Integrated electrophysiological and genomic profiles of single cells reveal spiking tumor cells in human glioma

被引:6
作者
Curry, Rachel N. [1 ,2 ]
Ma, Qianqian [3 ,4 ]
McDonald, Malcolm F. [2 ,5 ,6 ]
Ko, Yeunjung [2 ,7 ,8 ]
Srivastava, Snidgdha [3 ,5 ,9 ]
Chin, Pey-Shyuan [4 ]
He, Peihao [2 ,7 ,10 ]
Lozzi, Brittney [11 ]
Athukuri, Azwal [8 ]
Jing, Junzhan [3 ]
Wang, Su [8 ]
Harmanci, Arif O. [12 ]
Arenkiel, Benjamin [4 ,9 ]
Jiang, Xiaolong [3 ,4 ,13 ]
Deneen, Benjamin [1 ,2 ,6 ,7 ,8 ,10 ]
Harmanci, Akdes Serin [7 ,8 ]
Rao, Ganesh [7 ,8 ]
机构
[1] Baylor Coll Med, Integrat Mol & Biomed Sci Grad Program, Houston, TX 77030 USA
[2] Baylor Coll Med, Ctr Cell & Gene Therapy, Houston, TX 77030 USA
[3] Texas Childrens Hosp, Jan & Dan Duncan Neurol Res Inst, Houston, TX 77030 USA
[4] Baylor Coll Med, Dept Neurosurg, Houston, TX 77030 USA
[5] Baylor Coll Med, Med Scientist Training Program, Houston, TX USA
[6] Baylor Coll Med, Program Dev Dis Models & Therapeut, Houston, TX 77030 USA
[7] Baylor Coll Med, Ctr Canc Neurosci, Houston, TX 77030 USA
[8] Baylor Coll Med, Dept Neurosurg, Houston, TX 77030 USA
[9] Baylor Coll Med, Dept Human & Mol Genet, Houston, TX USA
[10] Baylor Coll Med, Program Canc Cell Biol, Houston, TX 77030 USA
[11] Baylor Coll Med, Program Genet & Genom, Houston, TX USA
[12] Univ Texas Hlth Sci Ctr, McWilliams Sch Biomed Informat, Houston, TX USA
[13] Baylor Coll Med, Dept Ophthalmol, Houston, TX 77030 USA
关键词
RNA-SEQ; OLIGODENDROCYTES; GLIA; POPULATION; MECHANISMS; PROMOTES; ORIGIN; ATLAS; IDH1;
D O I
10.1016/j.ccell.2024.08.009
中图分类号
R73 [肿瘤学];
学科分类号
100214 ;
摘要
Prior studies have described the complex interplay that exists between glioma cells and neurons; however, the electrophysiological properties endogenous to glioma cells remain obscure. To address this, we employed Patch-sequencing (Patch-seq) on human glioma specimens and found that one-third of patched cells in IDH mutant (IDHmut) mut ) tumors demonstrate properties of both neurons and glia. To define these hybrid cells (HCs), which fire single, short action potentials, and discern if they are of tumoral origin, we developed the single cell rule association mining (SCRAM) computational tool to annotate each cell individually. SCRAM revealed that HCs possess select features of GABAergic neurons and oligodendrocyte precursor cells, and include both tumor and non-tumor cells. These studies characterize the combined electrophysiological and molecular properties of human glioma cells and describe a cell type in human glioma with unique electrophysiological and transcriptomic properties that may also exist in the non-tumor brain.
引用
收藏
页码:1713 / 1728.e6
页数:23
相关论文
共 79 条
[1]   Spatial and cell type transcriptional landscape of human cerebellar development [J].
Aldinger, Kimberly A. ;
Thomson, Zachary ;
Phelps, Ian G. ;
Haldipur, Parthiv ;
Deng, Mei ;
Timms, Andrew E. ;
Hirano, Matthew ;
Santpere, Gabriel ;
Roco, Charles ;
Rosenberg, Alexander B. ;
Lorente-Galdos, Belen ;
Gulden, Forrest O. ;
O'Day, Diana ;
Overman, Lynne M. ;
Lisgo, Steven N. ;
Alexandre, Paula ;
Sestan, Nenad ;
Doherty, Dan ;
Dobyns, William B. ;
Seelig, Georg ;
Glass, Ian A. ;
Millen, Kathleen J. .
NATURE NEUROSCIENCE, 2021, 24 (08) :1163-1175
[2]   Single-cell profiling of myeloid cells in glioblastoma across species and disease stage reveals macrophage competition and specialization [J].
Antunes, Ana Rita Pombo ;
Scheyltjens, Isabelle ;
Lodi, Francesca ;
Messiaen, Julie ;
Antoranz, Asier ;
Duerinck, Johnny ;
Kancheva, Daliya ;
Martens, Liesbet ;
De Vlaminck, Karen ;
Van Hove, Hannah ;
Hansen, Signe Schmidt Kjolner ;
Bosisio, Francesca Maria ;
Van der Borght, Koen ;
De Vleeschouwer, Steven ;
Sciot, Raf ;
Bouwens, Luc ;
Verfaillie, Michiel ;
Vandamme, Niels ;
Vandenbroucke, Roosmarijn E. ;
De Wever, Olivier ;
Saeys, Yvan ;
Guilliams, Martin ;
Gysemans, Conny ;
Neyns, Bart ;
De Smet, Frederik ;
Lambrechts, Diether ;
Van Ginderachter, Jo A. ;
Movahedi, Kiavash .
NATURE NEUROSCIENCE, 2021, 24 (04) :595-610
[3]   Oligodendroglial GABAergic Signaling: More Than Inhibition! [J].
Bai, Xianshu ;
Kirchhoff, Frank ;
Scheller, Anja .
NEUROSCIENCE BULLETIN, 2021, 37 (07) :1039-1050
[4]   Comparative cellular analysis of motor cortex in human, marmoset and mouse [J].
Bakken, Trygve E. ;
Jorstad, Nikolas L. ;
Hu, Qiwen ;
Lake, Blue B. ;
Tian, Wei ;
Kalmbach, Brian E. ;
Crow, Megan ;
Hodge, Rebecca D. ;
Krienen, Fenna M. ;
Sorensen, Staci A. ;
Eggermont, Jeroen ;
Yao, Zizhen ;
Aevermann, Brian D. ;
Aldridge, Andrew I. ;
Bartlett, Anna ;
Bertagnolli, Darren ;
Casper, Tamara ;
Castanon, Rosa G. ;
Crichton, Kirsten ;
Daigle, Tanya L. ;
Dalley, Rachel ;
Dee, Nick ;
Dembrow, Nikolai ;
Diep, Dinh ;
Ding, Song-Lin ;
Dong, Weixiu ;
Fang, Rongxin ;
Fischer, Stephan ;
Goldman, Melissa ;
Goldy, Jeff ;
Graybuck, Lucas T. ;
Herb, Brian R. ;
Hou, Xiaomeng ;
Kancherla, Jayaram ;
Kroll, Matthew ;
Lathia, Kanan ;
van Lew, Baldur ;
Li, Yang Eric ;
Liu, Christine S. ;
Liu, Hanqing ;
Lucero, Jacinta D. ;
Mahurkar, Anup ;
McMillen, Delissa ;
Miller, Jeremy A. ;
Moussa, Marmar ;
Nery, Joseph R. ;
Nicovich, Philip R. ;
Niu, Sheng-Yong ;
Orvis, Joshua ;
Osteen, Julia K. .
NATURE, 2021, 598 (7879) :111-+
[5]   Evidence for oligodendrocyte progenitor cell heterogeneity in the adult mouse brain [J].
Beiter, Rebecca M. ;
Rivet-Noor, Courtney ;
Merchak, Andrea R. ;
Bai, Robin ;
Johanson, David M. ;
Slogar, Erica ;
Sol-Church, Katia ;
Overall, Christopher C. ;
Gaultier, Alban .
SCIENTIFIC REPORTS, 2022, 12 (01)
[6]   The cerebral cortex is a substrate of multiple interactions between GABAergic interneurons and oligodendrocyte lineage cells [J].
Benamer, Najate ;
Vidal, Marie ;
Angulo, Maria Cecilia .
NEUROSCIENCE LETTERS, 2020, 715
[7]   Generalizing RNA velocity to transient cell states through dynamical modeling [J].
Bergen, Volker ;
Lange, Marius ;
Peidli, Stefan ;
Wolf, F. Alexander ;
Theis, Fabian J. .
NATURE BIOTECHNOLOGY, 2020, 38 (12) :1408-1414
[8]   An atlas of cortical arealization identifies dynamic molecular signatures [J].
Bhaduri, Aparna ;
Sandoval-Espinosa, Carmen ;
Otero-Garcia, Marcos ;
Oh, Irene ;
Yin, Raymund ;
Eze, Ugomma C. ;
Nowakowski, Tomasz J. ;
Kriegstein, Arnold R. .
NATURE, 2021, 598 (7879) :200-+
[9]   Multimodal profiling of single-cell morphology, electrophysiology, and gene expression using Patch-seq [J].
Cadwell, Cathryn R. ;
Scala, Federico ;
Li, Shuang ;
Livrizzi, Giulia ;
Shen, Shan ;
Sandberg, Rickard ;
Jiang, Xiaolong ;
Tolias, Andreas S. .
NATURE PROTOCOLS, 2017, 12 (12) :2531-2553
[10]   Electrophysiological, transcriptomic and morphologic profiling of single neurons using Patch-seq [J].
Cadwell, Cathryn R. ;
Palasantza, Athanasia ;
Jiang, Xiaolong ;
Berens, Philipp ;
Deng, Qiaolin ;
Yilmaz, Marlene ;
Reimer, Jacob ;
Shen, Shan ;
Bethge, Matthias ;
Tolias, Kimberley F. ;
Sandberg, Rickard ;
Tolias, Andreas S. .
NATURE BIOTECHNOLOGY, 2016, 34 (02) :199-+