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Dr. Han-Yu Shih, Ph.D.
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<span>Dr. Han-Yu Shih, Ph.D.</span>
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<p class="title"><strong>Stadtman Investigator</strong></p><div class="c-staff__staff-group">
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<a href="/research/research-labs-and-branches/neuro-immune-regulome-unit" hreflang="en">Neuro-Immune Regulome Unit</a>
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<p class="c-staff__research-interest">
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<strong>Research interests:</strong>
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Regulation of cytokine loci and immune regulomes
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<a href="mailto:han-yu.shih@nih.gov" target="_blank">Email</a>
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<span>10 Center Dr</span>
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<span>Building 10, Room 5S261</span>
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<br />
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<span>Bethesda, </span>
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<span>
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Maryland
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20892
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<div class="c-section">
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<h2>Biography</h2>
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<div><p>Dr. Shih received her M.S. in Microbiology from National Taiwan University in 2006 and Ph.D. in Immunology from Duke University in 2012. As a graduate student, she worked in Dr. Michael Krangel’s lab studying the role of three-dimensional chromatin looping and the key looping factor, CTCF, in gene regulation during thymocyte development. In 2013, she joined John O’Shea’s lab in NIAMS where she began her work on lymphocyte regulomes as a postdoctoral fellow. She received a NIH K22 career development award in 2018 and was jointly appointed by NEI and NINDS as a Stadtman Tenure-track Investigator in 2019. Her research focuses on understanding the regulation of cytokine loci and immune regulomes in health and neurodegenerative diseases in eye and brain, with an ultimate goal of developing more specific and efficacious therapies.</p></div>
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<div class="c-section">
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<h2>Current research</h2>
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<div><p>The Neuro-Immune Regulome Unit (NIRU) aims to understand the mechanisms that precisely regulate gene expression in lymphoid cells through multidisciplinary genomic approaches. Lymphoid cells communicate the perturbation of homeostasis by production of cytokines, dysregulation of which results in neural and ocular inflammation in many disorders, including Alzheimer’s disease, Parkinson’s disease, multiple sclerosis, uveitis, and age-related macular degeneration. Understanding the basic pathophysiology of cytokine production in these contexts – for example, their source and regulation – represents a promising path for the development of more specific and efficacious therapies.</p><p>Precise orchestration of gene regulation in lymphocytes is mediated by networks of signaling molecules, transcription factors, and genomic regulatory regions, which in sum is termed regulomes. Previously, we have identified lineage-specific regulomes in tissue-resident innate and adaptive lymphocytes in both homeostatic and activated states by integrating cutting-edge techniques and computational approaches (Shih et al., Cell, 2016; Harrison et al., Science, 2018; Kobayashi et al., Cell, 2019; Nagashima et al., Immunity, 2019). We now are focusing on two key biological questions 1) How do distinct stimuli regulate cytokines in a context-specific manner? 2) How cytokines contribute to the progression of neurodegeneration, such as Alzheimer’s disease and age-related macular degeneration? By analyzing lymphocyte regulomes with distinct genetic background in human and engineered mice, we aim to further our understanding of molecular mechanisms that contribute to aging and neurodegenerative diseases.</p></div>
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</div>
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<div class="c-section">
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<h2>Selected publications</h2>
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<div>
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<div><div class="c-text">
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<ol><li>Liu C, Nagashima H, Fernando N, Signorella S, Montgomery W, Lim AI, Harrison O, Bass V, Reich L, Yao C, Sun HW, Brooks SR, Jiang K, Nagarajan V, Phillips R, Mikami Y, Lareau CA, Kanno Y, Jankovic D, Aryee M, Pekowska A, Belkaid Y, O’Shea JJ, Shih HY. <a href="https://pubmed.ncbi.nlm.nih.gov/38697116/">A distal CTCF binding site shapes Mdm1-Il22-Ifng locus regulation and is essential for early Th1 differentiation and specification. Immunity.</a> 2024 May</li><li>Fernando N, Gopalakrishnan J, Behensky A, Reich L, Liu C, Bass V, Bono M, Montgomery W, De Pace R, Mattapallil M, Nagarajan V, Brooks SR, Maric D, Caspi RR, McGavern DB, Shih HY. <a href="https://pubmed.ncbi.nlm.nih.gov/37090642/">Single-cell multiomic analysis reveals the involvement of Type I nterferon-responsive CD8+ T cells in amyloid beta associated memory loss. </a>bioRxiv. 2023. Preprint.</li><li>Hasim MS, Marotel M, Hodgins JJ, Vulpis E, Makinson OJ, Asif S, Shih HY, Scheer AK, MacMillan O, Alonso FG, Burke KP, Cook DP, Li R, Petrucci MT, Santoni A, Fallon PG, Sharpe AH, Sciumè G, Veillette A, Zingoni A, Gray DA, McCurdy A, Ardolino M. <a href="https://pubmed.ncbi.nlm.nih.gov/35417234/">When killers become thieves: Trogocytosed PD-1 inhibits NK cells in cancer.</a> Sci Adv. 2022</li><li>Yao Y, Kim G, Shafer S, Chen Z, Kubo S, Ji Y, Luo J, Yang W, Perner SP, Kanellopoulou C, Park AY, Jiang P, Li J, Baris S, Aydiner EK, Ertem D, Mulder DJ, Warner N, Griffiths AM, Topf-Olivestone C, Kori M, Werner L, Ouahed J, Field M, Liu C, Schwarz B, Bosio CM, Ganesan S, Song J, Urlaub H, Oellerich T, Malaker SA, Zheng L, Bertozzi CR, Zhang Y, Matthews H, Montgomery W, Shih HY, Jiang J, Jones M, Baras A, Shuldiner A, Gonzaga-Jauregui C, Snapper SB, Muise AM, Shouval DS, Ozen A, Pan KT, Wu C, Lenardo MJ. <a href="https://pubmed.ncbi.nlm.nih.gov/35303419/">Mucus sialylation determines intestinal host-commensal homeostasis.</a> Cell. 2022</li><li>Scott-Browne J, Shih HY. <a href="https://pubmed.ncbi.nlm.nih.gov/35034371/">Stability and change in epigenetic regulation of immune cells. Immunol Rev.</a> 2022</li><li>Morrison TA, Hudson WH, Chisolm DA, Kanno Y, Shih HY, Ahmed R, Henao-Mejia J, Hafner M, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/34001528/">Evolving Views of Long Noncoding RNAs and Epigenomic Control of Lymphocyte State and Memory.</a> Cold Spring Harb Perspect Biol. 2021.</li><li>Fernando N, Sciumè G, O'Shea JJ, Shih HY. <a href="https://pubmed.ncbi.nlm.nih.gov/33841440/">Multi-Dimensional Gene Regulation in Innate and Adaptive Lymphocytes: A View From Regulomes.</a> Front Immunol. 2021.</li><li>Wu W, Hill SE, Nathan WJ, Paiano J, Callen E, Wang D, Shinoda K, van Wietmarschen N, Colón-Mercado JM, Zong D, De Pace R, Shih HY, Coon S, Parsadanian M, Pavani R, Hanzlikova H, Park S, Jung SK, McHugh PJ, Canela A, Chen C, Casellas R, Caldecott KW, Ward ME, Nussenzweig A. <a href="https://pubmed.ncbi.nlm.nih.gov/33767446/">Neuronal enhancers are hotspots for DNA single-strand break repair.</a> Nature. 2021</li><li>Mikami Y, Philips RL, Sciumè G, Petermann F, Meylan F, Nagashima H, Yao C, Davis FP, Brooks SR, Sun HW, Takahashi H, Poholek AC, Shih HY, Afzali B, Muljo SA, Hafner M, Kanno Y, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/33767446/">MicroRNA-221 and -222 modulate intestinal inflammatory Th17 cell response as negative feedback regulators downstream of interleukin-23.</a> Immunity. 2021</li><li>Sciumè G, Mikami Y, Jankovic D, Nagashima H, Villarino AV, Morrison T, Yao C, Signorella S, Sun HW, Brooks SR, Fang D, Sartorelli V, Nakayamada S, Hirahara K, Zitti B, Davis FP, Kanno Y, O’Shea JJ, <strong>Shih HY</strong>. <a href="https://pubmed.ncbi.nlm.nih.gov/33010223/">Rapid enhancer landscape remodeling and transcription factor repurposing enable high magnitude gene induction upon acute activation of NK cells.</a> <em>Immunity</em>. 2020</li><li>Cannons JL, Villarino AV, Kapnick SM, Preite S, <strong>Shih HY</strong>, Gomez-Rodriguez J, Kaul Z, Shibata H, Reilley JM, Huang B, Handon R, McBain IT, Gossa S, Wu T, Su HC, McGavern DB, O'Shea JJ, McGuire PJ, Uzel G, Schwartzberg PL. <a href="https://pubmed.ncbi.nlm.nih.gov/34644563/">PI3Kδ coordinates transcriptional, chromatin, and metabolic changes to promote effector CD8 <sup>+</sup> T cells at the expense of central memory.</a> Cell Rep. 2021</li><li>Lim AI, McFadden T, Link VM, Han SJ, Karlsson RM, Stacy A, Farley TK, Lima-Junior DS, Harrison OJ, Desai JV, Lionakis MS, <strong>Shih HY</strong>, Cameron HA, Belkaid Y. <a href="https://pubmed.ncbi.nlm.nih.gov/34446580/">Prenatal maternal infection promotes tissue-specific immunity and inflammation in offspring.</a> Science. 2021</li><li>Di Censo C, Marotel M, Mattiola I, Müller L, Scarno G, Pietropaolo G, Peruzzi G, Laffranchi M, Mazej J, Hasim MS, Asif S, Russo E, Tomaipitinca L, Stabile H, Lee SH, Vian L, Gadina M, Gismondi A, <strong>Shih HY</strong>, Mikami Y, Capuano C, Bernardini G, Bonelli M, Sozzani S, Diefenbach A, Ardolino M, Santoni A, Sciumè G. <a href="https://pubmed.ncbi.nlm.nih.gov/34347289/">Granzyme A and CD160 expression delineates ILC1 with graded functions in the mouse liver.</a> Eur J Immunol. 2021</li><li>Göschl L, Preglej T, Boucheron N, Saferding V, Müller L, Platzer A, Hirahara K, <strong>Shih HY</strong>, Backlund J, Matthias P, Niederreiter B, Hladik A, Kugler M, Gualdoni GA, Scheinecker C, Knapp S, Seiser C, Holmdahl R, Tillmann K, Plasenzotti R, Podesser B, Aletaha D, Smolen JS, Karonitsch T, Steiner G, Ellmeier W, Bonelli M. <a href="https://pubmed.ncbi.nlm.nih.gov/31883829/">Histone deacetylase 1 (HDAC1): A key player of T cell-mediated arthritis.</a> J<em> Autoimmun</em>. 2020</li><li>Petermann F, Pękowska A, Johnson CA, Jankovic D, <strong>Shih HY</strong>, Jiang K, Hudson WH, Brooks SR, Sun HW, Villarino AV, Yao C, Singleton K, Akondy RS, Kanno Y, Sher A, Casellas R, Ahmed R, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/31377117/">The Magnitude of IFN-γ Responses Is Fine-Tuned by DNA Architecture and the Non-coding Transcript of Ifng-as1.</a> <em>Mol Cell</em>. 2019</li><li>Nagashima H, Mahlakõiv T, <strong>Shih HY</strong>, Davis FP, Meylan F, Huang Y, Harrison OJ, Yao C, Mikami Y, Urban JF Jr, Caron KM, Belkaid Y, Kanno Y, Artis D, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/31353223/">Neuropeptide CGRP Limits Group 2 Innate Lymphoid Cell Responses and Constrains Type 2 Inflammation.</a> <em>Immunity</em>. 2019</li><li>Yao C, Sun HW, Lacey NE, Ji Y, Moseman EA, <strong>Shih HY</strong>, Heuston EF, Kirby M, Anderson S, Cheng J, Khan O, Handon R, Reilley J, Fioravanti J, Hu J, Gossa S, Wherry EJ, Gattinoni L, McGavern DB, O'Shea JJ, Schwartzberg PL, Wu T. <a href="https://pubmed.ncbi.nlm.nih.gov/31209400/">Single-cell RNA-seq reveals TOX as a key regulator of CD8<sup>+</sup> T cell persistence in chronic infection.</a> <em>Nat Immunol</em>. 2019</li><li>Kobayashi T, Voisin B, Kim DY, Kennedy EA, Jo JH, <strong>Shih HY</strong>, Truong A, Doebel T, Sakamoto K, Cui CY, Schlessinger D, Moro K, Nakae S, Horiuchi K, Zhu J, Leonard WJ, Kong HH and Nagao K. <a href="https://pubmed.ncbi.nlm.nih.gov/30712873/">Homeostatic control of sebaceous glands by innate lymphoid cells regulates commensal bacteria equilibrium.</a> <em>Cell</em>. 2019</li><li>Schwartz DM, Farley T, Richoz N, Yao C, <strong>Shih HY</strong>, Petermann F, Zhang<sup> </sup>Y, Sun<sup> </sup>HW, Hayes E, Mikami<sup> </sup>Y, Jiang<sup> </sup>K, Davis<sup> </sup>FP, Kanno<sup> </sup>Y, Milner JD, Siegel<sup> </sup>R, Laurence<sup> </sup>A, Meylan<sup> </sup>F, O’Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/30650370/">Retinoic acid receptor alpha represses a Th9 transcriptional and epigenomic program.</a> <em>Immunity</em>. 2019</li><li>Harrison OJ, Linehan JL, <strong>Shih HY</strong>, Bouladoux N, Han SJ, Smelkinson M, Sen SK, Byrd AL, Enamorado M, Yao C, Tamoutounour S, Laethem FV, Hurabielle C, Collins N, Paun A, Salcedo R, O’Shea JJ, Belkaid Y. <a href="https://pubmed.ncbi.nlm.nih.gov/30523076/">Commensal-specific T cell plasticity promotes rapid tissue adaptation to injury.</a> <em>Science</em>. 2018</li><li>Povoleri G, Nova-Lamperti E, Scottà C, Fanelli G, Chen YC, Becker PD, Boardman D, Costantini B, Romano M, Pavlidis P, McGregor R, Pantazi E, Chauss D, Sun HW, <strong>Shih HY</strong>, Cousins DJ, Cooper N, Powell N, Kemper C, Pirooznia M, Laurence A, Shahram Kordasti S, Kazemian M, Lombardi G, Afzali B. <a href="https://pubmed.ncbi.nlm.nih.gov/30397350/">Human retinoic acid–regulated CD161<sup>+</sup>regulatory T cells support wound repair in intestinal mucosa.</a> <em>Nat Immunol.</em> 2018</li><li>Mikami Y, Scarno G, Zitti B, <strong>Shih HY</strong>, Kanno Y, Santoni A, O'Shea JJ, Sciumè G. <a href="https://pubmed.ncbi.nlm.nih.gov/29524223/">NCR+ ILC3 maintain larger STAT4 reservoir via T-BET to regulate type 1 features upon IL-23 stimulation in mice.</a> <em>Eur J Immunol.</em> 2018</li><li>Loguercio S, Barajas-Mora EM, <strong>Shih HY</strong>, Krangel MS, Feeney AJ. <a href="https://pubmed.ncbi.nlm.nih.gov/29593713/">Variable extent of lineage-specificity and developmental stage-specificity of cohesin and CCCTC-binding factor binding within the immunoglobulin and T cell receptor loci.</a> <em>Front Immunol.</em> 2018</li><li>Rahman MJ, Rodrigues KB, Quiel JA, Liu Y, Bhargava V, Zhao Y, Hotta-Iwamura C, <strong>Shih HY</strong>, Lau-Kilby AW, Malloy AM, Thoner TW, Tarbell KV. <a href="https://pubmed.ncbi.nlm.nih.gov/29415894/">Restoration of the type I IFN-IL-1 balance through targeted blockade of PTGER4 inhibits autoimmunity in NOD mice.</a> <em>JCI Insight.</em> 2018</li><li>Sciumè G, <strong>Shih HY</strong>, Mikami Y, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/29250060/">Epigenomic views of innate lymphoid cells.</a> <em>Front Immunol.</em> 2017</li><li>Iwata S, Mikami Y, Sun HW, Brooks SR, Jankovic D, Hirahara K, Onodera A, <strong>Shih HY</strong>, Kawabe T, Jiang K, Nakayama T, Sher A, O'Shea JJ, Davis FP, Kanno Y. <a href="https://pubmed.ncbi.nlm.nih.gov/28623086/">The transcription factor T-bet limits amplification of Type I IFN transcriptome and circuitry in T helper 1 cells.</a><em> Immunity</em>. 2017</li><li>Roychoudhuri R, Clever D, Li P, Wakabayashi Y, Quinn KM, Klebanoff CA, Ji Y, Sukumar M, Eil RL, Yu Z, Spolski R, Palmer DC, Pan JH, Patel SJ, Macallan DC, Fabozzi G, <strong>Shih HY</strong>, Kanno Y, Muto A, Zhu J, Gattinoni L, O'Shea JJ, Okkenhaug K, Igarashi K, Leonard WJ, Restifo NP. <a href="https://pubmed.ncbi.nlm.nih.gov/27158840/">BACH2 regulates CD8+ T cell differentiation by controlling access of AP-1 factors to enhancers.</a> <em>Nat Immunol.</em> 2016</li><li><strong>Shih HY</strong>*<sup>#</sup>, Sciumè G*, Mikami Y*, Guo L, Sun HW, Brooks S, Urban J, Davis F, Kanno Y, O’Shea JJ<sup>#</sup>. <a href="https://pubmed.ncbi.nlm.nih.gov/27156451/">Developmental acquisition of regulomes underlies innate lymphoid cell functionality.</a> <em>Cell.</em> 2016 <strong>(recommended by F1000PRime and rated as “Exceptional”)</strong> *co-first authors <sup>#</sup><strong>corresponding authors</strong></li><li>Villarino A, Laurence A, Robinson GW, Bonelli M, Dema B, Afzali B, <strong>Shih HY</strong>, Sun HW, Brooks SR, Hennighausen L, Kanno Y, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/26999798/">Signal transducer and activator of transcription 5 (STAT5) paralog dose governs T cell effector and regulatory functions.</a><em> Elife.</em> 2016</li><li>Dell'Orso S, Wang AH, <strong>Shih HY</strong>, Saso K, Berghella L, Gutierrez-Cruz G, Ladurner AG, O'Shea JJ, Sartorelli V, Zare H. <a href="https://pubmed.ncbi.nlm.nih.gov/26832413/">The Histone Variant macroH2A1.2 is necessary for the activation of muscle enhancers and recruitment of the transcription factor Pbx1.</a> <em>Cell Rep.</em> 2016</li><li>Chen L, Carico Z, <strong>Shih HY</strong>, Krangel MS. <a href="https://pubmed.ncbi.nlm.nih.gov/26258942/">A discrete chromatin loop in the mouse Tcra-Tcrd locus shapes the TCRδ and TCRα repertoires. </a><em>Nat Immunol.</em> 2015</li><li>Hirahara K, Onodera A, Villarino AV, Bonelli M, Sciumè G, Laurence A, Sun HW, Brooks SR, Vahedi G, <strong>Shih HY</strong>, Gutierrez-Cruz G, Iwata S, Suzuki R, Mikami Y, Okamoto Y, Nakayama T, Holland SM, Hunter CA, Kanno Y, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/25992861/">Asymmetric action of STAT transcription factors drives transcriptional outputs and cytokine specificity.</a> <em>Immunity</em>. 2015</li><li>Boudil A, Matei IR, <strong>Shih HY</strong>, Bogdanoski G, Yuan JS, Chang SG, Montpellier B, Kowalski PE, Voisin V, Bashir S, Bader GD, Krangel MS, Guidos CJ. <a href="https://pubmed.ncbi.nlm.nih.gov/25729925/">IL-7 coordinates proliferation, differentiation and Tcra recombination during thymocyte β-selection.</a> <em>Nat Immunol</em>. 2015</li><li><strong>Shih HY</strong>, Sciumè G, Poholek AC, Vahedi G, Hirahara K, Villarino AV, Bonelli M, Bosselut R, Kanno Y, Muljo SA, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/25123275/">Transcriptional and epigenetic networks of helper T and innate lymphoid cells.</a> <em>Immunol Rev. </em>2014</li><li>Bonelli M, <strong>Shih HY</strong>, Hirahara K, Singelton K, Laurence A, Poholek A, Hand T, Mikami Y, Vahedi G, Kanno Y, O'Shea JJ. <a href="https://pubmed.ncbi.nlm.nih.gov/24831346/">Helper T cell plasticity: impact of extrinsic and intrinsic signals on transcriptomes and epigenomes.</a> <em>Curr Top Microbiol Immunol.</em> 2014</li><li><strong>Shih HY</strong>, Krangel MS.<a href="https://pubmed.ncbi.nlm.nih.gov/23645930/"> Chromatin architecture, CTCF and V(D)J recombination: managing long-distance relationships at antigen receptor loci.</a> <em>J Immunol</em>. 2013</li><li><strong>Shih HY</strong>, Verma-Gaur V, Feeney AJ, Galjart N, Krangel MS. <a href="https://pubmed.ncbi.nlm.nih.gov/23169622/">T cell receptor alpha gene recombination is supported by a <em>Tcra</em> enhancer and CTCF-dependent chromatin hub.</a> <em>Proc Natl Acad Sci U S A.</em> 2012</li><li>Kondilis-Mangum HD, <strong>Shih HY</strong>, Mahowald G, Sleckman BP, Krangel MS.<a href="https://pubmed.ncbi.nlm.nih.gov/22079986/"> Regulation of TCRb allelic exclusion by gene segment proximity and accessibility.</a> <em>J Immunol</em>. 2011</li><li>Ko TM, Chung WH, Wei CY, <strong>Shih HY</strong>, Chen JK, Lin CH, Chen YT, Hung SI. <a href="https://pubmed.ncbi.nlm.nih.gov/21924464/">Shared and restricted T-cell receptor use is crucial for carbamazepine-induced Stevens-Johnson syndrome.</a> <em>J Allergy Clin Immunol.</em> 2011</li><li><strong>Shih HY</strong>, Hao B, Krangel MS. <a href="https://pubmed.ncbi.nlm.nih.gov/21128009/">Orchestrating T-cell receptor a gene assembly through changes in chromatin structure and organization.</a> <em>Immunol Res.</em> 2010</li><li><strong>Shih HY</strong>, Krangel MS. <a href="https://pubmed.ncbi.nlm.nih.gov/20696701/">Distinct contracted conformations of the Tcra/Tcrd locus during Tcra and Tcrd recombination.</a> <em>J Exp Med</em>. 2010</li><li>Hung SI, Chung WH, Jee SH, Chen WC, Chang YT, Lee WR, Hu SL, Wu MT, Chen GS, Wong TW, Hsiao PF, Chen WH, <strong>Shih HY</strong>, Fang WH, Wei CY, Lou YH, Huang YL, Lin JJ, Chen YT. <a href="https://pubmed.ncbi.nlm.nih.gov/16538176/">Genetic susceptibility to carbamazepine-induced cutaneous adverse drug reactions.</a><em> Pharmacogenet Genomics.</em> 2006</li></ol><p> </p><p><a href="https://pubmed.ncbi.nlm.nih.gov/?term=Shih%2C%20Han-Yu%5BAuthor%5D"><strong>PubMed search for Shih, H-Y.</strong></a></p>
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