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The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements

Nature Biotechnology volume 24, pages 1151–1161 (2006)Cite this article

Abstract

Over the last decade, the introduction of microarray technology has had a profound impact on gene expression research. The publication of studies with dissimilar or altogether contradictory results, obtained using different microarray platforms to analyze identical RNA samples, has raised concerns about the reliability of this technology. The MicroArray Quality Control (MAQC) project was initiated to address these concerns, as well as other performance and data analysis issues. Expression data on four titration pools from two distinct reference RNA samples were generated at multiple test sites using a variety of microarray-based and alternative technology platforms. Here we describe the experimental design and probe mapping efforts behind the MAQC project. We show intraplatform consistency across test sites as well as a high level of interplatform concordance in terms of genes identified as differentially expressed. This study provides a resource that represents an important first step toward establishing a framework for the use of microarrays in clinical and regulatory settings.

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Figure 1: Repeatability of expression signal within test sites.
Figure 2: Signal variation within and between test sites.
Figure 3: Concordance of detection calls within and between test sites.
Figure 4: Agreement of gene lists.
Figure 5: Agreement of log ratios across platforms and test sites.
Figure 6: Correlation between microarray and TaqMan data.

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Gene Expression Omnibus

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Acknowledgements

All MAQC participants freely donated their time and reagents for the completion and analysis of the MAQC project. Participants from the National Institutes of Health (NIH) were supported by the Intramural Research Program of NIH, Bethesda, Maryland. D.H. thanks Ian Korf for BLAST discussions. This study utilized a number of computing resources, including the high-performance computational capabilities of the Biowulf PC/Linux cluster at the NIH (http://biowulf.nih.gov/) as well as resources at the analysis sites.

Author information

Authors and Affiliations

  1. National Center for Toxicological Research, US Food and Drug Administration, 3900 NCTR Road, Jefferson, 72079, Arkansas, USA

    Leming Shi, Leming Shi, Weida Tong, Yvonne P Dragan, James J Chen, Xiao-hui Fan, James C Fuscoe, Weigong Ge, Lei Guo, Tao Han, Stephen C Harris, Nan Mei, Baitang Ning, Tucker A Patterson, Zhenqiang Su & William Slikker Jr

  2. Expression Analysis, Inc., 2605 Meridian Parkway, Durham, 27713, North Carolina, USA

    Laura H Reid & Wendell D Jones

  3. GE Healthcare, 7700 S. River Parkway, Suite 2603, Tempe, 85284, AZ, USA

    Richard Shippy & Alan Brunner

  4. Affymetrix, Inc., 3420 Central Expressway, Santa Clara, 95051, California, USA

    Janet A Warrington, Christopher Davies, Xu Guo, Chunmei Liu, Tim McDaniel & Yaron Turpaz

  5. Illumina,Inc. 9885 Towne Centre Drive, San Diego, 92121, California, USA

    Shawn C Baker & Eugene Chudin

  6. Agilent Technologies, Inc., 5301 Stevens Creek Blvd., Santa Clara, 95051, California, USA

    Patrick J Collins, Paul K Wolber, Anne Bergstrom Lucas, John Corson, Glenda Delenstarr, Stephanie Fulmer-Smentek, Svetlana Shchegrova & Alex Wong

  7. Eppendorf Array Technologies, rue du Séminaire 20a, Namur, 5000, Belgium

    Francoise de Longueville, Vincent Bertholet & Christophe Van

  8. NCI Advanced Technology Center, 8717 Grovemont Circle, Bethesda, 20892, Maryland, USA

    Ernest S Kawasaki & Yonghong Wang

  9. Applied Biosystems, 850 Lincoln Centre Drive, Foster City, 94404, California, USA

    Kathleen Y Lee, Yongming Andrew Sun, Lu Zhang, Catalin C Barbacioru, Roger Canales, Raymond R Samaha & Chunlin Xiao

  10. Panomics, Inc., 6519 Dumbarton Circle, Fremont, 94555, California, USA

    Yuling Luo, Yunqing Ma, Botoul Maqsodi & Wen Yang

  11. Medical University of Ohio, 3000 Arlington Avenue, Toledo, 43614, Ohio, USA

    James C Willey

  12. Ambion, An Applied Biosystems Business, 2130 Woodward Street, Austin, 78744, Texas, USA

    Robert A Setterquist, Mike Wilson & David Dorris

  13. Stratagene Corp., 11011 North Torrey Pines Road, La Jolla, 92130, California, USA

    Gavin M Fischer & Natalia Novoradovskaya

  14. Office of Research and Development, US Environmental Protection Agency, 109 TW Alexander Drive, Research Triangle Park, 27711, North Carolina, USA

    David J Dix, J Christopher Corton, Susan Hester, Hongzu Ren, Mitch Rosen & Beena Vallanat

  15. Center for Drug Evaluation and Research, US Food and Drug Administration, 10903 New Hampshire Avenue, Silver Spring, 20993, Maryland, USA

    Felix W Frueh, Federico M Goodsaid, Shashi Amur, Michael S Orr, P Scott Pine, Barry A Rosenzweig, Karol L Thompson & Sue Jane Wang

  16. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 8600 Rockville Pike, Bethesda, 20894, Maryland, USA

    Damir Herman, Jean Thierry-Mieg & Danielle Thierry-Mieg

  17. University of Massachusetts-Boston, 100 Morrissey Boulevard, Boston, 02125, Massachusetts, USA

    Roderick V Jensen, Aron C Eklund, Michael J Lombardi & Adam Papallo

  18. Asuragen, Inc., 2150 Woodward, Austin, 78744, Texas, USA

    Charles D Johnson, Mike Wilson & Timothy S Davison

  19. A Division of Clinical Data, Cogenicsâ„¢, Inc., 100 Perimeter Park Drive, Suite C, Morrisville, 27560, North Carolina, USA

    Edward K Lobenhofer, Patrick Hurban & Kenneth L Philips

  20. Center for Biologics Evaluation and Research, US Food and Drug Administration, 29 Lincoln Drive, Bethesda, 20892, Maryland, USA

    Raj K Puri & Jing Han

  21. Center for Devices and Radiological Health, US Food and Drug Administration, 2098 Gaither Road, Rockville, 20850, Maryland, USA

    Uwe Scherf & Zivana Tezak

  22. UCLA David Geffen School of Medicine, Transcriptional Genomics Core, Cedars-Sinai Medical Center, 8700 Beverly Boulevard, Los Angeles, 90048, California, USA

    Charles Wang, Xutao Deng & Jun Xu

  23. Solexa, Inc., 25861 Industrial Boulevard, Hayward, 94545, California, USA

    Lu Zhang & Gary P Schroth

  24. SAS Institute, Inc., 100 SAS Campus Drive, Cary, 27513, North Carolina, USA

    Wenjun Bao, Tzu-Ming Chu & Russ Wolfinger

  25. Vialogy Corp., 2400 Lincoln Avenue, Altadena, 91001, California, USA

    Cecilie Boysen & Bud Bromley

  26. Operon Biotechnologies, 2211 Seminole Drive, Huntsville, 35805, Alabama, USA

    Donna Brown

  27. Z-Tech Corp., 3900 NCTR Road, Jefferson, 72079, Arkansas, USA

    Xiaoxi Megan Cao, Hong Fang, Huixiao Hong, Roger G Perkins, Feng Qian, Hongmei Sun, Jie Wu & Qian Xie

  28. Center for Food Safety and Applied Nutrition, US Food and Drug Administration, 8401 Muirkirk Road, Laurel, 20708, Maryland, USA

    Thomas A Cebula, Scott A Jackson & J Eugene LeClerc

  29. CapitalBio Corp., 18 Life Science Parkway, Changping District, Beijing, 102206, China

    Jing Cheng & Liang Zhang

  30. Biogen Idec, 5200 Research Place, San Diego, 92122, California, USA

    Lisa J Croner

  31. US Environmental Protection Agency, Office of the Science Advisor, 1200 Pennsylvania Avenue, NW, DC 20460, Washington, USA

    Kathryn Gallagher

  32. Yale University, W.M. Keck Biotechnology Resource Laboratory, Microarray Resource, 300 George Street, New Haven, 06511, Connecticut, USA

    Janet Hager & Irina Tikhonova

  33. TeleChem ArrayIt, 524 E. Weddell Drive, Sunnyvale, 94089, California, USA

    Paul K Haje & Mark Schena

  34. Center for Veterinary Medicine, US Food and Drug Administration, 8401 Muirkirk Road, Laurel, 20708, Maryland, USA

    Heather C Harbottle

  35. Cold Spring Harbor Laboratory, 500 Sunnyside Boulevard, Woodbury, 11797, New York, USA

    Eli Hatchwell

  36. Burnham Institute, 10901 North Torrey Pines Road, La Jolla, 92037, California, USA

    Craig A Hauser

  37. Stanford University School of Medicine, 318 Campus Drive, Stanford, 94305, California, USA

    Hanlee Ji

  38. Gene Express, Inc., 975 Research Drive, Toledo, 43614, Ohio, USA

    Charles R Knight, Terry W Osborn & Elizabeth H Peters

  39. Department of Developmental Biology, Harvard School of Dental Medicine, 188 Longwood Avenue, Boston, 02115, Massachusetts, USA

    Winston P Kuo

  40. Vanderbilt University, 465 21st Avenue South, Nashville, 37232, Tennessee, USA

    Shawn Levy

  41. University Texas Southwestern Medical Center, 6000 Harry Hines Boulevard/ND6.504, Dallas, 75390, Texas, USA

    Quan-Zhen Li

  42. Department of Computer Science, University of Texas at Dallas, MS EC31 Richardson, 75083, Texas, USA

    Ying Liu

  43. GenUs BioSystems, Inc., 1808 Janke Drive Unit M, Northbrook, 60062, Illinois, USA

    Scott R Magnuson

  44. Norwegian Microarray Consortium, Rikshospitalet - Radiumhospitalet Health Centre, Montebello, Oslo, N0310, Norway

    Ola Myklebost

  45. Novartis, 250 Massachusetts Avenue, Cambridge, 02139, Massachusetts, USA

    Ron Peterson & Frank Staedtler

  46. Breast Medical Oncology Department-Unit 1354, MD Anderson Cancer Center, 1155 Pressler Street, Houston, 77230, Texas, USA

    Lajos Pusztai

  47. Luminex Corp., 12212 Technology Boulevard, 78727, Austin, Texas, USA

    Dave D Smith

  48. Children's Hospital Informatics Program at the Harvard-MIT Division of Health Sciences and Technology (CHIP@HST), Harvard Medical School, Boston, 02115, Massachusetts, USA

    Zoltan Szallasi

  49. Department of Physiology and Pharmacology, Wake Forest University School of Medicine, Medical Center Boulevard, Winston-Salem, 27157, North Carolina, USA

    Stephen J Walker

  50. Department of Bioengineering, University of Illinois at Urbana-Champaign, 1304 W. Springfield Avenue, Urbana, 61801, Illinois, USA

    Sheng Zhong

  51. Full Moon Biosystems, Inc., 754 N. Pastoria Avenue, Sunnyvale, 94085, California, USA

    Yaping Zong

Consortia

MAQC Consortium

  • Leming Shi
  • , Leming Shi
  • , Laura H Reid
  • , Wendell D Jones
  • , Richard Shippy
  • , Janet A Warrington
  • , Shawn C Baker
  • , Patrick J Collins
  • , Francoise de Longueville
  • , Ernest S Kawasaki
  • , Kathleen Y Lee
  • , Yuling Luo
  • , Yongming Andrew Sun
  • , James C Willey
  • , Robert A Setterquist
  • , Gavin M Fischer
  • , Weida Tong
  • , Yvonne P Dragan
  • , David J Dix
  • , Felix W Frueh
  • , Federico M Goodsaid
  • , Damir Herman
  • , Roderick V Jensen
  • , Charles D Johnson
  • , Edward K Lobenhofer
  • , Raj K Puri
  • , Uwe Scherf
  • , Jean Thierry-Mieg
  • , Charles Wang
  • , Mike Wilson
  • , Paul K Wolber
  • , Lu Zhang
  • , Shashi Amur
  • , Wenjun Bao
  • , Catalin C Barbacioru
  • , Anne Bergstrom Lucas
  • , Vincent Bertholet
  • , Cecilie Boysen
  • , Bud Bromley
  • , Donna Brown
  • , Alan Brunner
  • , Roger Canales
  • , Xiaoxi Megan Cao
  • , Thomas A Cebula
  • , James J Chen
  • , Jing Cheng
  • , Tzu-Ming Chu
  • , Eugene Chudin
  • , John Corson
  • , J Christopher Corton
  • , Lisa J Croner
  • , Christopher Davies
  • , Timothy S Davison
  • , Glenda Delenstarr
  • , Xutao Deng
  • , David Dorris
  • , Aron C Eklund
  • , Xiao-hui Fan
  • , Hong Fang
  • , Stephanie Fulmer-Smentek
  • , James C Fuscoe
  • , Kathryn Gallagher
  • , Weigong Ge
  • , Lei Guo
  • , Xu Guo
  • , Janet Hager
  • , Paul K Haje
  • , Jing Han
  • , Tao Han
  • , Heather C Harbottle
  • , Stephen C Harris
  • , Eli Hatchwell
  • , Craig A Hauser
  • , Susan Hester
  • , Huixiao Hong
  • , Patrick Hurban
  • , Scott A Jackson
  • , Hanlee Ji
  • , Charles R Knight
  • , Winston P Kuo
  • , J Eugene LeClerc
  • , Shawn Levy
  • , Quan-Zhen Li
  • , Chunmei Liu
  • , Ying Liu
  • , Michael J Lombardi
  • , Yunqing Ma
  • , Scott R Magnuson
  • , Botoul Maqsodi
  • , Tim McDaniel
  • , Nan Mei
  • , Ola Myklebost
  • , Baitang Ning
  • , Natalia Novoradovskaya
  • , Michael S Orr
  • , Terry W Osborn
  • , Adam Papallo
  • , Tucker A Patterson
  • , Roger G Perkins
  • , Elizabeth H Peters
  • , Ron Peterson
  • , Kenneth L Philips
  • , P Scott Pine
  • , Lajos Pusztai
  • , Feng Qian
  • , Hongzu Ren
  • , Mitch Rosen
  • , Barry A Rosenzweig
  • , Raymond R Samaha
  • , Mark Schena
  • , Gary P Schroth
  • , Svetlana Shchegrova
  • , Dave D Smith
  • , Frank Staedtler
  • , Zhenqiang Su
  • , Hongmei Sun
  • , Zoltan Szallasi
  • , Zivana Tezak
  • , Danielle Thierry-Mieg
  • , Karol L Thompson
  • , Irina Tikhonova
  • , Yaron Turpaz
  • , Beena Vallanat
  • , Christophe Van
  • , Stephen J Walker
  • , Sue Jane Wang
  • , Yonghong Wang
  • , Russ Wolfinger
  • , Alex Wong
  • , Jie Wu
  • , Chunlin Xiao
  • , Qian Xie
  • , Jun Xu
  • , Wen Yang
  • , Liang Zhang
  • , Sheng Zhong
  • , Yaping Zong
  •  & William Slikker Jr

Corresponding author

Correspondence to Leming Shi.

Ethics declarations

Competing interests

Many of the MAQC participants are employed by companies that manufacture gene expression products and/or perform testing services. J.C.W. is a consultant for and has significant financial interest in Gene Express, Inc.

Supplementary information

Supplementary Table 1

cRNA Size and Yields Collected from Microarray Platforms (XLS 45 kb)

Supplementary Table 2

Genes-to-NM Accession List for All Probes (TXT 2629 kb)

Supplementary Table 3

Most 3′ Probe-to-NM Accession List for 23,971 Common Probes (TXT 3272 kb)

Supplementary Table 4

One Probe-to-One Gene List for All Genes (TXT 1718 kb)

Supplementary Table 5

One Probe-to-One Gene List for 12,091 Common Genes (TXT 1211 kb)

Supplementary Methods

BLAST Analysis for the MAQC Project (PDF 67 kb)

Supplementary Notes

README for Probe Mapping Files (PDF 11 kb)

Supplementary Data

Supplementary Information on MAQC Study (PDF 663 kb)

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MAQC Consortium. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat Biotechnol 24, 1151–1161 (2006). https://doi.org/10.1038/nbt1239

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