Histatins: Multifunctional salivary antimicrobial peptides

Antimicrobial Peptides and Innate Immunity

Volumn , Issue , 2013, Pages 167-181

  Van 't Hof, Wim ^a,b   Oudhoff, Menno J ^a,b   Veerman, Enno C I ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84922369973     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-0348-0541-4_7     Document Type: Chapter

References (63)

1. Basak A, Ernst B, Brewer D, Seidah NG, Munzer JS, Lazure C, Lajoie GA (1997) Histidine-rich human salivary peptides are inhibitors of proprotein convertases furin and PC7 but act as substrates for PC1. J Pept Res 49:596-603
2. Bennick A (2002) Interaction of plant polyphenols with salivary proteins. Crit Rev Oral Biol Med 13:184-196
3. Brant EC, Santarpia RP III, Pollock JJ (1990) The role of pH in salivary histidine-rich polypeptide anti-fungal germ tube inhibitory activity. Oral Microbiol Immunol 5:336-339
4. Brewer D, Lajoie G (2000) Evaluation of the metal binding properties of the histidine-rich antimicrobial peptides histatin 3 and 5 by electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 14:1736-1745
5. Brewer D, Lajoie G (2002) Structure-based design of potent histatin analogues. Biochemistry 41:5526-5536
6. Calderon-Santiago M, Luque de Castro MD (2009) The dual trend in histatins research. Trends Anal Chem 28:1011-1018
7. Cohen S (2008) Origins of growth factors: NGF and EGF. J Biol Chem 283:33793-33797
8. Den Hertog AL, Wong Fong Sang HW, Kraayenhof R, Bolscher JGM, Van 't Hof W, Veerman ECI, Nieuw Amerongen AV (2004) Interactions of histatin 5 and histatin 5-derived peptides with liposome membranes: surface effects, translocation and permeabilization. Biochem J 379:665-672
9. Den Hertog AL, Van Marle J, Van Veen HA, Van 't Hof W, Bolscher JGM, Veerman ECI, Nieuw Amerongen AV (2005) Candidacidal effect of two antimicrobial peptides: histatin 5 causes small membrane defects, but LL-37 causes massive disruption of the cell membrane. Biochem J 388:689-695
10. Edgerton M, Raj PA, Levine MJ (1995) Surface-modified poly(methyl methacrylate) enhances adsorption and retains anticandidal activities of salivary histatin 5. J Biomed Mater Res 29:1277-1286
11. Edgerton M, Koshlukova SE, Lo TE, Chrzan BG, Straubinger RM, Raj PA (1998) Candidacidal activity of salivary histatins identification of a histatin 5-binding protein on Candida albicans. J Biol Chem 273:20438-20447
12. Edgerton M, Koshlukova SE, Araujo MW, Patel RC, Dong J, Bruenn JA (2000) Salivary histatin 5 and human neutrophil defensin 1 kill Candida albicans via shared pathways. Antimicrob Agents Chemother 44:3310-3316
13. Gusman H, Travis J, Helmerhorst EJ, Potempa J, Troxler RF, Oppenheim FG (2001) Salivary histatin5 is an inhibitor of both host and bacterial enzymes implicated in periodontal disease. Infect Immun 69:1402-1408
14. Helmerhorst EJ, Van 't Hof W, Veerman ECI, Simoons-Smit I, Nieuw Amerongen AV (1997) Synthetic histatin analogs with broad spectrum antimicrobial activity. Biochem J 326:39-45
15. Helmerhorst EJ, Reijnders IM, Van 't Hof W, Veerman ECI, Nieuw Amerongen AV (1999) A critical comparison of the hemolytic and fungicidal activities of cationic antimicrobial peptides. FEBS Lett 449:105-110
16. Helmerhorst EJ, Van 't Hof W, Breeuwer P, Veerman ECI, Abee T, Troxler RF, Nieuw Amerongen AV, Oppenheim FG (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
17. Hofmann A, Grella M, Botos I, Filipowicz W, Wlodawer A (2002) Crystal structures of the semireduced and inhibitor-bound forms of cyclic nucleotide phosphodiesterase from Arabidopsis thaliana. J Biol Chem 277:1419-1425
18. Houghton EA, Nicholas KM (2009) In vitro reactive oxygen species production by histatins and copper (I, II). J Biol Inorg Chem 14:243-251
19. Imatani T, Kato T, Minaguchi K, Okuda K (2000) Histatin 5 inhibits inflammatory cytokine induction from human gingival fibroblasts by Porphyromonas gingivalis. Oral Microbiol Immunol 15:378-382
20. Isola R, Isola M, Diaz G, Conti G, Lantini MS, Riva A (2007) Histatin-induced alterations in Candida albicans: a microscopic and submicroscopic comparison. Microsc Res Tech 70:607-616
21. Jang WS, Bajwa JS, Sun JN, Edgerton M (2010) Salivary histatin 5 internalization by translocation, but not endocytosis, is required for fungicidal activity in Candida albicans. Mol Microbiol 77:54-370
22. Kavanagh K, Dowd S (2004) Histatins; antimicrobial peptides with therapeutic potential. J Pharm Pharmacol 56:285-289
23. Koshlukova SE, Lloyd TL, Araujo MW, 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
24. Luque-Ortega JR, Van 't Hof W, Veerman ECI, Saugar JM, Rivas L (2008) Human antimicrobial peptide histatin5 is a cell-penetrating peptide targeting mitochondrial ATP synthesis in Leishmania. FASEB J 22:1817-1828
25. Mackay BJ, Denepitiya L, Jacono VJ, Krost SB, Pollock JJ (1984a) Growth-inhibitory and bactericidal effects of human parotid salivary histidine-rich polypeptides on Streptococcus mutans. Infect Immun 44:695-701
26. Mackay BJ, Pollock JJ, Jacono VJ, Baum BJ (1984b) Isolation of milligram quantities of a group histidine-rich polypeptides from human parotid saliva. Infect Immun 44:688-694
27. Melino S, Gallo M, Trotta E, Mondello F, Paci M, Petruzzelli R (2006) Metal-binding and nuclease activity of an antimicrobial peptide analogue of the salivary histatin 5. Biochemistry 45:15373-15383
28. Mochon AB, Liu H (2008) The antimicrobial peptide histatin 5 causes a spatially restricted disruption on the Candida albicans surface, allowing rapid entry of the peptide into the cytoplasm. PLOS Pathog 4(10):e1000190. doi:101371/journalppat1000190
29. Murakami Y, Nagat H, Amano A, Takagaki M, Shizukuishi S, Tsunemitsu A, Aimoto S (1991) Inhibitory effects of human salivary histatins and lysozyme on coaggregation between Porphyromonas gingivalis and Streptococcus mitis. Infect Immun 59:3284-3286
30. Murakami Y, Tamagawa H, Shizukuishi S, Tsunemitsu A, Aimoto S (1992) Biological role of an arginine residue present in a histidine-rich peptide which inhibits hemagglutination of Porphyromonas gingivalis. FEMS Microbiol Lett 98:201-204
31. Nishikata M, Kanehira T, Oh H, Tani H, Tazaki M, Kuboki Y (1991) Salivary histatin as an inhibitor of a protease produced by the oral bacterium Bacteroides gingivalis. Biochem Biophys Res Commun 174:625-630
32. O'Brien-Simpson NM, Dashper SG, Reynolds EC (1998) Histatin 5 is a substrate and not an inhibitor of the Arg- and Lys-specific proteinases of Porphyromonas gingivalis. Biochem Biophys Res Commun 250:474-478
33. Oppenheim FG, Yang Y-C, Diamond RD, Hyslop D, Offner GD, Troxler RF (1986) The primary structure and functional characterization of the neutral histidine-rich polypeptide from human parotid secretion. J Biol Chem 261:1177-1182
34. Oppenheim FG, Xu T, McMillian FM, Levitz SM, Diamond RD, Offner GD, Troxler RF (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
35. Oudhoff MJ, Bolscher JGM, Nazmi K, Kalay H, Van 't Hof W, Nieuw Amerongen AV, Veerman ECI (2008) Histatins are the major wound-closure stimulating factors in human saliva as identified in a cell culture assay. FASEB J 22:3805-3812
36. Oudhoff MJ, Kroeze K, Nazmi K, Van den Keijbus P, Van 't Hof W, Fernandez-Borja M, Hordijk PL, Gibbs S, Bolscher JGM, Veerman ECI (2009) Structure-activity analysis of histatin, a potent wound healing peptide from human saliva: cyclization of histatin potentiates molar activity 1,000-fold. FASEB J 23:3928-3935
37. Oudhoff MJ, Blaauboer ME, Nazmi K, Scheres N, Bolscher JGM, Veerman ECI (2010) The role of salivary histatin and the human cathelicidin LL-37 in wound healing and innate immunity. Biol Chem 391:541-548
38. Paquette DW, Simpson DM, Friden P, Braman V, Williams RC (2002) Safety and clinical effects of topical histatin gels in humans with experimental gingivitis. J Clin Periodontol 29:1051-1058
39. Pollock JJ, Denepitiya L, Mackay BJ, Jacono VJ (1984) Fungistatic and fungicidal activity of human parotid salivary histidine-rich polypeptides on Candida albicans. Infect Immun 44:702-707
40. Raj PA, Edgerton M, Levine MJ (1990) Salivary histatin 5: dependence of sequence, chain length and helical conformation for candidacidal activity. J Biol Chem 265:3898-3905
41. Raj PA, Soni S-D, Levine MJ (1994) Membrane-induced helical conformation of an active candidacidal fragment of salivary histatins. J Biol Chem 269:9610-9616
42. Raj PA, Marcus E, Sukumaran DK (1998) Structure of human salivary histatin 5 in aqueous and nonaqueous solutions. Biopolymers 45:51-67
43. Richardson CF, Johnsson M, Raj PA, Levine MJ, Nancollas GH (1993) The influence of histatin 5 fragments on the mineralization of hydroxyapatite. Arch Oral Biol 38:997-1002
44. Rothstein DM, Spacciapoli P, Tran LT, Xu T, Roberts FD, Dalla Serra M, Buxton DK, Oppenheim FG, Friden P (2001) Anticandida activity is retained in P-113, a 12-amino-acid fragment of histatin 5. Antimicrob Agents Chemother 45:1367-1373
45. Ruissen ALA, Groenink J, Helmerhorst EJ, Walgreen-Weterings E, Van 't Hof W, Veerman ECI, Nieuw Amerongen AV (2001) Effects of histatin 5 and derived peptides on Candida albicans. Biochem J 356:361-368
46. Ruissen ALA, Groenink J, Krijtenberg P, Walgreen-Weterings E, Van 't Hof W, Veerman ECI, Nieuw Amerongen AV (2003) Internalisation and degradation of histatin 5 by Candida albicans. Biol Chem 384:183-190
47. Sabatini LM, Azen EA (1989) Histatins, a family of salivary histidine-rich proteins, are encoded by at least two loci HIS1 and HIS2. Biochem Biophys Res Commun 160:495-502
48. Sabatini LM, Warner TF, Saitoh E, Azen EA (1989) Tissue distribution of RNAs for cystatins, histatins, statherin and proline-rich salivary proteins in humans and macaques. J Dent Res 68:1138-1145
49. Santarpia RP III, Pollock JJ, Renner RP, Gwinnett AJ (1991) In vivo antifungal efficacy of salivary histidine-rich polypeptides: preliminary findings in a denture stomatitis model system. J Prosthet Dent 66:693-699
50. Simmons G, Clapham PR, Picard L, Offord RE, Rosenkilde MM, Schwartz TW, Buser R, Wells TN, Proudfoot AE (1997) Potent inhibition of HIV-infectivity in macrophages and lymphocytes by a novel CCR5 antagonist. Science 276:276-279
51. Sugiyama K (1993) Anti-lipopolysaccharide activity of histatins, peptides from human saliva. Experientia 49:1095-1097
52. Tsai H, Raj PA, Bobek LA (1996) Candidacidal activity of recombinant human salivary histatin 5 and variants. Infect Immun 64:5000-5007
53. Van 't Hof W, Veerman ECI, Helmerhorst EJ, Nieuw Amerongen AV (2001) Antimicrobial peptides, properties and applicability. Biol Chem 382:597-619
54. Van Dyke T, Paquette D, Grossi S, Braman V, Massaro J, D'Agostino R, Dibart S, Friden P (2002) Clinical and microbial evaluation of a histatin-containing mouthrinse in humans with experimental gingivitis: a phase-2 multi-center study. J Clin Periodontol 29:168-176
55. Vanderspek JC, Offner GD, Troxler RF, Oppenheim FG (1990) Molecular cloning of human submandibular histatins. Arch Oral Biol 35:137-143
56. Veerman ECI, Nazmi K, Van 't Hof W, Bolscher JGM, Den Hertog AL, Nieuw Amerongen AV (2004) Reactive oxygen species play no role in the candidacidal activity of the salivary antimicrobial peptide histatin 5. Biochem J 381:447-452
57. Veerman ECI, Valentijn-Benz M, Nazmi K, Ruissen ALA, Walgreen-Weterings E, Van Marle J, Doust AB, Van 't Hof W, Bolscher JGM, Nieuw Amerongen AV (2007) Energy depletion protects Candida albicans against antimicrobial peptides by rigidifying its cell membrane. J Biol Chem 282:18831-18841
58. Welling MM, Brouwer CP, Van 't Hof W, Veerman ECI, Nieuw Amerongen AV (2007) Histatin-derived monomeric and dimeric synthetic peptides show strong bactericidal activity towards multidrug-resistant Staphylococcus aureus in vivo. Antimicrob Agents Chemother 51:3416-3419
59. Xu T, Telser E, Troxler RF, Oppenheim FG (1990) Primary structure and anticandidal activity of the major histatin from parotid secretion of the subhuman primate Macaca fascicularis. J Dent Res 69:1717-1723
60. Xu T, Choi YJ, Saxer C, Oppenheim FG (1993) Hydroxyapatite adsorption and candidacidal activity of histatins. J Dental Res 72:322 (Abstract)
61. Xu Y, Ambudkar I, Yamagishi H, Swaim W, Walsh TJ, O'Connell BC (1999) Histatin 3-mediated killing of Candida albicans: effect of extracellular salt concentration on binding and internalization. Antimicrob Agents Chemother 43:2256-2262
62. Yin A, Margolis HC, Grogan J, Yao Y, Troxler RF, Oppenheim FG (2003) Physical parameters of hydroxyapatite adsorption and effect on candidacidal activity of histatins. Arch Oral Biol 48:361-368
63. Yoshinari M, Kato T, Matsuzaka K, Hayakawa T, Inoue T, Oda Y, Okuda K, Shimono M (2006) Adsorption behavior of antimicrobial peptide histatin 5 on PMMA. J Biomed Mater Res B Appl Biomater 77:47-54