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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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Apparently low reproducibility of true differential expression discoveries in microarray studies
Bioinformatics, September 15, 2008; 24(18): 2057 - 2063.
[Abstract] [Full Text] [PDF]


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Molecular Cancer TherapeuticsHome page
J. Fukai, H. Yokote, R. Yamanaka, T. Arao, K. Nishio, and T. Itakura
EphA4 promotes cell proliferation and migration through a novel EphA4-FGFR1 signaling pathway in the human glioma U251 cell line
Mol. Cancer Ther., September 1, 2008; 7(9): 2768 - 2778.
[Abstract] [Full Text] [PDF]


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J. Bacteriol.Home page
B. Joseph, S. Mertins, R. Stoll, J. Schar, K. R. Umesha, Q. Luo, S. Muller-Altrock, and W. Goebel
Glycerol Metabolism and PrfA Activity in Listeria monocytogenes
J. Bacteriol., August 1, 2008; 190(15): 5412 - 5430.
[Abstract] [Full Text] [PDF]


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J. Bacteriol.Home page
J. Yun, B. Jeon, Y.-W. Barton, P. Plummer, Q. Zhang, and S. Ryu
Role of the DksA-Like Protein in the Pathogenesis and Diverse Metabolic Activity of Campylobacter jejuni
J. Bacteriol., July 1, 2008; 190(13): 4512 - 4520.
[Abstract] [Full Text] [PDF]


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J Exp BotHome page
C. Calderon-Vazquez, E. Ibarra-Laclette, J. Caballero-Perez, and L. Herrera-Estrella
Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels
J. Exp. Bot., June 6, 2008; (2008) ern115v2.
[Abstract] [Full Text] [PDF]


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Nucleic Acids ResHome page
S. Keles, C. L. Warren, C. D. Carlson, and A. Z. Ansari
CSI-Tree: a regression tree approach for modeling binding properties of DNA-binding molecules based on cognate site identification (CSI) data
Nucleic Acids Res., June 1, 2008; 36(10): 3171 - 3184.
[Abstract] [Full Text] [PDF]


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Rheumatology (Oxford)Home page
N. Sekiguchi, S. Kawauchi, T. Furuya, N. Inaba, K. Matsuda, S. Ando, M. Ogasawara, H. Aburatani, H. Kameda, K. Amano, et al.
Messenger ribonucleic acid expression profile in peripheral blood cells from RA patients following treatment with an anti-TNF-{alpha} monoclonal antibody, infliximab
Rheumatology, June 1, 2008; 47(6): 780 - 788.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
A. Nodop, D. Pietsch, R. Hocker, A. Becker, E. K. Pistorius, K. Forchhammer, and K.-P. Michel
Transcript Profiling Reveals New Insights into the Acclimation of the Mesophilic Fresh-Water Cyanobacterium Synechococcus elongatus PCC 7942 to Iron Starvation
Plant Physiology, June 1, 2008; 147(2): 747 - 763.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
S. Kumaraswamy, P. Chinnaiyan, U. T. Shankavaram, X. Lu, K. Camphausen, and P. J. Tofilon
Radiation-Induced Gene Translation Profiles Reveal Tumor Type and Cancer-Specific Components
Cancer Res., May 15, 2008; 68(10): 3819 - 3826.
[Abstract] [Full Text] [PDF]


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Genome ResHome page
R. A. Irizarry, C. Ladd-Acosta, B. Carvalho, H. Wu, S. A. Brandenburg, J. A. Jeddeloh, B. Wen, and A. P. Feinberg
Comprehensive high-throughput arrays for relative methylation (CHARM)
Genome Res., May 1, 2008; 18(5): 780 - 790.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
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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