Quantitative and Label-Free Detection of Protein Kinase A Activity Based on Surface-Enhanced Raman Spectroscopy with Gold Nanostars

Analytical Chemistry

Volumn 90, Issue 10, 2018, Pages 6071-6080

  He, Shuai ^a   Kyaw, Yi Mon Ei ^a   Tan, Eddie Khay Ming ^b   Bekale, Laurent ^a   Kang, Malvin Wei Cherng ^a   Kim, Susana Soo Yeon ^c   Tan, Ivan ^c   Lam, Kong Peng ^c   Kah, James Chen Yong ^a,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b TechnoSpex Pte Ltd   (Singapore)

^c AGENCY FOR SCIENCE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; CELL CULTURE; DISEASES; ENDOTHELIAL CELLS; ENZYME ACTIVITY; GOLD; GOLD COMPOUNDS; LIGHT TRANSMISSION; PHOSPHORYLATION; PHOTOBLEACHING; PRINCIPAL COMPONENT ANALYSIS; SUBSTRATES;

BOVINE SERUM ALBUMINS; EXTRACELLULAR PROTEINS; HIGH-AFFINITY PEPTIDES; HUMAN UMBILICAL VEIN ENDOTHELIAL (HUVEC) CELLS; MCF-7 BREAST CANCER CELLS; PRINCIPLE COMPONENT ANALYSIS; QUANTITATIVE MEASUREMENT; SURFACE ENHANCED RAMAN SPECTROSCOPY;

RAMAN SPECTROSCOPY;

BOVINE SERUM ALBUMIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; GOLD; KEMPTIDE; METAL NANOPARTICLE; OLIGOPEPTIDE;

ANIMAL; BOVINE; CHEMISTRY; HUMAN; METABOLISM; PHOSPHORYLATION; RAMAN SPECTROMETRY; SURFACE PROPERTY;

ANIMALS; CATTLE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GOLD; HUMANS; METAL NANOPARTICLES; OLIGOPEPTIDES; PHOSPHORYLATION; SERUM ALBUMIN, BOVINE; SPECTRUM ANALYSIS, RAMAN; SURFACE PROPERTIES;

EID: 85047315510     PISSN: 00032700     EISSN: 15206882     Source Type: Journal    
DOI: 10.1021/acs.analchem.7b05417     Document Type: Article

References (45)

1. Cohen, P. The role of protein phosphorylation in human health and disease. Eur. J. Biochem. 2001, 268 (19), 5001-5010, 10.1046/j.0014-2956.2001.02473.x
2. Nakanishi, K.; Sakamoto, M.; Yasuda, J.; Takamura, M.; Fujita, N.; Tsuruo, T.; Todo, S.; Hirohashi, S. Cancer Res. 2002, 62 (10), 2971-2975
3. Malik, S. N.; Brattain, M.; Ghosh, P. M.; Troyer, D. A.; Prihoda, T.; Bedolla, R.; Kreisberg, J. I. Clin. Cancer Res. 2002, 8 (4), 1168-1171
4. Kreisberg, J. I.; Malik, S. N.; Prihoda, T. J.; Bedolla, R. G.; Troyer, D. A.; Kreisberg, S.; Ghosh, P. M. Phosphorylation of Akt (Ser473) is an excellent predictor of poor clinical outcome in prostate cancer. Cancer Res. 2004, 64 (15), 5232-5236, 10.1158/0008-5472.CAN-04-0272
5. Caretta, A.; Mucignat-Caretta, C. Protein kinase A in cancer. Cancers 2011, 3 (1), 913-926, 10.3390/cancers3010913
6. Sapio, L.; Di Maiolo, F.; Illiano, M.; Esposito, A.; Chiosi, E.; Spina, A.; Naviglio, S. EXCLI J. 2014, 13, 843
7. Cvijic, M. E.; Kita, T.; Shih, W.; DiPaola, R. S.; Chin, K.-V. Clin. Cancer Res. 2000, 6 (6), 2309-2317
8. Kita, T.; Goydos, J.; Reitman, E.; Ravatn, R.; Lin, Y.; Shih, W.-C.; Kikuchi, Y.; Chin, K.-V. Extracellular cAMP-dependent protein kinase (ECPKA) in melanoma. Cancer Lett. 2004, 208 (2), 187-191, 10.1016/j.canlet.2004.02.018
9. Cho, Y. S.; Park, Y. G.; Lee, Y. N.; Kim, M.-K.; Bates, S.; Tan, L.; Cho-Chung, Y. S. Extracellular protein kinase A as a cancer biomarker: its expression by tumor cells and reversal by a myristate-lacking Cα and RIIβ subunit overexpression. Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (2), 835-840, 10.1073/pnas.97.2.835
10. Johnson, S. A.; Hunter, T. Kinomics: methods for deciphering the kinome. Nat. Methods 2005, 2 (1), 17, 10.1038/nmeth731
11. Hutti, J. E.; Jarrell, E. T.; Chang, J. D.; Abbott, D. W.; Storz, P.; Toker, A.; Cantley, L. C.; Turk, B. E. A rapid method for determining protein kinase phosphorylation specificity. Nat. Methods 2004, 1 (1), 27, 10.1038/nmeth708
12. Placzek, E. A.; Plebanek, M. P.; Lipchik, A. M.; Kidd, S. R.; Parker, L. L. A peptide biosensor for detecting intracellular Abl kinase activity using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal. Biochem. 2010, 397 (1), 73-78, 10.1016/j.ab.2009.09.048
13. Wang, Z.; Lévy, R.; Fernig, D. G.; Brust, M. Kinase-catalyzed modification of gold nanoparticles: a new approach to colorimetric kinase activity screening. J. Am. Chem. Soc. 2006, 128 (7), 2214-2215, 10.1021/ja058135y
14. Oishi, J.; Asami, Y.; Mori, T.; Kang, J. H.; Tanabe, M.; Niidome, T.; Katayama, Y. Measurement of homogeneous kinase activity for cell lysates based on the aggregation of gold nanoparticles. ChemBioChem 2007, 8 (8), 875-879, 10.1002/cbic.200700086
15. Gupta, S.; Andresen, H.; Stevens, M. M. Single-step kinase inhibitor screening using a peptide-modified gold nanoparticle platform. Chem. Commun. 2011, 47 (8), 2249-2251, 10.1039/c0cc04903d
16. Dou, X.; Takama, T.; Yamaguchi, Y.; Yamamoto, H.; Ozaki, Y. Enzyme immunoassay utilizing surface-enhanced Raman scattering of the enzyme reaction product. Anal. Chem. 1997, 69 (8), 1492-1495, 10.1021/ac960995x
17. Moore, B. D.; Stevenson, L.; Watt, A.; Flitsch, S.; Turner, N. J.; Cassidy, C.; Graham, D. Nat. Biotechnol. 2004, 22 (9), 1133, 10.1038/nbt1003
18. Ingram, A.; Byers, L.; Faulds, K.; Moore, B. D.; Graham, D. SERRS-based enzymatic probes for the detection of protease activity. J. Am. Chem. Soc. 2008, 130 (36), 11846-11847, 10.1021/ja803655h
19. Moger, J.; Gribbon, P.; Sewing, A.; Winlove, C. Feasibility study using surface-enhanced Raman spectroscopy for the quantitative detection of tyrosine and serine phosphorylation. Biochim. Biophys. Acta, Gen. Subj. 2007, 1770 (6), 912-918, 10.1016/j.bbagen.2007.01.018
20. Xu, S.; Liu, Y.; Wang, T.; Li, J. Highly sensitive electrogenerated chemiluminescence biosensor in profiling protein kinase activity and inhibition using gold nanoparticle as signal transduction probes. Anal. Chem. 2010, 82 (22), 9566-9572, 10.1021/ac102296g
21. Araujo, N. A.; Guevara, A.; Lorenzo, M. A.; Calabokis, M.; Bubis, J. Fluram-Kemptide-Lys8 Non-radioactive Assay for Protein Kinase A. Protein J. 2016, 35 (4), 247-255, 10.1007/s10930-016-9667-9
22. He, S.; Chua, J.; Tan, E. K. M.; Kah, J. C. Y. Optimizing the SERS enhancement of a facile gold nanostar immobilized paper-based SERS substrate. RSC Adv. 2017, 7 (27), 16264-16272, 10.1039/C6RA28450G
23. He, S.; Kang, M. W. C.; Khan, F. J.; Tan, E. K. M.; Reyes, M. A.; Kah, J. C. Y. Optimizing gold nanostars as a colloid-based surface-enhanced Raman scattering (SERS) substrate. J. Opt. 2015, 17 (11), 114013, 10.1088/2040-8978/17/11/114013
24. Nalbant Esenturk, E.; Hight Walker, A. Surface-enhanced Raman scattering spectroscopy via gold nanostars. J. Raman Spectrosc. 2009, 40 (1), 86-91, 10.1002/jrs.2084
25. Hutter, E.; Maysinger, D. Gold-nanoparticle-based biosensors for detection of enzyme activity. Trends Pharmacol. Sci. 2013, 34 (9), 497-507, 10.1016/j.tips.2013.07.002
26. Derman, S.; Akdeste, Z. M. Biyokim. Derg. 2015, 40 (4), 282-289, 10.1515/tjb-2015-0014
27. Simonian, M. H.; Smith, J. A. Spectrophotometric and colorimetric determination of protein concentration. Curr. Protoc. Mol. Biol. 2006, 10.1A, 10.1002/0471142727.mb1001as76
28. Rombouts, I.; Lagrain, B.; Scherf, K. A.; Lambrecht, M. A.; Koehler, P.; Delcour, J. A. Sci. Rep. 2015, 5, 12210, 10.1038/srep12210
29. Sayyed, D. R.; Jung, S.-H.; Kim, M.-S.; Han, E.-T.; Park, W. S.; Hong, S.-H.; Kim, Y.-M.; Ha, K.-S. In situ PKA activity assay by selective detection of its catalytic subunit using antibody arrays. BioChip J. 2017, 11 (1), 57-66, 10.1007/s13206-016-1108-5
30. Li, J.; Cai, R.; Kawazoe, N.; Chen, G. Facile preparation of albumin-stabilized gold nanostars for the targeted photothermal ablation of cancer cells. J. Mater. Chem. B 2015, 3 (28), 5806-5814, 10.1039/C5TB00633C
31. Peters, T. Serum albumin. Adv. Protein Chem. 1985, 37, 161-245, 10.1016/S0065-3233(08)60065-0
32. Cruz-Oliveira, C.; Freire, J. M.; Conceição, T. M.; Higa, L. M.; Castanho, M. A.; Da Poian, A. T. Receptors and routes of dengue virus entry into the host cells. FEMS microbiology reviews 2015, 39 (2), 155-170, 10.1093/femsre/fuu004
33. Peters, T., Jr. All About Albumin: Biochemistry, Genetics, and Medical Applications; Academic Press: San Diego, CA, 1995.
34. Mena-Ulecia, K.; Vergara-Jaque, A.; Poblete, H.; Tiznado, W.; Caballero, J. Study of the affinity between the protein kinase PKA and peptide substrates derived from kemptide using molecular dynamics simulations and MM/GBSA. PLoS One 2014, 9 (10), e109639, 10.1371/journal.pone.0109639
35. Yu, L.; Xu, L.; Xu, M.; Wan, B.; Yu, L.; Huang, Q. Role of Mg2+ ions in protein kinase phosphorylation: insights from molecular dynamics simulations of ATP-kinase complexes. Mol. Simul. 2011, 37 (14), 1143-1150, 10.1080/08927022.2011.561430
36. Thongboonkerd, V., Ed. Proteomics of Human Body Fluids: Principles, Methods, and Applications; Humana Press: Totowa, NJ, 2008.
37. Jo, B. H. Application of Laser Raman Spectroscopy in Conformational Analysis of Proteins. Ph.D. Thesis, Georgia Institute of Technology, 1975.
38. Movasaghi, Z.; Rehman, S.; Rehman, I. U. Raman spectroscopy of biological tissues. Appl. Spectrosc. Rev. 2007, 42 (5), 493-541, 10.1080/05704920701551530
39. Han, W.; Zhu, J.; Wang, S.; Xu, D. Understanding the Phosphorylation Mechanism by Using Quantum Chemical Calculations and Molecular Dynamics Simulations. J. Phys. Chem. B 2017, 121 (15), 3565-3573, 10.1021/acs.jpcb.6b09421
40. Zhang, G.-Y.; Cai, C.; Cosnier, S.; Zeng, H.-B.; Zhang, X.-J.; Shan, D. Zirconium-metalloporphyrin frameworks as a three-in-one platform possessing oxygen nanocage, electron media, and bonding site for electrochemiluminescence protein kinase activity assay. Nanoscale 2016, 8 (22), 11649-11657, 10.1039/C6NR01206J
41. Zhao, Z.; Zhou, X.; Xing, D. Highly sensitive protein kinase activity assay based on electrochemiluminescence nanoprobes. Biosens. Bioelectron. 2012, 31 (1), 299-304, 10.1016/j.bios.2011.10.035
42. Huefner, A.; Kuan, W.-L.; Barker, R. A.; Mahajan, S. Intracellular SERS nanoprobes for distinction of different neuronal cell types. Nano Lett. 2013, 13 (6), 2463-2470, 10.1021/nl400448n
43. Jiang, J.; Auchinvole, C.; Fisher, K.; Campbell, C. J. Quantitative measurement of redox potential in hypoxic cells using SERS nanosensors. Nanoscale 2014, 6 (20), 12104-12110, 10.1039/C4NR01263A
44. Huefner, A.; Kuan, W.-L.; Müller, K. H.; Skepper, J. N.; Barker, R. A.; Mahajan, S. Characterization and visualization of vesicles in the endo-lysosomal pathway with surface-enhanced Raman spectroscopy and chemometrics. ACS Nano 2016, 10 (1), 307-316, 10.1021/acsnano.5b04456
45. Wang, W.; Zhang, L.; Li, L.; Tian, Y. A single nanoprobe for ratiometric imaging and biosensing of hypochlorite and glutathione in live cells using surface-enhanced raman scattering. Anal. Chem. 2016, 88 (19), 9518-9523, 10.1021/acs.analchem.6b02081