The role of surface electrostatics on the stability, function and regulation of human cystathionine β-synthase, a complex multidomain and oligomeric protein

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 9, 2014, Pages 1453-1462

  Pey, Angel L ^a   Majtan, Tomas ^b   Kraus, Jan P ^b  

^a UNIVERSITY OF GRANADA   (Spain)

^b Children's Hospital Colorado   (United States)

Author keywords

Allostery; Conformational disease; Homocysteine metabolism; Ligand binding; Protein kinetic stability; Surface electrostatics

Indexed keywords

CYSTATHIONINE BETA SYNTHASE; S ADENOSYLMETHIONINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; ENTHALPY; ENTROPY; ENZYME ACTIVATION; ENZYME STABILITY; HOMOCYSTINURIA; HUMAN; INBORN ERROR OF METABOLISM; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN DOMAIN; REFRACTION INDEX; REGULATORY MECHANISM; SIGNAL NOISE RATIO; STATIC ELECTRICITY; SURFACE CHARGE; SURFACE PROPERTY; THERMOSTABILITY;

ALLOSTERY; CONFORMATIONAL DISEASE; HOMOCYSTEINE METABOLISM; LIGAND BINDING; PROTEIN KINETIC STABILITY; SURFACE ELECTROSTATICS;

ADENOSINE; CATALYTIC DOMAIN; CYSTATHIONINE BETA-SYNTHASE; ENZYME ACTIVATION; ETHIONINE; HUMANS; KINETICS; LIGANDS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SODIUM CHLORIDE; STATIC ELECTRICITY; SURFACE PROPERTIES; THERMODYNAMICS; UREA;

EID: 84902258532     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.04.015     Document Type: Article

References (45)

1. E.W. Miles, and J.P. Kraus Cystathionine beta-synthase: structure, function, regulation, and location of homocystinuria-causing mutations J. Biol. Chem. 279 2004 29871 29874
2. S. Singh, and R. Banerjee PLP-dependent H(2)S biogenesis Biochim. Biophys. Acta 1814 2011 1518 1527
3. J. Ereno-Orbea, T. Majtan, I. Oyenarte, J.P. Kraus, and L.A. Martinez-Cruz Structural basis of regulation and oligomerization of human cystathionine beta-synthase, the central enzyme of transsulfuration Proc. Natl. Acad. Sci. U. S. A. 110 2013 E3790 E3799
4. A.L. Pey, T. Majtan, J.M. Sanchez-Ruiz, and J.P. Kraus Human cystathionine beta-synthase (CBS) contains two classes of binding sites for S-adenosylmethionine (SAM): complex regulation of CBS activity and stability by SAM Biochem. J. 449 2013 109 121
5. V. Kozich, J. Sokolova, V. Klatovska, J. Krijt, M. Janosik, K. Jelinek, and J.P. Kraus Cystathionine beta-synthase mutations: effect of mutation topology on folding and activity Hum. Mutat. 31 2010 809 819
6. A. Hnizda, V. Jurga, K. Rakova, and V. Kozich Cystathionine beta-synthase mutants exhibit changes in protein unfolding: conformational analysis of misfolded variants in crude cell extracts J. Inherit. Metab. Dis. 35 2012 469 477
7. A. Hnizda, T. Majtan, L. Liu, A.L. Pey, J.F. Carpenter, M. Kodicek, V. Kozich, and J.P. Kraus Conformational properties of nine purified cystathionine beta-synthase mutants Biochemistry 51 2012 4755 4763
8. M. Janosik, J. Oliveriusova, B. Janosikova, J. Sokolova, E. Kraus, J.P. Kraus, and V. Kozich Impaired heme binding and aggregation of mutant cystathionine beta-synthase subunits in homocystinuria Am. J. Hum. Genet. 68 2001 1506 1513
9. T. Majtan, L. Liu, J.F. Carpenter, and J.P. Kraus Rescue of cystathionine beta-synthase (CBS) mutants with chemical chaperones: purification and characterization of eight CBS mutant enzymes J. Biol. Chem. 285 2010 15866 15873
10. M. Meier, M. Janosik, V. Kery, J.P. Kraus, and P. Burkhard Structure of human cystathionine beta-synthase: a unique pyridoxal 5′-phosphate- dependent heme protein EMBO J. 20 2001 3910 3916
11. S. Taoka, B.W. Lepore, O. Kabil, S. Ojha, D. Ringe, and R. Banerjee Human cystathionine beta-synthase is a heme sensor protein. Evidence that the redox sensor is heme and not the vicinal cysteines in the CXXC motif seen in the crystal structure of the truncated enzyme Biochemistry 41 2002 10454 10461
12. M. Meier, J. Oliveriusova, J.P. Kraus, and P. Burkhard Structural insights into mutations of cystathionine beta-synthase Biochim. Biophys. Acta 1647 2003 206 213
13. A. Prudova, Z. Bauman, A. Braun, V. Vitvitsky, S.C. Lu, and R. Banerjee S-adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity Proc. Natl. Acad. Sci. U. S. A. 103 2006 6489 6494
14. C. Bonaventura, M. Arumugam, R. Cashon, J. Bonaventura, and W.F. Moo-Penn Chloride masks effects of opposing positive charges in Hb A and Hb Hinsdale (beta 139 Asn→Lys) that can modulate cooperativity as well as oxygen affinity J. Mol. Biol. 239 1994 561 568
15. J.M. Sanchez-Ruiz, and G.I. Makhatadze To charge or not to charge? Trends Biotechnol. 19 2001 132 135
16. T.K. Harris, and G.J. Turner Structural basis of perturbed pKa values of catalytic groups in enzyme active sites IUBMB Life 53 2002 85 98
17. A. Warshel, P.K. Sharma, M. Kato, and W.W. Parson Modeling electrostatic effects in proteins Biochim. Biophys. Acta 1764 2006 1647 1676
18. G.R. Grimsley, K.L. Shaw, L.R. Fee, R.W. Alston, B.M. Huyghues-Despointes, R.L. Thurlkill, J.M. Scholtz, and C.N. Pace Increasing protein stability by altering long-range coulombic interactions Protein Sci. 8 1999 1843 1849
19. C.N. Pace, G.R. Grimsley, and J.M. Scholtz Protein ionizable groups: pK values and their contribution to protein stability and solubility J. Biol. Chem. 284 2009 13285 13289
20. V.V. Loladze, B. Ibarra-Molero, J.M. Sanchez-Ruiz, and G.I. Makhatadze Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface Biochemistry 38 1999 16419 16423
21. A.L. Pey, D. Rodriguez-Larrea, S. Bomke, S. Dammers, R. Godoy-Ruiz, M.M. Garcia-Mira, and J.M. Sanchez-Ruiz Engineering proteins with tunable thermodynamic and kinetic stabilities Proteins 71 2008 165 174
22. K.L. Schweiker, and G.I. Makhatadze Protein stabilization by the rational design of surface charge-charge interactions Methods Mol. Biol. 490 2009 261 283
23. A. Zarrine-Afsar, Z. Zhang, K.L. Schweiker, G.I. Makhatadze, A.R. Davidson, and H.S. Chan Kinetic consequences of native state optimization of surface-exposed electrostatic interactions in the Fyn SH3 domain Proteins 80 2012 858 870
24. O. Halskau Jr., R. Perez-Jimenez, B. Ibarra-Molero, J. Underhaug, V. Munoz, A. Martinez, and J.M. Sanchez-Ruiz Large-scale modulation of thermodynamic protein folding barriers linked to electrostatics Proc. Natl. Acad. Sci. U. S. A. 105 2008 8625 8630
25. X. Tadeo, B. Lopez-Mendez, T. Trigueros, A. Lain, D. Castano, and O. Millet Structural basis for the aminoacid composition of proteins from halophilic archea PLoS Biol. 7 2009 e1000257
26. T.M. Desai, M. Cerminara, M. Sadqi, and V. Munoz The effect of electrostatics on the marginal cooperativity of an ultrafast folding protein J. Biol. Chem. 285 2010 34549 34556
27. E. Sedlak, L. Stagg, and P. Wittung-Stafshede Effect of Hofmeister ions on protein thermal stability: roles of ion hydration and peptide groups? Arch. Biochem. Biophys. 479 2008 69 73
28. A.L. Pey, N. Mesa-Torres, L.R. Chiarelli, and G. Valentini Structural and energetic basis of protein kinetic destabilization in human phosphoglycerate kinase 1 deficiency Biochemistry 52 2013 1160 1170
29. D. Rodriguez-Larrea, S. Minning, T.V. Borchert, and J.M. Sanchez-Ruiz Role of solvation barriers in protein kinetic stability J. Mol. Biol. 360 2006 715 724
30. M. Costas, D. Rodriguez-Larrea, L. De Maria, T.V. Borchert, A. Gomez-Puyou, and J.M. Sanchez-Ruiz Between-species variation in the kinetic stability of TIM proteins linked to solvation-barrier free energies J. Mol. Biol. 385 2009 924 937
31. A.D. Robertson, and K.P. Murphy Protein structure and the energetics of protein stability Chem. Rev. 97 1997 1251 1268
32. J.K. Myers, C.N. Pace, and J.M. Scholtz Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4 1995 2138 2148
33. J.P. Kraus Cystathionine beta-synthase (human) Methods Enzymol. 143 1987 388 394
34. D.K. Wilkins, S.B. Grimshaw, V. Receveur, C.M. Dobson, J.A. Jones, and L.J. Smith Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38 1999 16424 16431
35. S.R. Tzeng, and C.G. Kalodimos Dynamic activation of an allosteric regulatory protein Nature 462 2009 368 372
36. I. Gomez-Garcia, I. Oyenarte, and L.A. Martinez-Cruz The crystal structure of protein MJ1225 from Methanocaldococcus jannaschii shows strong conservation of key structural features seen in the eukaryal gamma-AMPK J. Mol. Biol. 399 2010 53 70
37. H. Tuominen, A. Salminen, E. Oksanen, J. Jamsen, O. Heikkila, L. Lehtio, N.N. Magretova, A. Goldman, A.A. Baykov, and R. Lahti Crystal structures of the CBS and DRTGG domains of the regulatory region of Clostridium perfringens pyrophosphatase complexed with the inhibitor, AMP, and activator, diadenosine tetraphosphate J. Mol. Biol. 398 2010 400 413
38. S. Taoka, L. Widjaja, and R. Banerjee Assignment of enzymatic functions to specific regions of the PLP-dependent heme protein cystathionine beta-synthase Biochemistry 38 1999 13155 13161
39. S.R. Tzeng, and C.G. Kalodimos Allosteric inhibition through suppression of transient conformational states Nat. Chem. Biol. 9 2013 462 465
40. A. Prudova, M.V. Martinov, V.M. Vitvitsky, F.I. Ataullakhanov, and R. Banerjee Analysis of pathological defects in methionine metabolism using a simple mathematical model Biochim. Biophys. Acta 1741 2005 331 338
41. A. Matouschek, and A.R. Fersht Application of physical organic chemistry to engineered mutants of proteins: Hammond postulate behavior in the transition state of protein folding Proc. Natl. Acad. Sci. U. S. A. 90 1993 7814 7818
42. A. Fortian, D. Castano, G. Ortega, A. Lain, M. Pons, and O. Millet Uroporphyrinogen III synthase mutations related to congenital erythropoietic porphyria identify a key helix for protein stability Biochemistry 48 2009 454 461
43. Y. Aguirre, N. Cabrera, B. Aguirre, R. Perez-Montfort, A. Hernandez-Santoyo, H. Reyes-Vivas, S. Enriquez-Flores, M.T. de Gomez-Puyou, A. Gomez-Puyou, J.M. Sanchez-Ruiz, and M. Costas Different contribution of conserved amino acids to the global properties of triosephosphate isomerases Proteins 82 2014 323 335
44. J.M. Sanchez-Ruiz, J.L. Lopez-Lacomba, M. Cortijo, and P.L. Mateo Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin Biochemistry 27 1988 1648 1652
45. J.M. Sanchez-Ruiz Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry Biophys. J. 61 1992 921 935