Application and progress of highcontent imaging in molecular biology.
drug discovery
gene
high content imaging
microbiology
Journal
Biotechnology journal
ISSN: 1860-7314
Titre abrégé: Biotechnol J
Pays: Germany
ID NLM: 101265833
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
revised:
03
08
2023
received:
19
04
2023
accepted:
22
08
2023
pubmed:
28
8
2023
medline:
28
8
2023
entrez:
28
8
2023
Statut:
ppublish
Résumé
Humans have adopted many different methods to explore matter imaging, among which high content imaging (HCI) could conduct automated imaging analysis of cells while maintaining its structural and functional integrity. Meanwhile, as one of the most important research tools for diagnosing human diseases, HCI is widely used in the frontier of medical research, and its future application has attracted researchers' great interests. Here, the meaning of HCI was briefly explained, the history of optical imaging and the birth of HCI were described, and the experimental methods of HCI were described. Furthermore, the directions of the application of HCI were highlighted in five aspects: protein localization changes, gene identification, chemical and genetic analysis, microbiology, and drug discovery. Most importantly, some challenges and future directions of HCI were discussed, and the application and optimization of HCI were expected to be further explored.
Identifiants
pubmed: 37639283
doi: 10.1002/biot.202300170
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2300170Subventions
Organisme : Public Welfare Technology Application Research Program of Huzhou
ID : 2021GZB10
Organisme : Zhejiang Medical and Health Technology Project
ID : 2023KY313
Informations de copyright
© 2023 Wiley-VCH GmbH.
Références
Orchard, G., & Nation, B. (2014). Cell structure & function. Oxford University Press.
Mansuripur, M. (2002). Classical optics and its applications. Cambridge University Press.
Köhler, A. (1893). Ein neues Beleuchtungsverfahren für mikrophotographische Zwecke. Zeitschrift fur wissenschaftliche Mikroskopie, Published online, 433-440.
Zernike, F. (1942). Phase contrast, a new method for the microscopic observation of transparent objects. Physica, 9, 686-698.
Nomarski, G., & Weill, A. R. (1955). Application à la métallographie des méthodes interférentielles à deux ondes polarisées. La Revue de Métallurgie, 52(2), 121-134.
Paine, T. F. (1963). Gram staining without the clock. New England Journal of Medicine, 268, 941.
Stokes, G. (1852). On the change of refrangibility of light. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 142, 463-562.
Köhler, A., & Rohr, M. (1905). Photomicrography with ultra-violet light. Journal of the Royal Microscopical Society, 25, 513.
Heimstadt, H. (1911). Das Fluoreszenzmikroskop. Zeitschrift fur wissenschaftliche Mikroskopie, 28, 330-337.
Shimomura, O., Johnson, F. H., & Saiga, Y. (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. Journal of Cellular and Comparative Physiology, 59, 223-239.
Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W., & Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science, 263(5148), 802-805.
Heim, R., Prasher, D. C., & Tsien, R. Y. (1994). Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proceedings of the National Academy of Sciences of the United States of America, 91(26), 12501-12504.
Yao, Z., Zhang, B. S., & Prescher, J. A. (2018). Advances in bioluminescence imaging: New probes from old recipes. Current Opinion in Chemical Biology, 45, 148-156.
Bellini, M., Riva, B., Tinelli, V., Rizzuto, M. A., Salvioni, L., Colombo, M., Mingozzi, F., Visioli, A., Marongiu, L., Frascotti, G., Christodoulou, M. S., Passarella, D., Prosperi, D., & Fiandra, L. (2020). engineered ferritin nanoparticles for the bioluminescence tracking of nanodrug delivery in cancer. Small, 16(39), 2001450.
Galvez, T., Teruel, M. N., Heo, W., Jones, J. T., Kim, M., Liou, J., Myers, J. W., & Meyer, T. (2007). siRNA screen of the human signaling proteome identifies the PtdIns(3,4,5)P3-mTOR signaling pathway as a primary regulator of transferrin uptake. Genome Biology, 8(7), R142.
Shum, D., Smith, J. L., Hirsch, A. J., Bhinder, B., Radu, C., Stein, D. A., Nelson, J. A., Früh, K., & Djaballah, H. (2010). High-content assay to identify inhibitors of dengue virus infection. Assay and Drug Development Technologies, 8(5), 553-570.
Eggeling, C., Brand, L., Ullmann, D., & Jäger, S. (2003). Highly sensitive fluorescence detection technology currently available for HTS. Drug Discovery Today, 8(14), 632-641.
Zanella, F., Lorens, J. B., & Link, W. (2010). High content screening: Seeing is believing. Trends in Biotechnology, 28(5), 237-245.
Bickle, M. (2010). The beautiful cell: High-content screening in drug discovery. Analytical and Bioanalytical Chemistry, 398(1), 219-226.
Mattiazzi Usaj, M., Styles, E. B., Verster, A. J., Friesen, H., Boone, C., & Andrews, B. J. (2016). High-content screening for quantitative cell biology. Trends in Cell Biology, 26(8), 598-611.
Rimon, N., & Schuldiner, M. (2011). Getting the whole picture: Combining throughput with content in microscopy. Journal of Cell Science, 124(Pt 22), 3743-3751.
Chia, N.-Y., Chan, Y.-S., Feng, B., Lu, X., Orlov, Y. L., Moreau, D., Kumar, P., Yang, L., Jiang, J., Lau, M.-S., Huss, M., Soh, B.-S., Kraus, P., Li, P., Lufkin, T., Lim, B., Clarke, N. D., Bard, F., & Ng, H.-H. (2010). A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature, 468(7321), 316-320.
Desbordes, S. C., Placantonakis, D. G., Ciro, A., Socci, N. D., Lee, G., Djaballah, H., & Studer, L. (2008). High-throughput screening assay for the identification of compounds regulating self-renewal and differentiation in human embryonic stem cells. Cell Stem Cell, 2(6), 602-612.
Orvedahl, A., Sumpter, R., Xiao, G., Ng, A., Zou, Z., Tang, Y., Narimatsu, M., Gilpin, C., Sun, Q., Roth, M., Forst, C. V., Wrana, J. L., Zhang, Y. E., Luby-Phelps, K., Xavier, R. J., Xie, Y., & Levine, B. (2011). Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature, 480(7375), 113-117.
Link, W., Oyarzabal, J., Serelde, B. G., Albarran, M. I., Rabal, O., Cebriá, A., Alfonso, P., Fominaya, J., Renner, O., Peregrina, S., Soilán, D., Ceballos, P. A., Hernández, A.-I., Lorenzo, M., Pevarello, P., Granda, T. G., Kurz, G., Carnero, A., & Bischoff, J. R. (2009). Chemical interrogation of FOXO3a nuclear translocation identifies potent and selective inhibitors of phosphoinositide 3-kinases. Journal of Biological Chemistry, 284(41), 28392-28400.
Rämö, P., Drewek, A., Arrieumerlou, C., Beerenwinkel, N., Ben-Tekaya, H., Cardel, B., Casanova, A., Conde-Alvarez, R., Cossart, P., Csúcs, G., Eicher, S., Emmenlauer, M., Greber, U., Hardt, W.-D., Helenius, A., Kasper, C., Kaufmann, A., Kreibich, S., Kühbacher, A., … Dehio, C. (2014). Simultaneous analysis of large-scale RNAi screens for pathogen entry. BMC Genomics, 15, 1162.
Young, D. W., Bender, A., Hoyt, J., Mcwhinnie, E., Chirn, G.-W., Tao, C. Y., Tallarico, J. A., Labow, M., Jenkins, J. L., Mitchison, T. J., & Feng, Y. (2008). Integrating high-content screening and ligand-target prediction to identify mechanism of action. Nature Chemical Biology, 4(1), 59-68.
Moffat, J., Grueneberg, D. A., Yang, X., Kim, S. Y., Kloepfer, A. M., Hinkle, G., Piqani, B., Eisenhaure, T. M., Luo, B., Grenier, J. K., Carpenter, A. E., Foo, S. Y., Stewart, S. A., Stockwell, B. R., Hacohen, N., Hahn, W. C., Lander, E. S., Sabatini, D. M., & Root, D. E. (2006). A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell, 124(6), 1283-1298.
Hennig, C., Ilginus, C., Boztug, K., Skokowa, J., Marodi, L., Szaflarska, A., Sass, M., Pignata, C., Kilic, S. S., Caragol, I., Baumann, U., Klein, C., Welte, K., & Hansen, G. (2014). High-content cytometry and transcriptomic biomarker profiling of human B-cell activation. Journal of Allergy and Clinical Immunology, 133(1), 172-180.e1-10.
Marklein, R. A., Lo Surdo, J. L., Bellayr, I. H., Godil, S. A., Puri, R. K., & Bauer, S. R. (2016). High content imaging of early morphological signatures predicts long term mineralization capacity of human mesenchymal stem cells upon osteogenic induction. Stem Cells, 34(4), 935-947.
Cai, Y., Hossain, M. J, Hériché, J.-K., Politi, A. Z., Walther, N., Koch, B., Wachsmuth, M., Nijmeijer, B., Kueblbeck, M., Martinic-Kavur, M., Ladurner, R., Alexander, S., Peters, J.-M., & Ellenberg, J. (2018). Experimental and computational framework for a dynamic protein atlas of human cell division. Nature, 561(7723), 411-415.
Bray, M.-A., Singh, S., Han, H., Davis, C. T., Borgeson, B., Hartland, C., Kost-Alimova, M., Gustafsdottir, S. M., Gibson, C. C., & Carpenter, A. E. (2016). Cell painting, a high-content image-based assay for morphological profiling using multiplexed fluorescent dyes. Nature Protocols, 11(9), 1757-1774.
Vaisberg, E. A., Lenzi, D., Hansen, R. L., Keon, B. H., & Finer, J. T. (2006). An infrastructure for high-throughput microscopy: Instrumentation, informatics, and integration. Methods in Enzymology, 414, 484-512.
Eulenberg, P., Köhler, N., Blasi, T., Filby, A., Carpenter, A. E., Rees, P., Theis, F. J., & Wolf, F. A. (2017). Reconstructing cell cycle and disease progression using deep learning. Nature Communications, 8(1), 463.
Simm, J., Klambauer, G., Arany, A., Steijaert, M., Wegner, J. K., Gustin, E., Chupakhin, V., Chong, Y. T., Vialard, J., Buijnsters, P., Velter, I., Vapirev, A., Singh, S., Carpenter, A. E., Wuyts, R., Hochreiter, S., Moreau, Y., & Ceulemans, H. (2018). Repurposing high-throughput image assays enables biological activity prediction for drug discovery. Cell Chemical Biology, 25(5), 611-618.e3.
Wollmann, T., Gunkel, M., Chung, I., Erfle, H., Rippe, K., & Rohr, K. (2019). GRUU-Net: Integrated convolutional and gated recurrent neural network for cell segmentation. Medical Image Analysis, 56, 68-79.
Caicedo, J. C., Goodman, A., Karhohs, K. W., Cimini, B. A., Ackerman, J., Haghighi, M., Heng, C., Becker, T., Doan, M., Mcquin, C., Rohban, M., Singh, S., & Carpenter, A. E. (2019). Nucleus segmentation across imaging experiments: The 2018 Data Science Bowl. Nature Methods, 16(12), 1247-1253.
Allan, V. J. (1999). Basic Immunofluorescence. In Protein localization by fluorescence microscopy: A practical approach. Oxford University Press.
Melan, M. A., & Sluder, G. (1992). Redistribution and differential extraction of soluble proteins in permeabilized cultured cells. Implications for immunofluorescence microscopy. Journal of Cell Science, 101(Pt 4), 731-743.
Frigault, M. M., Lacoste, J., Swift, J. L., & Brown, C. M. (2009). Live-cell microscopy-tips and tools. Journal of Cell Science, 122(Pt 6), 753-767.
Ettinger, A., & Wittmann, T. (2014). Fluorescence live cell imaging. Methods in Cell Biology, 123, 77-94.
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, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676-682.
Arena, E. T., Rueden, C. T., Hiner, M. C., Wang, S., Yuan, M., & Eliceiri, K. W. (2017). Quantitating the cell: Turning images into numbers with ImageJ. Wiley Interdisciplinary Reviews Developmental Biology, 6(2), 260.
Mcquin, C., Goodman, A., Chernyshev, V., Kamentsky, L., Cimini, B. A., Karhohs, K. W., Doan, M., Ding, L., Rafelski, S. M., Thirstrup, D., Wiegraebe, W., Singh, S., Becker, T., Caicedo, J. C., & Carpenter, A. E. (2018). CellProfiler 3.0: Next-generation image processing for biology. PLoS Biology, 16(7), e2005970.
Wang, Y. L. (2007). Computational restoration of fluorescence images: Noise reduction, deconvolution, and pattern recognition. Methods in Cell Biology, 81, 435-445.
Zipfel, W. R., Williams, R. M., & Webb, W. W. (2003). Nonlinear magic: Multiphoton microscopy in the biosciences. Nature Biotechnology, 21(11), 1369-1377.
Hell, S. W. (2015). Nanoscopy with focused light (Nobel lecture). Angewandte Chemie (International ed in English), 54(28), 8054-8066.
Betzig, E. (2015). Single molecules, cells, and super-resolution optics (Nobel lecture). Angewandte Chemie (International ed in English), 54(28), 8034-8053.
Moerner, W. E. W. E. (2015). Single-molecule spectroscopy, imaging, and photocontrol: Foundations for super-resolution microscopy (Nobel lecture). Angewandte Chemie (International ed in English), 54(28), 8067-8093.
Graml, V., Studera, X., Lawson, J. L. D., Chessel, A., Geymonat, M., Bortfeld-Miller, M., Walter, T., Wagstaff, L., Piddini, E., & Carazo-Salas, R. E. (2014). A genomic multiprocess survey of machineries that control and link cell shape, microtubule organization, and cell-cycle progression. Developmental Cell, 31(2), 227-239.
Ohya, Y., Sese, J., Yukawa, M., Sano, F., Nakatani, Y., Saito, T. L., Saka, A., Fukuda, T., Ishihara, S., Oka, S., Suzuki, G., Watanabe, M., Hirata, A., Ohtani, M., Sawai, H., Fraysse, N., Latgé, J.-P., François, J. M., Aebi, M., … Morishita, S. (2005). High-dimensional and large-scale phenotyping of yeast mutants. Proceedings of the National Academy of Sciences of the United States of America, 102(52), 19015-19020.
Liberali, P., Snijder, B., & Pelkmans, L. (2014). A hierarchical map of regulatory genetic interactions in membrane trafficking. Cell, 157(6), 1473-1487.
Simpson, J. C., Joggerst, B., Laketa, V., Verissimo, F., Cetin, C., Erfle, H., Bexiga, M. G., Singan, V. R., Hériché, J.-K., Neumann, B., Mateos, A., Blake, J., Bechtel, S., Benes, V., Wiemann, S., Ellenberg, J., & Pepperkok, R. (2012). Genome-wide RNAi screening identifies human proteins with a regulatory function in the early secretory pathway. Nature Cell Biology, 14(7), 764-774.
Lindquist, R. A., Ottina, K. A., Wheeler, D. B., Hsu, P. P., Thoreen, C. C., Guertin, D. A., Ali, S. M., Sengupta, S., Shaul, Y. D., Lamprecht, M. R., Madden, K. L., Papallo, A. R., Jones, T. R., Sabatini, D. M., & Carpenter, A. E. (2011). Genome-scale RNAi on living-cell microarrays identifies novel regulators of Drosophila melanogaster TORC1-S6K pathway signaling. Genome Research, 21(3), 433-446.
Collinet, C., Stöter, M., Bradshaw, C. R., Samusik, N., Rink, J. C., Kenski, D., Habermann, B., Buchholz, F., Henschel, R., Mueller, M. S., Nagel, W. E., Fava, E., Kalaidzidis, Y., & Zerial, M. (2010). Systems survey of endocytosis by multiparametric image analysis. Nature, 464(7286), 243-249.
Chan, K. T., Paavolainen, L., Hannan, K. M., George, A. J., Hannan, R. D., Simpson, K. J., Horvath, P., & Pearson, R. B. (2016). Combining high-content imaging and phenotypic classification analysis of senescence-associated beta-galactosidase staining to identify regulators of oncogene-induced senescence. Assay and Drug Development Technologies, 14(7), 416-428.
Liu, C.-L., Li, X., Gan, L., He, Y.-Y., Wang, L.-L., & He, K.-L. (2016). High-content screening identifies inhibitors of the nuclear translocation of ATF6. International Journal of Molecular Medicine, 37(2), 407-414.
Kolla, L., Heo, D. S., Rosenberg, D. P., Barlow, S. A., Maximova, A. A., Cassio, E. E., & Buchser, W. J. (2018). High content screen for identifying small-molecule LC3B-localization modulators in a renal cancer cell line. Scientific Data, 5, 180116.
Lv, X., Chen, D., Yang, L., Zhu, N., Li, J., Zhao, J., Hu, Z., Wang, F.-J., & Zhang, L. W. (2016). Comparative studies on the immunoregulatory effects of three polysaccharides using high content imaging system. International Journal of Biological Macromolecules, 86, 28-42.
Harkness, T., Mcnulty, J. D., Prestil, R., Seymour, S. K., Klann, T., Murrell, M., Ashton, R. S., & Saha, K. (2015). High-content imaging with micropatterned multiwell plates reveals influence of cell geometry and cytoskeleton on chromatin dynamics. Biotechnology Journal, 10(10), 1555-1567.
Zhang, X., Yang, L., Liu, Y., Song, Z., Zhao, J., Chen, D., Yu, H., Li, R., Wang, Y., Yang, K., Chen, Y., Xia, M., & Zhang, L. W. (2018). Detection of nanocarrier potentiation on drug induced phospholipidosis in cultured cells and primary hepatocyte spheroids by high content imaging and analysis. Toxicology and Applied Pharmacology, 348, 54-66.
Okada, H., Ohnuki, S., Roncero, C., Konopka, J. B., & Ohya, Y. (2014). Distinct roles of cell wall biogenesis in yeast morphogenesis as revealed by multivariate analysis of high-dimensional morphometric data. Molecular Biology of the Cell, 25(2), 222-233.
Anilkumar, U., Weisova, P., Schmid, J., Bernas, T., Huber, H. J., Düssmann, H., Connolly, N. M. C., & Prehn, J. H. M. (2017). Defining external factors that determine neuronal survival, apoptosis and necrosis during excitotoxic injury using a high content screening imaging platform. PLoS ONE, 12(11), e0188343.
Poon, V. Y., Goh, C., Voorhoeve, P. M, & Fivaz, M. (2014). High-content imaging of presynaptic assembly. Frontiers in Cellular Neuroscience, 8, 66.
Laufer, C., Fischer, B., Billmann, M., Huber, W., & Boutros, M. (2013). Mapping genetic interactions in human cancer cells with RNAi and multiparametric phenotyping. Nature Methods, 10(5), 427-431.
Fischer, B., Sandmann, T., Horn, T., Billmann, M., Chaudhary, V., Huber, W., & Boutros, M. (2015). A map of directional genetic interactions in a metazoan cell. eLife, 4, e05464.
Collins, S. R., Miller, K. M., Maas, N. L., Roguev, A., Fillingham, J., Chu, C. S., Schuldiner, M., Gebbia, M., Recht, J., Shales, M., Ding, H., Xu, H., Han, J., Ingvarsdottir, K., Cheng, B., Andrews, B., Boone, C., Berger, S. L., Hieter, P., … Krogan, N. J. (2007). Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature, 446(7137), 806-810.
Costanzo, M., Vandersluis, B., Koch, E. N., Baryshnikova, A., Pons, C., Tan, G., Wang, W., Usaj, M., Hanchard, J., Lee, S. D., Pelechano, V., Styles, E. B., Billmann, M., Van Leeuwen, J., Van Dyk, N., Lin, Z.-Y., Kuzmin, E., Nelson, J., Piotrowski, J. S., … Boone, C. (2016). A global genetic interaction network maps a wiring diagram of cellular function. Science, 353(6306), aaf1420.
Kuijl, C., Savage, N. D. L., Marsman, M., Tuin, A. W., Janssen, L., Egan, D. A., Ketema, M., Van Den Nieuwendijk, R., Van Den Eeden, S. J. F., Geluk, A., Poot, A., Van Der Marel, G., Beijersbergen, R. L., Overkleeft, H., Ottenhoff, T. H. M., & Neefjes, J. (2007). Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature, 450(7170), 725-730.
Christophe, T., Ewann, F., Jeon, H. K., Cechetto, J., & Brodin, P. (2010). High-content imaging of Mycobacterium tuberculosis-infected macrophages: An in vitro model for tuberculosis drug discovery. Future Medicinal Chemistry, 2(8), 1283-1293.
Barczak, A. K., Avraham, R., Singh, S., Luo, S. S., Zhang, W. R., Bray, M.-A., Hinman, A. E., Thompson, M., Nietupski, R. M., Golas, A., Montgomery, P., Fitzgerald, M., Smith, R. S., White, D. W., Tischler, A. D., Carpenter, A. E., & Hung, D. T. (2017). Systematic, multiparametric analysis of Mycobacterium tuberculosis intracellular infection offers insight into coordinated virulence. PLoS Pathogens, 13(5), e1006363.
Manning, A. J., Ovechkina, Y., Mcgillivray, A., Flint, L., Roberts, D. M., & Parish, T. (2017). A high content microscopy assay to determine drug activity against intracellular Mycobacterium tuberculosis. Methods (San Diego, Calif.), 127, 3-11.
Greenwood, D. J., Dos Santos, M. S., Huang, S., Russell, M. R. G., Collinson, L. M., Macrae, J. I., West, A., Jiang, H., & Gutierrez, M. G. (2019). Subcellular antibiotic visualization reveals a dynamic drug reservoir in infected macrophages. Science, 364(6447), 1279-1282.
Antoniou, A. N., Powis, S. J., & Kriston-Vizi, J. (2019). High-content screening image dataset and quantitative image analysis of Salmonella infected human cells. BMC Research Res Notes, 12(1), 808.
Zoffmann, S., Vercruysse, M., Benmansour, F., Maunz, A., Wolf, L., Blum Marti, R., Heckel, T., Ding, H., Truong, H. H., Prummer, M., Schmucki, R., Mason, C. S., Bradley, K., Jacob, A. I., Lerner, C., Araujo Del Rosario, A., Burcin, M., Amrein, K. E., & Prunotto, M. (2019). Machine learning-powered antibiotics phenotypic drug discovery. Scientific Reports, 9(1), 5013.
Maes, M., Dyson, Z. A., Smith, S. E., Goulding, D. A., Ludden, C., Baker, S., Kellam, P., Reece, S. T., Dougan, G., & Bartholdson Scott, J. (2021). Publisher Correction: A novel therapeutic antibody screening method using bacterial high-content imaging reveals functional antibody binding phenotypes of Escherichia coli ST131. Scientific Reports, 11(1), 7366.
Petty, N. K., Ben Zakour, N. L., Stanton-Cook, M., Skippington, E., Totsika, M., Forde, B. M., Phan, M.-D., Gomes Moriel, D., Peters, K. M., Davies, M., Rogers, B. A., Dougan, G., Rodriguez-Baño, J., Pascual, A., Pitout, J. D. D., Upton, M., Paterson, D. L., Walsh, T. R., Schembri, M. A., & Beatson, S. A. (2014). Global dissemination of a multidrug resistant Escherichia coli clone. Proceedings of the National Academy of Sciences of the United States of America, 111(15), 5694-5699.
Szijártó, V., Guachalla, L. M., Visram, Z. C., Hartl, K., Varga, C., Mirkina, I., Zmajkovic, J., Badarau, A., Zauner, G., Pleban, C., Magyarics, Z., Nagy, E., & Nagy, G. (2015). Bactericidal monoclonal antibodies specific to the lipopolysaccharide O antigen from multidrug-resistant Escherichia coli clone ST131-O25b:H4 elicit protection in mice. Antimicrobial Agents and Chemotherapy, 59(6), 3109-3116.
Nonejuie, P., Burkart, M., Pogliano, K., & Pogliano, J. (2013). Bacterial cytological profiling rapidly identifies the cellular pathways targeted by antibacterial molecules. Proceedings of the National Academy of Sciences of the United States of America, 110(40), 16169-16174.
Quach, D. T., Sakoulas, G., Nizet, V., Pogliano, J., & Pogliano, K. (2016). Bacterial cytological profiling (BCP) as a rapid and accurate antimicrobial susceptibility testing method for Staphylococcus aureus. EBioMedicine, 4, 95-103.
Lamsa, A., Lopez-Garrido, J., Quach, D., Riley, E. P., Pogliano, J., & Pogliano, K. (2016). Rapid inhibition profiling in bacillus subtilis to identify the mechanism of action of new antimicrobials. ACS Chemical Biology, 11(8), 2222-2231.
Htoo, H. H., Brumage, L., Chaikeeratisak, V., Tsunemoto, H., Sugie, J., Tribuddharat, C., Pogliano, J., & Nonejuie, P. (2019). Bacterial cytological profiling as a tool to study mechanisms of action of antibiotics that are active against Acinetobacter baumannii. Antimicrobial Agents and Chemotherapy, 63(4), e02310-e02318.
Sridhar, S., Forrest, S., Warne, B., Maes, M., Baker, S., Dougan, G., & Bartholdson Scott, J. (2021). High-content imaging to phenotype antimicrobial effects on individual bacteria at scale. mSystems, 6(3), e00028.
Kondoh, Y., Honda, K., & Osada, H. (2015). Construction and application of a photo-cross-linked chemical array. Methods in Molecular Biology, 1263, 29-41.
Hughes, R. E., Elliott, R. J. R., Munro, A. F., Makda, A., O'neill, J. R, Hupp, T., & Carragher, N. O. (2020). High-content phenotypic profiling in esophageal adenocarcinoma identifies selectively active pharmacological classes of drugs for repurposing and chemical starting points for novel drug discovery. SLAS Discovery, 25(7), 770-782.
Pegoraro, G., Bavari, S., & Panchal, R. G. (2012). Shedding light on filovirus infection with high-content imaging. Viruses, 4(8), 1354-1371.
Xue, L., Qian, X., Jin, Q., Zhu, Y., Wang, X., Wang, D., Ge, G., & Yang, L. (2020). Construction and application of a high-content analysis for identifying human carboxylesterase 2 inhibitors in living cell system. Analytical and Bioanalytical Chemistry, 412(11), 2645-2654.
Nierode, G., Kwon, P. S., Dordick, J. S., & Kwon, S.-J. (2016). Cell-based assay design for high-content screening of drug candidates. Journal of Microbiology and Biotechnology, 26(2), 213-225.
Begley, C. G, & Ellis, L. M. (2012). Drug development: Raise standards for preclinical cancer research. Nature, 483(7391), 531-533.
Horvath, P., Aulner, N., Bickle, M., Davies, A. M., Nery, E. D., Ebner, D., Montoya, M. C., Östling, P., Pietiäinen, V., Price, L. S., Shorte, S. L., Turcatti, G., Von Schantz, C., & Carragher, N. O. (2016). Screening out irrelevant cell-based models of disease. Nature Reviews Drug Discovery, 15(11), 751-769.
Neumann, B., Walter, T., Hériché, J.-K., 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, M. H. A., Chapuis, C., Gerlich, D. W., … Ellenberg, J. (2010). Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature, 464(7289), 721-727.
Brandenberg, N., Hoehnel, S., Kuttler, F., Homicsko, K., Ceroni, C., Ringel, T., Gjorevski, N., Schwank, G., Coukos, G., Turcatti, G., & Lutolf, M. P. (2020). High-throughput automated organoid culture via stem-cell aggregation in microcavity arrays. Nature Biomedical Engineering, 4(9), 863-874.
Lee, S.-Y., Doh, I., Nam, D.-H., & Lee, D. W. (2018). 3D cell-based high-content screening (HCS) using a micropillar and microwell chip platform. Analytical Chemistry, 90(14), 8354-8361.
Norkin, M., Ordóñez-Morán, P., & Huelsken, J. (2021). High-content, targeted RNA-seq screening in organoids for drug discovery in colorectal cancer. Cell Reports, 35(3), 109026.
Martinez, N. J., Titus, S. A., Wagner, A. K., & Simeonov, A. (2015). High-throughput fluorescence imaging approaches for drug discovery using in vitro and in vivo three-dimensional models. Expert Opinion on Drug Discovery, 10(12), 1347-1361.
Celli, J. P., Rizvi, I., Blanden, A. R., Massodi, I., Glidden, M. D., Pogue, B. W., & Hasan, T. (2014). An imaging-based platform for high-content, quantitative evaluation of therapeutic response in 3D tumour models. Scientific Reports, 4, 3751.
Burgstaller, G., Oehrle, B., Koch, I., Lindner, M., & Eickelberg, O. (2013). Multiplex profiling of cellular invasion in 3D cell culture models. PLoS ONE, 8(5), e63121.
Yang, T.-M., Barbone, D., Fennell, D. A., & Broaddus, V. C. (2009). Bcl-2 family proteins contribute to apoptotic resistance in lung cancer multicellular spheroids. American Journal of Respiratory Cell and Molecular Biology, 41(1), 14-23.
Azaripour, A., Lagerweij, T., Scharfbillig, C., Jadczak, A. E., Willershausen, B., & Van Noorden, C. J. F. (2016). A survey of clearing techniques for 3D imaging of tissues with special reference to connective tissue. Progress in Histochemistry and Cytochemistry, 51(2), 9-23.
Gilbert, L. A., Horlbeck, M. A., Adamson, B., Villalta, J. E., Chen, Y., Whitehead, E. H., Guimaraes, C., Panning, B., Ploegh, H. L., Bassik, M. C., Qi, L. S., Kampmann, M., & Weissman, J. S. (2014). Genome-scale CRISPR-mediated control of gene repression and activation. Cell, 159(3), 647-661.
Lackner, D. H., Carré, A., Guzzardo, P. M., Banning, C., Mangena, R., Henley, T., Oberndorfer, S., Gapp, B. V., Nijman, S. M. B., Brummelkamp, T. R., & Bürckstümmer, T. (2015). A generic strategy for CRISPR-Cas9-mediated gene tagging. Nature Communications, 6, 10237.
Nazlamova, L., Thomas, N. S, Cheung, M.-K., Legebeke, J., Lord, J., Pengelly, R. J., Tapper, W. J., & Wheway, G. (2021). A CRISPR and high-content imaging assay compliant with ACMG/AMP guidelines for clinical variant interpretation in ciliopathies. Human Genetics, 140(4), 593-607.
Heiser, K., McLean, P. F., Davis, C. T., Fogelson, B., Gordon, H. B., Jacobson, P., Hurst, B., Miller, B., Alfa, R. W., Earnshaw, B. A., Victors, M. L., Chong, Y. T., Haque, I. S., Low, A. S., & Gibson, C. C. Identification of potential treatments for COVID-19 through artificial intelligence-enabled phenomic analysis of human cells infected with SARS-CoV-2. 2020.
Reisen, F., Sauty De Chalon, A., Pfeifer, M., Zhang, X., Gabriel, D., & Selzer, P. (2015). Linking phenotypes and modes of action through high-content screen fingerprints. Assay and Drug Development Technologies, 13(7), 415-427.
Gibson, C. C., Zhu, W., Davis, C. T., Bowman-Kirigin, J. A., Chan, A. C., Ling, J., Walker, A. E., Goitre, L., Delle Monache, S., Retta, S. F., Shiu, Y-T. E., Grossmann, A. H., Thomas, K. R., Donato, A. J., Lesniewski, L. A., Whitehead, K. J., & Li, D. Y. (2015). Strategy for identifying repurposed drugs for the treatment of cerebral cavernous malformation. Circulation, 131(3), 289-299.
Horvath, P., Wild, T., Kutay, U., & Csucs, G. (2011). Machine learning improves the precision and robustness of high-content screens: Using nonlinear multiparametric methods to analyze screening results. Journal of Biomolecular Screening: The Official Journal of the Society for Biomolecular Screening, 16(9), 1059-1067.
Gerlach, J. (1858). MikroskopischeStudienAus Dem Gebiete Der Menschlichen. Morphologie. Enke.
Jacobson, K., Wu, E., & Poste, G. (1976). Measurement of the translational mobility of concanavalin A in glycerol-saline solutions and on the cell surface by fluorescence recovery after photobleaching. Biochimica et Biophysica Acta, 433(1), 215-222.
Axelrod, D. (1981). Cell-substrate contacts illuminated by total internal reflection fluorescence. Journal of Cell Biology, 89(1), 141-145.
Denk, W., Strickler, J. H., & Webb, W. W. (1990). Two-photon laser scanning fluorescence microscopy. Science, 248(4951), 73-76.
Betzig, E., & Chichester, R. J. (1993). Single molecules observed by near-field scanning optical microscopy. Science, 262(5138), 1422-1425.
Klar, T. A., & Hell, S. W. (1999). Subdiffraction resolution in far-field fluorescence microscopy. Optics Letters, 24(14), 954-956.
Unadkat, H. V., Groen, N., Doorn, J., Fischer, B., Barradas, A. M. C., Hulsman, M., Van De Peppel, J., Moroni, L., Van Leeuwen, J. P., Reinders, M. J. T., Van Blitterswijk, C. A., & De Boer, J. (2013). High content imaging in the screening of biomaterial-induced MSC behavior. Biomaterials, 34(5), 1498-1505.
Leha, A., Moens, N., Meleckyte, R., Culley, O. J., Gervasio, M. K., Kerz, M., Reimer, A., Cain, S. A., Streeter, I., Folarin, A., Stegle, O., Kielty, C. M., Durbin, R., Watt, F. M., & Danovi, D. (2016). A high-content platform to characterise human induced pluripotent stem cell lines. Methods (San Diego, Calif.), 96, 85-96.
Soldati, C., Lopez-Fabuel, I., Wanderlingh, L. G., Garcia-Macia, M., Monfregola, J., Esposito, A., Napolitano, G., Guevara-Ferrer, M., Scotto Rosato, A., Krogsaeter, E. K., Paquet, D., Grimm, C. M., Montefusco, S., Braulke, T., Storch, S., Mole, S. E., De Matteis, M. A., Ballabio, A., Sampaio, J. L., … Medina, D. L. (2021). Repurposing of tamoxifen ameliorates CLN3 and CLN7 disease phenotype. EMBO Molecular Medicine, 13(10), e13742.
Garoffolo, G., Casaburo, M., Amadeo, F., Salvi, M., Bernava, G., Piacentini, L., Chimenti, I., Zaccagnini, G., Milcovich, G., Zuccolo, E., Agrifoglio, M., Ragazzini, S., Baasansuren, O., Cozzolino, C., Chiesa, M., Ferrari, S., Carbonaro, D., Santoro, R., Manzoni, M., … Pesce, M. (2022). Reduction of cardiac fibrosis by interference with YAP-dependent transactivation. Circulation Research, 131(3), 239-257.