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Abstract

The rapid increase in volume and complexity of biomedical data requires changes in research, communication, and clinical practices. This includes learning how to effectively integrate automated analysis with high–data density visualizations that clearly express complex phenomena. In this review, we summarize key principles and resources from data visualization research that help address this difficult challenge. We then survey how visualization is being used in a selection of emerging biomedical research areas, including three-dimensional genomics, single-cell RNA sequencing (RNA-seq), the protein structure universe, phosphoproteomics, augmented reality–assisted surgery, and metagenomics. While specific research areas need highly tailored visualizations, there are common challenges that can be addressed with general methods and strategies. Also common, however, are poor visualization practices. We outline ongoing initiatives aimed at improving visualization practices in biomedical research via better tools, peer-to-peer learning, and interdisciplinary collaboration with computer scientists, science communicators, and graphic designers. These changes are revolutionizing how we see and think about our data.

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2018-07-20
2024-04-19
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Literature Cited

  1. 1.  O'Donoghue SI, Gavin A-C, Gehlenborg N, Goodsell DS, Hériché J-K et al. 2010. Visualizing biological data—now and in the future. Nat. Methods 7:S2–4Nature Methods special issue on visualizing biological data, covering molecular biology, biomedical science, and evolution.
    [Google Scholar]
  2. 2.  Graber ML, Franklin N, Gordon R 2005. Diagnostic error in internal medicine. Arch. Intern. Med. 165:1493–99
    [Google Scholar]
  3. 3.  Pinto A, Brunese L 2010. Spectrum of diagnostic errors in radiology. World J. Radiol. 2:377–83
    [Google Scholar]
  4. 4.  Makary MA, Daniel M 2016. Medical error—the third leading cause of death in the US. BMJ 353:i2139
    [Google Scholar]
  5. 5.  Tufte ER 2009. The Visual Display of Quantitative Information Cheshire, CT: GraphicsInspirational, groundbreaking collection of historical and modern approaches to displaying quantitative data.
  6. 6.  Evanko D 2013. Data visualization: a view of every Points of View column. Methagora: A Blog from Nature Methods July 13. http://blogs.nature.com/methagora/2013/07/data-visualization-points-of-view.html Nature Methods regularly publishes 1-page articles focused on specific visualization issues faced by life scientists.
    [Google Scholar]
  7. 7.  Rougier NP, Droettboom M, Bourne PE 2014. Ten simple rules for better figures. PLOS Comput. Biol. 10:e1003833Concise, practical guide to principles and tools for creating scientific figures.
    [Google Scholar]
  8. 8.  Munzner T 2014. Visualization Analysis and Design Boca Raton, FL: CRCComprehensive overview of data visualization principles.
  9. 9.  Card SK, Mackinlay JD, Shneiderman B 1999. Readings in Information Visualization: Using Vision to Think San Francisco: Morgan KaufmannDefinitive, annotated guide to classic papers on information visualization.
  10. 10.  Borland D, Taylor MR II 2007. Rainbow color map (still) considered harmful. IEEE Comput. Graph. Appl. 27:14–17
    [Google Scholar]
  11. 11.  Craft M, Dobrenz B, Dornbush E, Hunter M, Morris J et al. 2015. An assessment of visualization tools for patient monitoring and medical decision making. Proc. Syst. Inf. Eng. Des. Symp., 24 Apr., Charlottesville, Va212–17 New York: IEEE
    [Google Scholar]
  12. 12.  Lewandowsky S, Spence I 1989. The perception of statistical graphs. Sociol. Methods Res. 18:200–42
    [Google Scholar]
  13. 13.  Koch K, McLean J, Segev R, Freed MA, Berry MJ 2nd et al. 2006. How much the eye tells the brain. Curr. Biol. 16:1428–34
    [Google Scholar]
  14. 14.  Healey CG, Enns JT 2012. Attention and visual memory in visualization and computer graphics. IEEE Trans. Vis. Comput. Graph. 18:1170–88
    [Google Scholar]
  15. 15.  Ball R, North C 2007. Realizing embodied interaction for visual analytics through large displays. Comput. Graph. 31:380–400
    [Google Scholar]
  16. 16.  Cleveland WS, Diaconis P, McGill R 1982. Variables on scatterplots look more highly correlated when the scales are increased. Science 216:1138–41
    [Google Scholar]
  17. 17.  Heer J, Kong N, Agrawala M 2009. Sizing the horizon: the effects of chart size and layering on the graphical perception of time series visualizations. Proc. Int. Conf. Human Factors Comput. Syst., Boston, Mass., 4–9 Apr1303–12 New York: Assoc. Comput. Mach.
    [Google Scholar]
  18. 18.  Inselberg A 1997. Multidimensional detective. Proc. IEEE Symp. Inf. Vis., Phoenix, Ariz., 21 Oct100–7 New York: IEEE
    [Google Scholar]
  19. 19.  Hegarty M 2011. The cognitive science of visual‐spatial displays: implications for design. Top. Cogn. Sci. 3:446–74
    [Google Scholar]
  20. 20.  Nielsen CB, Cantor M, Dubchak I, Gordon D, Wang T 2010. Visualizing genomes: techniques and challenges. Nat. Methods 7:S5–15
    [Google Scholar]
  21. 21.  Procter JB, Barton GJ, Thompson J, Westhof E, Creevey C, Letunic I 2010. Visualization of multiple alignments, phylogenies and gene family evolution. Nat. Methods 7:S16–25
    [Google Scholar]
  22. 22.  O'Donoghue SI, Goodsell DS, Frangakis AS, Jossinet F, Laskowski R et al. 2010. Visualization of macromolecular structures. Nat. Methods 7:S42–55
    [Google Scholar]
  23. 23.  Gehlenborg N, O'Donoghue SI, Baliga NS, Goesmann A, Hibbs MA et al. 2010. Visualization of omics data for systems biology. Nat. Methods 7:S56–68
    [Google Scholar]
  24. 24.  Walter T, Shattuck D, Baldock R, Bastin M, Carpenter AE et al. 2010. Visualization of image data from cells to organisms. Nat. Methods 7:S26–41
    [Google Scholar]
  25. 25.  Ware C 2004. Information Visualization: Perception for Design San Francisco: Morgan KaufmannOutline of key principles and methods for interactive display of visual information.
  26. 26.  Soegaard M, Rikke Friis D 2013. The Encyclopedia of Human-Computer Interaction Aarhus, Den: Interact. Des. Found 2nd ed. https://www.interaction-design.org/literature/book/the-encyclopedia-of-human-computer-interaction-2nd-ed
  27. 27.  Johnson GT, Hertig S 2014. A guide to the visual analysis and communication of biomolecular structural data. Nat. Rev. Mol. Cell Biol. 15:690–98Visual analysis and communication guide for biomolecular data; also relevant to other biomedical data.
    [Google Scholar]
  28. 28.  Inselberg A 2009. Parallel Coordinates: Visual Multidimensional Geometry and Its Applications New York: SpringerDefinitive guide to the theory and practice of using parallel coordinates to explore high-dimensional data.
  29. 29.  Levy SE, Myers RM 2016. Advancements in next-generation sequencing. Annu. Rev. Genom. Hum. Genet. 17:95–115
    [Google Scholar]
  30. 30.  Pavlopoulos GA, Malliarakis D, Papanikolaou N, Theodosiou T, Enright AJ, Iliopoulos I 2015. Visualizing genome and systems biology: technologies, tools, implementation techniques and trends, past, present and future. GigaScience 4:1–27
    [Google Scholar]
  31. 31.  Shneiderman B 1996. The eyes have it: a task by data type taxonomy for information visualizations. Proc. IEEE Symp. Vis. Lang., Boulder, Colo., 3–6 Sept.336–43 Los Alamitos, NM: IEEE Comput. Soc.
    [Google Scholar]
  32. 32.  Ernst J, Kellis M 2012. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9:215–16
    [Google Scholar]
  33. 33.  Pabinger S, Dander A, Fischer M, Snajder R, Sperk M et al. 2014. A survey of tools for variant analysis of next-generation genome sequencing data. Briefings Bioinform 15:256–78
    [Google Scholar]
  34. 34.  Schroeder MP, Gonzalez-Perez A, Lopez-Bigas N 2013. Visualizing multidimensional cancer genomics data. Genome Med 5:9
    [Google Scholar]
  35. 35.  Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93
    [Google Scholar]
  36. 36.  Serra F, Di Stefano M, Spill YG, Cuartero Y, Goodstadt M et al. 2015. Restraint-based three-dimensional modeling of genomes and genomic domains. FEBS Lett 589:2987–95
    [Google Scholar]
  37. 37.  Ay F, Noble WS 2015. Analysis methods for studying the 3D architecture of the genome. Genome Biol 16:183
    [Google Scholar]
  38. 38.  Durand NC, Robinson JT, Shamim MS, Machol I, Mesirov JP et al. 2016. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst 3:99–101
    [Google Scholar]
  39. 39.  Zhou X, Li D, Lowdon RF, Costello JF, Wang T 2014. methylC track: visual integration of single-base resolution DNA methylation data on the WashU EpiGenome Browser. Bioinformatics 30:2206–7
    [Google Scholar]
  40. 40.  Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R et al. 2009. Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–45
    [Google Scholar]
  41. 41.  Taberlay PC, Achinger-Kawecka J, Lun ATL, Buske FA, Sabir KS et al. 2016. Three-dimensional disorganisation of the cancer genome occurs coincident with long range genetic and epigenetic alterations. Genome Res 26:719–31
    [Google Scholar]
  42. 42.  Shalon D, Smith SJ, Brown PO 1996. A DNA microarray system for analyzing complex DNA samples using two-color fluorescent probe hybridization. Genome Res 6:639–45
    [Google Scholar]
  43. 43.  Wills QF, Livak KJ, Tipping AJ, Enver T, Goldson AJ et al. 2013. Single-cell gene expression analysis reveals genetic associations masked in whole-tissue experiments. Nat. Biotechnol. 31:748–52
    [Google Scholar]
  44. 44.  Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D et al. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320:1344–49
    [Google Scholar]
  45. 45.  Gierlinski M, Cole C, Schofield P, Schurch NJ, Sherstnev A et al. 2015. Statistical models for RNA-seq data derived from a two-condition 48-replicate experiment. Bioinformatics 31:3625–30
    [Google Scholar]
  46. 46.  Wilkinson L, Friendly M 2009. The history of the cluster heat map. Am. Stat. 63:179–84
    [Google Scholar]
  47. 47.  Wong B 2010. Points of view: color coding. Nat. Methods 7:573
    [Google Scholar]
  48. 48.  Pereverzeva M, Murray SO 2014. Luminance gradient configuration determines perceived lightness in a simple geometric illusion. Front. Hum. Neurosci. 8:977
    [Google Scholar]
  49. 49.  Trapnell C, Cacchiarelli D, Grimsby J, Pokharel P, Li S et al. 2014. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32:381–86
    [Google Scholar]
  50. 50.  Cao J, Packer JS, Ramani V, Cusanovich DA, Huynh C et al. 2017. Comprehensive single-cell transcriptional profiling of a multicellular organism by combinatorial indexing. Science 357:661–67
    [Google Scholar]
  51. 51.  Berman H, Henrick K, Nakamura H 2003. Announcing the worldwide Protein Data Bank. Nat. Struct. Biol. 10:980
    [Google Scholar]
  52. 52.  Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al. 2004. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605–12
    [Google Scholar]
  53. 53.  Kozlikova B, Krone M, Lindow N, Falk M, Baaden M et al. 2015. Visualization of biomolecular structures: state of the art. Proc. Eurograph. Conf. Vis., Cagliari, Ital., 25–29 May R Borgo, F Ganovelli, I Viola 61–82 Geneva: Eurograph. Assoc.
    [Google Scholar]
  54. 54.  Kendrew J, Dickerson R, Strandberg B, Hart R, Davies D et al. 1960. Structure of myoglobin: a three-dimensional Fourier synthesis at 2 Å. resolution. Nature 185:422–27
    [Google Scholar]
  55. 55.  Farrugia L 2012. WinGX and ORTEP for Windows: an update. J. Appl. Crystallogr. 45:849–54
    [Google Scholar]
  56. 56.  Chung JC, Harris MR, Brooks FP, Fuchs H, Kelley MT et al. 1989. Exploring virtual worlds with head-mounted displays. Proc. Non-Hologr. Three-Dimens. Vis. Disp. Technol., Los Angeles, Calif, 15–20 Jan SS Fisher, WE Robbins 15–20 Bellingham, Wash: SPIE
    [Google Scholar]
  57. 57.  Humphrey W, Dalke A, Schulten K 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33–38
    [Google Scholar]
  58. 58.  Gillet A, Sanner M, Stoffler D, Olson A 2005. Tangible interfaces for structural molecular biology. Structure 13:483–91
    [Google Scholar]
  59. 59.  Sabir KS, Stolte C, Tabor B, O'Donoghue SI 2013. The Molecular Control Toolkit: controlling 3D molecular graphics via gesture and voice. Proc. IEEE Symp. Biol. Data Vis., Atlanta, Ga., 13–14 Oct J Roerdink, J Kennedy 49–56 New York: IEEE
    [Google Scholar]
  60. 60.  Gillet A, Sanner M, Stoffler D, Goodsell D, Olson A 2004. Augmented reality with tangible auto-fabricated models for molecular biology applications. Proc. IEEE Visualization, Austin, Tex., 10–15 Oct H Rushmeier, G Turk, JJ van Wijk 245–41 New York: IEEE
    [Google Scholar]
  61. 61.  Heinrich J, Vuong J, Hammang CJ, Wu A, Rittenbruch M et al. 2016. Evaluating viewpoint entropy for ribbon representation of protein structure. Comput. Graph. Forum 35:181–90
    [Google Scholar]
  62. 62.  Lv Z, Tek A, Da Silva F, Empereur-Mot C, Chavent M, Baaden M 2013. Game on, science—how video game technology may help biologists tackle visualization challenges. PLOS ONE 8:e57990
    [Google Scholar]
  63. 63.  O'Donoghue SI, Sabir KS, Kalemanov M, Stolte C, Wellmann B et al. 2015. Aquaria: simplifying discovery and insight from protein structures. Nat. Methods 12:98–99
    [Google Scholar]
  64. 64.  Buja A, McDonald JA, Michalak J, Stuetzle W 1991. Interactive data visualization using focusing and linking. Proc. IEEE Conf. Vis., San Diego, Calif., 22–25 Oct GM Nielson, L Rosenblum 156–63 New York: IEEE
    [Google Scholar]
  65. 65.  Levitt M 2009. Nature of the protein universe. PNAS 106:11079–84
    [Google Scholar]
  66. 66.  Perdigão N, Heinrich J, Stolte C, Sabir KS, Buckley MJ et al. 2015. Unexpected features of the dark proteome. PNAS 112:15898–903
    [Google Scholar]
  67. 67.  Rysavy SJ, Beck DA, Daggett V 2014. Dynameomics: data‐driven methods and models for utilizing large‐scale protein structure repositories for improving fragment‐based loop prediction. Protein Sci 23:1584–95
    [Google Scholar]
  68. 68.  Bai X-C, McMullan G, Scheres SH 2015. How cryo-EM is revolutionizing structural biology. Trends Biochem. Sci. 40:49–57
    [Google Scholar]
  69. 69.  Johnson GT, Autin L, Al-Alusi M, Goodsell DS, Sanner MF, Olson AJ 2015. cellPACK: a virtual mesoscope to model and visualize structural systems biology. Nat. Methods 12:85–91
    [Google Scholar]
  70. 70.  Ghosh S, Matsuoka Y, Asai Y, Hsin K-Y, Kitano H 2011. Software for systems biology: from tools to integrated platforms. Nat. Rev. Genet. 12:821–32
    [Google Scholar]
  71. 71.  Kitano H 2002. Systems biology: a brief overview. Science 295:1662–64
    [Google Scholar]
  72. 72.  Schomburg D, Michal G 2012. Biochemical Pathways: An Atlas of Biochemistry and Molecular Biology Hoboken, NJ: Wiley
  73. 73.  Bader GD, Cary MP, Sander C 2006. Pathguide: a pathway resource list. Nucleic Acids Res 34:D504–6
    [Google Scholar]
  74. 74.  Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–504
    [Google Scholar]
  75. 75.  Bastian M, Heymann S, Jacomy M 2009. Gephi: an open source software for exploring and manipulating networks. Proc. Int. Conf. Weblogs Soc. Media, San Jose, Calif., 17–20 May361–62 Menlo Park, CA: Assoc. Adv. Artif. Intell.
    [Google Scholar]
  76. 76.  Kobourov SG 2013. Force-directed drawing algorithms. Handbook of Graph Drawing and Visualization R Tamassia 383–408 Boca Raton, FL: CRC
    [Google Scholar]
  77. 77.  Barsky A, Gardy JL, Hancock RE, Munzner T 2007. Cerebral: a Cytoscape plugin for layout of and interaction with biological networks using subcellular localization annotation. Bioinformatics 23:1040–42
    [Google Scholar]
  78. 78.  Holten D, Van Wijk JJ 2009. Force‐directed edge bundling for graph visualization. Comput. Graph. Forum 28:983–90
    [Google Scholar]
  79. 79.  Barsky A, Munzner T, Gardy J, Kincaid R 2008. Cerebral: visualizing multiple experimental conditions on a graph with biological context. IEEE Trans. Vis. Comput. Graph. 14:1253–60
    [Google Scholar]
  80. 80.  Zhou H-X, Rivas G, Minton AP 2008. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu. Rev. Biophys. 37:375–97
    [Google Scholar]
  81. 81.  Von Landesberger T, Kuijper A, Schreck T, Kohlhammer J, van Wijk JJ et al. 2011. Visual analysis of large graphs: state‐of‐the‐art and future research challenges. Presented at Comput. Graph. . Forum 30:1719–49
    [Google Scholar]
  82. 82.  Kwon O-H, Crnovrsanin T, Ma K-L 2017. What would a graph look like in this layout? A machine learning approach to large graph visualization. IEEE Trans. Vis. Comput. Graph 24:478–88
    [Google Scholar]
  83. 83.  Aebersold R, Mann M 2016. Mass-spectrometric exploration of proteome structure and function. Nature 537:347–55
    [Google Scholar]
  84. 84.  Humphrey SJ, Azimifar SB, Mann M 2015. High-throughput phosphoproteomics reveals in vivo insulin signaling dynamics. Nat. Biotechnol. 33:990–95
    [Google Scholar]
  85. 85.  Ma DK, Stolte C, Krycer JR, James DE, O'Donoghue SI 2015. SnapShot: insulin/IGF1 signaling. Cell 161:948.e1
    [Google Scholar]
  86. 86.  Burgess A, Vuong J, Rogers S, Malumbres M, O'Donoghue SI 2017. SnapShot: phosphoregulation of mitosis. Cell 169:1358.e1
    [Google Scholar]
  87. 87.  Sydor AM, Czymmek KJ, Puchner EM, Mennella V 2015. Super-resolution microscopy: from single molecules to supramolecular assemblies. Trends Cell Biol 25:730–48
    [Google Scholar]
  88. 88.  Reynaud EG, Peychl J, Huisken J, Tomancak P 2015. Guide to light-sheet microscopy for adventurous biologists. Nat. Methods 12:30–34
    [Google Scholar]
  89. 89.  Walter T, Shattuck DW, Baldock R, Bastin ME, Carpenter AE et al. 2010. Visualization of image data from cells to organisms. Nat. Methods 7:S26–41
    [Google Scholar]
  90. 90.  Rossner M, Yamada KM 2004. What's in a picture? The temptation of image manipulation. J. Cell Biol. 166:11–15
    [Google Scholar]
  91. 91.  Burel J-M, Besson S, Blackburn C, Carroll M, Ferguson RK et al. 2015. Publishing and sharing multi-dimensional image data with OMERO. Mamm. Genome 26:441–47
    [Google Scholar]
  92. 92.  Bernhardt S, Nicolau SA, Soler L, Doignon C 2017. The status of augmented reality in laparoscopic surgery as of 2016. Med. Image Anal. 37:66–90
    [Google Scholar]
  93. 93.  Maier-Hein L, Vedula SS, Speidel S, Navab N, Kikinis R et al. 2017. Surgical data science for next-generation interventions. Nat. Biomed. Eng. 1:691–96
    [Google Scholar]
  94. 94.  Ding W, Neher R 2014. panX Pangenome Vis. Tool. http://pangenome.tuebingen.mpg.de/
  95. 95.  Parks DH, Porter M, Churcher S, Wang S, Blouin C et al. 2009. GenGIS: a geospatial information system for genomic data. Genome Res 19:1896–904
    [Google Scholar]
  96. 96.  Argimon S, Abudahab K, Goater RJ, Fedosejev A, Bhai J et al. 2016. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb. Genom 2:e000093
    [Google Scholar]
  97. 97.  Paten B, Novak AM, Eizenga JM, Garrison E 2017. Genome graphs and the evolution of genome inference. Genome Res 27:665–76
    [Google Scholar]
  98. 98.  Wong B 2011. Points of view: color blindness. Nat. Methods 8:441
    [Google Scholar]
  99. 99.  Cromey DW 2010. Avoiding twisted pixels: ethical guidelines for the appropriate use and manipulation of scientific digital images. Sci. Eng. Ethics 16:639–67
    [Google Scholar]
  100. 100.  McGill G 2008. Molecular movies… Coming to a lecture near you. Cell 133:1127–32
    [Google Scholar]
  101. 101.  Iwasa JH 2015. Bringing macromolecular machinery to life using 3D animation. Curr. Opin. Struct. Biol. 31:84–88
    [Google Scholar]
  102. 102.  Van Noorden R, Maher B, Nuzzo R 2014. The top 100 papers. Nature 514:550–53
    [Google Scholar]
  103. 103.  Shneiderman B, Plaisant C, Cohen M, Jacobs S, Elmqvist N et al. 2018. Designing the User Interface: Strategies for Effective Human-Computer Interaction Boston: Pearson. , 6th ed..
  104. 104.  Sanyal J, Zhang S, Bhattacharya G, Amburn P, Moorhead R 2009. A user study to compare four uncertainty visualization methods for 1D and 2D datasets. IEEE Trans. Vis. Comput. Graph. 15:1209–18
    [Google Scholar]
  105. 105.  Callaway E 2016. The visualizations transforming biology. Nature 535:187–88
    [Google Scholar]
  106. 106.  Van Wijk JJ 2005. The value of visualization. Proc. IEEE Visualization, Minneap., Minn., 23–28 Oct.79–86 New York: IEEE
    [Google Scholar]
  107. 107.  Heer J, Bostock M 2010. Crowdsourcing graphical perception: using mechanical turk to assess visualization design. Proc. CHI Conf. Human Factors Comput. Syst., Atlanta, Ga., 10–15 Apr.203–12 New York: Assoc. Comput. Mach.Groundbreaking method using Amazon's Mechanical Turk crowdsourcing platform to evaluate the effectiveness of visual encoding.
    [Google Scholar]
  108. 108.  Blascheck T, Kurzhals K, Raschke M, Burch M, Weiskopf D, Ertl T 2014. State-of-the-art of visualization for eye tracking data. Proc. EuroVis Eurograph. Conf. Vis., Swansea, Wales, 9–13 June Geneva: Eurograph. Assoc.
    [Google Scholar]
  109. 109.  Anderson EW, Potter KC, Matzen LE, Shepherd JF, Preston GA, Silva CT 2011. A user study of visualization effectiveness using EEG and cognitive load. Comput. Graph. Forum 30:791–800
    [Google Scholar]
  110. 110.  Gehlenborg N, Wong B 2012. Mapping quantitative data to color: data structure informs choice of color maps. Nat. Methods 9:769–70
    [Google Scholar]
  111. 111.  Wong B 2011. Points of view: avoiding color. Nat. Methods 8:525
    [Google Scholar]
  112. 112.  Tufte ER 1990. Envisioning Information Chesire, CT: Graphics
  113. 113.  Gehlenborg N, Wong B 2012. Points of view: into the third dimension. Nat. Methods 9:851
    [Google Scholar]
  114. 114.  Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC 1990. Atomic structure of the actin:DNase I complex. Nature 347:37–44
    [Google Scholar]
  115. 115.  Hunter JD 2007. Matplotlib: a 2D graphics environment. Comput. Sci. Eng. 9:90–95
    [Google Scholar]
  116. 116.  Wickham H 2016. ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag
  117. 117.  Anscombe FJ 1973. Graphs in statistical analysis. Am. Statistician 27:17–21
    [Google Scholar]
  118. 118.  Matejka J, Fitzmaurice G 2017. Same stats, different graphs: generating datasets with varied appearance and identical statistics through simulated annealing. Proc. CHI Conf. Human Factors Comput. Syst., Denver, Colo., 6–11 May1290–94 New York: Assoc. Comput. Mach.
    [Google Scholar]
  119. 119.  Fry B 2008. Visualizing Data: Exploring and Explaining Data with the Processing Environment Sebastopol, CA: O'Reilly Media
  120. 120.  Moreland K 2016. Why we use bad color maps and what you can do about it. IS & T Int. Symp. Electron. Imaging, San Francisco, Calif., 14–18 Feb BE Rogowitz, TN Pappas, D de Ridder 1–6 6 Springfield, VA: Soc. Imaging Sci. Technol.
    [Google Scholar]
  121. 121.  Mackinlay JD 1986. Automating the design of graphical presentations of relational information. ACM Trans. Graph. 5:110–15
    [Google Scholar]
  122. 122.  Gehlenborg N, Wong B 2012. Points of view: heat maps. Nat. Methods 9:213
    [Google Scholar]
  123. 123.  Yates A, Akanni W, Amode MR, Barrell D, Billis K et al. 2015. Ensembl 2016. Nucleic Acids Res 44:D710–16
    [Google Scholar]
  124. 124.  Down TA, Piipari M, Hubbard TJ 2011. Dalliance: interactive genome viewing on the web. Bioinformatics 27:889–90
    [Google Scholar]
  125. 125.  Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1665–80
    [Google Scholar]
  126. 126.  van der Maaten L, Hinton G 2008. Visualizing data using t-SNE. J. Mach. Learn. Res. 9:2579–605
    [Google Scholar]
  127. 127.  Wattenberg M, Viégas F, Johnson I 2016. How to use t-SNE effectively. Distill Updated on 13 Oct. 2016. http://doi.org/10.23915/distill.00002
    [Crossref]
  128. 128.  Haghverdi L, Buettner F, Theis FJ 2015. Diffusion maps for high-dimensional single-cell analysis of differentiation data. Bioinformatics 31:2989–98
    [Google Scholar]
  129. 129.  Coifman RR, Lafon S, Lee AB, Maggioni M, Nadler B et al. 2005. Geometric diffusions as a tool for harmonic analysis and structure definition of data: diffusion maps. PNAS 102:7426–31
    [Google Scholar]
  130. 130.  McCarthy DJ, Campbell KR, Lun AT, Wills QF 2017. Scater: pre-processing, quality control, normalization and visualization of single-cell RNA-seq data in R. Bioinformatics 33:1179–86
    [Google Scholar]
  131. 131.  Camp JG, Sekine K, Gerber T, Loeffler-Wirth H, Binder H et al. 2017. Multilineage communication regulates human liver bud development from pluripotency. Nature 546:533–38
    [Google Scholar]
  132. 132.  Richardson JS, Richardson D, Tweedy N, Gernert K, Quinn T et al. 1992. Looking at proteins: representations, folding, packing, and design. Biophysical Society National Lecture, 1992. Biophys. J. 63:1185–1209
    [Google Scholar]
  133. 133.  Heinrich J, Kaur S, O'Donoghue SI 2015. Evaluating the effectiveness of color to convey uncertainty in macromolecular structures. Proc. IEEE Symp. Big Data Visual Anal., Hobart, Aust., 22–25 Sept U Engelke, J Heinrich, T Bednarz, K Klein, QV Nguyen 1–18 New York: IEEE
    [Google Scholar]
  134. 134.  Dosztanyi Z, Csizmok V, Tompa P, Simon I 2005. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21:3433–34
    [Google Scholar]
  135. 135.  Rose AS, Bradley AR, Valasatava Y, Duarte JM, Prlić A, Rose PW 2016. Web-based molecular graphics for large complexes. Proc. Int. Conf. Web3D Technol., 21st, Anaheim, Calif., 22–24 July185–86 New York: Assoc. Comput. Mech.
    [Google Scholar]
  136. 136.  Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B et al. 2013. Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497:643–46
    [Google Scholar]
  137. 137.  El Omari K, De Mesmaeker J Karia D, Ginn H, Bhattacharya S, Mancini EJ 2012. Structure of the DNA‐bound T‐box domain of human TBX1, a transcription factor associated with the DiGeorge syndrome. Proteins 80:655–60
    [Google Scholar]
  138. 138.  Isberg V, Mordalski S, Munk C, Rataj K, Harpsøe K et al. 2015. GPCRdb: an information system for G protein-coupled receptors. Nucleic Acids Res 44:D356–64
    [Google Scholar]
  139. 139.  Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P et al. 2001. Intrinsically disordered protein. J. Mol. Graph. Model. 19:26–59
    [Google Scholar]
  140. 140.  Humphrey SJ, Yang G, Yang P, Fazakerley DJ, Stöckli J et al. 2013. Dynamic adipocyte phosphoproteome reveals that Akt directly regulates mTORC2. Cell Metab 17:1009–20
    [Google Scholar]
  141. 141.  Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D et al. 2015. STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–52
    [Google Scholar]
  142. 142.  Lu CP, Hager GD, Mjolsness E 2000. Fast and globally convergent pose estimation from video images. IEEE Trans. Pattern Anal. Mach. Intell. 22:610–22
    [Google Scholar]
  143. 143.  Porter IM, McClelland SE, Khoudoli GA, Hunter CJ, Andersen JS et al. 2007. Bod1, a novel kinetochore protein required for chromosome biorientation. J. Cell Biol. 179:187–97
    [Google Scholar]
  144. 144.  Nolden M, Zelzer S, Seitel A, Wald D, Muller M et al. 2013. The Medical Imaging Interaction Toolkit: challenges and advances: 10 years of open-source development. Int. J. Comput. Assist. Radiol. Surg. 8:607–20
    [Google Scholar]
  145. 145.  Simpfendörfer T, Baumhauer M, Muller M, Gutt CN, Meinzer HP et al. 2011. Augmented reality visualization during laparoscopic radical prostatectomy. J. Endourol. 25:1841–45
    [Google Scholar]
  146. 146.  Han MV, Zmasek CM 2009. phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinform 10:356
    [Google Scholar]
  147. 147.  Darling ACE, Mau B, Blattner FR, Perna NT 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–403
    [Google Scholar]
  148. 148.  Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–36
    [Google Scholar]
  149. 149.  Rodgers P, Stapleton G, Chapman P 2015. Visualizing sets with linear diagrams. ACM Trans. Comput.-Hum. Interact. 22:27
    [Google Scholar]
  150. 150.  Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A et al. 2011. Moving pictures of the human microbiome. Genome Biol 12:R50
    [Google Scholar]
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