Novel inhibitors of the trypanosome alternative oxidase inhibit Trypanosoma brucei brucei growth and respiration

Acta Tropica

Volumn 100, Issue 3, 2006, Pages 172-184

  Ott, Robert ^a   Chibale, Kelly ^b   Anderson, Sedrick ^c   Chipeleme, Alex ^b   Chaudhuri, Minu ^c   Guerrah, Abdelmadjid ^c   Colowick, Nancy ^a   Hill, George C ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

African sleeping sickness; Inhibition kinetics; Trypanosoma brucei brucei; Trypanosome alternative oxidase

Indexed keywords

ACB15; ACB16; ACB40; CARBOHYDRATE; CYTOCHROME; OXIDOREDUCTASE; OXIDOREDUCTASE INHIBITOR; PRENYLAMINE; SALICYLIC ACID; TRYPANOSOME ALTERNATIVE OXIDASE; UBIQUINONE; UNCLASSIFIED DRUG;

ENZYME ACTIVITY; GROWTH RATE; INHIBITION; INHIBITOR; KINETICS; RESPIRATION; TRYPANOSOMIASIS;

AFRICAN TRYPANOSOMIASIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL RESPIRATION; COMPETITIVE INHIBITION; DOSE RESPONSE; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; ENZYME PURIFICATION; GROWTH INHIBITION; GROWTH RATE; INHIBITION KINETICS; LIVER MITOCHONDRION; MAMMAL CELL; NONHUMAN; RAT; SOLUBILITY; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA RHODESIENSE;

ANIMALS; CARBOHYDRATES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DESIGN; ENZYME INHIBITORS; GLUCOSIDES; MICE; OXIDOREDUCTASES; PROTOZOAN PROTEINS; RATS; SALICYLAMIDES; SALICYLIC ACID; SALICYLIC ACIDS; TRYPANOCIDAL AGENTS; TRYPANOSOMA BRUCEI BRUCEI;

AFRICA;

MAMMALIA; RATTUS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA BRUCEI RHODESIENSE;

EID: 33846632321     PISSN: 0001706X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actatropica.2006.10.005     Document Type: Article

References (76)

1. Affourtit C., Albury M.S., Crichton P.G., and Moore A.L. Exploring the molecular nature of alternative oxidase regulation and catalysis. FEBS Lett. 510 (2002) 121-126
2. Amole B.O., and Clarkson Jr. A.B. Trypanosoma brucei: host parasite interaction in parasite destruction by salicylhydroxamic acid and glycerol in mice. Exp. Parasitol. 51 (1981) 133-140
3. Awad A.M., Sobkowski M., and Seliger H. Enzymatic and hybridization properties of oligonucleotide analogs containing novel phosphoramidate internucleotide linkages. Nucleosides Nucleotides Nucleic Acids 23 (2004) 777-787
4. Bacchi C.J., Nathan H.C., Hutner S.H., McCann P.P., and Sjoerdsma A. Polyamine metabolism: a potential therapeutic target in trypanosomes. Science 210 (1980) 332-334
5. Bardaji E., Torres J.L., Clapes P., Albericio F., Barany G., Rodriguez R.E., Sacristan M.P., and Valencia G. Synthesis and biological activity of o-glycosylated morphiceptin analogs. J. Chem. Soc. Perkin Trans. 1 (1991) 1755-1759
6. Bell G.I., Burant C.F., Takeda J., and Gould G.W. Structure and function of mammalian facilitative sugar transporters. J. Biol. Chem. 268 (1993) 19161-19164
7. Benovitz D.E., and Spatola A.F. Enkephalin pseudopeptides: resistance to in vitro proteolytic degradation afforded by amide bond replacements extends to remote sites. Peptides 6 (1985) 257-261
8. Berthold D.A., Andersson M.E., and Nordlund P. New insight into the structure and function of the alternative oxidase. Biochim. Biophys. Acta 1460 (2000) 241-254
9. Bienen E.J., Hill G.C., and Shin K. Elaboration of mitochondrial function during Trypanosoma brucei differentiation. Mol. Biochem. Parasitol. 7 (1983) 75-86
10. Brohn F.H., and Clarkson A.B. Quantitative effects of salicylhydroxamic acid and glycerol on Trypanosoma brucei glycolysis in vitro and in vivo. Acta Trop. 35 (1978) 23-33
11. Brown R.C., Evans D.A., and Vickerman K. Changes in the oxidative metabolism and ultrastructure accompanying differentiation of the mitochondrion in Trypanosoma brucei. Int. J. Parasitol. 3 (1973) 691-704
12. Brun R., Schumacher R., Schmid C., Kunz C., and Burri C. The phenomenon of treatment failures in African Trypanosomiasis. Trop. Med. Int. Health 6 (2001) 906-914
13. Burchmore R.J., Ogbunude P.O., Enanga B., and Barrett M.P. Chemotherapy of human African trypanosomiasis. Curr. Pharm. Des. (2002) 256-267
14. Burri C., and Keiser J. Pharmacokinetic investigations in patients from northern Angola refractory to melarsoprol treatment. Trop. Med. Int. Health 6 (2001) 412-420
15. Burri C., and Brun R. Eflornithine for the treatment of human African trypanosomiasis. Parasitol. Res. 90 (2003) s49-s52
16. Carruthers V.B., and Cross G.A.M. High-efficiency clonal growth of bloodstream-and insect-form Trypanosoma brucei on agarose plates. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 8818-8821
17. Chappuis F., Udayraj N., Stietenroth K., Meussen A., and Bovier P.A. Eflornithine is safer than melarsoprol for the treatment of second-stage Trypanosoma brucei gambiense human African trypanosomiasis. Clin. Infect. Dis. 41 (2005) 748-751
18. Chaudhuri M., and Hill G.C. Cloning, sequencing, and functional activity of the Trypanosoma brucei brucei alternative oxidase. Mol. Biochem. Parasitol. 83 (1996) 125-129
19. Chaudhuri M., Ott R.D., Saha L., Williams S., and Hill G.C. The trypanosome alternative oxidase exists as a monomer in Trypanosoma brucei mitochondria. Parasitol. Res. 96 (2005) 178-183
20. Clarkson A.B., and Brohn F.H. Trypanosomiasis: an approach to chemotherapy by the inhibition of carbohydrate catabolism. Science 194 (1976) 204-206
21. Clarkson A.B., Bienen E.J., Pollakis G., and Grady R.W. Respiration of bloodstream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase. J. Biol. Chem. 264 (1989) 17770-17776
22. Clarkson Jr. A.B., Grady R.W., Grossman S.A., McCallum R.J., and Brohn F.H. Trypanosoma brucei brucei: a systematic screening for alternatives to the salicylhydroxamic acid-glycerol combination. Mol. Biochem. Parasitol. 3 (1981) 271-291
23. Cohen J. Prevention cocktails: combining tools to stop HIV's spread. Science 309 (2005) 1002-1005
24. Cross G.A.M. Trypanosomes at the gates. Science 309 (2005) 355
25. Dixon M. The determination of enzyme inhibitor constants. Biochem. J. 55 (1953) 170-171
26. Doggrell S.A. New drugs being developed for the treatment of tuberculosis. Expert Opin. Investig. Drugs 14 (2005) 917-920
27. Evans D.A., and Brown R.C. M-chlorobenzhydroxamic acid-an inhibitor of cyanide-insensitive respiration in Trypanosoma brucei. J. Protozool. 20 (1973) 157-160
28. Evans D.A., and Brown R.C. The inhibitory effects of aromatic hydroxamic acids on the cyanide-insensitive terminal oxidase of Trypanosoma brucei. Trans. R. Soc. Trop. Med. Hyg. 67 (1973) 258
29. Evans D.A., Brightman C.A., and Holland M.F. Salicylhydroxamic acid/glycerol in experimental trypanosomiasis. Lancet Infect. Dis. ii (1977) 769
30. Evans D.A., and Holland M.F. Effective treatment of Trypanosoma vivax infections with salicylhydroxamic acid (SHAM). Trans. R. Soc. Trop. Med. Hyg. 72 (1978) 203-204
31. Evans D.A., and Brightman C.A. Pleomorphism and the problem of recrudescent parasitemia following treatment with salicylhydroxamic acid in African trypanosomiasis. Trans. R. Soc. Trop. Med. Hyg. 74 (1980) 601-604
32. Fisher J.F., Harrison A.W., Bundy G.L., Wilkinson K.F., Rush B.D., and Ruwart M.J. Peptide to glycopeptide-glycosylated oligopeptide renin inhibitors with attenuated in vivo clearance properties. J. Med. Chem. 34 (1991) 3140-3143
33. Grady R.W., Bienen E.J., and Clarkson A.B. P-alkyloxy-benzhydroxamic acids, effective inhibitors of the trypanosome glycerol-3-phosphate oxidase. Mol. Biochem. Parasitol. 19 (1986) 231-240
34. Grady R.W., Bienen E.J., and Clarkson A.B. Esters of 3,4-dihydroxybenzoic acid, highly effective inhibitors of the sn-glycerol-3-phosphate oxidase of Trypanosoma brucei brucei. Mol. Biochem. Parasitol. 21 (1986) 55-63
35. Grady R.W., Bienen E.J., Dieck H.A., Saric M., and Clarkson Jr. A.B. N-n-Alkyl-3,4-dihydroxybenzamides as inhibitors of the trypanosome alternative oxidase: activity in vitro and in vivo. Antimicrob. Agents Chemother. 37 (1993) 1082-1085
36. Helfert S., Estevez A.M., Bakker B., Michels P., and Clayton C. Roles of triose phosphate isomerase and aerobic metabolism in Trypanosoma brucei. Biochem. J. 357 (2001) 117-125
37. Hill G.C. Electron transport systems in Kinetoplastida. Biochim. Biophys. Acta 456 (1976) 149-193
38. Hirumi H., and Hirumi K. Continuous cultivation of Trypanosoma brucei bloodstream forms in a medium containing a low concentration of serum proteins without feeder cell layers. J. Parasitol. 75 (1989) 985-989
39. Hoet S., Opperdoes F.R., Brun R., and Quetin-Leclercq J. Natural products active against African trypanosomes: a step towards new drugs. Nat. Prod. Rep. 21 (2004) 353-364
40. Juszczuk I.M., and Rychter A.M. Alternative oxidase in higher plants. Acta Biochim. Polon. 50 (2003) 1257-1271
41. Kim K.P., Whitehead C., Piazza G., and Wargovich M.J. Combinatorial chemoprevention: efficacy of lovastatin and exisulind on the formation and progression of aberrant crypt foci. Anticancer Res. 3a (2004) 1805-1811
42. Legros D., Evans S., Maiso F., Enyaru J.C.K., and Mbulamberi D. Risk factors for treatment failure after melarsoprol for Trypanosoma brucei gambiense trypanosomiasis in Uganda. Trans. R. Soc. Trop. Med. Hyg. 93 (1999) 439-442
43. Legros D., Ollivier G., Gastellu-Etchegorry M., Paquet C., Burri C., Jannin J., and Buscher P. Treatment of human African trypanosomiasis: present situation and needs for research and development. Lancet Infect. Dis. 2 (2002) 437-440
44. Matovu E., Seebeck T., Enyaru J.C.K., and Kaminsky R. Drug resistance in Trypanosoma brucei spp., the causative agents of sleeping sickness in man and nagana in cattle. Microbes Infect. 3 (2001) 763-770
45. McIntosh L. Molecular biology of the alternative oxidase. Plant Physiol. 105 (1994) 781-786
46. Moore A., and Richer M. Re-emergence of epidemic sleeping sickness in southern Sudan. Trop. Med. Int. Health 6 (2001) 342-347
47. Moore A.C. Prospects for improving African trypanosomiasis chemotherapy. J. Infect. Dis. 191 (2005) 1793-1795
48. Moore A.L., and Siedow J.N. The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim. Biophys. Acta 1059 (1991) 121-140
49. Mugnaini C., Petricci E., Corelli F., and Botta M. Combinatorial chemistry as a tool for targeting different stages of the replicative HIV-1 cycle. Comb. Chem. High Throughput Screening 5 (2005) 387-401
50. Nappi A.J., and Vass E. Parasites of Medical Importance (2002), Landes Bioscience, Georgetown, TX
51. Nathan A., Zalipsky S., Ertel S.I., Agathos S.N., Yarmush M.L., and Kohn J. Copolymers of lysine and polyethylene glycol: a new family of functionalized drug carriers. Bioconjug. Chem. 4 (1993) 54-62
52. Nihei C., Fukai Y., and Kita K. Trypanosome alternative oxidase as a target of chemotherapy. Biochim. Biophys. Acta 1587 (2002) 234-239
53. Nihei C., Fukai Y., Kawai K., Osanai A., Yabu Y., Suzuki T., Ohta N., Minagawa N., Nagai K., and Kita K. Purification of active recombinant trypanosome alternative oxidase. FEBS Lett. 538 (2003) 35-40
54. Opperdoes F.R., Aarsen P.N., van der Meer C., and Borst P. Trypanosoma brucei: an evaluation of salicylhydroxamic acid as a trypanocidal drug. Exp. Parasitol. 40 (1976) 198-205
55. Opperdoes F.R., and Borst P. Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett. 80 (1977) 360-364
56. Opperdoes F.R. Compartmentation of carbohydrate metabolism in trypanosomes. Annu. Rev. Microbiol. 41 (1987) 127-151
57. Parr M.J., Ansell S.M., Choi L.S., and Cullis P.R. Factors influencing the retention and chemical stability of poly(ethylene glycol)-lipid conjugates incorporated into large unilamellar vesicles. Biochim. Biophys. Acta 1195 (1994) 21-30
58. Pepin, J., Mpia, B., 2005. Trypanosomiasis relapse after melarsoprol therapy. Democratic Republic of Congo, 1982-2001. Emerg. Infect. Dis. 11, 921-927.
59. Polt R., Porecca F., Szabo L., and Hruby V.J. Synthesis of glycosyl-enkephalin analogs which rapidly cross the blood-brain barrier to produce analgesia in mice-an entirely new class of designer drugs. Glycoconj. J. 10 (1993) 261
60. Priest J.W., and Hajduk S.L. Developmental regulation of mitochondrial biogenesis in Trypanosoma brucei. J. Bioenerg. Biomembr. 26 (1994) 179-191
61. Rodriguez R.E., Rodriguez F.D., Sacristan M.P., Torres J.L., Valencia G., and Garcia Anton J.M. New glycosyl peptides with high antinociceptive activity. Neurosci. Lett. 101 (1989) 89-94
62. Schonbaum G.R., Bonner W.D., Storey B.T., and Bahr J.T. Specific inhibition of the cyanide-resistant respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiol. 47 (1971) 124-128
63. Siedow J.N., and Bickett M.D. Structural features required for inhibition of cyanide-insensitive electron transfer by propyl gallate. Arch. Biochem. Biophys. 207 (1981) 32-39
64. ter Kuile B.H. Membrane related processes and overall energy metabolism in Trypanosoma brucei and other kinetoplastid species. J. Bioenerg. Biomembr. 26 (1994) 167-179
65. Umbach A., and Siedow J. Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol. 103 (1993) 845-854
66. Van derMeer C., Versluijs-Broers J.A.M., and Opperdoes F.R. Trypanosoma brucei: trypanocidal effects of salicylhydroxamic acid plus glycerol in infected rats. Exp. Parasitol. 48 (1979) 126-134
67. van der Meer C., Versluij s-Broers J.A., van Duin C.T., van den Ingh T.S., Nieuwenhuijs J., and Zwart D. Pitfalls of salicylhydroxamic acid plus glycerol treatment of T. vivax infected goats. Tropenmed. Parasitol. 31 (1980) 275-282
68. van derMeer C., and Versluij s-Broers J.A. Trypanosoma brucei and T. vivax: salicylhydroxamic acid and glycerol treatment of acute and chronically infected rats. Exp. Parasitol. 62 (1986) 98-113
69. Verlinde C., Hannaert V., Blonski C., Wilson M., Perie J.J., Fothergill-Gilmore L.A., Opperdoes F.R., Gelb M.H., Hol W.G.J., and Michels P. Glycolysis as a target for the design of new anti-trypanosome drugs. Drug Resist. Updat. 4 (2001) 50-65
70. Vickerman K. Polymorphism and mitochondrial activity in sleeping sickness trypanosomes. Nature 208 (1965) 762-766
71. Vickerman K. Developmental cycles and biology of pathogenic trypanosomes. Br. Med. Bull. 41 (1985) 105-114
72. Wagner A.M., and Moore A.L. Structure and function of the plant alternative oxidase: its putative role in the oxygen defence mechanism. Biosci. Rep. 17 (1997) 319-333
73. Wang C.C. Molecular mechanisms and therapeutic approaches to the treatment of African trypanosomiasis. Annu. Rev. Pharmacol. Toxicol. 35 (1995) 93-127
74. WHO 2001. posting date. African trypanosomiasis or sleeping sickness. WHO [online].
75. Yabu Y., Yoshida A., Suzuki T., Nihei C., Kawai K., Minagawa N., Hosokawa T., Nagai K., Kita K., and Ohta N. The efficacy of ascofuranone in a consecutive treatment on Trypanosoma brucei brucei in mice. Parasitol. Int. 52 (2003) 155-164
76. Yabu Y., Suzuki T., Nihei C., Minagawa N., Hosokawa T., Nagai K., Kita K., and Ohta N. Chemotherapeutic efficacy of ascofuranone in Trypanosoma vivax-infected mice without glycerol. Parasitol. Int. 55 (2006) 39-43