|
|
Transcriptomics and proteomics in stem cell research |
Hai Wang, Qian Zhang, Xiangdong Fang() |
CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China |
|
|
Abstract Stem cells are capable of self-renewal and differentiation, and the processes regulating these events are among the most comprehensively investigated topics in life sciences. In particular, the molecular mechanisms of the self-renewal, proliferation, and differentiation of stem cells have been extensively examined. Multi-omics integrative analysis, such as transcriptomics combined with proteomics, is one of the most promising approaches to the systemic investigation of stem cell biology. We reviewed the available information on stem cells by examining published results using transcriptomic and proteomic characterization of the different stem cell processes. Comprehensive understanding of these important processes can only be achieved using a systemic methodology, and employing such method will strengthen the study on stem cell biology and promote the clinical applications of stem cells.
|
Keywords
embryonic stem cells
transcriptomics
proteomics
|
Corresponding Author(s):
Xiangdong Fang
|
Online First Date: 26 June 2014
Issue Date: 18 December 2014
|
|
1 |
SM Ahn, R Simpson, B Lee. Genomics and proteomics in stem cell research: the road ahead. Anat Cell Biol 2010; 43(1): 1–14
https://doi.org/10.5115/acb.2010.43.1.1
pmid: 21190000
|
2 |
VK Gangaraju, H Lin. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 2009; 10(2): 116–125
https://doi.org/10.1038/nrm2621
pmid: 19165214
|
3 |
AM Wobus, KR Boheler. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 2005; 85(2): 635–678
https://doi.org/10.1152/physrev.00054.2003
pmid: 15788707
|
4 |
PA Callinan, AP Feinberg. The emerging science of epigenomics. Hum Mol Genet 2006; 15(Spec No 1): R95–R101
https://doi.org/10.1093/hmg/ddl095
pmid: 16651376
|
5 |
MV Schneider, S Orchard. Omics technologies, data and bioinformatics principles. Methods Mol Biol 2011; 719: 3–30
https://doi.org/10.1007/978-1-61779-027-0_1
pmid: 21370077
|
6 |
LW Stanton, MM Bakre. Genomic and proteomic characterization of embryonic stem cells. Curr Opin Chem Biol 2007; 11(4): 399–404
https://doi.org/10.1016/j.cbpa.2007.05.029
pmid: 17646122
|
7 |
Z Wang, M Gerstein, M Snyder. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009; 10(1): 57–63
https://doi.org/10.1038/nrg2484
pmid: 19015660
|
8 |
S Efroni, R Duttagupta, J Cheng, H Dehghani, DJ Hoeppner, C Dash, DP Bazett-Jones, S Le Grice, RDG McKay, KH Buetow, TR Gingeras, T Misteli, E Meshorer. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2008; 2(5): 437–447
https://doi.org/10.1016/j.stem.2008.03.021
pmid: 18462694
|
9 |
MH Chin, MJ Mason, W Xie, S Volinia, M Singer, C Peterson, G Ambartsumyan, O Aimiuwu, L Richter, J Zhang, I Khvorostov, V Ott, M Grunstein, N Lavon, N Benvenisty, CM Croce, AT Clark, T Baxter, AD Pyle, MA Teitell, M Pelegrini, K Plath, WE Lowry. Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 2009; 5(1): 111–123
https://doi.org/10.1016/j.stem.2009.06.008
pmid: 19570518
|
10 |
I Ginis, Y Luo, T Miura, S Thies, R Brandenberger, S Gerecht-Nir, M Amit, A Hoke, MK Carpenter, J Itskovitz-Eldor, MS Rao. Differences between human and mouse embryonic stem cells. Dev Biol 2004; 269(2): 360–380
https://doi.org/10.1016/j.ydbio.2003.12.034
pmid: 15110706
|
11 |
B Bhattacharya, T Miura, R Brandenberger, J Mejido, Y Luo, AX Yang, BH Joshi, I Ginis, RS Thies, M Amit, I Lyons, BG Condie, J Itskovitz-Eldor, MS Rao, RK Puri. Gene expression in human embryonic stem cell lines: unique molecular signature. Blood 2004; 103(8): 2956–2964
https://doi.org/10.1182/blood-2003-09-3314
pmid: 15070671
|
12 |
R Brandenberger, I Khrebtukova, RS Thies, T Miura, C Jingli, R Puri, T Vasicek, J Lebkowski, M Rao. MPSS profiling of human embryonic stem cells. BMC Dev Biol 2004; 4(1): 10
https://doi.org/10.1186/1471-213X-4-10
pmid: 15304200
|
13 |
M Zhan. Genomic studies to explore self-renewal and differentiation properties of embryonic stem cells. Front Biosci 2008; 13(13): 276–283
https://doi.org/10.2741/2678
pmid: 17981546
|
14 |
F Djouad, C Bony, F Canovas, O Fromigué, T Rème, C Jorgensen, D Noël. Transcriptomic analysis identifies Foxo3A as a novel transcription factor regulating mesenchymal stem cell chrondrogenic differentiation. Cloning Stem Cells 2009; 11(3): 407–416
https://doi.org/10.1089/clo.2009.0013
pmid: 19751111
|
15 |
NB Ivanova, JT Dimos, C Schaniel, JA Hackney, KA Moore, IR Lemischka. A stem cell molecular signature. Science 2002; 298(5593): 601–604
https://doi.org/10.1126/science.1073823
pmid: 12228721
|
16 |
M Ramalho-Santos, S Yoon, Y Matsuzaki, RC Mulligan, DA Melton. “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science 2002; 298(5593): 597–600
https://doi.org/10.1126/science.1072530
pmid: 12228720
|
17 |
M Suárez-Fariñas, S Noggle, M Heke, A Hemmati-Brivanlou, MO Magnasco. Comparing independent microarray studies: the case of human embryonic stem cells. BMC Genomics 2005; 6(1): 99
https://doi.org/10.1186/1471-2164-6-99
pmid: 16042783
|
18 |
Y Yang, H Wang, KH Chang, H Qu, Z Zhang, Q Xiong, H Qi, P Cui, Q Lin, X Ruan, Y Yang, Y Li, C Shu, Q Li, EK Wakeland, J Yan, S Hu, X Fang. Transcriptome dynamics during human erythroid differentiation and development. Genomics 2013; 102(5-6): 431–441
https://doi.org/10.1016/j.ygeno.2013.09.005
pmid: 24121002
|
19 |
AA Sigova, AC Mullen, B Molinie, S Gupta, DA Orlando, MG Guenther, AE Almada, C Lin, PA Sharp, CC Giallourakis, RA Young. Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc Natl Acad Sci USA 2013; 110(8): 2876–2881
https://doi.org/10.1073/pnas.1221904110
pmid: 23382218
|
20 |
L Yan, M Yang, H Guo, L Yang, J Wu, R Li, P Liu, Y Lian, X Zheng, J Yan, J Huang, M Li, X Wu, L Wen, K Lao, R Li, J Qiao, F Tang. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 2013; 20(9): 1131–1139
https://doi.org/10.1038/nsmb.2660
pmid: 23934149
|
21 |
T MacRae, T Sargeant, S Lemieux, J Hébert, E Deneault, G Sauvageau. RNA-Seq reveals spliceosome and proteasome genes as most consistent transcripts in human cancer cells. PLoS ONE 2013; 8(9): e72884
https://doi.org/10.1371/journal.pone.0072884
pmid: 24069164
|
22 |
K Jääger, S Islam, P Zajac, S Linnarsson, T Neuman. RNA-seq analysis reveals different dynamics of differentiation of human dermis- and adipose-derived stromal stem cells. PLoS ONE 2012; 7(6): e38833
https://doi.org/10.1371/journal.pone.0038833
pmid: 22723894
|
23 |
G Gargiulo, M Cesaroni, M Serresi, N de Vries, D Hulsman, SW Bruggeman, C Lancini, M van Lohuizen.In vivo RNAi screen for BMI1 targets identifies TGF-β/BMP-ER stress pathways as key regulators of neural- and malignant glioma-stem cell homeostasis. Cancer Cell 2013; 23(5): 660–676
https://doi.org/10.1016/j.ccr.2013.03.030
pmid: 23680149
|
24 |
N Salomonis, CR Schlieve, L Pereira, C Wahlquist, A Colas, AC Zambon, K Vranizan, MJ Spindler, AR Pico, MS Cline, TA Clark, A Williams, JE Blume, E Samal, M Mercola, BJ Merrill, BR Conklin. Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc Natl Acad Sci USA 2010; 107(23): 10514–10519
https://doi.org/10.1073/pnas.0912260107
pmid: 20498046
|
25 |
JQ Wu, L Habegger, P Noisa, A Szekely, C Qiu, S Hutchison, D Raha, M Egholm, H Lin, S Weissman, W Cui, M Gerstein, M Snyder. Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing. Proc Natl Acad Sci USA 2010; 107(11): 5254–5259
https://doi.org/10.1073/pnas.0914114107
pmid: 20194744
|
26 |
R Brandenberger, H Wei, S Zhang, S Lei, J Murage, GJ Fisk, Y Li, C Xu, R Fang, K Guegler, MS Rao, R Mandalam, J Lebkowski, LW Stanton. Transcriptome characterization elucidates signaling networks that control human ES cell growth and differentiation. Nat Biotechnol 2004; 22(6): 707–716
https://doi.org/10.1038/nbt971
pmid: 15146197
|
27 |
SV Anisimov, KV Tarasov, D Tweedie, MD Stern, AM Wobus, KR Boheler. SAGE identification of gene transcripts with profiles unique to pluripotent mouse R1 embryonic stem cells. Genomics 2002; 79(2): 169–176
https://doi.org/10.1006/geno.2002.6687
pmid: 11829487
|
28 |
L He, GJ Hannon. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5(7): 522–531
https://doi.org/10.1038/nrg1379
pmid: 15211354
|
29 |
MR Suh, Y Lee, JY Kim, SK Kim, SH Moon, JY Lee, KY Cha, HM Chung, HS Yoon, SY Moon, VN Kim, KS Kim. Human embryonic stem cells express a unique set of microRNAs. Dev Biol 2004; 270(2): 488–498
https://doi.org/10.1016/j.ydbio.2004.02.019
pmid: 15183728
|
30 |
A Jouneau, C Ciaudo, O Sismeiro, V Brochard, L Jouneau, S Vandormael-Pournin, JY Coppée, Q Zhou, E Heard, C Antoniewski, M Cohen-Tannoudji. Naive and primed murine pluripotent stem cells have distinct miRNA expression profiles. RNA 2012; 18(2): 253–264
https://doi.org/10.1261/rna.028878.111
pmid: 22201644
|
31 |
FF Kirigin, K Lindstedt, M Sellars, M Ciofani, SL Low, L Jones, F Bell, F Pauli, R Bonneau, RM Myers, DR Littman, MMW Chong. Dynamic microRNA gene transcription and processing during T cell development. J Immunol 2012; 188(7): 3257–3267
https://doi.org/10.4049/jimmunol.1103175
pmid: 22379031
|
32 |
A Marson, SS Levine, MF Cole, GM Frampton, T Brambrink, S Johnstone, MG Guenther, WK Johnston, M Wernig, J Newman, JM Calabrese, LM Dennis, TL Volkert, S Gupta, J Love, N Hannett, PA Sharp, DP Bartel, R Jaenisch, RA Young. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008; 134(3): 521–533
https://doi.org/10.1016/j.cell.2008.07.020
pmid: 18692474
|
33 |
JS Mattick. A new paradigm for developmental biology. J Exp Biol 2007; 210(Pt 9): 1526–1547
https://doi.org/10.1242/jeb.005017
pmid: 17449818
|
34 |
J Sheik Mohamed, PM Gaughwin, B Lim, P Robson, L Lipovich. Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 2010; 16(2): 324–337
https://doi.org/10.1261/rna.1441510
pmid: 20026622
|
35 |
ME Dinger, PP Amaral, TR Mercer, KC Pang, SJ Bruce, BB Gardiner, ME Askarian-Amiri, K Ru, G Soldà, C Simons, SM Sunkin, ML Crowe, SM Grimmond, AC Perkins, JS Mattick. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 2008; 18(9): 1433–1445
https://doi.org/10.1101/gr.078378.108
pmid: 18562676
|
36 |
AD Ramos, A Diaz, A Nellore, RN Delgado, KY Park, G Gonzales-Roybal, MC Oldham, JS Song, DA Lim. Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 2013; 12(5): 616–628
https://doi.org/10.1016/j.stem.2013.03.003
pmid: 23583100
|
37 |
RD Unwin, SJ Gaskell, CA Evans, AD Whetton. The potential for proteomic definition of stem cell populations. Exp Hematol 2003; 31(12): 1147–1159
https://doi.org/10.1016/j.exphem.2003.08.012
pmid: 14662320
|
38 |
H Baharvand, A Fathi, D van Hoof, GH Salekdeh. Concise review: trends in stem cell proteomics. Stem Cells 2007; 25(8): 1888–1903
https://doi.org/10.1634/stemcells.2007-0107
pmid: 17495109
|
39 |
K Nagano, M Taoka, Y Yamauchi, C Itagaki, T Shinkawa, K Nunomura, N Okamura, N Takahashi, T Izumi, T Isobe. Large-scale identification of proteins expressed in mouse embryonic stem cells. Proteomics 2005; 5(5): 1346–1361
https://doi.org/10.1002/pmic.200400990
pmid: 15742316
|
40 |
D Nasrabadi, M Rezaei Larijani, L Pirhaji, H Gourabi, A Shahverdi, H Baharvand, GH Salekdeh. Proteomic analysis of monkey embryonic stem cell during differentiation. J Proteome Res 2009; 8(3): 1527–1539
https://doi.org/10.1021/pr800880v
pmid: 19226164
|
41 |
A Böser, HCA Drexler, H Reuter, H Schmitz, G Wu, HR Schöler, L Gentile, K Bartscherer. SILAC proteomics of planarians identifies Ncoa5 as a conserved component of pluripotent stem cells. Cell Reports 2013; 5(4): 1142–1155
https://doi.org/10.1016/j.celrep.2013.10.035
pmid: 24268775
|
42 |
Y Sun, Y Yang, S Zeng, Y Tan, G Lu, G Lin. Identification of proteins related to epigenetic regulation in the malignant transformation of aberrant karyotypic human embryonic stem cells by quantitative proteomics. PLoS ONE 2014; 9(1): e85823
https://doi.org/10.1371/journal.pone.0085823
pmid: 24465727
|
43 |
S D’Aguanno, D Barcaroli, C Rossi, M Zucchelli, D Ciavardelli, C Cortese, A De Cola, S Volpe, D D’Agostino, M Todaro, G Stassi, C Di Ilio, A Urbani, V De Laurenzi. p63 Isoforms Regulate Metabolism of Cancer Stem Cells. J Proteome Res 2014; 13(4): 2120–2136
https://doi.org/10.1021/pr4012574
pmid: 24597989
|
44 |
H Lin, E Lee, K Hestir, C Leo, M Huang, E Bosch, R Halenbeck, G Wu, A Zhou, D Behrens, D Hollenbaugh, T Linnemann, M Qin, J Wong, K Chu, SK Doberstein, LT Williams. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 2008; 320(5877): 807–811
https://doi.org/10.1126/science.1154370
pmid: 18467591
|
45 |
R Gonzalez, LL Jennings, M Knuth, AP Orth, HE Klock, W Ou, J Feuerhelm, MV Hull, E Koesema, Y Wang, J Zhang, C Wu, CY Cho, AI Su, S Batalov, H Chen, K Johnson, B Laffitte, DG Nguyen, EY Snyder, PG Schultz, JL Harris, SA Lesley. Screening the mammalian extracellular proteome for regulators of embryonic human stem cell pluripotency. Proc Natl Acad Sci USA 2010; 107(8): 3552–3557
https://doi.org/10.1073/pnas.0914019107
pmid: 20133595
|
46 |
M Gemei, C Corbo, F D’Alessio, R Di Noto, R Vento, L Del Vecchio. Surface proteomic analysis of differentiated versus stem-like osteosarcoma human cells. Proteomics 2013; 13(22): 3293–3297
https://doi.org/10.1002/pmic.201300170
pmid: 24106197
|
47 |
D Van Hoof, J Muñoz, SR Braam, MWH Pinkse, R Linding, AJR Heck, CL Mummery, J Krijgsveld. Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 2009; 5(2): 214–226
https://doi.org/10.1016/j.stem.2009.05.021
pmid: 19664995
|
48 |
LM Brill, W Xiong, KB Lee, SB Ficarro, A Crain, Y Xu, A Terskikh, EY Snyder, S Ding. Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 2009; 5(2): 204–213
https://doi.org/10.1016/j.stem.2009.06.002
pmid: 19664994
|
49 |
DL Swaney, CD Wenger, JA Thomson, JJ Coon. Human embryonic stem cell phosphoproteome revealed by electron transfer dissociation tandem mass spectrometry. Proc Natl Acad Sci USA 2009; 106(4): 995–1000
https://doi.org/10.1073/pnas.0811964106
pmid: 19144917
|
50 |
KT Rigbolt, TA Prokhorova, V Akimov, J Henningsen, PT Johansen, I Kratchmarova, M Kassem, M Mann, JV Olsen, B Blagoev. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal 2011; 4(164): rs3
https://doi.org/10.1126/scisignal.2001570
pmid: 21406692
|
51 |
H Xu, C Baroukh, R Dannenfelser, EY Chen, CM Tan, Y Kou, YE Kim, IR Lemischka, A Ma’ayan. ESCAPE: database for integrating high-content published data collected from human and mouse embryonic stem cells. Database (Oxford) 2013; 2013: bat045
https://doi.org/10.1093/database/bat045
pmid: 23794736
|
52 |
MH Chin, MJ Mason, W Xie, S Volinia, M Singer, C Peterson, G Ambartsumyan, O Aimiuwu, L Richter, J Zhang, I Khvorostov, V Ott, M Grunstein, N Lavon, N Benvenisty, CM Croce, AT Clark, T Baxter, AD Pyle, MA Teitell, M Pelegrini, K Plath, WE Lowry. Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 2009; 5(1): 111–123
https://doi.org/10.1016/j.stem.2009.06.008
pmid: 19570518
|
53 |
J Yu, K Hu, K Smuga-Otto, S Tian, R Stewart, II Slukvin, JA Thomson. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009; 324(5928): 797–801
https://doi.org/10.1126/science.1172482
pmid: 19325077
|
54 |
D Van Hoof, J Muñoz, SR Braam, MWH Pinkse, R Linding, AJR Heck, CL Mummery, J Krijgsveld. Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 2009; 5(2): 214–226
https://doi.org/10.1016/j.stem.2009.05.021
pmid: 19664995
|
55 |
J Munoz, TY Low, YJ Kok, A Chin, CK Frese, V Ding, A Choo, AJR Heck. The quantitative proteomes of human-induced pluripotent stem cells and embryonic stem cells. Mol Syst Biol 2011; 7: 550
https://doi.org/10.1038/msb.2011.84
pmid: 22108792
|
56 |
R Sridharan, M Gonzales-Cope, C Chronis, G Bonora, R McKee, C Huang, S Patel, D Lopez, N Mishra, M Pellegrini, M Carey, BA Garcia, K Plath. Proteomic and genomic approaches reveal critical functions of H3K9 methylation and heterochromatin protein-1γ in reprogramming to pluripotency. Nat Cell Biol 2013; 15(7): 872–882
https://doi.org/10.1038/ncb2768
pmid: 23748610
|
57 |
DH Phanstiel, J Brumbaugh, CD Wenger, S Tian, MD Probasco, DJ Bailey, DL Swaney, MA Tervo, JM Bolin, V Ruotti, R Stewart, JA Thomson, JJ Coon. Proteomic and phosphoproteomic comparison of human ES and iPS cells. Nat Methods 2011; 8(10): 821–827
https://doi.org/10.1038/nmeth.1699
pmid: 21983960
|
58 |
C Perez-Iratxeta, G Palidwor, CJ Porter, NA Sanche, MR Huska, BP Suomela, EM Muro, PM Krzyzanowski, E Hughes, PA Campbell, MA Rudnicki, MA Andrade. Study of stem cell function using microarray experiments. FEBS Lett 2005; 579(8): 1795–1801
https://doi.org/10.1016/j.febslet.2005.02.020
pmid: 15763554
|
59 |
SA Sansone, P Rocca-Serra, D Field, E Maguire, C Taylor, O Hofmann, H Fang, S Neumann, W Tong, L Amaral-Zettler, K Begley, T Booth, L Bougueleret, G Burns, B Chapman, T Clark, LA Coleman, J Copeland, S Das, A de Daruvar, P de Matos, I Dix, S Edmunds, CT Evelo, MJ Forster, P Gaudet, J Gilbert, C Goble, JL Griffin, D Jacob, J Kleinjans, L Harland, K Haug, H Hermjakob, SJ Ho Sui, A Laederach, S Liang, S Marshall, A McGrath, E Merrill, D Reilly, M Roux, CE Shamu, CA Shang, C Steinbeck, A Trefethen, B Williams-Jones, K Wolstencroft, I Xenarios, W Hide. Toward interoperable bioscience data. Nat Genet 2012; 44(2): 121–126
https://doi.org/10.1038/ng.1054
pmid: 22281772
|
60 |
SJ Ho Sui, K Begley, D Reilly, B Chapman, R McGovern, P Rocca-Sera, E Maguire, GM Altschuler, TAA Hansen, R Sompallae, A Krivtsov, RA Shivdasani, SA Armstrong, AC Culhane, M Correll, SA Sansone, O Hofmann, W Hide. The Stem Cell Discovery Engine: an integrated repository and analysis system for cancer stem cell comparisons. Nucleic Acids Res 2012; 40(Database issue): D984–D991
https://doi.org/10.1093/nar/gkr1051
pmid: 22121217
|
61 |
M Jung, H Peterson, L Chavez, P Kahlem, H Lehrach, J Vilo, J Adjaye. A data integration approach to mapping OCT4 gene regulatory networks operative in embryonic stem cells and embryonal carcinoma cells. PLoS ONE 2010; 5(5): e10709
https://doi.org/10.1371/journal.pone.0010709
pmid: 20505756
|
62 |
BS Mallon, JG Chenoweth, KR Johnson, RS Hamilton, PJ Tesar, AS Yavatkar, LJ Tyson, K Park, KG Chen, YC Fann, RDG McKay. StemCellDB: the human pluripotent stem cell database at the National Institutes of Health. Stem Cell Res (Amst) 2013; 10(1): 57–66
https://doi.org/10.1016/j.scr.2012.09.002
pmid: 23117585
|
63 |
V Costa, C Angelini, I De Feis, A Ciccodicola. Uncovering the complexity of transcriptomes with RNA-Seq. J Biomed Biotechnol 2010; 2010: 853916.
|
64 |
VE Velculescu, L Zhang, B Vogelstein, KW Kinzler. Serial analysis of gene expression. Science 1995; 270(5235): 484–487
https://doi.org/10.1126/science.270.5235.484
pmid: 7570003
|
65 |
SH Nagaraj, RB Gasser, S Ranganathan. A hitchhiker’s guide to expressed sequence tag (EST) analysis. Brief Bioinform 2007; 8(1): 6–21
https://doi.org/10.1093/bib/bbl015
pmid: 16772268
|
66 |
ER Mardis. The impact of next-generation sequencing technology on genetics. Trends Genet 2008; 24(3): 133–141
https://doi.org/10.1016/j.tig.2007.12.007
pmid: 18262675
|
67 |
S Uchida, P Gellert, T Braun. Deeply dissecting stemness: making sense to non-coding RNAs in stem cells. Stem Cell Rev 2012; 8(1): 78–86
https://doi.org/10.1007/s12015-011-9294-y
pmid: 21706141
|
68 |
YW Asmann, MB Wallace, EA Thompson. Transcriptome profiling using next-generation sequencing. Gastroenterology 2008; 135(5): 1466–1468
https://doi.org/10.1053/j.gastro.2008.09.042
pmid: 18848555
|
69 |
B Langmead, C Trapnell, M Pop, SL Salzberg. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10(3): R25
https://doi.org/10.1186/gb-2009-10-3-r25
pmid: 19261174
|
70 |
G Jean, A Kahles, VT Sreedharan, F De Bona, G Ratsch. RNA-Seq read alignments with PALMapper. Curr Protoc Bioinformatics 2010; Chapter 11: Unit 11 6
|
71 |
H Jiang, WH Wong. SeqMap: mapping massive amount of oligonucleotides to the genome. Bioinformatics 2008; 24(20): 2395–2396
https://doi.org/10.1093/bioinformatics/btn429
pmid: 18697769
|
72 |
K Wang, D Singh, Z Zeng, SJ Coleman, Y Huang, GL Savich, X He, P Mieczkowski, SA Grimm, CM Perou, JN MacLeod, DY Chiang, JF Prins, J Liu. MapSplice: accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Res 2010; 38(18): e178
https://doi.org/10.1093/nar/gkq622
pmid: 20802226
|
73 |
H Li, R Durbin. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25(14): 1754–1760
https://doi.org/10.1093/bioinformatics/btp324
pmid: 19451168
|
74 |
M Guttman, M Garber, JZ Levin, J Donaghey, J Robinson, X Adiconis, L Fan, MJ Koziol, A Gnirke, C Nusbaum, JL Rinn, ES Lander, A Regev. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010; 28(5): 503–510
https://doi.org/10.1038/nbt.1633
pmid: 20436462
|
75 |
KF Au, H Jiang, L Lin, Y Xing, WH Wong. Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic Acids Res 2010; 38(14): 4570–4578
https://doi.org/10.1093/nar/gkq211
pmid: 20371516
|
76 |
A Roberts, C Trapnell, J Donaghey, JL Rinn, L Pachter. Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol 2011; 12(3): R22
https://doi.org/10.1186/gb-2011-12-3-r22
pmid: 21410973
|
77 |
MR Friedländer, W Chen, C Adamidi, J Maaskola, R Einspanier, S Knespel, N Rajewsky. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 2008; 26(4): 407–415
https://doi.org/10.1038/nbt1394
pmid: 18392026
|
78 |
R Ronen, I Gan, S Modai, A Sukacheov, G Dror, E Halperin, N Shomron. miRNAkey: a software for microRNA deep sequencing analysis. Bioinformatics 2010; 26(20): 2615–2616
https://doi.org/10.1093/bioinformatics/btq493
pmid: 20801911
|
79 |
M Hackenberg, N Rodríguez-Ezpeleta, AM Aransay. miRanalyzer: an update on the detection and analysis of microRNAs in high-throughput sequencing experiments. Nucleic Acids Res 2011; 39(Web Server issue): W132–138
pmid: 21515631
|
80 |
PJ Huang, YC Liu, CC Lee, WC Lin, RRC Gan, PC Lyu, P Tang. DSAP: deep-sequencing small RNA analysis pipeline. Nucleic Acids Res 2010; 38(Web Server issue): W385–391
pmid: 20478825
|
81 |
BP Lewis, CB Burge, DP Bartel. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120(1): 15–20
https://doi.org/10.1016/j.cell.2004.12.035
pmid: 15652477
|
82 |
A Krek, D Grün, MN Poy, R Wolf, L Rosenberg, EJ Epstein, P MacMenamin, I da Piedade, KC Gunsalus, M Stoffel, N Rajewsky. Combinatorial microRNA target predictions. Nat Genet 2005; 37(5): 495–500
https://doi.org/10.1038/ng1536
pmid: 15806104
|
83 |
D Betel, M Wilson, A Gabow, DS Marks, C Sander. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008; 36(Database issue): D149–D153
pmid: 18158296
|
84 |
M Maragkakis, M Reczko, VA Simossis, P Alexiou, GL Papadopoulos, T Dalamagas, G Giannopoulos, G Goumas, E Koukis, K Kourtis, T Vergoulis, N Koziris, T Sellis, P Tsanakas, AG Hatzigeorgiou. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucleic Acids Res 2009; 37(Web Server issue): W273-276
pmid: 19406924
|
85 |
T Rabilloud, M Chevallet, S Luche, C Lelong. Two-dimensional gel electrophoresis in proteomics: Past, present and future. J Proteomics 2010; 73(11): 2064–2077
https://doi.org/10.1016/j.jprot.2010.05.016
pmid: 20685252
|
86 |
R Aebersold, M Mann. Mass spectrometry-based proteomics. Nature 2003; 422(6928): 198–207
https://doi.org/10.1038/nature01511
pmid: 12634793
|
87 |
B Domon, R Aebersold. Mass spectrometry and protein analysis. Science 2006; 312(5771): 212–217
https://doi.org/10.1126/science.1124619
pmid: 16614208
|
88 |
O Stoevesandt, MJ Taussig, M He. Protein microarrays: high-throughput tools for proteomics. Expert Rev Proteomics 2009; 6(2): 145–157
https://doi.org/10.1586/epr.09.2
pmid: 19385942
|
89 |
A Novak, M Amit, T Ziv, H Segev, B Fishman, A Admon, J Itskovitz-Eldor. Proteomics profiling of human embryonic stem cells in the early differentiation stage. Stem Cell Rev 2012; 8(1): 137–149
https://doi.org/10.1007/s12015-011-9286-y
pmid: 21732092
|
90 |
JW Gouw, J Krijgsveld. MSQuant: a platform for stable isotope-based quantitative proteomics. Methods Mol Biol 2012; 893: 511–522
https://doi.org/10.1007/978-1-61779-885-6_31
pmid: 22665320
|
91 |
PG Pedrioli, JK Eng, R Hubley, M Vogelzang, EW Deutsch, B Raught, B Pratt, E Nilsson, RH Angeletti, R Apweiler, K Cheung, CE Costello, H Hermjakob, S Huang, RK Julian, E Kapp, ME McComb, SG Oliver, G Omenn, NW Paton, R Simpson, R Smith, CF Taylor, W Zhu, R Aebersold. A common open representation of mass spectrometry data and its application to proteomics research. Nat Biotechnol 2004; 22(11): 1459–1466
https://doi.org/10.1038/nbt1031
pmid: 15529173
|
92 |
LN Mueller, MY Brusniak, DR Mani, R Aebersold. An assessment of software solutions for the analysis of mass spectrometry based quantitative proteomics data. J Proteome Res 2008; 7(1): 51–61
https://doi.org/10.1021/pr700758r
pmid: 18173218
|
93 |
J Cox, M Mann. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008; 26(12): 1367–1372
https://doi.org/10.1038/nbt.1511
pmid: 19029910
|
94 |
Z Khan, JS Bloom, BA Garcia, M Singh, L Kruglyak. Protein quantification across hundreds of experimental conditions. Proc Natl Acad Sci USA 2009; 106(37): 15544–15548
https://doi.org/10.1073/pnas.0904100106
pmid: 19717460
|
95 |
WT Lin, WN Hung, YH Yian, KP Wu, CL Han, YR Chen, YJ Chen, TY Sung, WL Hsu. Multi-Q: a fully automated tool for multiplexed protein quantitation. J Proteome Res 2006; 5(9): 2328–2338
https://doi.org/10.1021/pr060132c
pmid: 16944945
|
96 |
IP Shadforth, TPJ Dunkley, KS Lilley, C Bessant. i-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics 2005; 6(1): 145
https://doi.org/10.1186/1471-2164-6-145
pmid: 16242023
|
97 |
MO Arntzen, CJ Koehler, H Barsnes, FS Berven, A Treumann, B Thiede. IsobariQ: software for isobaric quantitative proteomics using IPTL, iTRAQ, and TMT. J Proteome Res 2011; 10(2): 913–920
https://doi.org/10.1021/pr1009977
pmid: 21067241
|
98 |
A Keller, J Eng, N Zhang, XJ Li, R Aebersold. A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol Syst Biol 2005; 1: 2005.0017
pmid: 16729052
|
99 |
MY Brusniak, B Bodenmiller, D Campbell, K Cooke, J Eddes, A Garbutt, H Lau, S Letarte, LN Mueller, V Sharma, O Vitek, N Zhang, R Aebersold, JD Watts. Corra: Computational framework and tools for LC-MS discovery and targeted mass spectrometry-based proteomics. BMC Bioinformatics 2008; 9(1): 542
https://doi.org/10.1186/1471-2105-9-542
pmid: 19087345
|
100 |
CC Tsou, CF Tsai, YH Tsui, PR Sudhir, YT Wang, YJ Chen, JY Chen, TY Sung, WL Hsu. IDEAL-Q, an automated tool for label-free quantitation analysis using an efficient peptide alignment approach and spectral data validation. Mol Cell Proteomics 2010; 9(1): 131–144
https://doi.org/10.1074/mcp.M900177-MCP200
pmid: 19752006
|
101 |
P Mortensen, JW Gouw, JV Olsen, SE Ong, KTG Rigbolt, J Bunkenborg, J Cox, LJ Foster, AJR Heck, B Blagoev, JS Andersen, M Mann. MSQuant, an open source platform for mass spectrometry-based quantitative proteomics. J Proteome Res 2010; 9(1): 393–403
https://doi.org/10.1021/pr900721e
pmid: 19888749
|
102 |
CH Hokke, JM Fitzpatrick, KF Hoffmann. Integrating transcriptome, proteome and glycome analyses of Schistosoma biology. Trends Parasitol 2007; 23(4): 165–174
https://doi.org/10.1016/j.pt.2007.02.007
pmid: 17336161
|
103 |
JA Nielsen, P Lau, D Maric, JL Barker, LD Hudson. Integrating microRNA and mRNA expression profiles of neuronal progenitors to identify regulatory networks underlying the onset of cortical neurogenesis. BMC Neurosci 2009; 10(1): 98
https://doi.org/10.1186/1471-2202-10-98
pmid: 19689821
|
104 |
F Liu, J Lu, W Hu, SY Wang, SJ Cui, M Chi, Q Yan, XR Wang, HD Song, XN Xu, JJ Wang, XL Zhang, X Zhang, ZQ Wang, CL Xue, PJ Brindley, DP McManus, PY Yang, Z Feng, Z Chen, ZG Han. New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2006; 2(4): e29
https://doi.org/10.1371/journal.ppat.0020029
pmid: 16617374
|
105 |
AS Tarun, X Peng, RF Dumpit, Y Ogata, H Silva-Rivera, N Camargo, TM Daly, LW Bergman, SHI Kappe. A combined transcriptome and proteome survey of malaria parasite liver stages. Proc Natl Acad Sci USA 2008; 105(1): 305–310
https://doi.org/10.1073/pnas.0710780104
pmid: 18172196
|
106 |
RD Unwin, AD Whetton. Systematic proteome and transcriptome analysis of stem cell populations. Cell Cycle 2006; 5(15): 1587–1591
https://doi.org/10.4161/cc.5.15.3101
pmid: 16861929
|
107 |
H Xu, IR Lemischka, A Ma’ayan. SVM classifier to predict genes important for self-renewal and pluripotency of mouse embryonic stem cells. BMC Syst Biol 2010; 4(1): 173
https://doi.org/10.1186/1752-0509-4-173
pmid: 21176149
|
108 |
SJ Ho Sui, K Begley, D Reilly, B Chapman, R McGovern, P Rocca-Sera, E Maguire, GM Altschuler, TA Hansen, R Sompallae, A Krivtsov, RA Shivdasani, SA Armstrong, AC Culhane, M Correll, SA Sansone, O Hofmann, W Hide. The Stem Cell Discovery Engine: an integrated repository and analysis system for cancer stem cell comparisons. Nucleic Acids Res 2012; 40(Database issue): D984–D991
https://doi.org/10.1093/nar/gkr1051
pmid: 22121217
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|