Light microscopy applications in systems biology: Opportunities and challenges

Cell Communication and Signaling

Volumn 11, Issue 1, 2013, Pages

  Antony, Paul Michel Aloyse ^a   Trefois, Christophe ^a   Stojanovic, Aleksandar ^a   Baumuratov, Aidos Sagatovich ^a   Kozak, Karol ^b,c  

^a UNIVERSITY OF LUXEMBOURG   (Luxembourg)

^b ETH ZURICH   (Switzerland)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Features; Image analysis; Machine learning; Microscopy; Segmentation; Systems biology

Indexed keywords

ACTIN; MESSENGER RNA; PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RNA;

ACCESS TO INFORMATION; BIOINFORMATICS; CAENORHABDITIS ELEGANS; CELL FUNCTION; COMPUTER PROGRAM; CYTOLOGY; DATA PROCESSING; DNA BARCODING; FACTUAL DATABASE; HIGH THROUGHPUT SCREENING; HUMAN; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; INVASIVE PROCEDURE; LOCOMOTION; MACHINE LEARNING; MICROSCOPY; MOLECULAR BIOLOGY; MOLECULAR IMAGING; MOLECULAR MECHANICS; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROCESS DEVELOPMENT; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REVIEW; SYSTEMS BIOLOGY; WORKFLOW; YEAST; ZEBRA FISH;

EID: 84876275534     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-11-24     Document Type: Review

References (173)

1. Fluorescence microscopy today. Yuste R, Nat Methods 2005 2 902 904 10.1038/nmeth1205-902 16299474
2. Imaging in systems biology. Megason SG, Fraser SE, Cell 2007 130 784 795 10.1016/j.cell.2007.08.031 17803903
3. Optical sectioning microscopy. Conchello J, Lichtman JW, Nat Methods 2005 2 920 931 10.1038/nmeth815 16299477
4. Live cell imaging and systems biology. Sung M-H, McNally JG, Wiley Interdiscip Rev Syst Biol Med 2010 3 167 182 20730797
5. Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination. Planchon TA, Gao L, Milkie DE, Davidson MW, Galbraith JA, Galbraith CG, Betzig E, Nat Methods 2011 8 417 423 10.1038/nmeth.1586 21378978
6. Light sheet microscopy for real-time developmental biology. Weber M, Huisken J, Curr Opin Genet Dev 2011 21 566 572 10.1016/j.gde.2011.09.009 21963791
7. Noninvasive Imaging beyond the Diffraction Limit of 3D Dynamics in Thickly Fluorescent Specimens. Gao L, Shao L, Higgins CD, Poulton JS, Peifer M, Davidson MW, Wu X, Goldstein B, Betzig E, Cell 2012 151 1370 1385 10.1016/j.cell.2012.10.008 23217717
8. Interferometric resolution improvement for confocal microscopes. Wicker K, Heintzmann R, Opt Express 2007 15 12206 12216 10.1364/OE.15.012206 19547588
9. Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Abrahamsson S, Chen J, Hajj B, Stallinga S, Katsov AY, Wisniewski J, Mizuguchi G, Soule P, Mueller F, Darzacq CD, Darzacq X, Wu C, Bargmann CI, Agard DA, Dahan M, Gustafsson MGL, Nat Methods 2013 10 60 63 23223154
10. Fluorescent proteins for live cell imaging: opportunities, limitations, and challenges. Wiedenmann J, Oswald F, Nienhaus GU, IUBMB Life 2009 61 1029 1042 10.1002/iub.256 19859977
11. The fluorescent protein palette: tools for cellular imaging. Day RN, Davidson MW, Chem Soc Rev 2009 38 2887 2921 10.1039/b901966a 19771335
12. Near-infrared fluorescent proteins. Shcherbo D, Shemiakina II, Ryabova AV, Luker KE, Schmidt BT, Souslova EA, Gorodnicheva TV, Strukova L, Shidlovskiy KM, Britanova OV, Zaraisky AG, Lukyanov KA, Loschenov VB, Luker GD, Chudakov DM, Nat Methods 2010 7 827 829 10.1038/nmeth.1501 20818379
13. Use of quantum dots for live cell imaging. Jaiswal JK, Goldman ER, Mattoussi H, Simon SM, Nat Methods 2004 1 73 78 10.1038/nmeth1004-73 16138413
14. Extending microscopic resolution with single-molecule imaging and active control. Thompson MA, Lew MD, Moerner WE, Annu Rev Biophys 2012 41 321 342 10.1146/annurev-biophys-050511-102250 22577822
15. Advances in the chemistry of small molecule fluorescent probes. Wysocki LM, Lavis LD, Curr Opin Chem Biol 2011 15 752 759 10.1016/j.cbpa.2011.10.013 22078994
16. Switchable fluorophores for protein labeling in living cells. Lukinavičius G, Johnsson K, Curr Opin Chem Biol 2011 15 768 774 10.1016/j.cbpa.2011.10.015 22079663
17. Optical molecular imaging for systems biology: from molecule to organism. Du W, Wang Y, Luo Q, Liu B-F, Anal Bioanal Chem 2006 386 444 457 10.1007/s00216-006-0541-z 16850295
18. F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Yasuda R, Noji H, Kinosita K, Yoshida M, Cell 1998 93 1117 1124 10.1016/S0092-8674(00)81456-7 9657145
19. Simple dark-field microscopy with nanometer spatial precision and microsecond temporal resolution. Ueno H, Nishikawa S, Iino R, Tabata KV, Sakakihara S, Yanagida T, Noji H, Biophys J 2010 98 2014 2023 10.1016/j.bpj.2010.01.011 20441766
20. Rotation and structure of FoF1-ATP synthase. Okuno D, Iino R, Noji H, J Biochem 2011 149 655 664 10.1093/jb/mvr049 21524994
21. Visualizing cell structure and function with point-localization superresolution imaging. Sengupta P, Van Engelenburg S, Lippincott-Schwartz J, Dev Cell 2012 23 1092 1102 10.1016/j.devcel.2012.09.022 23237943
22. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Lubeck E, Cai L, Nat Methods 2012 9 743 748 10.1038/nmeth.2069 22660740
23. From systems biology to systems biomedicine. Antony PMA, Balling R, Vlassis N, Curr Opin Biotechnol 2012 23 604 608 10.1016/j.copbio.2011.11.009 22119097
24. Nerve activity recordings in routine human intestinal biopsies. Cirillo C, Tack J, Vanden Berghe P, Gut 2012 65 227 235
25. Nanoscopy in a living mouse brain. Berning S, Willig KI, Steffens H, Dibaj P, Hell SW, Science 2012 335 551 10.1126/science.1215369 22301313
26. Genetically encoded probes for optical imaging of brain electrical activity. Perron A, Akemann W, Mutoh H, Knöpfel T, Prog Brain Res 2012 196 63 77 22341321
27. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Akemann W, Mutoh H, Perron A, Rossier J, Knöpfel T, Nat Methods 2010 7 643 649 10.1038/nmeth.1479 20622860
28. Assay development guidelines for image-based high content screening, high content analysis and high content imaging. Buchser W, Assay Guidance Manual Bethesda, MD: National Center for Advancing Translational Sciences (NCATS) 2012 1 69
29. Automated microscopy for high-content RNAi screening. Conrad C, Gerlich DW, J Cell Biol 2010 188 453 461 10.1083/jcb.200910105 20176920
30. Digital autofocus methods for automated microscopy. Shen F, Hodgson L, Hahn K, Methods Enzymol 2006 414 620 632 17110214
31. Spatio-temporal protein dynamics in single living cells. Ankers JM, Spiller DG, White MR, Harper CV, Curr Opin Biotechnol 2008 19 375 380 10.1016/j.copbio.2008.07.001 18662777
32. Clustering phenotype populations by genome-wide RNAi and multiparametric imaging. Fuchs F, Pau G, Kranz D, Sklyar O, Budjan C, Steinbrink S, Horn T, Pedal A, Huber W, Boutros M, Mol Syst Biol 2010 6 370 20531400
33. Cell Cognition: time-resolved phenotype annotation in high-throughput live cell imaging. Held M, Schmitz MHA, Fischer B, Walter T, Neumann B, Olma MH, Peter M, Ellenberg J, Gerlich DW, Nat Methods 2010 7 747 754 10.1038/nmeth.1486 20693996
34. An image analysis toolbox for high-throughput C. elegans assays. Wählby C, Kamentsky L, Liu ZH, Riklin-Raviv T, Conery AL, O'Rourke EJ, Sokolnicki KL, Visvikis O, Ljosa V, Irazoqui JE, Golland P, Ruvkun G, Ausubel FM, Carpenter AE, Nat methods 2012 9 714 716 10.1038/nmeth.1984 22522656
35. A 3D digital atlas of C. elegans and its application to single-cell analyses. Long F, Peng H, Liu X, Kim SK, Myers E, Nat Methods 2009 6 667 672 10.1038/nmeth.1366 19684595
36. ViBE-Z: a framework for 3D virtual colocalization analysis in zebrafish larval brains. Ronneberger O, Liu K, Rath M, Rueβ D, Mueller T, Skibbe H, Drayer B, Schmidt T, Filippi A, Nitschke R, Brox T, Burkhardt H, Driever W, Nat Methods 2012 9 735 742 10.1038/nmeth.2076 22706672
37. Miniaturized integration of a fluorescence microscope. Ghosh KK, Burns LD, Cocker ED, Nimmerjahn A, Ziv Y, Gamal AE, Schnitzer MJ, Nat Methods 2011 8 871 878 10.1038/nmeth.1694 21909102
38. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R, Sofroniew MV, Gastroenterology 2007 132 1344 1358 10.1053/j.gastro.2007.01.051 17408650
39. Imaging Translation in Single Cells Using Fluorescent Microscopy. Chao JA, Yoon YJ, Singer RH, Cold Spring Harb Perspect Biol 2012 4 1 2
40. Heterogeneity in the physiological states and pharmacological responses of differentiating 3 T3-L1 preadipocytes. Loo L-H, Lin H-J, Singh DK, Lyons KM, Altschuler SJ, Wu LF, J Cell Biol 2009 187 375 384 10.1083/jcb.200904140 19948481
41. Monitoring the dynamics of primary T cell activation and differentiation using long term live cell imaging in microwell arrays. Zaretsky I, Polonsky M, Shifrut E, Reich-Zeliger S, Antebi Y, Aidelberg G, Waysbort N, Friedman N, Lab Chip 2012 12 5007 5015 10.1039/c2lc40808b 23072772
42. In vitro maturation of dopaminergic neurons derived from mouse embryonic stem cells: implications for transplantation. Watmuff B, Pouton CW, Haynes JM, PLoS One 2012 7 31999 10.1371/journal.pone.0031999 22384125
43. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Tay S, Hughey JJ, Lee TK, Lipniacki T, Quake SR, Covert MW, Nature 2010 466 267 271 10.1038/nature09145 20581820
44. High-throughput, single-cell NF-κB dynamics. Lee TK, Covert MW, Curr Opin Genet Dev 2010 20 677 683 10.1016/j.gde.2010.08.005 20846851
45. FRET microscopy in the living cell: different approaches, strengths and weaknesses. Padilla-Parra S, Tramier M, Bioessays 2012 34 369 376 10.1002/bies.201100086 22415767
46. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Gilbert PM, Havenstrite KL, Magnusson KEG, Sacco A, Leonardi NA, Kraft P, Nguyen NK, Thrun S, Lutolf MP, Blau HM, Science 2010 329 1078 1081 10.1126/science.1191035 20647425
47. A batch algorithm using iterative application of the Viterbi algorithm to track cells and construct cell lineages. Magnusson K, Jaldén J, Biomed Imaging (ISBI) 2012 2012 382 385
48. Automatic identification and clustering of chromosome phenotypes in a genome wide RNAi screen by time-lapse imaging. Walter T, Held M, Neumann B, Hériché J-K, Conrad C, Pepperkok R, Ellenberg J, J Struct Biol 2010 170 1 9 10.1016/j.jsb.2009.10.004 19854275
49. Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Neumann B, Walter T, Hériché J, Bulkescher J, Erfle H, Conrad C, Rogers P, Poser I, Held M, Liebel U, Cetin C, Sieckmann F, Pau G, Kabbe R, Wünsche A, Satagopam V, Schmitz MHA, Chapuis C, Gerlich DW, Schneider R, Eils R, Huber W, Peters J, Hyman AA, Durbin R, Pepperkok R, Ellenberg J, Nature 2010 464 721 727 10.1038/nature08869 20360735
50. Micropilot: automation of fluorescence microscopy-based imaging for systems biology. Conrad C, Wünsche A, Tan TH, Bulkescher J, Sieckmann F, Verissimo F, Edelstein A, Walter T, Liebel U, Pepperkok R, Ellenberg J, Nat Methods 2011 8 246 249 10.1038/nmeth.1558 21258339
51. Functional profiling of the Saccharomyces cerevisiae genome. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Véronneau S, Dow S, Lucau-Danila A, Anderson K, André B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian K-D, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Güldener U, Hegemann JH, Hempel S, Herman Z, Nature 2002 418 387 391 10.1038/nature00935 12140549
52. A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Ni L, Snyder M, Mol Biol Cell 2001 12 2147 2170 11452010
53. Image processing and classification algorithm for yeast cell morphology in a microfluidic chip. Yang Yu B, Elbuken C, Ren CL, Huissoon JP, J Biomedical Optics 2011 16 1 9
54. Life span of individual yeast cells. Mortimer RK, JOHNSTON JR, Nature 1959 183 1751 1752 10.1038/1831751a0 13666896
55. Measuring replicative life span in the budding yeast. Steffen KK, Kennedy BK, Kaeberlein M, J Vis Exp 2009 1 5
56. Whole lifespan microscopic observation of budding yeast aging through a microfluidic dissection platform. Lee SS, Avalos Vizcarra I, Huberts DHEW, Lee LP, Heinemann M, Proc Natl Acad Sci U S A 2012 109 4916 4920 10.1073/pnas.1113505109 22421136
57. Single-cell quantification of molecules and rates using open-source microscope-based cytometry. Gordon A, Colman-Lerner A, Chin TE, Benjamin KR, Yu RC, Brent R, Nat Methods 2007 4 175 181 10.1038/nmeth1008 17237792
58. High-dimensional and large-scale phenotyping of yeast mutants. Ohya Y, Sese J, Yukawa M, Sano F, Nakatani Y, Saito TL, Saka A, Fukuda T, Ishihara S, Oka S, Suzuki G, Watanabe M, Hirata A, Ohtani M, Sawai H, Fraysse N, Latgé J-P, François JM, Aebi M, Tanaka S, Muramatsu S, Araki H, Sonoike K, Nogami S, Morishita S, Proc Natl Acad Sci U S A 2005 102 19015 19020 10.1073/pnas.0509436102 16365294
59. Development of image processing program for yeast cell morphology. Ohtani M, Saka A, Sano F, Ohya Y, Morishita S, J Bioinform Comput Biol 2004 1 695 709 10.1142/S0219720004000363 15290760
60. SCMD: Saccharomyces cerevisiae Morphological Database. Saito TL, Ohtani M, Sawai H, Sano F, Saka A, Watanabe D, Yukawa M, Ohya Y, Morishita S, Nucleic Acids Res 2004 32 319 D322 10.1093/nar/gkh113 14681423
61. High-content, image-based screening for drug targets in yeast. Ohnuki S, Oka S, Nogami S, Ohya Y, PLoS One 2010 5 10177 10.1371/journal.pone.0010177 20418956
62. Caenorhabditis elegans: a versatile platform for drug discovery. Artal-Sanz M, De Jong L, Tavernarakis N, Biotechnol J 2006 1 1405 1418 10.1002/biot.200600176 17109493
63. Modeling molecular and cellular aspects of human disease using the nematode Caenorhabditis elegans. Silverman GA, Luke CJ, Bhatia SR, Long OS, Vetica AC, Perlmutter DH, Pak SC, Pediatr Res 2009 65 10 18 10.1203/PDR. 0b013e31819009b0 18852689
64. From gene to identified neuron to behaviour in Caenorhabditis elegans. Rankin CH, Nat Rev Genet 2002 3 622 630 12154385
65. The art and design of genetic screens: caenorhabditis elegans. Jorgensen EM, Mango SE, Nat Rev Genet 2002 3 356 369 10.1038/nrg794 11988761
66. Automated high-content live animal drug screening using C. elegans expressing the aggregation prone serpin α1-antitrypsin Z. Gosai SJ, Kwak JH, Luke CJ, Long OS, King DE, Kovatch KJ, Johnston PA, Shun TY, Lazo JS, Perlmutter DH, Silverman GA, Pak SC, PloS one 2010 5 15460 10.1371/journal.pone. 0015460 21103396
67. The stress of misfolded proteins: C. elegans models for neurodegenerative disease and aging. Brignull HR, Morley JF, Morimoto RI, Adv Exp Med Biol 2007 594 167 189 10.1007/978-0-387-39975-1-15 17205684
68. Autonomous screening of C. elegans identifies genes implicated in synaptogenesis. Crane MM, Stirman JN, Ou C-Y, Kurshan PT, Rehg JM, Shen K, Lu H, Nat Methods 2012 9 977 980 10.1038/nmeth.2141 22902935
69. Using machine vision to analyze and classify Caenorhabditis elegans behavioral phenotypes quantitatively. Baek J-H, Cosman P, Feng Z, Silver J, Schafer WR, J Neurosci Methods 2002 118 9 21 10.1016/S0165-0270(02)00117-6 12191753
70. An automated system for measuring parameters of nematode sinusoidal movement. Cronin CJ, Mendel JE, Mukhtar S, Kim Y-M, Stirbl RC, Bruck J, Sternberg PW, BMC Genet 2005 6 5 15698479
71. An imaging system for standardized quantitative analysis of C. elegans behavior. Feng Z, Cronin CJ, Wittig JH, Sternberg PW, Schafer WR, BMC bioinformatics 2004 5 115 10.1186/1471-2105-5-115 15331023
72. Automatic tracking, feature extraction and classification of C elegans phenotypes. Geng W, Cosman P, Berry CC, Feng Z, Schafer WR, IEEE Trans Biomed Eng 2004 51 1811 1820 10.1109/TBME.2004.831532 15490828
73. Machine vision based detection of omega bends and reversals in C. elegans. Huang K-M, Cosman P, Schafer WR, J Neurosci Methods 2006 158 323 336 10.1016/j.jneumeth.2006.06.007 16839609
74. Automated detection and analysis of foraging behavior in Caenorhabditis elegans. Huang K-M, Cosman P, Schafer WR, J Neurosci Methods 2008 171 153 164 10.1016/j.jneumeth.2008.01.027 18342950
75. The Parallel Worm Tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. Ramot D, Johnson BE, Berry TL, Carnell L, Goodman MB, PLoS One 2008 3 2208 10.1371/journal.pone.0002208 18493300
76. Strategies for automated analysis of C. elegans locomotion. Buckingham SD, Sattelle DB, Invert Neurosci 2008 8 121 131 10.1007/s10158-008-0077-3 18688666
77. Computer-driven automatic identification of locomotion states in Caenorhabditis elegans. Hoshi K, Shingai R, J Neurosci Methods 2006 157 355 363 10.1016/j.jneumeth.2006.05.002 16750860
78. Nemo: a computational tool for analyzing nematode locomotion. Tsibidis GD, Tavernarakis N, BMC Neurosci 2007 8 86 10.1186/1471-2202-8-86 17941975
79. Fast, automated measurement of nematode swimming (thrashing) without morphometry. Buckingham SD, Sattelle DB, BMC Neurosci 2009 10 84 10.1186/1471-2202-10-84 19619274
80. A novel computational approach for simultaneous tracking and feature extraction of C. elegans populations in fluid environments. Tsechpenakis G, Bianchi L, Metaxas D, Driscoll M, IEEE Trans Biomed Eng 2008 55 1539 1549 18440900
81. Multi-environment model estimation for motility analysis of Caenorhabditis elegans. Sznitman R, Gupta M, Hager GD, Arratia PE, Sznitman J, PLoS One 2010 5 11631 10.1371/journal.pone.0011631 20661478
82. A high-resolution C. elegans essential gene network based on phenotypic profiling of a complex tissue. Green RA, Kao H-L, Audhya A, Arur S, Mayers JR, Fridolfsson HN, Schulman M, Schloissnig S, Niessen S, Laband K, Wang S, Starr DA, Hyman AA, Schedl T, Desai A, Piano F, Gunsalus KC, Oegema K, Cell 2011 145 470 482 10.1016/j.cell.2011.03.037 21529718
83. Straightening Caenorhabditis elegans images. Peng H, Long F, Liu X, Kim SK, Myers EW, Bioinformatics 2008 24 234 242 10.1093/bioinformatics/btm569 18025002
84. Image formation by linear and nonlinear digital scanned light-sheet fluorescence microscopy with Gaussian and Bessel beam profiles. Olarte OE, Licea-Rodriguez J, Palero JA, Gualda EJ, Artigas D, Mayer J, Swoger J, Sharpe J, Rocha-Mendoza I, Rangel-Rojo R, Loza-Alvarez P, Biomed Opt express 2012 3 1492 1505 10.1364/BOE.3.001492 22808423
85. The art and design of genetic screens: zebrafish. Patton EE, Zon LI, Nat Rev Genet 2001 2 956 966 10.1038/35103567 11733748
86. In vivo drug discovery in the zebrafish. Zon LI, Peterson RT, Nat Rev Drug Discov 2005 4 35 44 10.1038/nrd1606 15688071
87. High-throughput in vivo vertebrate screening. Pardo-Martin C, Chang T-Y, Koo BK, Gilleland CL, Wasserman SC, Yanik MF, Nat Methods 2010 7 634 636 10.1038/nmeth.1481 20639868
88. Small molecule screening in zebrafish: an in vivo approach to identifying new chemical tools and drug leads. Taylor KL, Grant NJ, Temperley ND, Patton EE, Cell Commun signal 2010 8 11 10.1186/1478-811X-8-11 20540792
89. Stages of embryonic development of the zebrafish. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, Dev Dyn 1995 203 253 310 10.1002/aja.1002030302 8589427
90. Automated feature detection and imaging for high-resolution screening of zebrafish embryos. Peravali R, Gehrig J, Giselbrecht S, Lütjohann DS, Hadzhiev Y, Müller F, Liebel U, Biotechniques 2011 50 319 324 21548893
91. Multitissue array review: a chronological description of tissue array techniques, applications and procedures. Eguíluz C, Viguera E, Millán L, Pérez J, Pathol Res Pract 2006 202 561 568 10.1016/j.prp.2006.04.003 16782284
92. Robust automated tumour segmentation on histological and immunohistochemical tissue images. Wang C-W, Fennell D, Paul I, Savage K, Hamilton P, PLoS One 2011 6 15818 10.1371/journal.pone.0015818 21386898
93. Ilastik: Interactive learning and segmentation toolkit. Sommer C, Straehle C, Kothe U, Hamprecht FA, IEEE Int Symp Biomed Imaging 2011 2011 230 233
94. A systematic approach to the development of fluorescent contrast agents for optical imaging of mouse cancer models. Kovar JL, Simpson MA, Schutz-Geschwender A, Olive DM, Anal Biochem 2007 367 1 12 10.1016/j.ab.2007.04. 011 17521598
95. Animal models: inside the minds of mice and men. Baker M, Nature 2011 475 123 128 10.1038/475123a 21734709
96. Computerized video analysis of social interactions in mice. De Chaumont F, Coura RD-S, Serreau P, Cressant A, Chabout J, Granon S, Olivo-Marin J-C, Nat Methods 2012 9 410 417 10.1038/nmeth.1924 22388289
97. Live-cell imaging of dendritic spines by STED microscopy. Nägerl UV, Willig KI, Hein B, Hell SW, Bonhoeffer T, Proc Natl Acad Sci U S A 2008 105 18982 18987 10.1073/pnas.0810028105 19028874
98. STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Urban NT, Willig KI, Hell SW, Nägerl UV, Biophys J 2011 101 1277 1284 10.1016/j.bpj.2011.07.027 21889466
99. Intravital microscopy: A practical guide on imaging intracellular structures in live animals. Masedunskas A, Milberg O, Porat-Shliom N, Sramkova M, Wigand T, Amornphimoltham P, Weigert R, Bioarchitecture 2012 2 143 157 10.4161/bioa.21758
100. Intravital microscopy: new insights into cellular interactions. Gavins FN, Curr Opin Pharmacol 2012 12 601 607 10.1016/j.coph.2012.08.006 22981814
101. Chronic in vivo imaging in the mouse spinal cord using an implanted chamber. Farrar MJ, Bernstein IM, Schlafer DH, Cleland TA, Fetcho JR, Schaffer CB, Nat Methods 2012 9 297 302 10.1038/nmeth.1856 22266542
102. In vivo microendoscopy of the hippocampus. Barretto RPJ, Schnitzer MJ, Cold Spring Harb Protoc 2012 2012 1092 1099 23028072
103. In Vivo Optical Microendoscopy for Imaging Cells Lying Deep within Live Tissue. Barretto RPJ, Schnitzer MJ, Cold Spring Harb Protoc 2012 2012 1029 1034 23028071
104. An infrared fluorescent protein for deeper imaging. Lecoq J, Schnitzer MJ, Nat Biotechnol 2011 29 715 716 10.1038/nbt.1941 21822247
105. Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy. Barretto RPJ, Ko TH, Jung JC, Wang TJ, Capps G, Waters AC, Ziv Y, Attardo A, Recht L, Schnitzer MJ, Nat Med 2011 17 223 228 10.1038/nm.2292 21240263
106. In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical systems scanning mirror. Piyawattanametha W, Cocker ED, Burns LD, Barretto RP, Jung JC, Ra H, Solgaard O, Schnitzer MJ, Opt Lett 2009 34 2309 2311 10.1364/OL.34.002309 19649080
107. In vivo fluorescence imaging with high-resolution microlenses. Barretto RPJ, Messerschmidt B, Schnitzer MJ, Nat Methods 2009 6 511 512 10.1038/nmeth.1339 19525959
108. High-speed, miniaturized fluorescence microscopy in freely moving mice. Flusberg BA, Nimmerjahn A, Cocker ED, Mukamel EA, Barretto RPJ, Ko TH, Burns LD, Jung JC, Schnitzer MJ, Nat Methods 2008 5 935 938 10.1038/nmeth.1256 18836457
109. Why bioimage informatics matters. Myers G, Nat Methods 2012 9 659 660 10.1038/nmeth.2024 22743769
110. Open source bioimage informatics for cell biology. Swedlow JR, Eliceiri KW, Trends Cell Biol 2009 19 656 660 10.1016/j.tcb.2009.08.007 19833518
111. Bioimage informatics: a new area of engineering biology. Peng H, Bioinformatics 2008 24 1827 1836 10.1093/bioinformatics/btn346 18603566
112. Biological imaging software tools. Eliceiri KW, Berthold MR, Goldberg IG, Ibáñez L, Manjunath BS, Martone ME, Murphy RF, Peng H, Plant AL, Roysam B, Stuurmann N, Swedlow JR, Tomancak P, Carpenter AE, Nat Methods 2012 9 697 710 10.1038/nmeth.2084 22743775
113. Davies ER, Computer and Machine Vision: Theory, Algorithms, Practicalities New York, NY: Academic Press 2012 1 912
114. Visualization of image data from cells to organisms. Walter T, Shattuck DW, Baldock R, Bastin ME, Carpenter AE, Duce S, Ellenberg J, Fraser A, Hamilton N, Pieper S, Ragan MA, Schneider JE, Tomancak P, Hériché J-K, Nat methods 2010 7 26 S41 10.1038/nmeth.1431 20195255
115. 1Click1View: Interactive Visualization Methodology for RNAi Cell-Based Microscopic Screening. Zwolinski L, Kozak M, Kozak K, BioMed Res Int 2013 2013 1 11
116. A high-level 3D visualization API for Java and ImageJ. Schmid B, Schindelin J, Cardona A, Longair M, Heisenberg M, BMC Bioinformatics 2010 11 274 10.1186/1471-2105-11-274 20492697
117. ACME: Automated Cell Morphology Extractor for Comprehensive Reconstruction of Cell Membranes. Mosaliganti KR, Noche RR, Xiong F, Swinburne IA, Megason SG, PLoS Comput Biol 2012 8 1002780 10.1371/journal.pcbi.1002780 23236265
118. Machine Learning Improves the Precision and Robustness of High-Content Screens: Using Nonlinear Multiparametric Methods to Analyze Screening Results. Horvath P, Wild T, Kutay U, Csucs G, J Biomol Screen 2011 16 1059 1067 10.1177/1087057111414878 21807964
119. A platform for bioimage analysis and management. Kvilekval K, Fedorov D, Obara B, Singh A, Manjunath BS: B, Bioinformatics (Oxford, England) 2010 26 544 552 10.1093/bioinformatics/btp699
120. The iPlant Collaborative: Cyberinfrastructure for Plant Biology. Goff SA, Vaughn M, McKay S, Lyons E, Stapleton AE, Gessler D, Matasci N, Wang L, Hanlon M, Lenards A, Muir A, Merchant N, Lowry S, Mock S, Helmke M, Kubach A, Narro M, Hopkins N, Micklos D, Hilgert U, Gonzales M, Jordan C, Skidmore E, Dooley R, Cazes J, McLay R, Lu Z, Pasternak S, Koesterke L, Piel WH, Front plant sci 2011 2 34 22645531
121. Metadata matters: access to image data in the real world. Linkert M, Rueden CT, Allan C, Burel J-M, Moore W, Patterson A, Loranger B, Moore J, Neves C, Macdonald D, Tarkowska A, Sticco C, Hill E, Rossner M, Eliceiri KW, Swedlow JR, J Cell Biol 2010 189 777 782 10.1083/jcb.201004104 20513764
122. BioImageXD: an open, general-purpose and high-throughput image-processing platform. Kankaanpää P, Paavolainen L, Tiitta S, Karjalainen M, Päivärinne J, Nieminen J, Marjomäki V, Heino J, White DJ, Nat Methods 2012 9 683 689 10.1038/nmeth.2047 22743773
123. CellClassifier: supervised learning of cellular phenotypes. Rämö P, Sacher R, Snijder B, Begemann B, Pelkmans L, Bioinformatics 2009 25 3028 3030 10.1093/bioinformatics/btp524 19729371
124. Analysis of cell-based RNAi screens. Boutros M, Brás LP, Huber W, Genome Biol 2006 7 66 10.1186/gb-2006-7-7-r66 16869968
125. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM, Genome biology 2006 7 100 10.1186/gb-2006-7-10-r100 17076895
126. Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software. Kamentsky L, Jones TR, Fraser A, Bray M-A, Logan DJ, Madden KL, Ljosa V, Rueden C, Eliceiri KW, Carpenter AE, Bioinformatics 2011 27 1179 1180 10.1093/bioinformatics/btr095 21349861
127. Scoring diverse cellular morphologies in image-based screens with iterative feedback and machine learning. Jones TR, Carpenter AE, Lamprecht MR, Moffat J, Silver SJ, Grenier JK, Castoreno AB, Eggert US, Root DE, Golland P, Sabatini DM, Proc Natl Acad Sci U S A 2009 106 1826 1831 10.1073/pnas.0808843106 19188593
128. CellProfiler Analyst: data exploration and analysis software for complex image-based screens. Jones TR, Kang IH, Wheeler DB, Lindquist RA, Papallo A, Sabatini DM, Golland P, Carpenter AE, BMC bioinformatics 2008 9 482 10.1186/1471-2105-9-482 19014601
129. EBImage - an R package for image processing with applications to cellular phenotypes. Pau G, Fuchs F, Sklyar O, Boutros M, Huber W, Bioinformatics 2010 26 979 981 10.1093/bioinformatics/btq046 20338898
130. Associative image analysis: a method for automated quantification of 3D multi-parameter images of brain tissue. Bjornsson CS, Lin G, Al-Kofahi Y, Narayanaswamy A, Smith KL, Shain W, Roysam B, J Neurosci Methods 2008 170 165 178 10.1016/j.jneumeth.2007.12.024 18294697
131. Fiji: an open-source platform for biological-image analysis. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A, Nat Methods 2012 9 676 682 10.1038/nmeth.2019 22743772
132. Visualizing and clustering high throughput sub-cellular localization imaging. Hamilton NA, Teasdale RD, BMC Bioinformatics 2008 9 81 10.1186/1471-2105-9-81 18241353
133. Statistical and visual differentiation of subcellular imaging. Hamilton NA, Wang JTH, Kerr MC, Teasdale RD, BMC Bioinformatics 2009 10 94 10.1186/1471-2105-10-94 19302715
134. A new open-source community image processing software. De Chaumont F, Dallongeville S, Olivo-Marin J-C ICY, 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro Chicago, IL: IEEE 2011 234 237
135. Icy: an open bioimage informatics platform for extended reproducible research. De Chaumont F, Dallongeville S, Chenouard N, Hervé N, Pop S, Provoost T, Meas-Yedid V, Pankajakshan P, Lecomte T, Le Montagner Y, Lagache T, Dufour A, Olivo-Marin J-C, Nat Methods 2012 9 690 696 10.1038/nmeth.2075 22743774
136. Automated detection and segmentation of synaptic contacts in nearly isotropic serial electron microscopy images. Kreshuk A, Straehle CN, Sommer C, Koethe U, Cantoni M, Knott G, Hamprecht FA, PLoS One 2011 6 24899 10.1371/journal.pone.0024899 22031814
137. Image Processing with ImageJ. Abràmoff MD, Hospitals I, Magalhães PJ, Abràmoff M, Biophotonics Int 2004 11 36 42
138. NIH Image to ImageJ: 25 years of image analysis. Schneider CA, Rasband WS, Eliceiri KW, Nat Methods 2012 9 671 675 10.1038/nmeth.2089 22930834
139. Collins T, ImageJ for microscopy. BioTechniques 2007 43 25 S30
140. ImgLib2 - generic image processing in Java. Pietzsch T, Preibisch S, Tomancák P, Saalfeld S, Bioinformatics 2012 28 3009 3011 10.1093/bioinformatics/bts543 22962343
141. Schroeder W, The ITK Software Guide Second Edition Updated for ITK version 2. 4 2005
142. KNIME-the Konstanz information miner. Berthold MR, Cebron N, Dill F, Gabriel TR, Kötter T, Meinl T, Ohl P, Thiel K, Wiswedel B, ACM SIGKDD Explorations Newsletter 2009 11 26 10.1145/1656274.1656280
143. Feature selection based on mutual information: criteria of max-dependency, max-relevance, and min-redundancy. Peng H, Long F, Ding C, IEEE Trans Pattern Anal Mach Intell 2005 27 1226 1238 16119262
144. The Open Microscopy Environment (OME) Data Model and XML file: open tools for informatics and quantitative analysis in biological imaging. Goldberg IG, Allan C, Burel J-M, Creager D, Falconi A, Hochheiser H, Johnston J, Mellen J, Sorger PK, Swedlow JR, Genome Biol 2005 6 47 10.1186/gb-2005-6-5-r47 15892875
145. Bioimage informatics for experimental biology. Swedlow JR, Goldberg IG, Eliceiri KW, Annu Rev Biophys 2009 38 327 346 10.1146/annurev.biophys.050708. 133641 19416072
146. OMERO: flexible, model-driven data management for experimental biology. Allan C, Burel J, Moore J, Blackburn C, Linkert M, Loynton S, Macdonald D, Moore WJ, Neves C, Patterson A, Porter M, Tarkowska A, Loranger B, Avondo J, Lagerstedt I, Lianas L, Leo S, Hands K, Hay RT, Patwardhan A, Best C, Kleywegt GJ, Zanetti G, Swedlow JR, Nat Methods 2012 9 245 253 10.1038/nmeth.1896 22373911
147. Open tools for storage and management of quantitative image data. Moore J, Allan C, Burel J-M, Loranger B, MacDonald D, Monk J, Swedlow JR, Methods Cell Biol 2008 85 555 570 18155479
148. OMERO.searcher: content-based image search for microscope images. Cho BH, Cao-Berg I, Bakal JA, Murphy RF, Nat Methods 2012 9 633 634 10.1038/nmeth.2086 22743762
149. openBIS: a flexible framework for managing and analyzing complex data in biology research. Bauch A, Adamczyk I, Buczek P, Elmer F-J, Enimanev K, Glyzewski P, Kohler M, Pylak T, Quandt A, Ramakrishnan C, Beisel C, Malmström L, Aebersold R, Rinn B, BMC Bioinformatics 2011 12 468 10.1186/1471-2105-12-468 22151573
150. Modular multiple sensors information management for computer-integrated surgery. Vaccarella A, Enquobahrie A, Ferrigno G, De ME, Int J Med Robot 2012 8 253 260 10.1002/rcs.1412 22407822
151. Object type recognition for automated analysis of protein subcellular location. Zhao T, Velliste M, Boland MV, Murphy RF, IEEE Trans Image Process 2005 14 1351 1359 16190470
152. Determining the distribution of probes between different subcellular locations through automated unmixing of subcellular patterns. Peng T, Bonamy GMC, Glory-Afshar E, Rines DR, Chanda SK, Murphy RF, Proc Natl Acad Sci U S A 2010 107 2944 2949 10.1073/pnas.0912090107 20133616
153. PhenoRipper: software for rapidly profiling microscopy images. Rajaram S, Pavie B, Wu LF, Altschuler SJ, Nat Methods 2012 9 635 637 10.1038/nmeth.2097 22743764
154. V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets. Peng H, Ruan Z, Long F, Simpson JH, Myers EW, Nat Biotechnol 2010 28 348 353 10.1038/nbt.1612 20231818
155. VANO: a volume-object image annotation system. Peng H, Long F, Myers EW, Bioinformatics 2009 25 695 697 10.1093/bioinformatics/btp046 19189978
156. VisBio: a computational tool for visualization of multidimensional biological image data. Rueden C, Eliceiri KW, White JG, Traffic 2004 5 411 417 10.1111/j.1600-0854.2004.00189.x 15117315
157. Schroeder W, Martin KW, LORENSEN B, The Visualization Toolkit An Object-Oriented Approach to 3-D Graphics N.J.: Prentice Hall PTR-Upper Saddle River 1996 1 826
158. Interactive Volume Rendering on Standard PC Graphics Hardware Using Multi-Textures and Multi-Stage Rasterization. Engel K, Bauer M, Greiner G, Ertl T, Group CG, Group IS, ACM SIGGRAPH/Eurographics Workshop on Graphics Hardware 2001 2000 109 118
159. WND-CHARM: Multi-purpose image classification using compound image transforms. Orlov N, Shamir L, Macura T, Johnston J, Eckley DM, Goldberg IG, Pattern Recognit Lett 2008 29 1684 1693 10.1016/j.patrec.2008.04.013 18958301
160. Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. Gustafsson MGL, Proc Natl Acad Sci U S A 2005 102 13081 13086 10.1073/pnas.0406877102 16141335
161. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Huang B, Wang W, Bates M, Zhuang X, Science 2008 319 810 813 10.1126/science.1153529 18174397
162. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Hess ST, Girirajan TPK, Mason MD, Biophys J 2006 91 4258 4272 10.1529/biophysj.106.091116 16980368
163. Fast, three-dimensional super-resolution imaging of live cells. Jones SA, Shim S-H, He J, Zhuang X, Nat Methods 2011 8 499 508 10.1038/nmeth.1605 21552254
164. Digital scanned laser light-sheet fluorescence microscopy (DSLM) of zebrafish and Drosophila embryonic development. Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EHK, Cold Spring Harb Protoc 2011 2011 1235 1243 21969622
165. TeraStitcher-A Tool for Fast Automatic 3D-Stitching of Teravoxel-Sized Microscopy Images. Bria A, Iannello G, BMC Bioinformatics 2012 13 316 10.1186/1471-2105-13-316 23181553
166. Current challenges in open-source bioimage informatics. Cardona A, Tomancak P, Nat Methods 2012 9 661 665 10.1038/nmeth.2082 22743770
167. A call for bioimaging software usability. Carpenter AE, Kamentsky L, Eliceiri KW, Nat Methods 2012 9 666 670 10.1038/nmeth.2073 22743771
168. Computer control of microscopes using μManager. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N, Current protocols in molecular biology, Ausubel FM, 2010 Chapter 14:Unit14.20
169. Pattern recognition software and techniques for biological image analysis. Shamir L, Delaney JD, Orlov N, Eckley DM, Goldberg IG, PLoS Comput Biol 2010 6 1000974 10.1371/journal.pcbi.1000974 21124870
170. Image-based multivariate profiling of drug responses from single cells. Loo L-H, Wu LF, Altschuler SJ, Nat Methods 2007 4 445 453 17401369
171. Quantitative image analysis reveals distinct structural transitions during aging in Caenorhabditis elegans tissues. Johnston J, Iser WB, Chow DK, Goldberg IG, Wolkow CA, PLoS One 2008 3 2821 10.1371/journal.pone.0002821 18665238
172. Multidimensional drug profiling by automated microscopy. Perlman ZE, Slack MD, Feng Y, Mitchison TJ, Wu LF, Altschuler SJ, Science 2004 306 1194 1198 10.1126/science.1100709 15539606
173. Phaedra, a protocol-driven system for analysis and validation of high-content imaging and flow cytometry. Cornelissen F, Cik M, Gustin E, J Biomol Screen 2012 17 496 506 10.1177/1087057111432885 22233649