A multi-enzyme cascade of hemoglobin proteolysis in the intestine of blood-feeding hookworms

Journal of Biological Chemistry

Volumn 279, Issue 34, 2004, Pages 35950-35957

  Williamson, Angela L ^a   Lecchi, Paolo ^b   Turk, Benjamin E ^c,d   Choe, Youngchool ^e   Hotez, Peter J ^a   McKerrow, James H ^e   Cantley, Lewis C ^c,d   Sajid, Mohammed ^e   Craik, Charles S ^e   Loukas, Alex ^a,f,g  

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

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^g UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; BLOOD;

CANINE HOOKWORM; PATHOGENS;

ENZYME KINETICS;

ASPARTIC PROTEINASE; CYSTEINE PROTEINASE; GLOBIN; HEMOGLOBIN; HEMOGLOBIN A; HEMOGLOBIN BETA CHAIN; METALLOPROTEINASE; PEPTIDE LIBRARY; RECOMBINANT PROTEIN;

ANCYLOSTOMA CANINUM; ANIMAL CELL; ARTICLE; BINDING SITE; COMBINATORIAL CHEMISTRY; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME MECHANISM; ENZYME REGULATION; GENETIC RECOMBINATION; HEMOGLOBIN DETERMINATION; HOOKWORM; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRITION; PLASMODIUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM; VACCINE PRODUCTION;

ANCYLOSTOMA; ANCYLOSTOMIASIS; ANIMALS; ASPARTIC ENDOPEPTIDASES; CYSTEINE ENDOPEPTIDASES; DOGS; HEMOGLOBINS; HYDROLYSIS; INTESTINES; METALLOPROTEASES; PEPTIDE HYDROLASES; RECOMBINANT PROTEINS;

ANCYLOSTOMA; ANCYLOSTOMA CANINUM; ANCYLOSTOMATOIDEA; ANIMALIA; CESTODA;

EID: 4143054944     PISSN: 00219258     EISSN: None     Source Type: Journal    
DOI: 10.1074/jbc.M405842200     Document Type: Article

References (59)

1. Francis, S. E., Gluzman, I. Y., Oksman, A., Knickerbocker, A., Mueller, R., Bryant, M. L., Sherman, D. R., Russell, D. G., and Goldberg, D. E. (1994) EMBO J. 13, 306-317
2. Gluzman, I. Y., Francis, S. E., Oksman, A., Smith, C. E., Duffin, K. L., and Goldberg, D. E. (1994) J. Clin. Investig. 93, 1602-1608
3. Goldberg, D. E., Slater, A. F., Cerami, A., and Henderson, G. B. (1990) Proc. Natl. Acad. Sci. U. S. A. 87, 2931-2935
4. Salas, F., Fichmann, J., Lee, G. K., Scott, M. D., and Rosenthal, P. J. (1995) Infect. Immun. 63, 2120-2125
5. Shenai, B. R., Sijwali, P. S., Singh, A., and Rosenthal, P. J. (2000) J. Biol. Chem. 275, 29000-29010
6. Sijwali, P. S., Shenai, B. R., Gut, J., Singh, A., and Rosenthal, P. J. (2001) Biochem. J. 360, 481-489
7. Eggleson, K. K., Duffin, K. L., and Goldberg, D. E. (1999) J. Biol. Chem. 274, 32411-32417
8. Lawrence, J. D. (1973) J. Parasitol. 59, 60-63
9. Hu, W., Yan, Q., Shen, D. K., Liu, F., Zhu, Z. D., Song, H. D., Xu, X. R., Wang, Z. J., Rong, Y. P., Zeng, L. C., Wu, J., Zhang, X., Wang, J. J., Xu, X. N., Wang, S. Y., Fu, G., Zhang, X. L., Wang, Z. Q., Brindley, P. J., McManus, D. P., Xue, C. L., Feng, Z., Chen, Z., and Han, Z. G. (2003) Nat. Genet. 35, 139-147
10. Brindley, P. J., Kalinna, B. H., Dalton, J. P., Day, S. R., Wong, J. Y., Smythe, M. L., and McManus, D. P. (1997) Mol. Biochem. Parasitol. 89, 1-9
11. Caffrey, C. R., McKerrow, J. H., Salter, J. P., and Sajid, M. (2004) Trends Parasitol. 20, 241-248
12. Hotez, P. J., Brooker, S., Bethony, J. M., Bottazzi, M. E., Loukas, A., and Xiao, S. H. (2004) New Eng. J. Med., in press
13. de Silva, N. R., Brooker, S., Hotez, P. J., Montresor, A., Engels, D., and Savioli, L. (2003) Trends Parasitol. 19, 547-551
14. Hotez, P. J. (2002) China Q. 172, 1029-1041
15. Cappello, M., Vlasuk, G. P., Bergum, P. W., Huang, S., and Hotez, P. J. (1995) Proc. Natl. Acad. Sci. U. S. A. 92, 6152-6156
16. Stassens, P., Bergum, P. W., Gansemans, Y., Jespers, L., Laroche, Y., Huang, S., Maki, S., Messens, J., Lauwereys, M., Cappello, M., Hotez, P. J., Lasters, I., and Vlasuk, G. P. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 2149-2154
17. Don, T. A., Jones, M. K., Smyth, D., O'Donoghue, P., Hotez, P. J., and Loukas, A. (2004) Int. J. Parasitol., in press
18. Williamson, A. L., Brindley, P. J., Knox, D. P., Hotez, P. J., and Loukas, A. (2003) Trends Parasitol. 19, 417-423
19. Williamson, A. L., Brindley, P. J., Abbenante, G., Prociv, P., Berry, C., Girdwood, K., Pritchard, D. I., Fairlie, D. P., Hotez, P. J., Zhan, B., and Loukas, A. (2003) J. Infect. Dis. 187, 484-494
20. Williamson, A. L., Brindley, P. J., Abbenante, G., Prociv, P., Berry, C., Girdwood, K., Pritchard, D. I., Fairlie, D. P., Hotez, P. J., Dalton, J. P., and Loukas, A. (2002) FASEB J. 16, 1458-1460
21. Loukas, A., Bethony, J., Williamson, A., Goud, G., Mendez, S., Zhan, B., Hawdon, J. M., Bottazzi, M. E., Brindley, P. J., and Hotez, P. (2004) J. Infect. Dis. 189, 1952-1961
22. Brown, A., Burleigh, J. M., Billett, E. E., and Pritchard, D. I. (1995) Parasitology 110, 555-563
23. Harrop, S. A., Prociv, P., and Brindley, P. J. (1996) Biochem. Biophys. Res. Commun. 227, 294-302
24. Harrop, S. A., Sawangjaroen, N., Prociv, P., and Brindley, P. J. (1995) Mol. Biochem. Parasitol. 71, 163-171
25. Jones, B. F., and Hotez, P. J. (2002) Mol. Biochem. Parasitol. 119, 107-116
26. Zhan, B., Hotez, P. J., Wang, Y., and Hawdon, J. M. (2002) Mol. Biochem. Parasitol. 120, 291-296
27. Williamson, A. L., Brindley, P. J., and Loukas, A. (2003) Parasitology 126, 179-185
28. Harris, J. L., Backes, B. J., Leonetti, F., Mahrus, S., Ellman, J. A., and Craik, C. S. (2000) Proc. Natl. Acad. Sci. U. S. A. 97, 7754-7759
29. Turk, B. E., Huang, L. L., Piro, E. T., and Cantley, L. C. (2001) Nat. Biotechnol. 19, 661-667
30. Eng, J., MacCormack, A. L., and Yates, J. R. (1994) J. Am. Soc. Mass Spectrom. 5, 976-989
31. Rawlings, N. D., and Barrett, A. J. (1994) Methods Enzymol. 244, 461-486
32. Mills, B. J., and Lang, C. A. (1996) Biochem. Pharmacol. 52, 401-406
33. Harrop, S. A., Prociv, P., and Brindley, P. J. (1995) Trop Med. Parasitol. 46, 119-122
34. Francis, S. E., Sullivan, D. J., Jr., and Goldberg, D. E. (1997) Annu. Rev. Microbiol. 51, 97-123
35. Banerjee, R., Liu, J., Beatty, W., Pelosof, L., Klemba, M., and Goldberg, D. E. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 990-995
36. Francis, S. E., Gluzman, I. Y., Oksman, A., Banerjee, D., and Goldberg, D. E. (1996) Mol. Biochem. Parasitol. 83, 189-200
37. Shenai, B. R., and Rosenthal, P. J. (2002) Mol. Biochem. Parasitol. 122, 99-104
38. Roche, M., and Layrisse, M. (1966) Am. J. Trop. Med. Hyg. 15, 1029-1102
39. Serveau, C., Lalmanach, G., Juliano, M. A., Scharfstein, J., Juliano, L., and Gauthier, F. (1996) Biochem. J. 313, 951-956
40. Smooker, P. M., Whisstock, J. C., Irving, J. A., Siyaguna, S., Spithill, T. W., and Pike, R. N. (2000) Protein Sci. 9, 2567-2572
41. Lecaille, F., Weidauer, E., Juliano, M. A., Bromme, D., and Lalmanach, G. (2003) Biochem. J. 375, 307-312
42. Choi, K. H., and Laursen, R. A. (2000) Eur. J. Biochem. 267, 1516-1526
43. Redmond, D. L., Knox, D. P., Newlands, G., and Smith, W. D. (1997) Mol. Biochem. Parasitol. 85, 77-87
44. Smith, W. D., Newlands, G. F., Smith, S. K., Pettit, D., and Skuce, P. J. (2003) Parasite Immunol. 25, 313-323
45. Murata, C. E., and Goldberg, D. E. (2003) J. Biol. Chem. 278, 38022-38028
46. Gavigan, C. S., Dalton, J. P., and Bell, A. (2001) Mol. Biochem. Parasitol. 117, 37-48
47. McCarthy, E., Stack, C., Donnelly, S. M., Doyle, S., Mann, V. H., Brindley, P. J., Stewart, M., Day, T. A., Maule, A. G., and Dalton, J. P. (2004) Int. J. Parasitol. 34, 703-714
48. Brady, C. P., Dowd, A. J., Brindley, P. J., Ryan, T., Day, S. R., and Dalton, J. P. (1999) Infect. Immun. 67, 368-374
49. Brindley, P. J., Kalinna, B. H., Wong, J. Y., Bogitsh, B. J., King, L. T., Smyth, D. J., Verity, C. K., Abbenante, G., Brinkworth, R. I., Fairlie, D. P., Smythe, M. L., Milburn, P. J., Bielefeldt-Ohmann, H., Zheng, Y., and McManus, D. P. (2001) Mol. Biochem. Parasitol. 112, 103-112
50. Lipps, G., Fullkrug, R., and Beck, E. (1996) J. Biol. Chem. 271, 1717-1725
51. Sajid, M., McKerrow, J. H., Hansell, E., Mathieu, M. A., Lucas, K. D., Hsieh, I., Greenbaum, D., Bogyo, M., Salter, J. P., Lim, K. C., Franklin, C., Kim, J. H., and Caffrey, C. R. (2003) Mol. Biochem. Parasitol. 131, 65-75
52. Ramalho-Ortigao, J. M., Kamhawi, S., Rowton, E. D., Ribeiro, J. M., and Valenzuela, J. G. (2003) Insect Biochem. Mol. Biol. 33, 163-171
53. Vizioli, J., Catteruccia, F., della Torre, A., Reckmann, I., and Muller, H. M. (2001) Eur. J. Biochem. 268, 4027-4035
54. Mulenga, A., Sugimoto, C., Ingram, G., Ohashi, K., and Misao, O. (2001) Insect Biochem. Mol. Biol. 31, 817-825
55. Bouchard, E., Cloutier, C., and Michaud, D. (2003) Mol. Ecol. 12, 2439-2446
56. Knox, D. P., Skuce, P.J., Newlands, G.F., Redmond, D.L. (2001) in Parasitic Nematodes: Molecular Biology, Biochemistry and Immunology. (Kennedy, M. W., and Harnett, W., eds) pp. 247-268, CAB International, New York
57. Knox, D. P., Smith, S. K., and Smith, W. D. (1999) Parasite Immunol. 21, 201-210
58. Smith, W. D., Skuce, P. J., Newlands, G. F., Smith, S. K., and Pettit, D. (2003) Parasite Immunol. 25, 521-530
59. Bakker, N., Vervelde, L., Kanobana, K., Knox, D. P., Cornelissen, A. W., de Vries, E., and Yatsuda, A. P. (2004) Vaccine 22, 618-628