The Role of Protein Denaturation Energetics and Molecular Chaperones in the Aggregation and Mistargeting of Mutants Causing Primary Hyperoxaluria Type I

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Mesa Torres, Noel ^a   Fabelo Rosa, Israel ^b   Riverol, Debora ^b   Yunta, Cristina ^c   Albert, Armando ^c   Salido, Eduardo ^b   Pey, Angel L ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

^c INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK COGNATE PROTEIN 70;

ANIMAL CELL; ARTICLE; CAUSAL ATTRIBUTION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENERGY TRANSFER; GENE EXPRESSION; GENE INTERACTION; GENE MUTATION; GENE TARGETING; GENETIC STABILITY; GENETIC VARIABILITY; IN VITRO STUDY; MITOCHONDRION; MOLECULAR PATHOLOGY; NONHUMAN; OXALOSIS 1; PROTEIN AGGREGATION; PROTEIN DENATURATION; PROTEIN FOLDING;

ANIMALS; CHO CELLS; CRICETULUS; HSC70 HEAT-SHOCK PROTEINS; HUMANS; HYPEROXALURIA, PRIMARY; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; TRANSAMINASES;

EID: 84883174258     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071963     Document Type: Article

References (47)

1. Williams EL, Acquaviva C, Amoroso A, Chevalier F, Coulter-Mackie M, et al. (2009) Primary hyperoxaluria type 1: update and additional mutation analysis of the AGXT gene. Hum Mutat 30: 910-917.
2. 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.
3. Cochat P, Hulton SA, Acquaviva C, Danpure CJ, Daudon M, et al. (2012) Primary hyperoxaluria Type 1: indications for screening and guidance for diagnosis and treatment. Nephrol Dial Transplant 27: 1729-1736.
4. 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.
5. Lumb MJ, Birdsey GM, Danpure CJ, (2003) Correction of an enzyme trafficking defect in hereditary kidney stone disease in vitro. Biochem J 374: 79-87.
6. 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.
7. Salido E, Pey AL, Rodriguez R, Lorenzo V, (2012) Primary hyperoxalurias: Disorders of glyoxylate detoxification. Biochim Biophys Acta 1822: 1453-1464.
8. Coulter-Mackie MB, Lian Q, (2006) Consequences of missense mutations for dimerization and turnover of alanine:glyoxylate aminotransferase: study of a spectrum of mutations. Mol Genet Metab 89: 349-359.
9. 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 U S A 100: 7277-7282.
10. Martin W, (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 365: 847-855.
11. 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.
12. Balch WE, Morimoto RI, Dillin A, Kelly JW, (2008) Adapting proteostasis for disease intervention. Science 319: 916-919.
13. Hartl FU, Bracher A, Hayer-Hartl M, (2011) Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332.
14. Gomes CM, (2012) Protein misfolding in disease and small molecule therapies. Curr Top Med Chem 12: 2460-2469.
15. Albert A, Yunta C, Arranz R, Pena A, Salido E, et al. (2010) Structure of GroEL in complex with an early folding intermediate of alanine glyoxylate aminotransferase. J Biol Chem 285: 6371-6376.
16. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T, (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4: 2411-2423.
17. Cellini B, Bertoldi M, Montioli R, Paiardini A, Borri Voltattorni C, (2007) Human wild-type alanine:glyoxylate aminotransferase and its naturally occurring G82E variant: functional properties and physiological implications. Biochem J 408: 39-50.
18. Rumsby G, Weir T, Samuell CT, (1997) A semiautomated alanine:glyoxylate aminotransferase assay for the tissue diagnosis of primary hyperoxaluria type 1. Ann Clin Biochem 34 (Pt 4) (): 400-404.
19. Rodriguez-Larrea D, Minning S, Borchert TV, Sanchez-Ruiz JM, (2006) Role of solvation barriers in protein kinetic stability. J Mol Biol 360: 715-724.
20. Kabsch W, (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
21. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
22. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
23. Zhang X, Roe SM, Hou Y, Bartlam M, Rao Z, et al. (2003) Crystal structure of alanine:glyoxylate aminotransferase and the relationship between genotype and enzymatic phenotype in primary hyperoxaluria type 1. J Mol Biol 331: 643-652.
24. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
25. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
26. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
27. DeLano WL (2002) Pymol. DeLano Scientific LLC.
28. Fodor K, Wolf J, Erdmann R, Schliebs W, Wilmanns M, (2012) Molecular requirements for peroxisomal targeting of alanine-glyoxylate aminotransferase as an essential determinant in primary hyperoxaluria type 1. PLoS Biol 10: e1001309.
29. Cellini B, Montioli R, Paiardini A, Lorenzetto A, Maset F, et al. (2010) Molecular defects of the glycine 41 variants of alanine glyoxylate aminotransferase associated with primary hyperoxaluria type I. Proc Natl Acad Sci U S A 107: 2896-2901.
30. Sanchez-Ruiz JM, (1992) Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys J 61: 921-935.
31. Robertson AD, Murphy KP, (1997) Protein Structure and the Energetics of Protein Stability. Chem Rev 97: 1251-1268.
32. Costas M, Rodriguez-Larrea D, De Maria L, Borchert TV, Gomez-Puyou A, et al. (2009) Between-species variation in the kinetic stability of TIM proteins linked to solvation-barrier free energies. J Mol Biol 385: 924-937.
33. Pey AL, Mesa-Torres N, Chiarelli LR, Valentini G, (2013) Structural and Energetic Basis of Protein Kinetic Destabilization in Human Phosphoglycerate Kinase 1 Deficiency. Biochemistry 52: 1160-1170.
34. Djordjevic S, Zhang X, Bartlam M, Ye S, Rao Z, et al. (2010) Structural implications of a G170R mutation of alanine:glyoxylate aminotransferase that is associated with peroxisome-to-mitochondrion mistargeting. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: 233-236.
35. Cellini B, Montioli R, Paiardini A, Lorenzetto A, Voltattorni CB, (2009) Molecular Insight into the Synergism between the Minor Allele of Human Liver Peroxisomal Alanine:Glyoxylate Aminotransferase and the F152I Mutation. J Biol Chem 284: 8349-8358.
36. Fargue S, Lewin J, Rumsby G, Danpure CJ, (2013) 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.
37. Fargue S, Rumsby G, Danpure CJ, (2013) Multiple mechanisms of action of pyridoxine in primary hyperoxaluria type 1. Biochim Biophys Acta.
38. 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.
39. van Woerden CS, Groothoff JW, Wijburg FA, Annink C, Wanders RJ, et al. (2004) Clinical implications of mutation analysis in primary hyperoxaluria type 1. Kidney Int 66: 746-752.
40. Cellini B, Lorenzetto A, Montioli R, Oppici E, Voltattorni CB, (2010) 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.
41. Pittman AM, Lage MD, Poltoratsky V, Vrana JD, Paiardini A, et al. (2012) Rapid profiling of disease alleles using a tunable reporter of protein misfolding. Genetics 192: 831-842.
42. di Salvo ML, Contestabile R, Safo MK, (2011) Vitamin B(6) salvage enzymes: mechanism, structure and regulation. Biochim Biophys Acta 1814: 1597-1608.
43. Casanueva MO, Burga A, Lehner B, (2012) Fitness trade-offs and environmentally induced mutation buffering in isogenic C. elegans. Science 335: 82-85.
44. Danpure CJ, editor. Primary hyperoxalurias.
45. Chakraborty K, Chatila M, Sinha J, Shi Q, Poschner BC, et al. (2010) Chaperonin-catalyzed rescue of kinetically trapped states in protein folding. Cell 142: 112-122.
46. Kerner MJ, Naylor DJ, Ishihama Y, Maier T, Chang HC, et al. (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122: 209-220.
47. Sanchez-Ruiz JM, Lopez-Lacomba JL, Cortijo M, Mateo PL, (1988) Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin. Biochemistry 27: 1648-1652.