Molecular and cellular reorganization of neural circuits in the human lineage

被引:164
作者
Sousa, Andre M. M. [1 ,2 ]
Zhu, Ying [1 ,2 ]
Raghanti, Mary Ann [3 ,4 ]
Kitchen, Robert R. [5 ,6 ,7 ,8 ]
Onorati, Marco [1 ,2 ,9 ]
Tebbenkamp, Andrew T. N. [1 ,2 ]
Stutz, Bernardo [10 ]
Meyer, Kyle A. [1 ,2 ]
Li, Mingfeng [1 ,2 ]
Kawasawa, Yuka Imamura [1 ,2 ,11 ,12 ,13 ]
Liu, Fuchen [1 ,2 ]
Perez, Raquel Garcia [14 ]
Mele, Marta [14 ]
Carvalho, Tiago [14 ]
Skarica, Mario [1 ,2 ]
Gulden, Forrest O. [1 ,2 ]
Pletikos, Mihovil [1 ,2 ]
Shibata, Akemi [1 ,2 ]
Stephenson, Alexa R. [3 ,4 ]
Edler, Melissa K. [3 ,4 ]
Ely, John J. [15 ]
Elsworth, John D. [8 ]
Horvath, Tamas L. [1 ,2 ,10 ]
Hof, Patrick R. [16 ,17 ]
Hyde, Thomas M. [18 ]
Kleinman, Joel E. [18 ]
Weinberger, Daniel R. [18 ]
Reimers, Mark [19 ]
Lifton, Richard P. [20 ,21 ,22 ]
Mane, Shrikant M. [23 ]
Noonan, James P. [20 ]
State, Matthew W. [24 ,25 ]
Lein, Ed S. [26 ]
Knowles, James A. [27 ,28 ]
Marques-Bonet, Tomas [14 ,29 ,30 ]
Sherwood, Chet C. [31 ]
Gerstein, Mark B. [5 ,6 ,7 ]
Sestan, Nenad [1 ,2 ,8 ,10 ,20 ,32 ,33 ]
机构
[1] Yale Sch Med, Dept Neurosci, New Haven, CT USA
[2] Yale Sch Med, Kavli Inst Neurosci, New Haven, CT USA
[3] Kent State Univ, Dept Anthropol, Kent, OH 44242 USA
[4] Kent State Univ, Sch Biomed Sci, Kent, OH 44242 USA
[5] Yale Univ, Program Computat Biol & Bioinformat, Dept Mol Biophys, New Haven, CT USA
[6] Yale Univ, Dept Biochem, Program Computat Biol & Bioinformat, New Haven, CT USA
[7] Yale Univ, Program Computat Biol & Bioinformat, Dept Comp Sci, POB 2158, New Haven, CT 06520 USA
[8] Yale Sch Med, Dept Psychiat, New Haven, CT USA
[9] Univ Pisa, Dept Biol, Unit Cell & Dev Biol, Pisa, Italy
[10] Program Integrat Cell Signaling & Neurobiol Metab, Dept Comparat Med, New Haven, CT USA
[11] Penn State Univ, Coll Med, Inst Personalized Med, Dept Pharmacol, Hershey, PA USA
[12] Penn State Univ, Coll Med, Dept Biochem, Inst Personalized Med, Hershey, PA USA
[13] Penn State Univ, Coll Med, Inst Personalized Med, Dept Mol Biol, Hershey, PA USA
[14] Univ Pompeu Fabra, Consejo Super Invest Cient, Barcelona Biomed Res Pk, Inst Biol Evolut, Barcelona, Catalonia, Spain
[15] Alamogordo Primate Facil, Holloman AFB, NM USA
[16] Icahn Sch Med Mt Sinai, Fishberg Dept Neurosci, New York, NY 10029 USA
[17] Icahn Sch Med Mt Sinai, Friedman Brain Inst, New York, NY 10029 USA
[18] Johns Hopkins Univ Med Campus, Lieber Inst Brain Dev, Baltimore, MD USA
[19] Michigan State Univ, Neurosci Program, E Lansing, MI 48824 USA
[20] Yale Sch Med, Dept Genet, New Haven, CT USA
[21] Yale Univ, Howard Hughes Med Inst, New Haven, CT 06511 USA
[22] Rockefeller Univ, Lab Human Genet & Genom, 1230 York Ave, New York, NY 10065 USA
[23] Yale Sch Med, Yale Ctr Genom Anal, New Haven, CT USA
[24] Univ Calif San Francisco, Dept Psychiat, San Francisco, CA USA
[25] Univ Calif San Francisco, Langley Porter Psychiat Inst, San Francisco, CA USA
[26] Allen Inst Brain Sci, Seattle, WA USA
[27] Univ Southern Calif, Keck Sch Med, Dept Psychiat, Los Angeles, CA USA
[28] Univ Southern Calif, Keck Sch Med, Zilkha Neurogenet Inst, Los Angeles, CA USA
[29] Inst Catalana Recerca & Estudis Avancats, Barcelona, Catalonia, Spain
[30] Ctr Nacl Anal Genom, Barcelona, Catalonia, Spain
[31] George Washington Univ, Dept Anthropol, Washington, DC USA
[32] Yale Sch Med, Program Cellular Neurosci Neurodegenerat & Repair, New Haven, CT USA
[33] Yale Sch Med, Yale Child Study Ctr, New Haven, CT USA
关键词
HYDROXYLASE-IMMUNOREACTIVE NEURONS; GENE-EXPRESSION LEVELS; TYROSINE-HYDROXYLASE; CEREBRAL-CORTEX; HUMAN BRAIN; EVOLUTION; PRIMATE; TRANSCRIPTOME; DIVERSITY; NUMBER;
D O I
10.1126/science.aan3456
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
To better understand the molecular and cellular differences in brain organization between human and nonhuman primates, we performed transcriptome sequencing of 16 regions of adult human, chimpanzee, and macaque brains. Integration with human single-cell transcriptomic data revealed global, regional, and cell-type-specific species expression differences in genes representing distinct functional categories. We validated and further characterized the human specificity of genes enriched in distinct cell types through histological and functional analyses, including rare subpallial-derived interneurons expressing dopamine biosynthesis genes enriched in the human striatum and absent in the nonhuman African ape neocortex. Our integrated analysis of the generated data revealed diverse molecular and cellular features of the phylogenetic reorganization of the human brain across multiple levels, with relevance for brain function and disease.
引用
收藏
页码:1027 / 1032
页数:6
相关论文
共 40 条
[1]   Both Noncoding and Protein-Coding RNAs Contribute to Gene Expression Evolution in the Primate Brain [J].
Babbitt, Courtney C. ;
Fedrigo, Olivier ;
Pfefferle, Adam D. ;
Boyle, Alan P. ;
Horvath, Julie E. ;
Furey, Terrence S. ;
Wray, Gregory A. .
GENOME BIOLOGY AND EVOLUTION, 2010, 2 :67-79
[2]   Genetic Changes Shaping the Human Brain [J].
Bae, Byoung-Il ;
Jayaraman, Divya ;
Walsh, Christopher A. .
DEVELOPMENTAL CELL, 2015, 32 (04) :423-434
[3]   Distribution of neurons expressing tyrosine hydroxylase in the human cerebral cortex [J].
Benavides-Piccione, Ruth ;
DeFelipe, Javier .
JOURNAL OF ANATOMY, 2007, 211 (02) :212-222
[4]   TRANSIENT EXPRESSION OF TYROSINE-HYDROXYLASE IMMUNOREACTIVITY IN SOME NEURONS OF THE RAT NEOCORTEX DURING POSTNATAL-DEVELOPMENT [J].
BERGER, B ;
VERNEY, C ;
GASPAR, P ;
FEBVRET, A .
DEVELOPMENTAL BRAIN RESEARCH, 1985, 23 (01) :141-144
[5]   Transcriptome-wide Discovery of microRNA Binding Sites in Human Brain [J].
Boudreau, Ryan L. ;
Jiang, Peng ;
Gilmore, Brian L. ;
Spengler, Ryan M. ;
Tirabassi, Rebecca ;
Nelson, Jay A. ;
Ross, Christopher A. ;
Xing, Yi ;
Davidson, Beverly L. .
NEURON, 2014, 81 (02) :294-305
[6]   The evolution of gene expression levels in mammalian organs [J].
Brawand, David ;
Soumillon, Magali ;
Necsulea, Anamaria ;
Julien, Philippe ;
Csardi, Gabor ;
Harrigan, Patrick ;
Weier, Manuela ;
Liechti, Angelica ;
Aximu-Petri, Ayinuer ;
Kircher, Martin ;
Albert, Frank W. ;
Zeller, Ulrich ;
Khaitovich, Philipp ;
Gruetzner, Frank ;
Bergmann, Sven ;
Nielsen, Rasmus ;
Paeaebo, Svante ;
Kaessmann, Henrik .
NATURE, 2011, 478 (7369) :343-+
[7]   Elevated gene expression levels distinguish human from non-human primate brains [J].
Cáceres, M ;
Lachuer, J ;
Zapala, MA ;
Redmond, JC ;
Kudo, L ;
Geschwind, DH ;
Lockhart, DJ ;
Preuss, TM ;
Barlow, C .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2003, 100 (22) :13030-13035
[8]   A genetic variant that disrupts MET transcription is associated with autism [J].
Campbell, Daniel B. ;
Sutcliffe, James S. ;
Ebert, Philip J. ;
Militerni, Roberto ;
Bravaccio, Carmela ;
Trillo, Simona ;
Elia, Maurizio ;
Schneider, Cindy ;
Melmed, Raun ;
Sacco, Roberto ;
Persico, Antonio M. ;
Levitt, Pat .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (45) :16834-16839
[9]  
Close JL, 2017, NEURON, V93, P1035, DOI [10.1016/j.neuron.2017.02.014, 10.1016/j.neuron.2017.10.024]
[10]   A survey of human brain transcriptome diversity at the single cell level [J].
Darmanis, Spyros ;
Sloan, Steven A. ;
Zhang, Ye ;
Enge, Martin ;
Caneda, Christine ;
Shuer, Lawrence M. ;
Gephart, Melanie G. Hayden ;
Barres, Ben A. ;
Quake, Stephen R. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (23) :7285-7290