Abstract

We demonstrate a simple approach for fabricating cell-compatible SERS substrates, using repeated gold deposition and thermal annealing. The substrates exhibit SERS enhancement up to six orders of magnitude and high uniformity. We have carried out Raman imaging of fixed mesenchymal stromal cells cultured directly on the substrates. Results of viability assays confirm that the substrates are highly biocompatible and Raman imaging confirms that cell attachment to the substrates is sufficient to realize significant SERS enhancement of cellular components. Using the SERS substrates as an in vitro sensing platform allowed us to identify multiple characteristic molecular fingerprints of the cells, providing a promising avenue towards non-invasive chemical characterization of biological samples.

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

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2018 (7)

I. R. Suhito, Y. Han, J. Min, H. Son, and T. H. Kim, “In situ label-free monitoring of human adipose-derived mesenchymal stem cell differentiation into multiple lineages,” Biomaterials 154, 223–233 (2018).
[Crossref]

X. S. Zheng, I. J. Jahn, K. Weber, D. Cialla-May, and J. Popp, “Label-free SERS in biological and biomedical applications: Recent progress, current challenges and opportunities,” Spectrochim. Acta, Part A 197, 56–77 (2018).
[Crossref]

S. Postaci, B. C. Yildiz, A. Bek, and M. E. Tasgin, “Silent enhancement of SERS signal without increasing hot spot intensities,” Nanophotonics 7(10), 1687–1695 (2018).
[Crossref]

V. Zivanovic, G. Semini, M. Laue, D. Drescher, T. Aebischer, and J. Kneipp, “Chemical Mapping of Leishmania Infection in Live Cells by SERS Microscopy,” Anal. Chem. 90(13), 8154–8161 (2018).
[Crossref]

Z. Xu, Z. He, Y. Song, X. Fu, M. Rommel, X. Luo, A. Hartmaier, J. Zhang, and F. Fang, “Topic Review: Application of Raman Spectroscopy Characterization in Micro/Nano-Machining,” Micromachines 9(7), 361 (2018).
[Crossref]

V. Caprettini, J. A. Huang, F. Moia, A. Jacassi, C. A. Gonano, N. Maccaferri, R. Capozza, M. Dipalo, and F. De Angelis, “Enhanced Raman Investigation of Cell Membrane and Intracellular Compounds by 3D Plasmonic Nanoelectrode Arrays,” Adv. Sci. 5(12), 1800560 (2018).
[Crossref]

Y. J. Zhang, Q. Y. Zeng, L. F. Li, M. N. Qi, Q. C. Qi, S. X. Li, and J. F. Xu, “Label-free rapid identification of tumor cells and blood cells with silver film SERS substrate,” Opt. Express 26(25), 33044–33056 (2018).
[Crossref]

2017 (5)

X. Cao, Y. Shan, L. Tan, X. Yu, M. Bao, W. Li, and H. Shi, “Hollow Au nanoflower substrates for identification and discrimination of the differentiation of bone marrow mesenchymal stem cells by surface-enhanced Raman spectroscopy,” J. Mater. Chem. B 5(30), 5983–5995 (2017).
[Crossref]

D. W. Shipp, F. Sinjab, and I. Notingher, “Raman spectroscopy: techniques and applications in the life sciences,” Adv. Opt. Photonics 9(2), 315–428 (2017).
[Crossref]

E. Sezgin, I. Levental, S. Mayor, and C. Eggeling, “The mystery of membrane organization: composition, regulation and roles of lipid rafts,” Nat. Rev. Mol. Cell Biol. 18(6), 361–374 (2017).
[Crossref]

Y. Bai, L. Yan, J. Wang, L. Su, N. Chen, and Z. Tan, “Highly reproducible and uniform SERS substrates based on Ag nanoparticles with optimized size and gap,” Photonics and Nanostructures - Fundamentals and Applications 23, 58–63 (2017).
[Crossref]

N. Wang, C. Chen, D. Yang, Q. Liao, H. Luo, X. Wang, F. Zhou, X. Yang, J. Yang, C. Zeng, and W. E. Wang, “Mesenchymal stem cells-derived extracellular vesicles, via miR-210, improve infarcted cardiac function by promotion of angiogenesis,” Biochim. Biophys. Acta, Mol. Basis Dis. 1863, 2085–2092 (2017).
[Crossref]

2016 (9)

T. Squillaro, G. Peluso, and U. Galderisi, “Clinical Trials With Mesenchymal Stem Cells: An Update,” Cell Transplant 25(5), 829–848 (2016).
[Crossref]

A. M. Jubb, Y. Jiao, G. Eres, S. T. Retterer, and B. Gu, “Elevated gold ellipse nanoantenna dimers as sensitive and tunable surface enhanced Raman spectroscopy substrates,” Nanoscale 8(10), 5641–5648 (2016).
[Crossref]

K. Simons, “Cell membranes: A subjective perspective,” Biochim. Biophys. Acta, Biomembr. 1858(10), 2569–2572 (2016).
[Crossref]

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
[Crossref]

R. P. Berger, M. Dookwah, R. Steet, and S. Dalton, “Glycosylation and stem cells: Regulatory roles and application of iPSCs in the study of glycosylation-related disorders,” BioEssays 38(12), 1255–1265 (2016).
[Crossref]

L. Zhang, C. Guan, Y. Wang, and J. Liao, “Highly effective and uniform SERS substrates fabricated by etching multi-layered gold nanoparticle arrays,” Nanoscale 8(11), 5928–5937 (2016).
[Crossref]

M. Altunbek, G. Kuku, and M. Culha, “Gold Nanoparticles in Single-Cell Analysis for Surface Enhanced Raman Scattering,” Molecules 21(12), 1617 (2016).
[Crossref]

F. Lussier, T. Brule, M. Vishwakarma, T. Das, J. P. Spatz, and J. F. Masson, “Dynamic-SERS Optophysiology: A Nanosensor for Monitoring Cell Secretion Events,” Nano Lett. 16(6), 3866–3871 (2016).
[Crossref]

Y. Sharma and A. Dhawan, “Plasmonic “nano-fingers on nanowires” as SERS substrates,” Opt. Lett. 41(9), 2085–2088 (2016).
[Crossref]

2015 (8)

M. Kang, S. G. Park, and K. H. Jeong, “Repeated Solid-state Dewetting of Thin Gold Films for Nanogap-rich Plasmonic Nanoislands,” Sci. Rep. 5(1), 14790 (2015).
[Crossref]

W. A. El-Said, S. U. Kim, and J.-W. Choi, “Monitoring in vitro neural stem cell differentiation based on surface-enhanced Raman spectroscopy using a gold nanostar array,” J. Mater. Chem. C 3(16), 3848–3859 (2015).
[Crossref]

C. Lee, R. P. Carney, S. Hazari, Z. J. Smith, A. Knudson, C. S. Robertson, K. S. Lam, and S. Wachsmann-Hogiu, “3D plasmonic nanobowl platform for the study of exosomes in solution,” Nanoscale 7(20), 9290–9297 (2015).
[Crossref]

L. Mikoliunaite, R. D. Rodriguez, E. Sheremet, V. Kolchuzhin, J. Mehner, A. Ramanavicius, and D. R. Zahn, “The substrate matters in the Raman spectroscopy analysis of cells,” Sci. Rep. 5(1), 13150 (2015).
[Crossref]

B. Kann, H. L. Offerhaus, M. Windbergs, and C. Otto, “Raman microscopy for cellular investigations - From single cell imaging to drug carrier uptake visualization,” Adv. Drug Delivery Rev. 89, 71–90 (2015).
[Crossref]

K. Czamara, K. Majzner, M. Z. Pacia, K. Kochan, A. Kaczor, and M. Baranska, “Raman spectroscopy of lipids: a review,” J. Raman Spectrosc. 46(1), 4–20 (2015).
[Crossref]

R. La Rocca, G. C. Messina, M. Dipalo, V. Shalabaeva, and F. De Angelis, “Out-of-Plane Plasmonic Antennas for Raman Analysis in Living Cells,” Small 11(36), 4632–4637 (2015).
[Crossref]

A. Kossoy, V. Merk, D. Simakov, K. Leosson, S. Kéna-Cohen, and S. A. Maier, “Optical and Structural Properties of Ultra-thin Gold Films,” Adv. Opt. Mater. 3(1), 71–77 (2015).
[Crossref]

2013 (9)

V. Merk, J. Kneipp, and K. Leosson, “Gap Size Reduction and Increased SERS Enhancement in Lithographically Patterned Nanoparticle Arrays by Templated Growth,” Adv. Opt. Mater. 1(4), 313–318 (2013).
[Crossref]

N. Lall, C. J. Henley-Smith, M. N. De Canha, C. B. Oosthuizen, and D. Berrington, “Viability Reagent, PrestoBlue, in Comparison with Other Available Reagents, Utilized in Cytotoxicity and Antimicrobial Assays,” Int J Microbiol 2013, 420601 (2013).
[Crossref]

M. Moskovits, “Persistent misconceptions regarding SERS,” Phys. Chem. Chem. Phys. 15(15), 5301–5311 (2013).
[Crossref]

E. C. Le Ru and P. G. Etchegoin, “Quantifying SERS enhancements,” MRS Bull. 38(8), 631–640 (2013).
[Crossref]

A. J. de Jesus and T. W. Allen, “The role of tryptophan side chains in membrane protein anchoring and hydrophobic mismatch,” Biochim. Biophys. Acta, Biomembr. 1828(2), 864–876 (2013).
[Crossref]

A. Rygula, K. Majzner, K. M. Marzec, A. Kaczor, M. Pilarczyk, and M. Baranska, “Raman spectroscopy of proteins: a review,” J. Raman Spectrosc. 44(8), 1061–1076 (2013).
[Crossref]

D. Wang, W. Zhu, M. D. Best, J. P. Camden, and K. B. Crozier, “Wafer-scale metasurface for total power absorption, local field enhancement and single molecule Raman spectroscopy,” Sci. Rep. 3(1), 2867 (2013).
[Crossref]

X. Sun and H. Li, “Gold nanoisland arrays by repeated deposition and post-deposition annealing for surface-enhanced Raman spectroscopy,” Nanotechnology 24(35), 355706 (2013).
[Crossref]

Q. Jiwei, L. Yudong, Y. Ming, W. Qiang, C. Zongqiang, W. Wudeng, L. Wenqiang, Y. Xuanyi, X. Jingjun, and S. Qian, “Large-area high-performance SERS substrates with deep controllable sub-10-nm gap structure fabricated by depositing Au film on the cicada wing,” Nanoscale Res. Lett. 8(1), 437 (2013).
[Crossref]

2012 (1)

M. S. Schmidt, J. Hubner, and A. Boisen, “Large area fabrication of leaning silicon nanopillars for surface enhanced Raman spectroscopy,” Adv. Mater. 24(10), OP11–OP18 (2012).
[Crossref]

2011 (2)

V. Joseph, A. Matschulat, J. Polte, S. Rolf, F. Emmerling, and J. Kneipp, “SERS enhancement of gold nanospheres of defined size,” J. Raman Spectrosc. 42(9), 1736–1742 (2011).
[Crossref]

U. Coskun and K. Simons, “Cell membranes: the lipid perspective,” Structure 19(11), 1543–1548 (2011).
[Crossref]

2010 (3)

T. Vo-Dinh, A. Dhawan, S. J. Norton, C. G. Khoury, H. N. Wang, V. Misra, and M. D. Gerhold, “Plasmonic Nanoparticles and Nanowires: Design, Fabrication and Application in Sensing,” J. Phys. Chem. C 114(16), 7480–7488 (2010).
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J. Kneipp, H. Kneipp, B. Wittig, and K. Kneipp, “Novel optical nanosensors for probing and imaging live cells,” Nanomedicine 6(2), 214–226 (2010).
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N. Ruiz, S. S. Chng, A. Hiniker, D. Kahne, and T. J. Silhavy, “Nonconsecutive disulfide bond formation in an essential integral outer membrane protein,” Proc. Natl. Acad. Sci. U. S. A. 107(27), 12245–12250 (2010).
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2007 (3)

Z. Movasaghi, S. Rehman, and I. U. Rehman, “Raman Spectroscopy of Biological Tissues,” Appl. Spectrosc. Rev. 42(5), 493–541 (2007).
[Crossref]

M. Sackmann, S. Bom, T. Balster, and A. Materny, “Nanostructured gold surfaces as reproducible substrates for surface-enhanced Raman spectroscopy,” J. Raman Spectrosc. 38(3), 277–282 (2007).
[Crossref]

A. K. Oyelere, P. C. Chen, X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Peptide-conjugated gold nanorods for nuclear targeting,” Bioconjugate Chem. 18(5), 1490–1497 (2007).
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2006 (3)

S. J. Lee, A. R. Morrill, and M. Moskovits, “Hot spots in silver nanowire bundles for surface-enhanced Raman spectroscopy,” J. Am. Chem. Soc. 128(7), 2200–2201 (2006).
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J. Kneipp, H. Kneipp, M. McLaughlin, D. Brown, and K. Kneipp, “In vivo molecular probing of cellular compartments with gold nanoparticles and nanoaggregates,” Nano Lett. 6(10), 2225–2231 (2006).
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A. Keating, “Mesenchymal stromal cells,” Curr. Opin. Hematol. 13(6), 419–425 (2006).
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2005 (5)

A. Kudelski, “Raman studies of rhodamine 6G and crystal violet sub-monolayers on electrochemically roughened silver substrates: Do dye molecules adsorb preferentially on highly SERS-active sites,” Chem. Phys. Lett. 414(4-6), 271–275 (2005).
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C. Krafft, L. Neudert, T. Simat, and R. Salzer, “Near infrared Raman spectra of human brain lipids,” Spectrochim. Acta, Part A 61(7), 1529–1535 (2005).
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M. Moskovits and B. Vlckova, “Adsorbate-induced silver nanoparticle aggregation kinetics,” J. Phys. Chem. B 109(31), 14755–14758 (2005).
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J. Kneipp, H. Kneipp, W. L. Rice, and K. Kneipp, “Optical probes for biological applications based on surface-enhanced Raman scattering from indocyanine green on gold nanoparticles,” Anal. Chem. 77(8), 2381–2385 (2005).
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C. J. Orendorff, A. Gole, T. K. Sau, and C. J. Murphy, “Surface-enhanced Raman spectroscopy of self-assembled monolayers: sandwich architecture and nanoparticle shape dependence,” Anal. Chem. 77(10), 3261–3266 (2005).
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2004 (1)

A. G. Tkachenko, H. Xie, Y. Liu, D. Coleman, J. Ryan, W. R. Glomm, M. K. Shipton, S. Franzen, and D. L. Feldheim, “Cellular trajectories of peptide-modified gold particle complexes: comparison of nuclear localization signals and peptide transduction domains,” Bioconjugate Chem. 15(3), 482–490 (2004).
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2003 (1)

F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, J. Sany, D. Noel, and C. Jorgensen, “Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals,” Blood 102(10), 3837–3844 (2003).
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1999 (1)

D. Borchman, D. Tang, and M. C. Yappert, “Lipid composition, membrane structure relationships in lens and muscle sarcoplasmic reticulum membranes,” Biospectroscopy 5(3), 151–167 (1999).
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1991 (1)

A. I. Caplan, “Mesenchymal stem cells,” J. Orthop. Res. 9(5), 641–650 (1991).
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1983 (1)

C. Korzeniewski and D. M. Callewaert, “An enzyme-release assay for natural cytotoxicity,” J. Immunol. Methods 64(3), 313–320 (1983).
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1977 (2)

D. L. Jeanmaire and R. P. Van Duyne, “Surface raman spectroelectrochemistry,” J. Electroanal. Chem. Interfacial Electrochem. 84(1), 1–20 (1977).
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M. G. Albrecht and J. A. Creighton, “Anomalously intense Raman spectra of pyridine at a silver electrode,” J. Am. Chem. Soc. 99(15), 5215–5217 (1977).
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1974 (1)

M. Fleischmann, P. J. Hendra, and A. J. Mcquillan, “Raman-Spectra of Pyridine Adsorbed at a Silver Electrode,” Chem. Phys. Lett. 26(2), 163–166 (1974).
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1972 (1)

P. B. Johnson and R. W. Christy, “Optical Constants of the Noble Metals,” Phys. Rev. B 6(12), 4370–4379 (1972).
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1939 (1)

J. H. Hibben, “The Raman effect and its chemical applications,” Industrial and Engineering Chemistry, News Edition 17, 556 (1939).
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Aebischer, T.

V. Zivanovic, G. Semini, M. Laue, D. Drescher, T. Aebischer, and J. Kneipp, “Chemical Mapping of Leishmania Infection in Live Cells by SERS Microscopy,” Anal. Chem. 90(13), 8154–8161 (2018).
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Alberts, B.

B. Alberts, J. H. Wilson, and T. Hunt, Molecular Biology of the Cell, 5th ed. (Garland Science, 2008), pp. xxxiii, 1601, 1690 p.

Albrecht, M. G.

M. G. Albrecht and J. A. Creighton, “Anomalously intense Raman spectra of pyridine at a silver electrode,” J. Am. Chem. Soc. 99(15), 5215–5217 (1977).
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Allen, T. W.

A. J. de Jesus and T. W. Allen, “The role of tryptophan side chains in membrane protein anchoring and hydrophobic mismatch,” Biochim. Biophys. Acta, Biomembr. 1828(2), 864–876 (2013).
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Altunbek, M.

M. Altunbek, G. Kuku, and M. Culha, “Gold Nanoparticles in Single-Cell Analysis for Surface Enhanced Raman Scattering,” Molecules 21(12), 1617 (2016).
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Apparailly, F.

F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, J. Sany, D. Noel, and C. Jorgensen, “Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals,” Blood 102(10), 3837–3844 (2003).
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Ashton, L.

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
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Bai, Y.

Y. Bai, L. Yan, J. Wang, L. Su, N. Chen, and Z. Tan, “Highly reproducible and uniform SERS substrates based on Ag nanoparticles with optimized size and gap,” Photonics and Nanostructures - Fundamentals and Applications 23, 58–63 (2017).
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Balster, T.

M. Sackmann, S. Bom, T. Balster, and A. Materny, “Nanostructured gold surfaces as reproducible substrates for surface-enhanced Raman spectroscopy,” J. Raman Spectrosc. 38(3), 277–282 (2007).
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Bao, M.

X. Cao, Y. Shan, L. Tan, X. Yu, M. Bao, W. Li, and H. Shi, “Hollow Au nanoflower substrates for identification and discrimination of the differentiation of bone marrow mesenchymal stem cells by surface-enhanced Raman spectroscopy,” J. Mater. Chem. B 5(30), 5983–5995 (2017).
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Baranska, M.

K. Czamara, K. Majzner, M. Z. Pacia, K. Kochan, A. Kaczor, and M. Baranska, “Raman spectroscopy of lipids: a review,” J. Raman Spectrosc. 46(1), 4–20 (2015).
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A. Rygula, K. Majzner, K. M. Marzec, A. Kaczor, M. Pilarczyk, and M. Baranska, “Raman spectroscopy of proteins: a review,” J. Raman Spectrosc. 44(8), 1061–1076 (2013).
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S. Postaci, B. C. Yildiz, A. Bek, and M. E. Tasgin, “Silent enhancement of SERS signal without increasing hot spot intensities,” Nanophotonics 7(10), 1687–1695 (2018).
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Berger, R. P.

R. P. Berger, M. Dookwah, R. Steet, and S. Dalton, “Glycosylation and stem cells: Regulatory roles and application of iPSCs in the study of glycosylation-related disorders,” BioEssays 38(12), 1255–1265 (2016).
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Berrington, D.

N. Lall, C. J. Henley-Smith, M. N. De Canha, C. B. Oosthuizen, and D. Berrington, “Viability Reagent, PrestoBlue, in Comparison with Other Available Reagents, Utilized in Cytotoxicity and Antimicrobial Assays,” Int J Microbiol 2013, 420601 (2013).
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Best, M. D.

D. Wang, W. Zhu, M. D. Best, J. P. Camden, and K. B. Crozier, “Wafer-scale metasurface for total power absorption, local field enhancement and single molecule Raman spectroscopy,” Sci. Rep. 3(1), 2867 (2013).
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Bird, B.

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
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Boisen, A.

M. S. Schmidt, J. Hubner, and A. Boisen, “Large area fabrication of leaning silicon nanopillars for surface enhanced Raman spectroscopy,” Adv. Mater. 24(10), OP11–OP18 (2012).
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Bom, S.

M. Sackmann, S. Bom, T. Balster, and A. Materny, “Nanostructured gold surfaces as reproducible substrates for surface-enhanced Raman spectroscopy,” J. Raman Spectrosc. 38(3), 277–282 (2007).
[Crossref]

Bony, C.

F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, J. Sany, D. Noel, and C. Jorgensen, “Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals,” Blood 102(10), 3837–3844 (2003).
[Crossref]

Borchman, D.

D. Borchman, D. Tang, and M. C. Yappert, “Lipid composition, membrane structure relationships in lens and muscle sarcoplasmic reticulum membranes,” Biospectroscopy 5(3), 151–167 (1999).
[Crossref]

Brown, D.

J. Kneipp, H. Kneipp, M. McLaughlin, D. Brown, and K. Kneipp, “In vivo molecular probing of cellular compartments with gold nanoparticles and nanoaggregates,” Nano Lett. 6(10), 2225–2231 (2006).
[Crossref]

Brule, T.

F. Lussier, T. Brule, M. Vishwakarma, T. Das, J. P. Spatz, and J. F. Masson, “Dynamic-SERS Optophysiology: A Nanosensor for Monitoring Cell Secretion Events,” Nano Lett. 16(6), 3866–3871 (2016).
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Butler, H. J.

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
[Crossref]

Callewaert, D. M.

C. Korzeniewski and D. M. Callewaert, “An enzyme-release assay for natural cytotoxicity,” J. Immunol. Methods 64(3), 313–320 (1983).
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Camden, J. P.

D. Wang, W. Zhu, M. D. Best, J. P. Camden, and K. B. Crozier, “Wafer-scale metasurface for total power absorption, local field enhancement and single molecule Raman spectroscopy,” Sci. Rep. 3(1), 2867 (2013).
[Crossref]

Cao, X.

X. Cao, Y. Shan, L. Tan, X. Yu, M. Bao, W. Li, and H. Shi, “Hollow Au nanoflower substrates for identification and discrimination of the differentiation of bone marrow mesenchymal stem cells by surface-enhanced Raman spectroscopy,” J. Mater. Chem. B 5(30), 5983–5995 (2017).
[Crossref]

Caplan, A. I.

A. I. Caplan, “Mesenchymal stem cells,” J. Orthop. Res. 9(5), 641–650 (1991).
[Crossref]

Capozza, R.

V. Caprettini, J. A. Huang, F. Moia, A. Jacassi, C. A. Gonano, N. Maccaferri, R. Capozza, M. Dipalo, and F. De Angelis, “Enhanced Raman Investigation of Cell Membrane and Intracellular Compounds by 3D Plasmonic Nanoelectrode Arrays,” Adv. Sci. 5(12), 1800560 (2018).
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Caprettini, V.

V. Caprettini, J. A. Huang, F. Moia, A. Jacassi, C. A. Gonano, N. Maccaferri, R. Capozza, M. Dipalo, and F. De Angelis, “Enhanced Raman Investigation of Cell Membrane and Intracellular Compounds by 3D Plasmonic Nanoelectrode Arrays,” Adv. Sci. 5(12), 1800560 (2018).
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Carney, R. P.

C. Lee, R. P. Carney, S. Hazari, Z. J. Smith, A. Knudson, C. S. Robertson, K. S. Lam, and S. Wachsmann-Hogiu, “3D plasmonic nanobowl platform for the study of exosomes in solution,” Nanoscale 7(20), 9290–9297 (2015).
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Chen, C.

N. Wang, C. Chen, D. Yang, Q. Liao, H. Luo, X. Wang, F. Zhou, X. Yang, J. Yang, C. Zeng, and W. E. Wang, “Mesenchymal stem cells-derived extracellular vesicles, via miR-210, improve infarcted cardiac function by promotion of angiogenesis,” Biochim. Biophys. Acta, Mol. Basis Dis. 1863, 2085–2092 (2017).
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Chen, N.

Y. Bai, L. Yan, J. Wang, L. Su, N. Chen, and Z. Tan, “Highly reproducible and uniform SERS substrates based on Ag nanoparticles with optimized size and gap,” Photonics and Nanostructures - Fundamentals and Applications 23, 58–63 (2017).
[Crossref]

Chen, P. C.

A. K. Oyelere, P. C. Chen, X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Peptide-conjugated gold nanorods for nuclear targeting,” Bioconjugate Chem. 18(5), 1490–1497 (2007).
[Crossref]

Chng, S. S.

N. Ruiz, S. S. Chng, A. Hiniker, D. Kahne, and T. J. Silhavy, “Nonconsecutive disulfide bond formation in an essential integral outer membrane protein,” Proc. Natl. Acad. Sci. U. S. A. 107(27), 12245–12250 (2010).
[Crossref]

Choi, J.-W.

W. A. El-Said, S. U. Kim, and J.-W. Choi, “Monitoring in vitro neural stem cell differentiation based on surface-enhanced Raman spectroscopy using a gold nanostar array,” J. Mater. Chem. C 3(16), 3848–3859 (2015).
[Crossref]

Christy, R. W.

P. B. Johnson and R. W. Christy, “Optical Constants of the Noble Metals,” Phys. Rev. B 6(12), 4370–4379 (1972).
[Crossref]

Cialla-May, D.

X. S. Zheng, I. J. Jahn, K. Weber, D. Cialla-May, and J. Popp, “Label-free SERS in biological and biomedical applications: Recent progress, current challenges and opportunities,” Spectrochim. Acta, Part A 197, 56–77 (2018).
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Cinque, G.

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
[Crossref]

Coleman, D.

A. G. Tkachenko, H. Xie, Y. Liu, D. Coleman, J. Ryan, W. R. Glomm, M. K. Shipton, S. Franzen, and D. L. Feldheim, “Cellular trajectories of peptide-modified gold particle complexes: comparison of nuclear localization signals and peptide transduction domains,” Bioconjugate Chem. 15(3), 482–490 (2004).
[Crossref]

Coskun, U.

U. Coskun and K. Simons, “Cell membranes: the lipid perspective,” Structure 19(11), 1543–1548 (2011).
[Crossref]

Creighton, J. A.

M. G. Albrecht and J. A. Creighton, “Anomalously intense Raman spectra of pyridine at a silver electrode,” J. Am. Chem. Soc. 99(15), 5215–5217 (1977).
[Crossref]

Crozier, K. B.

D. Wang, W. Zhu, M. D. Best, J. P. Camden, and K. B. Crozier, “Wafer-scale metasurface for total power absorption, local field enhancement and single molecule Raman spectroscopy,” Sci. Rep. 3(1), 2867 (2013).
[Crossref]

Culha, M.

M. Altunbek, G. Kuku, and M. Culha, “Gold Nanoparticles in Single-Cell Analysis for Surface Enhanced Raman Scattering,” Molecules 21(12), 1617 (2016).
[Crossref]

Curtis, K.

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
[Crossref]

Czamara, K.

K. Czamara, K. Majzner, M. Z. Pacia, K. Kochan, A. Kaczor, and M. Baranska, “Raman spectroscopy of lipids: a review,” J. Raman Spectrosc. 46(1), 4–20 (2015).
[Crossref]

Dalton, S.

R. P. Berger, M. Dookwah, R. Steet, and S. Dalton, “Glycosylation and stem cells: Regulatory roles and application of iPSCs in the study of glycosylation-related disorders,” BioEssays 38(12), 1255–1265 (2016).
[Crossref]

Das, T.

F. Lussier, T. Brule, M. Vishwakarma, T. Das, J. P. Spatz, and J. F. Masson, “Dynamic-SERS Optophysiology: A Nanosensor for Monitoring Cell Secretion Events,” Nano Lett. 16(6), 3866–3871 (2016).
[Crossref]

De Angelis, F.

V. Caprettini, J. A. Huang, F. Moia, A. Jacassi, C. A. Gonano, N. Maccaferri, R. Capozza, M. Dipalo, and F. De Angelis, “Enhanced Raman Investigation of Cell Membrane and Intracellular Compounds by 3D Plasmonic Nanoelectrode Arrays,” Adv. Sci. 5(12), 1800560 (2018).
[Crossref]

R. La Rocca, G. C. Messina, M. Dipalo, V. Shalabaeva, and F. De Angelis, “Out-of-Plane Plasmonic Antennas for Raman Analysis in Living Cells,” Small 11(36), 4632–4637 (2015).
[Crossref]

De Canha, M. N.

N. Lall, C. J. Henley-Smith, M. N. De Canha, C. B. Oosthuizen, and D. Berrington, “Viability Reagent, PrestoBlue, in Comparison with Other Available Reagents, Utilized in Cytotoxicity and Antimicrobial Assays,” Int J Microbiol 2013, 420601 (2013).
[Crossref]

de Jesus, A. J.

A. J. de Jesus and T. W. Allen, “The role of tryptophan side chains in membrane protein anchoring and hydrophobic mismatch,” Biochim. Biophys. Acta, Biomembr. 1828(2), 864–876 (2013).
[Crossref]

Dhawan, A.

Y. Sharma and A. Dhawan, “Plasmonic “nano-fingers on nanowires” as SERS substrates,” Opt. Lett. 41(9), 2085–2088 (2016).
[Crossref]

T. Vo-Dinh, A. Dhawan, S. J. Norton, C. G. Khoury, H. N. Wang, V. Misra, and M. D. Gerhold, “Plasmonic Nanoparticles and Nanowires: Design, Fabrication and Application in Sensing,” J. Phys. Chem. C 114(16), 7480–7488 (2010).
[Crossref]

Dipalo, M.

V. Caprettini, J. A. Huang, F. Moia, A. Jacassi, C. A. Gonano, N. Maccaferri, R. Capozza, M. Dipalo, and F. De Angelis, “Enhanced Raman Investigation of Cell Membrane and Intracellular Compounds by 3D Plasmonic Nanoelectrode Arrays,” Adv. Sci. 5(12), 1800560 (2018).
[Crossref]

R. La Rocca, G. C. Messina, M. Dipalo, V. Shalabaeva, and F. De Angelis, “Out-of-Plane Plasmonic Antennas for Raman Analysis in Living Cells,” Small 11(36), 4632–4637 (2015).
[Crossref]

Djouad, F.

F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, J. Sany, D. Noel, and C. Jorgensen, “Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals,” Blood 102(10), 3837–3844 (2003).
[Crossref]

Dookwah, M.

R. P. Berger, M. Dookwah, R. Steet, and S. Dalton, “Glycosylation and stem cells: Regulatory roles and application of iPSCs in the study of glycosylation-related disorders,” BioEssays 38(12), 1255–1265 (2016).
[Crossref]

Dorney, J.

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
[Crossref]

Drescher, D.

V. Zivanovic, G. Semini, M. Laue, D. Drescher, T. Aebischer, and J. Kneipp, “Chemical Mapping of Leishmania Infection in Live Cells by SERS Microscopy,” Anal. Chem. 90(13), 8154–8161 (2018).
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Eggeling, C.

E. Sezgin, I. Levental, S. Mayor, and C. Eggeling, “The mystery of membrane organization: composition, regulation and roles of lipid rafts,” Nat. Rev. Mol. Cell Biol. 18(6), 361–374 (2017).
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El-Said, W. A.

W. A. El-Said, S. U. Kim, and J.-W. Choi, “Monitoring in vitro neural stem cell differentiation based on surface-enhanced Raman spectroscopy using a gold nanostar array,” J. Mater. Chem. C 3(16), 3848–3859 (2015).
[Crossref]

El-Sayed, I. H.

A. K. Oyelere, P. C. Chen, X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Peptide-conjugated gold nanorods for nuclear targeting,” Bioconjugate Chem. 18(5), 1490–1497 (2007).
[Crossref]

El-Sayed, M. A.

A. K. Oyelere, P. C. Chen, X. Huang, I. H. El-Sayed, and M. A. El-Sayed, “Peptide-conjugated gold nanorods for nuclear targeting,” Bioconjugate Chem. 18(5), 1490–1497 (2007).
[Crossref]

Emmerling, F.

V. Joseph, A. Matschulat, J. Polte, S. Rolf, F. Emmerling, and J. Kneipp, “SERS enhancement of gold nanospheres of defined size,” J. Raman Spectrosc. 42(9), 1736–1742 (2011).
[Crossref]

Eres, G.

A. M. Jubb, Y. Jiao, G. Eres, S. T. Retterer, and B. Gu, “Elevated gold ellipse nanoantenna dimers as sensitive and tunable surface enhanced Raman spectroscopy substrates,” Nanoscale 8(10), 5641–5648 (2016).
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Esmonde-White, K.

H. J. Butler, L. Ashton, B. Bird, G. Cinque, K. Curtis, J. Dorney, K. Esmonde-White, N. J. Fullwood, B. Gardner, P. L. Martin-Hirsch, M. J. Walsh, M. R. McAinsh, N. Stone, and F. L. Martin, “Using Raman spectroscopy to characterize biological materials,” Nat. Protoc. 11(4), 664–687 (2016).
[Crossref]

Etchegoin, P. G.

E. C. Le Ru and P. G. Etchegoin, “Quantifying SERS enhancements,” MRS Bull. 38(8), 631–640 (2013).
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Fang, F.

Z. Xu, Z. He, Y. Song, X. Fu, M. Rommel, X. Luo, A. Hartmaier, J. Zhang, and F. Fang, “Topic Review: Application of Raman Spectroscopy Characterization in Micro/Nano-Machining,” Micromachines 9(7), 361 (2018).
[Crossref]

Feldheim, D. L.

A. G. Tkachenko, H. Xie, Y. Liu, D. Coleman, J. Ryan, W. R. Glomm, M. K. Shipton, S. Franzen, and D. L. Feldheim, “Cellular trajectories of peptide-modified gold particle complexes: comparison of nuclear localization signals and peptide transduction domains,” Bioconjugate Chem. 15(3), 482–490 (2004).
[Crossref]

Fleischmann, M.

M. Fleischmann, P. J. Hendra, and A. J. Mcquillan, “Raman-Spectra of Pyridine Adsorbed at a Silver Electrode,” Chem. Phys. Lett. 26(2), 163–166 (1974).
[Crossref]

Franzen, S.

A. G. Tkachenko, H. Xie, Y. Liu, D. Coleman, J. Ryan, W. R. Glomm, M. K. Shipton, S. Franzen, and D. L. Feldheim, “Cellular trajectories of peptide-modified gold particle complexes: comparison of nuclear localization signals and peptide transduction domains,” Bioconjugate Chem. 15(3), 482–490 (2004).
[Crossref]

Fu, X.

Z. Xu, Z. He, Y. Song, X. Fu, M. Rommel, X. Luo, A. Hartmaier, J. Zhang, and F. Fang, “Topic Review: Application of Raman Spectroscopy Characterization in Micro/Nano-Machining,” Micromachines 9(7), 361 (2018).
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Figures (9)

Fig. 1.
Fig. 1. Schematic illustrations of the fabrication process involving repeated gold deposition (A, C, E) and subsequent post-deposition thermal annealing (B, D, F) resulting in nanoparticle aggregation.
Fig. 2.
Fig. 2. A) Scanning electron micrographs of SERS substrates at different stages of fabrication. Upper images correspond to 1st, 2nd and 3rd gold deposition and lower images correspond to 1st, 2nd and 3rd thermal annealing. All scale bars represent 100 nm. B) Particle size distributions corresponding to each step of sample fabrication after annealing. C) AFM images corresponding to sequential steps of deposition and post-deposition annealing (step 1, 2 and 3).
Fig. 3.
Fig. 3. A) FDTD simulations showing the product of field intensities at an excitation wavelength of 785 nm and a Raman scattered wavelength of 830 nm (|E|2exc·|E|2Stokes), which relates to the SERS enhancement in the experiment. The calculations were performed for structures modelled according to the gold particle geometry following steps 1, 2 and 3 of substrate fabrication (Fig. 2A). The direction of polarization of the incident light is indicated with the white arrow. B) Maximum product of field intensities at excitation wavelength 785 nm and Stokes wavelength 830 nm for different heights above the glass surface. C) Maximum field enhancement factor obtained by FDTD simulations for sequential fabrication steps, averaged over the simulated range of heights and Stokes wavelengths.
Fig. 4.
Fig. 4. A) Representative single SERS spectrum of crystal violet (c = 10−4 M). The signal at 1618 cm−1 (marked in green) was used to estimate the enhancement factor (excitation: 785 nm, intensity: 2.0 × 105 W·cm−2, acquisition time: 1 s). B) Experimentally determined SERS enhancement factor for each step of substrate fabrication. Inset: Schematic distribution of enhancement factors at positions (x,y) on a substrate after three deposition and annealing steps. Data points are separated by 10 µm in x and y and the diameter of the probed spot was 1 µm (not to scale in the schematic).
Fig. 5.
Fig. 5. A) Results for PrestoBlue cell proliferation assay for BM-MSCs cultured on glass controls and on SERS substrates (n = 3), error bars represent the standard deviation. B) Results for LDH cell cytotoxicity assay for BM-MSCs cultured on glass controls and SERS substrates (n = 3), error bars represent the standard deviation. C) Representative confocal image of focal adhesion plaques (green), actin cytoskeleton (red) and nuclei of mesenchymal stromal cells (blue) grown on a SERS substrate and D) on a conventional culture slide as control. Scale bars: 20 µm.
Fig. 6.
Fig. 6. Representative Raman spectra obtained on mesenchymal stromal cell (BM-MSC) grown on a SERS substrate described in the text (red line) and on a glass cover slip (black line), respectively. The same excitation and collection conditions were used in both cases (excitation: 785 nm, intensity: 2.0 × 105 W·cm−2, acquisition time: 3 s).
Fig. 7.
Fig. 7. Representative SERS spectra extracted from the mapping datasets of two different mesenchymal stromal cells on two different SERS substrates (excitation: 785 nm, intensity: 2.0 × 105 W·cm−2, acquisition time: 3 s, step size: 2 µm).
Fig. 8.
Fig. 8. Raman maps showing the distribution of SERS signals in two different BM-MSCs on two different SERS substrates, and their overlay with microscope images. Raman maps are generated by mapping intensities at 418 cm−1 assigned to cholesterol (green), 1140 cm−1 to phospholipid alkyl chains (red), 1440 cm−1 to CH2 deformation in lipids (red) and 1270 cm−1 to C = C groups in unsaturated fatty acids (green), 524 cm−1 to S-S disulfide stretching in proteins (blue), 1002 cm−1 to phenylalanine symmetric C-C stretching (blue), 1552 cm−1 to tryptophan C = C stretching (blue) and 842 cm−1 to polysaccharides (yellow). Scale bars: 10 µm.
Fig. 9.
Fig. 9. Chemical image displaying the distribution of the band intensity at 418 cm−1, assigned to cholesterol, followed by example spectra extracted from the maps at two different points labeled in the panel. The SERS spectra represent two different intensities of the 418 cm−1 band (excitation: 785 nm, intensity: 2.0 × 105 W·cm−2, acquisition time: 3 s, step size: 2 µm). Scale bar: 10 µm.

Tables (1)

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Table 1. Tentative assignments of the most representative bands in the SERS spectra of BM-MSC cells obtained during mapping, based on Refs. [18,5055,5759]

Equations (1)

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E F = I S E R S N R S I R S N S E R S