Phosphorylation of cystic fibrosis transmembrane conductance regulator (CFTR) serine-511 by the combined action of tyrosine kinases and CK2: The implication of tyrosine-512 and phenylalanine-508

Amino Acids

Volumn 45, Issue 6, 2013, Pages 1423-1429

  Cesaro, Luca ^a   Marin, Oriano ^a   Venerando, Andrea ^a   Donella Deana, Arianna ^a   Pinna, Lorenzo A ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

CFTR; CK2; Hierarchical phosphorylation; Lyn; NBD1; Ser511

Indexed keywords

ALANINE; CASEIN KINASE II; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; PHENYLALANINE; PHOSPHOTYROSINE; PROTEIN KINASE LYN; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; SERINE; TYROSINE; CFTR PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; CHEMISTRY; HUMAN; METABOLISM; PHOSPHORYLATION;

CASEIN KINASE II; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; HUMANS; PHENYLALANINE; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; SERINE; TYROSINE;

EID: 84890566950     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-013-1613-y     Document Type: Article

References (32)

1. Atwell S, Brouillette CG, Conners K, Emtage S, Gheyi T, Guggino WB, Hendle J, Hunt JF, Lewis HA, Lu F, Protasevich II, Rodgers LA, Romero R, Wasserman SR, Weber PC, Wetmore D, Zhang FF, Zhao X (2010) Structures of a minimal human CFTR first nucleotide-binding domain as a monomer, head-to-tail homodimer, and pathogenic mutant. Protein Eng Des Sel 23:375-384. doi: 10.1093/protein/gzq004
2. Billet A, Luo Y, Balghi H, Hanrahan JW (2013) Role of tyrosine phosphorylation in the muscarinic activation of the Cystic Fibrosis Transmembrane Conductance Regulator (CFTR). J Biol Chem 288:21815-21823. doi: 10.1074/jbc.M113.479360
3. Carpino LA, Henklein P, Foxman BM, Abdelmoty I, Costisella B, Wray V, Domke T, El-Faham A, Mügge (2001) The solid state and solution structure of HAPyU. J Org Chem 66:5245-5247
4. Dalemans W, Barbry P, Champigny G, Jallat S, Dott K, Dreyer D, Crystal RG, Pavirani A, Lecocq JP, Lazdunski M (1991) Altered chloride ion channel kinetics associated with the delta F508 cystic fibrosis mutation. Nature 354:526-528. doi: 10.1038/354526a0
5. Fields GB, Noble RL (1990) Solid phase peptide synthesis utilizing 9- fluorenylmethoxycarbonyl amino acids. Int J Pept Protein Res 35:161-214
6. Glass DB, Masaracchia RA, Feramisco JR, Kemp BE (1978) Isolation of phosphorylated peptides and proteins on ion exange papers. Anal Biochem 87:566-575
7. Heda GD, Tanwani M, Marino CR (2001) The Delta F508 mutation shortens the biochemical half-life of plasma membrane CFTR in polarized epithelial cells. Am J Physiol Cell Physiol 280:166-174
8. Hornbeck PV, Kornhauser JM, Tkachev S et al (2011) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40:D261-D270. doi: 10.1093/nar/gkr1122
9. Hunt JF, Wang C, Ford RC (2013) Cystic fibrosis transmembrane conductance regulator (ABCC7) structure. Cold spring Harb Perspect Med 3:a009514. doi: 10.1101/cshperspect.a009514
10. Kato T Jr, Delhase M, Hoffmann A, Karin M (2003) CK2 is a C-terminal IkappaB kinase responsible for NF-kappaB activation during the UV response. Mol Cell 12:829-839. doi: 10.1016/S1097-2765(03)00358-7
11. Lubamba B, Dhooghe B, Noel S, Leal T (2012) Cystic fibrosis: insight into CFTR pathophysiology and pharmacotherapy. Clin Biochem 45:1132-1144. doi: 10.1016/j.clinbiochem.2012.05.034
12. Luz S, Kongsuphol P, Mendes AI, Romeiras F, Sousa M, Schreiber R, Matos P, Jordan P, Mehta A, Amaral MD, Kunzelmann K, Farinha CM (2011) Contribution of casein kinase 2 and spleen tyrosine kinase to CFTR trafficking and protein kinase A-induced activity. Mol Cell Biol 31:4392-4404. doi: 10.1128/MCB.05517-11
13. Määttänen P, Gehring K, Bergeron JJ, Thomas DY (2010) Protein quality control in the ER: the recognition of misfolded proteins. Semin Cell Dev Biol 21:500-511. doi: 10.1016/j.semcdb.2010.03.006
14. Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349-368. doi: 10.1096/fj.02-0473rev
15. Meggio F, Perich JW, Reynolds EC (1991) Pinna LA (1991) Phosphotyrosine as a specificity determinant for casein kinase-2, a growth related Ser/Thr-specific protein kinase. FEBS Lett 279:307-309. doi: 10.1016/0014-5793(91)80174-2
16. Mendes AI, Matos P, Moniz S et al (2011) Antagonistic regulation of cystic fibrosis transmembrane conductance regulator cell surface expression by protein kinases WNK4 and spleen tyrosine kinase. Mol Cell Biol 31:4076-4086. doi: 10.1128/MCB.05152-11
17. Mendoza JL, Schmidt A, Li Q, Nuvaga E, Barrett T, Bridges RJ, Feranchak AP, Brautigam CA, Thomas PJ (2012) Requirements for efficient correction of δF508 CFTR revealed by analyses of evolved sequences. Cell 148:164-174. doi: 10.1016/j.cell.2011.11.023
18. Pagano MA, Arrigoni G, Marin O, Sarno S, Meggio F, Treharne KJ, Mehta A, Pinna LA (2008) Modulation of protein kinase CK2 activity by fragments of CFTR encompassing F508 may reflect functional links with cystic fibrosis pathogenesis. Biochemistry 47:7925-7936. doi: 10.1021/bi800316z
19. Pinna LA, Ruzzene M (1996) How do protein kinases recognize their substrates? Biochim Biophys Acta 1314:191-225
20. Rabeh WM, Bossard F, Xu H, Okiyoneda T, Bagdany M, Mulvihill CM, Du K, di Bernardo S, Liu Y, Konermann L, Roldan A, Lukacs GL (2012) Correction of both NBD1 energetics and domain interface is required to restore ΔF508 CFTR folding and function. Cell 148:150-163. doi: 10.1016/j.cell.2011.11.024
21. Riordan JR (2008) CFTR function and prospects for therapy. Annu Rev Biochem 77:701-726. doi: 10.1146/annurev.biochem.75.103004.142532
22. Roach PJ (1991) Multisite and hierarchal protein phosphorylation. J Biol Chem 266:14139-14142
23. Salvi M, Sarno S, Cesaro L, Nakamura H, Pinna LA (2009) Extraordinary pleiotropy of protein kinase CK2 revealed by weblogo phosphoproteome analysis. Biochim Biophys Acta 1793:847-859. doi: 10.1016/j.bbamcr.2009.01.013
24. Sarno S, Vaglio P, Meggio F, Issinger OG, Pinna LA (1996) Protein kinase CK2 mutants defective in substrate recognition. Purification and kinetic analysis. J Biol Chem 271:10595-10601. doi: 10.1074/jbc.271.18.10595
25. Scaglioni PP, Yung TM, Cai LF, Erdjument-Bromage H, Kaufman AJ, Singh B, Teruya-Feldstein J, Tempst P, Pandolfi PP (2006) A CK2-dependent mechanism for degradation of the PML tumor suppressor. Cell 126:269-283. doi: 10.1016/j.cell.2006.05.041
26. Schagger H (2006) Tricine-SDS-PAGE. Nat Protoc 1:16-22. doi: 10.1038/nprot.2006.4
27. Serohijos AWR, Hegedus T, Riordan JR, Dokholyan NV (2008) Diminished self-chaperoning activity of the ΔF508 mutant of CFTR results in protein misfolding. PLoS Comput Biol 4:e1000008. doi: 10.1371/journal.pcbi.1000008
28. Thibodeau PH, Richardson JM 3rd, Wang W et al (2010) The cystic fibrosis-causing mutation deltaF508 affects multiple steps in cystic fibrosis transmembrane conductance regulator biogenesis. J Biol Chem 285:35825-35835. doi: 10.1074/jbc.M110.131623
29. Torres J, Pulido R (2001) The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implication for PTEN stability to proteasome-mediated degradation. J Biol Chem 276:993-998. doi: 10.1074/jbc.M009134200
30. Ubersax JA, Ferrell EL Jr (2007) Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8:530-541. doi: 10.1038/nrm2203
31. Venerando A, Franchin C, Cant N et al (2013) Detection of phospho-sites generated by protein kinase CK2 in CFTR: mechanistic aspects of Thr1471 phosphorylation. PLoS ONE 8:e74232. doi: 10.1371/journal.pone.0074232
32. Wang Y, Du D, Fang L, Yang G, Zhang C, Zeng R, Ullrich A, Lottspeich F, Chen Z (2006) Tyrosine phosphorylated Par3 regulates epithelial tight junction assembly promoted by EGFR signaling. EMBO J 25:5058-5070. doi: 10.1038/sj.emboj.7601384