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Biostatistics 4:249-264 (2003)
© 2003 Oxford University Press

Exploration, normalization, and summaries of high density oligonucleotide array probe level data

Rafael A. Irizarry*, Bridget Hobbs, Francois Collin, Yasmin D. Beazer-Barclay, Kristen J. Antonellis, Uwe Scherf and Terence P. Speed

Department of Biostatistics, Johns Hopkins University, Baltimore MD 21205, USA rafa{at}jhu.edu
Division of Genetics and Bioinformatics, WEHI, Melbourne, Australia
Gene Logic Inc., Berkeley, CA, USA
Gene Logic Inc., Gaithersburg, MD, USA
Gene Logic Inc., Gaithersburg, MD, USA
Gene Logic Inc., Gaithersburg, MD, USA
Division of Genetics and Bioinformatics, WEHI, Melbourne, Australia. Department of Statistics, University of California at Berkeley

*To whom correspondence should be addressed

In this paper we report exploratory analyses of high-density oligonucleotide array data from the Affymetrix GeneChip® system with the objective of improving upon currently used measures of gene expression. Our analyses make use of three data sets: a small experimental study consisting of five MGU74A mouse GeneChip® arrays, part of the data from an extensive spike-in study conducted by Gene Logic and Wyeth's Genetics Institute involving 95 HG-U95A human GeneChip® arrays; and part of a dilution study conducted by Gene Logic involving 75 HG-U95A GeneChip® arrays. We display some familiar features of the perfect match and mismatch probe (PM and MM) values of these data, and examine the variance–mean relationship with probe-level data from probes believed to be defective, and so delivering noise only. We explain why we need to normalize the arrays to one another using probe level intensities. We then examine the behavior of the PM and MM using spike-in data and assess three commonly used summary measures: Affymetrix's (i) average difference (AvDiff) and (ii) MAS 5.0 signal, and (iii) the Li and Wong multiplicative model-based expression index (MBEI). The exploratory data analyses of the probe level data motivate a new summary measure that is a robust multi-array average (RMA) of background-adjusted, normalized, and log-transformed PM values. We evaluate the four expression summary measures using the dilution study data, assessing their behavior in terms of bias, variance and (for MBEI and RMA) model fit. Finally, we evaluate the algorithms in terms of their ability to detect known levels of differential expression using the spike-in data. We conclude that there is no obvious downside to using RMA and attaching a standard error (SE) to this quantity using a linear model which removes probe-specific affinities.


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Regulator of sex-limitation KRAB zinc finger proteins modulate sex-dependent and -independent liver metabolism
Physiol Genomics, June 10, 2009; 38(1): 16 - 28.
[Abstract] [Full Text] [PDF]


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Drug Metab. Dispos.Home page
K. Mathijs, A. S. Kienhuis, K. J. J. Brauers, D. G. J. Jennen, A. Lahoz, J. C. S. Kleinjans, and J. H. M. van Delft
Assessing the Metabolic Competence of Sandwich-Cultured Mouse Primary Hepatocytes
Drug Metab. Dispos., June 1, 2009; 37(6): 1305 - 1311.
[Abstract] [Full Text] [PDF]


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Circ Cardiovasc GenetHome page
M. E. Putt, S. Hannenhalli, Y. Lu, P. Haines, H. R. Chandrupatla, E. E. Morrisey, K. B. Margulies, and T. P. Cappola
Evidence for Coregulation of Myocardial Gene Expression by MEF2 and NFAT in Human Heart Failure
Circ Cardiovasc Genet, June 1, 2009; 2(3): 212 - 219.
[Abstract] [Full Text] [PDF]


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Genome ResHome page
X. Wang, H. Tang, J. E. Bowers, and A. H. Paterson
Comparative inference of illegitimate recombination between rice and sorghum duplicated genes produced by polyploidization
Genome Res., June 1, 2009; 19(6): 1026 - 1032.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
R. Beroukhim, J.-P. Brunet, A. Di Napoli, K. D. Mertz, A. Seeley, M. M. Pires, D. Linhart, R. A. Worrell, H. Moch, M. A. Rubin, et al.
Patterns of Gene Expression and Copy-Number Alterations in von-Hippel Lindau Disease-Associated and Sporadic Clear Cell Carcinoma of the Kidney
Cancer Res., June 1, 2009; 69(11): 4674 - 4681.
[Abstract] [Full Text] [PDF]


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HeartHome page
P Meier, J Antonov, R Zbinden, A Kuhn, S Zbinden, S Gloekler, M Delorenzi, R Jaggi, and C Seiler
Non-invasive gene-expression-based detection of well-developed collateral function in individuals with and without coronary artery disease
Heart, June 1, 2009; 95(11): 900 - 908.
[Abstract] [Full Text] [PDF]


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GeneticsHome page
X. Deng, S. K. Koya, Y. Kong, and V. H. Meller
Coordinated Regulation of Heterochromatic Genes in Drosophila melanogaster Males
Genetics, June 1, 2009; 182(2): 481 - 491.
[Abstract] [Full Text] [PDF]


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BioinformaticsHome page
W. Pan
Network-based multiple locus linkage analysis of expression traits
Bioinformatics, June 1, 2009; 25(11): 1390 - 1396.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
K. Vandepoele, M. Quimbaya, T. Casneuf, L. De Veylder, and Y. Van de Peer
Unraveling Transcriptional Control in Arabidopsis Using cis-Regulatory Elements and Coexpression Networks
Plant Physiology, June 1, 2009; 150(2): 535 - 546.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
M. R. Aluru, J. Zola, A. Foudree, and S. R. Rodermel
Chloroplast Photooxidation-Induced Transcriptome Reprogramming in Arabidopsis immutans White Leaf Sectors
Plant Physiology, June 1, 2009; 150(2): 904 - 923.
[Abstract] [Full Text] [PDF]


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Am. J. Respir. Crit. Care Med.Home page
E. D. Crouser, D. A. Culver, K. S. Knox, M. W. Julian, G. Shao, S. Abraham, S. Liyanarachchi, J. E. Macre, M. D. Wewers, M. A. Gavrilin, et al.
Gene Expression Profiling Identifies MMP-12 and ADAMDEC1 as Potential Pathogenic Mediators of Pulmonary Sarcoidosis
Am. J. Respir. Crit. Care Med., May 15, 2009; 179(10): 929 - 938.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
M. V. Fournier, J. E. Fata, K. J. Martin, P. Yaswen, and M. J. Bissell
Interaction of E-cadherin and PTEN Regulates Morphogenesis and Growth Arrest in Human Mammary Epithelial Cells
Cancer Res., May 15, 2009; 69(10): 4545 - 4552.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
S. Saito, A. Furuno, J. Sakurai, A. Sakamoto, H.-R. Park, K. Shin-ya, T. Tsuruo, and A. Tomida
Chemical Genomics Identifies the Unfolded Protein Response as a Target for Selective Cancer Cell Killing during Glucose Deprivation
Cancer Res., May 15, 2009; 69(10): 4225 - 4234.
[Abstract] [Full Text] [PDF]


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Nucleic Acids ResHome page
V. Jayaswal, M. Lutherborrow, D. D. F. Ma, and Y. Hwa Yang
Identification of microRNAs with regulatory potential using a matched microRNA-mRNA time-course data
Nucleic Acids Res., May 1, 2009; 37(8): e60 - e60.
[Abstract] [Full Text] [PDF]


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Nucleic Acids ResHome page
Y.-S. Lee, C.-H. Chen, C.-N. Tsai, C.-L. Tsai, A. Chao, and T.-H. Wang
Microarray labeling extension values: laboratory signatures for Affymetrix GeneChips
Nucleic Acids Res., May 1, 2009; 37(8): e61 - e61.
[Abstract] [Full Text] [PDF]


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Brief BioinformHome page
W. B. Langdon, G. J. G. Upton, and A. P. Harrison
Probes containing runs of guanines provide insights into the biophysics and bioinformatics of Affymetrix GeneChips
Brief Bioinform, May 1, 2009; 10(3): 259 - 277.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
J. M. Bower, H. B. Gordon-Raagas, and M. A. Mulvey
Conditioning of Uropathogenic Escherichia coli for Enhanced Colonization of Host
Infect. Immun., May 1, 2009; 77(5): 2104 - 2112.
[Abstract] [Full Text] [PDF]


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Hum ReprodHome page
I. Van Vaerenbergh, L. Van Lommel, V. Ghislain, P. In't Veld, F. Schuit, H. M. Fatemi, P. Devroey, and C. Bourgain
In GnRH antagonist/rec-FSH stimulated cycles, advanced endometrial maturation on the day of oocyte retrieval correlates with altered gene expression
Hum. Reprod., May 1, 2009; 24(5): 1085 - 1091.
[Abstract] [Full Text] [PDF]


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Molecular Cancer TherapeuticsHome page
T. Yan, S. Deng, A. Metzger, U. Godtel-Armbrust, A. C.G. Porter, and L. Wojnowski
Topoisomerase II{alpha}-dependent and -independent apoptotic effects of dexrazoxane and doxorubicin
Mol. Cancer Ther., May 1, 2009; 8(5): 1075 - 1085.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
A. Fukushima, M. Kusano, N. Nakamichi, M. Kobayashi, N. Hayashi, H. Sakakibara, T. Mizuno, and K. Saito
Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination
PNAS, April 28, 2009; 106(17): 7251 - 7256.
[Abstract] [Full Text] [PDF]


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BloodHome page
N. S. Longo, P. L. Lugar, S. Yavuz, W. Zhang, P. H. L. Krijger, D. E. Russ, D. D. Jima, S. S. Dave, A. C. Grammer, and P. E. Lipsky
Analysis of somatic hypermutation in X-linked hyper-IgM syndrome shows specific deficiencies in mutational targeting
Blood, April 16, 2009; 113(16): 3706 - 3715.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
A. M. Taylor, N. C. Berchtold, V. M. Perreau, C. H. Tu, N. Li Jeon, and C. W. Cotman
Axonal mRNA in Uninjured and Regenerating Cortical Mammalian Axons
J. Neurosci., April 15, 2009; 29(15): 4697 - 4707.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
D. Getnet, C. H. Maris, E. L. Hipkiss, J. F. Grosso, T. J. Harris, H.-R. Yen, T. C. Bruno, S. Wada, A. Adler, R. W. Georgantas, et al.
Tumor Recognition and Self-Recognition Induce Distinct Transcriptional Profiles in Antigen-Specific CD4 T Cells
J. Immunol., April 15, 2009; 182(8): 4675 - 4685.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
V. C. Daniel, L. Marchionni, J. S. Hierman, J. T. Rhodes, W. L. Devereux, C. M. Rudin, R. Yung, G. Parmigiani, M. Dorsch, C. D. Peacock, et al.
A Primary Xenograft Model of Small-Cell Lung Cancer Reveals Irreversible Changes in Gene Expression Imposed by Culture In vitro
Cancer Res., April 15, 2009; 69(8): 3364 - 3373.
[Abstract] [Full Text] [PDF]


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CirculationHome page
O. Tornavaca, G. Pascual, M.L. Barreiro, M.T. Grande, A. Carretero, M. Riera, E. Garcia-Arumi, B. Bardaji, M. Gonzalez-Nunez, M.A. Montero, et al.
Kidney Androgen-Regulated Protein Transgenic Mice Show Hypertension and Renal Alterations Mediated by Oxidative Stress
Circulation, April 14, 2009; 119(14): 1908 - 1917.
[Abstract] [Full Text] [PDF]


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Physiol. GenomicsHome page
M. Marotta, C. Ruiz-Roig, Y. Sarria, J. L. Peiro, F. Nunez, J. Ceron, F. Munell, and M. Roig-Quilis
Muscle genome-wide expression profiling during disease evolution in mdx mice
Physiol Genomics, April 10, 2009; 37(2): 119 - 132.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. Schupp, A. G. Cristancho, M. I. Lefterova, E. A. Hanniman, E. R. Briggs, D. J. Steger, M. Qatanani, J. C. Curtin, J. Schug, S. A. Ochsner, et al.
Re-expression of GATA2 Cooperates with Peroxisome Proliferator-activated Receptor-{gamma} Depletion to Revert the Adipocyte Phenotype
J. Biol. Chem., April 3, 2009; 284(14): 9458 - 9464.
[Abstract] [Full Text] [PDF]


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Nucleic Acids ResHome page
J. Carrera, G. Rodrigo, and A. Jaramillo
Model-based redesign of global transcription regulation
Nucleic Acids Res., April 1, 2009; 37(5): e38 - e38.
[Abstract] [Full Text] [PDF]


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Appl. Environ. Microbiol.Home page
G. Panagiotou, M. R. Andersen, T. Grotkjaer, T. B. Regueira, J. Nielsen, and L. Olsson
Studies of the Production of Fungal Polyketides in Aspergillus nidulans by Using Systems Biology Tools
Appl. Envir. Microbiol., April 1, 2009; 75(7): 2212 - 2220.
[Abstract] [Full Text] [PDF]



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