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2024
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Mapping multimodal phenotypes to perturbations in cells and tissue with CRISPRmap. Gu, J., Iyer, A., Wesley, B., Taglialatela, A., Leuzzi, G., Hangai, S., Decker, A., Gu, R., Klickstein, N., Shuai, Y., Jankovic, K., Parker-Burns, L., Jin, Y., Zhang, J.Y., Hong, J., Niu, X., Costa, J.A., Pezet, M.G., Chou, J., Snoeck, H.W., Landau, D.A., Azizi, E., Chan, E.M., Ciccia, A., Gaublomme, J.T. (2024). Nat. Biotechnol. doi: 10.1038/s41587-024-02386-x
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Deciphering the impact of genomic variation on function. IGVF Consortium (2024). Nature, 633(8028):47-57. doi: 10.1038/s41586-024-07510-0.
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Mapping variant effects on anti-tumor hallmarks of primary human T cells with base-editing screens. Walsh, Z.H., Shah, P., Kothapalli, N., Shah, S.B., Nikolenyi, G., Brodtman, D.Z., Leuzzi, G., Rogava, M., Mu, M., Ho, P., Abuzaid, S., Vasan, N., AlQuraishi, M., Milner, J.D., Ciccia, A., Melms, J.C., and Izar, B. (2024). Nat. Biotechnol. doi: 10.1038/s41587-024-02235-x.
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Extrachromosomal Telomere DNA Derived from Excessive Strand Displacements. Lee, J., Lee, J., Sohn, E.J., Taglialatela, A., O'Sullivan, R.J., Ciccia, A., and Min J. (2024). Proc Natl Acad Sci U S A, 121(19):e2318438121.
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Mechanism of DNA unwinding by hexameric MCM8-9 in complex with HROB. Acharya, A., Bret, H., Huang, J.W., Mütze, M., Göse, M., Kissling, V., Seidel, R., Ciccia, A., Guérois, R., Cejka, P. (2024). Nat. Commun., 15(1):3584.
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BRCA1 and 53BP1 regulate reprogramming efficiency by mediating DNA repair pathway choice at replication-associated double-strand breaks. Georgieva, D., Wang, N., Taglialatela, A., Jerabek, S., Reczek, C.R., Lim, P.X., Sung, J., Du, Q., Horiguchi, M., Jasin, M., Ciccia, A., Baer, R., and Egli, D.(2024). Cell Reports, 43(4): 114006.
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SMARCAL1 is a dual regulator of innate immune signaling and PD-L1 expression that promotes tumor immune evasion. Leuzzi, G., Vasciaveo, A., Taglialatela, A., Chen, X., Firestone, T.M., Hickman, A.R., Mao, W., Thakar, T., Vaitsiankova, A., Huang, J.W., Cuella-Martin, R., Hayward, S.B., Kesner, J.S., Ghasemzadeh, A., Nambiar, T.S., Ho, P., Rialdi, A., Hebrard, M., Li, Y., Gao, J., Gopinath, S., Adeleke, O.A., Venters, B., Drake, C.G., Baer, R., Izar, B., Guccione, E., Keogh, M.C., Guerois, R., Sun, L., Lu, C., Califano, A., and Ciccia, A. (2024). Cell, 187: 1-21.
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Highlights: Feeding two birds with one scone: The dual roles of SMARCAL1 in antitumor immunity. Toufektchan, E., and Maciejowski, J. (2024). Mol. Cell, 85(5): 819-821; SMARCAL1 Favors Tumor Immune Evasion Through Dual Mechanisms. (2024). Cancer Discovery
2023
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Base-editing screens illuminate variant effects in human hematopoiesis. Vaitsiankova, A., Thakar, T., and Ciccia, A. (2023). Cell Reports Methods, 3(7): 100541.
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Context-defined cancer co-dependency mapping identifies a functional interplay between PRC2 and MLL-MEN1 complex in lymphoma. Chen, X., Li, Y., Zhu, F., Xu, X., Estrella, B., Pazos, M.A. 2nd, McGuire, J.T., Karagiannis, D., Sahu, V., Mustafokulov, M., Scuoppo, C., Sánchez-Rivera, F.J., Soto-Feliciano, Y.M., Pasqualucci, L., Ciccia, A., Amengual, J.E., and Lu, C. (2023). Nat. Commun., 14(1):4259.
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Oncogenic IDH mutations increase heterochromatin-related replication stress without impacting homologous recombination. Schvartzman, J.-M., Forsyth, G., Walch, H., Chatila, W., Taglialatela, A., Lee, B.J., Zhu, X., Gershik, S., Cimino, F.V., Santella, A., Menghrajani, K., Ciccia, A., Koche, R., Sánchez-Vega, F., Zha, S., and Thompson, C.B. (2023). Mol. Cell, 83(13):2347-2356.e8.
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RFWD3 promotes ZRANB3 recruitment to regulate the remodeling of stalled replication forks. Moore, C.E., Yalcindag, S.E., Czeladko, H., Ravindranathan, R., Hanthi, Y.W., Levy, J.C., Sannino, V., Schindler, D., Ciccia, A., Costanzo, V., and Elia, A.E.H.(2023). J. Cell Biol., 222 (5): e202106022.
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The DNA Damage Response and Inflammation in Cancer. Klapp, V., Alvarez-Abril, B., Leuzzi, G., Kroemer, G., Ciccia, A., Galluzzi, L.(2023). Cancer Discovery, OF1–OF25.
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Arginine shortage induces replication stress and confers genotoxic resistance by inhibiting histone H4 translation and promoting PCNA ubiquitination. Wang, Y.C., Kelso, A.A., Karamafrooz, A., Chen, Y.H., Chen, W.K., Cheng, C.T., Qi, Y., Gu, L., Malkas, L., Taglialatela, A., Kung, H.J., Moldovan, G.L., Ciccia, A., Stark, J.M., and Ann, D.K. (2023). Cell Reports, 42(4):112296.
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2022
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A genetic roadmap to the response to genotoxic agents in human cells. Ciccia, A., Greenberg, R.A., Lees-Miller, S.P., and Nussenzweig, A. (2022). Fac. Rev. 11:35.
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Partial loss-of-function mutations in GINS4 lead to NK cell deficiency with neutropenia. Conte, M.I., Poli, M.C., Taglialatela, A., Leuzzi, G., Chinn, I.K., Salinas, S.A., Rey-Jurado, E., Olivares, N., Veramendi-Espinoza, L., Ciccia, A., Lupski, J.R., Aldave Becerra, J.C., Mace, E.M., and Orange, J.S. (2022). JCI Insight 7(21):e154948.
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Histone methylation antagonism drives tumor immune evasion in squamous cell carcinomas. Li, Y., Goldberg, E.M., Xu, X., McGuire, J.T., Leuzzi, G., Karagiannis, D., Tate, T., Farhangdoost, N., Horth, C., Dai, E., Li, Z., Zhang, Z., Izar, B., Que, J., Ciccia, A., Majewski, J., Yoon, A.J., Ailles, L., Mendelsohn, C.L., and Lu, C. (2022). Mol. Cell 82(20), 3901-3918.
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Replication stress impairs chromosome segregation and preimplantation development in human embryos. Palmerola, K.L., Amrane, S., De Los Angeles, A., Xu, S., Wang, N., de Pinho, J., Zuccaro, M.V., Taglialatela, A., Massey, D.J., Turocy, J., Robles, A., Subbiah, A., Prosser, B., Lobo, R., Ciccia, A., Koren, A., Baslan, T., and Egli, D. (2022). Cell 185 (16), 2988-3007.
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Strand annealing and motor driven activities of SMARCAL1 and ZRANB3 are stimulated by RAD51 and the paralog complex. Halder, S., Ranjha, L., Taglialatela, A., Ciccia, A., and Cejka, P. (2022). Nucleic Acids Res. 50(14): 8008-8022.
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CRISPR-based genome editing through the lens of DNA repair. Nambiar, T.S., Baudrier, L., Billon, P., and Ciccia, A. (2022). Mol. Cell 82(2), 348-388.
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2021
Assessing kinetics and recruitment of DNA repair factors using high content screens. Martinez-Pastor, B., Silveira, G.G., Clarke, T.L., Chung, D., Gu, Y., Cosentino, C., Davidow, L.S., Mata, G., Hassanieh, S., Salsman, J., Ciccia, A., Bae, N., Bedford, M.T., Megias, D., Rubin, L.L., Efeyan, A., Dellaire, G., and Mostoslavsky, R. (2021). Cell Reports 37(13), 110176.​
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Towards a CRISPeR understanding of homologous recombination with high-throughput functional genomics. Hayward, S.B., and Ciccia, A. (2021). Curr. Opin. Genet. Dev. 71, 171-181
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REV1-Polζ maintains the viability of homologous recombination-deficient cancer cells through mutagenic repair of PRIMPOL-dependent ssDNA gaps. Taglialatela, A., Leuzzi, G., Sannino, V., Cuella-Martin, R., Huang, J.W., Wu-Baer, F., Baer, R., Costanzo, V., and Ciccia, A. (2021). Mol. Cell 81(19), 4008-4025.
Selected for the cover of Molecular Cell
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Functional interrogation of DNA damage response variants with base editing screens. Cuella-Martin, R., Hayward, S.B., Fan, X., Chen, X., Huang, J.W., Taglialatela, A., Leuzzi, G., Zhao, J., Rabadan, R., Lu, C., Shen, Y., and Ciccia, A. (2021). Cell 184(4), 1081-1097.
Highlights: CRISPR base editor screens identify variant function at scale. Parrish, P.C.R., and Berger, A.H. (2021).
Mol. Cell 81(4), 647-648; Finding function with base editing screens. Koch, L. (2021). Nature Reviews Genetics
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2020
HATtracting nucleases to stalled forks. Leuzzi, G., Taglialatela, A., and Ciccia, A. (2020). Mol. Cell 80(2), 177-180.
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Time for remodeling: SNF2-family DNA translocases in replication fork metabolism and human disease. Joseph, S.A., Taglialatela, A., Leuzzi, G., Huang, J.W., Cuella-Martin, R., and Ciccia, A. (2020). DNA Repair 95, 102943.
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MCM8IP activates the MCM8-9 helicase to promote DNA synthesis and homologous recombination upon DNA damage. Huang, J.W., Taglialatela, A., Acharya, A., Leuzzi, G., Nambiar, T.S., Cuella-Martin, R., Hayward, S.B., Joseph, S.A., Brunette, G.J., Anand, R., Soni, R.K., Clark, N.L., Bernstein, K.A., Cejka, P., and Ciccia, A. (2020). Nat. Commun. 11, 2948.
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Detection of marker-free precision genome editing and genetic variation through the capture of genomic signatures. Billon, P., Nambiar, T.S., Hayward, S.B., Zafra, M.P., Schatoff, E.M., Oshima, K., Dunbar, A., Wong, M., Breinig, M., Park, Y.C., Tschaharganeh, D.F., Levine, R.L., Baer, R., Ferrando, A.A., Dow, L.E., and Ciccia, A. (2020). Cell Reports 30(10), 3280-3295.
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2019
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Stimulation of CRISPR-mediated homology-directed repair by an engineered RAD18 variant. Nambiar, T.S., Billon, P., Diedenhofen, G., Hayward, S.B., Taglialatela, A., Cai, K., Huang, J.W., Leuzzi, G., Cuella-Martin, R., Palacios, A., Gupta, A., Egli, D., and Ciccia, A. (2019). Nat. Commun. 10, 3395.
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2018
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The BRCT domains of the BRCA1 and BARD1 tumor suppressors differentially regulate homology-directed repair and stalled fork protection. Billing, D., Horiguchi, M., Wu-Baer, F., Taglialatela, A., Leuzzi, G., Alvarez, S., Jiang, W., Zha, S., Szabolcs, M., Lin, C.-S., Ciccia, A., and Baer, R. (2018). Mol. Cell 72(1), 127-139.
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2017
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Restoration of replication fork stability in BRCA1- and BRCA2-deficient cells by inactivation of SNF2-family fork remodelers. Taglialatela, A., Alvarez, S., Leuzzi, G., Sannino, V., Ranjha, L., Huang, J.W., Madubata, C., Anand, R., Levy, B., Rabadan, R., Cejka, P., Costanzo, V., Ciccia, A. (2017). Mol. Cell 68(2), 414-430.
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CRISPR-mediated base editing enables efficient disruption of eukaryotic genes through induction of STOP codons. Billon, P., Bryant, E.E., Joseph, S.A., Nambiar, T.S., Hayward, S.B., Rothstein, R., Ciccia, A. (2017). Mol. Cell 67(6), 1068-1079.
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Replication fork slowing and reversal upon DNA damage require PCNA polyubiquitination and ZRANB3 DNA translocase activity. Vujanovic, M., Krietsch, J., Raso, M.C., Terraneo, N., Zellweger, R., Schmid, J.A., Taglialatela, A., Huang, J.W., Holland, C.L., Zwicky, K., Herrador, R., Jacobs, H., Cortez, D., Ciccia, A., Penengo, L., Lopes, M. (2017). Mol. Cell 67(5), 882-890.
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SMARCAL1-mediated fork reversal triggers MRE11-dependent degradation of nascent DNA in the absence of BRCA2 and stable RAD51 nucleofilaments. Kolinjivadi, A.M., Sannino, V., De Antoni, A., Zadorozhny, K., Kilkenny, M., Técher, H., Baldi, G., Shen, R., Ciccia, A., Pellegrini, L., Krejci, L., Costanzo, V. (2017). Mol. Cell 67(5), 867-881.
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2014-16
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Stressing out about RAD52. Ciccia, A.* and Symington, L.S.* (2016). Mol. Cell 64(6), 1017-1019.
* Corresponding authors
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A systematic analysis of factors localized to damaged chromatin reveals PARP-dependent recruitment of transcription factors. Izhar, L., Adamson, B., Ciccia, A., Lewis, J., Pontano-Vaites, L., Leng, Y., Liang, A.C., Westbrook, T.F., Harper, J.W., and Elledge, S.J. (2015). Cell Reports 11(9), 1486-1500.
Treacher Collins syndrome TCOF1 protein cooperates with NBS1 in the DNA damage response. Ciccia, A.*, Huang, J.W., Izhar, L., Sowa, M.E., Harper, J.W., and Elledge, S.J.* (2014). Proc. Natl. Acad. Sci U S A 111, 18631-18636.
* Corresponding authors
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2003-13
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Protein interaction discovery using parallel analysis of translated ORFs (PLATO). Zhu, J., Larman, H.B., Gao, G., Somwar, R., Zhang, Z., Laserson, U., Ciccia, A., Pavlova, N., Church, G., Zhang, W., Kesari, S., and Elledge, S.J. (2013). Nat. Biotechnol. 31(4), 331-334.
Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Ciccia, A., Nimonkar, A.V., Hu, Y., Hajdu, I., Achar, Y.J., Izhar, L., Petit, S.A., Adamson, B., Yoon, J.C., Kowalczykowski, S.C., Livingston, D.M., Haracska, L., and Elledge, S.J. (2012). Mol. Cell 47(3), 396-409.
Wolf-Hirschhorn syndrome candidate 1 is involved in the cellular response to DNA damage. Hajdu, I., Ciccia, A., Lewis, S.M., and Elledge, S.J. (2011). Proc. Natl. Acad. Sci. U S A 108(32), 13130-13134.
Proliferating cell nuclear antigen (PCNA)-associated KIAA0101/PAF15 protein is a cell cycle-regulated anaphase-promoting complex/cyclosome substrate. Emanuele, M.J., Ciccia, A., Elia, A.E., and Elledge, S.J. (2011). Proc. Natl. Acad. Sci. U S A 108(24), 9845-9850.
Autoantigen discovery with a synthetic human peptidome. Larman, H.B., Zhao, Z., Laserson, U., Li, M.Z., Ciccia, A., Gakidis, M.A., Church, G.M., Kesari, S., Leproust, E.M., Solimini, N.L., Elledge, S.J. (2011). Nat. Biotechnol. 29(6), 535-541.
The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo. Meerbrey, K.L., Hu, G., Kessler, J.D., Roarty, K., Li, M.Z., Fang, J.E., Herschkowitz, J.I., Burrows, A.E., Ciccia, A., Sun, T., Schmitt, E.M., Bernardi, R.J., Fu, X., Bland, C.S., Cooper, T.A., Schiff, R., Rosen, J.M., Westbrook, T.F., Elledge, S.J. (2011). Proc. Natl. Acad. Sci. U S A 108(9), 3665-3670.
A genome-wide camptothecin sensitivity screen identifies a mammalian MMS22L-NFKBIL2 complex required for genomic stability. O'Connell, B.C., Adamson, B., Lydeard, J.R., Sowa, M.E., Ciccia, A., Bredemeyer, A.L., Schlabach, M. Gygi, S.P., Elledge, S.J., and Harper, J.W. (2010). Mol. Cell 40(4), 645-657.
The DNA damage response: making it safe to play with knives. Ciccia, A., and Elledge, S.J. (2010). Mol. Cell 40(2) 179-204.
The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Ciccia, A., Bredemeyer, A.L., Sowa, M.E., Terret, M.E., Jallepalli, P.V., Harper, J.W., and Elledge, S.J. (2009). Genes Dev. 23(20), 2415-2425.
FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Collis, S.J, Ciccia, A., Deans, A.J., Horejsi, Z., Martin, J.S., Maslen, S.L., Skehel, J.M. Elledge S.J., West, S.C. and Boulton, S.J. (2008). Mol. Cell 32(3), 313- 324.
Structural and functional relationships of the XPF/MUS81 family of proteins. Ciccia, A., McDonald, N., and West, S.C. (2008). Annu. Rev. Biochem. 77, 259-287.
Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Ciccia, A., Ling, C., Coulthard, R., Yan, Z., Xue, Y., Meetei, A.R., Laghmani el, H., Joenje, H., McDonald, N., de Winter, J.P., Wang, W., and West, S.C. (2007). Mol. Cell 25(3), 331-343.
EME1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. Abraham, J, Lemmers, B., Hande, M. P., Moynahan, M. E., Chahwan, C., Ciccia, A., Essers, J., Hanada, K., Chahwan, R., Khaw, A. K., McPherson, P., Shehabeldin, A., Laister, R., Arrowsmith, C., Kanaar, R., West, S.C., Jasin, M., Hakem, R. (2003). EMBO J. 22, 6137-6147.
Identification and characterization of the human MUS81-EME1 endonuclease. Ciccia, A., Constantinou, A., and West, S. C (2003). J. Biol. Chem. 278(27), 25172-25178.