Amelioration of cryptosporidium parvum infection in vitro and in vivo by targeting parasite fatty acyl-coenzyme a synthetases

Journal of Infectious Diseases

Volumn 209, Issue 8, 2014, Pages 1279-1287

  Guo, Fengguang ^a   Zhang, Haili ^a   Fritzler, Jason M ^b   Rider, S Dean ^c   Xiang, Lixin ^a,f   Mcnair, Nina N ^d   Mead, Jan R ^d,e   Zhu, Guan ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b WEBER STATE UNIVERSITY   (United States)

^c WRIGHT STATE UNIVERSITY   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e ATLANTA VA MEDICAL CENTER   (United States)

^f ZHEJIANG UNIVERSITY   (China)

Author keywords

anti cryptosporidial efficacy; cryptosporidiosis; Cryptosporidium parvum; long chain fatty acyl CoA synthetase; triacsin C

Indexed keywords

ANTIPROTOZOAL AGENT; INTERLEUKIN 12; LONG CHAIN FATTY ACID COENZYME A LIGASE; TRIACSIN C; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICRYPTOSPORIDIAL ACTIVITY; ANTIPROTOZOAL ACTIVITY; ARTICLE; COLORIMETRY; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MICROBIAL GROWTH; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANTI-CRYPTOSPORIDIAL EFFICACY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; LONG CHAIN FATTY ACYL-COA SYNTHETASE; TRIACSIN C;

ANIMALS; CELL CULTURE TECHNIQUES; CLONING, ORGANISM; COENZYME A LIGASES; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; ENZYME INHIBITORS; HUMANS; MICE; TRIAZENES;

EID: 84897466212     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit645     Document Type: Article

References (46)

1. Chen XM, Keithly JS, Paya CV, LaRusso NF. Cryptosporidiosis. N Engl J Med 2002; 346:1723-31.
2. Kotloff KL, Nataro JP, Blackwelder WC, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): A prospective, case-control study. Lancet 2013; 382:209-222.
3. Abrahamsen MS, Templeton TJ, Enomoto S, et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 2004; 304:441-5.
4. Rider SD Jr, Zhu G. Cryptosporidium: Genomic and biochemical features. Exp Parasitol 2010; 124:2-9.
5. Andersson CS, Lundgren CA, Magnusdottir A, et al. The Mycobacterium tuberculosis very-long-chain fatty acyl-CoA synthetase: Structural basis for housing lipid substrates longer than the enzyme. Structure 2012; 20:1062-70.
6. Weimar JD, DiRusso CC, Delio R, Black PN. Functional role of fatty acyl-coenzyme A synthetase in the transmembrane movement and activation of exogenous long-chain fatty acids: Amino acid residues within the ATP/AMP signature motif of Escherichia coli FadD are required for enzyme activity and fatty acid transport. J Biol Chem 2002; 277: 29369-76.
7. Zou Z, Tong F, Faergeman NJ, Borsting C, Black PN, DiRusso CC. Vectorial acylation in Saccharomyces cerevisiae. Fat1p and fatty acyl-CoA synthetase are interacting components of a fatty acid import complex. J Biol Chem 2003; 278:16414-22.
8. Fujino T, Kang MJ, Suzuki H, Iijima H, Yamamoto T. Molecular characterization and expression of rat acyl-CoA synthetase 3. J Biol Chem 1996; 271:16748-52.
9. Berthiaume L, Deichaite I, Peseckis S, Resh MD. Regulation of enzymatic activity by active site fatty acylation: A new role for long chain fatty acid acylation of proteins. J Biol Chem 1994; 269:6498-505.
10. Marin EP, Derakhshan B, Lam TT, Davalos A, Sessa WC. Endothelial cell palmitoylproteomic identifies novel lipid-modified targets and potential substrates for protein acyl transferases. Circ Res 2012; 110: 1336-44.
11. Tomoda H, Igarashi K, Cyong JC, Omura S. Evidence for an essential role of long chain acyl-CoA synthetase in animal cell proliferation: Inhibition of long chain acyl-CoA synthetase by triacsins caused inhibition of Raji cell proliferation. J Biol Chem 1991; 266:4214-9.
12. Glick BS, Rothman JE. Possible role for fatty acyl-coenzyme-A in intracellular protein-Transport. Nature 1987; 326:309-312.
13. Korchak HM, Kane LH, Rossi MW, Corkey BE. Long chain acyl coenzyme A and signaling in neutrophils: An inhibitor of acyl coenzyme A synthetase, triacsin C, inhibits superoxide anion generation and degranulation by human neutrophils. J Biol Chem 1994; 269:30281-7.
14. Faergeman NJ, Knudsen J. Role of long-chain fatty acyl-CoA esters in the regulation of metabolism and in cell signalling. Biochem J 1997; 323(Pt 1):1-12.
15. Matesanz F, Tellez MM, Alcina A. The Plasmodium falciparum fatty acyl-CoA synthetase family (PfACS) and differential stage-specific expression in infected erythrocytes. Mol Biochem Parasitol 2003; 126: 109-12.
16. Arrowood MJ, Sterling CR. Isolation of Cryptosporidium oocysts and sporozoites using discontinuous sucrose and isopycnic percoll gradients. J Parasitol 1987; 73:314-319.
17. Zhang H, Guo F, Zhu G. Involvement of host cell integrin alpha2 in Cryptosporidium parvum infection. Infect Immun 2012; 80:1753-8.
18. Guo F, Zhu G. Presence and removal of a contaminating NADH oxidation activity in recombinant maltose-binding protein fusion proteins expressed in Escherichia coli. BioTechniques 2012; 52:247-53.
19. Bernson VSM. Acetyl-CoA hydrolase: Activity, regulation and physiological significance of enzyme in brown adipose-Tissue from hamster. Eur J Biochem 1976; 67:403-410.
20. Zhuravleva E, Gut H, Hynx D, et al. Acyl coenzyme A thioesterase Them5/Acot15 is involved in cardiolipin remodeling and fatty liver development. Mol Cell Biol 2012; 32:2685-97.
21. Cai X, Woods KM, Upton SJ, Zhu G. Application of quantitative realtime reverse transcription-PCR in assessing drug efficacy against the intracellular pathogen Cryptosporidium parvum in vitro. Antimicrob Agents Chemother 2005; 49:4437-42.
22. Fritzler JM, Zhu G. Novel anti-Cryptosporidium activity of known drugs identified by high-Throughput screening against parasite fatty acyl-CoA binding protein (ACBP). J Antimicrob Chemother 2012; 67: 609-17.
23. Campbell LD, Stewart JN, Mead Jr. Susceptibility to Cryptosporidium parvum infections in cytokine-And chemokine-receptor knockout mice. J Parasitol 2002; 88:1014-6.
24. Arrowood MJ, Hurd MR, Mead Jr. A new method for evaluating experimental cryptosporidial parasite loads using immunofluorescent flow cytometry. J Parasitol 1995; 81:404-9.
25. Arrowood MJ, Donaldson K. Improved purification methods for calfderived Cryptosporidium parvum oocysts using discontinuous sucrose and cesium chloride gradients. J Eukaryot Microbiol 1996; 43:89S.
26. Matesanz F, Duran-Chica I, Alcina A. The cloning and expression of Pfacs1, a Plasmodium falciparum fatty acyl coenzyme A synthetase-1 targeted to the host erythrocyte cytoplasm. J Mol Biol 1999; 291:59-70.
27. Fritzler JM, Zhu G. Functional characterization of the acyl-[acyl carrier protein] ligase in the Cryptosporidium parvum giant polyketide synthase. Int J Parasitol 2007; 37:307-16.
28. Ichihara K, Shibasaki Y. An enzyme-coupled assay for acyl-CoA synthetase. J Lipid Res 1991; 32:1709-12.
29. Yoshida K, Okamoto M, Umehara K, et al. Studies on new vasodilators, WS-1228 A and B. I. Discovery, taxonomy, isolation and characterization. J Antibiot (Tokyo) 1982; 35:151-6.
30. Tanaka H, Yoshida K, Itoh Y, Imanaka H. Studies on new vasodilators, WS-1228 A and B. II. Structure and synthesis. J Antibiot (Tokyo) 1982; 35:157-63.
31. Tomoda H, Igarashi K, Omura S. Inhibition of acyl-CoA synthetase by triacsins. Biochim Biophys Acta 1987; 921:595-8.
32. Omura S, Tomoda H, Xu QM, Takahashi Y, Iwai Y. Triacsins, new inhibitors of acyl-CoA synthetase produced by Streptomyces sp. J Antibiot (Tokyo) 1986; 39:1211-8.
33. Hartman EJ, Omura S, Laposata M. Triacsin C: A differential inhibitor of arachidonoyl-CoA synthetase and nonspecific long chain acyl-CoA synthetase. Prostaglandins 1989; 37:655-71.
34. Vessey DA, Kelley M, Warren RS. Characterization of triacsin C inhibition of short-, medium-, and long-chain fatty acid: CoA ligases of human liver. J Biochem Mol Toxicol 2004; 18:100-6.
35. Kim JH, Lewin TM, Coleman RA. Expression and characterization of recombinant rat acyl-CoA synthetases 1, 4, and 5. Selective inhibition by triacsin C and thiazolidinediones. J Biol Chem 2001; 276: 24667-73.
36. Van Horn CG, Caviglia JM, Li LO,Wang S, Granger DA, Coleman RA. Characterization of recombinant long-chain rat acyl-CoA synthetase isoforms 3 and 6: Identification of a novel variant of isoform 6. Biochemistry 2005; 44:1635-42.
37. Cheng Y, Prusoff WH. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 1973; 22: 3099-108.
38. Stockdale HD, Spencer JA, Blagburn BL. Prophylaxis and chemotherapy. In: Fayer R, Xiao L, eds. Cryptosporidium and cryptosporidiosis. 2nd ed. Boca Raton, FL: CRC Press, 2007; p. 255-88.
39. Mashima T, Sato S, Okabe S, et al. Acyl-CoA synthetase as a cancer survival factor: Its inhibition enhances the efficacy of etoposide. Cancer Sci 2009; 100:1556-62.
40. Matsuda D, Namatame I, Ohshiro T, Ishibashi S, Omura S, Tomoda H. Anti-Atherosclerotic activity of triacsin C, an acyl-CoA synthetase inhibitor. J Antibiot (Tokyo) 2008; 61:318-21.
41. Beaumelle BD, Vial HJ. Acyl-CoA synthetase activity in Plasmodium knowlesi-infected erythrocytes displays peculiar substrate specificities. Biochim Biophys Acta 1988; 958:1-9.
42. Camero L, Shulaw WP, Xiao L. Characterization of a Cryptosporidium parvum gene encoding a protein with homology to long chain fatty acid synthetase. J Eukaryot Microbiol 2003; 50(Suppl):534-8.
43. Theodos CM, Griffiths JK, D'Onfro J, Fairfield A, Tzipori S. Efficacy of nitazoxanide against Cryptosporidium parvum in cell culture and in animal models. Antimicrob Agents Chemother 1998; 42:1959-65.
44. Fujimoto Y, Onoduka J, Homma KJ, et al. Long-chain fatty acids induce lipid droplet formation in a cultured human hepatocyte in a manner dependent of acyl-CoA synthetase. Biol Pharm Bull 2006; 29:2174-80.
45. Igal RA, Wang P, Coleman RA. Triacsin C blocks de novo synthesis of glycerolipids and cholesterol esters but not recycling of fatty acid into phospholipid: Evidence for functionally separate pools of acyl-CoA. Biochem J 1997; 324(Pt 2):529-34.
46. Xie YL, Pan YE, Chang CJ, et al. Palmitic acid in chicken granulosa cell death-lipotoxic mechanisms mediate reproductive inefficacy of broiler breeder hens. Theriogenology 2012; 78:1917-28.