic questions without knowing where the endogenous sites of modification are. Previously, ADP-ribosylation sites could only be inferred by mutagenesis, but the deficiency of ADP-ribosylation in such site-specific mutants can also be explained by secondary effects. Recently, Dr. Leung’s lab has successfully developed a non-biased proteomics approach to identify ADP-ribosylation sites at all classes of amino acids at the proteome level inside cells. By comparison with other methods developed at the same time, his method is unique in that it identifies modifications on any amino acid. Dr. Leung’s team also recently developed the first publicly available database of ADP-ribosylated proteins (http://ADPriboDB.leunglab.org) for researchers inside and outside the field to appreciate the complexity and breadth of this therapeutically important protein modification.


date revised 1/21/2017

CURRICULUM VITAE Anthony K. L. Leung

PERSONAL DATA Business Address Johns Hopkins University Bloomberg School of Public Health 615 N. Wolfe Street, E8632 Baltimore, MD 21205 Phone: 410 502-8939 Email: [email protected] URL: www.leunglab.org Facebook: www.facebook.com/leunglab EDUCATION AND TRAINING Sep 1995–May 1999 Master in Biochemistry (4-year undergraduate degree), University of Oxford, UK

Sep 1999–Mar 2003 Ph.D. in Biochemistry, University of Dundee, UK Advisor: Professor Angus I. Lamond Thesis: Proteomics and Dynamics of the Human Nucleolus

Summers 2002/2003 Visiting Scientist, European Molecular Biology Laboratory, Heidelberg, Germany

Apr 2004–Jun 2009 Postdoctoral Fellow, Laboratory of Phillip A. Sharp, Massachusetts Institute of Technology, USA

Oct–Nov 2005 Course Attendee, Immunocytochemistry, in situ hybridization and live cell imaging, Cold Spring Harbor Laboratory, USA

Jul 2009–Jun 2010 Senior Postdoctoral Fellow, Laboratory of Phillip A. Sharp, Massachusetts Institute of Technology, USA with a secondary appointment at the laboratory of Paul Chang, MIT since Jan 2010

Jul 2010–Jan 2011 Research Scientist, Laboratory of Phillip A. Sharp, Massachusetts Institute of Technology, USA

PROFESSIONAL EXPERIENCE 2011– Assistant Professor, Johns Hopkins University, Bloomberg School of Public Health

(JHSPH), Department of Biochemistry and Molecular Biology (BMB)

2011– Preceptor, predoctoral training program in Cancer Research (T32CA009110–39), Bloomberg School of Public Health, Johns Hopkins University

2011– Affiliate Member, McKusick-Nathans Institute of Genetic Medicine (IGM), Johns Hopkins School of Medicine (JHSOM)

2011– Preceptor, predoctoral training program in Human Genetics (T32GM007814–35), JHSOM

2015– Assistant Professor of Oncology, School of Medicine, Johns Hopkins University, Baltimore Maryland

2015– Member, Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins


2015– Preceptor, pre-doctoral training program in Chemistry–Biology Interface (CBI, T32GM080189–09), Johns Hopkins University

PROFESSIONAL ACTIVITIES Society Memberships: RNA Society American Society of Cell Biology Invited activities: Plenary Luncheon Seminar, RNA meeting 2011 Kyoto, Japan

Lecturer in continuing education course on “MicroRNA Functions in Stress Responses” in the Society of Toxicology, Annual Meeting, March 2012, San Francisco, California

Lecturer in continuing education course on “MicroRNA Functions”, Teratology Society, Annual Meeting, June 2012, Baltimore, Maryland

Keynote Speaker, Genomics 2013, Boston, Massachusetts

Session Chair on NAD+ metabolism, FASEB Meeting "NAD+ Metabolism and Signalling 2015”, Germany.

Invited Speaker, Cold Spring Harbor Laboratory meeting on the PARP Family and ADP-ribosylation, USA (2016).

Session Chair on NAD+ metabolism, FASEB Meeting "NAD+ Metabolism and Signalling 2017”, USA.

Co-organizer, Workshop on the Biology, Chemistry and Physics of non-membranous granules at Johns Hopkins (with Drs. Taekjip Ha and Takanari Inoue)

EDITORIAL ACTIVITIES 2014– Member, Editorial Board Scientific Reports (Nature Publishing group) 2011– Member, Editorial Board

Frontiers in Genetics (Nature Publishing group) 2011– Manuscript Reviewer (number of manuscripts) - Molecular Cell (33 since 2011) Nucleic Acids Research (1 since 2011) PLOS Genetics (1 since 2012) BMC Genomics (1 since 2012) EMBO Journal (2 since 2012) Journal of Cell Biology (2 since 2013) Cell Report (2 since 2014) PLOS Biology (1 since 2014) Nature Communications (2 since 2015) Bioorganic and Medicinal Chemistry Letters (1 since 2015) Scientific Reports (4 since 2015) Nature Chemical Biology (3 since 2015) PLOS Pathogen (1 since 2015) Journal of Proteomics (2 since 2015)


Molecular and Cellular Biology (1 since 2016) FEBS Journal (2 since 2016) Nature Protocol (2 since 2016)

2011 Textbook Manuscript Reviewer on Chapter 11: Protein Modification and Targeting

Molecular Biology: Principles of Genome Function (2nd edition), by Nancy Craig, Orna Cohen-Fix, Rachel Green, Carol Greider, Gisela Storz, and Cynthia Wolberger Oxford University Press (ISBN: 978-0-19-956206-0)

Ad Hoc Grant Reviewer for

Chinese University of Hong Kong (2005), Royal Society, United Kingdom (2006), Human Frontier Science Program (2014). Netherlands Organisation for Scientific Research (NWO) (2015, 2016) Biotechnology and Biological Sciences Research Council (BBSRC), United Kingdom (2015) National Science Center (Narodowe Centrum Nauki), Poland (2016) Israel Science Foundation, Israel (2016) Health and Medical Research Fund from The Government of the Hong Kong Special Administrative Region (HKSAR) (2016)

Poster judge for the 9th Frontiers in Chemistry and Biology Interface Symposium, Baltimore, MD (2016) Poster judge for the 12th Annual Retreat for Johns Hopkins Chemistry–Biology Interface Graduate Program (2016) HONORS AND AWARDS

2016 Top 10 Finalist, American Society of Cell Biology (ASCB)–Gibco Emerging Leader Prize

2016 American Cancer Society Research Scholar Award

2015 Inaugural Johns Hopkins Catalyst Award

2013–2014 Faculty Innovation Award, Johns Hopkins Bloomberg School of Public Health

2013 Top 5 Finalist, Agilent Early Career Professor Award

2011–2013 Idea Award, Department of Defense Breast Cancer Research Program

2007–2010 Special Fellowship, The Leukemia & Lymphoma Society

2004–2007 Long-term Fellowship, Human Frontier Science Program

Jul–Aug 2003 Travelling Fellowship, Journal of Cell Science, Company of Biologist Limited

Jun–Jul 2002 European Advanced Light Microscopy Facility Fellowship, EMBL Heidelberg, Germany

1999–2002 Scholarship, Croucher Foundation, Hong Kong

1999–2002 Overseas Research Scheme Award, UK

1995–1999 Waugh Scholarship, University of Oxford, UK

1995–1999 Fitzgerald Prize, University of Oxford, UK

Awards for Leung Lab members

2016 John Scocca Achievement Award to PhD student, Casey Daniels, for excellence in bench research on the part of a PhD student in the Department of Biochemistry and Molecular Biology, JHSPH.


2015 Joy Cappel Young Investigator Award from the Rockland Immunochemicals Inc. to Postdoctoral Fellow, Dr. Hyunju Ryu. Winners have been selected based on their commitment and contributions to innovative and collaborative scientific achievements and advances in the life sciences for promising post-doctoral fellows and graduate students.

2015 Journal of Cell Science Travelling Fellowship to PhD student, Lyle McPherson.

2015 Postdoctoral Fellow Dr. Yoshinari Ando was awarded a Traveling Fellowship, 20th Annual Meeting, RNA Society (2015).

2014 Joy Cappel Young Investigator Award from the Rockland Immunochemicals Inc. to PhD student, Casey Daniels.

2014 Elsa Orent Keiles Fellowship in Biochemistry to PhD student, Casey Daniels. The fellowship is to recognize a PhD student who has performed admirably in the academic and research programs of the department of Biochemistry and Molecular Biology, JHSPH, and sets an example for his/her fellow students. One student is selected to receive this award each year.

2013 Postdoctoral Fellow Dr. Yoshinari Ando was awarded a Travel Grant Award to attend 36th Annual Meeting of the Molecular Biology Society of Japan.

2013 PhD student Casey Daniels attended Proteomics Course in Cold Spring Harbor Laboratory with scholarship support.

2012 Journal of Cell Science Travelling Fellowship to PhD student, Casey Daniels.

PUBLICATIONS Peer-reviewed Journal Articles * indicates corresponding authorship; #indicates co-first authorship; underlined indicates other Leung Lab member Publications cited at least 10 times (as of January 21st, 2017) are denoted below. Detailed citation information can be found (Citation: 4721; h-index=24): https://scholar.google.com/citations?user=h_vjSXoAAAAJ&hl=en

1. McPherson, R.L.#, Abraham, R.#, Sreekumar, E.#, Ong, S.E., Cheng, S.J., Baxter, V., Kistemaker, H.A.V., Filippov, D.V., Griffin, D.E.*, Leung, A.K.* ADP-ribosylhydrolase activity of macrodomain is required for Chikungunya viral replication. PNAS, in press.

2. Fischer, J., Leung, A.K.* CircRNAs: A Regulator Of Cellular Stress. Critical Review in Biochemistry and Molecular Biology, in press.

3. Daniels, C.M., Ong, S. E., and Leung, A.K.* ADP-ribosylated peptide enrichment and site identification: The phosphodiesterase based method. Methods in Molecular Biology, in press.

4. Vivelo, C.A. #, Wat R. #, Agrawal C., Tee H.Y., and Leung, A. K.* ADPriboDB: The Database of ADP-ribosylated Proteins. Nucleic Acids Research 2016; DOI: 10.1093/nar/gkw706 http://ADPriboDB.leunglab.org/

5. Palazzo, L. #, Daniels, C.M. #, Nettleship J.E., Rahman, N., McPherson R. L., Ong, S.E., Kato, K., Nureki, O., Leung, A.K.* and Ahel, I*. ENPP1 processes protein ADP-ribosylation in vitro. FEBS. J. 2016; 283(18):3371–88.

6. Hwang T., Park C.K., Leung A.K., Gao Y., Hyde T.M., Kleinman J.E., Rajpurohit N., Tao, R., Shin J.H., Weinberger D.R. Dynamic regulation of RNA editing in human brain development and disease. Nature Neuroscience 2016; 19(8):1093–9.


7. McPherson, R.L. and Leung A.K.*. ADPr-ChAP: Mapping ADP-Ribosylation onto the Genome. Mol Cell. 2016 Feb 4;61(3):327-8.

8. Fan A.C. and Leung A.K.* RNA Granules and Diseases — A Case Study of Stress Granules in ALS and FTLD. Adv Exp Med Biol 2016; 907:263–96.

9. Daniels, C.M., Thirawatananond, P., Ong, S.E.*, Gabelli, S.B.* and Leung, A.K.* Nudix hydrolases degrade protein-conjugated ADP-ribose. Sci Rep. 2015; 5:18271.

10. Leung A.K.* The Whereabouts of MicroRNA Actions: Cytoplasm and Beyond. Trends Cell Biol. 2015; 25:601-610. (cited 18 times)

11. Daniels C.M., Ong S.E., Leung A.K.* 2015 The Promise of Proteomics for the Study of ADP-Ribosylation. Mol Cell. 58(6):911-24. (cited 28 times)

12. Ando, Y. and Leung, A.K.* 2015. Methods for studying microRNA functions during stress. Methods Mol Biol 1292:115-28

13. Vivelo C.A., Leung A.K.* 2015 Proteomics approaches to identify mono-(ADP-ribosyl)ated and poly(ADP-ribosyl)ated proteins. Proteomics. 15(2-3):203-17.

14. Daniels, C.M., Ong, S. E.*, and Leung, A.K.* 2014. Phosphoproteomic Approach to Characterize Protein Mono- and Poly(ADP-ribosyl)ation Sites from Cells. J Proteome Res. 13:3510-22. (cited 36 times)

15. Leung, A.K.* 2014. Poly(ADP-ribose): An organizer of cellular architecture. J. Cell Biol. 205:613-9. (cited 39 times)

16. Ando, Y. and Leung, A.K.* 2013. Does an emergency visit to the ER make microRNAs stronger during stress. Mol. Cell, 52: 1-3.

17. Leung, A.K.* and Sharp, P.A. 2013. Quantifying Argonaute in and out of GW/P-bodies: Implication in microRNA silencing. Adv Exp Med Biol. 768:165-182. (cited 26 times)

18. Leung, A.K.*, Todorova, T., Ando Y. and Chang P. 2012. Poly(ADP-ribose) regulates post-transcriptional gene regulation in the cytoplasm. RNA Biol. 9(5): 542-548. (cited 36 times)

19. Leung, A.K., Vyas, S., Rood, J.E., Bhutkar, A.J., Sharp, P.A. and Chang, P. 2011. Poly(ADP-ribose) Regulates microRNA activity and stress responses in the Cytoplasm. Mol Cell 42:489-99. (cited 164 times)

20. Rood, J.E., Leung, A.K. and Chang, P. 2011 Strategies for purification of proteins associated with cellular poly(ADP-ribose) and PARP-specific poly(ADP-ribose). Methods in Molecular Biology 780:153-164.

21. Leung, A.K. #, Young, G.A. #, Bhutkar, A.J. Zheng, G.X. and Sharp, P.A. 2011. Genomewide Identification of Endogenous Argonaute Binding sites in Mouse Embryonic Stem Cells with and without Mature microRNAs. Nature Struct. Mol. Biol. 18:237-44. (cited 174 times)

22. Leung, A.K. and Sharp, P.A. 2010. MicroRNA Functions in Stress Responses. Mol Cell 40:205-15. (cited 427 times)

23. Singh, N., Agrawal, A., Leung, A.K., Sharp, P.A. and Bhatia, S. 2010. Effect of nanoparticle conjugation on gene silencing by RNA interference. J Am Chem Soc 132(24):8241-3. (cited 67 times)

24. Dafik, L., Kalsani, V., Leung, A.K., and Kumar, K. 2009. Fluorinated lipids permit facile passage of macromolecules into living cells. J Am Chem Soc 131(34):12091-3. (cited 17 times)

25. Leung, A.K. and Sharp, P.A. 2007. microRNAs: A safeguard against Turmoil? Cell 130:581-5. (cited 197 times)

26. Leung, A.K. and Sharp, P.A. 2006. Function and Localization of microRNAs in mammalian cells. Cold Spring Harb Symp Quant Biol 71:29-38. (cited 71 times)


27. Leung, A.K., Calabrese, M.J., and Sharp, P.A. 2006. Quantitative analysis of Argonaute protein reveals microRNA-dependent Localisation to Stress Granules. Proc Natl Acad Sci USA 103:18125-30. (cited 293 times)

28. Leung, A.K., Trinkle-Mulcahy, L., Lam, Y.W., Andersen, J.S., Mann, M., and Lamond, A.I. 2006. NOPdb: Nucleolar Proteome Database. Nucleic Acids Res 34 (Database issue): D218-220. (cited 97 times)

29. Andersen, J.S., Lam, Y.W., Leung, A.K., Ong, S.E., Lyon, C.E., Lamond, A.I., and Mann, M. 2005. Nucleolar proteome dynamics. Nature 433(7021):77-83. (cited 946 times)

30. Chen, D., Dundr, M., Wang, C., Leung, A., Lamond, A., Misteli, T., and Huang, S. 2005. Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J Cell Biol 168(1):41-54. (cited 170 times)

31. Leung, A.K., Gerlich, D., Miller, G., Lyon, C., Lam, Y.W., Lleres, D., Daigle, N., Zomerdijk, J., Ellenberg, J., and Lamond, A.I. 2004. Quantitative kinetic analysis of nucleolar breakdown and reassembly during mitosis in live human cells. J Cell Biol 166(6):787-800. (cited 142 times)

32. Leung A.K. and Lamond A.I. 2003 The Dynamics of the Nucleolus. Crit Rev Eukaryot Gene Expr 14:39-54. (cited 85 times)

33. Leung, A.K., Andersen, J.S., Mann, M., and Lamond, A.I. 2003. Bioinformatic analysis of the nucleolus. Biochem J 376(Pt 3):553-569. (cited 157 times)

34. Leung, A.K. and Lamond AI. 2002. In vivo analysis of NHPX reveals a novel nucleolar localization pathway involving a transient accumulation in splicing speckles. J Cell Biol 157:615-29. (cited 59 times)

35. Oeffinger, M., Leung, A., Lamond, A., Tollervey, D. 2002. Yeast Pescadillo is required for multiple activities during 60S ribosomal subunit synthesis. RNA 8:626-36. (cited 75 times)

36. Fox, A.H., Lam, Y.W., Leung, A.K., Lyon, C.E., Andersen, J., Mann, M., Lamond A.I. 2002. Paraspeckles: A novel nuclear domain. Curr Biol 12:13-25. (cited 322 times)

37. Andersen, J.S., Lyon, C.E., Fox, A.H., Leung, A.K., Lam, Y.W., Steen, H., Mann, M., and Lamond, A.I. 2002. Directed proteomic analysis of the human nucleolus. Curr Biol 12(1): 1-11. (cited 930 times)

38. Kolatkar, A.R., Leung, A.K., Isecke, R., Brossmer, R., Drickamer, K., Weis W.I. 1998. Mechanism of N-acetylgalactosamine binding to a C-type animal lectin carbohydrate recognition domain. J Biol Chem 273:19502-8. (cited 88 times)

Manuscript in Submission

1. Wu Y.C., Zhang T., Mullane P., He L., Hwang H-Y., Periz G., Wang, H., Shorter J., Ong S.E., Leung A.K.*, Wang J.* FUS/TLS regulates microRNA-mediated silencing. Under revision to Nature Communications.

2. Das S.*, Kohr M., Dunkerly B., Bedja D., Kent O.A., Leung, A.K., Henao-Mejia J., Henao-Mejia, J., Flavell R.A. and Steenbergen C. Role of miR-181 Family in the Heart: A Tale of Two Intracellular Compartments. Submitted to Journal of the American Heart Association.

Book Chapters

1. Leung, A.K.* MicroRNA Functions in Stress Responses. Continued Education Coursebook for the Society of Toxicology. (2012)

2. Leung, A.K.* Overview of microRNAs in Toxicology and Human Diseases. Continued Education Coursebook for the Teratology Society. (2012)


3. Lam, Y.W., Fox, A.H., Leung, A.K., Andersen, J., Mann, M. and Lamond, A.I. Nucleolar Proteomics. The Nucleolus. Olson, Mark O.J. (Ed) Landes Bioscience.

Patents

1. Methods and Compositions for increasing the activity of inhibitory RNA US 2011/0097328 A1

2. Compositions and Methods for treating cancer and modulating stress granule formation. US 2013/0156776 A1

3. The Use of Escherichia Coli RppH to Identify ADP-ribosylated Sites by Mass Spectrometry. Provisional patent US 62/173,554


CURRICULUM VITAE Anthony K. L. Leung

PART II

Student Advisement in Research Casey M. Daniels PhD Candidate, 06/11–08/15

Thesis Title: Characterization of the ADP-ribosylated Proteome by Mass Spectrometry Currently, Postdoctoral Fellow with Dr. Aleksandra Nita-Lazar at NIAID

Christina Vivelo PhD Candidate, 06/13–Current Lyle McPherson PhD Student, 04/15–Current Joe Fischer PhD Student, 06/15–Current Jennifer A. Pak ScM Candidate, 06/11–01/12 Ryan Weltzer ScM Candidate, 07/12–10/13 Haobo Wang MHS/ScM Candidate, 09/14–08/16 Jayson Baman MD Candidate, University of Rochester, 06/14–08/14

- supported via Offices for Medical Education Summer Research Fund, University of Rochester Medical Center

Ricky Wat MPH Candidate, Johns Hopkins University, Bloomberg School of Public Health, 09/15–06/16

Shang-Jung Cheng MHS/ScM Candidate, 01/16–Current Jerome Yu BSc Candidate, Fudan University, China, 06/14–08/14 Charul Agrawal BSc Candidate, Indian Institute of Technology, Delhi

- supported via Khorana Scholarship program, 05/15–07/15 Alexander Fan BSc Candidate (Bioengineering), University of Colorado, Boulder, 05/14–08/14 Hui Yi Tee BSc Candidate, Johns Hopkins University 11/14–Current Christine Shen Grade 12 High School student (Marriott Ridge High School, MD)

07/13–08/13 Postdoctoral Fellow Advisement Yoshinari Ando 09/11–Current Naoki Hida 08/12–04/13, currently Assistant Specialist, UC Merced. Hyunju Hyu 06/14–Current Aravinth Jayabalan 10/16–Current PhD rotation students JHSPH BMB: Hongfan Chen (2011), Casey Daniels (2011), Chynna Broxton (2011), Xin Sun (2012), Abigail Zieman (2012), Christina Vivelo (2013), Hana Odeh (2013), Pola Olczak (2014), Yajuan Guo (2014), Tianlu Ma (2014), Lyle McPherson (2015), Ed Culbertson (2015), Danielle Bouchard (2016) JHSOM IGM: Donghui Li (2012), Simeon Springer (2013), Joe Fischer (2015) JHU CBI: Morgan Dasovich (2016) Student Advisement in Teaching MHS Thesis advisor Aditi Kantipuly MHS Candidate, 12/13–04/14 Hema Chagarlamudi MHS Candidate, 12/14–04/15 Stephanie Owusu MHS Candidate, 12/14–04/15 Deasty Imara MHS Candidate, 12/15–04/16


Shae Rowlandson MHS Candidate, 12/15–04/16 Alex Cole MHS Candidate, 12/16–Current Amanda Lourenco MHS Candidate, 12/16–Current Balaganesh Natarajan MHS Candidate, 12/16–Current Bryanna Stukes MHS Candidate, 12/16–Current MHS advisor Joseph Shen MHS Candidate, 09/15–06/16 Megan Fong MHS Candidate, 09/15–06/16 Megyin Chen MHS Candidate, 09/16–Current Jingting Han MHS Candidate, 09/16–Current Esteban Urias MHS Candidate, 09/16–Current MHS Thesis reader Anthony Chen (BMB, JHSPH, 2011) Ryan Weltzer (BMB, JHSPH, 2012) Haobo Wang (BMB, JHSPH, 2015) Joseph Shen (BMB, JHSPH, 2016) Kaylin Gozalez (BMB, JHSPH, 2016) ScM Thesis reader Grace Hwang (BMB, 2012) Advisor: Daniela Drummond-Barbosa Mridula Balakrishnan (BMB, 2012) Advisor: Fengyi Wan CBI Project Proposal Reader Pinaki Bose (2015) Advisor: Heng Zhu Zach Mazanek (2016) Advisor: Jungsan Sohn Preliminary Oral Participation 1st Thesis Proposal Committee, BMB, JHSPH Daisy Colon-Lopez Exam Committee Member (2011) Advisor: Jürgen Bosch Shaina L. Palmere Exam Committee Member (2011) Advisor: Daniela Drummond-Barbosa Xin Sun Exam Committee Member (2012) Advisor: Fengyi Wan General Board Exam, BMB, JHSPH Shaina L. Palmere Exam Committee Member (2012) Advisor: Daniela Drummond-Barbosa Shuo Li Exam Committee Member (2016) Advisor: Elizabeth Chen General Board Exam, CBI, JHU Zach Mazanek Exam Committee Member (Alternative, 2016)

Advisor: Jungsan Sohn Project Proposal Exam, CBI, JHU Zach Mazanek Exam Committee Member (2016) Advisor: Jungsan Sohn Preliminary school wide exam Alyssa Frazee Exam Committee Member (2012) Advisor: Jeff Leek


Comprehensive Exam in Institute of Genetic Medicine, JHSOM Melissa Lee Exam Committee Member (2012) Advisor: Garry Cutting Jane Welch Exam Committee Member (2013) Advisor: Sarah Wheelan and

Kathleen Burn Jing You Exam Committee Member (2014) Advisor: Dave Valle Hannah Edelman Exam Committee Member (2015) Advisor: Andrew McCallion Sarah Robbins Exam Committee Member (2016) Advisor: Dave Valle Thesis Committee Member Institute of Genetic Medicine, JHSOM Tyler Creamer 2014–2015 Advisor: Dan Warren Joseph Tilghman 2016–Current Advisor: Aravinda Chakravarti Department of Biomedical Engineering, JHSOM Taeyoung Hwang 2014–2016 Advisor: Daniel Weinberger Department of Pathology, JHSOM Youngran Park 2016–Current Advisors: Tian-Li Wang and Ie-Ming Shih Chemistry–Biology Interface, JHU Sabrina Schatzman 2016–Current Advisor: Val Culotta Ryan Porell 2017–Current Advisor: Ron Schnaar Department of Biochemistry and Molecular Biology, JHSPH Elizabeth Alexander 2016–Current Advisor: Jiou Wang Stephen Wellard 2017–Current Advisor: Phil Jordan Final Thesis Defense/Reader Department of Biostatistics, JHSPH Samara Kiihl Exam Committee Member (2012) Advisor: Rafael Irizarry Alyssa Frazee Exam Committee Member (2014) Advisor: Jeff Leek Department of Environmental Health, JHSPH Suengwon Lee Exam Committee Member (2014) Advisor: James Sham Tyna Dao Exam Committee Member (2015) Advisor: Winnie Tang Department of Biomedical Engineering, JHSOM Taeyoung Hwang Exam Committee Member (2016) Advisor: Daniel Weinberger Classroom Instruction 2016– Lecturer, Molecular Toxicology (JHSPH, 187.632.01)

2016– Lecturer, CBI core course II (JHU cross departmental PhD program)

2014– Co-director, Introduction to Molecular Biology (JHSPH, 120.602.01)

2014 Lecturer, Molecular Mechanism of Disease (JHSOM, ME 710.702)

2013– Lecturer, Molecular Biology of Cellular Stress and Quality Control (JHSPH, 120.606.01)

2013– Lecturer, Introduction to Molecular Biology (JHSPH, 120.602.01)


2011– Faculty Leader, Core Research Literature (JHSPH, 120.852.01)

2011– Lecturer, Current Topics in BMB (JHSPH, 120.872.01)

2011– Lecturer, Advanced Topics in Human Genetics (JHSOM)

RESEARCH GRANT PARTICIPATION (i) Current 07/01/16–06/30/20 Increase microRNA activities by inhibiting poly(ADP-ribose) polymerases Research Scholar Award

Sponsor: American Cancer Society Principal Investigator: Leung, AKL

Effort: 25% The main goal of this project is to study the role of PARylation in microRNA

binding protein argonaute in breast cancer.

03/01/15–02/29/20 Post-transcriptional Gene Regulation by Cytoplasmic Poly(ADP-ribose)

polymerases R01GM104135

Sponsor: NIH/NIGMS Principal Investigator: Leung, AKL Effort: 50%

The main goal of this project is to study the role of PARylation in microRNA binding protein argonaute in virus infection.

09/01/15–08/31/17 Post-transcriptional Gene Regulation by Cytoplasmic Poly(ADP-ribose)

polymerases (Diversity Supplement) R01GM104135-S1 Sponsor: NIH/NIGMS Principal Investigator: Leung, AKL

This is a supplement for training a graduate student from under-represented minority.

04/01/15–03/31/17 Using PARylation Signature to Identify Prostate Cancer sensitive to PARP

inhibitor Pilot grant

Sponsor: Patrick C. Walsh Cancer Research Fund Principal Investigator: Leung, AKL

Effort: 5% The main goal of this project is to use a novel proteomics technique to identify biomarker for PARP inhibitors in prostate cancers.

04/01/15–03/31/17 Nucleolus: a novel paradigm for PARP1/2 functions and clinical application

Pilot grant Sponsor: Johns Hopkins–Allegheny Health Network Cancer Institute Principal Investigator: Laiho, M

Role: Co-Principal Investigator; Effort: 5% The main goal of this project is to use a novel proteomics technique to identify PARylation substrates in the nucleolus.


04/01/16–03/31/17 Fourier transform Orbitrap Fusion Lumos tribrid mass spectrometer with

ETD S10OD021844 Sponsor: National Institute of Health Principal Investigator: Akhilesh Pandey Role: Co-I The main goal of this project is to obtain a new Orbitrap Fusion Lumos tribrid mass

spectrometer with ETD to Johns Hopkins 01/15/16–01/14/17 The role of nsP3 in neurovirulence of chikungunya virus Pilot grant Sponsor: The Sherrilyn and Ken Fisher Center for Environmental Infectious

Diseases Discovery Program, Johns Hopkins University Principal Investigator: Griffin, DE Role: Co-I The main goal of this project is to identify the role of nsP3 in neurovirulence of

chikungunya virus. 07/01/15–12/31/16 A Novel Proteomics Approach for Characterizing Macrodomain—A Potential

Antiviral Drug Target Catalyst Award Sponsor: Johns Hopkins University Principal Investigator: Leung, AKL Effort: 5% The main goal of this project is to investigate the role of macrodomain in Sindbis

Virus

(ii) Previous Grants/Contracts 08/01/11–07/31/13 The Role of Poly(ADP-ribose) in microRNA activity in Breast Cancers Idea Award BC101881 Sponsor: Department of Defense Breast Cancer Research Program

Principal Investigator: Leung, AKL Effort: 20% The main goal of this project is to identify how AGO2 PARylation is dysregulated in

breast cancer cells through development of novel proteomics tools. 01/01/2013–12/31/2013 Designing inhibitors against PARP-12 – a member of a novel poly(ADP-

ribose) polymerase family subclass Translational Research Award

Sponsor: Johns Hopkins Medical Institute Brain Science Institute Principal Investigator: Leung, AKL

Effort: 5% The main goal of this project is to develop inhibitor against mono(ADP-

ribosyl)transferase PARP-12 05/01/2013–04/30/2014 Circulating RNAs as Trans-generational Gene Regulators and Disease

Biomarkers Faculty Innovation Award


Sponsor: Johns Hopkins Bloomberg School of Public Health Principal Investigator: Leung, AKL

Effort: 5% The main goal of this project is to profile circulating RNAs in fetal cord blood samples

09/1/2013–08/31/2014 Understanding the mechanism of poly(ADP-ribosyl)ation-regulated

ubiquitination Pilot grant Sponsor: Johns Hopkins Tech Center for Networks and Pathways derived from

U54–GM103520 Principal Investigator: Leung, AKL

Effort: 5% The main goal of this project is to identify the ubiquitinated proteome and quantitatively compare the proteomes in various conditions when poly(ADP-ribose) level is altered.

07/01/14–06/30/15 Novel Proteomics Approaches to Identify Breast Cancer Patients Responsive

to PARP inhibitors Pilot grant Sponsor: Safeway Research Foundation Principal Investigator: Leung, AKL

Effort: 5% The main goal of this project is to use a novel proteomics technique to identify biomarker for PARP inhibitors in breast cancers.

07/01/15–06/30/16 Novel Circular Supercoiling Biosensors for MicroRNA detection R43HG008709

Sponsor: NIH/SBIR Principal Investigator: Celedon, A Role: Co-Investigator; Effort=1.6%

The main goal of this project is to develop novel tools to identify microRNAs from cancer cells.

ACADEMIC SERVICE Department of Biochemistry and Molecular Biology 2012, 2016 Speaker, University of Maryland Baltimore County–Meyerhoff Bridge Day to promote science

amongst undergraduate minority students

2014– Chair, Online Communications Committee. Portfolio includes department website, PhD program website (www.jhu-bmb-phd.org) and e-newsletter.

2015– Member, Curriculum Revision Committee

2015 Ad hoc Member, Sharon Krag Achievement Award Committee

2016– Member, Curriculum Committee

2016 Ad hoc Member, PhD recruitment Committee

2016 Speaker, BMB PhD program recruitment

2017 Ad hoc Member, Sharon Krag, John Scocca and Larry Grossman Achievement Award Committee


Johns Hopkins Bloomberg School of Public Health 2016– Member, Focus group in reforming PhD education

2016–2018 Elected Faculty Senator

Johns Hopkins University 2015 Member, Core-In-A-Box Workgroup – a taskforce to reform the core facilities across the

University

2016 Reviewer, Provost’s Undergraduate Research Award (PURA)

INVITED PRESENTATION 65. Aug 2017 Session Chair and Invited Speaker, FASEB Meeting “NAD+ Metabolism and Signalling

2017”, Miami, USA (scheduled)

64. Jun 2017 Invited Speaker, University of Maryland Baltimore RNA Interest Group, Baltimore, Maryland, USA (scheduled)

63. Feb 2017 Invited Speaker, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Translational Research Conference, Baltimore, Maryland, USA (scheduled)

62. Jan 2017 Invited Speaker, Ribon Therapeutics, Inc., Lexington, Massachusetts, USA (scheduled)

61. Dec 2016 Invited Speaker, The Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Breast Cancer Tumor Board, Baltimore, Maryland, USA (scheduled)

60. Nov 2016 Student invited seminar, Catholic University of America, Washington D.C., USA (scheduled)

59. Oct 2016 Invited Speaker, 11th Annual Johns Hopkins Prostate Research Day, Baltimore, Maryland, USA

58. Oct 2016 Invited Discussant, Nutritional Genomics and Public Health Lectures, Johns Hopkins School of Public Health, Baltimore, Maryland, USA

57. Sep 2016 Invited Speaker, University of Pennsylvania, Department of Biochemistry and Biophysics, Philadelphia, Pennsylvania, USA

56. Sep 2016 Co-organizer and Session leader, Johns Hopkins University, Biology, Chemistry and Physics of Non-membranous Granules at Johns Hopkins, Baltimore, Maryland, USA

55. Jun 2016 Invited Speaker, Meyerhoff Bridge Day, Baltimore, Maryland, USA

54. Jun 2016 Invited Speaker, National Cancer Institute, Center for Cancer Research RNA seminar Series, Frederick, Maryland, USA

53. Apr 2016 Invited Speaker, Cold Spring Harbor Laboratory Meeting, The PARP Family & ADP-ribosylation, Cold Spring Harbor, New York, USA

52. Mar 2016 Invited Speaker, Johns Hopkins University, Chemistry–Biology Interface Forum, Baltimore, Maryland, USA

51. Feb 2016 Invited Speaker, Johns Hopkins University, Department of Biochemistry and Molecular Biology, PhD recruitment Program, Baltimore Maryland, USA

50. Nov 2015 Invited Speaker, Johns Hopkins University School of Medicine, Department of Radiation Oncology and Molecular Radiation Sciences, Baltimore, USA

49. Nov 2015 Invited Speaker, National Cancer Institute, Bethesda, Maryland, USA


48. Sep 2015 Invited Speaker, Johns Hopkins University, Bloomberg School of Public Health, Department of Biochemistry and Molecular Biology Maryland, USA

47. Sep 2015 Invited Speaker, Johns Hopkins Breast Cancer Survivorship Program, Maryland USA

46. Aug 2015 Session Chair and Invited Speaker, FASEB Meeting "NAD+ Metabolism and Signalling 2015”, Germany

45. Jul 2015 Fellow invited seminar, National Institute of Aging, Bayview Campus, Maryland, USA

44. Jun 2015 Invited Speaker, Penn State College of Medicine, Hershey, Pennsylvania, USA

43. May 2015 Invited Speaker, 8th Annual Safeway Breast Cancer Research Retreat, Baltimore, Maryland, USA

42. May 2015 Invited Speaker, RNAi/MicroRNAs-Boston-2015 Meeting, Boston, Massachusetts, USA

41. June 2014 Invited Speaker, 1st symposium on stress-associated RNA granules, Halifax, Canada.

40. April 2014 Invited Speaker, Inaugural Cold Spring Harbor Laboratory Meeting, The PARP Family & Friends: Gene Regulation and Beyond, Cold Spring Harbor, New York, USA

39. Mar 2014 Student invited seminar, Baltimore Life Scientists Association, Baltimore, Maryland, USA

38. Mar 2014 Invited Speaker, Johns Hopkins University, Breast Cancer Program Translational Research Seminar Series, Baltimore, Maryland, USA

37. Mar 2014 Invited Speaker, Baltimore Area repair Symposium, co-organized by Johns Hopkins University, University of Maryland and National Institute of Aging.

36. Sep 2013 Invited Speaker, PARP2013, 50th anniversary meeting for the discovery of poly(ADP-ribose), Quebec, Canada.

35. Jun 2013 Invited Speaker, Johns Hopkins University School of Medicine, Tech Center for Networks and Pathways, Baltimore, USA

34. May 2013 Keynote Speaker, Genomics Research 2013, Boston, Massachusetts, USA

33. Mar 2013 Invited Speaker, Johns Hopkins University School of Medicine, Department of Molecular and Comparative Pathobiology, Baltimore, USA

32. Jan 2013 Invited Speaker, Carnegie Institute for Science, Baltimore, Maryland, USA

31. Jun 2012 Invited Speaker, Meyerhoff Bridge Day, Baltimore, Maryland, USA

30. Jun 2012 Invited Lecturer, 52nd Annual meeting Teratology Society, Baltimore, Maryland, USA

Lecturer in continuing education course on “MicroRNA Functions in Stress Responses”

29. May 2012 Invited Speaker, University of Maryland, College Park, Maryland, USA

28. May 2012 Invited Speaker, National Institutes of Health, Bethesda, Maryland, USA

27. Apr 2012 Invited Speaker, Genomics Research 2012, Boston, Massachusetts, USA

26. Apr 2012 Invited Speaker, Johns Hopkins University School of Medicine, Department of Biological Chemistry, Baltimore, USA

25. Apr 2012 Invited Speaker, Johns Hopkins University School of Medicine, Brain Science Institute, Baltimore, USA

24. Mar 2012 Invited Lecturer, 51st Annual meeting of Society of Toxicology, San Francisco, California, USA. Lecturer in continuing education course on “MicroRNA Functions”

23. Mar 2012 Invited Speaker, University of Washington, Department of Pharmacology, Seattle, Washington, USA


22. Nov 2011 Invited Speaker, U.S. Air Force Office of Scientific Research, San Antonio, Texas USA

21. Oct 2011 Invited Speaker, Johns Hopkins University School of Medicine, Institute of Genetic Medicine, Baltimore, USA

20. Sep 2011 Invited Speaker, Johns Hopkins University School of Medicine, Department of Cell Biology, Baltimore, USA

19. Jun 2011 Invited Speaker, Osaka University, Immunology Frontier Research Center, Osaka, Japan

18. Jun 2011 Plenary Speaker, RNA meeting 2011, Kyoto, Japan

17. Jun 2011 Invited Speaker, Academia Sinica, Genomics Research Center, Taipei, Taiwan

16. Jun 2011 Invited Speaker, Hong Kong University of Science and Technology, Division of Life Science, Hong Kong, China

15. May 2011 Invited Speaker, Johns Hopkins University, Breast Cancer Program Translational Research Seminar Series, Baltimore, Maryland, USA

14. Apr 2011 Invited Speaker, 5th Annual RNAi and microRNA World Congress, Boston, Massachusetts, USA

13. Apr 2011 Invited Speaker, New England RNA Data Club, Harvard Medical School, Boston, Massachusetts, USA

12. Apr 2010 Invited Speaker, Johns Hopkins University Bloomberg School of Public Health, Department of Biochemistry and Molecular Biology, Baltimore, USA

11. Apr 2010 Invited Speaker, Harvard University School of Public Health, Department of Genetics and Complex Diseases, Boston, Massachusetts, USA

10. Apr 2010 Invited Speaker, Rockefeller University, New York, USA

9. Apr 2010 Invited Speaker, Columbia University Medical Center, Department of Biochemistry and Molecular Biophysics, New York, USA

8. Mar 2010 Invited Speaker, Buck Institute, San Francisco, California, USA

7. Feb 2010 Invited Speaker, London Research Institute, Cancer Research UK, London, UK

6. Feb 2010 Invited Speaker, Cleveland Clinic, Lerner Research Institute, Cleveland, Ohio, USA

5. Feb 2010 Invited Speaker, Duke University Medical Center, Department of Biochemistry, Durham, North Carolina, USA

4. Jan 2010 Invited Speaker, New York University, Center for Genomics & Systems Biology, New York, USA

3. May 2009 Invited Speaker, The New York Academy of Sciences, “RNA in Stress Response and Longevity Control” symposium, New York, USA

2. May 2008 Invited Speaker, Society of Biological Psychiatry, 63rd Annual Meeting, “MicroRNAs: Emerging Players of Brain Function and Mental Illness” symposium, Washington D.C., USA

1. Mar 2008 Invited Speaker, 1st HHMI RNA granules Meeting, Chevy Chase, Maryland, USA

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