Evidence for mitochondrial-derived alternative oxidase in the apicomplexan parasite Cryptosporidium parvum: A potential anti-microbial agent target

International Journal for Parasitology

Volumn 34, Issue 3, 2004, Pages 297-308

  Roberts, Craig W ^a,b   Roberts, Fiona ^b   Henriquez, Fiona L ^a   Akiyoshi, Donna ^c   Samuel, Benjamin U ^b   Richards, Thomas A ^d   Milhous, Wilbur ^e   Kyle, Dennis ^e   McIntosh, Lee ^f   Hill, George C ^g   Chaudhuri, Minu ^g   Tzipori, Saul ^c   McLeod, Rima ^b  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b UNIVERSITY OF CHICAGO   (United States)

^c TUFTS UNIVERSITY   (United States)

^d DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^e WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^f MICHIGAN STATE UNIVERSITY   (United States)

^g MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

Alternative oxidase; Anti microbial; Apicomplexan; Cryptosporidium parvum; Immutans; Mitochondria; Phylogeny; Plasmodium; Toxoplasma gondii

Indexed keywords

8 QUINOLINOL; ALTERNATIVE OXIDASE; AMINO ACID; ANTIINFECTIVE AGENT; CHLOROQUINE; MEFLOQUINE; MITOCHONDRIAL ENZYME; POLYPEPTIDE; PROTOZOAL PROTEIN; PYRIMETHAMINE; SULFADOXINE; UNCLASSIFIED DRUG;

PARASITOLOGY;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; CHLOROPLAST; CONTROLLED STUDY; CRYPTOSPORIDIUM PARVUM; ENDOSYMBIOSIS; FEMALE; GENE IDENTIFICATION; GENE SEQUENCE; GENE TARGETING; GENE TRANSFER; GENETIC CODE; GENOME ANALYSIS; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMODIUM FALCIPARUM; PROTOZOAL GENETICS; REVIEW; TROPHOZOITE;

APICOMPLEXA; CRYPTOSPORIDIUM PARVUM; FUNGI; PLASMODIUM FALCIPARUM; PROTOZOA; TOXOPLASMA GONDII;

EID: 10744228355     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2003.11.002     Document Type: Article

References (56)

1. Akiyoshi D.E., Feng X., Buckholt M.A., Widmer G., Tzipori S. Genetic analysis of a Cryptosporidium parvum human genotype 1 isolate passaged through different host species. Infect. Immun. 70:2002;5670-5675.
2. Alexander J., Hunter C.A. Immunoregulation during toxoplasmosis. Chem. Immunol. 70:1998;81-102.
3. Berthold D.A., Andersson M.E., Nordlund P. New insight into the structure and function of the alternative oxidase. Biochim. Biophys. Acta. 1460:2000;241-254.
4. Brown S.M.A., McDonald V., Denton H., Coombs G.H. The use of a new viability assay to determine the susceptibility of Cryptosporidium and Eimeria sporozoites to respiratory inhibitors and extremes of pH. FEMS Microbiol. Lett. 142:1996;203-208.
5. Carol P., Stevenson D., Bisanz C., Breitenbach J., Sandmann G., Mache R., Coupland G., Kuntz M. Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell. 11:1999;57-68.
6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
7. Claros M.G., Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241:1996;779-786.
8. Clough B., Strath M., Preiser P., Denny P., Wilson I.R. Thiostrepton binds to malarial plastid rRNA. FEBS Lett. 406:1997;123-125.
9. Cohen S.N., Chang A.C., Hsu L. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc. Natl. Acad. Sci. USA. 69:1972;2110-2114.
10. Coombs G.H., Muller S. Recent advances in the search for new anti-coccidial drugs. Int. J. Parasitol. 32:2002;497-508.
11. Coombs G.H. Biochemical peculiarities and drug targets in Cryptosporidium parvum: lessons from other coccidian parasites. Parasitol. Today. 15:1999;333-338.
12. Current W.L., Bick P.H. Immunobiology of Cryptosporidium spp. Pathol. Immunopathol. Res. 8:1989;141-160.
13. Denton H., Brown S.M.A., Roberts C.W., Alexander J., McDonald V., Thong K.W., Coombs G.H. Comparison of the phosphofructokinase and pyruvate kinase activities of Cryptosporidium parvum. Eimeria tenella and Toxoplasma gondii. Mol. Biochem. Parasitol. 76:1996;23-29.
14. Divo A.A., Geary T.G., Jensen J.B., Ginsburg H. The mitochondrion of Plasmodium falciparum visualized by rhodamine 123 fluorescence. J. Protozool. 32:1985;442-446.
15. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300:2000;1005-1016.
16. Entrala E., Mascaro C. Glycolytic enzymes acivities in Cryptosporidium parvum oocysts. FEMS Microbiol. Lett. 151:1997;51-57.
17. Finnegan P.M., Wooding A.R., Day D.A. An alternative oxidase monoclonal antibody recognises a highly conserved sequence among alternative oxidase subunits. FEBS Lett. 447:1999;21-24.
18. Fichera M.E., Roos D.S. A plastid organelle as a drug target in apicomplexan parasites. Nature. 390:1997;407-409.
19. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., Paulsen I.T., James K., Eisen J.A., Rutherford K., Salzberg S.L., Craig A., Kyes S., Chan M.S., Nene V., Shallom S.J., Suh B., Peterson J., Angiuoli S., Pertea M., Allen J., Selengut J., Haft D., Mather M.W., Vaidya A.B., Martin D.M., Fairlamb A.H., Fraunholz M.J., Roos D.S., Ralph S.A., McFadden G.I., Cummings L.M., Subramanian G.M., Mungall C., Venter J.C., Carucci D.J., Hoffman S.L., Newbold C., Davis R.W., Fraser C.M., Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 419:2002;498-511.
20. Hopkins J., Fowler R., Krishna S., Wilson I.R., Mitchell G., Bannister L. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist. 150:1999;283-295.
21. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 17:2001;754-755.
22. Hunter P.R., Nichols G. Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clin. Microbiol. Rev. 15:2002;145-154.
23. Josse E.M., Simkin A.J., Gaffe J., Laboure A.M., Kuntz M., Carol P. A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol. 123:2000;1427-1436.
24. Krungkrai J., Prapunwattana P., Krungkrai S.R. Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite. 7:2000;19-26.
25. Lang-Unnasch N., Reith M.E., Munholland J., Barta J.R. Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int. J. Parasitol. 28:1998;1743-1754.
26. Lyons R.E., Anthony J.P., Ferguson D.J.P., Byrne N., Alexander J., Roberts F., Roberts C.W. Immunological studies of chronic ocular toxoplasmosis: up-regulation of major histocompatibility complex I and Transforming growth factor β and a protective role for interferon-γ Infect. Immun. 69:2001;2589-2595.
27. Mack D.G., McLeod R. New micromethod to study the effect of antimicrobial agents on toxoplasma gondii: Comparison of sulfadoxine and sulfadiazine individually and in combination with pyrimethamine and study of clindamycin, metromidazole, and cyclosporin A. Antimicrob. Ag. Chemother. 26:1984;26-30.
28. Maidak B.L., Olsen G.J., Larsen N., Overbeek R., McCaughey M.J., Woese C.R. The Ribosomal Database Project (RDP). Nucleic Acids Res. 24:1996;82-85.
29. McFadden G.I., Roos D.S. Apicomplexan plastids as drug targets. Trends Microbiol. 7:1999;328-333.
30. McIntosh L. Molecular biology of the alternative oxidase. Plant Physiol. 105:1994;781-786.
31. McLeod R., Muensch S.P., Rafferty J.B., Kyle D.E., Mui E.J., Kirisits M.J., Mack D.G., Roberts C.W., Samuel B.U., Lyons R.E., Dorris M., Milhous W.K., Rice D.W. Triclosan inhibits the growth of Plasmodium falciparum and Toxoplasma gondii by inhibition of apicomplexan Fab I. Int. J. Parasitol. 31:2001;109-113.
32. Milani G., Jarmuszkiewicz W., Sluse-Goffart C.M., Schreiber A.Z., Vercesi A.E., Sluse F.E. Respiratory chain network in mitochondria of Candida parapsilosis: ADP/O appraisal of the multiple electron pathways. FEBS Lett. 508:2001;231-235.
33. Milhous W.K., Weatherly N.F., Bowdre J.H., Desjardins R.E. In vitro activities of and mechanisms of resistance to antifol antimalarial drugs. Antimicrob. Agents Chemother. 27:1985;525-530.
34. Millar A.H., Day D.A. Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett. 398:1996;155-158.
35. Murphy A.D., Lang-Unnasch N. Alternative oxidase inhibitors potentiate the activity of atovaquone against Plasmodium falciparum. Antimicrob. Agents Chemother. 43:1999;651-654.
36. Murphy A.D., Doeller J.E., Hearn B., Lang-Unnasch N. Plasmodium falciparum: cyanide-resistant oxygen consumption. Exp. Parasitol. 87:1997;112-120.
37. Nihei C., Fukai Y., Kita K. Trypanosome alternative oxidase as a target of chemotherapy. Biochim. Biophys. Acta. 1587:2002;234-239.
38. Oduola A.M., Milhous W.K., Weatherly N.F., Bowdre J.H., Desjardins R.E. Plasmodium falciparum: induction of resistance to mefloquine in cloned strains by continuous drug exposure in vitro. Exp. Parasitol. 67:1988;354-360.
39. Richards T., Hirt R.P., Wiliams A.P., Embley T.M. Horizontal Gene Transfer and the Evolution of Parasitic Protozoa. Protist. 154:2003;17-32.
40. Ridley R.G. Medical need, scientific opportunity and the drive for antimalarial drugs. Nature. 415:2002;686-693.
41. Riordan C.E., Langreth S.G., Sanchez L.B., Kayser O., Keithly J.S. Preliminary evidence for a mitochondrion in Cryptosporidium parvum: phylogenetic and therapeutic implications. J. Eukaryot. Microbiol. 46:1999;52S-55S.
42. Riordan C.E., Ault J.G., Langreth S.G., Keithly J.S. Cryptosporidium parvum Cpn60 targets a relict organelle. Curr. Genet. 2003;. in press.
43. Roberts C.W., Roberts F., Lyons R.E., Kirisits M.J., Mui E.J., Finnerty J., Johnson J.J., Ferguson D.J., Coggins J.R., Krell T., Coombs G.H., Milhous W.K., Kyle D.E., Tzipori S., Barnwell J., Dame J.B., Carlton J., McLeod R. The shikimate pathway and its branches in apicomplexan parasites. J. Infect. Dis. 185:2002;S25-S36.
44. Roberts F., Roberts C.W., Johnson J.J., Kyle D.E., Krell T., Coggins J.R., Coombs G.H., Milhous W.K., Tzipori S., Ferguson D.J., Chakrabarti D., McLeod R. Evidence for the shikimate pathway in apicomplexan parasites. Nature. 393:1998;801-805.
45. Rotte C., Stejskal F., Zhu G., Keithly J.S., Martin W. Pyruvate:NADP oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol. Biol. Evol. 18:2001;710-720.
46. Surolia N., Surolia A. Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat. Med. 7:2001;167-173.
47. Tanabe K., Murakami K. Reduction in mitochonrial membrane potential of Toxoplasma gondii after invasion of host cell. J. Cell Sci. 70:1984;73-81.
48. Tetley L., Brown S.M., McDonald V., Coombs G.H. Ultrastructural analysis of the sporozoite of Cryptosporidium parvum. Microbiology. 144:1998;3249-3255.
49. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:1997;4876-4882.
50. Tzipori S. Cryptosporidiosis: laboratory investigations and chemotherapy. Adv. Parasitol. 40:1998;187-221.
51. Uni S., Iseki M., Maekawa T., Moriya K., Takada S. Ultrastructure of Cryptosporidium muris (strain RN 66) parasitizing the murine stomach. Parasitol. Res. 74:1987;123-132.
52. Vanlerberghe G.C., McIntosh L. Alternative oxidase: from gene to function. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48:1997;703-734.
53. Viale A.M., Arakaki A.K. The chaperone connection to the origins of the eukaryotic organelles. FEBS Lett. 341:1994;146-151.
54. Wetzel C.M., Jiang C.Z., Meehan L.J., Voytas D.F., Rodermel S.R. Nuclear-organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J. 6:1994;161-175.
55. Widmer G., Tzipori S., Fichtenbaum C.J., Griffiths J.K. Genotypic and phenotypic characterization of Cryptosporidium parvum isolates from people with AIDS. J. Infect. Dis. 178:1998;834-840.
56. Williams B.A., Hirt R.P., Lucocq J.M., Embley T.M. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature. 418:2002;865-869.