Peptide microarrays for detailed, high-throughput substrate identification, kinetic characterization, and inhibition studies on protein kinase A

Analytical Biochemistry

Volumn 387, Issue 2, 2009, Pages 150-161

  Hilhorst, Riet ^a   Houkes, Liesbeth ^a   van den Berg, Adriënne ^a   Ruijtenbeek, Rob ^a  

^a PamGene International BV   (Netherlands)

Author keywords

AMP PNP; cAMP dependent protein kinase A; Enzymology; IC50; Kinetics; Mechanism of action; Michaelis constant; Peptide microarray; PKA; PKA inhibitor peptide; Staurosporin; Substrate identification

Indexed keywords

AMINO ACIDS; BIOASSAY; ENZYME INHIBITION; ENZYME KINETICS; KINETICS; PHOSPHORYLATION; SUBSTRATES;

AMP-PNP; ENZYMOLOGY; IC50; MECHANISM OF ACTION; MICHAELIS CONSTANTS; PROTEIN KINASE A; STAUROSPORIN;

PEPTIDES;

ADENOSINE TRIPHOSPHATE; ADENYLYLIMIDODIPHOSPHATE; AURORA A KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE CATALYTIC SUBUNIT; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DESMOPLAKIN; SERINE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; STAUROSPORINE; THREONINE; THREONYLTYROSYLALANYLASPARTYLPHENYLALANYLISOLEUCYLALANYLSERYLGLYCYLARGINYLTHREON YLGLYCYLARGINYLARGINYLASPARAGINYLALANYLISOLEUCINAMIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CORRELATION ANALYSIS; DRUG MECHANISM; ENZYME INHIBITION; ENZYME KINETICS; ENZYME SUBSTRATE; HIGH THROUGHPUT SCREENING; HUMAN; IC 50; MICROARRAY ANALYSIS; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VALIDATION PROCESS;

EID: 61849083039     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2009.01.022     Document Type: Article

References (46)

1. Luo K., Zhou P., and Lodish H.F. The specificity of the transforming growth factor beta receptor kinases determined by a spatially addressable peptide library. Proc. Natl. Acad. Sci. USA 92 (1995) 11761-11765
2. Cretich M., Damin F., Pirri G., and Chiari M. Protein and peptide arrays: recent trends and new directions. Biomol. Eng. 23 (2006) 77-88
3. Schutkowski M., Reineke U., and Reimer U. Peptide arrays for kinase profiling. ChemBioChem 6 (2005) 513-521
4. Knighton D.R., Zheng J.H., ten Eyck L.F., Ashford V.A., Xuong N.H., Taylor S.S., and Sowadski J.M. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253 (1991) 407-414
5. van Beuningen R., van Damme H., Boender P.J., Bastiaensen N., Chan A., and Kievits T. Fast and specific hybridization using flow-through microarrays on porous metal oxide. Clin. Chem. 47 (2001) 1931-1933
6. Wu Y., de Kievit P., Vahlkamp L., Pijnenburg D., Smit M., Dankers M., Melchers D., Stax M., Boender P.J., Ingham C., Bastiaensen N., de Wijn R., van Alewijk D., van Damme H., Raap A.K., Chan A.B., and van Beuningen R. Quantitative assessment of a novel flow-through porous microarray for the rapid analysis of gene expression profiles. Nucleic Acids Res. 32 (2004) e123
7. Zeng F., Ren Z.R., Huang S.Z., Kalf M., Mommersteeg M., Smit M., White S., Jin C.L., Xu M., Zhou D.W., Yan J.B., Chen M.J., van B.R., Huang S.Z., den Dunnen J., Zeng Y.T., and Wu Y. Array-MLPA: comprehensive detection of deletions and duplications and its application to DMD patients. Hum. Mutat. 29 (2008) 190-197
8. Lemeer S., Jopling C., Naji F., Ruijtenbeek R., Slijper M., Heck A.J., and den Hertog J. Protein-tyrosine kinase activity profiling in knock down zebrafish embryos. PLoS ONE 2 (2007) e581
9. Lemeer S., Ruijtenbeek R., Pinkse M.W., Jopling C., Heck A.J., den Hertog J., and Slijper M. Endogenous phosphotyrosine signaling in zebrafish embryos. Mol. Cell. Proteomics 6 (2007) 2088-2099
10. De Keersmaecker K., Versele M., Cools J., Superti-Furga G., and Hantschel O. Intrinsic differences between the catalytic properties of the oncogenic NUP214-ABL1 and BCR-ABL1 fusion protein kinases. Leukemia 22 (2008) 2208-2216
11. Peri S., Navarro J.D., Amanchy R., Kristiansen T.Z., Jonnalagadda C.K., Surendranath V., Niranjan V., Muthusamy B., Gandhi T.K., Gronborg M., Ibarrola N., Deshpande N., Shanker K., Shivashankar H.N., Rashmi B.P., Ramya M.A., Zhao Z., Chandrika K.N., Padma N., Harsha H.C., Yatish A.J., Kavitha M.P., Menezes M., Choudhury D.R., Suresh S., Ghosh N., Saravana R., Chandran S., Krishna S., Joy M., Anand S.K., Madavan V., Joseph A., Wong G.W., Schiemann W.P., Constantinescu S.N., Huang L., Khosravi-Far R., Steen H., Tewari M., Ghaffari S., Blobe G.C., Dang C.V., Garcia J.G., Pevsner J., Jensen O.N., Roepstorff P., Deshpande K.S., Chinnaiyan A.M., Hamosh A., Chakravarti A., and Pandey A. Development of human protein reference database as an initial platform for approaching systems biology in humans. Genome Res. 13 (2003) 2363-2371
12. Mishra G.R., Suresh M., Kumaran K., Kannabiran N., Suresh S., Bala P., Shivakumar K., Anuradha N., Reddy R., Raghavan T.M., Menon S., Hanumanthu G., Gupta M., Upendran S., Gupta S., Mahesh M., Jacob B., Mathew P., Chatterjee P., Arun K.S., Sharma S., Chandrika K.N., Deshpande N., Palvankar K., Raghavnath R., Krishnakanth R., Karathia H., Rekha B., Nayak R., Vishnupriya G., Kumar H.G., Nagini M., Kumar G.S., Jose R., Deepthi P., Mohan S.S., Gandhi T.K., Harsha H.C., Deshpande K.S., Sarker M., Prasad T.S., and Pandey A. Human protein reference database--2006 update. Nucleic Acids Res. 34 (2006) D411-D414
13. Diella F., Cameron S., Gemund C., Linding R., Via A., Kuster B., Sicheritz-Ponten T., Blom N., and Gibson T.J. Phospho ELM: a database of experimentally verified phosphorylation sites in eukaryotic proteins. BMC Bioinformatics 5 (2004) 79
14. UniProt Consortium. The universal protein resource (UniProt). Nucleic Acids Res. 36 (2008) D190-D195
15. Shabb J.B. Physiological substrates of cAMP-dependent protein kinase. Chem. Rev. 101 (2001) 2381-2411
16. Hjerrild M., Stensballe A., Rasmussen T.E., Kofoed C.B., Blom N., Sicheritz-Ponten T., Larsen M.R., Brunak S., Jensen O.N., and Gammeltoft S. Identification of phosphorylation sites in protein kinase A substrates using artificial neural networks and mass spectrometry. J. Proteome Res. 3 (2004) 426-433
17. Blom N., Sicheritz-Ponten T., Gupta R., Gammeltoft S., and Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4 (2004) 1633-1649
18. Charter N.W., Kauffman L., Singh R., and Eglen R.M. A generic, homogenous method for measuring kinase and inhibitor activity via adenosine 5'-diphosphate accumulation. J. Biomol. Screen. 11 (2006) 390-399
19. Cook P.F., Neville Jr. M.E., Vrana K.E., Hartl F.T., and Roskoski Jr. R. Adenosine cyclic 3′,5′-monophosphate dependent protein kinase: kinetic mechanism for the bovine skeletal muscle catalytic subunit. Biochemistry 21 (1982) 5794-5799
20. Whitehouse S., Feramisco J.R., Casnellie J.E., Krebs E.G., and Walsh D.A. Studies on the kinetic mechanism of the catalytic subunit of the cAMP-dependent protein kinase. J. Biol. Chem. 258 (1983) 3693-3701
21. Moore M.J., Adams J.A., and Taylor S.S. Structural basis for peptide binding in protein kinase A: role of glutamic acid 203 and tyrosine 204 in the peptide-positioning loop. J. Biol. Chem. 278 (2003) 10613-10618
22. Grant B.D., Tsigelny I., Adams J.A., and Taylor S.S. Examination of an active-site electrostatic node in the cAMP-dependent protein kinase catalytic subunit. Protein Sci. 5 (1996) 1316-1324
23. Kemp B.E., Graves D.J., Benjamini E., and Krebs E.G. Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinase. J. Biol. Chem. 252 (1977) 4888-4894
24. Kong C.T., and Cook P.F. Isotope partitioning in the adenosine 3',5'-monophosphate dependent protein kinase reaction indicates a steady-state random kinetic mechanism. Biochemistry 27 (1988) 4795-4799
25. Adams J.A., and Taylor S.S. Energetic limits of phosphotransfer in the catalytic subunit of cAMP-dependent protein kinase as measured by viscosity experiments. Biochemistry 31 (1992) 8516-8522
26. Goldstein A. The mechanism of enzyme-inhibitor-substrate reactions: illustrated by the cholinesterase-physostigmine-acetylcholine system. J. Gen. Physiol. 27 (1944) 529-580
27. Henderson P.J.F. A linear equation that describes the steady-state kinetics of enzymes and subcellular particles interacting with tightly bound inhibitors. Biochem. J. 127 (1972) 321-333
28. Qamar R., and Cook P.F. pH dependence of the kinetic mechanism of the adenosine 3',5'-monophosphate dependent protein kinase catalytic subunit in the direction of magnesium adenosine 5'-diphosphate phosphorylation. Biochemistry 32 (1993) 6802-6806
29. Meggio F., Donella D.A., Ruzzene M., Brunati A.M., Cesaro L., Guerra B., Meyer T., Mett H., Fabbro D., and Furet P. Different susceptibility of protein kinases to staurosporine inhibition: kinetic studies and molecular bases for the resistance of protein kinase CK2. Eur. J. Biochem. 234 (1995) 317-322
30. Cheng H.C., Kemp B.E., Pearson R.B., Smith A.J., Misconi L., Van Patten S.M., and Walsh D.A. A potent synthetic peptide inhibitor of the cAMP-dependent protein kinase. J. Biol. Chem. 261 (1986) 989-992
31. Glass D.B., Cheng H.C., Kemp B.E., and Walsh D.A. Differential and common recognition of the catalytic sites of the cGMP-dependent and cAMP-dependent protein kinases by inhibitory peptides derived from the heat-stable inhibitor protein. J. Biol. Chem. 261 (1986) 12166-12171
32. Cheng H.C., Van Patten S.M., Smith A.J., and Walsh D.A. An active twenty-amino-acid-residue peptide derived from the inhibitor protein of the cyclic AMP-dependent protein kinase. Biochem. J. 231 (1985) 655-661
33. Whitehouse S., and Walsh D.A. Mg X ATP2-dependent interaction of the inhibitor protein of the cAMP-dependent protein kinase with the catalytic subunit. J. Biol. Chem. 258 (1983) 3682-3692
34. 50) of an enzymatic reaction. Biochem. Pharmacol. 22 (1973) 3099-3108
35. Knighton D.R., Zheng J.H., ten Eyck L.F., Xuong N.H., Taylor S.S., and Sowadski J.M. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253 (1991) 414-420
36. Madhusudan, Trafny E.A., Xuong N.H., Adams J.A., ten Eyck L.F., Taylor S.S., and Sowadski J.M. cAMP-dependent protein kinase: crystallographic insights into substrate recognition and phosphotransfer. Protein Sci. 3 (1994) 176-187
37. Zheng J., Knighton D.R., ten Eyck L.F., Karlsson R., Xuong N., Taylor S.S., and Sowadski J.M. Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MgATP and peptide inhibitor. Biochemistry 32 (1993) 2154-2161
38. Laane C., Hilhorst R., and Veeger C. Design of reversed micellar media for the enzymatic synthesis of apolar compounds. Methods Enzymol. 136 (1987) 216-229
39. Verhaert R.M., Hilhorst R., Vermue M., Schaafsma T.J., and Veeger C. Description of enzyme kinetics in reversed micelles: I. Theory. Eur. J. Biochem. 187 (1990) 59-72
40. Verhaert R.M., Tyrakowska B., Hilhorst R., Schaafsma T.J., and Veeger C. Enzyme kinetics in reversed micelles: II. Behaviour of enoate reductase. Eur. J. Biochem. 187 (1990) 73-79
41. Tyrakowska B., Verhaert R.M., Hilhorst R., and Veeger C. Enzyme kinetics in reversed micelles: III. Behaviour of 20 beta-hydroxysteroid dehydrogenase. Eur. J. Biochem. 187 (1990) 81-88
42. Han X., Shigaki S., Yamaji T., Yamanouchi G., Mori T., Niidome T., and Katayama Y. A quantitative peptide array for evaluation of protein kinase activity. Anal. Biochem. 372 (2008) 106-115
43. Goldstein L. Microenvironmental effects on enzyme catalysis: a kinetic study of polyanionic and polycationic derivatives of chymotrypsin. Biochemistry 11 (1972) 4072-4084
44. Goldstein L. Kinetic behavior of immobilized enzyme systems. Methods Enzymol. 44 (1976) 397-443
45. Mori T., Inamori K., Inoue Y., Han X., Yamanouchi G., Niidome T., and Katayama Y. Evaluation of protein kinase activities of cell lysates using peptide microarrays based on surface plasmon resonance imaging. Anal. Biochem. 375 (2008) 223-231
46. Diks S.H., Kok K., O'Toole T., Hommes D.W., van Dijken P., Joore J., and Peppelenbosch M.P. Kinome profiling for studying lipopolysaccharide signal transduction in human peripheral blood mononuclear cells. J. Biol. Chem. 279 (2004) 49206-49213