Therapeutic approaches using host defence peptides to tackle herpes virus infections

Viruses

Volumn 1, Issue 3, 2009, Pages 939-964

  Jenssen, Håvard ^a  

^a ROSKILDE UNIVERSITY   (Denmark)

Author keywords

Antimicrobial peptides; Antiviral therapy; Cationic host defence peptides; Herpes; Immune stimulation; Innate defense regulators

Indexed keywords

EID: 84861370079     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v1030939     Document Type: Review

References (164)

1. World Health Statistics, www.who.int/whosis/whostat/2008/en/index.html.
2. Hamill, P.; Brown, K.; Jenssen, H.; Hancock, R.E.W. Novel anti-infectives: is host defence the answer? Curr. Opin. Biotechnol. 2008, 19, 628-636
3. Lai, Y.; Gallo, R.L. Toll-like receptors in skin infections and inflammatory diseases. Infect. Disord. Drug Targets 2008, 8, 144-155.
4. O'Neill, L.A. Targeting signal transduction as a strategy to treat inflammatory diseases. Nat. Rev. Drug Discov. 2006, 5, 549-563.
5. Kanzler, H.; Barrat, F.J.; Hessel, E.M.; Coffman, R.L. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat. Med. 2007, 13, 552-559.
6. Romagne, F. Current and future drugs targeting one class of innate immunity receptors: the Tolllike receptors. Drug Discov. Today 2007, 12, 80-87.
7. Wales, J.; Andreakos, E.; Feldmann, M.; Foxwell, B. Targeting intracellular mediators of pattern-recognition receptor signalling to adjuvant vaccination. Biochem. Soc. Trans. 2007, 35, 1501-1503.
8. Esmann, J. The many challenges of facial herpes simplex virus infection. J. Antimicrob. Chemother. 2001, 47 Suppl T1, 17-27.
9. Mitchell, B.M.; Bloom, D.C.; Cohrs, R.J.; Gilden, D.H.; Kennedy, P.G. Herpes simplex virus-1 and varicella-zoster virus latency in ganglia. J. Neurovirol. 2003, 9, 194-204.
10. Shieh, M.T.; WuDunn, D.; Montgomery, R.I.; Esko, J.D.; Spear, P.G. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J. Cell Biol. 1992, 116, 1273-1281.
11. WuDunn, D.; Spear, P.G. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 1989, 63, 52-58.
12. Mardberg, K.; Trybala, E.; Tufaro, F.; Bergstrom, T. Herpes simplex virus type 1 glycoprotein C is necessary for efficient infection of chondroitin sulfate-expressing gro2C cells. J. Gen. Virol. 2002, 83, 291-300.
13. Gruenheid, S.; Gatzke, L.; Meadows, H.; Tufaro, F. Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans. J. Virol. 1993, 67, 93-100.
14. Banfield, B.W.; Leduc, Y.; Esford, L.; Visalli, R.J.; Brandt, C.R.; Tufaro, F. Evidence for an interaction of herpes simplex virus with chondroitin sulfate proteoglycans during infection. Virology 1995, 208, 531-539.
15. Spear, P.G.; Eisenberg, R.J.; Cohen, G.H. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 2000, 275, 1-8.
16. Montgomery, R.I.; Warner, M.S.; Lum, B.J.; Spear, P.G. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 1996, 87, 427-436.
17. Warner, M.S.; Geraghty, R.J.; Martinez, W.M.; Montgomery, R.I.; Whitbeck, J.C.; Xu, R.; Eisenberg, R.J.; Cohen, G.H.; Spear, P.G. A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 1998, 246, 179-189.
18. Geraghty, R.J.; Krummenacher, C.; Cohen, G.H.; Eisenberg, R.J.; Spear, P.G. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 1998, 280, 1618-1620.
19. Cocchi, F.; Menotti, L.; Mirandola, P.; Lopez, M.; Campadelli-Fiume, G. The ectodomain of a novel member of the immunoglobulin subfamily related to the poliovirus receptor has the attributes of a bona fide receptor for herpes simplex virus types 1 and 2 in human cells. J. Virol. 1998, 72, 9992-10002.
20. Shukla, D.; Liu, J.; Blaiklock, P.; Shworak, N.W.; Bai, X.; Esko, J.D.; Cohen, G.H.; Eisenberg, R.J.; Rosenberg, R.D.; Spear, P.G. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 1999, 99, 13-22.
21. Xia, G.; Chen, J.; Tiwari, V.; Ju, W.; Li, J.P.; Malmstrom, A.; Shukla, D.; Liu, J. Heparan sulfate 3-O-sulfotransferase isoform 5 generates both an antithrombin-binding site and an entry receptor for herpes simplex virus, type 1. J. Biol. Chem. 2002, 277, 37912-37919.
22. Dingwell, K.S.; Brunetti, C.R.; Hendricks, R.L.; Tang, Q.; Tang, M.; Rainbow, A.J.; Johnson, D.C. Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. J. Virol. 1994, 68, 834-845.
23. Balan, P.; Davis-Poynter, N.; Bell, S.; Atkinson, H.; Browne, H.; Minson, T. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. J. Gen. Virol. 1994, 75 (Pt 6), 1245-1258.
24. Dingwell, K.S.; Johnson, D.C. The herpes simplex virus gE-gI complex facilitates cell-to-cell spread and binds to components of cell junctions. J. Virol. 1998, 72, 8933-8942.
25. Creagh, E.M.; O'Neill, L.A. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol. 2006, 27, 352-357.
26. Dziarski, R.; Gupta, D. The peptidoglycan recognition proteins (PGRPs). Genome Biol. 2006, 7, 232.
27. Kinghorn, G.R.; Woolley, P.D.; Thin, R.N.; De Maubeuge, J.; Foidart, J.M.; Engst, R. Acyclovir vs isoprinosine (immunovir) for suppression of recurrent genital herpes simplex infection. Genitourin Med. 1992, 68, 312-316.
28. Chilukuri, S.; Rosen, T. Management of acyclovir-resistant herpes simplex virus. Dermatol. Clin. 2003, 21, 311-320.
29. De Clercq, E. Antivirals and antiviral strategies. Nat. Rev. Microbiol. 2004, 2, 704-720.
30. Hancock, R.E.W.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24, 1551-1557.
31. Oppenheim, J.J.; Yang, D. Alarmins: chemotactic activators of immune responses. Curr. Opin. Immunol. 2005, 17, 359-365.
32. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415, 389-395.
33. Fjell, C.D.; Hancock, R.E.W.; Cherkasov, A. AMPer: a database and an automated discovery tool for antimicrobial peptides. Bioinformatics 2007, 23, 1148-1155.
34. Brogden, K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 2005, 3, 238-250.
35. Wu, M.; Maier, E.; Benz, R.; Hancock, R.E.W. Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 1999, 38, 7235-7242.
36. Matsuzaki, K.; Murase, O.; Fujii, N.; Miyajima, K. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 1996, 35, 11361-11368.
37. Ehrenstein, G.; Lecar, H. Electrically gated ionic channels in lipid bilayers. Q Rev. Biophys. 1977, 10, 1-34.
38. Pouny, Y.; Rapaport, D.; Mor, A.; Nicolas, P.; Shai, Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 1992, 31, 12416-12423.
39. Andersen, J.H.; Jenssen, H.; Sandvik, K.; Gutteberg, T.J. Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface. J. Med. Virol. 2004, 74, 262-271.
40. Haukland, H.H.; Ulvatne, H.; Sandvik, K.; Vorland, L.H. The antimicrobial peptides lactoferricin B and magainin 2 cross over the bacterial cytoplasmic membrane and reside in the cytoplasm. FEBS Lett. 2001, 508, 389-393.
41. Lau, Y.E.; Rozek, A.; Scott, M.G.; Goosney, D.L.; Davidson, D.J.; Hancock, R.E.W. Interaction and cellular localization of the human host defense peptide LL-37 with lung epithelial cells. Infect. Immun. 2005, 73, 583-591.
42. Bowdish, D.M.; Davidson, D.J.; Speert, D.P.; Hancock, R.E.W. The human cationic peptide LL-37 induces activation of the extracellular signal-regulated kinase and p38 kinase pathways in primary human monocytes. J. Immunol. 2004, 172, 3758-3765.
43. Wachinger, M.; Kleinschmidt, A.; Winder, D.; von Pechmann, N.; Ludvigsen, A.; Neumann, M.; Holle, R.; Salmons, B.; Erfle, V.; Brack-Werner, R. Antimicrobial peptides melittin and cecropin inhibit replication of human immunodeficiency virus 1 by suppressing viral gene expression. J. Gen. Virol. 1998, 79 (Pt 4), 731-740.
44. Mygind, P.H.; Fischer, R.L.; Schnorr, K.M.; Hansen, M.T.; Sonksen, C.P.; Ludvigsen, S.; Raventos, D.; Buskov, S.; Christensen, B.; De Maria, L.; Taboureau, O.; Yaver, D.; Elvig-Jorgensen, S.G.; Sorensen, M.V.; Christensen, B.E.; Kjaerulff, S.; Frimodt-Moller, N.; Lehrer, R.I.; Zasloff, M.; Kristensen, H.H. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 2005, 437, 975-980.
45. Hwang, P.M.; Zhou, N.; Shan, X.; Arrowsmith, C.H.; Vogel, H.J. Three-dimensional solution structure of lactoferricin B, an antimicrobial peptide derived from bovine lactoferrin. Biochemistry 1998, 37, 4288-4298.
46. Wang, G. Structures of Human Host Defense Cathelicidin LL-37 and Its Smallest Antimicrobial Peptide KR-12 in Lipid Micelles. J. Biol. Chem. 2008, 283, 32637-32643.
47. Rozek, A.; Friedrich, C.L.; Hancock, R.E.W. Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry 2000, 39, 15765-15774.
48. Koradi, R.; Billeter, M.; Wuthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 1996, 14, 51-55, 29-32.
49. Bastian, A.; Schafer, H. Human alpha-defensin 1 (HNP-1) inhibits adenoviral infection in vitro. Regul. Pept. 2001, 101, 157-161.
50. Horne, W.S.; Wiethoff, C.M.; Cui, C.; Wilcoxen, K.M.; Amorin, M.; Ghadiri, M.R.; Nemerow, G.R. Antiviral cyclic D, L-alpha-peptides: targeting a general biochemical pathway in virus infections. Bioorg. Med. Chem. 2005, 13, 5145-5153.
51. McCann, K.B.; Lee, A.; Wan, J.; Roginski, H.; Coventry, M.J. The effect of bovine lactoferrin and lactoferricin B on the ability of feline calicivirus (a norovirus surrogate) and poliovirus to infect cell cultures. J. Appl. Microbiol. 2003, 95, 1026-1033.
52. Pietrantoni, A.; Ammendolia, M.G.; Tinari, A.; Siciliano, R.; Valenti, P.; Superti, F. Bovine lactoferrin peptidic fragments involved in inhibition of Echovirus 6 in vitro infection. Antiviral Res. 2006, 69, 98-106.
53. Benincasa, M.; Skerlavaj, B.; Gennaro, R.; Pellegrini, A.; Zanetti, M. In vitro and in vivo antimicrobial activity of two alpha-helical cathelicidin peptides and of their synthetic analogs. Peptides 2003, 24, 1723-1731.
54. Ourth, D.D.; Lockey, T.D.; Renis, H.E. Induction of cecropin-like and attacin-like antibacterial but not antiviral activity in Heliothis virescens larvae. Biochem. Biophys. Res. Commun. 1994, 200, 35-44.
55. Yasin, B.; Pang, M.; Turner, J.S.; Cho, Y.; Dinh, N.N.; Waring, A.J.; Lehrer, R.I.; Wagar, E.A. Evaluation of the inactivation of infectious Herpes simplex virus by host-defense peptides. Eur. J. Clin. Microbiol. Infect. Dis. 2000, 19, 187-194.
56. Aboudy, Y.; Mendelson, E.; Shalit, I.; Bessalle, R.; Fridkin, M. Activity of two synthetic amphiphilic peptides and magainin-2 against herpes simplex virus types 1 and 2. Int. J. Pept. Protein Res. 1994, 43, 573-582.
57. Albiol Matanic, V.C.; Castilla, V. Antiviral activity of antimicrobial cationic peptides against Junin virus and herpes simplex virus. Int. J. Antimicrob. Agents 2004, 23, 382-389.
58. Belaid, A.; Aouni, M.; Khelifa, R.; Trabelsi, A.; Jemmali, M.; Hani, K. In vitro antiviral activity of dermaseptins against herpes simplex virus type 1. J. Med. Virol. 2002, 66, 229-234.
59. Andersen, J.H.; Jenssen, H.; Gutteberg, T.J. Lactoferrin and lactoferricin inhibit Herpes simplex 1 and 2 infection and exhibit synergy when combined with acyclovir. Antiviral Res. 2003, 58, 209-215.
60. Daher, K.A.; Selsted, M.E.; Lehrer, R.I. Direct inactivation of viruses by human granulocyte defensins. J. Virol. 1986, 60, 1068-1074.
61. Jenssen, H.; Andersen, J.H.; Uhlin-Hansen, L.; Gutteberg, T.J.; Rekdal, O. Anti-HSV activity of lactoferricin analogues is only partly related to their affinity for heparan sulfate. Antiviral Res. 2004, 61, 101-109.
62. Lehrer, R.I.; Szklarek, D.; Ganz, T.; Selsted, M.E. Correlation of binding of rabbit granulocyte peptides to Candida albicans with candidacidal activity. Infect. Immun. 1985, 49, 207-211.
63. Sinha, S.; Cheshenko, N.; Lehrer, R.I.; Herold, B.C. NP-1, a rabbit alpha-defensin, prevents the entry and intercellular spread of herpes simplex virus type 2. Antimicrob. Agents Chemother. 2003, 47, 494-500.
64. Yasin, B.; Wang, W.; Pang, M.; Cheshenko, N.; Hong, T.; Waring, A.J.; Herold, B.C.; Wagar, E.A.; Lehrer, R.I. Theta defensins protect cells from infection by herpes simplex virus by inhibiting viral adhesion and entry. J. Virol. 2004, 78, 5147-5156.
65. Robinson, W.E., Jr.; McDougall, B.; Tran, D.; Selsted, M.E. Anti-HIV-1 activity of indolicidin, an antimicrobial peptide from neutrophils. J. Leukoc. Biol. 1998, 63, 94-100.
66. Jenssen, H.; Andersen, J.H.; Mantzilas, D.; Gutteberg, T.J. A wide range of medium-sized, highly cationic, alpha-helical peptides show antiviral activity against herpes simplex virus. Antiviral Res. 2004, 64, 119-126.
67. Tamamura, H.; Murakami, T.; Masuda, M.; Otaka, A.; Takada, W.; Ibuka, T.; Nakashima, H.; Waki, M.; Matsumoto, A.; Yamamoto, N.; et al. Structure-activity relationships of an anti-HIV peptide, T22. Biochem. Biophys. Res. Commun. 1994, 205, 1729-1735.
68. Lee, D.G.; Hahm, K.S.; Shin, S.Y. Structure and fungicidal activity of a synthetic antimicrobial peptide, P18, and its truncated peptides. Biotechnol. Lett. 2004, 26, 337-341.
69. Jenssen, H.; Gutteberg, T.J.; Lejon, T. Modelling of anti-HSV activity of lactoferricin analogues using amino acid descriptors. J. Pept. Sci. 2005, 11, 97-103.
70. Giansanti, F.; Massucci, M.T.; Giardi, M.F.; Nozza, F.; Pulsinelli, E.; Nicolini, C.; Botti, D.; Antonini, G. Antiviral activity of ovotransferrin derived peptides. Biochem. Biophys. Res. Commun. 2005, 331, 69-73.
71. Gesell, J.; Zasloff, M.; Opella, S.J. Two-dimensional 1H NMR experiments show that the 23-residue magainin antibiotic peptide is an alpha-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution. J. Biomol. NMR 1997, 9, 127-135.
72. Ramos-Onsins, S.; Aguade, M. Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes. Genetics 1998, 150, 157-171.
73. Habermann, E.; Jentsch, J. [Sequence analysis of melittin from tryptic and peptic degradation products]. Hoppe Seylers Z Physiol. Chem. 1967, 348, 37-50.
74. Gudmundsson, G.H.; Agerberth, B.; Odeberg, J.; Bergman, T.; Olsson, B.; Salcedo, R. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur. J. Biochem. 1996, 238, 325-332.
75. Conlon, J.M.; Al-Ghaferi, N.; Abraham, B.; Jiansheng, H.; Cosette, P.; Leprince, J.; Jouenne, T.; Vaudry, H. Antimicrobial peptides from diverse families isolated from the skin of the Asian frog, Rana grahami. Peptides 2006, 27, 2111-2117.
76. Tang, Y.Q.; Yuan, J.; Osapay, G.; Osapay, K.; Tran, D.; Miller, C.J.; Ouellette, A.J.; Selsted, M.E. A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated alpha-defensins. Science 1999, 286, 498-502.
77. Sawai, M.V.; Jia, H.P.; Liu, L.; Aseyev, V.; Wiencek, J.M.; McCray, P.B., Jr.; Ganz, T.; Kearney, W.R.; Tack, B.F. The NMR structure of human beta-defensin-2 reveals a novel alphahelical segment. Biochemistry 2001, 40, 3810-3816.
78. McManus, A.M.; Dawson, N.F.; Wade, J.D.; Carrington, L.E.; Winzor, D.J.; Craik, D.J. Threedimensional structure of RK-1: a novel alpha-defensin peptide. Biochemistry 2000, 39, 15757-15764.
79. Mor, A.; Nguyen, V.H.; Delfour, A.; Migliore-Samour, D.; Nicolas, P. Isolation, amino acid sequence, and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin. Biochemistry 1991, 30, 8824-8830.
80. Nakamura, T.; Furunaka, H.; Miyata, T.; Tokunaga, F.; Muta, T.; Iwanaga, S.; Niwa, M.; Takao, T.; Shimonishi, Y. Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure. J. Biol. Chem. 1988, 263, 16709-16713.
81. Aumelas, A.; Mangoni, M.; Roumestand, C.; Chiche, L.; Despaux, E.; Grassy, G.; Calas, B.; Chavanieu, A. Synthesis and solution structure of the antimicrobial peptide protegrin-1. Eur. J. Biochem. 1996, 237, 575-583.
82. Andersen, J.H.; Osbakk, S.A.; Vorland, L.H.; Traavik, T.; Gutteberg, T.J. Lactoferrin and cyclic lactoferricin inhibit the entry of human cytomegalovirus into human fibroblasts. Antiviral Res. 2001, 51, 141-149.
83. Marr, A.K.; Jenssen, H.; Moniri, M.R.; Hancock, R.E.W.; Pante, N. Bovine lactoferrin and lactoferricin interfere with intracellular trafficking of Herpes simplex virus-1. Biochimie 2009, 91, 160-164.
84. Bellamy, W.; Wakabayashi, H.; Takase, M.; Kawase, K.; Shimamura, S.; Tomita, M. Killing of Candida albicans by lactoferricin B, a potent antimicrobial peptide derived from the N-terminal region of bovine lactoferrin. Med. Microbiol. Immunol. (Berl) 1993, 182, 97-105.
85. Hug, D.H.; Hunter, J.K.; Dunkerson, D.D. Malnutrition, urocanic acid, and sun may interact to suppress immunity in sojourners to high altitude. Aviat. Space Environ. Med. 2001, 72, 136-145.
86. Kolset, S.O.; Gallagher, J.T. Proteoglycans in haemopoietic cells. Biochim. Biophys. Acta 1990, 1032, 191-211.
87. Iozzo, R.V.; Murdoch, A.D. Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. Faseb J. 1996, 10, 598-614.
88. Bernfield, M.; Kokenyesi, R.; Kato, M.; Hinkes, M.T.; Spring, J.; Gallo, R.L.; Lose, E.J. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 1992, 8, 365-393.
89. Parker, K.H.; Winlove, C.P.; Maroudas, A. The theoretical distributions and diffusivities of small ions in chondroitin sulphate and hyaluronate. Biophys. Chem. 1988, 32, 271-282.
90. Iida, J.; Meijne, A.M.; Oegema, T.R., Jr.; Yednock, T.A.; Kovach, N.L.; Furcht, L.T.; McCarthy, J.B. A role of chondroitin sulfate glycosaminoglycan binding site in alpha4beta1 integrinmediated melanoma cell adhesion. J. Biol. Chem. 1998, 273, 5955-5962.
91. Pettersson, I.; Kusche, M.; Unger, E.; Wlad, H.; Nylund, L.; Lindahl, U.; Kjellen, L. Biosynthesis of heparin. Purification of a 110-kDa mouse mastocytoma protein required for both glucosaminyl N-deacetylation and N-sulfation. J. Biol. Chem. 1991, 266, 8044-8049.
92. Camejo, E.H.; Rosengren, B.; Camejo, G.; Sartipy, P.; Fager, G.; Bondjers, G. Interferon gamma binds to extracellular matrix chondroitin-sulfate proteoglycans, thus enhancing its cellular response. Arterioscler. Thromb. Vasc. Biol. 1995, 15, 1456-1465.
93. Hoogewerf, A.J.; Kuschert, G.S.; Proudfoot, A.E.; Borlat, F.; Clark-Lewis, I.; Power, C.A.; Wells, T.N. Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 1997, 36, 13570-13578.
94. Lookene, A.; Savonen, R.; Olivecrona, G. Interaction of lipoproteins with heparan sulfate proteoglycans and with lipoprotein lipase. Studies by surface plasmon resonance technique. Biochemistry 1997, 36, 5267-5275.
95. Olsson, U.; Camejo, G.; Hurt-Camejo, E.; Elfsber, K.; Wiklund, O.; Bondjers, G. Possible functional interactions of apolipoprotein B-100 segments that associate with cell proteoglycans and the ApoB/E receptor. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 149-155.
96. Mettenleiter, T.C. Brief overview on cellular virus receptors. Virus Res. 2002, 82, 3-8.
97. Spillmann, D. Heparan sulfate: anchor for viral intruders? Biochimie 2001, 83, 811-817.
98. Jenssen, H.; Sandvik, K.; Andersen, J.H.; Hancock, R.E.W.; Gutteberg, T.J. Inhibition of HSV cell-to-cell spread by lactoferrin and lactoferricin. Antiviral Res. 2008, 79, 192-198.
99. Song, B.H.; Lee, G.C.; Moon, M.S.; Cho, Y.H.; Lee, C.H. Human cytomegalovirus binding to heparan sulfate proteoglycans on the cell surface and/or entry stimulates the expression of human leukocyte antigen class I. J. Gen. Virol. 2001, 82, 2405-2413.
100. Argyris, E.G.; Acheampong, E.; Nunnari, G.; Mukhtar, M.; Williams, K.J.; Pomerantz, R.J. Human immunodeficiency virus type 1 enters primary human brain microvascular endothelial cells by a mechanism involving cell surface proteoglycans independent of lipid rafts. J. Virol. 2003, 77, 12140-12151.
101. James, S.; Gibbs, B.F.; Toney, K.; Bennett, H.P. Purification of antimicrobial peptides from an extract of the skin of Xenopus laevis using heparin-affinity HPLC: characterization by ion-spray mass spectrometry. Anal. Biochem. 1994, 217, 84-90.
102. Schmidtchen, A.; Frick, I.M.; Andersson, E.; Tapper, H.; Bjorck, L. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 2002, 46, 157-168.
103. Schmidtchen, A.; Frick, I.M.; Bjorck, L. Dermatan sulphate is released by proteinases of common pathogenic bacteria and inactivates antibacterial alpha-defensin. Mol. Microbiol. 2001, 39, 708-713.
104. Mann, D.M.; Romm, E.; Migliorini, M. Delineation of the glycosaminoglycan-binding site in the human inflammatory response protein lactoferrin. J. Biol. Chem. 1994, 269, 23661-23667.
105. Shimazaki, K.; Tazume, T.; Uji, K.; Tanaka, M.; Kumura, H.; Mikawa, K.; Shimo-Oka, T. Properties of a heparin-binding peptide derived from bovine lactoferrin. J. Dairy Sci. 1998, 81, 2841-2849.
106. Fromm, J.R.; Hileman, R.E.; Caldwell, E.E.; Weiler, J.M.; Linhardt, R.J. Differences in the interaction of heparin with arginine and lysine and the importance of these basic amino acids in the binding of heparin to acidic fibroblast growth factor. Arch. Biochem. Biophys. 1995, 323, 279-287.
107. Hileman, R.E.; Fromm, J.R.; Weiler, J.M.; Linhardt, R.J. Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 1998, 20, 156-167.
108. Stenlund, P.; Lindberg, M.J.; Tibell, L.A. Structural requirements for high-affinity heparin binding: alanine scanning analysis of charged residues in the C-terminal domain of human extracellular superoxide dismutase. Biochemistry 2002, 41, 3168-3175.
109. Jenssen, H.; Gutteberg, T.J.; Rekdal, O.; Lejon, T. Prediction of activity, synthesis and biological testing of anti-HSV active peptides. Chem. Biol. Drug Des. 2006, 68, 58-66.
110. Hutton, R.D.; Ewert, D.L.; French, G.R. Differentiation of types 1 and 2 herpes simplex virus by plaque inhibition with sulfated polyanions. Proc. Soc. Exp. Biol. Med. 1973, 142, 27-29.
111. Langeland, N.; Moore, L.J.; Holmsen, H.; Haarr, L. Interaction of polylysine with the cellular receptor for herpes simplex virus type 1. J. Gen. Virol. 1988, 69 (Pt 6), 1137-1145.
112. Dathe, M.; Wieprecht, T. Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells. Biochim. Biophys. Acta 1999, 1462, 71-87.
113. Sitaram, N.; Nagaraj, R. Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity. Biochim Biophys Acta 1999, 1462, 29-54.
114. Lorin, C.; Saidi, H.; Belaid, A.; Zairi, A.; Baleux, F.; Hocini, H.; Belec, L.; Hani, K.; Tangy, F. The antimicrobial peptide dermaseptin S4 inhibits HIV-1 infectivity in vitro. Virology 2005, 334, 264-275.
115. Murakami, T.; Niwa, M.; Tokunaga, F.; Miyata, T.; Iwanaga, S. Direct virus inactivation of tachyplesin I and its isopeptides from horseshoe crab hemocytes. Chemotherapy 1991, 37, 327-334.
116. Perez, A.; Li, Q.X.; Perez-Romero, P.; Delassus, G.; Lopez, S.R.; Sutter, S.; McLaren, N.; Fuller, A.O. A new class of receptor for herpes simplex virus has heptad repeat motifs that are common to membrane fusion proteins. J. Virol. 2005, 79, 7419-7430.
117. Perez-Romero, P.; Fuller, A.O. The C terminus of the B5 receptor for herpes simplex virus contains a functional region important for infection. J. Virol. 2005, 79, 7431-7437.
118. Bowdish, D.M.; Davidson, D.J.; Scott, M.G.; Hancock, R.E.W. Immunomodulatory activities of small host defense peptides. Antimicrob. Agents Chemother. 2005, 49, 1727-1732.
119. Javadpour, M.M.; Barkley, M.D. Self-assembly of designed antimicrobial peptides in solution and micelles. Biochemistry 1997, 36, 9540-9549.
120. Chang, T.L.; Vargas, J., Jr.; DelPortillo, A.; Klotman, M.E. Dual role of alpha-defensin-1 in anti-HIV-1 innate immunity. J. Clin. Invest. 2005, 115, 765-773.
121. Futaki, S.; Nakase, I.; Suzuki, T.; Youjun, Z.; Sugiura, Y. Translocation of branched-chain arginine peptides through cell membranes: flexibility in the spatial disposition of positive charges in membrane-permeable peptides. Biochemistry 2002, 41, 7925-7930.
122. Futaki, S. Arginine-rich peptides: potential for intracellular delivery of macromolecules and the mystery of the translocation mechanisms. Int. J. Pharm. 2002, 245, 1-7.
123. Suzuki, T.; Futaki, S.; Niwa, M.; Tanaka, S.; Ueda, K.; Sugiura, Y. Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem. 2002, 277, 2437-2443.
124. Penco, S.; Scarfi, S.; Giovine, M.; Damonte, G.; Millo, E.; Villaggio, B.; Passalacqua, M.; Pozzolini, M.; Garre, C.; Benatti, U. Identification of an import signal for, and the nuclear localization of, human lactoferrin. Biotechnol. Appl. Biochem. 2001, 34, 151-159.
125. Hsu, C.H.; Chen, C.; Jou, M.L.; Lee, A.Y.; Lin, Y.C.; Yu, Y.P.; Huang, W.T.; Wu, S.H. Structural and DNA-binding studies on the bovine antimicrobial peptide, indolicidin: evidence for multiple conformations involved in binding to membranes and DNA. Nucleic Acids Res. 2005, 33, 4053-4064.
126. Kanyshkova, T.G.; Semenov, D.V.; Buneva, V.N.; Nevinsky, G.A. Human milk lactoferrin binds two DNA molecules with different affinities. FEBS Lett. 1999, 451, 235-237.
127. Park, C.B.; Kim, H.S.; Kim, S.C. Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun. 1998, 244, 253-257.
128. Song, Y.M.; Park, Y.; Lim, S.S.; Yang, S.T.; Woo, E.R.; Park, I.S.; Lee, J.S.; Kim, J.I.; Hahm, K.S.; Kim, Y.; Shin, S.Y. Cell selectivity and mechanism of action of antimicrobial model peptides containing peptoid residues. Biochemistry 2005, 44, 12094-12106.
129. Sandgren, S.; Wittrup, A.; Cheng, F.; Jonsson, M.; Eklund, E.; Busch, S.; Belting, M. The human antimicrobial peptide LL-37 transfers extracellular DNA plasmid to the nuclear compartment of mammalian cells via lipid rafts and proteoglycan-dependent endocytosis. J. Biol. Chem. 2004, 279, 17951-17956.
130. Bowdish, D.M.; Davidson, D.J.; Lau, Y.E.; Lee, K.; Scott, M.G.; Hancock, R.E.W. Impact of LL-37 on anti-infective immunity. J. Leukoc. Biol. 2005, 77, 451-459.
131. Scott, M.G.; Davidson, D.J.; Gold, M.R.; Bowdish, D.; Hancock, R.E.W. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J. Immunol. 2002, 169, 3883-3891.
132. Luebke, R.W.; Parks, C.; Luster, M.I. Suppression of immune function and susceptibility to infections in humans: association of immune function with clinical disease. J. Immunotoxicol. 2004, 1, 15-24.
133. Suntharalingam, G.; Perry, M.R.; Ward, S.; Brett, S.J.; Castello-Cortes, A.; Brunner, M.D.; Panoskaltsis, N. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N. Engl. J. Med. 2006, 355, 1018-1028.
134. Niyonsaba, F.; Someya, A.; Hirata, M.; Ogawa, H.; Nagaoka, I. Evaluation of the effects of peptide antibiotics human beta-defensins-1/-2 and LL-37 on histamine release and prostaglandin D(2) production from mast cells. Eur. J. Immunol. 2001, 31, 1066-1075.
135. Gilliet, M.; Lande, R. Antimicrobial peptides and self-DNA in autoimmune skin inflammation. Curr. Opin. Immunol. 2008, 20, 401-407.
136. Podolsky, D.K. Inflammatory bowel disease. N. Engl. J. Med. 2002, 347, 417-429.
137. Wehkamp, J.; Fellermann, K.; Herrlinger, K.R.; Baxmann, S.; Schmidt, K.; Schwind, B.; Duchrow, M.; Wohlschlager, C.; Feller, A.C.; Stange, E.F. Human beta-defensin 2 but not betadefensin 1 is expressed preferentially in colonic mucosa of inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol. 2002, 14, 745-752.
138. Wehkamp, J.; Harder, J.; Weichenthal, M.; Mueller, O.; Herrlinger, K.R.; Fellermann, K.; Schroeder, J.M.; Stange, E.F. Inducible and constitutive beta-defensins are differentially expressed in Crohn's disease and ulcerative colitis. Inflamm. Bowel Dis. 2003, 9, 215-223.
139. Schauber, J.; Rieger, D.; Weiler, F.; Wehkamp, J.; Eck, M.; Fellermann, K.; Scheppach, W.; Gallo, R.L.; Stange, E.F. Heterogeneous expression of human cathelicidin hCAP18/LL-37 in inflammatory bowel diseases. Eur. J. Gastroenterol. Hepatol. 2006, 18, 615-621.
140. Wehkamp, J.; Schmid, M.; Stange, E.F. Defensins and other antimicrobial peptides in inflammatory bowel disease. Curr. Opin. Gastroenterol. 2007, 23, 370-378.
141. Biron, E.; Chatterjee, J.; Ovadia, O.; Langenegger, D.; Brueggen, J.; Hoyer, D.; Schmid, H.A.; Jelinek, R.; Gilon, C.; Hoffman, A.; Kessler, H. Improving oral bioavailability of peptides by multiple N-methylation: somatostatin analogues. Angew. Chem. Int. Ed. Engl. 2008, 47, 2595-2599.
142. Chatterjee, J.; Gilon, C.; Hoffman, A.; Kessler, H. N-methylation of peptides: a new perspective in medicinal chemistry. Acc. Chem. Res. 2008, 41, 1331-1342.
143. Barnard, D.L. Pegasys (Hoffmann-La Roche). Curr. Opin. Investig. Drugs 2001, 2, 1530-1538.
144. Davidson, D.J.; Currie, A.J.; Reid, G.S.; Bowdish, D.M.; MacDonald, K.L.; Ma, R.C.; Hancock, R.E.W.; Speert, D.P. The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J. Immunol. 2004, 172, 1146-1156.
145. Schijns, V.E. Immunological concepts of vaccine adjuvant activity. Curr. Opin. Immunol. 2000, 12, 456-463.
146. Graham, B.S.; Johnson, T.R.; Peebles, R.S. Immune-mediated disease pathogenesis in respiratory syncytial virus infection. Immunopharmacology 2000, 48, 237-247.
147. Waris, M.E.; Tsou, C.; Erdman, D.D.; Zaki, S.R.; Anderson, L.J. Respiratory synctial virus infection in BALB/c mice previously immunized with formalin-inactivated virus induces enhanced pulmonary inflammatory response with a predominant Th2-like cytokine pattern. J. Virol. 1996, 70, 2852-2860.
148. Kovacs-Nolan, J.; Mapletoft, J.W.; Lawman, Z.; Babiuk, L.A.; van Drunen Littel-van den Hurk, S. Formulation of bovine respiratory syncytial virus fusion protein with CpG oligodeoxynucleotide, cationic host defence peptide and polyphosphazene enhances humoral and cellular responses and induces a protective type 1 immune response in mice. J. Gen. Virol. 2009, 90, 1892-1905.
149. Kovacs-Nolan, J.; Mapletoft, J.W.; Latimer, L.; Babiuk, L.A.; Hurk, S.D. CpG oligonucleotide, host defense peptide and polyphosphazene act synergistically, inducing long-lasting, balanced immune responses in cattle. Vaccine 2009, 27, 2048-2054.
150. Kovacs-Nolan, J.; Latimer, L.; Landi, A.; Jenssen, H.; Hancock, R.E.W.; Babiuk, L.A.; van Drunen Littel-van den Hurk, S. The novel adjuvant combination of CpG ODN, indolicidin and polyphosphazene induces potent antibody-and cell-mediated immune responses in mice. Vaccine 2009, 27, 2055-2064.
151. Kindrachuk, J.; Jenssen, H.; Elliott, M.; Townsend, R.; Nijnik, A.; Lee, S.F.; Gerdts, V.; Babiuk, L.A.; Halperin, S.A.; Hancock, R.E.W. A novel vaccine adjuvant comprised of a synthetic innate defence regulator peptide and CpG oligonucleotide links innate and adaptive immunity. Vaccine 2009, 27, 4662-4671.
152. Fritz, J.H.; Brunner, S.; Birnstiel, M.L.; Buschle, M.; Gabain, A.; Mattner, F.; Zauner, W. The artificial antimicrobial peptide KLKLLLLLKLK induces predominantly a TH2-type immune response to co-injected antigens. Vaccine 2004, 22, 3274-3284.
153. Lingnau, K.; Egyed, A.; Schellack, C.; Mattner, F.; Buschle, M.; Schmidt, W. Poly-L-arginine synergizes with oligodeoxynucleotides containing CpG-motifs (CpG-ODN) for enhanced and prolonged immune responses and prevents the CpG-ODN-induced systemic release of proinflammatory cytokines. Vaccine 2002, 20, 3498-3508.
154. Aichinger, M.C.; Ortbauer, M.; Reipert, S.; Zauner, W.; Bogner, P.; Froschauer, E.; Nowikovsky, K.; Lingnau, K.; von Gabain, A.; Schweyen, R.; Henics, T. Unique membraneinteracting properties of the immunostimulatory cationic peptide KLKL(5)KLK (KLK). Cell Biol. Int. 2008, 32, 1449-1458.
155. Schellack, C.; Prinz, K.; Egyed, A.; Fritz, J.H.; Wittmann, B.; Ginzler, M.; Swatosch, G.; Zauner, W.; Kast, C.; Akira, S.; von Gabain, A.; Buschle, M.; Lingnau, K. IC31, a novel adjuvant signaling via TLR9, induces potent cellular and humoral immune responses. Vaccine 2006, 24, 5461-5472.
156. Andersson, L.; Blomberg, L.; Flegel, M.; Lepsa, L.; Nilsson, B.; Verlander, M. Large-scale synthesis of peptides. Biopolymers 2000, 55, 227-250.
157. Schneider, S.E.; Bray, B.L.; Mader, C.J.; Friedrich, P.E.; Anderson, M.W.; Taylor, T.S.; Boshernitzan, N.; Niemi, T.E.; Fulcher, B.C.; Whight, S.R.; White, J.M.; Greene, R.J.; Stoltenberg, L.E.; Lichty, M. Development of HIV fusion inhibitors. J. Pept. Sci. 2005, 11, 744-753.
158. Gottlieb, C.T.; Thomsen, L.E.; Ingmer, H.; Mygind, P.H.; Kristensen, H.H.; Gram, L. Antimicrobial peptides effectively kill a broad spectrum of Listeria monocytogenes and Staphylococcus aureus strains independently of origin, sub-type, or virulence factor expression. BMC Microbiol. 2008, 8, 205.
159. Goldstein, A.L.; Low, T.L.; McAdoo, M.; McClure, J.; Thurman, G.B.; Rossio, J.; Lai, C.Y.; Chang, D.; Wang, S.S.; Harvey, C.; Ramel, A.H.; Meienhofer, J. Thymosin alpha1: isolation and sequence analysis of an immunologically active thymic polypeptide. Proc. Natl. Acad. Sci. U S A 1977, 74, 725-729.
160. Rasi, G.; Pierimarchi, P.; Sinibaldi Vallebona, P.; Colella, F.; Garaci, E. Combination therapy in the treatment of chronic viral hepatitis and prevention of hepatocellular carcinoma. Int Immunopharmacol 2003, 3, 1169-1176.
161. Anisimov, V.N.; Khavinson, V.K.; Morozov, V.G. Immunomodulatory synthetic dipeptide LGlu-L-Trp slows down aging and inhibits spontaneous carcinogenesis in rats. Biogerontology 2000, 1, 55-59.
162. Tulpule, A.; Scadden, D.T.; Espina, B.M.; Cabriales, S.; Howard, W.; Shea, K.; Gill, P.S. Results of a randomized study of IM862 nasal solution in the treatment of AIDS-related Kaposi's sarcoma. J. Clin. Oncol. 2000, 18, 716-723.
163. Bergeon, J.A.; Toth, I. Enhancement of oral drug absorption-effect of lipid conjugation on the enzymatic stability and intestinal permeability of l-Glu-l-Trp-NH(2). Bioorg. Med. Chem. 2007, 15, 7048-7057.
164. Rose, W.A., 2nd; Tuthill, C.; Pyles, R.B. An immunomodulating dipeptide, SCV-07, is a potential therapeutic for recurrent genital herpes simplex virus type 2 (HSV-2). Int. J. Antimicrob. Agents 2008, 32, 262-266.