Single-neuron sequencing analysis of l1 retrotransposition and somatic mutation in the human brain

Cell

Volumn 151, Issue 3, 2012, Pages 483-496

  Evrony, Gilad D ^a,c   Cai, Xuyu ^a,c   Lee, Eunjung ^b,d   Hills, L Benjamin ^c   Elhosary, Princess C ^c   Lehmann, Hillel S ^c   Parker, J J ^c   Atabay, Kutay D ^c   Gilmore, Edward C ^e   Poduri, Annapurna ^a,c   Park, Peter J ^b,c,d   Walsh, Christopher A ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Harvard Medical School Center for Biomedical Informatics   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84868032982     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.09.035     Document Type: Article

References (63)

1. J.K. Baillie, M.W. Barnett, K.R. Upton, D.J. Gerhardt, T.A. Richmond, F. De Sapio, P.M. Brennan, P. Rizzu, S. Smith, and M. Fell Somatic retrotransposition alters the genetic landscape of the human brain Nature 479 2011 534 537
2. C.R. Beck, P. Collier, C. Macfarlane, M. Malig, J.M. Kidd, E.E. Eichler, R.M. Badge, and J.V. Moran LINE-1 retrotransposition activity in human genomes Cell 141 2010 1159 1170
3. P.C. Blainey, and S.R. Quake Digital MDA for enumeration of total nucleic acid contamination Nucleic Acids Res. 39 2011 e19
4. M.A. Cantrell, L. Scott, C.J. Brown, A.R. Martinez, and H.A. Wichman Loss of LINE-1 activity in the megabats Genetics 178 2008 393 404
5. N.G. Coufal, J.L. Garcia-Perez, G.E. Peng, G.W. Yeo, Y. Mu, M.T. Lovci, M. Morell, K.S. O'Shea, J.V. Moran, and F.H. Gage L1 retrotransposition in human neural progenitor cells Nature 460 2009 1127 1131
6. F.B. Dean, S. Hosono, L. Fang, X. Wu, A.F. Faruqi, P. Bray-Ward, Z. Sun, Q. Zong, Y. Du, and J. Du Comprehensive human genome amplification using multiple displacement amplification Proc. Natl. Acad. Sci. USA 99 2002 5261 5266
7. R.P. Erickson Somatic gene mutation and human disease other than cancer: an update Mutat. Res. 705 2010 96 106
8. A.D. Ewing, and H.H. Kazazian Jr. High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes Genome Res. 20 2010 1262 1270
9. L. Flores-Sarnat, H.B. Sarnat, G. Dávila-Gutiérrez, and A. Alvarez Hemimegalencephaly: part 2. Neuropathology suggests a disorder of cellular lineage J. Child Neurol. 18 2003 776 785
10. D. Frumkin, A. Wasserstrom, S. Kaplan, U. Feige, and E. Shapiro Genomic variability within an organism exposes its cell lineage tree PLoS Comput. Biol. 1 2005 e50
11. R. Gittins, and P.J. Harrison Neuronal density, size and shape in the human anterior cingulate cortex: a comparison of Nissl and NeuN staining Brain Res. Bull. 63 2004 155 160
12. J.G. Gleeson, S. Minnerath, R.I. Kuzniecky, W.B. Dobyns, I.D. Young, M.E. Ross, and C.A. Walsh Somatic and germline mosaic mutations in the doublecortin gene are associated with variable phenotypes Am. J. Hum. Genet. 67 2000 574 581
13. D.C. Hancks, and H.H. Kazazian Jr. Active human retrotransposons: variation and disease Curr. Opin. Genet. Dev. 22 2012 191 203
14. Y. Hou, L. Song, P. Zhu, B. Zhang, Y. Tao, X. Xu, F. Li, K. Wu, J. Liang, and D. Shao Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm Cell 148 2012 873 885
15. R.C. Iskow, M.T. McCabe, R.E. Mills, S. Torene, W.S. Pittard, A.F. Neuwald, E.G. Van Meir, P.M. Vertino, and S.E. Devine Natural mutagenesis of human genomes by endogenous retrotransposons Cell 141 2010 1253 1261
16. T. Kalisky, P. Blainey, and S.R. Quake Genomic analysis at the single-cell level Annu. Rev. Genet. 45 2011 431 445
17. M. Krzywinski, J. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S.J. Jones, and M.A. Marra Circos: an information aesthetic for comparative genomics Genome Res. 19 2009 1639 1645
18. R.S. Lasken, and T.B. Stockwell Mechanism of chimera formation during the Multiple Displacement Amplification reaction BMC Biotechnol. 7 2007 19
19. E. Lee, R. Iskow, L. Yang, O. Gokcumen, P. Haseley, L.J. Luquette III, J.G. Lohr, C.C. Harris, L. Ding, R.K. Wilson Cancer Genome Atlas Research Network Landscape of somatic retrotransposition in human cancers Science 337 2012 967 971
20. J.H. Lee, M. Huynh, J.L. Silhavy, S. Kim, T. Dixon-Salazar, A. Heiberg, E. Scott, V. Bafna, K.J. Hill, and A. Collazo De novo somatic mutations in components of the PI3K-AKT3-mTOR pathway cause hemimegalencephaly Nat. Genet. 44 2012 941 945
21. S. Magavi, D. Friedmann, G. Banks, A. Stolfi, and C. Lois Coincident generation of pyramidal neurons and protoplasmic astrocytes in neocortical columns J. Neurosci. 32 2012 4762 4772
22. A. Matevossian, and S. Akbarian Neuronal nuclei isolation from human postmortem brain tissue J. Vis. Exp. 20 2008 e914
23. Y. Miki, I. Nishisho, A. Horii, Y. Miyoshi, J. Utsunomiya, K.W. Kinzler, B. Vogelstein, and Y. Nakamura Disruption of the APC gene by a retrotransposal insertion of L1 sequence in a colon cancer Cancer Res. 52 1992 643 645
24. S.E. Mills Histology for pathologists Third Edition 2007 Lippincott Williams & Wilkins Philadelphia
25. R.J. Mullen, C.R. Buck, and A.M. Smith NeuN, a neuronal specific nuclear protein in vertebrates Development 116 1992 201 211
26. A.R. Muotri, and F.H. Gage Generation of neuronal variability and complexity Nature 441 2006 1087 1093
27. A.R. Muotri, V.T. Chu, M.C.N. Marchetto, W. Deng, J.V. Moran, and F.H. Gage Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition Nature 435 2005 903 910
28. A.R. Muotri, M.C. Marchetto, N.G. Coufal, R. Oefner, G. Yeo, K. Nakashima, and F.H. Gage L1 retrotransposition in neurons is modulated by MeCP2 Nature 468 2010 443 446
29. N. Navin, J. Kendall, J. Troge, P. Andrews, L. Rodgers, J. McIndoo, K. Cook, A. Stepansky, D. Levy, and D. Esposito Tumour evolution inferred by single-cell sequencing Nature 472 2011 90 94
30. I. Ovchinnikov, A. Rubin, and G.D. Swergold Tracing the LINEs of human evolution Proc. Natl. Acad. Sci. USA 99 2002 10522 10527
31. A. Parent, and M.B. Carpenter Carpenter's human neuroanatomy 1996 Williams & Wilkins Baltimore, MD
32. A. Poduri, G.D. Evrony, X. Cai, P.C. Elhosary, R. Beroukhim, M.K. Lehtinen, L.B. Hills, E.L. Heinzen, A. Hill, and R.S. Hill Somatic activation of AKT3 causes hemispheric developmental brain malformations Neuron 74 2012 41 48
33. S.K. Rehen, Y.C. Yung, M.P. McCreight, D. Kaushal, A.H. Yang, B.S. Almeida, M.A. Kingsbury, K.M. Cabral, M.J. McConnell, and B. Anliker Constitutional aneuploidy in the normal human brain J. Neurosci. 25 2005 2176 2180
34. J.B. Rivière, G.M. Mirzaa, B.J. O'Roak, M. Beddaoui, D. Alcantara, R.L. Conway, J. St-Onge, J.A. Schwartzentruber, K.W. Gripp, S.M. Nikkel Finding of Rare Disease Genes (FORGE) Canada Consortium De novo germline and postzygotic mutations in AKT3, PIK3R2 and PIK3CA cause a spectrum of related megalencephaly syndromes Nat. Genet. 44 2012 934 940
35. S.J. Salipante, J.M. Thompson, and M.S. Horwitz Phylogenetic fate mapping: theoretical and experimental studies applied to the development of mouse fibroblasts Genetics 178 2008 967 977
36. T. Singer, M.J. McConnell, M.C. Marchetto, N.G. Coufal, and F.H. Gage LINE-1 retrotransposons: mediators of somatic variation in neuronal genomes? Trends Neurosci. 33 2010 345 354
37. K.L. Spalding, R.D. Bhardwaj, B.A. Buchholz, H. Druid, and J. Frisén Retrospective birth dating of cells in humans Cell 122 2005 133 143
38. J.A.J.M. Van den Hurk, I.C. Meij, M.C. Seleme, H. Kano, K. Nikopoulos, L.H. Hoefsloot, E.A. Sistermans, I.J. de Wijs, A. Mukhopadhyay, and A.S. Plomp L1 retrotransposition can occur early in human embryonic development Hum. Mol. Genet. 16 2007 1587 1592
39. J. Wang, H.C. Fan, B. Behr, and S.R. Quake Genome-wide single-cell analysis of recombination activity and de novo mutation rates in human sperm Cell 150 2012 402 412
40. H.K. Wolf, R. Buslei, R. Schmidt-Kastner, P.K. Schmidt-Kastner, T. Pietsch, O.D. Wiestler, and I. Blümcke NeuN: a useful neuronal marker for diagnostic histopathology J. Histochem. Cytochem. 44 1996 1167 1171
41. X. Xu, Y. Hou, X. Yin, L. Bao, A. Tang, L. Song, F. Li, S. Tsang, K. Wu, and H. Wu Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor Cell 148 2012 886 895
42. K. Zhang, A.C. Martiny, N.B. Reppas, K.W. Barry, J. Malek, S.W. Chisholm, and G.M. Church Sequencing genomes from single cells by polymerase cloning Nat. Biotechnol. 24 2006 680 686
43. Dombroski, B.A.; Mathias, S.L.; Nanthakumar, E.; Scott, A.F.; and Kazazian, H.H.; Jr. (1991). Isolation of an active human transposable element. Science 254, 1805-1808.
44. Esteban, J.A.; Salas, M.; and Blanco, L. (1993). Fidelity of phi 29 DNA polymerase. Comparison between protein-primed initiation and DNA polymerization. J. Biol. Chem. 268, 2719-2726.
45. Ewing, A.D.; and Kazazian, H.H.; Jr. (2011). Whole-genome resequencing allows detection of many rare LINE-1 insertion alleles in humans. Genome Res. 21, 985-990.
46. Goecks, J.; Nekrutenko, A.; and Taylor, J.; Galaxy Team (2010). Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 11, R86.
47. Huang, C.R.; Schneider, A.M.; Lu, Y.; Niranjan, T.; Shen, P.; Robinson, M.A.; Steranka, J.P.; Valle, D.; Civin, C.I.; Wang, T.; et al. (2010). Mobile interspersed repeats are major structural variants in the human genome. Cell 141, 1171-1182.
48. Kent, W.J.; Sugnet, C.W.; Furey, T.S.; Roskin, K.M.; Pringle, T.H.; Zahler, A.M.; and Haussler, D. (2002). The human genome browser at UCSC. Genome Res. 12, 996-1006.
49. Kircher, M.; Sawyer, S.; and Meyer, M. (2012). Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3.
50. Langmead, B.; Trapnell, C.; Pop, M.; and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
51. Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R.; et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
52. Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; and Durbin, R.; 1000 Genome Project Data Processing Subgroup (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079.
53. Lyck, L.; Dalmau, I.; Chemnitz, J.; Finsen, B.; and Schroder, H.D. (2008). Immunohistochemical markers for quantitative studies of neurons and glia in human neocortex. J. Histochem. Cytochem. 56, 201-221.
54. Nielsen, S.; Nagelhus, E.A.; Amiry-Moghaddam, M.; Bourque, C.; Agre, P.; and Ottersen, O.P. (1997). Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17, 171-180.
55. Quinlan, A.R.; and Hall, I.M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842.
56. R Development Core Team (2011). R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna. http://www.r-project.org.
57. Robinson, J.T.; Thorvaldsdóttir, H.; Winckler, W.; Guttman, M.; Lander, E.S.; Getz, G.; and Mesirov, J.P. (2011). Integrative genomics viewer. Nat. Biotechnol. 29, 24-26.
58. Rozen, S.; and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386.
59. Smit, A.F.A.; Hubley, R.; and Green, P. (2010). RepeatMasker Open-3.0. http://www.repeatmasker.org.
60. Stewart, C.; Kural, D.; Strömberg, M.P.; Walker, J.A.; Konkel, M.K.; Stütz, A.M.; Urban, A.E.; Grubert, F.; Lam, H.Y.K.; Lee, W.-P.; et al.; 1000 Genomes Project (2011). A comprehensive map of mobile element insertion polymorphisms in humans. PLoS Genet. 7, e1002236.
61. Sudhof, T.C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547.
62. Wang, J.; Song, L.; Grover, D.; Azrak, S.; Batzer, M.A.; and Liang, P. (2006). dbRIP: a highly integrated database of retrotransposon insertion polymorphisms in humans. Hum. Mutat. 27, 323-329.
63. Yamada, T.; Soma, H.; and Morishita, S. (2006). PrimerStation: a highly specific multiplex genomic PCR primer design server for the human genome. Nucleic Acids Res. 34, W665-W669.