Statistical Design and Analysis of RNA Sequencing Data
Open accessAbstract
Next-generation sequencing technologies are quickly becoming the preferred approach for characterizing and quantifying entire genomes. Even though data produced from these technologies are proving to be the most informative of any thus far, very little attention has been paid to fundamental design aspects of data collection and analysis, namely sampling, randomization, replication, and blocking. We discuss these concepts in an RNA sequencing framework. Using simulations we demonstrate the benefits of collecting replicated RNA sequencing data according to well known statistical designs that partition the sources of biological and technical variation. Examples of these designs and their corresponding models are presented with the goal of testing differential expression.
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Batch effects can be minimized by appropriate experimental design or removed by batch-correction methods such as COMBAT or ARSyN.
“These effects can be minimized by appropriate experimental design [51] or, alternatively, removed by batch-correction methods such as COMBAT [52] or ARSyN [20, 53].”
From A survey of best practices for RNA-seq data analysis (2016) · cites this paper as [51]
Without careful experimental design, it is difficult to separate gene expression variability caused by technical artifacts from biological signal.
“In the absence of careful experimental design, distinguishing gene expression variability due to technical artifacts and biological signal is challenging (Auer and Doerge, 2010).”
From Guidance for RNA-seq co-expression network construction and analysis: safety in numbers (2015) · cites this paper as Auer and Doerge, 2010
Cites
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
Mapping and quantifying mammalian transcriptomes by RNA-Seq
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., & Wold, B. (2008) · Nature Methods · doi:10.1038/nmeth.1226 · Cited by 13,696 · see citing works
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) · Genome Biology · doi:10.1186/gb-2004-5-10-r80 · Cited by 13,133 · see citing works
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829 · see citing works
Quantitative Monitoring of Gene Expression Patterns with a Complementary DNA Microarray
Schena, M., Shalon, D., Davis, R. W., & Brown, P. O. (1995) · Science · doi:10.1126/science.270.5235.467 · Cited by 9,609 · see citing works
Hapeman, D. E., & Agresti, A. (1991) · Technometrics · doi:10.1080/00401706.1991.10484817 · Cited by 9,406 · see citing works
Fisher, R. A. (1936) · BMJ · doi:10.1136/bmj.1.3923.554-a · Cited by 4,980 · see citing works
Serial Analysis of Gene Expression
Velculescu, V. E., Zhang, L., Vogelstein, B., & Kinzler, K. W. (1995) · Science · doi:10.1126/science.270.5235.484 · Cited by 3,713 · see citing works
Accurate whole human genome sequencing using reversible terminator chemistry
Bentley, D. R., Balasubramanian, S., Swerdlow, H. P., Smith, G. P., Milton, J., Brown, C. G., Hall, K. P., Evers, D. J., Barnes, C. L., Bignell, H. R., et al. (2008) · Nature · doi:10.1038/nature07517 · Cited by 3,684 · see citing works
The Significance of Digital Gene Expression ProfilesPreprint
Audic, S., & Claverie, J. (1997) · Genome Research · doi:10.1101/gr.7.10.986 · Cited by 2,793 · see citing works
RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays
Marioni, J. C., Mason, C. E., Mane, S. M., Stephens, M., & Gilad, Y. (2008) · Genome Research · doi:10.1101/gr.079558.108 · Cited by 2,771 · see citing works
The Transcriptional Landscape of the Yeast Genome Defined by RNA Sequencing
Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M., & Snyder, M. (2008) · Science · doi:10.1126/science.1158441 · Cited by 2,479 · see citing works
ChIP–seq: advantages and challenges of a maturing technology
Park, P. J. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2641 · Cited by 2,217 · see citing works
Analysis of Variance for Gene Expression Microarray Data
Kerr, K. F., Martin, M., & Churchill, G. A. (2000) · Journal of Computational Biology · doi:10.1089/10665270050514954 · Cited by 1,310 · see citing works
Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex
Hamady, M., Walker, J. J., Harris, J. K., Gold, N. J., & Knight, R. (2008) · Nature Methods · doi:10.1038/nmeth.1184 · Cited by 1,310 · see citing works
Sultan, M., Schulz, M. H., Richard, H., Magen, A., Klingenhoff, A., Scherf, M., Seifert, M., Borodina, T., Soldatov, A., Parkhomchuk, D., et al. (2008) · Science · doi:10.1126/science.1160342 · Cited by 1,293 · see citing works
The Logic of Inductive Inference
Fisher, R. A. (1935) · Journal Of The Royal Statistical Society · doi:10.2307/2342435 · Cited by 1,292 · see citing works
Small-sample estimation of negative binomial dispersion, with applications to SAGE data
Robinson, M. D., & Smyth, G. K. (2007) · Biostatistics · doi:10.1093/biostatistics/kxm030 · Cited by 1,073 · see citing works
Fundamentals of experimental design for cDNA microarrays
Churchill, G. A. (2002) · Nature Genetics · doi:10.1038/ng1031 · Cited by 1,049 · see citing works
Stem cell transcriptome profiling via massive-scale mRNA sequencing
Cloonan, N., Forrest, A. R. R., Kolle, G., Gardiner, B. B. A., Faulkner, G. J., Brown, M. K., Taylor, D. F., Steptoe, A. L., Wani, S., Bethel, G., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1223 · Cited by 1,035 · cited 1× · see citing works
“At present, there are three widely accepted commercially available NGS devices [Illumina’s Genome Analyzer, Applied Biosystems’ (Foster City, CA) SOLiD, and the 454 Genome Sequencer FLX] for RNA-Seq (C loonan et al .”
Method124: The Logic of Inductive Inference.
Fisher, R. A. (1935) · Adelaide Research & Scholarship (AR&S) (University of Adelaide) · Cited by 872 · see citing works
Lee, M. T., Kuo, F. C., Whitmore, G. A., & Sklar, J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.18.9834 · Cited by 861 · see citing works
Moderated statistical tests for assessing differences in tag abundance
Robinson, M. D., & Smyth, G. K. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm453 · Cited by 856 · see citing works
Extending the Linear Model with R
Faraway, J. J. (2016) · Chapman & Hall/CRC eBooks · doi:10.1201/9781315382722 · Cited by 832 · see citing works
Personalized copy number and segmental duplication maps using next-generation sequencing
Alkan, C., Kidd, J. M., Marques-Bonet, T., Aksay, G., Antonacci, F., Hormozdiari, F., Kitzman, J. O., Baker, C., Malig, M., Mutlu, O., et al. (2009) · Nature Genetics · doi:10.1038/ng.437 · Cited by 748 · see citing works
Experimental design for gene expression microarrays
Kerr, K. F. (2001) · Biostatistics · doi:10.1093/biostatistics/2.2.183 · Cited by 709 · see citing works
Applications of New Sequencing Technologies for Transcriptome Analysis
Morozova, O., Hirst, M., & Marra, M. A. (2009) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082908-145957 · Cited by 568 · see citing works
Statistical design and the analysis of gene expression microarray data
Kerr, K. F., & Churchill, G. A. (2007) · Genetics Research · doi:10.1017/s0016672308009713 · Cited by 561 · see citing works
Statistical design and the analysis of gene expression microarray data
Kerr, K. F., & Churchill, G. A. (2001) · Genetics Research · doi:10.1017/s0016672301005055 · Cited by 501 · see citing works
A first course in design and analysis of experiments
Oehlert, G. W. (2000) · University of Minnesota Digital Conservancy (University of Minnesota) · Cited by 387 · see citing works
Gasparini, M., & Rogantin, M. P. (2008) · PORTO Publications Open Repository TOrino (Politecnico di Torino) · Cited by 383 · see citing works
Kal, A. J., van Zonneveld, A. J., Beneš, V., van den Berg, M., Koerkamp, M. J. A. G., Albermann, K., Strack, N., Ruijter, J. M., Richter, A., Dujon, B., et al. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.6.1859 · Cited by 346 · see citing works
The beginning of the end for microarrays?
Shendure, J. (2008) · Nature Methods · doi:10.1038/nmeth0708-585 · Cited by 331 · see citing works
Identification of genetic variants using bar-coded multiplexed sequencing
Craig, D. W., Pearson, J. V., Szelinger, S., Sekar, A., Redman, M., Corneveaux, J. J., Pawlowski, T. L., Laub, T., Nunn, G. B., Stephan, D. A., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1251 · Cited by 301 · see citing works
Detection of single nucleotide variations in expressed exons of the human genome using RNA-Seq
Chepelev, I., Wei, G., Tang, Q., & Zhao, K. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp507 · Cited by 182 · see citing works
Bloom, J. S., Khan, Z., Kruglyak, L., Singh, M., & Caudy, A. A. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-221 · Cited by 178 · see citing works
POWER_SAGE: comparing statistical tests for SAGE experiments
Man, M. Z., Wang, X., & Wang, Y. (2000) · Bioinformatics · doi:10.1093/bioinformatics/16.11.953 · Cited by 168 · see citing works
Balwierz, P. J., Carninci, P., Daub, C. O., Kawai, J., Hayashizaki, Y., Belle, W. V., Beisel, C., & van Nimwegen, E. (2009) · Genome biology · doi:10.1186/gb-2009-10-7-r79 · Cited by 125 · see citing works
Statistical evaluation of SAGE libraries: consequences for experimental design
Ruijter, J. M., van Kampen, A. H. C., & Baas, F. F. (2002) · Physiological Genomics · doi:10.1152/physiolgenomics.00042.2002 · Cited by 114 · see citing works
Transcript Profiling by 3′-Untranslated Region Sequencing Resolves Expression of Gene Families
Eveland, A. L., McCarty, D. R., & Koch, K. E. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.108597 · Cited by 108 · see citing works
Probabilistic base calling of Solexa sequencing data
Rougemont, J., Amzallag, A., Iseli, C., Farinelli, L., Xénarios, I., & Naef, F. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-431 · Cited by 99 · see citing works
Lu, J., Tomfohr, J. K., & Kepler, T. B. (2005) · BMC Bioinformatics · doi:10.1186/1471-2105-6-165 · Cited by 79 · see citing works
Genome sequencing: the third generation
Hayden, E. C. (2009) · Nature · doi:10.1038/news.2009.86 · Cited by 69 · see citing works
Vêncio, R. Z. N., Brentani, H., Patrão, D. F. D. C., & Pereira, C. A. D. B. (2004) · BMC Bioinformatics · doi:10.1186/1471-2105-5-119 · Cited by 65 · see citing works
Romualdi, C. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.19.2133 · Cited by 62 · see citing works
Overdispersed logistic regression for SAGE: Modelling multiple groups and covariates
Baggerly, K., Deng, L., Morris, J. S., & Aldaz, C. M. (2004) · BMC Bioinformatics · doi:10.1186/1471-2105-5-144 · Cited by 58 · see citing works
Basic properties and information theory of Audic-Claverie statistic for analyzing cDNA arrays
Peter Tiňo, B. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-310 · Cited by 49 · see citing works
RNA-MATE: a recursive mapping strategy for high-throughput RNA-sequencing data
Cloonan, N., Xu, Q., Faulkner, G. J., Taylor, D. F., Tang, D. T. P., Kolle, G., & Grimmond, S. M. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp459 · Cited by 46 · see citing works
Nonlinear Regression, Quasi Likelihood, and Overdispersion in Generalized Linear Models
Tjur, T. (1998) · The American Statistician · doi:10.1080/00031305.1998.10480567 · Cited by 41 · see citing works
Modeling Sage data with a truncated gamma-Poisson model
Thygesen, H. H., & Zwinderman, A. H. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-157 · Cited by 34 · see citing works
Philippe, N., Boureux, A., Bréhélin, L., Tarhio, J., Commes, T., & Rivals, É. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp492 · Cited by 30 · see citing works
Britain hits a hurdle in replacing key animal-pathogen facility
Gilbert, N. (2009) · Nature · doi:10.1038/457769a · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 53 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., Couger, M. B., Eccles, D., Li, B., Lieber, M., et al. (2013) · Nature Protocols · doi:10.1038/nprot.2013.084 · Cited by 8,464 · see citing works
McCarthy, D. J., Chen, Y., & Smyth, G. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks042 · Cited by 5,195 · see citing works
A survey of best practices for RNA-seq data analysis
Conesa, A., Madrigal, P., Tarazona, S., Gomez-Cabrero, D., Cervera, A., McPherson, A., Szcześniak, M. W., Gaffney, D. J., Elo, L. L., Zhang, X., et al. (2016) · Genome Biology · doi:10.1186/s13059-016-0881-8 · Cited by 2,794 · see citing works
Shen, S., Park, J. W., Lu, Z.-X., Lin, L., Henry, M. D., Wu, Y. N., Zhou, Q., & Xing, Y. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419161111 · Cited by 2,713 · see citing works
Normalization and microbial differential abundance strategies depend upon data characteristics
Weiss, S. J., Xu, Z. Z., Peddada, S. D., Amir, A., Bittinger, K. L., González, A., Lozupone, C., Zaneveld, J., Vázquez‐Baeza, Y., Birmingham, A., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0237-y · Cited by 2,121 · see citing works
Fernandes, A. D., Reid, J. N., Macklaim, J. M., McMurrough, T. A., Edgell, D. R., & Gloor, G. B. (2014) · Microbiome · doi:10.1186/2049-2618-2-15 · Cited by 1,329 · see citing works
Count-based differential expression analysis of RNA sequencing data using R and Bioconductor
Anders, S., McCarthy, D. J., Chen, Y., Okoniewski, M. J., Smyth, G. K., Huber, W. K., & Robinson, M. D. (2013) · Nature Protocols · doi:10.1038/nprot.2013.099 · Cited by 1,129 · see citing works
Schurch, N. J., Schofield, P., Gierliński, M., Cole, C., Sherstnev, A., Singh, V., Wrobel, N., Gharbi, K., Simpson, G. G., Owen-Hughes, T., et al. (2016) · RNA · doi:10.1261/rna.053959.115 · Cited by 966 · see citing works
Kukurba, K. R., & Montgomery, S. B. (2015) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top084970 · Cited by 924 · see citing works
Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package
Tarazona, S., Furió‐Tarí, P., Turrà, D., Pietro, A. D., Nueda, M. J., Ferrer, A., & Conesa, A. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv711 · Cited by 757 · see citing works
From RNA-seq reads to differential expression results
Oshlack, A., Robinson, M. D., & Young, M. D. (2010) · Genome biology · doi:10.1186/gb-2010-11-12-220 · Cited by 697 · see citing works
Microarrays, deep sequencing and the true measure of the transcriptome
Malone, J. H., & Oliver, B. (2011) · BMC Biology · doi:10.1186/1741-7007-9-34 · Cited by 546 · see citing works
Transcriptome-wide measurement of translation by ribosome profiling
McGlincy, N. J., & Ingolia, N. T. (2017) · Methods · doi:10.1016/j.ymeth.2017.05.028 · Cited by 547 · see citing works
RNA-seq differential expression studies: more sequence or more replication?
Liu, Y., Zhou, J., & White, K. P. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt688 · Cited by 497 · see citing works
Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders
Parikshak, N. N., Gandal, M. J., & Geschwind, D. H. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3934 · Cited by 430 · see citing works
Design and computational analysis of single-cell RNA-sequencing experiments
Bacher, R. L., & Kendziorski, C. M. (2016) · Genome biology · doi:10.1186/s13059-016-0927-y · Cited by 437 · see citing works
Characterizing Mutational Signatures in Human Cancer Cell Lines Reveals Episodic APOBEC Mutagenesis
Petljak, M., Alexandrov, L. B., Brammeld, J. S., Price, S., Wedge, D. C., Großmann, S., Dawson, K. J., Ju, Y. S., Iorio, F., Tubío, J. M. C., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.012 · Cited by 404 · see citing works
Yu, X., Taylor, A. M. W., Nagai, J., Golshani, P., Evans, C. J., Coppola, G., & Khakh, B. S. (2018) · Neuron · doi:10.1016/j.neuron.2018.08.015 · Cited by 399 · see citing works
Transcriptomics in the RNA-seq era
McGettigan, P. (2013) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2012.12.008 · Cited by 360 · see citing works
DrImpute: imputing dropout events in single cell RNA sequencing data
Gong, W., Kwak, I., Pota, P., Koyano‐Nakagawa, N., & Garry, D. J. (2018) · BMC Bioinformatics · doi:10.1186/s12859-018-2226-y · Cited by 319 · see citing works
The fate of duplicated genes in a polyploid plant genome
Roulin, A. C., Auer, P. L., Libault, M., Schlueter, J. A., Farmer, A. D., May, G. D., Stacey, G. S., Doerge, R. W., & Jackson, S. A. (2012) · The Plant Journal · doi:10.1111/tpj.12026 · Cited by 303 · see citing works
Self-citationRNA-seq: technical variability and sampling
McIntyre, L. M., Lopiano, K. K., Morse, A. M., Amin, V., Oberg, A. L., Young, L. J., & Nuzhdin, S. V. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-293 · Cited by 285 · see citing works
Guidance for RNA-seq co-expression network construction and analysis: safety in numbers
Ballouz, S., Verleyen, W., & Gillis, J. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv118 · Cited by 215 · see citing works
Injured adult neurons regress to an embryonic transcriptional growth state
Poplawski, G. H. D., Kawaguchi, R., Van Niekerk, E., Lu, P., Mehta, N., Canete, P., Lie, R., Dragatsis, I., Meves, J. M., Zheng, B., et al. (2020) · Nature · doi:10.1038/s41586-020-2200-5 · Cited by 247 · see citing works
Design and validation issues in RNA-seq experiments
Fang, Z., & Cui, X. (2011) · Briefings in Bioinformatics · doi:10.1093/bib/bbr004 · Cited by 229 · see citing works
The power and promise of RNA ‐seq in ecology and evolution
Todd, E. V., Black, M. A., & Gemmell, N. J. (2016) · Molecular Ecology · doi:10.1111/mec.13526 · Cited by 233 · see citing works
Designing a transcriptome next‐generation sequencing project for a nonmodel plant species1
Strickler, S. R., Bombarely, A., & Mueller, L. A. (2012) · American Journal of Botany · doi:10.3732/ajb.1100292 · Cited by 222 · see citing works
Principles of transcriptome analysis and gene expression quantification: an RNA ‐seq tutorial
Wolf, J. B. W. (2013) · Molecular Ecology Resources · doi:10.1111/1755-0998.12109 · Cited by 219 · see citing works
Targeted enrichment strategies for next‐generation plant biology
Cronn, R., Knaus, B. J., Liston, A., Maughan, P. J., Parks, M., Syring, J. V., & Udall, J. A. (2012) · American Journal of Botany · doi:10.3732/ajb.1100356 · Cited by 218 · see citing works
Berens, A. J., Hunt, J. H., & Toth, A. L. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu330 · Cited by 198 · see citing works
Classification and clustering of sequencing data using a Poisson model
Witten, D. (2011) · The Annals of Applied Statistics · doi:10.1214/11-aoas493 · Cited by 186 · see citing works
ISEV position paper: extracellular vesicle RNA analysis and bioinformatics
Hill, A. F., Pegtel, D. M., Lambertz, U., Leonardi, T., O’Driscoll, L., Pluchino, S., Ter‐Ovanesyan, D., & Hoen, E. N. M. N. (2013) · Journal of Extracellular Vesicles · doi:10.3402/jev.v2i0.22859 · Cited by 171 · see citing works
Forero, A., Li, Y., Chen, D., Grizzle, W. E., Updike, K. L., Merz, N. D., Downs-Kelly, E. P., Burwell, T. C., Vaklavas, C., Buchsbaum, D. J., et al. (2016) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-15-0243 · Cited by 170 · see citing works
Wang, Y., Yang, M., Wei, S., Qin, F., Zhao, H., & Suo, B. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2016.02024 · Cited by 167 · see citing works
RNAi screens in mice identify physiological regulators of oncogenic growth
Beronja, S., Janki, P., Heller, E., Lien, W., Keyes, B. E., Oshimori, N., & Fuchs, E. V. (2013) · Nature · doi:10.1038/nature12464 · Cited by 162 · see citing works
ReCount: A multi-experiment resource of analysis-ready RNA-seq gene count datasets
Frazee, A. C., Langmead, B., & Leek, J. T. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-449 · Cited by 155 · see citing works
powsimR: power analysis for bulk and single cell RNA-seq experiments
Vieth, B., Ziegenhain, C., Parekh, S., Enard, W., & Hellmann, I. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx435 · Cited by 155 · see citing works
Whole-transcriptome RNAseq analysis from minute amount of total RNA
Tariq, M., Kim, H. J., Jejelowo, O. A., & Pourmand, N. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr547 · Cited by 146 · see citing works
Yates, S. A., Swain, M., Hegarty, M., Chernukin, I., Lowe, M., Allison, G. G., Ruttink, T., Abberton, M. T., Jenkins, G., & Skøt, L. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-453 · Cited by 144 · see citing works
Barrero‐Gil, J., Huertas, R., Rambla, J. L., Granell, A., & Salinas, J. (2016) · Plant Cell & Environment · doi:10.1111/pce.12799 · Cited by 140 · see citing works
Experimental design for single-cell RNA sequencing
Baran‐Gale, J., Chandra, T., & Kirschner, K. (2017) · Briefings in Functional Genomics · doi:10.1093/bfgp/elx035 · Cited by 128 · see citing works
Wong, R. Y., Oxendine, S. E., & Godwin, J. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-348 · Cited by 128 · see citing works
Astrocyte–neuron subproteomes and obsessive–compulsive disorder mechanisms
Soto, J. S., Jami‐Alahmadi, Y., Chacon, J., Moye, S. L., Castro, B. D., Wohlschlegel, J. A., & Khakh, B. S. (2023) · Nature · doi:10.1038/s41586-023-05927-7 · Cited by 132 · see citing works
Models for transcript quantification from RNA-SeqPreprint
Pachter, L. S. (2011) · arXiv (Cornell University) · doi:10.48550/arxiv.1104.3889 · Cited by 155 · see citing works
Context-Specific Striatal Astrocyte Molecular Responses Are Phenotypically Exploitable
Yu, X., Nagai, J., Martí-Solano, M., Soto, J. S., Coppola, G., Babu, M. M., & Khakh, B. S. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.021 · Cited by 121 · see citing works
Extracellular vesicles and their nucleic acids for biomarker discovery
Momen‐Heravi, F., Getting, S. J., & Moschos, S. A. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.08.002 · Cited by 121 · see citing works
Assefa, A. T., Vandesompele, J., & Thas, O. (2020) · BMC Genomics · doi:10.1186/s12864-020-6721-y · Cited by 120 · see citing works
DeBiasse, M. B., & Kelly, M. W. (2015) · Journal of Heredity · doi:10.1093/jhered/esv073 · Cited by 122 · see citing works
The evolution of gene expression and the transcriptome–phenotype relationship
Harrison, P. W., Wright, A. E., & Mank, J. E. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.12.004 · Cited by 121 · see citing works
quantro: a data-driven approach to guide the choice of an appropriate normalization method
Hicks, S. C., & Irizarry, R. A. (2015) · Genome biology · doi:10.1186/s13059-015-0679-0 · Cited by 112 · see citing works
Wang, Y., Brahmakshatriya, V., Lupiani, B., Reddy, S. M., Soibam, B., Benham, A. L., Gunaratne, P. H., Liu, H., Trakooljul, N., Ing, N. H., et al. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-278 · Cited by 111 · see citing works
Systems biology approaches to new vaccine development
Oberg, A. L., Kennedy, R. B., Li, P., Ovsyannikova, I. G., & Poland, G. A. (2011) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.04.005 · Cited by 111 · see citing works
Gunter, H. M., Fan, S., Xiong, F., Franchini, P., Fruciano, C., & Meyer, A. (2013) · Molecular Ecology · doi:10.1111/mec.12417 · Cited by 109 · see citing works
Lamarre, S., Frasse, P., Zouine, M., Labourdette, D., Sainderichin, E., Hu, G., Berre, V. L., Bouzayen, M., & Maza, É. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00108 · Cited by 107 · see citing works
Buschmann, D., Haberberger, A., Kirchner, B., Spornraft, M., Riedmaier, I., Schelling, G., & Pfaffl, M. W. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw545 · Cited by 102 · see citing works
Genomic toolboxes for conservation biologists
Angeloni, F., Wagemaker, C. A. M., Vergeer, P., & Ouborg, J. (2011) · Evolutionary Applications · doi:10.1111/j.1752-4571.2011.00217.x · Cited by 103 · see citing works
Current RNA-seq methodology reporting limits reproducibility
Simoneau, J., Dumontier, S., Gosselin, R., & Scott, M. S. (2019) · Briefings in Bioinformatics · doi:10.1093/bib/bbz124 · Cited by 98 · see citing works
A Survey for Novel Imprinted Genes in the Mouse Placenta by mRNA-seq
Wang, X., Soloway, P. D., & Clark, A. G. (2011) · Genetics · doi:10.1534/genetics.111.130088 · Cited by 96 · see citing works
Dual RNA-Sequencing to Elucidate the Plant-Pathogen Duel
Naidoo, S., Visser, E. A., Zwart, L., du Toit, Y., Bhadauria, V., & Shuey, L. S. (2017) · Current Issues in Molecular Biology · doi:10.21775/cimb.027.127 · Cited by 95 · see citing works
RNA‐seq Data: Challenges in and Recommendations for Experimental Design and Analysis
Williams, A. G., Thomas, S., Wyman, S. K., & Holloway, A. K. (2014) · Current Protocols in Human Genetics · doi:10.1002/0471142905.hg1113s83 · Cited by 93 · see citing works
A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning
Battat, M., Eitan, A., Rogachev, I., Hanhineva, K., Fernie, A. R., Tohge, T., Beekwilder, J., & Aharoni, A. (2019) · PLANT PHYSIOLOGY · doi:10.1104/pp.19.00009 · Cited by 92 · see citing works
Goyer, A., Hamlin, L. L., Crosslin, J. M., Buchanan, A., & Chang, J. H. (2015) · BMC Genomics · doi:10.1186/s12864-015-1666-2 · Cited by 92 · see citing works
Transcriptional profiling of the Arabidopsis abscission mutant hae hsl2by RNA-Seq
Niederhuth, C. E., Patharkar, O. R., & Walker, J. C. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-37 · Cited by 91 · see citing works
Co-expression analysis of high-throughput transcriptome sequencing data with Poisson mixture models
Rau, A., Maugis-Rabusseau, C., Martin‐Magniette, M., & Celeux, G. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu845 · Cited by 90 · see citing works
Shin, H., Shannon, C. P., Fishbane, N., Ruan, J., Zhou, M., Balshaw, R. F., Wilson-McManus, J., Ng, R. T., McManus, B. M., & Tebbutt, S. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091041 · Cited by 89 · see citing works
Wang, N., Wang, R., Wang, R., & Chen, S. (2018) · Functional & Integrative Genomics · doi:10.1007/s10142-018-0595-y · Cited by 88 · see citing works
Effects of library size variance, sparsity, and compositionality on the analysis of microbiome dataPreprint
Weiss, S. J., Xu, Z. Z., Amir, A., Peddada, S., Bittinger, K. L., Gonzalez, A., Lozupone, C., Zaneveld, J., Vázquez‐Baeza, Y., Birmingham, A., et al. (2015) · doi:10.7287/peerj.preprints.1157v1 · Cited by 88 · see citing works
Arambula, S. E., Belcher, S. M., Planchart, A., Turner, S. D., & Patisaul, H. B. (2016) · Endocrinology · doi:10.1210/en.2016-1339 · Cited by 87 · see citing works
Statistical models for RNA-seq data derived from a two-condition 48-replicate experiment
Gierliński, M., Cole, C., Schofield, P., Schurch, N., Sherstnev, A., Singh, V., Wrobel, N., Gharbi, K., Simpson, G. G., Owen‐Hughes, T., et al. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv425 · Cited by 84 · see citing works
multiHiCcompare: joint normalization and comparative analysis of complex Hi-C experiments
Stansfield, J. C., Cresswell, K. G., & Dozmorov, M. G. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz048 · Cited by 81 · see citing works
Comparison of differential accessibility analysis strategies for ATAC-seq data
Gontarz, P. M., Fu, S., Xing, X., Liu, S., Miao, B., Bazylianska, V., SHARMA, A. K., Madden, P. A. F., Cates, K. L., Yoo, A. S. J., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-66998-4 · Cited by 80 · see citing works
Microbiome of Deep Dentinal Caries from Reversible Pulpitis to Irreversible Pulpitis
Zheng, J., Zhou, W., Niu, K., Xie, Y., Hu, X., Fu, J., Tian, D., Fu, K., Zhao, B., Kong, W., et al. (2019) · Journal of Endodontics · doi:10.1016/j.joen.2018.11.017 · Cited by 79 · see citing works
RNA-Sequencing: A tool to explore new frontiers in animal genetics
Wickramasinghe, S., Cánovas, Á., Rincón, G., & Medrano, J. F. F. (2014) · Livestock Science · doi:10.1016/j.livsci.2014.06.015 · Cited by 79 · see citing works
Phylogenetic Analysis of Gene Expression
Dunn, C. W., Luo, X., & Wu, Z. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict068 · Cited by 78 · see citing works
RNA-Seq analysis implicates dysregulation of the immune system in schizophrenia
Xu, J., Sun, J., Chen, J., Wang, L. H.-C., Li, A., Helm, M., Dubovsky, S. L., Bacanu, S., Zhao, Z., & Chen, X. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-s8-s2 · Cited by 77 · see citing works
Next-Generation Sequencing for MicroRNA Expression Profile
Hu, Y., Lan, W., & Miller, D. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7046-9_12 · Cited by 77 · see citing works
Aghababazadeh, F. A., Li, Q., & Fridley, B. L. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206312 · Cited by 76 · see citing works
Omics Approaches for the Assessment of Biological Responses to Nanoparticles.
Abdelkader, Y., Pérez-Dávalos, L., Leduc, R., Zahedi, R., & Labouta, H. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.114992 · Cited by 62 · see citing works
van Delft, J. H. M., Gaj, S., Lienhard, M., Albrecht, M. W., Кирпий, А. А., Brauers, K. J. J., Claessen, S. M. H., Lizárraga, D., Lehrach, H. R., Herwig, R., et al. (2012) · Toxicological Sciences · doi:10.1093/toxsci/kfs250 · Cited by 74 · see citing works
Choi, Y.-J., Aliota, M. T., Mayhew, G. F., Erickson, S. M., & Christensen, B. M. (2014) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002905 · Cited by 72 · see citing works
Dynamics of the chili pepper transcriptome during fruit development
Martínez-López, L. A., Ochoa‐Alejo, N., & Martínez, O. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-143 · Cited by 71 · see citing works
Hübner, S., Korol, A. B., & Schmid, K. J. (2015) · BMC Plant Biology · doi:10.1186/s12870-015-0528-z · Cited by 70 · see citing works
Multi-study inference of regulatory networks for more accurate models of gene regulation
Castro, D. M., Veaux, N. D., Miraldi, E. R., & Bonneau, R. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006591 · Cited by 69 · see citing works
Mycobacterial infection induces a specific human innate immune response
Blischak, J., Tailleux, L., Mitrano, A., Barreiro, L. B., & Gilad, Y. (2015) · Scientific Reports · doi:10.1038/srep16882 · Cited by 65 · see citing works
Rubio, M., Rodríguez‐Moreno, L., Ballester, A., de Moura, M. C., Bonghi, C., Candresse, T., & Martínez-Gómez, P. (2014) · Molecular Plant Pathology · doi:10.1111/mpp.12169 · Cited by 66 · see citing works
McLoughlin, K. E., Nalpas, N., Rue-Albrecht, K., Browne, J. A., Magee, D. A., Killick, K. E., Park, S. D. E., Hokamp, K., Meade, K. G., O’Farrelly, C., et al. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00396 · Cited by 67 · see citing works
Limited sex-biased neural gene expression patterns across strains in Zebrafish (Danio rerio)
Wong, R. Y., McLeod, M. M., & Godwin, J. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-905 · Cited by 68 · see citing works
Resnyk, C., Chen, C., Huang, H., Wu, C. H., Simon, J., Bihan-Duval, É. L., Duclos, M. J. M. J., & Cogburn, L. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0139549 · Cited by 65 · see citing works
LEVERAGING BIOLOGICAL REPLICATES TO IMPROVE ANALYSIS IN CHIP-SEQ EXPERIMENTS
Yang, Y., Fear, J. M., Hu, J., Häecker, I., Zhou, L. J., Renne, R., Bloom, D. C., & McIntyre, L. M. (2014) · Computational and Structural Biotechnology Journal · doi:10.5936/csbj.201401002 · Cited by 62 · see citing works
Willette, D. A., Allendorf, F. W., Barber, P. H., Barshis, D. J., Carpenter, K. E., Crandall, E. D., Cresko, W. A., Fernández-Silva, I., Matz, M. V., Meyer, E., et al. (2014) · Bulletin of Marine Science · doi:10.5343/bms.2013.1008 · Cited by 63 · see citing works
Shin, S., Zheng, P., Fazio, G., Mazzola, M., Main, D., & Zhu, Y. (2016) · Physiological and Molecular Plant Pathology · doi:10.1016/j.pmpp.2016.03.003 · Cited by 63 · see citing works
Radhakrishnan, S., Literman, R., Neuwald, J. L., Severin, A. J., & Valenzuela, N. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172044 · Cited by 63 · see citing works
Juknat, A., Gao, F., Coppola, G., Vogel, Z., & Kozela, E. (2019) · PLoS ONE · doi:10.1371/journal.pone.0212039 · Cited by 63 · see citing works
Mäder, U., Nicolas, P., Richard, H., Bessières, P., & Aymerich, S. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.10.003 · Cited by 61 · see citing works
Fumagalli, D., Blanchet-Cohen, A., Brown, D. N., Desmedt, C., Gacquer, D., Michiels, S., Rothé, F., Majjaj, S., Salgado, R., Larsimont, D., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1008 · Cited by 59 · see citing works
Transcriptomic Insight Into the Polygenic Mechanisms Underlying Psychiatric Disorders
Hernandez, L. M., Kim, M., Hoftman, G. D., Haney, J. R., de la Torre-Ubieta, L., Paşaniuc, B., & Gandal, M. J. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.06.005 · Cited by 57 · see citing works
Meta‐analysis and meta‐regression of transcriptomic responses to water stress in Arabidopsis
Rest, J. S., Wilkins, O., Wei, Y., Purugganan, M. D., & Gurevitch, J. (2016) · The Plant Journal · doi:10.1111/tpj.13124 · Cited by 59 · see citing works
Holtman, I. R., Noback, M. A., Bijlsma, M., Duong, K. N., van der Geest, M. A., Ketelaars, P. T., Brouwer, N., Vainchtein, I. D., Eggen, B. J. L., & Boddeke, H. W. G. M. (2015) · Glia · doi:10.1002/glia.22810 · Cited by 57 · see citing works
A comparison of analog and Next-Generation transcriptomic tools for mammalian studies
Roy, N. C., Altermann, E., Park, Z. A., & McNabb, W. C. (2011) · Briefings in Functional Genomics · doi:10.1093/bfgp/elr005 · Cited by 58 · see citing works
Transcriptome Analysis in Domesticated Species: Challenges and Strategies
Hekman, J. P., Johnson, J. L., & Kukekova, A. V. (2015) · Bioinformatics and Biology Insights · doi:10.4137/bbi.s29334 · Cited by 59 · see citing works
- Authors
- Auer, P. L., & Doerge, R. W.
- Affiliations
- Purdue University West Lafayette (US)
- Corresponding author
- Doerge, R W
- ORCID
- Auer, Paul L
- Venue
- Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-06-01
- Volume
- 185
- Issue
- 2
- Pages
- 405-416
- ISSN
- 0016-6731 (ISSN-L)
- 1943-2631
- PMC
- PMC2881125
- OpenAlex
- W1995070233
- Cited by
- 393
- References
- 53
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 12 · 2023: 11 · 2022: 14 · 2021: 17 · 2020: 24 · 2019: 18 · 2018: 43 · 2017: 25 · 2016: 32 · 2015: 49 · 2014: 42 · 2013: 39 · 2012: 28
- FWCI
- 12.26
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Genetics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene expression and cancer classification
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Social Sciences › Decision Sciences › Management Science and Operations Research › Optimal Experimental Design Methods
- Keywords
- RNA sequencing, statistical design, sampling, randomization, replication, blocking, differential gene expression, biological variation, technical variability, experimental design, gene expression quantification
- MeSH terms
- Base Sequence, Research Design, Clinical Laboratory Techniques
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