Dramatic Increase in Glycerol Biosynthesis upon Oxidative Stress in the Anaerobic Protozoan Parasite Entamoeba histolytica

PLoS Neglected Tropical Diseases

Volumn 6, Issue 9, 2012, Pages

  Husain, Afzal ^a,b,e   Sato, Dan ^c   Jeelani, Ghulam ^a,c   Soga, Tomoyoshi ^c   Nozaki, Tomoyoshi ^a,d  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KEIO UNIVERSITY   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ALCOHOL; CHITIN; GLYCEROL; GLYCEROPHOSPHATE; HYDROGEN PEROXIDE; NUCLEOSIDE TRIPHOSPHATE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE;

ALCOHOL PRODUCTION; AMINO ACID METABOLISM; ARTICLE; BIOSYNTHESIS; CAPILLARY ELECTROPHORESIS; CONTROLLED STUDY; ENERGY METABOLISM; ENTAMOEBA HISTOLYTICA; ENZYME ACTIVITY; GLYCOLYSIS; METABOLIC REGULATION; METABOLITE; METABOLOME; NONHUMAN; NUCLEIC ACID METABOLISM; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; SIGNAL TRANSDUCTION; SPECTROFLUOROMETRY; TIME OF FLIGHT MASS SPECTROMETRY; TROPHOZOITE;

ANIMALS; ELECTROPHORESIS, CAPILLARY; ENTAMOEBA HISTOLYTICA; GLYCEROL; HYDROGEN PEROXIDE; METABOLOME; OXIDATIVE STRESS; PARAQUAT; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STRESS, PHYSIOLOGICAL;

EID: 84866938000     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001831     Document Type: Article

References (64)

1. Imlay JA, (2003) Pathways of oxidative damage. Annu Rev Microbiol 57: 395-418.
2. Apel K, Hirt H, (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399.
3. Perrone GG, Tan SX, Dawes IW, (2008) Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta 1783: 1354-1368.
4. Clement MV, Pervaiz S, (1999) Reactive oxygen intermediates regulate cellular response to apoptotic stimuli: an hypothesis. Free Radic Res 30: 247-252.
5. Nandi N, Sen A, Banerjee R, Kumar S, Kumar V, Ghosh AN, Das P, (2010) Hydrogen peroxide induces apoptosis-like death in Entamoeba histolytica trophozoites. Microbiol 156: 1926-41.
6. Ghosh AS, Dutta S, Raha S, (2010) Hydrogen peroxide-induced apoptosis-like cell death in Entamoeba histolytica. Parasitol Int 59: 166-72.
7. Temple MD, Perrone GG, Dawes IW, (2005) Complex cellular responses to reactive oxygen species. Trends Cell Biol 15: 319-326.
8. Ralser M, Walmelink MM, Kowald A, Gerisch B, Heeren G, et al. (2003) Dynamic re-routing of the carbohydrate flux is key to counteracting oxidative stress. J Biol 6: 10.
9. Stanley SL Jr, (2003) Amoebiasis. Lancet 361: 1025-1034.
10. Weinbach EC, Diamond LS, (1974) Entamoeba histolytica. I. Aerobic metabolism. Exp. Parasitol 35: 232-243.
11. Bogdan C, Rollinghoff M, Diefenbach A, (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12: 64-76.
12. Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, et al. (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433: 865-868.
13. Mehlotra RK, (1996) Antioxidant defense mechanisms in parasitic protozoa. Crit Rev Microbiol 22: 295-314.
14. Fahey RC, Newton GL, Arrick B, Overdank-Bogart T, Aley SB, (1984) Entamoeba histolytica: a eukaryote without glutathione metabolism. Science 224: 70-72.
15. Saraiva LM, Vicente JB, Teixeira M, (2004) The role of the flavodiiron proteins in microbial nitric oxide detoxification. Adv Microb Physiol 49: 77-129.
16. Sen A, Chatterjee NS, Akbar MA, Nandi N, et al. (2007) The 29-kilodalton thiol-dependent peroxidase of Entamoeba histolytica is a factor involved in pathogenesis and survival of the parasite during oxidative stress. Eukaryot Cell 6: 664-673.
17. Jackson JB, (1991) The proton-translocating nicotinamide adenine dinucleotide transhydrogenase. J Bioenerg Biomembr 23: 715-741.
18. Yousuf MA, Mi-ichi F, Nakada-Tsukui K, Nozaki T, (2010) Localization and targeting of an unusual pyridine nucleotide transhydrogenase in Entamoeba histolytica. Eukaryot Cell 9: 926-33.
19. Vicente J, Ehrenkaufer G, Saraiva L, Teixeira M, Singh U, (2008) Entamoeba histolytica modulates a complex repertoire of novel genes in response to oxidative and nitrosative stresses: implications for amebic pathogenesis. Cell Microbiol 11: 51-69.
20. Godon C, Lagniel G, Lee J, Buhler JM, Kieffer S, et al. (1998) The H2O2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273: 22480-224892.
21. Demple B, Amabile-Cuevas CF, (1991) Redox redux: the control of oxidative stress responses. Cell 67: 837-839.
22. Pineda E, Encalada R, Rodríguez-Zavala JS, Olivos-García A, Moreno-Sánchez R, Saavedra E, (2010) Pyruvate:ferredoxin oxidoreductase and bifunctional aldehyde-alcohol dehydrogenase are essential for energy metabolism under oxidative stress in Entamoeba histolytica. FEBS J 277: 3382-3395.
23. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, et al. (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317: 1921-1926.
24. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, et al. (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315: 207-212.
25. Soga T, Baran R, Suematsu M, Ueno Y, Ikeda S, et al. (2006) Differential metabolomics reveals ophthalmic acid as an oxidative stress biomarker indicating hepatic glutathione consumption. J Biol Chem 281: 16768-16776.
26. Sato S, Soga T, Nishioka T, Tomita M, (2004) Simultaneous determination of the main metabolites in rice leaves using capillary electrophoresis mass spectrometry and capillary electrophoresis diode array detection. Plant J 40: 151-163.
27. Soga T, Ohashi Y, Ueno Y, Naraoka H, Tomita M, Nishioka T, (2003) Quantitative metabolome analysis using capillary electrophoresis mass spectrometry. J Proteome Res 2: 488-494.
28. 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.
29. Clark CG, Diamond LS, (2002) Methods for cultivation of luminal parasitic protists of clinical importance. Clin Microbiol Rev 15: 329-341.
30. 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.
31. Jeelani G, Sato D, Husain A, Escueta-de Cadiz A, Sugimoto M, et al. (2012) Metabolic profiling of the protozoan parasite Entamoeba invadens revealed activation of unpredicted pathway during encystation. PLoS ONE 7(5): e37740.
32. Ohashi Y, Hirayama A, Ishikawa T, Nakamura S, Shimizu K, et al. (2008) Depiction of metabolome changes in histidine-starved Escherichia coli by CE-TOFMS. Mol Biosyst 4: 135-147.
33. Soga T, Heiger DN, (2000) Amino acid analysis by capillary electrophoresis electrospray ionization mass spectrometry. Anal Chem 72: 1236-1241.
34. 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.
35. 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.
36. 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.
37. 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: 779-87.
38. Baran R, Kochi H, Saito N, Suematsu M, Soga T, Nishioka T, et al. (2006) MathDAMP: a package for differential analysis of metabolite profiles. BMC Bioinformatics 13: 530.
39. Clark CG, Alsmark UC, Tazreiter M, Saito-Nakano Y, Ali V, Marion S, (2007) Structure and content of the Entamoeba histolytica genome. Adv Parasitol 65: 51-190.
40. Ramos-Martínez E, Olivos-García A, Saavedra E, Nequiz M, Sánchez EC, et al. (2009) Entamoeba histolytica: oxygen resistance and virulence. Int J Parasitol 39: 693-702.
41. Ramos-Martínez E, Olivos-García A, Nequiz M, Saavedra E, Tello E, et al. (2007) Entamoeba histolytica: apoptosis induced in vitro by nitric oxide species. Exp Parasitol 116: 257-65.
42. Susskind BM, Warren LG, Reeves RE, (1982) A pathway for the interconversion of hexose and pentose in the parasitic amoeba Entamoeba histolytica. Biochem J 204: 191-196.
43. Krüger A, Grüning NM, Wamelink MM, Kerick M, Kirpy A, et al. (2011) The pentose phosphate pathway is a metabolic redox sensor and regulates transcription during the antioxidant response. Antioxid Redox Signal 15(2): 311-24.
44. Pollak N, Dolle C, Ziegler M, (2007) The power to reduce: pyridine nucleotides-small molecules with a multitude of functions. Biochem J 402: 205-218.
45. Arroyo-Begovich A, Carabez-Trejo A, Ruíz-Herrera J, (1978) Composition of the cell wall of Entamoeba invadens cysts. Arch Invest Med (Mex) 9: 99-104.
46. Chávez-Munguía B, Martínez-Palomo A, (2011) High-resolution electron microscopical study of cyst walls of Entamoeba spp. J Eukaryot Microbiol 58: 480-486.
47. Aguilar-Diaz H, Diaz-Gallardo M, Laclette JP, Carrero JC, (2010) In vitro Induction of Entamoeba histolytica Cyst-like Structures from Trophozoites. PLoS Negl Trop Dis 4(2): e607.
48. Luján HD, Mowatt MR, Nash TE, (1997) Mechanisms of Giardia lamblia differentiation into cysts. Microbiol Mol Biol Rev 61: 294-304.
49. Ngo DN, Kim MM, Kim SK, (2008) Chitin oligosaccharides inhibit oxidative stress in live cells. Carbohydr Polym 74: 228-234.
50. Anderson IJ, Loftus BJ, (2005) Entamoeba histolytica: Observations on metabolism based on the genome sequence. Experimental Parasitology 110: 173-177.
51. Nozaki T, Ali V, Tokoro M, (2005) Sulfur-containing amino acid metabolism in parasitic protozoa. Adv Parasitol 60: 1-99.
52. Ali V, Nozaki T, (2007) Current therapeutics, their problems, and sulfur-containing amino-acid metabolism as a novel target against infections by "amitochondriate" protozoan parasites. Clin Microbiol Rev 20: 164-187.
53. Tokoro M, Asai T, Kobayashi S, Takeuchi T, Nozaki T, (2003) Identification and characterization of two isoenzymes of methionine gamma-lyase from Entamoeba histolytica: a key enzyme of sulfur-amino acid degradation in an anaerobic parasitic protest that lacks forward and reverse trans-sulfuration pathways. J Biol Chem 278: 42717-42727.
54. 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.
55. 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.
56. Hussain S, Ali V, Jeelani G, Nozaki T, (2009) Isoform-dependent feedback regulation of serine O-acetyltransferase isoenzymes involved in L-cysteine biosynthesis of Entamoeba histolytica. Mol Biochem Parasitol 2009 Jan;163 (1) ():: 39-47.
57. Shenton D, Grant CM, (2003) Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem J 374: 513-519.
58. Colussi C, Albertini MC, Coppola S, Rovidati S, Galli F, Ghibelli L, (2000) H2O2-induced block of glycolysis as an active ADP-ribosylation reaction protecting cells from apoptosis. FASEB J 14: 2266-2276.
59. Saavedra E, Marín-Hernández A, Encalada R, Olivos A, Mendoza-Hernández G, Moreno-Sánchez R, (2007) Kinetic modeling can describe in vivo glycolysis in Entamoeba histolytica. FEBS J 274: 4922-4940.
60. Reeves RE, Lobelle-Rich P, (1983) Absence of alpha-glycerophosphate dehydrogenase in axenically grown Entamoeba histolytica. Am J Trop Med Hyg 32: 1177-1178.
61. Chapman A, Linstead DJ, Lloyd D, Williams J, (1985) 13C-NMR reveals glycerol as an unexpected major metabolite of the protozoan parasite Trichomonas vaginalis. FEBS 191: 287-92.
62. Hammond DJ, Bowman IB, (1980) Studies on glycerol kinase and its role in ATP synthesis in Trypanosoma brucei. Mol Biochem Parasitol 2: 77-91.
63. Lian LY, Al-Helal M, Roslaini AM, Fisher N, Bray PG, (2009) Glycerol: an unexpected major metabolite of energy metabolism by the human malaria parasite. Malar J 6: 38.
64. Pahlman AK, Granath K, Ansell R, Hohmann S, Adler L, (2001) The yeast glycerol 3-phosphatases Gpp1p and Gpp2p are required for glycerol biosynthesis and differentially involved in the cellular responses to osmotic, anaerobic, and oxidative stress. J Biol Chem 276: 3555-3363.