Decoding neuroproteomics: Integrating the genome, translatome and functional anatomy

Nature Neuroscience

Volumn 17, Issue 11, 2014, Pages 1491-1499

  Kitchen, Robert R ^a,b   Rozowsky, Joel S ^a   Gerstein, Mark B ^a,c   Nairn, Angus C ^b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Yale University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; BRAIN NERVE CELL; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; DNA RNA HYBRIDIZATION; FLUORESCENCE ACTIVATED CELL SORTING; FUNCTIONAL ANATOMY; FUNCTIONAL GENOMICS; GENOME; HUMAN; MASS SPECTROMETRY; NERVOUS TISSUE; NONHUMAN; POLYSOME; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE TRAIT LOCUS; REVIEW; RNA EDITING; TRANSCRIPTOMICS; ANATOMY AND HISTOLOGY; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; METABOLISM; PROCEDURES;

PROTEIN;

ANIMALS; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION PROFILING; GENOMICS; HUMANS; MASS SPECTROMETRY; PROTEINS; PROTEOMICS;

EID: 84908529852     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3829     Document Type: Review

References (124)

1. Pollock, J.D., Wu, D.-Y. & Satterlee, J.S. Molecular neuroanatomy: a generation of progress. Trends Neurosci. 37, 106-123 (2014
2. Medland, S.E., Jahanshad, N., Neale, B.M. & Thompson, P.M. Whole-genome analyses of whole-brain data: working within an expanded search space. Nat. Neurosci. 17, 791-800 (2014
3. Arenkiel, B.R. & Ehlers, M.D. Molecular genetics and imaging technologies for circuit-based neuroanatomy. Nature 461, 900-907 (2009
4. Van Essen, D.C. & Ugurbil, K. The future of the human connectome. Neuroimage 62, 1299-1310 (2012
5. Lichtman, J.W., Livet, J. & Sanes, J.R. A technicolour approach to the connectome. Nat. Rev. Neurosci. 9, 417-422 (2008
6. Ekstrand, M.I. et al. Molecular profiling of neurons based on connectivity. Cell 157, 1230-1242 (2014
7. Deisseroth, K. et al. Next-generation optical technologies for illuminating genetically targeted brain circuits. J. Neurosci. 26, 10380-10386 (2006
8. Sunkin, S.M. et al. Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system. Nucleic Acids Res. 41, D996-D1008 (2013
9. Uhlen, M. et al. Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 28, 1248-1250 (2010
10. Kang, H.J. et al. Spatio-temporal transcriptome of the human brain. Nature 478, 483-489 (2011
11. Johnson, M.B. et al. Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62, 494-509 (2009
12. Hawrylycz, M.J. et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489, 391-399 (2012
13. Heintz, N. Gene expression nervous system atlas (GENSAT). Nat. Neurosci. 7, 483 (2004
14. Korbel, J.O. et al. Paired-end mapping reveals extensive structural variation in the human genome. Science 318, 420-426 (2007
15. Park, P.J. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10, 669-680 (2009
16. Li, J.B. & Church, G.M. Deciphering the functions and regulation of brain-enriched A-to-I RNA editing. Nat. Neurosci. 16, 1518-1522 (2013
17. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R.S. & Weissman, J.S. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324, 218-223 (2009
18. Licatalosi, D.D. et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456, 464-469 (2008
19. Aebersold, R. & Mann, M. Mass spectrometry-based proteomics. Nature 422, 198-207 (2003
20. Stergachis, A.B., MacLean, B., Lee, K., Stamatoyannopoulos, J.A. & MacCoss, M.J. Rapid empirical discovery of optimal peptides for targeted proteomics. Nat. Methods 8, 1041-1043 (2011
21. Ong, S.-E. & Mann, M. Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262 (2005
22. Vidal, M. et al. The human proteome-a scientific opportunity for transforming diagnostics, therapeutics, and healthcare. Clin. Proteomics 9, 6 (2012
23. Wilhelm, M. et al. Mass-spectrometry-based draft of the human proteome. Nature 509, 582-587 (2014
24. Kim, M.-S. et al. A draft map of the human proteome. Nature 509, 575-581 (2014
25. Cox, J. & Mann, M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 80, 273-299 (2011
26. Altelaar, A.F.M., Munoz, J. & Heck, A.J.R. Next-generation proteomics: towards an integrative view of proteome dynamics. Nat. Rev. Genet. 14, 35-48 (2013
27. Nesvizhskii, A.I., Vitek, O. & Aebersold, R. Analysis and validation of proteomic data generated by tandem mass spectrometry. Nat. Methods 4, 787-797 (2007
28. Ahrens, C.H., Brunner, E., Qeli, E., Basler, K. & Aebersold, R. Generating and navigating proteome maps using mass spectrometry. Nat. Rev. Mol. Cell Biol. 11, 789-801 (2010
29. Bensimon, A., Heck, A.J.R. & Aebersold, R. Mass spectrometry-based proteomics and network biology. Annu. Rev. Biochem. 81, 379-405 (2012
30. Craft, G.E., Chen, A. & Nairn, A.C. Recent advances in quantitative neuroproteomics. Methods 61, 186-218 (2013
31. Cox, B. & Emili, A. Tissue subcellular fractionation and protein extraction for use in mass-spectrometry-based proteomics. Nat. Protoc. 1, 1872-1878 (2006
32. Boisvert, F.-M., Lam, Y.W., Lamont, D. & Lamond, A.I. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 9, 457-470 (2010
33. Schwanhäusser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011
34. Naegle, K.M. et al. PTMScout, a Web resource for analysis of high throughput post-translational proteomics studies. Mol. Cell. Proteomics 9, 2558-2570 (2010
35. Oppermann, F.S. et al. Large-scale proteomics analysis of the human kinome. Mol. Cell. Proteomics 8, 1751-1764 (2009
36. Deribe, Y.L., Pawson, T. & Dikic, I. Post-translational modifications in signal integration. Nat. Struct. Mol. Biol. 17, 666-672 (2010
37. Edwards, A.V.G., Edwards, G.J., Schwämmle, V., Saxtorph, H. & Larsen, M.R. Spatial and temporal effects in protein post-translational modification distributions in the developing mouse brain. J. Proteome Res. 13, 260-267 (2014
38. Seyfried, N.T. et al. Quantitative analysis of the detergent-insoluble brain proteome in frontotemporal lobar degeneration using SILAC internal standards. J. Proteome Res. 11, 2721-2738 (2012
39. Min, S.-W. et al. Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron 67, 953-966 (2010
40. Toffolo, E. et al. Phosphorylation of neuronal lysine-specific demethylase 1LSD1/KDM1A impairs transcriptional repression by regulating interaction with CoREST and histone deacetylases HDAC1/2. J. Neurochem. 128, 603-616 (2014
41. Sridharan, R. et al. Proteomic and genomic approaches reveal critical functions of H3K9 methylation and heterochromatin protein-1? in reprogramming to pluripotency. Nat. Cell Biol. 15, 872-882 (2013
42. Mirzaei, H. et al. Systematic measurement of transcription factor-DNA interactions by targeted mass spectrometry identifies candidate gene regulatory proteins. Proc. Natl. Acad. Sci. USA 110, 3645-3650 (2013
43. Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858 (2009
44. Zou, F. et al. Brain expression genome-wide association study (eGWAS) identifies human disease-associated variants. PLoS Genet. 8, e1002707 (2012
45. Kislinger, T. et al. Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling. Cell 125, 173-186 (2006
46. Shawahna, R. et al. Transcriptomic and quantitative proteomic analysis of transporters and drug metabolizing enzymes in freshly isolated human brain microvessels. Mol. Pharm. 8, 1332-1341 (2011
47. Elvira, G. et al. Characterization of an RNA granule from developing brain. Mol. Cell. Proteomics 5, 635-651 (2006
48. Moghaddas Gholami, A. et al. Global proteome analysis of the NCI-60 cell line panel. Cell Reports 4, 609-620 (2013
49. Geiger, T., Cox, J., Ostasiewicz, P., Wisniewski, J.R. & Mann, M. Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat. Methods 7, 383-385 (2010
50. Yu, L.-R. et al. Global analysis of the cortical neuron proteome. Mol. Cell. Proteomics 3, 896-907 (2004
51. Chen, R. et al. Personal omics profiling reveals dynamic molecular and medical phenotypes. Cell 148, 1293-1307 (2012
52. Phanstiel, D.H. et al. Proteomic and phosphoproteomic comparison of human ES and iPS cells. Nat. Methods 8, 821-827 (2011
53. Butovsky, O. et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17, 131-143 (2014
54. Greenbaum, D., Colangelo, C., Williams, K. & Gerstein, M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol. 4, 117 (2003
55. Lundberg, E. et al. Defining the transcriptome and proteome in three functionally different human cell lines. Mol. Syst. Biol. 6, 450 (2010
56. Ingolia, N.T., Lareau, L.F. & Weissman, J.S. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789-802 (2011
57. Li, J.J., Bickel, P.J. & Biggin, M.D. System wide analyses have underestimated protein abundances and the importance of transcription in mammals. PeerJ 2, e270 (2014
58. Heiman, M. et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748 (2008
59. Kong, J. & Lasko, P. Translational control in cellular and developmental processes. Nat. Rev. Genet. 13, 383-394 (2012
60. Brar, G.A. et al. High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335, 552-557 (2012
61. Gonzalez, C. et al. Ribosome profiling reveals a cell-type-specific translational landscape in brain tumors. J. Neurosci. 34, 10924-10936 (2014
62. Mercer, T.R., Dinger, M.E. & Mattick, J.S. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10, 155-159 (2009
63. Guttman, M., Russell, P., Ingolia, N.T., Weissman, J.S. & Lander, E.S. Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154, 240-251 (2013
64. Boisvert, F.M. et al. A quantitative spatial proteomics analysis of proteome turnover in human cells. Mol. Cell Proteomics 11, M111.011429 (2012
65. Aviner, R., Geiger, T. & Elroy-Stein, O. Genome-wide identification and quantification of protein synthesis in cultured cells and whole tissues by puromycin-associated nascent chain proteomics (PUNCH-P). Nat. Protoc. 9, 751-760 (2014
66. Wu, J.Q. et al. Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing. Proc. Natl. Acad. Sci. USA 107, 5254-5259 (2010
67. Nakata, K. et al. DISC1 splice variants are upregulated in schizophrenia and associated with risk polymorphisms. Proc. Natl. Acad. Sci. USA 106, 15873-15878 (2009
68. Sheynkman, G.M., Shortreed, M.R., Frey, B.L. & Smith, L.M. Discovery and mass spectrometric analysis of novel splice-junction peptides using RNA-Seq. Mol. Cell. Proteomics 12, 2341-2353 (2013
69. Soares, D.C., Carlyle, B.C., Bradshaw, N.J. & Porteous, D.J. DISC1: structure, function, and therapeutic potential for major mental illness. ACS Chem. Neurosci. 2, 609-632 (2011
70. Gonzàlez-Porta, M., Frankish, A., Rung, J., Harrow, J. & Brazma, A. Transcriptome analysis of human tissues and cell lines reveals one dominant transcript per gene. Genome Biol. 14, R70 (2013
71. Djebali, S. et al. Landscape of transcription in human cells. Nature 489, 101-108 (2012
72. Corominas, R. et al. Protein interaction network of alternatively spliced isoforms from brain links genetic risk factors for autism. Nat. Commun. 5, 3650 (2014
73. Sharon, D., Tilgner, H., Grubert, F. & Snyder, M. A single-molecule long-read survey of the human transcriptome. Nat. Biotechnol. 31, 1009-1014 (2013
74. Tran, J.C. et al. Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature 480, 254-258 (2011
75. Engström, P.G. et al. Systematic evaluation of spliced alignment programs for RNA-seq data. Nat. Methods 10, 1185-1191 (2013
76. Treutlein, B., Gokce, O., Quake, S.R. & Südhof, T.C. Cartography of neurexin alternative splicing mapped by single-molecule long-read mRNA sequencing. Proc. Natl. Acad. Sci. USA 111, E1291-E1299 (2014
77. Sakurai, M. et al. A biochemical landscape of A-to-I RNA editing in the human brain transcriptome. Genome Res. 24, 522-534 (2014
78. Lomeli, H. et al. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266, 1709-1713 (1994
79. Higuchi, M. et al. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406, 78-81 (2000
80. Kawahara, Y. et al. Dysregulated editing of serotonin 2C receptor mRNAs results in energy dissipation and loss of fat mass. J. Neurosci. 28, 12834-12844 (2008
81. Burns, C.M. et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387, 303-308 (1997
82. Pickrell, J.K., Gilad, Y. & Pritchard, J.K. Comment on "Widespread RNA and DNA sequence differences in the human transcriptome." Science 335, 1302 (2012
83. Buckland, P.R. Allele-specific gene expression differences in humans. Hum. Mol. Genet. 13, R255-R260 (2004
84. Khan, Z. et al. Quantitative measurement of allele-specific protein expression in a diploid yeast hybrid by LC-MS. Mol. Syst. Biol. 8, 602 (2012
85. Gregg, C. et al. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 329, 643-648 (2010
86. Butter, F. et al. Proteome-wide analysis of disease-associated SNPs that show allele-specific transcription factor binding. PLoS Genet. 8, e1002982 (2012
87. Holdt, L.M. et al. Quantitative trait loci mapping of the mouse plasma proteome (pQTL). Genetics 193, 601-608 (2013
88. Liu, C. et al. Whole-genome association mapping of gene expression in the human prefrontal cortex. Mol. Psychiatry 15, 779-784 (2010
89. Wu, L. et al. Variation and genetic control of protein abundance in humans. Nature 499, 79-82 (2013
90. Agam, G. et al. Knockout mice in understanding the mechanism of action of lithium. Biochem. Soc. Trans. 37, 1121-1125 (2009
91. Hangauer, M.J., Vaughn, I.W. & McManus, M.T. Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet. 9, e1003569 (2013
92. Martens, L. et al. PRIDE: the proteomics identifications database. Proteomics 5, 3537-3545 (2005
93. Desiere, F. et al. The PeptideAtlas project. Nucleic Acids Res. 34, D655-D658 (2006
94. Ahmad, Y. & Lamond, A.I. A perspective on proteomics in cell biology. Trends Cell Biol. 24, 257-264 (2014
95. Sun, Q. et al. PPDB, the Plant Proteomics Database at Cornell. Nucleic Acids Res. 37, D969-D974 (2009
96. Martens, L. et al. A comparison of the HUPO Brain Proteome Project pilot with other proteomics studies. Proteomics 6, 5076-5086 (2006
97. Bell, A.W. et al. A HUPO test sample study reveals common problems in mass spectrometry-based proteomics. Nat. Methods 6, 423-430 (2009
98. Menschaert, G. et al. Deep proteome coverage based on ribosome profiling aids mass spectrometry-based protein and peptide discovery and provides evidence of alternative translation products and near-cognate translation initiation events. Mol. Cell. Proteomics 12, 1780-1790 (2013
99. Lopez-Casado, G. et al. Enabling proteomic studies with RNA-Seq: the proteome of tomato pollen as a test case. Proteomics 12, 761-774 (2012
100. Wang, X. et al. Protein identification using customized protein sequence databases derived from RNA-Seq data. J. Proteome Res. 11, 1009-1017 (2012
101. Wang, X. & Zhang, B. customProDB: an R package to generate customized protein databases from RNA-Seq data for proteomics search. Bioinformatics 29, 3235-3237 (2013
102. Bayés, A. & Grant, S.G.N. Neuroproteomics: understanding the molecular organization and complexity of the brain. Nat. Rev. Neurosci. 10, 635-646 (2009
103. Sun, F. & Cavalli, V. Neuroproteomics approaches to decipher neuronal regeneration and degeneration. Mol. Cell. Proteomics 9, 963-975 (2010
104. Gebriel, M. et al. Zebrafish brain proteomics reveals central proteins involved in neurodegeneration. J. Neurosci. Res. 92, 104-115 (2014
105. Seo, J.-W., Kim, Y., Hur, J., Park, K.-S. & Cho, Y.-W. Proteomic analysis of primary cultured rat cortical neurons in chemical ischemia. Neurochem. Res. 38, 1648-1660 (2013
106. Liu, X. et al. Proteomics reveal energy metabolism and mitogen-activated protein kinase signal transduction perturbation in human Borna disease virus Hu-H1-infected oligodendroglial cells. Neuroscience 268, 284-296 (2014
107. Macaulay, I.C. & Voet, T. Single cell genomics: advances and future perspectives. PLoS Genet. 10, e1004126 (2014
108. Romanova, E.V., Aerts, J.T., Croushore, C.A. & Sweedler, J.V. Small-volume analysis of cell-cell signaling molecules in the brain. Neuropsychopharmacology 39, 50-64 (2014
109. Liu, X. et al. Molecular imaging of drug transit through the blood-brain barrier with MALDI mass spectrometry imaging. Sci. Rep. 3, 2859 (2013
110. Giesen, C. et al. Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat. Methods 11, 417-422 (2014
111. Biesemann, C. et al. Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting. EMBO J. 33, 157-170 (2014
112. Dammer, E.B. et al. Neuron enriched nuclear proteome isolated from human brain. J. Proteome Res. 12, 3193-3206 (2013
113. Spalding, K.L. et al. Dynamics of hippocampal neurogenesis in adult humans. Cell 153, 1219-1227 (2013
114. Ernst, A. et al. Neurogenesis in the striatum of the adult human brain. Cell 156, 1072-1083 (2014
115. Holt, C.E. & Schuman, E.M. The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 80, 648-657 (2013
116. Kavalali, E.T. & Jorgensen, E.M. Visualizing presynaptic function. Nat. Neurosci. 17, 10-16 (2014
117. Cheng, D. et al. Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol. Cell. Proteomics 5, 1158-1170 (2006
118. O'Rourke, N.A., Weiler, N.C., Micheva, K.D. & Smith, S.J. Deep molecular diversity of mammalian synapses: why it matters and how to measure it. Nat. Rev. Neurosci. 13, 365-379 (2012
119. Portales-Casamar, E. et al. A regulatory toolbox of MiniPromoters to drive selective expression in the brain. Proc. Natl. Acad. Sci. USA 107, 16589-16594 (2010
120. Jordi, E. et al. Differential effects of cocaine on histone posttranslational modifications in identified populations of striatal neurons. Proc. Natl. Acad. Sci. USA 110, 9511-9516 (2013
121. Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930 (2009
122. Selimi, F., Cristea, I.M., Heller, E., Chait, B.T. & Heintz, N. Proteomic studies of a single CNS synapse type: the parallel fiber/Purkinje cell synapse. PLoS Biol. 7, e83 (2009
123. Fernández, E. et al. Targeted tandem affinity purification of PSD-95 recovers core postsynaptic complexes and schizophrenia susceptibility proteins. Mol. Syst. Biol. 5, 269 (2009
124. Bateup, H.S. et al. Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat. Neurosci. 11, 932-939 (2008