By combining photonic crystal label-free biosensor imaging with photonic crystal enhanced fluorescence, it is possible to selectively enhance the fluorescence emission from regions of the PC surface based upon the density of immobilized capture molecules. A label-free image of the capture molecules enables determination of optimal coupling conditions of the laser used for fluorescence imaging of the photonic crystal surface on a pixel-by-pixel basis, allowing maximization of fluorescence enhancement factor from regions incorporating a biomolecule capture spot and minimization of background autofluorescence from areas between capture spots. This capability significantly improves the contrast of enhanced fluorescent images, and when applied to an antibody protein microarray, provides a substantial advantage over conventional fluorescence microscopy. Using the new approach, we demonstrate detection limits as low as 0.97 pg/ml for a representative protein biomarker in buffer.

© 2011 OSA

1. M. Schena and R. W. Davis, “Genes, Genomes, and chips,” in DNA Microarrays: A Practical Approach, M. Schena, ed. (Oxford Press, New York, 1999).
2. R. Beneke, “Microarray detection with laser scanning device,” in Advanced Methods: DNA Microarrays, U. A. Nuber, ed. (Taylor & Francis Group, New York, 2005).
3. C. R. Sabanayagam and J. R. Lakowicz, “Increasing the sensitivity of DNA microarrays by metal-enhanced fluorescence using surface-bound silver nanoparticles,” Nucleic Acids Res.35(2), e13 (2006). [CrossRef] [PubMed]
4. R. A. Irizarry, D. Warren, F. Spencer, I. F. Kim, S. Biswal, B. C. Frank, E. Gabrielson, J. G. Garcia, J. Geoghegan, G. Germino, C. Griffin, S. C. Hilmer, E. Hoffman, A. E. Jedlicka, E. Kawasaki, F. Martínez-Murillo, L. Morsberger, H. Lee, D. Petersen, J. Quackenbush, A. Scott, M. Wilson, Y. Yang, S. Q. Ye, and W. Yu, “Multiple-laboratory comparison of microarray platforms,” Nat. Methods2(5), 345–350 (2005). [CrossRef] [PubMed]
5. Y. Fu and J. R. Lakowicz, “Enhanced fluorescence of Cy5-labeled DNA tethered to silver island films: fluorescence images and time-resolved studies using single-molecule spectroscopy,” Anal. Chem.78(17), 6238–6245 (2006). [CrossRef] [PubMed]
6. R. C. Zangar, S. M. Varnum, and N. Bollinger, “Studying cellular processes and detecting disease with protein microarrays,” Drug Metab. Rev.37(3), 473–487 (2005). [CrossRef] [PubMed]
7. R. C. Zangar, D. S. Daly, and A. M. White, “ELISA microarray technology as a high-throughput system for cancer biomarker validation,” Expert Rev. Proteomics3(1), 37–44 (2006). [CrossRef] [PubMed]
8. S. F. Kingsmore, “Multiplexed protein measurement: technologies and applications of protein and antibody arrays,” Nat. Rev. Drug Discov.5(4), 310–321 (2006). [CrossRef] [PubMed]
9. G. MacBeath and S. L. Schreiber, “Printing proteins as microarrays for high-throughput function determination,” Science289(5485), 1760–1763 (2000). [PubMed]
10. H. Jin and R. C. Zangar, “Protein modifications as potential biomarkers in breast cancer,” Biomark. Insights4, 191–200 (2009). [PubMed]
11. Y. Arima, Y. Teramura, H. Takiguchi, K. Kawano, H. Kotera, and H. Iwata, “Surface plasmon resonance and surface plasmon field-enhanced fluorescence spectroscopy for sensitive detection of tumor markers,” Methods Mol. Biol.503, 3–20 (2009). [CrossRef] [PubMed]
12. T. Shtoyko, E. G. Matveeva, I.-F. Chang, Z. Gryczynski, E. Goldys, and I. Gryczynski, “Enhanced fluorescent immunoassays on silver fractal-like structures,” Anal. Chem.80(6), 1962–1966 (2008). [CrossRef] [PubMed]
13. C. D. Geddes, A. Parfenov, D. Roll, M. J. Uddin, and J. R. Lakowicz, “Fluorescence Spectral Properties of Indocyanine Green on a Roughened Platinum Electrode: Metal-Enhanced Fluorescence,” J. Fluoresc.13(6), 453–457 (2003). [CrossRef] [PubMed]
14. Y. Fu and J. R. Lakowicz, “Enhanced fluorescence of Cy5-labeled DNA tethered to silver island films: fluorescence images and time-resolved studies using single-molecule spectroscopy,” Anal. Chem.78(17), 6238–6245 (2006). [CrossRef] [PubMed]
15. J. R. Lakowicz, “Radiative decay engineering 5: metal-enhanced fluorescence and plasmon emission,” Anal. Biochem.337(2), 171–194 (2005). [CrossRef] [PubMed]
16. K. Sokolov, G. Chumanov, and T. M. Cotton, “Enhancement of molecular fluorescence near the surface of colloidal metal films,” Anal. Chem.70(18), 3898–3905 (1998). [CrossRef] [PubMed]
17. J. Kümmerlen, A. Leitner, H. Brunner, F. R. Aussenegg, and A. Wokaun, “Enhanced dye fluorescence over silver island films: analysis of the distance dependence,” Mol. Phys.80(5), 1031–1046 (1993). [CrossRef]
18. A. Pokhriyal, M. Lu, V. Chaudhery, C.-S. Huang, S. Schulz, and B. T. Cunningham, “Photonic crystal enhanced fluorescence using a quartz substrate to reduce limits of detection,” Opt. Express18(24), 24793–24808 (2010). [CrossRef] [PubMed]
19. H. Y. Wu, W. Zhang, P. C. Mathias, and B. T. Cunningham, “Magnification of photonic crystal fluorescence enhancement via TM resonance excitation and TE resonance extraction on a dielectric nanorod surface,” Nanotechnology21(12), 125–203 (2010). [CrossRef] [PubMed]
20. N. Ganesh, W. Zhang, P. C. Mathias, E. Chow, J. A. N. T. Soares, V. Malyarchuk, A. D. Smith, and B. T. Cunningham, “Enhanced fluorescence emission from quantum dots on a photonic crystal surface,” Nat. Nanotechnol.2(8), 515–520 (2007). [CrossRef] [PubMed]
21. N. Ganesh, P. C. Mathias, W. Zhang, and B. T. Cunningham, “Distance dependence of fluorescence enhancement from photonic crystal surfaces,” J. Appl. Phys.103(8), 083104 (2008). [CrossRef]
22. I. D. Block, L. L. Chan, and B. T. Cunningham, “Photonic crystal optical biosensor incorporating structured low-index porous dielectric,” Sens. Actuators B Chem.120(1), 187–193 (2006). [CrossRef]
23. N. Ganesh and B. T. Cunningham, “Photonic-crystal near-ultraviolet reflectance filters fabricated by nanoreplica molding,” Appl. Phys. Lett.88(7), 071110–071113 (2006). [CrossRef]
24. I. D. Block, L. L. Chan, and B. T. Cunningham, “Large-Area submicron replica molding of porous low-k dielectric films and application to photonic crystal biosensor fabrication,” Microelectron. Eng.84(4), 603–608 (2007). [CrossRef]
25. S. Y. Chou, P. R. Krauss, and P. J. Renstrom, “Imprint of sub-25 nm vias and trenches in polymers,” Appl. Phys. Lett.67(21), 3114–3116 (1995). [CrossRef]
26. S. Y. Chou, P. R. Krauss, and P. J. Renstrom, “Imprint Lithography with 25-Nanometer Resolution,” Science272(5258), 85–87 (1996). [CrossRef]
27. P. C. Mathias, H.-Y. Wu, and B. T. Cunningham, “Employing two distinct photonic crystal resonances to improve fluorescence enhancement,” Appl. Phys. Lett.95(2), 021111 (2009). [CrossRef] [PubMed]
28. I. D. Block, P. C. Mathias, N. Ganesh, S. I. Jones, B. R. Dorvel, V. Chaudhery, L. O. Vodkin, R. Bashir, and B. T. Cunningham, “A detection instrument for enhanced-fluorescence and label-free imaging on photonic crystal surfaces,” Opt. Express17(15), 13222–13235 (2009). [CrossRef] [PubMed]
29. V. Chaudhery, M. Lu, C. S. Huang, S. George, and B. T. Cunningham, “Photobleaching on photonic crystal enhanced fluorescence surfaces,” J. Fluoresc.21(2), 707–714 (2011). [CrossRef] [PubMed]
30. P. C. Mathias, S. I. Jones, H. Y. Wu, F. Yang, N. Ganesh, D. O. Gonzalez, G. Bollero, L. O. Vodkin, and B. T. Cunningham, “Improved sensitivity of DNA microarrays using photonic crystal enhanced fluorescence,” Anal. Chem.82(16), 6854–6861 (2010). [CrossRef] [PubMed]
31. P. C. Mathias, N. Ganesh, and B. T. Cunningham, “Application of photonic crystal enhanced fluorescence to a cytokine immunoassay,” Anal. Chem.80(23), 9013–9020 (2008). [CrossRef] [PubMed]
32. C.-S. Huang, S. George, M. Lu, V. Chaudhery, R. Tan, R. C. Zangar, and B. T. Cunningham, “Application of photonic crystal enhanced fluorescence to cancer biomarker microarrays,” Anal. Chem.83(4), 1425–1430 (2011). [CrossRef] [PubMed]
33. B. T. Cunningham, B. Lin, J. Qiu, P. Li, J. Pepper, and B. Hugh, “A plastic colorimetric resonant optical biosensor for multiparallel detection of label-free biochemical interactions,” Sens. Actuators B Chem.85(3), 219–226 (2002). [CrossRef]
34. B. T. Cunningham, P. Li, S. Schulz, B. Lin, C. Baird, J. Gerstenmaier, C. Genick, F. Wang, E. Fine, and L. Laing, “Label-free assays on the BIND system,” J. Biomol. Screen.9(6), 481–490 (2004). [CrossRef] [PubMed]
35. W. A. Challener, J. D. Edwards, R. W. McGowan, J. Skorjanec, and Z. Yang, “A multilayer grating-based evanescent wave sensing technique,” Sens. Actuators B Chem.71(1-2), 42–46 (2000). [CrossRef]
36. S. George, I. D. Block, S. I. Jones, P. C. Mathias, V. Chaudhery, P. Vuttipittayamongkol, H. Y. Wu, L. O. Vodkin, and B. T. Cunningham, “Label-free prehybridization DNA microarray imaging using photonic crystals for quantitative spot quality analysis,” Anal. Chem.82(20), 8551–8557 (2010). [CrossRef] [PubMed]
37. V. Chaudhery, M. Lu, A. Pokhriyal, S. C. Schulz, and B. T. Cunningham, “Angle-scanning photonic crystal enhanced fluorescence microscopy,” IEEE Sens. J. (Accepted).
38. R. Zangar, R. Woodbury, and S. Varnum, “Development of a user-friendly microarray ELISA for the analysis of potential protein markers of breast cancer,” FASEB J.17, A986–A986 (2003).
39. R. L. Woodbury, S. M. Varnum, and R. C. Zangar, “Elevated HGF levels in sera from breast cancer patients detected using a protein microarray ELISA,” J. Proteome Res.1(3), 233–237 (2002). [CrossRef] [PubMed]
40. S. L. Seurynck-Servoss, C. L. Baird, K. D. Rodland, and R. C. Zangar, “Surface chemistries for antibody microarrays,” Front. Biosci.12(8-12), 3956–3964 (2007). [CrossRef] [PubMed]
41. R. M. Gonzalez, S. L. Seurynck-Servoss, S. A. Crowley, M. Brown, G. S. Omenn, D. F. Hayes, and R. C. Zangar, “Development and validation of sandwich ELISA microarrays with minimal assay interference,” J. Proteome Res.7(6), 2406–2414 (2008). [CrossRef] [PubMed]
42. R. C. Zangar, D. S. Daly, A. M. White, S. L. Servoss, R. M. Tan, and J. R. Collett, “ProMAT calibrator: A tool for reducing experimental bias in antibody microarrays,” J. Proteome Res.8(8), 3937–3943 (2009). [CrossRef] [PubMed]
43. S. M. Varnum, R. L. Woodbury, and R. C. Zangar, “A protein microarray ELISA for screening biological fluids,” Methods Mol. Biol.264, 161–172 (2004). [PubMed]
44. S. L. Servoss, R. Gonzalez, S. Varnum, and R. C. Zangar, “High-throughput analysis of serum antigens using sandwich ELISAs on microarrays,” Methods Mol. Biol.520, 143–150 (2009). [CrossRef] [PubMed]

Anal. Biochem.

• J. R. Lakowicz, “Radiative decay engineering 5: metal-enhanced fluorescence and plasmon emission,” Anal. Biochem.337(2), 171–194 (2005). [CrossRef] [PubMed]

Anal. Chem.

• K. Sokolov, G. Chumanov, and T. M. Cotton, “Enhancement of molecular fluorescence near the surface of colloidal metal films,” Anal. Chem.70(18), 3898–3905 (1998). [CrossRef] [PubMed]
• T. Shtoyko, E. G. Matveeva, I.-F. Chang, Z. Gryczynski, E. Goldys, and I. Gryczynski, “Enhanced fluorescent immunoassays on silver fractal-like structures,” Anal. Chem.80(6), 1962–1966 (2008). [CrossRef] [PubMed]
• Y. Fu and J. R. Lakowicz, “Enhanced fluorescence of Cy5-labeled DNA tethered to silver island films: fluorescence images and time-resolved studies using single-molecule spectroscopy,” Anal. Chem.78(17), 6238–6245 (2006). [CrossRef] [PubMed]
• Y. Fu and J. R. Lakowicz, “Enhanced fluorescence of Cy5-labeled DNA tethered to silver island films: fluorescence images and time-resolved studies using single-molecule spectroscopy,” Anal. Chem.78(17), 6238–6245 (2006). [CrossRef] [PubMed]
• P. C. Mathias, S. I. Jones, H. Y. Wu, F. Yang, N. Ganesh, D. O. Gonzalez, G. Bollero, L. O. Vodkin, and B. T. Cunningham, “Improved sensitivity of DNA microarrays using photonic crystal enhanced fluorescence,” Anal. Chem.82(16), 6854–6861 (2010). [CrossRef] [PubMed]
• P. C. Mathias, N. Ganesh, and B. T. Cunningham, “Application of photonic crystal enhanced fluorescence to a cytokine immunoassay,” Anal. Chem.80(23), 9013–9020 (2008). [CrossRef] [PubMed]
• C.-S. Huang, S. George, M. Lu, V. Chaudhery, R. Tan, R. C. Zangar, and B. T. Cunningham, “Application of photonic crystal enhanced fluorescence to cancer biomarker microarrays,” Anal. Chem.83(4), 1425–1430 (2011). [CrossRef] [PubMed]
• S. George, I. D. Block, S. I. Jones, P. C. Mathias, V. Chaudhery, P. Vuttipittayamongkol, H. Y. Wu, L. O. Vodkin, and B. T. Cunningham, “Label-free prehybridization DNA microarray imaging using photonic crystals for quantitative spot quality analysis,” Anal. Chem.82(20), 8551–8557 (2010). [CrossRef] [PubMed]

Appl. Phys. Lett.

• P. C. Mathias, H.-Y. Wu, and B. T. Cunningham, “Employing two distinct photonic crystal resonances to improve fluorescence enhancement,” Appl. Phys. Lett.95(2), 021111 (2009). [CrossRef] [PubMed]
• N. Ganesh and B. T. Cunningham, “Photonic-crystal near-ultraviolet reflectance filters fabricated by nanoreplica molding,” Appl. Phys. Lett.88(7), 071110–071113 (2006). [CrossRef]
• S. Y. Chou, P. R. Krauss, and P. J. Renstrom, “Imprint of sub-25 nm vias and trenches in polymers,” Appl. Phys. Lett.67(21), 3114–3116 (1995). [CrossRef]

Biomark. Insights

• H. Jin and R. C. Zangar, “Protein modifications as potential biomarkers in breast cancer,” Biomark. Insights4, 191–200 (2009). [PubMed]

Drug Metab. Rev.

• R. C. Zangar, S. M. Varnum, and N. Bollinger, “Studying cellular processes and detecting disease with protein microarrays,” Drug Metab. Rev.37(3), 473–487 (2005). [CrossRef] [PubMed]

Expert Rev. Proteomics

• R. C. Zangar, D. S. Daly, and A. M. White, “ELISA microarray technology as a high-throughput system for cancer biomarker validation,” Expert Rev. Proteomics3(1), 37–44 (2006). [CrossRef] [PubMed]

FASEB J.

• R. Zangar, R. Woodbury, and S. Varnum, “Development of a user-friendly microarray ELISA for the analysis of potential protein markers of breast cancer,” FASEB J.17, A986–A986 (2003).

Front. Biosci.

• S. L. Seurynck-Servoss, C. L. Baird, K. D. Rodland, and R. C. Zangar, “Surface chemistries for antibody microarrays,” Front. Biosci.12(8-12), 3956–3964 (2007). [CrossRef] [PubMed]

IEEE Sens. J.

• V. Chaudhery, M. Lu, A. Pokhriyal, S. C. Schulz, and B. T. Cunningham, “Angle-scanning photonic crystal enhanced fluorescence microscopy,” IEEE Sens. J. (Accepted).

J. Appl. Phys.

• N. Ganesh, P. C. Mathias, W. Zhang, and B. T. Cunningham, “Distance dependence of fluorescence enhancement from photonic crystal surfaces,” J. Appl. Phys.103(8), 083104 (2008). [CrossRef]

J. Biomol. Screen.

• B. T. Cunningham, P. Li, S. Schulz, B. Lin, C. Baird, J. Gerstenmaier, C. Genick, F. Wang, E. Fine, and L. Laing, “Label-free assays on the BIND system,” J. Biomol. Screen.9(6), 481–490 (2004). [CrossRef] [PubMed]

J. Fluoresc.

• V. Chaudhery, M. Lu, C. S. Huang, S. George, and B. T. Cunningham, “Photobleaching on photonic crystal enhanced fluorescence surfaces,” J. Fluoresc.21(2), 707–714 (2011). [CrossRef] [PubMed]
• C. D. Geddes, A. Parfenov, D. Roll, M. J. Uddin, and J. R. Lakowicz, “Fluorescence Spectral Properties of Indocyanine Green on a Roughened Platinum Electrode: Metal-Enhanced Fluorescence,” J. Fluoresc.13(6), 453–457 (2003). [CrossRef] [PubMed]

J. Proteome Res.

• R. M. Gonzalez, S. L. Seurynck-Servoss, S. A. Crowley, M. Brown, G. S. Omenn, D. F. Hayes, and R. C. Zangar, “Development and validation of sandwich ELISA microarrays with minimal assay interference,” J. Proteome Res.7(6), 2406–2414 (2008). [CrossRef] [PubMed]
• R. C. Zangar, D. S. Daly, A. M. White, S. L. Servoss, R. M. Tan, and J. R. Collett, “ProMAT calibrator: A tool for reducing experimental bias in antibody microarrays,” J. Proteome Res.8(8), 3937–3943 (2009). [CrossRef] [PubMed]
• R. L. Woodbury, S. M. Varnum, and R. C. Zangar, “Elevated HGF levels in sera from breast cancer patients detected using a protein microarray ELISA,” J. Proteome Res.1(3), 233–237 (2002). [CrossRef] [PubMed]

Methods Mol. Biol.

• S. M. Varnum, R. L. Woodbury, and R. C. Zangar, “A protein microarray ELISA for screening biological fluids,” Methods Mol. Biol.264, 161–172 (2004). [PubMed]
• S. L. Servoss, R. Gonzalez, S. Varnum, and R. C. Zangar, “High-throughput analysis of serum antigens using sandwich ELISAs on microarrays,” Methods Mol. Biol.520, 143–150 (2009). [CrossRef] [PubMed]
• Y. Arima, Y. Teramura, H. Takiguchi, K. Kawano, H. Kotera, and H. Iwata, “Surface plasmon resonance and surface plasmon field-enhanced fluorescence spectroscopy for sensitive detection of tumor markers,” Methods Mol. Biol.503, 3–20 (2009). [CrossRef] [PubMed]

Microelectron. Eng.

• I. D. Block, L. L. Chan, and B. T. Cunningham, “Large-Area submicron replica molding of porous low-k dielectric films and application to photonic crystal biosensor fabrication,” Microelectron. Eng.84(4), 603–608 (2007). [CrossRef]

Mol. Phys.

• J. Kümmerlen, A. Leitner, H. Brunner, F. R. Aussenegg, and A. Wokaun, “Enhanced dye fluorescence over silver island films: analysis of the distance dependence,” Mol. Phys.80(5), 1031–1046 (1993). [CrossRef]

Nanotechnology

• H. Y. Wu, W. Zhang, P. C. Mathias, and B. T. Cunningham, “Magnification of photonic crystal fluorescence enhancement via TM resonance excitation and TE resonance extraction on a dielectric nanorod surface,” Nanotechnology21(12), 125–203 (2010). [CrossRef] [PubMed]

Nat. Methods

• R. A. Irizarry, D. Warren, F. Spencer, I. F. Kim, S. Biswal, B. C. Frank, E. Gabrielson, J. G. Garcia, J. Geoghegan, G. Germino, C. Griffin, S. C. Hilmer, E. Hoffman, A. E. Jedlicka, E. Kawasaki, F. Martínez-Murillo, L. Morsberger, H. Lee, D. Petersen, J. Quackenbush, A. Scott, M. Wilson, Y. Yang, S. Q. Ye, and W. Yu, “Multiple-laboratory comparison of microarray platforms,” Nat. Methods2(5), 345–350 (2005). [CrossRef] [PubMed]

Nat. Nanotechnol.

• N. Ganesh, W. Zhang, P. C. Mathias, E. Chow, J. A. N. T. Soares, V. Malyarchuk, A. D. Smith, and B. T. Cunningham, “Enhanced fluorescence emission from quantum dots on a photonic crystal surface,” Nat. Nanotechnol.2(8), 515–520 (2007). [CrossRef] [PubMed]

Nat. Rev. Drug Discov.

• S. F. Kingsmore, “Multiplexed protein measurement: technologies and applications of protein and antibody arrays,” Nat. Rev. Drug Discov.5(4), 310–321 (2006). [CrossRef] [PubMed]

Nucleic Acids Res.

• C. R. Sabanayagam and J. R. Lakowicz, “Increasing the sensitivity of DNA microarrays by metal-enhanced fluorescence using surface-bound silver nanoparticles,” Nucleic Acids Res.35(2), e13 (2006). [CrossRef] [PubMed]

Opt. Express

• A. Pokhriyal, M. Lu, V. Chaudhery, C.-S. Huang, S. Schulz, and B. T. Cunningham, “Photonic crystal enhanced fluorescence using a quartz substrate to reduce limits of detection,” Opt. Express18(24), 24793–24808 (2010). [CrossRef] [PubMed]
• I. D. Block, P. C. Mathias, N. Ganesh, S. I. Jones, B. R. Dorvel, V. Chaudhery, L. O. Vodkin, R. Bashir, and B. T. Cunningham, “A detection instrument for enhanced-fluorescence and label-free imaging on photonic crystal surfaces,” Opt. Express17(15), 13222–13235 (2009). [CrossRef] [PubMed]

Science

• S. Y. Chou, P. R. Krauss, and P. J. Renstrom, “Imprint Lithography with 25-Nanometer Resolution,” Science272(5258), 85–87 (1996). [CrossRef]
• G. MacBeath and S. L. Schreiber, “Printing proteins as microarrays for high-throughput function determination,” Science289(5485), 1760–1763 (2000). [PubMed]

Sens. Actuators B Chem.

• I. D. Block, L. L. Chan, and B. T. Cunningham, “Photonic crystal optical biosensor incorporating structured low-index porous dielectric,” Sens. Actuators B Chem.120(1), 187–193 (2006). [CrossRef]
• B. T. Cunningham, B. Lin, J. Qiu, P. Li, J. Pepper, and B. Hugh, “A plastic colorimetric resonant optical biosensor for multiparallel detection of label-free biochemical interactions,” Sens. Actuators B Chem.85(3), 219–226 (2002). [CrossRef]
• W. A. Challener, J. D. Edwards, R. W. McGowan, J. Skorjanec, and Z. Yang, “A multilayer grating-based evanescent wave sensing technique,” Sens. Actuators B Chem.71(1-2), 42–46 (2000). [CrossRef]

Other

• M. Schena and R. W. Davis, “Genes, Genomes, and chips,” in DNA Microarrays: A Practical Approach, M. Schena, ed. (Oxford Press, New York, 1999).
• R. Beneke, “Microarray detection with laser scanning device,” in Advanced Methods: DNA Microarrays, U. A. Nuber, ed. (Taylor & Francis Group, New York, 2005).

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