Publications
Selected Publications:
Shukla V, Samaniego-Castruita D, Dong Z, Gonzalez-Avalos E, Yan Q, Sarma K, Rao A. TET deficiency perturbs mature B cell homeostasis and promotes oncogenesis associated with accumulation of G-quadruplex and R-loop structures. Nature Immunology 2022; 23: 99-108. [PubMed]
Li X, Yue X, Sepulveda H, Burt RA, Scott DA, Carr SA, Myers SA, Rao A. OGT controls mammalian cell viability by regulating the proteasome/ mTOR/ mitochondrial axis. bioRxiv 2021 [bioRxiv]
Yue X, Samaniego-Castruita D, González-Avalos E, Barwick B, Rao A. Whole genome analysis of TET dioxygenase function in regulatory T cells. EMBO Reports 2021; 22: e52716. [PubMed]
Onodera A, González-Avalos E, Lio C-W J, Georges R, Bellacosa A, Nakayama T, Rao A. Roles of TET and TDG in DNA demethylation in proliferating and non-proliferating immune cells. Genome Biology 2021; 22: 186. [PubMed]
Seo H, Gonzàlez-Avalos E, Zhang W, Ramchandani P, Lio C-W J, Rao A, Hogan PG. BATF and IRF4 cooperate to counter exhaustion in tumour-infiltrating CAR T cells. Nature Immunology 2021; 22: 983-995. [PubMed]
Rao A. Scientific divagations: from signalling and transcription to chromatin changes in T cells. Nature Immunology 2020; 21: 1473-1476. [PubMed]
Shukla V, Halabelian L, Balagere S, Samaniego-Castruita D, Feldman DE, Arrowsmith CH, Rao A, Aravind L. HMCES functions in the alternative end-joining pathway of DNA DSB repair during class switch recombination in B cells. Mol Cell 2020; 77: 384-394. [PubMed]
Lio C-W J, Yue X, López-Moyado IF, Tahiliani M, Aravind L, Rao A. TET methylcytosine oxidases: new insights from a decade of research. J Biosci 2020; 45: 21. [PubMed]
López-Moyado IF, Tsagaratou A, Yuita H, Seo H, Delatte B, Heinz S, Benner C, Rao A. Paradoxical association of TET loss of function with genome-wide DNA hypomethylation. Proc Natl Acad Sci USA 2019; 116: 16933-16942. [PubMed]
Seo H, Chen J, González-Avalos E, Samaniego-Castruita D, López-Moyado IF, Georges R, Zhang W, Onodera A, Wu C-J, Das A, Wang YH, Lu L-F, Hogan PG, Bhandoola A, Rao A. TOX and TOX2 transcription factors cooperate with NR4A transcription factors to impose CD8+ T cell exhaustion. Proc Natl Acad Sci USA 2019; 116: 12410-12415. [PubMed]
Mognol GP, Gonzáles-Avalos E, Ghosh S, Spreafico R, Rao A, Damoiseaux R, Hogan PG. Targeting the NFAT:AP-1 complex on DNA with a small-molecule inhibitor. Proc Natl Acad Sci USA 2019; 116: 9959-9968. [PubMed]
The role of TET proteins in class switch recombination and AID gene expression in B cells. Science Immunology. 2019; 4: eaau7523. [PubMed]
Loss of TET2 and TET3 in regulatory T cells unleashes effector function. Nature Communications. 2019; 10: 2011. [PubMed]
TET enzymes augment activation-induced deaminase (AID) expression via 5-hydroxymethylcytosine modifications at the Aicdasuperenhancer. Science Immunology. 2019; 4. [PubMed]
NR4A transcription factors limit CAR T cell function in solid tumours. Nature. 2019; 567: 530-534. [PubMed]
TET Enzymes and 5hmC in Adaptive and Innate Immune Systems. Frontiers in Immunology. 2019; 10: 210. [PubMed]
Scott-Browne JP, Lio CJ, Rao A. TET proteins in natural and induced differentiation. Current Opinion in Genetics & Development. 2017; 46: 202-208. [PubMed]
Pereira RM, Hogan PG, Rao A, Martinez GJ. Transcriptional and epigenetic regulation of T cell hyporesponsiveness. Journal of Leukocyte Biology. 2017; 102: 601-615. [PubMed]
Tsagaratou A, Lio CJ, Yue X, Rao A. TET Methylcytosine Oxidases in T Cell and B Cell Development and Function. Frontiers in Immunology. 2017; 8: 220. [PubMed]
Mognol GP, Spreafico R, Wong V, Scott-Browne JP, Togher S, Hoffmann A, Hogan PG, Rao A, Trifari S. Exhaustion-associated regulatory regions in CD8+ tumor-infiltrating T cells. Proceedings of the National Academy of Sciences of the United States of America. 2017; 114: E2776-E2785. [PubMed]
Tsagaratou A, González-Avalos E, Rautio S, Scott-Browne JP, Togher S, Pastor WA, Rothenberg EV, Chavez L, Lähdesmäki H, Rao A. TET proteins regulate the lineage specification and TCR-mediated expansion of iNKT cells. Nature Immunology. 2017; 18: 45-53. [PubMed]
Scott-Browne JP, López-Moyado IF, Trifari S, Wong V, Chavez L, Rao A, Pereira RM. Dynamic Changes in Chromatin Accessibility Occur in CD8+ T Cells Responding to Viral Infection. Immunity. 2016; 45: 1327-1340. [PubMed]
Li X, Yue X, Pastor WA, Lin L, Georges R, Chavez L, Evans SM, Rao A. Tet proteins influence the balance between neuroectodermal and mesodermal fate choice by inhibiting Wnt signaling. Proceedings of the National Academy of Sciences of the United States of America. 2016; 113: E8267-E8276. [PubMed]
Lio CW, Zhang J, González-Avalos E, Hogan PG, Chang X, Rao A. Tet2 and Tet3 cooperate with B-lineage transcription factors to regulate DNA modification and chromatin accessibility. eLife. 2016; 5. [PubMed]
Yue X, Trifari S, Äijö T, Tsagaratou A, Pastor WA, Zepeda-Martínez JA, Lio CW, Li X, Huang Y, Vijayanand P, Lähdesmäki H, Rao A. Control of Foxp3 stability through modulation of TET activity. The Journal of Experimental Medicine. 2016; 213: 377-97. [PubMed]
Ko M, An J, Rao A. DNA methylation and hydroxymethylation in hematologic differentiation and transformation. Current Opinion in Cell Biology. 2015; 37: 91-101. [PubMed]
An J, González-Avalos E, Chawla A, Jeong M, López-Moyado IF, Li W, Goodell MA, Chavez L, Ko M, Rao A. Acute loss of TET function results in aggressive myeloid cancer in mice. Nature Communications. 2015; 6: 10071. [PubMed]
Kang J, Lienhard M, Pastor WA, Chawla A, Novotny M, Tsagaratou A, Lasken RS, Thompson EC, Surani MA, Koralov SB, Kalantry S, Chavez L, Rao A. Simultaneous deletion of the methylcytosine oxidases Tet1 and Tet3 increases transcriptome variability in early embryogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112: E4236-E4245. [PubMed]
Balasubramani A, Larjo A, Bassein JA, Chang X, Hastie RB, Togher SM, Lähdesmäki H, Rao A. Cancer-associated ASXL1 mutations may act as gain-of-function mutations of the ASXL1-BAP1 complex. Nature Communications. 2015; 6: 7307. [PubMed]
Martinez GJ, Pereira RM, Äijö T, Kim EY, Marangoni F, Pipkin ME, Togher S, Heissmeyer V, Zhang YC, Crotty S, Lamperti ED, Ansel KM, Mempel TR, Lähdesmäki H, Hogan PG, Rao A. The transcription factor NFAT promotes exhaustion of activated CD8⁺ T cells. Immunity. 2015; 42: 265-278. [PubMed]
Chavez L, Huang Y, Luong K, Agarwal S, Iyer LM, Pastor WA, Hench VK, Frazier-Bowers SA, Korol E, Liu S, Tahiliani M, Wang Y, Clark TA, Korlach J, Pukkila PJ, Aravind L, Rao A. Simultaneous sequencing of oxidized methylcytosines produced by TET/JBP dioxygenases in Coprinopsis cinerea. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111: E5149-E5158. [PubMed]
Huang Y, Rao A. Connections between TET proteins and aberrant DNA modification in cancer. Trends in Genetics: TIG. 2014; 30: 464-474. [PubMed]
Tsagaratou A, Äijö T, Lio CW, Yue X, Huang Y, Jacobsen SE, Lähdesmäki H, Rao A. Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111: E3306-E3315. [PubMed]
Iyer LM, Zhang D, de Souza RF, Pukkila PJ, Rao A, Aravind L. Lineage-specific expansions of TET/JBP genes and a new class of DNA transposons shape fungal genomic and epigenetic landscapes. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111: 1676-1683. [PubMed]
Huang Y, Chavez L, Chang X, Wang X, Pastor WA, Kang J, Zepeda-Martínez JA, Pape UJ, Jacobsen SE, Peters B, Rao A. Distinct roles of the methylcytosine oxidases Tet1 and Tet2 in mouse embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111: 1361-1366. [PubMed]
Sharma S, Quintana A, Findlay GM, Mettlen M, Baust B, Jain M, Nilsson R, Rao A, Hogan PG. An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry. Nature. 2013; 499: 238-242. [PubMed]
Pastor WA, Aravind L, Rao A. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nature Reviews. Molecular Cell Biology. 2013; 14: 341-356. [PubMed]
Oh-Hora M, Komatsu N, Pishyareh M, Feske S, Hori S, Taniguchi M, Rao A, Takayanagi H. Agonist-selected T cell development requires strong T cell receptor signaling and store-operated calcium entry. Immunity. 2013; 38: 881-895. [PubMed]
Ko M, An J, Bandukwala HS, Chavez L, Aijö T, Pastor WA, Segal MF, Li H, Koh KP, Lähdesmäki H, Hogan PG, Aravind L, Rao A. Modulation of TET2 expression and 5-methylcytosine oxidation by the CXXC domain protein IDAX. Nature. 2013; 497: 122-126. [PubMed]
Koh KP, Rao A. DNA methylation and methylcytosine oxidation in cell fate decisions. Current Opinion in Cell Biology. 2013; 25: 152-161. [PubMed]
Yigit E, Zhang Q, Xi L, Grilley D, Widom J, Wang JP, Rao A, Pipkin ME. High-resolution nucleosome mapping of targeted regions using BAC-based enrichment. Nucleic Acids Research. 2013; 41: e87. [PubMed]
Huang Y, Pastor WA, Zepeda-Martínez JA, Rao A. The anti-CMS technique for genome-wide mapping of 5-hydroxymethylcytosine. Nature Protocols. 2012; 7: 1897-1908. [PubMed]
Bandukwala HS, Gagnon J, Togher S, Greenbaum JA, Lamperti ED, Parr NJ, Molesworth AM, Smithers N, Lee K, Witherington J, Tough DF, Prinjha RK, Peters B, Rao A. Selective inhibition of CD4+ T-cell cytokine production and autoimmunity by BET protein and c-Myc inhibitors. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109: 14532-14537. [PubMed]
Vijayanand P, Seumois G, Simpson LJ, Abdul-Wajid S, Baumjohann D, Panduro M, Huang X, Interlandi J, Djuretic IM, Brown DR, Sharpe AH, Rao A, Ansel KM. Interleukin-4 production by follicular helper T cells requires the conserved Il4 enhancer hypersensitivity site V. Immunity. 2012; 36: 175-187. [PubMed]
Ko M, Bandukwala HS, An J, Lamperti ED, Thompson EC, Hastie R, Tsangaratou A, Rajewsky K, Koralov SB, Rao A. Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108: 14566-14571. [PubMed]
Sharma S, Findlay GM, Bandukwala HS, Oberdoerffer S, Baust B, Li Z, Schmidt V, Hogan PG, Sacks DB, Rao A. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNA-protein scaffold complex. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108: 11381-11386. [PubMed]
Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, Ko M, McLoughlin EM, Brudno Y, Mahapatra S, Kapranov P, Tahiliani M, Daley GQ, Liu XS, Ecker JR, Milos PM, Agarwal S, Rao A. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature. 2011; 473: 394-397. [PubMed]
Bandukwala HS, Wu Y, Feuerer M, Chen Y, Barboza B, Ghosh S, Stroud JC, Benoist C, Mathis D, Rao A, Chen L. Structure of a domain-swapped FOXP3 dimer on DNA and its function in regulatory T cells. Immunity. 2011; 34: 479-491. [PubMed]
Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M, Sommer CA, Mostoslavsky G, Lahesmaa R, Orkin SH, Rodig SJ, Daley GQ, Rao A. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell. 2011; 8: 200-213. [PubMed]
Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, An J, Lamperti ED, Koh KP, Ganetzky R, Liu XS, Aravind L, Agarwal S, Maciejewski JP, Rao A. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature. 2010; 468: 839-843. [PubMed]
Pipkin ME, Sacks JA, Cruz-Guilloty F, Lichtenheld MG, Bevan MJ, Rao A. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity. 2010; 32: 79-90. [PubMed]
Huang Y, Pastor WA, Shen Y, Tahiliani M, Liu DR, Rao A. The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PloS One. 2010; 5: e8888. [PubMed]
Hogan PG, Lewis RS, Rao A. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annual Review of Immunology. 2010; 28: 491-533. [PubMed]
Sharma S, Rao A. RNAi screening: Tips and techniques. Nature Immunol 2009; 10: 799-804. [PubMed]
Iyer LM, Tahiliani M, Rao A, Aravind L. Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids. Cell Cycle 2009; 8: 1698-1710. [PubMed]
Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324: 930-935. [PubMed]
Rao A. Signaling to gene expression: calcium, calcineurin and NFAT. Nat Immunol 2009; 10: 3-5. [PubMed]
Oberdoerffer S, Moita LF, Neems DS, Freitas RA, Hacohen N, Rao A. Regulation of CD45 alternative splicing by the heterogeneous ribonucleoprotein, HnRNPLL. Science 2008; 321: 686-691. [PubMed]
Oh-hora M, Yamashita M, Hogan PG, Sharma S, Lamperti E, Chung W, Prakriya M, Feske S, Rao A. Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nature Immunol 2008; 9: 432-443. [PubMed]
Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, Murphy A, Frendewey D, Valenzuela D, Kutok JL, Schmidt-Supprian M, Rajewsky N, Yancopoulos G, Rao A, Rajewsky K. Regulation of the germinal center response by microRNA-155. Science 2007; 316: 604-608. [PubMed]
Tahiliani M, Mei P, Fang R, Leonor T, Rutenberg M, Shimizu F, Li J, Rao A, Shi Y. A histone 3 lysine 4 demethylase, SMCX, links REST target genes to X-linked mental retardation. Nature 2007; 447: 601-605. [PubMed]
Djuretic IM, Levanon D, Negreanu V, Groner Y, Rao A, Ansel KM. Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in Th1 cells. Nature Immunol 2006; 8: 145-53. [PubMed]
Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG. Orai1 is an essential pore subunit subunit of the CRAC channel. Nature 2006; 443: 230-233. [PubMed]
Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC, Bates DL, Guo L, Han A, Ziegler SF, Mathis D, Benoist C, Chen L, Rao A. FOXP3 controls T regulatory function through cooperation with NFAT. Cell 2006; 126: 375-387. [PubMed]
Gwack Y, Sharma S, Nardone J, Tanasa B, Iuga A, Srikanth S, Okamura H, Bolton D, Feske S, Hogan PG, Rao A. A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 2006; 441: 646-650. [PubMed]
Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel S-H, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A. A mutation in Orai1 causes immune deficiency by abrogating store-operated Ca2+ entry and CRAC channel function. Nature 2006; 441: 179-185. [PubMed]
Ansel KM. Djuretic I, Tanasa B, Rao A. Regulation of Th2 differentiation and Il4 locus acessibility. Annu Rev Immunol 2006; 24: 607-656 (review). [PubMed]
Monticelli S, Ansel KM, Xiao C, Socci ND, Krichevsky AM, Thai TH, Rajewsky N, Marks DS, Sander C, Rajewsky K, Rao A, Kosik K. MicroRNA profiling of the murine hematopoietic system. Genome Biol 2005; 6: R71. [PubMed]
Ansel KM, Greenwald RJ, Agarwal S, Bassing CH, Monticelli S, Interlandi J, Djuretic IM, Lee DU, Sharpe AH, Alt FW, Rao A. Deletion of a conserved Il4 silencer impairs T helper type 1-mediated immunity. Nature Immunol 2004; 5: 1251-1259. [PubMed]
Okamura H, Garcia-Rodriguez C, Martinson H, Qin J, Virshup DM, Rao A. A conserved docking motif for CK1 binding controls the nuclear localization of NFAT. Mol Cell Biol 2004; 24: 4184-4195. [PubMed]
Heissmeyer V, Macián F, Im S-H, Varma R, Feske S, Venuprasad K, Jeon M-S, Gu H, Liu Y-C, Dustin ML, Rao A. Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nature Immunol 2004; 5: 255-265. [PubMed]
Hogan PG, Chen L, Nardone J, Rao A. Transcriptional regulation by calcium, calcineurin and NFAT. Genes & Development 2003; 17: 2205-2232 (review). [PubMed]
Solymar DC, Agarwal S, Bassing CH, Alt FW, Rao A. A 3’ enhancer in the IL-4 gene regulates cytokine production by Th2 cells and mast cells. Immunity 2002; 17: 41-50. [PubMed]
Macian F, Cozar FJG, Im S-H, Horton HF, Byrne MC, Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2002; 109: 719-731. [PubMed]
Lee DU, Agarwal S, Rao A. Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 2002; 16: 649-660. [PubMed]
Macian F, Garcia-Rodriguez C, Rao A. Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. EMBO J 2000; 19: 4783-4795. [PubMed]
Okamura H, Aramburu J, Garcia-Rodriguez C, Viola JPB, Raghavan A, Zhang X, Qin J, Hogan PG, Rao, A. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol Cell 2000; 6: 539-550. [PubMed]
Agarwal S, Avni O, Rao A. Cell-type-restricted binding of the transcription factor NFAT1 to a distal IL-4 enhancer in vivo. Immunity 2000; 12: 643-652. [PubMed]
Aramburu J, Yaffe MB, Lopez-Rodriguez C, Cantley LC, Hogan PG, Rao, A. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 1999; 285: 2129-2133. [PubMed]
Lopez-Rodriguez C, Aramburu J, Rakeman AS, Rao A. NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc Natl Acad Sci USA 1999; 96: 7214-7219. [PubMed]
Agarwal S, Rao A. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 1998; 9: 765-775. [PubMed]
Aramburu J, Cozar FG, Raghavan A, Okamura H, Rao A, Hogan PG. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targetting site of NFAT. Mol Cell 1998; 1: 627-637. [PubMed]
Chen L, Glover JNM, Hogan PG, Rao A, Harrison SC. Structure of the DNA-binding domains of NFAT, Fos and Jun bound to DNA. Nature 1998; 392: 42-48. [PubMed]
Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL, Li J, Young D, Barbosa M, Mann M, Manning A, Rao A. IKK-1 and IKK-2, Cytokine-activated IkB kinases essential for NF-kB activation. Science 1997; 278: 860-865. [PubMed]
Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 1997; 15: 707-747 (review). [PubMed]
Rao A. NFATp, a cyclosporin-sensitive transcription factor implicated in cytokine gene induction. J Leuk Biol 1995; 57: 536-542 (review). [PubMed]
McCaffrey PG, Luo C, Kerppola TK, Jain J, Badalian TM, Ho AM, Burgeon E, Lane WS, Lambert JL, Curran T, Verdine GL, Rao A, Hogan PG. Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 1993; 262: 750-754. [PubMed]
Jain J, McCaffrey PG, Miner Z, Kerppola TK, Lambert JN, Verdine GL, Curran T, Rao A. The T cell transcription factor NFATp is a substrate for calcineurin and interacts with the DNA-binding domains of Fos and Jun. Nature 1993; 365: 352-355. [PubMed]
Jain J, Miner Z, Rao A. Analysis of the preexisting and nuclear forms of NF-AT (nuclear factor of activated T cells). J Immunol 1993; 151: 837-848. [PubMed]