Modulation of cytokine gene expression by cathelicidin BMAP-28 in LPS-stimulated and -unstimulated macrophages

Immunobiology

Volumn 217, Issue 10, 2012, Pages 962-971

  D'Este, Francesca ^a   Tomasinsig, Linda ^a   Skerlavaj, Barbara ^a   Zanetti, Margherita ^a  

^a UNIVERSITY OF UDINE   (Italy)

Author keywords

Cathelicidin; Cytokines; Host defence peptides; Innate immunity; Lipopolysaccharide; Toll like receptor 4

Indexed keywords

BETA INTERFERON; CATHELICIDIN; CATHELICIDIN BMAP 28; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY SPECIFICITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BINDING AFFINITY; CELL CULTURE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE RESPONSE; DRUG MECHANISM; ENZYME ACTIVATION; GENE; GENE EXPRESSION REGULATION; GENE INDUCTION; IL 1BETA GENE; IL 6 GENE; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CYTOKINES; GENE EXPRESSION REGULATION; INFLAMMATION; INTERFERON REGULATORY FACTOR-3; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NF-KAPPA B; PROTEIN BINDING; PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4;

EID: 84865367697     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.01.010     Document Type: Article

References (56)

1. Ahmad A., Asthana N., Azmi S., Srivastava R.M., Pandey B.K., Yadav V., Ghosh J.K. Structure-function study of cathelicidin-derived bovine antimicrobial peptide BMAP-28: design of its cell-selective analogs by amino acid substitutions in the heptad repeat sequences. Biochim. Biophys. Acta 2009, 1788:2411-2420.
2. Akashi S., Saitoh S., Wakabayashi Y., Kikuchi T., Takamura N., Nagai Y., Kusumoto Y., Fukase K., Kusumoto S., Adachi Y., Kosugi A., Miyake K. Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14. J. Exp. Med. 2003, 198:1035-1042.
3. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
4. Beevers A.J., Dixon A.M. Helical membrane peptides to modulate cell function. Chem. Soc. Rev. 2010, 39:2146-2157.
5. 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.
6. Beutler B., Rietschel E.T. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 2003, 3:169-176.
7. Bhor V.M., Thomas C.J., Surolia N., Surolia A. Polymyxin B: an ode to an old antidote for endotoxic shock. Mol. Biosyst. 2005, 1:213-222.
8. Bjorkbacka H., Fitzgerald K.A., Huet F., Li X., Gregory J.A., Lee M.A., Ordija C.M., Dowley N.E., Golenbock D.T., Freeman M.W. The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades. Physiol. Genomics 2004, 19:319-330.
9. Buck M.A., Olah T.A., Weitzmann C.J., Cooperman B.S. Protein estimation by the product of integrated peak area and flow rate. Anal. Biochem. 1989, 182:295-299.
10. Byrd-Leifer C.A., Block E.F., Takeda K., Akira S., Ding A. The role of MyD88 and TLR4 in the LPS-mimetic activity of Taxol. Eur. J. Immunol. 2001, 31:2448-2457.
11. Chang C.L., Lin M.E., Hsu H.Y., Yao C.L., Hwang S.M., Pan C.Y., Hsu C.Y., Lee H. Lysophosphatidic acid-induced interleukin-1 beta expression is mediated through Gi/Rho and the generation of reactive oxygen species in macrophages. J. Biomed. Sci. 2008, 15:357-363.
12. Cohen J. The immunopathogenesis of sepsis. Nature 2002, 420:885-891.
13. Cooperstock M.S. Inactivation of endotoxin by polymyxin B. Antimicrob. Agents Chemother. 1974, 6:422-425.
14. Di Nardo A., Braff M.H., Taylor K.R., Na C., Granstein R.D., McInturff J.E., Krutzik S., Modlin R.L., Gallo R.L. Cathelicidin antimicrobial peptides block dendritic cell TLR4 activation and allergic contact sensitization. J. Immunol. 2007, 178:1829-1834.
15. Doyle S., Vaidya S., O'Connell R., Dadgostar H., Dempsey P., Wu T., Rao G., Sun R., Haberland M., Modlin R., Cheng G. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 2002, 17:251-263.
16. Edelhoch H. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry (Mosc.) 1967, 6:1948-1954.
17. Fitzpatrick F.A., Wheeler R. The immunopharmacology of paclitaxel (Taxol), docetaxel (Taxotere), and related agents. Int. Immunopharmacol. 2003, 3:1699-1714.
18. Gautier G., Humbert M., Deauvieau F., Scuiller M., Hiscott J., Bates E.E., Trinchieri G., Caux C., Garrone P. A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J. Exp. Med. 2005, 201:1435-1446.
19. Giacometti A., Cirioni O., Ghiselli R., Bergnach C., Orlando F., D'Amato G., Mocchegiani F., Silvestri C., Del Prete M.S., Skerlavaj B., Saba V., Zanetti M., Scalise G. The antimicrobial peptide BMAP-28 reduces lethality in mouse models of staphylococcal sepsis. Crit. Care Med. 2004, 32:2485-2490.
20. Giocondi M.C., Mamdouh Z., Le Grimellec C. Benzyl alcohol differently affects fluid phase endocytosis and exocytosis in renal epithelial cells. Biochim. Biophys. Acta 1995, 1234:197-202.
21. Hancock R.E., Sahl H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24:1551-1557.
22. Harada S. The broad anti-viral agent glycyrrhizin directly modulates the fluidity of plasma membrane and HIV-1 envelope. Biochem. J. 2005, 392:191-199.
23. Henry T., Kirimanjeswara G.S., Ruby T., Jones J.W., Peng K., Perret M., Ho L., Sauer J.D., Iwakura Y., Metzger D.W., Monack D.M. Type I IFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J. Immunol. 2010, 184:3755-3767.
24. Hirotani T., Yamamoto M., Kumagai Y., Uematsu S., Kawase I., Takeuchi O., Akira S. Regulation of lipopolysaccharide-inducible genes by MyD88 and Toll/IL-1 domain containing adaptor inducing IFN-beta. Biochem. Biophys. Res. Commun. 2005, 328:383-392.
25. Hirsch T., Metzig M., Niederbichler A., Steinau H.U., Eriksson E., Steinstraesser L. Role of host defense peptides of the innate immune response in sepsis. Shock 2008, 30:117-126.
26. Hoebe K., Du X., Georgel P., Janssen E., Tabeta K., Kim S.O., Goode J., Lin P., Mann N., Mudd S., Crozat K., Sovath S., Han J., Beutler B. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003, 424:743-748.
27. Husebye H., Halaas O., Stenmark H., Tunheim G., Sandanger O., Bogen B., Brech A., Latz E., Espevik T. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 2006, 25:683-692.
28. Iwamura T., Yoneyama M., Yamaguchi K., Suhara W., Mori W., Shiota K., Okabe Y., Namiki H., Fujita T. Induction of IRF-3/-7 kinase and NF-kappaB in response to double-stranded RNA and virus infection: common and unique pathways. Genes Cells 2001, 6:375-388.
29. Kagan J.C., Su T., Horng T., Chow A., Akira S., Medzhitov R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat. Immunol. 2008, 9:361-368.
30. Karaghiosoff M., Steinborn R., Kovarik P., Kriegshauser G., Baccarini M., Donabauer B., Reichart U., Kolbe T., Bogdan C., Leanderson T., Levy D., Decker T., Muller M. Central role for type I interferons and Tyk2 in lipopolysaccharide-induced endotoxin shock. Nat. Immunol. 2003, 4:471-477.
31. Kawai T., Adachi O., Ogawa T., Takeda K., Akira S. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 1999, 11:115-122.
32. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
33. Kindrachuk J., Scruten E., Attah-Poku S., Bell K., Potter A., Babiuk L.A., Griebel P.J., Napper S. Stability, toxicity, and biological activity of host defense peptide BMAP28 and its inversed and retro-inversed isomers. Biopolymers 2011, 96:14-24.
34. Lai Y., Gallo R.L. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol. 2009, 30:131-141.
35. McGettrick A.F., O'Neill L.A. Regulators of TLR4 signaling by endotoxins. Subcell. Biochem. 2010, 53:153-171.
36. Murphree L.J., Sullivan G.W., Marshall M.A., Linden J. Lipopolysaccharide rapidly modifies adenosine receptor transcripts in murine and human macrophages: role of NF-kappaB in A(2A) adenosine receptor induction. Biochem. J. 2005, 391:575-580.
37. Nagaoka I., Hirota S., Niyonsaba F., Hirata M., Adachi Y., Tamura H., Heumann D. Cathelicidin family of antibacterial peptides CAP18 and CAP11 inhibit the expression of TNF-alpha by blocking the binding of LPS to CD14(+) cells. J. Immunol. 2001, 167:3329-3338.
38. Nagarajan U.M., Prantner D., Sikes J.D., Andrews C.W., Goodwin A.M., Nagarajan S., Darville T. Type I interferon signaling exacerbates Chlamydia muridarum genital infection in a murine model. Infect. Immun. 2008, 76:4642-4648.
39. Navarini A.A., Recher M., Lang K.S., Georgiev P., Meury S., Bergthaler A., Flatz L., Bille J., Landmann R., Odermatt B., Hengartner H., Zinkernagel R.M. Increased susceptibility to bacterial superinfection as a consequence of innate antiviral responses. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15535-15539.
40. Pochet S., Tandel S., Querriere S., Tre-Hardy M., Garcia-Marcos M., De Lorenzi M., Vandenbranden M., Marino A., Devleeschouwer M., Dehaye J.P. Modulation by LL-37 of the responses of salivary glands to purinergic agonists. Mol. Pharmacol. 2006, 69:2037-2046.
41. Qiu H., Fan Y., Joyee A.G., Wang S., Han X., Bai H., Jiao L., Van Rooijen N., Yang X. Type I IFNs enhance susceptibility to Chlamydia muridarum lung infection by enhancing apoptosis of local macrophages. J. Immunol. 2008, 181:2092-2102.
42. Rosenfeld Y., Shai Y. Lipopolysaccharide (endotoxin)-host defense antibacterial peptides interactions: role in bacterial resistance and prevention of sepsis. Biochim. Biophys. Acta 2006, 1758:1513-1522.
43. Sainte-Marie J., Vignes M., Vidal M., Philippot J.R., Bienvenue A. Effects of benzyl alcohol on transferrin and low density lipoprotein receptor mediated endocytosis in leukemic guinea pig B lymphocytes. FEBS Lett. 1990, 262:13-16.
44. Schrofelbauer B., Raffetseder J., Hauner M., Wolkerstorfer A., Ernst W., Szolar O.H. Glycyrrhizin, the main active compound in liquorice, attenuates pro-inflammatory responses by interfering with membrane-dependent receptor signalling. Biochem. J. 2009, 421:473-482.
45. Shahangian A., Chow E.K., Tian X., Kang J.R., Ghaffari A., Liu S.Y., Belperio J.A., Cheng G., Deng J.C. Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J. Clin. Invest. 2009, 119:1910-1920.
46. Shai Y. 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.
47. Skerlavaj B., Gennaro R., Bagella L., Merluzzi L., Risso A., Zanetti M. Biological characterization of two novel cathelicidin-derived peptides and identification of structural requirements for their antimicrobial and cell lytic activities. J. Biol. Chem. 1996, 271:28375-28381.
48. Steinstraesser L., Kraneburg U., Jacobsen F., Al-Benna S. Host defense peptides and their antimicrobial-immunomodulatory duality. Immunobiology 2011, 216:322-333.
49. Thomas K.E., Galligan C.L., Newman R.D., Fish E.N., Vogel S.N. Contribution of interferon-beta to the murine macrophage response to the toll-like receptor 4 agonist, lipopolysaccharide. J. Biol. Chem. 2006, 281:31119-31130.
50. Tomasinsig L., De Conti G., Skerlavaj B., Piccinini R., Mazzilli M., D'Este F., Tossi A., Zanetti M. Broad-spectrum activity against bacterial mastitis pathogens and activation of mammary epithelial cells support a protective role of neutrophil cathelicidins in bovine mastitis. Infect. Immun. 2010, 78:1781-1788.
51. Tomasinsig L., Pizzirani C., Skerlavaj B., Pellegatti P., Gulinelli S., Tossi A., Di Virgilio F., Zanetti M. The human cathelicidin LL-37 modulates the activities of the P2X7 receptor in a structure-dependent manner. J. Biol. Chem. 2008, 283:30471-30481.
52. Toshchakov V., Jones B.W., Lentschat A., Silva A., Perera P.Y., Thomas K., Cody M.J., Zhang S., Williams B.R., Major J., Hamilton T.A., Fenton M.J., Vogel S.N. TLR2 and TLR4 agonists stimulate unique repertoires of host resistance genes in murine macrophages: interferon-beta-dependent signaling in TLR4-mediated responses. J. Endotoxin Res. 2003, 9:169-175.
53. Tyteca D., Schanck A., Dufrene Y.F., Deleu M., Courtoy P.J., Tulkens P.M., Mingeot-Leclercq M.P. The macrolide antibiotic azithromycin interacts with lipids and affects membrane organization and fluidity: studies on Langmuir-Blodgett monolayers, liposomes and J774 macrophages. J. Membr. Biol. 2003, 192:203-215.
54. Yamamoto M., Sato S., Hemmi H., Hoshino K., Kaisho T., Sanjo H., Takeuchi O., Sugiyama M., Okabe M., Takeda K., Akira S. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003, 301:640-643.
55. Yamamoto M., Sato S., Hemmi H., Uematsu S., Hoshino K., Kaisho T., Takeuchi O., Takeda K., Akira S. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 2003, 4:1144-1150.
56. Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 2004, 75:39-48.