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Nucleic Acids Research, 2002, Vol. 30, No. 4 e15
© 2002 Oxford University Press

Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation

Yee Hwa Yang1, Sandrine Dudoit2, Percy Luu3, David M. Lin3, Vivian Peng3,4, John Ngai3,4,5 and Terence P. Speed1,6,*

1Department of Statistics, 2Division of Biostatistics, 3Department of Molecular and Cell Biology, 4Functional Genomics Laboratory and 5Neurogenomics Center, Helen Wills Neuroscience Institute, University of California, Berkeley, CA 94720-3860, USA and 6Division of Genetics and Bioinformatics, The Walter and Eliza Hall Institute, Melbourne, Australia

There are many sources of systematic variation in cDNA microarray experiments which affect the measured gene expression levels (e.g. differences in labeling efficiency between the two fluorescent dyes). The term normalization refers to the process of removing such variation. A constant adjustment is often used to force the distribution of the intensity log ratios to have a median of zero for each slide. However, such global normalization approaches are not adequate in situations where dye biases can depend on spot overall intensity and/or spatial location within the array. This article proposes normalization methods that are based on robust local regression and account for intensity and spatial dependence in dye biases for different types of cDNA microarray experiments. The selection of appropriate controls for normalization is discussed and a novel set of controls (microarray sample pool, MSP) is introduced to aid in intensity-dependent normalization. Lastly, to allow for comparisons of expression levels across slides, a robust method based on maximum likelihood estimation is proposed to adjust for scale differences among slides.

* To whom correspondence should be addressed at: Department of Statistics, University of California, 367 Evans Hall, #3860 Berkeley, CA 94720-3860, USA. Tel: +1 510 642 2781; Fax: +1 510 642 7892; Email: terry{at}stat.berkeley.eduThe authors wish it to be known that, in their opinion, the first three authors should be regarded as joint First Authors


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E. J. Nam, H. Yoon, S. W. Kim, H. Kim, Y. T. Kim, J. H. Kim, J. W. Kim, and S. Kim
MicroRNA Expression Profiles in Serous Ovarian Carcinoma
Clin. Cancer Res., May 1, 2008; 14(9): 2690 - 2695.
[Abstract] [Full Text] [PDF]

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 BioinformaticsHome page
A. A. Shabalin, H. Tjelmeland, C. Fan, C. M. Perou, and A. B. Nobel
Merging two gene-expression studies via cross-platform normalization
Bioinformatics, May 1, 2008; 24(9): 1154 - 1160.
[Abstract] [Full Text] [PDF]

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 BioinformaticsHome page
R. F. Thompson, M. Reimers, B. Khulan, M. Gissot, T. A. Richmond, Q. Chen, X. Zheng, K. Kim, and J. M. Greally
An analytical pipeline for genomic representations used for cytosine methylation studies
Bioinformatics, May 1, 2008; 24(9): 1161 - 1167.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
M. G. Wade, A. Kawata, A. Williams, and C. Yauk
Methoxyacetic Acid-Induced Spermatocyte Death Is Associated with Histone Hyperacetylation in Rats
Biol Reprod, May 1, 2008; 78(5): 822 - 831.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
R. Bhati, C. Patterson, C. A. Livasy, C. Fan, D. Ketelsen, Z. Hu, E. Reynolds, C. Tanner, D. T. Moore, F. Gabrielli, et al.
Molecular Characterization of Human Breast Tumor Vascular Cells
Am. J. Pathol., May 1, 2008; 172(5): 1381 - 1390.
[Abstract] [Full Text] [PDF]

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 Plant Physiol.Home page
R. A. Chavez Montes, P. Ranocha, Y. Martinez, Z. Minic, L. Jouanin, M. Marquis, L. Saulnier, L. M. Fulton, C. S. Cobbett, F. Bitton, et al.
Cell Wall Modifications in Arabidopsis Plants with Altered {alpha}-L-Arabinofuranosidase Activity
Plant Physiology, May 1, 2008; 147(1): 63 - 77.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
T. del Castillo, E. Duque, and J. L. Ramos
A Set of Activators and Repressors Control Peripheral Glucose Pathways in Pseudomonas putida To Yield a Common Central Intermediate
J. Bacteriol., April 1, 2008; 190(7): 2331 - 2339.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
K. Heurlier, M. J. Thomson, N. Aziz, and J. W. B. Moir
The Nitric Oxide (NO)-Sensing Repressor NsrR of Neisseria meningitidis Has a Compact Regulon of Genes Involved in NO Synthesis and Detoxification
J. Bacteriol., April 1, 2008; 190(7): 2488 - 2495.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Hausmann, B. Samans, R. Lill, and U. Muhlenhoff
Cellular and Mitochondrial Remodeling upon Defects in Iron-Sulfur Protein Biogenesis
J. Biol. Chem., March 28, 2008; 283(13): 8318 - 8330.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
B. Guo, Y. Wang, F. Shi, Y.-W. Barton, P. Plummer, D. L. Reynolds, D. Nettleton, T. Grinnage-Pulley, J. Lin, and Q. Zhang
CmeR Functions as a Pleiotropic Regulator and Is Required for Optimal Colonization of Campylobacter jejuni In Vivo
J. Bacteriol., March 15, 2008; 190(6): 1879 - 1890.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
A. T. Beek, B. J. F. Keijser, A. Boorsma, A. Zakrzewska, R. Orij, G. J. Smits, and S. Brul
Transcriptome Analysis of Sorbic Acid-Stressed Bacillus subtilis Reveals a Nutrient Limitation Response and Indicates Plasma Membrane Remodeling
J. Bacteriol., March 1, 2008; 190(5): 1751 - 1761.
[Abstract] [Full Text] [PDF]

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 Genome ResHome page
C. Cazalet, S. Jarraud, Y. Ghavi-Helm, F. Kunst, P. Glaser, J. Etienne, and C. Buchrieser
Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species
Genome Res., March 1, 2008; 18(3): 431 - 441.
[Abstract] [Full Text] [PDF]

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 Mol Hum ReprodHome page
C. Bredhult, L. Sahlin, and M. Olovsson
Gene expression analysis of human endometrial endothelial cells exposed to op'-DDT
Mol. Hum. Reprod., February 1, 2008; 14(2): 97 - 106.
[Abstract] [Full Text] [PDF]

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 BioinformaticsHome page
D. Yang, Y. Li, H. Xiao, Q. Liu, M. Zhang, J. Zhu, W. Ma, C. Yao, J. Wang, D. Wang, et al.
Gaining confidence in biological interpretation of the microarray data: the functional consistence of the significant GO categories
Bioinformatics, January 15, 2008; 24(2): 265 - 271.
[Abstract] [Full Text] [PDF]

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 Nucleic Acids ResHome page
S. Gagnot, J.-P. Tamby, M.-L. Martin-Magniette, F. Bitton, L. Taconnat, S. Balzergue, S. Aubourg, J.-P. Renou, A. Lecharny, and V. Brunaud
CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform
Nucleic Acids Res., January 11, 2008; 36(suppl_1): D986 - D990.
[Abstract] [Full Text] [PDF]

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 MicrobiologyHome page
T. Hindre, H. Bruggemann, C. Buchrieser, and Y. Hechard
Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation
Microbiology, January 1, 2008; 154(1): 30 - 41.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
A. B. Hervas, I. Canosa, and E. Santero
Transcriptome Analysis of Pseudomonas putida in Response to Nitrogen Availability
J. Bacteriol., January 1, 2008; 190(1): 416 - 420.
[Abstract] [Full Text] [PDF]

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 BioinformaticsHome page
R. Kelley, H. Feizi, and T. Ideker
Correcting for gene-specific dye bias in DNA microarrays using the method of maximum likelihood
Bioinformatics, January 1, 2008; 24(1): 71 - 77.
[Abstract] [Full Text] [PDF]

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 J. Mol. Diagn.Home page
A. A. Melnikov, D. M. Scholtens, E. L. Wiley, S. A. Khan, and V. V. Levenson
Array-Based Multiplex Analysis of DNA Methylation in Breast Cancer Tissues
J. Mol. Diagn., January 1, 2008; 10(1): 93 - 101.
[Abstract] [Full Text] [PDF]

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 BloodHome page
P. U. Magnusson, A. Dimberg, S. Mellberg, A. Lukinius, and L. Claesson-Welsh
FGFR-1 regulates angiogenesis through cytokines interleukin-4 and pleiotrophin
Blood, December 15, 2007; 110(13): 4214 - 4222.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
M. L. Madsen, M. J. Oneal, S. W. Gardner, E. L. Strait, D. Nettleton, E. L. Thacker, and F. C. Minion
Array-Based Genomic Comparative Hybridization Analysis of Field Strains of Mycoplasma hyopneumoniae
J. Bacteriol., November 15, 2007; 189(22): 7977 - 7982.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
S. Chen, M. A. de Vries, and S. P. Bell
Orc6 is required for dynamic recruitment of Cdt1 during repeated Mcm2 7 loading
Genes & Dev., November 15, 2007; 21(22): 2897 - 2907.
[Abstract] [Full Text] [PDF]

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 Physiol. GenomicsHome page
F. I. J. Crawford, C. L. Hodgkinson, E. Ivanova, L. B. Logunova, G. J. Evans, S. Steinlechner, and A. S. I. Loudon
Influence of torpor on cardiac expression of genes involved in the circadian clock and protein turnover in the Siberian hamster (Phodopus sungorus)
Physiol Genomics, November 14, 2007; 31(3): 521 - 530.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
C. Scheele, A. R. Nielsen, T. B. Walden, D. A. Sewell, C. P. Fischer, R. J. Brogan, N. Petrovic, O. Larsson, P. A. Tesch, K. Wennmalm, et al.
Altered regulation of the PINK1 locus: a link between type 2 diabetes and neurodegeneration?
FASEB J, November 1, 2007; 21(13): 3653 - 3665.
[Abstract] [Full Text] [PDF]


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