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Publications

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The Single-Cell Opioid Responses in the Context of HIV (SCORCH) Consortium

Ament, S., Campbell, R., Lobo, M.K., Receveur, J., Agrawal, K., Borjabad, A., Chang, L., Clarke, D., Cleary, J., Byrareddy, S., Emani, P., Gabuzda, D., Gaulton, K., Giglio, M., Giorgi, F., Gok, B., Guda, C., Hadas, E., Herb, B.R., Hu, W., Huttner, A., Ishmam, M., Jacobs, M., Kelschenbach, J., Kim, D.-W., Lee, C., Liu, X., Liu, S., Madras, B., Mahurkar, A., Mash, D., Mukamel, E., Niu, M., O’Connor, R., Pagan, C., Pang, A., Pillai, P., Repunte-Canonigo, V., Ruzicka, W.R., Stanley, J., Tickle, T., Tsai, S.-Y., Wang, A., Wills, L., Wilson, A., Wright, S., Xu, S., Yang, J., Zand, M., Zhang, L., Zhang, J., Akbarian, S., Buch, S., Cheng, C., Corley, M., Fox, H., Gerstein, M., Gummuluru, S., Heiman, M., Ho, Y.-C., Kellis, M., Kenny, P., Kluger, Y., Milner, T., Moore, D., Morgello, S., Ndhlovu, L., Rana, T., Sanna, P.P., Satterlee, J., Sestan, N., Spector, S., Spudich, S., Tilgner, H., Volsky, D., White, O., Williams, D., and Zeng, H. (2024). Molecular Psychiatry, doi: 10.1038/s41380-024-02620-7.

TDP-43 Proteinopathy in ALS is Triggered by Loss of ASRGL1 and Associated with HML-2 Expression

Garcia-Montojo, M., Fathi, S., Rastegar C, Simula, E.R., Doucet-O’Hare, T., Cheng, Y.H.H., Abrams, R.P.M., Pasternack, N., Malik, N., Bachani, M., Disanza, B., Maric, D., Lee, M.H., Wang, H., Santamaria, U., Li, W., Sampson, K., Lorenzo, J.R., Sanchez, I.E., Mezghrani, A., Li, Y., Sechi, L.A., Pineda, S., Heiman, M., Kellis, M., Steiner, J., and Nath, A. (2024). Nature Communications, 15(1):4163.

Single-Cell Dissection of the Human Motor and Prefrontal Cortices in ALS and FTLD

Pineda, S.S., Lee, H., Ulloa-Navas, M.J., Linville, R.M., Garcia, F.J., Galani, K., Engelberg-Cook, E., Castanedes, M.C., Fitzwalter, B.E., Pregent, L.J., Gardashli, M.E., Morales-Gallel, R., Garcia-Verdugo, J.M., DeTure, M., Vera-Garcia, D.V., Hucke, A.T.S., Oskarsson, B.E., Murray, M.E., Dickson, D.W., Heiman, M., Belzil, V.V., and Kellis, M. (2024). Cell, 187(8):1971-1989.e16.

Huntington’s Disease: Pathogenic Mechanisms and Implications for Therapeutics

Editors: X. Yang, W., Thompson, L.M., and Heiman, M. 1st Edition – February 7, 2024; Elsevier; ISBN: 9780323956727.

Defining Diurnal Fluctuations in Mouse Choroid Plexus and CSF at High Molecular, Spatial, and Temporal Resolution

Fame, R.M., Kalugin, P.N., Petrova, B., Xu, H., Soden, P.A., Shipley, F.B, Dani, N., Grant, B., Pragana, A., Head, J.P., Gupta, S., Shannon, M.L., Chifamba, F.F., Hawks-Mayer, H., Vernon, A., Gao, F., Zhang, Y., Holtzman, M.J., Heiman, M., Andermann, M.L., Kanarek, N., Lipton, J.O., and Lehtinen, M.K. (2023). Nature Communications, 14 (1), 3720.

Transcriptional Vulnerabilities of Striatal Neurons in Human and Rodent Models of Huntington’s Disease

Matsushima, A., Pineda, S.S., Crittenden, J.R., Lee, H., Galani, K., Mantero, J., Tombaugh, G., Kellis, M., Heiman, M., and Graybiel, A.M. (2023) Nature Communications 14, 282.

A Partnership Between the Lipid Scramblase XK and the Lipid Transfer Protein VPS13A at the Plasma Membrane

Guillén-Samander, A., Wu, Y., Pineda, S.S., Garcia, F.J., Eisen, J.N., Leonzino, M., Ugur, B., Kellis, M., Heiman, M., and De Camilli, P. (2022) Proceedings of the National Academy of Sciences of the USA, 119(35):e2205425119.

Back-to-BACs in Huntington’s Disease Modeling

Lee, H. and Heiman, M. (2022). Neuron, 110(7):1087-1089.

Single-Cell Dissection of the Human Brain Vasculature

Garcia, F.J., Sun, N., Lee, H., Godlewski, B., Mathys, H., Galani, K., Zhou, B., Jiang, X., Ng, A.P., Mantero, J., Tsai, L.-H., Bennett, D.A., Sahin, M., Kellis, M. and Heiman, M. (2022). Nature, 603(7903):893-899.

An Amygdala Circuit That Suppresses Social Engagement

Kwon, J-T., Ryu, C., Lee, H., Sheffield, A., Fan, J., Cho, D.H., Bigler, S., Sullivan, H. A., Choe, H. K., Wickersham, I. R., Heiman, M., and Choi, G. B. (2021). Nature, 593(7857):114-118.

Shape Deformation Analysis Reveals the Temporal Dynamics of Cell-type-specific Homeostatic and Pathogenic Responses to Mutant Huntingtin

Megret, L., Gris, B., Nair, S.S., Cevost, J., Wertz, M., Aaronson, J., Rosinski, J., Vogt, T.F.,  Wilkinson, H., Heiman, M., Neri, C. (2021). eLife, 10:e64984.

Choroid Plexus NKCC1 Mediates Cerebrospinal Fluid Clearance During Mouse Early Postnatal Development

Xu, H., Fame, R.M., Sadegh, C., Sutin, J., Naranjo, C., Syau, D., Cui, J., Shipley, F.B., Vernon, A., Gao, F., Zhang, Y., Holtzman, M., Heiman, M., Warf, B.C., Lin, P.-Y, and Lehtinen, M.K. (2021). Nature Communications, 12(1):447.

Cell Type-Specific Transcriptomics Reveals that Mutant Huntingtin Leads to Mitochondrial RNA Release and Neuronal Innate Immune Activation

Lee, H., Fenster, R.J., Pineda, S.S.P., Gibbs, W.S., Mohammadi, S., Davila-Velderrain, J., Garcia, F.G., Therrien, M., Novis, H.S., Gao, F., Wilkinson, H., Vogt, T., Kellis, M, LaVoie, M.J., Heiman M. (2020). Neuron 107, 1-18.

Selective Neuronal Vulnerability in Alzheimer’s Disease: A Network-Based Analysis

Roussarie, J-P., Yao, V., Rodriguez-Rodriguez, P., Oughtred, R., Rust, J., Plautz, Z., Kasturia, S., Albornoz, C., Wang, W., Schmidt, E.F., Dannenfelser, R., Tadych, A., Brichta, L., Barnea-Cramer, A., Heintz, N., Hof, P.R., Heiman, M., Dolinski, K., Flajolet, M., Troyanskaya, O.G., Greengard P. (2020). Neuron 107, 1-15.

Interleukin-6 Deficiency Exacerbates Huntington’s Disease Model Phenotypes

Wertz, M. H., Pineda, S. S., Lee H., Kulicke, R., Kellis, M., Heiman, M. (2020). Mol Neurodegener. 15(1):29.

Genome-wide In Vivo CNS Screening Identifies Genes that Modify CNS Neuronal Survival and mHTT Toxicity

Wertz, M. H., Mitchem, M. R., Pineda, S. S., Hachigia, L. J. , Lee, H., Lau, V., Powers, A., Kulicke, R., Madan, G. K., Colic, M., Therrien, M., Vernon, A., Beja-Glasser, V. F., Hegde, M., Gao, F., Kellis, M., Hart, T., Doench, J. G., Heiman, M. (2020). Neuron 106, 1-14.

A Cortical-Brainstem Circuit Predicts and Governs Compulsive Alcohol Drinking

Siciliano, C.A., Noamany, H., Chang, C.-J., Brown, A.R., Chen, X., Leible, X., Lee J.J., Wang, J., Vernon, A.N., Vander Weele, C.M., Kimchi, E.Y., Heiman, M., and Tye, K.M. (2019). Science 366, 1008-1012.

Small Molecule Targets TMED9 and Promotes Lysosomal Degradation to Reverse Proteinopathy

Dvela-Levitt, M.,  Kost-Alimova, M., Emani, M., Kohnert, E., Thompson, R., Sidhom, E.-H., Rivadeneira, A., Sahakian, N.,  Roignot, J., Papagregoriou, G., Montesinos, M.S.,  Clark, A.R., McKinney, D., Gutierrez, J., Rot,h M., Ronco, L., Elonga, E., Carter, T.A., Gnirke, A., Melanson, M., Hartland, K., Wieder, N., Hsu, J.C.H., Deltas, C., Hughey, R., Bleyer, A.J., Kmoch, S.,  Živná, M., Barešova, V., Kota, S., Schlondorff, J., Heiman, M., Alper, S.L., Wagner, F., Weins, A., Golub, T.R., Lander, E.S., and Greka, A. (2019). Cell 178, 521–535.

Widespread Accumulation of Ribosome-Associated Isolated 3′ UTRs in Neuronal Cell Populations of the Aging Brain

Sudmant, P.H., Lee, H., Dominguez, D., Heiman, M., and Burge. C,B. (2018). Cell Reports 9, 2447-2456.

Normal Aging Induces A1-like Astrocyte Reactivity

Clarke, L.E., Liddelow, S.A., Chakraborty, C., Münch, A.E., Heiman, M., and Barres, B.A. (2018). Proceedings of the National Academy of Sciences of the United States of America 115, E1896-E1905.

Control of Huntington’s Disease-Associated Phenotypes by the Striatum-Enriched Transcription Factor Foxp2

Hachigian, L.J., Carmona, V., Fenster, R.J., Kulicke, R., Heilbut, A., Sittler, A., Pereira de Almeida, L., Mesirov, J.P., Gao, F., Kolaczyk, E.D., and Heiman, M. (2017). Cell Reports 21, 2688-2695.

Identifying Novel Therapeutic Targets by Combining Transcriptional Data with Ordinal Clinical Measurements

Pirhaji, L., Milani, P., Dalin, S.,  Wassie, B.T., Dunn, D., Fenster, R.J., Avila-Pacheco, J., Greengard, P.,  Clish, C.B., Heiman, M., Lo, D., and Fraenkel, E. (2017). Nature  Communications 8, 623.

Genome-Wide Genetic Screening in the Mammalian Central Nervous System

Wertz, M., and Heiman, M.  Genome Editing in Neurosciences, Springer. In Press.

Hypothalamic Amylin Acts in Concert with Leptin to Regulate Food Intake

Li, Z., Kelly, L., Heiman, M., Greengard, P., and Friedman, J.M. (2016). Cell Metabolism 23, 945.

The Stress-Induced Atf3-Gelsolin Cascade Underlies Dendritic Spine Deficits in Neuronal Models of Tuberous Sclerosis Complex

Nie, D., Chen, Z., Ebrahimi-Fakhari, D., Di Nardo, A., Julich, K., Robson, V.K., Cheng, Y.C., Woolf, C.J., Heiman, M., and  Sahin, M. (2015). Journal of Neuroscience 35, 10762-72.

Protein Kinase A Directly Phosphorylates Metabotropic Glutamate Receptor 5 to Modulate its Function

Uematsu, K., Heiman, M., Zelenina, M., Padovan, J., Chait, B.T., Aperia, A., Nishi, A., and Greengard, P. (2015).  Journal of Neurochemistry 132, 677-86.

Synthetic Lethal Screening in the Mammalian Central Nervous System Identifies Gpx6 as a Modulator of Huntington’s Disease

Shema, R., Kulicke, R., Cowley, G.S., Stein, R., Root, D.E., and Heiman, M. (2015)  Proceedings of the National Academy of Sciences of the USA 112, 268-72.

Nitric Oxide Regulates Synaptic Transmission Between Spiny Projection Neurons

Sagi, Y., Heiman, M., Peterson, J.D., Musatov, S., Scarduzio, M., Logan, S.M., Kaplitt, M.G., Surmeier, D.J., Heintz, N., and Greengard, P. (2014) Proceedings of the National Academy of Sciences of the USA 111, 17636-41.

Cell Type-Specific Plasticity of Striatal Projection Neurons in Parkinsonism and L-DOPA-Induced Dyskinesia

Fieblinger, T., Graves, S.M., Sebel, L.E., Alcacer, C., Plotkin, J.L., Gertler, T.S., Chan, C.S., Heiman, M., Greengard, P., Cenci, M.A., and Surmeier, D.J. (2014). Nature Communications 5, 5316.

Cell Type-Specific mRNA Purification by Translating Ribosome Affinity Purification (TRAP)

Heiman, M., Kulicke, R., Fenster, R.J., Greengard, P., and Heintz, N. (2014) Nature Protocols 9, 1282-91.

Molecular Adaptations of Striatal Spiny Projection neurons During Levodopa-Induced Dyskinesia

Heiman, M., Heilbut, A., Francardo, V., Kulicke, R., Fenster, R.J., Kolaczyk, E.D., Mesirov, J.P., Surmeier, D.J., Cenci, M.A., and Greengard, P. (2014) Proceedings of the National Academy of Sciences of the USA. 111, 4578-83.

Differential Effects of Cocaine on Histone Posttranslational Modifications in Identified Populations of Striatal Neurons

Jordi, E., Heiman, M., Marion-Poll, L., Guermonprez, P., Cheng, S.K., Nairn, A.C., Greengard, P., and Girault, J.A. (2013) Proceedings of the National Academy of Sciences of the USA 110, 9511-6.

IRE1α Induces Thioredoxin-Interacting Protein to Activate the NLRP3 Inflammasome and Promote Programmed Cell Death Under Irremediable ER Stress

Lerner, A.G., Upton, J.P., Praveen, P.V., Ghosh, R., Nakagawa, Y., Igbaria, A., Shen, S., Nguyen, V., Backes, B.J., Heiman, M., Heintz, N., Greengard, P., Hui, S., Tang, Q., Trusina, A., Oakes, S.A., and Papa, F.R. (2012) Cell Metabolism 16, 250-64.

Strain-Specific Regulation of Striatal Phenotype in Drd2-eGFP BAC Transgenic Mice

Chan, C.S., Peterson, J.D., Gertler, T.S., Glajch, K.E., Quintana, R.E., Cui, Q., Sebel, L.E., Plotkin, J.L., Shen, W., Heiman, M., Heintz, N., Greengard, P., and Surmeier, D.J. (2012) Journal of Neuroscience 32, 9124-32.

Inhibition of mTOR Signaling in Parkinson’s Disease Prevents L-DOPA-Induced Dyskinesia

Santini, E., Heiman, M., Greengard, P., Valjent, E., and Fisone, G. (2009) Science Signaling 2, ra36.

L-DOPA Activates ERK Signaling and Phosphorylates Histone H3 in the Striatonigral Medium Spiny Neurons of Hemiparkinsonian Mice

Santini, E., Alcacer, C., Cacciatore, S., Heiman, M., Hervé, D., Greengard, P., Girault, J.A., Valjent, E., and Fisone, G. (2009) Journal of Neurochemistry 108, 621-33.

A Translational Profiling Approach for the Molecular Characterization of CNS Cell Types

Heiman, M., Schaefer, A., Gong, S., Peterson, J.D., Day, M., Ramsey, K.E., Suárez-Fariñas, M., Schwarz, C., Stephan, D.A., Surmeier, D.J., Greengard, P., and Heintz, N. (2008) Cell 135, 738-48.

Application of a Translational Profiling Approach for the Comparative Analysis of CNS Cell Types

Doyle, J.P., Dougherty, J.D., Heiman, M., Schmidt, E.F., Stevens, T.R., Ma, G., Bupp, S., Shrestha, P., Shah, R.D., Doughty, M.L., Gong, S., Greengard, P., and Heintz, N. (2008) Cell 135, 749-62.

Regulation of Alzheimer’s Disease Amyloid-Beta Formation by Casein Kinase I

Flajolet, M., He, G., Heiman, M., Lin, A., Nairn, A.C., and Greengard, P. (2007) Proceedings of the National Academy of Sciences of the USA 104, 4159-64.

Essential Role of Calcineurin in Response to Endoplasmic Reticulum Stress

Bonilla, M., Nastase, K.K. and Cunningham, K.W.  (2002) EMBO Journal 21, 2343-53.

Subunit Organization in Cytoplasmic Dynein Subcomplexes

King, S.J., Bonilla, M., Rodgers, M.E., and Schroer. T.A. (2002) Protein Science 11, 1239-50.

Calcium Release and Influx in Yeast: TRPC and VGCC Rule Another Kingdom

Bonilla, M. and Cunningham, K.W. (2002) Science Signaling 127, pe17.

A Homolog of Voltage-Gated Ca(2+) Channels Stimulated by Depletion of Secretory Ca(2+) in Yeast

Locke, E.G., Bonilla, M., Liang, L., Takita, Y., and Cunningham, K.W. (2000) Molecular and Cellular Biology 20(18),6686-94.