Abstract

Fluorescence-based expansion microscopy (ExM) is a new technique which can yield nanoscale resolution of biological specimen on a conventional fluorescence microscope through physical sample expansion up to 20 times its original dimensions while preserving structural information. It however inherits known issues of fluorescence microscopy such as photostability and multiplexing capabilities, as well as an ExM-specific issue in signal intensity reduction due to a dilution effect after expansion. To address these issues, we propose using antigen-targeting plasmonic nanoparticle labels which can be imaged using surface-enhanced Raman scattering spectroscopy (SERS) and dark-field spectroscopy. We demonstrate that the nanoparticles enable multimodal imaging: bright-field, dark-field and SERS, with excellent photostability, contrast enhancement and brightness.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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  3. M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3, 793–795 (2006).
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  5. T. Ku, J. Swaney, J.-Y. Park, A. Albanese, E. Murray, J. H. Cho, Y.-G. Park, V. Mangena, J. Chen, and K. Chung, “Multiplexed and scalable super-resolution imaging of three-dimensional protein localization in size-adjustable tissues,” Nat. Biotechnol. 34, 973–981 (2016).
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  20. J. Qi and W.-C. Shih, “Performance of line-scan Raman microscopy for high-throughput chemical imaging of cell population,” Appl. Opt. 53, 2881–2885 (2014).
    [Crossref] [PubMed]
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    [Crossref]
  25. A. M. Lavezzi, M. F. Corna, and L. Matturri, “Neuronal nuclear antigen (NeuN): a useful marker of neuronal immaturity in sudden unexplained perinatal death,” J. Neurol. Sci. 329, 45–50 (2013).
    [Crossref] [PubMed]
  26. S. Schlücker, B. Küstner, A. Punge, R. Bonfig, A. Marx, and P. Ströbel, “Immuno-Raman microspectroscopy: in situ detection of antigens in tissue specimens by surface-enhanced Raman scattering,” J. Raman Spectrosc. 37, 719–721 (2006).
    [Crossref]
  27. A. Indrasekara, B. J. Paladini, D. J. Naczynski, V. Starovoytov, P. V. Moghe, and L. Fabris, “Dimeric gold nanoparticle assemblies as tags for SERS-based cancer detection,” Adv. Healthcare Mater. 2, 1370–1376 (2013).
    [Crossref]
  28. W. L. Barnes, A. Dereux, and T. W. Ebbesen, “Surface plasmon subwavelength optics,” Nature 424, 824 (2003).
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  29. G. W. Bryant, F. J. García de Abajo, and J. Aizpurua,“Mapping the plasmon resonances of metallic nanoantennas,” Nano Lett. 8, 631–636 (2008).
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  30. J. N. Anker, W. P. Hall, O. Lyandres, N. C. Shah, J. Zhao, and R. P. Van Duyne, “Biosensing with plasmonic nanosensors,” Nat. Mater. 7, 442–453 (2008).
    [Crossref] [PubMed]
  31. K. A. Willets and R. P. Van Duyne, “Localized surface plasmon resonance spectroscopy and sensing,” Annu. Rev. Phys. Chem. 58, 267–297 (2007).
    [Crossref]
  32. J. Chen, F. Saeki, B. J. Wiley, H. Cang, M. J. Cobb, Z.-Y. Li, L. Au, H. Zhang, M. B. Kimmey, Li, and Y. Xia, “Gold nanocages: bioconjugation and their potential use as optical imaging contrast agents,” Nano Lett. 5, 473–477 (2005).
    [Crossref] [PubMed]
  33. K. Sokolov, M. Follen, J. Aaron, I. Pavlova, A. Malpica, R. Lotan, and R. Richards-Kortum, “Real-time vital optical imaging of precancer using anti-epidermal growth factor receptor antibodies conjugated to gold nanoparticles,” Cancer Res. 63, 1999–2004 (2003).
    [PubMed]
  34. I. H. El-Sayed, X. Huang, and M. A. El-Sayed, “Surface plasmon resonance scattering and absorption of anti-EGFR antibody conjugated gold nanoparticles in cancer diagnostics: applications in oral cancer,” Nano Lett. 5, 829–834 (2005).
    [Crossref] [PubMed]
  35. C. Yu, H. Nakshatri, and J. Irudayaraj, “Identity profiling of cell surface markers by multiplex gold nanorod probes,” Nano Lett. 7, 2300–2306 (2007).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  37. F. Zhao, M. M. P. Arnob, O. Zenasni, J. Li, and W.-C. Shih, “Far-field plasmonic coupling in 2-dimensional polycrystalline plasmonic arrays enables wide tunability with low-cost nanofabrication,” Nanoscale Horiz. 2267 (2017).
  38. C.-F. Chen, S.-D. Tzeng, H.-Y. Chen, K.-J. Lin, and S. Gwo, “Tunable plasmonic response from alkanethiolate-stabilized gold nanoparticle superlattices: evidence of near-field coupling,” J. Am. Chem. Soc. 130, 824–826 (2008).
    [Crossref] [PubMed]
  39. P. K. Jain and M. A. El-Sayed, “Plasmonic coupling in noble metal nanostructures,” Chem. Phys. Lett. 487, 153–164 (2010).
    [Crossref]
  40. J. Zuloaga and P. Nordlander, “On the energy shift between near-field and far-field peak intensities in localized plasmon systems,” Nano Lett. 11, 1280–1283 (2011).
    [Crossref] [PubMed]
  41. P. K. Jain, K. S. Lee, I. H. El-Sayed, and M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110, 7238–7248 (2006).
    [Crossref] [PubMed]
  42. M. M. P. Arnob, F. Zhao, J. Li, and W.-C. Shih, “Ebl-based fabrication and different modeling approaches for nanoporous gold nanodisks,” ACS Photonics 4, 1870–1878 (2017).
    [Crossref]
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    [Crossref] [PubMed]
  44. G. von Maltzahn, A. Centrone, J.-H. Park, R. Ramanathan, M. J. Sailor, T. A. Hatton, and S. N. Bhatia, “SERS-coded gold nanorods as a multifunctional platform for densely multiplexed near-infrared imaging and photothermal heating,” Adv. Mater. 21, 3175–3180 (2009).
    [Crossref]
  45. X. Wei, S. Su, Y. Guo, X. Jiang, Y. Zhong, Y. Su, C. Fan, S.-T. Lee, and Y. He, “A molecular beacon-based signal-off surface-enhanced Raman scattering strategy for highly sensitive, reproducible, and multiplexed dna detection,” Small 9, 2493–2499 (2013).
    [Crossref] [PubMed]
  46. X. Wei, S. Su, Y. Guo, X. Jiang, Y. Zhong, Y. Su, C. Fan, S.-T. Lee, and Y. He, “Label-free, in situ SERS monitoring of individual DNA hybridization in microfluidics,” Nanoscale 6, 8521–8526 (2014).
    [Crossref]

2017 (5)

J.-B. Chang, F. Chen, Y.-G. Yoon, E. E. Jung, H. Babcock, J. S. Kang, S. Asano, H.-J. Suk, N. Pak, P. W. Tillberg, A. T. Wassie, D. Cai, and E. S. Boyden, “Iterative expansion microscopy,” Nat. Methods 14, 593–599 (2017).
[Crossref] [PubMed]

Y. Zhao, O. Bucur, H. Irshad, F. Chen, A. Weins, A. L. Stancu, E.-Y. Oh, M. DiStasio, V. Torous, B. Glass, I. E. Stillman, S. J. Schnitt, A. H. Beck, and E. S. Boyden, “Nanoscale imaging of clinical specimens using pathology-optimized expansion microscopy,” Nat. Biotechnol. 352 (2017).
[Crossref]

L. Wei, Z. Chen, L. Shi, R. Long, A. V. Anzalone, L. Zhang, F. Hu, R. Yuste, V. W. Cornish, and W. Min, “Super-multiplex vibrational imaging,” Nature 544, 465–470 (2017).
[Crossref] [PubMed]

F. Zhao, M. M. P. Arnob, O. Zenasni, J. Li, and W.-C. Shih, “Far-field plasmonic coupling in 2-dimensional polycrystalline plasmonic arrays enables wide tunability with low-cost nanofabrication,” Nanoscale Horiz. 2267 (2017).

M. M. P. Arnob, F. Zhao, J. Li, and W.-C. Shih, “Ebl-based fabrication and different modeling approaches for nanoporous gold nanodisks,” ACS Photonics 4, 1870–1878 (2017).
[Crossref]

2016 (2)

T. Ku, J. Swaney, J.-Y. Park, A. Albanese, E. Murray, J. H. Cho, Y.-G. Park, V. Mangena, J. Chen, and K. Chung, “Multiplexed and scalable super-resolution imaging of three-dimensional protein localization in size-adjustable tissues,” Nat. Biotechnol. 34, 973–981 (2016).
[Crossref] [PubMed]

P. W. Tillberg, F. Chen, K. D. Piatkevich, Y. Zhao, C.-C. J. Yu, B. P. English, L. Gao, A. Martorell, H.-J. Suk, F. Yoshida, E. M. DeGennaro, D. H. Roossien, G. Gong, U. Seneviratne, S. R. Tannenbaum, R. Desimone, D. Cai, and E. S. Boyden, “Protein-retention expansion microscopy of cells and tissues labeled using standard fluorescent proteins and antibodies,” Nat. Biotechnol. 34, 987–992 (2016).
[Crossref] [PubMed]

2015 (3)

L. Fabris, “Gold-based SERS tags for biomedical imaging,” J. Opt. 17, 114002 (2015).
[Crossref]

F. Chen, P. W. Tillberg, and E. S. Boyden, “Expansion microscopy,” Science 347, 543–548 (2015).
[Crossref] [PubMed]

A. Pallaoro, G. B. Braun, and M. Moskovits, “Biotags based on surface-enhanced Raman can be as bright as fluorescence tags,” Nano Lett. 15, 6745–6750 (2015).
[Crossref] [PubMed]

2014 (4)

J. Qi and W.-C. Shih, “Performance of line-scan Raman microscopy for high-throughput chemical imaging of cell population,” Appl. Opt. 53, 2881–2885 (2014).
[Crossref] [PubMed]

N. Sudheendran, J. Qi, E. D. Young, A. J. Lazar, D. C. Lev, R. E. Pollock, K. V. Larin, and W.-C. Shih, “Line-scan Raman microscopy complements optical coherence tomography for tumor boundary detection,” Laser Phys. Lett. 11, 105602 (2014).
[Crossref]

M. Salehi, L. Schneider, P. Ströbel, A. Marx, J. Packeisen, and S. Schlücker, “Two-color SERS microscopy for protein co-localization in prostate tissue with primary antibody–protein A/G –gold nanocluster conjugates,” Nanoscale 6, 2361–2367 (2014).
[Crossref] [PubMed]

X. Wei, S. Su, Y. Guo, X. Jiang, Y. Zhong, Y. Su, C. Fan, S.-T. Lee, and Y. He, “Label-free, in situ SERS monitoring of individual DNA hybridization in microfluidics,” Nanoscale 6, 8521–8526 (2014).
[Crossref]

2013 (4)

X. Wei, S. Su, Y. Guo, X. Jiang, Y. Zhong, Y. Su, C. Fan, S.-T. Lee, and Y. He, “A molecular beacon-based signal-off surface-enhanced Raman scattering strategy for highly sensitive, reproducible, and multiplexed dna detection,” Small 9, 2493–2499 (2013).
[Crossref] [PubMed]

C. M. MacLaughlin, N. Mullaithilaga, G. Yang, S. Y. Ip, C. Wang, and G. C. Walker, “Surface-enhanced Raman scattering dye-labeled Au nanoparticles for triplexed detection of leukemia and lymphoma cells and SERS flow cytometry,” Langmuir 29, 1908–1919 (2013).
[Crossref] [PubMed]

A. M. Lavezzi, M. F. Corna, and L. Matturri, “Neuronal nuclear antigen (NeuN): a useful marker of neuronal immaturity in sudden unexplained perinatal death,” J. Neurol. Sci. 329, 45–50 (2013).
[Crossref] [PubMed]

A. Indrasekara, B. J. Paladini, D. J. Naczynski, V. Starovoytov, P. V. Moghe, and L. Fabris, “Dimeric gold nanoparticle assemblies as tags for SERS-based cancer detection,” Adv. Healthcare Mater. 2, 1370–1376 (2013).
[Crossref]

2012 (1)

Y. Wang, B. Yan, and L. Chen, “SERS tags: novel optical nanoprobes for bioanalysis,” Chem. Rev. 113, 1391–1428 (2012).
[Crossref]

2011 (1)

J. Zuloaga and P. Nordlander, “On the energy shift between near-field and far-field peak intensities in localized plasmon systems,” Nano Lett. 11, 1280–1283 (2011).
[Crossref] [PubMed]

2010 (1)

P. K. Jain and M. A. El-Sayed, “Plasmonic coupling in noble metal nanostructures,” Chem. Phys. Lett. 487, 153–164 (2010).
[Crossref]

2009 (2)

G. von Maltzahn, A. Centrone, J.-H. Park, R. Ramanathan, M. J. Sailor, T. A. Hatton, and S. N. Bhatia, “SERS-coded gold nanorods as a multifunctional platform for densely multiplexed near-infrared imaging and photothermal heating,” Adv. Mater. 21, 3175–3180 (2009).
[Crossref]

L. Tong, Q. Wei, A. Wei, and J.-X. Cheng, “Gold nanorods as contrast agents for biological imaging: optical properties, surface conjugation and photothermal effects,” Photochem. Photobiol. 85, 21–32 (2009).
[Crossref] [PubMed]

2008 (6)

G. W. Bryant, F. J. García de Abajo, and J. Aizpurua,“Mapping the plasmon resonances of metallic nanoantennas,” Nano Lett. 8, 631–636 (2008).
[Crossref] [PubMed]

J. N. Anker, W. P. Hall, O. Lyandres, N. C. Shah, J. Zhao, and R. P. Van Duyne, “Biosensing with plasmonic nanosensors,” Nat. Mater. 7, 442–453 (2008).
[Crossref] [PubMed]

B. Lutz, C. Dentinger, L. Sun, L. Nguyen, J. Zhang, A. Chmura, A. Allen, S. Chan, and B. Knudsen, “Raman nanoparticle probes for antibody-based protein detection in tissues,” J. Histochem. Cytochem. 56, 371–379 (2008).
[Crossref]

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, and X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322, 1857–1861 (2008).
[Crossref] [PubMed]

K. Faulds, R. Jarvis, W. E. Smith, D. Graham, and R. Goodacre, “Multiplexed detection of six labelled oligonucleotides using surface enhanced resonance Raman scattering (SERRS),” Analyst 133, 1505–1512 (2008).
[Crossref] [PubMed]

C.-F. Chen, S.-D. Tzeng, H.-Y. Chen, K.-J. Lin, and S. Gwo, “Tunable plasmonic response from alkanethiolate-stabilized gold nanoparticle superlattices: evidence of near-field coupling,” J. Am. Chem. Soc. 130, 824–826 (2008).
[Crossref] [PubMed]

2007 (3)

E. Le Ru, E. Blackie, M. Meyer, and P. G. Etchegoin, “Surface enhanced Raman scattering enhancement factors: a comprehensive study,” J. Phys. Chem. C 111, 13794–13803 (2007).
[Crossref]

K. A. Willets and R. P. Van Duyne, “Localized surface plasmon resonance spectroscopy and sensing,” Annu. Rev. Phys. Chem. 58, 267–297 (2007).
[Crossref]

C. Yu, H. Nakshatri, and J. Irudayaraj, “Identity profiling of cell surface markers by multiplex gold nanorod probes,” Nano Lett. 7, 2300–2306 (2007).
[Crossref] [PubMed]

2006 (5)

S. Schlücker, B. Küstner, A. Punge, R. Bonfig, A. Marx, and P. Ströbel, “Immuno-Raman microspectroscopy: in situ detection of antigens in tissue specimens by surface-enhanced Raman scattering,” J. Raman Spectrosc. 37, 719–721 (2006).
[Crossref]

J.-H. Kim, J.-S. Kim, H. Choi, S.-M. Lee, B.-H. Jun, K.-N. Yu, E. Kuk, Y.-K. Kim, D. H. Jeong, M.-H. Cho, and Y.-S. Lee, “Nanoparticle probes with surface enhanced Raman spectroscopic tags for cellular cancer targeting,” Anal. Chem. 78, 6967–6973 (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, 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, 793–795 (2006).
[Crossref] [PubMed]

P. K. Jain, K. S. Lee, I. H. El-Sayed, and M. A. El-Sayed, “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine,” J. Phys. Chem. B 110, 7238–7248 (2006).
[Crossref] [PubMed]

2005 (3)

D. Lind, S. Franken, J. Kappler, J. Jankowski, and K. Schilling, “Characterization of the neuronal marker NeuN as a multiply phosphorylated antigen with discrete subcellular localization,” J. Neurosci. Res. 79, 295–302 (2005).
[Crossref]

I. H. El-Sayed, X. Huang, and M. A. El-Sayed, “Surface plasmon resonance scattering and absorption of anti-EGFR antibody conjugated gold nanoparticles in cancer diagnostics: applications in oral cancer,” Nano Lett. 5, 829–834 (2005).
[Crossref] [PubMed]

J. Chen, F. Saeki, B. J. Wiley, H. Cang, M. J. Cobb, Z.-Y. Li, L. Au, H. Zhang, M. B. Kimmey, Li, and Y. Xia, “Gold nanocages: bioconjugation and their potential use as optical imaging contrast agents,” Nano Lett. 5, 473–477 (2005).
[Crossref] [PubMed]

2003 (3)

K. Sokolov, M. Follen, J. Aaron, I. Pavlova, A. Malpica, R. Lotan, and R. Richards-Kortum, “Real-time vital optical imaging of precancer using anti-epidermal growth factor receptor antibodies conjugated to gold nanoparticles,” Cancer Res. 63, 1999–2004 (2003).
[PubMed]

W. L. Barnes, A. Dereux, and T. W. Ebbesen, “Surface plasmon subwavelength optics,” Nature 424, 824 (2003).
[Crossref] [PubMed]

S. Schlücker, M. D. Schaeberle, S. W. Huffman, and I. W. Levin, “Raman microspectroscopy: a comparison of point, line, and wide-field imaging methodologies,” Anal. Chem. 75, 4312–4318 (2003).
[Crossref] [PubMed]

1994 (1)

S. W. Hell and J. Wichmann, “Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy,” Opt Lett 19, 780–782 (1994).
[Crossref] [PubMed]

1992 (1)

R. J. Mullen, C. R. Buck, and A. M. Smith, “NeuN, a neuronal specific nuclear protein in vertebrates,” Development 116, 201–211 (1992).
[PubMed]

Aaron, J.

K. Sokolov, M. Follen, J. Aaron, I. Pavlova, A. Malpica, R. Lotan, and R. Richards-Kortum, “Real-time vital optical imaging of precancer using anti-epidermal growth factor receptor antibodies conjugated to gold nanoparticles,” Cancer Res. 63, 1999–2004 (2003).
[PubMed]

Aizpurua, J.

G. W. Bryant, F. J. García de Abajo, and J. Aizpurua,“Mapping the plasmon resonances of metallic nanoantennas,” Nano Lett. 8, 631–636 (2008).
[Crossref] [PubMed]

Albanese, A.

T. Ku, J. Swaney, J.-Y. Park, A. Albanese, E. Murray, J. H. Cho, Y.-G. Park, V. Mangena, J. Chen, and K. Chung, “Multiplexed and scalable super-resolution imaging of three-dimensional protein localization in size-adjustable tissues,” Nat. Biotechnol. 34, 973–981 (2016).
[Crossref] [PubMed]

Allen, A.

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L. Wei, Z. Chen, L. Shi, R. Long, A. V. Anzalone, L. Zhang, F. Hu, R. Yuste, V. W. Cornish, and W. Min, “Super-multiplex vibrational imaging,” Nature 544, 465–470 (2017).
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ACS Photonics (1)

M. M. P. Arnob, F. Zhao, J. Li, and W.-C. Shih, “Ebl-based fabrication and different modeling approaches for nanoporous gold nanodisks,” ACS Photonics 4, 1870–1878 (2017).
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Nanoscale (2)

X. Wei, S. Su, Y. Guo, X. Jiang, Y. Zhong, Y. Su, C. Fan, S.-T. Lee, and Y. He, “Label-free, in situ SERS monitoring of individual DNA hybridization in microfluidics,” Nanoscale 6, 8521–8526 (2014).
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Figures (5)

Fig. 1
Fig. 1 UV-visible extinction spectrum (a) (Hitachi UV-vis spectrophotometer U-2001) and SERS spectrum (b) of the construct as received, diluted 20 times in PBS 1X (Sigma), which corresponds to an approximate concentration of 6.1012 nanoparticles per mL (c) Streptavidin conjugated NPs markers for immuno-labeling. SERS measuremements were obtained with 785 nm line excitation, 60 mW total power at the sample plane and 1 s integration. The SERS spectrum of the label A features a sharp and intense characteristic mode at 590 cm−1 (red arrow on b).

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Fig. 2
Fig. 2 Validation pre-expansion of the SERS nanoparticles labeling of NeuN in mouse brain coronal 10 μm sections. a) Dark-field mosaic microphotograph. Bright-field (b), DAPI (c) and SERS (d) detail of the dentate gyrus granule cell layer and pyramidal layer. Close-up dark-field (e,f) photographs and corresponding SERS (g,h) maps of the densely packed granule cells with larger pyramidal cells in between. Raw SERS spectrum (i) collected from the circled area in (d). The SERS images are mapping the total integrated intensity of the 590 cm−1 peak. SERS spectras acquisition 1 s, 60 mW total power incident at the sample plane.

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Fig. 3
Fig. 3 Expansion of the brain sections stained for NeuN with the SERS nanoparticles. Dark-field (a) and SERS (590 cm−1 band) (b) images of the expanded isocortex. (c) SERS spectrum collected from the circled area, total incident power at the sample plane 630 mW, integration 0.5 s.

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Fig. 4
Fig. 4 Dark-field (a) and UV-vis total integrated extinction map (b) of the dentate gyrus pre-expansion. UV-vis extinction spectra (c) collected at the circled areas in (b) and average extinction spectrum over the whole image. Dark-field (d) and UV-vis total integrated extinction map (e) of neurons in the cerebral cortex after expansion. UV-vis extinction spectra (f) collected at the circled areas in (e) and average extinction spectrum over the whole image. For images taken through the eyepiece port, the black lines are the measuring graticules inside the eyepiece.

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Fig. 5
Fig. 5 Dark-field colorimetric discrimination of the aggregation state of the NPs labels. Dark-field detail (a) of a picture of the pure nanoparticles (1.2 × 1014 particles per mL) drop-dried on a glass slide. Note the visible color difference between aggregated and non-aggregated areas. Simulation results (b) for the extinction of two 10 nm gold nanospheres with spacing varying between 0.5 nm and 20 nm. Dark-field images of NeuN-NPs structures in expanded brain section before (c) and after (d) hue correction.

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