Mechanisms of cell death induced by the neutrophil antimicrobial peptides α-defensins and LL-37

Inflammation Research

Volumn 55, Issue 3, 2006, Pages 119-127

  Aarbiou, J ^a   Tjabringa, G S ^a   Verhoosel, R M ^a   Ninaber, D K ^a   White, S R ^b   Peltenburg, L T C ^a,c   Rabe, K F ^a   Hiemstra, P S ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF CHICAGO   (United States)

^c CRUCELL HOLLAND BV   (Netherlands)

Author keywords

Antimicrobial peptides; Caspases; Cathelicidins; Cytotoxicity; Defensins

Indexed keywords

ALPHA DEFENSIN; CASPASE 3; CASPASE 7; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CYTOCHROME C; DEFENSIN 1; DEFENSIN 2; DEFENSIN 3; DNA; LIPOCORTIN 5; NEUTROPHIL DEFENSIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POLYPEPTIDE ANTIBIOTIC AGENT; PROPIDIUM IODIDE; PROTEIN BCL 2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BRONCHUS MUCOSA; CELL DEATH; CONTROLLED STUDY; CULTURE MEDIUM; DNA STRAND BREAKAGE; DRUG CYTOTOXICITY; ENZYME INDUCTION; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LUNG ALVEOLUS EPITHELIUM; MITOCHONDRION; NEUTROPHIL; NICK END LABELING;

ALPHA-DEFENSINS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; APOPTOSIS; CASPASE 3; CASPASE 7; CELL LINE, TUMOR; CYTOCHROMES C; HUMANS; MITOCHONDRIA; NEUTROPHILS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 33646516620     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-005-0062-9     Document Type: Article

References (49)

1. Bals R, Hiemstra PS. Innate immunity in the lung: how epithelial cells fight against respiratory pathogens. Eur Respir J 2004; 23: 327-33.
2. Agerberth B, Charo J, Werr J, Olsson B, Idali F, Lindbom L et al. The human antimicrobial and chemotactic peptides LL-37 and alpha-defensins are expressed by specific lymphocyte and monocyte populations. Blood 2000; 96: 3086-93.
3. Obata-Onai A, Hashimoto S, Onai N, Kurachi M, Nagai S, Shizuno K et al. Comprehensive gene expression analysis of human NK cells and CD8(+) T lymphocytes. Int Immunol 2002; 14: 1085-98. Erratum: Int Immunol 2002; 14: 1469.
4. Ganz T, Selsted ME, Lehrer RI. Defensins. Eur J Haematol 1990; 44: 1-8.
5. Aarbiou J, Rabe KF, Hiemstra PS. Role of defensins in inflammatory lung disease. Ann Med 2002; 34: 96-101.
6. Soong LB, Ganz T, Ellison A, Caughey GH. Purification and characterization of defensins from cystic fibrosis sputum. Inflamm Res 1997; 46: 98-102.
7. Gudmundsson GH, 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: 325-32.
8. Frohm NM, Sandstedt B, Sorensen O, Weber G, Borregaard N, Stahle-Backdahl M. The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6. Infect Immun 1999; 67: 2561-6.
9. Bals R, Wang X, Zasloff M, Wilson JM. The peptide antibiotic LL-37/hCAP-18 is expressed in epithelia of the human lung where it has broad antimicrobial activity at the airway surface. Proc Natl Acad Sci USA 1998; 95: 9541-6.
10. Frohm M, Agerberth B, Ahangari G, Stahle-Backdahl M, Liden S, Wigzell H et al. The expression of the gene coding for the antibacterial peptide LL-37 is induced in human keratinocytes during inflammatory disorders. J Biol Chem 1997; 272: 15258-63.
11. Di Nardo A, Vitiello A, Gallo RL. Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. J Immunol 2003; 170: 2274-8.
12. Sorensen OE, Follin P, Johnsen AH, Calafat J, Tjabringa GS, Hiemstra PS et al. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 2001; 97: 3951-9.
13. Sorensen OE, Gram L, Johnsen AH, Andersson E, Bangsboll S, Tjabringa GS et al. Processing of seminal plasma hCAP-18 to ALL-38 by gastricsin: a novel mechanism of generating antimicrobial peptides in vagina. J Biol Chem 2003; 278: 28540-6.
14. Aarbiou J, Verhoosel RM, van Wetering S, de Boer WI, van Krieken JHJM, Litvinov SV et al. Neutrophil defensins enhance lung epithelial wound closure and mucin gene expression in vitro. Am J Respir Cell Mol Biol 2003; 30: 193-201.
15. Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 2004; 75: 39-48.
16. Okrent DG, Lichtenstein AK, Ganz T. Direct cytotoxicity of polymorphonuclear leukocyte granule proteins to human lung-derived cells and endothelial cells. Am Rev Respir Dis 1990; 141: 179-85.
17. van Wetering S, Mannesse-Lazeroms SP, Dijkman JH, Hiemstra PS. Effect of neutrophil serine proteinases and defensins on lung epithelial cells: modulation of cytotoxicity and IL-8 production. J Leukoc Biol 1997; 62: 217-26.
18. Johansson J, Gudmundsson GH, Rottenberg ME, Berndt KD, Agerberth B. Conformation-dependent Antibacterial Activity of the Naturally Occurring Human Peptide LL-37. J Biol Chem 1998; 273: 3718-24.
19. Gera JF, Lichtenstein A. Human neutrophil peptide defensins induce single strand DNA breaks in target cells. Cell Immunol 1991; 138: 108-20.
20. Henzler Wildman KA, Lee DK, Ramamoorthy A. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 2003; 42: 6545-58.
21. Wimley WC, Selsted ME, White SH. Interactions between human defensins and lipid bilayers: evidence for formation of multimeric pores. Protein Sci 1994; 3: 1362-73.
22. Oren Z, Lerman JC, Gudmundsson GH, Agerberth B, Shai Y. Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: relevance to the molecular basis for its non-cell-selective activity. Biochem J 1999; 341: 501-13.
23. Lichtenstein AK, Ganz T, Nguyen TM, Selsted ME, Lehrer RI. Mechanism of target cytolysis by peptide defensins. Target cell metabolic activities, possibly involving endocytosis, are crucial for expression of cytotoxicity. J Immunol 1988; 140: 2686-94.
24. Zaharatos GJ, He T, Lopez P, Yu W, Yu J, Zhang L. alpha-Defensins Released Into Stimulated CD8+ T-Cell Supernatants Are Likely Derived From Residual Granulocytes Within the Irradiated Allogeneic Peripheral Blood Mononuclear Cells Used as Feeders. J Acquir Immune Defic Syndr 2004; 36: 993-1005.
25. van Wetering S, Mannesse-Lazeroms SP, van Sterkenburg MA, Daha MR, Dijkman JH, Hiemstra PS. Effect of defensins on interleukin-8 synthesis in airway epithelial cells. Am J Physiol 1997; 272: L888-L896.
26. Werner AB, de Vries E, Tait SWG, Bontjer I, Borst J. Bcl-2 Family Member Bfl-1/A1 Sequesters Truncated Bid to Inhibit Its Collaboration with Pro-apoptotic Bak or Bax. J Biol Chem 2002; 277: 22781-8.
27. van Wetering S, van der Linden AC, van Sterkenburg MA, Rabe KF, Schalkwijk J, Hiemstra PS. Regulation of secretory leukocyte proteinase inhibitor (SLPI) production by human bronchial epithelial cells: increase of cell-associated SLPI by neutrophil elastase. J Investig Med 2000; 48: 359-66.
28. Aarbiou J, Ertmann M, van Wetering S, Van Noort P, Rook D, Rabe KF et al. Human neutrophil defensins induce lung epithelial cell proliferation in vitro. J Leukoc Biol 2002; 72: 167-74.
29. de Bruin EC, Meersma D, de Wilde J, den Otter I, Schipper EM, Medema JP et al. A serine protease is involved in the initiation of DNA damage-induced apoptosis. Cell Death Differ 2003; 10: 1204-12.
30. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994; 84: 1415-20.
31. White SR, Williams P, Wojcik KR, Sun S, Hiemstra PS, Rabe KF et al. Initiation of Apoptosis by Actin Cytoskeletal Derangement in Human Airway Epithelial Cells. Am J Respir Cell Mol Biol 2001; 24: 282-94.
32. Risso A, Zanetti M, Gennaro R. Cytotoxicity and apoptosis mediated by two peptides of innate immunity. Cell Immunol 1998; 189: 107-15.
33. Risso A, Braidot E, Sordano MC, Vianello A, Macri F, Skerlavaj B et al. BMAP-28, an Antibiotic Peptide of Innate Immunity, Induces Cell Death through Opening of the Mitochondrial Permeability Transition Pore. Mol Cell Biol 2002; 22: 1926-35.
34. Okumura K, Itoh A, Isogai E, Hirose K, Hosokawa Y, Abiko Y et al. C-terminal domain of human CAP18 antimicrobial peptide induces apoptosis in oral squamous cell carcinoma SAS-H1 cells. Cancer Lett 2004; 212: 185-94.
35. Ashkenazi A, Dixit VM. Death Receptors: Signaling and Modulation. Science 1998; 281: 1305-8.
36. Fiers W, Beyaert R, Declercq W, Vandenabeele P. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 1999; 18: 7719-30.
37. Chittenden T. BH3 domains: intracellular death-ligands critical for initiating apoptosis. Cancer Cell 2002; 2: 165-6.
38. Chen LB. Mitochondrial membrane potential in living cells. Annu Rev Cell Biol 1988; 4: 155-81.
39. Modica-Napolitano JS, Brunelli BT, Koya K, Chen LB. Photoactivation enhances the mitochondrial toxicity of the cationic rhodacyanine MKT-077. Cancer Res 1998; 58: 71-5.
40. Pfeiffer DR, Gudz TI, Novgorodov SA, Erdahl WL. The Peptide Mastoparan Is a Potent Facilitator of the Mitochondrial Permeability Transition. J Biol Chem 1995; 270: 4923-32.
41. Ellerby HM, Arap W, Ellerby LM, Kain R, Andrasiak R, Rio GD et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med 1999; 5: 1032-8.
42. Jacotot E, Ravagnan L, Loeffler M, Ferri KF, Vieira HLA, Zamzami N et al. The HIV-1 Viral Protein R Induces Apoptosis via a Direct Effect on the Mitochondrial Permeability Transition Pore. J Exp Med 2000; 191: 33-46.
43. Lohner K, Latal A, Lehrer RI, Ganz T. Differential scanning microcalorimetry indicates that human defensin, HNP-2, interacts specifically with biomembrane mimetic systems. Biochemistry 1997; 36: 1525-31.
44. Panyutich AV, Hiemstra PS, van Wetering S, Ganz T. Human neutrophil defensin and serpins form complexes and inactivate each other. Am J Respir Cell Mol Biol 1995; 12: 351-7.
45. Panyutich AV, Panyutich EA, Krapivin VA, Baturevich EA, Ganz T. Plasma defensin concentrations are elevated in patients with septicemia or bacterial meningitis. J Lab Clin Med 1993; 122: 202-7.
46. Agerberth B, Grunewald I, Castanos-Velez E, Olsson B, Jornvall H, Wigzell H et al. Antibacterial components in bronchoalveolar lavage fluid from healthy individuals and sarcoidosis patients. Am J Respir Crit Care Med 1999; 160: 283-90.
47. Schaller-Bals S, Schulze A, Bals R. Increased levels of antimicrobial peptides in tracheal aspirates of newborn infants during infection. Am J Respir Crit Care Med 2002; 165: 992-5.
48. Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002; 347: 1151-60.
49. Ganz T. Extracellular release of antimicrobial defensins by human polymorphonuclear leukocytes. Infect Immun 1987; 55: 568-71.