Structural characterization of a neuroblast-specific phosphorylated region of MARCKS

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 4, 2014, Pages 837-849

  Tinoco, Luzineide W ^a   Fraga, Jully L ^a   Anobom, Cristiane D ^a   Zolessi, Flavio R ^b   Obal, Gonzalo ^c   Toledo, Andrea ^b   Pritsch, Otto ^c   Arruti, Cristina ^b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

Author keywords

Antibody binding; Circular Dichroism; MARCKS; Nuclear Magnetic Resonance; Serine phosphorylation; Surface Plasmon Resonance

Indexed keywords

MARCKS PROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 3C3; PROTEIN; S25P PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; CHICK EMBRYO; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HYDROGEN BOND; IONIC STRENGTH; KINETICS; MOUSE; NERVE CELL DIFFERENTIATION; NEUROBLAST; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE; UNFOLDED PROTEIN RESPONSE;

ANTIBODY BINDING; CIRCULAR DICHROISM; MARCKS; NUCLEAR MAGNETIC RESONANCE; SERINE PHOSPHORYLATION; SURFACE PLASMON RESONANCE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN CHEMISTRY; CHICK EMBRYO; CIRCULAR DICHROISM; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN KINASE C; PROTEIN STRUCTURE, SECONDARY; SURFACE PLASMON RESONANCE;

EID: 84896259069     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.02.016     Document Type: Article

References (48)

1. A. Arbuzova, A.A. Schmitz, and G. Vergeres Cross-talk unfolded: MARCKS proteins Biochem. J. 362 2002 1 12 (Pubitemid 34174456)
2. S. McLaughlin, J. Wang, A. Gambhir, and D. Murray PIP(2) and proteins: interactions, organization, and information flow Annu. Rev. Biophys. Biomol. Struct. 31 2002 151 175
3. A. Arbuzova, J. Wang, D. Murray, J. Jacob, D.S. Cafiso, and S. McLaughlin Kinetics of interaction of the myristoylated alanine-rich C kinase substrate, membranes, and calmodulin J. Biol. Chem. 272 1997 27167 27177 (Pubitemid 27452675)
4. S. McLaughlin, and A. Aderem The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions Trends Biochem. Sci. 20 1995 272 276
5. S. Ohmori, N. Sakai, Y. Shirai, H. Yamamoto, E. Miyamoto, N. Shimizu, and N. Saito Importance of protein kinase C targeting for the phosphorylation of its substrate, myristoylated alanine-rich C-kinase substrate J. Biol. Chem. 275 2000 26449 26457
6. J.T. Seykora, M.M. Myat, L.A. Allen, J.V. Ravetch, and A. Aderem Molecular determinants of the myristoyl-electrostatic switch of MARCKS J. Biol. Chem. 271 1996 18797 18802 (Pubitemid 26322749)
7. M.R. Bubb, R.H. Lenox, and A.S. Edison Phosphorylation-dependent conformational changes induce a switch in the actin-binding function of MARCKS J. Biol. Chem. 274 1999 36472 36478
8. J.H. Hartwig, M. Thelen, A. Rosen, P.A. Janmey, A.C. Nairn, and A. Aderem MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin Nature 356 1992 618 622
9. S. Manenti, O. Sorokine, A. Van Dorsselaer, and H. Taniguchi Affinity purification and characterization of myristoylated alanine-rich protein kinase C substrate (MARCKS) from bovine brain. Comparison of the cytoplasmic and the membrane-bound forms J. Biol. Chem. 267 1992 22310 22315
10. H. Taniguchi, S. Manenti, M. Suzuki, and K. Titani Myristoylated alanine-rich C kinase substrate (MARCKS), a major protein kinase C substrate, is an in vivo substrate of proline-directed protein kinase(s). A mass spectroscopic analysis of the post-translational modifications J. Biol. Chem. 269 1994 18299 18302
11. E. Yamauchi, R. Kiyonami, M. Kanai, and H. Taniguchi Presence of conserved domains in the C-terminus of MARCKS, a major in vivo substrate of protein kinase C: application of ion trap mass spectrometry to the elucidation of protein structures J. Biochem. 123 1998 760 765 (Pubitemid 28197497)
12. M.I. Mosevitsky Nerve ending "signal" proteins GAP-43, MARCKS, and BASP1 Int. Rev. Cytol. 245 2005 245 325
13. F.R. Zolessi, and C. Arruti Apical accumulation of MARCKS in neural plate cells during neurulation in the chick embryo BMC Dev. Biol. 1 2001 7
14. F.R. Zolessi, and C. Arruti MARCKS in advanced stages of neural retina histogenesis Dev. Neurosci. 26 2004 371 379 (Pubitemid 40663245)
15. F.R. Zolessi, R. Duran, U. Engstrom, C. Cervenansky, U. Hellman, and C. Arruti Identification of the chicken MARCKS phosphorylation site specific for differentiating neurons as Ser 25 using a monoclonal antibody and mass spectrometry J. Proteome Res. 3 2004 84 90 (Pubitemid 38233454)
16. A. Toledo, F.R. Zolessi, and C. Arruti A novel effect of MARCKS phosphorylation by activated PKC: the dephosphorylation of its serine 25 in chick neuroblasts PLoS One 8 2013 e62863
17. A. Toledo, and C. Arruti Actin modulation of a MARCKS phosphorylation site located outside the effector domain Biochem. Biophys. Res. Commun. 383 2009 353 357
18. E.G. Yarmola, A.S. Edison, R.H. Lenox, and M.R. Bubb Actin filament cross-linking by MARCKS: characterization of two actin-binding sites within the phosphorylation site domain J. Biol. Chem. 276 2001 22351 22358
19. J.M. Graff, D.J. Stumpo, and P.J. Blackshear Molecular cloning, sequence, and expression of a cDNA encoding the chicken myristoylated alanine-rich C kinase substrate (MARCKS) Mol. Endocrinol. 3 1989 1903 1906 (Pubitemid 20003677)
20. J. Li, and A. Aderem MacMARCKS, a novel member of the MARCKS family of protein kinase C substrates Cell 70 1992 791 801
21. K.K. Lee, C. Joo, S. Yang, H. Han, and M. Cho Phosphorylation effect on the GSSS peptide conformation in water: infrared, vibrational circular dichroism, and circular dichroism experiments and comparisons with molecular dynamics simulations J. Chem. Phys. 126 2007 235102
22. A. Tholey, A. Lindemann, V. Kinzel, and J. Reed Direct effects of phosphorylation on the preferred backbone conformation of peptides: a nuclear magnetic resonance study Biophys. J. 76 1999 76 87 (Pubitemid 29202439)
23. L.M. Espinoza-Fonseca, D. Kast, and D.D. Thomas Thermodynamic and structural basis of phosphorylation-induced disorder-to-order transition in the regulatory light chain of smooth muscle myosin J. Am. Chem. Soc. 130 2008 12208 12209
24. N. Homeyer, T. Essigke, H. Meiselbach, G.M. Ullmann, and H. Sticht Effect of HPr phosphorylation on structure, dynamics, and interactions in the course of transcriptional control J. Mol. Model. 13 2007 431 444 (Pubitemid 46477016)
25. Y.J. Kang, L.M. Zuo, and S.Z. Luo Hydrogen-bonding interactions induced by phosphorylation influence the local conformation of phosphopeptides Int. J. Pept. Res. Ther. 16 2010 87 93
26. F.F. Miranda, M. Thorolfsson, K. Teigen, J.M. Sanchez-Ruiz, and A. Martinez Structural and stability effects of phosphorylation: localized structural changes in phenylalanine hydroxylase Protein Sci. 13 2004 1219 1226 (Pubitemid 38526086)
27. F.R. Zolessi, U. Hellman, A. Baz, and C. Arruti Characterization of MARCKS (myristoylated alanine-rich C kinase substrate) identified by a monoclonal antibody generated against chick embryo neural retina Biochem. Biophys. Res. Commun. 257 1999 480 487 (Pubitemid 29301469)
28. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
29. B.A. Johnson, and R.A. Blevins NMR View: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
30. S.G. Hyberts, M.S. Goldberg, T.F. Havel, and G. Wagner The solution structure of eglin c based on measurements of many NOEs and coupling constants and its comparison with X-ray structures Protein Sci. 1 1992 736 751 (Pubitemid 23007313)
31. Y.S. Day, C.L. Baird, R.L. Rich, and D.G. Myszka Direct comparison of binding equilibrium, thermodynamic, and rate constants determined by surface- and solution-based biophysical methods Protein Sci. 11 2002 1017 1025 (Pubitemid 34441221)
32. Y.C. Huang, Y.C. Chen, H.J. Tsay, C.L. Chyan, C.Y. Chen, H.B. Huang, and T.H. Lin The effect of PKA-phosphorylation on the structure of inhibitor-1 studied by NMR spectroscopy J. Biochem. 147 2010 273 278
33. S. Kar, K. Sakaguchi, Y. Shimohigashi, S. Samaddar, R. Banerjee, G. Basu, V. Swaminathan, T.K. Kundu, and S. Roy Effect of phosphorylation on the structure and fold of transactivation domain of p53 J. Biol. Chem. 277 2002 15579 15585 (Pubitemid 34967827)
34. S.M. Kelly, T.J. Jess, and N.C. Price How to study proteins by circular dichroism Biochim. Biophys. Acta 1751 2005 119 139 (Pubitemid 41112231)
35. K. Wüthrich NMR of Proteins and Nucleic Acids 1986 Wiley New York
36. N.J. Baxter, and M.P. Williamson Temperature dependence of 1H chemical shifts in proteins J. Biomol. NMR 9 1997 359 369 (Pubitemid 127505398)
37. M. Akke NMR methods for characterizing microsecond to millisecond dynamics in recognition and catalysis Curr. Opin. Struct. Biol. 12 2002 642 647 (Pubitemid 35449073)
38. C. Cruzeiro-Silva, F. Gomes-Neto, L.W. Tinoco, E.M. Cilli, P.V. Barros, P.A. Lapido-Loureiro, P.M. Bisch, F.C. Almeida, and A.P. Valente Structural biology of membrane-acting peptides: conformational plasticity of anticoccidial peptide PW2 probed by solution NMR Biochim. Biophys. Acta 1768 2007 3182 3192 (Pubitemid 350236085)
39. J.P. Loria, R.B. Berlow, and E.D. Watt Characterization of enzyme motions by solution NMR relaxation dispersion Acc. Chem. Res. 41 2008 214 221
40. S. Megy, G. Bertho, J. Gharbi-Benarous, F. Baleux, R. Benarous, and J.P. Girault Solution structure of a peptide derived from the oncogenic protein beta-catenin in its phosphorylated and nonphosphorylated states Peptides 26 2005 227 241 (Pubitemid 40051418)
41. J. Kitchen, R.E. Saunders, and J. Warwicker Charge environments around phosphorylation sites in proteins BMC Struct. Biol. 8 2008 19
42. J. Li, D.J. Bigelow, and T.C. Squier Phosphorylation by cAMP-dependent protein kinase modulates the structural coupling between the transmembrane and cytosolic domains of phospholamban Biochemistry 42 2003 10674 10682 (Pubitemid 37102107)
43. D.J. Mandell, I. Chorny, E.S. Groban, S.E. Wong, E. Levine, C.S. Rapp, and M.P. Jacobson Strengths of hydrogen bonds involving phosphorylated amino acid side chains J. Am. Chem. Soc. 129 2007 820 827 (Pubitemid 46183932)
44. S. Kumar, and R. Nussinov Salt bridge stability in monomeric proteins J. Mol. Biol. 293 1999 1241 1255
45. H. Tapp, I.M. Al-Naggar, E.G. Yarmola, A. Harrison, G. Shaw, A.S. Edison, and M.R. Bubb MARCKS is a natively unfolded protein with an inaccessible actin-binding site: evidence for long-range intramolecular interactions J. Biol. Chem. 280 2005 9946 9956 (Pubitemid 40395843)
46. E. Barbar NMR characterization of partially folded and unfolded conformational ensembles of proteins Biopolymers 51 1999 191 207 (Pubitemid 29500937)
47. A.J. McCoy, V. Chandana Epa, and P.M. Colman Electrostatic complementarity at protein/protein interfaces J. Mol. Biol. 268 1997 570 584 (Pubitemid 27208075)
48. I. Kumagai, and K. Tsumoto Antigen-Antibody Binding, Encyclopedia of Life Sciences (ELS) 2010 John Wiley & Sons, Ltd. Chichester