Quantum dot semiconductor nanocrystals for immunophenotyping by polychromatic flow cytometry
Abstract
Immune responses arise from a wide variety of cells expressing unique combinations of multiple cell-surface proteins. Detailed characterization is hampered, however, by limitations in available probes and instrumentation. Here, we use the unique spectral properties of semiconductor nanocrystals (quantum dots) to extend the capabilities of polychromatic flow cytometry to resolve 17 fluorescence emissions. We show the need for this power by analyzing, in detail, the phenotype of multiple antigen-specific T-cell populations, revealing variations within complex phenotypic patterns that would otherwise remain obscure. For example, T cells specific for distinct epitopes from one pathogen, and even those specific for the same epitope, can have markedly different phenotypes. The technology we describe, encompassing the detection of eight quantum dots in conjunction with conventional fluorophores, should expand the horizons of flow cytometry, as well as our ability to characterize the intricacies of both adaptive and innate cellular immune responses.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Gating of N barcodes simultaneously in parallel optical channels offers file selection sensitivity of 1 in 10^6N total files, where common commercial FAS systems offer up to N = 17 channels.
“This strategy also applies to gating of N barcodes simultaneously in parallel optical channels, which offers file selection sensitivity of 1 in 106N total files, where common commercial FAS systems offer up to N = 17 channels38,39.”
From Random access DNA memory using Boolean search in an archival file storage system (2021) · cites this paper as [39]
Cites
Semiconductor Nanocrystals as Fluorescent Biological Labels
Bruchez, M. P., Moronne, M. M., Gin, P., Weiss, S., & Alivisatos, A. P. (1998) · Science · doi:10.1126/science.281.5385.2013 · Cited by 8,614 · see citing works
Self-citationQuantum Dots for Live Cells, in Vivo Imaging, and Diagnostics
Michalet, X., Pinaud, F. F., Bentolila, L. A., Tsay, J. M., Doose, S., Li, J. J., Sundaresan, G., Wu, A. M., Gambhir, S. S., & Weiss, S. (2005) · Science · doi:10.1126/science.1104274 · Cited by 7,794 · see citing works
Quantum Dot Bioconjugates for Ultrasensitive Nonisotopic Detection
Chan, W. C. W., & Nie, S. (1998) · Science · doi:10.1126/science.281.5385.2016 · Cited by 7,284 · see citing works
Two subsets of memory T lymphocytes with distinct homing potentials and effector functions
Sallusto, F., Lenig, D., Förster, R., Lipp, M., & Lanzavecchia, A. (1999) · Nature · doi:10.1038/44385 · Cited by 5,846 · see citing works
Long-term multiple color imaging of live cells using quantum dot bioconjugates
Jaiswal, J. K., Mattoussi, H. M., Mauro, J. M., & Simon, S. M. (2002) · Nature Biotechnology · doi:10.1038/nbt767 · Cited by 2,002 · see citing works
Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections
Appay, V., Dunbar, P. R., Callan, M. F. C., Klenerman, P., Gillespie, G. M. A., Papagno, L., Ogg, G. S., King, A., Lechner, F., Spina, C. A., et al. (2002) · Nature Medicine · doi:10.1038/nm0402-379 · Cited by 1,556 · see citing works
Current protocols in immunology
Nezlin, R. S. (1992) · Molecular Immunology · doi:10.1016/0161-5890(92)90114-d · Cited by 1,413 · see citing works
Phenotypic and functional separation of memory and effector human CD8+ T cells
Hamann, D., Baars, P. A., Rep, M. H. G., Hooibrink, B., Kerkhof-Garde, S. R., Klein, M. R., & Lier, R. A. W. V. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.186.9.1407 · Cited by 1,366 · see citing works
Noninvasive Imaging of Quantum Dots in Mice
Ballou, B. T., Lagerholm, B. C., Ernst, L. A., Bruchez, M. P., & Waggoner, A. S. (2003) · Bioconjugate Chemistry · doi:10.1021/bc034153y · Cited by 1,141 · see citing works
Self-citationBrenchley, J. M., Karandikar, N. J., Betts, M. R., Ambrozak, D. R., Hill, B. J., Crotty, L. E., Casazza, J. P., Kuruppu, J., Migueles, S. A., Connors, M., et al. (2003) · Blood · doi:10.1182/blood-2002-07-2103 · Cited by 1,073 · see citing works
Self-citationSeventeen-colour flow cytometry: unravelling the immune system
Perfetto, S. P., Chattopadhyay, P. K., & Roederer, M. (2004) · Nature Reviews Immunology · doi:10.1038/nri1416 · Cited by 1,019 · see citing works
Self-citationSkewed maturation of memory HIV-specific CD8 T lymphocytes
Champagne, P., Ogg, G. S., King, A. S., Knabenhans, C., Ellefsen, K., Nobile, M., Appay, V., Rizzardi, G. P., Fleury, S., Lipp, M., et al. (2001) · Nature · doi:10.1038/35065118 · Cited by 1,002 · see citing works
Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection
Price, D. A., Goulder, P., Klenerman, P., Sewell, A. K., Easterbrook, P., Troop, M., Bangham, C. R. M., & Phillips, R. E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.5.1890 · Cited by 687 · see citing works
Self-citationSpectral compensation for flow cytometry: Visualization artifacts, limitations, and caveats
Roederer, M. (2001) · Cytometry · doi:10.1002/1097-0320(20011101)45:3 · Cited by 561 · see citing works
Self-citationSelection of Quantum Dot Wavelengths for Biomedical Assays and Imaging
Lim, Y. T., Kim, S., Nakayama, A., Stott, N. E., Bawendi, M. G., & Frangioni, J. V. (2003) · Molecular Imaging · doi:10.1162/153535003765276282 · Cited by 559 · see citing works
Rosa, S. C. D., Herzenberg, L. A., Herzenberg, L. A., & Roederer, M. (2001) · Nature Medicine · doi:10.1038/84701 · Cited by 455 · see citing works
Self-citationDiamond, D. J., York, J., Sun, J., Wright, C. L., & Forman, S. J. (1997) · Blood · doi:10.1182/blood.v90.5.1751 · Cited by 246 · see citing works
T cell response to Epstein-Barr virus transactivators in chronic rheumatoid arthritis.
Scotet, E., David-Ameline, J., Peyrat, M., Moreau‐Aubry, A., Pinczon, D., Lim, A., Even, J., Sémana, G., Berthelot, J., Breathnach, R., et al. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.184.5.1791 · Cited by 167 · see citing works
Chen, G., Shankar, P., Lange, C. G., Valdez, H., Skolnik, P. R., Wu, L., Manjunath, N., & Lieberman, J. (2001) · Blood · doi:10.1182/blood.v98.1.156 · Cited by 159 · see citing works
Quantum dots are powerful multipurpose vital labeling agents in zebrafish embryos
Rieger, S., Kulkarni, R. P., Darcy, D., Fraser, S. E., & Köster, R. W. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20524 · Cited by 116 · see citing works
Hutchinson, S., Wooldridge, L., Tafuro, S., Laugel, B., Glick, M., Boulter, J. M., Jakobsen, B. K., Price, D. A., & Sewell, A. K. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300633200 · Cited by 90 · see citing works
Self-citationAmlot, P. L., Tahami, F., Chinn, D. L., & Rawlings, E. (1996) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1996.d01-722.x · Cited by 68 · see citing works
Applications of Quantum Dots in Biology: An Overview
Hotz, C. Z. (2005) · Humana Press eBooks · doi:10.1385/1-59259-901-x:001 · Cited by 47 · see citing works
Activation and differentiation antigens on T cells of healthy, at-risk, and HIV-infected children.
Plaeger-Marshall, S., Hultin, P. M., Bertolli, J., O'Rourke, S. S., Kobayashi, R., Kobayashi, A. L., Giorgi, J. V., Bryson, Y. J., & Stiehm, E. R. (1993) · PubMed · Cited by 45 · see citing works
Fluoroimmunoassays Using Antibody-Conjugated Quantum Dots
Goldman, E. R., Mattoussi, H. M., Anderson, G. P., Medintz, I. L., & Mauro, J. M. (2005) · Humana Press eBooks · doi:10.1385/1-59259-901-x:019 · Cited by 39 · see citing works
Rowland‐Jones, S., Powis, S. H., Sutton, J., Mockridge, I., Gotch, F. M., Murray, N., Hill, A. B., Rosenberg, W. M., Trowsdale, J., & McMichael, A. J. (1993) · European Journal of Immunology · doi:10.1002/eji.1830230841 · Cited by 32 · see citing works
Sing, G. K., Butterworth, L. A., Chen, X., Bryant, A., & Cooksley, G. (1998) · Journal of Viral Hepatitis · doi:10.1046/j.1365-2893.1998.00088.x · Cited by 21 · see citing works
Compensation is not dependent on signal intensity or on number of parameters
Roederer, M. (2001) · Cytometry · doi:10.1002/cyto.10008 · Cited by 20 · see citing works
Self-citationViable Infectious Cell Sorting in a BSL-3 Facility
Perfetto, S. P., Ambrozak, D. R., Roederer, M., & Koup, R. A. (2004) · Humana Press eBooks · doi:10.1385/1-59259-773-4:419 · Cited by 15 · see citing works
Self-citationImmunophenotyping of T Cell Subpopulations in HIV Disease
Chattopadhyay, P. K., & Roederer, M. (2005) · Current Protocols in Immunology · doi:10.1002/0471142735.im1212s65 · Cited by 12 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Bendall, S. C., Simonds, E. F., Qiu, P., Amir, E.-A. D., Krutzik, P. O., Finck, R., Bruggner, R. V., Melamed, R., Trejo, A., Ornatsky, O. I., et al. (2011) · Science · doi:10.1126/science.1198704 · Cited by 2,279 · see citing works
Kim, B. Y. S., Rutka, J. T., & Chan, W. C. W. (2010) · New England Journal of Medicine · doi:10.1056/nejmra0912273 · Cited by 1,153 · see citing works
Designing multifunctional quantum dots for bioimaging, detection, and drug delivery
Zrazhevskiy, P., Sena, M., & Gao, X. (2010) · Chemical Society Reviews · doi:10.1039/b915139g · Cited by 999 · see citing works
Extracting a cellular hierarchy from high-dimensional cytometry data with SPADE
Qiu, P., Simonds, E. F., Bendall, S. C., Gibbs, K. D., Bruggner, R. V., Linderman, M. D., Sachs, K., Nolan, G. P., & Plevritis, S. K. (2011) · Nature Biotechnology · doi:10.1038/nbt.1991 · Cited by 956 · see citing works
Single-cell RNA-seq: advances and future challenges
Saliba, A.-E., Westermann, A. J., Gorski, S. A., & Vogel, J. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku555 · Cited by 847 · see citing works
SPICE: Exploration and analysis of post‐cytometric complex multivariate datasets
Roederer, M., Nozzi, J. L., & Nason, M. (2011) · Cytometry Part A · doi:10.1002/cyto.a.21015 · Cited by 822 · see citing works
Self-citationSemiconductor Quantum Dots for Bioimaging and Biodiagnostic Applications
Kairdolf, B. A., Smith, A. M., Stokes, T. H., Wang, M. D., Young, A. N., & Nie, S. (2013) · Annual Review of Analytical Chemistry · doi:10.1146/annurev-anchem-060908-155136 · Cited by 674 · see citing works
A deep profiler's guide to cytometry
Bendall, S. C., Nolan, G. P., Roederer, M., & Chattopadhyay, P. K. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.02.010 · Cited by 653 · see citing works
Self-citationDiffusion maps for high-dimensional single-cell analysis of differentiation data
Haghverdi, L., Buettner, F., & Theis, F. J. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv325 · Cited by 649 · see citing works
Revealing the vectors of cellular identity with single-cell genomics
Wagner, A., Regev, A., & Yosef, N. (2016) · Nature Biotechnology · doi:10.1038/nbt.3711 · Cited by 632 · see citing works
Paths to stemness: building the ultimate antitumour T cell
Gattinoni, L., Klebanoff, C. A., & Restifo, N. P. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3322 · Cited by 599 · see citing works
Petryayeva, E., Algar, W. R., & Medintz, I. L. (2013) · Applied Spectroscopy · doi:10.1366/12-06948 · Cited by 590 · see citing works
Multiplexed mass cytometry profiling of cellular states perturbed by small-molecule regulators
Bodenmiller, B., Zunder, E. R., Finck, R., Chen, T. J., Savig, E. S., Bruggner, R. V., Simonds, E. F., Bendall, S. C., Sachs, K., Krutzik, P. O., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2317 · Cited by 546 · see citing works
Bioconjugated quantum dots for multiplexed and quantitative immunohistochemistry
Xing, Y., Chaudry, Q., Shen, C., Kong, K. Y., Zhau, H. E., Chung, L. W. K., Petros, J. A., O'Regan, R. M., Yezhelyev, M. V., Simons, J. W., et al. (2007) · Nature Protocols · doi:10.1038/nprot.2007.107 · Cited by 528 · see citing works
T Cell Responses to Whole SARS Coronavirus in Humans
Li, C. K., Wu, H., Yan, H., Ma, S., Wang, L., Zhang, M., Tang, X., Temperton, N. J., Weiss, R. A., Brenchley, J. M., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.8.5490 · Cited by 488 · see citing works
Precopio, M., Betts, M. R., Parrino, J., Price, D. A., Emma Gostick, D., Ambrozak, D. R., Asher, T. E., Douek, D. C., Harari, A., Pantaleo, G., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20062363 · Cited by 484 · see citing works
Self-citationApoptosis and Beyond: Cytometry in Studies of Programmed Cell Death
Włodkowic, D., Telford, W. G., Skommer, J., & Darżynkiewicz, Z. (2011) · Methods in cell biology · doi:10.1016/b978-0-12-385493-3.00004-8 · Cited by 470 · see citing works
Highly multiparametric analysis by mass cytometry
Ornatsky, O., Bandura, D. R., Baranov, V. I., Nitz, M., Winnik, M. A., & Tanner, S. D. (2010) · Journal of Immunological Methods · doi:10.1016/j.jim.2010.07.002 · Cited by 368 · see citing works
Single-cell technologies for monitoring immune systems
Chattopadhyay, P. K., Gierahn, T. M., Roederer, M., & Love, J. C. (2014) · Nature Immunology · doi:10.1038/ni.2796 · Cited by 368 · see citing works
Self-citationZhu, J., Koelle, D. M., Cao, J., Vazquez, J., Huang, M. L., Hladik, F., Wald, A., & Corey, L. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20061792 · Cited by 340 · see citing works
Delivering quantum dots into cells: strategies, progress and remaining issues
Delehanty, J. B., Mattoussi, H. M., & Medintz, I. L. (2008) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-008-2410-4 · Cited by 327 · see citing works
Flow Cytometry-Based Apoptosis Detection
Włodkowic, D., Skommer, J., & Darżynkiewicz, Z. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-017-5_2 · Cited by 325 · see citing works
Hadrup, S. R., Bakker, A. H., Shu, C. J., Andersen, R. S., van Veluw, J., Hombrink, P., Castermans, E., thor Straten, P., Blank, C., Haanen, J. B., et al. (2009) · Nature Methods · doi:10.1038/nmeth.1345 · Cited by 306 · see citing works
Klebanoff, C. A., Gattinoni, L., & Restifo, N. P. (2012) · Journal of Immunotherapy · doi:10.1097/cji.0b013e31827806e6 · Cited by 276 · see citing works
Intracellular cytokine optimization and standard operating procedure
Lamoreaux, L., Roederer, M., & Koup, R. (2006) · Nature Protocols · doi:10.1038/nprot.2006.268 · Cited by 268 · see citing works
Self-citationChattopadhyay, P. K., Betts, M. R., Price, D. A., Emma Gostick, D., Horton, H., Roederer, M., & Rosa, S. C. D. (2008) · Journal of Leukocyte Biology · doi:10.1189/jlb.0208107 · Cited by 260 · see citing works
Self-citationAutoimmune diseases — connecting risk alleles with molecular traits of the immune system
Gutiérrez‐Arcelus, M., Rich, S. S., & Raychaudhuri, S. (2015) · Nature Reviews Genetics · doi:10.1038/nrg.2015.33 · Cited by 254 · see citing works
Polyfunctional T cell responses are a hallmark of HIV‐2 infection
Duvall, M. G., Precopio, M., Ambrozak, D. R., Jaye, A., McMichael, A. J., Whittle, H. C., Roederer, M., Rowland‐Jones, S., & Koup, R. A. (2008) · European Journal of Immunology · doi:10.1002/eji.200737768 · Cited by 241 · see citing works
Self-citationAutissier, P., Soulas, C., Burdo, T. H., & Williams, K. C. (2010) · Cytometry Part A · doi:10.1002/cyto.a.20859 · Cited by 234 · see citing works
Single-cell analysis targeting the proteome
Labib, M., & Kelley, S. O. (2020) · Nature Reviews Chemistry · doi:10.1038/s41570-020-0162-7 · Cited by 233 · see citing works
Single-cell mass cytometry for analysis of immune system functional states
Bjornson, Z. B., Nolan, G. P., & Fantl, W. J. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.07.004 · Cited by 227 · see citing works
Beveridge, N. E. R., Price, D. A., Casazza, J. P., Pathan, A. A., Sander, C. R., Asher, T. E., Ambrozak, D. R., Precopio, M., Scheinberg, P., Alder, N. C., et al. (2007) · European Journal of Immunology · doi:10.1002/eji.200737504 · Cited by 222 · see citing works
Self-citationCD27 deficiency is associated with combined immunodeficiency and persistent symptomatic EBV viremia
van Montfrans, J. M., Hoepelman, A. I. M., Otto, S. A., van Gijn, M. E., van de Corput, L., de Weger, R. A., Monaco-Shawver, L., Banerjee, P. P., Sanders, E. A. M., der Zijde, C. M. J., et al. (2011) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2011.11.013 · Cited by 215 · see citing works
Self-citationSuzuki, M. M., Husimi, Y., Komatsu, H., Suzuki, K., & Douglas, K. T. (2008) · Journal of the American Chemical Society · doi:10.1021/ja710870e · Cited by 212 · see citing works
Optical hyperspectral imaging in microscopy and spectroscopy - a review of data acquisition
Gao, L. S., & Smith, R. T. (2014) · Journal of Biophotonics · doi:10.1002/jbio.201400051 · Cited by 211 · see citing works
Tsai, C., Hung, Y., Chou, Y., Huang, D., Hsiao, J., Chang, C., Chen, Y., & Mou, C. (2008) · Small · doi:10.1002/smll.200700457 · Cited by 206 · see citing works
Optimizing a Multicolor Immunophenotyping Assay
Mahnke, Y. D., & Roederer, M. (2007) · Clinics in Laboratory Medicine · doi:10.1016/j.cll.2007.05.002 · Cited by 201 · see citing works
Self-citationData analysis in flow cytometry: The future just started
Lugli, E., Roederer, M., & Cossarizza, A. (2010) · Cytometry Part A · doi:10.1002/cyto.a.20901 · Cited by 199 · see citing works
Self-citationA Reactive Peptidic Linker for Self-Assembling Hybrid Quantum Dot−DNA Bioconjugates
Medintz, I. L., Berti, L., Pons, T., Grimes, A. F., English, D. S., Alessandrini, A., Facci, P., & Mattoussi, H. M. (2007) · Nano Letters · doi:10.1021/nl070782v · Cited by 195 · see citing works
Multifunctional Photonic Nanomaterials for Diagnostic, Therapeutic, and Theranostic Applications
Kim, H., Beack, S., Han, S., Shin, M., Lee, T., Park, Y., Kim, K. S., Yetisen, A. K., Yun, S. H., Kwon, W., et al. (2018) · Advanced Materials · doi:10.1002/adma.201701460 · Cited by 191 · see citing works
Tricks with tetramers: how to get the most from multimeric peptide–MHC
Wooldridge, L., Lissina, A., Cole, D. K., van den Berg, H. A., Price, D. A., & Sewell, A. K. (2009) · Immunology · doi:10.1111/j.1365-2567.2008.02848.x · Cited by 184 · see citing works
Self-citationQuantum Dot−Fluorescent Protein Pairs as Novel Fluorescence Resonance Energy Transfer Probes
Dennis, A. M., & Bao, G. (2008) · Nano Letters · doi:10.1021/nl080358+ · Cited by 183 · see citing works
Liu, R., Zhang, S., Wei, C. F., Xing, Z., Zhang, S., & Zhang, X. (2016) · Accounts of Chemical Research · doi:10.1021/acs.accounts.5b00509 · Cited by 179 · see citing works
A Mechanism for TCR Sharing between T Cell Subsets and Individuals Revealed by Pyrosequencing
Venturi, V., Quigley, M. F., Greenaway, H. Y., Ng, P. C., Ende, Z. S., McIntosh, T. C., Asher, T. E., Almeida, J. R., Levy, S., Price, D. A., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003898 · Cited by 175 · see citing works
Self-citationNanoparticles for Applications in Cellular Imaging
Thurn, K. T., Brown, E., Wu, A., Vogt, S., Lai, B. C. H., Maser, J. M., Paunesku, T., & Woloschak, G. E. (2007) · Nanoscale Research Letters · doi:10.1007/s11671-007-9081-5 · Cited by 174 · see citing works
A chromatic explosion: the development and future of multiparameter flow cytometry
Chattopadhyay, P. K., Högerkorp, C., & Roederer, M. (2008) · Immunology · doi:10.1111/j.1365-2567.2008.02989.x · Cited by 166 · see citing works
Self-citationLissina, A., Ladell, K., Skowera, A., Clement, M., Edwards, E. S. J., Seggewiss, R., van den Berg, H. A., Emma Gostick, D., Gallagher, K., Jones, E., et al. (2008) · Journal of Immunological Methods · doi:10.1016/j.jim.2008.09.014 · Cited by 154 · see citing works
Self-citationReview Article: Recent advancements in optofluidic flow cytometer
Cho, S. H., Godin, J. M., Chen, C., Qiao, W., Lee, H., & Lo, Y. (2010) · Biomicrofluidics · doi:10.1063/1.3511706 · Cited by 149 · see citing works
Quality assurance for polychromatic flow cytometry using a suite of calibration beads
Perfetto, S. P., Ambrozak, D., Nguyen, R., Chattopadhyay, P. K., & Roederer, M. (2012) · Nature Protocols · doi:10.1038/nprot.2012.126 · Cited by 148 · see citing works
Self-citationMinimizing Nonspecific Cellular Binding of Quantum Dots with Hydroxyl-Derivatized Surface Coatings
Kairdolf, B. A., Mancini, M. C., Smith, A. M., & Nie, S. (2008) · Analytical Chemistry · doi:10.1021/ac800068q · Cited by 144 · see citing works
Bioconjugated quantum dots as fluorescent probes for bioanalytical applications
Frasco, M. F., & Chaniotakis, N. A. (2009) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-009-3033-0 · Cited by 144 · see citing works
Random access DNA memory using Boolean search in an archival file storage system
Banal, J. L., Shepherd, T. R., Berleant, J., Huang, H., Reyes, M., Ackerman, C. M., Blainey, P. C., & Bathe, M. (2021) · Nature Materials · doi:10.1038/s41563-021-01021-3 · Cited by 143 · see citing works
Britten, C. M., Gouttefangeas, C., Welters, M. J. P., Pawelec, G., Koch, S. D., Ottensmeier, C. H. H., Mander, A., Walter, S., Paschen, A., Müller‐Berghaus, J., et al. (2007) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-007-0378-0 · Cited by 143 · see citing works
Anderson, R., & Chan, W. C. W. (2008) · ACS Nano · doi:10.1021/nn700450g · Cited by 143 · see citing works
Harari, A., Enders, F. B., Cellerai, C., Bart, P., & Pantaleo, G. (2009) · Journal of Virology · doi:10.1128/jvi.02528-08 · Cited by 141 · see citing works
Multifunctional quantum dots for personalized medicine
Zrazhevskiy, P., & Gao, X. (2009) · Nano Today · doi:10.1016/j.nantod.2009.07.004 · Cited by 135 · see citing works
Cytometry: Today’s technology and tomorrow’s horizons
Chattopadhyay, P. K., & Roederer, M. (2012) · Methods · doi:10.1016/j.ymeth.2012.02.009 · Cited by 134 · see citing works
Self-citationTaniguchi, M., Cramer, D. L., Bhise, A. D., Kee, H. L., Bocian, D. F., Holten, D., & Lindsey, J. S. (2008) · New Journal of Chemistry · doi:10.1039/b717803d · Cited by 126 · see citing works
Interrogating the repertoire: broadening the scope of peptide–MHC multimer analysis
Davis, M. M., Altman, J. D., & Newell, E. W. (2011) · Nature Reviews Immunology · doi:10.1038/nri3020 · Cited by 124 · see citing works
Minimal Residual Disease in Acute Lymphoblastic Leukemia: Technical and Clinical Advances
Starza, I. D., Chiaretti, S., Propris, M. S. D., Elia, L., Cavalli, M., Novi, L. A. D., Soscia, R., Messina, M., Vitale, A., Guarini, A., et al. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00726 · Cited by 122 · see citing works
β-Cell–Specific CD8 T Cell Phenotype in Type 1 Diabetes Reflects Chronic Autoantigen Exposure
Skowera, A., Ladell, K., McLaren, J. E., Dolton, G. M., Matthews, K. K., Emma Gostick, D., Kronenberg‐Versteeg, D., Eichmann, M., Knight, R. R., Heck, S., et al. (2014) · Diabetes · doi:10.2337/db14-0332 · Cited by 118 · see citing works
Self-citationChattopadhyay, P. K., Gaylord, B. S., Palmer, A., Jiang, N., Raven, M. A., Lewis, G., Reuter, M. A., Rahman, A. K. M. N., Price, D. A., Betts, M. R., et al. (2012) · Cytometry Part A · doi:10.1002/cyto.a.22043 · Cited by 118 · see citing works
Self-citationA flow cytometer for the measurement of Raman spectra
Watson, D. A., Brown, L. O., Gaskill, D. F., Naivar, M. A., Graves, S. W., Doorn, S. K., & Nolan, J. P. (2008) · Cytometry Part A · doi:10.1002/cyto.a.20520 · Cited by 116 · see citing works
Tanner, S. D., Bandura, D. R., Ornatsky, O., Baranov, V. I., Nitz, M., & Winnik, M. A. (2008) · Pure and Applied Chemistry · doi:10.1351/pac200880122627 · Cited by 115 · see citing works
Hahn, M. A., Keng, P. C., & Krauss, T. D. (2008) · Analytical Chemistry · doi:10.1021/ac7018365 · Cited by 113 · see citing works
Makedonas, G., Hutnick, N. A., Haney, D., Amick, A. C., Gardner, J. S., Cosma, G. L., Hersperger, A. R., Dolfi, D. V., Wherry, E. J., Ferrari, G., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000798 · Cited by 112 · see citing works
Self-citationDetection of minimal residual disease in pediatric acute lymphoblastic leukemia
Gaipa, G., Basso, G., Biondi, A., & Campana, D. (2013) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.21101 · Cited by 111 · see citing works
Fluorescent nanocrystal-encoded microbeads for multiplexed cancer imaging and diagnosis
Sukhanova, A. V., & Nabiev, I. R. (2008) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2008.05.006 · Cited by 111 · see citing works
Inductively coupled plasma mass spectrometry‐based immunoassay: A review
Liu, R., Wu, P., Yang, L., Hou, X., & Lv, Y. (2013) · Mass Spectrometry Reviews · doi:10.1002/mas.21391 · Cited by 106 · see citing works
Lugli, E., Pinti, M., Nasi, M., Troiano, L., Ferraresi, R., Mussi, C., Salvioli, G., Patsekin, V., Robinson, J. P., Durante, C., et al. (2007) · Cytometry Part A · doi:10.1002/cyto.a.20387 · Cited by 105 · see citing works
Wang, G., Leng, Y., Dou, H., Wang, L., Li, W., Wang, X., Sun, K., Shen, L., Yuan, X., Li, J., et al. (2012) · ACS Nano · doi:10.1021/nn3045215 · Cited by 101 · see citing works
MHC‐Peptide Tetramers to Visualize Antigen‐Specific T Cells
Altman, J. D., & Davis, M. M. (2016) · Current Protocols in Immunology · doi:10.1002/cpim.14 · Cited by 99 · see citing works
Empty peptide-receptive MHC class I molecules for efficient detection of antigen-specific T cells
Saini, S. K., Tamhane, T., Anjanappa, R., Saikia, A., Ramskov, S., Donia, M., Svane, I. M., Jakobsen, S. N., García-Alai, M., Zacharias, M., et al. (2019) · Science Immunology · doi:10.1126/sciimmunol.aau9039 · Cited by 96 · see citing works
Loré, K., Adams, W. C. T., Havenga, M. J. E., Precopio, M., Holterman, L., Goudsmit, J., & Koup, R. A. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.3.1721 · Cited by 91 · see citing works
Self-citationDetection, phenotyping, and quantification of antigen-specific T cells using a peptide-MHC dodecamer
Huang, J., Zeng, X., Sigal, N., Lund, P. J., Su, L. F., Huang, H., Chien, Y., & Davis, M. M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602488113 · Cited by 90 · see citing works
Reactive Semiconductor Nanocrystals for Chemoselective Biolabeling and Multiplexed Analysis
Jennings, T. L., Becker-Catania, S. G., Triulzi, R. C., Tao, G., Scott, B., Sapsford, K. E., Spindel, S., Oh, E., Jain, V., Delehanty, J. B., et al. (2011) · ACS Nano · doi:10.1021/nn201050g · Cited by 90 · see citing works
Modular Nucleic Acid Assembled p/MHC Microarrays for Multiplexed Sorting of Antigen-Specific T Cells
Kwong, G. A., Radu, C. G., Hwang, K., Shu, C. J., Ma, C., Koya, R. C., Comin-Anduix, B., Hadrup, S. R., Bailey, R. C., Witte, O. N., et al. (2009) · Journal of the American Chemical Society · doi:10.1021/ja9006707 · Cited by 88 · see citing works
Cytometry in cell necrobiology revisited. Recent advances and new vistas
Włodkowic, D., Skommer, J., & Darżynkiewicz, Z. (2010) · Cytometry Part A · doi:10.1002/cyto.a.20889 · Cited by 86 · see citing works
Flow cytometry for drug discovery, receptor pharmacology and high-throughput screening
Sklar, L. A., Carter, M. B., & EDWARDS, B. (2007) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.06.006 · Cited by 86 · see citing works
Huenecke, S., Behl, M. J., Fadler, C., Zimmermann, S. Y., Bochennek, K., Tramsen, L., Esser, R., Klarmann, D., Kamper, M., Sattler, A., et al. (2008) · European Journal Of Haematology · doi:10.1111/j.1600-0609.2008.01052.x · Cited by 85 · see citing works
Li, H., Lasaro, M. O., Jia, B., Lin, S. W., Haut, L. H., High, K. A., & Ertl, H. C. (2011) · Molecular Therapy · doi:10.1038/mt.2011.81 · Cited by 83 · see citing works
Makedonas, G., Banerjee, P. P., Pandey, R., Hersperger, A. R., Sanborn, K. B., Hardy, G. A. D., Orange, J. S., & Betts, M. R. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803945 · Cited by 82 · see citing works
Self-citationUnique Temperature Dependence and Blinking Behavior of CdTe/CdSe (Core/Shell) Type-II Quantum Dots
Chon, B., Bang, J., Park, J., Jeong, C., Choi, J. H., Lee, J., Joo, T., & Kim, S. (2010) · The Journal of Physical Chemistry C · doi:10.1021/jp109229u · Cited by 80 · see citing works
Mishra, N., Dutt, V. G. V., & Arciniegas, M. P. (2019) · Chemistry of Materials · doi:10.1021/acs.chemmater.8b05363 · Cited by 78 · see citing works
Wölfl, M., Kuball, J. H. E., Eyrich, M. K., Schlegel, P. G., & Greenberg, P. D. (2008) · Cytometry Part A · doi:10.1002/cyto.a.20594 · Cited by 75 · see citing works
Jokerst, J. V., Floriano, P. N., Christodoulides, N. J., Simmons, G. W., & McDevitt, J. T. (2008) · Lab on a Chip · doi:10.1039/b817116e · Cited by 75 · see citing works
Konecny, A., Mage, P. L., Tyznik, A. J., Prlic, M., & Mair, F. (2024) · Cytometry Part A · doi:10.1002/cyto.a.24841 · Cited by 74 · see citing works
SYTO probes in the cytometry of tumor cell death
Włodkowic, D., Skommer, J., & Darżynkiewicz, Z. (2008) · Cytometry Part A · doi:10.1002/cyto.a.20535 · Cited by 74 · see citing works
Estévez, M. ‐., O’Donoghue, M. B., Chen, X., & Tan, W. (2009) · Nano Research · doi:10.1007/s12274-009-9041-8 · Cited by 73 · see citing works
Balmuri, S. R., Selvaraj, U., Kumar, V. V., Anthony, S. P., Tsatsakis, A. M., Golokhvast, K. S., & Raman, T. (2016) · Environmental Research · doi:10.1016/j.envres.2016.10.005 · Cited by 72 · see citing works
Multiplex Charge-Transfer Interactions between Quantum Dots and Peptide-Bridged Ruthenium Complexes
Medintz, I. L., Farrell, D. F., Susumu, K., Trammell, S. A., Deschamps, J. R., Brunel, F. M., Dawson, P. E., & Mattoussi, H. M. (2009) · Analytical Chemistry · doi:10.1021/ac900412j · Cited by 71 · see citing works
Luo, Y., Zhang, B., Chen, M., Jiang, T., Zhou, D., Huang, J., & Fu, W. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-24 · Cited by 70 · see citing works
Human Immunodeficiency Virus Type 1 Protease Cleaves Procaspase 8 In Vivo
Nie, Z., Bren, G. D., Vlahakis, S. R., Schimnich, A. A., Brenchley, J. M., Trushin, S. A., Warren, S. E., Schnepple, D. J., Kovacs, C. M., Loutfy, M. R., et al. (2007) · Journal of Virology · doi:10.1128/jvi.02798-06 · Cited by 69 · see citing works
Luminescent nanoparticles and their applications in the life sciences
Sreenivasan, V. K. A., Zvyagin, A. V., & Goldys, E. M. (2013) · Journal of Physics Condensed Matter · doi:10.1088/0953-8984/25/19/194101 · Cited by 68 · see citing works
Multicolor multicycle molecular profiling with quantum dots for single-cell analysis
Zrazhevskiy, P., True, L. D., & Gao, X. (2013) · Nature Protocols · doi:10.1038/nprot.2013.112 · Cited by 68 · see citing works
flow C lean: Automated identification and removal of fluorescence anomalies in flow cytometry data
Fletez‐Brant, K., Špidlen, J., Brinkman, R. R., Roederer, M., & Chattopadhyay, P. K. (2016) · Cytometry Part A · doi:10.1002/cyto.a.22837 · Cited by 68 · see citing works
Self-citationLee, H.-M., Shin, D.-M., Song, H.-M., Yuk, J.-M., Lee, Z.-W., Lee, S.-H., Hwang, S. M., Kim, J.-M., Lee, C.-S., & Jo, E.-K. (2009) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2009.05.010 · Cited by 67 · see citing works
Recent Advances in Diagnosis, Prevention, and Treatment of Human Respiratory Syncytial Virus
Bawage, S. S., Tiwari, P. M., Pillai, S., Dennis, V. A., & Singh, S. R. (2013) · Advances in Virology · doi:10.1155/2013/595768 · Cited by 64 · see citing works
Immune cell profiling to guide therapeutic decisions in rheumatic diseases
Ermann, J., Rao, D. A., Teslovich, N. C., Brenner, M. B., & Raychaudhuri, S. (2015) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2015.71 · Cited by 63 · see citing works
Nicholas, K. J., Greenplate, A. R., Flaherty, D. K., Matlock, B. K., Juan, J. S., Smith, R. M., Irish, J. M., & Kalams, S. A. (2015) · Cytometry Part A · doi:10.1002/cyto.a.22799 · Cited by 62 · see citing works
- Authors
- Chattopadhyay, P. K., Price, D. A., Harper, T. F., Betts, M. R., Yu, J., Gostick, E., Perfetto, S. P., Goepfert, P., Koup, R. A., De Rosa, S. C., Bruchez, M. P., & Roederer, M.
- Affiliations
- National Institutes of Health (US)
- University of Alabama at Birmingham (US)
- Carnegie Mellon University (US)
- Corresponding author
- Roederer, Mario
- ORCID
- Venue
- Nature Medicine
- Published
- 2006-07-23
- Volume
- 12
- Issue
- 8
- Pages
- 972-977
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W2072723772
- Cited by
- 372
- References
- 30
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 11 · 2023: 3 · 2022: 7 · 2021: 7 · 2020: 10 · 2019: 12 · 2018: 14 · 2017: 17 · 2016: 19 · 2015: 23 · 2014: 23 · 2013: 26 · 2012: 27
- FWCI
- 21.96
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (Z99 AI999999)
- National Institute of Biomedical Imaging and Bioengineering (R01EB000364)
- Topics
- Physical Sciences › Materials Science › Materials Chemistry › Quantum Dots Synthesis And Properties
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
- Keywords
- quantum dots, polychromatic flow cytometry, immunophenotyping, T cell phenotype, antigen-specific T cells, epitope-specific T cells, cell-mediated immunity, innate immune response
- MeSH terms
- Epitopes, Flow Cytometry, Fluorescent Dyes, HLA-DR Antigens, Humans, Major Histocompatibility Complex, Semiconductors, T-Lymphocytes, Immunophenotyping, Fluorescein-5-isothiocyanate, CD8 Antigens, CD3 Complex, Nanotechnology, Quantum Dots
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review