Protein homeostasis disorders of key enzymes of amino acids metabolism: Mutation-induced protein kinetic destabilization and new therapeutic strategies

Amino Acids

Volumn 45, Issue 6, 2013, Pages 1331-1341

  Pey, Angel L ^a  

^a UNIVERSITY OF GRANADA   (Spain)

Author keywords

Amino acid metabolism; Conformational disease; Ligand binding; Pharmacological therapy; Protein homeostasis; Protein stability

Indexed keywords

ALANINE GLYOXYLATE AMINOTRANSFERASE; CHAPERONE; CYSTATHIONINE BETA SYNTHASE; PHENYLALANINE 4 MONOOXYGENASE; PYRIDOXINE; TETRAHYDROBIOPTERIN; AMINO ACID; PROTEIN;

BIOPHYSICS; CELL ORGANELLE; DRUG EFFICACY; DRUG MECHANISM; HOMOCYSTINURIA; HUMAN; KINETICS; LIGAND BINDING; MUTATION; NONHUMAN; OXALOSIS 1; PHENYLKETONURIA; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; THERMODYNAMICS; ANIMAL; CHEMISTRY; ENZYMOLOGY; GENETICS; HOMEOSTASIS; METABOLISM; POINT MUTATION; PROTEOSTASIS DEFICIENCIES;

ANIMALIA;

AMINO ACIDS; ANIMALS; HOMEOSTASIS; HUMANS; KINETICS; POINT MUTATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEINS; PROTEOSTASIS DEFICIENCIES;

EID: 84890556483     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-013-1609-7     Document Type: Review

References (83)

1. Albert A, Yunta C, Arranz R, Peña A, Salido E, Valpuesta MJ, Martin-Benito J (2010) Structure of GroEL in complex with an early folding intermediate of alanine glyoxylate aminotransferase. J Biol Chem 285:6371-6376
2. Baker D, Agard DA (1994) Kinetics versus thermodynamics in protein folding. Biochemistry 33:7505-7509
3. Baker D, Sohl JL, Agard DA (1992) A protein-folding reaction under kinetic control. Nature 356:263-265
4. Balch WE, Morimoto RI, Dillin A, Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319:916-919
5. Calamini B, Silva MC, Madoux F, Hutt DM, Khanna S, Chalfant MA, Saldanha SA, Hodder P, Tait BD, Garza D, Balch WE, Morimoto RI (2011) Small-molecule proteostasis regulators for protein conformational diseases. Nat Chem Biol 8:185-196
6. Casanueva MO, Burga A, Lehner B (2012) Fitness trade-offs and environmentally induced mutation buffering in isogenic C. elegans. Science 335:82-85
7. Cellini B, Montioli R, Paiardini A, Lorenzetto A, Maset F, Bellini T, Oppici E, Voltattorni CB (2010a) Molecular defects of the glycine 41 variants of alanine glyoxylate aminotransferase associated with primary hyperoxaluria type I. Proc Natl Acad Sci USA 107:2896-2901
8. Cellini B, Lorenzetto A, Montioli R, Oppici E, Voltattorni CB (2010b) Human liver peroxisomal alanine:glyoxylate aminotransferase: different stability under chemical stress of the major allele, the minor allele, and its pathogenic G170R variant. Biochimie 92:1801-1811
9. Cellini B, Montioli R, Voltattorni CB (2011) Human liver peroxisomal alanine:glyoxylate aminotransferase: characterization of the two allelic forms and their pathogenic variants. Biochim Biophys Acta 1814:1577-1584
10. Chen X, Wang L, Fazlieva R, Kruger WD (2006) Contrasting behaviors of mutant cystathionine beta-synthase enzymes associated with pyridoxine response. Hum Mutat 27:474-482
11. Clayton PT (2006) B6-responsive disorders: a model of vitamin dependency. J Inherit Metab Dis 29:317-326
12. Danpure CJ (2001) Primary hyperoxalurias. The metabolic and molecular bases of disease. In: Scriver CR, Beaudet A, Sly W, Valle D, Childs B, Kinzler K, Vogelstein B (eds). 8th Edn. McGraw-Hill, New York, pp 3323-3367
13. Danpure CJ (2006) Primary hyperoxaluria type 1: AGT mistargeting highlights the fundamental differences between the peroxisomal and mitochondrial protein import pathways. Biochim Biophys Acta 1763:1776-1784
14. di Salvo ML, Contestabile R, Safo MK (2011) Vitamin B(6) salvage enzymes: mechanism, structure and regulation. Biochim Biophys Acta 1814:1597-1608
15. Dill KA, Ozkan SB, Shell MS, Weikl TR (2008) The protein folding problem. Annu Rev Biophys 37:289-316
16. Dobrowolski SF, Pey AL, Koch R, Levy H, Ellingson CC, Naylor EW, Martinez A (2009) Biochemical characterization of mutant phenylalanine hydroxylase enzymes and correlation with clinical presentation in hyperphenylalaninaemic patients. J Inherit Metab Dis 32:10-21
17. Erlandsen H, Pey AL, Gámez A, Pérez B, Desviat LR, Aguado C, Koch R, Surendran S, Tyring S, Matalon R, Scriver CR, Ugarte M, Martínez A, Stevens RC (2004) Correction of kinetic and stability defects by tetrahydrobiopterin in phenylketonuria patients with certain phenylalanine hydroxylase mutations. Proc Natl Acad Sci USA 101:16903-16908
18. Fargue S, Rumsby G, Danpure CJ (2013a) Multiple mechanisms of action of pyridoxine in primary hyperoxaluria type 1. Biochim Biophys Acta 1832:1776-1783
19. Fargue S, Lewin J, Rumsby G, Danpure CJ (2013b) Four of the most common mutations in primary hyperoxaluria type 1 unmask the cryptic mitochondrial targeting sequence of alanine:glyoxylate aminotransferase encoded by the polymorphic minor allele. J Biol Chem 288:2475-2484
20. Fitzpatrick PF (2012) Allosteric regulation of phenylalanine hydroxylase. Arch Biochem Biophys 519(2):194-201
21. Flydal MI, Martinez A (2013) Phenylalanine hydroxylase: function, structure, and regulation. IUBMB Life 65:341-349
22. Gamez A, Perez B, Ugarte M, Desviat LR (2000) Expression analysis of phenylketonuria mutations. Effect on folding and stability of the phenylalanine hydroxylase protein. J Biol Chem 275:29737-29742
23. Gersting SW, Kemter KF, Staudigl M, Messing DD, Danecka MK, Lagler FB, Sommerhoff CP, Roscher AA, Muntau AC (2008) Loss of function in phenylketonuria is caused by impaired molecular motions and conformational instability. Am J Hum Genet 83:5-17
24. Gersting SW, Lagler FB, Eichinger A, Kemter KF, Danecka MK, Messing DD, Staudigl M, Domdey KA, Zsifkovits C, Fingerhut R, Glossmann H, Roscher AA, Muntau AC (2010) Pahenu1 is a mouse model for tetrahydrobiopterin-responsive phenylalanine hydroxylase deficiency and promotes analysis of the pharmacological chaperone mechanism in vivo. Hum Mol Genet 19:2039-2049
25. Gomes CM (2012) Protein misfolding in disease and small molecule therapies. Curr Top Med Chem 12:2460-2469
26. Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16:574-581
27. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324-332
28. HnÍzda A, Majtan T, Liu L, Pey AL, Carpenter JF, KodÍček V, Kožich M, Kraus JP (2012) Conformational properties of nine purified cystathionine beta-synthase mutants. Biochemistry 51:4755-4763
29. Kozich V, Sokolová J, Klatovská V, Krijt J, Janosík M, Jelínek K, Kraus JP (2010) Cystathionine beta-synthase mutations: effect of mutation topology on folding and activity. Hum Mutat 31:809-819
30. Kure S, Hou DC, Ohura T, Iwamoto H, Suzuki S, Sugiyama N, Sakamoto O, Fujii K, Matsubara Y, Narisawa K (1999) Tetrahydrobiopterin-responsive phenylalanine hydroxylase deficiency. J Pediatr 135:375-378
31. Lehner B (2013) Genotype to phenotype: lessons from model organisms for human genetics. Nat Rev Genet 14:168-178
32. Lumry R, Eyring R (1954) Conformation changes in proteins. J Phys Chem 58:110-120
33. Majtan T, Liu L, Carpenter JF, Kraus JP (2010) Rescue of cystathionine beta-synthase (CBS) mutants with chemical chaperones: purification and characterization of eight CBS mutant enzymes. J Biol Chem 285:15866-15873
34. Martinez A, Calvo AC, Teigen K, Pey AL (2008) Rescuing proteins of low kinetic stability by chaperones and natural ligands phenylketonuria, a case study. Prog Mol Biol Transl Sci 83:89-134
35. Meier M, Oliveriusova J, Kraus JP, Burkhard P (2003) Structural insights into mutations of cystathionine beta-synthase. Biochim Biophys Acta 1647:206-213
36. Mesa-Torres N, Fabelo-Rosa I, Riverol D, Yunta C, Albert A, Salido E, Pey AL (2013) Protein folding and stability defects associated with aggregation and mistargeting mechanisms underlying primary hyperoxaluria type I. PLoS One 8:e71963
37. Miles EW, Kraus JP (2004) Cystathionine beta-synthase: structure, function, regulation, and location of homocystinuria-causing mutations. J Biol Chem 279:29871-29874
38. Miranda FF, Teigen K, Thórólfsson M, Svebak RM, Knappskog PM, Flatmark T, Martínez A (2002) Phosphorylation and mutations of Ser(16) in human phenylalanine hydroxylase. Kinetic and structural effects. J Biol Chem 277:40937-40943
39. Mitnaul LJ, Shiman R (1995) Coordinate regulation of tetrahydrobiopterin turnover and phenylalanine hydroxylase activity in rat liver cells. Proc Natl Acad Sci USA 92(3):885-889
40. Monico CG, Rossetti S, Olson JB, Milliner DS (2005) Pyridoxine effect in type I primary hyperoxaluria is associated with the most common mutant allele. Kidney Int 67:1704-1709
41. Mudd SH, Levy HL, Kraus JP (2001) Disorders of transulfuration. The metabolic and molecular bases of disease. In: Scriver CR, Beaudet A, Sly W, Valle D, Childs B, Kinzler K, Vogelstein B (eds). 8th Edn. McGraw-Hill, New York, pp 2007-2056
42. Muntau AC, Gersting SW (2010) Phenylketonuria as a model for protein misfolding diseases and for the development of next generation orphan drugs for patients with inborn errors of metabolism. J Inherit Metab Dis 33:649-658
43. Nordlund A, Oliveberg M (2008) SOD1-associated ALS: a promising system for elucidating the origin of protein-misfolding disease. HFSP J 2:354-364
44. Ong DS, Kelly JW (2011) Chemical and/or biological therapeutic strategies to ameliorate protein misfolding diseases. Curr Opin Cell Biol 23:231-238
45. Oppici E, Montioli R, Lorenzetto A, Bianconi S, Borri Voltattorni C, Cellini B (2012) Biochemical analyses are instrumental in identifying the impact of mutations on holo and/or apo-forms and on the region(s) of alanine:glyoxylate aminotransferase variants associated with primary hyperoxaluria type I. Mol Genet Metab 105:132-140
46. Oppici E, Fodor K, Paiardini A, Williams C, Voltattorni CB, Willmanns M, Cellini B (2013) Crystal structure of the S187F variant of human liver alanine: glyoxylate aminotransferase associated with primary hyperoxaluria type I and its functional implications. Proteins 81:1457-1465
47. Park C, Marqusee S (2004) Probing the high energy states in proteins by proteolysis. J Mol Biol 343:1467-1476
48. Pey AL, Martinez A (2007) Tetrahydrobiopterin for patients with phenylketonuria. Lancet 370(9586):462-463
49. Pey AL, Desviat LR, Gámez A, Ugarte M, Pérez B (2003) Phenylketonuria: genotype-phenotype correlations based on expression analysis of structural and functional mutations in PAH. Hum Mutat 21:370-378
50. Pey AL, Pérez B, Desviat LR, Martínez MA, Aguado C, Erlandsen H, Gámez A, Stevens RC, Thórólfsson M, Ugarte M, Martínez A (2004a) Mechanisms underlying responsiveness to tetrahydrobiopterin in mild phenylketonuria mutations. Hum Mutat 24:388-399
51. Pey AL, Thórólfsson M, Teigen K, Ugarte M, Martínez A (2004b) Thermodynamic characterization of the binding of tetrahydropterins to phenylalanine hydroxylase. J Am Chem Soc 126:13670-13678
52. Pey AL, Stricher F, Serrano L, Martinez A (2007) Predicted effects of missense mutations on native-state stability account for phenotypic outcome in phenylketonuria, a paradigm of misfolding diseases. Am J Hum Genet 81:1006-1024
53. Pey AL, Ying M, Cremades N, Velazquez-Campoy A, Scherer T, Thöny B, Sancho J, Martinez A (2008) Identification of pharmacological chaperones as potential therapeutic agents to treat phenylketonuria. J Clin Invest 118:2858-2867
54. Pey AL, Salido E, Sanchez-Ruiz JM (2011) Role of low native state kinetic stability and interaction of partially unfolded states with molecular chaperones in the mitochondrial protein mistargeting associated with primary hyperoxaluria. Amino Acids 41:1233-1245
55. Pey AL, Mesa-Torres N, Chiarelli LR, Valentini G (2013a) Structural and Energetic Basis of Protein Kinetic Destabilization in Human Phosphoglycerate Kinase 1 Deficiency. Biochemistry 52:1160-1170
56. Pey AL, Majtan T, Sanchez-Ruiz JM, Kraus JP (2013b) 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 449:109-121
57. Plaza del Pino IM, Ibarra-Molero B, Sanchez-Ruiz JM (2000) Lower kinetic limit to protein thermal stability: a proposal regarding protein stability in vivo and its relation with misfolding diseases. Proteins 40:58-70
58. Powers ET, Balch WE (2013) Diversity in the origins of proteostasis networks - a driver for protein function in evolution. Nat Rev Mol Cell Biol 14:237-248
59. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 78:959-991
60. Prudova A, Bauman Z, Braun A, Vitvitsky V, Lu SC, Banerjee R (2006) S-adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity. Proc Natl Acad Sci USA 103:6489-6494
61. Rodrigues JV, Henriques BJ, Lucas TG, Gomes CM (2012) Cofactors and metabolites as protein folding helpers in metabolic diseases. Curr Top Med Chem 12:2546-2559
62. Salido E, Pey AL, Rodriguez R, Lorenzo V (2012) Primary hyperoxalurias: disorders of glyoxylate detoxification. Biochim Biophys Acta 1822:1453-1464
63. Sánchez-Romero I, Ariza A, Wilson KS, Skjøt M, Vind J, De Maria L, Skov LK, Sánchez-Ruiz JM (2013) Mechanism of protein kinetic stabilization by engineered disulfide crosslinks. PLoS One 8:e70013
64. Sanchez-Ruiz JM (1992) Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys J 61:921-935
65. Sanchez-Ruiz JM (2010) Protein kinetic stability. Biophys Chem 148:1-15
66. Sánchez-Ruiz JM, López-Lacomba JL, Cortijo M, Mateo PL (1988) Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin. Biochemistry 27:1648-1652
67. Santana A, Salido E, Torres A, Shapiro LJ (2003) Primary hyperoxaluria type 1 in the Canary Islands: a conformational disease due to I244T mutation in the P11L-containing alanine:glyoxylate aminotransferase. Proc Natl Acad Sci USA 100:7277-7282
68. Santos-Sierra S, Kirchmair J, Perna AM, Reiss D, Kemter K, Röschinger W, Glossmann H, Gersting SW, Muntau AC, Wolber G, Lagler FB (2012) Novel pharmacological chaperones that correct phenylketonuria in mice. Hum Mol Genet 21:1877-1887
69. Sarkissian CN, Ying M, Scherer T, Thöny B, Martinez A (2012) The mechanism of BH4 -responsive hyperphenylalaninemia-as it occurs in the ENU1/2 genetic mouse model. Hum Mutat 33:1464-1473
70. Scavelli R, Ding Z, Blau N, Haavik J, Martínez A, Thöny B (2005) Stimulation of hepatic phenylalanine hydroxylase activity but not Pah-mRNA expression upon oral loading of tetrahydrobiopterin in normal mice. Mol Genet Metab 86:S153-S155
71. Smith AT, Su Y, Stevens DJ, Majtan T, Kraus JP, Burstyn JN (2012) Effect of the disease-causing R266K mutation on the heme and PLP environments of human cystathionine beta-synthase. Biochemistry 51:6360-6370
72. Staudigl M, Gersting SW, Danecka MK, Messing DD, Woidy M, Pinkas D, Kemter KF, Blau N, Muntau AC (2011) The interplay between genotype, metabolic state and cofactor treatment governs phenylalanine hydroxylase function and drug response. Hum Mol Genet 20:2628-2641
73. Thöny B, Ding Z, Martínez A (2004) Tetrahydrobiopterin protects phenylalanine hydroxylase activity in vivo: implications for tetrahydrobiopterin-responsive hyperphenylalaninemia. FEBS Lett 577:507-511
74. Thórólfsson M, Ibarra-Molero B, Fojan P, Petersen SB, Sanchez-Ruiz JM, Martínez A (2002) l-Phenylalanine binding and domain organization in human phenylalanine hydroxylase: a differential scanning calorimetry study. Biochemistry 41:7573-7585
75. Thórólfsson M, Teigen K, Martínez A (2003) Activation of phenylalanine hydroxylase: effect of substitutions at Arg68 and Cys237. Biochemistry 42:3419-3428
76. Thorson MK, Majtan T, Kraus JP, Barrios AM (2013) Identification of cystathionine beta-synthase inhibitors using a hydrogen sulfide selective probe. Angew Chem Int Ed Engl 52:4641-4644
77. Underhaug J, Aubi O, Martinez A (2012) Phenylalanine hydroxylase misfolding and pharmacological chaperones. Curr Top Med Chem 12:2534-2545
78. van Woerden CS, Groothoff JW, Wijburg FA, Annink C, Wanders RJ, Waterham HR (2004) Clinical implications of mutation analysis in primary hyperoxaluria type 1. Kidney Int 66:746-752
79. Wilcken DE, Wilcken B (1997) The natural history of vascular disease in homocystinuria and the effects of treatment. J Inherit Metab Dis 20:295-300
80. Williams EL, Acquaviva C, Amoroso A, Chevalier F, Coulter-Mackie M, Monico CG, Giachino D, Owen T, Robbiano A, Salido E, Waterham H, Rumsby G (2009) Primary hyperoxaluria type 1: update and additional mutation analysis of the AGXT gene. Hum Mutat 30:910-917
81. Wiseman RL, Powers ET, Buxbaum JN, Kelly JW, Balch WE (2007) An adaptable standard for protein export from the endoplasmic reticulum. Cell 131:809-821
82. Yap S, Naughten ER, Wilcken B, Wilcken DE, Boers GH (2000) Vascular complications of severe hyperhomocysteinemia in patients with homocystinuria due to cystathionine beta-synthase deficiency: effects of homocysteine-lowering therapy. Semin Thromb Hemost 26:335-340
83. Yap S, Boers GH, Wilcken B, Wilcken DE, Brenton DP, Lee PJ, Walter JH, Howard PM, Naughten ER (2001) Vascular outcome in patients with homocystinuria due to cystathionine beta-synthase deficiency treated chronically: a multicenter observational study. Arterioscler Thromb Vasc Biol 21:2080-2085