Multiple-antigenic peptides of histidine-rich protein II of Plasmodium falciparum: Dendrimeric biomineralization templates

Journal of the American Chemical Society

Volumn 121, Issue 11, 1999, Pages 2395-2400

  Ziegler, James ^a   Chang, Richard T ^a   Wright, David W ^a  

^a DUQUESNE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; HEME; HISTIDINE; PARASITE ANTIGEN; PEPTIDE; POLYHISTIDINE; PROTOPORPHYRIN; PROTOPORPHYRIN ZINC; PROTOZOAL PROTEIN;

ARTICLE; BINDING SITE; DETOXIFICATION; MINERALIZATION; NONHUMAN; PLASMODIUM FALCIPARUM; TANDEM REPEAT;

EID: 0033599541     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja983220+     Document Type: Article

References (58)

1. (a) Tropical Disease Research News (News from the WHO Division of Tropical Diseases) 1994, 46, 5.
2. (b) Anderson, J.; MacLean, M.; Davies, C. Malaria Research: An Audit of International Activity; Prism Report 7, The Wellcome Centre for Medical Sciences: London, 1996.
3. (c) Peters, W. Chemotherapy and Drug Resistance in Malaria, 2nd ed.; Academic Press: London, 1987.
4. During the intraerythrocytic phase of its life cycle, the malaria parasite can degrade up to 80% of an infected erythrocyte's hemoglobin to obtain requisite amino acids for its maturation; (a) Olliaro, P. L.; Goldberg, D. E. Parasitol. Today 1995, 11, 294-297. (b) Rosenthal, P. J.; McKerrow, J. H.; Aikawa, M.; Nagasawa, H.; Leech, J. H. J. Clin. Invest. 1988, 82, 1560-1566. (c) Goldberg, D. E.; Slater, A. F. G.; Cerami, A.; Henderson, G. B. Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 2931-2935.
5. During the intraerythrocytic phase of its life cycle, the malaria parasite can degrade up to 80% of an infected erythrocyte's hemoglobin to obtain requisite amino acids for its maturation; (a) Olliaro, P. L.; Goldberg, D. E. Parasitol. Today 1995, 11, 294-297. (b) Rosenthal, P. J.; McKerrow, J. H.; Aikawa, M.; Nagasawa, H.; Leech, J. H. J. Clin. Invest. 1988, 82, 1560-1566. (c) Goldberg, D. E.; Slater, A. F. G.; Cerami, A.; Henderson, G. B. Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 2931-2935.
6. During the intraerythrocytic phase of its life cycle, the malaria parasite can degrade up to 80% of an infected erythrocyte's hemoglobin to obtain requisite amino acids for its maturation; (a) Olliaro, P. L.; Goldberg, D. E. Parasitol. Today 1995, 11, 294-297. (b) Rosenthal, P. J.; McKerrow, J. H.; Aikawa, M.; Nagasawa, H.; Leech, J. H. J. Clin. Invest. 1988, 82, 1560-1566. (c) Goldberg, D. E.; Slater, A. F. G.; Cerami, A.; Henderson, G. B. Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 2931-2935.
7. (a) Slater, A. F. G. Exp. Parisitology 1992, 74, 362.
8. (b) Jamjoom, G. A. Rev. Infect. Dis. 1988, 10, 1029.
9. (a) Fitch, C. D.; Kanjananggulpan, P. J. Biol. Chem. 1987, 262, 15552.
10. (b) Slater, A. F. G.; Swiggard, W. J.; Orton, B. R.; Flitter, W. D.; Goldberg, D. E.; Cerami, A.; Henderson, G. B. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 325.
11. (c) Bohle, D. S.; Helms, J. B. Biochem. Biophys. Res. Commun. 1993, 193, 504.
12. (d) Bremard, C.; Girerd, J. J.; Kowalewski, P.; Merlin, J. C.; Moreau, S. Appl. Spectrosc. 1993, 47, 1837.
13. Bohle, S. D.; Dinnebier, R. E.; Madsen, S. K.; Stephens, P. W. J. Biol. Chem. 1997, 272, 713.
14. Sullivan, D. J., Jr.; Gluzman, I. Y.; Goldberg, D. E. Science 1996, 272, 219-222.
15. Recent studies have also examined the possible role of lipids as nucleating templates, showing that an acetonitrile extract of trophozoites and several lipids of undefined phase are also capable of initiating hemozoin formation; (a) Dorn, A.; Stoffel, R.; Matile, H.; Bubendorf, A.; Ridley, R. G. Nature 1995, 374, 269-271. (b) Dorn, A.; Sudha, R. V.; Matile, H.; Bubendorf, A.; Vennerstrom, J. L.; Ridley, R. G. Biochem. Pharmacol. 1998, 55, 737-747.
16. Recent studies have also examined the possible role of lipids as nucleating templates, showing that an acetonitrile extract of trophozoites and several lipids of undefined phase are also capable of initiating hemozoin formation; (a) Dorn, A.; Stoffel, R.; Matile, H.; Bubendorf, A.; Ridley, R. G. Nature 1995, 374, 269-271. (b) Dorn, A.; Sudha, R. V.; Matile, H.; Bubendorf, A.; Vennerstrom, J. L.; Ridley, R. G. Biochem. Pharmacol. 1998, 55, 737-747.
17. (a) Mann, S. J. Chem. Soc. Dalton Trans. 1993, 1-9.
18. (b) Mann, S. Nature 1993, 365, 499.
19. (c) Biomimetic Materials Chemistry; Mann, S., Ed.; VCH Publishers: New York, 1996.
20. (a) Tam, J. P. Proc. Natl. Acad. Sci. U. S.A. 1988, 85, 5409-5413.
21. (b) Defoort, J. P.; Nardelli, B.; Huang, W.; Ho, D., Tam, J. P. Proc. Natl. Acad. Sci. U. S. A. 1992, 89, 3879-3883.
22. (c) Tam, J. P.; Clavijo, P.; Lu, Y. A.; Nussenzweig, V.; Nussenzweig, R.; Zavala, F. J. Exp. Med. 1990, 171, 299-306.
23. Tam, J. P.; Zavala, F. J. Immunol. Methods 1989, 124, 53-61.
24. Yoshida, M.; Tam, J. P.; Merrifield, R. B. In Peptide Chemistry, Proceedings of the 2nd Japan Simposium on Peptide Chemistry: Yanaihara, N., Ed.; Escom: Leiden, 1993; pp 297-299.
25. (a) Hahn, K. W.; Klis, W. A.; Stewart, J. M. Science 1990, 248, 1544-1547.
26. (b) Montal, M.; Montal, M. S.; Tomich, J. M. Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 6929-6933.
27. r 27kD) contains 28 Ala-His-His sequences (56% of the mature protein is histidine and alanine). Wellems. T E.; Howard, R. J. Proc. Natl. Acad. Sci. U. S. A. 1986, 83, 6065-6069.
28. r 10 kD) contains 31% histidine predominantly. Stahl, H. D.; Crewther, P. E.; Scanlon, D. B.; Woodrow, G.; Brown, G V.; Bianco, A. F.; Anders, R. F.; Coppel, R. L. Nucleic Acids Res. 1985, 13, 7837-7846.
29. (c) Lenstra, R.; d'Auriol, L.; Andrieu, B.; Le Bras, J.; Galibert, F. Biochem. Biophys. Res. Commun. 1987, 146, 368-377.
30. (a) Bodansky, M.; Bodansky, A. The Practice of Peptide Synthesis, 2nd ed.; Springer-Verlag: Amsterdam, 1994.
31. (b) Synthetic Peptides, A User's Guide; Grant, G. A., Ed.; W. H. Freeman and Co.: New York, 1992.
32. (c) Fields, G. B.; Noble, R. L. Solid-phase peptide synthesis utilizing 9-fluoromethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 1990, 35, 161-214.
33. (d) Stuber, W. Synthesis of peptide amides by Fmoc solid-phase peptide synthesis and acid labile anchor groups. Int. J. Pept. Protein Res. 1989, 334, 215-221.
34. (e) Atterson, E. Peptide synthesis. Part 10. Use of pentafluorophenyl esters of Fmoc amino acids in solid-phase peptide synthesis. Tetrahedron 1988, 44, 843-857.
35. (a) Use of allyl-based protecting groups for the automated synthesis of multiple antigenic (MAP) peptides on the 9050 plus PepSynthesizer. Peptide Synthesis: application note; Millipore: 1996, 1-7.
36. (b) Multiple antigenic Peptides. Novabiochem Catalog and Peptide Syntehsis Handbook: synthesis note; 1998, S17.
37. (c) Pioneer Peptide Synthesis System User's Guide; PerSeptive Biosystem, 1996.
38. (d) Pioneer Workstation Software Guide; PerSeptive Biosystem, 1997.
39. "Parasight F" is a robust monoclonal antibody test for the direct, instrument-free qualitative detection of the HRP II in the field and was generously provided for this work by Becton-Dickinson Pharmaceutical.
40. (a) Morgan, W. T. Biochem. 1985, 24, 1496-1501.
41. (b) Burch, M. K.; Morgan, W. T. Biochemistry 1985, 24, 5919-5924.
42. D.
43. (a) Naylor, A. M.; Goddard, W. A., III.; Kiefer, G. E.; Tomalia, D. A. J. Am. Chem. Soc. 1989, 111, 2339.
44. (b) Ottaviani, M. F.; Bossmann, S.; Turro, N. J.; Tomalia, D. A. J. Am. Chem. Soc. 1994, 116, 661.
45. (c) Dandliker, P. J.; Diederich, F.; Gross, M.; Knobler, C. B.; Louati, A.; Sanford, E. M. Angew. Chem., Int. Ed. Engl. 1994, 33, 1739.
46. Further, UV - vis of the template-associated Fe(III)PPIX complex does not show any of the features associated with histidine axial ligation (Supporting Information).
47. Katagiri, M.; Tsutsui, K.; Yamano, T.; Shiminishi, Y.; Ishibashi, F. Biochem. Biophys. Res. Comm. 1987, 149, 1070-1076.
48. (a) Shelnutt, J. A. Inorg. Chem. 1983, 22, 2535-2544.
49. (b) Shelnutt, J. A.; Dobry, M. M., Satterlee, J. D. J. Phys. Chem. 1984, 88, 4980-4987.
50. (c) Shelnutt, J. A. J. Phys. Chem. 1984, 88, 4988-4992.
51. Olliaro, P. Differential solubility is a common bench test for the presence of hemozoin. Free heme is soluble in the sodium bicarbonate buffer (pH 9.5), while hemozoin is not. Recent studies have suggested that a DMSO wash removes short oligomers from the bulk polymer. Personal communication.
52. Bürger, H. In Porphyrins and Metalloporphyrins; Smith, K. M., Ed.; Elsevier: Amsterdam, 1975; 115.
53. Pandey, A. V.; Joshi, R.; Tekwani, B. L.; Singh, R. L.; Chauhan, V. S. Mol. Biochem. Parisitol. 1997, 90, 281-287.
54. It should be emphasized that the nucleation model of Ala-His-His-Ala-His-His-Ala-Ala-Asp presented above does not represent a unique organization of the Ala-His-His tripeptides in HRP II, but simply an initial organization which results in nucleation. An alternate sequence currently under investigation is Ala-His-His-Ala-Ala-Asp-Ala-His-His. Tandem occupation of each Ala-His-His subsite would still be required for hemozoin nucleation.
55. Such a function has been attributed to many scaffolding proteins. Relevant examples include (a) the α-helical anti-freeze protein of fish; Madura, J. D.; Wierzbicki, A.; Harrington, J. P.; Raymond, J. A.; Sikes, C. S. J. Am. Chem. Soc. 1994, 116, 417. (b) the β-pleated sheet proteins of many sea organisms; Albeck, S.; Aizenberg, J.; Weiner, S. J. Am. Chem. Soc. 1993, 115, 11691 and Aizenberg, J.; Hanson, J.; Koetzle, T. F.; Weiner, S.; Addadi, L. J. Am. Chem. Soc. 1997, 119, 881.
56. Such a function has been attributed to many scaffolding proteins. Relevant examples include (a) the α-helical anti-freeze protein of fish; Madura, J. D.; Wierzbicki, A.; Harrington, J. P.; Raymond, J. A.; Sikes, C. S. J. Am. Chem. Soc. 1994, 116, 417. (b) the β-pleated sheet proteins of many sea organisms; Albeck, S.; Aizenberg, J.; Weiner, S. J. Am. Chem. Soc. 1993, 115, 11691 and Aizenberg, J.; Hanson, J.; Koetzle, T. F.; Weiner, S.; Addadi, L. J. Am. Chem. Soc. 1997, 119, 881.
57. Such a function has been attributed to many scaffolding proteins. Relevant examples include (a) the α-helical anti-freeze protein of fish; Madura, J. D.; Wierzbicki, A.; Harrington, J. P.; Raymond, J. A.; Sikes, C. S. J. Am. Chem. Soc. 1994, 116, 417. (b) the β-pleated sheet proteins of many sea organisms; Albeck, S.; Aizenberg, J.; Weiner, S. J. Am. Chem. Soc. 1993, 115, 11691 and Aizenberg, J.; Hanson, J.; Koetzle, T. F.; Weiner, S.; Addadi, L. J. Am. Chem. Soc. 1997, 119, 881.
58. Martiney, J. A.; Cerami, A.; Salter, A. F. G. Mol. Med. (Tokyo) 1996, 2, 236-246.