Molecular cloning, biochemical characterization, and partial protective immunity of the heme-binding glutathione S-transferases from the human hookworm Necator americanus

Infection and Immunity

Volumn 78, Issue 4, 2010, Pages 1552-1563

  Zhan, Bin ^a   Perally, Samirah ^b   Brophy, Peter M ^b   Xue, Jian ^c   Goud, Gaddam ^a   Liu, Sen ^a   Deumic, Vehid ^a   De Oliveira, Luciana M ^a   Bethony, Jeffrey ^a   Bottazzi, Maria Elena ^a   Jiang, Desheng ^a   Gillespie, Portia ^a   Xiao, Shu Hua ^c   Gupta, Richi ^a   Loukas, Alex ^d   Ranjit, Najju ^d   Lustigman, Sara ^e   Oksov, Yelena ^e   Hotez, Peter ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b ABERYSTWYTH UNIVERSITY   (United Kingdom)

^c CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^e NEW YORK BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM HYDROXIDE; AMINO ACID; GLUTATHIONE TRANSFERASE; HEME; LIPID PEROXIDASE; VACCINE;

ADJUVANT THERAPY; AMINO ACID SEQUENCE; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVITY; GLUTATHIONE METABOLISM; HOOKWORM; IMMUNITY; MOLECULAR CLONING; NECATOR AMERICANUS; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORGANISM; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; STATISTICAL SIGNIFICANCE;

ADJUVANTS, IMMUNOLOGIC; ALUMINUM HYDROXIDE; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, HELMINTH; CLONING, MOLECULAR; CRICETINAE; DNA, COMPLEMENTARY; DNA, HELMINTH; GENE EXPRESSION; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HEME; HUMANS; LIPID PEROXIDATION; MOLECULAR SEQUENCE DATA; NECATOR AMERICANUS; NECATORIASIS; OPEN READING FRAMES; PICHIA; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; VACCINES, SUBUNIT;

EID: 77950278221     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00848-09     Document Type: Article

References (70)

1. Albonico, M., Q. Bickle, M. Ramsan, A. Montresor, L. Savioli, and M. Taylor. 2003. Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bull. World Health Organ. 81:343-352.
2. Albonico, M., P. G. Smith, E. Ercole, A. Hall, H. M. Chwaya, K. S. Alawi, and L. Savioli. 1995. Rate of reinfection with intestinal nematodes after treatment of children with mebendazole or albendazole in a highly endemic area. Trans. R. Soc. Trop. Med. Hyg. 89:538-541.
3. Asojo, Q. A., K. Homma, M. Sedlacek, M. Ngamelue, G. N. Goud, B. Zhan, V. Deumic, O. Asojo, and P. J. Hotez. 2007. X-ray structures of Na-GST-1 and Na-GST-2 two glutathione s-transferase from the human hookworm Necator americanus. BMC Struct. Biol. 7:42-53.
4. Balloul, J. M., J. M. Grzych, R. J. Pierce, and A. Capron. 1987. A purified 28,000 dalton protein from Schistosoma mansoni adult worms protects rats and mice against experimental schistosomiasis. J. Immunol. 138:3448-3453.
5. Basavaraju, S., B. Zhan, M. W. Kennedy, Y. Liu, J. Hawdon, and P. J. Hotez. 2003. Ac-FAR-1, a 20 kDa fatty acid- and retinol-binding protein secreted by adult Ancylostoma caninum hookworms: gene transcription pattern, ligand binding properties and structural characterisation. Mol. Biochem. Parasitol. 126:63-71.
6. Bennett, A., and H. Guyatt. 2000. Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. Parasitol. Today 16:71-74.
7. Boulanger, D., A. Warter, B. Sellin, V. Lindner, R. J. Pierce, J. P. Chippaux, and A. Capron. 1999. Vaccine potential of a recombinant glutathione Stransferase cloned from Schistosoma haematobium in primates experimentally infected with a homologous challenge. Vaccine 17:319-326.
8. Boyer, T. D., and E. Olsen. 1991. Role of glutathione S-transferases in heme transport. Biochem. Pharmacol. 42:188-190.
9. Brooker, S., P. J. Hotez, and D. A. P. Bundy. 2008. Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl. Trop. Dis. 2:e291.
10. Brooker, S., A. Jardim-Botelho, R. J. Quinnell, S. M. Geiger, I. R. Caldas, F. Fleming, P. J. Hotez, R. Correa-Oliveira, L. C. Rodrigues, and J. M. Bethony. 2007. Age-related changes in hookworm infection, anemia and iron deficiency in an area of high Necator americanus hookworm transmission in southeastern Brazil. Trans. R. Soc. Trop. Med. Hyg. 101:146-154.
11. Brophy, P. M., and J. Barrett. 1990. Glutathione transferase in helminths. Parasitology 100:345-349.
12. Brophy, P. M., L. H. Patterson, A. Brown, and D. I. Pritchard. 1995. Glutathione S-transferase (GST) expression in the human hookworm Necator americanus: potential roles for excretory-secretory forms of GST. Acta Trop. 59:259-263.
13. Brophy, P. M., and D. I. Pritchard. 1992. Metabolism of lipid peroxidation products by the gastro-intestinal nematodes Necator americanus, Ancylostoma ceylanicum and Heligmosomoides polygyrus. Int. J. Parasitol. 22:1009-1012.
14. Cabot, E. L., and A. T. Beckenbach. 1989. Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput. Appl. Biosci. 5:233-234.
15. Capron, A., G. Riveau, M. Capron, and F. Trottein. 2005. Schistosomes: the road from host-parasite interactions to vaccines in clinical trials. Trends Parasitol. 21:143-149.
16. C. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans, a platform for investigating biology. Science 282:2012-2018.
17. Cervi, L., G. Rossi, and D. T. Masih. 1999. Potential role for excretory-secretory forms of glutathione-S-transferase (GST) in Fasciola hepatica. Parasitology 119:627-633.
18. Chan, M. S. 1997. The global burden of intestinal nematode infections - fifty years on. Parasitol. Today 13:438-443.
19. Chen, J. J., and I. M. London. 1995. Regulation of protein synthesis by heme-regulated eIF-2 alpha kinase. Trends Biochem. Sci. 20:105-108.
20. De Clercq, D., M. Sacko, J. Behnke, F. Gilbert, P. Dorny, and J. Vercruysse. 1997. Failure of mebendazole in treatment of human hookworm infections in the southern region of Mali. Am. J. Trop. Med. Hyg. 57:25-30.
21. DeSilva, N., S. Brooker, P. Hotez, A. Montresor, D. Engels, and L. Savioli. 2003. Soil transmitted helminth infections: updating the global picture. Trends Parasitol. 12:547-551.
22. Diemert, D. J., J. M. Bethony, and P. J. Hotez. 2008. Hookworm vaccines. Clin. Infect. Dis. 46:282-288.
23. Dowling, D. J., C. M. Hamilton, S. Donnelly, J. La Course, P. M. Brophy, J. Dalton, and S. M. O'Neill. 16 November 2009. Major secretory antigens of the helminth Fasciola hepatica activate a suppressive dendritic cell phenotype that attenuates Th17 cells but fails to activate Th2 immune responses. Infect. Immun. doi:10.1128/IAI.00573-09.
24. Ghosh, K., W. Wu, A. D. Antoine, M. E. Bottazzi, J. G. Valenzuela, P. J. Hotez, and S. Mendez. 2006. The impact of concurrent and treated Ancylostoma ceylanicum hookworm infections on the immunogenicity of a recombinant hookworm vaccine in hamsters. J. Infect. Dis. 193:155-162.
25. Görg, A., C. Obermaier, G. Boguth, A. Harder, B. Scheibe, R. Wildgruber, and W. Weiss. 2000. The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21:1037-1053.
26. Goud, G. N., M. E. Bottazzi, B. Zhan, S. Mendez, V. Deumic, J. Plieskatt, S. Liu, Y. Wang, L. Beuno, R. Fujiwara, A. Samuel, S. Y. Ahn, M. Solanki, O. A. Asojo, J. Wang, J. M. Bethony, A. Loukas, M. Roy, and P. J. Hotez. 2005. Expression of the Necator americanus hookworm larval antigen Na-ASP-2 in Pichia pastoris and purification of the recombinant protein for use in human clinical trials. Vaccine 23:4754-4764.
27. Habig, W. H., and W. B. Jakoby. 1981. Assay for differentiation of glutathione S-transferases. Methods Enzymol. 77:398-405.
28. Harwaldt, P., S. Rahlfs, and K. Becker. 2002. Glutathione S-transferase of the malarial parasite Plasmodium falciparum: characterization of a potential drug target. Biol. Chem. 383:821-830.
29. Hawdon, J. M., B. F. Jones, and P. J. Hotez. 1995. Cloning and characterization of a cDNA encoding the catalytic subunit of a cAMP-dependent protein kinase from Ancylostoma caninum third-stage infective larvae. Mol. Biochem. Parasitol. 69:127-130.
30. Hotez, P. J., S. Brooker, J. M. Bethony, M. E. Bottazzi, A. Loukas, and S. H. Xiao. 2004. Hookworm infection. N. Engl. J. Med. 351:799-807.
31. Hotez, P. J., and M. T. Ferris. 2006. The antipoverty vaccines. Vaccine 24:5787-5799.
32. Hotez, P. J., B. Zhan, J. Bethony, J. Qun, J. M. Hawdon, H. A. Young, S. Simmens, R. Hitzelberg, and B. C. Zook. 2002. Natural history of primary canine hookworm infections after three different oral doses of third-stage infective larvae of Ancylostoma caninum. Comp. Parasitol. 69:72-80.
33. Jaffe, E. K. 2003. An unusual phylogenetic variation in the metal ion binding sites of porphobilinogen synthase. Chem. Biol. 10:25-34.
34. Kampkotter, A., T. E. Volkmann, S. H. de Castro, B. Leiers, L. O. Klotz, T. E. Johnson, C. D. Link, and K. Henkle-Duhrsen. 2003. Functional analysis of the glutathione S-transferase 3 from Onchocerca volvulus (Ov-GST-3): a parasite GST confers increased resistance to oxidative stress in Caenorhabditis elegans. J. Mol. Biol. 325:25-37.
35. Keiser, J., and J. Utzinger. 2008. Efficacy of current drugs against soiltransmitted helminth infections: systematic review and meta-analysis. JAMA 299:1937-1948.
36. Lathrop, J. T., and M. P. Timko. 1993. Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259:522-525.
37. Lewis, D. F. 2004. 57 varieties: the human cytochromes P450. Pharmacogenomics 5:305-318.
38. Loukas, A., J. Bethony, S. Brooker, and P. Hotez. 2006. Hookworm vaccines: past, present, and future. Lancet Infect. Dis. 6:733-741.
39. Loukas, A., A. P. Brown, and D. I. Pritchard. 2002. Na-ctl-2, a cDNA encoding a C-type lectin expressed exclusively in adult Necator americanus hookworms. DNA Seq. 13:61-65.
40. Lustigman, S., B. Brotman, T. Huima, A. M. Prince, and J. H. McKerrow. 1992. Molecular cloning and characterization of onchocystatin, a cysteine proteinase inhibitor of Onchocerca volvulus. J. Biol. Chem. 267:17339-17346.
41. McManus, D. P., and A. Loukas. 2008. Current status of vaccines for schistosomiasis. Clin. Microbiol. Rev. 21:225-242.
42. Mendez, S., J. G. Valenzuela, W. Wu, and P. J. Hotez. 2005. Host cytokine production, lymphoproliferation, and antibody responses during the course of Ancylostoma ceylanicum infection in the Golden Syrian hamster. Infect. Immun. 73:3402-3407.
43. Mendez, S., B. Zhan, G. Goud, K. Ghosh, A. Dobardzic, W. Wu, S. Liu, V. Deumic, R. Dobardzic, Y. Liu, J. Bethony, and P. J. Hotez. 2005. Effect of combining the larval antigens Ancylostoma secreted protein 2 (ASP-2) and metalloprotease 1 (MTP-1) in protecting hamsters against hookworm infection and disease caused by Ancylostoma ceylanicum. Vaccine 23:3123-3130.
44. Meshnick, S. R., S. H. Blobstein, R. W. Grady, and A. Cerami. 1978. An approach to the development of new drugs for African trypanosomiasis. J. Exp. Med. 148:569-579.
45. Morgan, C., E. J. LaCourse, B. J. Rushbrook, D. Greetham, J. V. Hamilton, J. Barrett, K. Bailey, and P. M. Brophy. 2006. Plasticity demonstrated in the proteome of a parasitic nematode within the intestine of different host strains. Proteomics 6:4633-4645.
46. Nakajima, O., S. Takahashi, H. Harigae, K. Furuyama, N. Hayashi, S. Sassa, and M. Yamamoto. 1999. Heme deficiency in erythroid lineage causes differentiation arrest and cytoplasmic iron overload. EMBO J. 18:6282-6289.
47. Nguyen, P. H., K. C. Nguyen, B. Le Mai, T. V. Nguyen, K. H. Ha, C. Bern, R. Flores, and R. Martorell. 2006. Risk factors for anemia in Vietnam. Southeast Asian J. Trop. Med. Public Health 37:1-11.
48. Page, R. D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
49. Perally, S., E. J. LaCourse, A. M. Campbell, and P. M. Brophy. 2008. Heme trafficking and detoxification in nematodes: subproteomics evidence of differential role of glutathione transferases. J. Proteome Res. 7:4557-4565.
50. Qi, Z., I. Hamza, and M. R. O'Brian. 1999. Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc. Natl. Acad. Sci. U. S. A. 96:13056-13061.
51. Rao, A. U., L. K. Carta, E. Lesuisse, and I. Hamza. 2005. Lack of heme synthesis in a free-living eukaryote. Proc. Natl. Acad. Sci. U. S. A. 102:4270-4275.
52. Roche, M., and M. Layrisse. 1966. Nature and causes of "hookworm anemia." Am. J. Trop. Med. Hyg. 15:1029-1102.
53. Rodgers, K. R. 1999. Heme-based sensors in biological systems. Curr. Opin. Chem. Biol. 3:158-167.
54. Schuller, D. J., Q. Liu, I. A. Kriksunov, A. M. Campbell, J. Barrett, P. M. Brophy, and Q. Hao. 2005. Crystal structure of a new class of glutathione transferase from the model human hookworm nematode Heligmosomoides polygyrus. Proteins 61:1024-1031.
55. Stoltzfus, R. J., M. L. Dreyfuss, H. M. Chwaya, and M. Albonico. 1997. Hookworm control as a strategy to prevent iron deficiency. Nutr. Rev. 55: 223-232.
56. Sun, J., H. Hoshino, K. Takaku, O. Nakajima, A. Muto, H. Suzuki, S. Tashiro, S. Takahashi, S. Shibahara, and J. Alam. 2002. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J. 21:5216-5224.
57. Torres-Rivera, A., and A. Landa. 2008. Glutathione transferases from parasites: a biochemical view. Acta Trop. 105:99-112.
58. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76:4350-4354.
59. van Rossum, A. J., J. R. Jefferies, F. A. Rijsewijk, E. J. LaCourse, P. Teesdale-Spittle, J. Barrett, A. Tait, and P. M. Brophy. 2004. Binding of hematin by a new class of glutathione transferase from the blood-feeding parasitic nematode Haemonchus contortus. Infect. Immun. 72:2780-2790.
60. Wenger, R. H. 2000. Mammalian oxygen sensing, signalling and gene regulation. J. Exp. Biol. 203(Pt. 8):1253-1263.
61. W.H.O. 2005. Deworming for health and development. Report of the third global meeting of the partners for parasite control. World Health Organization, Geneva, Switzerland.
62. Williamson, A. L., P. J. Brindley, G. Abbenante, P. Prociv, C. Berry, K. Girdwood, D. I. Pritchard, D. P. Fairlie, P. J. Hotez, J. P. Dalton, and A. Loukas. 2002. Cleavage of hemoglobin by hookworm cathepsin D aspartic proteases and its potential contribution to host specificity. FASEB J. 16: 1458-1460.
63. Williamson, A. L., P. Lecchi, B. E. Turk, Y. Choe, P. J. Hotez, J. H. McKerrow, L. C. Cantley, M. Saiid, C. S. Craik, and A. Loukas. 2004. A multi-enzyme cascade of hemoglobin proteolysis in the intestine of bloodfeeding hookworms. J. Biol. Chem. 279:35950-35957.
64. Wu, B., L. Conway, J. Novelli, J. Foster, and B. Slatko. 2008. Wolbachia heme biosynthesis as a potential anti-filariasis target set. Am. J. Trop. Med. Hyg. 79:516.
65. Xiao, S., B. Zhan, J. Xue, G. N. Goud, A. Loukas, Y. Liu, A. Williamson, S. Liu, V. Deumic, and P. Hotez. 2008. The evaluation of recombinant hookworm antigens as vaccines in hamsters (Mesocricetus auratus) challenged with human hookworm, Necator americanus. Exp. Parasitol. 118:32-40.
66. Xue, J., S. H. Xiao, H. Q. Qiang, S. Liu, P. Hotez, B. G. Shen, H. C. Xue, T. H. Li, and B. Zhan. 2003. Necator americanus: maintenance through one hundred generations in golden hamsters (Mesocricetus auratus). II. Morphological development of the adult and its comparison with humans. Exp. Parasitol. 105:192-200.
67. Zhan, B., M. Badamchian, B. Meihua, J. Ashcom, J. Feng, J. Hawdon, X. Shuhua, and P. J. Hotez. 2002. Molecular cloning and purification of Ac-TMP, a developmentally regulated putative tissue inhibitor of metalloprotease released in relative abundance by adult Ancylostoma hookworms. Am. J. Trop. Med. Hyg. 66:238-244.
68. Zhan, B., J. Hawdon, Q. Shan, H. Ren, H. Qiang, S. H. Xiao, T. H. Li, Z. Feng, and P. Hotez. 2000. Construction and analysis of cDNA library of the third stage larvae of Necator americanus. Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi 18:26-28.
69. Zhan, B., S. Liu, S. Perally, J. Xue, R. Fujiwara, P. M. Brophy, S. Xiao, Y. Liu, J. Feng, A. Williamson, Y. Wang, L. L. Bueno, S. Mendez, G. Goud, J. M. Bethony, J. M. Hawdon, A. Loukas, K. Jones, and P. J. Hotez. 2005. Biochemical characterization and vaccine potential of a heme-binding glutathione transferase from the adult hookworm Ancylostoma caninum. Infect. Immun. 73:6903-6911.
70. Zhan, B., Y. Wang, Y. Liu, A. Williamson, A. Loukas, J. M. Hawdon, H. Xue, S. Xiao, and P. J. Hotez. 2004. Ac-SAA-1, an immunodominant 16 kDa surface-associated antigen of infective larvae and adults of Ancylostoma caninum. Int. J. Parasitol. 34:1037-1045.