Display options
Cite
Cirnaru MD, Creus-Muncunill J, Nelson S, et al. Striatal Cholinergic Dysregulation after Neonatal Decrease in X-Linked Dystonia Parkinsonism-Related TAF1 Isoforms. Mov Disord. 2021;doi: 10.1002/mds.28750.
Cirnaru, M. D., Creus-Muncunill, J., Nelson, S., Lewis, T. B., Watson, J., Ellerby, L. M., Gonzalez-Alegre, P., & Ehrlich, M. E. (2021). Striatal Cholinergic Dysregulation after Neonatal Decrease in X-Linked Dystonia Parkinsonism-Related TAF1 Isoforms. Movement disorders : official journal of the Movement Disorder Society, . https://doi.org/10.1002/mds.28750
Cirnaru, Maria-Daniela, et al. "Striatal Cholinergic Dysregulation after Neonatal Decrease in X-Linked Dystonia Parkinsonism-Related TAF1 Isoforms." Movement disorders : official journal of the Movement Disorder Society vol. (2021). doi: https://doi.org/10.1002/mds.28750
Cirnaru MD, Creus-Muncunill J, Nelson S, Lewis TB, Watson J, Ellerby LM, Gonzalez-Alegre P, Ehrlich ME. Striatal Cholinergic Dysregulation after Neonatal Decrease in X-Linked Dystonia Parkinsonism-Related TAF1 Isoforms. Mov Disord. 2021 Aug 17; doi: 10.1002/mds.28750. Epub 2021 Aug 17. PMID: 34403156.
Copy Download .nbib Format: NLM
Share it on

Mov Disord. 2021 Aug 17; doi: 10.1002/mds.28750. Epub 2021 Aug 17.

Striatal Cholinergic Dysregulation after Neonatal Decrease in X-Linked Dystonia Parkinsonism-Related TAF1 Isoforms.

Movement disorders : official journal of the Movement Disorder Society

Maria-Daniela Cirnaru, Jordi Creus-Muncunill, Shareen Nelson, Travis B Lewis, Jaime Watson, Lisa M Ellerby, Pedro Gonzalez-Alegre, Michelle E Ehrlich

Affiliations

  1. Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
  2. Raymond G. Perelman Center for Cellular & Molecular Therapeutics, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
  3. Department of Neurology, Perelman School of Medicine, The University of Pennsylvania, Philadelphia, Pennsylvania, USA.
  4. Buck Institute for Research on Aging, Novato, California, USA.

PMID: 34403156 DOI: 10.1002/mds.28750

Abstract

BACKGROUND: X-linked dystonia parkinsonism is a generalized, progressive dystonia followed by parkinsonism with onset in adulthood and accompanied by striatal neurodegeneration. Causative mutations are located in a noncoding region of the TATA-box binding protein-associated factor 1 (TAF1) gene and result in aberrant splicing. There are 2 major TAF1 isoforms that may be decreased in symptomatic patients, including the ubiquitously expressed canonical cTAF1 and the neuronal-specific nTAF1.

OBJECTIVE: The objective of this study was to determine the behavioral and transcriptomic effects of decreased cTAF1 and/or nTAF1 in vivo.

METHODS: We generated adeno-associated viral (AAV) vectors encoding microRNAs targeting Taf1 in a splice-isoform selective manner. We performed intracerebroventricular viral injections in newborn mice and rats and intrastriatal infusions in 3-week-old rats. The effects of Taf1 knockdown were assayed at 4 months of age with evaluation of motor function, histology, and RNA sequencing of the striatum, followed by its validation.

RESULTS: We report motor deficits in all cohorts, more pronounced in animals injected at P0, in which we also identified transcriptomic alterations in multiple neuronal pathways, including the cholinergic synapse. In both species, we show a reduced number of striatal cholinergic interneurons and their marker mRNAs after Taf1 knockdown in the newborn.

CONCLUSION: This study provides novel information regarding the requirement for TAF1 in the postnatal maintenance of striatal cholinergic neurons, the dysfunction of which is involved in other inherited forms of dystonia. © 2021 International Parkinson and Movement Disorder Society.

© 2021 International Parkinson and Movement Disorder Society.

Keywords: TAF1; X-linked dystonia parkinsonism; cholinergic interneurons; striatum

References

  1. Lee LV, Rivera C, Teleg RA, et al. The unique phenomenology of sex-linked dystonia parkinsonism (XDP, DYT3, “Lubag”). Int J Neurosci 2011;121(suppl 1):3-11. - PubMed
  2. Bragg DC, Sharma N, Ozelius LJ. X-linked dystonia-parkinsonism: recent advances. Curr Opin Neurol 2019;32(4):604-609. - PubMed
  3. Goto S, Lee LV, Munoz EL, et al. Functional anatomy of the basal ganglia in X-linked recessive dystonia-parkinsonism. Ann Neurol 2005;58(1):7-17. - PubMed
  4. Domingo A, Amar D, Grutz K, et al. Evidence of TAF1 dysfunction in peripheral models of X-linked dystonia-parkinsonism. Cell Mol Life Sci 2016;73(16):3205-3215. - PubMed
  5. Bruggemann N, Heldmann M, Klein C, et al. Neuroanatomical changes extend beyond striatal atrophy in X-linked dystonia parkinsonism. Parkinsonism Relat Disord 2016;31:91-97. - PubMed
  6. Bruggemann N, Rosales RL, Waugh JL, et al. Striatal dysfunction in X-linked dystonia-parkinsonism is associated with disease progression. Eur J Neurol 2017;24(5):680-686. - PubMed
  7. Blood AJ, Waugh JL, Munte TF, et al. Increased insula-putamen connectivity in X-linked dystonia-parkinsonism. Neuroimage Clin 2018;17:835-846. - PubMed
  8. Hanssen H, Heldmann M, Prasuhn J, et al. Basal ganglia and cerebellar pathology in X-linked dystonia-parkinsonism. Brain 2018;141(10):2995-3008. - PubMed
  9. Hanssen H, Prasuhn J, Heldmann M, et al. Imaging gradual neurodegeneration in a basal ganglia model disease. Ann Neurol 2019;86(4):517-526. - PubMed
  10. Arasaratnam CJ, Singh-Bains MK, Waldvogel HJ, Faull RLM. Neuroimaging and neuropathology studies of X-linked dystonia parkinsonism. Neurobiol Dis 2020;148:105186. - PubMed
  11. Makino S, Kaji R, Ando S, Tomizawa M, et al. Reduced neuron-specific expression of the TAF1 gene is associated with X-linked dystonia-parkinsonism. Am J Hum Genet 2007;80(3):393-406. - PubMed
  12. Petrozziello T, Mills AN, Vaine CA, et al. Neuroinflammation and histone H3 citrullination are increased in X-linked dystonia parkinsonism post-mortem prefrontal cortex. Neurobiol Dis 2020;144:105032. - PubMed
  13. Wang H, Curran EC, Hinds TR, Wang EH, Zheng N. Crystal structure of a TAF1-TAF7 complex in human transcription factor IID reveals a promoter binding module. Cell Res 2014;24(12):1433-1444. - PubMed
  14. Muller U, Herzfeld T, Nolte D. The TAF1/DYT3 multiple transcript system in X-linked dystonia-parkinsonism. Am J Hum Genet 2007;81(2):415-417. - PubMed
  15. Capponi S, Stoffler N, Irimia M, et al. Neuronal-specific microexon splicing of TAF1 mRNA is directly regulated by SRRM4/nSR100. RNA Biol 2020;17(1):62-74. - PubMed
  16. Jambaldorj J, Makino S, Munkhbat B, Tamiya G. Sustained expression of a neuron-specific isoform of the Taf1 gene in development stages and aging in mice. Biochem Biophys Res Commun 2012;425(2):273-277. - PubMed
  17. Nolte D, Niemann S, Muller U. Specific sequence changes in multiple transcript system DYT3 are associated with X-linked dystonia parkinsonism. Proc Natl Acad Sci U S A 2003;100(18):10347-10352. - PubMed
  18. Bragg DC, Mangkalaphiban K, Vaine CA, et al. Disease onset in X-linked dystonia-parkinsonism correlates with expansion of a hexameric repeat within an SVA retrotransposon in TAF1. Proc Natl Acad Sci U S A 2017;114(51):E11020-E11028. - PubMed
  19. Aneichyk T, Hendriks WT, Yadav R, et al. Dissecting the causal mechanism of X-linked dystonia-parkinsonism by integrating genome and transcriptome assembly. Cell 2018;172(5):897-909. - PubMed
  20. Westenberger A, Reyes CJ, Saranza G, et al. A hexanucleotide repeat modifies expressivity of X-linked dystonia parkinsonism. Ann Neurol 2019;85(6):812-822. - PubMed
  21. O'Rawe JA, Wu Y, Dorfel MJ, et al. TAF1 variants are associated with dysmorphic features, intellectual disability, and neurological manifestations. Am J Hum Genet 2015;97(6):922-932. - PubMed
  22. Hurst SE, Liktor-Busa E, Moutal A, et al. A novel variant in TAF1 affects gene expression and is associated with X-linked TAF1 intellectual disability syndrome. Neuronal Signal 2018;2(3):NS20180141. - PubMed
  23. Gudmundsson S, Wilbe M, Filipek-Gorniok B, et al. TAF1, associated with intellectual disability in humans, is essential for embryogenesis and regulates neurodevelopmental processes in zebrafish. Sci Rep 2019;9(1):10730. - PubMed
  24. Janakiraman U, Yu J, Moutal A, et al. TAF1-gene editing alters the morphology and function of the cerebellum and cerebral cortex. Neurobiol Dis 2019;132:104539. - PubMed
  25. Janakiraman U, Dhanalakshmi C, Yu J, et al. The investigation of the T-type calcium channel enhancer SAK3 in an animal model of TAF1 intellectual disability syndrome. Neurobiol Dis 2020;143:105006. - PubMed
  26. Wassarman DA, Aoyagi N, Pile LA, Schlag EM. TAF250 is required for multiple developmental events in drosophila. Proc Natl Acad Sci U S A 2000;97(3):1154-1159. - PubMed
  27. Kobayashi A, Miyake T, Kawaichi M, Kokubo T. Mutations in the histone fold domain of the TAF12 gene show synthetic lethality with the TAF1 gene lacking the TAF N-terminal domain (TAND) by different mechanisms from those in the SPT15 gene encoding the TATA box-binding protein (TBP). Nucleic Acids Res 2003;31(4):1261-1274. - PubMed
  28. Rakovic A, Domingo A, Grutz K, et al. Genome editing in induced pluripotent stem cells rescues TAF1 levels in X-linked dystonia-parkinsonism. Mov Disord 2018;33(7):1108-1118. - PubMed
  29. Capetian P, Stanslowsky N, Bernhardi E, et al. Altered glutamate response and calcium dynamics in iPSC-derived striatal neurons from XDP patients. Exp Neurol 2018;308:47-58. - PubMed
  30. McBride JL, Boudreau RL, Harper SQ, et al. Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: implications for the therapeutic development of RNAi. Proc Natl Acad Sci U S A 2008;105(15):5868-5873. - PubMed
  31. Foster GA, Schultzberg M, Kokfelt T, et al. Ontogeny of the dopamine and cyclic adenosine-3′:5′-monophosphate-regulated phosphoprotein (DARPP-32) in the pre- and postnatal mouse central nervous system. Int J Dev Neurosci 1988;6(4):367-386. - PubMed
  32. Ivkovic S, Ehrlich ME. Expression of the striatal DARPP-32/ARPP-21 phenotype in GABAergic neurons requires neurotrophins in vivo and in vitro. J Neurosci 1999;19(13):5409-5419. - PubMed
  33. Martin JN, Wolken N, Brown T, Dauer WT, Ehrlich ME, Gonzalez-Alegre P. Lethal toxicity caused by expression of shRNA in the mouse striatum: implications for therapeutic design. Gene Ther 2011;18(7):666-673. - PubMed
  34. Chakrabarty P, Rosario A, Cruz P, et al. Capsid serotype and timing of injection determines AAV transduction in the neonatal mice brain. PLoS One 2013;8(6):e67680. - PubMed
  35. Eng LF, Ghirnikar RS, Lee YL. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 2000;25(9-10):1439-1451. - PubMed
  36. Gunther A, Luczak V, Abel T, Baumann A. Caspase-3 and GFAP as early markers for apoptosis and astrogliosis in shRNA-induced hippocampal cytotoxicity. J Exp Biol 2017;220(Pt 8):1400-1404. - PubMed
  37. Francis C, Natarajan S, Lee MT, et al. Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution. BMC Genomics 2014;15:883. - PubMed
  38. Ellenbroek B, Youn J. Rodent models in neuroscience research: is it a rat race? Dis Model Mech 2016;9(10):1079-1087. - PubMed
  39. Li J, Kim S, Pappas SS, Dauer WT. CNS critical periods: implications for dystonia and other neurodevelopmental disorders. JCI Insight 2021;6(4):e142483. - PubMed
  40. Li J, Levin DS, Kim AJ, Pappas SS, Dauer WT. TorsinA restoration in a mouse model identifies a critical therapeutic window for DYT1 dystonia. J Clin Invest 2021;131(6):e139606. - PubMed
  41. Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000;28(1):27-30. - PubMed
  42. Kanehisa M. Toward understanding the origin and evolution of cellular organisms. Protein Sci 2019;28(11):1947-1951. - PubMed
  43. Kanehisa M, Sato Y, Furumichi M, Morishima K, Tanabe M. New approach for understanding genome variations in KEGG. Nucleic Acids Res 2019;47(D1):D590-D595. - PubMed
  44. Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M. KEGG: integrating viruses and cellular organisms. Nucleic Acids Res 2021;49(D1):D545-D551. - PubMed
  45. Raymond LA. Striatal synaptic dysfunction and altered calcium regulation in Huntington disease. Biochem Biophys Res Commun 2017;483(4):1051-1062. - PubMed
  46. Smith-Dijak AI, Sepers MD, Raymond LA. Alterations in synaptic function and plasticity in Huntington disease. J Neurochem 2019;150(4):346-365. - PubMed
  47. Crapser JD, Ochaba J, Soni N, Reidling JC, Thompson LM, Green KN. Microglial depletion prevents extracellular matrix changes and striatal volume reduction in a model of Huntington's disease. Brain 2020;143(1):266-288. - PubMed
  48. Sciamanna G, Hollis R, Ball C, et al. Cholinergic dysregulation produced by selective inactivation of the dystonia-associated protein torsinA. Neurobiol Dis 2012;47(3):416-427. - PubMed
  49. Pappas SS, Darr K, Holley SM, et al. Forebrain deletion of the dystonia protein torsinA causes dystonic-like movements and loss of striatal cholinergic neurons. Elife 2015;4:e08352. - PubMed
  50. Eskow Jaunarajs KL, Scarduzio M, Ehrlich ME, McMahon LL, Standaert DG. Diverse mechanisms Lead to common dysfunction of striatal cholinergic interneurons in distinct genetic mouse models of dystonia. J Neurosci 2019;39(36):7195-7205. - PubMed
  51. Marin O, Anderson SA, Rubenstein JL. Origin and molecular specification of striatal interneurons. J Neurosci 2000;20(16):6063-6076. - PubMed
  52. Bonsi P, Cuomo D, Martella G, et al. Centrality of striatal cholinergic transmission in basal ganglia function. Front Neuroanat 2011;5:6. - PubMed
  53. Lopes R, Verhey van Wijk N, Neves G, Pachnis V. Transcription factor LIM homeobox 7 (Lhx7) maintains subtype identity of cholinergic interneurons in the mammalian striatum. Proc Natl Acad Sci U S A 2012;109(8):3119-3124. - PubMed
  54. Tomioka T, Shimazaki T, Yamauchi T, Oki T, Ohgoh M, Okano H. LIM homeobox 8 (Lhx8) is a key regulator of the cholinergic neuronal function via a tropomyosin receptor kinase a (TrkA)-mediated positive feedback loop. J Biol Chem 2014;289(2):1000-1010. - PubMed
  55. Allaway KC, Machold R. Developmental specification of forebrain cholinergic neurons. Dev Biol 2017;421(1):1-7. - PubMed
  56. Saunders A, Macosko EZ, Wysoker A, et al. Molecular diversity and specializations among the cells of the adult mouse brain. Cell 2018;174(4):1015-1030. - PubMed
  57. Lalonde R, Strazielle C. Brain regions and genes affecting limb-clasping responses. Brain Res Rev 2011;67(1-2):252-259. - PubMed
  58. Rial D, Castro AA, Machado N, et al. Behavioral phenotyping of Parkin-deficient mice: looking for early preclinical features of Parkinson's disease. PLoS One 2014;9(12):e114216. - PubMed
  59. LeDoux M. Movement Disorders: Genetics and Models. 2nd ed. New York: Elsevier; 2005. - PubMed
  60. Rozas G, Lopez-Martin E, Guerra MJ, Labandeira-Garcia JL. The overall rod performance test in the MPTP-treated-mouse model of parkinsonism. J Neurosci Methods 1998;83(2):165-175. - PubMed
  61. Durieux PF, Schiffmann SN, de Kerchove d'Exaerde A. Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J 2012;31(3):640-653. - PubMed
  62. Yu-Taeger L, Petrasch-Parwez E, Osmand AP, et al. A novel BACHD transgenic rat exhibits characteristic neuropathological features of Huntington disease. J Neurosci 2012;32(44):15426-15438. - PubMed
  63. Rangel-Barajas C, Rebec GV. Overview of Huntington's disease models: neuropathological, molecular, and behavioral differences. Curr Protoc Neurosci 2018;83(1):e47. - PubMed
  64. Chandra R, Francis TC, Konkalmatt P, et al. Opposing role for Egr3 in nucleus accumbens cell subtypes in cocaine action. J Neurosci 2015;35(20):7927-7937. - PubMed
  65. Humbert S. Is Huntington disease a developmental disorder? EMBO Rep 2010;11(12):899. - PubMed
  66. Kerschbamer E, Biagioli M. Huntington's disease as neurodevelopmental disorder: altered chromatin regulation, coding, and non-coding RNA transcription. Front Neurosci 2015;9:509. - PubMed
  67. Arendt T, Stieler J, Ueberham U. Is sporadic Alzheimer's disease a developmental disorder? J Neurochem 2017;143(4):396-408. - PubMed
  68. Wiatr K, Szlachcic WJ, Trzeciak M, Figlerowicz M, Figiel M. Huntington disease as a neurodevelopmental disorder and early signs of the disease in stem cells. Mol Neurobiol 2018;55(4):3351-3371. - PubMed
  69. Wood H. Huntington disease-a neurodevelopmental disorder? Nat Rev Neurol 2018;14(11):632-633. - PubMed
  70. Marcello E, di Luca M, Gardoni F. Synapse-to-nucleus communication: from developmental disorders to Alzheimer's disease. Curr Opin Neurobiol 2018;48:160-166. - PubMed
  71. vonder Embse AN, Hu Q, DeWitt JC. Dysfunctional microglia:neuron interactions with significant female bias in a developmental gene × environment rodent model of Alzheimer's disease. Int Immunopharmacol 2019;71:241-250. - PubMed
  72. Barnat M, Capizzi M, Aparicio E, et al. Huntington's disease alters human neurodevelopment. Science 2020;369(6505):787-793. - PubMed
  73. Moehle MS, Conn PJ. Roles of the M4 acetylcholine receptor in the basal ganglia and the treatment of movement disorders. Mov Disord 2019;34(8):1089-1099. - PubMed
  74. Abreu-Villaca Y, Filgueiras CC, Manhaes AC. Developmental aspects of the cholinergic system. Behav Brain Res 2011;221(2):367-378. - PubMed
  75. Zahalka EA, Seidler FJ, Lappi SE, Yanai J, Slotkin TA. Differential development of cholinergic nerve terminal markers in rat brain regions: implications for nerve terminal density, impulse activity and specific gene expression. Brain Res 1993;601(1-2):221-229. - PubMed
  76. Ward NL, Hagg T. BDNF is needed for postnatal maturation of basal forebrain and neostriatum cholinergic neurons in vivo. Exp Neurol 2000;162(2):297-310. - PubMed
  77. Magno L, Barry C, Schmidt-Hieber C, Theodotou P, Hausser M, Kessaris N. NKX2-1 is required in the embryonic septum for cholinergic system development, learning, and memory. Cell Rep 2017;20(7):1572-1584. - PubMed
  78. Boskovic Z, Meier S, Wang Y, et al. Regulation of cholinergic basal forebrain development, connectivity, and function by neurotrophin receptors. Neuronal Signal 2019;3(1):NS20180066. - PubMed
  79. Abudukeyoumu N, Hernandez-Flores T, Garcia-Munoz M, Arbuthnott GW. Cholinergic modulation of striatal microcircuits. Eur J Neurosci 2019;49(5):604-622. - PubMed
  80. Klein C, Breakefield XO, Ozelius LJ. Genetics of primary dystonia. Semin Neurol 1999;19(3):271-280. - PubMed
  81. Pisani A, Martella G, Tscherter A, et al. Altered responses to dopaminergic D2 receptor activation and N-type calcium currents in striatal cholinergic interneurons in a mouse model of DYT1 dystonia. Neurobiol Dis 2006;24(2):318-325. - PubMed
  82. Sciamanna G, Tassone A, Martella G, et al. Developmental profile of the aberrant dopamine D2 receptor response in striatal cholinergic interneurons in DYT1 dystonia. PLoS One 2011;6(9):e24261. - PubMed
  83. Sciamanna G, Ponterio G, Tassone A, et al. Negative allosteric modulation of mGlu5 receptor rescues striatal D2 dopamine receptor dysfunction in rodent models of DYT1 dystonia. Neuropharmacology 2014;85:440-450. - PubMed
  84. Bonsi P, Ponterio G, Vanni V, et al. RGS9-2 rescues dopamine D2 receptor levels and signaling in DYT1 dystonia mouse models. EMBO Mol Med 2019;11(1):e9283. - PubMed
  85. van der Weijden MCM, Rodriguez-Contreras D, Delnooz CCS, et al. A gain-of-function variant in dopamine D2 receptor and progressive chorea and dystonia phenotype. Mov Disord 2021;36(3):729-739. - PubMed
  86. Melis C, Beauvais G, Muntean BS, Cirnaru MD, Otrimski G, Creus-Muncunill J, et al. Striatal dopamine induced ERK phosphorylation is altered in mouse models of monogenic dystonia. Mov Disord 2021;36(5):1147-1157. - PubMed
  87. Thompson VB, Jinnah HA, Hess EJ. Convergent mechanisms in etiologically-diverse dystonias. Expert Opin Ther Targets 2011;15(12):1387-1403. - PubMed
  88. Zakirova Z, Fanutza T, Bonet J, et al. Mutations in THAP1/DYT6 reveal that diverse dystonia genes disrupt similar neuronal pathways and functions. PLoS Genet 2018;14(1):e1007169. - PubMed
  89. Graybiel AM. Correspondence between the dopamine islands and striosomes of the mammalian striatum. Neuroscience 1984;13(4):1157-1187. - PubMed
  90. Crittenden JR, Graybiel AM. Basal ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front Neuroanat 2011;5:59. - PubMed
  91. Brimblecombe KR, Cragg SJ. The Striosome and matrix compartments of the striatum: a path through the labyrinth from neurochemistry toward function. ACS Chem Nerosci 2017;8(2):235-242. - PubMed
  92. Hagimoto K, Takami S, Murakami F, Tanabe Y. Distinct migratory behaviors of striosome and matrix cells underlying the mosaic formation in the developing striatum. J Comp Neurol 2017;525(4):794-817. - PubMed
  93. Miyamoto Y, Katayama S, Shigematsu N, Nishi A, Fukuda T. Striosome-based map of the mouse striatum that is conformable to both cortical afferent topography and uneven distributions of dopamine D1 and D2 receptor-expressing cells. Brain Struct Funct 2018;223(9):4275-4291. - PubMed
  94. Fujiyama F, Unzai T, Karube F. Thalamostriatal projections and striosome-matrix compartments. Neurochem Int 2019;125:67-73. - PubMed
  95. Prager EM, Plotkin JL. Compartmental function and modulation of the striatum. J Neurosci Res 2019;97(12):1503-1514. - PubMed
  96. McGregor MM, McKinsey GL, Girasole AE, Bair-Marshall CJ, Rubenstein JLR, Nelson AB. Functionally distinct connectivity of developmentally targeted Striosome neurons. Cell Rep 2019;29(6):1419-1428. - PubMed
  97. Martin A, Calvigioni D, Tzortzi O, Fuzik J, Warnberg E, Meletis K. A Spatiomolecular map of the striatum. Cell Rep 2019;29(13):4320-4333. - PubMed
  98. Cirnaru M-D, Song S, Tshilenge K-T, et al. Transcriptional and epigenetic characterization of early striosomes identifies Foxf2 and Olig2 as factors required for development of striatal compartmentation and neuronal phenotypic differentiation. bioRxiv 2020. https://doi.org/10.1101/2020.05.19.105171 - PubMed
  99. Dawson TM, Golde TE, Lagier-Tourenne C. Animal models of neurodegenerative diseases. Nat Neurosci 2018;21(10):1370-1379. - PubMed

Publication Types

Grant support