A survey and comparative study of statistical tests for identifying differential expressionfrom microarray data

IEEE/ACM Transactions on Computational Biology and Bioinformatics

Volumn 11, Issue 1, 2014, Pages 95-115

  Bandyopadhyay, Sanghamitra ^a   Mallik, Saurav ^a   Mukhopadhyay, Anirban ^b  

^a INDIAN STATISTICAL INSTITUTE   (India)

^b UNIVERSITY OF KALYANI   (India)

Author keywords

Differentially expressed transcripts; multiple testing corrections; parametric and nonparametric tests; power of test

Indexed keywords

RNA; SURVEYS; TESTING;

COMPARATIVE STUDIES; DIFFERENTIAL EXPRESSIONS; DIFFERENTIALLY EXPRESSED TRANSCRIPTS; EXPERIMENTAL CONDITIONS; MICROARRAY DATA SETS; MULTIPLE TESTING; NON-PARAMETRIC TEST; STATISTICAL TESTING METHODS;

STATISTICAL TESTS;

MESSENGER RNA;

ANALYSIS OF VARIANCE; BIOLOGICAL MODEL; BIOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; PROCEDURES; REPRODUCIBILITY; STATISTICAL MODEL;

ANALYSIS OF VARIANCE; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; MODELS, GENETIC; MODELS, STATISTICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER;

EID: 84901343580     PISSN: 15455963     EISSN: None     Source Type: Journal    
DOI: 10.1109/TCBB.2013.147     Document Type: Article

References (80)

1. J. Phillips and V. Corces, "CTCF: Master Weaver of the Genome, " Cell, vol. 137, pp. 1194-1201, 2009.
2. R. Ramanathan, S. Varma, J. Ribeiro, T. Myers, T. Nolan, D. Abraham, J. Lok, and T. Nutman, "Microarray-Based Analysis of Differential Gene Expression between Infective and Nonin-fective Larvae of Strongyloides stercoralis, " PLoS Neglect Trop D, vol. 5, no. 5, p. 1039, 2011.
3. U. Maulik, A. Mukhopadhyay, and S. Bandyopadhyay, "Combining Pareto-Optimal Clusters Using Supervised Learning for Identifying Co-Expressed Genes, " BMC Bioinformatics, vol. 10, article 27, pp. 1-16, 2009.
4. U. Maulik, S. Bandyopadhyay, and A. Mukhopadhyay, "Multi-Class Clustering of Cancer Subtypes through SVM Based Ensemble of Pareto-Optimal Solutions for Gene Marker Identification, " PLoS One, vol. 5, no. 11, p. e13803, 2010.
5. A. Mukhopadhyay, U. Maulik, and S. Bandyopdhyay, "On Biclus-tering of Gene Expression Data, " Current Bioinformatics, vol. 5, no. 3, pp. 204-216, 2010.
6. U. Maulik and A. Mukhopadhyay, "Simulated Annealing Based Automatic Fuzzy Clustering Combined with ANN Classification for Analyzing Microarray Data, " Computers & Operations Research, vol. 37, no. 8, pp. 1369-1380, 2010.
7. B. Wu, "Differential Gene Expression Detection and Sample Classification Using Penalized Linear Regression Models, " Bioinfor-matics, vol. 22, pp. 472-476, 2006. (Pubitemid 43231423)
8. Z. Joseph, A. Gitter, and I. Simon, "Studying and Modelling Dynamic Biological Processes Using Time-Series Gene Expression Data, " Nature Reviews Genetics, vol. 13, pp. 552-564, 2012.
9. S. Mallik, A. Mukhopadhyay, U. Maulik, and S. Bandyopadhyay, "Integrated Analysis of Gene Expression and Genome-Wide DNA Methylation for Tumor Prediction: An Association Rule Mining-Based Approach, " Proc. IEEE Symp. Computational Intelligence in Bioinformatics and Computational Biology (CIBCB), IEEE Symp. Series on Computational Intelligence (SSCI '13), pp. 120-127, Apr. 2013.
10. S. Mallik, A. Mukhopadhyay, and U. Maulik, "Integrated Statistical and Rule-Mining Techniques for DNA Methylation and Gene Expression Data Analysis, " J. Artificial Intelligence and Soft Computing Research, vol. 3, no. 2, pp. 1-17, 2013.
11. J. Hacia, J. Fan, O. Ryder, L. Jin, K. Edgemon, G. Ghandour, R. Mayer, B. Sun, L. Hsie, C. Robbins, L. Brody, D. Wang, E. Lander, R. Lipshutz, S. Fodor, and F. Collins, "Determination of Ancestral Alleles for Human Single-Nucleotide Polymorphisms Using High-Density Oligonucleotide Arrays, " Nature Genetics, vol. 22, pp. 164-167, 1999. (Pubitemid 29264810)
12. W. Alvord, J. Roayaei, O. Quinones, and K. Schneider, "A Micro-array Analysis for Differential Gene Expression in the Soybean Genome Using Bioconductor and R, " Briefings in Bioinformatics, vol. 8, no. 6, pp. 415-431, 2007. (Pubitemid 350186921)
13. W. Pan, "A Comparative Review of Statistical Methods for Discovering Differentially Expressed Genes in Replicated Microarray Experiments, " Bioinformatics, vol. 12, pp. 546-554, 2002. (Pubitemid 34521044)
14. A. Vickers, "Parametric versus Non-Parametric Statistics in the Analysis of Randomized Trials with Non-Normally Distributed Data, " BMC Medical Research Methodology, vol. 5, article 35, pp. 1-12, 2005.
15. S.Y. Kim, J.W. Lee, and I.S. Sohn, "Comparison of Various Statistical Methods for Identifying Differential Gene Expression in Replicated Microarray Data, " Statistical Methods in Medical Research, vol. 15, pp. 3-20, 2006. (Pubitemid 43231075)
16. J. Sreekumar, K.K. Jose, "Statistical Tests for Identification of Differentially Expressed Genes in cDNAMicroarray Experiments, " Indian J. Biotechnology, vol. 7, pp. 423-436, 2008.
17. C. Murie, O. Woody, A. Lee, and R. Nadon, "Comparison of Small n Statistical Tests of Differential Expression Applied to Micro-arrays, " BMC Bioinformatics, vol. 10, article 45, pp. 1-18, 2009.
18. X. Cui, J. Hwang, J. Qiu, N. Blades, and G. Churchill, "Improved Statistical Tests for Differential Gene Expression by Shrinking Variance Components Estimates, " Biostatistics, vol. 6, no. 1, pp. 59-75, 2005. (Pubitemid 41240370)
19. G. Smyth, "Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments, " Statistical Applications in Genetics and Molecular Biology, vol. 3, no. 1, article 3, 2004.
20. O. ElBakry, M. Ahmad, and M. Swamy, "Identification of Differentially Expressed Genes for Time-Course Microarray Data Based on Modified RM ANOVA, " IEEE/ACM Trans. Computational Biology and Bioinformatics, vol. 9, no. 2, pp. 451-466, Mar./Apr. 2012.
21. U. Maulik and A. Mukhopadhyay, "Towards Improving Fuzzy Clustering Using Support Vector Machine: Application to Gene Expression Data, " Pattern Recognition, vol. 42, no. 11, pp. 2744-2763, 2009.
22. J. Lu, G Get, EA. Miska, E. Alvarez-Saavedra, J. Lamb, D. Peck, A. Sweet-Cordero, B.L. Ebert, R.H. Mak, AA. Ferrando, J.R. Downing, T. Jacks, H.R. Horvitz, and T.R. Golub, "MicroRNA Expression Profiles Classify Human Cancers, " Nature, vol. 435, pp. 834-838, 2005. (Pubitemid 40839735)
23. R. Bourgon, R. Gentleman, and W. Huber, "Independent Filtering Increases Detection Power for High-Throughput Experiments, " Proc. Natl Academy Sciences USA, vol. 107, no. 21, pp. 9546-9551, 2010.
24. T. Jayalakshmi and A. Santhakumaran, "Statistical Normalization and Back Propagation for Classification, " Int'l J. Computer Theory and Eng., vol. 3, no. 1, pp. 1793-8201, 2011.
25. B.M. Bolstad, RA. Irizarry, M. Astrand, and T. Speed, "A Comparison of Normalization Methods for High Density Oligonucleotide Array Data Based on Variance and Bias, " Bioinformatics, vol. 19, no. 2, pp. 185-193, 2003. (Pubitemid 36181903)
26. W. Huber, A.V. Heydebreck, H. Sultmann, A. Poustka, and M. Vingron, "Variance Stabilization Applied to Microarray Data Calibration and to the Quantification of Differential Expression, " Bioinformatics, vol. 18, no. suppl. 1, pp. S96-S104, 2002. (Pubitemid 41185642)
27. T. Thadewald and H. Buning, "Jarque-Bera Test and Its Competitors for Testing Normality, " J. Applied Statistics, vol. 34, no. 1, pp. 87-105, 2007.
28. N. Razali and Y. Wah, "Power Comparisons of Shapiro-Wilk, Kolmogorov-Smirnov, Lilliefors and Anderson-Darling Tests, " J. Statistical Modeling and Analytics, vol. 2, no. 1, pp. 21-33, 2011.
29. V.G. Tusher, R. Tibshirani, and G Chu, "Significance Analysis of Microarrays Applied to the Ionizing Radiation Response, " Proc. Natl Academy Sciences USA, vol. 98, pp. 5116-5121, 2001. (Pubitemid 32397092)
30. S.E. Choe, M. Boutros, A.M. Michelson, GM. Church, and M.S. Halfon, "Preferred Analysis Methods for Affymetrix Genechips Revealed by a Wholly Defined Control Dataset, " Genome Biology, vol. 6, no. 2, article R16, pp. 1-16, 2005.
31. Y. Chen and H. Hu, "An Overlapping Cluster Algorithm to Provide Non-Exhaustive Clustering, " European J. Operational Research, vol. 173, pp. 762-780, 2006. (Pubitemid 43866325)
32. B. Welch, "The Significance of the Difference between Two Means when the Population Variances Are Unequal, " Biometrika, vol. 29, pp. 350-362, 1938.
33. A. McCluskey and A. Lalkhen, "Statistics IV: Interpreting the Results of Statistical Tests, " Continuing Education in Anaesthesia, Critical Care & Pain, vol. 7, no. 6, pp. 208-212, 2007.
34. K. Rothman, "Curbing Type I and Type II Errors, " European J. Epidemiology, vol. 25, no. 4, pp. 223-224, 2010.
35. J. Aldrich, "Correlations Genuine and Spurious in Pearson and Yule, " Statistical Science, vol. 10, no. 4, pp. 364-376, 1995.
36. M. Anderson, "Permutation Tests for Univariate or Multivariate Analysis of Variance and Regression, " Canadian J. Fisheries and Aquatic Science, vol. 58, pp. 626-639, 2001. (Pubitemid 32333566)
37. Wilcoxon, Frank, "Individual Comparisons by Ranking Methods, " Biometrics Bull, vol. 1, no. 6, pp. 80-83, 1945.
38. R. Walpole and R. Myers, Probability and Statistics for Engineers and Scientists, vol. 5, Macmillan, 1993.
39. OG Troyanskaya, M.E. Garber, P.O. Brown, D. Botstein, and R.B. Altman, "Nonparametric Methods for Identifying Differentially Expressed Genes in Microarray Data, " Bioinformatics, vol. 18, pp. 1454-1461, 2002. (Pubitemid 35414536)
40. I. Lonnstedt and T. Speed, "Replicated Microarray Data, " Statistical Sinica, vol. 12, pp. 31-46, 2002.
41. B. Efron, "Size, Power, and False Discovery Rates, " The Annals of Statistics, vol. 35, no. 4, pp. 1351-1377, 2006.
42. R.O. Rhein and K. Strimmer, "Accurate Ranking of Differentially Expressed Genes by a Distribution-Free Shrinkage Approach, " Statistical Applications in Genetics and Molecular Biology, vol. 6, article 9, 2007.
43. Kruskal, Wallis, "Use of Ranks in One-Criterion Variance Analysis, " J. Am. Statistical Assoc., vol. 47, no. 260, pp. 583-621, 1952.
44. A. Kolmogorov, "Sulla Determinazione Empirica di Una Legge di Distribuzione, " Giomale dell' Instituto Italiano degli attuari, vol. 4, pp. 83-91, 1933.
45. Y. Pawitan, S. Michiels, S. Koscielny, A. Gusnanto, and A. Ploner, "False Discovery Rate, Sensitivity and Sample Size for Microarray Studies, " Bioinformatics, vol. 21, pp. 3017-3024, 2005. (Pubitemid 40916427)
46. S. Dudoit, J. Shaffer, and J. Boldrick, "Multiple Hypothesis Testing in Microarray Experiments, " Statistical Science, vol. 18, no. 1, pp. 71-103, 2003. (Pubitemid 41461823)
47. J. Shaffer, "Multiple Hypothesis Testing: A Review, " Ann. Rev. Psychology, vol. 46, pp. 561-584, 1995.
48. S. Lise, C. Archambeau, M. Pontil, and D. Jones, "Prediction of Hot Spot Residues at Protein-Protein Interfaces by Combining Machine Learning and Energy-Based Methods, " BMC Bioinformat-ics, vol. 10, article 365, 2009.
49. E. Bonferroni, "Teoria statistica delle classi e calcolo delle proba-bilita, " Pubblicazioni del R Istituto Superiore di Scienze Economiche e Commerciali di Firenze, vol. 8, pp. 3-62, 1936.
50. S. Holm, "A Simple Sequential Rejective Multiple Test Procedure, " Scandinavian J. Statistics, vol. 6, pp. 65-70, 1979.
51. P. Westfall and S. Young, "Resampling-Based Multiple Testing, ". John Wiley & Sons, 1993.
52. Y. Benjamini and Y. Hochberg, "On the Adaptive Control of the False Discovery Rate in Multiple Testing with Independent Statistics, " J. Educational and Behavioral Statistics, vol. 25, pp. 60-83, 2000.
53. J. Storey, "A Direct Approach to False Discovery Rates, " J. Royal Statistical Soc. Series, B, vol. 64, pp. 479-498, 2002.
54. Y. Benjamini and Y. Hochberg, "Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing, " J. the Royal Statistical Soc., Series B, vol. 85, pp. 289-300, 1995.
55. B. Efron, "Robbins, Empirical Bayes, and Microarrays, " The Annals of Statistics, vol. 31, no. 2, pp. 366-378, 2003.
56. B. Efron, R. Tibshirani, J. Strey, and V. Tusher, "Empirical Bayes Analysis of a Microarray Experiment, " J. the Am. Statistical Assoc., vol. 96, pp. 1151-1160, 2001. (Pubitemid 33695570)
57. B. Efron, "Microarrays, Empirical Bayes and the Two-Groups Model, " Statistical Science, vol. 23, pp. 1-22, 2008.
58. Y. Benjamini and D. Yekutieli, "The Control of the False Discovery Rate in Multiple Testing under Dependency, " The Annals of Statistics, vol. 29, pp. 1165-1188, 2001. (Pubitemid 33575263)
59. J. Leek and J. Storey, "Capturing Heterogeneity in Gene Expression Studies by Surrogate Variable Analysis, " PLoS Genetics, vol. 3, no. 9, pp. 1724-1735, 2007. (Pubitemid 47510264)
60. J. Storey and T.R., "Statistical Significance for Genome-Wide Studies, " Proc. Nat'l Academy of Sciences USA, vol. 100, no. 16, pp. 9440-9445, 2003.
61. Y. Sun, N. Zhang, and A. Owen, "Multiple Hypothesis Testing Adjusted for Latent Variables, with an Application to the Agemap Gene Expression Data, " J. Applied Statistics, vol. 6, no. 4, pp. 1664-1688, 2013.
62. J. Leek and J. Storey, "A General Framework for Multiple Testing Dependence, " Proc. Nat'l Academy of Sciences USA, vol. 105, no. 48, pp. 18718-18723, 2008.
63. J. Leek, R. Scharpf, H. Bravo, D. Simcha, B. Langmead, W. Johnson, D. Geman, K. Baggerly, and R.A. Irizarry, "Tackling the Widespread and Critical Impact of Batch Effects in High-Throughput Data, " Nature Rev. Genetics, vol. 11, pp. 733-739, 2010.
64. A. Scherer, Batch Effects and Noise in Microarray Experiments: Sources and Solutions. John Wiley & Sons, 2009.
65. J. Lucas, C. Carvalho, Q. Wang, A. Bild, J. Nevins, and M. West, "Sparse Statistical Modelling in Gene Expression Genomics, " Bayesian Inference for Gene Expression and Proteomics, pp. 155-176, Cambridge Univ. Press, 2006.
66. J. Gagnon Bartsch and T. Speed, "Using Control Genes to Correct for Unwanted Variation in Microarray Data, " Biostatistics, vol. 13, no. 3, pp. 539-552, 2012.
67. H. Luo, "Generation of Non-Normal Data a Study of Fleishmans Power Method, " Working Paper, Dept. of Statistics Uppsala Univ., Mar. 2011.
68. W. Reinartz, R. Echambadi, A. Lee, and W. Chin, "Generating Non-Normal Data for Simulation of Structural Equation Models Using Mattsons Method, " Multivariate Behavioral Research, vol. 37, no. 2, pp. 227-244, 2002. (Pubitemid 36630365)
69. R. Simon, E. Korn, and L. McSchane, Design and Analysis of DNA Microarray Investigations, pp. 75-84, Springer, 2003.
70. J. Zou, S. Zas, and M. Aldea, "Expression Profiling Soybean Response to Pseudomonal Syringae Reveals New Defense-Related Genes and Rapid HR-Specific Downregulation of Photosynthesis, " Molecular Plant-Microbe Interactions, vol. 18, pp. 1161-1174, 2005. (Pubitemid 41484239)
71. S. S. Shapiro and M. B. Wilk, "An Analysis of Variance Test for Normality (Complete Samples), " Biometrika, vol. 52, no. 3/4, pp. 591-611, 1965.
72. B. Hertogh, B. Meulder, F. Berger, M. Pierre, E. Bareke, A. Gaigneaux, and E. Depiereux, "A Benchmark for Statistical Micro-array Data Analysis that Preserves Actual Biological and Technical Variance, " BMC Bioinformatics, vol. 11, article 17, pp. 1-14, 2010.
73. S. Dudoit, Y. Yang, T. Speed, and M. Callow, "Statistical Methods for Identifying Differentially Expressed Genes in Replicated cDNA Microarray Experiments, " Statistica Sinica, vol. 12, pp. 111-139, 2002.
74. H. Bar, J. Booth, E. Schifano, and M. Wells, "Laplace Approximated EM Microarray Analysis: An Empirical Bayes Approach for Comparative Microarray Experiments, " Statistical Science, vol. 25, no. 3, pp. 388-407, 2010.
75. P. Delmar, S. Robin, and J. Daudin, "Varmixt: Efficient Variance Modelling for the Differential Analysis of Replicated Gene Expression Data, " Bioinformatics, vol. 21, no. 4, pp. 502-508, 2005. (Pubitemid 40310237)
76. G. Wright and R. Simon, "A Random Variance Model for Detection of Differential Gene Expression in Small Microarray Experiments, " Bioinformatics, vol. 19, no. 18, pp. 2448-2455, 2003. (Pubitemid 38016644)
77. F. Jaffrezic, G. Marot, S. Degrelle, I. Hue, and J. Foulley, "A Structural Mixed Model for Variances in Differential Gene Expression Studies, " Genetics Research, vol. 89, pp. 19-25, 2007. (Pubitemid 46839606)
78. A. Sjogren, E. Kristiansson, M. Rudemo, and O. Nerman, "Weighted Analysis of General Microarray Experiments, " BMC Bioinformatics, vol. 8, pp. 387-401, 2007.
79. M. Jeanmougin, A. Reynies, L. Marisa, C. Paccard, G. Nuel, and M. Guedj, "Should We Abandon the t-Test in the Analysis of Gene Expression Microarray Data: A Comparison of Variance Modeling Strategies, " PLoS One, vol. 5, no. 9, p. e12336, 2010.
80. S. Bandyopadhyay and M. Bhattacharyya, "A Biologically Inspired Measure for Coexpression Analysis, " IEEE/ACM Trans. Computational Biology and Bioinformatics, vol. 8, no. 4, pp. 929-942, July/Aug. 2011.