Mass spectrometric analysis of L-Cysteine metabolism: Physiological role and fate of L-Cysteine in the enteric protozoan parasite Entamoeba histolytica

mBio

Volumn 5, Issue 6, 2014, Pages

  Jeelani, Ghulam ^a   Sato, Dan ^b,d   Soga, Tomoyoshi ^b   Watanabe, Haruo ^a   Nozaki, Tomoyoshi ^a,c  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 ETHYL THIAZOLIDINE 4 CARBOXYLIC ACID; 2 METHYL THIAZOLIDINE 4 CARBOXYLIC ACID; 2 THIAZOLIDINE 4 CARBOXYLIC ACID; ALANINE; ALDEHYDE DERIVATIVE; CARBOXYLIC ACID; CYSTEINE; REACTIVE OXYGEN METABOLITE; TIMONACIC; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ARTICLE; CAPILLARY ELECTROPHORESIS; CELL PROTECTION; CONTROLLED STUDY; ENTAMOEBA HISTOLYTICA; ENZYME DEGRADATION; IN VIVO STUDY; ISOTOPE LABELING; MASS SPECTROMETRY; MICROBIAL GROWTH; NONHUMAN; OXIDATIVE STRESS; TIME OF FLIGHT MASS SPECTROMETRY; TROPHOZOITE; DNA SEQUENCE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY;

ENTAMOEBA HISTOLYTICA; EUKARYOTA; PROTOZOA;

CYSTEINE; ENTAMOEBA HISTOLYTICA; ISOTOPE LABELING; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; SEQUENCE ANALYSIS, DNA;

EID: 84920911911     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01995-14     Document Type: Article

References (67)

1. Nozaki T, Ali V, Tokoro M. 2005. Sulfur-containing amino acid metabolism in parasitic protozoa. Adv. Parasitol. 60:1–99. http://dx.doi.org/10.1016/S0065-308X(05)60001-2.
2. Kessler D. 2006. Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30:825–840. http://dx.doi.org/10.1111/j.1574-6976.2006.00036.x.
3. Beinert H, Holm RH, Münck E. 1997. Iron-sulfur clusters: nature’s modular, multipurpose structures. Science 277:653–659. http://dx.doi.org/10.1126/science.277.5326.653.
4. Park S, Imlay JA. 2003. High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J. Bacteriol. 185: 942–950. http://dx.doi.org/10.1128/JB.185.6.1942-1950.2003.
5. Stipanuk MH, Dominy JE, Jr, Lee JI, Coloso RM. 2006. Mammalian cysteine metabolism: new insights into regulation of cysteine metabolism. J. Nutr. 136:1652S–1659S.
6. Stanley SL, Jr.. 2003. Amoebiasis. Lancet 361:1025–1034. http://dx.doi.org/10.1016/S0140-6736(03)12830-9.
7. Weinbach EC, Diamond LS. 1974. Entamoeba histolytica. I. Aerobic metabolism. Exp. Parasitol. 35:232–243. http://dx.doi.org/10.1016/0014-4894(74)90027-7.
8. Mehlotra RK. 1996. Antioxidant defense mechanisms in parasitic protozoa. Crit. Rev. Microbiol. 22:295–314. http://dx.doi.org/10.3109/10408419609105484.
9. Fahey RC, Newton GL, Arrick B, Overdank-Bogart T, Aley SB. 1984. Entamoeba histolytica: a eukaryote without glutathione metabolism. Science 224:70–72. http://dx.doi.org/10.1126/science.6322306.
10. Gillin FD, Diamond LS. 1981. Entamoeba histolytica and Giardia lamblia: effects of cysteine and oxygen tension on trophozoite attachment to glass and survival in culture media. Exp. Parasitol. 52:9–17. http://dx.doi.org/10.1016/0014-4894(81)90055-2.
11. Jeelani G, Husain A, Sato D, Ali V, Suematsu M, Soga T, Nozaki T. 2010. Two atypical L-cysteine-regulated NADPH-dependent oxidoreductases involved in redox maintenance, L-cystine and iron reduction, and metronidazole activation in the enteric protozoan Entamoeba histolytica. J. Biol. Chem. 285:26889–26899. http://dx.doi.org/10.1074/jbc.M110.106310.
12. Husain A, Jeelani G, Sato D, Nozaki T. 2011. Global analysis of gene expression in response to L-cysteine deprivation in the anaerobic protozoan parasite Entamoeba histolytica. BMC Genomics 12:275. http://dx.doi.org/10.1186/1471-2164-12-275.
13. Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, Squares R, Whitehead S, Quail MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillén N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, El- Sayed NM, Petri WA, Jr, Clark CG, Embley TM, Barrell B, Fraser CM, Hall N. 2005. The genome of the protist. Parasite Entamoeba histolytica. Nature 433:865–868. http://dx.doi.org/10.1038/nature03291.
14. Tokoro M, Asai T, Kobayashi S, Takeuchi T, Nozaki T. 2003. Identification and characterization of two isoenzymes of methionine γ-lyase from Entamoeba histolytica: a key enzyme of sulfur-amino acid degradation in an anaerobic parasitic protest that lacks forward and reverse transsulfuration pathways. J. Biol. Chem. 278:42717–42727. http://dx.doi.org/10.1074/jbc.M212414200.
15. Sato D, Yamagata W, Harada S, Nozaki T. 2008. Kinetic characterization of methionine gamma-lyases from the enteric protozoan parasite Entamoeba histolytica against physiological substrates and trifluoromethionine, a promising lead compound against amoebiasis. FEBS J. 275:548–560. http://dx.doi.org/10.1111/j.1742-4658.2007.06221.x.
16. Nozaki T, Asai T, Kobayashi S, Ikegami F, Noji M, Saito K, Takeuchi T. 1998. Molecular cloning and characterization of the genes encoding two isoforms of cysteine synthase in the enteric protozoan parasite Entamoeba histolytica. Mol. Biochem. Parasitol. 97:33–44. http://dx.doi.org/10.1016/S0166-6851(98)00129-7.
17. Nozaki T, Asai T, Sanchez LB, Kobayashi S, Nakazawa M, Takeuchi T. 1999. Characterization of the gene encoding serine acetyltransferase, a regulated enzyme of cysteine biosynthesis from the protist parasites Entamoeba histolytica and Entamoeba dispar. Regulation and possible function of the cysteine biosynthetic pathway in Entamoeba. J. Biol. Chem. 274:32445–32452.
18. Husain A, Sato D, Jeelani G, Mi-ichi F, Ali V, Suematsu M, Soga T, Nozaki T. 2010. Metabolome analysis revealed increase in S-methylcysteine and phosphatidylisopropanolamine synthesis upon L-cysteine deprivation in the anaerobic protozoan parasite Entamoeba histolytica. J. Biol. Chem. 285:39160–39170. http://dx.doi.org/10.1074/jbc.M110.167304.
19. Gillin FD, Diamond LS. 1981. Entamoeba histolytica and Giardia lamblia: growth responses to reducing agents. Exp. Parasitol. 51:382–391. http://dx.doi.org/10.1016/0014-4894(81)90125-9.
20. Stipanuk MH. 2004. Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu. Rev. Nutr. 24:539–577. http://dx.doi.org/10.1146/annurev.nutr.24.012003.132418.
21. Ali V, Nozaki T. 2007. Current therapeutics, their problems, and sulfurcontaining- amino-acid metabolism as a novel target against infections by “amitochondriate” protozoan parasites. Clin. Microbiol. Rev. 20: 164–187. http://dx.doi.org/10.1128/CMR.00019-06.
22. Enos-Berlage JL, Downs DM. 1999. Biosynthesis of the pyrimidine moiety of thiamine independent of the PurF enzyme (phosphoribosylpyrophosphate amidotransferase) in Salmonella typhimurium: incorporation of stable isotope-labeled glycine and formate. J. Bacteriol. 181:841–848.
23. Saunders EC, Ng WW, Chambers JM, Ng M, Naderer T, Krömer JO, Likic VA, McConville MJ. 2011. Isotopomer profiling of Leishmania mexicana promastigotes reveals important roles for succinate fermentation and aspartate uptake in tricarboxylic acid cycle (TCA) anaplerosis, glutamate synthesis, and growth. J. Biol. Chem. 286:27706–27717. http://dx.doi.org/10.1074/jbc.M110.213553.
24. Macrae JI, Sheiner L, Nahid A, Tonkin C, Striepen B, McConville MJ. 2012. Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of Toxoplasma gondii. Cell Host Microbe 12:682–692. http://dx.doi.org/10.1016/j.chom.2012.09.013.
25. Cobbold SA, Vaughan AM, Lewis IA, Painter HJ, Camargo N, Perlman DH, Fishbaugher M, Healer J, Cowman AF, Kappe SH, Llinás M. 2013. Kinetic flux profiling elucidates two independent acetyl-CoA biosynthetic pathways in Plasmodium falciparum. J. Biol. Chem. 288:36338–36350. http://dx.doi.org/10.1074/jbc.M113.503557.
26. Creek DJ, Chokkathukalam A, Jankevics A, Burgess KE, Breitling R, Barrett MP. 2012. Stable isotope-assisted metabolomics for network wide metabolic pathway elucidation. Anal. Chem. 84:8442–8447. http://dx.doi.org/10.1021/ac3018795.
27. Eylert E, Schär J, Mertins S, Stoll R, Bacher A, Goebel W, Eisenreich W. 2008. Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol. Microbiol. 69:1008–1017. http://dx.doi.org/10.1111/j.1365-2958.2008.06337.x.
28. Fan TW, Lane AN, Higashi RM, Farag MA, Gao H, Bousamra M, Miller DM. 2009. Altered regulation of metabolic pathways in human lung cancer discerned by 13 C stable isotope-resolved metabolomics (SIRM). Mol. Cancer 8:41. http://dx.doi.org/10.1158/1535-7163.TARG-09-A41.
29. Eylert E, Herrmann V, Jules M, Gillmaier N, Lautner M, Buchrieser C, Eisenreich W, Heuner K. 2010. Isotopologue profiling of Legionella pneumophila. J. Biol. Chem. 285:22232–22243. http://dx.doi.org/10.1074/jbc.M110.128678.
30. Ali V, Shigeta Y, Tokumoto U, Takahashi Y, Nozaki T. 2004. An intestinal parasitic protist, Entamoeba histolytica, possesses a nonredundant nitrogen fixation-like system for iron-sulfur cluster assembly under anaerobic conditions. J. Biol. Chem. 279:16863–16874. http://dx.doi.org/10.1074/jbc.M313314200.
31. Ratner S, Clarke HT. 1937. The action of formaldehyde upon cysteine. J. Am. Chem. Soc. 59:200–209. http://dx.doi.org/10.1021/ja01280a050.
32. Bullock C. 1990. The biochemistry of alcohol metabolism-a brief review. Biochem. Educ. 18:62–66. http://dx.doi.org/10.1016/0307-4412(90)90174-M.
33. Von Wartburg JP. 1987. Acute aldehyde syndrome and chronic aldehydism. Mutat. Res. 186:249–259. http://dx.doi.org/10.1016/0165-1110(87)90007-8.
34. Lo HS, Reeves RE. 1978. Pyruvate-to-ethanol pathway in Entamoeba histolytica. Biochem. J. 171:225–230.
35. Yang W, Li E, Kairong T, Stanley SL, Jr. 1994. Entamoeba histolytica has an alcohol dehydrogenase homologous to the multifunctional adhE gene product of Escherichia coli. Mol. Biochem. Parasitol. 64:253–260. http://dx.doi.org/10.1016/0166-6851(93)00020-A.
36. Zhang WW, Shen PS, Descoteaux S, Samuelson J. 1994. Cloning and expression of the gene for anNADP_-dependent aldehyde dehydrogenase of Entamoeba histolytica. Mol. Biochem. Parasitol. 63:157–161. http://dx.doi.org/10.1016/0166-6851(94)90019-1.
37. Cavallini D, DeMarco C, Mondovi B, Trasarti F. 1956. Studies of the metabolism of thiazolidine carboxylic acid by rat liver homogenate. Biochim. Biophys. Acta 22:558–564.
38. Debey HJ, Mackenzie JB, Mackenzie CG. 1958. The replacement by thiazolidine carboxylic acid of exogenous cystine and cysteine. J. Nutr. 66:607–619.
39. Roquebert J, Dufour P, Ploux D. 1975. Action of sulfur compounds derived from cysteine on the hepatotoxic effects of carbon tetrachloride. Bull. Soc. Pharm. Bordeaux 114:7–11.
40. Siegers CP, Strubelt O, Völpel M. 1978. The antihepatotoxic activity of dithiocarb as compared with six other thio compounds in mice. Arch. Toxicol. 41:79–88. http://dx.doi.org/10.1007/BF00351772.
41. Strubelt O, Siegers CP, Schütt A. 1974. The curative effects of cysteamine, cysteine, and dithiocarb in experimental paracetamol poisoning. Arch. Toxicol. 33:55–64.
42. Peres G, Dumas M. 1972. Liver protecting effects of thiazolidine carboxylic acid with respect to tetracycline. Gazz. Med. Ital. 131:276–282.
43. Mackenzie CG, Harris J. 1957. N-formylcysteine synthesis in mitochondria from formaldehyde and L-cysteine via thiazolidine carboxylic acid. J. Biol. Chem. 227:393–406.
44. Miquel J, Fleming J, Economos AC. 1982. Antioxidants, metabolic rate and aging in Drosophila. Arch. Gerontol. Geriatr. 1:159–165. http://dx.doi.org/10.1016/0167-4943(82)90016-4.
45. Miquel J, Economos AC. 1979. Favorable effects of the antioxidants sodium and magnesium thiazolidine carboxylate on the vitality and life span of Drosophila and mice. Exp. Gerontal 14:279–285.
46. Brugarolas A, Gosalvez M, Gerety RJ. 1980. Treatment of cancer by an inducer of reverse transformation. Lancet ii:68–70.
47. Kurashima Y, Tsuda M, Sugimura T. 1990. Marked formation of thiazolidine-4-carboxylic acid, an effective nitrite trapping agent in vivo, on boiling of dried shiitake mushroom (Lentinus edodes). J. Agric. Food Chem. 38:1945–1949. http://dx.doi.org/10.1021/jf00100a015.
48. Unger L, DeMoss RD. 1966. Metabolism of a proline analogue, L-thiazolidine-4-carboxylic acid, by Escherichia coli. J. Bacteriol. 91: 1564–1569.
49. Elthon TE, Stewart CR. 1984. Effects of the proline analogue l-thiazolidine-4-carboxylic acid on proline metabolism. Plant Physiol. 74: 213–218. http://dx.doi.org/10.1104/74.2.213.
50. Deutch CE. 1992. Oxidation of l-thiazolidine-4-carboxylateby l-proline dehydrogenase in Escherichia coli. J. Gen. Microbiol. 138:1593–1598. http://dx.doi.org/10.1099/00221287-138-8-1593.
51. Lorenzi HA, Puiu D, Miller JR, Brinkac LM, Amedeo P, Hall N, Caler EV. 2010. New assembly, reannotation and analysis of the Entamoeba histolytica genome reveal new genomic features and protein content information. PLoS Negl. Trop Dis. 4:e716. http://dx.doi.org/10.1371/journal.pntd.0000716.
52. Wlodek L, Rommelspacher H, Susilo R, Radomski J, Höfle G. 1993. Thiazolidine derivatives as source of free L-cysteine in rat tissue. Biochem. Pharmacol. 46:1917–1928. http://dx.doi.org/10.1016/0006-2952(93)90632-7.
53. Zuo X, Coombs GH. 1995. Amino acid consumption by the parasitic, amoeboid protists Entamoeba histolytica and E. invadens. FEMS Microbiol. Lett. 130:253–258. http://dx.doi.org/10.1111/j.1574-6968.1995.tb07728.x.
54. Clark CG, Alsmark UC, Tazreiter M, Saito-Nakano Y, Ali V, Marion S, Weber C, Mukherjee C, Bruchhaus I, Tannich E, Leippe M, Sicheritz- Ponten T, Foster PG, Samuelson J, Noël CJ, Hirt RP, Embley TM, Gilchrist CA, Mann BJ, Singh U, Ackers JP, Bhattacharya S, Bhattacharya A, Lohia A, Guillén N, Duchêne M, Nozaki T, Hall N. 2007. Structure and content of the Entamoeba histolytica genome. Adv. Parasitol. 65:51–190. http://dx.doi.org/10.1016/S0065-308X(07)65002-7.
55. Weber HU, Fleming JF, Miquel J. 1982. Thiazolidine-4-carboxylic acid, a physiologic sulfhydryl antioxidant with potential value in geriatric medicine. Arch. Gerontol. Geriatr. 1:299–310. http://dx.doi.org/10.1016/0167-4943(82)90030-9.
56. Diamond LS, Harlow DR, Cunnick CC. 1978. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. R. Soc. Trop. Med. Hyg. 72:431–432. http://dx.doi.org/10.1016/0035-9203(78)90144-X.
57. Jeelani G, Sato D, Husain A, Escueta-de Cadiz A, Sugimoto M, Soga T, Suematsu M, Nozaki T. 2012. Metabolic profiling of the protozoan parasite Entamoeba invadens revealed activation of unpredicted pathway during encystation. PLoS One 7:e37740. http://dx.doi.org/10.1371/journal.pone.0037740.
58. Ohashi Y, Hirayama A, Ishikawa T, Nakamura S, Shimizu K, Ueno Y, Tomita M, Soga T. 2008. Depiction of metabolome changes in histidinestarved Escherichia coli by ce-TOFMS. Mol. Biosyst. 4:135–147. http://dx.doi.org/10.1039/b714176a.
59. Soga T, Heiger DN. 2000. Amino acid analysis by capillary electrophoresis electrospray ionization mass spectrometry. Anal. Chem. 72: 1236–1241. http://dx.doi.org/10.1021/ac990976y.
60. Soga T, Ueno Y, Naraoka H, Ohashi Y, Tomita M, Nishioka T. 2002. Simultaneous determination of anionic intermediates for Bacillus subtilis metabolic pathways by capillary electrophoresis electrospray ionization mass spectrometry. Anal. Chem. 74:2233–2239. http://dx.doi.org/10.1021/ac020064n.
61. Soga T, Igarashi K, Ito C, Mizobuchi K, Zimmermann HP, Tomita M. 2009. Metabolomic profiling of anionic metabolites by CE-MS. Anal. Chem. 81:6165–6174. http://dx.doi.org/10.1021/ac900675k.
62. Sugimoto M, Wong DT, Hirayama A, Soga T, Tomita M. 2010. Capillary electrophoresis mass spectrometry-based saliva metabolomics identified oral, breast and pancreatic cancer-specific profiles. Metabolomics 6:78–95. http://dx.doi.org/10.1007/s11306-009-0178-y.
63. Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G. 2006. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 78: 779–787. http://dx.doi.org/10.1021/ac051437y.
64. Baran R, Kochi H, Saito N, Suematsu M, Soga T, Nishioka T, Robert M, Tomita M. 2006. MathDAMP: a package for differential analysis of metabolite profiles. BMC Bioinformatics 7:530. http://dx.doi.org/10.1186/1471-2105-7-530.
65. Soga T, Baran R, Suematsu M, Ueno Y, Ikeda S, Sakurakawa T, Kakazu Y, Ishikawa T, Robert M, Nishioka T, Tomita M. 2006. Differential metabolomics reveals ophthalmic acid as an oxidative stress biomarker indicating hepatic glutathione consumption. J. Biol. Chem. 281: 16768–16776. http://dx.doi.org/10.1074/jbc.M601876200.
66. Gaitonde MK. 1967. A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem. J. 104:627–633.
67. Jeelani G, Husain A, Sato D, Soga T, Suematsu M, Nozaki T. 2013. Biochemical and functional characterization of novel NADHkinase in the enteric protozoan parasite Entamoeba histolytica. Biochimie 95:309–319. http://dx.doi.org/10.1016/j.biochi.2012.09.034.