Integrative RNA-seq and microarray data analysis reveals GC content and gene length biases in the psoriasis transcriptome

Physiological Genomics

Volumn 46, Issue 15, 2014, Pages 533-546

  Swindell, William R ^a   Xing, Xianying ^a   Voorhees, John J ^a   Elder, James T ^a   Johnston, Andrew ^a   Gudjonsson, Johann E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Degradation; Gene expression; Ribonuclease; RNase 7; RNase L

Indexed keywords

MESSENGER RNA; TRANSCRIPTOME;

AREA UNDER THE CURVE; ARTICLE; CORRELATION ANALYSIS; DNA BASE COMPOSITION; EPIDERMIS; GENE EXPRESSION PROFILING; GENE STRUCTURE; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSORIASIS; RNA DEGRADATION; RNA SEQUENCE; BIOPSY; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; QUALITY CONTROL; SEQUENCE ANALYSIS; SKIN;

BASE COMPOSITION; BASE SEQUENCE; BIOPSY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MICROARRAY ANALYSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PSORIASIS; QUALITY CONTROL; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SKIN; TRANSCRIPTOME;

EID: 84905253096     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00022.2014     Document Type: Article

References (78)

1. Affymetrix Inc. Design and Performance of the GeneChip® Human Genome U133 Plus 2.0 and Human Genome U133A 2.0 Arrays. Affymetrix. http://media.affymetrix.com/support/technical/technotes/hgu133_ p2_technote.pdf (27 Feb. 2014).
2. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 11: R106, 2010
3. Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat Protoc 8: 1765-1786, 2013
4. Andrews S. FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (27 Feb. 2014).
5. Atz M, Walsh D, Cartagena P, Li J, Evans S, Choudary P, Overman K, Stein R, Tomita H, Potkin S, Myers R, Watson SJ, Jones EG, Akil H, Bunney WE Jr, Vawter MP, Members of National Institute of Mental Health Conte Center, Pritzker Neuropsychiatric Disorders Research Consortium. Methodological considerations for gene expression profiling of human brain. J Neurosci Methods 163: 295-309, 2007
6. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a powerful and practical approach to multiple testing. J Roy Stat Soc B 57: 289-300, 1995
7. Benjamini Y, Speed TP. Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res 40: e72, 2012
8. Bentley DL. Coupling mRNA processing with transcription in time and space. Nat Rev Genet 15: 163-175, 2014
9. Bigler J, Rand HA, Kerkof K, Timour M, Russell CB. Cross-study homogeneity of psoriasis gene expression in skin across a large expression range. PLoS One 8: e52242, 2013
10. Black MB, Parks BB, Pluta L, Chu TM, Allen BC, Wolfinger RD, Thomas RS. Comparison of microarrays and RNA-seq for gene expression analyses of dose-response experiments. Toxicol Sci 137: 385-403, 2014
11. Bolstad BM, Collin F, Brettschneider J, Simpson K, Cope L, Irizarry RA, Speed TP. Quality assessment of Affymetrix GeneChip data. In: Bioinformatics and Computational Biology Solutions using R and Bioconductor, edited by Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S. New York: Springer, 2005
12. Bottomly D, Walter NA, Hunter JE, Darakjian P, Kawane S, Buck KJ, Searles RP, Mooney M, McWeeney SK, Hitzemann R. Evaluating gene expression in C57BL/6J and DBA/2J mouse striatum using RNA-Seq and microarrays. PLoS One 6: e17820, 2011
13. Bradford JR, Hey Y, Yates T, Li Y, Pepper SD, Miller CJ. A comparison of massively parallel nucleotide sequencing with oligonucleotide microarrays for global transcription profiling. BMC Genomics 11: 282, 2010
14. Bullard JH, Purdom E, Hansen KD, Dudoit S. Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11: 94, 2010
15. Chavan SS, Bauer MA, Peterson EA, Heuck CJ, Johann DJ. Towards the integration, annotation and association of historical microarray experiments with RNA-seq. BMC Bioinformatics 14, Suppl 14: S4, 2013
16. Chung LM, Ferguson JP, Zheng W, Qian F, Bruno V, Montgomery RR, Zhao H. Differential expression analysis for paired RNA-Seq data. BMC Bioinformatics 14: 110, 2013
17. Dohm JC, Lottaz C, Borodina T, Himmelbauer H. Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res 36: e105, 2008
18. Förster FJ, Neufahrt A, Stockum G, Bauer K, Frenkel S, Fertig U, Leonhardi G. Subcellular distribution of phosphatases, proteinases, and ribonucleases in normal human stratum corneum and psoriatic scales. Arch Dermatol Res 254: 23-28, 1975
19. Gulati N, Krueger JG, Suárez-Fariñas M, Mitsui H. Creation of differentiation-specific genomic maps of human epidermis through laser capture microdissection. J Invest Dermatol 133: 2640-4642, 2013
20. Han JQ, Wroblewski G, Xu Z, Silverman RH, Barton DJ. Sensitivity of hepatitis C virus RNA to the antiviral enzyme ribonuclease L is determined by a subset of efficient cleavage sites. J Interferon Cytokine Res 24: 664-676, 2004
21. Hannon GJ. FASTX-Toolkit. Cold Spring Harbor Laboratory. http://hannonlab.cshl.edu/fastx_toolkit//(27 Feb. 2014).
22. Hansen KD, Brenner SE, Dudoit S. Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 38: e131, 2010
23. Harder J, Dressel S, Wittersheim M, Cordes J, Meyer-Hoffert U, Mrowietz U, Fölster-Holst R, Proksch E, Schröder JM, Schwarz T, Gläser R. Enhanced expression and secretion of antimicrobial peptides in atopic dermatitis and after superficial skin injury. J Invest Dermatol 130: 1355-1364, 2010
24. Harder J, Schroder JM. RNase 7, a novel innate immune defense antimicrobial protein of healthy human skin. J Biol Chem 277: 46779-46784, 2002
25. Harder J, Schröder JM. Psoriatic scales: a promising source for the isolation of human skin-derived antimicrobial proteins. J Leukoc Biol 77: 476-486, 2005
26. Head SR, Komori HK, Hart GT, Shimashita J, Schaffer L, Salomon DR, Ordoukhanian PT. Method for improved Illumina sequencing library preparation using NuGEN Ovation RNA-Seq System. Biotechniques 50: 177-180, 2011
27. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15, 2003
28. Jabbari A, Suárez-Fariñas M, Dewell S, Krueger JG. Transcriptional profiling of psoriasis using RNA-seq reveals previously unidentified differentially expressed genes. J Invest Dermatol 132: 246-249, 2012
29. Jiang H, Wong WH. Statistical inferences for isoform expression in RNA-Seq. Bioinformatics 25: 1026-1032, 2009
30. Johnston A, Guzman AM, Swindell WR, Wang F, Kang S, Gudjonsson JE. Early tissue responses in psoriasis to the anti-TNF- biologic etanercept suggest reduced IL-17R expression and signalling. Br J Dermatol [Epub ahead of print].
31. Joyce CE, Zhou X, Xia J, Ryan C, Thrash B, Menter A, Zhang W, Bowcock AM. Deep sequencing of small RNAs from human skin reveals major alterations in the psoriasis miRNAome. Hum Mol Genet 20: 4025-4040, 2011
32. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36, 2013
33. Kitamura H, Matsuzaki Y, Kimura K, Nakano H, Imaizumi T, Satoh K, Hanada K. Cytokine modulation of retinoic acid-inducible gene-I (RIG-I) expression in human epidermal keratinocytes. J Dermatol Sci 45: 127-134, 2007
34. Kogenaru S, Qing Y, Guo Y, Wang N. RNA-seq and microarray complement each other in transcriptome profiling. BMC Genomics 13: 629, 2012
35. Kvam VM, Liu P, Si Y. A comparison of statistical methods for detecting differentially expressed genes from RNA-seq data. Am J Bot 99: 248-256, 2012
36. Landau WM, Liu P. Dispersion estimation and its effect on test performance in RNA-seq data analysis: a simulation-based comparison of methods. PLoS One 8: e81415, 2013
37. Li B, Tsoi LC, Swindell WR, Gudjonsson JE, Tejasvi T, Johnston A, Ding J, Stuart PE, Xing X, Kochkodan JJ, Voorhees JJ, Kang HM, Nair RP, Abecasis GR, Elder JT. Transcriptome analysis of psoriasis in a large case-control sample: RNA-seq provides insights into disease mechanisms. J Invest Dermatol [Epub ahead of print].
38. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; Subgroup, 1000 Genome Project Data Processing. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079, 2009
39. Li XL, Ezelle HJ, Hsi TY, Hassel BA. A central role for RNA in the induction and biological activities of type 1 interferons. Wiley Interdiscip Rev RNA 2: 58-78, 2011
40. Lu X, Du J, Liang J, Zhu X, Yang Y, Xu J. Transcriptional regulatory network for psoriasis. J Dermatol 40: 48-53, 2013
41. McClintick JN, Edenberg HJ. Effects of filtering by Present call on analysis of microarray experiments. BMC Bioinformatics 7: 49, 2006
42. Melbye SW, Brant BA, Freedberg IW. Epidermal nucleases. III. The ribonucleases of human epidermis. Br J Dermatol 97: 355-364, 1977
43. Nair RP, Duffin KC, Helms C, Ding J, Stuart PE, Goldgar D, Gudjonsson JE, Li Y, Tejasvi T, Feng BJ, Ruether A, Schreiber S, Weichenthal M, Gladman D, Rahman P, Schrodi SJ, Prahalad S, Guthery SL, Fischer J, Liao W, Kwok PY, Menter A, Lathrop GM, Wise CA, Begovich AB, Voorhees JJ, Elder JT, Krueger GG, Bowcock AM, Abecasis GR; Collaborative Association Study of Psoriasis. Genome-wide scan reveals association of psoriasis with IL-23 and NFkappaB pathways. Nat Genet 41: 199-204, 2009
44. Nookaew I, Papini M, Pornputtapong N, Scalcinati G, Fagerberg L, Uhlén M, Nielsen J. A comprehensive comparison of RNA-Seq-based transcriptome analysis from reads to differential gene expression and cross-comparison with microarrays: a case study in Saccharomyces cerevisiae. Nucleic Acids Res 40: 10084-10097, 2012
45. Opitz L, Salinas-Riester G, Grade M, Jung K, Jo P, Emons G, Ghadimi BM, Beissbarth T, Gaedcke J. Impact of RNA degradation on gene expression profiling. BMC Med Genomics 3: 36, 2010
46. Oshlack A, Wakefield MJ. Transcript length bias in RNA-seq data confounds systems biology. Biol Direct 4: 14, 2009
47. Paulsen MT, Veloso A, Prasad J, Bedi K, Ljungman EA, Magnuson B, Wilson TE, Ljungman M. Use of Bru-Seq and BruChase-Seq for genome-wide assessment of the synthesis and stability of RNA. Methods 67: 45-54, 2014
48. Perera GK, Ainali C, Semenova E, Hundhausen C, Barinaga G, Kassen D, Williams AE, Mirza MM, Balazs M, Wang X, Rodriguez RS, Alendar A, Barker J, Tsoka S, Ouyang W, Nestle FO. Integrative biology approach identifies cytokine targeting strategies for psoriasis. Sci Transl Med 6: 223ra22, 2014
49. Popova T, Mennerich D, Weith A, Quast K. Effect of RNA quality on transcript intensity levels in microarray analysis of human post-mortem brain tissues. BMC Genomics 9: 91, 2008
50. Prens EP, Kant M, van Dijk G, van der Wel LI, Mourits S, van der Fits L. IFN-alpha enhances poly-IC responses in human keratinocytes by inducing expression of cytosolic innate RNA receptors: relevance for psoriasis. J Invest Dermatol 128: 932-938, 2008
51. Rapaport F, Khanin R, Liang Y, Pirun M, Krek A, Zumbo P, Mason CE, Socci ND, Betel D. Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol 14: R95, 2013
52. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140, 2010
53. Santiago TC, Purvis IJ, Bettany AJ, Brown AJ. The relationship between mRNA stability and length in Saccharomyces cerevisiae. Nucleic Acids Res 14: 8347-8360, 1986
54. Simanski M, Rademacher F, Schröder L, Schumacher HM, Gläser R, Harder J. IL-17A and IFN-γ synergistically induce RNase 7 expression via STAT3 in primary keratinocytes. PLoS One 8: e59531, 2013
55. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: 3, 2004
56. Solier S, Ryan MC, Martin SE, Varma S, Kohn KW, Liu H, Zeeberg BR, Pommier Y. Transcription poisoning by Topoisomerase I is controlled by gene length, splice sites, and miR-142-3p. Cancer Res 73: 4830-4839, 2013
57. Stalteri MA, Harrison AP. Interpretation of multiple probe sets mapping to the same gene in Affymetrix GeneChips. BMC Bioinformatics 8: 13, 2007
58. Suárez-Fariñas M, Li K, Fuentes-Duculan J, Hayden K, Brodmerkel C, Krueger JG. Expanding the psoriasis disease profile: interrogation of the skin and serum of patients with moderate-to-severe psoriasis. J Invest Dermatol 132: 2552-2564, 2012
59. Su Z, Li Z, Chen T, Li QZ, Fang H, Ding D, Ge W, Ning B, Hong H, Perkins RG, Tong W, Shi L. Comparing next-generation sequencing and microarray technologies in a toxicological study of the effects of aristolochic acid on rat kidneys. Chem Res Toxicol 24: 1486-1493, 2011
60. Swindell WR, Johnston A, Voorhees JJ, Elder JT, Gudjonsson JE. Dissecting the psoriasis transcriptome: inflammatory- and cytokine-driven gene expression in lesions from 163 patients. BMC Genomics 14: 527, 2013
61. Swindell WR, Johnston A, Xing X, Voorhees JJ, Elder JT, Gudjonsson JE. Modulation of epidermal transcription circuits in psoriasis: new links between inflammation and hyperproliferation. PLoS One 8: e79253, 2013
62. Swindell WR, Xing X, Stuart PE, Chen CS, Aphale A, Nair RP, Voorhees JJ, Elder JT, Johnston A, Gudjonsson JE. Heterogeneity of inflammatory and cytokine networks in chronic plaque psoriasis. PLoS One 7: e34594, 2012
63. 't Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, de Menezes RX, Boer JM, van Ommen GJ, den Dunnen JT. Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36: e141, 2008
64. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515, 2010
65. van Dijk EL, Jaszczyszyn Y, Thermes C. Library preparation methods for next-generation sequencing: Tone down the bias. Exp Cell Res 322: 12-20, 2014
66. Veloso A, Biewen B, Paulsen MT, Berg N, Carmo de Andrade Lima L, Prasad J, Bedi K, Magnuson B, Wilson TE, Ljungman M. Genomewide transcriptional effects of the anti-cancer agent camptothecin. PLoS One 8: e78190, 2013
67. Wang L, Wang S, Li W. RSeQC: quality control of RNA-seq experiments. Bioinformatics 28: 2184-2185, 2012
68. Washenberger CL, Han JQ, Kechris KJ, Jha BK, Silverman RH, Barton DJ. Hepatitis C virus RNA: dinucleotide frequencies and cleavage by RNase L. Virus Res 130: 85-95, 2007
69. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, Dicuccio M, Edgar R, Federhen S, Feolo M, Geer LY, Helmberg W, Kapustin Y, Khovayko O, Landsman D, Lipman DJ, Madden TL, Maglott DR, Miller V, Ostell J, Pruitt KD, Schuler GD, Shumway M, Sequeira E, Sherry ST, Sirotkin K, Souvorov A, Starchenko G, Tatusov RL, Tatusova TA, Wagner L, Yaschenko E. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 36: D13-D21, 2008
70. Wongpalee SP, Sharma S. The pre-mRNA splicing reaction. Methods Mol Biol 1126: 3-12, 2014
71. Wreschner DH, McCauley JW, Skehel JJ, Kerr IM. Interferon action-sequence specificity of the ppp(A2=p)nA-dependent ribonuclease. Nature 289: 414-417, 1981
72. Wu D, Smyth GK. Camera: a competitive gene set test accounting for inter-gene correlation. Nucleic Acids Res 40: e133, 2012
73. Xia J, Joyce CE, Bowcock AM, Zhang W. Noncanonical microRNAs and endogenous siRNAs in normal and psoriatic human skin. Hum Mol Genet 22: 737-748, 2013
74. Xu X, Zhang Y, Williams J, Antoniou E, McCombie WR, Wu S, Zhu W, Davidson NO, Denoya P, Li E. Parallel comparison of Illumina RNA-Seq and Affymetrix microarray platforms on transcriptomic profiles generated from 5-aza-deoxy-cytidine treated HT-29 colon cancer cells and simulated datasets. BMC Bioinformatics 14, Suppl 9: S1, 2013
75. Yao Y, Richman L, Morehouse C, de los Reyes M, Higgs BW, Boutrin A, White B, Coyle A, Krueger J, Kiener PA, Jallal B. Type I interferon: potential therapeutic target for psoriasis? PLoS One 3: e2737, 2008
76. Zaba LC, Suárez-Fariñas M, Fuentes-Duculan J, Nograles KE, Guttman- Yassky E, Cardinale I, Lowes MA, Krueger JG. Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes. J Allergy Clin Immunol 124: 1022-1010, 2009
77. Zhao S, Fung-Leung WP, Bittner A, Ngo K, Liu X. Comparison of RNA-seq and microarray in transcriptome profiling of activated T cells. PLoS One 9: e78644, 2014
78. Zibert JR, Løvendorf MB, Litman T, Olsen J, Kaczkowski B, Skov L. MicroRNAs and potential target interactions in psoriasis. J Dermatol Sci 58: 177-185, 2010.