Abstract

Single-molecule localization microscopy (SMLM) has become an essential tool for examining a wide variety of biological structures and processes. However, the relatively long acquisition time makes SMLM prone to drift-induced artifacts. Here we report an optical design with an electrically tunable lens (ETL) that actively stabilizes a SMLM in three dimensions and nearly eliminates the mechanical drift (RMS ~0.7 nm lateral and ~2.7 nm axial). The bifocal design that employed fiducial markers on the coverslip was able to stabilize the sample regardless of the imaging depth. The effectiveness of the ETL was demonstrated by imaging endosomal transferrin receptors near the apical surface of B-lymphocytes at a depth of 8 µm. The drift-free images obtained with the stabilization system showed that the transferrin receptors were present in distinct but heterogeneous clusters with a bimodal size distribution. In contrast, the images obtained without the stabilization system showed a broader unimodal size distribution. Thus, this stabilization system enables a more accurate analysis of cluster topology. Additionally, this ETL-based stabilization system is cost-effective and can be integrated into existing microscopy systems.

© 2016 Optical Society of America

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References

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2016 (1)

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
[Crossref] [PubMed]

2015 (3)

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
[Crossref] [PubMed]

F. Levet, E. Hosy, A. Kechkar, C. Butler, A. Beghin, D. Choquet, and J.-B. Sibarita, “SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data,” Nat. Methods 12(11), 1065–1071 (2015).
[Crossref] [PubMed]

D. Baddeley, “Detecting nano-scale protein clustering,” Nat. Methods 12(11), 1019–1020 (2015).
[Crossref] [PubMed]

2013 (3)

H. Kobayashi and M. Fukuda, “Arf6, Rab11 and transferrin receptor define distinct populations of recycling endosomes,” Commun. Integr. Biol. 6(5), e25036 (2013).
[Crossref] [PubMed]

F. O. Fahrbach, F. F. Voigt, B. Schmid, F. Helmchen, and J. Huisken, “Rapid 3D light-sheet microscopy with a tunable lens,” Opt. Express 21(18), 21010–21026 (2013).
[Crossref] [PubMed]

R. McGorty, D. Kamiyama, and B. Huang, “Active microscope stabilization in three dimensions using image correlation,” Opt. Nanoscopy 2(1), 3 (2013).
[Crossref] [PubMed]

2012 (4)

2011 (1)

2010 (2)

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
[Crossref] [PubMed]

2008 (4)

2007 (1)

2006 (4)

O. Pishnyak, S. Sato, and O. D. Lavrentovich, “Electrically tunable lens based on a dual-frequency nematic liquid crystal,” Appl. Opt. 45(19), 4576–4582 (2006).
[Crossref] [PubMed]

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

I. Moreno, C. Ferreira, and M. M. Sánchez-López, “Ray matrix analysis of anamorphic fractional Fourier systems,” J. Opt. A, Pure Appl. Opt. 8(5), 427–435 (2006).
[Crossref]

2004 (1)

A. Yildiz, M. Tomishige, R. D. Vale, and P. R. Selvin, “Kinesin walks hand-over-hand,” Science 303(5658), 676–678 (2004).
[Crossref] [PubMed]

2003 (1)

A. Yildiz, J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldman, and P. R. Selvin, “Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization,” Science 300(5628), 2061–2065 (2003).
[Crossref] [PubMed]

2002 (1)

E. M. van Dam, T. Ten Broeke, K. Jansen, P. Spijkers, and W. Stoorvogel, “Endocytosed Transferrin Receptors Recycle via Distinct Dynamin and Phosphatidylinositol 3-Kinase-dependent Pathways,” J. Biol. Chem. 277(50), 48876–48883 (2002).
[Crossref] [PubMed]

1999 (1)

P. Ponka and C. N. Lok, “The transferrin receptor: role in health and disease,” Int. J. Biochem. Cell Biol. 31(10), 1111–1137 (1999).
[Crossref] [PubMed]

1989 (1)

J. Futran, J. D. Kemp, E. H. Field, A. Vora, and R. F. Ashman, “Transferrin receptor synthesis is an early event in B cell activation,” J. Immunol. 143(3), 787–792 (1989).
[PubMed]

1986 (1)

R. S. Ajioka and J. Kaplan, “Intracellular pools of transferrin receptors result from constitutive internalization of unoccupied receptors,” Proc. Natl. Acad. Sci. U.S.A. 83(17), 6445–6449 (1986).
[Crossref] [PubMed]

1985 (1)

B. T. Pan, K. Teng, C. Wu, M. Adam, and R. M. Johnstone, “Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes,” J. Cell Biol. 101(3), 942–948 (1985).
[Crossref] [PubMed]

1984 (2)

L. M. Neckers, G. Yenokida, and S. P. James, “The role of the transferrin receptor in human B lymphocyte activation,” J. Immunol. 133(5), 2437–2441 (1984).
[PubMed]

T. Szoplik, W. Kosek, and C. Ferreira, “Nonsymmetric Fourier transforming with an anamorphic system,” Appl. Opt. 23(6), 905 (1984).
[Crossref] [PubMed]

1983 (2)

C. Harding, J. Heuser, and P. Stahl, “Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes,” J. Cell Biol. 97(2), 329–339 (1983).
[Crossref] [PubMed]

C. R. Hopkins, “Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells,” Cell 35(1), 321–330 (1983).
[Crossref] [PubMed]

1967 (1)

1966 (1)

1896 (1)

L. Rayleigh, “XV. On the theory of optical images, with special reference to the microscope,” Philos. Mag. Series 5 42(255), 167–195 (1896).
[Crossref]

Abraham, L.

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
[Crossref] [PubMed]

Adam, M.

B. T. Pan, K. Teng, C. Wu, M. Adam, and R. M. Johnstone, “Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes,” J. Cell Biol. 101(3), 942–948 (1985).
[Crossref] [PubMed]

Agard, D. A.

V. Mennella, B. Keszthelyi, K. L. McDonald, B. Chhun, F. Kan, G. C. Rogers, B. Huang, and D. A. Agard, “Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization,” Nat. Cell Biol. 14(11), 1159–1168 (2012).
[Crossref] [PubMed]

Ajioka, R. S.

R. S. Ajioka and J. Kaplan, “Intracellular pools of transferrin receptors result from constitutive internalization of unoccupied receptors,” Proc. Natl. Acad. Sci. U.S.A. 83(17), 6445–6449 (1986).
[Crossref] [PubMed]

Alchenberger, D.

Andilla, J.

Arnold, C. B.

Ashman, R. F.

J. Futran, J. D. Kemp, E. H. Field, A. Vora, and R. F. Ashman, “Transferrin receptor synthesis is an early event in B cell activation,” J. Immunol. 143(3), 787–792 (1989).
[PubMed]

Baday, M.

Baddeley, D.

D. Baddeley, “Detecting nano-scale protein clustering,” Nat. Methods 12(11), 1019–1020 (2015).
[Crossref] [PubMed]

Baer, E.

Bates, M.

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

Beadie, G.

Beghin, A.

F. Levet, E. Hosy, A. Kechkar, C. Butler, A. Beghin, D. Choquet, and J.-B. Sibarita, “SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data,” Nat. Methods 12(11), 1065–1071 (2015).
[Crossref] [PubMed]

Betzig, E.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]

Bewersdorf, J.

Bonifacino, J. S.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]

Butler, C.

F. Levet, E. Hosy, A. Kechkar, C. Butler, A. Beghin, D. Choquet, and J.-B. Sibarita, “SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data,” Nat. Methods 12(11), 1065–1071 (2015).
[Crossref] [PubMed]

Cai, E.

Callahan, S. P.

Carter, A. R.

Chhun, B.

V. Mennella, B. Keszthelyi, K. L. McDonald, B. Chhun, F. Kan, G. C. Rogers, B. Huang, and D. A. Agard, “Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization,” Nat. Cell Biol. 14(11), 1159–1168 (2012).
[Crossref] [PubMed]

Choi, K.

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
[Crossref] [PubMed]

Choquet, D.

F. Levet, E. Hosy, A. Kechkar, C. Butler, A. Beghin, D. Choquet, and J.-B. Sibarita, “SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data,” Nat. Methods 12(11), 1065–1071 (2015).
[Crossref] [PubMed]

G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
[Crossref] [PubMed]

Chou, K. C.

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
[Crossref] [PubMed]

Chu, S.

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

Ciepielewski, D.

Cognet, L.

G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
[Crossref] [PubMed]

Constals, A.

G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
[Crossref] [PubMed]

Coombs, D.

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
[Crossref] [PubMed]

Dahan, M.

Darzacq, X.

Das, R.

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
[Crossref] [PubMed]

Davidson, M. W.

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]

Dlasková, A.

Egner, A.

El Beheiry, M.

Fahrbach, F. O.

Ferreira, C.

I. Moreno, C. Ferreira, and M. M. Sánchez-López, “Ray matrix analysis of anamorphic fractional Fourier systems,” J. Opt. A, Pure Appl. Opt. 8(5), 427–435 (2006).
[Crossref]

T. Szoplik, W. Kosek, and C. Ferreira, “Nonsymmetric Fourier transforming with an anamorphic system,” Appl. Opt. 23(6), 905 (1984).
[Crossref] [PubMed]

Field, E. H.

J. Futran, J. D. Kemp, E. H. Field, A. Vora, and R. F. Ashman, “Transferrin receptor synthesis is an early event in B cell activation,” J. Immunol. 143(3), 787–792 (1989).
[PubMed]

Forkey, J. N.

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Helmchen, F.

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G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
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Hsu, B. E.

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
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Izeddin, I.

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R. McGorty, D. Kamiyama, and B. Huang, “Active microscope stabilization in three dimensions using image correlation,” Opt. Nanoscopy 2(1), 3 (2013).
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J. Futran, J. D. Kemp, E. H. Field, A. Vora, and R. F. Ashman, “Transferrin receptor synthesis is an early event in B cell activation,” J. Immunol. 143(3), 787–792 (1989).
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H. Kobayashi and M. Fukuda, “Arf6, Rab11 and transferrin receptor define distinct populations of recycling endosomes,” Commun. Integr. Biol. 6(5), e25036 (2013).
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E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
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E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
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McDonald, K. L.

V. Mennella, B. Keszthelyi, K. L. McDonald, B. Chhun, F. Kan, G. C. Rogers, B. Huang, and D. A. Agard, “Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization,” Nat. Cell Biol. 14(11), 1159–1168 (2012).
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R. McGorty, D. Kamiyama, and B. Huang, “Active microscope stabilization in three dimensions using image correlation,” Opt. Nanoscopy 2(1), 3 (2013).
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A. Yildiz, J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldman, and P. R. Selvin, “Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization,” Science 300(5628), 2061–2065 (2003).
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V. Mennella, B. Keszthelyi, K. L. McDonald, B. Chhun, F. Kan, G. C. Rogers, B. Huang, and D. A. Agard, “Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization,” Nat. Cell Biol. 14(11), 1159–1168 (2012).
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Mlodzianoski, M. J.

Moore, E. D. W.

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
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B. T. Pan, K. Teng, C. Wu, M. Adam, and R. M. Johnstone, “Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes,” J. Cell Biol. 101(3), 942–948 (1985).
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E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
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G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
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S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
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M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
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I. Moreno, C. Ferreira, and M. M. Sánchez-López, “Ray matrix analysis of anamorphic fractional Fourier systems,” J. Opt. A, Pure Appl. Opt. 8(5), 427–435 (2006).
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R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
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Sibarita, J.-B.

F. Levet, E. Hosy, A. Kechkar, C. Butler, A. Beghin, D. Choquet, and J.-B. Sibarita, “SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data,” Nat. Methods 12(11), 1065–1071 (2015).
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G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
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E. M. van Dam, T. Ten Broeke, K. Jansen, P. Spijkers, and W. Stoorvogel, “Endocytosed Transferrin Receptors Recycle via Distinct Dynamin and Phosphatidylinositol 3-Kinase-dependent Pathways,” J. Biol. Chem. 277(50), 48876–48883 (2002).
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C. Harding, J. Heuser, and P. Stahl, “Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes,” J. Cell Biol. 97(2), 329–339 (1983).
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E. M. van Dam, T. Ten Broeke, K. Jansen, P. Spijkers, and W. Stoorvogel, “Endocytosed Transferrin Receptors Recycle via Distinct Dynamin and Phosphatidylinositol 3-Kinase-dependent Pathways,” J. Biol. Chem. 277(50), 48876–48883 (2002).
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Tafteh, R.

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
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Tampé, R.

G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
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E. M. van Dam, T. Ten Broeke, K. Jansen, P. Spijkers, and W. Stoorvogel, “Endocytosed Transferrin Receptors Recycle via Distinct Dynamin and Phosphatidylinositol 3-Kinase-dependent Pathways,” J. Biol. Chem. 277(50), 48876–48883 (2002).
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Tomishige, M.

A. Yildiz, M. Tomishige, R. D. Vale, and P. R. Selvin, “Kinesin walks hand-over-hand,” Science 303(5658), 676–678 (2004).
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Vale, R. D.

A. Yildiz, M. Tomishige, R. D. Vale, and P. R. Selvin, “Kinesin walks hand-over-hand,” Science 303(5658), 676–678 (2004).
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E. M. van Dam, T. Ten Broeke, K. Jansen, P. Spijkers, and W. Stoorvogel, “Endocytosed Transferrin Receptors Recycle via Distinct Dynamin and Phosphatidylinositol 3-Kinase-dependent Pathways,” J. Biol. Chem. 277(50), 48876–48883 (2002).
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Volkmann, H.

Vora, A.

J. Futran, J. D. Kemp, E. H. Field, A. Vora, and R. F. Ashman, “Transferrin receptor synthesis is an early event in B cell activation,” J. Immunol. 143(3), 787–792 (1989).
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B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
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Wong, H. S.

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
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B. T. Pan, K. Teng, C. Wu, M. Adam, and R. M. Johnstone, “Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes,” J. Cell Biol. 101(3), 942–948 (1985).
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Xianyu, H.

Xu, S.

Yang, Y.

Yenokida, G.

L. M. Neckers, G. Yenokida, and S. P. James, “The role of the transferrin receptor in human B lymphocyte activation,” J. Immunol. 133(5), 2437–2441 (1984).
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Yildiz, A.

A. Yildiz, M. Tomishige, R. D. Vale, and P. R. Selvin, “Kinesin walks hand-over-hand,” Science 303(5658), 676–678 (2004).
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A. Yildiz, J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldman, and P. R. Selvin, “Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization,” Science 300(5628), 2061–2065 (2003).
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Zhang, R.

Zhang, Y.

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
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Zhuang, X.

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
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M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
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Appl. Opt. (4)

Biophys. J. (1)

G. Giannone, E. Hosy, F. Levet, A. Constals, K. Schulze, A. I. Sobolevsky, M. P. Rosconi, E. Gouaux, R. Tampé, D. Choquet, and L. Cognet, “Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density,” Biophys. J. 99(4), 1303–1310 (2010).
[Crossref] [PubMed]

Cell (1)

C. R. Hopkins, “Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells,” Cell 35(1), 321–330 (1983).
[Crossref] [PubMed]

Commun. Integr. Biol. (1)

H. Kobayashi and M. Fukuda, “Arf6, Rab11 and transferrin receptor define distinct populations of recycling endosomes,” Commun. Integr. Biol. 6(5), e25036 (2013).
[Crossref] [PubMed]

Int. J. Biochem. Cell Biol. (1)

P. Ponka and C. N. Lok, “The transferrin receptor: role in health and disease,” Int. J. Biochem. Cell Biol. 31(10), 1111–1137 (1999).
[Crossref] [PubMed]

J. Biol. Chem. (1)

E. M. van Dam, T. Ten Broeke, K. Jansen, P. Spijkers, and W. Stoorvogel, “Endocytosed Transferrin Receptors Recycle via Distinct Dynamin and Phosphatidylinositol 3-Kinase-dependent Pathways,” J. Biol. Chem. 277(50), 48876–48883 (2002).
[Crossref] [PubMed]

J. Biophotonics (1)

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
[Crossref] [PubMed]

J. Cell Biol. (2)

B. T. Pan, K. Teng, C. Wu, M. Adam, and R. M. Johnstone, “Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes,” J. Cell Biol. 101(3), 942–948 (1985).
[Crossref] [PubMed]

C. Harding, J. Heuser, and P. Stahl, “Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes,” J. Cell Biol. 97(2), 329–339 (1983).
[Crossref] [PubMed]

J. Immunol. (2)

J. Futran, J. D. Kemp, E. H. Field, A. Vora, and R. F. Ashman, “Transferrin receptor synthesis is an early event in B cell activation,” J. Immunol. 143(3), 787–792 (1989).
[PubMed]

L. M. Neckers, G. Yenokida, and S. P. James, “The role of the transferrin receptor in human B lymphocyte activation,” J. Immunol. 133(5), 2437–2441 (1984).
[PubMed]

J. Opt. A, Pure Appl. Opt. (1)

I. Moreno, C. Ferreira, and M. M. Sánchez-López, “Ray matrix analysis of anamorphic fractional Fourier systems,” J. Opt. A, Pure Appl. Opt. 8(5), 427–435 (2006).
[Crossref]

J. Opt. Soc. Am. (1)

Nat. Cell Biol. (1)

V. Mennella, B. Keszthelyi, K. L. McDonald, B. Chhun, F. Kan, G. C. Rogers, B. Huang, and D. A. Agard, “Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization,” Nat. Cell Biol. 14(11), 1159–1168 (2012).
[Crossref] [PubMed]

Nat. Commun. (1)

S. A. Freeman, V. Jaumouillé, K. Choi, B. E. Hsu, H. S. Wong, L. Abraham, M. L. Graves, D. Coombs, C. D. Roskelley, R. Das, S. Grinstein, and M. R. Gold, “Toll-like receptor ligands sensitize B-cell receptor signalling by reducing actin-dependent spatial confinement of the receptor,” Nat. Commun. 6, 6168 (2015).
[Crossref] [PubMed]

Nat. Methods (3)

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

F. Levet, E. Hosy, A. Kechkar, C. Butler, A. Beghin, D. Choquet, and J.-B. Sibarita, “SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data,” Nat. Methods 12(11), 1065–1071 (2015).
[Crossref] [PubMed]

D. Baddeley, “Detecting nano-scale protein clustering,” Nat. Methods 12(11), 1019–1020 (2015).
[Crossref] [PubMed]

Nature (1)

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

Opt. Express (7)

C. Geisler, T. Hotz, A. Schönle, S. W. Hell, A. Munk, and A. Egner, “Drift estimation for single marker switching based imaging schemes,” Opt. Express 20(7), 7274–7289 (2012).
[Crossref] [PubMed]

M. J. Mlodzianoski, J. M. Schreiner, S. P. Callahan, K. Smolková, A. Dlasková, J. Santorová, P. Ježek, and J. Bewersdorf, “Sample drift correction in 3D fluorescence photoactivation localization microscopy,” Opt. Express 19(16), 15009–15019 (2011).
[Crossref] [PubMed]

G. Beadie, M. L. Sandrock, M. J. Wiggins, R. S. Lepkowicz, J. S. Shirk, M. Ponting, Y. Yang, T. Kazmierczak, A. Hiltner, and E. Baer, “Tunable polymer lens,” Opt. Express 16(16), 11847–11857 (2008).
[Crossref] [PubMed]

S. H. Lee, M. Baday, M. Tjioe, P. D. Simonson, R. Zhang, E. Cai, and P. R. Selvin, “Using fixed fiduciary markers for stage drift correction,” Opt. Express 20(11), 12177–12183 (2012).
[Crossref] [PubMed]

F. O. Fahrbach, F. F. Voigt, B. Schmid, F. Helmchen, and J. Huisken, “Rapid 3D light-sheet microscopy with a tunable lens,” Opt. Express 21(18), 21010–21026 (2013).
[Crossref] [PubMed]

I. Izeddin, M. El Beheiry, J. Andilla, D. Ciepielewski, X. Darzacq, and M. Dahan, “PSF shaping using adaptive optics for three-dimensional single-molecule super-resolution imaging and tracking,” Opt. Express 20(5), 4957–4967 (2012).
[Crossref] [PubMed]

H. Ren, H. Xianyu, S. Xu, and S.-T. Wu, “Adaptive dielectric liquid lens,” Opt. Express 16(19), 14954–14960 (2008).
[Crossref] [PubMed]

Opt. Lett. (1)

Opt. Nanoscopy (1)

R. McGorty, D. Kamiyama, and B. Huang, “Active microscope stabilization in three dimensions using image correlation,” Opt. Nanoscopy 2(1), 3 (2013).
[Crossref] [PubMed]

Philos. Mag. Series 5 (1)

L. Rayleigh, “XV. On the theory of optical images, with special reference to the microscope,” Philos. Mag. Series 5 42(255), 167–195 (1896).
[Crossref]

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

R. S. Ajioka and J. Kaplan, “Intracellular pools of transferrin receptors result from constitutive internalization of unoccupied receptors,” Proc. Natl. Acad. Sci. U.S.A. 83(17), 6445–6449 (1986).
[Crossref] [PubMed]

Science (4)

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

A. Yildiz, J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldman, and P. R. Selvin, “Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization,” Science 300(5628), 2061–2065 (2003).
[Crossref] [PubMed]

A. Yildiz, M. Tomishige, R. D. Vale, and P. R. Selvin, “Kinesin walks hand-over-hand,” Science 303(5658), 676–678 (2004).
[Crossref] [PubMed]

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]

Other (3)

S. Kuiper, B. H. Hendriks, L. J. Huijbregts, A. M. Hirschberg, C. A. Renders, and M. A. van As, “Variable-focus liquid lens for portable applications,” SPIE Proceedings Vol. 5523: Current Developments in Lens Design and Optical Engineering V, 100–109 (2004).
[Crossref]

N. Piro, T. Pengo, N. Olivier, and S. Manley, “Improved 3D Superresolution Localization Microscopy Using Adaptive Optics,” arXiv:1401.0879 [physics] (2014).

H. Hogan, “Focusing on the Experiment,” Biophoton. Int. (May): 48–51 (2006).

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Figures (4)

Fig. 1
Fig. 1

Schematic layout of the imaging system. The 405 nm and the 639 nm laser beams were expanded with lenses L1-L4, combined with a dichroic mirror (DM1), circularly polarized with a quarter-wave plate (QWP), and focused by a lens (L5) before entering the objective lens. Mirrors (M3 and M4) and L5 were mounted on a translational stage to control the incidence angle of the laser beams. A 3D piezo stage (PZ) with a controller and a feedback loop was used to move the sample. The signals were separated by a dichroic mirror (DM2) and went a notch filter (NF). The fluorescence signals from the cell and the fiducial markers were separated using a dichroic mirror (DM3). In the tracking path, the signal went through a relay system consisting of a tube lens (TL2) and two relay lenses (RL1 and RL2). An ETL with its controller, as shown in the inset, was used to keep the fiducial markers focused on the CCD. A cylindrical lens assembly (CL2) introduced the astigmatism to determine the axial position of the fiducial markers. A cylindrical lens assembly (CL1) and a tube lens (TL1) were used to image the sample on the EMCCD. A 2.5X zoom lens (ZL) was used to obtain a magnification of 150 × on the EMCCD. The black and red dashed lines indicate the focal planes of the sample and the fiducial markers, respectively. Bandpass filters (BPF1 and BPF2) were used before each camera.

Fig. 2
Fig. 2

Characteristics of the ETL and cylindrical lens assembly. (a) Schematic representation of an ETL based on the shape-changing polymer membrane technology. (b) Axial focal shift in the sample vs. the current applied to the ETL. The black line is a polynomial fitting curve. (c) Schematic representation of the compound cylindrical lens assembly. (d) Images of an astigmatically-aberrated PSF at various axial positions. (e) Aspect ratio (Rxy) of the astigmatic PSF as a function of axial position (z). The black line is a polynomial fitting curve. The black arrow indicates the range of aspect ratio used for tracking the fiducial markers.

Fig. 3
Fig. 3

Performance of the stabilization system with an ETL. (a) Positions of the sample in x, y, and z directions over 10 min with (red curves) and without (blue curves) the stabilization system enabled. (b) Histograms of the sample’s positional fluctuations in each direction. Standard deviations were 0.69 nm in x, 0.65 nm in y and 2.71 nm in z.

Fig. 4
Fig. 4

Comparison of a drift-free image with a drifted image of TfRs in B cells. SMLM images of TfR in a B cell were obtained with (a) and without (b) the stabilization system. (c) The actual drift in the x (red curve), y (black curve), and z (blue curve) directions during the acquisition of 40k frames over 13 min. (d-e) Enlarged images of the regions marked by white boxes in (a-b). (f-g) 3D representations of the regions marked by green rectangles in (d-e). (h-i) Voronoï tessellation maps of the regions indicated by red boxes in (d-e). Distribution of the cluster density (j), cluster diameter (k) and cluster circularity (l). Scale bars: 2 µm in (a-b), 500 nm in (d-e), and 200 nm in (f-i).

Equations (3)

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δz= n f RL2 M 2 f ETL,eff
S CL2,x =( 1 0 f cl 1 1 )( 1 d 0 1 )( 1 0 f cl 1 1 )= ( 1d f cl 1 1 d f cl 2 1+d f cl 1 )
I k ( x,y )= I 0 ( erf( x x 0 +0.5 2 σ x )erf( x x 0 0.5 2 σ x ) )×( erf( y y 0 +0.5 2 σ y )erf( y y 0 0.5 2 σ y ) )+ b 0

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