About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 687658, 15 pages
http://dx.doi.org/10.1155/2013/687658
Review Article

Protein Homeostasis Defects of Alanine-Glyoxylate Aminotransferase: New Therapeutic Strategies in Primary Hyperoxaluria Type I

1Departamento de Química-Física, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva s/n, 18071 Granada, Spain
2Departamento de Cristalografía y Biología Estructural, Instituto de Química Física “Rocasolano”, Consejo Superior de Investigaciones Científicas, Serrano 119, 28006 Madrid, Spain
3Centre for Biomedical Research on Rare Diseases (CIBERER), University Hospital of the Canary Islands, and CIBICAN, University of La Laguna, 38320 Tenerife, Spain

Received 28 April 2013; Accepted 23 May 2013

Academic Editor: Barbara Cellini

Copyright © 2013 Angel L. Pey et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. Hoppe, “An update on primary hyperoxaluria,” Nature Reviews Nephrology, vol. 8, pp. 467–475, 2012. View at Publisher · View at Google Scholar
  2. E. Salido, A. L. Pey, R. Rodriguez, and V. Lorenzo, “Primary hyperoxalurias: disorders of glyoxylate detoxification,” Biochimica et Biophysica Acta, vol. 1822, no. 9, pp. 1453–1464, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. C. J. Danpure, “Primary hyperoxalurias,” in The Metabolic and Molecular Bases of Inherited Disease, C. R. Scriver, A. L. Beaudet, W. S. Sly et al., Eds., vol. 2, pp. 3323–3367, McGraw-Hill, New York, NY, USA, 8th edition, 2001.
  4. M. Zylicz, T. Yamamoto, N. McKittrick, S. Sell, and C. Georgopoulos, “Purification and properties of the dnaJ replication protein of Escherichia coli,” The Journal of Biological Chemistry, vol. 260, no. 12, pp. 7591–7598, 1985. View at Scopus
  5. W. Martin, “Evolutionary origins of metabolic compartmentalization in eukaryotes,” Philosophical Transactions of the Royal Society B, vol. 365, no. 1541, pp. 847–855, 2010. View at Publisher · View at Google Scholar
  6. R. J. A. Wanders and H. R. Waterham, “Biochemistry of mammalian peroxisomes revisited,” Annual Review of Biochemistry, vol. 75, pp. 295–332, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Rokka, V. D. Antonenkov, R. Soininen et al., “Pxmp2 is a channel-forming protein in mammalian peroxisomal membrane,” PLoS ONE, vol. 4, no. 4, Article ID e5090, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. B. Cellini, M. Bertoldi, R. Montioli, A. Paiardini, and C. B. Voltattorni, “Human wild-type alanine:glyoxylate aminotransferase and its naturally occurring G82E variant: functional properties and physiological implications,” Biochemical Journal, vol. 408, no. 1, pp. 39–50, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Knight and R. P. Holmes, “Mitochondrial hydroxyproline metabolism: implications for primary hyperoxaluria,” The American Journal of Nephrology, vol. 25, no. 2, pp. 171–175, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Knight, J. Jiang, D. G. Assimos, and R. P. Holmes, “Hydroxyproline ingestion and urinary oxalate and glycolate excretion,” Kidney International, vol. 70, no. 11, pp. 1929–1934, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Adams and L. Frank, “Metabolism of proline and the hydroxyprolines,” Annual Review of Biochemistry, vol. 49, pp. 1005–1061, 1980. View at Scopus
  12. R. P. Holmes and D. G. Assimos, “Glyoxylate synthesis, and its modulation and influence on oxalate synthesis,” Journal of Urology, vol. 160, no. 5, pp. 1617–1624, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. J. M. Phang, C. A. Hu, and D. Valle, “Disorders in proline and hidroxyproline metabolism,” in The Metabolic and Molecular Bases of Inherited Disease, C. R. Scriver, A. Beaudet, W. Sly, D. Valle, and B. Childs, Eds., pp. 1821–1838, McGraw-Hill, New York, NY, USA, 2001.
  14. P. Cochat, A. Deloraine, M. Rotily, F. Olive, I. Liponski, and N. Deries, “Epidemiology of primary hyperoxaluria type 1,” Nephrology Dialysis Transplantation, vol. 10, supplement 8, pp. 3–7, 1995. View at Scopus
  15. N. Kopp and E. Leumann, “Changing pattern of primary hyperoxaluria in Switzerland,” Nephrology Dialysis Transplantation, vol. 10, no. 12, pp. 2224–2227, 1995. View at Scopus
  16. C. S. van Woerden, J. W. Groothoff, R. J. A. Wanders, J. Davin, and F. A. Wijburg, “Primary hyperoxaluria type 1 in The Netherlands: prevalence and outcome,” Nephrology Dialysis Transplantation, vol. 18, no. 2, pp. 273–279, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. V. Lorenzo, A. Alvarez, A. Torres, V. Torregrosa, D. Hernández, and E. Salido, “Presentation and role of transplantation in adult patients with type 1 primary hyperoxaluria and the I244T AGXT mutation: single-center experience,” Kidney International, vol. 70, no. 6, pp. 1115–1119, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Harambat, K. J. van Stralen, L. Espinosa et al., “Characteristics and outcomes of children with primary oxalosis requiring renal replacement therapy,” Clinical Journal of the American Society of Nephrology, vol. 7, no. 3, pp. 458–465, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. A. A. Al-Eisa, M. Samhan, and M. Naseef, “End-stage renal disease in Kuwaiti children: an 8-year experience,” Transplantation Proceedings, vol. 36, no. 6, pp. 1788–1791, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Kamoun and R. Lakhoua, “End-stage renal disease of the Tunisian child: epidemiology, etiologies, and outcome,” Pediatric Nephrology, vol. 10, no. 4, pp. 479–482, 1996. View at Publisher · View at Google Scholar · View at Scopus
  21. C. J. Danpure and P. R. Jennings, “Peroxisomal alanine:glyoxylate aminotransferase deficiency in primary hyperoxaluria type I,” FEBS Letters, vol. 201, no. 1, pp. 20–24, 1986. View at Scopus
  22. E. Leumann and B. Hoppe, “The primary hyperoxalurias,” Journal of the American Society of Nephrology, vol. 12, no. 9, pp. 1986–1993, 2001. View at Scopus
  23. K. Nishiyama, G. Berstein, T. Oda, and A. Ichiyama, “Cloning and nucleotide sequence of cDNA encoding human liver serine-pyruvate aminotransferase,” European Journal of Biochemistry, vol. 194, no. 1, pp. 9–18, 1990. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Takada, N. Kaneko, H. Esumi, P. E. Purdue, and C. J. Danpure, “Human peroxisomal L-alanine:glyoxylate aminotransferase. Evolutionary loss of a mitochondrial targeting signal by point mutation of the initiation codon,” Biochemical Journal, vol. 268, no. 2, pp. 517–520, 1990. View at Scopus
  25. T. Oda, T. Funai, and A. Ichiyama, “Generation from a single gene of two mRNAs that encode the mitochondrial and peroxisomal serine:pyruvate aminotransferase of rat liver,” The Journal of Biological Chemistry, vol. 265, no. 13, pp. 7513–7519, 1990. View at Scopus
  26. P. E. Purdue, M. J. Lumb, M. Fox et al., “Characterization and chromosomal mapping of a genomic clone encoding human alanine: glyoxylate aminotransferase,” Genomics, vol. 10, no. 1, pp. 34–42, 1991. View at Publisher · View at Google Scholar · View at Scopus
  27. X. Zhang, S. M. Roe, Y. Hou et al., “Crystal structure of alanine:glyoxylate aminotransferase and the relationship between genotype and enzymatic phenotype in primary hyperoxaluria type 1,” Journal of Molecular Biology, vol. 331, no. 3, pp. 643–652, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Ghosh and J. M. Berg, “A proteome-wide perspective on peroxisome targeting signal 1(PTS1)-Pex5p affinities,” Journal of the American Chemical Society, vol. 132, no. 11, pp. 3973–3979, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. P. A. J. Huber, G. M. Birdsey, M. J. Lumb et al., “Peroxisomal import of human alanine:glyoxylate aminotransferase requires ancillary targeting information remote from its C terminus,” The Journal of Biological Chemistry, vol. 280, no. 29, pp. 27111–27120, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Fodor, J. Wolf, R. Erdmann, W. Schliebs, and M. Wilmanns, “Molecular requirements for peroxisomal targeting of alanine-glyoxylate aminotransferase as an essential determinant in primary hyperoxaluria type 1,” PLoS Biology, vol. 10, no. 4, Article ID e1001309, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. E. L. Williams, C. Acquaviva, A. Amoroso et al., “Primary hyperoxaluria type 1: update and additional mutation analysis of the AGXT gene,” Human Mutation, vol. 30, no. 6, pp. 910–917, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Williams and G. Rumsby, “Selected exonic sequencing of the AGXT gene provides a genetic diagnosis in 50% of patients with primary hyperoxaluria type I,” Clinical Chemistry, vol. 53, no. 7, pp. 1216–1221, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. C. J. Danpure and G. Rumsby, “Molecular aetiology of primary hyperoxaluria and its implications for clinical management,” Expert Reviews in Molecular Medicine, vol. 6, no. 1, pp. 1–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Santana, E. Salido, A. Torres, and L. J. Shapiro, “Primary hyperoxaluria type 1 in the Canary Islands: a conformational disease due to I244T mutation in the P11L-containing alanine:glyoxylate aminotransferase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 12, pp. 7277–7282, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. C. J. Danpure, P. R. Jennings, P. Fryer, P. E. Purdue, and J. Allsop, “Primary hyperoxaluria type 1: genotypic and phenotypic heterogeneity,” Journal of Inherited Metabolic Disease, vol. 17, no. 4, pp. 487–499, 1994. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Nishiyama, T. Funai, S. Yokota, and A. Ichiyama, “ATP-dependent degradation of a mutant serine:pyruvate/alanine:glyoxylate aminotransferase in a primary hyperoxaluria type 1 case,” Journal of Cell Biology, vol. 123, no. 5, pp. 1237–1248, 1993. View at Publisher · View at Google Scholar · View at Scopus
  37. C. J. Danpure, P. J. Cooper, P. J. Wise, and P. R. Jennings, “An enzyme trafficking defect in two patients with primary hyperoxaluria type 1: peroxisomal analine/glyoxylate aminotransferase rerouted to mitochondria,” Journal of Cell Biology, vol. 108, no. 4, pp. 1345–1352, 1989. View at Scopus
  38. C. J. Danpure, P. E. Purdue, P. Fryer et al., “Enzymological and mutational analysis of a complex primary hyperoxaluria type I phenotype involving alanine:glyoxylate aminotransferase peroxisome-to-mitochondrion mistargeting and intraperoxisomal aggregation,” The American Journal of Human Genetics, vol. 53, no. 2, pp. 417–432, 1993. View at Scopus
  39. P. E. Purdue, Y. Takada, and C. J. Danpure, “Identification of mutations associated with peroxisome-to-mitochondrian mistargeting of alanine/glyoxylate aminotransferase in primary hyperoxaluria Type 1,” Journal of Cell Biology, vol. 111, no. 6 I, pp. 2341–2351, 1990. View at Publisher · View at Google Scholar · View at Scopus
  40. M. J. Lumb and C. J. Danpure, “Functional synergism between the most common polymorphism in human alanine:glyoxylate aminotransferase and four of the most common disease-causing mutations,” The Journal of Biological Chemistry, vol. 275, no. 46, pp. 36415–36422, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. C. J. Danpure, “Primary hyperoxaluria type 1: AGT mistargeting highlights the fundamental differences between the peroxisomal and mitochondrial protein import pathways,” Biochimica et Biophysica Acta, vol. 1763, no. 12, pp. 1776–1784, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. L. M. Luheshi and C. M. Dobson, “Bridging the gap: from protein misfolding to protein misfolding diseases,” FEBS Letters, vol. 583, no. 16, pp. 2581–2586, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Cellini, R. Montioli, A. Paiardini et al., “Molecular defects of the glycine 41 variants of alanine glyoxylate aminotransferase associated with primary hyperoxaluria type I,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 7, pp. 2896–2901, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Cellini, R. Montioli, and C. B. Voltattorni, “Human liver peroxisomal alanine:glyoxylate aminotransferase: characterization of the two allelic forms and their pathogenic variants,” Biochimica et Biophysica Acta, vol. 1814, no. 11, pp. 1577–1584, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Pirulli, M. Marangella, and A. Amoroso, “Primary hyperoxaluria: genotype-phenotype correlation,” Journal of Nephrology, vol. 16, no. 2, pp. 297–309, 2003. View at Scopus
  46. G. Rumsby, E. Williams, and M. Coulter-Mackie, “Evaluation of mutation screening as a first line test for the diagnosis of the primary hyperoxalurias,” Kidney International, vol. 66, no. 3, pp. 959–963, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Hoppe, C. J. Danpure, G. Rumsby et al., “A vertical (pseudodominant) pattern of inheritance in the autosomal recessive disease primary hyperoxaluria type 1: lack of relationship between genotype, enzymic phenotype, and disease severity,” The American Journal of Kidney Diseases, vol. 29, no. 1, pp. 36–44, 1997. View at Scopus
  48. N. Mesa-Torres, I. Fabelo-Rosa, D. Riverol, et al., “The role of protein denaturation energetics and molecular chaperones in the aggregation and mistargeting of mutants causing primary hyperoxaluria type I,” PLoS ONE. In press.
  49. S. Djordjevic, X. Zhang, M. Bartlam, S. Ye, Z. Rao, and C. J. Danpure, “Structural implications of a G170R mutation of alanine:glyoxylate aminotransferase that is associated with peroxisome-to-mitochondrion mistargeting,” Acta Crystallographica F, vol. 66, no. 3, pp. 233–236, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Albert, C. Yunta, R. Arranz et al., “Structure of GroEL in complex with an early folding intermediate of alanine glyoxylate aminotransferase,” The Journal of Biological Chemistry, vol. 285, no. 9, pp. 6371–6376, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. W. E. Balch, R. I. Morimoto, A. Dillin, and J. W. Kelly, “Adapting proteostasis for disease intervention,” Science, vol. 319, no. 5865, pp. 916–919, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. E. T. Powers, R. I. Morimoto, A. Dillin, J. W. Kelly, and W. E. Balch, “Biological and chemical approaches to diseases of proteostasis deficiency,” Annual Review of Biochemistry, vol. 78, pp. 959–991, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. F. U. Hartl, A. Bracher, and M. Hayer-Hartl, “Molecular chaperones in protein folding and proteostasis,” Nature, vol. 475, no. 7356, pp. 324–332, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. R. I. Morimoto, “Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging,” Genes and Development, vol. 22, no. 11, pp. 1427–1438, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. B. Cellini, A. Lorenzetto, R. Montioli, E. Oppici, and C. B. Voltattorni, “Human liver peroxisomal alanine:glyoxylate aminotransferase: different stability under chemical stress of the major allele, the minor allele, and its pathogenic G170R variant,” Biochimie, vol. 92, no. 12, pp. 1801–1811, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. E. D. Hopper, A. M. C. Pittman, M. C. Fitzgerald, and C. L. Tucker, “In vivo and in vitro examination of stability of primary hyperoxaluria-associated human alanine:glyoxylate aminotransferase,” The Journal of Biological Chemistry, vol. 283, no. 45, pp. 30493–30502, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. A. L. Pey, E. Salido, and J. M. Sanchez-Ruiz, “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, vol. 41, no. 5, pp. 1233–1245, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. M. B. Coulter-Mackie, Q. Lian, and S. G. Wong, “Overexpression of human alanine:glyoxylate aminotransferase in Escherichia coli: renaturation from guanidine-HCl and affinity for pyridoxal phosphate co-factor,” Protein Expression and Purification, vol. 41, no. 1, pp. 18–26, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Oppici, R. Montioli, A. Lorenzetto, S. Bianconi, C. B. Voltattorni, and B. Cellini, “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,” Molecular Genetics and Metabolism, vol. 105, no. 1, pp. 132–140, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. A. M. Pittman, M. D. Lage, V. Poltoratsky et al., “Rapid profiling of disease alleles using a tunable reporter of protein misfolding,” Genetics, vol. 192, no. 3, pp. 831–842, 2012. View at Publisher · View at Google Scholar
  61. J. M. Sanchez-Ruiz, “Protein kinetic stability,” Biophysical Chemistry, vol. 148, no. 1–3, pp. 1–15, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. B. Cellini, R. Montioli, A. Paiardini, A. Lorenzetto, and C. B. Voltattorni, “Molecular insight into the synergism between the minor allele of human liver peroxisomal alanine:glyoxylate aminotransferase and the F1521 mutation,” The Journal of Biological Chemistry, vol. 284, no. 13, pp. 8349–8358, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. C. G. Monico, S. Rossetti, J. B. Olson, and D. S. Milliner, “Pyridoxine effect in type I primary hyperoxaluria is associated with the most common mutant allele,” Kidney International, vol. 67, no. 5, pp. 1704–1709, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. C. S. van Woerden, J. W. Groothoff, F. A. Wijburg, C. Annink, R. J. A. Wanders, and H. R. Waterham, “Clinical implications of mutation analysis in primary hyperoxaluria type 1,” Kidney International, vol. 66, no. 2, pp. 746–752, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. M. L. di Salvo, R. Contestabile, and M. K. Safo, “Vitamin B6 salvage enzymes: mechanism, structure and regulation,” Biochimica et Biophysica Acta, vol. 1814, no. 11, pp. 1597–1608, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Park and S. Marqusee, “Probing the high energy states in proteins by proteolysis,” Journal of Molecular Biology, vol. 343, no. 5, pp. 1467–1476, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. M. B. Coulter-Mackie and Q. Lian, “Consequences of missense mutations for dimerization and turnover of alanine:glyoxylate aminotransferase: study of a spectrum of mutations,” Molecular Genetics and Metabolism, vol. 89, no. 4, pp. 349–359, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. M. B. Coulter-Mackie and Q. Lian, “Partial trypsin digestion as an indicator of mis-folding of mutant alanine:glyoxylate aminotransferase and chaperone effects of specific ligands. Study of a spectrum of missense mutants,” Molecular Genetics and Metabolism, vol. 94, no. 3, pp. 368–374, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Tur-Arlandis, D. Rodriguez-Larrea, B. Ibarra-Molero, and J. M. Sanchez-Ruiz, “Proteolytic scanning calorimetry: a novel methodology that probes the fundamental features of protein kinetic stability,” Biophysical Journal, vol. 98, no. 6, pp. L12–L14, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. C. J. Danpure, “Variable peroxisomal and mitochondrial targeting of alanine: glyoxylate aminotransferase in mammalian evolution and disease,” BioEssays, vol. 19, no. 4, pp. 317–326, 1997. View at Scopus
  71. J. D. Holbrook and C. J. Danpure, “Molecular basis for the dual mitochondrial and cytosolic localization of alanine:glyoxylate aminotransferase in amphibian liver cells,” The Journal of Biological Chemistry, vol. 277, no. 3, pp. 2336–2344, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. G. M. Birdsey, J. Lewin, J. D. Holbrook, V. R. Simpson, A. A. Cunningham, and C. J. Danpure, “A comparative analysis of the evolutionary relationship between diet and enzyme targeting in bats, marsupials and other mammals,” Proceedings of the Royal Society B, vol. 272, no. 1565, pp. 833–840, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Fargue, J. Lewin, G. Rumsby, and C. J. Danpure, “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,” The Journal of Biological Chemistry, vol. 288, no. 4, pp. 2475–2484, 2013. View at Publisher · View at Google Scholar
  74. P. E. Purdue, J. Allsop, G. Isaya, L. E. Rosenberg, and C. J. Danpure, “Mistargeting of peroxisomal L-alanine:glyoxylate aminotransferase to mitochondria in primary hyperoxaluria patients depends upon activation of a cryptic mitochondrial targeting sequence by a point mutation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 23, pp. 10900–10904, 1991. View at Scopus
  75. A. Matouschek, A. Azem, K. Ratliff, B. S. Glick, K. Schmid, and G. Schatz, “Active unfolding of precursor proteins during mitochondrial protein import,” EMBO Journal, vol. 16, no. 22, pp. 6727–6736, 1997. View at Scopus
  76. A. J. Wilcox, J. Choy, C. Bustamante, and A. Matouschek, “Effect of protein structure on mitochondrial import,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 43, pp. 15435–15440, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. J. C. Young, N. J. Hoogenraad, and F. U. Hartl, “Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70,” Cell, vol. 112, no. 1, pp. 41–50, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. H. Yamamoto, K. Fukui, H. Takahashi et al., “Roles of Tom70 in import of presequence-containing mitochondrial proteins,” The Journal of Biological Chemistry, vol. 284, no. 46, pp. 31635–31646, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. M. O. Casanueva, A. Burga, and B. Lehner, “Fitness trade-offs and environmentally induced mutation buffering in isogenic C. elegans,” Science, vol. 335, no. 6064, pp. 82–85, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. F. U. Hartl and M. Hayer-Hartl, “Converging concepts of protein folding in vitro and in vivo,” Nature Structural and Molecular Biology, vol. 16, no. 6, pp. 574–581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. D. W. Neef, M. L. Turski, and D. J. Thiele, “Modulation of heat shock transcription factor 1 as a therapeutic target for small molecule intervention in neurodegenerative disease,” PLoS Biology, vol. 8, no. 1, Article ID e1000291, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. D. S. T. Ong and J. W. Kelly, “Chemical and/or biological therapeutic strategies to ameliorate protein misfolding diseases,” Current Opinion in Cell Biology, vol. 23, no. 2, pp. 231–238, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. B. Calamini, M. C. Silva, F. Madoux et al., “Small-molecule proteostasis regulators for protein conformational diseases,” Nature Chemical Biology, vol. 8, no. 2, pp. 185–196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Prakash and A. Matouschek, “Protein unfolding in the cell,” Trends in Biochemical Sciences, vol. 29, no. 11, pp. 593–600, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. A. J. McClellan, S. Tam, D. Kaganovich, and J. Frydman, “Protein quality control: chaperones culling corrupt conformations,” Nature Cell Biology, vol. 7, no. 8, pp. 736–741, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. H. H. Kampinga and E. A. Craig, “The HSP70 chaperone machinery: J proteins as drivers of functional specificity,” Nature Reviews Molecular Cell Biology, vol. 11, no. 8, pp. 579–592, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. L. Borghi, T. Meschi, F. Amato, A. Briganti, A. Novarini, and A. Giannini, “Urinary volume, water and recurrences in idiopathic calcium nephrolithiasis: a 5-year randomized prospective study,” Journal of Urology, vol. 155, no. 3, pp. 839–843, 1996. View at Publisher · View at Google Scholar · View at Scopus
  88. D. A. Gibbs and R. W. Watts, “The action of pyridoxine in primary hyperoxaluria,” Clinical science, vol. 38, no. 2, pp. 277–286, 1970. View at Scopus
  89. R. W. E. Watts, N. Veall, P. Purkiss, M. A. Mansell, and E. F. Haywood, “The effect of pyridoxine on oxalate dynamics in three cases of primary hyperoxaluria (with glycollic aciduria),” Clinical Science, vol. 69, no. 1, pp. 87–90, 1985. View at Scopus
  90. B. Hoppe, K. Latta, C. von Schnakenburg, and M. J. Kemper, “Primary hyperoxaluria—the German experience,” The American Journal of Nephrology, vol. 25, no. 3, pp. 276–281, 2005. View at Publisher · View at Google Scholar · View at Scopus
  91. B. Hoppe, B. B. Beck, and D. S. Milliner, “The primary hyperoxalurias,” Kidney International, vol. 75, no. 12, pp. 1264–1271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. A. L. Pey, M. Ying, N. Cremades et al., “Identification of pharmacological chaperones as potential therapeutic agents to treat phenylketonuria,” Journal of Clinical Investigation, vol. 118, no. 8, pp. 2858–2867, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. J. Underhaug, O. Aubi, and A. Martinez, “Phenylalanine hydroxylase misfolding and pharmacological chaperones,” Current Topics in Medicinal Chemistry, vol. 12, no. 22, pp. 2534–2545, 2012.
  94. S. Connelly, S. Choi, S. M. Johnson, J. W. Kelly, and I. A. Wilson, “Structure-based design of kinetic stabilizers that ameliorate the transthyretin amyloidoses,” Current Opinion in Structural Biology, vol. 20, no. 1, pp. 54–62, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. D. W. Bolen and G. D. Rose, “Structure and energetics of the hydrogen-bonded backbone in protein folding,” Annual Review of Biochemistry, vol. 77, pp. 339–362, 2008. View at Publisher · View at Google Scholar · View at Scopus