Unraveling a phosphorylation event in a folded protein by NMR spectroscopy: Phosphorylation of the Pin1 WW domain by PKA

Journal of Biomolecular NMR

Volumn 55, Issue 4, 2013, Pages 323-337

  Smet Nocca, Caroline ^a   Launay, Hélène ^a   Wieruszeski, Jean Michel ^a   Lippens, Guy ^a   Landrieu, Isabelle ^a  

^a UNIV LILLE   (France)

Author keywords

NMR spectroscopy; Phosphorylation; Pin1 WW binding module; Post translational modifications; Protein

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PEPTIDYLPROLYL ISOMERASE PIN1;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DYNAMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTON NUCLEAR MAGNETIC RESONANCE; STOICHIOMETRY;

BINDING SITES; CYCLIC AMP-DEPENDENT PROTEIN KINASES; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDYLPROLYL ISOMERASE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN FOLDING;

EID: 84877875858     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-013-9716-z     Document Type: Article

References (51)

1. Ando K, Dourlen P, Sambo AV, Bretteville A, Belarbi K, Vingtdeux V, Eddarkaoui S, Drobecq H, Ghestem A, Begard S, Demey-Thomas E, Melnyk P, Smet C, Lippens G, Maurage CA, Caillet-Boudin ML, Verdier Y, Vinh J, Landrieu I, Galas MC, Blum D, Hamdane M, Sergeant N, Buee L (2012) Tau pathology modulates Pin1 post-translational modifications and may be relevant as biomarker. Neurobiol Aging 34(3):757-769
2. Andrew CD, Warwicker J, Jones GR, Doig AJ (2002) Effect of phosphorylation on alpha-helix stability as a function of position. Biochemistry 41(6):1897-1905 (Pubitemid 34132265)
3. Arosio B, Bulbarelli A, Bastias Candia S, Lonati E, Mastronardi L, Romualdi P, Candeletti S, Gussago C, Galimberti D, Scarpini E, Dell'Osso B, Altamura C, MacCarrone M, Bergamaschini L, D'Addario C, Mari D (2012) Pin1 contribution to Alzheimer's disease: transcriptional and epigenetic mechanisms in patients with late-onset Alzheimer's disease. Neuro Degener Dis 10(1-4):207-211
4. Bai Y, Milne JS, Mayne L, Englander SW (1993) Primary structure effects on peptide group hydrogen exchange. Proteins 17(1):75-86 (Pubitemid 23261059)
5. Baker JM, Hudson RP, Kanelis V, Choy WY, Thibodeau PH, Thomas PJ, Forman-Kay JD (2007) CFTR regulatory region interacts with NBD1 predominantly via multiple transient helices. Nat Struct Mol Biol 14(8):738-745 (Pubitemid 47220063)
6. Balastik M, Lim J, Pastorino L, Lu KP (2007) Pin1 in Alzheimer's disease: multiple substrates, one regulatory mechanism? Biochim Biophys Acta 1772(4):422-429 (Pubitemid 46400391)
7. Baldwin AJ, Kay LE (2009) NMR spectroscopy brings invisible protein states into focus. Nat Chem Biol 5(11):808-814
8. Bayer E, Goettsch S, Mueller JW, Griewel B, Guiberman E, Mayr LM, Bayer P (2003) Structural analysis of the mitotic regulator hPin1 in solution: insights into domain architecture and substrate binding. J Biol Chem 278(28):26183-26193 (Pubitemid 36835387)
9. Bienkiewicz EA, Lumb KJ (1999) Random-coil chemical shifts of phosphorylated amino acids. J Biomol NMR 15(3):203-206 (Pubitemid 30016118)
10. Bulbarelli A, Lonati E, Cazzaniga E, Gregori M, Masserini M (2009) Pin1 affects Tau phosphorylation in response to Abeta oligomers. Mol Cell Neurosci 42(1):75-80
11. Du JT, Li YM, Wei W, Wu GS, Zhao YF, Kanazawa K, Nemoto T, Nakanishi H (2005) Low-barrier hydrogen bond between phosphate and the amide group in phosphopeptide. J Am Chem Soc 127(47):16350-16351 (Pubitemid 41740358)
12. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, Skalicky JJ, Kay LE, Kern D (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438(7064):117-121 (Pubitemid 41599831)
13. Eto M, Kitazawa T, Matsuzawa F, Aikawa S, Kirkbride JA, Isozumi N, Nishimura Y, Brautigan DL, Ohki SY (2007) Phosphorylation-induced conformational switching of CPI-17 produces a potent myosin phosphatase inhibitor. Structure 15(12):1591-1602 (Pubitemid 350213414)
14. Golovanov AP, Blankley RT, Avis JM, Bermel W (2007) Isotopically discriminated NMR spectroscopy: a tool for investigating complex protein interactions in vitro. J Am Chem Soc 129(20):6528-6535 (Pubitemid 46799351)
15. Hamdane M, Smet C, Sambo AV, Leroy A, Wieruszeski JM, Delobel P, Maurage CA, Ghestem A, Wintjens R, Begard S, Sergeant N, Delacourte A, Horvath D, Landrieu I, Lippens G, Buee L (2002) Pin1: a therapeutic target in Alzheimer neurodegeneration. J Mol Neurosci 19(3):275-287 (Pubitemid 36051518)
16. Hwang TL, van Zijl PC, Mori S (1998) Accurate quantitation of water-amide proton exchange rates using the phase-modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme. J Biomol NMR 11(2):221-226 (Pubitemid 128511271)
17. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32(3):1037-1049 (Pubitemid 38854704)
18. Johnson LN, Barford D (1993) The effects of phosphorylation on the structure and function of proteins. Annu Rev Biophys Biomol Struct 22:199-232 (Pubitemid 23180322)
19. Kay LE (2005) NMR studies of protein structure and dynamics. J Magn Reson 173(2):193-207 (Pubitemid 40352443)
20. Landrieu I, Lacosse L, Leroy A, Wieruszeski JM, Trivelli X, Sillen A, Sibille N, Schwalbe H, Saxena K, Langer T, Lippens G (2006) NMR analysis of a Tau phosphorylation pattern. J Am Chem Soc 128(11):3575-3583
21. Landrieu I, Leroy A, Smet-Nocca C, Huvent I, Amniai L, Hamdane M, Sibille N, Buee L, Wieruszeski JM, Lippens G (2010) NMR spectroscopy of the neuronal tau protein: normal function and implication in Alzheimer's disease. Biochem Soc Trans 38(4):1006-1011
22. Liou YC, Sun A, Ryo A, Zhou XZ, Yu ZX, Huang HK, Uchida T, Bronson R, Bing G, Li X, Hunter T, Lu KP (2003) Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 424(6948):556-561 (Pubitemid 36975777)
23. Lippens G, Landrieu I, Hanoulle X (2008) Studying posttranslational modifications by in-cell NMR. Chem Biol 15(4):311-312 (Pubitemid 351508430)
24. Lonati E, Masserini M, Bulbarelli A (2011) Pin1: a new outlook in Alzheimer's disease. Curr Alzheimer Res 8(6):615-622
25. Lu KP, Hanes SD, Hunter T (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380(6574):544-547 (Pubitemid 26111332)
26. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399(6738):784-788 (Pubitemid 29293174)
27. Lu PJ, Zhou XZ, Liou YC, Noel JP, Lu KP (2002) Critical role of WW domain phosphorylation in regulating phosphoserine binding activity and Pin1 function. J Biol Chem 277(4):2381-2384 (Pubitemid 34953258)
28. Ma SL, Pastorino L, Zhou XZ, Lu KP (2012) Prolyl isomerase Pin1 promotes amyloid precursor protein (APP) turnover by inhibiting glycogen synthase kinase-3beta (GSK3beta) activity: novel mechanism for Pin1 to protect against Alzheimer disease. J Biol Chem 287(10):6969-6973
29. Mittermaier A, Kay LE (2006) New tools provide new insights in NMR studies of protein dynamics. Science 312(5771):224-228
30. Ohki S, Eto M, Kariya E, Hayano T, Hayashi Y, Yazawa M, Brautigan D, Kainosho M (2001) Solution NMR structure of the myosin phosphatase inhibitor protein CPI-17 shows phosphorylation-induced conformational changes responsible for activation. J Mol Biol 314(4):839-849 (Pubitemid 34087851)
31. Pastorino L, Sun A, Lu PJ, Zhou XZ, Balastik M, Finn G, Wulf G, Lim J, Li SH, Li X, Xia W, Nicholson LK, Lu KP (2006) The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440(7083):528-534
32. Peng T, Zintsmaster JS, Namanja AT, Peng JW (2007) Sequence-specific dynamics modulate recognition specificity in WW domains. Nat Struct Mol Biol 14(4):325-331 (Pubitemid 46608337)
33. Piotto M, Saudek V, Sklenar V (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2(6):661-665
34. Prabakaran S, Everley RA, Landrieu I, Wieruszeski JM, Lippens G, Steen H, Gunawardena J (2011) Comparative analysis of Erk phosphorylation suggests a mixed strategy for measuring phospho-form distributions. Mol Syst Biol 7:482
35. Pufall MA, Lee GM, Nelson ML, Kang HS, Velyvis A, Kay LE, McIntosh LP, Graves BJ (2005) Variable control of Ets-1 DNA binding by multiple phosphates in an unstructured region. Science 309(5731):142-145 (Pubitemid 40934995)
36. Pullen K, Rajagopal P, Branchini BR, Huffine ME, Reizer J, Saier MH Jr, Scholtz JM, Klevit RE (1995) Phosphorylation of serine-46 in HPr, a key regulatory protein in bacteria, results in stabilization of its solution structure. Protein Sci 4(12):2478-2486
37. Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89(6):875-886 (Pubitemid 27513514)
38. Rangasamy V, Mishra R, Sondarva G, Das S, Lee TH, Bakowska JC, Tzivion G, Malter JS, Rana B, Lu KP, Kanthasamy A, Rana A (2012) Mixed-lineage kinase 3 phosphorylates prolyl-isomerase Pin1 to regulate its nuclear translocation and cellular function. Proc Natl Acad Sci USA 109(21):8149-8154
39. Sharpe T, Jonsson AL, Rutherford TJ, Daggett V, Fersht AR (2007) The role of the turn in beta-hairpin formation during WW domain folding. Protein Sci 16(10):2233-2239 (Pubitemid 47481658)
40. Smet C, Duckert JF, Wieruszeski JM, Landrieu I, Buee L, Lippens G, Deprez B (2005a) Control of protein-protein interactions: structure-based discovery of low molecular weight inhibitors of the interactions between Pin1 WW domain and phosphopeptides. J Med Chem 48(15):4815-4823 (Pubitemid 41033124)
41. Smet C, Sambo AV, Wieruszeski JM, Leroy A, Landrieu I, Buee L, Lippens G (2004) The peptidyl prolyl cis/trans-isomerase Pin1 recognizes the phospho-Thr212-Pro213 site on Tau. Biochemistry 43(7):2032-2040 (Pubitemid 38233265)
42. Smet C, Wieruszeski JM, Buee L, Landrieu I, Lippens G (2005b) Regulation of Pin1 peptidyl-prolyl cis/trans isomerase activity by its WW binding module on a multi-phosphorylated peptide of Tau protein. FEBS Lett 579(19):4159-4164 (Pubitemid 41021806)
43. Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Markesbery WR, Zhou XZ, Lu KP, Butterfield DA (2006) Oxidative modification and down-regulation of Pin1 in Alzheimer's disease hippocampus: a redox proteomics analysis. Neurobiol Aging 27(7):918-925
44. Teriete P, Thai K, Choi J, Marassi FM (2009) Effects of PKA phosphorylation on the conformation of the Na, K-ATPase regulatory protein FXYD1. Biochim Biophys Acta 1788(11):2462-2470
45. Theillet FX, Smet-Nocca C, Liokatis S, Thongwichian R, Kosten J, Yoon MK, Kriwacki RW, Landrieu I, Lippens G, Selenko P (2012) Cell signaling, post-translational protein modifications and NMR spectroscopy. J Biomol NMR 54(3):217-236
46. Verdecia MA, Bowman ME, Lu KP, Hunter T, Noel JP (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Biol 7(8):639-643 (Pubitemid 30636673)
47. Wintjens R, Wieruszeski JM, Drobecq H, Rousselot-Pailley P, Buee L, Lippens G, Landrieu I (2001) 1H NMR study on the binding of Pin1 Trp-Trp domain with phosphothreonine peptides. J Biol Chem 276(27):25150-25156
48. Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley JL, Sykes BD (1995) 1H, 13C and 15 N chemical shift referencing in biomolecular NMR. J Biomol NMR 6(2):135-140
49. Wishart DS, Sykes BD (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J Biomol NMR 4(2):171-180
50. Wittekind M, Reizer J, Deutscher J, Saier MH, Klevit RE (1989) Common structural changes accompany the functional inactivation of HPr by seryl phosphorylation or by serine to aspartate substitution. Biochemistry 28(26):9908-9912 (Pubitemid 20033671)
51. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld JU, Xu J, Kuang J, Kirschner MW, Fischer G, Cantley LC, Lu KP (1997) Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278(5345):1957-1960 (Pubitemid 28013239)