TAT-Mediated Delivery of Human Alanine:Glyoxylate Aminotransferase in a Cellular Model of Primary Hyperoxaluria Type I

Behnam JT, Williams EL, Brink S, Rumsby G, Danpure CJ (2006) Reconstruction of human hepatocyte glyoxylate metabolic pathways in stably transformed Chinese-hamster ovary cells. Biochem J 394(Pt 2):409–416 Bertoldi M, Cellini B, Clausen T, Voltattorni CB (2002) Spectroscopic and kinetic analyses reveal the pyridoxal 5′-phosphate binding mode and the catalytic features of Treponema denticola cystalysin. Biochemistry 41(29):9153–9164 Caron NJ, Quenneville SP, Tremblay JP (2004) Endosome disruption enhances the functional nuclear delivery of Tat-fusion proteins. Biochem Biophys Res Commun 319(1):12–20. doi:10.1016/j.bbrc.2004.04.180 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(1):39–50. doi:10.1042/BJ20070637 Cellini B, Montioli R, Bianconi S, Lopez-Alonso JP, Voltattorni CB (2008) Construction, purification and characterization of untagged human liver alanine-glyoxylate aminotransferase expressed in Escherichia coli. Protein Pept Lett 15(2):153–159 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(13):8349–8358. doi:10.1074/jbc.M808965200 Cellini B, Lorenzetto A, Montioli R, Oppici E, Voltattorni CB (2010a) 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(12):1801–1811. doi:10.1016/j.biochi.2010.08.005 Cellini B, Montioli R, Paiardini A, Lorenzetto A, Maset F, Bellini T, Oppici E, Voltattorni CB (2010b) Molecular defects of the glycine 41 variants of alanine glyoxylate aminotransferase associated with primary hyperoxaluria type I. Proc Natl Acad Sci USA 107(7):2896–2901. doi:10.1073/pnas.0908565107 Cellini B, Oppici E, Paiardini A, Montioli R (2012) Molecular insights into primary hyperoxaluria type 1 pathogenesis. Front Biosci 17:621–634 Cochat P, Hulton SA, Acquaviva C, Danpure CJ, Daudon M, De Marchi M, Fargue S, Groothoff J, Harambat J, Hoppe B, Jamieson NV, Kemper MJ, Mandrile G, Marangella M, Picca S, Rumsby G, Salido E, Straub M, van Woerden CS, OxalEurope (2012) Primary hyperoxaluria Type 1: indications for screening and guidance for diagnosis and treatment. Nephrol Dial Transplant 27(5):1729–1736. doi:10.1093/ndt/gfs078 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(4):349–359 Coulter-Mackie MB, Lian Q (2008) 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. Mol Genet Metab 94(3):368–374 Coulter-Mackie MB, Lian Q, Applegarth DA, Toone J, Waters PJ, Vallance H (2008) Mutation-based diagnostic testing for primary hyperoxaluria type 1: survey of results. Clin Biochem 41(7–8):598–602. doi:10.1016/j.clinbiochem.2008.01.018 Daidone F, Montioli R, Paiardini A, Cellini B, Macchiarulo A, Giardina G, Bossa F, Borri Voltattorni C (2012) Identification by virtual screening and in vitro testing of human DOPA decarboxylase inhibitors. PLoS One 7(2):e31610. doi:10.1371/journal.pone.0031610 Danpure CJ (2005) Molecular etiology of primary hyperoxaluria type 1: new directions for treatment. Am J Nephrol 25(3):303–310 Danpure CJ, Jennings PR (1986) Peroxisomal alanine:glyoxylate aminotransferase deficiency in primary hyperoxaluria type I. FEBS Lett 201(1):20–24 Danpure CJ, Cooper PJ, Wise PJ, Jennings PR (1989) An enzyme trafficking defect in two patients with primary hyperoxaluria type 1: peroxisomal alanine/glyoxylate aminotransferase rerouted to mitochondria. J Cell Biol 108(4):1345–1352 Danpure CJ, Jennings PR, Fryer P, Purdue PE, Allsop J (1994) Primary hyperoxaluria type 1: genotypic and phenotypic heterogeneity. J Inherit Metab Dis 17(4):487–499 Deegan PB (2012) Fabry disease, enzyme replacement therapy and the significance of antibody responses. J Inherit Metab Dis 35(2):227–243. doi:10.1007/s10545-011-9400-y di Salvo ML, Safo MK, Contestabile R (2012) Biomedical aspects of pyridoxal 5′-phosphate availability. Front Biosci (Elite Ed) 4:897–913 Ferreira GC (1993) Erythroid 5-aminolevulinate synthase and X-linked sideroblastic anemia. J Fla Med Assoc 80(7):481–483 Fittipaldi A, Giacca M (2005) Transcellular protein transduction using the Tat protein of HIV-1. Adv Drug Deliv Rev 57(4):597–608. doi:10.1016/j.addr.2004.10.011 Fittipaldi A, Ferrari A, Zoppe M, Arcangeli C, Pellegrini V, Beltram F, Giacca M (2003) Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J Biol Chem 278(36):34141–34149. doi:10.1074/jbc.M303045200 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(4):e1001309. doi:10.1371/journal.pbio.1001309 Giardina G, Montioli R, Gianni S, Cellini B, Paiardini A, Voltattorni CB, Cutruzzola F (2011) Open conformation of human DOPA decarboxylase reveals the mechanism of PLP addition to Group II decarboxylases. Proc Natl Acad Sci USA 108(51):20514–20519. doi:10.1073/pnas.1111456108 Gump JM, Dowdy SF (2007) TAT transduction: the molecular mechanism and therapeutic prospects. Trends Mol Med 13(10):443–448. doi:10.1016/j.molmed.2007.08.002 Hopper ED, Pittman AM, Fitzgerald MC, Tucker CL (2008) In vivo and in vitro examination of stability of primary hyperoxaluria-associated human alanine:glyoxylate aminotransferase. J Biol Chem 283(45):30493–30502 Humbert O, Davis L, Maizels N (2012) Targeted gene therapies: tools, applications, optimization. Crit Rev Biochem Mol Biol 47(3):264–281. doi:10.3109/10409238.2012.658112 Lumb MJ, Danpure CJ (2000) Functional synergism between the most common polymorphism in human alanine:glyoxylate aminotransferase and four of the most common disease-causing mutations. J Biol Chem 275(46):36415–36422 Mdluli K, Booth MP, Brady RL, Rumsby G (2005) A preliminary account of the properties of recombinant human glyoxylate reductase (GRHPR), LDHA and LDHB with glyoxylate, and their potential roles in its metabolism. Biochim Biophys Acta 1753(2):209–216. doi:10.1016/j.bbapap.2005.08.004 Monico CG, Olson JB, Milliner DS (2005) Implications of genotype and enzyme phenotype in pyridoxine response of patients with type I primary hyperoxaluria. Am J Nephrol 25(2):183–188 Montioli R, Cellini B, Borri Voltattorni C (2011) Molecular insights into the pathogenicity of variants associated with the aromatic amino acid decarboxylase deficiency. J Inherit Metab Dis 34(6):1213–1224. doi:10.1007/s10545-011-9340-6 Montioli R, Fargue S, Lewin J, Zamparelli C, Danpure CJ, Borri Voltattorni C, Cellini B (2012) The N-terminal extension is essential for the formation of the active dimeric structure of liver peroxisomal alanine:glyoxylate aminotransferase. Int J Biochem Cell Biol 44(3):536–546. doi:10.1016/j.biocel.2011.12.007 Motley A, Lumb MJ, Oatey PB, Jennings PR, De Zoysa PA, Wanders RJ, Tabak HF, Danpure CJ (1995) Mammalian alanine/glyoxylate aminotransferase 1 is imported into peroxisomes via the PTS1 translocation pathway. Increased degeneracy and context specificity of the mammalian PTS1 motif and implications for the peroxisome-to-mitochondrion mistargeting of AGT in primary hyperoxaluria type 1. J Cell Biol 131(1):95–109 Muller IB, Wu F, Bergmann B, Knockel J, Walter RD, Gehring H, Wrenger C (2009) Poisoning pyridoxal 5-phosphate-dependent enzymes: a new strategy to target the malaria parasite Plasmodium falciparum. PLoS One 4(2):e4406. doi:10.1371/journal.pone.0004406 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(1):132–140. doi:10.1016/j.ymgme.2011.09.033 Pegg AE, Shantz LM, Coleman CS (1995) Ornithine decarboxylase as a target for chemoprevention. J Cell Biochem Suppl 22:132–138 Pittman AM, Lage MD, Poltoratsky V, Vrana JD, Paiardini A, Roncador A, Cellini B, Hughes RM, Tucker CL (2012) Rapid profiling of disease alleles using a tunable reporter of protein misfolding. Genetics. doi:10.1534/genetics.112.143750 Rapoport M, Salman L, Sabag O, Patel MS, Lorberboum-Galski H (2011) Successful TAT-mediated enzyme replacement therapy in a mouse model of mitochondrial E3 deficiency. J Mol Med (Berl) 89(2):161–170. doi:10.1007/s00109-010-0693-3 Ringe D, Petsko GA (2009) What are pharmacological chaperones and why are they interesting? J Biol 8(9):80 Rucktaschel R, Girzalsky W, Erdmann R (2011) Protein import machineries of peroxisomes. Biochim Biophys Acta 1808(3):892–900. doi:10.1016/j.bbamem.2010.07.020 Salido EC, Li XM, Lu Y, Wang X, Santana A, Roy-Chowdhury N, Torres A, Shapiro LJ, Roy-Chowdhury J (2006) Alanine-glyoxylate aminotransferase-deficient mice, a model for primary hyperoxaluria that responds to adenoviral gene transfer. Proc Natl Acad Sci USA 103(48):18249–18254 Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285(5433):1569–1572 Sloots A, Wels WS (2005) Recombinant derivatives of the human high-mobility group protein HMGB2 mediate efficient nonviral gene delivery. FEBS J 272(16):4221–4236. doi:10.1111/j.1742-4658.2005.04834.x Toro A, Grunebaum E (2006) TAT-mediated intracellular delivery of purine nucleoside phosphorylase corrects its deficiency in mice. J Clin Invest 116(10):2717–2726. doi:10.1172/JCI25052 Toro A, Paiva M, Ackerley C, Grunebaum E (2006) Intracellular delivery of purine nucleoside phosphorylase (PNP) fused to protein transduction domain corrects PNP deficiency in vitro. Cell Immunol 240(2):107–115. doi:10.1016/j.cellimm.2006.07.003 van den Berg A, Dowdy SF (2011) Protein transduction domain delivery of therapeutic macromolecules. Curr Opin Biotechnol 22(6):888–893. doi:10.1016/j.copbio.2011.03.008 Vyas PM, Tomamichel WJ, Pride PM, Babbey CM, Wang Q, Mercier J, Martin EM, Payne RM (2012) A TAT-frataxin fusion protein increases lifespan and cardiac function in a conditional Friedreich’s ataxia mouse model. Hum Mol Genet 21(6):1230–1247. doi:10.1093/hmg/ddr554 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 Wu F, Christen P, Gehring H (2011) A novel approach to inhibit intracellular vitamin B6-dependent enzymes: proof of principle with human and plasmodium ornithine decarboxylase and human histidine decarboxylase. FASEB J 25(7):2109–2122. doi:10.1096/fj.10-174383 Zhang X, Roe SM, Hou Y, Bartlam M, Rao Z, Pearl LH, Danpure CJ (2003) Crystal structure of alanine:glyoxylate aminotransferase and the relationship between genotype and enzymatic phenotype in primary hyperoxaluria type 1. J Mol Biol 331(3):643–652 Zhu W, Lin A, Banerjee R (2008) Kinetic properties of polymorphic variants and pathogenic mutants in human cystathionine gamma-lyase. Biochemistry 47(23):6226–6232. doi:10.1021/bi800351a