Purification and Molecular Cloning of and Immunization with Ancylostoma ceylanicum Excretory-Secretory Protein 2, An Immunoreactive Protein Produced by Adult Hookworms

Infection and Immunity

Volumn 72, Issue 4, 2004, Pages 2203-2213

  Bungiro Jr , Richard D ^a   Solis, Carolina V ^a   Harrison, Lisa M ^a   Cappello, Michael ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM POTASSIUM SULFATE; AMINO ACID; ANCYLOSTOMA CEYLANICUM EXCRETORY SECRETORY PROTEIN 2; ANTIBODY; COMPLEMENTARY DNA; PROTEIN; RECOMBINANT ANCYLOSTOMA CEYLANICUM EXCRETORY SECRETORY PROTEIN 2; RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANCYLOSTOMA CEYLANICUM; ANEMIA; ANIMAL MODEL; ANTIGEN ANTIBODY REACTION; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HAMSTER; HOOKWORM; HOOKWORM INFECTION; HOST PARASITE INTERACTION; IMMUNIZATION; IMMUNOREACTIVITY; MOLECULAR CLONING; MORBIDITY; NONHUMAN; PARASITOSIS; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; VACCINATION; WEIGHT REDUCTION; WESTERN BLOTTING;

ADMINISTRATION, ORAL; AMINO ACID SEQUENCE; ANCYLOSTOMA; ANCYLOSTOMIASIS; ANIMALS; ANTIBODIES, HELMINTH; ANTIGENS, HELMINTH; BASE SEQUENCE; CLONING, MOLECULAR; CRICETINAE; HELMINTH PROTEINS; IMMUNIZATION; IMMUNIZATION, PASSIVE; INJECTIONS, SUBCUTANEOUS; MESOCRICETUS; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; VACCINES;

EID: 1842484056     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.4.2203-2213.2004     Document Type: Article

References (69)

1. Albonico, M., D. W. Crompton, and L. Savioli. 1999. Control strategies for human intestinal nematode infections. Adv. Parasitol. 42:277-341.
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. Awasthi, S., D. A. Bundy, and L. Savioli. 2003. Helminthic infections. Br. Med. J. 327:431-433.
4. 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.
5. Behnke, J. M., J. Guest, and R. Rose. 1997. Expression of acquired immunity to the hookworm Ancylostoma ceylanicum in hamsters. Parasite Immunol. 19:309-318.
6. Behnke, J. M. 1987. Do hookworms elicit protective immunity in man? Parasitol. Today 3:200-206.
7. Blaxter, M. 2000. Genes and genomes of Necator americanus and related hookworms. Int. J. Parasitol. 30:347-355.
8. Borkow, G., Q. Leng, Z. Weisman, M. Stein, N. Galai, A. Kalinkovich, and Z. Bentwich. 2000. Chronic immune activation associated with intestinal helminth infections results in impaired signal transduction and anergy. J. Clin. Investig. 106:1053-1060.
9. Borkow, G., Z. Weisman, Q. Leng, M. Stein, A. Kalinkovich, D. Wolday, and Z. Bentwich. 2001. Helminths, human immunodeficiency virus and tuberculosis. Scand. J. Infect. Dis. 33:568-571.
10. Bouvet, J. P., N. Decroix, and P. Pamonsinlapatham. 2002. Stimulation of local antibody production: parenteral or mucosal vaccination? Trends Immunol. 23:209-213.
11. Bouvet, J. P., and V. A. Fischetti. 1999. Diversity of antibody-mediated immunity at the mucosal barrier. Infect. Immun. 67:2687-2691.
12. Bungiro, R. D., L. M. Harrison, and M. Cappello. 2002. Ancylostoma ceylanicum excretory/secretory protein 1: purification and molecular cloning of a major secretory protein from adult hookworms. Mol. Biochem. Parasitol. 119:147-151.
13. Bungiro, R. D., Jr., B. R. Anderson, and M. Cappello. 2003. Oral transfer of adult Ancylostoma ceylanicum hookworms into permissive and nonpermissive host species. Infect. Immun. 71:1880-1886.
14. Bungiro, R. D., Jr., J. Greene, E. Kruglov, and M. Cappello. 2001. Mitigation of hookworm disease by immunization with soluble extracts of Ancylostoma ceylanicum. J. Infect. Dis. 183:1380-1387.
15. Cappello, M., L. P. Clyne, P. McPhedran, and P. J. Hotez. 1993. Ancylostoma factor Xa inhibitor: partial purification and its identification as a major hookworm-derived anticoagulant in vitro. J. Infect. Dis. 167:1474-1477.
16. Cappello, M., L. M. Harrison, R. D. Bungiro, Jr., R. C. Chadderdon, A. Milstone, A. Nerlinger, and P. Kuzmic. 2003. Molecular pathogenesis of hookworm anemia: prospects for a disease-based vaccine. J. Parasitol. 89: S158-S164.
17. Cappello, M., J. M. Hawdon, B. F. Jones, W. P. Kennedy, and P. J. Hotez. 1996. Ancylostoma caninum anticoagulant peptide: cloning by PCR and expression of soluble, active protein in E. coli. Mol. Biochem. Parasitol. 80:113-117.
18. Cappello, M., G. P. Vlasuk, P. W. Bergum, S. Huang, and P. J. Hotez. 1995. Ancylostoma caninum anticoagulant peptide: a hookworm-derived inhibitor of human coagulation factor Xa. Proc. Natl. Acad. Sci. 92:6152-6156.
19. Carroll, S. M., and D. I. Grove. 1986. Response of dogs to challenge with Ancylostoma ceylanicum during the tenure of a primary hookworm infection. Trans. R. Soc. Trop. Med. Hyg. 80:406-411.
20. Chadderdon, R. C., and M. Cappello. 1999. The hookworm platelet inhibitor: functional blockade of integrins GPIIb/IIIa (alphaIIbbeta3) and GPIa/IIa (alpha2beta1) inhibits platelet aggregation and adhesion in vitro. J. Infect. Dis. 179:1235-1241.
21. Chan, M. S., G. F. Medley, D. Jamison, and D. A. Bundy. 1994. The evaluation of potential global morbidity attributable to intestinal nematode infections. Parasitology 109:373-387.
22. Chu, D., R. D. Bungiro, Jr., M. Ibanez, L. M. Harrison, E. Campodonico, B. F. Jones, J. Mieszczanek, P. Kuzmic, and M. Cappello. 2004. Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine protease inhibitor: evidence for a role in hookworm-associated growth delay. Infect. Immun. 72:2214-2221.
23. Crompton, D. W. 1999. How much human helminthiasis is there in the world? J. Parasitol. 85:397-403.
24. Crompton, D. W., and M. C. Nesheim. 2002. Nutritional impact of intestinal helminthiasis during the human life cycle. Annu. Rev. Nutr. 22:35-59.
25. Daub, J., A. Loukas, D. I. Pritchard, and M. Blaxter. 2000. A survey of genes expressed in adults of the human hookworm, Necator americanus. Parasitology 120:171-184.
26. 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.
27. Del Valle, A., B. F. Jones, L. M. Harrison, R. C. Chadderdon, and M. Cappello. 2003. Isolation and molecular cloning of a secreted hookworm platelet inhibitor from adult Ancylostoma caninum. Mol. Biochem. Parasitol. 129:167-177.
28. Despommier, D. D., R. W. Gwadz, P. J. Hotez, and C. A. Knirsch. 2000. Parasitic diseases, 4th ed., p. 111-118. Apple Trees Productions, LLC, New York, N.Y.
29. Garside, P., and J. M. Behnke. 1989. Ancylostoma ceylanicum in the hamster: observations on the host-parasite relationship during primary infection. Parasitology 98:283-289.
30. Garside, P., J. M. Behnke, and R. A. Rose. 1990. Acquired immunity to Ancylostoma ceylanicum in hamsters. Parasite Immunol. 12:247-258.
31. Ghosh, K., and P. J. Hotez. 1999. Antibody-dependent reductions in mouse hookworm burden after vaccination with Ancylostoma caninum secreted protein 1. J. Infect. Dis. 180:1674-1681.
32. Harrop, S. A., P. Prociv, and P. J. Brindley. 1996. Acasp, a gene encoding a cathepsin D-like aspartic protease from the hookworm Ancylostoma caninum. Biochem. Biophys. Res. Commun. 227:294-302.
33. Harrop, S. A., N. Sawangjaroen, P. Prociv, and P. J. Brindley. 1995. Characterization and localization of cathepsin B proteinases expressed by adult Ancylostoma caninum hookworms. Mol. Biochem. Parasitol. 71:163-171.
34. Holmgren, J., C. Czerkinsky, K. Eriksson, and A. Mharandi. 2003. Mucosal immunisation and adjuvants: a brief overview of recent advances and challenges. Vaccine 21(Suppl. 2):S89-S95.
35. Hotez, P. J., and D. I. Pritchard. 1995. Hookworm infection. Sci. Am. 272:68-74.
36. Hotez, P. J., B. Zhan, J. M. Bethony, A. Loukas, A. Williamson, G. N. Goud, J. M. Hawdon, A. Dobardzic, R. Dobardzic, K. Ghosh, M. E. Bottazzi, S. Mendez, B. Zook, Y. Wang, S. Liu, I. Essiet-Gibson, S. Chung-Debose, S. Xiao, D. Knox, M. Meagher, M. Inan, R. Correa-Oliveira, P. Vilk, H. R. Shepherd, W. Brandt, and P. K. Russell. 2003. Progress in the development of a recombinant vaccine for human hookworm disease: The Human Hookworm Vaccine Initiative. Int. J. Parasitol. 33:1245-1258.
37. Jones, B. F., and P. J. Hotez. 2002. Molecular cloning and characterization of Ac-mep-1, a developmentally regulated gut luminal metalloendopeptidase from adult Ancylostoma caninum hookworms. Mol. Biochem. Parasitol. 119:107-116.
38. Kasper, G., A. Brown, M. Eberl, L. Vallar, N. Kieffer, C. Berry, K. Girdwood, P. Eggleton, R. Quinnell, and D. I. Pritchard. 2001. A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signalling domains of some integrins. Parasite Immunol. 23:141-152.
39. Khan, A. M., S. Gupta, J. C. Katiyar, and V. K. Srivastava. 1996. Correlation between degree of protection and humoral antibody response in hamsters immunized with somatic and excretory secretory antigens of Ancylostoma ceylanicum. Indian J. Exp. Biol. 34:1015-1018.
40. Loeb, L., and M. S. Fleisher. 1910. The influence of extracts of Anchylostoma caninum on the coagulation of the blood and on hemolysis. J. Infect. Dis. 7:625-631.
41. 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.
42. Loukas, A., and P. Prociv. 2001. Immune responses in hookworm infections. Clin. Microbiol. Rev. 14:689-703.
43. McGuire, C., W. C. Chan, and D. Wakelin. 2002. Nasal immunization with homogenate and peptide antigens induces protective immunity against Trichinella spiralis. Infect. Immun. 70:7149-7152.
44. Menon, S., and M. K. Bhopale. 1985. Efficacy of UV-irradiated larval vaccine of Ancylostoma ceylanicum (Looss, 1911) in golden hamsters (Mesocricetus auratus). J. Helminthol. 59:287-293.
45. Mieszczanek, J., W. Kofta, and H. Wedrychowicz. 2000. Molecular cloning of a cysteine proteinase cDNA from adult Ancylostoma ceylanicum by the method of rapid amplification of cDNA ends using polymerase chain reaction. Parasitol. Res. 86:993-998.
46. Miller, T. A. 1971. Vaccination against the canine hookworm diseases. Adv. Parasitol. 9:153-183.
47. Milstone, A. M., L. M. Harrison, R. D. Bungiro, P. Kuzmic, and M. Cappello. 2000. A broad spectrum kunitz type serine protease inhibitor secreted by the hookworm Ancylostoma ceylanicum. J. Biol. Chem. 275:29391-29399.
48. Moyle, M., D. L. Foster, D. E. McGrath, S. M. Brown, Y. Laroche, J. De Meutter, P. Stanssens, C. A. Bogowitz, V. A. Fried, J. A. Ely, et al. 1994. A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD11b/CD18. J. Biol. Chem. 269:10008-10015.
49. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
50. Poulain, J., P. Pery, and G. Luffau. 1976. Protection of rats against Nippostrongylus brasiliensis with worm antigens by oral administration. Ann. Immunol. (Paris) 127:209-213.
51. Pritchard, D. I., A. Brown, G. Kasper, P. McElroy, A. Loukas, C. Hewitt, C. Berry, R. Fullkrug, and E. Beck. 1999. A hookworm allergen which strongly resembles calreticulin. Parasite Immunol. 21:439-450.
52. Quinnell, R. J., J. Griffin, M. A. Nowell, A. Raiko, and D. I. Pritchard. 2001. Predisposition to hookworm infection in Papua New Guinea. Trans. R. Soc. Trop. Med. Hyg. 95:139-142.
53. Quinnell, R. J., A. F. Slater, P. Tighe, E. A. Walsh, A. E. Keymer, and D. I. Pritchard. 1993. Reinfection with hookworm after chemotherapy in Papua New Guinea. Parasitology 106:379-385.
54. Reynoldson, J. A., J. M. Behnke, L. J. Pallant, M. G. Macnish, F. Gilbert, S. Giles, R. J. Spargo, and R. C. Thompson. 1997. Failure of pyrantel in treatment of human hookworm infections (Ancylostoma duodenale) in the Kimberley region of north west Australia. Acta Trop. 68:301-312.
55. Santiso, R. 1997. Effects of chronic parasitosis on women's health. Int. J. Gynaecol. Obstet. 58:129-136.
56. Savioli, L., D. Gundy, and A. Tomkins. 1992. Intestinal parasitic infections: a soluble public health problem. Trans. R. Soc. Trop. Med. Hyg. 86:353-354.
57. Schad, G. A., and R. M. Anderson. 1985. Predisposition to hookworm infection in humans. Science 228:1537-1540.
58. Smillie, W. G., and D. L. Augustine. 1926. Hookworm infestation: the effect of varying intensities on the physical condition of school children. Am. J. Dis. Child. 31:151-168.
59. Stassens, P., P. W. Bergum, Y. Gansemans, L. Jespers, Y. Laroche, S. Huang, S. Maki, J. Messens, M. Lauwereys, M. Cappello, P. J. Hotez, I. Lasters, and G. P. Vlasuk. 1996. Anticoagulant repertoire of the hookworm Ancylostoma caninum. Proc. Natl. Acad. Sci. 93:2149-2154.
60. Stoltzfus, R. J., H. M. Chwaya, J. M. Tielsch, K. J. Schulze, M. Albonico, and L. Savioli. 1997. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. Am. J. Clin. Nutr. 65:153-159.
61. Stone, K. L., D. E. McNulty, M. L. LoPresti, J. M. Crawford, R. DeAngelis, and K. R. Williams. 1992. Techniques in protein chemistry III. Academic Press, Inc., New York, N.Y.
62. Tsuji, N., K. Suzuki, H. Kasuga-Aoki, T. Isobe, T. Arakawa, and Y. Matsumoto. 2003. Mice intranasally immunized with a recombinant 16-kilodalton antigen from roundworm Ascaris parasites are protected against larval migration of Ascaris suum. Infect. Immun. 71:5314-5323.
63. Tsuji, N., K. Suzuki, H. Kasuga-Aoki, Y. Matsumoto, T. Arakawa, K. Ishiwata, and T. Isobe. 2001. Intranasal immunization with recombinant Ascaris suum 14-kilodalton antigen coupled with cholera toxin B subunit induces protective immunity to A. suum infection in mice. Infect. Immun. 69:7285-7292.
64. Williams, K. R., S. M. Samandar, K. L. Stone, M. Saylor, and J. Rush. 1996. Matrix-assisted laser desorption ionization mass spectrometry as a complement to internal protein sequencing, p. 541-555. In J. M. Walker (ed.), The protein protocols handbook. Humana Press, Totowa, N.J.
65. 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.
66. World Health Organization. 1996. Report of the W. H. O. informal consultation on hookworm infection and anaemia in girls and women. Publication W. H. O./CTD/SIP/96.1. World Health Organization, Geneva, Switzerland.
67. World Health Organization. 2002. The world health report 2002: reducing risks, promoting healthy life. World Health Organization, Geneva, Switzerland.
68. Xlao, S., H. Ren, Y. Yang, H. Xue, H. Qiang, S. Liu, Z. Feng, and P. J. Hotez. 1998. Protective immunity in mice elicited by living infective third-stage hookworm larvae (Shanghai strain of Ancylostoma caninum). Chin. Med. J. (Engl. Ed.) 111:43-48.
69. 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.