Abstract

Fluorescence and bioluminescence are widely used to study biological systems from a molecular to a whole organism level. However, their broadband emission is often a bottleneck for sensitive spectral measurements and multiplexing. To overcome the limitation, the emitters can be coupled with optical cavity modes to generate narrow spectral lines. Here we demonstrate several types of emitter–resonator complexes made of fluorescent or bioluminescent proteins and artificially or naturally formed optical resonators. We engineered cells to express green fluorescent protein (GFP) fused with ABHD5, which binds to oil or lipid droplets supporting whispering gallery modes (WGMs). The genetically integrated complexes feature well-defined WGM spectral peaks. We measured WGM peaks from GFP-coated BaTiO3 beads (2.56 μm in diameter) during mitosis. Finally, we demonstrate cavity-enhanced bioluminescence using luciferase-coated beads and biochemical excitation. The ability to tailor spontaneous emission via cavity resonance inside biological systems should have applications in biological sensing, imaging, and cell tagging.

© 2017 Optical Society of America

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    [Crossref]

2016 (2)

M. Humar, S. J. J. Kwok, M. Choi, S. Cho, A. K. Yetisen, and S.-H. Yun, “Towards biomaterial-based implantable photonic devices,” Nanophotonics 5, 60–80 (2016).

W. B. Rogers, W. M. Shih, and V. N. Manoharan, “Using DNA to program the self-assembly of colloidal nanoparticles and microparticles,” Nat. Rev. Mater. 1, 16008 (2016).
[Crossref]

2015 (4)

Y. R. Kim, S. Kim, J. W. Choi, S. Y. Choi, S.-H. Lee, H. Kim, S. K. Hahn, G. Y. Koh, and S. H. Yun, “Bioluminescence-activated deep-tissue photodynamic therapy of cancer,” Theranostics 5, 805–817 (2015).
[Crossref]

N. Riesen, T. Reynolds, A. François, M. R. Henderson, and T. M. Monro, “Q-factor limits for far-field detection of whispering gallery modes in active microspheres,” Opt. Express 23, 28896–28904 (2015).
[Crossref]

M. Humar and S. H. Yun, “Intracellular microlasers,” Nat. Photonics 9, 572–576 (2015).
[Crossref]

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15, 5647–5652 (2015).
[Crossref]

2014 (3)

A. Jonas, A. Kiraz, A. Jonáš, M. Aas, Y. Karadag, S. Manioğlu, S. Anand, D. McGloin, H. Bayraktar, and A. Kiraz, “In vitro and in vivo biolasing of fluorescent proteins suspended in liquid microdroplet cavities,” Lab Chip 14, 3093–3100 (2014).
[Crossref]

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14, 4590–4595 (2014).
[Crossref]

M. C. Gather and S. H. Yun, “Bio-optimized energy transfer in densely packed fluorescent protein enables near-maximal luminescence and solid-state lasers,” Nat. Commun. 5, 5722 (2014).
[Crossref]

2013 (3)

A. R. Thiam, R. V. Farese, and T. C. Walther, “The biophysics and cell biology of lipid droplets,” Nat. Rev. Mol. Cell Biol. 14, 775–786 (2013).
[Crossref]

S. Nizamoglu, M. C. Gather, and S. H. Yun, “All-biomaterial laser using vitamin and biopolymers,” Adv. Mater. 25, 5943–5947 (2013).
[Crossref]

X. Wu, Q. Chen, Y. Sun, and X. Fan, “Bio-inspired optofluidic lasers with luciferin,” Appl. Phys. Lett. 102, 11–13 (2013).

2012 (1)

M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
[Crossref]

2011 (2)

2010 (1)

J. A. Fan, C. Wu, K. Bao, J. Bao, R. Bardhan, N. J. Halas, V. N. Manoharan, P. Nordlander, G. Shvets, and F. Capasso, “Self-assembled plasmonic nanoparticle clusters,” Science 328, 1135–1138 (2010).
[Crossref]

2009 (1)

M. Himmelhaus and A. Francois, “In vitro sensing of biomechanical forces in live cells by a whispering gallery mode biosensor,” Biosens. Bioelectron. 25, 418–427 (2009).
[Crossref]

2007 (2)

R. M. Kramer, W. J. Crookes-Goodson, and R. R. Naik, “The self-organizing properties of squid reflectin protein,” Nat. Mater. 6, 533–538 (2007).
[Crossref]

A. M. Loening, A. M. Wu, and S. S. Gambhir, “Red-shifted Renilla reniformis luciferase variants for imaging in living subjects,” Nat. Methods 4, 641–643 (2007).
[Crossref]

2006 (2)

P. W. K. Rothemund, “Folding DNA to create nanoscale shapes and patterns,” Nature 440, 297–302 (2006).
[Crossref]

M. L. Gorodetsky and A. E. Fomin, “Geometrical theory of whispering-gallery modes,” IEEE J. Sel. Top. Quantum Electron. 12, 33–39 (2006).
[Crossref]

2004 (2)

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

T. Yamaguchi, N. Omatsu, S. Matsushita, and T. Osumi, “CGI-58 interacts with perilipin and is localized to lipid droplets, possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome,” J. Biol. Chem. 279, 30490–30497 (2004).
[Crossref]

2002 (1)

C. H. Contag and M. H. Bachmann, “Advances in in vivo bioluminescence imaging of gene expression,” Annu. Rev. Biomed. Eng. 4, 235–260 (2002).
[Crossref]

2001 (1)

B. Gayral, “Controlling spontaneous emission dynamics in semiconductor micro cavities,” Ann. Phys. 26, 1–135 (2001).

1998 (2)

S. Holler, N. L. Goddard, and S. Arnold, “Spontaneous emission spectra from microdroplets,” J. Chem. Phys. 108, 6545–6547 (1998).
[Crossref]

A. R. Ribeiro, R. M. Santos, L. M. Rosário, and M. H. Gil, “Immobilization of luciferase from a firefly lantern extract on glass strips as an alternative strategy for luminescent detection of ATP,” J. Biolumin. Chemilumin. 13, 371–378 (1998).
[Crossref]

1997 (1)

S. Arnold, “Cavity-enhanced fluorescence decay rates from microdroplets,” J. Chem. Phys. 106, 8280–8282 (1997).
[Crossref]

1992 (1)

G. J. Cannon and J. A. Swanson, “The macrophage capacity for phagocytosis,” J. Cell Sci. 101, 907–913 (1992).

1991 (1)

A. J. Campillo, J. D. Eversole, and H.-B. Lin, “Cavity quantum electrodynamic enhancement of stimulated emission in microdroplets,” Phys. Rev. Lett. 67, 437–440 (1991).
[Crossref]

1980 (1)

R. E. Benner, P. W. Barber, J. F. Owen, and R. K. Chang, “Observation of structure resonances in the fluorescence-spectra from microspheres,” Phys. Rev. Lett. 44, 475–478 (1980).
[Crossref]

Aas, M.

A. Jonas, A. Kiraz, A. Jonáš, M. Aas, Y. Karadag, S. Manioğlu, S. Anand, D. McGloin, H. Bayraktar, and A. Kiraz, “In vitro and in vivo biolasing of fluorescent proteins suspended in liquid microdroplet cavities,” Lab Chip 14, 3093–3100 (2014).
[Crossref]

Anand, S.

A. Jonas, A. Kiraz, A. Jonáš, M. Aas, Y. Karadag, S. Manioğlu, S. Anand, D. McGloin, H. Bayraktar, and A. Kiraz, “In vitro and in vivo biolasing of fluorescent proteins suspended in liquid microdroplet cavities,” Lab Chip 14, 3093–3100 (2014).
[Crossref]

Arnold, S.

S. Holler, N. L. Goddard, and S. Arnold, “Spontaneous emission spectra from microdroplets,” J. Chem. Phys. 108, 6545–6547 (1998).
[Crossref]

S. Arnold, “Cavity-enhanced fluorescence decay rates from microdroplets,” J. Chem. Phys. 106, 8280–8282 (1997).
[Crossref]

Bachmann, M. H.

C. H. Contag and M. H. Bachmann, “Advances in in vivo bioluminescence imaging of gene expression,” Annu. Rev. Biomed. Eng. 4, 235–260 (2002).
[Crossref]

Bao, J.

J. A. Fan, C. Wu, K. Bao, J. Bao, R. Bardhan, N. J. Halas, V. N. Manoharan, P. Nordlander, G. Shvets, and F. Capasso, “Self-assembled plasmonic nanoparticle clusters,” Science 328, 1135–1138 (2010).
[Crossref]

Bao, K.

J. A. Fan, C. Wu, K. Bao, J. Bao, R. Bardhan, N. J. Halas, V. N. Manoharan, P. Nordlander, G. Shvets, and F. Capasso, “Self-assembled plasmonic nanoparticle clusters,” Science 328, 1135–1138 (2010).
[Crossref]

Barber, P. W.

R. E. Benner, P. W. Barber, J. F. Owen, and R. K. Chang, “Observation of structure resonances in the fluorescence-spectra from microspheres,” Phys. Rev. Lett. 44, 475–478 (1980).
[Crossref]

Bardhan, R.

J. A. Fan, C. Wu, K. Bao, J. Bao, R. Bardhan, N. J. Halas, V. N. Manoharan, P. Nordlander, G. Shvets, and F. Capasso, “Self-assembled plasmonic nanoparticle clusters,” Science 328, 1135–1138 (2010).
[Crossref]

Bayraktar, H.

A. Jonas, A. Kiraz, A. Jonáš, M. Aas, Y. Karadag, S. Manioğlu, S. Anand, D. McGloin, H. Bayraktar, and A. Kiraz, “In vitro and in vivo biolasing of fluorescent proteins suspended in liquid microdroplet cavities,” Lab Chip 14, 3093–3100 (2014).
[Crossref]

Benink, H. A.

M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
[Crossref]

Benner, R. E.

R. E. Benner, P. W. Barber, J. F. Owen, and R. K. Chang, “Observation of structure resonances in the fluorescence-spectra from microspheres,” Phys. Rev. Lett. 44, 475–478 (1980).
[Crossref]

Bhattacharyya, S.

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

Binkowski, B. F.

M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
[Crossref]

Brasaemle, D. L.

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

Butler, B. L.

M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
[Crossref]

Campbell, E. C.

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15, 5647–5652 (2015).
[Crossref]

Campillo, A. J.

A. J. Campillo, J. D. Eversole, and H.-B. Lin, “Cavity quantum electrodynamic enhancement of stimulated emission in microdroplets,” Phys. Rev. Lett. 67, 437–440 (1991).
[Crossref]

Cannon, G. J.

G. J. Cannon and J. A. Swanson, “The macrophage capacity for phagocytosis,” J. Cell Sci. 101, 907–913 (1992).

Capasso, F.

J. A. Fan, C. Wu, K. Bao, J. Bao, R. Bardhan, N. J. Halas, V. N. Manoharan, P. Nordlander, G. Shvets, and F. Capasso, “Self-assembled plasmonic nanoparticle clusters,” Science 328, 1135–1138 (2010).
[Crossref]

Chang, R. K.

R. E. Benner, P. W. Barber, J. F. Owen, and R. K. Chang, “Observation of structure resonances in the fluorescence-spectra from microspheres,” Phys. Rev. Lett. 44, 475–478 (1980).
[Crossref]

Chen, Q.

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14, 4590–4595 (2014).
[Crossref]

X. Wu, Q. Chen, Y. Sun, and X. Fan, “Bio-inspired optofluidic lasers with luciferin,” Appl. Phys. Lett. 102, 11–13 (2013).

Cho, S.

M. Humar, S. J. J. Kwok, M. Choi, S. Cho, A. K. Yetisen, and S.-H. Yun, “Towards biomaterial-based implantable photonic devices,” Nanophotonics 5, 60–80 (2016).

Choi, J. W.

Y. R. Kim, S. Kim, J. W. Choi, S. Y. Choi, S.-H. Lee, H. Kim, S. K. Hahn, G. Y. Koh, and S. H. Yun, “Bioluminescence-activated deep-tissue photodynamic therapy of cancer,” Theranostics 5, 805–817 (2015).
[Crossref]

Choi, M.

M. Humar, S. J. J. Kwok, M. Choi, S. Cho, A. K. Yetisen, and S.-H. Yun, “Towards biomaterial-based implantable photonic devices,” Nanophotonics 5, 60–80 (2016).

Choi, S. Y.

Y. R. Kim, S. Kim, J. W. Choi, S. Y. Choi, S.-H. Lee, H. Kim, S. K. Hahn, G. Y. Koh, and S. H. Yun, “Bioluminescence-activated deep-tissue photodynamic therapy of cancer,” Theranostics 5, 805–817 (2015).
[Crossref]

Cohen, A. W.

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

Contag, C. H.

C. H. Contag and M. H. Bachmann, “Advances in in vivo bioluminescence imaging of gene expression,” Annu. Rev. Biomed. Eng. 4, 235–260 (2002).
[Crossref]

Crookes-Goodson, W. J.

R. M. Kramer, W. J. Crookes-Goodson, and R. R. Naik, “The self-organizing properties of squid reflectin protein,” Nat. Mater. 6, 533–538 (2007).
[Crossref]

Dolios, G.

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M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15, 5647–5652 (2015).
[Crossref]

Shapiro, L.

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

Shih, W. M.

W. B. Rogers, W. M. Shih, and V. N. Manoharan, “Using DNA to program the self-assembly of colloidal nanoparticles and microparticles,” Nat. Rev. Mater. 1, 16008 (2016).
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J. A. Fan, C. Wu, K. Bao, J. Bao, R. Bardhan, N. J. Halas, V. N. Manoharan, P. Nordlander, G. Shvets, and F. Capasso, “Self-assembled plasmonic nanoparticle clusters,” Science 328, 1135–1138 (2010).
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Slater, M. R.

M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
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Steude, A.

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15, 5647–5652 (2015).
[Crossref]

Subramanian, V.

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
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Sun, Y.

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14, 4590–4595 (2014).
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X. Wu, Q. Chen, Y. Sun, and X. Fan, “Bio-inspired optofluidic lasers with luciferin,” Appl. Phys. Lett. 102, 11–13 (2013).

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B. Kay, S. Thai, and V. Volgina, “High-throughput biotinylation of proteins,” in High Throughput Protein Expression and Purification, S. Doyle, ed., Vol. 498 of Methods in Molecular Biology (Humana, 2009), pp. 185–198.

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A. R. Thiam, R. V. Farese, and T. C. Walther, “The biophysics and cell biology of lipid droplets,” Nat. Rev. Mol. Cell Biol. 14, 775–786 (2013).
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M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
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M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
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M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
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B. Kay, S. Thai, and V. Volgina, “High-throughput biotinylation of proteins,” in High Throughput Protein Expression and Purification, S. Doyle, ed., Vol. 498 of Methods in Molecular Biology (Humana, 2009), pp. 185–198.

Walther, T. C.

A. R. Thiam, R. V. Farese, and T. C. Walther, “The biophysics and cell biology of lipid droplets,” Nat. Rev. Mol. Cell Biol. 14, 775–786 (2013).
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V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

V. Subramanian, A. Rothenberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, D. L. Brasaemle, A. Rotlienberg, C. Gomez, A. W. Cohen, A. Garcia, S. Bhattacharyya, L. Shapiro, G. Dolios, R. Wang, M. P. Lisanti, and D. L. Brasaemle, “Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes,” J. Biol. Chem. 279, 42062–42071 (2004).
[Crossref]

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M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
[Crossref]

Wood, M. G.

M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
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A. M. Loening, A. M. Wu, and S. S. Gambhir, “Red-shifted Renilla reniformis luciferase variants for imaging in living subjects,” Nat. Methods 4, 641–643 (2007).
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J. A. Fan, C. Wu, K. Bao, J. Bao, R. Bardhan, N. J. Halas, V. N. Manoharan, P. Nordlander, G. Shvets, and F. Capasso, “Self-assembled plasmonic nanoparticle clusters,” Science 328, 1135–1138 (2010).
[Crossref]

Wu, X.

X. Wu, Q. Chen, Y. Sun, and X. Fan, “Bio-inspired optofluidic lasers with luciferin,” Appl. Phys. Lett. 102, 11–13 (2013).

Yamaguchi, T.

T. Yamaguchi, N. Omatsu, S. Matsushita, and T. Osumi, “CGI-58 interacts with perilipin and is localized to lipid droplets, possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome,” J. Biol. Chem. 279, 30490–30497 (2004).
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M. Humar, S. J. J. Kwok, M. Choi, S. Cho, A. K. Yetisen, and S.-H. Yun, “Towards biomaterial-based implantable photonic devices,” Nanophotonics 5, 60–80 (2016).

Yun, S. H.

Y. R. Kim, S. Kim, J. W. Choi, S. Y. Choi, S.-H. Lee, H. Kim, S. K. Hahn, G. Y. Koh, and S. H. Yun, “Bioluminescence-activated deep-tissue photodynamic therapy of cancer,” Theranostics 5, 805–817 (2015).
[Crossref]

M. Humar and S. H. Yun, “Intracellular microlasers,” Nat. Photonics 9, 572–576 (2015).
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M. C. Gather and S. H. Yun, “Bio-optimized energy transfer in densely packed fluorescent protein enables near-maximal luminescence and solid-state lasers,” Nat. Commun. 5, 5722 (2014).
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S. Nizamoglu, M. C. Gather, and S. H. Yun, “All-biomaterial laser using vitamin and biopolymers,” Adv. Mater. 25, 5943–5947 (2013).
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M. C. Gather and S. H. Yun, “Single-cell biological lasers,” Nat. Photonics 5, 406–410 (2011).
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M. Humar, S. J. J. Kwok, M. Choi, S. Cho, A. K. Yetisen, and S.-H. Yun, “Towards biomaterial-based implantable photonic devices,” Nanophotonics 5, 60–80 (2016).

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M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
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ACS Chem. Biol. (1)

M. P. Hall, J. Unch, B. F. Binkowski, M. P. Valley, B. L. Butler, M. G. Wood, P. Otto, K. Zimmerman, G. Vidugiris, T. MacHleidt, M. B. Robers, H. A. Benink, C. T. Eggers, M. R. Slater, P. L. Meisenheimer, D. H. Klaubert, F. Fan, L. P. Encell, and K. V. Wood, “Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate,” ACS Chem. Biol. 7, 1848–1857 (2012).
[Crossref]

Adv. Mater. (1)

S. Nizamoglu, M. C. Gather, and S. H. Yun, “All-biomaterial laser using vitamin and biopolymers,” Adv. Mater. 25, 5943–5947 (2013).
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X. Wu, Q. Chen, Y. Sun, and X. Fan, “Bio-inspired optofluidic lasers with luciferin,” Appl. Phys. Lett. 102, 11–13 (2013).

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[Crossref]

T. Yamaguchi, N. Omatsu, S. Matsushita, and T. Osumi, “CGI-58 interacts with perilipin and is localized to lipid droplets, possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome,” J. Biol. Chem. 279, 30490–30497 (2004).
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M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15, 5647–5652 (2015).
[Crossref]

Nanophotonics (1)

M. Humar, S. J. J. Kwok, M. Choi, S. Cho, A. K. Yetisen, and S.-H. Yun, “Towards biomaterial-based implantable photonic devices,” Nanophotonics 5, 60–80 (2016).

Nat. Commun. (1)

M. C. Gather and S. H. Yun, “Bio-optimized energy transfer in densely packed fluorescent protein enables near-maximal luminescence and solid-state lasers,” Nat. Commun. 5, 5722 (2014).
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M. C. Gather and S. H. Yun, “Single-cell biological lasers,” Nat. Photonics 5, 406–410 (2011).
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M. Humar and S. H. Yun, “Intracellular microlasers,” Nat. Photonics 9, 572–576 (2015).
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Y. R. Kim, S. Kim, J. W. Choi, S. Y. Choi, S.-H. Lee, H. Kim, S. K. Hahn, G. Y. Koh, and S. H. Yun, “Bioluminescence-activated deep-tissue photodynamic therapy of cancer,” Theranostics 5, 805–817 (2015).
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B. Kay, S. Thai, and V. Volgina, “High-throughput biotinylation of proteins,” in High Throughput Protein Expression and Purification, S. Doyle, ed., Vol. 498 of Methods in Molecular Biology (Humana, 2009), pp. 185–198.

Supplementary Material (1)

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Figures (5)

Fig. 1.
Fig. 1.

GFP on high-index microspheres. (a) Illustration of GFP molecules binding onto the surface of a BaTiO3 bead. (b) Fluorescence spectra measured at 30 and 100 s, after adding a GFP solution to beads in dispersion. (c) Intensity of the WGM peaks and background fluorescence after the addition of GFP. (d) A BaTiO3 glass bead coated with GFP molecules. The fluorescent light from the GFP molecules is coupled into WGMs. (e) Fluorescence spectrum of a BaTiO3 bead. Curve fitting indicates the oscillation of the first- and second-order radial modes (marked) and predicts a bead diameter of 4.85 μm. Insets show bright-field (left) and fluorescence (right) images of the bead. (f) The output spectrum from a 2.56 μm bead, showing the excitation of only the first-order radial modes. Scale bars, 5 μm.

Fig. 2.
Fig. 2.

Intracellular GFP-coated glass bead during cell division. (a) Bright-field images showing the transmission of the bead during telophase (t=0  s) and after cytokinesis (t=2000  s). Scale bars, 5 μm. (b) Measured spectral shifts of the WGM peaks from telophase to the completion of mitosis.

Fig. 3.
Fig. 3.

Microcavities in cells with GFP fluorescent material formed in situ. (a) Bright-field image of two GFP-ABHD5-producing HeLa cells 2 days after injecting PPE oil droplets into the cytosol. (b) Fluorescence image of the cells, showing bright green fluorescence from the accumulated GFP on the surface of the droplets. (c) Typical output spectrum from the cell under CW pumping. (d) Reduced fluorescence emission after photobleaching by high-intensity optical pumping. (e) Increased fluorescence by continuous production and replenishment of GFP in vitro over 6 h after the bleaching. Scale bars, 10 μm.

Fig. 4.
Fig. 4.

All-biological self-assembled microcavity. (a) Schematic of the intracellular GFP-droplet system. (b) Fluorescence image of GFP-ABHD5-transduced 3T3-L1 mature adipocytes. The fluorescence is mainly emitted from the edges of the droplets. (c) A typical output spectrum from a single GFP-bound lipid droplet (inset). (d) Time-lapse variation of the fluorescence intensity during photobleaching and after partial recovery 18 h later. Inset: fluorescence image at t=0. Scale bars, 20 μm.

Fig. 5.
Fig. 5.

Cavity-modified bioluminescence. (a) Schematic of a polystyrene or glass bead coated with luciferase proteins. Upon addition of luciferin, light is generated and coupled into WGMs. (b) Bright-field image of polystyrene beads coated with luciferase (top) and bioluminescence emission when CTZ is added (bottom). Scale bar, 20 μm. (c) A representative bioluminescence spectrum from a luciferase-coated bead. The spectral peaks of WGMs are fitted to theory to determine the mode orders and bead diameter. (d) The effective bead diameter measured over time. The standard deviation fluctuation (gray area) is 190  ppm.

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