Mammalian antimicrobial proteins and peptides: Overview on the RNase A superfamily members involved in innate host defence

Molecular BioSystems

Volumn 3, Issue 5, 2007, Pages 317-335

  Boix, Ester ^a   Nogués, M Victòria ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; PANCREATIC RIBONUCLEASE; PEPTIDE; PROTEIN;

ANIMAL; ARTICLE; BACTERIUM; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM;

ANIMALS; ANTI-INFECTIVE AGENTS; BACTERIA; HUMANS; IMMUNITY, NATURAL; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; PEPTIDES; PROTEINS; RIBONUCLEASE, PANCREATIC;

BACTERIA (MICROORGANISMS); BOVINAE; EUKARYOTA; FUNGI; MAMMALIA;

EID: 34247645414     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/b617527a     Document Type: Article

References (141)

1. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 2002 415 389 395
2. V. M. D'Costa K. M. McGrann D. W. Hughes G. D. Wright Sampling the antibiotic resistome Science 2006 311 374 377
3. R. E. Hancock H. G. Sahl Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat. Biotechnol. 2006 24 1551 1557
4. J. P. Powers R. E. Hancock The relationship between peptide structure and antibacterial activity Peptides 2003 24 1681 1691
5. K. L. Brown R. E. Hancock Cationic host defense (antimicrobial) peptides Curr. Opin. Immunol. 2006 18 24 30
6. P. Bulet R. Stocklin L. Menin Anti-microbial peptides: from invertebrates to vertebrates Immunol. Rev. 2004 198 169 184
7. R. E. Hancock Cationic peptides: effectors in innate immunity and novel antimicrobials Lancet Infect. Dis. 2001 1 156 164
8. C. A. Muller I. B. Autenrieth A. Peschel Innate defenses of the intestinal epithelial barrier Cell. Mol. Life Sci. 2005 62 1297 1307
9. D. T. Fearon R. M. Locksley The instructive role of innate immunity in the acquired immune response Science 1996 272 50 53
10. R. E. Hancock Peptide antibiotics Lancet 1997 349 418 422
11. O. Levy Antimicrobial proteins and peptides of blood: templates for novel antimicrobial agents Blood 2000 96 2664 2672
12. I. Ginsburg Bactericidal cationic peptides can also function as bacteriolysis-inducing agents mimicking beta-lactam antibiotics?; it is enigmatic why this concept is consistently disregarded Med. Hypotheses 2004 62 367 374
13. N. Papo Y. Shai Host defense peptides as new weapons in cancer treatment Cell. Mol. Life Sci. 2005 62 784 790
14. T. Nurnberger F. Brunner Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns Curr. Opin. Plant Biol. 2002 5 318 324
15. C. Zipfel G. Felix Plants and animals: a different taste for microbes? Curr. Opin. Plant Biol. 2005 8 353 360
16. M. Caroff D. Karibian Structure of bacterial lipopolysaccharides Carbohydr. Res. 2003 338 2431 2447
17. H. Nikaido Molecular basis of bacterial outer membrane permeability revisited Microbiol. Mol. Biol. Rev. 2003 67 593 656
18. Y. Rosenfeld N. Papo Y. Shai Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides. Peptide properties and plausible modes of action J. Biol. Chem. 2006 281 1636 1643
19. J. Cohen The immunopathogenesis of sepsis Nature 2002 420 885 891
20. B. A. Dmitriev F. V. Toukach K. J. Schaper O. Holst E. T. Rietschel S. Ehlers Tertiary structure of bacterial murein: the scaffold model J. Bacteriol. 2003 185 3458 3468
21. B. A. Dmitriev F. V. Toukach O. Holst E. T. Rietschel S. Ehlers Tertiary structure of Staphylococcus aureus cell wall murein J. Bacteriol. 2004 186 7141 7148
22. D. D. Leonidas E. Boix R. Prill M. Suzuki R. Turton K. Minson G. J. Swaminathan R. J. Joule K. R. Acharya Mapping the ribonucleolytic active site of eosinophil-derived neurotoxin (EDN). High resolution crystal structures of EDN complexes with adenylic nucleotide inhibitors J. Biol. Chem. 2001 276 15009 15017
23. F. C. Neuhaus J. Baddiley A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria Microbiol. Mol. Biol. Rev. 2003 67 686 723
24. A. R. Archibald J. Baddiley J. E. Heckels Molecular arrangement of teichoic acid in the cell wall of Staphylococcus lactis Nat. New. Biol. 1973 241 29 31
25. T. Arizono A. Umeda K. Amako Distribution of capsular materials on the cell wall surface of strain Smith diffuse of Staphylococcus aureus J. Bacteriol. 1991 173 4333 4340
26. L. L. Graham T. J. Beveridge Structural differentiation of the Bacillus subtilis 168 cell wall J. Bacteriol. 1994 176 1413 1421
27. T. Gutberlet J. Frank H. Bradaczek W. Fischer Effect of lipoteichoic acid on thermotropic membrane properties J. Bacteriol. 1997 179 2879 2883
28. D. Andreu L. Rivas Animal antimicrobial peptides: an overview Biopolymers 1998 47 415 433
29. K. Hilpert R. Volkmer-Engert T. Walter R. E. Hancock High-throughput generation of small antibacterial peptides with improved activity Nat. Biotechnol. 2005 23 1008 1012
30. Y. Shai Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides Biochim. Biophys. Acta 1999 1462 55 70
31. Z. Oren Y. Shai Mode of action of linear amphipathic alpha-helical antimicrobial peptides Biopolymers 1998 47 451 463
32. G. H. Gudmundsson B. Agerberth Neutrophil antibacterial peptides, multifunctional effector molecules in the mammalian immune system J. Immunol. Methods 1999 232 45 54
33. K. During P. Porsch A. Mahn O. Brinkmann W. Gieffers The non-enzymatic microbicidal activity of lysozymes FEBS Lett. 1999 449 93 100
34. H. Kuwata T. T. Yip M. Tomita T. W. Hutchens Direct evidence of the generation in human stomach of an antimicrobial peptide domain (lactoferricin) from ingested lactoferrin Biochim. Biophys. Acta 1998 1429 129 141
35. P. H. Nibbering E. Ravensbergen M. M. Welling L. A. van Berkel P. H. van Berkel E. K. Paulwels J. H. Nuijens Human lactoferrin and peptides derived from its N terminus are highly effective against infections with antibiotic-resistant bacteria Infect. Immun. 2001 69 1469 1476
36. M. Zanetti R. Gennaro D. Romeo Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain FEBS Lett. 1995 374 1 5
37. T. Ayabe D. P. Satchell P. Pesendorfer, et al. Activation of Paneth cell alpha-defensins in mouse small intestine J. Biol. Chem. 2002 277 5219 5228
38. K. Matsuzaki Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes Biochim. Biophys. Acta 1999 1462 1 10
39. K. Lohner S. E. Blondelle Molecular mechanisms of membrane perturbation by antimicrobial peptides and the use of biophysical studies in the design of novel peptide antibiotics Comb. Chem. High Throughput Screening 2005 8 241 256
40. A. S. Ulrich W. Tichelaar G. Forster O. Zschornig S. Weinkauf H. W. Meyer Ultrastructural characterization of peptide-induced membrane fusion and peptide self-assembly in the lipid bilayer Biophys. J. 1999 77 829 841
41. A. D. Ferguson W. Welte E. Hofmann, et al. A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins Structure 2000 8 585 592
42. A. D. Ferguson E. Hofmann J. W. Coulton K. Diederichs W. Welte Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide Science 1998 282 2215 2220
43. R. E. Hancock D. S. Chapple Peptide antibiotics Antimicrob. Agents Chemother. 1999 43 1317 1323
44. D. S. Chapple R. Hussain C. L. Joannou, et al. Structure and association of human lactoferrin peptides with Escherichia coli lipopolysaccharide Antimicrob. Agents Chemother. 2004 48 2190 2198
45. N. Papo Y. Shai Can we predict biological activity of antimicrobial peptides from their interactions with model phospholipid membranes? Peptides 2003 24 1693 1703
46. R. Dziarski D. Gupta Peptidoglycan recognition in innate immunity J. Endotoxin Res. 2005 11 304 310
47. S. E. Girardin D. J. Philpott Mini-review: the role of peptidoglycan recognition in innate immunity Eur. J. Immunol. 2004 34 1777 1782
48. R. E. Hancock A. Rozek Role of membranes in the activities of antimicrobial cationic peptides FEMS Microbiol. Lett. 2002 206 143 149
49. E. S. Lander L. M. Linton B. Birren, et al. Initial sequencing and analysis of the human genome Nature 2001 409 860 921
50. J. P. Bielawski Z. Yang A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J. Mol. Evol. 2004 59 121 132
51. R. I. Lehrer D. Szklarek A. Barton T. Ganz K. J. Hamann G. J. Gleich Antibacterial properties of eosinophil major basic protein and eosinophil cationic protein J. Immunol. 1989 142 4428 4434
52. W. C. Wimley M. E. Selsted S. H. White Interactions between human defensins and lipid bilayers: evidence for formation of multimeric pores Protein Sci. 1994 3 1362 1373
53. J. Harder J. M. Schroder RNase 7, a novel innate immune defense antimicrobial protein of healthy human skin J. Biol. Chem. 2002 277 46779 46784
54. A. Di Nardo A. Vitiello R. L. Gallo Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide J. Immunol. 2003 170 2274 2278
55. M. D. Davis D. A. Plager T. J. George E. A. Weiss G. J. Gleich K. M. Leiferman Interactions of eosinophil granule proteins with skin: limits of detection, persistence, and vasopermeabilization J. Allergy Clin. Immunol. 2003 112 988 994
56. L. J. Beamer S. F. Carroll D. Eisenberg The BPI/LBP family of proteins: a structural analysis of conserved regions Protein Sci. 1998 7 906 914
57. L. J. Beamer S. F. Carroll D. Eisenberg Crystal structure of human BPI and two bound phospholipids at 2.4 angstrom resolution Science 1997 276 1861 1864
58. L. J. Beamer Structure of human BPI (bactericidal/permeability-increasing protein) and implications for related proteins Biochem. Soc. Trans. 2003 31 791 794
59. P. Elsbach J. Weiss Role of the bactericidal/permeability-increasing protein in host defence Curr. Opin. Immunol. 1998 10 45 49
60. J. E. Gabay Ubiquitous natural antibiotics Science 1994 264 373 374
61. L. J. Beamer S. F. Carroll D. Eisenberg The three-dimensional structure of human bactericidal/permeability-increasing protein: implications for understanding protein-lipopolysaccharide interactions Biochem. Pharmacol. 1999 57 225 229
62. W. Strober P. J. Murray A. Kitani T. Watanabe Signalling pathways and molecular interactions of NOD1 and NOD2 Nat. Rev. Immunol. 2006 6 9 20
63. R. T. Ellison, 3rd T. J. Giehl Killing of gram-negative bacteria by lactoferrin and lysozyme J. Clin. Invest. 1991 88 1080 1091
64. A. A. Glynn C. M. Milne Lysozyme and immune bacteriolysis Nature 1965 207 1309 1310
65. P. Jolles J. Jolles What's new in lysozyme research? Always a model system, today as yesterday Mol. Cell. Biochem. 1984 63 165 189
66. K. Brandenburg M. H. Koch U. Seydel Biophysical characterisation of lysozyme binding to LPS Re and lipid A Eur. J. Biochem. 1998 258 686 695
67. G. J. Gleich Mechanisms of eosinophil-associated inflammation J. Allergy Clin. Immunol. 2000 105 651 663
68. A. A. Humbles C. M. Lloyd S. J. McMillan D. S. Friend G. Xanthou E. E. McKenna S. Ghiran N. P. Gerard C. Yu S. H. Orkin C. Gerard A critical role for eosinophils in allergic airways remodeling Science 2004 305 1776 1779
69. R. I. Abu-Ghazaleh G. J. Gleich F. G. Prendergast Interaction of eosinophil granule major basic protein with synthetic lipid bilayers: a mechanism for toxicity J. Membr. Biol. 1992 128 153 164
70. Y. Raab K. Fredens B. Gerdin R. Hallgren Eosinophil activation in ulcerative colitis: studies on mucosal release and localization of eosinophil granule constituents Dig. Dis. Sci. 1998 43 1061 1070
71. S. Winterkamp M. Raithel E. G. Hahn Secretion and tissue content of eosinophil cationic protein in Crohn's disease J. Clin. Gastroenterol. 2000 30 170 175
72. K. D. Dyer H. F. Rosenberg The RNase a superfamily: Generation of diversity and innate host defense Mol. Divers. 2006 10 585 597
73. R. T. Raines Ribonuclease A Chem. Rev. 1998 98 1045 1066
74. S. Cho J. J. Beintema J. Zhang The ribonuclease A superfamily of mammals and birds: identifying new members and tracing evolutionary histories Genomics 2005 85 208 220
75. J. Zhang K. D. Dyer H. F. Rosenberg RNase 8, a novel RNase A superfamily ribonuclease expressed uniquely in placenta Nucleic Acids Res. 2002 30 1169 1175
76. J. Y. Dubois B. M. Ursing J. A. Kolkman J. J. Beintema Molecular evolution of mammalian ribonucleases 1 Mol. Phylogenet. Evol. 2003 27 453 463
77. M. V. Nogues M. Moussaoui E. Boix M. Vilanova M. Ribo C. M. Cuchillo The contribution of noncatalytic phosphate-binding subsites to the mechanism of bovine pancreatic ribonuclease A Cell. Mol. Life Sci. 1998 54 766 774
78. L. V. Hooper T. S. Stappenbeck C. V. Hong J. I. Gordon Angiogenins: a new class of microbicidal proteins involved in innate immunity Nat. Immunol. 2003 4 269 273
79. K. Ishihara K. Asai M. Nakajima S. Mue K. Ohuchi Preparation of recombinant rat eosinophil-associated ribonuclease-1 and -2 and analysis of their biological activities Biochim. Biophys. Acta 2003 1638 164 172
80. E. Carreras E. Boix H. F. Rosenberg C. M. Cuchillo M. V. Nogues Both aromatic and cationic residues contribute to the membrane-lytic and bactericidal activity of eosinophil cationic protein Biochemistry 2003 42 6636 6644
81. E. Carreras E. Boix S. Navarro H. F. Rosenberg C. M. Cuchillo M. V. Nogues Surface-exposed amino acids of eosinophil cationic protein play a critical role in the inhibition of mammalian cell proliferation Mol. Cell. Biochem. 2005 272 1 7
82. H. F. Rosenberg Recombinant human eosinophil cationic protein. Ribonuclease activity is not essential for cytotoxicity J. Biol. Chem. 1995 270 7876 7881
83. T. Nitto K. D. Dyer M. Czapiga H. F. Rosenberg Evolution and function of leukocyte RNase A ribonucleases of the avian species, Gallus gallus J. Biol. Chem. 2006 281 25622 25634
84. Y. C. Huang Y. M. Lin T. W. Chang S. J. Wu Y. S. Lee D. T. Chang C. Chen S. H. Wu Y. D. Liao The flexible and clustered lysine residues of human ribonuclease 7 are critical for membrane permeability and antimicrobial activity J. Biol. Chem. 2006
85. H. F. Rosenberg K. D. Dyer H. L. Tiffany M. Gonzalez Rapid evolution of a unique family of primate ribonuclease genes Nat. Genet. 1995 10 219 223
86. E. Boix Z. Nikolovski G. P. Moiseyev H. F. Rosenberg C. M. Cuchillo M. V. Nogues Kinetic and product distribution analysis of human eosinophil cationic protein indicates a subsite arrangement that favors exonuclease-type activity J. Biol. Chem. 1999 274 15605 15614
87. J. B. Domachowske C. A. Bonville K. D. Dyer H. F. Rosenberg Evolution of antiviral activity in the ribonuclease A gene superfamily: evidence for a specific interaction between eosinophil-derived neurotoxin (EDN/RNase 2) and respiratory syncytial virus Nucleic Acids Res. 1998 26 5327 5332
88. A. L. McDevitt M. S. Deming H. F. Rosenberg K. D. Dyer Gene structure and enzymatic activity of mouse eosinophil-associated ribonuclease 2 Gene 2001 267 23 30
89. M. T. Rugeles C. M. Trubey V. I. Bedoya L. A. Pinto J. J. Oppenheim S. M. Rybak G. M. Shearer Ribonuclease is partly responsible for the HIV-1 inhibitory effect activated by HLA alloantigen recognition Aids 2003 17 481 486
90. P. Venge J. Bystrom M. Carlson L. Hakansson M. Karawacjzyk C. Peterson L. Seveus A. Trulson Eosinophil cationic protein (ECP): molecular and biological properties and the use of ECP as a marker of eosinophil activation in disease Clin. Exp. Allergy 1999 29 1172 1186
91. E. Boix Eosinophil cationic protein Methods Enzymol. 2001 341 287 305
92. H. F. Rosenberg K. D. Dyer Eosinophil cationic protein and eosinophil-derived neurotoxin. Evolution of novel function in a primate ribonuclease gene family J. Biol. Chem. 1995 270 21539 21544
93. K. Fredens H. Dybdahl R. Dahl U. Baandrup Extracellular deposit of the cationic proteins ECP and EPX in tissue infiltrations of eosinophils related to tissue damage Apmis 1988 96 711 719
94. J. M. Hohlfeld A. Schmiedl V. J. Erpenbeck P. Venge N. Krug Eosinophil cationic protein alters pulmonary surfactant structure and function in asthma J. Allergy Clin. Immunol. 2004 113 496 502
95. W. Luck M. Becker B. Niggemann U. Wahn In vitro release of eosinophil cationic protein from peripheral eosinophils reflects disease activity in childhood Crohn disease and ulcerative colitis Eur. J. Pediatr. 1997 156 921 924
96. M. Carlson Y. Raab C. Peterson R. Hallgren P. Venge Increased intraluminal release of eosinophil granule proteins EPO, ECP, EPX, and cytokines in ulcerative colitis and proctitis in segmental perfusion Am. J. Gastroenterol. 1999 94 1876 1883
97. C. J. Pronk-Admiraal R. K. Linskens A. A. Van Bodegraven H. A. Tuynman P. C. Bartels Serum eosinophil cationic protein in active and quiescent ulcerative colitis Clin. Chem. Lab. Med. 2000 38 619 622
98. O. Saitoh K. Kojima K. Sugi R. Matuse K. Uchida K. Tabata K. Nakagawa M. Kayazawa I. Hirata K. Katsu Fecal eosinophil granule-derived proteins reflect disease activity in inflammatory bowel disease Am. J. Gastroenterol. 1999 94 3513 3520
99. C. G. Peterson E. Eklund Y. Taha Y. Raab M. Carlson A new method for the quantification of neutrophil and eosinophil cationic proteins in feces: establishment of normal levels and clinical application in patients with inflammatory bowel disease Am. J. Gastroenterol. 2002 97 1755 1762
100. J. D. Young C. G. Peterson P. Venge Z. A. Cohn Mechanism of membrane damage mediated by human eosinophil cationic protein Nature 1986 321 613 616
101. M. Torrent E. Cuyas E. Carreras S. Navarro O. Lopez A. D. Maza M. V. Nogues Y. K. Reshetnyak E. Boix Topography Studies on the Membrane Interaction Mechanism of the Eosinophil Cationic Protein Biochemistry 2007 46 720 733
102. S. Motojima E. Frigas D. A. Loegering G. J. Gleich Toxicity of eosinophil cationic proteins for guinea pig tracheal epithelium in vitro Am. Rev. Respir. Dis. 1989 139 801 805
103. N. A. Singhania K. D. Dyer J. Zhang M. S. Deming C. A. Bonville J. B. Domachowske H. F. Rosenberg Rapid evolution of the ribonuclease A superfamily: adaptive expansion of independent gene clusters in rats and mice J. Mol. Evol. 1999 49 721 728
104. J. Zhang K. D. Dyer H. F. Rosenberg Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection Proc. Natl. Acad. Sci. U. S. A. 2000 97 4701 4706
105. Y. N. Kaznessis S. Kim R. G. Larson Specific mode of interaction between components of model pulmonary surfactants using computer simulations J. Mol. Biol. 2002 322 569 582
106. T. Nittoh M. Hirakata S. Mue K. Ohuchi Identification of cDNA encoding rat eosinophil cationic protein/eosinophil-associated ribonuclease Biochim. Biophys. Acta 1997 1351 42 46
107. D. Batten K. D. Dyer J. B. Domachowske H. F. Rosenberg Molecular cloning of four novel murine ribonuclease genes: unusual expansion within the ribonuclease A gene family Nucleic Acids Res. 1997 25 4235 4239
108. T. Nittoh M. Hirakata S. Mue K. Ohuchi Identification of cDNA for rat homologues of human major basic protein and eosinophil cationic protein Int. Arch. Allergy Immunol. 1998 117 5 9
109. J. Zhang H. F. Rosenberg Sequence variation at two eosinophil-associated ribonuclease loci in humans Genetics 2000 156 1949 1958
110. S. A. Cormier K. A. Larson S. Yuan T. L. Mitchell K. Lindenburger P. Carrigan N. A. Lee J. J. Lee Mouse eosinophil-associated ribonucleases: a unique subfamily expressed during hematopoiesis Mamm. Genome 2001 12 352 361
111. M. Nakajima M. Hirakata T. Nittoh K. Ishihara K. Ohuchi Expression and purification of recombinant rat eosinophil-associated ribonucleases, homologues of human eosinophil cationic protein and eosinophil-derived neurotoxin, and their characterization Int. Arch. Allergy. Immunol. 2001 125 241 249
112. D. J. Strydom The angiogenins Cell. Mol. Life Sci. 1998 54 811 824
113. M. Moenner M. Gusse E. Hatzi J. Badet The widespread expression of angiogenin in different human cells suggests a biological function not only related to angiogenesis Eur. J. Biochem. 1994 226 483 490
114. M. Suzuki S. K. Saxena E. Boix R. J. Prill V. M. Vasandani J. E. Ladner C. Sung R. J. Joule Engineering receptor-mediated cytotoxicity into human ribonucleases by steric blockade of inhibitor interaction Nat. Biotechnol. 1999 17 265 270
115. A. Egesten K. D. Dyer D. Batten J. B. Domachowske H. F. Rosenberg Ribonucleases and host defense: identification, localization and gene expression in adherent monocytes in vitro Biochim. Biophys. Acta 1997 1358 255 260
116. K. A. Olson S. J. Verselis J. W. Fett Angiogenin is regulated in vivo as an acute phase protein Biochem. Biophys. Res. Commun. 1998 242 480 483
117. J. Zhang K. D. Dyer H. F. Rosenberg Human RNase 7: a new cationic ribonuclease of the RNase A superfamily Nucleic Acids Res. 2003 31 602 607
118. J. Harder J. M. Schroder Antimicrobial peptides in human skin Chem. Immunol. Allergy 2005 86 22 41
119. D. Varoga T. Pufe R. Mentlein S. Kohrs S. Grohmann B. Tillmann J. Hassenpflug F. Paulsen Expression and regulation of antimicrobial peptides in articular joints Ann. Anat. 2005 187 499 508
120. A. Tafech T. Bassett D. Sparanese C. H. Lee Destroying RNA as a therapeutic approach Curr. Med. Chem. 2006 13 863 881
121. J. M. Mancheno M. Gasset M. Onaderra J. G. Gavilanes G. D'Alessio Bovine seminal ribonuclease destabilizes negatively charged membranes Biochem. Biophys. Res. Commun. 1994 199 119 124
122. J. E. Gabay R. P. Almeida Antibiotic peptides and serine protease homologs in human polymorphonuclear leukocytes: defensins and azurocidin Curr. Opin. Immunol. 1993 5 97 102
123. G. Gotte M. Bertoldi M. Libonati Structural versatility of bovine ribonuclease A. Distinct conformers of trimeric and tetrameric aggregates of the enzyme Eur. J. Biochem. 1999 265 680 687
124. L. P. Liu C. M. Deber Anionic phospholipids modulate peptide insertion into membranes Biochemistry 1997 36 5476 5482
125. G. Gotte F. Vottariello M. Libonati Thermal aggregation of ribonuclease A. A contribution to the understanding of the role of 3D domain swapping in protein aggregation J. Biol. Chem. 2003 278 10763 10769
126. C. G. Glabe Common mechanisms of amyloid oligomer pathogenesis in degenerative disease Neurobiol. Aging 2006 27 570 575
127. R. J. Youle D. Newton Y. N. Wu M. Gadina S. M. Rybak Cytotoxic ribonucleases and chimeras in cancer therapy Crit. Rev. Ther. Drug Carrier Syst. 1993 10 1 28
128. J. Costanzi D. Sidransky A. Navon H. Goldsweig Ribonucleases as a novel pro-apoptotic anticancer strategy: review of the preclinical and clinical data for ranpirnase Cancer Invest. 2005 23 643 650
129. D. L. Newton H. J. Hansen S. M. Mikulski D. M. Goldenberg S. M. Rybak Potent and specific antitumor effects of an anti-CD22-targeted cytotoxic ribonuclease: potential for the treatment of non-Hodgkin lymphoma Blood 2001 97 528 535
130. S. M. Rybak H. R. Hoogenboom H. M. Meade J. C. Raus D. Schwartz R. J. Youle Humanization of immunotoxins Proc. Natl. Acad. Sci. U. S. A. 1992 89 3165 3169
131. N. Pavlakis N. J. Vogelzang Ranpirnase-an antitumour ribonuclease: its potential role in malignant mesothelioma Expert Opin. Biol. Ther. 2006 6 391 399
132. J. Gesell M. Zasloff S. J. Opella 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
133. R. L. Fahrner T. Dieckmann S. S. Harwig R. I. Lehrer D. Eisenberg J. Feigon Solution structure of protegrin-1, a broad-spectrum antimicrobial peptide from porcine leukocytes Chem. Biol. 1996 3 543 550
134. B. Cornet J. M. Bonmatin C. Hetru J. A. Hoffmann M. Ptak F. Vovelle Refined three-dimensional solution structure of insect defensin A Structure 1995 3 435 448
135. F. Bauer K. Schweimer E. Kluver, et al. Structure determination of human and murine beta-defensins reveals structural conservation in the absence of significant sequence similarity Protein Sci. 2001 10 2470 2479
136. E. Gasteiger A. Gattiker C. Hoogland I. Ivanyi R. D. Appel A. Bairoch ExPASy: The proteomics server for in-depth protein knowledge and analysis Nucleic Acids Res. 2003 31 3784 3788
137. E. Boix D. D. Leonidas Z. Nikolovski M. V. Nogues C. M. Cuchillo K. R. Acharya Crystal structure of eosinophil cationic protein at 2.4 A resolution Biochemistry 1999 38 16794 16801
138. D. D. Leonidas R. Shapiro S. C. Allen G. V. Subbarao K. Veluraja K. R. Acharya Refined crystal structures of native human angiogenin and two active site variants: implications for the unique functional properties of an enzyme involved in neovascularisation during tumour growth J. Mol. Biol. 1999 285 1209 1233
139. B. Fournier D. J. Philpott Recognition of Staphylococcus aureus by the innate immune system Clin. Microbiol. Rev. 2005 18 521 540
140. G. Mallorqui-Fernandez J. Pous R. Peracaula J. Aymami T. Maeda H. Tada H. Yamada M. Seno R. de Llorens F. X. Gomis-Ruth M. Coll Three-dimensional crystal structure of human eosinophil cationic protein (RNase 3) at 1.75 A resolution J. Mol. Biol. 2000 300 1297 1307
141. P. Gouet E. Courcelle D. I. Stuart F. Metoz ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 1999 15 305 308