A community effort to assess and improve drug sensitivity prediction algorithms

James C. Costello, Laura M. Heiser, Elisabeth Georgii, Mehmet Gönen, Michael P. Menden, Nicholas J. Wang, Mukesh Bansal, Muhammad Ammad-Ud-Din, Petteri Hintsanen, Suleiman A. Khan, John Patrick Mpindi, Olli Kallioniemi, Antti Honkela, Tero Aittokallio, Krister Wennerberg, James J. Collins, Dan Gallahan, Dinah Singer, Julio Saez-Rodriguez, Samuel Kaski & 113 others Joe W. Gray, Gustavo Stolovitzky, Jean Paul Abbuehl, Jeffrey Allen, Russ B. Altman, Shawn Balcome, Alexis Battle, Andreas Bender, Bonnie Berger, Jonathan Bernard, Madhuchhanda Bhattacharjee, Krithika Bhuvaneshwar, Andrew A. Bieberich, Fred Boehm, Andrea Califano, Christina Chan, Beibei Chen, Ting Huei Chen, Jaejoon Choi, Luis Pedro Coelho, Thomas Cokelaer, James C. Collins, Chad J. Creighton, Jike Cui, Will Dampier, V. Jo Davisson, Bernard De Baets, Raamesh Deshpande, Barbara DiCamillo, Murat Dundar, Zhana Duren, Adam Ertel, Haoyang Fan, Hongbin Fang, Robinder Gauba, Assaf Gottlieb, Michael Grau, Yuriy Gusev, Min Jin Ha, Leng Han, Michael Harris, Nicholas Henderson, Hussein A. Hejase, Krisztian Homicsko, Jack P. Hou, Woochang Hwang, Adriaan P. IJzerman, Bilge Karacali, Sunduz Keles, Christina Kendziorski, Junho Kim, Min Kim, Youngchul Kim, David A. Knowles, Daphne Koller, Junehawk Lee, Jae K. Lee, Eelke B. Lenselink, Biao Li, Bin Li, Jun Li, Han Liang, Jian Ma, Subha Madhavan, Sean Mooney, Chad L. Myers, Michael A. Newton, John P. Overington, Ranadip Pal, Jian Peng, Richard Pestell, Robert J. Prill, Peng Qiu, Bartek Rajwa, Anguraj Sadanandam, Francesco Sambo, Hyunjin Shin, Jiuzhou Song, Lei Song, Arvind Sridhar, Michiel Stock, Wei Sun, Tram Ta, Mahlet Tadesse, Ming Tan, Hao Tang, Dan Theodorescu, Gianna Maria Toffolo, Aydin Tozeren, William Trepicchio, Nelle Varoquaux, Jean Philippe Vert, Willem Waegeman, Thomas Walter, Qian Wan, Difei Wang, Wen Wang, Yong Wang, Zhishi Wang, Joerg K. Wegner, Tongtong Wu, Tian Xia, Guanghua Xiao, Yang Xie, Yanxun Xu, Jichen Yang, Yuan Yuan, Shihua Zhang, Xiang Sun Zhang, Junfei Zhao, Chandler Zuo, Herman W T Van Vlijmen, Gerard J P Van Westen

Research output: Contribution to journalArticle

  • 164 Citations

Abstract

Predicting the best treatment strategy from genomic information is a core goal of precision medicine. Here we focus on predicting drug response based on a cohort of genomic, epigenomic and proteomic profiling data sets measured in human breast cancer cell lines. Through a collaborative effort between the National Cancer Institute (NCI) and the Dialogue on Reverse Engineering Assessment and Methods (DREAM) project, we analyzed a total of 44 drug sensitivity prediction algorithms. The top-performing approaches modeled nonlinear relationships and incorporated biological pathway information. We found that gene expression microarrays consistently provided the best predictive power of the individual profiling data sets; however, performance was increased by including multiple, independent data sets. We discuss the innovations underlying the top-performing methodology, Bayesian multitask MKL, and we provide detailed descriptions of all methods. This study establishes benchmarks for drug sensitivity prediction and identifies approaches that can be leveraged for the development of new methods.

LanguageEnglish (US)
Pages1202-1212
Number of pages11
JournalNature Biotechnology
Volume32
Issue number12
DOIs
StatePublished - Dec 1 2014

Profile

Reverse engineering
Microarrays
Gene expression
Pharmaceutical Preparations
Medicine
Benchmarking
Precision Medicine
National Cancer Institute (U.S.)
Innovation
Cells
Epigenomics
Proteomics
Breast Neoplasms
Gene Expression
Cell Line
Datasets
Therapeutics

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Biotechnology
  • Molecular Medicine
  • Bioengineering
  • Biomedical Engineering

Cite this

Costello, J. C., Heiser, L. M., Georgii, E., Gönen, M., Menden, M. P., Wang, N. J., ... Van Westen, G. J. P. (2014). A community effort to assess and improve drug sensitivity prediction algorithms. Nature Biotechnology, 32(12), 1202-1212. DOI: 10.1038/nbt.2877

A community effort to assess and improve drug sensitivity prediction algorithms. / Costello, James C.; Heiser, Laura M.; Georgii, Elisabeth; Gönen, Mehmet; Menden, Michael P.; Wang, Nicholas J.; Bansal, Mukesh; Ammad-Ud-Din, Muhammad; Hintsanen, Petteri; Khan, Suleiman A.; Mpindi, John Patrick; Kallioniemi, Olli; Honkela, Antti; Aittokallio, Tero; Wennerberg, Krister; Collins, James J.; Gallahan, Dan; Singer, Dinah; Saez-Rodriguez, Julio; Kaski, Samuel; Gray, Joe W.; Stolovitzky, Gustavo; Abbuehl, Jean Paul; Allen, Jeffrey; Altman, Russ B.; Balcome, Shawn; Battle, Alexis; Bender, Andreas; Berger, Bonnie; Bernard, Jonathan; Bhattacharjee, Madhuchhanda; Bhuvaneshwar, Krithika; Bieberich, Andrew A.; Boehm, Fred; Califano, Andrea; Chan, Christina; Chen, Beibei; Chen, Ting Huei; Choi, Jaejoon; Coelho, Luis Pedro; Cokelaer, Thomas; Collins, James C.; Creighton, Chad J.; Cui, Jike; Dampier, Will; Davisson, V. Jo; De Baets, Bernard; Deshpande, Raamesh; DiCamillo, Barbara; Dundar, Murat; Duren, Zhana; Ertel, Adam; Fan, Haoyang; Fang, Hongbin; Gauba, Robinder; Gottlieb, Assaf; Grau, Michael; Gusev, Yuriy; Ha, Min Jin; Han, Leng; Harris, Michael; Henderson, Nicholas; Hejase, Hussein A.; Homicsko, Krisztian; Hou, Jack P.; Hwang, Woochang; IJzerman, Adriaan P.; Karacali, Bilge; Keles, Sunduz; Kendziorski, Christina; Kim, Junho; Kim, Min; Kim, Youngchul; Knowles, David A.; Koller, Daphne; Lee, Junehawk; Lee, Jae K.; Lenselink, Eelke B.; Li, Biao; Li, Bin; Li, Jun; Liang, Han; Ma, Jian; Madhavan, Subha; Mooney, Sean; Myers, Chad L.; Newton, Michael A.; Overington, John P.; Pal, Ranadip; Peng, Jian; Pestell, Richard; Prill, Robert J.; Qiu, Peng; Rajwa, Bartek; Sadanandam, Anguraj; Sambo, Francesco; Shin, Hyunjin; Song, Jiuzhou; Song, Lei; Sridhar, Arvind; Stock, Michiel; Sun, Wei; Ta, Tram; Tadesse, Mahlet; Tan, Ming; Tang, Hao; Theodorescu, Dan; Toffolo, Gianna Maria; Tozeren, Aydin; Trepicchio, William; Varoquaux, Nelle; Vert, Jean Philippe; Waegeman, Willem; Walter, Thomas; Wan, Qian; Wang, Difei; Wang, Wen; Wang, Yong; Wang, Zhishi; Wegner, Joerg K.; Wu, Tongtong; Xia, Tian; Xiao, Guanghua; Xie, Yang; Xu, Yanxun; Yang, Jichen; Yuan, Yuan; Zhang, Shihua; Zhang, Xiang Sun; Zhao, Junfei; Zuo, Chandler; Van Vlijmen, Herman W T; Van Westen, Gerard J P.

In: Nature Biotechnology, Vol. 32, No. 12, 01.12.2014, p. 1202-1212.

Research output: Contribution to journalArticle

Costello, JC, Heiser, LM, Georgii, E, Gönen, M, Menden, MP, Wang, NJ, Bansal, M, Ammad-Ud-Din, M, Hintsanen, P, Khan, SA, Mpindi, JP, Kallioniemi, O, Honkela, A, Aittokallio, T, Wennerberg, K, Collins, JJ, Gallahan, D, Singer, D, Saez-Rodriguez, J, Kaski, S, Gray, JW, Stolovitzky, G, Abbuehl, JP, Allen, J, Altman, RB, Balcome, S, Battle, A, Bender, A, Berger, B, Bernard, J, Bhattacharjee, M, Bhuvaneshwar, K, Bieberich, AA, Boehm, F, Califano, A, Chan, C, Chen, B, Chen, TH, Choi, J, Coelho, LP, Cokelaer, T, Collins, JC, Creighton, CJ, Cui, J, Dampier, W, Davisson, VJ, De Baets, B, Deshpande, R, DiCamillo, B, Dundar, M, Duren, Z, Ertel, A, Fan, H, Fang, H, Gauba, R, Gottlieb, A, Grau, M, Gusev, Y, Ha, MJ, Han, L, Harris, M, Henderson, N, Hejase, HA, Homicsko, K, Hou, JP, Hwang, W, IJzerman, AP, Karacali, B, Keles, S, Kendziorski, C, Kim, J, Kim, M, Kim, Y, Knowles, DA, Koller, D, Lee, J, Lee, JK, Lenselink, EB, Li, B, Li, B, Li, J, Liang, H, Ma, J, Madhavan, S, Mooney, S, Myers, CL, Newton, MA, Overington, JP, Pal, R, Peng, J, Pestell, R, Prill, RJ, Qiu, P, Rajwa, B, Sadanandam, A, Sambo, F, Shin, H, Song, J, Song, L, Sridhar, A, Stock, M, Sun, W, Ta, T, Tadesse, M, Tan, M, Tang, H, Theodorescu, D, Toffolo, GM, Tozeren, A, Trepicchio, W, Varoquaux, N, Vert, JP, Waegeman, W, Walter, T, Wan, Q, Wang, D, Wang, W, Wang, Y, Wang, Z, Wegner, JK, Wu, T, Xia, T, Xiao, G, Xie, Y, Xu, Y, Yang, J, Yuan, Y, Zhang, S, Zhang, XS, Zhao, J, Zuo, C, Van Vlijmen, HWT & Van Westen, GJP 2014, 'A community effort to assess and improve drug sensitivity prediction algorithms' Nature Biotechnology, vol. 32, no. 12, pp. 1202-1212. DOI: 10.1038/nbt.2877
Costello JC, Heiser LM, Georgii E, Gönen M, Menden MP, Wang NJ et al. A community effort to assess and improve drug sensitivity prediction algorithms. Nature Biotechnology. 2014 Dec 1;32(12):1202-1212. Available from, DOI: 10.1038/nbt.2877
Costello, James C. ; Heiser, Laura M. ; Georgii, Elisabeth ; Gönen, Mehmet ; Menden, Michael P. ; Wang, Nicholas J. ; Bansal, Mukesh ; Ammad-Ud-Din, Muhammad ; Hintsanen, Petteri ; Khan, Suleiman A. ; Mpindi, John Patrick ; Kallioniemi, Olli ; Honkela, Antti ; Aittokallio, Tero ; Wennerberg, Krister ; Collins, James J. ; Gallahan, Dan ; Singer, Dinah ; Saez-Rodriguez, Julio ; Kaski, Samuel ; Gray, Joe W. ; Stolovitzky, Gustavo ; Abbuehl, Jean Paul ; Allen, Jeffrey ; Altman, Russ B. ; Balcome, Shawn ; Battle, Alexis ; Bender, Andreas ; Berger, Bonnie ; Bernard, Jonathan ; Bhattacharjee, Madhuchhanda ; Bhuvaneshwar, Krithika ; Bieberich, Andrew A. ; Boehm, Fred ; Califano, Andrea ; Chan, Christina ; Chen, Beibei ; Chen, Ting Huei ; Choi, Jaejoon ; Coelho, Luis Pedro ; Cokelaer, Thomas ; Collins, James C. ; Creighton, Chad J. ; Cui, Jike ; Dampier, Will ; Davisson, V. Jo ; De Baets, Bernard ; Deshpande, Raamesh ; DiCamillo, Barbara ; Dundar, Murat ; Duren, Zhana ; Ertel, Adam ; Fan, Haoyang ; Fang, Hongbin ; Gauba, Robinder ; Gottlieb, Assaf ; Grau, Michael ; Gusev, Yuriy ; Ha, Min Jin ; Han, Leng ; Harris, Michael ; Henderson, Nicholas ; Hejase, Hussein A. ; Homicsko, Krisztian ; Hou, Jack P. ; Hwang, Woochang ; IJzerman, Adriaan P. ; Karacali, Bilge ; Keles, Sunduz ; Kendziorski, Christina ; Kim, Junho ; Kim, Min ; Kim, Youngchul ; Knowles, David A. ; Koller, Daphne ; Lee, Junehawk ; Lee, Jae K. ; Lenselink, Eelke B. ; Li, Biao ; Li, Bin ; Li, Jun ; Liang, Han ; Ma, Jian ; Madhavan, Subha ; Mooney, Sean ; Myers, Chad L. ; Newton, Michael A. ; Overington, John P. ; Pal, Ranadip ; Peng, Jian ; Pestell, Richard ; Prill, Robert J. ; Qiu, Peng ; Rajwa, Bartek ; Sadanandam, Anguraj ; Sambo, Francesco ; Shin, Hyunjin ; Song, Jiuzhou ; Song, Lei ; Sridhar, Arvind ; Stock, Michiel ; Sun, Wei ; Ta, Tram ; Tadesse, Mahlet ; Tan, Ming ; Tang, Hao ; Theodorescu, Dan ; Toffolo, Gianna Maria ; Tozeren, Aydin ; Trepicchio, William ; Varoquaux, Nelle ; Vert, Jean Philippe ; Waegeman, Willem ; Walter, Thomas ; Wan, Qian ; Wang, Difei ; Wang, Wen ; Wang, Yong ; Wang, Zhishi ; Wegner, Joerg K. ; Wu, Tongtong ; Xia, Tian ; Xiao, Guanghua ; Xie, Yang ; Xu, Yanxun ; Yang, Jichen ; Yuan, Yuan ; Zhang, Shihua ; Zhang, Xiang Sun ; Zhao, Junfei ; Zuo, Chandler ; Van Vlijmen, Herman W T ; Van Westen, Gerard J P. / A community effort to assess and improve drug sensitivity prediction algorithms. In: Nature Biotechnology. 2014 ; Vol. 32, No. 12. pp. 1202-1212
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abstract = "Predicting the best treatment strategy from genomic information is a core goal of precision medicine. Here we focus on predicting drug response based on a cohort of genomic, epigenomic and proteomic profiling data sets measured in human breast cancer cell lines. Through a collaborative effort between the National Cancer Institute (NCI) and the Dialogue on Reverse Engineering Assessment and Methods (DREAM) project, we analyzed a total of 44 drug sensitivity prediction algorithms. The top-performing approaches modeled nonlinear relationships and incorporated biological pathway information. We found that gene expression microarrays consistently provided the best predictive power of the individual profiling data sets; however, performance was increased by including multiple, independent data sets. We discuss the innovations underlying the top-performing methodology, Bayesian multitask MKL, and we provide detailed descriptions of all methods. This study establishes benchmarks for drug sensitivity prediction and identifies approaches that can be leveraged for the development of new methods.",
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AU - Stolovitzky,Gustavo

AU - Abbuehl,Jean Paul

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AU - Bhuvaneshwar,Krithika

AU - Bieberich,Andrew A.

AU - Boehm,Fred

AU - Califano,Andrea

AU - Chan,Christina

AU - Chen,Beibei

AU - Chen,Ting Huei

AU - Choi,Jaejoon

AU - Coelho,Luis Pedro

AU - Cokelaer,Thomas

AU - Collins,James C.

AU - Creighton,Chad J.

AU - Cui,Jike

AU - Dampier,Will

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AU - De Baets,Bernard

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AU - Peng,Jian

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AU - Prill,Robert J.

AU - Qiu,Peng

AU - Rajwa,Bartek

AU - Sadanandam,Anguraj

AU - Sambo,Francesco

AU - Shin,Hyunjin

AU - Song,Jiuzhou

AU - Song,Lei

AU - Sridhar,Arvind

AU - Stock,Michiel

AU - Sun,Wei

AU - Ta,Tram

AU - Tadesse,Mahlet

AU - Tan,Ming

AU - Tang,Hao

AU - Theodorescu,Dan

AU - Toffolo,Gianna Maria

AU - Tozeren,Aydin

AU - Trepicchio,William

AU - Varoquaux,Nelle

AU - Vert,Jean Philippe

AU - Waegeman,Willem

AU - Walter,Thomas

AU - Wan,Qian

AU - Wang,Difei

AU - Wang,Wen

AU - Wang,Yong

AU - Wang,Zhishi

AU - Wegner,Joerg K.

AU - Wu,Tongtong

AU - Xia,Tian

AU - Xiao,Guanghua

AU - Xie,Yang

AU - Xu,Yanxun

AU - Yang,Jichen

AU - Yuan,Yuan

AU - Zhang,Shihua

AU - Zhang,Xiang Sun

AU - Zhao,Junfei

AU - Zuo,Chandler

AU - Van Vlijmen,Herman W T

AU - Van Westen,Gerard J P

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