Quality control in tRNA charging - editing of homocysteine

• Autorzy: Jakubowski H.
• Języki publikacji: EN

Abstrakty

EN

 All living organisms conduct protein synthesis with a high degree of accuracy maintained in the transmission and flow of information from a gene to protein product. One crucial "quality control" point in maintaining a high level of accuracy is the selectivity by which aminoacyl-tRNA synthetases furnish correctly activated amino acids, attached to tRNA species, as the building blocks for growing protein chains. When differences in binding energies of amino acids to an aminoacyl-tRNA synthetase are inadequate, editing is used as a major determinant of enzyme selectivity. Some incorrect amino acids are edited at the active site before the transfer to tRNA (pre-transfer editing), while others are edited after transfer to tRNA at a separate editing site (post-transfer editing). Access of natural non-protein amino acids, such as homocysteine, homoserine, or ornithine to the genetic code is prevented by the editing function of aminoacyl-tRNA synthetases. Disabling editing function leads to tRNA mischarging errors and incorporation of incorrect amino acids into protein, which is detrimental to cell homeostasis and inhibits growth. Continuous homocysteine editing by methionyl-tRNA synthetase, resulting in the synthesis of homocysteine thiolactone, is part of the process of tRNA aminoacylation in living organisms, from bacteria to man. Excessive homocysteine thiolactone synthesis in hyperhomocysteinemia caused by genetic or nutritional deficiencies is linked to human vascular and neurological diseases.

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2011
• Tom: 58
• Numer: 2
• Opis fizyczny: p.149-163,fig.,ref.

Twórcy

autor

Jakubowski H.

• UMDNJ-New Jersey Medical School, Department of Microbiology and Molecular Genetics, International Center for Public Health, Newark, USA

Bibliografia

• Ahel I, Stathopoulos C, Ambrogelly A, Sauerwald A, Toogood H, Hartsch T, Soll D (2002) Cysteine activation is an inherent in vitro property of prolyl-tRNA synthetases. J Biol Chem 277: 34743-34748. 
• Ahel I, Korencic D, Ibba M, Soll D (2003) Trans-editing of mischarged tRNAs. Proc Natl Acad Sci USA 100: 15422-15427. 
• Baldwin AN , Berg P (1966) Transfer ribonucleic acid-induced hydrolysis of valyladenylate bound to isoleucyl ribonucleic acid synthetase J Biol Chem 241: 839-845. 
• Beebe K, Ribas L, De Pouplana, Schimmel P (2003) Elucidation of tRNA-dependent editing by a class II tRNA synthetase and significance for cell viability. EMBO J 22: 668-675. 
• Beebe K, Mock M, Merriman E, Schimmel P (2008) Distinct domains of tRNA synthetase recognize the same base pair. Nature 451: 90-93. 
• Bhattacharyya T, Nicholls SJ, Topol EJ, Zhang RL, Yang X, Schmitt D, Fu XM, Shao MY, Brennan DM, Ellis SG, Brennan ML, Allayee H, Lusis AJ, Hazen SL (2008) Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk. J Am Med Ass 299: 1265-1276. 
• Bonaa KH, Njolstad I, Ueland PM, Schirmer H, Tverdal A, Steigen T, Wang H, Nordrehaug JE, Arnesen E, Rasmussen K (2006) Homocysteine lowering and cardiovascular events after acute myocardial infarction. N Engl J Med 354: 1578-1588. 
• Boniecki MT, Vu MT, Betha AK, Martinis SA (2008) CP1-dependent partitioning of pretransfer and posttransfer editing in leucyl-tRNA synthetase. Proc Natl Acad Sci USA 105: 19223-19228. 
• Borowczyk K, Tisonczyk J, Jakubowski H (2011) Changes in Homocysteine Thiolactone Disposition and Neurotoxicity in Bleomycin Hydrolase (Blmh) and Paraoxonase 1 (Pon1) Knock-out Mice. 8th International Conference on Homocysteine Metabolism Lisbon Portugal.
• Bromme D, Rossi AB, Smeekens SP, Anderson DC, Payan DG (1996) Human bleomycin hydrolase: molecular cloning sequencing functional expression and enzymatic characterization. Biochemistry 35: 6706-6714. 
• Brosnan JT, Jacobs RL, Stead LM, Brosnan ME (2004) Methylation demand: a key determinant of homocysteine metabolism. Acta Biochim Pol 51: 405-413. 
• Calendar R, Berg P (1967) D-Tyrosyl RNA: formation hydrolysis and utilization for protein synthesis. J Mol Biol 26: 39-54. 
• Chong YE, Yang XL, Schimmel P (2008) Natural homolog of tRNA synthetase editing domain rescues conditional lethality caused by mistranslation. J Biol Chem 283: 30073-30078. 
• Chwatko G, Jakubowski H (2005) Urinary excretion of homocysteine-thiolactone in humans. Clin Chem 51: 408-415. 
• Chwatko G, Boers GH, Strauss KA, Shih DM, Jakubowski H (2007) Mutations in methylenetetrahydrofolate reductase or cystathionine beta-synthase gene or a high-methionine diet increase homocysteine thiolactone levels in humans and mice. Faseb J 21: 1707-1713. 
• Cilia La Corte AL, Ali M, Głowacki R, Jakubowski H, Ridger V, Pease R, Scott J, Ariëns RA, Philippou H (2011) In vivo homocysteinylation of fibrinogen and its role in thrombosis. In: 23rd Congress of the ISTH Kyoto Japan.
• Dock-Bregeon A, Sankaranarayanan R, Romby P, Caillet J, Springer M, Rees B, Francklyn CS, Ehresmann C, Moras D (2000) Transfer RNA-mediated editing in threonyl-tRNA synthetase. The class II solution to the double discrimination problem. Cell 103: 877-884. 
• Domagała TB, Łacinski M, Trzeciak WH, Mackness MI, Jakubowski H (2006) The correlation of homocysteine-thiolactonase activity of the paraoxonase (PON1) protein with coronary heart disease status. Cell Mol Biol (Noisy-le-grand) 52: 4-10. 
• Doring V, Mootz HD, Nangle LA, Hendrickson TL, de Crecy-Lagard V, Schimmel P, Marliere P (2001) Enlarging the amino acid set of Escherichia coli by infiltration of the valine coding pathway. Science 292: 501-504. 
• Dulic M, Cvetesic N, Perona JJ, Gruic-Sovulj I (2010) Partitioning of tRNA-dependent editing between pre- and post-transfer pathways in class I aminoacyl-tRNA synthetases. J Biol Chem 285: 23799-23809. 
• Dwivedi S, Kruparani SP, Sankaranarayanan R (2005) A d-amino acid editing module coupled to the translational apparatus in archaea. Nat Struct Mol Biol 12: 556-557. 
• Ebbing M, Bonaa KH, Arnesen E, Ueland PM, Nordrehaug JE, Rasmussen K, Njolstad I, Nilsen DW, Refsum H, Tverdal A, Vollset SE, Schirmer H, Bleie O, Steigen T, Midttun O, Fredriksen A, Pedersen ER, Nygard O (2010) Combined analyses and extended follow-up of two randomized controlled homocysteine-lowering B-vitamin trials. J Intern Med 268: 367-382. 
• Eldred EW, Schimmel PR (1972) Rapid deacylation by isoleucyl transfer ribonucleic acid synthetase of isoleucine-specific transfer ribonucleic acid aminoacylated with valine. J Biol Chem 247: 2961-2964. 
• Ferretti G, Bacchetti T, Moroni C, Vignini A, Nanetti L, Curatola G (2004) Effect of homocysteinylation of low density lipoproteins on lipid peroxidation of human endothelial cells. J Cell Biochem 92: 351-360. 
• Ferri-Fioni ML, Schmitt E, Soutourina J, Plateau P, Mechulam Y, Blanquet S (2001) Structure of crystalline d-Tyr-tRNA(Tyr) deacylase A representative of a new class of tRNA-dependent hydrolases. J Biol Chem 276: 47285-47290. 
• Fersht AR (1977) Editing mechanisms in protein synthesis. Rejection of valine by the isoleucyl-tRNA synthetase. Biochemistry 16: 1025-1030. 
• Fersht AR (1986) The chargimg of tRNA. In: Accuracy in Molecular Processes; pp 68-82, London New York: Chapman, Hall.
• Fersht AR (2000) Structure and mechansim in protein science. WH Freeman and Company New York.
• Fersht AR, Kaethner MM (1976) Enzyme hyperspecificity. Rejection of threonine by the valyl-tRNA synthetase by misacylation and hydrolytic editing. Biochemistry 15: 3342-3346. 
• Fersht AR, Dingwall C (1979) Establishing the misacylation/deacylation of the tRNA pathway for the editing mechanism of prokaryotic and eukaryotic valyl-tRNA synthetases. Biochemistry 18: 1238-1245. 
• Francklyn CS (2008) DNA polymerases and aminoacyl-tRNA synthetases: shared mechanisms for ensuring the fidelity of gene expression. Biochemistry 47: 11695-11703. 
• Glowacki R, Jakubowski H (2004) Cross-talk between Cys34 and lysine residues in human serum albumin revealed by N-homocysteinylation. J Biol Chem 279: 10864-10871. 
• Glushchenko AV, Jacobsen DW (2007) Molecular targeting of proteins by l-homocysteine: mechanistic implications for vascular disease. Antioxid Redox Signal 9: 1883-1898. 
• Gruic-Sovulj I, Uter N Bullock T, Perona JJ (2005) tRNA-dependent aminoacyl-adenylate hydrolysis by a nonediting class I aminoacyl-tRNA synthetase. J Biol Chem 280: 23978-23986. 
• Gruic-Sovulj I, Rokov-Plavec J, Weygand-Durasevic I (2007) Hydrolysis of non-cognate aminoacyl-adenylates by a class II aminoacyl-tRNA synthetase lacking an editing domain. FEBS Lett 581: 5110-5114. 
• Gu W, Lu J, Yang G, Dou J, Mu Y, Meng J, Pan C (2008) Plasma homocysteine thiolactone associated with risk of macrovasculopathy in Chinese patients with type 2 diabetes mellitus. Adv Ther 25: 914-924. 
• Hale SP, Schimmel P (1996) Protein synthesis editing by a DNA aptamer. Proc Natl Acad Sci USA 93: 2755-2758. 
• Hale SP, Auld DS, Schmidt E, Schimmel P (1997) Discrete determinants in transfer RNA for editing and aminoacylation. Science 276: 1250-1252. 
• Hendrickson TL, Nomanbhoy TK, Schimmel P (2000) Errors from selective disruption of the editing center in a tRNA synthetase. Biochemistry 39: 8180-8186. 
• Hussain T, Kamarthapu V, Kruparani SP, Deshmukh MV, Sankaranarayanan R (2010) Mechanistic insights into cognate substrate discrimination during proofreading in translation. Proc Natl Acad Sci USA 107: 22117-22121. 
• Ibba M, Soll D (1999) Quality control mechanisms during translation. Science 286: 1893-1897. 
• Ibba M, Soll D (2000) Aminoacyl-tRNA synthesis. Annu Rev Biochem 69: 617-650. 
• Igloi GL, von der Haar F, Cramer F (1978) Aminoacyl-tRNA synthetases from yeast: generality of chemical proofreading in the prevention of misaminoacylation of tRNA. Biochemistry 17: 3459-3468. 
• Jakubowski H (1980) Valyl-tRNA synthetase form yellow lupin seeds: hydrolysis of the enzyme-bound noncognate aminoacyl adenylate as a possible mechanism of increasing specificity of the aminoacyl-tRNA synthetase. Biochemistry 19: 5071-5078. 
• Jakubowski H (1990) Proofreading in vivo: editing of homocysteine by methionyl-tRNA synthetase in Escherichia coli. Proc Natl Acad Sci USA 87: 4504-4508. 
• Jakubowski H (1991) Proofreading in vivo: editing of homocysteine by methionyl-tRNA synthetase in the yeast Saccharomyces cerevisiae. Embo J 10: 593-598. 
• Jakubowski H (1995a) Proofreading in vivo. Editing of homocysteine by aminoacyl-tRNA synthetases in Escherichia coli. J Biol Chem 270: 17672-17673. 
• Jakubowski H (1995b) Synthesis of cysteine-containing dipeptides by aminoacyl-tRNA synthetases. Nucleic Acids Res 23: 4608-4615. 
• Jakubowski H (1996a) Proofreading in trans by an aminoacyl-tRNA synthetase: a model for single site editing by isoleucyl-tRNA synthetase. Nucleic Acids Res 24: 2505-2510. 
• Jakubowski H (1996b) The synthetic/editing active site of an aminoacyl-tRNA synthetase: evidence for binding of thiols in the editing subsite. Biochemistry 35: 8252-8259. 
• Jakubowski H (1997a) Aminoacyl thioester chemistry of class II aminoacyl-tRNA synthetases. Biochemistry 36: 11077-11085. 
• Jakubowski H (1997b) Metabolism of homocysteine thiolactone in human cell cultures. Possible mechanism for pathological consequences of elevated homocysteine levels. J Biol Chem 272: 1935-1942. 
• Jakubowski H (1998) Aminoacylation of coenzyme A and pantetheine by aminoacyl-tRNA synthetases: possible link between noncoded and coded peptide synthesis. Biochemistry 37: 5147-5153. 
• Jakubowski H (1999a) Misacylation of tRNALys with noncognate amino acids by lysyl-tRNA synthetase. Biochemistry 38: 8088-8093. 
• Jakubowski H (1999b) Protein homocysteinylation: possible mechanism underlying pathological consequences of elevated homocysteine levels. Faseb J 13: 2277-2283. 
• Jakubowski H (2000a) Amino acid selectivity in the aminoacylation of coenzyme A and RNA minihelices by aminoacyl-tRNA synthetases. J Biol Chem 275: 34845-34848. 
• Jakubowski H (2000b) Calcium-dependent human serum homocysteine thiolactone hydrolase A protective mechanism against protein N-homocysteinylation. J Biol Chem 275: 3957-3962. 
• Jakubowski H (2000c) Translational incorporation of S-nitrosohomocysteine into protein. J Biol Chem 275: 21813-21816. 
• Jakubowski H (2001a) Biosynthesis and reactions of homocysteine thiolactone. In: Homocysteine in Health and Disease. Jacobson D, Carmel R, eds, pp 21-31. Cambridge University Press, Cambridge UK.
• Jakubowski H (2001b) Translational accuracy of aminoacyl-tRNA synthetases: implications for atherosclerosis. J Nutr 131: 2983S-2987S. 
• Jakubowski H (2002a) From accuracy of protein synthesis to cardiovascular disease: The role of homocysteine. Biotechnologia (Poznan) 58: 11-24.
• Jakubowski H (2002b) Homocysteine is a protein amino acid in humans. Implications for homocysteine-linked disease. J Biol Chem 277: 30425-30428. 
• Jakubowski H (2004) Molecular basis of homocysteine toxicity in humans. Cell Mol Life Sci 61: 470-487. 
• Jakubowski H (2005a) Accuracy of aminoacyl-tRNA synthetases: proofreading of amino acids. In: The Aminoacyl-tRNA Synthetases. Ibba M, Francklyn C, Cusack S, eds. pp 384-396. Georgetown TX: Landes Bioscience/Eurekah.com.
• Jakubowski H (2005b) Anti-N-homocysteinylated protein autoantibodies and cardiovascular disease. Clin Chem Lab Med 43: 1011-1014. 
• Jakubowski H (2006) Mechanism of the condensation of homocysteine thiolactone with aldehydes. Chemistry 12: 8039-8043. 
• Jakubowski H (2007) The molecular basis of homocysteine thiolactone-mediated vascular disease. Clin Chem Lab Med 45: 1704-1716. 
• Jakubowski H (2008) The pathophysiological hypothesis of homocysteine thiolactone-mediated vascular disease. J Physiol Pharmacol 59 (Suppl 9): 155-167. 
• Jakubowski H, Fersht AR (1981) Alternative pathways for editing non-cognate amino acids by aminoacyl-tRNA synthetases. Nucleic Acids Res 9: 3105-3117. 
• Jakubowski H, Goldman E (1992) Editing of errors in selection of amino acids for protein synthesis. Microbiol Rev 56: 412-429. 
• Jakubowski H, Goldman E (1993) Synthesis of homocysteine thiolactone by methionyl-tRNA synthetase in cultured mammalian cells. FEBS Lett 317: 237-240. 
• Jakubowski H, Guranowski A (2003) Metabolism of homocysteine-thiolactone in plants. J Biol Chem 278: 6765-6770. 
• Jakubowski H, Zhang L, Bardeguez A, Aviv A (2000) Homocysteine thiolactone and protein homocysteinylation in human endothelial cells: implications for atherosclerosis. Circ Res 87: 45-51. 
• Jakubowski H, Ambrosius WT, Pratt JH (2001) Genetic determinants of homocysteine thiolactonase activity in humans: implications for atherosclerosis. FEBS Lett 491: 35-39. 
• Jakubowski H, Boers GH, Strauss KA (2008) Mutations in cystathionine beta-synthase or methylenetetrahydrofolate reductase gene increase N-homocysteinylated protein levels in humans. Faseb J 22: 4071-4076. 
• Jakubowski H, Perla-Kajan J, Finnell RH, Cabrera RM, Wang H, Gupta S, Kruger WD, Kraus JP, Shih DM (2009) Genetic or nutritional disorders in homocysteine or folate metabolism increase protein N-homocysteinylation in mice. Faseb J 23: 1721-1727. 
• Kajiya A, Kaji H, Isobe T, Takeda A (2006a) Processing of amyloid beta-peptides by neutral cysteine protease bleomycin hydrolase. Protein Pept Lett 13: 119-123. 
• Kajiya A, Kaji H, Isobe T, Takeda A (2006b) Processing of amyloid beta-peptides by neutral cysteine protease bleomycin hydrolase. Protein Pept Lett 13: 119-123. 
• Kamata Y, Itoh Y, Kajiya A, Karasawa S, Sakatani C, Takekoshi S, Osamura RY, Takeda A (2007) Quantification of neutral cysteine protease bleomycin hydrolase and its localization in rat tissues. J Biochem 141: 69-76. 
• Kamata Y, Taniguchi A, Yamamoto M, Nomura J, Ishihara K, Takahara H, Hibino T, Takeda A (2009) Neutral cysteine protease bleomycin hydrolase is essential for the breakdown of deiminated filaggrin into amino acids. J Biol Chem 284: 12829-12836. 
• Kerkeni M, Tnani M, Chuniaud L, Miled A, Maaroufi K, Trivin F (2006) Comparative study on in vitro effects of homocysteine thiolactone and homocysteine on HUVEC cells: evidence for a stronger proapoptotic and proinflammative homocysteine thiolactone. Mol Cell Biochem 291: 119-126. 
• Kim HY, Ghosh G, Schulman LH, Brunie S, Jakubowski H (1993) The relationship between synthetic and editing functions of the active site of an aminoacyl-tRNA synthetase. Proc Natl Acad Sci USA 90: 11553-11557. 
• Korencic D, Ahel I, Schelert J, Sacher M, Ruan B, Stathopoulos C, Blum P, Ibba M, Soll D (2004) A freestanding proofreading domain is required for protein synthesis quality control in Archaea. Proc Natl Acad Sci USA 101: 10260-10265. 
• Latour P, Thauvin-Robinet C, Baudelet-Mery C, Soichot P, Cusin V, Faivre L, Locatelli MC, Mayencon M, Sarcey A, Broussolle E, Camu W, David A, Rousson R (2010) A major determinant for binding and aminoacylation of tRNA(Ala) in cytoplasmic alanyl-tRNA synthetase is mutated in dominant axonal Charcot-Marie-Tooth disease. Am J Hum Genet 86: 77-82. 
• Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, Cook SA, Davisson MT, Sundberg JP, Schimmel P, Ackerman SL (2006) Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443: 50-55. 
• Lefterov IM, Koldamova RP, Lefterova MI, Schwartz DR, Lazo JS (2001) Cysteine 73 in bleomycin hydrolase is critical for amyloid precursor protein processing. Biochem Biophys Res Commun 283: 994-999. 
• Lentz SR (2005) Mechanisms of homocysteine-induced atherothrombosis. J Thromb Haemost 3: 1646-1654. 
• Lin L, Hale SP, Schimmel P (1996) Aminoacylation error correction. Nature 384: 33-34. 
• Lin SX, Baltzinger M, Remy P (1984) Fast kinetic study of yeast phenylalanyl-tRNA synthetase: role of tRNAPhe in the discrimination between tyrosine and phenylalanine. Biochemistry 23: 4109-4116. 
• Lindahl T, Wood RD (1999) Quality control by DNA repair. Science 286: 1897-1905. 
• Ling J, Reynolds N, Ibba M (2009) Aminoacyl-tRNA synthesis and translational quality control. Annu Rev Microbiol 63: 61-78. 
• Ling J, Soll D (2010) Severe oxidative stress induces protein mistranslation through impairment of an aminoacyl-tRNA synthetase editing site. Proc Natl Acad Sci USA 107: 4028-4033. 
• Lue SW, Kelley SO (2005) An aminoacyl-tRNA synthetase with a defunct editing site. Biochemistry 44: 3010-3016. 
• Luo S, Levine RL (2009) Methionine in proteins defends against oxidative stress. Faseb J 23: 464-472. 
• Maestro de las Casas C, Epeldegui M, Tudela C, Varela-Moreiras G, Perez-Miguelsanz J (2003) High exogenous homocysteine modifies eye development in early chick embryos. Birth Defects Res A Clin Mol Teratol 67: 35-40. 
• Manolescu BN, Oprea E, Farcasanu IC, Berteanu M, Cercasov C (2010) Homocysteine and vitamin therapy in stroke prevention and treatment: a review. Acta Biochim Pol 57: 467-477. 
• Marczak L, Sikora M, Stobiecki M, Jakubowski H (2011) Analysis of site-specific N-homocysteinylation of human serum albumin in vitro and in vivo using MALDI-ToF and LC-MS/MS mass spectrometry. J Proteomics 74: 967-974. 
• Marsillach J, Mackness B, Mackness M, Riu F, Beltran R, Joven J, Camps J (2008) Immunohistochemical analysis of paraoxonases-1, 2, and 3 expression in normal mouse tissues. Free Radic Biol Med 45: 146-157. 
• Martinis SA, Boniecki MT (2010) The balance between pre- and post-transfer editing in tRNA synthetases. FEBS Lett 584: 455-459. 
• Minajigi A, Francklyn CS (2010) Aminoacyl transfer rate dictates choice of editing pathway in threonyl-tRNA synthetase. J Biol Chem 285: 23810-23817. 
• Mocibob M, Ivic N, Bilokapic S, Maier T, Luic M, Ban N, Weygand-Durasevic I (2010) Homologs of aminoacyl-tRNA synthetases acylate carrier proteins and provide a link between ribosomal and nonribosomal peptide synthesis. Proc Natl Acad Sci USA 107: 14585-14590. 
• Mudd SH, Skovby F, Levy HL, Pettigrew KD, Wilcken B, Pyeritz RE, Andria G, Boers GH, Bromberg IL, Cerone R, et al. (1985) The natural history of homocystinuria due to cystathionine beta-synthase deficiency. Am J Hum Genet 37: 1-31. 
• Mudd SH, Levy HL, Krauss JP (2001) Disorders of transsulfuration. In: The metabolic and molecular bases of inherited disease. Scriver C, Beaudet R, Sly AL, Valle WS, Childs D, Kinzler B, Vogelstein B (eds) pp 2007-2056. Mc Graw-Hill, New York.
• Mulvey RS, Fersht AR (1977) Editing mechanisms in aminoacylation of tRNA: ATP consumption and the binding of aminoacyl-tRNA by elongation factor. Biochemistry 16: 4731-4737. 
• Nawaz MH, Merriman E, Yang XL, Schimmel P (2011) p23H implicated as cis/trans regulator of AlaXp-directed editing for mammalian cell homeostasis. Proc Natl Acad Sci USA 108: 2723-2728. 
• Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, Schneider JR, Boone D, Eves EM, Rosner MR, Gibbs JS, Embry A, Dolan B, Das S, Hickman HD, Berglund P, Bennink JR, Yewdell JW, Pan T (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462: 522-526. 
• Nureki O, Vassylyev DG, Tateno M, Shimada A, Nakama T, Fukai S, Konno M, Hendrickson TL, Schimmel P, Yokoyama S (1998) Enzyme structure with two catalytic sites for double-sieve selection of substrate. Science 280: 578-582. 
• Paoli P, Sbrana F, Tiribilli B, Caselli A, Pantera B, Cirri P, De Donatis A, Formigli L, Nosi D, Manao G, Camici G, Ramponi G (2010) Protein N-homocysteinylation induces the formation of toxic amyloid-like protofibrils. J Mol Biol 400: 889-907. 
• Papassotiropoulos A, Bagli M, Jessen F, Frahnert C, Rao ML, Maier W, Heun R (2000) Confirmation of the association between bleomycin hydrolase genotype and Alzheimer's disease. Mol Psychiatry 5: 213-215. 
• Park SG, Schimmel P, Kim S (2008) Aminoacyl tRNA synthetases and their connections to disease. Proc Natl Acad Sci USA 105: 11043-11049. 
• Pauling L (1957) The probability of errors in the process of synthesis of protein molecules In: Festschrift Arthur Stoll, pp 597. Birkhauser Verlag, Basel.
• Perla-Kajan J, Jakubowski H (2010) Paraoxonase 1 protects against protein N-homocysteinylation in humans. Faseb J 24: 931-936. 
• Perla-Kajan J, Marczak L, Kajan L, Skowronek P, Twardowski T, Jakubowski H (2007a) Modification by homocysteine thiolactone affects redox status of cytochrome C. Biochemistry 46: 6225-6231. 
• Perla-Kajan J, Twardowski T, Jakubowski H (2007b) Mechanisms of homocysteine toxicity in humans. Amino Acids 32: 561-572. 
• Perla-Kajan J, Stanger O, Luczak M, Ziolkowska A, Malendowicz LK, Twardowski T, Lhotak S, Austin RC, Jakubowski H (2008) Immunohistochemical detection of N-homocysteinylated proteins in humans and mice. Biomed Pharmacother 62: 473-479. 
• Ribas de Pouplana L, Schimmel P (2001) Operational RNA code for amino acids in relation to genetic code in evolution. J Biol Chem 276: 6881-6884. 
• Roy H, Ling J, Irnov M, Ibba M (2004) Post-transfer editing in vitro and in vivo by the beta subunit of phenylalanyl-tRNA synthetase. EMBO J 23: 4639-4648. 
• Roybal CN, Yang S, Sun CW, Hurtado D, Vander DL, Jagt Townes TM, Abcouwer SF (2004) Homocysteine increases the expression of vascular endothelial growth factor by a mechanism involving endoplasmic reticulum stress and transcription factor ATF4. J Biol Chem 279: 14844-14852. 
• Ruan B, Soll D (2005) The bacterial YbaK protein is a Cys-tRNAPro and Cys-tRNA Cys deacylase. J Biol Chem 280: 25887-25891. 
• Sankaranarayanan R, Moras D (2001) The fidelity of the translation of the genetic code. Acta Biochim Pol 48: 323-335. 
• Sauls DL, Lockhart E, Warren ME, Lenkowski A, Wilhelm SE, Hoffman M (2006) Modification of fibrinogen by homocysteine thiolactone increases resistance to fibrinolysis: a potential mechanism of the thrombotic tendency in hyperhomocysteinemia. Biochemistry 45: 2480-2487. 
• Sauls DL, Warren M, Hoffman M (2011) Homocysteinylated fibrinogen forms disulfide-linked complexes with albumin. Thromb Res 127: 576-581. 
• Schimmel P (2008) Development of tRNA synthetases and connection to genetic code and disease. Protein Sci 17: 1643-1652. 
• Schmidt E, Schimmel P (1994) Mutational isolation of a sieve for editing in a transfer RNA synthetase. Science 264: 265-267. 
• Schmidt E, Schimmel P (1995) Residues in a class I tRNA synthetase which determine selectivity of amino acid recognition in the context of tRNA. Biochemistry 34: 11204-11210. 
• Schulman LH (1991) Recognition of tRNAs by aminoacyl-tRNA synthetases. Prog Nucleic Acid Res Mol Biol 41: 23-87. 
• Schwartz DR, Homanics GE, Hoyt DG, Klein E, Abernethy J, Lazo JS (1999) The neutral cysteine protease bleomycin hydrolase is essential for epidermal integrity and bleomycin resistance. Proc Natl Acad Sci USA 96: 4680-4685. 
• Serre L, Verdon G, Choinowski T, Hervouet N, Risler JL, Zelwer C (2001) How methionyl-tRNA synthetase creates its amino acid recognition pocket upon l-methionine binding. J Mol Biol 306: 863-876. 
• Shih DM, Gu L, Xia YR, Navab M, Li WF, Hama S, Castellani LW, Furlong CE, Costa LG, Fogelman AM, Lusis AJ (1998) Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 394: 284-287. 
• Sibrian-Vazquez M, Escobedo JO, Lim S, Samoei GK, Strongin RM (2010) Homocystamides promote free-radical and oxidative damage to proteins. Proc Natl Acad Sci USA 107: 551-554. 
• Sikora M, Jakubowski H (2009) Homocysteine editing and growth inhibition in Escherichia coli. Microbiology 155: 1858-1865. 
• Sikora M, Marczak L, Twardowski T, Stobiecki M, Jakubowski H (2010) Direct monitoring of albumin lysine-525 N-homocysteinylation in human serum by liquid chromatography/mass spectrometry. Anal Biochem 405: 132-134. 
• Smith AD, Smith SM, de Jager CA, Whitbread P, Johnston C, Agacinski G, Oulhaj A, Bradley KM, Jacoby R, Refsum H (2010) Homocysteine-lowering by B vitamins slows the rate of accelerated brain atrophy in mild cognitive impairment: a randomized controlled trial. PLoS One 5: e12244. 
• Soutourina J, Plateau P, Blanquet S (2000) Metabolism of d-aminoacyl-tRNAs in Escherichia coli and Saccharomyces cerevisiae cells. J Biol Chem 275: 32535-32542. 
• Soutourina O, Soutourina J, Blanquet S, Plateau P (2004) Formation of d-tyrosyl-tRNATyr accounts for the toxicity of d-tyrosine toward Escherichia coli. J Biol Chem 279: 42560-42565. 
• Splan KE, Ignatov ME, Musier-Forsyth K (2008) Transfer RNA modulates the editing mechanism used by class II prolyl-tRNA synthetase. J Biol Chem 283: 7128-7134. 
• Strauss KA, Morton DH, Puffenberger EG, Hendrickson C, Robinson DL, Wagner C, Stabler SP, Allen RH, Chwatko G, Jakubowski H, Niculescu MD, Mudd SH (2007) Prevention of brain disease from severe 5,10-methylenetetrahydrofolate reductase deficiency. Mol Genet Metab 91: 165-175. 
• Stum M, McLaughlin HM, Kleinbrink EL, Miers KE, Ackerman SL, Seburn KL, Antonellis A, Burgess RW (2011) An assessment of mechanisms underlying peripheral axonal degeneration caused by aminoacyl-tRNA synthetase mutations. Mol Cell Neurosci 46: 432-443. 
• Suszynska J, Tisonczyk J, Lee HG, Smith MA, Jakubowski H (2010) Reduced homocysteine-thiolactonase activity in Alzheimer's disease. J Alzheimers Dis 19: 1177-1183. 
• Undas A, Perla J, Lacinski M, Trzeciak W, Kazmierski R, Jakubowski H (2004) Autoantibodies against N-homocysteinylated proteins in humans: implications for atherosclerosis. Stroke 35: 1299-1304. 
• Undas A, Jankowski M, Twardowska M, Padjas A, Jakubowski H, Szczeklik A (2005) Antibodies to N-homocysteinylated albumin as a marker for early-onset coronary artery disease in men. Thromb Haemost 93: 346-350. 
• Undas A, Brozek J, Jankowski M, Siudak Z, Szczeklik A, Jakubowski H (2006a) Plasma homocysteine affects fibrin clot permeability and resistance to lysis in human subjects. Arterioscler Thromb Vasc Biol 26: 1397-1404. 
• Undas A, Stepien E, Glowacki R, Tisonczyk J, Tracz W, Jakubowski H (2006b) Folic acid administration and antibodies against homocysteinylated proteins in subjects with hyperhomocysteinemia. Thromb Haemost 96: 342-347. 
• Wang Z, Tang WH, Cho L, Brennan DM, Hazen SL (2009) Targeted metabolomic evaluation of arginine methylation and cardiovascular risks: potential mechanisms beyond nitric oxide synthase inhibition. Arterioscler Thromb Vasc Biol 29: 1383-1391. 
• Wong FC, Beuning PJ, Silvers C, Musier-Forsyth K (2003) An isolated class II aminoacyl-tRNA synthetase insertion domain is functional in amino acid editing. J Biol Chem 278: 52857-52864. 
• Wydau S, van der Rest G, Aubard C, Plateau P, Blanquet S (2009) Widespread distribution of cell defense against d-aminoacyl-tRNAs. J Biol Chem 284: 14096-14104. 
• Yang X, Gao Y, Zhou J, Zhen Y, Yang Y, Wang J, Song L, Liu Y, Xu H, Chen Z, Hui R (2006) Plasma homocysteine thiolactone adducts associated with risk of coronary heart disease. Clin Chim Acta 364: 230-234. 
• Yao P, Zhu B, Jaeger S, Eriani G, Wang ED (2008) Recognition of tRNALeu by Aquifex aeolicus leucyl-tRNA synthetase during the aminoacylation and editing steps. Nucleic Acids Res 36: 2728-2738. 
• Zabczyk M, Glowacki R, Machnik A, Herod P, Kazek G, Jakubowski H, Undas A (2011) Elevated concentrations of Nɛ-homocysteinyl-lysine isopeptide in acute myocardial infarction: links with ADMA formation. Clin Chem Lab Med 49: 729-735. 
• Zhu B, Yao P, Tan M, Eriani G, Wang ED (2009) tRNA-independent pretransfer editing by class I leucyl-tRNA synthetase. J Biol Chem 284: 3418-3424. 
• Zimny J, Sikora M, Guranowski A, Jakubowski H (2006) Protective mechanisms against homocysteine toxicity: the role of bleomycin hydrolase. J Biol Chem 281: 22485-22492.

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