Metal-binding and nuclease activity of an antimicrobial peptide analogue of the salivary histatin 5

Biochemistry

Volumn 45, Issue 51, 2006, Pages 15373-15383

  Melino, Sonia ^c   Gallo, Mariana ^a   Trotta, Edoardo ^b   Mondello, Francesca ^c   Paci, Maurizio ^a   Petruzzelli, Raffaele ^d  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b CNR   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d UNIVERSITY OF CHIETI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL PEPTIDE ANALOGUE; SALIVARY PEPTIDES; ZINC ION COORDINATION;

AMINO ACIDS; BIOASSAY; DNA; HYDROPHOBICITY; MOLECULAR WEIGHT; POSITIVE IONS;

ENZYME KINETICS;

ASCORBIC ACID; CATION; COPPER ION; HISTATIN 5; NUCLEASE; PEPTIDE DERIVATIVE; PROTEIN ATCUN C16; SALIVA PROTEIN; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; ASSAY; BINDING SITE; BIOTECHNOLOGY; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; ENZYME ACTIVITY; GEL RETARDATION ASSAY; HYDROLYSIS; HYDROPHOBICITY; METAL BINDING; MOLECULAR MODEL; MOLECULAR WEIGHT; OXIDATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; COPPER; DEOXYRIBONUCLEASES; HISTATINS; HUMANS; MOLECULAR SEQUENCE DATA; NICKEL; PEPTIDE FRAGMENTS; SALIVARY PROTEINS;

EID: 33845921608     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0615137     Document Type: Article

References (53)

1. Oppenheim, F. G., Xu, T., McMillian, F. M., Levitz, S. M., Diamond, R. D., Offner, G. D., and Troxler, R. F. (1988) Histatins, a novel family of histidine-rich proteins in human parotid secretion. Isolation, characterization, primary structure, and fungistatic effects on Candida albicans, J. Biol. Chem. 263, 7472-7477.
2. Tsai, H., and Bobek, L. A. (1997) Human salivary histatin-5 exerts potent fungicidal activity against Cryptococcus neoformans, Biochim. Biophys. Acta 1336, 367-369.
3. Tsai, H., and Bobek, L. A. (1997) Studies of the mechanism of human salivary histatin-5 candidacidal activity with histatin-5 variants and azole-sensitive and -resistant Candida species, Antimicrob. Agents Chemother. 41, 2224-2228.
4. MacKay, B. J., Denepitiya, L., Iacono, V. J., Krost, S. B., and Pollock, J. J. (1984) Growth-inhibitory and bactericidal effects of human parotid salivary histidine-rich polypeptides on Streptococcus mutans, Infect. Immun. 44, 695-701.
5. Murakami, Y., Nagata, H., Amano, A., Takagaki, M., Shizukuishi, S., Tsunemitsu, A., and Aimoto, S. (1991) Inhibitory effects of human salivary histatins and lysozyme on coaggregation between Porphyromonas gingivalis and Streptococcus mitis, Infect. Immun. 59, 3284-3286.
6. Heimerhorst, E. J., Breeuwer, P., van't Hof, W., Walgreen-Weterings, E., Oomen, L. C., Veerman, E. C., Amerongen, A. V., and Abee, T. (1999) The cellular target of histatin 5 on Candida albicans is the energized mitochondrion, J. Biol. Chem. 274, 7286-7291.
7. Edgerton, M., Koshlukova, S. E., Lo, T. E., Chrzan, B. G., Straubinger, R. M., and Raj, P. A. (1998) Candidacidal activity of salivary histatins. Identification of a histatin 5-binding protein on Candida albicans, J. Biol. Chem. 273, 20438-20447.
8. Helmerhorst, E. J., van't Hof, W., Breeuwer, P., Veerman, E. C., Abee, T., Troxler, R. F., Amerongen, A. V., and Oppenheim, F. G. (2001) Characterization of histatin 5 with respect to amphipathicity, hydrophobicity, and effects on cell and mitochondrial membrane integrity excludes a candidacidal mechanism of pore formation, J. Biol. Chem. 276, 5643-5649.
9. Li, X. S., Reddy, M. S., Baev, D., and Edgerton, M. (2003) Candida albicans Ssa1/2p is the cell envelope binding protein for human salivary histatin 5, J. Biol. Chem. 278, 28553-28561.
10. Li, X. S., Sun, J. N., Okamoto-Shibayama, K., and Edgerton, M. (2006) Candida albicans cell wall SSA proteins bind and facilitate import of salivary histatin 5 required for toxicity, J. Biol. Chem. 281, 22453-22463.
11. Helmerhorst, E. J., Troxler, R. F., and Oppenheim, F. G. (2001) The human salivary peptide histatin 5 exerts its antifungal activity through the formation of reactive oxygen species, Proc. Natl. Acad. Sci. U.S.A. 98, 14637-14642.
12. Koshlukova, S. E., Lloyd, T. L., Araujo, M. W., and Edgerton, M. (1999) Salivary histatin 5 induces non-lytic release of ATP from Candida albicans leading to cell death, J. Biol. Chem. 274, 18872-18879.
13. Baev, D., Rivetta, A., Vylkova, S., Sun, J. N., Zeng, G. F., Slayman, C. L., and Edgerton, M. (2004) The TRK1 potassium transporter is the critical effector for killing of Candida albicans by the cationic protein, Histatin 5, J. Biol. Chem. 279, 55060-55072.
14. 2+ Ions Selectively Induce Antimicrobial Salivary Peptide Histatin-5 to Fuse Negatively Charged Vesicles. Identification and Characterization of a Zinc-Binding Motif Present in the Functional Domain, Biochemistry 38, 9626-9633.
15. Gusman, H., Lendenmann, U., Grogan, J., Troxler, R. F., and Oppenheim, F. G. (2001) Is salivary histatin 5 a metallopeptide?, Biochim. Biophys. Acta 1545, 86-95.
16. Grogan, J., McKnight, C. J., Troxler, R. F., and Oppenheim, F. G. (2001) Zinc and copper bind to unique sites of histatin 5, FEBS Lett. 491, 76-80.
17. 1H NMR Spectroscopy, Biochemistry 23, 2832-2838.
18. Rakhit, G., and Sarkar, B. (1981) Electron spin resonance study of the copper(II) complexes of human and dog serum albumins and some peptide analogs, J. Inorg. Biochem. 15, 233-241.
19. Lau, S. J., Kruck, T. P., and Sarkar, B. (1974) A peptide molecule mimicking the copper(II) transport site of human serum albumin. A comparative study between the synthetic site and albumin, J. Biol. Chem. 249, 5878-5884.
20. Long, E. C. (1999) Ni(II)·Xaa-Xaa-His Metallopeptide-DNA/RNA Interactions, Acc. Chem. Res. 32, 827-835.
21. Bal, W., Lukszo, J., and Kasprazak, K. S. (1996) Interactions of nickel(II) with histones: enhancement of 2′-deoxyguanosine oxidation by Ni(II) complexes with CH3CO-Cys-Ala-Ile-His-NH2, a putative metal binding sequence of histone H3, Chem. Res. Toxicol. 9, 535-540.
22. Kimoto, E., Tanaka, H., Gyotoku, J., Morishige, F., and Pauling, L. (1983) Enhancement of antitumor activity of ascorbate against Ehrlich ascites tumor cells by the copper:glycylglycylhistidine complex, Cancer Res. 43, 824-828.
23. Mack, D. P., and Dervan, P. B. (1990) Nickel-Mediated Sequence-Specific Oxidative Cleavage of DNA by a Designed Metalloprotein, J. Am. Chem. Soc. 112, 4604-4606.
24. Mack, D. P., and Dervan, P. B. (1992) Sequence-Specific Oxidative Cleavage of DNA by a Designed Metalloprotein, Ni(II)·GGH-(Hin139-190), Biochemistry 31, 9399-9405.
25. 2, J. Am. Chem. Soc. 120, 248-257.
26. Long, E. C., and Claussen, C. A. (2004) in Small Molecule DNA and RNA Binders (Demeunynck, M., Bailly, C., Wilson, W. D., Eds.) Vol. 1, pp 88-125, Wiley-VCH, Weinheim, Germany.
27. Brittain, I. J., Huang, X., Long, E. C. (1998) Selective Recognition and Cleavage of RNA Loop Structures by Ni(H)·Xaa-Gly-His Metallopeptides, Biochemistry 37, 12113-12120.
28. Copeland, K. D., Fitzsimons, M. P., Houser, R. P., and Barton, J. K. (2002) DNA Hydrolysis and Oxidative Cleavage by Metal-Binding Peptides Tethered to Rhodium Intercalators, Biochemistry 41, 343-356.
29. Raj, P. A., Edgerton, M., and Levine, M. J. (1990) Salivary histatin 5: dependence of sequence, chain length, and helical conformation for candidacidal activity, J. Biol. Chem. 265, 3898-3905.
30. Helmerhorst, E. J., Venuleo, C., Beri, A., and Oppenheim, F. G. (2005) Candida glabrata is unusual with respect to its resistance to cationic antifungal proteins, Yeast 22, 705-714.
31. Marion, D., and Wuthrich, K. (1983) Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of 1H-1H spin-spin coupling constants in proteins, Biochem. Biophys. Res. Commun. 113, 967-974.
32. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
33. Jhonoson, B. A., and Blevins, R. A. (1994) NMRView. a computer program for the visualization and analysis of NMR data, J. Biomol. NMR 6, 603-614.
34. Bax, A., and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy, J. Magn. Reson. 65, 355-360.
35. Harford, C., and Sarkar, B. (1997) Amino Terminal Cu(II)- and Ni(II)- Binding (ATCUN) Motif of Proteins and Peptides: Metal Binding, DNA Cleavage, and Other Properties, Acc. Chem. Res. 30, 123-130.
36. Sigel, H., and Martin, B. (1982) Coordinating properties of the amide bond. Stability and structure of metal ion complexes of peptides and related ligands, Chem. Rev. 82, 385-426.
37. .- scavenger activity: Cu(II)-peptide complexes as superoxide dismutase models, J. Inorg. Biochem. 73, 157-165.
38. Nagane, R., Koshigoe, T., and Chikira, M. (2003) Interaction of Cu(II)-Arg-Gly-His-Xaa metallopeptides with DNA: effect of C-terminal residues, Leu and Glu, J. Inorg. Biochem. 93, 204-212.
39. Andrade, M. A., Chacon, P., Merelo, J. J., and Moran, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network, Protein Eng. 6, 383-390.
40. Merelo, J. J., Andrade, M. A., Prieto, A., and Morán, F. (1994) Proteinotopic Feature Maps, Neurocomputing 6, 443-454.
41. Wishart, D. S., Bigam, C. G., Yao, J., Abildgaard, F., Dyson, H. J., Oldfield, E., Markley, J. L., and Sykes, B. D. (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR, J. Biomol. NMR. 6, 135-140.
42. α and Protein Backbone Conformation, J. Am. Chem. Soc. 114, 9674-9675.
43. Manning, M. C., and Woody, R. W. (1991) Theoretical CD studies of polypeptide helices: examination of important electronic and geometric factors, Biopolymers 31, 569-586.
44. Beychok S. (1967) Protein Models for Conformational Studies, in poly-α-Amino Acid (Fasman, G. D., Ed.) pp 293-337 Dekker, New York.
45. Jin, Y., and Cowan, J. A. (2005) DNA Cleavage by Copper-ATCUN Complexes. Factors Influencing Cleavage Mechanism and Linearization of dsDNA, J. Am. Chem. Soc. 127, 8408-8415.
46. Fang, Y. Y., Ray, B. D., Claussen, C. A., Lipkowitz, K. B., and Long, E. C. (2004) Ni(II)·Arg-Gly-His-DNA Interactions: Investigation into the Basis for Minor-Groove Binding and Recognition, J. Am. Chem. Soc. 126, 5403-5412.
47. Branum, M. E., Tipton, A. K., Zhu, S., and Que, L., Jr. (2001) Double-Strand Hydrolysis of Plasmid DNA by Dicerium Complexes at 37 °C, J. Am. Chem. Soc. 123, 1898-1904.
48. Uma, V., Kanthimathi, M., Subramanian, J., and Unni Nair, B. (2006) A new dinuclear biphenylene bridged copper(II) complex: DNA cleavage under hydrolytic conditions, Biochim. Biophys. Acta 1760, 814-819.
49. Brewer, D., and Lajoie, G. (2002) Structure-Based Design of Potent Histatin Analogues, Biochemistry 41, 5526-5536.
50. Bal, W., Wojcik, J., Maciejczyk, M., Grochowski, P., and Kasprzak, K. S. (2000) Induction of a Secondary Structure in the N-terminal Pentadecapeptide of Human Protamine HP2 through Ni(II) Coordination. An NMR study, Chem. Res. Toxicol. 13, 823-830.
51. Beese, L. S., and Steitz, T. A. (1991) Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism, EMBO J. 10, 25-33.
52. Ma, L., Tibbitts, T. T., and Kantrowitz, E. R. (1995) Escherichia coli alkaline phosphatase: X-ray structural studies of a mutant enzyme (His-412→Asn) at one of the catalytically important zinc binding sites Protein Sci. 4, 1498-1506.
53. Baev, D., Li, X. S., Dong, J., Keng, P., and Edgerton, M. (2002) Human salivary histatin 5 causes disordered volume regulation and cell cycle arrest in Candida albicans, Infect. Immun. 70, 4777-4784.