High fidelity processing and activation of the human α-defensin HNP1 precursor by neutrophil elastase and proteinase 3

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Tongaonkar, Prasad ^a   Golji, Amir E ^a   Tran, Patti ^a   Ouellette, André J ^a,b   Selsted, Michael E ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DEFENSIN; CATHEPSIN G; CONVERTASE; DEFENSIN 1; DEFENSIN 2; DEFENSIN 3; DIPEPTIDE; ENZYME; HUMAN NEUTROPHIL PEPTIDE 1 PRECURSOR; HUMAN NEUTROPHIL PEPTIDE 4; LEUKOCYTE ELASTASE; MICROBICIDE; MYELOBLASTIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN PRECURSOR; PROTEIN VARIANT; SERINE PROTEINASE; UNCLASSIFIED DRUG; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL GRANULE; CONTROLLED STUDY; DISULFIDE BOND; ESCHERICHIA COLI; IN VITRO STUDY; INTRACELLULAR KILLING; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; STAPHYLOCOCCUS AUREUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MASS SPECTROMETRY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGICAL EXAMINATION; MOLECULAR GENETICS; WESTERN BLOTTING;

STAPHYLOCOCCUS AUREUS;

ALPHA-DEFENSINS; AMINO ACID SEQUENCE; BLOTTING, WESTERN; CATHEPSIN G; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HUMANS; LEUKOCYTE ELASTASE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MYELOBLASTIN; PROTEIN FOLDING; PROTEIN PRECURSORS; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STAPHYLOCOCCUS AUREUS;

EID: 84858629612     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032469     Document Type: Article

References (47)

1. Risso A, (2000) Leukocyte antimicrobial peptides: multifunctional effector molecules of innate immunity. J Leukoc Biol 68: 785-792.
2. Selsted ME, Ouellette AJ, (2005) Mammalian defensins in the antimicrobial immune response. Nat Immunol 6: 551-557.
3. Ganz T, (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3: 710-720.
4. Ericksen B, Wu Z, Lu W, Lehrer RI, (2005) Antibacterial activity and specificity of the six human α-defensins. Antimicrob Agents Chemother 49: 269-275.
5. Mambula SS, Simons ER, Hastey R, Selsted ME, Levitz SM, (2000) Human neutrophil-mediated nonoxidative antifungal activity against Cryptococcus neoformans. Infect Immun 68: 6257-6264.
6. Newman SL, Gootee L, Gabay JE, Selsted ME, (2000) Identification of constituents of human neutrophil azurophil granules that mediate fungistasis against Histoplasma capsulatum. Infect Immun 68: 5668-5672.
7. Daher KA, Selsted ME, Lehrer RI, (1986) Direct inactivation of viruses by human granulocyte defensins. J Virol 60: 1068-1074.
8. Hazrati E, Galen B, Lu W, Wang W, Ouyang Y, et al. (2006) Human α- and β-defensins block multiple steps in herpes simplex virus infection. J Immunol 177: 8658-8666.
9. Quinones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, et al. (2003) Human epithelial β-defensins 2 and 3 inhibit HIV-1 replication. Aids 17: F39-48.
10. Aley SB, Zimmerman M, Hetsko M, Selsted ME, Gillin FD, (1994) Killing of Giardia lamblia by cryptdins and cationic neutrophil peptides. Infect Immun 62: 5397-5403.
11. Wohlford-Lenane CL, Meyerholz DK, Perlman S, Zhou H, Tran D, et al. (2009) Rhesus θ-defensin prevents death in a mouse model of severe acute respiratory syndrome coronavirus pulmonary disease. J Virol 83: 11385-11390.
12. Semple F, Webb S, Li HN, Patel HB, Perretti M, et al. (2010) Human β-defensin 3 has immunosuppressive activity in vitro and in vivo. Eur J Immunol 40: 1073-1078.
13. Hashimoto S, Uto H, Kanmura S, Sakiyama T, Oku M, et al. (2011) Human neutrophil peptide-1 aggravates dextran sulfate sodium-induced colitis. Inflamm Bowel Dis. [Epub ahead of print].
14. Oppenheim JJ, Biragyn A, Kwak LW, Yang D, (2003) Roles of antimicrobial peptides such as defensins in innate and adaptive immunity. Ann Rheum Dis 62 (Suppl 2): ii17-21.
15. Panyutich AV, Panyutich EA, Krapivin VA, Baturevich EA, Ganz T, (1993) Plasma defensin concentrations are elevated in patients with septicemia or bacterial meningitis. J Lab Clin Med 122: 202-207.
16. Thomas NJ, Carcillo JA, Doughty LA, Sasser H, Heine RP, (2002) Plasma concentrations of defensins and lactoferrin in children with severe sepsis. Pediatr Infect Dis J 21: 34-38.
17. Aarbiou J, Ertmann M, van Wetering S, van Noort P, Rook D, et al. (2002) Human neutrophil defensins induce lung epithelial cell proliferation in vitro. J Leukoc Biol 72: 167-174.
18. Muller CA, Markovic-Lipkovski J, Klatt T, Gamper J, Schwarz G, et al. (2002) Human α-defensins HNPs-1,-2, and-3 in renal cell carcinoma: influences on tumor cell proliferation. Am J Pathol 160: 1311-1324.
19. Han W, Wang W, Mohammed KA, Su Y, (2009) α-Defensins increase lung fibroblast proliferation and collagen synthesis via the beta-catenin signaling pathway. Febs J 276: 6603-6614.
20. Economopoulou M, Bdeir K, Cines DB, Fogt F, Bdeir Y, et al. (2005) Inhibition of pathologic retinal neovascularization by alpha-defensins. Blood 106: 3831-3838.
21. Chavakis T, Cines DB, Rhee JS, Liang OD, Schubert U, et al. (2004) Regulation of neovascularization by human neutrophil peptides (α-defensins): a link between inflammation and angiogenesis. Faseb J 18: 1306-1308.
22. Chertov O, Michiel DF, Xu L, Wang JM, Tani K, et al. (1996) Identification of defensin-1, defensin-2, and CAP37/azurocidin as T-cell chemoattractant proteins released from interleukin-8-stimulated neutrophils. J Biol Chem 271: 2935-2940.
23. Lillard JW Jr, Boyaka PN, Chertov O, Oppenheim JJ, McGhee JR, (1999) Mechanisms for induction of acquired host immunity by neutrophil peptide defensins. Proc Natl Acad Sci U S A 96: 651-656.
24. Syeda F, Liu HY, Tullis E, Liu M, Slutsky AS, et al. (2008) Differential signaling mechanisms of HNP-induced IL-8 production in human lung epithelial cells and monocytes. J Cell Physiol 214: 820-827.
25. Li J, Raghunath M, Tan D, Lareu RR, Chen Z, et al. (2006) Defensins HNP1 and HBD2 stimulation of wound-associated responses in human conjunctival fibroblasts. Invest Ophthalmol Vis Sci 47: 3811-3819.
26. Daher KA, Lehrer RI, Ganz T, Kronenberg M, (1988) Isolation and characterization of human defensin cDNA clones. Proc Natl Acad Sci U S A 85: 7327-7331.
27. Michaelson D, Rayner J, Couto M, Ganz T, (1992) Cationic defensins arise from charge-neutralized propeptides: a mechanism for avoiding leukocyte autocytotoxicity? J Leukoc Biol 51: 634-639.
28. Valore EV, Martin E, Harwig SS, Ganz T, (1996) Intramolecular inhibition of human defensin HNP-1 by its propiece. J Clin Invest 97: 1624-1629.
29. Wu Z, Prahl A, Powell R, Ericksen B, Lubkowski J, et al. (2003) From pro defensins to defensins: synthesis and characterization of human neutrophil pro α-defensin-1 and its mature domain. J Pept Res 62: 53-62.
30. Ghosh D, Porter E, Shen B, Lee SK, Wilk D, et al. (2002) Paneth cell trypsin is the processing enzyme for human defensin-5. Nat Immunol 3: 583-590.
31. Wilson CL, Ouellette AJ, Satchell DP, Ayabe T, Lopez-Boado YS, et al. (1999) Regulation of intestinal α-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286: 113-117.
32. Kamdar K, Maemoto A, Qu X, Young SK, Ouellette AJ, (2008) In vitro activation of the rhesus macaque myeloid α-defensin precursor proRMAD-4 by neutrophil serine proteinases. J Biol Chem 283: 32361-32368.
33. Scocchi M, Skerlavaj B, Romeo D, Gennaro R, (1992) Proteolytic cleavage by neutrophil elastase converts inactive storage proforms to antibacterial bactenecins. Eur J Biochem 209: 589-595.
34. Sorensen OE, Follin P, Johnsen AH, Calafat J, Tjabringa GS, et al. (2001) Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97: 3951-3959.
35. Valore EV, Ganz T, (1992) Posttranslational processing of defensins in immature human myeloid cells. Blood 79: 1538-1544.
36. Borregaard N, Sorensen OE, Theilgaard-Monch K, (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol 28: 340-345.
37. Zhang Y, Lu W, Hong M, (2010) The membrane-bound structure and topology of a human α-defensin indicate a dimer pore mechanism for membrane disruption. Biochemistry 49: 9770-9782.
38. Varkey J, Nagaraj R, (2005) Antibacterial activity of human neutrophil defensin HNP-1 analogs without cysteines. Antimicrob Agents Chemother 49: 4561-4566.
39. Wanniarachchi YA, Kaczmarek P, Wan A, Nolan EM, (2011) Human Defensin 5 Disulfide Array Mutants: Disulfide Bond Deletion Attenuates Antibacterial Activity against Staphylococcus aureus. Biochemistry 50: 8005-8017.
40. Maemoto A, Qu X, Rosengren KJ, Tanabe H, Henschen-Edman A, et al. (2004) Functional analysis of the α-defensin disulfide array in mouse cryptdin-4. J Biol Chem 279: 44188-44196.
41. Harwig SS, Park AS, Lehrer RI, (1992) Characterization of defensin precursors in mature human neutrophils. Blood 79: 1532-1537.
42. Wilson CL, Schmidt AP, Pirila E, Valore EV, Ferri N, et al. (2009) Differential Processing of α- and β-Defensin Precursors by Matrix Metalloproteinase-7 (MMP-7). J Biol Chem 284: 8301-8311.
43. Faurschou M, Kamp S, Cowland JB, Udby L, Johnsen AH, et al. (2005) Prodefensins are matrix proteins of specific granules in human neutrophils. J Leukoc Biol 78: 785-793.
44. Pham CT, (2008) Neutrophil serine proteases fine-tune the inflammatory response. Int J Biochem Cell Biol 40: 1317-1333.
45. Tran D, Tran PA, Tang YQ, Yuan J, Cole T, et al. (2002) Homodimeric θ-defensins from rhesus macaque leukocytes: isolation, synthesis, antimicrobial activities, and bacterial binding properties of the cyclic peptides. J Biol Chem 277: 3079-3084.
46. Tongaonkar P, Tran P, Roberts K, Schaal J, Osapay G, et al. (2011) Rhesus macaque θ-defensin isoforms: expression, antimicrobial activities, and demonstration of a prominent role in neutrophil granule microbicidal activities. J Leukoc Biol 89: 283-290.
47. Garcia AE, Osapay G, Tran PA, Yuan J, Selsted ME, (2008) Isolation, synthesis, and antimicrobial activities of naturally occurring θ-defensin isoforms from baboon leukocytes. Infect Immun 76: 5883-5891.