Abstract

Optical cell manipulation has become increasingly valuable in cell-based assays. In this paper, we demonstrate the translational and rotational manipulation of filamentous cells using multiple cooperative microrobots automatically driven by holographic optical tweezers. The photodamage of the cells due to direct irradiation of the laser beam can be effectively avoided. The proposed method will enable fruitful biomedical applications where precise cell manipulation and less photodamage are required.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref]
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    [Crossref]
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    [Crossref]
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    [Crossref]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  26. S. Hu and D. Sun, “Automatic transportation of biological cells with a robot-tweezer manipulation system,” Int. J. Robot. Res. 30(14), 1681–1694 (2011).
    [Crossref]
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    [Crossref]
  28. T. D’Orazio, C. Guaragnella, M. Leo, and A. Distante, “A new algorithm for ball recognition using circle Hough transform and neural classifier,” Pattern Recognit. 37(3), 393–408 (2004).
    [Crossref]
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    [Crossref] [PubMed]

2019 (1)

A. Bunea and J. Glückstad, “Strategies for optical trapping in biological samples: aiming at microrobotic surgeons,” Laser Photonics Rev. 13(4), 1800227 (2019).
[Crossref]

2018 (1)

S. Nocentini, C. Parmeggiani, D. Martella, and D. S. Wiersma, “Optically driven soft micro robotics,” Adv. Opt. Mater. 6(14), 1800207 (2018).
[Crossref]

2017 (4)

E. Avci, M. Grammatikopoulou, and G. Z. Yang, “Laser-printing and 3D optical-control of untethered microrobots,” Adv. Opt. Mater. 5(19), 1700031 (2017).
[Crossref]

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

S. Hu, S. Chen, S. Chen, G. Xu, and D. Sun, “Automated transportation of multiple cell types using a robot-aided cell manipulation system with holographic optical tweezers,” IEEE/ASME Trans. Mechatron. 22(2), 804–814 (2017).
[Crossref]

X. Li and C. C. Cheah, “A simple trapping and manipulation method of biological cell using robot-assisted optical tweezers: singular perturbation approach,” IEEE Trans. Ind. Electron. 64(2), 1656–1663 (2017).
[Crossref]

2016 (3)

M. J. Villangca, D. Palima, A. R. Bañas, and J. Glückstad, “Light-driven micro-tool equipped with a syringe function,” Light Sci. Appl. 5(9), e16148 (2016).
[Crossref] [PubMed]

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

B. L. Aekbote, T. Fekete, J. Jacak, G. Vizsnyiczai, P. Ormos, and L. Kelemen, “Surface-modified complex SU-8 microstructures for indirect optical manipulation of single cells,” Biomed. Opt. Express 7(1), 45–56 (2016).
[Crossref] [PubMed]

2014 (2)

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

J. Wang and A. W. Poon, “Unfolding a design rule for microparticle buffering and dropping in microring-resonator-based add-drop devices,” Lab Chip 14(8), 1426–1436 (2014).
[Crossref] [PubMed]

2013 (3)

A. Arias, S. Etcheverry, P. Solano, J. P. Staforelli, M. J. Gallardo, H. Rubinsztein-Dunlop, and C. Saavedra, “Simultaneous rotation, orientation and displacement control of birefringent microparticles in holographic optical tweezers,” Opt. Express 21(1), 102–111 (2013).
[Crossref] [PubMed]

H. Chen, C. Wang, and Y. Lou, “Flocking multiple microparticles with automatically controlled optical tweezers: solutions and experiments,” IEEE Trans. Biomed. Eng. 60(6), 1518–1527 (2013).
[Crossref] [PubMed]

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

2012 (4)

K. Sugiura and S. Itoh, “Single-cell confocal spectrometry of a filamentous cyanobacterium Nostoc at room and cryogenic temperature. Diversity and differentiation of pigment systems in 311 cells,” Plant Cell Physiol. 53(8), 1492–1506 (2012).
[Crossref] [PubMed]

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

M. A. Miled and M. Sawan, “Dielectrophoresis-based integrated Lab-on-Chip for nano and micro-particles manipulation and capacitive detection,” IEEE Trans. Biomed. Circuits Syst. 6(2), 120–132 (2012).
[Crossref] [PubMed]

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

2011 (3)

S. Hu and D. Sun, “Automatic transportation of biological cells with a robot-tweezer manipulation system,” Int. J. Robot. Res. 30(14), 1681–1694 (2011).
[Crossref]

G. Markou and D. Georgakakis, “Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: A review,” Appl. Energy 88(10), 3389–3401 (2011).
[Crossref]

B. Koss, S. Chowdhury, T. Aabo, S. K. Gupta, and W. Losert, “Indirect optical gripping with triplet traps,” J. Opt. Soc. Am. B 28(5), 982–985 (2011).
[Crossref]

2007 (1)

B. Hu, G. Yang, W. Zhao, Y. Zhang, and J. Zhao, “MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120,” Mol. Microbiol. 63(6), 1640–1652 (2007).
[Crossref] [PubMed]

2006 (2)

2004 (1)

T. D’Orazio, C. Guaragnella, M. Leo, and A. Distante, “A new algorithm for ball recognition using circle Hough transform and neural classifier,” Pattern Recognit. 37(3), 393–408 (2004).
[Crossref]

2003 (1)

F. Arai, H. Maruyama, T. Sakami, A. Ichikawa, and T. Fukuda, “Pinpoint injection of microtools for minimaly invasive micromanipulation of microbe by laser trap,” IEEE/ASME Trans. Mechatron. 8(1), 3–9 (2003).
[Crossref]

1996 (1)

Y. Liu, G. J. Sonek, M. W. Berns, and B. J. Tromberg, “Physiological monitoring of optically trapped cells: assessing the effects of confinement by 1064-nm laser tweezers using microfluorometry,” Biophys. J. 71(4), 2158–2167 (1996).
[Crossref] [PubMed]

1995 (1)

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-in microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

1994 (1)

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct. 23(1), 247–285 (1994).
[Crossref] [PubMed]

1986 (1)

Aabo, T.

Acasandrei, A. M.

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Aekbote, B. L.

Arai, F.

F. Arai, H. Maruyama, T. Sakami, A. Ichikawa, and T. Fukuda, “Pinpoint injection of microtools for minimaly invasive micromanipulation of microbe by laser trap,” IEEE/ASME Trans. Mechatron. 8(1), 3–9 (2003).
[Crossref]

Arias, A.

Ashkin, A.

Avci, E.

E. Avci, M. Grammatikopoulou, and G. Z. Yang, “Laser-printing and 3D optical-control of untethered microrobots,” Adv. Opt. Mater. 5(19), 1700031 (2017).
[Crossref]

Bañas, A. R.

M. J. Villangca, D. Palima, A. R. Bañas, and J. Glückstad, “Light-driven micro-tool equipped with a syringe function,” Light Sci. Appl. 5(9), e16148 (2016).
[Crossref] [PubMed]

Benkovic, S. J.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Berns, M. W.

Y. Liu, G. J. Sonek, M. W. Berns, and B. J. Tromberg, “Physiological monitoring of optically trapped cells: assessing the effects of confinement by 1064-nm laser tweezers using microfluorometry,” Biophys. J. 71(4), 2158–2167 (1996).
[Crossref] [PubMed]

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-in microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

Bjorkholm, J. E.

Block, S. M.

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct. 23(1), 247–285 (1994).
[Crossref] [PubMed]

Bunea, A.

A. Bunea and J. Glückstad, “Strategies for optical trapping in biological samples: aiming at microrobotic surgeons,” Laser Photonics Rev. 13(4), 1800227 (2019).
[Crossref]

Casper, R. F.

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

Chait, R.

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Chapin, S. C.

Cheah, C. C.

X. Li and C. C. Cheah, “A simple trapping and manipulation method of biological cell using robot-assisted optical tweezers: singular perturbation approach,” IEEE Trans. Ind. Electron. 64(2), 1656–1663 (2017).
[Crossref]

Chen, H.

H. Chen, C. Wang, and Y. Lou, “Flocking multiple microparticles with automatically controlled optical tweezers: solutions and experiments,” IEEE Trans. Biomed. Eng. 60(6), 1518–1527 (2013).
[Crossref] [PubMed]

Chen, S.

S. Hu, S. Chen, S. Chen, G. Xu, and D. Sun, “Automated transportation of multiple cell types using a robot-aided cell manipulation system with holographic optical tweezers,” IEEE/ASME Trans. Mechatron. 22(2), 804–814 (2017).
[Crossref]

S. Hu, S. Chen, S. Chen, G. Xu, and D. Sun, “Automated transportation of multiple cell types using a robot-aided cell manipulation system with holographic optical tweezers,” IEEE/ASME Trans. Mechatron. 22(2), 804–814 (2017).
[Crossref]

Chen, Z.

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

Chiang, I. K.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Chowdhury, S.

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

B. Koss, S. Chowdhury, T. Aabo, S. K. Gupta, and W. Losert, “Indirect optical gripping with triplet traps,” J. Opt. Soc. Am. B 28(5), 982–985 (2011).
[Crossref]

Chu, S.

D’Orazio, T.

T. D’Orazio, C. Guaragnella, M. Leo, and A. Distante, “A new algorithm for ball recognition using circle Hough transform and neural classifier,” Pattern Recognit. 37(3), 393–408 (2004).
[Crossref]

Dhar, N.

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Dinescu, M.

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Ding, X.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Distante, A.

T. D’Orazio, C. Guaragnella, M. Leo, and A. Distante, “A new algorithm for ball recognition using circle Hough transform and neural classifier,” Pattern Recognit. 37(3), 393–408 (2004).
[Crossref]

Dufresne, E. R.

Dziedzic, J. M.

Esfandiari, N.

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

Etcheverry, S.

Fekete, T.

Fukuda, T.

F. Arai, H. Maruyama, T. Sakami, A. Ichikawa, and T. Fukuda, “Pinpoint injection of microtools for minimaly invasive micromanipulation of microbe by laser trap,” IEEE/ASME Trans. Mechatron. 8(1), 3–9 (2003).
[Crossref]

Gallardo, M. J.

Georgakakis, D.

G. Markou and D. Georgakakis, “Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: A review,” Appl. Energy 88(10), 3389–3401 (2011).
[Crossref]

Germain, V.

Gibson, G.

Glückstad, J.

A. Bunea and J. Glückstad, “Strategies for optical trapping in biological samples: aiming at microrobotic surgeons,” Laser Photonics Rev. 13(4), 1800227 (2019).
[Crossref]

M. J. Villangca, D. Palima, A. R. Bañas, and J. Glückstad, “Light-driven micro-tool equipped with a syringe function,” Light Sci. Appl. 5(9), e16148 (2016).
[Crossref] [PubMed]

Grammatikopoulou, M.

E. Avci, M. Grammatikopoulou, and G. Z. Yang, “Laser-printing and 3D optical-control of untethered microrobots,” Adv. Opt. Mater. 5(19), 1700031 (2017).
[Crossref]

Guaragnella, C.

T. D’Orazio, C. Guaragnella, M. Leo, and A. Distante, “A new algorithm for ball recognition using circle Hough transform and neural classifier,” Pattern Recognit. 37(3), 393–408 (2004).
[Crossref]

Gupta, S. K.

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

B. Koss, S. Chowdhury, T. Aabo, S. K. Gupta, and W. Losert, “Indirect optical gripping with triplet traps,” J. Opt. Soc. Am. B 28(5), 982–985 (2011).
[Crossref]

Hu, B.

B. Hu, G. Yang, W. Zhao, Y. Zhang, and J. Zhao, “MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120,” Mol. Microbiol. 63(6), 1640–1652 (2007).
[Crossref] [PubMed]

Hu, S.

S. Hu, S. Chen, S. Chen, G. Xu, and D. Sun, “Automated transportation of multiple cell types using a robot-aided cell manipulation system with holographic optical tweezers,” IEEE/ASME Trans. Mechatron. 22(2), 804–814 (2017).
[Crossref]

S. Hu and D. Sun, “Automatic transportation of biological cells with a robot-tweezer manipulation system,” Int. J. Robot. Res. 30(14), 1681–1694 (2011).
[Crossref]

Huang, T. J.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Ichikawa, A.

F. Arai, H. Maruyama, T. Sakami, A. Ichikawa, and T. Fukuda, “Pinpoint injection of microtools for minimaly invasive micromanipulation of microbe by laser trap,” IEEE/ASME Trans. Mechatron. 8(1), 3–9 (2003).
[Crossref]

Itoh, S.

K. Sugiura and S. Itoh, “Single-cell confocal spectrometry of a filamentous cyanobacterium Nostoc at room and cryogenic temperature. Diversity and differentiation of pigment systems in 311 cells,” Plant Cell Physiol. 53(8), 1492–1506 (2012).
[Crossref] [PubMed]

Jacak, J.

Kelemen, L.

Kiraly, B.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

König, K.

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-in microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

Koss, B.

Leach, J.

Leibler, S.

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Leo, M.

T. D’Orazio, C. Guaragnella, M. Leo, and A. Distante, “A new algorithm for ball recognition using circle Hough transform and neural classifier,” Pattern Recognit. 37(3), 393–408 (2004).
[Crossref]

Leung, C.

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

Li, S.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Li, X.

X. Li and C. C. Cheah, “A simple trapping and manipulation method of biological cell using robot-assisted optical tweezers: singular perturbation approach,” IEEE Trans. Ind. Electron. 64(2), 1656–1663 (2017).
[Crossref]

Liang, H.

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-in microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

Lin, S. C.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Liu, B.

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

Liu, Y.

Y. Liu, G. J. Sonek, M. W. Berns, and B. J. Tromberg, “Physiological monitoring of optically trapped cells: assessing the effects of confinement by 1064-nm laser tweezers using microfluorometry,” Biophys. J. 71(4), 2158–2167 (1996).
[Crossref] [PubMed]

Losert, W.

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

B. Koss, S. Chowdhury, T. Aabo, S. K. Gupta, and W. Losert, “Indirect optical gripping with triplet traps,” J. Opt. Soc. Am. B 28(5), 982–985 (2011).
[Crossref]

Lou, Y.

H. Chen, C. Wang, and Y. Lou, “Flocking multiple microparticles with automatically controlled optical tweezers: solutions and experiments,” IEEE Trans. Biomed. Eng. 60(6), 1518–1527 (2013).
[Crossref] [PubMed]

Lu, Z.

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

Luculescu, C. R.

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Markou, G.

G. Markou and D. Georgakakis, “Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: A review,” Appl. Energy 88(10), 3389–3401 (2011).
[Crossref]

Martella, D.

S. Nocentini, C. Parmeggiani, D. Martella, and D. S. Wiersma, “Optically driven soft micro robotics,” Adv. Opt. Mater. 6(14), 1800207 (2018).
[Crossref]

Maruyama, H.

F. Arai, H. Maruyama, T. Sakami, A. Ichikawa, and T. Fukuda, “Pinpoint injection of microtools for minimaly invasive micromanipulation of microbe by laser trap,” IEEE/ASME Trans. Mechatron. 8(1), 3–9 (2003).
[Crossref]

McKinney, J. D.

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Mihailescu, M.

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Miled, M. A.

M. A. Miled and M. Sawan, “Dielectrophoresis-based integrated Lab-on-Chip for nano and micro-particles manipulation and capacitive detection,” IEEE Trans. Biomed. Circuits Syst. 6(2), 120–132 (2012).
[Crossref] [PubMed]

Miles, M.

Mustaciosu, C. C.

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Nocentini, S.

S. Nocentini, C. Parmeggiani, D. Martella, and D. S. Wiersma, “Optically driven soft micro robotics,” Adv. Opt. Mater. 6(14), 1800207 (2018).
[Crossref]

Ormos, P.

Padgett, M.

Palima, D.

M. J. Villangca, D. Palima, A. R. Bañas, and J. Glückstad, “Light-driven micro-tool equipped with a syringe function,” Light Sci. Appl. 5(9), e16148 (2016).
[Crossref] [PubMed]

Parmeggiani, C.

S. Nocentini, C. Parmeggiani, D. Martella, and D. S. Wiersma, “Optically driven soft micro robotics,” Adv. Opt. Mater. 6(14), 1800207 (2018).
[Crossref]

Paun, I. A.

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Poon, A. W.

J. Wang and A. W. Poon, “Unfolding a design rule for microparticle buffering and dropping in microring-resonator-based add-drop devices,” Lab Chip 14(8), 1426–1436 (2014).
[Crossref] [PubMed]

Qin, K.

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

Robert, D.

Rubinsztein-Dunlop, H.

Saavedra, C.

Sakami, T.

F. Arai, H. Maruyama, T. Sakami, A. Ichikawa, and T. Fukuda, “Pinpoint injection of microtools for minimaly invasive micromanipulation of microbe by laser trap,” IEEE/ASME Trans. Mechatron. 8(1), 3–9 (2003).
[Crossref]

Sawan, M.

M. A. Miled and M. Sawan, “Dielectrophoresis-based integrated Lab-on-Chip for nano and micro-particles manipulation and capacitive detection,” IEEE Trans. Biomed. Circuits Syst. 6(2), 120–132 (2012).
[Crossref] [PubMed]

Schneider, K.

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Shi, J.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Signorino-Gelo, F.

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Solano, P.

Sonek, G. J.

Y. Liu, G. J. Sonek, M. W. Berns, and B. J. Tromberg, “Physiological monitoring of optically trapped cells: assessing the effects of confinement by 1064-nm laser tweezers using microfluorometry,” Biophys. J. 71(4), 2158–2167 (1996).
[Crossref] [PubMed]

Staforelli, J. P.

Sugiura, K.

K. Sugiura and S. Itoh, “Single-cell confocal spectrometry of a filamentous cyanobacterium Nostoc at room and cryogenic temperature. Diversity and differentiation of pigment systems in 311 cells,” Plant Cell Physiol. 53(8), 1492–1506 (2012).
[Crossref] [PubMed]

Sun, D.

S. Hu, S. Chen, S. Chen, G. Xu, and D. Sun, “Automated transportation of multiple cell types using a robot-aided cell manipulation system with holographic optical tweezers,” IEEE/ASME Trans. Mechatron. 22(2), 804–814 (2017).
[Crossref]

S. Hu and D. Sun, “Automatic transportation of biological cells with a robot-tweezer manipulation system,” Int. J. Robot. Res. 30(14), 1681–1694 (2011).
[Crossref]

Sun, Y.

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

Svec, P.

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

Svoboda, K.

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct. 23(1), 247–285 (1994).
[Crossref] [PubMed]

Thakur, A.

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

Tromberg, B. J.

Y. Liu, G. J. Sonek, M. W. Berns, and B. J. Tromberg, “Physiological monitoring of optically trapped cells: assessing the effects of confinement by 1064-nm laser tweezers using microfluorometry,” Biophys. J. 71(4), 2158–2167 (1996).
[Crossref] [PubMed]

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-in microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

Villangca, M. J.

M. J. Villangca, D. Palima, A. R. Bañas, and J. Glückstad, “Light-driven micro-tool equipped with a syringe function,” Light Sci. Appl. 5(9), e16148 (2016).
[Crossref] [PubMed]

Vizsnyiczai, G.

Wakamoto, Y.

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Wang, C.

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

H. Chen, C. Wang, and Y. Lou, “Flocking multiple microparticles with automatically controlled optical tweezers: solutions and experiments,” IEEE Trans. Biomed. Eng. 60(6), 1518–1527 (2013).
[Crossref] [PubMed]

Wang, J.

J. Wang and A. W. Poon, “Unfolding a design rule for microparticle buffering and dropping in microring-resonator-based add-drop devices,” Lab Chip 14(8), 1426–1436 (2014).
[Crossref] [PubMed]

Whyte, G.

Wiersma, D. S.

S. Nocentini, C. Parmeggiani, D. Martella, and D. S. Wiersma, “Optically driven soft micro robotics,” Adv. Opt. Mater. 6(14), 1800207 (2018).
[Crossref]

Xiang, C.

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

Xie, H.

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

Xu, G.

S. Hu, S. Chen, S. Chen, G. Xu, and D. Sun, “Automated transportation of multiple cell types using a robot-aided cell manipulation system with holographic optical tweezers,” IEEE/ASME Trans. Mechatron. 22(2), 804–814 (2017).
[Crossref]

Yang, G.

B. Hu, G. Yang, W. Zhao, Y. Zhang, and J. Zhao, “MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120,” Mol. Microbiol. 63(6), 1640–1652 (2007).
[Crossref] [PubMed]

Yang, G. Z.

E. Avci, M. Grammatikopoulou, and G. Z. Yang, “Laser-printing and 3D optical-control of untethered microrobots,” Adv. Opt. Mater. 5(19), 1700031 (2017).
[Crossref]

Yu, M.

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

Yue, H.

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Zamfirescu, M.

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Zhang, X.

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

Zhang, Y.

B. Hu, G. Yang, W. Zhao, Y. Zhang, and J. Zhao, “MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120,” Mol. Microbiol. 63(6), 1640–1652 (2007).
[Crossref] [PubMed]

Zhao, J.

B. Hu, G. Yang, W. Zhao, Y. Zhang, and J. Zhao, “MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120,” Mol. Microbiol. 63(6), 1640–1652 (2007).
[Crossref] [PubMed]

Zhao, W.

B. Hu, G. Yang, W. Zhao, Y. Zhang, and J. Zhao, “MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120,” Mol. Microbiol. 63(6), 1640–1652 (2007).
[Crossref] [PubMed]

Adv. Opt. Mater. (2)

S. Nocentini, C. Parmeggiani, D. Martella, and D. S. Wiersma, “Optically driven soft micro robotics,” Adv. Opt. Mater. 6(14), 1800207 (2018).
[Crossref]

E. Avci, M. Grammatikopoulou, and G. Z. Yang, “Laser-printing and 3D optical-control of untethered microrobots,” Adv. Opt. Mater. 5(19), 1700031 (2017).
[Crossref]

Annu. Rev. Biophys. Biomol. Struct. (1)

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct. 23(1), 247–285 (1994).
[Crossref] [PubMed]

Appl. Energy (1)

G. Markou and D. Georgakakis, “Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: A review,” Appl. Energy 88(10), 3389–3401 (2011).
[Crossref]

Appl. Surf. Sci. (1)

I. A. Paun, M. Zamfirescu, C. R. Luculescu, A. M. Acasandrei, C. C. Mustaciosu, M. Mihailescu, and M. Dinescu, “Electrically responsive microreservoires for controllable delivery of dexamethasone in bone tissue engineering,” Appl. Surf. Sci. 392, 321–331 (2017).
[Crossref]

Biomed. Opt. Express (1)

Biophys. J. (1)

Y. Liu, G. J. Sonek, M. W. Berns, and B. J. Tromberg, “Physiological monitoring of optically trapped cells: assessing the effects of confinement by 1064-nm laser tweezers using microfluorometry,” Biophys. J. 71(4), 2158–2167 (1996).
[Crossref] [PubMed]

IEEE Trans. Autom. Sci. Eng. (1)

S. Chowdhury, A. Thakur, P. Svec, C. Wang, W. Losert, and S. K. Gupta, “Automated manipulation of biological cells using gripper formations controlled by optical tweezers,” IEEE Trans. Autom. Sci. Eng. 11(2), 338–347 (2014).
[Crossref]

IEEE Trans. Biomed. Circuits Syst. (1)

M. A. Miled and M. Sawan, “Dielectrophoresis-based integrated Lab-on-Chip for nano and micro-particles manipulation and capacitive detection,” IEEE Trans. Biomed. Circuits Syst. 6(2), 120–132 (2012).
[Crossref] [PubMed]

IEEE Trans. Biomed. Eng. (2)

X. Zhang, C. Leung, Z. Lu, N. Esfandiari, R. F. Casper, and Y. Sun, “Controlled aspiration and positioning of biological cells in a micropipette,” IEEE Trans. Biomed. Eng. 59(4), 1032–1040 (2012).
[Crossref] [PubMed]

H. Chen, C. Wang, and Y. Lou, “Flocking multiple microparticles with automatically controlled optical tweezers: solutions and experiments,” IEEE Trans. Biomed. Eng. 60(6), 1518–1527 (2013).
[Crossref] [PubMed]

IEEE Trans. Ind. Electron. (1)

X. Li and C. C. Cheah, “A simple trapping and manipulation method of biological cell using robot-assisted optical tweezers: singular perturbation approach,” IEEE Trans. Ind. Electron. 64(2), 1656–1663 (2017).
[Crossref]

IEEE/ASME Trans. Mechatron. (2)

S. Hu, S. Chen, S. Chen, G. Xu, and D. Sun, “Automated transportation of multiple cell types using a robot-aided cell manipulation system with holographic optical tweezers,” IEEE/ASME Trans. Mechatron. 22(2), 804–814 (2017).
[Crossref]

F. Arai, H. Maruyama, T. Sakami, A. Ichikawa, and T. Fukuda, “Pinpoint injection of microtools for minimaly invasive micromanipulation of microbe by laser trap,” IEEE/ASME Trans. Mechatron. 8(1), 3–9 (2003).
[Crossref]

Int. J. Robot. Res. (1)

S. Hu and D. Sun, “Automatic transportation of biological cells with a robot-tweezer manipulation system,” Int. J. Robot. Res. 30(14), 1681–1694 (2011).
[Crossref]

J. Opt. Soc. Am. B (1)

Lab Chip (1)

J. Wang and A. W. Poon, “Unfolding a design rule for microparticle buffering and dropping in microring-resonator-based add-drop devices,” Lab Chip 14(8), 1426–1436 (2014).
[Crossref] [PubMed]

Laser Photonics Rev. (1)

A. Bunea and J. Glückstad, “Strategies for optical trapping in biological samples: aiming at microrobotic surgeons,” Laser Photonics Rev. 13(4), 1800227 (2019).
[Crossref]

Light Sci. Appl. (1)

M. J. Villangca, D. Palima, A. R. Bañas, and J. Glückstad, “Light-driven micro-tool equipped with a syringe function,” Light Sci. Appl. 5(9), e16148 (2016).
[Crossref] [PubMed]

Lixue Xuebao (1)

M. Yu, Z. Chen, C. Xiang, B. Liu, H. Xie, and K. Qin, “Microfluidic-based single cell trapping using a combination of stagnation point flow and physical barrier,” Lixue Xuebao 32(3), 422–429 (2016).
[Crossref]

Mol. Microbiol. (1)

B. Hu, G. Yang, W. Zhao, Y. Zhang, and J. Zhao, “MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120,” Mol. Microbiol. 63(6), 1640–1652 (2007).
[Crossref] [PubMed]

Nature (1)

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-in microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

Opt. Express (3)

Opt. Lett. (1)

Pattern Recognit. (1)

T. D’Orazio, C. Guaragnella, M. Leo, and A. Distante, “A new algorithm for ball recognition using circle Hough transform and neural classifier,” Pattern Recognit. 37(3), 393–408 (2004).
[Crossref]

Plant Cell Physiol. (1)

K. Sugiura and S. Itoh, “Single-cell confocal spectrometry of a filamentous cyanobacterium Nostoc at room and cryogenic temperature. Diversity and differentiation of pigment systems in 311 cells,” Plant Cell Physiol. 53(8), 1492–1506 (2012).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (1)

X. Ding, S. C. Lin, B. Kiraly, H. Yue, S. Li, I. K. Chiang, J. Shi, S. J. Benkovic, and T. J. Huang, “On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves,” Proc. Natl. Acad. Sci. U.S.A. 109(28), 11105–11109 (2012).
[Crossref] [PubMed]

Science (1)

Y. Wakamoto, N. Dhar, R. Chait, K. Schneider, F. Signorino-Gelo, S. Leibler, and J. D. McKinney, “Dynamic persistence of antibiotic-stressed mycobacteria,” Science 339(6115), 91–95 (2013).
[Crossref] [PubMed]

Supplementary Material (2)

NameDescription
» Visualization 1       Translational manipulation of the filamentous cells.
» Visualization 2       Rotation of the filamentous cells.

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Figures (8)

Fig. 1
Fig. 1 Schematic of cell manipulation with HOT.
Fig. 2
Fig. 2 (a) Schematic of the designed microtool. (b) Front view of SolidWorks engineering drawing of the designed microtool.
Fig. 3
Fig. 3 (a) 3D printing principle of the microrobot. (b) Micrograph of the microrobots coated with 5 nm-thick gold layers under an ESEM.
Fig. 4
Fig. 4 Recognition of the microrobot through image processing. (a) Original color image. (b) Filtered grayscale image. (c) Edges of the microrobot. (d) Binary image. (e) Location of two handling spheres of the microrobot. (f) Pose of the microrobot.
Fig. 5
Fig. 5 (a) Two microrobots that are driven to push a filamentous cell. (b) Two microrobots that are driven to rotate a filamentous cell.
Fig. 6
Fig. 6 Translational movement of the filamentous cells. (a) t = 0 s. (b) t = 5 s. (c) t = 10 s. (d) t = 15 s (see Visualization 1).
Fig. 7
Fig. 7 Rotation of the filamentous cells. (a) t = 0 s. (b) t = 7 s. (c) t = 14 s. (d) t = 21 s (see Visualization 2).
Fig. 8
Fig. 8 Manipulation of the filamentous cells. (a) “‖”-shaped cell pattern. (b) “⊥”-shaped cell pattern. (c) The cells are immobilized with two microrobots.