Stage-specific isoforms of Ascaris suum complex II: The fumarate reductase of the parasitic adult and the succinate dehydrogenase of free- living larvae share a common iron-sulfur subunit

Molecular and Biochemical Parasitology

Volumn 106, Issue 1, 2000, Pages 63-76

  Amino, Hisako ^a   Wang, Hua ^a   Hirawake, Hiroko ^a   Saruta, Fumiko ^a   Mizuchi, Daisuke ^a   Mineki, Reiko ^b   Shindo, Noriko ^b   Murayama, Kimie ^b   Takamiya, Shinzaburo ^b   Aoki, Takashi ^b   Kojima, Somei ^c   Kita, Kiyoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JUNTENDO UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Ascaris suum; Caenorhabditis elegans; Fumarate reductase; Iron sulfur protein; Succinate dehydrogenase

Indexed keywords

COMPLEMENTARY DNA; CYTOCHROME C OXIDASE; FLAVOPROTEIN; FUMARATE REDUCTASE; IRON SULFUR PROTEIN; SUCCINATE DEHYDROGENASE;

AMINO ACID COMPOSITION; ANAEROBIC METABOLISM; ARTICLE; ASCARIS SUUM; CAENORHABDITIS ELEGANS; ELECTRON TRANSPORT; ENZYME ACTIVITY; GENE SEQUENCE; LARVA; MITOCHONDRION; MOLECULAR CLONING; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ASCARIS SUUM; BASE SEQUENCE; BLOTTING, NORTHERN; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CHROMATOGRAPHY, ION EXCHANGE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ELECTRON TRANSPORT COMPLEX II; IRON-SULFUR PROTEINS; ISOENZYMES; LARVA; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; OXIDOREDUCTASES; RNA, HELMINTH; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SUCCINATE DEHYDROGENASE;

EID: 0033953887     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(99)00200-5     Document Type: Article

References (55)

1. Takamiya S., Kita K., Wang H., Weinstein P.P., Hiraishi A., Oya H., Aoki H. Developmental changes in the respiratory chain of Ascaris mitochondria. Biochim. Biophys. Acta. 1141:1993;65-74.
2. Kita K. Electron-transfer complexes of mitochondria in Ascaris suum. Parasitol. Today. 8:1992;155-159.
3. Komuniecki R., Komuniecki P.R. Aerobic-anaerobic transitions in energy metabolism during the development of the parasitic nematode Ascaris suum. Boothroyd J.C., Komuniecki R. Molecular Approaches to Parasitology. 1995;109-121 Wiley-Liss, Inc, New York.
4. Kita K., Hirawake H., Takamiya S. Cytochromes in the respiratory chain of helminth mitochondria. Int. J. Parasitol. 27:1997;617-630.
5. Tielens A.G.M., Van Hellemond J.J. The electron transport chain in anaerobically functioning eukaryotes. Biochim. Biophys. Acta. 1365:1998;71-78.
6. b558. Biochim. Biophys. Acta. 848:1986;99-107.
7. Kita K., Takamiya S., Furushima R., Ma Y.C., Oya H. Complex II is a major component of the respiratory chain in the muscle mitochondria of Ascaris suum with high fumarate reductase activity. Comp. Biochem. Physiol. 89B:1988;31-34.
8. Kita K., Takamiya S., Furushima R., Ma Y.C., Suzuki H., Ozawa T., Oya H. Electron-transfer complexes of Ascaris suum muscle mitochondria. III. Composition and fumarate reductase activity of complex II. Biochim. Biophys. Acta. 935:1988;130-140.
9. Saruta F., Kuramochi T., Nakamura K., Takamiya S., Yu Y., Aoki T., Sekimizu K., Kojima S., Kita K. Stage-specific isoforms of complex II (succinate-ubiquinone oxidoreductase) in mitochondria from the parasitic nematode, Ascaris suum. J. Biol. Chem. 270:1995;928-932.
10. Hederstedt L., Ohnishi T. Progress in succinate: quinone oxidoreductase research. Ernster L. Molecular Mechanisms in Bioenergetics. 1992;163-198 Elsevier, Amsterdam.
11. Hägerhall C. Succinate:quinone oxidoreductases. Variations on a conserved theme. Biochim. Biophys. Acta. 1320:1997;107-141.
12. Kita K., Oya H., Gennis R., Ackrell B.A.C., Kasahara M. Human complex II (succinate-ubiquinone oxidoreductase): cDNA cloning of iron sulfur (Ip) subunit of liver mitochondria. Biochem. Biophys. Res. Commun. 166:1990;101-108.
13. Hirawake H., Wang H., Kuramochi T., Kojima S., Kita K. Human complex II (succinate-ubiquinone oxidoreductase): cDNA cloning of the flavoprotein (Fp) subunit of liver mitochondria. J. Biochem. 116:1994;221-227.
14. Hirawake H., Taniwaki M., Tamura A., Kojima S., Kita K. Cytochrome b in human complex II (succinate-ubiquinone oxidoreductase): cDNA cloning of the components in liver mitochondria and chromosome assignment of the genes for the large (SDHC) and small (SDHD) subunits to 1q21 and 11q23. Cytogenet. Cell Genet. 79:1997;132-138.
15. Kita K., Mizuchi D., Wang H., Takarnlya S., Aoki T., Kojima S. cDNA sequence of three cysteine-rich clusters in the iron-sulfur subunit of complex II (succinate-ubiquinone oxidoreductase) from C. elegans determined by automated DNA sequencer. Electrophoresis. 13:1992;506-511.
16. Kuramochi T., Hirawake H., Kojima S., Takamiya S., Furushima R., Aoki T., Komuniecki R., Kita K. Sequence comparison between the flavoprotein subunit of the fumarate reductase (complex II) of the anaerobic parasitic nematode, Ascaris suum and the succinate dehydrogenase of the aerobic, free-living nematode, Caenorhabditis elegans. Mol. Biochem. Parasitol. 68:1994;177-187.
17. Kuramochi T., Kita K., Takamiya S., Kojima S., Hayasaki M. Comparative study and cDNA cloning of the flavoprotein subunit of mitochondrial complex II (succinate-ubiquinone oxidoreductase: fumarate reductase) from the dog heartworm, Dirofilaria immitis. Comp. Biochem. Physiol. 111B:1995;491-502.
18. 558 (cybS) of mitochondrial fumarate reductase (complex II) from adult Ascaris suum. Biochim. Biophys. Acta. 1276:1996;1-5.
19. Iverson T.M., Luna-Chavez C., Cecchini G., Rees D.C. Structure of Escherichia coli fumarate reductase respiratory complex. Science. 284:1999;1961-1966.
20. Hata-Tanaka A., Kita K., Furushima R., Oya H., Itoh S. ESR studies on iron-sulfur clusters of complex II in Ascaris suum mitochondria which exhibits strong fumarate reductase activity. FEBS Lett. 242:1988;183-186.
21. Unden G., Albracht S.P.J., Kröger A. Redox potentials and kinetic properties of fumarate reductase complex from Vibrio succinogenes. Biochim. Biophys. Acta. 767:1984;460-469.
22. Cole S.T., Condon C., Lemire B.D., Weiner J.H. Molecular biology, biochemistry and bioenergetics of fumarate reductase, a complex membrane-bound iron-sulfur flavoenzyme of Escherichia coli. Biochim. Biophys. Acta. 811:1985;381-403.
23. Tielens A.G.M. Energy generation in parasitic helminths. Parasitol. Today. 10:1994;346-352.
24. Roos M.H., Tielens A.G.M. Differential expression of two succinate dehydrogenase subunit-B genes and a transition in energy metabolism during the development of the parasitic nematode Haemonchus contortus. Mol. Biochem. Parasitol. 66:1994;273-281.
25. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocynate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
26. Gould S.J., Subramani S., Scheffler E. Use of the DNA polymerase chain reaction for homology probing: isolation of partial cDNA of genomic clones encoding the iron-sulfur protein of succinate dehydrogenase from several species. Proc. Natl. Acad. Sci. USA. 86:1989;1934-1938.
27. Nilsen T., Shambaugh J., Denker J., Chubb G., Faser C., Putnam L., Bennett K. Characterization and expression of a spliced leader RNA in the parasitic nematode Ascaris lumbricoides var. suum. Mol. Cell. Biol. 9:1989;3543-3547.
28. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. Current Protocols in Molecular Biology. 1987;Greene Publishing Associates and Wiley-Interscience, New York.
29. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 262:1987;10035-10038.
30. Shindo N., Nojima S., Fujimura T., Taka H., Mineki R., Murayama K. Separation of 18 6-aminoquinolyl-carbamyl-amino acids by ion-pair chromatography. Anal. Biochem. 249:1997;79-82.
31. Shindo N., Fujimura T., Nojima-Kazuno S., Mineki R., Furusawa S., Sasaki K., Murayama K. Identification of multidrug resistant protein 1 of mouse leukemia P388 cells on a PVDF membrane using 6-aminoquinolyl-carbamyl (AQC)-amino acid analysis and world wide web (WWW) accessible tools. Anal. Biochem. 264:1998;251-258.
32. Wilkins M.R., Gasteiger E., Bairoch A7 Sanchez J.-C., Williams K.L., Appel R.D., Hochstrasser D.F. Protein identification and analysis tools in the ExPASy server. Link A.J. 2-D Proteome Analysis Protocols. 1999;531-552 Numana Press, New Jersey.
33. Futai M. Membrane D-lactate dehydrogenase from Escherichia coli Purification and properties. Biochemistry. 12:1986;2468-2474.
34. Lemire B.D., Weiner J.H. Fumarate reductase of Escherichia coli. Fleischer S., Fleischer B. Methods in Enzymology. 1986;377-386 Academic Press, ;126, Orlando.
35. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:1951;265-275.
36. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:1979;4350-4354.
37. Wang H., Takarnlya S., Kita K., Oya H., Aoki T. Comparative study on the primary structure of the iron-sulfur subunit of complex II in Ascaris suum mitochondria. Jpn. J. Parasitol. 41:1992;122-131.
38. Hurt E.C., Van Loon A.P. How proteins find mitochondria and intramitochondrial compartments. Trends Biochem. Sci. 11:1986;204-207.
39. Cole S.T., Grundstrom T., Jaurin B., Robinson J.J., Weiner J.H. Loeation and nucleotide sequence of frdB, the gene coding for the iron-sulphur protein subunit of the fumarate reductase of Escherichia coli. Eur. J. Biochem. 126:1982;211-216.
40. Darlison M.G., Guest J.R. Nucleotide sequence encoding the iron-sulphur protein subunit of the succinate dehydrogenase of Escherichia coli. Biochem. J. 223:1984;507-517.
41. Broomfield P.L.E., Hargreaves J.A. A single amino-acid change in the iron-sulphur protein subunit of succinate dehydrogenase confers resistance to carboxin in Ustilago maydis. Curr. Genet. 22:1992;117-121.
42. Skinner W., Bailey A., Renwick A., Keon J., Gurr S., Hargreaves J. A single amino-acid substitution in the iron-sulphur protein subunit of succinate dehydrogenase determines resistance to carboxin in Mycosphaerella graminicola. Curr. Genet. 34:1998;393-398.
43. Matsson M., Aekrell B.A.C., Cochran B., Hederstedt L. Carboxin resistance in Paracoccus denitrificans conferred by a mutation in the membrane-anchor domain of succinate:quinone reductase (complex II). Arch. Microbiol. 170:1998;27-37.
44. Waldeck A.R., Stowell M.H.B., Lee H.K., Hung S.C., Matsson M., Hederstedt L., Aekrell B.A.C., Chan S.I. Eleetron paramagnetic resonance studies of succinate:ubiquinone oxidoreductase from Paracoccus denitrificans. Evidence for a magnetic interaction between the 3Fe-4S cluster and cytochrome b. J. Biol. Chem. 272:1997;19373-19382.
45. Barrett J. Aetivation of succinate dehydrogenase from adult Fasciola hepatica (Trematoda). Parasitology. 76:1978;269-275.
46. Van Hellemond J.J., Van Remoortere A., Tielens A.G.M. Schistosoma mansoni sporocysts contain rhodoquinone and produce succinate by fumarate reduction. Parasitology. 115:1997;177-182.
47. Sulston J., Du Z., Thomas K., Wilson R., Hillier L., Staden R., Halloran N., Green P., Thierry-Mieg J., Qiu L., Dear S., Coulson A., Craxton M., Durbin R., Berks M., Metzstein M., Hawkins T., Ainseough R., Waterston R. The C. elegans genome sequencing project: a beginning. Nature. 356:1992;37-41.
48. Coulson A., Sulston J., Brenner S., Karn J. Toward a physical map of the genome of nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 83:1986;7821-7825.
49. Coulson A., Waterston R., Kiff J., Sulston J., Kohara Y. Genome linking with yeast artificial chromosomes. Nature. 335:1988;184-186.
50. Coulson A., Kozono Y., LuKerbach B., Shownkeen R., Sulston J., Waterston R. YACs and the Caenorhabditis elegans genome. BioEssays. 13:1991;413-417.
51. Waterston R., Martin C., Craxton M., Huynh C., Coulson A., Hillier L., Durbin R., Green P., Shownkeen R., Halloran N., Metzstein M., Hawkins T., Wilson R., Berks M., Du Z., Thomas K., Thierry-Mieg J., Sulston J. A survey of expressed genes in Caenorhabditis elegans. Nature Genes. 1:1992;114-123.
52. The C. elegans sequencing consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998;282:2012-2018.
53. Au H.C., Scheffler I.E. Characterization of the gene encoding the iron-sulfur protein subunit of succinate dehydrogenase from Drosophila melanogaster. Gene. 149:1994;261-265.
54. Au H.C., Ream-Robinson D., Bellew L.A., Broomfield P.L.E., Saghbini M., Scheffler I.E. Structural organization of the gene encoding the human iron-sulfur subunit of succinate dehydrogenase. Gene. 159:1995;249-253.
55. Hobohm U., Sander C. A sequence property approach to searching protein databases. J. Mol. Biol. 251:1995;390-399.