The hinge region operates as a stability switch in cGMP-dependent protein kinase Iα

FEBS Journal

Volumn 274, Issue 9, 2007, Pages 2274-2286

  Scholten, Arjen ^a,b   Fuß, Hendrik ^a,d   Heck, Albert J R ^b   Dostmann, Wolfgang R ^a,c  

^a UNIVERSITY OF VERMONT   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

cGMP; cGMP dependent protein kinase I ; Limited proteolysis; Mass spectrometry; Tryptophan fluorescence

Indexed keywords

ARGININE; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE 1ALPHA; LEUCINE; MUTANT PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ELECTROSPRAY MASS SPECTROMETRY; ENTHALPY; ENZYME STABILITY; FLUORESCENCE ANALYSIS; LIQUID CHROMATOGRAPHY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; THERMODYNAMICS; TIME OF FLIGHT MASS SPECTROMETRY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CATTLE; CELL LINE; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENZYME STABILITY; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; THERMODYNAMICS; TRYPTOPHAN;

BOVINAE;

EID: 34247344842     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05764.x     Document Type: Article

References (43)

1. Lincoln TM, Wu X, Sellak H, Dey N Choi CS (2006) Regulation of vascular smooth muscle cell phenotype by cyclic GMP and cyclic GMP-dependent protein kinase. Front Biosci 11, 356 367.
2. Feil R, Hofmann F Kleppisch T (2005) Function of cGMP-dependent protein kinases in the nervous system. Rev Neurosci 16, 23 41.
3. Hofmann F, Feil R, Kleppisch T Schlossmann J (2006) Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol Rev 86, 1 23.
4. Landgraf W Hofmann F (1989) The amino terminus regulates binding to and activation of cGMP-dependent protein kinase. Eur J Biochem 181, 643 650.
5. Hofmann F, Gensheimer H-P Göbel C (1985) cGMP-dependent protein kinase; Autophosphorylation changes the characteristics of binding site 1. Eur J Biochem 147, 361 365.
6. Landgraf W, Hullin R, Göbel C Hofmann F (1986) Phosphorylation of cGMP-dependent protein kinase increases the affinity for cyclic AMP. Eur J Biochem 154, 113 117.
7. Chu DM, Francis SH, Thomas JW, Maksymovitch EA, Fosler M Corbin JD (1998) Activation by autophosphorylation or cGMP binding produces a similar apparent conformational change in cGMP-dependent protein kinase. J Biol Chem 273, 14649 14656.
8. Hofmann F, Ammendola A Schlossmann J (2000) Rising behind NO: cGMP-dependent protein kinase. J Cell Sci 113, 1671 1676.
9. Vo NK, Gettemy JM Coghlan VM (1998) Identification of cGMP-dependent protein kinase anchoring proteins (GKAPs). Biochem Biophys Res Commun 246, 831 835.
10. Yuasa K, Michibata H, Omori K Yanaka N (1999) A novel interaction of cGMP-dependent protein kinase I with troponin T. J Biol Chem 274, 37429 37434.
11. Busch JL, Bessay EP, Francis SH Corbin JD (2002) A conserved serine juxtaposed to the pseudosubstrate site of type I cGMP-dependent protein kinase contributes strongly to autoinhibition and lower cGMP affinity. J Biol Chem 277, 34048 34054.
12. Francis SH, Smith JA, Colbran JL, Grimes K, Walsh KA, Kumar S Corbin JD (1996) Arginine 75 in the pseudosubstrate sequence of type Ibeta cGMP-dependent protein kinase is critical for autoinhibition, although autophosphorylated serine 63 is outside this sequence. J Biol Chem 271, 20748 20755.
13. Ruth P, Pfeifer A, Kamm S, Klatt P, Dostmann WRG Hofmann F (1997) Identification of the amino acid sequences responsible for high affinity activation of cGMP kinase Ia. J Biol Chem 272, 10522 10528.
14. Reed RB, Sandberg M, Jahnsen T, Lohmann SM, Francis SH Corbin JD (1996) Fast and slow cyclic nucleotide-dissociation sites in cAMP-dependent protein kinase are transposed in type Ibeta cGMP-dependent protein kinase. J Biol Chem 271, 17570 17575.
15. Corbin JD Doskeland SO (1983) Studies of two different intrachain cGMP-binding sites of cGMP-dependent protein kinase. J Biol Chem 258, 11391 11397.
16. Monken CE Gill GN (1980) Structural analysis of cGMP-dependent kinase using limited proteolysis. J Biol Chem 255, 7067 7070.
17. Heil WG, Landgraf W Hofmann F (1987) A catalytically active fragment of cGMP-dependent protein kinase; occupation of its cGMP-binding sites does not effect its phosphotransferase activity. Eur J Biochem 168, 117 121.
18. Dostmann WRG, Koep N Endres R (1996) The catalytic domain of the cGMP-dependent protein kinase Ia modulates the cGMP-characteristics of its regulatory domain. FEBS Lett 398, 206 210.
19. Takio K, Wade RD, Smith SB, Krebs EG, Walsh KA Titani K (1984) Guanosine cyclic-3′,5′-phosphate dependent protein kinase, a chimeric protein homologous with two separate protein families. Biochemistry 23, 4207 4218.
20. Wall ME Francis SH, Corbin JD, Grimes K, Richie-Jannetta R, Kotera J, Macdonald BA, Gibson RR, Trewhella J (2003) Mechanisms associated with cGMP binding and activation of cGMP-dependent protein kinase. Proc Natl Acad Sci USA 100, 2380 2385.
21. Zhao J, Trewhella J, Corbin J, Francis S, Mitchell R, Brushia R Walsh D (1997) Progressive cyclic nucleotide-induced conformational changes in the cGMP-dependent protein kinase studied by small angle X-ray scattering in solution. J Biol Chem 272, 31929 31936.
22. Chu DM, Corbin JD, Grimes KA Francis SH (1997) Activation by cyclic GMP binding causes an apparent conformational change in cGMP-dependent protein kinase. J Biol Chem 272, 31922 31928.
23. Kim C, Xuong NH Taylor SS (2005) Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA. Science 307, 690 696.
24. Atkinson RA, Saudek V, Huggins JP Pelton JT (1991) 1H NMR and circular dichroism studies of the N-terminal domain of cyclic GMP dependent protein kinase: a leucine/isoleucine zipper. Biochemistry 30, 9387 9395.
25. Tandon S Horowitz PM (1990) The detection of kinetic intermediate(s) during refolding of rhodanese. J Biol Chem 265, 5967 5970.
26. Leon DA, Dostmann WR Taylor SS (1991) Unfolding of the regulatory subunit of cAMP-dependent protein kinase I. Biochemistry 30, 3035 3040.
27. Leon DA, Canaves JM Taylor SS (2000) Probing the multidomain structure of the type I regulatory subunit of cAMP-dependent protein kinase using mutational analysis: role and environment of endogenous tryptophans. Biochemistry 39, 5662 5671.
28. Feil R, Müller S Hofmann F (1993) High-level expression of functional cGMP-dependent protein kinase using the baculovirus system. FEBS Lett 336, 163 167.
29. Pöhler D, Butt E, Meißner J, Müller S, Lohse M, Walter U, Lohmann SM Jarchau T (1995) Expression, purification and characterization of the cGMP-dependent protein kinase Iβ and II using the baculovirus system. FEBS Lett 374, 419 425.
30. Dostmann WRG, Nickl CK, Thiel S, Tsigelny I, Frank R Tegge WJ (1999) Delineation of selective cyclic GMP-dependent protein kinase Ia substrate and inhibitor peptides based on combinatorial peptide libraries on paper. Pharmacol Ther 82, 373 387.
31. Pinkse MW, Heck AJ, Rumpel K Pullen F (2004) Probing noncovalent protein-ligand interactions of the cGMP-dependent protein kinase using electrospray ionization time of flight mass spectrometry. J Am Soc Mass Spectrom 15, 1392 1399.
32. van den Heuvel RH Heck AJ (2004) Native protein mass spectrometry: from intact oligomers to functional machineries. Curr Opin Chem Biol 8, 519 526.
33. Heck AJ Van Den Heuvel RH (2004) Investigation of intact protein complexes by mass spectrometry. Mass Spectrom Rev 23, 368 389.
34. van Duijn E, Bakkes PJ, Heeren RM, van den Heuvel RH, van Heerikhuizen H, van der Vies SM Heck AJ (2005) Monitoring macromolecular complexes involved in the chaperonin-assisted protein folding cycle by mass spectrometry. Nat Methods 2, 371 376.
35. Wu J, Brown S, Xuong NH Taylor SS (2004) RIalpha subunit of PKA: a cAMP-free structure reveals a hydrophobic capping mechanism for docking cAMP into site B. Structure (Camb) 12, 1057 1065.
36. Su Y, Dostmann WR, Herberg FW, Durick K, Xuong NH, Ten Eyck L, Taylor SS Varughese KI (1995) Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains. Science 269, 807 813.
37. Aitken A, Hemmings BA Hofmann F (1984) Identification of the residues on cyclic GMP-dependent protein kinase that are autophophorylated in the presence of cyclic AMP and cyclic GMP. Biochim Biophys Acta 790, 219 225.
38. Pinkse MW, Uitto PM, Hilhorst MJ, Ooms B Heck AJ (2004) Selective isolation at the femtomole level of phosphopeptides from proteolytic digests using 2D-NanoLC-ESI-MS/MS and titanium oxide precolumns. Anal Chem 76, 3935 3943.
39. Yuasa K, Michibata H, Omori K Yanaka M (2000) Identification of a conserved residue responsible for the autoinhibition of cGMP-dependent protein kinase Ia and Iβ. FEBS Lett 466, 175 178.
40. Tegge W, Frank R, Hofmann F Dostmann WR (1995) Determination of cyclic nucleotide-dependent protein kinase substrate specificity by the use of peptide libraries on cellulose paper. Biochemistry 34, 10569 10577.
41. Wernet W, Flockerzi V Hofmann F (1989) The cDNA of the two isoforms of bovine cGMP-dependent protein kinase. FEBS Lett 251, 191 196.
42. Keilbach A, Ruth P Hofmann F (1992) Detection of cGMP-dependent protein kinase isozymes by specific antibodies. FEBS Lett 208, 467 473.
43. Pace C, Shirley B Thomson J (1989) In Protein Function: a Practical Approach (Creighton, T, ed). IRL Press, Oxford.