Label-free high-throughput cell screening in flow

Ata Mahjoubfar; Claire Chen; Kayvan R. Niazi; Shahrooz Rabizadeh; Bahram Jalali

doi:10.1364/BOE.4.001618

Label-free high-throughput cell screening in flow

Ata Mahjoubfar, Claire Chen, Kayvan R. Niazi, Shahrooz Rabizadeh, and Bahram Jalali

Biomedical Optics Express
Vol. 4,
Issue 9,
pp. 1618-1625
(2013)
•https://doi.org/10.1364/BOE.4.001618

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Ata Mahjoubfar, Claire Chen, Kayvan R. Niazi, Shahrooz Rabizadeh, and Bahram Jalali, "Label-free high-throughput cell screening in flow," Biomed. Opt. Express 4, 1618-1625 (2013)

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Related Topics
Table of Contents Category
- Cell Studies
Optics & Photonics Topics
?

The topics in this list come from the OSA Optics and Photonics Topics applied to this article.
Previously assigned OCIS codes
- Phase retrieval (100.5070)
- Microscopy (170.0180)
- Cell analysis (170.1530)
- Medical optics instrumentation (170.3890)
- Ultrafast technology (170.7160)

About this Article
History
- Original Manuscript: June 14, 2013
- Revised Manuscript: July 24, 2013
- Manuscript Accepted: August 6, 2013
- Published: August 12, 2013

Accessible

Open Access

Abstract

Flow cytometry is a powerful tool for cell counting and biomarker detection in biotechnology and medicine especially with regards to blood analysis. Standard flow cytometers perform cell type classification both by estimating size and granularity of cells using forward- and side-scattered light signals and through the collection of emission spectra of fluorescently-labeled cells. However, cell surface labeling as a means of marking cells is often undesirable as many reagents negatively impact cellular viability or provide activating/inhibitory signals, which can alter the behavior of the desired cellular subtypes for downstream applications or analysis. To eliminate the need for labeling, we introduce a label-free imaging-based flow cytometer that measures size and cell protein concentration simultaneously either as a stand-alone instrument or as an add-on to conventional flow cytometers. Cell protein concentration adds a parameter to cell classification, which improves the specificity and sensitivity of flow cytometers without the requirement of cell labeling. This system uses coherent dispersive Fourier transform to perform phase imaging at flow speeds as high as a few meters per second.

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References

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|
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[Crossref] [PubMed]
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[Crossref] [PubMed]
K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. Di Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” Proc. Natl. Acad. Sci. U.S.A. 109(29), 11630–11635 (2012).
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[Crossref]
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2013 (2)

K. Goda and B. Jalali, “Dispersive Fourier transformation for fast continuous single-shot measurements,” Nat. Photonics 7(2), 102–112 (2013).
[Crossref]

A. Mahjoubfar, K. Goda, C. Wang, A. Fard, J. Adam, D. R. Gossett, A. Ayazi, E. Sollier, O. Malik, E. Chen, Y. Liu, R. Brown, N. Sarkhosh, D. Di Carlo, and B. Jalali, “3D ultrafast laser scanner,” Proc. SPIE 8611,Frontiers in Ultrafast Optics: Biomedical, Scientific, and Industrial Applications XIII, 86110N, 86110N-7 (2013).
[Crossref]

2012 (7)

K. Goda, A. Mahjoubfar, C. Wang, A. Fard, J. Adam, D. R. Gossett, A. Ayazi, E. Sollier, O. Malik, E. Chen, Y. Liu, R. Brown, N. Sarkhosh, D. Di Carlo, and B. Jalali, “Hybrid Dispersion Laser Scanner,” Sci Rep 2, 445 (2012).
[Crossref] [PubMed]

K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. Di Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” Proc. Natl. Acad. Sci. U.S.A. 109(29), 11630–11635 (2012).
[Crossref] [PubMed]

S. S. Gorthi and E. Schonbrun, “Phase imaging flow cytometry using a focus-stack collecting microscope,” Opt. Lett. 37(4), 707–709 (2012).
[Crossref] [PubMed]

J. Chun, T. A. Zangle, T. Kolarova, R. S. Finn, M. A. Teitell, and J. Reed, “Rapidly quantifying drug sensitivity of dispersed and clumped breast cancer cells by mass profiling,” Analyst (Lond.) 137(23), 5495–5498 (2012).
[Crossref] [PubMed]

K. G. Phillips, A. Kolatkar, K. J. Rees, R. Rigg, D. Marrinucci, M. Luttgen, K. Bethel, P. Kuhn, and O. J. T. McCarty, “Quantification of cellular volume and sub-cellular density fluctuations: comparison of normal peripheral blood cells and circulating tumor cells identified in a breast cancer patient,” Front Oncol 2, 96 (2012).
[PubMed]

K. G. Phillips, C. R. Velasco, J. Li, A. Kolatkar, M. Luttgen, K. Bethel, B. Duggan, P. Kuhn, and O. J. T. McCarty, “Optical quantification of cellular mass, volume, and density of circulating tumor cells identified in an ovarian cancer patient,” Front Oncol 2, 72 (2012).
[PubMed]

V. Gupta, I. Jafferji, M. Garza, V. O. Melnikova, D. K. Hasegawa, R. Pethig, and D. W. Davis, “ApoStream™, a new dielectrophoretic device for antibody independent isolation and recovery of viable cancer cells from blood,” Biomicrofluidics 6(2), 024133 (2012).
[Crossref] [PubMed]

2011 (4)

W. H. Grover, A. K. Bryan, M. Diez-Silva, S. Suresh, J. M. Higgins, and S. R. Manalis, “Measuring single-cell density,” Proc. Natl. Acad. Sci. U.S.A. 108(27), 10992–10996 (2011).
[Crossref] [PubMed]

R. K. Bista, S. Uttam, P. Wang, K. Staton, S. Choi, C. J. Bakkenist, D. J. Hartman, R. E. Brand, and Y. Liu, “Quantification of nanoscale nuclear refractive index changes during the cell cycle,” J. Biomed. Opt. 16(7), 070503 (2011).
[Crossref] [PubMed]

A. M. Fard, A. Mahjoubfar, K. Goda, D. R. Gossett, D. Di Carlo, and B. Jalali, “Nomarski serial time-encoded amplified microscopy for high-speed contrast-enhanced imaging of transparent media,” Biomed. Opt. Express 2(12), 3387–3392 (2011).
[Crossref] [PubMed]

A. Mahjoubfar, K. Goda, A. Ayazi, A. Fard, S. H. Kim, and B. Jalali, “High-speed nanometer-resolved imaging vibrometer and velocimeter,” Appl. Phys. Lett. 98(10), 101107 (2011).
[Crossref]

2009 (2)

K. Goda, K. K. Tsia, and B. Jalali, “Serial time-encoded amplified imaging for real-time observation of fast dynamic phenomena,” Nature 458(7242), 1145–1149 (2009).
[Crossref] [PubMed]

N. Lue, W. Choi, G. Popescu, Z. Yaqoob, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Live cell refractometry using Hilbert phase microscopy and confocal reflectance microscopy,” J. Phys. Chem. A 113(47), 13327–13330 (2009).
[Crossref] [PubMed]

2007 (1)

X. J. Liang, A. Q. Liu, C. S. Lim, T. C. Ayi, and P. H. Yap, “Determining refractive index of single living cell using an integrated microchip,” Sens. Actuator A-Phys. 133(2), 349–354 (2007).
[Crossref]

2006 (1)

G. Popescu, T. Ikeda, K. Goda, C. A. Best-Popescu, M. Laposata, S. Manley, R. R. Dasari, K. Badizadegan, and M. S. Feld, “Optical Measurement of Cell Membrane Tension,” Phys. Rev. Lett. 97(21), 218101 (2006).
[Crossref] [PubMed]

2005 (3)

T. Ikeda, G. Popescu, R. R. Dasari, and M. S. Feld, “Hilbert phase microscopy for investigating fast dynamics in transparent systems,” Opt. Lett. 30(10), 1165–1167 (2005).
[Crossref] [PubMed]

B. Rappaz, P. Marquet, E. Cuche, Y. Emery, C. Depeursinge, and P. Magistretti, “Measurement of the integral refractive index and dynamic cell morphometry of living cells with digital holographic microscopy,” Opt. Express 13(23), 9361–9373 (2005).
[Crossref] [PubMed]

C. L. Curl, C. J. Bellair, T. Harris, B. E. Allman, P. J. Harris, A. G. Stewart, A. Roberts, K. A. Nugent, and L. M. D. Delbridge, “Refractive index measurement in viable cells using quantitative phase-amplitude microscopy and confocal microscopy,” Cytometry A 65(1), 88–92 (2005).
[Crossref] [PubMed]

2000 (1)

G. Vona, A. Sabile, M. Louha, V. Sitruk, S. Romana, K. Schütze, F. Capron, D. Franco, M. Pazzagli, M. Vekemans, B. Lacour, C. Bréchot, and P. Paterlini-Bréchot, “Isolation by size of epithelial tumor cells : a new method for the immunomorphological and molecular characterization of circulatingtumor cells,” Am. J. Pathol. 156(1), 57–63 (2000).
[Crossref] [PubMed]

1998 (1)

D. Maric, I. Maric, and J. L. Barker, “Buoyant density gradient fractionation and flow cytometric analysis of embryonic rat cortical neurons and progenitor cells,” Methods 16(3), 247–259 (1998).
[Crossref] [PubMed]

1990 (1)

S. J. Martin, J. G. Bradley, and T. G. Cotter, “HL-60 cells induced to differentiate towards neutrophils subsequently die via apoptosis,” Clin. Exp. Immunol. 79(3), 448–453 (1990).
[Crossref] [PubMed]

1985 (1)

D. H. Tycko, M. H. Metz, E. A. Epstein, and A. Grinbaum, “Flow-cytometric light scattering measurement of red blood cell volume and hemoglobin concentration,” Appl. Opt. 24(9), 1355–1365 (1985).
[Crossref] [PubMed]

1982 (1)

A. H. Wyllie and R. G. Morris, “Hormone-induced cell death. Purification ad properties of thymocytes undergoing apoptosis after glucocorticoid treatment,” Am. J. Pathol. 109(1), 78–87 (1982).
[PubMed]

1981 (1)

K. Bosslet, R. Ruffmann, P. Altevogt, and V. Schirrmacher, “A rapid method for the isolation of metastasizing tumour cells from internal organs with the help of isopycnic density-gradient centrifugation in Percoll,” Br. J. Cancer 44(3), 356–362 (1981).
[Crossref] [PubMed]

1979 (1)

J. E. Mrema, G. H. Campbell, R. Miranda, A. L. Jaramillo, and K. H. Rieckmann, “Concentration and separation of erythrocytes infected with Plasmodium falciparum by gradient centrifugation,” Bull. World Health Organ. 57(1), 133–138 (1979).
[PubMed]

1977 (1)

P. Whur, H. Koppel, C. M. Urquhart, and D. C. Williams, “Substrate retention of fractured retraction fibres during detachment of trypsinized BHK21 fibroblasts,” J. Cell Sci. 24, 265–273 (1977).
[PubMed]

1974 (1)

J. P. Revel, P. Hoch, and D. Ho, “Adhesion of culture cells to their substratum,” Exp. Cell Res. 84(1), 207–218 (1974).
[Crossref] [PubMed]

1972 (1)

D. A. Wolff and H. Pertoft, “Separation of HeLa cells by colloidal silica density gradient centrifugation. I. Separation and partial synchrony of mitotic cells,” J. Cell Biol. 55(3), 579–585 (1972).
[Crossref] [PubMed]

1954 (1)

R. Barer and S. Joseph, “Refractometry of living cells,” J. Cell Sci. 95, 399–423 (1954).

Adam, J.

Allman, B. E.

Altevogt, P.

Ayazi, A.

A. Mahjoubfar, K. Goda, A. Ayazi, A. Fard, S. H. Kim, and B. Jalali, “High-speed nanometer-resolved imaging vibrometer and velocimeter,” Appl. Phys. Lett. 98(10), 101107 (2011).
[Crossref]

Ayi, T. C.

Badizadegan, K.

Bakkenist, C. J.

Barer, R.

R. Barer and S. Joseph, “Refractometry of living cells,” J. Cell Sci. 95, 399–423 (1954).

Barker, J. L.

Bellair, C. J.

Best-Popescu, C. A.

Bethel, K.

Bista, R. K.

Bosslet, K.

Brackbill, N.

Bradley, J. G.

Brand, R. E.

Bréchot, C.

Brown, R.

Bryan, A. K.

Campbell, G. H.

Capron, F.

Chen, E.

Choi, S.

Choi, W.

Chun, J.

Cotter, T. G.

Cuche, E.

Curl, C. L.

Dasari, R. R.

T. Ikeda, G. Popescu, R. R. Dasari, and M. S. Feld, “Hilbert phase microscopy for investigating fast dynamics in transparent systems,” Opt. Lett. 30(10), 1165–1167 (2005).
[Crossref] [PubMed]

Davis, D. W.

Delbridge, L. M. D.

Depeursinge, C.

Di Carlo, D.

Diez-Silva, M.

Duggan, B.

Emery, Y.

Epstein, E. A.

Fard, A.

A. Mahjoubfar, K. Goda, A. Ayazi, A. Fard, S. H. Kim, and B. Jalali, “High-speed nanometer-resolved imaging vibrometer and velocimeter,” Appl. Phys. Lett. 98(10), 101107 (2011).
[Crossref]

Fard, A. M.

Feld, M. S.

T. Ikeda, G. Popescu, R. R. Dasari, and M. S. Feld, “Hilbert phase microscopy for investigating fast dynamics in transparent systems,” Opt. Lett. 30(10), 1165–1167 (2005).
[Crossref] [PubMed]

Finn, R. S.

Franco, D.

Garza, M.

Goda, K.

K. Goda and B. Jalali, “Dispersive Fourier transformation for fast continuous single-shot measurements,” Nat. Photonics 7(2), 102–112 (2013).
[Crossref]

A. Mahjoubfar, K. Goda, A. Ayazi, A. Fard, S. H. Kim, and B. Jalali, “High-speed nanometer-resolved imaging vibrometer and velocimeter,” Appl. Phys. Lett. 98(10), 101107 (2011).
[Crossref]

K. Goda, K. K. Tsia, and B. Jalali, “Serial time-encoded amplified imaging for real-time observation of fast dynamic phenomena,” Nature 458(7242), 1145–1149 (2009).
[Crossref] [PubMed]

Gorthi, S. S.

S. S. Gorthi and E. Schonbrun, “Phase imaging flow cytometry using a focus-stack collecting microscope,” Opt. Lett. 37(4), 707–709 (2012).
[Crossref] [PubMed]

Gossett, D. R.

Grinbaum, A.

Grover, W. H.

Gupta, V.

Harris, P. J.

Harris, T.

Hartman, D. J.

Hasegawa, D. K.

Higgins, J. M.

Ho, D.

J. P. Revel, P. Hoch, and D. Ho, “Adhesion of culture cells to their substratum,” Exp. Cell Res. 84(1), 207–218 (1974).
[Crossref] [PubMed]

Hoch, P.

J. P. Revel, P. Hoch, and D. Ho, “Adhesion of culture cells to their substratum,” Exp. Cell Res. 84(1), 207–218 (1974).
[Crossref] [PubMed]

Hur, S. C.

Ikeda, T.

T. Ikeda, G. Popescu, R. R. Dasari, and M. S. Feld, “Hilbert phase microscopy for investigating fast dynamics in transparent systems,” Opt. Lett. 30(10), 1165–1167 (2005).
[Crossref] [PubMed]

Jafferji, I.

Jalali, B.

K. Goda and B. Jalali, “Dispersive Fourier transformation for fast continuous single-shot measurements,” Nat. Photonics 7(2), 102–112 (2013).
[Crossref]

A. Mahjoubfar, K. Goda, A. Ayazi, A. Fard, S. H. Kim, and B. Jalali, “High-speed nanometer-resolved imaging vibrometer and velocimeter,” Appl. Phys. Lett. 98(10), 101107 (2011).
[Crossref]

K. Goda, K. K. Tsia, and B. Jalali, “Serial time-encoded amplified imaging for real-time observation of fast dynamic phenomena,” Nature 458(7242), 1145–1149 (2009).
[Crossref] [PubMed]

Jaramillo, A. L.

Joseph, S.

R. Barer and S. Joseph, “Refractometry of living cells,” J. Cell Sci. 95, 399–423 (1954).

Kim, S. H.

A. Mahjoubfar, K. Goda, A. Ayazi, A. Fard, S. H. Kim, and B. Jalali, “High-speed nanometer-resolved imaging vibrometer and velocimeter,” Appl. Phys. Lett. 98(10), 101107 (2011).
[Crossref]

Kolarova, T.

Kolatkar, A.

Koppel, H.

Kuhn, P.

Lacour, B.

Laposata, M.

Li, J.

Liang, X. J.

Lim, C. S.

Liu, A. Q.

Liu, Y.

Lonappan, C. K.

Louha, M.

Lue, N.

Luttgen, M.

Magistretti, P.

Mahjoubfar, A.

A. Mahjoubfar, K. Goda, A. Ayazi, A. Fard, S. H. Kim, and B. Jalali, “High-speed nanometer-resolved imaging vibrometer and velocimeter,” Appl. Phys. Lett. 98(10), 101107 (2011).
[Crossref]

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Fig. 1

Optical setup of Coherent-STEAM; A Coherent-STEAM setup is formed by combination of STEAM and a Michelson interferometer. A pair of diffraction gratings generates a 1D rainbow with different wavelength components imaging different points on the cells flowing in a microfluidic channel. A pellicle beam-splitter and two identical long working-distance objective lenses are used to form the interferometer for phase measurement. Back apertures of objective lenses are fully illuminated with each wavelength component of the broadband mode-locked laser pulses to ensure diffraction-limited resolution. An amplified time-stretch system chirps, stretches, and amplifies each pulse, so that different wavelength components reach the photodetector serially. A very shallow microfluidic channel with hydrodynamic focusing is designed and fabricated to align cells within the focal depth of the system.

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Fig. 2

Digital signal processing of Coherent-STEAM; (a) The photodetector output signal is digitized and recorded by an ADC. This signal shows sequential laser pulses. (b) Each pulse is saved separately as a frame for further processing. (c) The analytic form of high-frequency components of each pulse is generated using Hilbert transformation, and the phase component of this analytic form is extracted. (d) An unwrapping algorithm is used to fix unrealistic phase jumps, and the result shows an approximately linear phase increase. (e) If the phase component of the interferometer fringe frequency is removed, the phase induced by cells in optical pulse can be seen. (f) Many of these line images generated from subsequent frames are used to form a spatial map of optical path difference in two dimensions, which is used for cell characterization.

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Fig. 3

Calibration with NIST traceable beads; Polystyrene beads with a NIST traceable diameter of 5 μm are used to calibrate the image processing algorithm for size measurements. (a) A custom designed image processing algorithm in CellProfiler software is used to find the beads in spatial map of optical path difference and measure the diameter. (b) Histogram of bead diameters demonstrates the measured size distribution has an expected mean of 5 µm and a standard deviation within the range of optical resolution limit. (c) Since all the beads are made out of the same material, the coefficient of variation for refractive indices (0.014/1.57 = 0.89%) is much smaller than that of diameters (0.405/5.06 = 8.00%).

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Fig. 4

Cell classification based on size and protein concentration measurement by Coherent-STEAM; Images of (a) SW480 and (b) OTII cells taken by Coherent-STEAM setup show that they are spherical. (c) Scattering plot of cell protein concentration versus diameter is shown for OTII (blue) and SW480 (green) cells. (d) Comparison of the ROC curves of size measurement only (purple line) to that of simultaneous size and protein concentration measurement (orange line) shows significant improvement in sensitivity.

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Equations (4)

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Δ φ (t) = unwrap (\arg (I_{B P} (t) + j \cdot {\hat{I}}_{B P} (t))) - 2 π f_{m} t - φ_{0}

O P D (x, y) = \frac{λ (x)}{2 π} Δ φ (x, y)

O P D (x, y) = 2 Δ n_{c e l l} \cdot t (x, y)

Δ n_{c e l l} = \frac{\iint_{c e l l} O P D (x, y) d x d y}{2 V}