Publications

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[* co-first authors; co-corresponding authors]


2024

Onconeural antigen NOVA1 dysregulates alternative splicing in breast cancer

Moakley, D.F., Zhang, C.

In submission.

preprint


Disentangling the splicing factor programs underlying complex molecular phenotypes

Anglada-Girotto, M., Moakley, D.F., Zhang, C., Miravet-Verde, S., Califano, A., Serrano, L.

In submission.

preprint


Reverse engineering neuron type-specific and type-orthogonal splicing-regulatory networks using single-cell transcriptomes

Moakley, D.F., Campbell, M., Anglada-Girotto, M., Feng, H., Califano, A., Au, E., Zhang, C.

In submission.

preprint software


Reference-informed prediction of alternative splicing and splicing-altering mutations from sequences

Xu, C.*, Bao, S.*, Wang, Y., Li, W., Chen, H., Shen, Y., Jiang, T. †, Zhang, C.

Genome Res. 34:1052–1065.

PubMedPDF software


Lineage-specific splicing regulation reveals adaptation of MAPT function in the primate brain

Recinos, Y.*, Bao, S.*, Wang, X.*, Phillips, B.L., Weyn-Vanhentenryck, S.M., Swanson, M.S., Zhang, C.

Cell Genomics, https://doi.org/10.1016/j.xgen.2024.100563.

Preview: Aya, F. and J. Valcarcel (2024). Shaping human brain development and vulnerability through alternative splicing. Cell Genom 4: 100584.

PubMed PDF


CRISPR/dCas13d-based deep screening of proximal and distal splicing-regulatory elements

Recinos, Y., Ustianenko, D., Yeh, Y.T., Wang, X., Jacko, M., Yesantharao, L.V., Wu, Q., Zhang, C.

Nat Commun. 15:3839.

PubMed PDF software


Structure-based prediction and characterization of photo-crosslinking in native protein-RNA complexes

Feng,H., Lu, X.-J., Maji, S., Liu, L., Ustianenko, M., Rudnick, N., Zhang, C.

Nat Commun.15: 2279.

PubMed PDF software

2023

Lineage tracing and single-cell profiling unravel coordinated bone marrow stromal remodeling and identify glial cells as a therapeutic target in myelofibrosis

Sarkaria, S., Zhou, J., Bao, S., Zhao, W., Fang, Y., Que, J., Bhagat, G., Zhang, C., Ding, L.

Cell Stem Cell, 30:832-850.e6.

PubMed PDF


Multiomics analyses reveal DARS1-AS1/YBX1-controlled posttranscriptional circuits promoting glioblastoma tumorigenesis/radioresistance

Zheng, C., Wei, Y., Zhang, Q., Sun, M., Wang, Y., Hou, J., Zhang, P., Lv, X., Su, D., Jiang, Y., Gumin, J., Sahni, N., Hu, B., Wang, W., Chen, X., McGrail, D.J., Zhang, C., Huang, S., Xu, H., Chen, J., Lang, F.F., Hu, J., Chen, Y.

Sci Adv. 2023 9:eadf3984.

PubMed PDF


Trans-cellular control of synapse properties by a cell type-specific splicing regulator

Traunmüller, L., Schulz, J., Feng, H., Furlanis, E., Gomez, A., Schreiner, D., Bischofberger, J., Zhang, C., Scheiffele, P.

Cell Rep. 42: 112183.

PubMed PDF

2022

The germ cell-specific RNA binding protein RBM46 is essential for spermatogonial differentiation in mice

Peart, N. J., Johnson, T. A., Lee, S., Sears, M. J., Yang, F., Quesnel-Vallieres, M., Feng, H., Recinos, Y., Barash, Y., Zhang, C., Hermann, B. P., Wang, P. J., Geyer, C. B., Carstens, R.

PLoS Genet. 18: e1010416.

PubMed PDF


Endothelial Notch signaling directly regulates the small GTPase RND1 to facilitate Notch suppression of endothelial migration

Swaminathan, B., Youn, S.-W. Naiche, L.A., Du, J., Villa, S.R., Metz, J.B., Feng, H., Zhang, C., Kopan, R., Sims, P.A., Kitajewski, J.K. 2022.

Sci Rep 12:1655. doi: 10.1038/s41598-022-05666-1.

PubMed PDF

2021

Vascular-derived SPARC and SerpinE1 regulate interneuron tangential migration and maturation

Genestine, M., Ambriz, D., Crabtree, G.W., Dummer, P., Molotkova, A., Quintero, M., Mela, A., Biswas, S., Feng, H., Zhang, C., Canoll, P., Hargus, G., Agalliu, D., Gogos, J.A., Au, E.

eLife. 10:e56063. DOI: 10.7554/eLife.56063.

PubMed PDF


Gain of toxic function by long-term AAV9-mediated SMN overexpression in the sensory-motor circuit

Alstyne, M.V., Tattoli1,I., Delestree,N., Recinos, Y., Workman, E., Shihabuddin, L.S., Zhang, C., Mentis, G.Z., Pellizzoni, L., 2021.

Nat Neurosci. https://doi.org/10.1038/s41593-021-00827-3.

PubMed PDF


Complexity and graded regulation of neuronal cell type-specific alternative splicing revealed by single-cell RNA sequencing

Feng, H., Moakley, D.F., Chen, S., McKenzie, M.G., Menon, V., Zhang, C. 2021.

Proc. Nat. Acad. Sci. USA. 118:e2013056118

PubMed PDF

2020

Alternative splicing at neuroligin site A regulates glycan interaction and synaptogenic activity

Oku, S., Feng, H., Connor, S.A., Toledo, A., Zhang, P., Zhang, Y., Thoumine, O, Zhang, C., Craig, A.M. 2020. eLife. 9:e58668. PubMed PDF


Proteome-scale analysis of phase-separated proteins in immunofluorescence images

Yu, C., Shen, B., You, K., Huang, Q., Shi, M., Wu, C., Chen, Y., Zhang, C., Li, T. , 2020.

Brief Bioinform. DOI: 10.1093/bib/bbaa187.

PubMed PDF


Brain translation – a feather tips the scale

Ustianenko, D., McKenzie, M.G., Zhang, C., 2020.

Mol Cell. 77:1155-1156. (preview)

PubMed PDF

2019

Modeling RNA-binding protein specificity in vivo by precisely registering protein-RNA crosslink sites

Feng, H.*, Bao, S.*, Rahman, M.,A., Weyn-Vanhentenryck, S.M., Khan, A., Wong, J., Shah, A., Flynn, E.D., Krainer, A.R., Zhang, C., 2019.

Mol Cell. 74:1189-1204.E6.

PubMed PDF software/database


A role for sensory end organ‐derived signals in regulating muscle spindle proprioceptor phenotype

Wu, D., Schieren, I., Qian, Y., Zhang, C., Jessell, T.M., de Nooij, J.C., 2019.

J Neurosci. 39:4252-4267.

PubMed PDF


Stage-specific requirement for Mettl3-dependent m6A mRNA methylation during haematopoietic stem cell differentiation

Lee, H. Bao, S., Qian, Y., Geula, S., Leslie, J., Zhang, C., Hanna, J., Ding, L. , 2019.

Nat Cell Biol. 6:700-709.

PubMed PDF


The splicing code goes deep

Bao, S., Moakley, D.,F., Zhang, C., 2019.

Cell, 176:414-416 (preview).

PubMed PDF

2018

DAZL regulates germ cell survival through a network of polyA-proximal mRNA interactions

Zagore, L.L., Sweet, T.J., Hannigan, M.M., ‘’‘Weyn-Vanhentenryck, S.M.’‘’, Jobava, R., Hatzoglou, M., Zhang, C., Licatalosi, D.D. 2018.

Cell Rep. 25: 1225-1240.

PubMed PDF


Special issue on RNA processing and regulation

Xiao, X.†, Zhang, C.† 2018.

Quant Biol, 6:193-194. (Editorial)

PDF Content of the special issue


Cell type-specific CLIP reveals that NOVA regulates cytoskeleton interactions in motoneurons

Yuan, Y., Xie, S., Darnell, J. C., Darnell, A. J., Saito, Y., Phatnani, H., Murphy, E. A., Zhang, C., Maniatis, T. & Darnell, R. B. 2018.

Genome Biol, 19:117.

PubMed PDF


LIN28 selectively modulates a subclass of let-7 microRNAs

Ustianenko,D.*, Chiu,H-S*, Treiber, T.*, Weyn-Vanhentenryck, S.M., Treiber, N., Meister, G., Sumazin,P.†, Zhang, C.† 2018.

Mol Cell, 71:271-283.e5. (cover story)

PubMed PDF

LIN28 cover.jpg


Precise temporal regulation of alternative splicing during neural development

Weyn-Vanhentenryck, S. M.*, Feng, H.*, Ustianenko, D., Duffié, R., Yan, Q., Jacko, M., Martinez, J. C., Goodwin, M., Zhang, X., Hengst, U., Lomvardas, S., Swanson, M. S. & Zhang, C. 2018.

Nat Commun,9: 2189.

PubMed PDF software


Systematic reconstruction of autism biology from massive genetic mutation profiles

Luo,W., Zhang,C., Jiang,Y., Brouwer,C.R. 2018.

Science Advances, 4:e1701799.

PubMed PDF


Rbfox splicing factors promote neuronal maturation and axon initial segment assembly

Jacko, M., Weyn-Vanhentenryck, S. M., Smerdon, J. W., Yan, R., Feng, H., Williams, D. J., Pai, J., Xu, K., Wichterle, H.† & Zhang, C.† 2018.

Neuron, 97: 853-868.e6.

PubMed PDF

-Issue highlight.

-Press release: “Research Unveils a Developmental Splicing Program Controlling Neuronal Maturation and Excitability”. CUMC News Room. http://newsroom.cumc.columbia.edu/blog/2018/02/08/new-insights-neurons-become-mature-excitable/.


Capturing the interactome of newly transcribed RNA

Bao, X., Guo, X., Yin, M., Tariq, M., Lai, Y., Kanwal, S., Zhou, J., Li, N., Lv, Y., Pulido-Quetglas, C., Wang, X., Ji, L., Khan, M. J., Zhu, X., Luo, Z., Shao, C., Lim, D.-H., Liu, X., Li, N., Wang, W., He, M., Liu, Y.-L., Ward, C., Wang, T., Zhang, G., Wang, D., Yang, J., Chen, Y., Zhang, C., Jauch, R., Yang, Y.-G., Wang, Y., Qin, B., Anko, M.-L., Hutchins, A. P., Sun, H., Wang, H., Fu, X.-D., Zhang, B. & Esteban, M. A. 2018.

Nat Meth, 15:213-220.

PubMed PDF

2017

Microexons: discovery, regulation, and function

Ustianenko,D., Weyn-Vanhentenryck, S.M., Zhang, C. 2017.

WIRES RNA, e1418. DOI: 10.1002/wrna.1418 (review)

PubMed PDF


A cell type-specific expression signature predicts haploinsufficient autism-susceptibility genes

Zhang,C.*,†, Shen,Y.*,† 2017.

Human Mutation, 38: 204-215.

PubMed PDF preprint at bioRxiv

-News release: “Third-party gene scores added to SFARI Gene”. SFARI. https://www.sfari.org/2017/12/14/third-party-gene-scores-added-to-sfari-gene/.


CLIP Tool Kit (CTK): a flexible and robust pipeline to analyze CLIP sequencing data

Shah,A., Qian,Y., Weyn-Vanhentenryck,S.M., Zhang,C. 2017.

Bioinformatics. 33:566-567. DOI: 10.1093/bioinformatics/btw653.

PubMed PDF Software

2016

mCarts: genome-wide prediction of clustered sequence motifs as binding sites for RNA-binding proteins

Weyn-Vanhentenryck,S.M., Zhang,C. 2016.

Methods Mol Biol. 1421:215-226.

PubMed PDF

2015

MBNL sequestration by toxic RNAs and RNA misprocessing in the myotonic dystrophy brain

Goodwin, M., Mohan, A. Batra, R., Lee, K.-Y., Charizanis, K., Francisco Jose Fernandez-Gomez, F.J., Eddarkaoui, S., Sergeant, N., Buee, L., Kimura, T., Clark, H.B., Dalton, J., Takamura, K., Weyn-Vanhentenryck, S.M. , Zhang, C., Reid, T., Ranum, L.P.W., Day, J.W., Swanson, M.S. 2015.

Cell Rep. 12:1159-1168.

PubMed PDF


mRIN for direct assessment of genome-wide and gene-specific mRNA integrity from large-scale RNA sequencing data

Feng, H., Zhang, X., Zhang, C. , 2015.

Nat Comm. 6:7816. doi: 10.1038/ncomms8816.

PubMed PDF Software

- Research highlights, “How good are those RNA-seq data?”, Nature Methods, 12:910 (2015).


Systematic discovery of regulated and conserved alternative exons in the mammalian brain reveals NMD modulating chromatin regulators.

Yan, Q.*, Weyn-Vanhentenryck, S.M.*,Wu, J., Sloan, S.A., Zhang, Y., Chen, K., Wu, J.-Q., Barres, B.A.†, Zhang, C.†, 2015.

Proc. Nat. Acad. Sci. USA. 112:3445-3450.

PubMed PDF Supp Info

2014

Loss of MBNL function leads to disruption of developmentally regulated alternative polyadenylation in RNA-mediated disease

Batra, R., Charizanis, K., Manchanda, M., Mohan, A., Li, M., Finn, D.J., Goodwin, Zhang, C., Sobczak,K., Thornton, C.A., Swanson, M.S. 2014.

Mol Cell. 56: 311-322.

PubMed PDF


An RNA-Sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex

Zhang, Y., Chen, K., Sloan, S., Bennett, M.L., Scholze, A.R., O’Keeffe, S., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., Deng, S., Liddelow, S.A., Zhang, C., Daneman, R., Maniatis, T., Barres, B.A., Wu, J.-Q. 2014.

J Neurosci. 34:11929-11947.

PubMed PDF


HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism

Weyn-Vanhentenryck, S.M.*, Mele,A.*, Yan,Q.*, Sun,S., Farny,N., Zhang,Z., Xue,C., Herre,M., Silver,P.A., Zhang,M.Q., Krainer,A.R., Darnell,R.B. †, Zhang,C. † 2014.

Cell Rep. 6:1139-1152.

PubMed PDF software


Mapping Argonaute and conventional RNA-binding protein interactions with RNA at single-nucleotide resolution using HITS-CLIP and CIMS analysis

Moore, M.*, Zhang, C.*, Gantman, E.C., Mele, A., Darnell, J.C., Darnell, R.B. 2014.

Nat Protocols, 9:263-293.

PubMed PDF software

2013

Progressive impairment of muscle regeneration in Muscleblind-like 3 isoform knockout mice

Poulos, M.G., Batra, R., Li, M., Yuan, Y., Zhang, C., Darnell, R.B., Swanson, M.S. 2013.

Hum Mol Genet. 22:3547-3558.

PubMed PDF


Prediction of clustered RNA-binding protein motif sites in the mammalian genome

Zhang, C. †, Lee, K.-Y., Swanson, M.S., Darnell, R.B. † 2013.

Nucleic Acids Res. 41:6793-6807.

PDF software


OLego: Fast and sensitive mapping of spliced mRNA-Seq reads using small seeds

Wu,J., Anczukow,O., Krainer,A.R., Zhang,M.Q. †, Zhang,C. †, 2013.

Nucleic Acids Res. 41:5149-5163.

PubMed PDF software



[Publications before my own lab]

2012

NOVA-dependent regulation of cryptic NMD exons controls synaptic protein levels after seizure

Eom,T., Zhang,C., Wang,H., Lay,K., Fak,J., Noebels,J.L., Darnell,R.B. 2012.

eLife, 2:e00178.

PubMed PDF


Neuronal Elav-like (Hu) Proteins Regulate RNA Splicing and Abundance to Control Glutamate Levels and Neuronal Excitability

Ince-Dunn, G., Okano, H.J., Jensen, K.B., Park, W.Y., Zhong, R., Ule, J., Mele,A., Fak, J.J., Yang, C., Zhang,C., Yoo, J., Herre, M., Okano, H., Noebels, J.L., Darnell, R.B., 2012.

Neuron, 75:1067-1080.

PubMed PDF


The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult

Zhang,B., Arun,G., Mao,Y.S., Lazar,Z., Hung,G., Bhattacharjee,G., Xiao,X., Booth,C.J., Wu,J., Zhang,C., Spector,D.L., 2012.

Cell Reports, 2:111-123.

PubMed PDF


Muscleblind-like 2 mediated alternative splicing in the developing brain and dysregulation in myotonic dystrophy

Charizanis, K., Lee, K.-Y., Batra, R., Goodwin, M., Zhang,C., Yuan, Y., Shuie, L., Cline, M., Scotti, M.M., Xia, G., Kumar,A., Ashizawa, T., Clark, H.B., Kimura, T., Takahashi, M.P., Fujimura, H., Jinnai, K., Yoshikawa, H., Pereira,M.G., Gourdon,G., Sakai,N., Nishino,S., Foster,T.C., Ares, M. Jr, Darnell, R.B. Swanson, M.S., 2012.

Neuron, 75:437-450.

PubMed PDF


Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain

Licatalosi,D.D., Yano,M., Fak,J.J., Mele,A., Grabinski,S.E., Zhang,C., Darnell,R.B., 2012.

Genes Dev, 26:1626-1642.

PubMed PDF

2011

Identification of novel androgen-regulated pathways and mRNA isoforms through genome-wide exon-specific profiling of the LNCaP transcriptome

Rajan P., Dalgliesh, C., Carling, P., Buist, T., Zhang,C., Grellscheid, S., Armstrong, K., Stockley, J., Simillion, C., Gaughan, L., Kalna, G., Zhang, M.Q., Robson, C., Leung, H., Elliott, D. 2011.

PLoS One, 6: e29088.

PubMed PDF


Study of FoxA pioneer factor at silent genes reveals Rfx-repressed enhancer at Cdx2 and a potential indicator of esophageal adenocarcinoma development

Watts, J.A., Zhang,C., Klein-Szanto, A.J., Kormish, J.D., Fu, J., Zhang, M.Q., Zaret, K.S. 2011.

PLoS Genet, 7: e1002277.

PubMed PDF


FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism

Darnell, J.C., Van Driesche, S.J., Zhang,C., Hung, K.Y.S., Mele, A., Fraser, C.E., Stone, E.F., Chen, C., Fak, J.J., Chi, S.W., Licatalosi, D.D., Richter, J.D., Darnell, R.B., 2011.

Cell, 146:247-261.

PubMed PDF


Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data

Zhang,C.†, Darnell, R.B.† 2011.

Nat. Biotech. 29:607-614.

PubMed PDF software

2010

Integrative modeling defines the Nova splicing-regulatory network and its combinatorial controls

Zhang,C.†, Frias, M.A., Mele, A., Ruggiu, M., Eom, T., Marney, C.B., Wang, H., Licatalosi, D.D., Fak, J.J., Darnell, R.B.† 2010.

Science. 329: 439-443. PubMed PDF

- Editor’s choice, Pickersgill, H. 2010. Making the Final Cut. Sci. Signal. 3:ec234;

- Nominated by leading researchers as one of the 33 papers that represent breakthroughs in computational biology in 2010. Mak H.C., 2011. Trends in computational biology-2010. Nat Biotech. 29, doi:10.1038/nbt.1747.


Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence

Chicas, A., Wang, X., Zhang,C., McCurrach, M., Zhao Z., Ozlem, M., Dickins, R., Narita, M., Zhang, M.Q., and Lowe, S.W. 2010.

Cancer Cell. 17:376-387.

PubMed PDF

- Comment in Cancer Cell. 2010 Apr 13;17(4):313-4.

2008 or earlier

Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines

Castle, J.C., Zhang,C., Shah, J.K., Kulkarni, A.V., Cooper, T.A., Johnson, J.M. 2008.

Nature Genet. 40:1416-1425.

PubMed PDF


Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2

Zhang,C.*, Zhang, Z.*, Castle, J., Sun, S., Johnson, J., Krainer, A.R. and Zhang, M.Q. 2008.

Genes Dev. 22:2550-2563.

PubMed PDF


An RNA landscape of evolution for optimal exon and intron discrimination

Zhang,C., Li, W.-H., Krainer, A.R. and Zhang, M.Q. 2008.

Proc. Nat. Acad. Sci. USA. 105:5797-802.

PubMed PDF


Dual-specificity splice sites function alternatively as 5' and 3' splice sites

Zhang,C., Hasting, M.L., Krainer, A.R., Zhang, M.Q. 2007.

Proc. Nat. Acad. Sci. USA. 104(38): 15028-15033

PubMed PDF.


Evolutionary impact of limited splicing fidelity in mammalian genes

Zhang,C., Krainer A.R., Zhang, M.Q. 2007.

Trends Genet. 23(10): 484-488.

PubMed PDF


An increased specificity score matrix for the prediction of SF2/ASF-specific exonic splicing enhancers

Smith, P.J., Zhang,C., Wang, J., Chew, S.L., Zhang, M.Q., Krainer, A.R. 2006.

Hum Mol Genet, 15:16):2490-2508.

PubMed PDF


Profiling alternatively spliced mRNA isoforms for prostate cancer classification

Zhang,C., Li, H.-R., Fan, J.-B., Wang-Rodriguez, J., Downs, T., Fu, X.-D. and Zhang, M.Q. 2006.

BMC Bioinformatics, 7:202.

PubMed PDF


Neighbor Number, Valley Seeking and Clustering

Zhang,C., Zhang, X., Zhang, M.Q. and Li, Y. 2007.

Pattern Recognition Letters,28:173-180.


A Clustering property of highly-degenerate transcription factor binding sites in the mammalian genome

Zhang,C., Xuan, Z., Otto, S., Hover, J.R., McCorkle, S.R., Mandel, G. and Zhang, M.Q. 2006.

Nucl Acids Res, 34: 2238-2246.

PubMed PDF


Significance of Gene Ranking for Classification of Microarray Samples

Zhang,C.*, Lu, X.* and Zhang, X. 2005.

IEEE/ACM Transactions on Computational Biology and Bioinformatics, 3(3): 312-320.

PubMed

Book Chapters

Identification of Splicing Factor Target Genes by High-Throughput Sequencing

Zhang,C., Zhang,M.Q. 2012.

Chapter 51 in Alternative pre-mRNA Splicing: Theory and Protocols. (S. Stamm, C.W. J. Smith, R. Lührmann, ed). Wiley-VCH Verlag GmbH & Co.


Functional in sillico analysis of gene regulatory polymorphism

Zhang,C., Zhao,X. and Zhang,M.Q. 2006.

Chapter 12. In Bioinformatics for Geneticists: A Bioinformatics primer for the analysis of genetic data.  2nd Ed. (M.R. Barnes, ed.)  John Wiley & Sons, LTD.


Biomedical literature mining

Zhang,C., Zhang,M.Q. 2007.

Chap 10. in Introduction to Bioinformatics: A workbook approach. (V. Mathura ed) Elsevier.