Abstract

We present a novel optical device developed for the monitoring of dynamic behavior in extended 3D-tissue models in various culture environments based on variations in their speckle patterns. The results presented point out the benefit of the technology in terms of detection, accuracy, sensitivity and a reasonable read-out speed as well as reproducibility for the measurements and monitoring of cardiac contractions. We show that the optical read-out technology is suitable for long time monitoring and for drug screening. The method is discussed and compared to other techniques, in particular calcium imaging. The device is flexible and easily adaptable to 2D and 3D-tissue model screenings using different culture environments. The technology can be parallelized for automated read-out of different multi-well-plate formats.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2019 (2)

B. Nugraha, M. F. Buono, L. von Boehmer, S. P. Hoerstrup, and M. Y. Emmert, “Human Cardiac Organoids for Disease Modeling”,” Clin. Pharmacol. Ther. 105(1), 79–85 (2019).
[Crossref]

C. Zuppinger, “3D Cardiac Cell Culture: A Critical Review of Current Technologies and Applications,” Front. Cardiovasc. Med. 6, 87 (2019).
[Crossref]

2018 (3)

C. L. Mummery, “Perspectives on the Use of Human Induced Pluripotent Stem Cell-Derived Cardiomyocytes in Biomedical Research,” Stem Cell Rep. 11(6), 1306–1311 (2018).
[Crossref]

M. Devarasetty, A. R. Mazzochi, and A. Skarda, “Applications of Bioengineered 3D Tissue and Tumor Organoids,” BioDrugs 32(1), 53–68 (2018).
[Crossref]

I. Moon, K. Jaferzadeh, E. Ahmadzadeh, and B. Javidi, “Automated quantitative analysis of multiple cardiomyocytes at the single-cell level with three-dimensional holographic imaging informatics,” J. Biophotonics 11(12), e201800116 (2018).
[Crossref]

2017 (3)

M. Devarasetty, S. Forsythe, T. D. Shupe, S. Soker, C. E. Bishop, A. Atala, and A. Skardal, “Optical Tracking and Digital Quantification of Beating Behavior in Bioengineered Human Cardiac Organoids,” Biosensors 7(4), 24 (2017).
[Crossref]

M. Gepp, R. Duckstein, F. Kayatz, N. Rodler, Z. Scheuerer, J. C. Neubauer, K. Lachmann, C. Stramm, A. Liebmann, M. Thomas, and H. Zimmermann, “Labbag - a versatile bag-based cultivation system for expansion, differentiation and cryopreservation of human stem cells,” Current Directions in Biomedical Engineering 3(2), 371–374 (2017).
[Crossref]

O. Sirenko, M. K. Hancock, C. Crittenden, M. Hammer, S. Keating, C. B. Carlson, and G. Chandy, “Phenotypic assays for characterizing compound effects on induced pluripotent stem cell-derived cardiac spheroids,” Assay Drug Dev. Technol. 15(6), 280–296 (2017).
[Crossref]

2016 (1)

E. Laurila, A. Ahola, J. Hyttinen, and K. Aalto-Setälä, “Methods for in vitro functional analysis of iPSC derived cardiomyocytes - Special focus on analyzing the mechanical beating behavior,” Biochim. Biophys. Acta, Mol. Cell Res. 1863(7), 1864–1872 (2016).
[Crossref]

2015 (3)

B. Rappaz, I. Moon, F. Yi, B. Javidi, P. Marquet, and G. Turcatti, “Automated multi-parameter measurement of cardiomyocytes dynamics with digital holographic microscopy,” Opt. Express 23(10), 13333–13347 (2015).
[Crossref]

N. Huebsch, P. Loskill, M. A. Mandegar, N. C. Marks, A. S. Sheehan, Z. Ma, A. Mathur, T. N. Nguyen, J. C. Yoo, L. M. Judge, C. I. Spencer, A. C. Chukka, C. R. Russell, P. L. So, B. R. Conklin, and K. E. Healy, “Automated Video-Based Analysis of Contractility and Calcium Flux in Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes Cultured over Different Spatial Scales,” Tissue Eng., Part C 21(5), 467–479 (2015).
[Crossref]

M. Zhang, J. S. Schulte, A. Heinick, I. Piccini, J. Rao, R. Quaranta, D. Zeuschner, D. Malan, K. P. Kim, A. Röpke, P. Sasse, M. Araúzo-Bravo, G. Seebohm, H. Schöler, L. Fabritz, P. Kirchhof, F. U. Müller, and B. Greber, “Universal cardiac induction of human pluripotent stem cells in two and three-dimensional formats: implications for in vitro maturation,” Stem Cells 33(5), 1456–1469 (2015).
[Crossref]

2014 (3)

Y. Zhou, S. Zhu, C. Cai, P. Yuan, C. Li, Y. Huang, and W. Wei, “High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells,” Nature 509(7501), 487–491 (2014).
[Crossref]

A. Ahola, A. L. Kiviaho, K. Larsson, M. Honkanen, K. Aalto-Setälä, and J. Hyttinen, “Video image-based analysis of single human induced pluripotent stem cell derived cardiomyocyte beating dynamics using digital image correlation,” BioMed. Eng. Online 13(1), 39 (2014).
[Crossref]

T. Hayakawa, T. Kunihiro, T. Ando, S. Kobayashi, E. Matsui, H. Yada, Y. Kanda, J. Kurokawa, and T. and Furukawa, “Image-based evaluation of contraction - relaxation kinetics of human-induced pluripotent stem cell-derived cardiomyocytes: Correlation and complementarity with extracellular electrophysiology,” J. Mol. Cell. Cardiol. 77, 178–191 (2014).
[Crossref]

2013 (2)

D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
[Crossref]

C. W. Scott, M. F. Peters, and Y. P. Dragan, “Human induced pluripotent stem cells and their use in drug discovery for toxicity testing,” Toxicol. Lett. 219(1), 49–58 (2013).
[Crossref]

2012 (3)

K. Basak, M. Manjunatha, and P. K. Dutta, “Review of laser speckle-based analysis in medical imaging,” Med. Biol. Eng. Comput. 50(6), 547–558 (2012).
[Crossref]

M. F. Peters, C. W. Scott, R. Ochalski, and Y. P. Dragan, “Evaluation of Cellular Impedance Measures of Cardiomyocyte Cultures for Drug Screening Applications,” Assay Drug Dev. Technol. 10(6), 525–532 (2012).
[Crossref]

Y. A. Abassi, B. Xi, N. Li, W. Ouyang, A. Seiler, M. Watzele, R. Kettenhofen, H. Bohlen, A. Ehlich, E. Kolossov, X. Wang, and X. Xu, “Dynamic monitoring of beating periodicity of stem cell-derived cardiomyocytes as a predictive tool for preclinical safety assessment,” Br. J. Pharmacol. 165(5), 1424–1441 (2012).
[Crossref]

2011 (7)

M. K. B. Jonsson, Q.-D. Wang, and B. Becker, “Impedance-based detection of beating rhythm and proarrhythmic effects of compounds on stem cell-derived cardiomyocytes,” Assay Drug Dev. Technol. 9(6), 589–599 (2011).
[Crossref]

A. E. M. Seiler and H. Spielmann, “The validated embryonic stem cell test to predict embryotoxicity in vitro,” Nat. Protoc. 6(7), 961–978 (2011).
[Crossref]

V. Planelles, F. Wolschendorf, and O. Kutsch, “Facts and Fiction: Cellular Models for High Throughput Screening for HIV-1 Reactivating,” Curr. HIV Res. 9(8), 568–578 (2011).
[Crossref]

J. T. Dimos, I. Griswold-Prenner, M. Grskovic, S. Irion, C. Johnson, and E. Vaisberg, “Induced Pluripotent Stem Cells as Human Disease Models,” Annu. Rep. Med. Chem. 46, 369–383 (2011).
[Crossref]

M. Drewitz, M. Helbling, N. Fried, M. Bieri, W. Moritz, J. Lichtenberg, and J. M. Kelm, “Towards automated production and drug sensitivity testing using scaffold-free spherical tumor microtissues,” Biotechnol. J. 6(12), 1488–1496 (2011).
[Crossref]

M. Chen, Y. Q. Lin, S. L. Xie, H. F. Wu, and J. F. Wang, “Enrichment of cardiac differentiation of mouse embryonic stem cells by optimizing the hanging drop method,” Biotechnol. Lett. 33(4), 853–858 (2011).
[Crossref]

J. T. Russell, “Imaging Calcium Signals in Vivo: A Powerful Tool in Physiology and Pharmacology,” Br. J. Pharmacol. 163(8), 1605–1625 (2011).
[Crossref]

2010 (1)

2009 (1)

A. Kamgoué, J. Ohayon, Y. Usson, L. Riou, and P. Tracqui, “Quantification of cardiomyocyte contraction based on image correlation analysis,” Cytometry, Part A 75A(4), 298–308 (2009).
[Crossref]

2007 (1)

F. Pampaloni, E. G. Reynaud, and E. H. Stelzer, “The third dimension bridges the gap between cell culture and live tissue,” Nat. Rev. Mol. Cell Biol. 8(10), 839–845 (2007).
[Crossref]

2003 (1)

A. Abbott, “Cell culture: biology's new dimension,” Nature 424(6951), 870–872 (2003).
[Crossref]

1996 (1)

J. A. Cole and M. H. Tinker, “Laser speckle spectroscopy - a new method for using small swimming organisms as biomonitors,” Bioimaging 4(4), 243–253 (1996).
[Crossref]

Aalto-Setälä, K.

E. Laurila, A. Ahola, J. Hyttinen, and K. Aalto-Setälä, “Methods for in vitro functional analysis of iPSC derived cardiomyocytes - Special focus on analyzing the mechanical beating behavior,” Biochim. Biophys. Acta, Mol. Cell Res. 1863(7), 1864–1872 (2016).
[Crossref]

A. Ahola, A. L. Kiviaho, K. Larsson, M. Honkanen, K. Aalto-Setälä, and J. Hyttinen, “Video image-based analysis of single human induced pluripotent stem cell derived cardiomyocyte beating dynamics using digital image correlation,” BioMed. Eng. Online 13(1), 39 (2014).
[Crossref]

Abassi, Y. A.

Y. A. Abassi, B. Xi, N. Li, W. Ouyang, A. Seiler, M. Watzele, R. Kettenhofen, H. Bohlen, A. Ehlich, E. Kolossov, X. Wang, and X. Xu, “Dynamic monitoring of beating periodicity of stem cell-derived cardiomyocytes as a predictive tool for preclinical safety assessment,” Br. J. Pharmacol. 165(5), 1424–1441 (2012).
[Crossref]

Abbott, A.

A. Abbott, “Cell culture: biology's new dimension,” Nature 424(6951), 870–872 (2003).
[Crossref]

Ahmadzadeh, E.

I. Moon, K. Jaferzadeh, E. Ahmadzadeh, and B. Javidi, “Automated quantitative analysis of multiple cardiomyocytes at the single-cell level with three-dimensional holographic imaging informatics,” J. Biophotonics 11(12), e201800116 (2018).
[Crossref]

Ahola, A.

E. Laurila, A. Ahola, J. Hyttinen, and K. Aalto-Setälä, “Methods for in vitro functional analysis of iPSC derived cardiomyocytes - Special focus on analyzing the mechanical beating behavior,” Biochim. Biophys. Acta, Mol. Cell Res. 1863(7), 1864–1872 (2016).
[Crossref]

A. Ahola, A. L. Kiviaho, K. Larsson, M. Honkanen, K. Aalto-Setälä, and J. Hyttinen, “Video image-based analysis of single human induced pluripotent stem cell derived cardiomyocyte beating dynamics using digital image correlation,” BioMed. Eng. Online 13(1), 39 (2014).
[Crossref]

and Furukawa, T.

T. Hayakawa, T. Kunihiro, T. Ando, S. Kobayashi, E. Matsui, H. Yada, Y. Kanda, J. Kurokawa, and T. and Furukawa, “Image-based evaluation of contraction - relaxation kinetics of human-induced pluripotent stem cell-derived cardiomyocytes: Correlation and complementarity with extracellular electrophysiology,” J. Mol. Cell. Cardiol. 77, 178–191 (2014).
[Crossref]

Ando, T.

T. Hayakawa, T. Kunihiro, T. Ando, S. Kobayashi, E. Matsui, H. Yada, Y. Kanda, J. Kurokawa, and T. and Furukawa, “Image-based evaluation of contraction - relaxation kinetics of human-induced pluripotent stem cell-derived cardiomyocytes: Correlation and complementarity with extracellular electrophysiology,” J. Mol. Cell. Cardiol. 77, 178–191 (2014).
[Crossref]

Araúzo-Bravo, M.

M. Zhang, J. S. Schulte, A. Heinick, I. Piccini, J. Rao, R. Quaranta, D. Zeuschner, D. Malan, K. P. Kim, A. Röpke, P. Sasse, M. Araúzo-Bravo, G. Seebohm, H. Schöler, L. Fabritz, P. Kirchhof, F. U. Müller, and B. Greber, “Universal cardiac induction of human pluripotent stem cells in two and three-dimensional formats: implications for in vitro maturation,” Stem Cells 33(5), 1456–1469 (2015).
[Crossref]

Atala, A.

M. Devarasetty, S. Forsythe, T. D. Shupe, S. Soker, C. E. Bishop, A. Atala, and A. Skardal, “Optical Tracking and Digital Quantification of Beating Behavior in Bioengineered Human Cardiac Organoids,” Biosensors 7(4), 24 (2017).
[Crossref]

Basak, K.

K. Basak, M. Manjunatha, and P. K. Dutta, “Review of laser speckle-based analysis in medical imaging,” Med. Biol. Eng. Comput. 50(6), 547–558 (2012).
[Crossref]

Becker, B.

M. K. B. Jonsson, Q.-D. Wang, and B. Becker, “Impedance-based detection of beating rhythm and proarrhythmic effects of compounds on stem cell-derived cardiomyocytes,” Assay Drug Dev. Technol. 9(6), 589–599 (2011).
[Crossref]

Bieri, M.

M. Drewitz, M. Helbling, N. Fried, M. Bieri, W. Moritz, J. Lichtenberg, and J. M. Kelm, “Towards automated production and drug sensitivity testing using scaffold-free spherical tumor microtissues,” Biotechnol. J. 6(12), 1488–1496 (2011).
[Crossref]

Bishop, C. E.

M. Devarasetty, S. Forsythe, T. D. Shupe, S. Soker, C. E. Bishop, A. Atala, and A. Skardal, “Optical Tracking and Digital Quantification of Beating Behavior in Bioengineered Human Cardiac Organoids,” Biosensors 7(4), 24 (2017).
[Crossref]

Bohlen, H.

Y. A. Abassi, B. Xi, N. Li, W. Ouyang, A. Seiler, M. Watzele, R. Kettenhofen, H. Bohlen, A. Ehlich, E. Kolossov, X. Wang, and X. Xu, “Dynamic monitoring of beating periodicity of stem cell-derived cardiomyocytes as a predictive tool for preclinical safety assessment,” Br. J. Pharmacol. 165(5), 1424–1441 (2012).
[Crossref]

Briers, D.

D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
[Crossref]

Buono, M. F.

B. Nugraha, M. F. Buono, L. von Boehmer, S. P. Hoerstrup, and M. Y. Emmert, “Human Cardiac Organoids for Disease Modeling”,” Clin. Pharmacol. Ther. 105(1), 79–85 (2019).
[Crossref]

Bursac, N.

Cai, C.

Y. Zhou, S. Zhu, C. Cai, P. Yuan, C. Li, Y. Huang, and W. Wei, “High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells,” Nature 509(7501), 487–491 (2014).
[Crossref]

Carlson, C. B.

O. Sirenko, M. K. Hancock, C. Crittenden, M. Hammer, S. Keating, C. B. Carlson, and G. Chandy, “Phenotypic assays for characterizing compound effects on induced pluripotent stem cell-derived cardiac spheroids,” Assay Drug Dev. Technol. 15(6), 280–296 (2017).
[Crossref]

Chandy, G.

O. Sirenko, M. K. Hancock, C. Crittenden, M. Hammer, S. Keating, C. B. Carlson, and G. Chandy, “Phenotypic assays for characterizing compound effects on induced pluripotent stem cell-derived cardiac spheroids,” Assay Drug Dev. Technol. 15(6), 280–296 (2017).
[Crossref]

Chen, M.

M. Chen, Y. Q. Lin, S. L. Xie, H. F. Wu, and J. F. Wang, “Enrichment of cardiac differentiation of mouse embryonic stem cells by optimizing the hanging drop method,” Biotechnol. Lett. 33(4), 853–858 (2011).
[Crossref]

Chukka, A. C.

N. Huebsch, P. Loskill, M. A. Mandegar, N. C. Marks, A. S. Sheehan, Z. Ma, A. Mathur, T. N. Nguyen, J. C. Yoo, L. M. Judge, C. I. Spencer, A. C. Chukka, C. R. Russell, P. L. So, B. R. Conklin, and K. E. Healy, “Automated Video-Based Analysis of Contractility and Calcium Flux in Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes Cultured over Different Spatial Scales,” Tissue Eng., Part C 21(5), 467–479 (2015).
[Crossref]

Cole, J. A.

J. A. Cole and M. H. Tinker, “Laser speckle spectroscopy - a new method for using small swimming organisms as biomonitors,” Bioimaging 4(4), 243–253 (1996).
[Crossref]

Conklin, B. R.

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Assay Drug Dev. Technol. (3)

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Supplementary Material (1)

NameDescription
» Visualization 1       Video of dynamic behavior of Speckle pattern of a cardio cell aggregate

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Figures (9)

Fig. 1.
Fig. 1. (A) Side view of hanging drops with a volume of 40 µl in a specific 96 well plate, (B) Microphotography of cardiomyocyte cell aggregates in a hanging drop, (C) Speckle pattern of a cardio cell aggregate.
Fig. 2.
Fig. 2. Contraction Reader device photography in its safety enclosure (A), schematic overview of the different elements constituting the optical device (B), Intuitive user interface for control, visualization and signal monitoring (C).
Fig. 3.
Fig. 3. Monitored signal of the speckle pattern depicted in Fig. 1(C). The period of the contractions is of 3.9 ± 0.8s with an SNR of about 20 dB.
Fig. 4.
Fig. 4. Speckle patterns recorded at (A) −1 mm, (B) 0 mm (see Visualization 1), (C) +1 mm defocusing. The Speckle grain size decreases significantly compared to sample-in-focus conditions. Large grains lead to strong signals. However, if defocused detection is necessary, e.g. for wider illumination areas, the signal can still be extracted from the finer patterns
Fig. 5.
Fig. 5. 10 min time monitoring of the contractions of cell aggregates in hanging drop (A). Zoom of the contractions signal from 0 to 60 s (B), from 300 to 360 s (C), and from 540 to 600 s (D). Average frequencies measured at 60, 360 and 600 s (E). The contractions period stays almost constant at 2.35 ± 0.05 s. Note the variations in amplitude and shape. The contraction spikes are partially negative.
Fig. 6.
Fig. 6. Addition of Isoprenalin, a stimulant compound. Contractions were measured without addition (A), the period of the contractions is 2 ± 0.05 s and with addition (B), the period is reduced to 0.9 ± 0.05 s, the beating rhythm is faster.
Fig. 7.
Fig. 7. Data showing an overlay of two independent contraction traces (see arrows) with two independent frequencies. This is due to two separated contracting sites within the same cardiac tissue model.
Fig. 8.
Fig. 8. Comparison measurements of contractions on several plate formats and geometries in 2D and 3D tissue models. In a 96 and 384 hanging drop well plate, in a 96-V and -U bottom well plate and in a LabBag.
Fig. 9.
Fig. 9. Comparison of the contraction signal measured by Calcium Imaging (A) and by the Contraction Reader (B). Both traces were recorded on the same specimen, but not simultaneouisly.

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